Review Article

B Blake Levitt Henry C Lai and Albert M Manville II

Effects of non-ionizing electromagnetic fields onflora and fauna Part 2 impacts how speciesinteract with natural and man-made EMFhttpsdoiorg101515reveh-2021-0050Received April 20 2021 accepted May 26 2021published online July 8 2021

Abstract Ambient levels of nonionizing electromagneticfields (EMF) have risen sharply in the last five decades tobecome a ubiquitous continuous biologically active envi-ronmental pollutant even in rural and remote areas Manyspecies of flora and fauna because of unique physiologiesand habitats are sensitive to exogenous EMF in ways thatsurpass human reactivity This can lead to complex endog-enous reactions that are highly variable largely unseen anda possible contributing factor in species extinctions some-times localized Non-humanmagnetoreceptionmechanismsare explored Numerous studies across all frequencies andtaxa indicate that current low-level anthropogenic EMF canhave myriad adverse and synergistic effects including onorientation and migration food finding reproductionmating nest and den building territorial maintenance anddefense and on vitality longevity and survivorship itselfEffects have been observed in mammals such as bats cer-vids cetaceans and pinnipeds among others and on birdsinsects amphibians reptiles microbes andmany species offlora Cyto- and geno-toxic effects have long been observedin laboratory research on animal models that can beextrapolated to wildlife Unusual multi-systemmechanismscan come into play with non-human speciesmdash including inaquatic environments mdash that rely on the Earthrsquos naturalgeomagnetic fields for critical life-sustaining informationPart 2 of this 3-part series includes four online supplementtables of effects seen in animals from both ELF and RFR at

vanishingly low intensities Taken as a whole this indicatesenough information to raise concerns about ambient expo-sures to nonionizing radiation at ecosystem levels Wildlifeloss is often unseen and undocumented until tipping pointsare reached It is time to recognize ambient EMF as a novelform of pollution and develop rules at regulatory agenciesthat designate air as lsquohabitatrsquo so EMF can be regulated likeother pollutants Long-term chronic low-level EMF exposurestandards which do not now exist should be set accordinglyfor wildlife and environmental laws should be strictlyenforcedmdash a subject explored in Part 3

Keywords cell phone towersmastsbase stations Earthrsquosgeomagnetic fields magnetoreception radiofrequencyradiation (RFR) nonionizing electromagnetic fields (EMF)plants wildlife

Introduction electromagneticfields mdash natural and man-made

In Part 1 of this three-part series rising ambient EMF levelswere explored Part 2 focuses specifically on the uniquemagnetoreception physiologies found in wildlife as well asthe mechanisms by which they interact with the Earthrsquosnatural geomagnetic fields and man-made EMF at in-tensities now commonly found in the environment Part 2Supplements contain tables of studies showing effects atextremely low intensity exposures comparable to todayrsquosambient levels

Energy is a part of nature affecting every living thing inpositive negative and neutral ways The Earth itself is adipole magnet with a north and a south pole All livingthings have evolved within the protective cradle of theEarthrsquos natural geomagnetic fields In fact magnetic os-cillations emanate from the Earthrsquos molten iron corearound 10 times per second (10 Hz) where relaxed but alerthuman thoughtbrainwaves occur between 8 and 14 Hz

In addition to the Earthrsquos natural emanations vastSchumannResonances (SR) that constantly circle the globe

Corresponding author B Blake Levitt PO Box 2014 New PrestonCT 06777 USA E-mail blakelevitt2gmailcom andblakelevitcscomHenryC LaiDepartment of Bioengineering University ofWashingtonSeattle WA USA E-mail hlaiuweduAlbert M Manville II Advanced Academic Programs Krieger Schoolof Arts and Sciences Environmental Sciences and Policy JohnsHopkins University Washington DC Campus USAE-mail amanvil1jhuedu

Rev Environ Health 2021 aop

were theorized in 1952 by physicist Windfried Otto Schu-mann and reliably measured in the 1960s [1 2] SR are aglobal electromagnetic phenomenon caused by a complexrelationship between lightening at the Earthrsquos surface andthe ionosphere Excited by the 2000 thunderstorms thatoccur globally at any given time and approximately 50flashes of lightening every second the space betweenEarth and the ionosphere 60 miles (97 km) above it form aresonant cavity and closed waveguide [3] SchumannResonances occur in the ELF bands between 3 and 60 Hzwith distinct fundamental peaks around 783 Hz Since the1960s scientists have discovered that variations in theresonances correspond to seasonal changes in solar ac-tivity the Earthrsquos magnetic environment in atmosphericwater aerosols and various other earth-bound phenomenaincluding increased weather activity due to climatechange There are an estimated 12 billion lighteningflashes globally each year 25 million in the US alone [4]not all of which are of sufficient length to contribute to theresonances

Many behavioral aspects in biology are thought to besynchronized with both the Earthrsquos natural fields and theSchumann Resonances Many species rely on the Earthrsquosnatural fields for daily movement seasonal migrationreproduction food-finding and territorial location as wellas diurnal and nocturnal activities Human circadianrhythms mainly regulated by light targeting signaling

pathways in the hypothalamic suprachiasmatic nucleusare known to be finely tuned to the Earthrsquos daynight cyclesas well as natural seasonal variations as are most species[5ndash8] Artificial ELF-EMF is also known to adversely affecthuman circadian clocks possibly through modulation incircadian clock gene expression itself [9]

Nonionizing electromagnetic fields (EMF 0ndash300 GHz)include all the frequencies that fall between visible lightbelow the ultraviolet range and the Earthrsquos natural staticfields The nonionizing bands are used in virtually everythinginvolved with communications and energy propagation souseful in modern life including electric power productiondistribution all wireless technologies and accompanyinginfrastructure for cell phones WiFi babyhome monitoringsystems lsquosmartrsquogridmeters all lsquosmartrsquo technologydevices2-through-5G Internet of Things AMFM broadcast radio andtelevision shortwave and HAM radio surveillancesecuritysystems satellites radar many military applicationsand myriad medical diagnostic tools like MRIrsquos to namebut a few (see Figure 1)

In its natural state very little radiofrequency radiation(RFR) reaches the Earthrsquos surface Aside from the Earthrsquosnatural extremely low frequency (ELF) direct current (DC)magnetic fields lightening and sunlight would primarilycomprise our normal exposures to the electromagneticspectrumMost harmful radiation coming from outer space isblocked by the Earthrsquos magnetosphere But now for the first

Figure 1 The electromagnetic spectrumThe electromagnetic spectrum is divided into ionizing and nonionizing radiation Ionizing radiation falls at and above the ultra violet range inthe light frequencies Examples of ionizing radiation include gamma rays cosmic rays X-rays and various military and civilian nuclearactivities It is the nonionzing bands that we have completely filled in with modern technology

2 Levitt et al EMF and wildlife

time in evolutionary history we have infused the Earthrsquossurface with a blanket of artificial energy exposures with noclear understanding of what the consequences may be

And although ldquonaturalrdquo not all energy is alike Man-made exposures contain propagation characteristicsmdash suchas alternating current modulation complex signaling char-acteristics (eg pulsed digital and phased array) unusualwave forms (eg square and sawtooth shapes) and atheightened power intensities at the Earthrsquos surface that sim-ply donot exist in nature These are allman-madeartifacts Inour embrace of technology we have completely altered theEarthrsquos electromagnetic signature in which all life hasevolved in essence bypassing the magnetospherersquos protec-tion And because so much of wireless technology is satellitebased increasing exposures are no longer just ground-generated All atmospheric levels are now affected byincreasing ambient exposures (see Part 1 and Part 1 Supple-ment) This is especially true in the lower atmosphere whichis lsquohabitatrsquo (beyondmere oxygen and clean air standards) forall species thatmatemigrate and feed in the airmdash includingbirds mammals (such as bats) insects and some arachnids

Species extinctions

There has been an unprecedented rate of biodiversitydecline in recent decades according to the InternationalUnion for Conservation of Nature [10] which maintains aldquoRed List of Threatened Speciesrdquo that is considered theworldrsquos most comprehensive source on the global conser-vation status of animal fungi and plant species mdash allcritical indicators of planetary health

IUCNrsquos 2018 list showed that 26000 species are threat-ened with extinction which reflected more than 27 of allspecies assessed This was greatly increased from their 2004report that found at least 15 species had already gone extinctbetween 1984 and 2004 and another 12 survived only incaptivity Current extinction rates arenowat least 100 to 1000times higher than natural rates found in the fossil record

The more recent May 2019 report by the Intergovern-mental Science and Policy Platform on Biodiversity andEcosystem Services Paris France [11] projected that at least 1million plant and animal species worldwide are at imminentthreat of extinction if our current humanactions and activitiesare not immediately reversed A review of 73 reports bySanchez-Bayo and Wyckhuys [12] found those rates hadgreatly accelerated The authors noted that biodiversity ofinsects in particular is threatened worldwide with dramaticdeclines that could lead to a 40 extinction of insect speciesover the next several decades In terrestrial ecosystems theyfound Lepidoptera Hymenoptera and Coleoptera (dung

beetles) were most affected while in aquatic ecosystemsOdonata Plecoptera Trichoptera and Ephemeroptera havealready lost a considerable proportion of species Affectedinsect groups included niche specialist species as well ascommon and generalist species many of which are criticallyimportant for pollination aswell as seed fruit nut andhoneyproduction and natural pest control among others ofimmeasurable economic and ecological value

Humans are the primary cause for most declines viahabitat destructiondegradation over-exploitation for foodpets cattle and medicine artificially introduced speciespollutioncontamination pesticides and disease Climatechange is increasingly establishedas a serious threat aswellas agricultural practices like monoculture crops for cattlefeed biofuels and timber New pesticides and weed killersintroduced within the last 20 years using neonicotinoidsglyphosphate and fipronil are especially damaging sincethey are long-lasting and capable of sterilizing soil of bene-ficial microorganisms including worms and grubs whichcan then extend to areas far beyond applications sites

One example of multi-factorial damage includes theiconic AmericanMonarch butterfly (Danaus plexippus)whichis found across America and Southern Canada and generallygeographically divided into eastern and western migratorygroups by the RockyMountains That species has declined bya full 994 in the west since the 1980smdash 85 of that beingsince 2017 [13 14] According to the Center for Biological Di-versity [15] the eastern monarch population has shrunk by90 in the past two decades Massive habitat loss wildfiresclimate change droughts enhanced storm ferocity and the1990s introduction of Monsanto ldquoRoundup Readyrdquo cropscapable of surviving herbicides that kill other weeds mdashincluding milkweed which monarchs need for breeding andas their sole food supply along their migratory routes mdash arethought to be the primary culprits

Here we argue environmental EMF should be addedto this list since many insects and other living species havesensitive receptors for EMF eg monarchs were found tohave light sensitive magnetoreceptors in their antennaethat serve as an inclination compass when daylight isabsent [16] RFR is also known to alter the time periodneeded for a butterfly to complete morphogenesis plusgastrulation and larval growth can be accelerated [17] Andthe devastating loss of pollinating insects like honey beesand other wild pollinators may also be related to environ-mental EMF (see ldquoInsectsrdquo below)

Anecdotally many people recall when there weresignificantly more insects and far more abundant wildlifeSince about 1980 there has been a steady almost imper-ceptible biodiversity diminishment among many speciesglobally [18ndash20] In 2018 scientists estimated that the

Levitt et al EMF and wildlife 3

largest king penguin colony shrank by 88 in just 35 years[21] due in major part to effects from climate change whileaccording to the International Scientific Committee forTuna and Tuna-like Species in the North Pacific Oceanover 97 of bluefin tuna have disappeared from theworldrsquos oceans primarily due to industrial overfishing butexacerbated by oil spills contamination and climatechange Tree and cave-dwelling bats until recently werecommon including in the Eastern United States Now withthe massive impacts from White-nosed Syndrome (a fatalbat fungal disease) annual wind-turbine bat collisionmortality estimated at nearly 1 million per year in the USalone [22 23] and pesticide use few bats are seen Batsspecies are also sensitive to EMF Impacts fromEMF as nowseen in extensive reviews add only yet another troublingvariable for all wildlife [24ndash36]

Since all food webs are uniquely tied together there arenegative cascading effects across all ecosystems Birds thateat insects are hard hit 8-in-10 partridges have disappearedfrom French farmlands while there has been a 50ndash80reduction in nightingales and turtledoves respectively in theUK Since 1980 the number of birds that typically inhabitEuropersquos farmlands has shrunk by 55 while in the last 17years French farmland-bird counts dropped by a full thirdIntensified agricultural practices are thought responsiblewith loss of insects being the largest contributor [12 37] Inthe United States of the 1027 species of migratory birdscurrently protected under the Migratory Bird Treaty Act of1918 anestimated40are indeclinebasedonbreedingbirdsurveys [38] Christmas Bird Counts [39] and other moni-toring tools [22 23] This trend is comparable to what ishappening globallyWhat role EMFplays in these declines isunclear but remains a disturbing possibility Nor do we un-derstand the limits of tolerance any given species has forenvironmental disturbance mdash some show high flexibilitywhile others thrive only within the narrowest ranges

One estimate of Earthrsquos species finds that since 1970wild animal populations have been reduced on average by60 Popularly called the ldquosixthmass extinctionrdquo [40] theterm connotes the sixth time in the Earthrsquos history thatlarge numbers of species have rapidly disappeared over arelatively short period this time due to human activity notasteroid strikes or volcanic activity Though not officiallyso-designated many now refer to this most recentgeologicecosystem period as the ldquoAnthropocenerdquo mdash theAge of Man [41ndash46]

Insect populations have been especially hard hit withextinctions eight times faster than that of mammals birdsand reptiles [12] Insect total mass is falling by an estimated25 per year suggesting they could vanish by the nextcentury And what affects insect populations affects

everything in the food web in one way or another Loss ofinsect diversity and abundance can cause devastating ef-fects throughout food webs and endanger entire ecosys-tems [12] In Europe Hallmann et al [47] found amore than75 decline over 27 years in total flying insect biomass in63 protected areas many throughout Germany There wasan 82 decline in mid-summer flying insect mass ManyEuropean insect speciesmigrate fromdistances as far awayas Africa The researchers noted that changes in weatherland use and habitat characteristics alone cannot explainthe overall decline and that there may be more than oneunrecognized factor involved in evaluating declines inoverall species abundance That unrecognized factor maybe the steadily rising ambient EMF that directly parallelsthese declines (see Part 1 Supplement 1)

Similar alarming invertebrate declines were discoveredin the Western Hemisphere in 2017 when American ento-mologist Bradford Lister after 40 years revisited the ElYunqueNational Forest in PuertoRico to followupona studybegun in 1976 [48] In the ensuing decades populations ofarthropods including numerous flying insects centipedesand spiders had fallen by 98 in El Yunque a pristinetropical rainforest within the US National Forest SystemInsectivoresmdash including birds lizards and toadsmdash showedsimilar declines with some species vanishing entirely Aftercontrolling for factors like habitat degradation or loss andpesticide use the researchers concluded that climate changewas the primary factor since the average maximum temper-ature in that rainforest had increased by 4 degF during thatperiod They did not factor in the large US military VLFinstallation in Aquada that communicates with submarinesall over the world or the multiple sweeping over-the-horizonphased array radar units aimed at Puerto Rico from coastalsites in the US that irradiate deep into that forest or themultiple NOAADoppler weather radar sites scattered all overthe small island to track hurricanes or the many cell towersthere too

These global declines are truly alarming with impli-cations for planetary health as well as human and wildlifeintegrity Many who study this say that climate changealone is not the only factor and that something new is goingon [47] The question is could steadily rising environ-mental EMF as one of the most ubiquitous but unrecog-nized new environmental genotoxins introduced since the1980s be contributing to these unprecedented specieslosses beginningwith insects but nowmanifesting in otherspecies too The upper microwave bands couple maxi-mally with some insects the size of fruit flies and arecapable of creating devastating resonance and other ef-fects Historically radiofrequency radiation (RFR) impactsto insects were among the first biological effects to be

4 Levitt et al EMF and wildlife

studied [49] with the hope of discovering new forms ofinsect control [50] All insect metamorphic developmentshave been studied including egg larva pupa and adultstages One hypothesis holds that some adult speciesare more sensitive than at larval stages because adultappendages act as conducting pathways to the body(see ldquoInsectsrdquo below)

It is these exact frequency bands between 30 kHz and3 GHz used in telecommunications technology that havebeen on the rise during this period And 5G is on the hori-zon which may specifically target insect populations (seePart 1)

Species sensitivity to EMFs

Other species have vastly more complex electromagneticsensing tools than humans as well as unique physiologiesthat evolved to sense weak fields Many species are highlysensitive to the Earthrsquos natural electromagnetic fields as wellas geographic and seasonal variations In fact it appears thatmost living things mdash including many species of mammalsbirds fish and bacteria mdash are tuned to the Earthrsquos electro-magnetic background in ways once considered as ldquosuper-powersrdquo but are now known to be physiological even asmechanisms are still imperfectly understood For examplemany animals have been observed sensing earthquakes longbeforehuman instrumentsdetect them including snakes andscorpions that seek shelter cattle that stampede birds thatsingat thewrong timesofday and female cats that franticallymove kittens [7]

This ability is likely due in part to numerous speciesreacting to changes in the Earthrsquos magnetic field andelectrostatic charges in the air detected through a naturallyoccurring mineral called magnetite found in many species[51 52] In fact honey bees are able to detect static mag-netic field fluctuations as weak as 26 nT against back-ground earth-strengthmagneticfields that aremuchhigher[53] and to sense weak alternating fields at frequencies of10 and 60 Hz [54] Magnetite reacts a million times morestrongly to external electromagnetic fields than any otherknown magnetic material Authors Kobayshi and Kirch-vink [52] and Kirchvink et al [53 54] hypothesized resultswere consistent with biophysical predictions of amagnetite-based magnetoreceptor Other mechanismslike radical pair mechanisms and cryptochromes may alsobe responsible (see ldquoMechanismsrdquo below)

Much has been written about magnetoreceptionmdash theterm used to describe how species sense electromagneticfieldsmdashwhich is well established but not well understoodMany species use information about the Earthrsquos natural

fields for migration mating food-finding homing nest-ing and numerous other activities Migratory bird species[55 56] honey bees [57] fish [58] mammals [59] bats [60]numerous insect species [61] mollusks [62] and evenbacteria [63] are known to sense Earthrsquos magnetic fields invarious ways Magnetoreception may enable some birdspecies to actually see the Earthrsquos fields [64]

Some insect and arachnid species (eg Trichobothria)can detect natural atmospheric electric fields [65] whichtrigger ballooning behaviormdash eg climbing to the highestplace letting out silk and traveling onwind currents usinghair-like Trichobothria that detects airborne vibrationscurrents and electrical charge Some have been found ashigh as 25mi (4 km) in the sky dispersing over hundreds ofkilometers Morley and Robert [65] found that the presenceof a weak natural vertical e-field elicited ballooningbehavior and takeoff in the spiders their mechano-sensoryhairs function as putative sensory receivers which areactivated by natural weak electric-fields in response toboth e-field and air-flow stimuli The researchers hypoth-esized that atmospheric electricity was key to the massmigration patterns of some arthropod fauna

Even soil nematodes (Caenorhabditis elegans) orient toearth-strength magnetic fields in their burrowing behav-iors and a recent study byVidal-Gadea [66] found thatweakstaticfields slightly above Earthrsquos naturalfields determinedstem cell regeneration in flatworms (Planaria) [67]

Large ruminant mammalian species also orient to theEarthrsquos fields Grazing cattle and deer were first observedaligning to geomagnetic field lines by Begall et al [68]Using satellite imagery field observations and measuringldquodeerbedsrdquo in snow they noted that domestic cattle acrossthe globe aswell as grazing and resting red (Cervus alphas)and roe (Capreolus capreolus) deer consistently align theirbody axis in a general northndashsouth direction and that roedeer also orient their heads northward when grazing orresting Burda et al [69] discovered however that man-made ELF-EMF disrupted the north-south alignment withthe geomagnetic field in resting cattle and roe deer whenthey found body orientation was random on pastures un-der or near power lines with the disturbed pattern dimin-ishing with distance from conductors Cattle exposed tovarious magnetic field patterns directly beneath or nearpower lines exhibited distinct patterns of alignment Theyconcluded there was evidence for magnetic sensation inlarge mammals as well as overt behavioral reactions toweak ELF-MF in vertebrates implying cellular and mo-lecular effects Slaby et al [70] also found cattle align alonga north-south axis but suggested that such alignment maydepend on herd density as the affect disappeared in herdswith higher numbers Fedrowitz [71] expanded this to

Levitt et al EMF and wildlife 5

include bovine sensitivity to other weak ELF-EMF frompowerlines but with observed effects due to combinedelectric and magnetic fields rather than the electric fieldexposure alone (see ldquoBovinesrdquobelow)

Cerveny et al [72] found red fox (Vulpes vulpes) usegeomagnetic fields during hunting Even domestic dogswere found by Hart et al [73] to be sensitive to small varia-tions in the Earthrsquos orientation in their excretion habitspreferring a general north-south axis for both defecation andurination depending on geomagnetic field changes AndNieszligner et al [74] found dogs and some other species mayactually ldquoseerdquo geomagneticfields through blue-light sensingphotoreceptor proteins in their eyes called cryptochromes

According to the USUK World Magnetic Model [75]sensitivity to the geomagnetic field may further complicateissues for migratory species (eg some turtles sea ani-mals birds and insects) because the Earthrsquos magneticnorth pole is shifting faster than at any time in humanhistory Compared to the period between 1900 and 1980 ithas greatly accelerated to about 30 mi (50 km) distance peryear mdash moving west from over Canadarsquos Ellesmere Islandits traditional allocation for most of recorded history mdashtoward Russia [76] Magnetic north fluctuates according tochanges in the Earthrsquosmolten core unlike true northwhichaligns according to the Earthrsquos axis This trend may indi-cate a coming pole reversal with north and south tradingplaces something that occurs approximately every400000 yearswith the last being about 780000 years agoSome animalsmaybe capable of recalibrating navigationalcues but that remains to be seen Since somemigratory birdspecies may see geomagnetic fields through special re-ceptor cells in their eyes and via other mechanisms theycould be thrown off course It is unclear how many otherspecies also see geomagnetic fields but some crustaceansand several insect species especially thosewith compoundeye structures consisting of thousands of ommatidiamdash tinyindependent photoreception units with a cornea lens andphotoreceptor cells that orient in different directions anddistinguish brightness and many more bands of color thanhumans mdash are good candidates Compared to single-aperture eyes compound eyes have a very large view anglethat can detect fast movement and in some cases lightpolarization

In aquatic environments some lakes have more than200 species of fish that use some form of electromagnetismto locate food and reproduce Electric eels can deliver a500-V zap to kill prey Sharks have an array of electro-magnetic sensors These include magnetic field receptorsin their mouths eyes that are 10 times more sensitive thanhumans and their perception of tiny electric neuronaldischarges from the moving muscles in prey (including

humans) guides their attackingfeeding behavior (seeldquoFishrdquobelow) Sharks are often attracted by low-levelelectromagnetic fields surrounding underwater electriccables and are sometimes electrocuted when they mistakethe conduit for living prey and bite into it Many fish havelateral lines on either side of their bodies that are composedof magnetite which allows fish to swim in synchronousschools [52]

Many other animals evolved special receptor organs todetect environmental EMF The duck-billed platypus(Ornithorhynchus anatinus) a semi-aquatic primitive egg-laying mammal has thousands of electric sensors on itsbill skin As noted in Lai [77] using these electroreceptorsand interacting with another type of mechanoreceptor aplatypus can detect an electric field of 20 μVcm [78] mdashequivalent to that produced by the muscles of a shrimpThe information is processed by the somatosensory cortexof the platypus to fix the location of prey This type ofelectroreception is common in the three species of mono-tremes platypus and long (Zaglossus bruijni) and short-bill (Tachyglossus aculeatus) echidna Electric fish (elas-mobranchs) emit EMF that covers a distance of severalcentimeters [79 80] This allows location of potential preyby comparing its electrical properties with that in its im-mediate vicinity Their electroreceptors have been shownto detect a field of 5 nVcm Such EMF-sensing systems arehighly sensitive and efficient but also highly vulnerable todisruption by unnatural fields Organisms that use thegeomagnetic field for migration have the capability notonly to detect the field but also the orientation of the field

Anthropogenic light frequencies affect wildlife in wayswe have only recently grasped Ecological studies havefound that artificial light-at-night is disrupting nocturnalanimals in devastating ways including disorientation anddisruption in breeding and migration cycles in turtlesflying insects birds butterflies and a host of other wildlifeincluding mammals [81ndash84] As much as 30 of nocturnalvertebrates and over 60 of invertebrates may be affectedby artificial light [85] Illumination reflected off of cloudsknown as ldquosky glowrdquo can produce unnaturally brightconditions at night from various wavelength spectra thatimpact different species with the potential to alter thebalance of species interactions [86 87] It has been foundthat changing the color of the light can help some speciesyet harm another [88] For instance low-pressure sodiumlights that havemore yellow in their spectrum reducemothdeaths around the bulbs but salamanders cannot navigatefrom one pond to the next under yellow or red light Somefrogs have been observed to freeze for hours even afterlights have been turned off and to suspend both feedingand reproduction [83]

6 Levitt et al EMF and wildlife

One of naturersquos greatmysteries involves ldquonatal homingbehaviorrdquo mdash the ability of some animal species to return totheir original location of birth in order to reproducesometimes over great distances Natal homing behavioris known in sea turtles [89] eels [90] and salmon [91]among other species The underlying mechanism thoughimperfectly understood involves such species ldquoremem-beringrdquo the geomagnetic field configurations of theirbirthplace via a process known as ldquoimprintingrdquo and thuscan locate and return to it even if they are thousands ofmileskilometers away at reproduction time Apparentlynewborns of these species are imprinted with the memoryof the intensity and the inclination angle of the localgeomagnetic field This information is then later used tolocate their place of birth where they return to breed

The question is whether man-made EMF could distortthis imprintingmemory in later locating the site For examplewhat if RFR-emitting facilities are locatednear turtle breedingsites Could that interfere with imprinting There is someevidence from Landler et al [92] of adverse effects in turtlesThe researchers found that RFR could disrupt a naturalorientation establish its own orientation and reversecompletely a natural orientation indicating a need forresearch to further investigate as we simply do not know thefull effects to other species from anthropogenic EMF

Energy conduction in differentspecies unique physiologies andmorphologies

The unique physiology and morphology of non-humanspecies create additional complexities For instancequadrapedal species with four feet on the ground havedifferent and potentially more efficient conductivity thanbipedal species with two feet One example is bovineheightened sensitivity to increased ground current nearhigh tension lines [93 94] and cell towers [95ndash97] Alsobodies that are predominately parallel to the groundwhich includes most four-legged mammals rather than aperpendicular upright gait conduct EMF in different waysthan vertical species like humans apes and other pri-mates Species that hug the ground like snakes sala-manders and frogs have unique exposures to groundcurrents especially on rainy nights when water as aconductivemedium can increase exposures [98] This maymake some species more sensitive to artificial groundcurrent caused by electric utility companies using the Earthas their neutral return back to the substation for excess

alternating current on their lines instead of running addi-tional neutral lines on utility poles [99]

Hair and whiskers and related appendages in variousspecies are known to detect small variations in electro-magnetic fields as well as water and weather alterations[100] In fact ants have been observed to use theirantennae as ldquoEMF antennasrdquo when subjected by re-searchers to external electromagnetic fields aligningthemselves to ldquochannelrdquo RFR away from the colony [7]Species such as birds as well as some insects with com-pound eyes structures can see vastly more colors thanhumans while cats dogs and owls for instance hearmany more sound frequencies at incredibly low levels

Magnetoreception mechanismselectroreceptor cells magnetitecryptochromesradical pairs

According to Lai [77] ldquohellipin order for an environmentalentity to affect the functions of an organism the followingcriteria have to be met the organism should be able todetect the entity the level of the entity should be similar tothose in the normal ambient environment which is gener-ally much lower than the level of the entity used inexperimental studies and the organism must haveresponse mechanisms tuned to certain parameters of theentity that allow immediate detection of the presence andchanges of the entity Thus a variation of the entity wouldbe detected as an aberrant input and trigger a responsereaction In order to understand how man-made EMF af-fects wildlife the above criteria must be consideredincluding multiple sensory mechanisms that vary fromspecies to speciesrdquo

The questions are How do diverse species detect weaknatural geomagnetic signals distinguish the subtle inter-nal microcurrent and magnetic fields inherent to allbiology from external fields then get beyond both internaland external background noise to make use of that elec-tromagnetic information

There are three primary mechanisms used to under-stand magnetoreception(1) Magnetic induction of weak electrical signals in

specialized sensory receptors [101](2) Magnetomechanical interactions with localized de-

posits of single-domain magnetite crystals [52 102103]

(3) Radical-pair photoreceptors which may be the mostplausible [104ndash111]

Levitt et al EMF and wildlife 7

In the induction model (mechanism 1) according to Lin[102] the first category of electrodynamic interactions withweak magnetic fields is epitomized by elasmobranchsincluding sharks rays and skates with heads that containlong jelly-filled canals with high electrical conductivityknown as the Ampullae of Lorenzini As these fish swimthrough the Earthrsquos geomagnetic lines of flux smallvoltage gradients are induced in these canals with electricfield detections as low as 05 μVm [101] The polarity of theinduced field in relation to the geomagnetic field providesdirectional cues for the fish However in birds insects andland-based animals such cells have not been foundindicating this may not be a universal mechanism butrather are environmentspecies-specific factors [111]

The magnetomechanical model (mechanism 2) in-volves the naturally occurring iron-based crystalline min-eral called magnetite found in most species [52] Itsfunction is most simply demonstrated in magnetotacticbacteria [63] with high iron content where biogenicmagnetite is manufactured in 20ndash30 single domain crystalchains [112] Orientation is patterned according to thegeomagnetic field Blakemore et al [113] found that mag-netotactic bacteria in the northern hemisphere migratetoward the north pole of the geomagnetic field whereas thesame strainsmigrate toward the South Pole in the southernhemisphere At the equator they are nearly equally dividedin north- and- south seeking orientations [114] And they allmigrate downward in response to the geomagnetic fieldrsquosvertical component which in aqueous environments maybe essential for their survival in bottom sediments

Among the many species where magnetite has beenfound include the cranium and neck muscles of pigeons[115 116] denticles of mollusks [117 118] and the abdom-inal area of bees [119] Tenforde [103] delineated otherspecies with localized magnetite including dolphinstuna salmon butterflies turtles mice and humans

The third mechanistic model (mechanism 3) gettingresearch attention today involves a complex free-radical-pair reaction and conversion of the forms of electrons(singlet-triplet inter-conversion) in a group of proteincompounds known as cryptochromes Cryptochromeshave been found in the retinas of nocturnal migratorysongbirds by Heyers et al [55] and Moller et al [56]showing complex communication with the brain fororientation when relying on magnetoreception Gegearet al [61] found cryptochromes to be a critical magneto-reception component in fruit flies (Drosophila mela-nogaster) As noted in Lai [77] cryptochrones are alsopresent in the retinas of some animals [120] RFR [121] andoscillating magnetic fields [122] have been reported todisrupt the migratory compass orientation in migratory

birds There are also reports that indicate the presence ofcryptochromes in plants which may be responsible for theeffect of EMF on plant growth [123] Cryptochromes are alsoknown to be involved with circadian rhythms [56 124] Foran excellent review on plausibility theories and com-plexities of cryptochromeradical pairs see Ritz et al [111]

Many species likely use a combination of thesemechanisms as well as more subtle influences as yet un-detected The vector of the geomagnetic field may providethe directional information while intensity andor incli-nation provide the positional information needed fororientation In behavioral studies [125 126]Wiltschko et alfound that birds used both magnetite and cryptochromemechanisms when they responded to a short strongmagnetic pulse capable of changing magnetization ofmagnetite particles while their orientation was light-dependent and easily disrupted by high-frequency mag-netic fields in the MHz range indicating radical pair pro-cesses These findings suggest that along withelectrophysiological and histological studies birds have aradical pair mechanism located in the right eye that pro-vides compass-like directional information while magne-tite in the upper beak senses magnetic intensity thusproviding positional information However Pakhomovet al [122] pointed out that the songbird magnetic compasscan be disrupted by an oscillating 1403-MHz magneticfield of 2ndash3 nT at a level that cannot be explained by theradical-pair mechanism

Light plays a significant role [127] which is of envi-ronmental concern today as more technology moves to-ward using the infrared bands for communications and theincrease of satellites create artificialunfamiliar star-likelights in the night sky that are potentially capable ofimpacting night migration patterns There is other evi-dence that species use a combination of photoreceptorsand magnetite-based magnetoreception As mentionedabove in birds the two mechanisms exist side by sidemediating different types of magnetic information asneeded such as flight on sunny vs cloudy days ornocturnal flights and they can be easily disrupted [106128ndash130] Birds may co-process visual information withmagnetic information and be able to distinguish betweenthe two [131 132] This function likely occurs in the eye orhigher avian brain areas via light-dependent informationprocessing and radical pair cryptochromes [131 133] Birdsrsquomagnetic compass is an inclination compass and RFRfields in the Larmor frequencies near 133 MHz were foundto disrupt birdsrsquo orientation in an extremely sensitiveresonance relationship Blue-light absorbing photopig-ment cryptochromes have been found in the retinas ofbirds RFR appears to directly interfere with the primary

8 Levitt et al EMF and wildlife

processes of magnetoreception and disable the aviancompass as long as the exposure is present [126 128]

Mammals have also demonstrated magnetoreceptionindicating radical-pair mechanisms Malkemper et al [134]found that the surface-dwelling wood mouse (Apodemussylvaticus) built nests in the northern and southern sectors ofa visually symmetrical circular arena using the ambientmagnetic field or in a field rotated by 90deg indicating theanimals usedmagnetic cuesWhen themicewere also testedin the ambient magnetic field with a superimposed radiofrequency magnetic field (100 nT 09 to 5 MHz frequencysweep) they changed preference from north-south to east-west nest building But unlike birds that have been foundsensitive to a constant Larmor frequency exposure at133 MHz that range had no effect on mice orientation In-dividual animal physiology clearly plays a role in howvarious species respondMalewski et al [135] also found thatthe Earthrsquos magnetic field acts as a common directional in-dicator in five species of subterranean digging rodents Andfor the first time research also found that human brainwaves exhibit a strong response to ecologically-relevant ro-tations of Earth-strength magnetic fields [136]

We need far better understanding of magneto-receptionrsquos neural cellular and molecular processesbecause the ultimate question is given our constant risingbackground levels of EMF is this ambient noise reaching atipping point beyond which species simply cannot ldquohearrdquoAre we artificially overwhelming living speciesrsquo ability tofunction with innate natural biological sensors thatevolved over eons in a far more ldquoelectro-silentrdquoworld Theelectroreception mechanisms described above mdash electro-receptors magnetite and cryptochroneradical-pairs mdashenable living organisms to detect the presence and imme-diate changes in environmental fields of very low intensityAnd thus they can be easily disturbed by the presence ofunfamiliar low-intensity man-made fields

Electrohypersensitivity in humans has also showninstantaneous response to EMF at low intensity [137] Ac-cording to Lai [77] one wonders whether the underlyingmechanisms of electrohypersensivity are similar to thosedescribed above Electrohypersensitivity may be a remnantof the evolutionary responses of living organisms to elec-tromagnetic fields mdash particularly magnetic fields mdash in theenvironment Similarities include responsiveness to verylow-field intensity the response is persistent and built intothe physiology of an organism and the response is imme-diate and reacts quickly to the fields Cryptochrome-freeradicalmechanismsmay be involved Some people aremoresensitive than others Perhaps non-sensitive people cantolerate and compensate for effects andor have lostresponsiveness to natural magnetic fields and thus have

becomeevolutionarily aberrant Electrosensitivity is an issuein need of more careful and systematic study and has yet tobe broadly highlightedas a health or publicwelfare concern

One recent theory by Johnsen et al [138] postulates thatmagnetoreception in animal species may be ldquonoisyrdquo mdashmeaning that the magnetic signal is small compared tothermal and other receptor noise for instance They specu-late that magnetoreception may serve as a redundant ldquoas-neededrdquo source of information otherwise animal specieswould use it as their primary source of information Manyspecies they note preferentially exploit non-magnetic cuesfirst if they are available despite the fact that the Earthrsquosgeomagnetic field is pervasive and ever-present Theyspeculate that magnetic receptors may thus be unable toinstantaneously attain highly precise magnetic informationand therefore more extensive time-averaging andor otherhigher-order neural processing of magnetic information isrequired This may render ldquohellipthe magnetic sense inefficientrelative to alternative cues that can be detected faster andwith less effortrdquo Magnetoreception may have been main-tained however they said by natural selection because thegeomagnetic field may sometimes be the only availablesource of directional andor positional information

We already know that some species use variousmechanisms to detect EMFs as noted throughout this pa-per With new environmental factors from anthropogeniccauses such as artificial light-at-night airwater pollutionclimate change impacting visibility as environmental cuesand rising background RFR mdash all of which can obscurenatural information mdash magnetoreception may in factbecomemore necessary as an evolutionary survival tool astime goes on not less

Other mechanisms of biologicalsignificance DNA mdash direct andindirect effects(See Part 2 Supplements 1 and 2for tables of ELF and RFR geneticsstudies)

A significant biological effect in any toxicology researchinvolves the basic genetics of an exposed organism Ge-netic effects consist mainly of gene expression chromatinconformational changes and genotoxicity All such effectscan influence normal physiological functions Relevant tothis paper is the fact that genetic effects are found at EMFlevels similar to those in ambient environments far below

Levitt et al EMF and wildlife 9

levels from communication devices and infrastructure (seePart 1 Supplement 1)

DNA the fundamental building block of all life is amolecular double helix that is coiled twisted and foldedwithin the nucleus of each living cell It is essentiallyidentical among species with variations only in numberand specific genes along chromosomes on DNArsquos twistedchains that distinguish various species and their charac-teristics from one another DNA damage repeatedly seen inone species can therefore be extrapolated to other speciesalthough not all species react the same to external stimuli

Many factors both endogenous and exogenousdamage DNA which is then normally repaired by DNAenzymes But an absence of adequate repair can result inthe accumulation of damaged DNA which will eventuallylead to aging cell death (apotosis) andor cancer DNAbreaks occur as both single and double strand eventsdouble strand breaks are difficult to repair correctly andcan lead to mutations DNA damage from endogenousfactors can include free radical formation from mitochon-drial respiration and metabolism exogenous factorsinclude chemicals ionizing and nonionizing radiationand ultra violet light among others [139]

In several early studies Lai and Singh [140 141] foundboth double and single strandDNAbreaks in the brain cellsof rats exposed to RFR for 2 h at 2450MHz andwhole bodySAR levels of 06 and 12 Wkg The effects were interest-ingly blocked by antioxidants [142] suggesting free radicalinvolvement which could indicate an indirect cause forDNA damage (see below) The low-intensity genetic effectslisted in Part 2 Supplements 1 and 2 are at 01 Wkg andless Therefore the Lai and Singh [140 141] RFR studies arenot included in those Supplements Very similar effectshave also been found by Lai and Singh [143 144] with60-Hz magnetic field exposure

There has also been much study of ELF genetic effectsAs discussed in Phillips et al [139] numerous studiesfound that ELF-EMF leads to DNA damage [143ndash158] Twostudies [159 160] showed that ELF also affects DNA repairmechanisms Sarimov et al [161] found chromatin confor-mational changes in human lymphocytes exposed to a50-Hz magnetic field at 5ndash20 microT EMF-induced changes incellular free radicals are also well studied [77 162]

Others investigated DNA damage early on but withoutthe availability of todayrsquos more sensitive assays Sarkaret al [163] exposed mice to 2450-MHz microwaves at apower density of 1 mWcm2 for 2 hday over 120 150 and200 days They found DNA rearrangement in the testis andbrain of exposed animals that suggested DNA strandbreakage Phillips et al [164] were the first to use the cometassay to study two different forms of cell phone signals mdash

multi-frequency time division multiple access (TDMA) andintegrated digital enhanced network (iDEN) mdash on DNAdamage in Molt-4 human lymphoblastoid cells usingrelatively low intensities of 24ndash26 Wg for 2ndash21 h Theauthors reported seeming conflicting increases and de-creases in DNA damage depending on the type of signalstudied as well as the intensity and duration of exposureThey speculated the fields could affect DNA repair mech-anisms in cells accounting for the conflicting results

In a recent literature review of EMF genetic effects byLai [165] analysis found more research papers reportingeffects than no effects For RFR 224 studies (65) showedgenetic effects while 122 publications (35) found no ef-fects For ELF and static-EMF studies 160 studies (77)found effectswhile in 43 studies (23) no effectswere seen

Research now points to the duration signaling charac-teristics and type of exposure as the determining factors inpotential damage [164 166] not the traditional demarcationbetween ionizing and nonionzing radiation Long-term low-level nonionizing radiation exposures common today arethought to be as detrimental to living cells as are short-termhigh-intensity exposures from ionizing radiation Effectsmay just take longer to manifest [167] Nonionizing EMF atenvironmental levels does cause genetic damage Thesehave also been shown in humans exposed to environmentallevels of EMF in both ELF and RFR ranges [168ndash171]Conceivably similar genetic effects could happen in otherspecies living in similar environments

This body of genetics work goes against the pervasivemyth that low-level low-intensity nonionizing radiationcannot cause detrimental genetic effects That premise is infact the bedrock belief upon which vested interests andgovernment agencies rely in support of current exposurestandards But in fact biological systems are far morecomplex than physics models can ever predict [6 8 172] Anew biological model is needed because todayrsquos exposuresno longer fit that framework [173] for humans and wildlifeEnough research now indicates a reassessment is neededperhaps including the very physics model used to backthose traditional approaches (see Part 1)

Direct mechanisms DNA as fractalantennas cell membranes ionchannels

DNA as fractal antennas

There are several likely mechanisms for DNA damage fromnonionizing radiation far below heating thresholds both

10 Levitt et al EMF and wildlife

direct and indirect intracellular intercellular and extra-cellular Suchmechanisms potentially apply to all wildlifeOne direct mechanism theorizes that DNA itself acts as afractal antenna for EMFRFR [174] capable of receivinginformation from exogenous exposures

According to Blank and Goodman [174] DNA hasinteresting electrical characteristics due to its uniquestructure of intertwined strands connected by rungs ofmolecules called nucleotides (also called bases) with eachrung composed of two nucleotides (one from each strand)in bonded pairs The nucleotides are held together byhydrogen bonds in close proximity that results in a strongattraction between the two strands There are electrons onboth molecular surfaces making the symmetrical nucleo-tides capable of conducting electron current along theentire DNA chain a phenomenon called electron transferThis makes DNA a most efficient electrical conductorsomething not lost on nanotechnology researchers

DNAmay also act as an efficient fractal antenna due toits tightly packed shape within the cell nucleus Blank andGoodman [174] characterized DNA properties in differentfrequency ranges and considered electronic conductionwithin DNArsquos compact construction in the nucleus Theyconcluded that the wide frequency range of observed in-teractions seen with EMF is the functional characteristic ofa fractal antenna and that DNA itself possesses the twostructural characteristics of fractal antennas mdash electronicconduction and self symmetry They noted that theseproperties contribute to greater reactivity of DNAwith EMFin the environment and that direct DNA damage couldaccount for cancer increases as well as the many otherbiological effects seen with EMF exposures

A fractal is a self-repetitive pattern of sometimes geo-metric shapes marked by a larger originating design pro-gressing to small identical designs with a potentiallyunlimited periphery Each part of the shape looks like thewhole shape Fractal designs are quite common in natureeg in snailmollusk shells some deciduous tree leaves andconifer needles pine cones many flowering plants somereptile scales bird feathers and animal fur patterns snow-flakes and crystals forming on cold winter glass windowsMineralsmdash both inert and biologicalmdash can also be fractals

The varying sizes within fractals are what make theminherently multi-frequency By mimicking nature repeti-tive fractal patterns are also designed into mechanicaltransceiver antennas that radiate in multiband frequencieswith more or less efficiency [175] Cell phones WiFi digitalTV and many other transceivers use fractal antennas tooperate

The complex twisted shape and coiled structure ofDNA mdash small coils coiled into larger coils or coiled coils

which Blank and Goodman [174] note that no matter howfar you zoom in or out the shape looks the same mdash is theexact structure of a fractal that maximizes the length of anantenna within a compact space while boosting multi-frequency signals As such DNAmay be acting as a hiddenintracellular biological fractal capable of interacting withexogenous EMF across a range of frequencies In fact oneof DNArsquos fundamental functions may be specifically tointeract with exogenous natural energy and as suchmay bemore sensitive to EMF than other larger protein moleculeswithin any living system Once thought safely tucked awayand protected within the nucleus DNA may be acting as amost efficient electrical conductor at the nexus of all lifeThis interesting theory unfortunately has not been fol-lowed up by others to test its biological validity althoughfractals have been mimicked widely in technology

Cell membranesion channels

Another direct effect from EMF is at the cell membraneitself While DNA is lifersquos fundamental building block cellsare DNArsquos complex electron-coherent architecturalexpression The cellrsquos membrane is far more than just aboundary It is rather the most important ordering tool inthe biological space between intracellular and extracel-lular activities ldquohellip a window through which a unitarybiological element can sense its chemical and electricalenvironmentrdquo [176] And it is replete with microcurrent

The cellrsquos outer surface containsmolecules that receiveinnumerable electrochemical signals from extracellularactivities Specific binding portals on the cell membraneset in motion a sequence leading to phosphorylation ofspecific enzymes that activate proteins for cellular lsquoworkrsquoThat includes everything from information processing inthe central nervous system mechanical functions such asmuscle movements nutrient metabolism and the defensework of the immune system amongmany others includingthe production of enzymes hormones antibodies andneurotransmitters [177] Complex microcurrent signalingpathways exist from the cellrsquos outside to the inside viaprotein intramembraneous particles in the phospholipidplasma membrane These convey information on externalstimuli to the cellrsquos interior to allow cellular function

The cell membrane also has electrical propertiesMicrocurrent constantly moves from the interior to theexterior and vice versa of the cell membrane According toAdey and Sheppard [176] some of these properties influ-ence proteins that form voltage gatedmembrane channelswhich is one way that cells control ion flow andmembraneelectromagnetic potential essential to life There are

Levitt et al EMF and wildlife 11

specific windows that react according to frequencyamplitude and duration differences indicating anonlinear and non-equilibrium character to exogenousexposures on cells [177ndash185]

Some pulsed fields are more biologically active thannon-pulsed fields and different forms of pulsing also createdifferent effects As far back as 1983 Goodman et al [186]found pulsed weak electromagnetic fields modified bio-logical processes via DNA transcription when a repetitivesingle pulse and the repetitive pulse train were used Thesingle pulse increased the specific activity of messengerRNA after 15 and 45 min while the pulse train increasedspecific activity only after 45 min of exposure Digitaltechnology simulates pulsing and is the most commonform of environmental exposure today

Cellular calcium ion channels have long been of in-terest and may be particularly sensitive targets for EMFsdue to possible increased calcium flux through the chan-nels which can lead to secondary responses mediatedthrough Ca2+calmodulin stimulation of nitric oxide syn-thesis calcium signaling elevated nitric oxide (NO) NOsignaling peroxynitrite free radical formation andoxidative stress mdash many with implications to DNA as hy-pothesized by Pall [187] Calcium is essential to signaltransduction between cells and is significant to everythingfrom metabolism bonecellblood regeneration hormoneproduction and neurotransmissions among many othersThese cellular calcium responses to EMF indicate an arti-ficial change in the signaling processes at the cell mem-branemdash considered a switchboard for information betweenthe exterior environment and intracellular activities thatguide cell differentiation and control growth [188]

Pall [187] cited 23 studies of effects to voltage gatedcalcium channels (VGCC) and noted nonthermal mecha-nisms were the most likely since many studies showed ef-fects were blocked by calcium channel blockers (widelyprescribed for heart irregularities having nothing to dowith thermal issues) Pall [189] noted that many otherstudies showed EMF changes in calcium fluxes and intra-cellular calcium signaling He hypothesized that alter-ations in intracellular calciumactivitymay explain some ofthe myriad biological effects seen with EMF exposureincluding oxidative stress DNA breaks some cancersinfertility hormonal alterations cardiac irregularities anddiverse neuropsychiatric effects These end points needfurther study and verification

There is much to be learned about calcium effects asstudies are contradictory Changes in free radicals (seebelow) also affect calcium metabolism There are morestudies showing EMF effects on free radicals than calciumchanges Calcium activates the nitric oxide free radical

pathway but there are only a few studies of this pathwayfollowing EMF exposure mdash less than 5 of EMF-oxidativechange studies are on nitric oxide mechanisms Also ofinterest is the fact that power density and frequency win-dows were seen in early research at rising harmonic in-crements along the electromagnetic spectrum beginning inthe ELF bands [190ndash195] Observed effects were quite dra-matic in what researchers described as calcium efflux orlsquodumpingrsquo from cells The most dramatic effects were seenat 180 Hz in the ELF range This appears to contradict Pallrsquoswork [189] cited above as increased calcium efflux is theopposite of what Pallrsquos hypothesis would predict egcalcium influx Withmore research both calcium influx andefflux effects may be found to be caused by different vari-ables andor EMF exposures

In addition exogenous signaling characteristics arealso important to how cells react to both ELF and RFRranges Building on the work that demonstrated carrierwaves of 50 and 147 MHz when sinusoidally amplitudemodulated at 16 Hz ELF in in vitro chick brain tissue [190191] and in live awake cat brain models [196] that createdfrequency windows for calcium efflux Blackman et al[194] additionally found that signaling characteristicswerealso significant Research showed that calcium effluxoccurred only when tissue samples are exposed to specificintensity ranges of an ELF-modulated carrier wave un-modulated carrier waves did not affect ion efflux Black-man et al [194] further wrote that cells may be capable ofdemodulating signals The authors reported that 16-Hz si-nusoidal fields in the absence of a carrier wave altered theefflux rate of calcium ions and showed a frequency-dependent field-induced enhancement of calcium-ionefflux within the ranges 5ndash75 Vm and 35ndash50 Vm (peak-to-peak incident field in air) with no enhancement withinthe ranges 1ndash2 10ndash30 and 60ndash70 Vm This body of workindicates that living cells interact with and are capable oftaking direction from exogenous fields in far more com-plex ways than ever imagined at intensities barely abovebackground levels This work may be particularly impor-tant to new technology that turns previously wired ELFfrequencies into wireless applications such as ldquowirelesselectricityrdquo to charge electric cars

Blackman et al [197] found for the first time a linkbetween the ELFEMF being studied and the density of thenatural local geomagnetic field (LGF) in the production of abiological response Calcium efflux changes could bemanipulated by controlling the LGF along with ELF andRF-EMF exposures In a local geomagnetic field at a densityof 38 μT 15- and 45-Hz electromagnetic signals had beenshown to induce calcium ion efflux from the exposed tis-sues whereas 1- and- 30-Hz signals did not Bawin and

12 Levitt et al EMF and wildlife

Adey [190] found a reduction in efflux when using anelectric field Blackman et al [194] found an increase whenusing an electromagnetic field thus identifyingisolatingfor the first time the significance of the magnetic fieldcomponent in exposure parameters Building on the win-dow ranges noted above Blackman et al [197] demon-strated that the enhanced calcium efflux field-induced15-Hz signal could be rendered ineffective when the LGF isreduced to 19 μT with Helmholtz coils In addition theineffective 30-Hz signal became effective when the LGFwas altered to k253 μT or to +76 μT The results demon-strated that the net intensity of the local geomagnetic field isan important cofactor in biological response and a poten-tially hidden variable in research The results they notedappear to describe a resonance-like relationship in whichthe frequency of the electromagnetic field can induce achange in calcium efflux proportional to LGF density (seeLiboff [198 199] below for more detail)

The bottom line is that changes of this magnitude atthe cellular levelmdash be it directly to DNAwithin the nucleusor via voltage gated channels at the cellrsquos membranemdash canlead to direct effects on DNAwithin and across species Theevidence cited above illustrates the degree likelihood andvariety of impacts from EMF directly on cellular physiologythat are capable of affecting DNA in all living systems inmyriad ways

Indirect mechanisms free radicalsstress proteins resonance Earthrsquosgeomagnetic fields

Free radicals

An indirect or secondary mechanism for DNA damagewouldbe through free radical formationwithin cellswhich isthe most consistently reported with both ELF and RFR ex-posures under many different conditions in biological sys-tems According to Phillips et al [139] free radicals may alsointeractwithmetals like iron [142 151 152 158] andplay a rolein genotoxic effects from something called the Fenton ef-fect mdash a process ldquohellipcatalyzed by iron in which hydrogenperoxide a product of oxidative respiration in the mito-chondria is converted into hydroxyl free radicals which arevery potent and cytotoxic moleculesrdquo [139]

The significance of free radical processes may even-tually answer some questions regarding how EMF interactswith biological systems There are about 200ndash300 papersshowing EMF effects on free radicals [77 168 200] Free

radicals are important compounds involved in numerousbiological functions that affect many species Increases infree radicals explain effects from damage to macromole-cules such as DNA protein and membrane lipidsincreased heat shock proteins neurodegenerative dis-eases and many more

Yakymenko et al [168] published a review on oxidativestress from low-level RFR and found induced molecular ef-fects in living cells including significant activation of keypathways generating reactive oxygen species (ROS) activa-tion of peroxidation oxidative damage in DNA and changesin the activity of antioxidant enzymes In 100 peer-reviewedstudies 93 confirmed that RFR induced oxidative effects inbiological systems and that their involvement in cellsignaling pathways could explain a high pathogenic rangeof biologicalhealth effects They concluded that low-intensity RFR should be recognized as one of the primarymechanisms of biological activity of nonionizing radiationIn a follow-up study Yakymenko et al [200] investigatedthe oxidative and mutagenic effects of low intensity GSM1800 MHz RFR on developing quail embryos exposed inovo (032 μWcm2 48 s On 12 s Off) during 5 days before and14 days through the incubation period They found statisti-cally significant oxidative effects in embryonic cells thatincluded a 2-fold increase in superoxide generation rate an85 increase in nitrogen oxide generation and oxidativedamage to DNA up to twice the increased levels of 8-oxo-dGin cells of 1-day old chicks RFR exposure almost doubledembryo mortality and was statistically significant Theyconcluded that such exposures should be recognized as arisk factor for living cells including embryonic integrity

Lai [77] focused a review on static magnetic fieldELF-EMF and found that changes in free radical activitiesare one of the most consistent effects Such changes canaffect numerous physiological functions including DNAdamage immune system and inflammatory response cellproliferation and differentiation wound healing neuralelectrical activities and behavior Given that many specieshave proven sensitive to natural static geomagnetic fieldsand use such information in critical survival skills somewildlife species may also be adversely affected via freeradical alterations from anthropogenic exposures But Lai[77] noted the inherent contradictions from EMF-inducedchanges in free radicals particularly on cell proliferationand differentiation since those processes can affect cancerdevelopment as well as growth and development Inducedfree-radical changes may therefore have therapeutic ap-plications in killing cancer cells via the generation of thehighly cytotoxic hydroxyl free radical by the Fenton Re-action (noted above) thereby creating a non-invasive low-side-effect cancer therapy

Levitt et al EMF and wildlife 13

Stress proteins

Another potentially indirect effect to DNA is via proteinsynthesis required by all cells to function A living animalconverts animal and plant proteins that it ingests into otherproteins needed for lifersquos activities mdash antibodies forinstance are a self-manufactured protein DNA is critical toprotein synthesis and can create in humans about 25000different kinds of proteins with which the body can thencreate 2000000 types in order to fully function

There are many different classes of proteins Theseinclude stress proteins stimulated by potentially harmfulenvironmental factors to help cells cope and repair damagedue to factors like acute temperatures changes in oxygenlevels chemicalsheavy metals exposure viralbacterialinfections ultraviolet light and other ionizing andnonionizing radiation exposures [124]

The presence of stress proteins indicates healthy repairaction by an organism and is considered beneficial up to apoint as a protective mechanism According to Blank andGoodman [201] ldquoThe 20 different stress protein families areevolutionarily conserved and act as lsquochaperonesrsquo in the cellwhen they lsquohelprsquo repair and refold damaged proteins andtransport them across cell membranes Induction of thestress response involves activation of DNArdquo Stress proteinsare also considered a yardstick to determine what livingcells experience as stress that requires remediation in thefirst placemdash something not always obvious especiallywithsubtle environmental exposures like low-level EMF barelyabove natural background levels

Whether an effect is thermal or nonthermal adverse orsimply observed biologically has been subject to fiercedebate for decades thus tissue-heating DNA pathways arealso central to this paper Heat as a cellular stressor wasfirst observed in the 1960s by Italian researcher FerruccioRitossa in fruit flies (D melanogaster) when experimentaltemperatures were accidentally raised by a few degreesand he observed enlarged chromosomes at particular sites(Drosophilae are often used in research because they onlyhave four pairs of chromosomes are relatively easy toworkwith have a fast breeding cycle and lay numerous eggs)As cited in Blank [124] as Ritossarsquos observation becamebetter understood with effects subsequently seen overdecades in animals plants and yeast cells it came to becalled the ldquoheat shock responserdquo Extensive researchestablished that the heat shock response lead to the for-mation of a unique protein class mdash heat shock proteins(HSP) that repair other proteins from potentially fataltemperature damage as well as assist cells to be morethermo-tolerant Research has gone on to prove that cells

produce other similar proteins to various stressors nowgenerally called stress proteins but most are still catego-rized as ldquoHSPrdquo from the original demarcation

Goodman and Blank [202 203] found that EMF is acellular stressor even at low intensities in the absence ofelevated temperatures They found the protein distributionpatterns synthesized in response to ELF-EMF resembledthose of heat shock with the same sequence of changes eventhough the energy of the two stimuli differed bymany ordersof magnitude Their results indicated that ELF-EMF stimu-lates a similar gene expression pathway as that of thermalshock and is itself a cellular stressor Of particular signifi-cance is the fact that over-expression of stress genes is foundin a number of human tumors and is characteristic of a va-riety of neoplasia [202] Increased stress proteins are seen innumerous animal model studies pertinent to wildlife

Blank and Goodman [201] further noted that both ELFand RFR activate the cellular stress response despite thelarge energy difference between them that the samecellular pathways respond in both frequency ranges andthat models suggest that EMF can interact directly withelectrons in DNA They note that low energy EMF interactswith DNA to induce the stress response while the increasedenergy in RFR can lead to DNA strand breaks As such thismakes the stress response a frequency-dependent direct andindirect cause of DNA damage mdash a significant finding Theyconcluded that exposure standards should not be based onexposure intensity alone but on biological responses longbefore thermal thresholds are met or crossed

Resonance and geomagnetic fields

There are other important direct and indirect ways that EMFsinteractwith and effect biological systems includingvariousforms of resonance mdash cyclotron electron paramagneticnuclear and stochastic mdash as well as through inherentlyproduced biological materials such as magnetite found inbird brains and many other species (see below)

Resonance is the phenomenon that occurs when acertain aspect of a force (like a frequency wave) matches aphysical characteristic (like a cell or whole living organ-ism) and the power inherent in the force is transferred tothe physical object causing it to resonate or vibrate Withinthe object the resonance is self-perpetuating The classicexample is of an opera singer hitting high C in the presenceof a crystal goblet for a sustained period until it shatters

Following the work of Blackman et al [197] who foundthe Earthrsquos local geomagnetic fields (LGF) could influencecalcium ions moving through membrane channels (see

14 Levitt et al EMF and wildlife

above) Liboff [198 199] proposed that cyclotron resonancewas a plausible mechanism for coupling interactions be-tween the LGM and living cells Liboff found cyclotronresonance consistent with other indications that showedmany membrane channels have helical configurationsthat the model could apply to other circulating chargedcomponents within the cell and that cyclotron resonancecould lead to direct resonant electromagnetic energytransfer to selected cell compartments

All resonance is based on a relationship Cyclotron reso-nance is based on the relationship between a constant mag-netic field and an oscillating (time-varying) electric ormagnetic field that can affect the motion of charged particlessuch as ions some molecules electrons atomic nuclei orDNA in living tissue Living systems are filled with chargedparticles necessary for life including calcium sodiumlithium and potassium ions that all pass through the cellmembrane and are capable of affecting DNA Cyclotronresonance occurs when an ion is exposed to a steady mag-netic field (such as the Earthrsquos) which causes the ion to movein a circular orbit at a right angle to the field The speed of theorbit is determined by the charge andmass of the ion and thestrength of themagnetic field If an electric field is added thatoscillates at exactly the same frequency and that is also at aright angle to the magnetic field energy will be transferredfrom the electric field to the ion causing it tomove faster Thesame effect can be created by applying an additional mag-netic field parallel to the constant magnetic field This isimportant because it provides aplausiblemechanism forhowliving cells interact with both natural and artificial fields andexplainshowvanishingly low levels of EMFs cancreatemajorbiological activity when concentrated on ion particles It alsopoints to living systemsrsquo ability to demodulate mdash or take di-rection frommdash certain aspects of electromagnetic informationfrom both natural and artificial exposures [7] Resonanceshould not be underestimated It applies to all frequenciesand is not based on power density alone

Another subtle energy relationship in biology is calledstochastic resonance that has been determined to be sig-nificant in how various species interact with their naturalenvironments in some instances for their survival Sto-chastic resonance is a phenomenon where a signal belownormal sensing can be boosted by adding wide-spectrumwhite noise signals The frequencies in the white noise thatmatch the original signalrsquos frequencies will resonate witheach other and amplify the original signal while notamplifying the rest of thewhite noise This increase inwhatis called the signal-to-noise ratio makes the original signalmore prominent Some fish for instance can ldquohearrdquopredators better in the noise of running water than in stillwater due to stochastic resonance (see ldquoFishrdquo below)

The signal-to-noise ratio has been a prominent aspectof EMF research with some scientists long holding thatenergy exposures below the bodyrsquos natural signal-to-noiseratio could not possibly damage living tissue But the mostrecent research that finds effects to DNA from lowintensity EMF indicates that many variables affect biolog-ical processes often in nonlinear patterns far below thesignal-to-noise ratio Some of the most cutting edgeresearch mdash with an eye toward treating human in uterobirth defects and adult limb regeneration mdash is being donebymanipulating the electric charge across cell membranes(called membrane potential) via intentional manipulationof genes that form ion channels Pai et al [204] found thatby putting ion channels into cells to raise the voltage up ordown they could control the size and location of the brainin embryonic African clawed frogs (Xenopus laevis) thusdemonstrating the importance of microcurrents on mem-brane potential in growth and development The researchgroup also studied endogenous bioelectricity on clawedfrog brain patterning during embryogenesis noting thatearly frog embryos exhibit a characteristic hyperpolar-ization of cells lining the neural tube Disruption of thisspatial gradient of the transmembrane potential (Vmem)diminished or eliminated the expression of early brainmarkers in frogs causing anatomical mispatterningincluding absent or malformed regions of the brain Thiseffect was mediated by voltage-gated calcium signalingand gap-junctional communication The authors hypoth-esized that voltage modulation is a tractable strategy forintervention in certain classes of birth defects in humansbut they did not make the leap to potential environmentaldamage to other species from such ambient exposures

In general whether direct indirect or synergistic tounderstand ambient effects to wildlife one also needs toknow if effects are cumulative what compensatorymechanisms a species may have and when or if homeo-stasis will deteriorate to the point of no return [205] Inlooking at environmental contaminants we have histor-ically focused on chemicals for both direct and indirecteffects such as endocrine disruption But primary bio-logical manifestation is more physical than chemicalsince the only thing that distinguishes one chemical fromanother on the Periodic Table is the amount of electronsbeing traded up and down on the scale Chemicals areactually secondary manifestations of initial atomic prin-ciples not the other way around Plus the synergisticeffects of the Earthrsquos natural fields can no longer be dis-missed as an interesting artifact that is not biologicallyactive or relevant All living systems are first and foremostexpressions of biological energy in various states ofrelationship

Levitt et al EMF and wildlife 15

For a Table of more low-level effects studies on DNAsee Part 2 Supplements 1 and 2

What the studies show

The literature is voluminous on EMF effects to nonhumanspecies goingbackat least to the1930susingmodernmethodsof inquiry We have after all been using animal plant andmicrobial models in experiments for decades We may in factknow less about effects to humans than to other species

In this paper we focused on exposures common intodayrsquos environment In Part 1 Rising Background Levelswe defined low level RFR as power density of 0001 mWcm2 (1 μWcm2) or a SAR of 0001 Wkg Part 2 Supple-ments 3 and 4 contain extensive tables with pertinentstudies that apply to fauna and flora respectively Thesections that follow in Part 2 on individual species includeselected studies of particular interest to how EMF coupleswith and potentially affects wildlife In most studies asillustrated in Part 2 Supplement 3 the intensity of theincident EMF was provided in μWcm2 or Vm To beconsistent throughout the paper we converted intensity inthe studies to μWcm2 However such conversion (ie Vmto μWcm2) tends to overestimate the exposure level anddoes not represent the full picture Therefore where studiesprovided the amount of energy absorbed eg the specificabsorption rate (SAR) they were also included in Supple-ment 3 (inWkg) Very low levels of energy absorption haveshown effects in all living organisms studied

Levitt and Lai [167] reported numerous biological ef-fects fromRFR at very low intensities and SARs comparableto far-field exposures within 197ndash492 ft (60ndash150 m) fromcell towers Included were in vivo and in vitro low-intensityRFR studies Effects included genetic growth and repro-ductive changes increased permeability of the blood brainbarrier changes in stress proteins behavioral responsesand molecular cellular genetic and metabolic alter-ations All are applicable to migratory birds mammalsreptiles and other wildlife and to plant communities andto far-field exposures in general (An update of that tableappears in Part 2 Supplement 3) It is apparent that envi-ronmental levels of RFR can elicit biologicalhealth effectsin living organisms Although there are not enough data onlow-intensity effects of static ELF-EMF to formulate aseparate table some effects of low-intensity static ELF-EMFare also described throughout this paper ELF genotoxiceffects can be found in Part 2 Supplement 2 and ELF inflora are also listed separately in Part 2 Supplement 4

Effects however do not easily translate from the lab-oratory to the field Cucurachi et al [31] reported on 113

studies with a limited number of ecological studies Themajority were conducted in laboratory settings using birdembryos or eggs small rodents and plants In 65 of thestudies effects from EMF (50 of the animal studies andabout 75 of the plant studies) were found at both highand low intensities indicating broad potential effectsBut lack of standardization among the studies and limitedsampling size made generalizing results from organism toecosystem difficult The researchers concluded that due tothe number of variables no clear dosendashresponse relation-ship could be determined Nevertheless effects from somestudies were well documented and can serve as predictorsfor effects to wild migratory birds and other wildlife

As noted elsewhere throughout this paper living or-ganisms can sense and react to very low-intensity electro-magnetic fields necessary for their survival as seen forinstance in studies by Nicholls and Racey [206 207] onbats andmany others Bats are already in serious trouble inNorth America from white-nosed syndrome and commer-cial wind turbine blade collisions Due to the increased useof tracking radars for bird and bat studies impacts willlikely only increase [22 23] Presence of low levels of RFRfrom tracking radars could adversely affect bat foragingactivity which in turn could affect the composition of in-sect populations in the vicinity Many insects includinghoney bees (Apis mellifera var) and butterflies also dependon the Earthrsquos electromagnetic fields for orientation andforaging Presence of exogenous RFR can disturb thesefunctions This is particularly relevant for pollinator in-sects such as bees and butterflies Pollinators are essentialin producing commercial crops for human consumptionincluding almonds apples pears cherries numerousberry crops citrus fruits melons tomatoes sunflowerssoybeans and much more The strongest disruptive effectto insect pollinators occurs at 12 MHz known as the Larmorfrequency [208] which is related to radical pair resonanceand superoxide radical formation This is an importantindication that effects from RFR are frequency-dependent

Lai [77] citing Shepherd et al [209] noted that EMFcan disrupt the directional sense in insects The fact thatmany animals are able to differentiate the north and southpoles of a magnetic field known as the polarity compass[68 73 134 210 211] indicates they are susceptible tohaving that important sense impaired These polaritycompass traits confer survival competitiveness to organ-isms but are of particular concern since directional cuescan be easily disturbed by man-made EMF [69 134 212]

Bird migration also depends on proper sensing andorientation to natural electromagnetic fields A study byEngels et al [213] showed that magnetic noise at 2 kHzndash9 MHz (within the range of AM radio transmission) could

16 Levitt et al EMF and wildlife

disrupt magnetic compass orientation in migratory Euro-pean Robins (Erithacus rubecula) The disruption can occurat a vanishingly low levelof001Vm or00000265μWcm2Similar effects of RFR interference on magnetoreceptionhave also been reported in a night-migratory songbird [214]and the European Robin [126] Migration is already a taxingand dangerous activity for birds adding another potentialnegative impact to bird survival is troubling

Lai [77] also noted that another consideration is theldquonatal homing behaviorrdquo exhibited in some animals thatreturn to their natal birth places to reproduce Theseinclude sea turtles [89] eels [90] and salmon [91] New-borns of these animals are imprinted with the memory ofthe intensity and the inclination angle of the localgeomagnetic field later used to locate their place of birthwhen they return to breed There are indications that man-made EMF can distort this imprinting memory to locate thesite (see ldquoFishrdquo and ldquoTurtlesrdquobelow) This has importantconsequences to the survival of particular species since itinterrupts their reproductive processes

It is clear that biological effects can occur at levels ofman-made RFR in our present environment therebyconceivably altering delicate ecosystems from a largelyunrecognized danger

Mammals

The majority of EMF laboratory research some going backto the 1800s has been conducted on a variety of mammalspecies using mice rats rabbits monkeys pigs dogs andothers (The second and third most used models are oninsects and yeast respectively) Thus with varying degreesof confidence we know a significant amount about howenergy couples with and affects laboratory mammalianspecies across a range of frequencies However this evi-dence does not automatically transfer at the same confi-dence level regarding how this vast body of researchapplies to wildlife including mammalian species

There is unfortunately a dearth of field research onEMF effects to wildlife Referenced below however aremany potential indicator studies The effects seen includereproductive behavioral mating growth hormonalcellular and others

Rodents

Rodents are the most frequently used mammalian speciesin laboratory research across a range of frequencies andintensities While studies are inconsistent there are

enough troubling indications regarding potential EMFimplications for wildlife

In the RFR range there have been several reviews offertility and other issues in rodentmodelswith citations toonumerous to mention heremdash see La Vignera e al [215] andMerhi [216]mdash but some stand out as potentially pertinent towildlife

Magras and Xenos [217] investigated effects of RFR onprenatal development in mice using RFR measurementsand in vivo experiments at several locations near an an-tenna park with measured RFR power densities between0168 and 1053 μWcm2 Divided into two groups were 12pairs of mice placed in locations of different power den-sities and mated five times One hundred eighteen new-borns were collected measured weighed and examinedmacro- and microscopically With each generation re-searchers found a progressive decrease in the number ofnewborns per dam ending in irreversible infertility How-ever the crown-rump length body weight and number oflumbar sacral and coccygeal vertebrae was improved inprenatal development of some newborns RFR was belowexposure standards and comparable to far-field exposuresthat mice could experience in the wild

Aldad et al [218] in a laboratory setting investigatedcell phoneRFR (800ndash1900MHzSARof 16Wkg) exposuresin in-uteromouse models and effects on neurodevelopmentandbehavior They foundsignificant adult behavioral effectsin prenatally exposed mice vs controls Mice exposed in-uterowere hyperactive had decreasedmemory and anxietyand alteredneuronal developmental programming Exposedmice had dose-response impaired glutamatergic synaptictransmission onto layer V pyramidal neurons of the pre-frontal cortex This was the first evidence of neuropathologyinmice from in-utero RFR at cell phone frequencies now themost prevalent in the environment Effects persisted intoadulthood and were transmissible to next generations Suchchanges can affect survival in wild populations

Meral et al [219] looked at effects in guinea pigs (Caviaparcels) from 900 MHz cell phone frequency exposures onbrain tissue and blood malondialdehyde (MDA) gluta-thione (GSH) retinol (vitamin A) vitamin D(3) andtocopherol (vitamin E) levels as well as catalase (CAT)enzyme activity Fourteenmale guinea pigs were randomlydivided into control and RFR-exposed groups containingseven animals each Animals were exposed to 890- to-915MHz RFR (217 Hz pulse rate 2Wmaximumpeak powerSAR 095 Wkg) from a cellular phone for 12 hday (11 h45 min stand-by and 15 min spiking mode) for 30 daysControls were housed in a separate room without cellphone radiation Blood samples were collected throughcardiac puncture biochemical analysis of brain tissue was

Levitt et al EMF and wildlife 17

done after decapitation at the end of the 30-day periodResults found MDA levels increased (plt005) and GSHlevels and CAT enzyme activity decreased while vitaminsA E and D(3) levels did not change significantly in thebrain tissue of exposed animals In blood samples of theexposed group MDA vitamins A D(3) and E levels andCAT enzyme activity increased (plt005) while GSH levelsdecreased (plt005) They concluded that cell phone radi-ation could cause oxidative stress in brain tissue of guineapigs but more studies were needed to determine if effectsare harmful andor affect neural functions

Lai et al [220] found that Sprague-Dawley rats exposedto RFR during water maze testing showed spatial workingmemory deficits compared to controls But similar studies[221ndash223] did notfindperformance effects in spatial tasks oralterations in brain development after similar exposuresHowever subsequent studies in the last two decades haveshown memory and learning effects in animals andhumans after RFR exposure [224]

Several studies also investigated RFR behavioral effectsin rodent models on learning memory mood disturbancesand anxiety behaviors with contradictory results Danielset al [225] found decreased locomotor activity increasedgrooming and increased basal corticosterone levels in ratsexposed to RFR for 3 h per day at 840MHz but no significantdifferences were seen between controls and test animals inspatial memory testing or morphological brain assessmentThe researchers concluded that RFR exposure may lead toabnormal brain functioning

Lee et al [226 227] looked specifically at effects onpregnant mice and rat testicular function from combinedRFR mobile network signal characteristics used in wide-band code division multiple access (W-CDMA) or CDMAused in 3G mobile communications Experiments showedno observable adverse effects on development reproduc-tion or mutation in tested subjects And no significant ef-fects were seen by Poulletier de Gannes et al [228] in in-utero and post-natal development of rats with wireless fi-delity (WiFi) at 2450 MHz Also Imai et al [229] found notesticular toxicity from 195 GHz W-CDMA

Oneextremelyhigh frequency (EHF) study comparable to5G on a mouse model by Kolomytseva et al [230] looked atleukocyte numbers and the functional activity of peripheralblood neutrophils In healthy mice under whole-body expo-sures to low-intensity extremely-high-frequency electromag-netic radiation (EHF 420 GHz 015 mWcm2 20 min daily)found that the phagocytic activity of peripheral blood neu-trophils was suppressed by about 50 (plt001 as comparedwith the sham-exposed control) in 2ndash3 h after the singleexposure Effects persisted for 1 day and thereafter returned tonormal within 3 days But a significant modification of the

leukocyte blood profile was observed inmice exposed to EHFfor 5 days after exposure cessation Leukocytes increased by44 (plt005 as comparedwith sham-exposed animals) Theyconcluded that EHF effects can be mediated via metabolicsystems and further said results indicated whole-body low-intenstiy EHF exposure of healthymice had a profound effecton the indices of nonspecific immunity These low levels willbe common near 5G infrastructure

In well-designed non-rodent mammal field studiesNicholls and Racey [206 207] found that foraging batsshowed aversive behavioral responses near large air trafficcontrol andweather radars Four civil air traffic control (ATC)radar stations three military ATC radars and three weatherradars were selected each surrounded by heterogeneoushabitat Three sampling points were carefully selected formatched habitats type structure altitude and surroundingland class at increasing distances from each station Radarfield strengthswere taken at three distances from the sourceclose proximity (lt656 ft200 m) with a high EMF strengthgt2 Vm (106 μWcm2) an intermediate line-of sight point(656ndash1312 ft200ndash400 m) with EMF strength lt2 Vm and acontrol location out of radar sight (gt1312 ft400 m) regis-tering 0 Vm Bat activity was recorded three times for a totalof 90 samples 30 within each field strength categoryMeasured from sunset to sunrise they found that bat activitywas significantly reduced in habitats exposed to an EMFgreater than 2 Vm compared to 0 EMF sites but suchreduced activity was not significantly different at lower EMFlevels within 400 m of the radar They concluded that thereduced bat activity was likely due to thermal induction andan increased risk of hyperthermia This was a large fieldstudy near commercial radar installations with mostly highintensity exposures but low-level effects cannot be excludedgiven known magneto-sensitivity in bats

In another field study using a small portable marineradar unit significantly less powerful than their earliermeasured field study Nicholls and Racey [207] found thesmaller signal could also deter batsrsquo foraging behaviorsFirst in summer 2007 bat activity was compared at 20foraging sites in northeast Scotland during experimentaltrials with radar switched on and in controls with no radarsignal After sunset bat activity was recorded for a periodof 30 min with the order of the trials alternating betweennights Then in summer 2008 aerial insects were sampledat 16 of the sites using two small light-suction traps onewith a radar signal the other a control Bat activity andforaging were found significantly reduced when the radarsignal was unidirectional creating a maximized exposureof 1767ndash2624 Vm (83ndash183 μWcm2) The radar had nosignificant effect on the abundance of insects captured bythe traps despite reduced bat activity

18 Levitt et al EMF and wildlife

Balmori [231] also noted significantly reduced bat ac-tivity in a free-tailed bat colony (Tadarida teniotis) wherethe number of bats decreased when several cell towerswere placed 262 ft (80 m) from the colony

In the ELF range Janać et al [232] investigated ELFMFeffects mdash comparable to powerline and stray voltageground currentmdash onmotor behavior patterns inMongoliangerbils (Meriones unguiculatus) and found age-dependentchanges in locomotion stereotypy and immobility in 3-and 10-month-old males Animals were continuouslyexposed to ELF-MF (50 Hz 01 025 and 05 mT) for sevendays with behavior monitored for 60 min in the open fieldafter the 1st 2nd 4th and 7th day (to capture immediateeffects) as well as three days after exposure (to capturedelayed effects) They found that exposure to 3-month-oldgerbils increased motor behavior (locomotion and stereo-typy) and therefore decreased immobility In the 3-monthold gerbils ELFMF also showed a delayed effect (except at025 mT) on stereotypy and immobility In 10-month-oldgerbils ELFMF of 01 025 and 05 mT induced decreasedlocomotion a slight increase in stereotypy and pro-nounced stimulation of motor behavior Increased motorbehavior was observed three days after exposure indi-cating long lasting effects Researchers concluded that in 3-and 10-month-old gerbils specific temporal patterns ofmotor behavior changes were induced by ELFMF due toage-dependent morpho-functional differences in brainareas that control motor behavior

The above is a very small sample of rodent studies SeePart 2 Supplements 1 and 2 for more genetic effects to ro-dents and Supplement 3 for additional studies

Bovines

Due to domestication and easy accessibility there arenumerous studies of dairy cows (Bos taurus) which appearparticularly sensitive to both natural andman-made EMFsFedrowitz [71] published a thorough review with citationstoo numerous to mention here Noted in the review is thefact that bovines although easily accessible are difficult tostudy with precision due to their size which createshandling and dosimetric complexities Also noted are thatbovines today are at their milk- and beef-productionphysiological limits and that the addition of even a weakstressor may be capable of altering a fragile bovine phys-iological balance It is clear in the Fedrowitz review thatcows respond to environmental exposures from a broadrange of frequencies and properties even as some studieslack good exposure assessment RFR exposure createdavoidance behavior reduced ruminating and lying times

and alterations in oxidative stress enzymes among otherproblems while ELF-EMF found contradictory evidenceaffecting milk production fat content hormone imbal-ances and important changes in other physiological pa-rameters Cows have also been found sensitive to strayvoltage and transient harmonics with problematic milkproduction health reproduction and behavioral effects

The question is how much of this body of work couldtranslate to other ruminants and largemammals on-field orin the wild such as deercervids mdash behaviorally repro-ductively and physiologically Stray voltage and ELF-EMFnear powerlines and rural area RFR from both ground-based and satellite transmitters for instance may affectwild migratory herds and large ungulates in remote areasthat go undetected

Bovines and RFR

Loscher and Kas [233] observed abnormal behavior in a dairyherd kept in close proximity to a TV and radio transmitterThey found reduction in milk yield health problems andbehavioral abnormalities After evaluating other factors theyconcluded the high levels of RFR were possibly responsibleThey removed one cow with abnormal behavior to anotherstable 20 km away from the antenna resulting in normali-zation of behavior within five days Symptoms reappearedwhen the cowwas returned to the stablenear theantennas Ina later survey Loscher [234] also found effects of RFR on theproduction health and behavior of farm animals includingavoidance behavior alterations in oxidative stress parame-ters and ruminating duration

Balode [59] obtained blood samples from female browncows from a farm close to and in front of the Skrunda Ra-dar ndash located in Latvia at an early warning radar systemoperating in the 156ndash162MHz frequency rangemdashand samplesfrom cows in a control area They found micronuclei in pe-ripheral erythrocyteswere significantly higher in the exposedcows indicating DNA damage

Staumlrk et al [235] investigated short-wave (3ndash30 MHz)RFR on salivary melatonin levels in dairy cattle with oneherd at a farm located at 1640 ft500 m (consideredhigher exposure) and a second control herd located 13123ft4000 m from the transmitter (considered unexposed)The average nightly magnetic field strength readingswere 21-fold greater on the exposed farm (159 mAm)than on the control farm (0076 mAm) At both farmsafter initially monitoring five cowsrsquo salivary melatoninconcentrations at 2-h intervals during night dark phasefor 10 consecutive days and with the short-wave trans-mitter switched off during three of the 10 days (off phase)samples were analyzed using a radioimmunoassay They

Levitt et al EMF and wildlife 19

reported that mean values of the two initial nights did notshow a statistically significant difference betweenexposed and unexposed cows and concluded thatchronic melatonin reduction was unlikely But on the firstnight of re-exposure after the transmitter had been off forthree days the difference in salivary melatonin concen-tration between the two farms (389 pgml CI 204 741)was statistically significant indicating a two-to-seven-fold increase of melatonin concentration Theyconcluded that a delayed acute effect of EMF on mela-tonin concentration could not be excluded and called forfurther trials to confirm results

Haumlssig et al [95] conducted a cohort study to evaluatethe prevalence of nuclear cataracts in veal calves nearmobilephone base stations with follow-up of each dam and its calffrom conception through fetal development and up toslaughter Particular emphasis was focused on the firsttrimester of gestation (organogenesis) Selected protectiveantioxidants (superoxide dismutase catalase glutathioneperoxidase [GPx]) were assessed in the aqueous humor of theeye to evaluate redox status They found that of 253 calves 79(32) had various degrees of nuclear cataracts but only 9(36)of calveshad severenuclear cataracts Theyconcludedthat a relationship between the location of veal calves withnuclear cataracts in the first trimester of gestation and thestrength of antennas was demonstrated The number of an-tennas within 328ndash653 ft (100ndash199 m) was associated withoxidative stress and there was an association betweenoxidative stress and the distance to the nearest base stationOxidative stress was increased in eyes with cataract (OR perkilometer 080 confidence interval 95 062 093) But theresearchers further concluded that it hadnot been shown thatthe antennas actually affected stress Hosmer-Lemeshowstatistics showed an accuracy of 100 in negative cases withlow radiation andonly 1111accuracy inpositive caseswithhigh radiation This reflected in their opinion that there are alot of other likely causes for nuclear cataracts beside basestations and called for additional studies on EMF duringembryonic development

Haumlssig et al [96] further examined a dairy farm inSwitzerland where a large number of calves were born withnuclear cataractsafter amobilephonebase stationwaserectednear the barn Calves showed a 35 times higher risk for heavycataracts if born there compared to theSwissaverageAll usualcauses for cataracts could be excluded but they neverthelessconcluded that the incidence remained unknown

Bovines and swine ELF-EMF stray electric current

Bovines appear unusually sensitive to ELF-EMF from straycurrent caused by both normal industrial and faulty

grounding methods near high tension transmission linesclose to dairy farms Stray current can cover large areas andoccurs when current flows between the grounded circuitconductor (neutral) of a farm and the Earth through dairyhousing equipment like metal grates It typically involvessmall steady power frequency currents [99] not hightransient shocks although that also can sometimes occurunderwetweather conditions According toHultgren [236]dairy cattle can perceive alternating currents exceeding1 mA between the mouth and all four hooves with behav-ioral effects in cows usually occurring above 3 mA Straycurrent can act as a major physical stressor in cows andother animals [237] This may also be happening in wildmigratory species moving through such areas

At the request of dairymen veterinarians and countyextension agents in Michigan US Kirk et al [238] inves-tigated stray current on 59 Michigan dairy farms On 32farms stray current sources were detected Where voltageexceeded 1 V alternating current increased numbers ofdairy cows showed abnormal behavior in the milking fa-cility and increased prevalence of clinical mastitis Re-covery from the stray current-induced abnormalities wasrelated to the type of abnormality and themagnitude of theexposure voltage

Burchard et al [239] in a small but well-controlledalternating exposure study of non-pregnant lactating Hol-stein cows found a longer estrous cycle in cows exposed to avertical electric field of 10 kVm and a uniform horizontalmagneticfield of 30 μT at 60Hz compared towhen theywerenot exposed Rodriguez et al [240] also found that exposureto EMFmay increase the duration of the bovine estrous cycleBurchard et al [241] evaluated effects on milk production inHolsteins exposed to a vertical electric field of 10 kVm and auniformhorizontalMFof 30μTat 60Hzand foundanaveragedecrease of 497 1378 and 1639 inmilk yield fat correctedmilk yield and milk fat respectively in exposed groups andan increase of 475 in dry matter food intake And Buchardet al [242] in two experiments investigated blood thyroxine(T4) levels in lactating pregnant and non-lactating non-pregnant Holstein cows exposed to 10 kVm 30 microT EMF andfound a significant change depending on the time of bloodsampling in exposed groups They concluded that exposureof dairy cattle to ELF-EMF could moderately affect the bloodlevels of thyroxine

Hillman et al [93 94] reported that harmonic distor-tion and power quality itself could be another variable inbovine sensitivity to stray current They found behaviorhealth and milk production were adversely affected bytransients at the 3rd 5th 7th and triplen harmonic cur-rents on utility power lines after a cell tower was foundcharging the ground neutral with 10+ V causing the

20 Levitt et al EMF and wildlife

distortion After installing a shielded neutral isolationtransformer between the utility and the dairy the distor-tion was reduced to near zero Animal behavior improvedimmediately and milk production which had been sup-pressed for three years gradually returned to normalwithin 18 months

Swine (Sus scrofa domesticus) mdash like rats and mice mdashhave demonstrated aversive behavior to ELF-EMF electricfields Hjeresen et al [243] found miniature pigs exposedto 60‐Hz electric fields (30 kVm for 20 hday 7 daysweekup to 6 months) preferred an absence of the field during a235‐h period by spendingmore time out of the electric fieldthan in it during sleep periods And Sikov et al [244] aspart of a broad study of Hanford Miniature swine onreproductive and developmental toxicology (includingteratology) over three breeding cycles found a strong as-sociation between chronic exposure to a vertical uniformelectric field (60‐Hz 30‐kVm for 20 hday 7 daysweek)and adverse developmental effects vs control Theyconcluded that an association exists between chronicexposure to strong electric fields and adverse develop-mental effects in swine (75malformations in exposed vs29 sham) in first generation with consistent results in twosubsequent generations

Avian

Birds are important indicators of ecosystemwell-being andoverall condition Even subtle effects can be apparent dueto their frequent presence in RFR areas Their hollowfeathers have dielectric and piezoelectric propertiesmeaning they are conductive and capable of acting as awaveguide directing external RFR energy directly anddeeply into avian body cavities [245ndash249] Their thin skullshave both magnetite and radical pair receptors (seeldquoMechanismsrdquo above) and they are highly mobile mdash oftentraveling across great migratory distances of tens to asmuch as a hundred thousand kilometers round-trip peryear resulting in potential multi-frequency cumulativeeffects from chronic near middle and far-field exposuresAvian populations are declining worldwide especiallyamong migratory species This means that birds may beuniquely sensitive to adverse effects from environmentalRFR since their natural habitat is air and they often fly atlateral levels with infrastructure emissions bringing themthat much closer to generating sources

Tower and building construction as direct obstaclesare known hazards to birds One tower at 150 feet (46 m)above ground level is thought to account for as many as3000 songbird deaths per month in migratory pathways

during peak migration [250] and communication towercollisions have been documented to kill more than 10000migratory birds in one night at a TV tower in Wisconsin[251 252] It has been known for years that the songbirdpopulations of North America and Europe are plummetingOnly recently were towers considered a significant factorBut is the problem solely due to obstacles in direct migra-tory pathways or is something else involved

RFR from towers may be acting as an attractant to birdsdue to their singular physiology Avian eyes and beaks areuniquely magnetoreceptive with both magnetite and crypt-chrome radical pair receptors One definitive studybyBeasonand Semm [253] demonstrated that the common cell phonefrequency (900-MHz carrier frequency modulated at 217 Hz)at nonthermal intensities produced firing in several types ofnervous system neurons in Zebra Finches (Taeniopygia gut-tate) Brain neurons of irradiated anesthetized birds showedchanges in neural activity in 76 of responding cells whichincreased their firing rates by an average 35-fold vs controlsOther responding cells exhibited a decrease in rates ofspontaneous activity The Beason and Semm study [253]could explain why birds may be attracted to cell towers atheoretical premise they previously observed with Bobolinks(Dolichonyx oryzivorus [254])

RFR may also act as an avian stressorirritant Earlywork by Wasserman et al [255] in field studies on 12 flocksof migratory birds subjected to various combinations ofmicrowave power density and duration under winter con-ditions at Monomet MA using birds from two additionalflocks as controls showed increased levels of aggression insome of the irradiated birds

Other research indicated a range of effects capable ofbroad adverse environmental outcomes Laboratorystudies by Di Carlo et al [256] found decreases in heatshock protein production in chick embryos The re-searchers used 915-MHz RFR on domestic chicken em-bryos and found that exposure typical of some cell phoneemissions reduced heat shock proteins (HSP-70) andcaused heart attacks and death in some embryos Con-trols were unaffected In replicated experiments similarresults were found by Grigorrsquoev [257] and Xenos andMagras [258] Batellier et al [259] found significantlyelevated embryomortality in exposed vs sham groups ofeggs incubated with a nearby cell phone repeatedlycalling a 10-digit number at 3-min intervals over theentire incubation period Heat shock proteins helpmaintain the conformation of cellular proteins duringperiods of stress A decrease in their productiondiminishes cellular protection possibly leading to can-cer other diseases heart failure and reduction in pro-tection against hypoxia and ultraviolet light

Levitt et al EMF and wildlife 21

Not all results are adverse Tysbulin et al [260 261]investigated both short and prolonged GSM 900 MHz cellphone signal exposure on embryo development in Quail(Coturnix coturnix japonica) irradiating fresh fertilizedeggs during the first 38 h and 14 days of incubation using acell phone in connecting mode continuously activatedthrough a computer systemMaximum intensity of incidentradiation on the eggrsquos surface was 02 mWcm2 Resultsfound a significant (plt0001) increase in differentiatedsomites in 38-h exposed embryos and a significant (plt005)increase in total survival of embryos in eggs after 14 daysexposure They also found the level of thiobarbituric acid(TBA) reactive substances was significantly (p 005ndash0001)higher in the brains and livers of hatchlings from exposedembryos and hypothesized that a facilitating effect existsdue to enhanced metabolism in exposed embryos via per-oxidation mechanisms They concluded low-levelnonthermal effects from GSM 900 MHz to quail embryo-genesis is possible and that effects can be explained via ahormesis effect induced by reactive oxygen species (ROS)

Signaling characteristics such as pulsing vs contin-uous wave are also important Berman et al [262] in amulti-lab study of pulsed ELF magnetic fields found ahighly significant incidence of abnormalities in exposedchick eggs vs controls And Ubeda et al [263] found irre-versible damage to chick embryos from weak pulsedELF-EMF magnetic fields that are common in the environ-ment today Initial studies on freshly fertilized chickeneggs were exposed during the first 48 h of post-laying in-cubation to pulsed magnetic fields (PMFs) with 100 Hzrepetition rate 10 μT peak-to-peak amplitude and 500 μspulse duration Two different pulse waveforms were usedwith rise and fall times of 85 μs or 21 μs A two-day expo-sure found significant increased developmental abnor-malities In follow-up research after exposure eggs wereincubated for an additional nine days without PMFs Em-bryos removed from eggs showed an excess of develop-mental anomalies in the PMF-exposed groups comparedwith the sham-exposed samples There was a high rate ofembryonic death in the 21 μs risefall time Results indicatePMFs can cause irreversible developmental changes con-firming that a pulse waveform can determine embryonicresponse to ELF magnetic fields common today

Between 1999 and 2005 Fernie et al for the first timeinvestigated various potential reproductive effects on acaptive raptor species mdash the American Kestrel (Falcosparverius) mdash from ELF-EMF equivalent to that of wildnesting pairs on power transmission lines In a series ofstudies captive pairs were typically bred under control orEMF exposure over 1ndash3 breeding cycles In 1999 Fernieet al [264] investigated photo phasic plasma melatonin in

reproducing adult and fledgling kestrels finding that EMFsaffected plasma melatonin in adult male kestrels sup-pressing it midway through but elevating it at the end ofthe breeding season In long-term but not short-term EMFexposure of adults plasma melatonin was supressed intheir fledglings too which could affect migratory successMolt happened earlier in adult EMF-exposed males than incontrols EMF exposure had no effect on plasmamelatoninin adult females In avian species melatonin is involved inbody temperature regulation seasonal metabolism loco-motor activity feeding patterns migration and plumagecolor changes important for mate selection Melatonin alsoplays a key role in the growth and development of youngbirds The researchers concluded it is likely that the resultsare relevant to wild raptors nesting within EMF exposures

In 2000 Fernie et al [265] focused on reproductivesuccess in captive American Kestrels exposed to ELF-EMFagain equivalent to that experienced by wild reproducingkestrels Kestrels were bred one season per year for twoyears under EMF or controlled conditions In some yearsbut not others EMF-exposed birds showed a weak asso-ciationwith reduced egg laying higher fertility larger eggswithmore yolk albumen andwater but thinner egg shellsthan control eggs Hatching successwas lower in EMFpairsthan control pairs but fledging success was higher thancontrol pairs in one year They concluded that EMF expo-sure such as what kestrels would experience in the wildwas biologically active in a number of ways leading toreduced hatching success

Also in 2000 Fernie et al [266] further investigatedbehavioral changes in American Kestrels to ELF-EMFagain in captive birds comparable to nesting pairs thatcommonly use electrical transmission structures for nest-ing perching hunting and roosting The amount of EMFexposure time of wild reproducing American Kestrels wasfirst determined at between 25 and 75 of the observedtime On a 24-h basis estimated EMF exposure in wildspecies ranged from 71 during courtship to 90 duringincubation Then effects of EMFs on the behavior of captivereproducing kestrels were examined at comparable expo-sures of 88of a 24-h period Additionally captive kestrelswere exposed to EMF levels experienced by wild kestrelsnesting under 735-kV power lines There appeared to be astimulatorystress effect Captive EMF females were moreactive more alert and perched on the pen roof morefrequently than control females during courtship EMF fe-males preened and rested less often during brood rearingEMF-exposed male kestrels were more active than controlmales during courtship and more alert during incubationThe researchers concluded that the increased activity ofkestrels during courtship may be linked to changes in

22 Levitt et al EMF and wildlife

corticosterone but not to melatonin as found in earlierwork [264] but said the behavioral changes observed wereunlikely to result in previously reported effects inEMF-exposed birds as noted above They added thatbehavioral changes of captive EMF-exposed kestrels mayalso be observed in wild kestrels with uncertain results

In 2001 Fernie and Bird [267] looked at ELF-EMFoxidative stress levels in captive American Kestrels usingthe same test parameters described above to see if ELF-EMFexposure elicited an immune system response In captivemale kestrels bred under control or EMF conditionsequivalent to those experienced by wild kestrels short-term EMF exposure (one breeding season) suppressedplasma total proteins hematocrits and carotenoids in thefirst half of the breeding season It also suppressed eryth-rocyte cells and lymphocyte proportions but elevatedgranulosa proportions at the end of the breeding seasonLong-term EMF exposure (two breeding seasons) alsosuppressed hematocrits in the first half of the reproductiveperiod But results found that only short-termEMF-exposed birds experienced an immune responseparticularly during the early half of the breeding seasonThe elevation of granulocytes and the suppression of ca-rotenoids total proteins and melatonin [264] in the samekestrel species indicated that the short-term EMF-exposedmale kestrels had higher levels of oxidative stress due to animmune response andor EMF exposure The researchersnoted that long-termEMF exposuremay be linked to higherlevels of oxidative stress solely through EMF exposureOxidative stress contributes to cancer neurodegenerativediseases and immune disorders And in 2005 Fernie andReynolds [268] noted most studies of birds and EMF indi-cate changes on behavior reproductive success growthand development physiology and endocrinology andoxidative stress mdash with effects not always consistent or inthe same direction under EMF conditions The entire bodyof work by this research group has implications for all wildspecies that encounter a wide range of EMFs on a regularbasis

In field studies on wild birds in Spain Balmori [269]found strong negative correlations between low levels ofmicrowave radiation and bird breeding nesting roostingand survival in the vicinity of communication towers Hedocumented nest and site abandonment plumage deteri-oration locomotion problems and death in Wood Storks(Mycteria americana) House Sparrows (Passer domes-ticus) Rock Doves (Columba livia) Magpies (Pica pica)Collared Doves (Streptopelia decaocto) and other speciesWhile these species had historically been documented toroost and nest in these areas Balmori [269] did not observethese symptoms prior to construction and operation of the

cell phone towers Results were most strongly negativelycorrelated with proximity to antennas and Stork nestingand survival Twelve nests (40 of his study sample) werelocated within 656 ft (200 m) of the antennas and neversuccessfully raised any chicks while only one nest (33)located further than 984 ft (300 m) never had chicksStrange behaviors were observed at Stork nesting siteswithin 328 ft (100 m) of one or several cell tower antennasBirds impacted directly by the main transmission lobe(ie electric field intensity gt 2 Vm) included young thatdied from unknown causes Within 100 m paired adultsfrequently fought over nest construction sticks and failedto advance nest construction (sticks fell to the ground)Balmori further reported that some nests were nevercompleted and that Storks remained passively in front ofcell site antennas The electric field intensity was higher onnests within 200 m (236 plusmn 082 Vm 148 μWcm2) than onnests further than 300 m (053 plusmn 082 Vm 0074 μWcm2)RF-EMF levels including for nests lt100 m from the an-tennas were not intense enough to be classified as thermalexposures Power densities need to be at least 10 mWcm2

to produce tissue heating of even 05 degC [270] Balmorirsquosresults indicated that RFR could potentially affect one ormore reproductive stages including nest constructionnumber of eggs produced embryonic developmenthatching and mortality of chicks and young in first-growthstages

Balmori and Hallberg [271] and Everaert and Bauwens[272] found similar strong negative correlations amongmale House Sparrows (Passer domestics) throughout mul-tiple sites in Spain and Belgium associated with ambientRFR between 1 MHz and 3 GHz at various proximities toGSM cell base stations House Sparrow declines in Europehave been gradual but cumulative for this species oncehistorically well adapted to urban environments Thesharpest bird density declines were in male House Spar-rows in relatively high electric fields near base stationsindicating that long-term exposure at higher RFR levelsnegatively affected both abundance andor behavior ofwild House Sparrows In another review Balmori [25] re-ported health effects to birds that were continuously irra-diated They suffered long-term effects that includedreduced territorial defense posturing deterioration of birdhealth problems with reproduction and reduction ofuseful territories due to habitat deterioration

Birds have been observed avoiding areas with highand low-intensity EMF in daylight as well as nocturnallyAn early study by Southern in 1975 [273] observed that gullchicks reacted to the US militaryrsquos Project Sanguin ELFtransmitter Tested on clear days in the normal geomag-netic field birds showed significant clustering with

Levitt et al EMF and wildlife 23

predicted bearing corresponding with migration directionbut when the large antenna was energized they dispersedrandomly He concluded that magnetic fields associatedwith such conductors were sufficient to disorient birdsLarkin and Sutherland [274] observed that radar tracking ofindividual nocturnal migrating birds flying over a largealternating-current antenna system caused birds to turn orchange altitude more frequently when the antenna systemwas operating than when it was not The results suggestedthat birds sense low-intensity alternating-current EMFduring nocturnal migratory flight

In a well-designedmulti-year avian study ofmagneto-disruption Engels et al [213] investigated environmentalbroadband electromagnetic lsquonoisersquo emitted everywherehumans use electronics including devices and infra-structure They found migratory birds were unable to usetheir magnetic compass in the presence of a typical urbanenvironment today European Robins (E rubecula)exposed to the background electromagnetic lsquonoisersquo presentin unscreened wooden huts at the University of Oldenburgcampus could not orient using their magnetic compassBut when placed in electrically grounded aluminum-screened huts creating Faraday cages that attenuatedelectromagnetic lsquonoisersquo by approximately two orders ofmagnitude their magnetic orientation returned The re-searchers were able to determine the frequency range from50 kHz to 5 MHz was the most disruptive When groundingwas removed or additional broadband electromagneticlsquonoisersquo was deliberately generated inside the screened andgrounded huts birds again lost magnetic orientationabilities They concluded that RFRrsquos magneto-disruptioneffects are not confined to a narrow frequency band Birdstested far from sources of EMFs required no screening toorientwith theirmagnetic compass Thiswork documenteda reproducible effect of anthropogenic electromagneticambient lsquonoisersquo on the behavior of an intact vertebrate Themagnetic compass is integral to bird movement andmigration Thefindings clearly demonstrated anonthermaleffect on European Robins and serves as a predictor foreffects to othermigratory birds especially those flying overurban areas Such fields are much weaker than minimumlevels expected to produce any effects and far below anyexposure standards

Intensity windows in different species have also beenfound where effects can be more extreme at lower in-tensities than at higher ones due to compensatory mech-anisms such as cell apotosis Panagopoulos andMargaritas[34] found an unexpected intensity window at thermallevels around 10 mWcm2 RFR mdash not uncommon near celltowersmdashwhere effects weremore severe than at intensitieshigher than 200 mWcm2 This window appeared at a

distance of 8ndash12 in (20ndash30 cm) from a cell phone antennacorresponding to a distance of about 66ndash98 ft (20ndash30 m)from a base station antenna This could be considered aclassic nonlinear effect and would apply to far-field expo-sures Since cell base station antennas are frequentlylocated within residential areas where birds nest often atdistances 20ndash30 m from such antennas migratory birdsnon-migratory avifauna and other wildlife may beexposed up to 24-h per day

Concerns also apply to impacts from commercial radiosignals on migratory birds The human anatomy is reso-nant with the FM bands so exposure standards are moststringent in that range High intensity (gt6000 W) com-mercial FM transmitters are typically located on the highestground available to blanket a wider area Low powered FMtransmitters (lt1000 W) can be placed closer to the humanpopulation High intensity locations which can be multi-transmitter sites (colloquially called ldquoantenna farmsrdquo) forother services also provide convenient perches and nestsites formigratory birds FMdigital signals which simulatepulsed waves pose additional health concerns to migra-tory birds This creates a dangerous frequency potential forprotected migratory birds such as Bald Eagles with wing-spans that extend to about 6 ft (183 m)mdash a resonant matchwith the length of the FM signalmdash creating a potential full-body resonant effect for both humans and Bald EaglesBirds could experience both thermal and non-thermaleffects

All migratory birds are potentially at risk includingBald Eagles Golden Eagles birds of conservation concern[275] federal andor state-listed bird species birds na-tionally or regionally in peril as well as birds whose pop-ulations are stable Sadly addressing these concerns mdashbeginning with independent research conducted by sci-entists with no vested interest in the outcomes mdash has notbeen a priority for government agencies or the communi-cations industry

Insects and arachnids

Insects are the most abundant and diverse of all animalgroups with more than one million described speciesrepresenting more than half of all known living speciesand potentially millions more yet to be discovered andidentified They may represent as much as 90 of all lifeforms on Earth Though some are considered pests to farmcrops and others as disease vectors insects remainessential to life and planetary health Found in nearly allenvironments they are the only invertebrates that fly butadults of most insect species walk while some swim

24 Levitt et al EMF and wildlife

Because of these different environmental adaptationsdifferent species will encounter different EMF exposures invarying degrees For instance ground-based walking in-sects may be more susceptible to effects from 60 Hz straycurrent while flying insects may be more susceptible towireless exposures However all species tested have beenaffected across a range of the nonionizing electromagneticbands

Most insects have an exoskeleton three-part bodyconsisting of a head thorax and abdomen three pairs ofjointed legs compound eye structures capable to seeingmany more colors widths and images than humans andone pair of antennae capable of sensing subtle meteoro-logical changes and Earthrsquos geomagnetic fields They livein close harmonywith the natural environment for survivaland mating purposes The most diverse insect groups co-evolved with flowering plants many of which would notsurvive without them Most insect species are highly sen-sitive to temperature variations and climate alterations asthey do not dissipate heat efficiently

Nearly all insects hatch from eggs that are laid inmyriad ways and habitats Growth involves a series ofmolts and stages (called instars) with immature stagesgreatly differing from mature insects in appearancebehavior and preferred habitat Some undergo a four-stage metamorphosis (with a pupal stage) and others athree-stage metamorphosis through a series of nyphalstages

While most insects are solitary some mdash like beestermites and antsmdash evolved into social networks living inldquocooperativerdquo organized colonies that can function as oneunit as evidenced in swarming behaviors Some even showmaternal care over eggs and young They communicatethrough various sounds pheromones light signals andthrough their antennae such as during the beesrsquo ldquowaggledancerdquo (see below)

As far back as the 1800s even though testing methodswere primitive by todayrsquos standards researchers werecurious about electromagnetismrsquos effect on insect devel-opment particularly teratogenicity [276] Research on EMFacross frequencies and insect populations has beenongoing since at least the 1930s with an eye toward usingenergy as an insecticide and anti-contaminant in graintypically at high intensity thermal exposures that wouldnot exist in the natural environment Mckinley and Charles[277] found that wasps die within seconds of high fre-quency exposure But not all early work was strictly highintensity or all effects observed due to thermal factors

There were interesting theories introduced by earlyresearchers regarding how energy couples with variousinsect species Frings [278] found larval stages are more

tolerant to heat than adult insects with appendages thatcan act as conducting pathways to the body and that themore specialized the insect species the more susceptiblethey appear to microwave exposure Carpenter and Liv-ingstone [279] studied effects of 10 GHz continuous-wavemicrowaves at 80 mWcm2 for 20 or 30 min or at 20 mWcm2 for 120 min on pupae of mealworm beetles (Tenebriomolitor)mdash clearlywithin thermal ranges In control groups90 metamorphosed into normal adult beetles whereasonly 24 of exposed groups developed normally 25died and 51 developed abnormally Effects wereassumed to be thermally induced abnormalities until theysimulated the same temperature exposure using radiantheat and found 80 of pupae developed normally Theyconcluded that microwaves were capable of inducingabnormal effects other than through thermal damage

Fruit flies

Insects at all metamorphic stages of development havebeen studied using RFR including egg larva pupa andadult stages Much work has been done on genetic andother effects with fruit flies (D melanogaster) because oftheirwell-described genetic system ease of exposure largebrood size minimal laboratory space needed and fastreproductive rates Over several decades Goodman andBlank using ELF-EMF on Drosophilamodels found effectsto heat shock proteins and several other effects ([201] andsee ldquoMechanismsrdquo above) It is considered a model com-parable to other insects in thewild approximating that sizeD melanogaster may be the most lab-studied insect onEarth although honey and related bee species due to theirdevastating losses over the last decade and significance toagriculture are quickly catching up

Michaelson and Lin [50] noted that RFR-exposed in-sects first react by attempting to escape followed bydisturbance of motor coordination stiffening immobilityand eventually death depending on duration of exposureand insect type For example D melanogaster survivedlonger than 30minwhile certain tropical insects live only afew seconds at the same field intensity Also noted wereconcentration changes in many metabolic products andeffects to embryogenesis mdash the period needed for a but-terfly to complete metamorphosis mdash with acceleratedgastrulation and larval growth [17] Michaelson and Lin[50] cited several negative studies with D melanogasterexposed with continuous-wave RFR between 25 and2450 MHz on larval growth [280 281] and mutagenicity[282] This was after Heller andMickey [283] found a tenfoldrise in sex-linked recessive mutations with pulsed RFR

Levitt et al EMF and wildlife 25

between 30 and 60 MHz It was among the earliest studiesthat found pulsing alone to be a biologically activeexposure

As reported in Michaelson and Lin [50] Tell [284]looked at D melanogasterrsquos physiological absorptionproperties and found that a group of 6-day old male wild-type flies exposed to 2450 MHz for 55 min at an intensefield caused a dramatic 65 reduction in bodyweight Thiswas thought to be from dehydration They then sought tocalculate the fruit flyrsquos absorption properties in relation toplane electromagnetic waves and found that a fly has onlya 11000th effective area of its geometric cross section andthus is an inefficient test species for absorbed microwaveradiation However they concluded that fruit flies wereresponsive to absorbed energy at thermal levels as a blackbody resonator at a power density of 1044 times 104 mWcm2corresponding to a thermal flux density of 0562 times 10minus3 calThese are levels found in close proximity to broadcast fa-cilities and cell phone towers today

More recent investigations of RFR by Weisbrot et al[285] using GSM multiband mobile phones (9001900 MHz SAR approximately 14 Wkg) on D mela-nogaster during the 10-day developmental period from egglaying through pupation found that non-thermal radiationincreased numbers of offspring elevated heat shockprotein-70 levels increased serum response element (SRE)DNA-binding and induced the phosphorylation of the nu-clear transcription factor ELK-1Withinminutes therewasa rapid increase of hsp70 which was apparently not athermal effect Taken together with the identified compo-nents of signal transduction pathways the researchersconcluded the study provided sensitive and reliable bio-markers for realistic RFR safety guidelines

Panagopoulos et al [286] found severe effects in earlyand mid-stage oogenesis in D melanogaster when flieswere exposed in vivo to either GSM 900-MHz or DCS1800-MHz radiation from a common digital cell phone atnon-thermal levels for a few minutes per day during thefirst 6 days of adult life Results suggested that the decreasein oviposition previously reported [287ndash289] was due todegeneration of large numbers of egg chambers after DNAfragmentation of their constituent cells which was inducedby both types of mobile phone radiation Induced celldeath was recorded for the first time in all types of cellsconstituting an egg chamber (follicle cells nurse cells andthe oocyte) and in all stages of early and mid-oogenesisfrom germarium to stage 10 during which programmedcell death does not physiologically occur Germarium andstages 7ndash8 were found to also be the most sensitivedevelopmental stages in response to electromagnetic stressinduced by the GSM and DCS fields Germarium was also

found to be more sensitive than stages 7ndash8 These paperstaken collectively indicate serious potential effects to allinsect species of similar size to fruit flies from cell phonetechnology including from infrastructure and transmittingdevices

Fruit flies have also been found sensitive to ELF-EMFGonet et al [290] found 50 Hz ELF-EMF exposure affectedall developmental stages of oviposition and developmentof D melanogaster females and weakened oviposition insubsequent generations

Savić et al [291] found staticmagneticfields influencedboth development and viability in two species ofDrosophila (D melanogaster and D hydei) Both speciescompleted development (egg-to-adult) in and out of thestatic magnetic field induced by a double horseshoe mag-net Treated vials with eggswere placed in the gap betweenmagnetic poles (47 mm) and exposed to the average mag-netic induction of 60 mT while control groups were keptfar from the magnetic field source They found that expo-sure to the static magnetic field reduced development timein both species but only results for D hydei were statisti-cally significant In addition the average viability of bothspecies was significantly weaker compared to controlsThey concluded a 60 mT static magnetic field could be apotential stressor influencing on different levels bothembryonic and post-embryonic fruit fly development

Beetles

Other insect species also react to both ELF-EMF andRF-EMF Newland et al [292] found behavioral avoidancein cockroaches (Periplaneta americana) to static electricfields pervasive in the environment from both natural andman-made sources Such fields could exist near powerlinesor where utilities ground neutral lines into the Earth Theyfound insect behavioral changes in response to electricfields as tested with a Y-choice chamber with an electricfield generated in one arm of the chamber Locomotorbehavior and avoidance were affected by the magnitude ofthe electric fields with up to 85 of individuals avoidingthe charged arm when the static e-field at the entrance tothe arm was above 8ndash10 kVm Seeking to determinemechanisms of perception and interaction they then sur-gically ablated the antennae and cockroaches were unableto avoid electric fields They concluded that antennae arecrucial in cockroach detection of electric fields that therebyhelps them avoid such fields They also noted that cock-roach ability to detect e-fields is due to long antennaewhich are easily charged and displaced by such fields notbecause of a specialized detection system This leads to the

26 Levitt et al EMF and wildlife

possibility that other insects may also respond to electricfields via antennae alone

Vaacutecha et al [208] found that cockroaches (P americana)were sensitive to weak RFR fields and that the Larmor fre-quency at 12 MHz in particular had a ldquodeafening effectrdquo onmagnetoreception The parameter they studied was the in-crease in locomotor activity of cockroaches induced by peri-odic changes in geomagnetic North positions by 60deg Theonset of the disruptive effect of a 12 MHz field was foundbetween 12 and 18 nT whereas the threshold of a field twicethe frequency (24 MHz) fell between 18 and 44 nT A 7 MHzfield showed no significant effect even at maximal of 44 nTThe results suggested resonance effects and that insects maybe equipped with the same magnetoreception systemas birds

Prolić et al [293] investigated changes in behavior viathe nervous system of cerambycid beetles (Morimus fune-reus) in an open field before and after exposure to a 50 HzELF-MF at 2 mT Experimental groups were divided intoseveral activity categories Results showed activityincreased in the groups with medium and low motor ac-tivity but decreased in highly active individuals High in-dividual variability was found in the experimental groupsas well as differences in motor activities between the sexesboth before and after exposure to ELF‐MF They assumedactivity changes in both sexeswere due to exposure to ELF‐MF Only a detailed analysis of the locomotor activity at 1‐min intervals showed some statistically significant differ-ences in behavior between the sexes

Ants

Ants are another taxa found sensitive to EMF Ants comprisebetween 15 and 25 of the terrestrial animal biomass andthrive in most ecosystems on almost every landmass onEarth By comparison the total estimatedbiomass (weight) ofall ants worldwide equates to the total estimated biomass ofall humans Their complex social organization in colonieswith problem-solving abilities division of labor and bothindividual and whole colony communication via complexbehavioral and pheromone signaling may account for theirsuccess in so many environments Some ant species (egFormica rufa-group) are known to build colonies on activeearthquake faults and have been found to change behaviorhours in advance of earthquakes [294] thus demonstratingpredictive possibilities Ants can modify habitats influencebroad nutrient cycling spread seeds tap resources anddefend themselves Ants co-evolvedwith other specieswhichled to many different kinds of mutual beneficial and antag-onistic relationships

Ants (eg Solenopsis invictus) are long known to besensitive to magnetic fields both natural and manmade[295] Ants (eg Atta colombica) like birds have beenfound to be sensitive to the Earthrsquos natural fields and to useboth a solar compass on sunny days as well as a magneticcompasswhen there is cloud cover [296] Jander and Jander[297] similarly found that the weaver ant (Oecophylla spp)had amore efficient light compass orientation with amuchless efficient magnetic compass orientation suggestingthat they switch from the former to the latter when visualcelestial compass cues become unavailable There is evi-dence from Esquivel et al [298] that such magneto-reception is due to the presence of varying sized magnetiteparticles and paramagnetic resonance in fire ants (Sol-enopsis spp) But Riveros and Srygley [299] found a morecomplex relationship toward a magnetic compass ratherthan the presence of magnetite alone when leafcutter ants(Atta columbica) were subjected to a brief but strongmagnetic pulse which caused complete disorientationregarding nest-finding They found external exposurescould interfere with antsrsquo natural magnetic compass inhome path integration which indicated evidence of acompass based on multi-domain andor super-paramagnetic particles rather than on single-domain par-ticles like magnetite

Acosta-Avalos et al [300] found that fire ants aresensitive to 60 Hz alternating magnetic fields as well asconstant magnetic fields changing their magnetic orien-tation and magnetosensitivity depending on the relationbetween both types of magnetic fields Alternating currenthad the ability to disrupt ant orientation raising thequestion of effects to wild species from underground wir-ing and the common practice of powerline utility com-panies using the Earth as a neutral return pathway tosubstations creating stray current along the way [99]

Camelitepe et al [301] tested black-meadow antsrsquo(Formica pratensis) response under both natural geomag-netic and artificial earth-strength static EMFs (245 μT)They found that under the natural geomagnetic field whenall other orientational cues were eliminated there wassignificant heterogeneity of ant distribution with the ma-jority seeking geomagnetic north in darkness while underlight conditions ants did not discriminate geomagneticnorth Under artificial EMF exposure however ant orien-tation was predominantly on the artificial magnetic NSaxis with significant preference for artificial north in bothlight and dark conditions This indicated EMF abilities toalter ant orientation

Ants are also shown to react to RFR [302 303] Cam-maerts et al [304] found that exposures to GSM 900MHz at00795 μWcm2 significantly inhibited memory and

Levitt et al EMF and wildlife 27

association between food sites and visual and olfactorycues in ants (Myrmica sabuleti) and eventually wiped outmemory altogether Subsequent exposure after a brief re-covery period accelerated memoryolfactory loss within afew hours vs a few days indicating a cumulative effecteven at very low intensity The overall state of the exposedant colonies eventually appeared similar to that exhibitedby honey bee (Apis mellifera) colony collapse disorderAlthough the impact of GSM900MHz radiationwas greateron the visual memory than on the olfactory memory theresearchers concluded that such exposures mdash common tocell phonestowers mdash were capable of a disastrous impacton a wide range of insects using olfactory andor visualmemory including bees Many ant species (eg Lasiusneglectus Nylanderia fulva Camponotus spp Hymenopteraformicidae Solenopsis invicta among others) are attractedto electricity electronic devices and powerlines therebycausing short circuits and fires One hypothesis [305] is thatthe accumulation of ants in electrical equipment may bedue to a few foraging ldquoworker antsrdquo seeking warmth andfinding their way into small spaces completing electricalcontacts which then causes a release of alarm exocrinegland pheromones that attract other ants which then gothrough the same cycle In their study they found thatworkers subjected to a 120 V alternating-current releasedvenom alkaloids alarm pheromones and recruitmentpheromones that elicited both attraction and orientation inants as well as some other unknown behavior-modifyingsubstances But given how ants are affected by EMFs ingeneral it is likely that an attractant factor is also involvednot just warmth and small spaces

There is evidence that ants use their antennae asldquoantennasrdquo in two-way electrochemical communicationsOver 100 hundred years ago Swiss researcher AugusteForel [306] removed the antennae of different species ofants and put them together in one place What would havenormally evoked aggressive behaviors among the differentspecies did not occur and they got along as if belonging tothe same colony To Forel this indicated an ability of antantennae to help different ant species identify each other

Two mechanisms in ants have long been known forchemical receptivity as well as electromagnetic sensitivityRecently Wang et al [307] found evidence that chemicalsignals located specific to antennae vs other body areasdrew more attention from non-nest mates When cuticularhydrocarbons (CHCs) were removed by a solvent fromantennae non-nest mates responded less aggressivelythan to other areas of the body indicating that antennaereveal nest-mate identity conveying and receiving socialsignals Regarding magnetoreception magnetic measure-ments [308ndash310] found the presence of biogenic magnetite

was concentrated in antennae and other body parts of theant Pachycondyla marginata De Oliveira et al [311] alsofound evidence of magnetite and other magnetic materialsimbedded in various locations of antennae tissue inP marginata indicating that antennae function as magne-toreceptors The amount of magnetic material appearedsufficient to produce a magnetic-field-modulated mecha-nosensory output and therefore demonstrated a magneto-receptiontransduction sense in migratory ants

Ticks

Ticks are members of the order Arachnida shared withscorpions and spiders Recent papers in a tick species(Dermacentor reticulates) mirrors an attraction to somefrequencies but not others Vargovaacute et al [312 313] foundthat exposure to RFRmaybe apotential factor altering bothpresence and distribution of ticks in the environmentStudies were conducted to determine potential affinity ofticks for RFR using radiation-shielded tubes (RST) undercontrolled conditions in an electromagnetic compatibilitylaboratory in an anechoic chamber Ticks were irradiatedusing a Double-RidgedWaveguide Horn Antenna to RF-EMFat 900 and 5000 MHz 0 MHz served as control Resultsfound that 900 MHz RFR induced a higher concentration ofticks on the irradiated arm of RSTwhereas at 5000MHz ticksescaped to the shielded arm In addition 900 MHz RFR hadbeen shown to cause unusual specific sudden tick move-ments during exposure manifested as body or leg jerking[312] These studies are the first experimental evidence of RFRpreference and behavioral changes in D reticulates with im-plications forRFR introduced into thenatural environment bydevices and infrastructure In a further study Frątczak et al[314] reported that Ixodes ricinus ticks were attracted to900 MHz RFR at 01 μWcm2 particularly those infected withRickettsia (spotted fever)

RFR may be a new factor in tick distribution alongwith known factors like humidity temperature and hostpresence causing concentrated non-homogenous ormosaic tick distribution in natural habitats Tick preferencefor 900 MHz frequencies common to most cell phones haspossibly important ecological and epidemiological conse-quences Increasing exposures from use of personal de-vices and infrastructure in natural habitats where ticksoccur may increase both tick infestation and diseasetransmission Further studies need to investigate thisworkgiven the ubiquity of ticks today their northward spreaddue to climate change in the Northern Hemisphere and theincreasing and sometimes life-threatening illnesses theytransmit to humans pets and wildlife alike

28 Levitt et al EMF and wildlife

Monarch butterflies

The American Monarch butterfly (D plexippus) has fasci-nated researchers for over 100 years as it is the only insectknown to migrate in multi-generational stages [315ndash319]with the ability to find their exact birthplace on specificmilkweed plants (Asclepias spp) at great distances acrossland and oceans

Monarchs (D plexippus) found across Southern Can-ada the United States and South America are generallydivided by the Rocky Mountains into eastern and westernmigratory groups Their population has precipitouslydeclined by 994 since the 1980s (85 of that since 2017)and by 90 in the past two decades in both western andeastern populations [13 15] These steep declines are fromnumerous anthropogenic causes and may have alreadycrossed extinction thresholds thereby leaving us bereft notonly of their beauty and inspiration but also the perfectmodel for long-distance animalmigration study in general

Monarch butterflies are among North Americarsquos mostbeloved invertebrates They have for centuries navigatedthousands of mileskilometers in an iconic fall migrationfrom southern Canada and the mid- and northeastern USto a small area of about 800 square miles (2072 squarekilometers) in Central Mexico where they once winteredover in the millions in small remote oyamel fir forests Bythe time they reach their final destination some will havetraveled distances exceeded only by some migratoryseabird species The monarch is the only insect known tomigrate annually over 3000miles (4828 km) atsim 250miles(402 km) per day in the fall from the Canadian border toMexico and in the springtime back again Similar to somebird species it is the only butterfly known to have a two-way migration pattern Monarchs are only followed byarmy cutwormmoths (Euxoa auxiliaris) whichmaymigrateseveral thousand kilometers to high elevation sites in theRocky Mountains to escape lowland heat and drought

But monarchs are more interesting than for this oneamazing migrational feat alone How they do this is a long-standing mystery since their entire lifecycle includingtheir two-stage spring return migration is multi-generational indicating genetic factors in directionalmapping since the final return fall migration south cannotbe considered ldquolearnedrdquo Several multifaceted mecha-nisms must come into play as well as little understoodcomplexities in how those mechanisms cooperate andtrade off with each other under different environmentalcircumstances Monarchs also go from solitary insectsduring early developmental stages confined to specificlocations then exhibit social insect behaviors after thethird generation has reached northern latitudes and turned

south during the final fall migration And all of this hap-pens in a brain the size of a grain of sand

Reppert et al [320] published an excellent review in2010 on the complexities of monarch migration noting ldquohelliprecent studies of the fall migration have illuminated themechanisms behind the navigation south using a time-compensated sun compass Skylight cues such as the sunitself and polarized light are processed through both eyesand likely integrated in the brainrsquos central complex thepresumed site of the sun compass Time compensation isprovidedbycircadianclocks thathaveadistinctivemolecularmechanism and that reside in the antennae Monarchs mayalso use a magnetic compass because they possess twocryptochromes that have the molecular capability for light-dependent magnetoreception Multiple genomic approachesare being utilized to ultimately identify navigation genesMonarch butterflies are thus emerging as an excellent modelorganism to study the molecular and neural basis of long-distancemigrationrdquoReppert anddeRoode [321] updated thatinformation in 2018

Although it has been known for some time that mon-archs use a circadian rhythm time-compensated direc-tional sun compass [316 322ndash338] many questions remainabout its dynamics and concerns regarding effects fromradiation

Monarch antennae are known to contain magnetite[339 340] and cryptochromes [335 336 341 342] mdash bothunderstood to play a role in magnetoreception (seeldquoMechanismsrdquoabove) One early study by Jones and Mac-Fadden [343] found magnetic materials located primarilyin the head and thorax areas of dissected monarchs Morerecently Guerra et al [16] found convincing evidence thatmonarchs use a magnetic compass to aid their longest fallmigration back to Mexico Those researchers used flightsimulator studies to show that migrants possess an incli-nation magnetic compass to assist fall migration towardthe equator They found this inclination compass is light-dependent utilizing ultraviolet-Ablue light between 380and 420 nm and noted that the significance of light(lt420 nm) for an inclination compass function had notbeen considered in previous monarch studies They alsonoted that antennae are important for an inclinationcompass since they contain light-sensitive magneto-sensors Like some migratory birds the presence of aninclination compass would serve as an orientation mech-anism when directional daylight cues are impeded bycloudy or inclement weather or during nighttime flight Itmay also augment time-compensated sun compass orien-tation for appropriate directionality throughout migrationThe inclination compass was found to function at earth-strength magnetic fields an important metric

Levitt et al EMF and wildlife 29

The question remains Can the magnetic compass inmonarchs be disrupted by anthropogenic EMF like it doeswithgeomagnetic orientation inmigratorybirds [213] There issome indication this is possible Perez et al [330] foundmonarchs completely disorient after exposure to a strongmagnetic field (04-T MF for 10 s or approximately 15000times the Earthrsquos magnetic field) immediately before releasevs controls This is a high exposure but within range of man-made exposures today very close to powerlines

Bees wasps and others

Pollinators bees in particular are keystone specieswithout which adverse effects would occur throughoutfood webs and the Earthrsquos entire biome were pollinators todisappear Because of their central role and accessibilityfor research bee studies have created a wealth of infor-mation including regarding anthropogenic EMFs

Bees mdash especially honey and bumble bees mdash areanother iconic insect species beloved for their role inpollination honey propolis royal jelly and beeswax pro-duction their critical importance to our food supply andtheir crucial role in global ecological health and stabilityFound on every continent except Anarctica wherever thereare flowering plants requiring insect pollination there areover 16000 known species of bees in seven different bio-logical families consisting of four main branches Somespecies live socially in colonies while others are solitaryThe western honey bee (Apis mellifera) is the best knownand most studied due in part to its central role in agricul-ture Bees feed on nectar for energy and pollen for proteinnutrients and have co-evolved with many plant species inastoundingly complex ways They are also highly sensitiveto both natural and anthropogenic EMFs Beeswax itselfhas electrical properties [50]

Human apiculture has been practiced since the time ofancient Egyptian and Greek cultures and bees have beenclosely studied since the 1800s Almost all bee speciesincluding commercially raised and wild species are underdecades-long multiple assaults These include from pesti-cides herbicides climate change various bacterialviraldiseases infestations from parasitic mite species mdashparticularly Apis cerana Varroa destructor and Varroajacobsoni beginning in the mid-1980s mdash and predationfrom introduced species that attack bees directly (eg theinvasive giant bee-eating hornet Vespa mandarinia) aswell as alter plant ecology over time to adversely affect beefood supply Somehave suggested that vanishing beesmayalso have to do with premature aging due to environmen-tally caused shortened telomeres [344]

Whole colony collapse disorder (CCD) is the mostdramatic manifestation of domesticated bee demise inwhich worker bees abruptly disappear from a hive withouta trace resulting in an empty hive with perhaps aremaining queen and a few worker bees despite ampleresources left behind Few if any dead bees are ever foundnear the hive CCDwas first described in the US in 2006 inFlorida in commercial western honey bee colonies VanEnglesdorp et al [345] quantified bee losses across allbeekeeping operations and estimated that between 075and 100 million honey bee colonies died in the UnitedStates over the winter of 2007ndash2008 Up until that surveyestimates of honey bee population decline had notincluded losses occurring during the wintering periodthus underestimating actual colony mortality

The same phenomenon had been described by bee-keepers in France in 1994 [346] mdash later attributed to thetiming of sunflower blooming and the use of imidacloprid(IMD) a chlorinated nicotine-based insecticide or ldquoneon-icotinoidrdquo being applied to sunflowers for the first time there[347] Similar to DDT but considered safer for mammalsincludinghumans neonicotinoidsare a slow-release class ofneurotoxins that block insect nervous systems via acetyl-choline receptors interferingwith neuronal signaling acrosssynapses Sublethal doses can interfere with bee navigation

Since then similar phenomena have been seenthroughout Europe [348] and some Asian countries Causalhypotheses included all of the above factors with varyingfoci on pesticide classes like neonicotinoids and geneti-cally modified crops but no single agent adequately ex-plains CCD Bromenshenk et al [349] however identifiedpathogen pairingco-infection with two previously unre-ported RNA virusesmdash V destructor-1 and Kakugo virusesand a new irridescent virus (IIV) (Iridoviridae) along withNosema ceranaemdash in North American honey bees that wereassociated with all sampled CCD colonies The pathogenpairing was not seen in non-CCD colonies Later cage trialswith IIV type-6 and N ceranae confirmed that co-infectionwith those two pathogens was more lethal to bees thaneither pathogen alone Still many questions remain

There are two national surveying groups in the USmdashthe US Department of Agriculture (USDA) which begansurveying managed bee populations in 2015 but fundingwas cut in late 2019 and the Bee Informed Partnership(BIP) a non-profit that coordinates with research facilitiesand universities Prior to USDArsquos funding cuts managedcolonies decreased from CCD by 40 [350] with an addi-tional 26 over the same quarter in 2019 [351] BIPrsquos surveyperiod for April 1 2018 through April 1 2019 found USbeekeepers lost an estimated 407 of their managedhoney bee colonies The previous year had similar annual

30 Levitt et al EMF and wildlife

losses of 401 The average annual rate of loss reported bybeekeepers since 2010ndash11 was 378 [352]

Also in theUS for the first time in 2016 seven species ofHawaiian yellow-faced bees (Hylaeus anthracinusHylaeus longiceps Hylaeus assimulans Hylaeus facilisHylaeus hilaris Hylaeus kuakea and Hylaeus mana) wereadded to the federal endangered species list as well as therusty patched bumble bee (Bombus affinis) which prior to thelate 1990s had been widely dispersed across 31 US states[353] Mathiasson and Rehan [354] examined 119 species inmuseum specimens in New Hampshire going back 125 yearsand concluded that 14 species found across New Englandwere on the decline by as much as 90 including the lesserstudied leafcutter and mining bees that nest in the groundunlike honeybees that nest in commercial hives or in treesshrubs and rock crevices in the wild

Worldwide many bee and other pollinator pop-ulations have also declined over the last two decadesManaged honey bee (Apis mellifera) colonies decreased by25over 20 years in Europe and 59over 58 years in NorthAmerica with many wild bumble bee populations inEurope and North America having gone locally extinct[355ndash358] But while dramatic range contractions havebeen seen not all bees in all places are declining somepopulations are growing depending on opportunistic andspecies-adaptability factors Formany species data are stillinsufficient of poor quality or nonexistent [359] In addi-tion bee declines can affect flora survival Miller-Struttmann et al [360] recorded flower declines of 60with 40 years of climate warming in alpine meadows mdashareas largely protected from land-use changes Insects arehighly sensitive to temperature changes

A comprehensive UK survey of pollinator species [361]found that of 353 wild bee and hoverfly species acrossBritain from 1980 to 2013 25 had disappeared from theplaces they had inhabited in 1980 Further estimates foundanet loss of over 27million in 06mi (1 km) grid cells acrossall species Declining pollinator evenness suggested losseswere concentrated in rare species Losses linked to specifichabitats were also identified with a 55 decline amongwild upland species while dominant crop pollinatorsincreased by 12 possibly due to agricultural businessinterventions The general declines found a fundamentaldeterioration in both wider biodiversity and non-croppollination services

There is no question that the huge diversity of polli-nator species across the planet is suffering and that lossescould be catastrophicwith an estimated 90ofwild plantsand 30 of world crops in jeopardy [362]

There is a likelihood that rising EMF background levelsplay a role Bees have been known for decades to have an

astute sense of the Earthrsquos DC magnetic fields [363 364]and rely on that perception for survival For centuriesbeekeepers had noticed curious movements in bee hivesbut Austrian ethologist Karl von Frisch finally interpretedthat activity in the 1940s winning the Nobel Prize in 1973for what came to be known as the honey bee ldquowaggledancerdquo Through complex circles and waggle patternsbees communicate the location of food sources to othermembers of the hive using the orientation of the sun andthe Earthrsquos magnetic fields as a gravity vector ldquodancingrdquoout a map for hive members to follow like naturersquos ownimbeddedGPS Bees also detect the sunrsquos direction throughpolarized light and on overcast days use the Earthrsquos mag-netic fields likely through the presence of magnetite intheir abdominal area and employ complex associativelearning and memory [365]

Building on the earlier work of Gould et al [119]Kobayashi and Kirschvink [52] noted that biogenicmagnetite in honey bees is located primarily in the anteriordorsal abdomen When small magnetized bits of wire wereglued over those areas it interfered with beesrsquo ability tolearn to discriminate magnetic anomalies in conditioningexperiments while nonmagnetized wire used in controlsdid not interfere [366] Kirschvink and Kobayashi [367]found that when pulse-remagnetization techniques wereused on bees trained to exit from a T-maze that north-exiting bees could be converted to a south-exiting directionsimilar to what was observed in magnetobacteria andartificial reorientation by Blakemore [113] Honeybeescould also be trained to respond to very small changes inthe geomagnetic field intensity [368] Valkova and Vacha[369] discussed the possibility that honey bees use acombination of both radical paircryptochromes andmagnetite to detect the geomagnetic field and use it fordirection like many birds

Given these sensitivities bees may be reacting nega-tively through muti-sensory mechanisms to numeroussources of anthropogenic multi-frequency interferenceBumble bees (Bombus terrestris) a solitary species andhoney bees (Apis mellifera) a social hive species areknown to detect weak electric fields in different behavioralcontexts using different sensorymechanisms Bumble beee-field detection is likely through mechanosensory hairs[370ndash372] while honey bees reportedly use their antennae[373] that are electro-mechanically coupled to the sur-rounding e-field taking place in the antennal Johnstonrsquosorgan Greggers et al [373] found that honey bee antennaeoscillate under electric field stimulation that can thenstimulate activity in the antennal nerve The latter occursdue to bees being electrically charged and thus subject toelectrostatic forces Erickson [374] found different surface

Levitt et al EMF and wildlife 31

potentials in bees when leaving or entering hives andColin et al [375] found seasonal variability between posi-tive and negative charges in resting bees It has also beenshown that honey bees with removed or fixed antennae areless able to associate food reward with electric field stimuliand that bees emanate modulated electric fields whenmoving their wings (at about 230 Hz) and body (at about165 Hz) during the waggle dance [373]

Electro-ecological interplay between flowers andpollinators has also been known since the 1960s and iscritical to pollen transfer from flowers to bees [376ndash378]It is known that as bees fly through the air they accu-mulate a positive charge Flowers on the other handwhich are electrically grounded through their root sys-tems tend to have a negative charge in their petalscreated by surrounding air that carries around 100 V forevery meter above ground The accumulating positivecharge around the flower induces a negative charge in itspetals which then interacts with the positive charge inbees In fact bees do not even need to land on flowers forpollen transfer to occur pollen can ldquojumprdquo from theflower to the bee as the bee approaches due to chargedifferentials between the two Thus it appears that beesand flowers have been ldquocommunicatingrdquo via electricfields all along [379] Bees can also learn color discrimi-nation tasks faster when color cues are paired with arti-ficial electric field cues similar to those surroundingnatural flowers but did not learn as readily in an elec-trically neutral environment [370]

This evidence points to floral e-fields being used in aco-evolutionary symbiotic relationship with bees Clarkeet al [370 371] even found that bumblebees can distin-guish between flowers that give off different electric fieldsas floral cues to attract pollinators Like visual cues floralelectric fields exhibit complex variations in pattern andstructure that bumblebees can distinguish contributing tothe myriad complex cues that create a pollinatorrsquos memoryof floral food sources And because floral electric fieldscanmdash and domdash change within seconds of being visited bypollinators this sensory ability likely facilitates rapid anddynamic ldquoinformation exchangerdquo between flowers andtheir pollinators Bumblebees can even amazingly useelectric field information to discriminate between nectar-rewarding and unrewarding flowers [370]

Bees locusts ELF-EMF

Bees are also known to be sensitive to anthropogenicELF-EMF In 1973Wellenstein [380] found that high ten-sion powerlines adversely affected honey bees in woodenhives This in part prompted the Bonneville Power

Administration an American federal agency operating inthe Pacific Northwest under the US Department of Energy(US DOE) to investigate in 1974 [381ndash384] the effects oftransmission lines on people plants and animalsincluding honey bees The industry group Electric PowerResearch Institute also followed up on bee research [385386] Both of those studies confirmed that transmission lineelectric fields can affect honey bees inside wooden hives aswood is a poor insulator and current can be induced whenhives are placed in electric fields whether metal is presentor not The strength of the current inside the hive wasinfluenced by the electric field strength hive height andmoisture conditions with effects noticeable when inducedcurrent exceeded 002ndash004 mA Depending on hiveheight this occurred in field strengths between 2 and 4 kVm Effects included increased motor activity with transientincrease in hive temperature excessive propolis produc-tion (a resinous material used by bees as a hive sealer)decreased colony weight gains increased irritability andmortality abnormal production of queen cells queen lossdecreased seal brood andpoor over-winter colony survival[387] Impacts were most likely caused by electric shocksinside the hives [386 388] Effects were mitigated withgrounded metal screenshielding of hives [385] howeverbees appeared unaffected by magnetic fields whichpermeate metal shielding The authors concluded that theshielding results indicated that bees were unaffected byflying through an external electric field up to 11 kVm butnoted that the study design could not reveal if subtle effectswere occurring

A more recent study of electric fields by Migdał [389]focused on honey bee behavioral effects on walkinggrooming flight stillness contact between individualsand wing movement They found that the selected fre-quency intensity and duration of exposure effects beesrsquobehavioral patterns Bees were exposed for 1 3 and 6 h toE-fields at 50 kVm 115 kVm 230 kVm or 345 kVm(with controls under E-field lt20 kVm) Within theexposed groups results showed that exposure for 3 hcaused decreased time that bees spent on select behaviorsas well as the frequency of behaviors whereas after both 1and 6 h the behavioral parameters increased within thegroups The researchers concluded that a barrier allowingbehavioral patterns to normalize for some periods wasindicated although none of the exposed groups returned toreference values in controls which adhered to normalbehavioral patterns Bees may have compensatory win-dows that appear to be both time and intensity dependentfor E-fields The significance of this study is that bees mustaccomplish certain activities mdash like flight frequency andthe honey bee lsquowaggle dancersquo noted above mdash that are

32 Levitt et al EMF and wildlife

critical for life expectancy and survival Even slightsequential disturbances may have cascading effects

In an early-1988 study Korall et al [390] also foundeffects to bees from magnetic fields (MF) Bursts compa-rable to some of todayrsquos pulsed exposures of artificial MF at250 Hz mdash the frequency of buzzing during the waggledance mdash were applied parallel to natural EMF field linesand induced unequivocal lsquojumpsrsquo of misdirection by up to+10deg in bees during the waggle dance This alone couldcause directional confusion in hives Continuous fields of250 Hz with bursts perpendicular to the static MF howevercaused no effects They concluded that a resonance rela-tionship other than classic resonance models was indi-cated (see ldquoMechanismsrdquo above) This early work hasimplications for subsequent digital pulsing and all wirelessbroadband technology

More recent work on honey bees and ELF-EMF byShepherd et al [209] in 2018 found that acute exposure to50 Hz fields at levels from 20ndash100 μT (at ground level un-derneath powerline conductors) to 1000ndash7000 μT(within 1 m of the conductors) reduced olfactory learningforaging flight success toward food sources and feeding aswell as altered flight dynamics Their results indicated that50 Hz ELF-EMFs from powerlines is an important envi-ronmental honey bee stressor with potential impacts oncognitive and motor abilities

Some wasp species have also been found sensitive toELF-EMF Pereira-Bomfim et al [391] investigated themagnetic sensitivity of the social paper wasp (Polybiapaulista) by analyzing wasp behavior in normal geomag-netic fields and in the presence of external magnetic fieldsaltered by either permanent magnets (DC fields) or byHelmholtz coils (AC fields) They evaluated the change inforaging rhythm and colony behavior as well as the fre-quency of departinghomeward flights and the behavioralresponses of worker wasps located on the outer nest sur-face They found that the alteredmagneticfield from theDCpermanent magnet produced an increase in the frequencyof departing foraging flights and also that wasps groupedtogether on the nest surface in front of the magnet withtheir heads and antennae pointing toward the perturbationsource possibly indicating a response to a potential threatas a defense strategy Controls showed no such groupingbehavior The AC fields created by the Helmholtz coils alsoincreased foraging flights but individuals did not showgrouping behavior The AC fields however induced waspworkers to perform ldquolearning flightsrdquo They concluded thatfor the first time P paulista demonstrated sensitivity to anartificial modification of the local geomagnetic field andthat mechanisms may be due to both cryptochroneradicalpairs and magnetite

Another flying insect model mdash desert locust (Schisto-cerca gregaria)mdashwas found susceptible to entrainment byELF-EMF In a complex study Shepherd et al [392]analyzed acute exposure to sinusoidal AC 50 Hz EMF (fieldstrength range 10 to 10000 μT) vs controls on flights ofindividual locusts tethered between copper wire coilsgenerating EMFs at various frequencies and recorded onhigh-speed video Results found that acute exposure to50 Hz EMFs significantly increased absolute change inwingbeats in a field-strength-dependent manner Applyinga range of ELF-EMF close to normal wingbeat occurancethey found that locusts entrained to the exact frequency ofthe applied EMF They concluded that ELF exposure canlead to small but significant changes in locust wingbeatslikely due to direct acute effects on insect physiology (vscryptochrome ormagnetite-basedmagnetoreception) andor behavioral avoidance responses to molecularphysio-logical stressWyszkowska et al [393] also found effects onlocustsmdash exposure to ELF-EMF above 4mT led to dramaticeffects on behaviour physiology and increased Hsp70protein expression Such higher exposures may be foundnear high tension lines

Bees RF-EMF

The effects of RF-EMF on bees is of increasing interest sincethat is the fastest rising EMF environmental exposure of thepast 30 years [369] Beginning in the early 2000s studies ofcell phones placed in the bottom of hives began to appearHoney bees showed disturbed behavior when returning tohives after foraging and under various RFR exposures[394ndash396] Early methodologies however were not welldesigned or controlled For instance Favre [397] foundincreased piping mdash a distress signal that honey bees giveoff to alert hive mates of threats andor to announce theswarming process Both active and inactive mobile phonehandsetswere placed in close proximity to honey beeswithsounds recorded and analyzed Audiograms and spectro-grams showed that active phone handsets had a dramaticeffect on bee behavior in inducedworker piping This studywas criticized by Darney et al [398] for using music in theactive RFR exposurewhichmay have introduced a variablecapable of affecting bee piping in response to the addedsound alone

In a complex study Darney et al [398] tested highfrequency (HF) and ultra high frequency (UHF) used inRFID technology in order to develop a method to auto-matically record honey bees going in and out of hives Theyglued RFID tags onto individual bee dorsal surfaces thatwere detected at the hive entrance by readers emitting HFradio waves They then looked for possible HF adverse

Levitt et al EMF and wildlife 33

effects on honey beesrsquo survival Eight-day-old honey beeswere exposed to HF 1356 MHz or UHF 868 MHz RFR for 2 hsplit into ON and OFF periods of different durations Deadbees were counted daily with cumulative mortality rates ofexposed and non-exposed honey bees compared sevendays after exposure Two out of five experimental condi-tions found increased mortality once after HF and onceafter UHF exposure with OFF duration of 5 min or moreafter which they recommended limiting honey bee expo-sure to RFR to less than 2 h per day They also curiouslyconcluded that the RFID parameters they used for moni-toring hive activity presented no adverse effects but themultifrequency peak exposures and RFID attachmentsneed further study in light of other works on RFID effects(see Part 1 for discussion of RFID)

In another study using an active cell phone attached tohive frames Odemer and Odemer [399] investigated RFReffects on honey bee queen development and mating suc-cess Control hives had an inactive cell phone attachedAfter exposing honey bee queen larvae to GSM 900 MHzRFR during all stages of pre-adult development (includingpupation) hatching of adult queens was assessed 14 daysafter exposure and mating success after an additional11 days They found that chronic RFR exposure signifi-cantly reduced honey bee queen hatching that mortalitiesoccurred during pupation but not at the larval stages thatmating success was not adversely affected by the irradia-tion and that after exposure surviving queenswere able toestablish intact colonies They therefore determined thatmobile phone radiation had significantly reduced thehatching ratio but not mating success if queens survivedand if treated queens successfully mated colony devel-opment was not adversely affected Even though theyfound strong evidence of mobile phone RFR damage topupal development they cautioned its interpretationnoting that the studyrsquos worst-case exposure scenario wasthe equivalent of a cell phone held to a userrsquos head not at alevel found in typical urban or rural hive settings Theyconcluded that while no acute negative effects on beehealth were seen in the mid-term they also could not ruleout effects on bee health at lower chronic doses such asfound in ambient environments and urgently called forlong term research on sublethal exposures present inmajorcity environments

Sharma andKumar [400] found similar abnormalitiesin honey bee behavior when they compared the perfor-mance of honey bees in RFR exposed and unexposedcolonies Two of four test colonies were designated andeach equipped with two functional cell phones mdash a highexposuremdash placed on two different hive side walls in callmode at GSM 900 MHz The average RFR power density

was measured at 8549 μWcm2 (568 Vm electric field)One control colony had a dummy phone the other had nophone Exposure was delivered in 15 min intervals twiceper day during the period of peak bee activity Theexperiment was performed twice a week during Februaryto April It covered two brood cycles with all aspects ofhive behavior observed including brood area comprisingeggs larvae and sealed brood queen proficiency in egg-laying rate foraging flight behavior returning abilitycolony strength including pollen storage and other var-iables Results included a significant decline in colonystrength and egg laying and reduced foraging to the pointwhere there was no pollen honey brood or bees by theend of the experiment One notable difference in thisstudy was that the number of bees leaving the hivedecreased following exposure There was no immediateexodus of bees as a result of exposure mdash instead beesbecame quiet still andor confused ldquohellipas if unable todecide what to dohelliprdquo the researchers said Such aresponse had not been reported before The authorsconcluded that colony collapse disorder is related to cellphone radiation exposures

Vilić et al [401] investigated RFR and oxidative stressand genotoxicity in honey bees specifically on the activityof catalase superoxide dismutase glutathione S-trans-ferase lipid peroxidation levels and DNA damage Larvaewere exposed to 900 MHz RFR at field levels of 10 23 41and 120 Vmminus1 for 2 h At a field level of 23 Vmminus1 the effect of80AM 1 kHz sinusoidal and 217 Hz modulation were alsoinvestigated They found that catalase activity and the lipidperoxidation levels significantly decreased in larvaeexposed to the unmodulated field at 10 V mminus1 (27 μWcm2)compared to the control Superoxide dismutase andglutathione S-transferase activity in honey bee larvaeexposed to unmodulated fields were not statisticallydifferent compared to the control DNA damage increasedsignificantly in larvae exposed to modulated (80 AM at1 kHz) field at 23 V mminus1 (140 μWcm2) compared to controland all other exposure groups Their results suggested thatRFR effects in honey bee larvae manifested only aftercertain EMF exposure conditions Interestingly they foundthat increased field levels did not cause a linear dose-response in any of the measured parameters whilemodulated RFR produced more negative effects than thecorresponding unmodulated field They concluded thatwhile honey bees in natural environments would not beexposed to the high exposures in their experiments theresults indicated additional intensive research is needed inall stages of honey bee development since the cellular ef-fects seen could affect critical aspects of bee health andsurvival

34 Levitt et al EMF and wildlife

Kumar et al [402] also found biochemical changes inworker honey bees exposed to RFR A wooden box wasdesigned with glass on the front and back and wire gauzefor ventilation on two sides for both exposed bees andcontrols Cell phones (same make model and networkconnection) were kept in listen-talk mode for 40 min Atintervals of 10 20 and 40 min 10 exposed and 10 controlbees were collected at the same times Hemolymph wasthen extracted from the inter-segmental region of bee ab-domens and analyzed Results included increased con-centration of total carbohydrates in exposed bees in the10 min exposure period compared to unexposed beesIncreasing the exposure time to 20min resulted in a furtherincrease in the concentration but exposure at 40min had areverse effect with declines in carbohydrate concentrationalthough it was still higher than controls Hemolymphglycogen and glucose content also showed the sameexposure pattern mdash increase in content up to 20 min afterwhich a slight decline that was still higher than controlsChanges in total lipidscholesterol mdash the major energy re-serves in insects mdash can affect numerous biological pro-cesses Some lipids are crucial membrane structurecomponents while others act as rawmaterials in hormonesand pheromones Changes in these parameters are signif-icant to every biological activity including reproductionAlso of interest in this study was that as exposure timeincreased the bees appeared to have identified the sourceof disturbance There was a large scale movement ofworkers toward the talk-mode (with higher RFR exposureduring transmission function) but not the listening modeBees also showed slight aggression and agitation withwing beating The researchers hypothesized that thisincreased activity could be responsible for increased en-ergy use thereby accounting for the decrease in concen-tration of carbohydrates and lipids in the 40 min exposedsample The researchers concluded that cell phone radia-tion influences honey bee behavior and physiologySharma [403] had also reported increased glycogen andglucose levels in exposed honey bee pupa

It must be pointed out that the cell phone emissionconditions used in some experiments are questionable inparticular where there was no detail regarding how thephones were activated to achieve emission

Not all studies demonstrated adverse effects Mall andKumar [404] found no apparent RFR effects on brood rearinghoney production or foraging behavior in honey bees in hiveswith cell phones inside or near a cell tower and Mixon et al[405] also found no effects of GSM-signal RFR on increasedhoney bee aggression They concluded that RFR did notimpact foraging behavior or honey bee navigation andtherefore was unlikely to impact colony health

Although there are several anectodal reports of insectlosses near communication towers there are only ahandful of ambient RFR field studies conducted on in-vertebrates thus far In the first large survey of wild polli-nating species at varying distances from cell towers Laacutezaroet al [406] found both positive and negative effects fromRFR in a broad range of insects on two islands (Lesvos andLimnos) in the northeastern Aegean Sea near GreeceMeasured ambient RFR levels included all frequencyranges used in cell communications broadcast RFR isabsent on the islands RFR values did not significantlydiffer between islands (Lesvos 027 plusmn 005 Vm Limnos021 plusmn 004 Vm v3 2 = 008 p=0779) and did not decreasewith the distance to the antenna possibly they hypothe-sized because some sampling points near the antennamayhave beenoutside or at the edge of the emission lobes Theymeasured RFR at four distances of 50 100 200 and 400 m(164 328 656 and 1312 ft respectively) from 10 antennas(5 on Lesvos Island and 5 on Limnos Island) and correlatedRFR values with insect abundance (numbers of insects)and richness (general health and vitality)mdash the latter onlyfor wild bees and hoverflies The researchers conductedcareful flowering planttree- and- insect inventories inseveral low-lying grassland areas including for wild beeshoverflies bee flies other remaining flies beetles butter-flies and of various types Honey beeswere not included inthis study as they are a managed species subject tobeekeeper decisions and therefore not a wild species OnLesvos 11547 insects were collected and on Limnos 5544Varied colored pan traps for both nocturnal and diurnalsamples were used Results found all pollinator groupsexcept butterflieswere affected by RFR (both positively andnegatively) and for most pollinator groups effects wereconsistent on both islands Abundance for beetles waspsand hoverflies significantly decreased with RFR but overallabundance of wild bees and bee flies significantlyincreased with exposure Further analysis showed thatonly abundance of underground-nesting wild bees waspositively related to RFR while wild bees nesting aboveground were not affected RFR effects between islandsdiffered only on abundance of remaining flies On speciesrichness RFR tended to only have a negative effect onhoverflies in Limnos Regarding the absence of effects seenin butterflies they hypothesized that the pan trap collec-tion method is not efficient for collecting butterflies (but-terflies accounted for only 13 of total specimens) andthat a different samplingmethodmight produce a differentresult They concluded that with RFRrsquos negative effects oninsect abundance in several groups leading to an alteredcomposition of wild pollinators in natural habitats it waspossible this could affect wild plant diversity and crop

Levitt et al EMF and wildlife 35

production They further said the negative relationshipbetween RFR on the abundance of wasps beetles andhoverflies could indicate higher sensitivity of these insectsto EMFs Potentially more EMF-tolerant pollinators suchas underground-nestingwild bees andbeefliesmayfill thevacant niches left by less tolerant species thus resulting intheir population increases Another possible explanation isthat EMFs may have particularly detrimental effects onmore sensitive larval stages and if so larvae developingabove ground (many beetles wasps hoverflies) may bemore vulnerable than those developing underground sincethe former could be exposed to higher radiation levels

In another field study Taye et al [407] placed fivehives from December to May at varying distances of 1000500 300 200 and 100 m (3280 1640 984 656 and 328 ftrespectively) from a cell tower in India to measure flightactivity returning ability and pollen foraging efficiency inhoney bees (Apis cerana F) They foundmost effects closestto towers with the least returning bees at 100 m distancefrom the tower Maximum foraging and return ability to thecolonies was seen at 500 m followed by 1000 m and indescending order at 300 and 200 m with the fewestreturning bees at 100 m from the tower The study alsofound that if bees returned the pollen load per minute wasnot significantly affected

Vijver et al [408] however challenged the accuracy ofdistance from towers that is often used as a proxy for EMFgradients such as the study above In a field study in TheNetherlands the researchers tested exposure to RFR from acell base station (GSM 900 MHz) on the reproductive ca-pacity of small virgin invertebrates during the most sensi-tive developmental periods spanning preadolescent tomating stages when reproductive effects would most likelybe seen Careful RFR field measurements were taken todetermine null points in order to see if distance fromemitters is a reliable RFR exposure model in field studiesThey exposed four different invertebrate hexapod speciesSpringtails (Folsomia candida) predatory lsquobugsrsquo (Oriuslaevigatus) parasitic wasps (Asobara japonica) and fruit-flies (D melanogaster) were placed in covered pedestalcontainers within the radius of approximately 150 m of a900 MHz mobile phone base station for a 48-h period Sixcontrol groups were placed within 66 ft (2 m) of thetreatment groups and covered in Farady cages Afterexposure all groups were brought to the laboratory tofacilitate reproduction with resulting fecundity and num-ber of offspring then analyzed Results showed that dis-tance was not an adequate proxy to explain dose-responseregressions After complex data synthesis no significantimpact from the exposure conditions measures of centraltendency or temporal variability of EMF on reproductive

endpoints were found although there was some variabilitybetween insect groups As seen in other studies distance isoften used to create a gradient in energy exposures instudies but this study found the intensity of the transmitterand the direction of transmission to be more relevant asdid Bolte andEikelboom [409 410] The direction and tilt ofthe transmitter determines whether the location of interestin field studies is in the main beam In some instances thecloser promixity to the transmitter provided lower readingsthan further away which they found between two loca-tions They also noted that the organisms selected in thestudy were small in size springtails have a body length onaverage of 2 mm wasps are about 3 mm insect sizes from14 to 24 mm with the largest organisms tested being fe-male fruit flies at about 25 mm length and males slightlysmaller Due to size limited absorption and little energyuptake capacity none of these insects are efficient whole-body receptors for 900 MHz waves with a wavelength ofapproximately 13 in (33 cm) But they further noted that thiswas a linear regression study and that biological effects areoften non-linear However finding no distinct effects didnot exclude physiological changes They concluded thatbecause of RFR exposurersquos increasing ubiquity urgentattention to potential effects on biodiversity is needed

The issue of insect size nonlinearity and antenna tiltdirection are factors of critical importance with 5G radia-tion which will create extremely complex near- and- far-field ambient exposures to species in urban and rural en-vironments alike not only fromadensification of small cellantennas close to the ground but also from increased sat-ellite networks circling in low Earth orbits (see Part 1) Therange of frequencies used for wireless telecommunicationsystems will increase from below 6 GHz (2G 3G 4G andWiFi) to frequencies up to 120 GHz for 5G which due tosmaller wavelengths is therefore a better resonant matchfor small insects An alarming study by Thielens et al [411]drawing on numerous robust studies of RFRrsquos decades-long use as a thermal insecticide modeled absorbed RFRin four different types of insects as a function of fre-quency alone from 2 to 120 GHz A set of insect modelswas obtained using novel Micro-CT (computer tomogra-phy) imaging and used for the first time in finite-difference time-domain electromagnetic simulationsAll insects showed frequency-dependent absorbed po-wer and a general increase in absorbed RFR at and above6 GHz in comparison to the absorbed RFR power below6 GHz Their simulations showed that a shift of 10of theincident power density to frequencies above 6 GHzwould lead to an increase in absorbed power between3ndash370 mdash a large differential of serious potentialconsequence to numerous insect species

36 Levitt et al EMF and wildlife

Using a similar approach Thielens et al [412] focusedon the western honey bee (Apis mellifera) with RF-EMFusing a combination of in-situ exposure measurementsnear bee hives in Belgium and numerical simulationsAround five honey bee models were exposed to planewaves at frequencies from 06 to 120 GHz mdash frequenciescarved out for 5G Simulations quantified whole-bodyaveraged RFR absorbed as a function of frequency andfound that the average increased by factors of 16ndash121(depending on the specimen) when frequency increasedfrom 06 to 6 GHz for a fixed incident electric field strengthA relatively small decrease in absorption was observed forall studied honey bees between 12 and 120 GHz due tointerior attenuation RFR measurements were taken at 10bee hive sites near five different locations Results foundaverage total incident RFR field strength of 006 Vm thosevalues were then used to assess absorption and a realisticrate was estimated between 01 and 07 nW Theyconcluded that with an assumed 10 incident powerdensity shift to frequencies higher than 3 GHz this wouldlead to an RFR absorption increase in honey bees between390 and 570 mdash a frequency shift expected with thebuildout of 5G

The two previous studies alone should give pauseregarding environmental effects to invertebrates in thesehigher 5G frequency ranges

Kumar [413] noted that RFR should be included ascausal agents of bee CCD and that test protocols need to bestandardized and established Standardization is criticalsincemany studies conductedwith cell phones in hives areof very uneven quality and only indicative of potential ef-fects Placing cell phones in hives and assuming that RFR isthe only exposure is inaccurate and misleading ELF-EMFsare always present in all telecommunications technologyusing pulsed and modulated signals [414] All of thesecharacteristics have been found to be highly biologicallyactive apart from frequency alone Such studies are likelycapturing ELF effects without identifying them All aspectsof transmission including transmission engineering itselffrom towers need to be considered to determine accurateexposures and delineate causative agents Vibration andheatmust also be consideredmdash cell phones in transmissionmode could raise hive temperature quickly and bees arehighly temperature sensitive Due to ldquowaggle dancerdquo spe-cifics in creating foraging ldquoroadmapsrdquo bees should not beartificially relocated from hives to determine return abilityafter EMF exposure They may be confused by relocationalone adversely affecting their return abilities Such testsalso involve only one stressor when there are multiplestressors on insect species today Understanding such co-factors is critical in determining accurate data and

outcomes [415 416] Translating laboratory studies to fieldrelevance has always been problematic but understandingEMF effects to insects has become urgent with everincreasing low-level ambient exposure from devices andinfrastructure especially in light of the new 5G networksbeing built There are numerous variables that studies haveyet to factor in All of the above indicates a critical need tostandardize experimental protocols and to take electro-ecology far more seriously especially regarding aerialspecies in light of 5G

Aquatic environments

There are fundamental electrical differences in conduc-tivity (how well a material allows electric current to flow)and resistivity (how strongly amaterial opposes the flow ofelectric current) between air and water Through waterEMF propagation is very different than through air becausewater has higher permittivity (ability to form dipoles) andelectrical conductivity Plane wave attenuation (dissipa-tion) is higher in water than air and increases rapidly withfrequency This is one reason that RFR has not traditionallybeen used in underwater communication while ELF hasbeen Conductivity of seawater is typically around 4 Smwhile fresh water varies but typically is in the mSm rangethus making attenuation significantly lower in fresh waterthan in seawater Fresh water however has similarpermittivity as sea water There is little direct effect on themagnetic field component in water mediums propagationloss is mostly caused by conduction on the electric fieldcomponent Energy propagation continually cycles be-tween electric and magnetic fields and higher conductionleads to strong attenuationdissipation of EMF [98]

Because of these essential medium differences electro-receptormechanisms in aquatic speciesmay be very differentthan those previously described in aerial species since air is aless conductive and resistive medium with less attenuationThat is why RFR travels more easily and directly through airIn aquatic species electroreception may be a result of trans-mission via water directly to the nervous system throughunique receptor channels called Ampullae of Lorenzini [371]In frogs amphibians fish some worm species and othersreceptor channels may be through the skin as well as viamechanisms more common in aerial species such as in thepresence of magnetite (see ldquoMechanismsrdquo above) There canbe great variation in electroreceptive sensitivities in speciesinhabiting the two fundamentally different environmentsSome amphibian species however have physical charac-teristics that span both mediums and therefore varied mag-netoreception mechanisms

Levitt et al EMF and wildlife 37

Amphibians frogs salamandersreptiles regeneration abilities

Amphibians are the class of animals that include frogs

toads salamanders newts some reptiles and caecilians

The common term lsquofrogrsquo is used to describe thousands of

tailless amphibian species in theOrderAnura There are over

6300 anuran species recorded thus far with many more

likely disappearing today due to climate change and other

factors before we even knew they existed Informal distinc-

tions are made between frogs (thin-skinned species) and

toads (thick warty skins) but such distinctions are not used

for taxonomic reasons While the greatest concentration of

diverse frog species is in tropical rainforests they are widely

foundall over theworld from the tropics to subarctic regions

Most adult frogs live in fresh water andor on dry land while

some species have adapted to living in trees or underground

Their skin varies in all manner of colors and patterns from

graygreen and brownblack to bright redsyellowsFrog skin is smooth and glandular mdash something of

concern given nascent 5G technology (see Part 1)mdash and cansecrete toxins to ward off predators Frog skin is also semi-permeable which makes them highly susceptible to dehy-dration and pollutants With radical weather shifts due toclimate change and unpredictable swings betweenabnormal droughts followed by flooding in previouslyweather-stable regions environmentally sensitive am-phibians like frogs are considered bell-weather speciesFrequently time may be insufficient for some localregional species to regenerate in between radical weathercycles leading to population collapse

Since the 1950s there has been a significant decline infrog populations with more than one third of species todayconsidered threatened with extinction while over 120 spe-cies are already believed to have gone extinct since the1980s [10 417 418] This amphibian decline is consideredpart of an ongoing global mass extinction with populationcrashes as well as local extinctions creating grave impli-cations for planetary biodiversity [419] Amphibianextinction results are from climate change [420ndash422]habitat lossdestruction [423 424] introduced species[425] pollution [426] parasites [423 427] pesticides her-bicides and fungicides [428ndash430] disease [431ndash435] andincreased ultraviolet-B radiation [436ndash439] among othersAnthropogenic sound pollution may also affect amphibiancall rates and therefore impact reproduction [440] andartificial night lights affectmale green frog (Rana clamitausmelanota) breeding [441] Nonionizing electromagneticfields may also play a role [442]

McCallum [443] calculated that the current extinctionrate of amphibians could be 211 times greater than theirpre-anthropogenic natural ldquobackground extinctionrdquo ratewith the estimate rising 25000ndash45000 times if endan-gered species are also included in the computation Todaydeclining amphibian populations are seen in thousands ofspecies across numerous ecosystems including pristineforested areas [418] and declines are now recognizedamong the most severe impacts of the anthropocene era[417 442]

In addition the number of frogs with severe malfor-mations often incompatible with survival has risensharply Deformities are a complex issue related to physi-ology anatomy reproduction development water qual-ity changing environmental conditions and ecology ingeneral Any time deformities are observed in large seg-ments of wildlife populations there are indications ofserious environmental problems [442] Amphibian mal-formations are presumed due to an aggressive infectiousfungal disease called Chytridiomycosisy caused by thechytrid fungi Batrachochytrium dendrobatodis and Batra-chochytrium salamandrivorans [432ndash435] and by parasiteslike Ribeiroia ondatrae [427] Chytridiomycosis has beenlinked to dramatic amphibian declines and extinctions inNorth Central and South America across sections ofAustralia and Africa and on Caribbean islands likeDominica and Montserrat First identified in the 1970s inColorado US it continues to spread globally at analarming rate Some populations witness sporadic deathswhile others experience 100 mortality There is noeffective measure to control the disease in wild pop-ulations Herbicides like glyphosate used in Rounduptradeand atrazine an endocrine disruptor have also been foundto cause severe malformations in both aquatic and landamphibian species from farmland pesticideherbicidefungicide runoff [428ndash430]

Frogs are known to be highly sensitive to natural andmanmade EMF Much research into the electrophysiologyof frogs has been conducted because they are good labmodels for human nervous system research readilyavailable and easily handled As far back as 1780 theItalian physicist Luigi Galvani discovered what we nowunderstand to be the electrical basis of nerve impulseswhile studying static electricity (the only kind then known)when he accidentally made frog legmuscles contract whileconnected to the spinal cord by two different metal wires[444] Galvani thought he had discovered animalmagnetismrdquo but had actually discovered direct current andwhat later became known as a natural ldquocurrent of injuryrdquomdashthe process by which an injured limb for instance pro-duces a negative charge at the injury site that will later turn

38 Levitt et al EMF and wildlife

to a positive charge at the same site in some species asdiscovered in the 1960s by Robert O Becker [444ndash451] Theearliest curiosity about natural current continuedthroughout the 1800s on various aspects of EMF and laterthroughout the 1920s to 1940s in pioneering researchersElmer J Lund [452ndash454] and Harold Saxon Burr [455ndash457]who worked to establish the first unified electrodynamicfield theory of life using hydra frog and salamandermodels among several others because of their morpho-genic properties [458] While frogs do not regenerate limbsthe way salamanders do both are so similar in taxonomythat curiosity was high in the early pioneers cited abovethroughout the 1960s to 1990s about what fundamentallyallowed limb regeneration in one species by not the otherMuch was learned in the process about amphibian elec-trophysiology and cellular microcurrent in wound healingas well as the electrophysiological properties of cellulardifferentiation and eventually dedifferentiation pertinentto all contemporary stem cell research Today the impli-cations of this early work have gained new interest andtargeted research regarding endogenous microcurrent andlimb regeneration potential in humans as well as dedif-fentiationstem cellmorphogenesis in general for cancertreatment and other healing modalities For a thoroughreview of studies on morphogenesis see Levin [459]

Ubiquitous low-level ambient EMFs today match someof the natural low-level microcurrent found critical to thefundamental processes of amphibian growth reproduc-tion morphogenesis and regeneration lending newmeaning to the early research that defined amphibianelectrophysiology We just need to make far better use of itto understand what role if any todayrsquos ambient exposuresmay be contributing to amphibian losses (To comparetables between rising ambient EMF levels and low leveleffects in wildlife see Part 1 Supplement 1 and Part 2Supplement 3)

Amphibian and reptile magnetoreception

How amphibians perceive natural and manmade EMF issimilar to other species reviewed above and for amphibianmechanism reviews see Phillips et al [460 461] Likemanybird and insect species evidence indicates that amphib-ians perceive the Earthrsquos geomagnetic fields by at least twodifferent biophysical magnetoreception mechanismsnaturally occurring ferromagnetic crystals (magnetite)and light-induced reactions via specialized photo-receptorcells (cryptochromes) that form spin-correlated radicalpairs Like birds both mechanisms are present in someamphibians Cryptochromes provide a directional

lsquocompassrsquo and the non-light-dependent magnetite pro-vides the geographical lsquomaprsquo

In a thorough discussion of many magnetoreceptionstudies in anura and urodela species Diego-Rasilla et al[462] found evidence that Iberian green frog tadpoles(Pelophylax perezi) had a light-dependent magnetic com-pass and Diego-Rasilla et al [463] also found that tadpolesof the European common frog (Rana temporaria) arecapable of using the Earthrsquos magnetic field for orientingalong a learned y-axis In these studies they investigated ifthis orientation is accomplished using a light-dependentmagnetic compass similar to that found in the earlier ex-periments with other species of frogs and newts [460462ndash470] or from some other factor They concluded thatthe magnetic compass provided a reliable source of direc-tional information under a wide range of natural lightingconditions They also compared their findings to studies[470] that showed the pineal organ of newts to be the site ofthe light-dependent magnetic compass as well as to recentneurophysiological evidence showing magnetic fieldsensitivity located in the frog frontal organ which is anoutgrowth of the pineal gland They hypothesized thiswork could indicate a common ancestor as long ago as 294million years

To determine if orientation using Earthrsquos magneticfields changed according to seasonal migration patternsShakhparonov and Ogurtsov [471] tested marsh frogs(Pelophylax ridibundus) in the laboratory to see if frogscould determine migratory direction between the breedingpond and their wintering site according to magnetic cuesAdult frogs (n=32) were tested individually in a T-maze127 cm long inside a three-axis Helmholtz coil system(diameter 3 m) Maze arms were positioned parallel to thenatural migratory route and measured in accordance withthe magnetic field Frogs were tested in the breedingmigratory state and the wintering state mediated by atemperaturelight regime Frog choice in a T-maze wasevident when analyzed according to the magnetic fielddirection They moved along the migratory route to thebreeding pond and followed the reversion of the horizontalcomponent of the magnetic field The preference was seenin both sexes but only during the breeding migratory stateThey concluded that adult frogs obtained directional in-formation from the Earthrsquos magnetic field

Diego-Rasilla et al [472] found similar evidence in twospecies of lacertid lizards (Podarcismuralis and Podarcislilfordi) that exhibited spontaneous longitudinal body axisalignment relative to the Earthrsquos magnetic field during sunbasking periods Both species exhibited a highly signifi-cant bimodal orientation along the north-northeast andsouth-southwest magnetic axis Lizard orientations were

Levitt et al EMF and wildlife 39

significantly correlated over a five-year period withgeomagnetic field values at the time of each observationThis suggested the behavior provides lizards with a con-stant directional reference possibly creating a spacialmental map to facilitate escape This was the first study toprovide spontaneous magnetic alignment behavior in free-living reptiles although studies of terrapins have alsofound such spontaneousmagnetic alignment [92 323 473]Nishimura et al [474 475] also found sensitivity toELF-EMF (sinusoidal 6 and 8 Hz peak magnetic field26 μT peak electric field (10 Vm) in a lizard species(Pogona vitticeps) as demonstrated by significant increasedtail lifting mdash a reproductive behavior Interestingly thistail-lifting response to ELF-EMF disappeared when theparietal eye was covered suggesting that the parietal eyecontributes to light-dependent magnetoreception and thatexposure to ELF-EMFs may increase magnetic-field sensi-tivity in the lizards A further experiment [476] showed thatlight at a wavelength lower than 580 nm was needed toactivate the light-dependent magnetoreception of the pa-rietal eye

Amphibians RF-EMF

Most frogs spend significant time on land but lay eggs inwater where they hatch into tadpoles with tails and inter-nal gills However some species bypass the tadpole stageandor deposit eggs on land Frogs are thus subject to ex-posures from both land-based and aquatic environmentsA frogrsquos life cycle is complete when metamorphosis into anadult form occursMany adverse effects do not appear untilafter metamorphosis is completed but problems have beenfound throughout the entire life cycle after exposures toboth ELF-EMF and RFR

Most early research on frogs (other than the Beckeret al regeneration inquiries noted above) was conducted athigh thermal levels rarely encountered in the environmentbut some are included here because they helped delineateamphibian electrophysiology with effects later supportedin low-level research Some early work did use frog modelsto investigate cardiac effects with lower intensity expo-sures Levitina [477] found that intact frog whole-bodyexposure caused a decrease in heart rate while irradiationof just the head caused an increase Using VHF frequencyRFR at a power density of 60 μWcm2 A=125 cm Levitinaattributed the cardiac changes to peripheral nervous sys-tem effects but according to Frey and Siefert [478] becauseof the wavelengths used in that study little energetic bodypenetration would be expected They said a skin receptorhypothesis was therefore reasonable

Following on Levitinarsquos work Frey and Seifert [478]mdashusing isolated frog hearts UHF frequencies that penetratetissue more efficiently and low intensity pulse modula-tion mdash found that pulsed microwaves at 1425 GHz couldalter frog heart rates depending on the timing of exposurebetween the phase of heart action and themoment of pulseaction Twenty-two isolated frog hearts were irradiatedwith pulses synchronized with the P-wave of the ECGspulses were of 10 s duration triggered at the peak of theP-wave Two control groups were used without RFR ex-posures with no effects noted They found heart rate ac-celeration occurred with pulsing at about 200 ms after theP-wave But if the pulse occurred simultaneously with theP-wave no increases were induced Arrhythmias occurredin half the samples some resulting in cardiac cessationClearly from this study RFR affected frog heart rhythm andcould cause death

A more recent work by Miura and Okada [479] foundsevere vasodilation in frog foot webs from RFR In a seriesof three experiments using 44 anesthetized frogs (X laevis)at thermal and non-thermal intensities researchersexposed foot webs to pulsed RFR in three parameters withthe monitor coil set at 1 V peak-to-peak 100 kHz 582-3 mGand 17476 V cmminus1 10 MHz 73 mG and 219 V cmminus1 1 MHz539 mG and 1611 V cmminus1 They found not only dilated ar-terioles of the web which had already been re-constrictedwith noradrenaline but also dilated arterioles under non-stimulated conditions Vasodilatation increased slowlyand reached a plateau 60 min after radiationrsquos onset Afterradiation ceased vasodilation remained for 10ndash20 minbefore slowly subsiding Vasodilation was optimum whenpulsation was applied 50 of the total time at a 10 kHzburst rate at 10 MHz Effects were non-thermal The patternof vasodilation induced by warm Ringer solution wasdifferent from the vasodilatory effect of weak RFRinvolving the level of intracellular Ca2+ They hypothesizedthat since Ca2+ ATPase is activated by cyclic GMP which isproduced by the enzymatic action of guanylate cyclaseRF-EMF may activate guanylate cyclase to facilitate cyclicGMP production They concluded the study indicates for thefirst time that RFR dilates peripheral resistance vessels byneither pharmacological vasodilator agents nor physicalthermal radiation but that the precise mechanisms of acti-vation of guanylate cyclase by RFR at the molecular levelrequired further study Vasodilation and constriction affectsevery part of the body and can affect all organ systems

Prior to this Schwartz et al [480] found changes incalcium ions in frog hearts in response to a weak VHF fieldthat was modulated at 16 Hz This would be an exposurecommon in the environment Calcium ions are critical toheart function

40 Levitt et al EMF and wildlife

Balmori [24ndash30 442] and Balmori and Hallberg [271]have focused widely on EMF effects to wildlife with twopapers on amphibians Balmori [442] in a review notedthat RFR in the microwave range is a possible cause fordeformations and decline of some amphibian populationsand Balmori [481] in 2010 found increased mortality intadpoles exposed to RFR in an urban environment In the2010 study tadpoles of the common frog (Rana temporaria)were exposed to RFR from severalmobile phone towers at adistance of 459 ft (140 m) Two month exposures lastedthrough egg phase to advanced tadpole growth prior tometamorphosis RF andMW field intensity between 18 and35 Vm (086ndash32 μWcm2) were measured with threedifferent devices Results determined that the exposedgroup (n=70) had low coordination of movements andasynchronous growth that resulted in both large and smalltadpoles aswell as a disturbing 90highmortality rate Inthe control group (n=70) a Faraday cage was used underthe same conditions Controls found movement coordina-tion to be normal and development synchronous withmortality rate at a low 42 These results indicated thatRFR from cell towers in a field situation could affect bothdevelopment and mortality of tadpoles Prior to this studyGrefner et al [482] also found increased death in tadpoles(Rana temporaria L) exposed to EMF as well as highermortality rates and slower less synchronous development

Mortazavi et al [483] found changes in muscle con-tractions in frogs exposed to 900-MHz cell phone radiationfor 30 min gastrocnemimus muscles were then isolatedand exposed to a switched onoff mobile phone radiationfor three 10-min intervals The authors reportedRFR-induced effects on pulse height and latency period ofmuscle contractions SARs of the nerve-muscle preparationwere calculated to be 066 (muscle) and 0407 (nerve)Wkg

Rafati et al [484] investigated the effects of RFR onfrogs frommobile phone jamming equipment emitting RFRin the same frequencies as mobile phones (Althoughillegal inmany countries jammers are nevertheless used tointerfere with signals and stop communication) The studysought to follow up on reports of non-thermal effects ofRFR on amphibians regarding alterations of musclecontraction patterns They focused on three parametersthe pulse height of leg muscle contractions the time in-terval between two subsequent contractions and the la-tency period of frogrsquos isolated gastrocnemius muscle afterstimulation with single square pulses of 1 V (1 Hz) Animalsin the jammer group were exposed to RFR at a distance of1 m from the jammerrsquos antenna for 2 h while the controlfrogs were sham exposed All were then sacrificed andisolated gastrocnemius muscles were exposed to onoff

jammer radiation for three subsequent 10 min intervals(SAR for nerve and muscle of the different forms of jammerradiation was between 001 and 0052 Wkg) Resultsshowed that neither the pulse height of muscle contrac-tions nor the time interval between two subsequent con-tractions were affected but the latency period (timeinterval between stimulus and response) was statisticallysignificantly altered in the RFR-exposed samples Theyconcluded the results supported earlier reports of non-thermal effects of EMF on amphibians including the effectson the pattern of muscle contractions Control shamexposed samples showed no effects

Amphibians reptiles ELF-EMF

Amphibians are highly sensitive to ELF-EMF An early-1969study by Levengood [485] using a magnetic field probefound increased high rates of teratogenesis in frogs (Ranasylvatica) and salamanders (Ambystoma maculatum) Twoidentical probes using different field strengths wereemployed mdash both operated in the kilogauss region withhigh field gradients Amphibian eggs and embryos wereexposed at various stages of development with gross ab-normalities found in developing larvae vs control At thehatching stage severe abnormalities were noted in bothanuran and urodele larvae from probe-treated eggsHatching abnormalities included microcephaly altereddevelopment andmultiple oedematous growths In probe-treated frogs there was a delay in the appearance of a highpercentage of malformations until the climax stage ofmetamorphosis Until that stage the larvae were of thesame appearance as control specimens thus camouflagingthe damage after just a brief treatment of early embryosThe frog abnormalities at metamorphosis differed fromthose in the hatching tadpoles and consisted mainly ofsevere subepidermal blistering and leg malformationsincluding formation of multiple deformed limbs incom-patiblewith life Over 90of themorphological alterationsat metamorphosis climax were also found to be associatedwith deformed kidneys The gastrula stages of develop-ment appeared to be the most sensitive in the delayed-effects category While this was a high-field exposureexperiment it is an intensity that is found in some envi-ronments today especially near high tension lines and inabnormal ground current situations

Neurath [486] also found strongly inhibited early em-bryonic growth of the common leopard frog (Rana pipiens)by a high static magnetic field with a high gradient (1T) mdashan exposure sometimes found in the environmentmdash whileUeno and Iwasaka [487] found abnormal growth and

Levitt et al EMF and wildlife 41

increased incidence of malformations in embryos exposedto magnetic fields up to 8T but exposures that high aretypically near industrial sites and rarely found in nature

Severini et al [488] specifically addressed whetherweak ELF magnetic fields could affect tadpole develop-ment and found delayed maturation in tadpoles Two co-horts of X laevis laevis (Daudin) tadpoles were exposed for60 days during immaturity to a 50 Hz magnetic field of639ndash764 μT rms (root mean square average values)magnetic flux density in a solenoid Controls were twocomparable cohorts remotely located away from the sole-noid The experiment was replicated three times Resultsshowed reduced mean developmental rate of exposed co-horts vs controls (043 vs 048 stagesday plt 0001)beginning from early larval stages exposure increased themean metamorphosis period of tadpoles by 24 days vscontrols (p lt 0001) and during the maturation periodmaturation rates of exposed vs control tadpoles werealtered No increases in mortality malformations or tera-togenic effects were seen in exposed groups The re-searchers concluded that relatively weak 50 Hz magneticfields can cause sub-lethal effects in tadpoles via slowedlarval development and delays in metamorphosis Suchexposures are found in the environment today in somelocations and even though the changes were smallcoupled with climate change such sub-lethal effects mayimpact some wildlife populations in some environments

In similar followup work Severini and Bosco [489]found sensitivity to small variations of magnetic flux den-sity (50 Hz 22-day continuous exposure magnetic fluxdensities between 639 and 764 microT) in tadpoles exposed toa stronger field vs controls exposed to a weaker field Asignificant delay in development of 25 days was found inexposed vs controls They concluded the delaywas causedby the slightly differentmagnetic flux densities with resultssuggesting a field threshold around 70 microT in controlling thetadpole developmental rate

Schlegel in 1997 found European blind cave salaman-ders (Proteus anguinus) and Pyrenean newts (Euproctusasper) to be sensitive to low level electric fields in water[490] And Schlegel and Bulog [491] in followup workfound thresholds of overt avoidance behavior to electricfields as a function of frequency of continuous sine-wavesin water Nine salamanders from different Slovenian pop-ulations of the urodele (P anguinus) that included threespecimens of its lsquoblackrsquo variety (P anguinus parkelj)showed thresholds between 03 mVcm (ca 100 nAcm2)and up to 2 mVcm (670 nAcm2) with the most reactivefrequencies around 30 Hz Sensitivity included a total fre-quency range below 1 Hz (excluding DC) up to 1ndash2 kHzwithup to 40 dB higher thresholds These are ranges that may

be found in the wild near high tension lines and utilitygrounding practices near water by some underwater ca-bling and by some RFR transmitters

Landesman and Douglas in 1990 [492] found somenewt species showed accelerated abnormal limb growthwhen pulsed electromagnetic fields were added to thenormal limb regeneration process While normal limbregeneration found normal regrowth patterns in 72 ofspecimens 28 were abnormal Abnormalities includedloss of a digit fused carpals and long bone defects whichoccurred singly or in combination with one another Whenexposure to a PEMF was added for the first 30 days post-amputation followed by a 3ndash4 month postamputationperiod a group of forelimbs with unique gross defectsincreased by an additional 12 Defects (singly or incombination) included the loss of two or more digits withassociated loss of carpals absence of the entire handpattern and abnormalities associated with the radius andulna The researchers offered no explanation Exposureintensities were similar to those used to facilitate non-juncture fracture healing in humans

Komazaki and Takano in 2007 [493] found acceleratedearly development growth rates with 50 Hz 5ndash30 mTalternating current exposures in the fertilized eggs of Jap-anese newts (Cynops pyrrhogaster) The period of gastru-lation was shortened via EMF-promoted morphogeneticcell movements and increased [Ca2+]i They said their re-sults indicated that EMF specifically increased the [Ca2]i ofgastrula cells thereby accelerating growth This study onlyobserved through the larval stages and they did not see anymalformations under EMF exposures which they attrib-uted to possible differences in the intensity and mode ofEMF

With amphibians and some reptiles demonstratinghigh sensitivity to natural background EMF for importantbreeding and orientation needs amphibians living inaquatic terrestrial and aerial environments (ie tree frogspecies) may be affected from multi-frequency anthropo-genic EMF in ways we do not fully understand There arepotential effects mdash especially from 5G MMW that couplemaximally with skin mdash to all aspects of their developmentand life cycles including secondary effects

Fish marine mammals lobstersand crabs

Aquatic animals are exquisitely sensitive to natural EMFand therefore potentially to anthropogenic disturbanceThe Earthrsquos dipole geomagnetic field yields a consistent

42 Levitt et al EMF and wildlife

though varying source of directional information in bothland and aquatic species for use in homing behaviororientation during navigation and migration This infor-mation is used both as a lsquomaprsquo for positional information aswell as a lsquocompassrsquo for direction [494ndash497] Aquatic speciesare known to be sensitive to static geomagnetic fields at-mospheric changes and sunspot activities [498] For recentcomprehensive reviews onmagnetic field sensitivity in fishand effects on behavior see Tricas and Gill [36] and Krylovet al [33] Some biological lsquomagnetic mapsrsquo may beinherited [499] And for a recent extensive discussion of theEarthrsquos natural fields and magnetoreception in marineanimals with a focus on effects from electromagnetic sur-veys that use localized strong EMFs to map petroleum de-posits under seabeds see Nyqvist et al [498] and below

As mentioned above because of the difference inconductivity of water and other factors the way someaquatic species sense EMF may rely on unique modes ofphysiological perception as well as those employed byterrestrial animals There may also be sensory combina-tions not yet understood in some aquatic and semi-aquaticspecies For instance what role does the neural conduc-tivity of whiskers (vibrissae) in seals sea lions and walrusplay other than for food finding Aquatic speciesrsquo densenetwork of whiskers is larger with greater blood flow thanterrestrial species and can contain 1500 nerves per folliclevs cats at 200 per follicle Seal whiskers also varygeometrically from terrestrial species and the largest partof the seal brain is linked to whisker function Seals usewhiskers to map the size shape and external structure ofobjects and can find prey even when blindfolded Theirwhiskers are also sensitive to weak changes in water mo-tion [100] But are they also using them as a location ordirectional compass in relation to the geomagnetic fieldThat has yet to be studied

Unique sensory differences in aquatic species have longbeen documented Joshberger et al [500] noted that in 1678Stefano Lorenzini [501] was the first to describe a network oforgans in the torpedo ray that became known as the Ampullaeof Lorenzini (AoL) Its purpose was unknown for 300 yearsuntil Murray [502] measured AoLrsquos electrical properties inelasmobranch fishmdash sharks rays and skates Later work [101503ndash508] confirmed and greatly added to this knowledgeResearchers now know that AoL is likely the primary mecha-nism that allows elasmobranch fish to detect and map a po-tential preyrsquos physiology via the very weak changes in electricfields given off by preyrsquos muscle contractions

Individual ampullae are skin pores that open to theaquatic environment with a jelly-filled canal leading to analveolus containing a series of electrosensing cells Withinthe alveolus the electrosensitive cells of the ampullae

communicate with neurons and this integration of signalsfrom multiple ampullae is what allows elasmobranch fish todetect electric field changes as small as 5 nVcm [503 506509 510] TheAoL jelly has been reported as a semiconductorwith temperature-dependence conductivity and thermoelec-tric behavior [500 509 510] as well as a simple ionicconductor with the same electrical properties as the sur-rounding seawater [503 506] Josberger et al [500] attemptedto clarify what AoLrsquos role is in electrosensing by measuringAoLrsquos proton conductivity They found that room-temperature proton conductivity of AoL jelly is very high at2 plusmn 1 mScmmdash only 40-fold lower than some current state-of-the-art manmade proton-conducting polymers That makesAoL the highest conductive biological material reported thusfar They suggested that the polyglycans contained in theAoLjelly may contribute to its high proton conductivity

Other aquatic magneto-sensory mechanisms more inharmony with terrestrial animals include the presence offerromagnetic particles in magnetite mdash tiny naturally pro-duced magnets that align with the Earthrsquos magnetic fieldallowing for speciesrsquo direction and orientation Magnetite ap-pears to transmit necessary information through a connectionwith the central nervous system [340 497 511] A magnetite-based system is plausible for cetaceans [512 513] as magnetitehas been found in the meninges dura mater surrounding thebrains ofwhales anddolphins [514 515] There is also evidencethat local variationsanomalies in the geomagnetic field incertain underwater topographies may play a role in live ceta-cean strandings [516 517]which indicates amagnetic compassbased on magnetite And free-ranging cetaceans have shownevidence of magnetoreception-based navigation eg Finwhale migration routes have been correlated with lowgeomagnetic intensity [513]

Recently Granger et al [518] found correlations in databetween 31 years of gray whale (Eschrichtius robustus)strandings and sunspot activity especially with RF lsquonoisersquoin the 2800 MHz range The 11-year sunspot cycle stronglycorrelateswith the intense releases of high-energy particlesknown as solar storms which can temporarily modify thegeomagnetic field and in turn may modify orientation inmagnetoreceptive species Solar storms also cause an in-crease in natural broadband RF lsquonoisersquo They examinedchanges in both geomagnetic fields and RF lsquonoisersquo andfound RF to be a determinant Further they hypothesizedthat increased strandings during high solar activity is morelikely due to radical pair mechanisms which are morereactive with RFR than magnetite which appears morereactive to ELF-EMF Two previous studies also foundcorrelations with cetacean strandings and solar activities[519 520] Both mechanisms may come into play underdifferent circumstances or act in synergy

Levitt et al EMF and wildlife 43

Kremers et al [512] investigated the spontaneousmagnetoreception response in six captive free-swimmingbottlenose dolphins (Tursiops truncates) to introducedmagnetized and demagnetized devices used as controlsThey found a shorter latency in dolphins that approachedthe device containing a strong magnetized neodymiumblock compared to a control demagnetized block identicalin form and density and therefore indistinguishable withecholocation They concluded that dolphins can discrimi-nate on the basis of magnetic properties mdash a prerequisitefor magnetoreception-based navigation Stafne andManger [521] also observed that captive bottlenose dol-phins in the northern hemisphere swim predominantly in acounter-clockwise directionwhile dolphins in the southernhemisphere swim predominantly in clockwise directionNo speculation was offered for this behavior

How salmon navigate vast distances mdash from theirhatching grounds in freshwater river bottoms to lakesduring juvenile growth then the open ocean duringmaturity and with a final return to their neonatal birthinggrounds to spawn and die (for most anadromous salmo-nids)mdash has fascinated researchers for decades Research in-dicates they may use several magneto-senses to accomplishthis including inherited mechanisms [522] imprinting [499522] a magnetic compass [499 522 523] and biomagneticmaterials Salmon have been found to have crystal chains ofmagnetite [524] One recent study found that strongmagneticpulses were capable of disrupting orientation in salmonmodels [525] indicating a magnetite-based mechanism Insalmon the migration process is complicated by the fact thatthe ability to sense geomagnetic fields can be altered bychanges in salinity between fresh and salt water thuspointing to multi-sensory mechanisms [499]

Speculation that salmon use the geomagnetic field insome capacity for their iconic migration goes back decades[526] Quinn [527] found evidence that sockeye salmon(Oncorhynchus nerka) frey use both a celestial and magneticcompass when migrating from river hatching to lakes Put-man et al [499] whohavewritten extensively on this subjectfocused on how salmon navigate to specific oceanic feedingareas mdash a challenge since juvenile salmon reach feedinghabitats thousands of kilometers from natal locations Theresearchers experimentally found that juvenile Chinooksalmon (Oncorhynchus tshawytscha) responded to magneticfields similar to latitudes of their extreme ocean range byorienting in directions that would lead toward their marinefeeding grounds They further found that fish use the com-bination ofmagnetic intensity and inclination angle to assesstheir geographic location and concluded that the magneticmap of salmon appears to be inherited since the fish had noprior migratory experience These results paired with

findings in sea turtles (see below) indicate that magneticmapsarewidespread in aquatic species and likely explain theextraordinary navigational abilities seen in long-distanceunderwater migrants [499]

It is less likely that light-sensing radical pair crypto-chromes play much of a role in aquatic species thoughsome hypothesize the possibility [528] Krylov et al [33]however noted that there are no anatomical structures orneurophysiological mechanisms presently known forradical pair receptors in the brains of fish and that sincelight decreases with water depth and fish are capable oforienting in complete darkness using the geomagneticfield their opinion was that it is too early to say fish havemagnetoreception mechanisms based on free radicalslight-dependent or otherwise

Fish lobsters crabs ELF-EMF

For several reasons having to do with differences in con-ductivity in water vs air (see above) RFR is of far lessconcern in aquatic environments at present than is ELFWith the ever-increasing number of underwater cablesused for everything from transcontinental datacommu-nications to power supplies for islands marine platformsunderwater observatories off-shore drilling wind facil-ities tidal and wave turbines among others many newsources of both AC and DC electric current are beingcreated in sea and freshwater environments alike Ac-cording to Ardelean and Minnebo writing in 2015 [529]almost 4971 mi (8000 km) of high voltage direct current(HVDC) cables were present on the seabedworldwide 70of which were in European waters and this is only ex-pected to grow dramatically as new sources of renewableenergy are built to replace fossil fuels globally

Curiosity about potential adverse effects from cable-generated ELF-EMF on all phases of fish life has alsogrown especially in benthic and demersal species thatspend significant time near cables in deeper bottom envi-ronments for egg laying larvae growth and developmentfor most if not all of their adult lives

Fey et al [494 495] and Oumlhman et al [530] noted thatthere are two types of anthropogenic exposures created bycables high voltage direct current (HVDC) that emits staticmagnetic fields and three-phase alternating current (ACpower transmission) that emit time-varying electromag-netic fields The density of electric current near underwatercables on the sea floor can vary significantly depending onthe type of cable and whether they are positioned on thesea bottom or buried [36 530] Noticeable magnetic fieldchanges can occur within meters but generally not more

44 Levitt et al EMF and wildlife

than several meters from the cable However Hutchinsonet al [531] in a robust field study and extensive reviewfound surprisingly stronger and more complex exposuresthan anticipated (see below)

Since fish are highly sensitive to static magnetic fields(MF) it is important to delineate static fields from anthro-pogenic alternating current EMF in aquatic studies Infreshwater species under laboratory conditions Fey et al[494] found similar results to those of salmon studies(noted above) in northern pike (Esox lucius) exposed to astatic magnetic field from DC cables (10 mT) during theembryonic phase and in the first six days of post-hatchingNo statistically significant MF effect was seen on hatchingsuccess larvae mortality larvae size at hatching andgrowth rate during the first six days of life However sig-nificant MF effects were seen on hatching time (one dayearlier in a magnetic field than in control) yolk-sac sizewas smaller and yolk-sac absorption rate was faster Theyinterpreted the faster yolk-sac absorption in a magneticfield as an indication of increasedmetabolic rate but addedthat even if some negative consequences were expected asa result that the actual risk for increased northern pikelarvae mortality seemed negligible Though higher than10 mT magnetic field values are hazardous for fish larvaethey added such values do not occur in the natural envi-ronment even along underwater cables

But in follow-up work of longer duration the samegeneral research group reached a different conclusion Feyet al [495] studied effects on eggs and larvae of rainbowtrout (Oncorhynchus mykiss) exposed to a static magneticfield (MF) of 10 mT and a 50 Hz EMF of 1 mT for 36 days(ie from eyed egg stage to approximately 26 days posthatching) They found that while neither the static MF northe 50-Hz EMF had significant effects on embryoniclarvalmortality hatching time larval growth or the time oflarvae swim-up from the bottom both fields did howeverenhance the yolk-sac absorption rates While they said thiswas not directly related to a MF effect it was shown thatlarvaewith absorbed yolk-sacs by the time of swim-upwereless efficient in taking advantage of available food at firstfeeding and gained less weight They concluded that theseexposures could negatively affect the yolk-sac absorptionrate thereby hampering fish in important feeding activitiesneeded for fast weight gain and increased survival In anadditional study Fey et al [532] observed that rainbowtrout reared in a laboratory for 37 days and exposed to astatic MF (10 mT) or a 50-Hz EMF (1 mT) showed defects inotolith of the inner ear which is responsible for hearing andbalance in fish The authors concluded that underwaterconstruction andor cables that emit a MF of 10 mT orhigher can affect living organisms within a few meters

distance especially species like trout in settled life stageson the sediment bottom during early development

Zebrafish (Danio rerio) are often used in EMF research intoxicology and developmental biology investigating effectson humans because the genomes are so similar Li et al [533]studied ELF-MF on the development of fertilized zebrafishembryos divided into seven groups Embryos of experi-mental groups were continuously exposed to 50-Hz sinu-soidal MF with intensities of 30 100 200 400 or 800 μT for96 h The sham group was identical but without ELF-MFexposure Results showed that ELF-MF caused delayedhatching and decreased heart rate at early developmentalstages but no significant differences were seen in embryomortality or abnormality Acridine orange staining assaysshowed notable signs of apoptosis in the ventral fin andspinal column and transcription of apoptosis-related genes(caspase-3 caspase-9) was significantly up-regulated inELF-MF-exposed embryos They concluded that ELF-EMFdemonstrated detrimental effects on zebrafish embryonicdevelopment including on hatching decreased heart rateand induced apoptosis although such effects were not amortal threat The lower range exposures of this study arefound in some aquatic environments

Sedigh et al [534] investigated effects on zebrafishexposed to static magnetic fields Exposures of 1-week acuteand 3-week subacute exposures to different static magneticfields at 25 5 and 75 mT were measured on stress indices(cortisol and glucose) sex steroid hormones (17β-estradioland 17-α hydroxy progesterone) and fecundity They found asignificant change in cortisol glucose 17β-estradiol (E2) and17-α hydroxy progesterone (17-OHP) levels with increasedintensity and duration of exposure and concluded that staticmagnetic fields at higher intensities showed harmful effectson the reproductive biology of zebrafish during both acuteand subacute exposures

Recent laboratory research by Hunt et al [535] used thetransparent glass catfish (Kryptopterus vitreolus) found inslow moving waters in Southeast Asia as a model toinvestigate magnetoreception The study used Y-mazechambers animal tracking software and artificial intelli-gence techniques to quantify effects of magnetic fields onthe swimming direction of catfish They placed a perma-nent Neodymium Rare Earth Magnet (115 times 318 times 22 cm)with a horizontal magnetic flux of 577 mT at the magnetrsquossurface at 10 cm from the endof one of the Y-maze arms andfound that catfish consistently swam away from magneticfields over 20 μT The catfish also showed adaptability tochanging magnetic field direction and location The mag-netic avoidance was not influenced by school behaviorSham exposures produced no avoidance Such exposuresmight be found near some underwater cables

Levitt et al EMF and wildlife 45

To further elucidate findings of species reactions nearunderwater cables and fill in knowledge gaps since the2011 Tricas and Gill review [36] Hutchinson et al [531]conducted both field and laboratory modeling studies ofboth AC and DC fields on the American lobster (Homarusamericanus) and the little skate (Leucoraja erinacea) Theynoted that in previous studies while behavioral responseshad been seen findings were unable to determine if sig-nificant biological effects (eg population changes)occurred TheAmerican lobsterwasmodeled because it is amagnetosensitive species [536] and concern existed thatEMF from cables might restrict movements andor migra-tion Lobsters may migrate up to 50 mi (80 km) one wayfrom deep waters to shallow breeding grounds The littleskate was used as a model for the most electro-sensitivetaxa of the elasmobranchs which may be attracted bytothe EMF of cables particularly for benthic species therebyaltering their foraging or movement behavior Bothmodelswere therefore thought indicative of potential EMF im-pacts In this robust field study the researchers found thatthe American lobster exhibited a statistically significantbut subtle change in behavioral activity when exposed tothe EMF of theHVDC cable (operated at a constant power of330 MW at 1175 Amps) The little skate exhibited a strongbehavioral response to EMF from a cable powered for624 of the study with the most frequently transmittedelectrical current at 16 Amps (at 0 MW 375 of time) 345Amps (100 MW 286) and 1175 Amps (330 MW 152)They concluded that for both species the behavioralchanges have biological relevance regarding how they willmove around and are distributed in a cable-EMF zone butthey noted that the EMF did not constitute a barrier tomovements across the cable for either species

Of interest in this study were the actual field readingsnear cables Unexpected significant ACmagnetic and electricfields did not match computer models and were observed tobe associated with both of the DC power cables studied Themaximum observed AC values along the cable axis were015 μT and 07 mVm for the magnetic and electric fieldsrespectively for one cable and 004 μT and 04 mVmrespectively for the other cable Also the cross section of theEMF peaks exhibited by the DC subsea power cables werebroader than anticipated at both studied The DC and ACmagnetic fields reached background levels on either side ofthe cable on a scale of ca5 and 10m from the peak observedvalue respectively whereas the AC electric fields reachedbackground on a scale of 100 m (328 ft) from the peak valuePeak observed values occurred almost directly above thecable axis location there was an offset of 33 ft (lt1 m) wherethe cable was twisted The researchers noted that thisobservation of AC fields with broad areas of EMF distortion

being associated with DC cables increased the complexity ofinterpreting the studies of EMFrsquos biological effects from DCcables TheACelectricfieldsassociatedwith theACsea2shorecable (1ndash25 mVm) were higher than the unanticipated ACelectricfieldsproducedby theDCcables (04ndash07mVm) Themagnetic field produced by the AC sea2shore cable (range of005ndash03 μT) was sim10 times lower than modeled valuescommissioned by the grid operator indicating that the three-conductor twisted design achieves significant self-cancellation This entire aspect of the study indicates theneed for accurate field assessment not just computermodeling andwell-designed systems since anomalies occur

Nyqvist et al [498] in a thorough review focused onmarine mammals and the use of underwater electromag-netic surveys that map petroleum deposits in seabeds viastrong induced EMFs in varied directional applicationsThey found that EMFs created during such active surveyingwere within the detectable ranges of marine animals andthe fields can potentially affect behavior in electro-perceptive species but they noted that effects should belimited to within a few kilometers as the electric andmagnetic fields created attenuate rapidly They added thatin migrating marine animals exposures are of shortduration and most are close to naturally occurring levelsbut cautioned that lack of studies is a concern especiallyfor the most sensitive elasmobranchs at highest risk fordisturbance to electric fields They also noted that withinduced magnetic fields animals using magnetic cues formigration or local orientation during certain time-windowsfor migration orientation or breeding could be mostaffected by this surveying technology

Taorimina et al [537] studied both static and time-varying magnetic fields on the behavior of juvenile Euro-pean lobsters (Homarus gammarus) Using two differentbehavioral assays day-light conditions to stimulate shel-tering behavior and exposures to an artificial magneticfield gradient (maximum intensity of 200 μT) they foundthat juvenile lobsters did not exhibit any behavioralchanges compared to non-exposed lobsters in the ambientmagnetic field No differences were noted on the lobstersrsquoability to find shelter or modified their exploratorybehavior after one week of exposure to anthropogenicmagnetic fields (225 plusmn 5 μT) which remained similar tobehavior in controls They concluded that neither static nortime-varying anthropogenic magnetic fields at those in-tensities significantly impacted the behavior of juvenileEuropean lobsters in daylight conditions but they notedthat evidence exists showing magnetosensitivity changesduring different life stages in lobster species and that sincetheir modeling was on juveniles their study was thereforean incomplete picture requiring further study

46 Levitt et al EMF and wildlife

Scott et al [538] focused on ELF-EMF effects oncommercially important ediblebrown crab species (Can-cer pagurus) and what they found was startling In labo-ratory tanks they simulated EMF (with Helmholtz coils28 mT evenly distributed assessments during 24 h pe-riods) that would be emitted from sub-sea power cablesnow commonly used at offshore renewable energy facil-ities They measured stress related parameters ((L-lactateD-glucose haemocyanin and respiration rate) along withbehavioral and response parameters (antennal flickingactivity level attractionavoidance shelter preference andtime spent restingroaming) They found that althoughthere was no EMF effect on haemocyanin concentrationsrespiration rate activity level or antennal flicking ratethere were significant changes in haemolymph L-lactateand D-glucose natural circadian rhythms indicating al-terations in hormones Crabs also showed an unusuallyhigh attraction to EMF-exposed shelter areas (69)compared to control shelter areas (9) and significantlyreduced their time roaming by 21 with adverse impli-cations for food foraging mating and overall health Theynoted that EMF clearly altered behavior Crabs spent lesstime roaming around the tank andmore time in a shelter indirect contact with the EMF source indicating naturalroamingfood-or-mate-seeking behavior had been over-ridden by attraction to EMF In fact crabs consistentlychose an EMF-exposed shelter over a non-exposed one andwere always drawn to the EMF The results appear topredict that in benthic areas surrounding EMF-emittingcables there will be an increase in the abundance ofCancer pagurus present They noted that such potentialcrab aggregation around benthic cables and the subse-quent physiological changes in L-lactate and D-glucoselevels caused by EMF exposure is a concern regardingfeeding rates mating and especially egg incubationdirectly in increased EMF environments They concludedthat long term investigations are needed regarding chronicEMF exposure especially on egg development hatchingsuccess and larval fitness and added that EMF emitted inmarine environments from renewable energy devicesmustbe considered as part of the study of cumulative impactsduring the planning stages

Clearly ELF-EMF can affect myriad aquatic species atintensity levels found in proximity to underwater cables atenvironmental intensities

Fish RF-EMF

As mentioned RFR is of minimal environmental concernfor fish since aquatic environments while highly

conductive mediums also highly attenuate EMF at higherfrequencies This may change in the near future as newtechnologies now exist thatmay surpass these obstacles [98]thereby introducing for the first time novel new RFR expo-sures underwater Longer wave wireless ELF with expandedranges are used in anthropogenic sonar (sound navigationranging) primarily for military applications These traveleasily through water and are known to adversely affect ce-taceans and other species that rely on their natural sonar forcommunication migration reproduction and food findingBut soundwaves are not considered ldquoEMFrdquo in the strict senseof the term since the focus of this paper is EMF soundwavesare tangential here But acoustic damage especially to ceta-ceans from military and commercial applications is welldocumented and ELF cables used for underwater militarysubmarine communications can have significant EMF expo-sures near cables Just because this paper does not addressimpacts from sound waves in detail does not mean they arewithout serious effects

There are however three recent studies of RFR onzebrafish included here because it is plausible that suchexposures could exist near shallow aquatic environmentsunder some circumstances Nirwane et al [539] studied900-MHz GSM RFR effects on zebrafish (D rerio) neuro-behavioral changes and brain oxidative stress as a modelfor human exposures to cell phones Exposures wereapplied daily for 1 h 14 days with SAR 134 WKg Theyfound 900-MHz GSM radiation significantly decreased so-cialization and increased anxiety as demonstrated by sig-nificant increased time spent in bottom areas freezingbehaviors and duration and decreased distance travelledas well as decreased average velocity and number of en-tries to the upper half of the tank Exposed zebrafish spentless time in the novel armof a Y-Maze indicating significantimpaired learning compared to the control group Expo-sure also decreased superoxide dismutase (SOD) andcatalase (CAT) activities while increased levels of reducedglutathione (GSH) and lipid peroxidation (LPO) wereencountered indicating compromised antioxidant defensePost-exposure treatment with melatonin in the waterhowever significantly reversed the induced neuro-behavioral and oxidative changes

Piccinettia et al [540] investigated in vivo effects onembryonic development in zebrafish at 100 MHz thermaland nonthermal intensities via a multidisciplinary proto-col Results found 100 MHz RFR affected embryonicdevelopment from 24 to 72 h post fertilization in all theanalyzed pathways Most notably at 48 h post fertilizationreduced growth increased transcription of oxidative stressgenes onset of apoptoticautophagic processes and amodification in cholesterol metabolism were seen EMF

Levitt et al EMF and wildlife 47

affected stress by triggering detoxification mechanisms At72 h post fertilization fish partially recovered and reachedhatching time comparable to controls The researchersconcluded that EMF-RFR unequivocally showed in vivoeffects at non-thermal levels

Dasgupta et al [541] used embryonic zebrafish modelsat 35 GHz SAR asymp 827 Wkg and exposed developingzebrafish from 6 to 48 h post fertilization then measuredmorphological and behavioral endpoints at 120 h postfertilization Results found no significant impacts on mor-tality morphology or photomotor response but noted amodest inhibition of startle response suggesting somelevels of sensorimotor disruptions They concluded thatexposures at low GHz levels are likely benign but never-theless entailed subtle sensorimotor effects Such effectscan affect fish survival in variousways including inhibitedresponse time to predators among others This study wasdone with an eye toward potential human bioeffects atfrequencies used in 4 and 5G technology It was also con-ducted at intensities higher than the focus of this paper

If new technology overcomes the conductivityatten-uation limitations of aquatic environments and introducesmore RFR to aquatic species studies like those cited abovemay soon have more environmental relevance even athigher intensities than explored here

Turtles

Oceanic sea turtle migration joins that of other renownedlong-distance migratory species like salmon and over-landmonarch butterfly treks spanning thousands of kilometersand traversingmultiple complex environments throughouttheir life cycles Sea turtles have long been known to usegeomagnetic fields for orientation [542 543] Freshwaterspecies (eg Chelydra serpentina) have also been shown tohave a magnetic sense capable of artificial disruption [92]as do terrestrial box turtles (Terrapene carolina [544])

Sea turtles demonstrate natal homing behavior mdash theability to return over great distances to their exact birthlocation to reproduce [89] and because of anthropogenicdisruptions of nesting grounds along beaches this repro-ductive homing drive imperils them today The underlyingmechanism is still imperfectly understood but involveslsquoimprintingrsquo of the intensity and inclination angle of thegeomagnetic field at the birth location [545] The informa-tion is then later used in maturity to return to their place oforigin

Sea turtles are by far the most studiedmodels for turtlemagnetoreception especially by the Lohmann Laboratoryat the University of North Carolina US [323 546ndash558]

Irwin and Lohmann [559] discussed the advantagesand disadvantages of various research approaches used toinvestigate magnetic orientation behavior in turtles Theseinclude the use of largemagnetic coil systems in laboratorysettings to generate relatively uniform fields over largeareas [560] which allow the magnetic field to be artificiallyaltered and carefully controlled to determine changes inbehavioral orientation This approach however is un-suited for manipulating exposures around animals innatural environments or for studying localized body mag-netoreceptors which in turtles are still a mystery Anotherapproach is to attach a small magnet or electromagneticcoil to an animal to disrupt magnetic orientationbehavior mdash a far easier approach in hatchlings than injuvenile ormature free-swimming species They note that ifthe imposed field from an attachedmagnet or coil is strongenough to interfere with the Earthrsquos field behavioralorientation changes [116 544 561] and the performance ofa conditioned response [367 562] can be observed Thislatter approach has been used in field studies for the pur-pose of blocking access to normal magnetic information[544 561 563ndash565] and to localize magnetoreceptors bydisrupting the field around a specific terrapin body part[562] This techniquersquos disadvantage however is thatfields rapidly change with distance from the source mak-ing it difficult to quantify the fields that the animal actuallyexperiences

Most sea turtle studies have involved large magneticcoil systems but Irwin and Lohmann [559] attached smallmagnets greater in strength than the Earthrsquos fields to twogroups of loggerhead sea turtle hatchlings (Caretta carettaL) under laboratory conditions in which turtles are knownto orient magnetically [473 546 548ndash550] They found thatmagnetic orientation behavior in hatchling turtles can bedisrupted via small magnets attached to the carapacewhich then create exposures over the entire body Theyconcluded that such an approach can be used to finallydetermine local magnetoreceptors by varying the locationof themagnet and using smaller weakermagnets that alterthe field only around specific anatomical target sites

In loggerhead sea turtles there is evidence of aninclination compass [473 550] that is functionlly similar tothe bird magnetic compass reported in European Robins[566 567] Lohmann and Lohmann [550] investigated aninclination compass in sea turtles and found it was apossible mechanism for determining latitude Also inves-tigated were detection of magnetic intensity [551] naturalregional magnetic fields used as navigational markers forsea turtles [557] and sea turtle hatchlingsrsquo mapping abili-ties [545] Sea turtles are also known to have magnetite intheir heads [104 568] Studies with young sea turtles have

48 Levitt et al EMF and wildlife

shown that a significant portion of their navigationalabilities involve magnetoreception following hatching[569] mdash imprinting with the Earthrsquos magnetic field beingone of several cues hatchlings use as they first migrateoffshore [546 554] The magnetic fields that are unique todifferent areas at sea eventually serve as navigationalmarkers to guide swimming direction to important migra-tory routes As juveniles mature they form topographicalmagnetic maps where they live that direct them to specificregions But it has remained largely unknown if matureturtles specifically nesting females use such mechanismsin open-sea homing as this magneto-sense may changeover time

Field studies are notoriously difficult with large spe-cies at sea but Papi et al [564] studied mature green turtles(Chelonia mydas) during their post-nesting migration over1243 mi (2000 km) from their nesting grounds on Ascen-sion Island in themiddle of the Atlantic Ocean back to theirBrazilian feeding grounds They were investigatingwhether mature female turtles use an inclination compassand geomagnetic fields for direction or by inference (oncethat sense is disturbed) by some other means as yetdetermined Papi et al [564] attached very strong DCmagnets mdash significantly stronger than the Earthrsquos fields mdashto disturb and overcome natural magnetoreception andthereby determine if they could still navigate back to As-cension Island Controls had nonmagnetic brass barsattached and some had transmitters glued to their headsAll had tracking devices that communicatedwith satellitesthus creating strongmulti-frequency static and pulsed RFRexposures Seven turtles were each fitted with six powerfulstatic magnets that produced variable artificial fields sur-rounding the whole turtle making reliance on a geomag-netic map impossible The studyrsquos travel courses were verysimilar to those of eight turtles without magnets that hadbeen tracked via satellite over the same period in the pre-vious year No differences between the magneticallyexposed test turtles and untreated turtles were foundregarding navigational performance and general coursedirection They concluded that magnetic cues were notessential to turtles on the return trip and speculated thatperhaps other factors such as smell or wave current di-rection may come into play

Luschi et al [563] like Papi et al [564] also investi-gated the role of magnetoreception and homing in maturesea turtles but used a different design and found verydifferent results In a large field study in the MozambiqueChannel 20 mature pre-nesting green turtles were alsoequipped with both strong magnets and satellite trackingdevices The turtles were gathered at their nesting beach onMayotte Island before egg-laying and transported to four

open-sea sites 62ndash75 mi (100ndash120 km respectively) awayThere were five releases of four turtles each with threedifferent treatments turtles magnetically lsquodisturbedrsquo onlyduring transportation with magnets removed beforerelease those treated only during the homing trip withmagnets attached just prior to release and controls withnonmagnetic brass discs attached to their heads Treatedturtles had very strongmoveable magnets attached to theirheads to induce varying magnetic fields around themeither at the nesting beach at the start of the relocationjourney or on the boat just prior to release for the homingtrip All groups had satellite transmitters attached to theircarapaces thereby creating in the opinion of the authors ofthis paper an additional exposure that was not consideredas a variable The researchers also included ocean currentsin their assessments estimated by using oceanographicremote sensing measurements All but one turtle eventu-ally returned to Mayotte to complete delayed egg-layingBut treated turtles whether treated during transportationor homing took significantly longer to reach the destina-tion vs controls mdash a surprising finding Most homingroutes showed very long circuitous curved and loopingpatterns before reaching their target Control paths weredirect Both treated turtle groups were clearly impaired bythe MF exposure indicating significant recovery timeneeded between exposure and correcting positionalbehavior The researchers hypothesized the existence of anavigational role for geomagnetic information beinggathered by those turtles in the passive transportationgroup as well as the possibility that magnetic disturbanceduring transportation may have persisted for some timeafter the removal of the magnets in that group thusrendering the two treated groups functionally equivalentduring their homing journeys They also noted that expo-suresmay have physically alteredmagnetite particles thuscreating a longer lasting effect but they said that since long-lasting after-effects of magnet application have not beendescribed this theory could neither be inferred nordismissed

Lohmann [323] reviewed both of the above studies andadded that in addition to the two causal hypotheses ofLuschi et al [563] regarding their unexpected findings ofturtle circuitous migration routes another explanationwould include the positioning of the satellite transmittersin the Papi et al [564] study on turtle heads vs on thecarapace of the Luschi models He added that since satel-lite transmitters also produce magnetic fields capable ofdisrupting magnetoreception and since the Papi groupalso attached satellite transmitters on the heads of severalcontrol turtles that re-analyzing the Papi study using onlyturtles with satellite transmitters placed on the carapace

Levitt et al EMF and wildlife 49

like the Luschi study could show evidence consistent withthe hypothesis that adult turtles exploit magnetic cues innavigation He concluded that sea turtles like all otheranimals studied to date likely exploit multiple cues fornavigation since even with artificial magnetic disturbancecausing impaired performance themagnets in either studydid not prevent turtles from eventually reaching theirtarget beaches This implies that turtles can also rely onother sources of information [570 571] such as celestialcompasses wave direction [572] or olfactory cues likeother species mdash a significant finding

The sum total of the studies mentioned above is thatsea turtle species are highly sensitive to Earthrsquos fields andare capable of adapting to subtle anthropogenicdisruption

Turtles RF-EMF

Turtles may also be senstitive to RFR especially duringincubation while on land andor initial hatchling stages ifthey are exposed to anthopogenic RF-EMF that coulddistort the imprintingmemory they use in later life to locatetheir birthsite beaches again For example if a radar orcommunications base station is installed on or near thebeach of a nesting site could that affect the initialldquoimprintingrdquo process Perhaps augment imprinting andmake return easier Or conversely overwhelm the subtleimprinting process at the start and make return impos-sible If the latter is valid such technology could lead toextinction of sensitive species since it interrupts thereproduction process In the very least in sensitive speciesdisorientation might result as discussed above

To characterize the underlying compass mechanismsin turtles Landler et al [92] studied freshwater juvenilesnapping turtlesrsquo (Chelydra serpentine) ability for sponta-neous magnetic alignment to the Earthrsquos geomagneticfields Using exposure to low-level RFR near the Larmorfrequency (12 MHz) that is related to free radical pair for-mation turtles were first introduced to the testing envi-ronment without the presence of RFR (ldquoRF off RF offrdquo) andthey were found to consistently align toward magneticnorth But when subsequent magnetic testing conditionswere initially free of RFR then included an introducedsignal (ldquoRF off RF onrdquo) they became disoriented Thusintroduction of a RFR field could affect the turtlesrsquo align-ment response to the natural magnetic field The RFR fieldusedwas only 30ndash52 nT (143MHz) In the following reversescenario when the turtles were initially introduced to thetesting environment with RFR present but then removed(ldquoRF on RF offrdquo) they became disoriented when tested

without RFR And with RFR on in both cases (ldquoRF on RFonrdquo) they aligned in the opposite direction toward mag-netic south Clearly test turtles were affected by the expo-sures The researchers concluded that the sensitivity of thespontaneous magnetic alignment response of the turtles toRFR was consistent with a radical pair mechanism (seeldquoMechanismsrdquo above) In addition they concluded that theeffect of RFR appeared to result from a change in thepattern of magnetic input rather than elimination ofmagnetic input altogether Their findings indicated thatturtles when first exposed to a novel environment form alasting association between the pattern of magnetic inputand their surroundings and that they may form a largerinternal GPS-like mapping ability when theymeet any newmagnetic reference framework based on natural magneticcues from multiple sites and localities

They also showed that RFR at or near the Larmor fre-quency (12ndash143 MHz) had the ability to disrupt snappingturtle natural orientation establish its own novel orienta-tion and completely reverse a natural orientation leadingback to the complex questions asked above regardingimprinting and possible reproductive disruption Althoughthe Landler et al study [92] was conducted in a freshwaternon-homing species snapping turtles are long-lived with alow reproduction success rate Even small disruptions tothis species from anthropogenic sources could have anoutsized population effect over time If this freshwaterspecies is any indication of potential RFR effects re-searchers need to further investigate RFR in long-distancemigrating turtle species that imprint on landWe simply donot know the full range of possible effects across fre-quencies with which turtle species come in contact atvulnerable points throughout development and lifetimes

Nematodes and smaller biota

There are reports of sensitivity to EMF in lesser taxa aswellEMF is known to affect numerous other species includingnematodes (Earth and aquatic worms) mollusks (snails)amoeba (single-celled organisms) molds algae pro-tozoans yeast fungi bacteria and viruses (to a limitedextent) mdash with ramifications for creation of antibioticresistant bacteria strains Below are some representativeexamples of observed effects

Nematodes

Common soil-based nematode species like C elegans serveas a useful whole-organism model for genetic and

50 Levitt et al EMF and wildlife

multicellular organism investigations They are routinelyused as a research model to investigate key biologicalprocesses including aging neural system functioning andmuscle degeneration to name a few This speciesrsquo geneticand phenotypic traits are extremely well documented andthey can thus be used as important proxies for quantitativeanalyses [573] Nematodes have a short lifespan are her-maphrodites and demonstrate effects quickly As labmodels they are used primarily for information that can beapplied to humans but we can also glean important in-formation and extrapolate to environmental exposuresunder certain circumstances Healthy soil worm pop-ulations are critical to soil health upon which we alldepend

Hung et al [574] investigated static magnetic field(SMF) effects on life span and premature aging inC elegans Nematodes were grown in SMFs varying from0 to 200 mT They found that SMFrsquos accelerated develop-ment and reduced lifespan in wild-type nematodes Theyalso found increases in heat shock proteins that were se-lective and dose dependent

Vidal-Gadea et al [66] investigated magnetic orienta-tion in C elegans to identify magnetosensory neurons andfound that they orient to the Earthrsquos geomagnetic fieldduring vertical burrowing migrations Well-fed wormsmigrated up while starved worms migrated down Pop-ulations isolated from around the world were found tomigrate at angles to the magnetic vector that would verti-cally translate to their native soil with northern- andsouthern-hemisphere worms displaying opposite migra-tory preferences in conjunction with natural geomagneticfields They also found that magnetic orientation and ver-ticalmigrations required the TAX-4 cyclic nucleotide-gatedion channel in the AFD sensory neuron pair while calciumimaging showed that these neurons respond to magneticfields even without synaptic input They hypothesized thatC elegans may have adapted magnetic orientation tosimplify their vertical burrowingmigration by reducing theorientation task from three dimensions to one

C elegans have also demonstrated sensitivity to elec-tric fields via electrotaxis (also known as galvanotaxis)which is the directed motion of living cells or organismsguided by an electric field or current and often seen inwound healing Sukul and Croll [575] found that nema-todes exposed to an electrical current (002ndash004 mA po-tential differences 2ndash6 V) demonstrated a directionalsensorily-mediated orientation toward the current at firstbut at 2mm from the electrode individualworms increasedreversing behaviors which then remained uniform as theymoved in a constant direction parallel to the exposure Afew which did not reverse direction died (presumably from

electrocution) at 6 V or 04 mA They concluded that adultC elegans move directionally at selected combinations ofvoltage and potential differences and that electrophoresiscould be eliminated

Gabel et al [576] also investigated electric field effectson directionality on C elegans with an eye toward betterunderstanding how the nervous system transforms sensoryinputs into motor outputs They used time-varying electricfields modulated at 100 Hz across an agar surface with adefined direction and amplitude up to 25 Vcm They foundthat the nematodes deliberately crawl toward the negativepole in an electric field at specific angles to the direction ofthe electric field in persistent forward movements with thepreferred angle proportional to field strength They alsofound that the nematodes orient in response to time-varying electric fields by using sudden turns and reversals(normal reorientation maneuvers) They also found thatcertain mutations or laser ablation that disrupt the struc-ture and function of amphid sensory neurons also dis-rupted their electrosensory behavior and that specificneurons are sensitive to the direction and strength ofelectric fields via intracellular calcium dynamics amongthe amphid sensory neurons This study showed thatelectrosensory behavior is crucial to how the C elegansnervous system navigates and can be disrupted at someintensities found in the environment

Maniere et al [573] also found Celegans was sensitiveto electric fields and that when submitted to a moderateelectric field worms move steadily along straight trajec-tories They hypothesized that imposing electric fields inresearch settings was an inexpensive method to measurewormsrsquo crawling velocities and a method to get them toself-sort quickly by taking advantage of their electrotacticskills

An early RFR study of C elegans by Daniells et al [577]found this species to be a useful model for investigatingstress-responses In the majority of investigations theyused 750 MHz with a nominal power of 27 dBm controlswere shielded and all temperatures were strictlycontrolled Stress responses were measured in terms ofbeta-galactosidase (reporter) induction above controllevels Response to continuous microwave radiationshowed significant differences from 25 degrees C in con-trols at 2 and 16 h but not at 4 or 8 h Using a 5 times 5multiwellplate array exposed for 2 h the 25 microwaved samplesshowed highly significant responses compared with asimilar control array Experiments in which the frequencyandor power settings were varied suggested a greaterresponse at 21 than at 27 dBm both at 750 and 300 MHzindicating a nonlinear effect although extremely variableresponses were observed at 24 dBm and 750 MHz Lower

Levitt et al EMF and wildlife 51

power levels tended to induce greater responses mdash theopposite of simple heating effects They concluded thatmicrowave radiation causes measurable stress to trans-genic nematodes via increased levels of protein damagewithin cells at nonthermal levels

Tkalec et al [578] found oxidative and genotoxic ef-fects in earthworms (Eisenia fetida) exposed in vivo to RFRat 900 MHz at 10 23 41 and 120 V m(-1) for 2 h using aGigahertz Transversal Electromagnetic (GTEM) cell Allexposures induced significant effects with modulationincreasing such effects Their results also indicated anti-oxidant stress response induction with enhanced catalaseand glutathione reductase activity indicating lipid andprotein oxidative damage Antioxidant responses anddamage to lipids proteins and DNA differed depending onEMF level modulation and exposure duration

Aquatic and semi-aquatic worm species also showsensitivity to EMF Jakubowska et al [579] investigatedbehavioral and bioenergetic effects of EMF at 50 Hz 1 mTfields (comparable to exposures near underwater cables) inpolychaete ragworms (Hediste diversicolor) that live andburrow in the sandmudof beaches andestuaries in intertidalareas of the North Atlantic While they found no attraction oravoidancebehavior toEMFburrowingactivitywasenhancedwith EMF exposure indicating a stimulatory effect Foodconsumption and respiration rates were unaffected butammonia excretion rate was significantly reduced inEMF-exposed animals compared to control conditions at onlygeomagnetic fields The mechanisms remained unclear Theauthors said this was the first study to demonstrate effects ofenvironmentally realistic EMF values on the behavior andphysiology of marine invertebrates

Van Huizen et al [67] investigated effects of weakmagnetic fields (WMF) on stem-cells and regeneration inan in vivomodel using free-swimming flatworms (Planariassp) that are capable of regenerating all tissues includingthe central nervous system and brain This regenerationability is due to the fact that about 25 of all their cells areadult stem cells (ASC) Injury is followed by a systemicproliferative ASC response that initially peaks at sim 4 hfollowed by ASC migration to the wound site over the first72 h when a second mitotic peak occurs Like salamanderregeneration (see ldquoAmphibiansrdquo above) this activity pro-duces a blastema mdash a group of ASC cell growth that formsthe core of new tissues Full regeneration of damagedplanaria tissues or organs occurs through new tissuegrowth and apototic remodelingscaling of old tissueswithin 2ndash3 weeks Following amputation above and belowthe pharynx (feeding tube) they exposed amputation sitesto 200 μTWMF At three days post-amputation they foundthat 200 μT exposure produced significantly reduced

blastema sizes compared to both untreated and earth-normal 45 μT field strength controls indicating a WMFinterference effect to regeneration They also found that the200 μT exposure was required early and had to be main-tained throughout blastema formation to affect growthand that shorter single-day exposures failed to affect blas-tema size In addition they found weak magnetic fieldsproduced field strengthndashdependent effects These includedsignificant reductions of blastema size observed from 100ndash400 μT but conversely a significant increase in outgrowthoccurred at 500 μT They hypothesized thatWMFeffects werecausedbyaltered reactive oxygen species (ROS) levelswhichpeak at the wound site around 1-h post-amputation and arerequired for planarian blastema formation This study showsthat weak anthropogenic magnetic fields can affect stem cellproliferation and subsequent differentiation in a regenerativespecies and that field strength can increase or decrease newtissue formation in vivo This is a significant finding forregenerating species of all kinds and may affect non-regenerating species as well Sea lamprey eels (Petromyzonmarinus) a fish species are also known to regenerate evenafter multiple amputations [580]

Mollusks amoeba molds algaeprotozoans

Mollusks (marine versions are called chitons) are longknownto manufacture magnetite in their teeth and to use fieldsweaker than the geomagnetic field for kinetic movement anddirection [52 117 340 524] Lowenstam [118] first discoveredthat magnetite was the major mineral in the teeth of marinechitons thought to give teeth their natural hardness ButRatner [62] discovered chitons use magnetite as a magneticcompass when he found a number of chiton species haveradulae (tongues) that are covered by ferro-magnetic(magnetite) denticles The radulae of Acompapleura gran-ulata and Chiton squamosis were also found to be ferro-magnetic but the shells were not Live specimens of a chiton(Chaetopleura apiculata) that also have ferro-magneticradulae were found to rotate more and move farther in amagnetic field weaker than in the Earthrsquos stronger geomag-netic field indicating a nonlinear directionality Ratnerconcluded that chitons are responsive to magnetic fields anddemonstrate kinetic movements within them

Some snails are sensitive to EMFs Nittby et al [581]observed analygesic effects in land snails (Helix pomatia)caused by GSM-1900 RFRs when snails lost sensitivity topain on a hot plate test after nonthernal exposure to RFR

Smaller organisms have also long shown effects fromEMF Goodman et al [582] found delays in mitotic cell

52 Levitt et al EMF and wildlife

division in slime mold (Physarum polycephalum) withELF-EMF exposures Friend et al [583] found perpendic-ular and parallel elongation of the giant amoeba Chaoschaos (Chaos carolinensis) in alternating electric fields overa wide frequency range (1 Hzndash10 MHz) with characteristicchanges as a function of frequency Marron et al [584]found effects on ATP and oxygen levels in another speciesof slime mold (P polycephalum) after exposures to 60 Hzsinusoidal electric and magnetic fields Luchien et al [585]found a stimulating effect on the productivity of the algalbiomass (Chlorella sorokiniana) for a magnetic field of50 Hz but an inhibitory effect at 15 Hz in these microalgae

Protozoans thought to bemore related to animals thanmicrobes also show sensitivity to EMF Protozoans assingle-celled eukaryotes are generally larger than bacteriawhich are classified as prokaryotes The two organisms arestructurally different bacterial cells lack a nucleus whileprotozoa contain organelles such as mitochondria Bacte-ria generally absorb nutrients through their cell wallswhileprotozoa feed on bacteria tissue and organic matter andcan be both infectious and parasitic These protozoainclude human parasites that cause diseases such asamoebic dysentery malaria giardiasis leishmaniasistrichomoniaisis toxoplasmosis and others Animal speciesare also affected by protozoans which can severely weakenand shorten their lifespans

Rodriguez-de la Fuente et al [586] tested ELF-EMF(60 Hz 20 mT for 72 h) on two infectious protozoans Tri-chomonas vaginalis andGiardia lamblia and found growthalterations in both species which they attributed to alter-ations in cell cycle progression and cellular stress Cam-maerts et al [587] used RFR (GSM 900-MHz at 2 W vscontrol) on protozoans (Paramecium caudatum) and foundindividuals moved more slowly and sinuously than usualand that their physiology was affected Paramecia becamebroader pulse vesicles had difficulty expelling content tothe outside of their cells cilia moved less efficiently andtrichocysts became more visible mdash all effects that indicatepoor functioning or cell membrane damage They hy-pothesized that the first impact of RFR could be to cellmembranes

Clearly there are multiple effects at all levels docu-mented in lower taxa from multi-frequency exposures thatare now found in the environment

Yeast and fungi

Yeast is often used in lab models especially since 1996when a complete genomic sequence of Saccharomycescerevisiae was created In fact it is now considered a

ldquopremiermodelrdquo [588] for eukaryotic cell biology as well ashaving helped establishwhole newfields of inquiry such asldquofunctional genomicsrdquo and ldquosystems biologyrdquowhich focuson the interactions of individual genes and proteins toreveal specific properties of living cells and wholeorganisms

EMF research is rich with studies using yeast modelstoo numerous to fully analyze here However we include asmall sample of recent EMF research with potential sig-nificance to environmental exposures

Lin et al [589] investigated glucose uptake and tran-scriptional gene response to ELF-EMF (50 Hz) and RFR(20 GHz) on several strains of budding yeast (S cerevisiae)Results determined that ELF-EMF and RFR exposure canupregulate the expression of genes involved in glucosetransportation and the tricarboxylic acid (TCA) cycle butnot glycolysis pathways thus showing that such exposurescan affect energy metabolism which is closely related withcellular response to environmental stress Glucose meta-bolism is fundamental to all living cellsrsquo need for energywith related significance to many disease states includingmost cancers

In amagnetic field study byMercado-Saenz et al [590]premature aging and cellular instability were found inyeast (S cerevisiae) exposed to low frequency low in-tensity sinusoidal magnetic fields (SMF continuous expo-sure at 245 mT 50 Hz) and pulsed magnetic fields (PMF15 mT 25 Hz 8 hday) Chronological aging was evaluatedduring 40 days and cellular stability was evaluated by aspontaneous mutation count and the index of respiratorycompetence (IRC) They found exposure to PMF producedaccelerated aging while SMF did not and decreasedmitochondrial mutation during aging was also seen withPMF No alterations in respiratory competence wereobserved for either SMF or PMF exposures They concludedthat exposure to PMF accelerated chronological aging andaltered the spontaneous frequency of mitochondrial mu-tation during the aging process whereas the SMF used hadno effect thus showing abnormal effects on cell activityfrom pulsed exposures

Because yeast cells are known to be sensitive to mag-netic fields some industrial and therapeutic applicationsto human health have been investigated These in-vestigations serve to illuminate what we know about yeastand fungal reactions to EMF in general as well as specificuses For industrial applications Wang et al [591] inves-tigated low level static magnetic fields (SMF) on mold(Aspergillus versicolor) growth which can have high im-pacts on metal corrosion in environmental conditionsconducive to mold growth This is especially problematicin fine electronic circuit boards produced today Using a

Levitt et al EMF and wildlife 53

10 mT static magnetic field (SMF) perpendicular to thesurface of printed circuit boards they found the magneticfield inhibited mold growth and surface corrosion whichwere slowed down unlike control boards without appliedmagnetic fields where mold formed a spore-centeredcorrosion pit that then led to macroscopic regional uni-form corrosion This demonstrated changes in cellsporegrowth at a low intensity exposure that can be found in theenvironment

Also with an eye toward commercial possibilities Sunet al [592] found that a polysaccharide of Irpex lacteus (awhite-rot fungus found widely in the environment whichbreaks down organic materials but also is commerciallyused to treat nephritis in humans) was sensitive to low-intensity ELF-EMF as demonstrated by increased biomassand polysaccharide content as well as inducedmalformedtwists on the sample cell surfaces Polysaccharides arecarbohydrates with a large number of sugar moleculesused as energy sources in living cells They identifiedvarying changes in multiple differentially expressed genesafter exposure to alternating current EMF (50 Hz 35 mT3 h per day for 4 days) They found initial sharp increasesin growth rates in exposed samples that were then markedby significant declines in EMFrsquos influence over timealthough there were also important lasting effects Globalgene expression alterations fromEMF indicated pleiotropiceffects (capable of affecting multiple proteins or catalyzingmultiple reactions) were related to transcription cell pro-liferation cell wall and membrane components aminoacid biosynthesis and metabolism Polysaccharidebiosynthesis and metabolism were also significantlyenriched in the EMF-exposed samples They concludedthat EMF significantly increased amino acid contents andwas therefore deemed a suitable method for increasingfermentation of microorganisms presumably for com-mercial use However the significance of this study toenvironmental exposures relates to the multiple ways thatELF alternating current common to electric power gener-ation changed yeast gene expression There is at least oneclinical case of a different strain of I lacteus taking on a rareinfectious and dangerous quality in an immuno-compromised human [593] The question is can now-ubiquitous ELF-EMF contribute to potentially emergingnew forms of yeast contagion

The same question arises with Candida albicans andother pathogenic yeasts that have rapidly developedresistance to antifungal medications C albicans can liveharmlessly in human microflora but certain lifestyle cir-cumstances or immunosuppression can turn it into anopportunistic pathogen It can also infect somenon-humananimals While chronic mucocutaneous candidiasis can

infect the skin nails and oral and genital mucosae underhigh host immunodeficiency C albicans can enter thebloodstream and induce systemic infections withmortalitybetween 30 and 80 [594] There has been increasingresistance of C albicans to traditional antifungal agentssuch as fluconazole and amphotericin B [595 596] Resis-tance mechanisms include overproduction of membranedrug efflux transporters andor changes in gene expression[597]

Two investigations in search of new therapeutic stra-tegies were conducted using EMF Sztafrowski et al [594]investigated the use of staticmagneticfields (SMF 05 T) onC albicans cultures in the presence of two commonly usedantifungal medications Their aim was to assess whetherSMF had any impact on general viability of C albicanshyphal transition and its susceptibility to fluconazole andamphotericin B They found reduction of C albicans hy-phal length in EMF-exposed samples They also found astatistically significant effect on C albicans viability whenSMF was combined with amphotericin B They hypothe-sized that this synergistic effect may be due to the plasmamembrane binding effects of amphotericin B and that SMFcould influence domain orientation in the plasma mem-brane They concluded with caution that the use of a SMFin antifungal therapy could be a new supporting option fortreating candidas infections

Novickij et al [598] also focused on therapeutic pos-sibilities given the multi-drug resistance and side effects toantifungal therapies Their aim was to optimize theelectroporation-mediated induction of apoptosis usingpulses of varied duration (separately and in combinationwith formic acid treatment) and to identify yeast apoptoticphenotypes They focused on nonthermal nanosecondpulsed electric fields (PEF 3 kV 100 ns ndash 1 ms squarewaveand 250 500 750 ns duration 30 kVcm PEF 50 pulses1 kHz) as a therapeutic alternative andor to enhance ef-fects in combinationwith conventional treatments In threeyeast models S cerevisiae (as control) and drug resistantCandida lusitaniae and Candida guilliermondii they foundthat nanosecondPEF induced apoptosis in all three strainsCombining PEF with a weak formic acid solution improvedinduced apotosis and inactivation efficacy in the majorityof the yeast population Yeast cells showed DNA breaksand other changes They concluded that PEF could be auseful newnon-toxic protocol to treat some fungal diseasesand minimize tissue damage

Choe et al [599] studied ion transportation and stressresponse on a yeast strain (K667) to ELF-EMF (60 Hz01 mT sinusoidal or square waves) specifically investi-gating internal ionic homeostasis via the cell membraneinvolving metal ions and cation transports (cations are

54 Levitt et al EMF and wildlife

ionic species of both atoms and molecules with a positivecharge) They found significantly enhanced intracellularcation concentrations as ELF-EMF exposure timeincreased as well as other changes This study has impli-cations for soil health as yeast can be an integral aspect ofhow healthy organic soil matter is formed They concludedthat EMF and yeast could also play a role in the bioreme-diation processes in metal-polluted environments

Lian et al [600] studied effects of ELF-EMF (50 Hz 0ndash70 mT) and RFR (20 GHz 20 Vm temperature at 30 degCaverage SAR single cell012 Wkg) on two budding yeaststrains (NT64C and SB34) and prion generationpropaga-tion They found under both EMF exposures that de novogeneration and propagation of yeast prions (URE3) wereelevated in both yeast strains The prion elevationincreased over time and effects were dose-dependent Thetranscription and expression levels of heat shock proteinsand chaperoneswere not statistically significantly elevatedafter exposure but levels of reactive oxygen species (ROS)as well as superoxide dismutase (SOD) and catalase (CAT)activities were significantly elevated after short-term butnot long-term exposure This work demonstrated for thefirst time that EMF exposure could elevate the de novogeneration and propagation of yeast prions supporting theresearcherrsquos hypothesis that ROS may play a role in theeffects of EMF on protein misfolding ROS levels alsomediate other broad effects of EMF on cell function Theyconcluded that effects of EMF exposure on ROS levels andprotein folding may initiate a cascade of effects negativelyimpacting many biological processes

The effects of EMF on protein folding cannot be over-stated Proteins must fold into proper three-dimensionalconformations to carry out their specific functionsmdash intactproteins are critical to the existence of all life Misfoldingnot only impairs function but leads to disease Foldinginside of cells does not happen spontaneously but ratherdepends on molecular helpers called chaperones Proteinmisfolding has been implicated in Alzheimerrsquos Parkin-sonrsquos and Huntingtonrsquos diseases among others Thedevastating CreutzfeldtndashJakob disease is caused by prionmisfolding in the brain which causes abnormal signalingin neurons that eventually leads to paralysis and deathWildlife can also suffer from prion diseases such as chronicwasting in deer elk and other cervids and cattle can sufferfrom so-called ldquomad-cowrdquo disease The two studies fromabove [599 600] have implications for how such diseasesare spread through soil with possible links to environ-mental EMFs

It is clear from the above that ELF-EMF and RF-EMFusing multiple signaling characteristics are biologicallyactive in both temporary and permanent ways in yeast

fungi species with wide environmental implications acrossnumerous taxa

Bacteria

Strains of bacteria are known to be magnetotactic and usegeomagnetic fields for direction Blakemore [63] was thefirst to suggest in 1973 that bacteria in North Americansaltwater marsh muds use magnetite as a sensor when hediscovered not only that bacteria were highly attracted toan external magnet but they also had magnetite crystalsthat caused them to align with the lines of the Earthrsquosmagnetic fields This was also discovered to be geo-location specific to the North Pole in northern samples andSouth Pole-seeking in southern species [52 63 511] Thebacteria showed ldquomud-uprdquo and ldquomud-downrdquo behavioralong magnetic field gradients when mud was disturbedindicating a magnetic compass Since that early work awhole new field called electromicrobiology has developedwith discoveries that include some electro-active bacteriabeing responsible for magnetite formation with otherscreating their own electric ldquowiresrdquo in mud flats with im-plications for new technologies [601]

Among the more troubling EMF effects are bacterial al-terations with pressing implications for antibiotic resistanceSince the 1940s [602] nonthermal effects were documentedin bacterial viral and tissue cultures with applied low-repetition 20-MHz pulses Most studies spanning the 1940sthough the 1980s focused on EMFrsquos ability to kill microbesand fungi in human food sources at high intensity conse-quently most research was focused on thermal intensitiesThat work still continues today as microwaves have beenshown to be an efficient means for killing microbes [50] Butmicrobes also react to much lower nonlethal intensities andrecent work finds effects from both ELF and RFR

The common bacteria Escherichia coli which can liveharmlessly in the gut of humans and many other animalspecies can also turn virulent and kill through food-borneillnesses E coli comes inmany strains is well studied andnow considered the most genetically and physiologicallycharacterized bacterium E coli encounter varied andnumerous environmental stressors during growth sur-vival and infection including heat cold changes in Phlevels availability of foodwater supplies and EMF Alongwith other bacteria they respond by activating groups ofgenes and heat shock proteins (see ldquoMechanismsrdquo above)which can eventually lead to stress tolerance for survivalpurposes But induced stress tolerance can also lead toincreased virulence as well as enhanced tolerance to otherstressors that confer cross‐protection [603]

Levitt et al EMF and wildlife 55

Salmen and colleagues [604 605] published papers ofEMF effects on bacterial strains documenting the growinginvestigation of microbes related to antibiotic resistancewith many findings stressing responses to EMF [606ndash610]Cellini et al [611] investigated E colirsquos adaptability toenvironmental stress induced by ELF exposures to 50-Hzmagnetic fields at low intensities (01 05 10mT) vs shamcontrols They found exposed samples and controls dis-played similar total and culturable counts but increasedcell viability was observed in exposed samples re-incubated for 24 h outside of the test solenoid comparedto controls Exposure to 50 Hz EMF (20ndash120 min) alsoproduced a significant change in E colimorphotype with apresence of coccoid cells aggregated in clusters after re-incubation of 24 h outside of the magnetic field-solenoidAtypically lengthened bacterial forms were also notedindicating probable alteration during cell division Somedifferences in RNA-AFLP analysis were also seen for allintensities evaluated They concluded that exposure to50-Hz ELF-EMF is a bacterial stressor as evidenced by itsimmediate response in modifying morphology (frombacillary to coccoid) and inducing phenotypical and tran-scriptional changes Despite this stressor effect it was alsoseen that exposed samples significantly increasedviability suggesting the presence of VBNC cells Theyconcluded that further studies were needed to better un-derstand ELF-EMF in bacterial cell organization They didnot extrapolate to the obviousmdash that E coliwas changed inan abnormal way but nevertheless strengthened inviability mdash a recipe for antibiotic resistance

Crabtree et al [612] in a small human study investi-gated the biomic relationship of human bacteria exposed toboth static magnetic fields (SMF) and RFR Using laboratoryculture strains and isolates of skin bacteria collected fromthe hand cheek and chin areas of four volunteers who haddifferent (self-reported) cell phone use histories they foundvaried growth patterns of E coli Pseudomonas aeruginosaand Staphylococcus epidermidis under static magnetic fieldson different bacterial species Isolates of skin microbiotashowed inconsistent growth among the test subjects likelydue to their differing cell phone usage histories (classified asheavymediumand light) andother variables The growthofStaphylococci was increased under RFR in certain in-dividuals while in others growth was suppressed This wascomplicated by the different body areas tested some withhigher chronic exposures such as the hands aswell as othervariables when one test subject used an antibacterial facewash Volunteers in the heavy use category showed lessbacterial growth on the hands possibly due to microbehabituation Overall and despite the small sample theyconcluded RFR can disrupt the balance in skin microbiota

making it more vulnerable to infection by specific opportu-nistic andor other foreign pathogens They noted that bothSMF and RF-EMFs have significant but variable effects onthe growth of common human bacteria that bacterialgrowth was either unaffected increased or suppresseddepending on the species of bacteria and that bacterial re-sponses seemed to be determined by historic exposure toRF-EMF and life style This study even with inherent limi-tations indicates changes in microbes with EMFs and mayprove a novel way to study bacteria with significance forreal-life exposures to humans and animals alike

Salmen et al [605] also found highly variable resultsfromRFR (900 and 1800MHz) effects onDNA growth rateand antibiotic susceptibility in Staphylococcus aureusStaphylococcus epidermidis and P aeruginosa Using anactive cell phone handset they exposed bacteria to 900and 1800 MHz for 2 h then injected samples into a newmedium where growth rate and antibiotic susceptibilitywere evaluated Regarding DNA they found no differencesin S aureus and S epidermidis when exposed to 900 and1800 MHz vs controls but P aeruginosa showed changesinDNAbandpatterns following such exposures Regardinggrowth rates with the exception of a significant decreaseafter 12 h exposure to 900 MHz no significant effects ongrowth of S aureus and S epidermidis were seen But thegrowth of P aeruginosa was significantly reducedfollowing exposure for 10 and 12 h to 900 MHz while nosignificant reduction in growth followed exposure to1800 MHz Regarding antibiotic susceptibility in thedrugs studied (ie amoxicillin 30 mg azithromycin 15 mgchloramphenicol 10 mg and ciprofloxacin 5 mg) with theexception of S aureus treated with amoxicillin (30 mg)EMF-exposure had no significant effect on bacterialsensitivity to antibiotics This study shows variabilityamong bacterial species not only to different frequenciescommon in the environment today but also to changes insensitivity to some antibiotics but not others There mayhave been design problems with this study however

Several studies investigated WiFi signals on bacterialstrains Taheri et al [610] assessed exposure to 900-MHzGSM mobile phone radiation and 24-GHz RFR from com-mon WiFi routers to see if cultures of Listeria mono-cytogenes and E coli resulted in altered susceptibility to 10different antibiotics They found narrowwindows in whichmicrobes became more resistant For L monocytogenes nosignificant changes in antibacterial activity betweenexposed and nonexposed samples mdash except for Tetracy-cline (Doxycycline) mdash were noted For E coli howeverthere was a significant change in antimicrobial activitiessuggesting RFR exposures can influence antibiotic sus-ceptibility of E coli more than in Listeria For window and

56 Levitt et al EMF and wildlife

pronounced effects they found L monocytogenes exhibi-ted different responses to each antibiotic For Doxycyclinethe window occurred after 6 h exposure toWiFi andmobilephone-RFR After 9 h of exposure to WiFi for Ciprofloxacinand Sulfonamide (Tremethoprinsulfamethoxazole) bac-teria tended to become more resistant By contrast thepattern for Levofloxacin and Penicillin (CefotaximeDef-triaxone) showed increased sensitivity For Ecoli thepattern of the response to WiFi and mobile phone RFR wasthe same maximum antibiotic resistance was seen be-tween 6 and 9 h of exposure but after 12 h a stress responselead to a return to preexposure conditions indicating anadaptive reaction Taheri et al [609] found similarnonlinearwindoweffects anddifferences in growth rates inKlebsiella pneumonia while Mortazavi et al [613] foundsimilar window effects in E coli In addition they saw sig-nificant increased growth rates after radiation exposures inboth Gram-negative E coli and Gram-positiveL monocytogenes They concluded that such window ef-fects can be determined by intensity and dose rate thatexposure to RFR within a narrow window can make mi-croorganisms resistant to antibiotics and that this adap-tive phenomenon is a human health threat The same canbe inferred for many non-human species

Said-Salman et al [614] evaluated non-thermal effectsofWiFi at 24 GHz for 24 and 48 h (using aWiFi router as thesource) on the pathogenic bacterial strains E coli 0157H7S aureus and S epidermis for antibiotic resistancemotility metabolic activity and biofilm formation Resultsfound that WiFi exposure altered motility and antibioticsusceptibility of E coli but there was no effect on S aureusand S epidermis However exposed cells (vs unexposedcontrols) showed an increased metabolic activity and bio-film formation ability in E coli S aureus and S epidermisThey concluded that WiFi exposure acted as a bacterialstressor by increasing antibiotic resistance and motility ofE coli as well as enhancing biofilm formation in all strainsstudied They indicated the findingsmay have implicationsfor the management of serious bacterial infections

Movahedi et al [615] also investigated antibioticresistance using short-term exposure to RFR from amobilephone simulator (900 MHz 24 h) on P aeruginosa andS aureus against 11 antibiotics They found significantchanges in structural properties and resistance to thenumerous antibiotics studied P aeruginosa was resistantto all antibiotics after 24 h of exposure vs non-exposedcontrols while S aureus bacteria were resistant to about50 They also found structural changes in all exposedsamples and increased cell wall permeability

In a field study near cell towers Sharma et al [616]looked at changes in microbial diversity and antibiotic

resistance patterns in soil samples taken near four differentbase stations with control samples taken gt300 m awayStenotrophomonas maltophilia Chryseobacterium gleumand Kocuria rosea were isolated and identified in soilsamples collected near the exposed zones They foundgreater antibiotic resistance in microbes from soil nearbase stations compared to controls with a statisticallysignificant difference in the pattern of antibiotic resistancefound with nalidixic acid and cefixime when used asantimicrobial agents They concluded that cell tower ra-diation can significantly alter the vital systems in microbesand make them multi-drug resistant

Researchers have also investigated ELF-EMF effects onbacterial growth and antibiotic sensitivity Segatore et al[608] investigated 2 mT 50 Hz exposures on E coli ATCC25922 and P aeruginosa ATCC 27853 and found EMFsignificantly influenced the growth rate of both strainsnotably at 4 6 and 8 h of incubation The number of cellswas significantly decreased in exposed bacteria vs con-trols And at 24 h incubation the percentage of cellsincreased (P aeruginosa sim 42 E coli sim 5) in treatedgroups vs controls which suggested to the researchers aprogressive adaptive response However they saw noremarkable change in antibiotic sensitivity Potenza at al[617] also found effects at high-intensity static magneticfields at 300 mT on growth and gene expression in Ecolibut that would be a high environmental exposure

Viruses

There is a paucity of research on viral species and EMFlikely due to the fact that viruses lack ferromagnetic ma-terials are difficult to study and donrsquot make good generallab models other than to investigate their direct impact onspecific in vivo end points Virology research thrives in itsown specialized niche and has not been used for basicmodeling like so many other living life forms as notedthroughout this paper There is long-standing debate onwhether viruses are even alive

However one wide-ranging discussion by Zaporozhanand Ponomarenko [618] hypothesized a possible complexmechanistic link between influenza pandemics naturalsun spot cycles and non-thermal effects of weak magneticfields via cryptochromesradical pairs gene expressionpathways and stress-induced host immunological alter-ations favorable to influenza epidemics Noting thatmost mdash though not all mdash major influenza epidemicsoccurred in time intervals starting 2ndash3 years before andending 2ndash3 years after maximum solar activity they hy-pothesized that solar cycles are able to both regulate and

Levitt et al EMF and wildlife 57

entrain processes of biological microevolution in viralspecies (among others) as well as influence human bio-rhythms in synergistic ways that could lead to influenzaepidemics Although others have also noted links betweeninfluenza pandemics and sunspot activity mdash possiblybased on changes in migratory bird patterns as viral vec-tors [619ndash621]mdash and some have linked sun spots with otheradverse human health events these effects remain of in-terest but are still hypothetical UV radiation which is notcovered in this paper is known to suppress cell-mediatedimmunity and is therefore capable of adversely affectingthe course of a viral infection in some mammal speciesAmbient EMF in lower frequency ranges may also bereducing immune viability across species which cantheoretically foster opportunistic virulence Far more EMFresearch needs to be conducted on viruses one fruitfulapproach might be synergistic investigations in virus-infected plant species

The previous studies of microbes show a pattern ofsensitivity inmicroorganisms to EMFwith associations thatencompass a wide range of critical changes includingconsistent stress responses alterations in growth andviability cell membrane alterations and clear patterns ofhow easily antibiotic resistance forms in microbial life tonow ubiquitous EMF levels

Plants (see Part 2 Supplement 4for a table of flora studies ELF RFR)

Plants have evolved in highly sensitive ways to natural andmanmade EMF in all phases of germination growth andmaturation [31] Magnetoreception which is well docu-mented in animals such as birds has also been describedin plants [622] and plant species can respond to subtlechanges in EMF in the environment including in wholeplant communities [623] They may even lsquocommunicatersquoand gather various kinds of lsquoinformationrsquo via electricalsignals in neuron-like cells in root tips and elsewhere [624]Some hypothesize [625] that a form of vibrational andacoustic sensitivity around 220 Hz may play a role in plantlife although not everyone agrees [626]

Almost all vegetation is subject to complex multi-frequency fields due to their soil-based root systems andhigh water content plus above-ground ambient RFR ex-posures makes plants uniquely susceptible to effects neartransmission towers [623 627] Many EMF studies havefound both growth stimulation as well as dieback Thepresence of numerous RFR-emitters in the German andSwiss Alps is thought to have played a role in the

deforestation there [628] The lsquobrowningrsquo of treetops isoften observed near cell towers especially when water isnear tree root bases [25] Treetops with their high moisturecontent and often thick vegetative canopy are known RFRwaveguides In fact military applications utilize thiscapability in treetops for communication signal propaga-tion in remote areas and for guidance of low-flyingweapons systems [629]

How flora interacts with EMF is still a mystery but aclear pattern has emerged in researching the database forthis paper static ELF-EMF has largely been found benefi-cial to plant and seed growth [630] while RFR is detri-mental Plants clearly have magnetoreception in theirstationary condition The normal ground state of magneticfields for plants is the relatively constant naturalgeomagnetic field that averages between 25 and 65 μTdepending on location and seasonal variations [631] At-mospheric changes such as thunderstorms and lightningcan cause intermittent changes in ambient magnetic fieldsThese activities are also generally associated with rain-water critical to virtually all plant life Plants can detectthese changes and prepare for growth using the upcomingrainfall Trees are seen extending their branches skywardlong before rain actually occurs and such changes matchalterations in tree polarities [632]

There are many studies showing an increase in thegrowth rate in plants such as studies of seed germinationexposed to alternatingmagnetic fields Plants also respondsimilarly to high intensity static magnetic fields This maymean that the physiological mechanism in plants thatcauses magnetic field-induced growth is finely tuned to acertain intensity of magnetic flux Any variation in in-tensity or shape of the ambient magnetic field could acti-vate or hinder this growth mechanism

Lightning for instance generates fast and intenseelectromagnetic pulses (EMP) EMP has consistently beenshown to cause biological effects [633] with just one pulsePlants may have mechanisms so sensitive that they candetect the energy of EMP from kilometers away The pulsecauses a transient change in the environmental magneticfield that may be detected by one or more of the mecha-nisms mentioned in the ldquoMechanismsrdquo section above aswell as discussed below EMPhas been closely investigatedfor military applications for its ability at high intensities todisable electronics While much of the military-supportedresearch finds no biological effects from EMP exposurenon-military supported research does show effects Thisparallels the same findings in industry vs non-industryresearch patterns [165 634]

There is a long history on the study of effects of EMFexposure on plant growth notably the work of the Indian

58 Levitt et al EMF and wildlife

scientist Sir Jagadish Bose (1858ndash1937) who proposed theelectric nature of plant responses to environmental stimuliand studied effects of microwaves on plant tissues andmembrane potentials [635] Interestingly Bose investi-gated the effects of millimeter waves [636] now applicableto 5G technology Bose arguably was a pioneer of wirelesscommunication

Another early pioneer in EMF effects on plants wasHarold Saxon Burr (1889ndash1973) at Yale University whoinvestigated the electric potential of trees in two tree spe-cies (a maple and an elm) located on one property andanother maple tree for comparison growing 40 miles(64 km) away Measurements of numerous parameterswere taken using embedded electrodes that recordedhourly from 1953 to 1961 [637] Simultaneous records oftemperature humidity barometric pressure sunlightmoon cycles sunspot activity weather conditionsatmospheric-potential gradients earth-potential gradi-ents and cosmic rays were correlated with tree potentialsBurr also installed equipment that measured the potentialbetween electrodes in the Earth (about 10 miles apart) andthe potential gradient of the air and found that the air andEarth potentials fluctuated exactly with the phase of thetree potentials although the trees were not always syn-chronous Burr ultimately found that the electrical envi-ronment correlated closely with tree potentials in a kind ofentrainment to diurnal lunar and annual cycles Meteo-rological parameters did not correlate in any immediateway other than when passing thunderstorms elicitedanomalous behavior in the trees in direct parallel to mea-surements with the Earth electrodes This follows the the-ory noted above that plants can sense EMP and takeimmediate information from it

There are no other long-term field studies as detailedas Burrrsquos of magnetic field effects on a plant speciesHowever another field study of RFR in Latvia [638]measured effects directly on trees near the Skrunda RadioLocation Station an early warning radar system thatoperated from 1971 to 1998 The systemoperated in the 156ndash162 MHz frequency range transmitting from four pulsedtwo-way antennas that had operated continuously for over20 years by the time of the study In permanent plots in pineforest stands at varying distances from the radar stationand in control areas tree growth changes were measuredand analyzed using retrospective tree ring data Theyfound a statistically significant negative correlation be-tween the relative additional increment in tree growth andthe intensity of the electric field with the radial growth ofpine trees diminished in all plots exposed to RFR Thedecreased growth began after 1970 which coincided withthe initial operation of the station and was subsequently

observed throughout the period of study The effects ofmany other environmental and anthropogenic factors werealso evaluated but no significant effects on tree growthwere correlated This may have been the first detailed fieldstudy of plants and RFR

Many studies of EMFandplants are today conducted inlaboratories and have often focused on growth promotionto create higher yields of food-producing plants Effects ofstatic EMF pulsed EMF ELF-EMF and RF-EMF have beenreported There are in fact over 200 studies on plants andEMF alone mdash too numerous to review here See Part 2Supplement 4 for a Table of studies on plant seedlings anddevelopment based on the types of EMFrsquos tested

As noted in Supplement 4 and in Halgamuge [627]frequently static and ELF-magnetic fields generallyimprove plant growth whereas RFR retards it This is theopposite of results from animal and animal-cell cultureexperiments in which ELF-MF usually produces the sameeffects as RFR It is interesting to note that Hajnorouzi et al[639] and Radhakrishma et al [640] proposed that MF de-creases environmental stress in plants whereas Vian et al[641 642] considered RFR as a systemic stressor A majormorphological difference between animal andplant cells isthat plant cells have a cell wall that is an active physio-logical organelle which regulates growth and cell divisionand controls cellular communications The cell wall con-tains a considerable amount of water [643] Is it possiblethat absorption of RFR by cell-wall water causes a micro-thermal effect that adversely affects plant cell functionsand even causes cell death whereas thermal effects are notlikely to occur with ELF-EMF exposure

Some plant roots have been found sensitive to bothELF and RFR Belyavskaya [644] found a strong cyto-chemical reaction in pea root cells after exposure to lowlevel magnetic fields Kumar et al [645] found cyto- andgenotoxicity in root meristems of Allium cepa with900-MHz and 1800-MHz RFR Chandel et al [646] studiedcytotoxic and genotoxic activity on DNA integrity in rootmeristems of A cepa using 2100-MHz RFR and foundexposure caused DNA damage with a significant decreasein HDNA accompanied by an increase in TDNA while TMand OTM did not change significantly compared to con-trols Biological effects were dependent on the duration ofexposure with maximum changes seen at 4 h

In a series of studies Stefi et al [647ndash649] investigatedthe effects of long termRFR exposure from the base units ofcommon cordless DECT phone systems (pulsed trans-mission mode 1882 MHz 24 hday 7 dweek) on variousplant species (Arabidopsis thaliana Pinus halepensisGossypium hirsutum respectively) and found structural andbiochemical alterations Compared to controls in Faraday

Levitt et al EMF and wildlife 59

cages exposed plant biomass was greatly reduced and leafstructure was only half as thick Leaves were thinner andpossessed greatly reduced chloroplasts which contributedto overall reduced vitality Root systems were alsoadversely affected They concluded that RFR is a stressorandnoxious to plant life A study of similar design [650] didnot find the same effects on maize (Zea mays) which theyattributed to that plantrsquos structural differences althoughchloroplasts were severely affected (see also Kumar et al[651])

Jayasanka and Asaeda [652] published a lengthy re-view that focused on microwave effects in plants Studiesindicate effects depend on the plant family and growthstage involved and exposure duration frequency andpower density among other factors They concluded thateven for short exposure periods (lt15 min to a few hours)nonthermal effects were seen that can persist for long pe-riods even if initial exposures were very short In additionthey noted that since base stations operate 24 hdayneither short exposures nor recovery periods are possiblein natural habitats as plants are continuously exposedthroughout their life cycles They said that variations in thepower density and frequency of microwaves exert complexinfluences on plants and that clearly diverse plant speciesrespond differently to such factors They concluded it isnecessary to rethink the exposure guidelines that currentlydo not take nonthermal effects into consideration

There are numerous reports of adverse RFR effects onmature flora Waldman-Salsam et al [653] reported leafdamage in trees near mobile phone towersmasts In adetailed long-termfieldmonitoring study from2006 to 2015in two German cities they found unusual and unexplain-able tree damage on the sides of trees facing the towers andcorrelated it to RFR measurements vs control areaswithout exposures They found that tree-side differences inmeasured values of power flux density corresponded totree-side differences in damage Controls which consistedof 30 selected trees in low radiation areas without visualcontact to any phone mast and power flux density under50 μWm2 showed no damage They concluded thatnonthermal RFR from mobile phone towers is harmful totrees and that damage that affects one side eventuallyspreads to the whole tree

Vian et al [642] published a review of plant in-teractions with high frequency RFR between 300 MHz and3 GHz and noted that reports at the cellular molecular andwhole plant scale included numerous modified metabolicactivities (reactive oxygen species metabolism α- andβ-amylase Krebs cycle pentose phosphate pathwaychlorophyll content and terpene emission among others)altered gene expression (calmodulin calcium-dependent

protein kinase and proteinase inhibitor) and reducedgrowth (stem elongation and dry weight) after nonthermalRFR exposure They said changes occur in directly exposedtissues as well as systemically in distant tissues and pro-posed that high-frequency RFR be considered a genuineenvironmental factor highly capable of evoking changes inplant metabolism

Halgamuge [627] also published a review that foundweak non-thermal RFR affects living plants The authoranalyzed data from 45 peer-reviewed studies of 29 differentplant species from 1996 to 2016 that described 169 experi-mental observations of physiological and morphologicalchanges The review concluded that the data substantiatedthat RFR showed physiological andor morphological ef-fects (899 plt0001) The results also demonstrated thatmaize roselle pea fenugreek duckweeds tomato onionsand mungbean plants are highly sensitive to RFR and thatplants appear more responsive to certain frequencies be-tween 800 and 1500MHz (plt00001) 1500 and 2400MHz(p 00001) and 3500 and 8000 MHz (p=00161) Hal-gamuge [627] concluded that the literature shows signifi-cant trends of RFR influence on plants

There is particular concern for impacts to flora and 5Gsince millions of small antennas mounted on utility polestransmitting in MMW and other broadband frequenciesalready are mdash or will soon be mdash in very close proximity tovegetation creating both near- and -far field exposures Asnoted in Halgamuge [627] the following are some studiesinvestigating GHz frequencies already in use or planned for5G that found significant effects on plants Tanner andRomero-Sierra [654] on accelerated growth ofMimosa plant(10 GHz 190 mWcm2 5ndash10 min) Scialabba and Tambur-ello [655] on reduced hypocotyls growth rate in radish(Raphanus sativus) (105 GHz 8 mW or 12658 GHz 14 mWfor 96 h) Tafforeau et al [656] induced meristem (activelydividing group of cells) production in Linum usitatissimum(105 GHz for 2 h at 01 mWcm2) and Ragha et al [657](96 GHz 30 min) found germination depended on expo-sure parameters on Vigna radiata Vigna aconitifolia Cicerarietinum and Triticum aestivum plants This is an area inimmediate need of further investigation given the resultsfrom the previous studies

A thorough review of RFR effects to trees and otherplants was published by Czerwinski et al [622] who re-ported that ecological effects on whole plant communitiescould occur at a very low exposure level of 001ndash10 μWcm2 mdash certainly comparable to limits examined in thispaper They focused on frequencies between 07 and18 GHz and includedmultiple complex indicators for planttypes biometrics and environmental factors It was thefirst comprehensive paper that extended beyond using

60 Levitt et al EMF and wildlife

narrower research methods They noted that although theliterature on the effects of RFR on plants is extensive not asingle field study had assessed the biological response atthe level of awhole plant community biome or ecosystembut rather focused mostly on short-term laboratory studiesconducted on single species They said ldquohellipThis disso-nance is particularly striking in view of the fact that alter-ations in a plant communityrsquos structure and compositionhave long been considered to be well founded sensitiveand universal environmental indicatorsrdquo The paper servesas a predictive model for complex future field studies onlarger ecosystems

Interesting EMF synergistic effects were found withstatic magnetic fields and bacteria in plants Seeking non-chemical methods to improve seed germination after pro-longed periods of storage when seed viability can deteri-orate Jovičić-Petrović et al [658] studied the combinedeffects of bacterial inoculation (Bacillus amyloliquefaciensD5 ARV) and static magnetic fields (SMF 90 mT 5 and15 min) on white mustard (Sinapis alba L) seeds Theirresults found that biopriming with the plant growth-promoting B amyloliquefaciens increased seed growth by4043 Seed response to SMF alone was dependent ontreatment duration While SMF at 5 min increased thegermination percentage exposure at 15 min lowered seedgermination compared with the control However thenegative effect at the longer exposure was neutralizedwhen combined with the bacterial inoculation Bothgermination percentages were significantly higher whenSMF was combined with the bacteria (SMF 5 min + D5ARV and SMF 15 min + D5 ARV 4468 and 5320respectively) compared with control They concluded thatbiopriming and SMF treatment gave better results thanbacterial inoculation alone The highest germination per-centagemdash 5320of germinated seedsmdashwas seenwith thebacterium and 15 min exposure to 90 mT demonstrating asynergistic effect They concluded that such techniquescan be used for old seed revitalization and improvedgermination

Even aquatic plants have been found sensitive toartificial electric fields Klink et al [659] assessed electricfield exposures on growth rates and the content of tracemetals of Elodea canadensis Plants were exposed in alaboratory to an electric field of 54 kVm for seven daysPlant length and Fe Mn Ni Pb and Zn were measuredResults showed the applied electric fields slightlyenhanced root growth They also found changes inmineralabsorption Mn and Ni were significantly lower while Pband Zn were significantly higher in exposed plants Fecontent did not differ between control and exposed plantsThey concluded that electric fields had potential use for

phytoremediation in tracemetal contaminatedwaters Thisstudy also has implications for long term aquatic planthealth in general

Alsoworkingwith electric fields Kral et al [660] foundfascinating regeneration in plant root tips inArabidopsis atvarying electric field exposures and time durationswith theweaker exposures producing the most growth They foundthat imposed electric fields can perturb apical root regen-eration and that varying the position of the cut and the timeinterval between excision and stimulation made a differ-ence They also found that a brief pulse of an electric fieldparallel to the root could increase by up to two‐fold theprobability of its regeneration perturb the local distribu-tion of the hormone auxin and alter cell division regula-tion with the orientation of the root towards the anode orthe cathode playing a role

While mechanisms are still unclear regarding howEMFs affect plants oxidative effects appear to play a sig-nificant role Oxidative changes have been reported inmany studies in plants after exposure to EMF [578 639661ndash671] EMF-related stress has been proposed by Vianet al [641 642] Roux et al [672 673] and Radhakrishmaet al [640] Other mechanisms affecting plants such asferromagnetism radical-pairs calcium ions and crypto-chromes have also been proposed [674 675]

It is apparent that plant growth and physiologymdashwiththeir root systems anchored in the ground while theirlsquoheadsrsquo manifest in the air mdash are affected by exposure toEMF in complex synergistic ways and that they are sus-ceptible to multi-frequency exposures throughout their lifespans

Conclusion

Effects from both natural and man-made EMF over a widerange of frequencies intensities wave forms andsignaling characteristics have been observed in all speciesof animals and plants investigated The database is nowvoluminous with in vitro in vivo and field studies fromwhich to extrapolate The majority of studies have foundbiological effects at both high and low-intensityman-madeexposures many with implications for wildlife health andviability It is clear that ambient environmental levels arebiologically active in all non-human species which canhave unique physiological mechanisms that require natu-ral geomagnetic information for their lifersquos most importantactivities Sensitive magnetoreception allows living or-ganisms including plants to detect small variations inenvironmental EMF and react immediately as well as overthe long term but it can also make some organisms

Levitt et al EMF and wildlife 61

exquisitely vulnerable to man-made fields AnthropogenicEMFmay be contributing more than we currently realize tospeciesrsquo diminishment and extinction Exposures continueto escalate without understanding EMF as a potentialcausative andor co-factorial agent It is time to recognizeambient EMF as a potential novel stressor to other speciesdesign technology to reduce exposures to as low asreasonably achievable keep systems wired as much aspossible to reduce ambient RFR and create laws accord-ingly mdash a subject explored more thoroughly in Part 3

Research funding None declaredAuthor contributions All authors have acceptedresponsibility for the entire content of this manuscriptand approved its submissionCompeting interests Authors state no conflict of interestInformed consent Not applicableEthical approval Not applicable

Part 2 supplements

Supplement 1 Genetic Effects of RFR ExposureSupplement 2 Genetic Effects at Low Intensity StaticELF EMF ExposureSupplement 3 Biological Effects in Animals and PlantsExposed to Low Intensity RFRSupplement 4 Effects of EMF on plant growth

References

1 Besser B Synopsis of the historical development of Schumannresonances Radio Sci 200742RS2S02

2 Balser M Wagner CA Measurements of the spectrum of radionoise from 50 to 100 cycles per second 1 J Res Nat Bur Stand DRadio Propag 196064D34ndash42

3 NASA 2021 httpswwwnasagovmission_pagessunearthnewsgalleryschumann-resonancehtml

4 Friedman JS Out of the blue a history of lightening sciencesuperstition and amazing stories of survival NY Delecorte Press2008101 p

5 AdeyWR Electromagnetic fields and the essence of living systemsIn Andersen JB editor Modern radio science New York NY USAOxford University Press 19901ndash37 pp

6 Becker RO Cross currents the perils of electropollution thepromise of electromedicine Los Angeles USA Jeremy Tarcher199067ndash81 pp

7 Levitt BB Electromagnetic fields A consumerrsquos guide to the issuesand how to protect ourselves Orlando FL USA First editionHarcourt Brace and Co 1995 iUniverse Authors GuildBackinprintcom edition 2007 Lincoln NE USA

8 Levitt BB Moving beyond public policy paralysis InClements-Croome D editor Electromagnetic environments and

health in buildings NewYork NY USA Spon Press 2004501ndash18pp

9 Manzella N Bracci M Ciarapica V Staffolani S Strafella ERapisarda V et al Circadian gene expression and extremely low-frequencymagnetic fields an in vitro study Bioelectromagnetics201536294ndash301

10 IUCN 2018 The International Union for Conservation of NatureVersion 2018-1 Red List of Threatened Species 2018

11 Intergovernmental Science and Policy Platform on Biodiversityand Ecosystem Services Paris France (IPBES) In Brondizio ESSettele J Diacuteaz S Ngo HT editors Global assessment report onbiodiversity and ecosystem services of the IntergovernmentalScience-Policy Platform on Biodiversity and Ecosystem ServicesBonn Germany IPBES Secretariat 2019

12 Sanchez-Bayo F Wyckhuys AG Worldwide decline of theentomofauna a review of its drivers Biol Conserv 20192328ndash27

13 Schultz CB Brown LM Pelton E Crone EE Citizen sciencemonitoring demonstrates dramatic declines of monarchbutterflies in western North America Biol Conserv 2017214343ndash6

14 Xerces Society for Invertebrate Conservation 2019Available from httpsxercesorgmonarchs

15 Center for Biological Diversity Monarch butterfly populationdrops by nearly one-third iconic butterfly has declined by morethan 80 percent in recent decades 2017 Available from httpswwwbiologicaldiversityorgnewspress_releases2017monarch-butterfly-02-09-2017php

16 Guerra PA Gegear RJ Reppert SM A magnetic compass aidsmonarch butterfly migration Nat Commun 201454164

17 Marha K Musil J Tuha H Electromagnetic fields and the livingenvironment Praguel Hungary State Health Publishing House1968 (Trans SBN 911302-13-7 San Francisco Press 1971)

18 Ceballos G Garciacutea A Ehrlich PR The sixth extinction crisis lossof animal populations and species J Cosmol 201081821ndash31

19 Ceballos G Ehrlich PR Barnosky AD Garciacutea A Pringle RM PalmerTM Acceleratedmodernhuman-induced species losses enteringthe sixth mass extinction Sci Adv 20151e1400253

20 Ceballos G Ehrlich PR Dirzo R Biological annihilation via theongoing sixth mass extinction signaled by vertebrate populationlosses and declines Proc Natl Acad Sci Unit States Am 2017114E6089ndash96

21 Weimerskirch H Le Bouard F Ryan PG Bost CA Massive declineof the worldrsquos largest king penguin colony at Ile aux CochonsCrozet Anartic Sci 201830236ndash42

22 Manville AM II Impacts to birds and bats due to collisions andelectrocutions from some tall structures in the United States mdashwires towers turbines and solar arrays state of the art inaddressing the problems In Angelici FM editor Problematicwildlife a cross-disciplinary approach New York NY USASpringer International Publishers 2016415ndash42 pp Chap 20

23 Manville AM II Towers turbines power lines and solar arraysthe good the bad and the ugly facing migratory birds and batsmdashsteps to address problems Invited presentation Earth Scienceand Policy Class GEOL 420 GeorgeMasonUniversity 201639 pPowerPoint slides available online

24 Balmori A The effects of microwave radiation on wildlifepreliminary results 2003 Available from httpwwwemrpolicyorglitigationcase_lawbeebe_hillbalmori_wildlife_studypdf

62 Levitt et al EMF and wildlife

time in evolutionary history we have infused the Earthrsquossurface with a blanket of artificial energy exposures with noclear understanding of what the consequences may be

And although ldquonaturalrdquo not all energy is alike Man-made exposures contain propagation characteristicsmdash suchas alternating current modulation complex signaling char-acteristics (eg pulsed digital and phased array) unusualwave forms (eg square and sawtooth shapes) and atheightened power intensities at the Earthrsquos surface that sim-ply donot exist in nature These are allman-madeartifacts Inour embrace of technology we have completely altered theEarthrsquos electromagnetic signature in which all life hasevolved in essence bypassing the magnetospherersquos protec-tion And because so much of wireless technology is satellitebased increasing exposures are no longer just ground-generated All atmospheric levels are now affected byincreasing ambient exposures (see Part 1 and Part 1 Supple-ment) This is especially true in the lower atmosphere whichis lsquohabitatrsquo (beyondmere oxygen and clean air standards) forall species thatmatemigrate and feed in the airmdash includingbirds mammals (such as bats) insects and some arachnids

Species extinctions

There has been an unprecedented rate of biodiversitydecline in recent decades according to the InternationalUnion for Conservation of Nature [10] which maintains aldquoRed List of Threatened Speciesrdquo that is considered theworldrsquos most comprehensive source on the global conser-vation status of animal fungi and plant species mdash allcritical indicators of planetary health

IUCNrsquos 2018 list showed that 26000 species are threat-ened with extinction which reflected more than 27 of allspecies assessed This was greatly increased from their 2004report that found at least 15 species had already gone extinctbetween 1984 and 2004 and another 12 survived only incaptivity Current extinction rates arenowat least 100 to 1000times higher than natural rates found in the fossil record

The more recent May 2019 report by the Intergovern-mental Science and Policy Platform on Biodiversity andEcosystem Services Paris France [11] projected that at least 1million plant and animal species worldwide are at imminentthreat of extinction if our current humanactions and activitiesare not immediately reversed A review of 73 reports bySanchez-Bayo and Wyckhuys [12] found those rates hadgreatly accelerated The authors noted that biodiversity ofinsects in particular is threatened worldwide with dramaticdeclines that could lead to a 40 extinction of insect speciesover the next several decades In terrestrial ecosystems theyfound Lepidoptera Hymenoptera and Coleoptera (dung

beetles) were most affected while in aquatic ecosystemsOdonata Plecoptera Trichoptera and Ephemeroptera havealready lost a considerable proportion of species Affectedinsect groups included niche specialist species as well ascommon and generalist species many of which are criticallyimportant for pollination aswell as seed fruit nut andhoneyproduction and natural pest control among others ofimmeasurable economic and ecological value

Humans are the primary cause for most declines viahabitat destructiondegradation over-exploitation for foodpets cattle and medicine artificially introduced speciespollutioncontamination pesticides and disease Climatechange is increasingly establishedas a serious threat aswellas agricultural practices like monoculture crops for cattlefeed biofuels and timber New pesticides and weed killersintroduced within the last 20 years using neonicotinoidsglyphosphate and fipronil are especially damaging sincethey are long-lasting and capable of sterilizing soil of bene-ficial microorganisms including worms and grubs whichcan then extend to areas far beyond applications sites

One example of multi-factorial damage includes theiconic AmericanMonarch butterfly (Danaus plexippus)whichis found across America and Southern Canada and generallygeographically divided into eastern and western migratorygroups by the RockyMountains That species has declined bya full 994 in the west since the 1980smdash 85 of that beingsince 2017 [13 14] According to the Center for Biological Di-versity [15] the eastern monarch population has shrunk by90 in the past two decades Massive habitat loss wildfiresclimate change droughts enhanced storm ferocity and the1990s introduction of Monsanto ldquoRoundup Readyrdquo cropscapable of surviving herbicides that kill other weeds mdashincluding milkweed which monarchs need for breeding andas their sole food supply along their migratory routes mdash arethought to be the primary culprits

Here we argue environmental EMF should be addedto this list since many insects and other living species havesensitive receptors for EMF eg monarchs were found tohave light sensitive magnetoreceptors in their antennaethat serve as an inclination compass when daylight isabsent [16] RFR is also known to alter the time periodneeded for a butterfly to complete morphogenesis plusgastrulation and larval growth can be accelerated [17] Andthe devastating loss of pollinating insects like honey beesand other wild pollinators may also be related to environ-mental EMF (see ldquoInsectsrdquo below)

Anecdotally many people recall when there weresignificantly more insects and far more abundant wildlifeSince about 1980 there has been a steady almost imper-ceptible biodiversity diminishment among many speciesglobally [18ndash20] In 2018 scientists estimated that the

Levitt et al EMF and wildlife 3

largest king penguin colony shrank by 88 in just 35 years[21] due in major part to effects from climate change whileaccording to the International Scientific Committee forTuna and Tuna-like Species in the North Pacific Oceanover 97 of bluefin tuna have disappeared from theworldrsquos oceans primarily due to industrial overfishing butexacerbated by oil spills contamination and climatechange Tree and cave-dwelling bats until recently werecommon including in the Eastern United States Now withthe massive impacts from White-nosed Syndrome (a fatalbat fungal disease) annual wind-turbine bat collisionmortality estimated at nearly 1 million per year in the USalone [22 23] and pesticide use few bats are seen Batsspecies are also sensitive to EMF Impacts fromEMF as nowseen in extensive reviews add only yet another troublingvariable for all wildlife [24ndash36]

Since all food webs are uniquely tied together there arenegative cascading effects across all ecosystems Birds thateat insects are hard hit 8-in-10 partridges have disappearedfrom French farmlands while there has been a 50ndash80reduction in nightingales and turtledoves respectively in theUK Since 1980 the number of birds that typically inhabitEuropersquos farmlands has shrunk by 55 while in the last 17years French farmland-bird counts dropped by a full thirdIntensified agricultural practices are thought responsiblewith loss of insects being the largest contributor [12 37] Inthe United States of the 1027 species of migratory birdscurrently protected under the Migratory Bird Treaty Act of1918 anestimated40are indeclinebasedonbreedingbirdsurveys [38] Christmas Bird Counts [39] and other moni-toring tools [22 23] This trend is comparable to what ishappening globallyWhat role EMFplays in these declines isunclear but remains a disturbing possibility Nor do we un-derstand the limits of tolerance any given species has forenvironmental disturbance mdash some show high flexibilitywhile others thrive only within the narrowest ranges

One estimate of Earthrsquos species finds that since 1970wild animal populations have been reduced on average by60 Popularly called the ldquosixthmass extinctionrdquo [40] theterm connotes the sixth time in the Earthrsquos history thatlarge numbers of species have rapidly disappeared over arelatively short period this time due to human activity notasteroid strikes or volcanic activity Though not officiallyso-designated many now refer to this most recentgeologicecosystem period as the ldquoAnthropocenerdquo mdash theAge of Man [41ndash46]

Insect populations have been especially hard hit withextinctions eight times faster than that of mammals birdsand reptiles [12] Insect total mass is falling by an estimated25 per year suggesting they could vanish by the nextcentury And what affects insect populations affects

everything in the food web in one way or another Loss ofinsect diversity and abundance can cause devastating ef-fects throughout food webs and endanger entire ecosys-tems [12] In Europe Hallmann et al [47] found amore than75 decline over 27 years in total flying insect biomass in63 protected areas many throughout Germany There wasan 82 decline in mid-summer flying insect mass ManyEuropean insect speciesmigrate fromdistances as far awayas Africa The researchers noted that changes in weatherland use and habitat characteristics alone cannot explainthe overall decline and that there may be more than oneunrecognized factor involved in evaluating declines inoverall species abundance That unrecognized factor maybe the steadily rising ambient EMF that directly parallelsthese declines (see Part 1 Supplement 1)

Similar alarming invertebrate declines were discoveredin the Western Hemisphere in 2017 when American ento-mologist Bradford Lister after 40 years revisited the ElYunqueNational Forest in PuertoRico to followupona studybegun in 1976 [48] In the ensuing decades populations ofarthropods including numerous flying insects centipedesand spiders had fallen by 98 in El Yunque a pristinetropical rainforest within the US National Forest SystemInsectivoresmdash including birds lizards and toadsmdash showedsimilar declines with some species vanishing entirely Aftercontrolling for factors like habitat degradation or loss andpesticide use the researchers concluded that climate changewas the primary factor since the average maximum temper-ature in that rainforest had increased by 4 degF during thatperiod They did not factor in the large US military VLFinstallation in Aquada that communicates with submarinesall over the world or the multiple sweeping over-the-horizonphased array radar units aimed at Puerto Rico from coastalsites in the US that irradiate deep into that forest or themultiple NOAADoppler weather radar sites scattered all overthe small island to track hurricanes or the many cell towersthere too

These global declines are truly alarming with impli-cations for planetary health as well as human and wildlifeintegrity Many who study this say that climate changealone is not the only factor and that something new is goingon [47] The question is could steadily rising environ-mental EMF as one of the most ubiquitous but unrecog-nized new environmental genotoxins introduced since the1980s be contributing to these unprecedented specieslosses beginningwith insects but nowmanifesting in otherspecies too The upper microwave bands couple maxi-mally with some insects the size of fruit flies and arecapable of creating devastating resonance and other ef-fects Historically radiofrequency radiation (RFR) impactsto insects were among the first biological effects to be

4 Levitt et al EMF and wildlife

studied [49] with the hope of discovering new forms ofinsect control [50] All insect metamorphic developmentshave been studied including egg larva pupa and adultstages One hypothesis holds that some adult speciesare more sensitive than at larval stages because adultappendages act as conducting pathways to the body(see ldquoInsectsrdquo below)

It is these exact frequency bands between 30 kHz and3 GHz used in telecommunications technology that havebeen on the rise during this period And 5G is on the hori-zon which may specifically target insect populations (seePart 1)

Species sensitivity to EMFs

Other species have vastly more complex electromagneticsensing tools than humans as well as unique physiologiesthat evolved to sense weak fields Many species are highlysensitive to the Earthrsquos natural electromagnetic fields as wellas geographic and seasonal variations In fact it appears thatmost living things mdash including many species of mammalsbirds fish and bacteria mdash are tuned to the Earthrsquos electro-magnetic background in ways once considered as ldquosuper-powersrdquo but are now known to be physiological even asmechanisms are still imperfectly understood For examplemany animals have been observed sensing earthquakes longbeforehuman instrumentsdetect them including snakes andscorpions that seek shelter cattle that stampede birds thatsingat thewrong timesofday and female cats that franticallymove kittens [7]

This ability is likely due in part to numerous speciesreacting to changes in the Earthrsquos magnetic field andelectrostatic charges in the air detected through a naturallyoccurring mineral called magnetite found in many species[51 52] In fact honey bees are able to detect static mag-netic field fluctuations as weak as 26 nT against back-ground earth-strengthmagneticfields that aremuchhigher[53] and to sense weak alternating fields at frequencies of10 and 60 Hz [54] Magnetite reacts a million times morestrongly to external electromagnetic fields than any otherknown magnetic material Authors Kobayshi and Kirch-vink [52] and Kirchvink et al [53 54] hypothesized resultswere consistent with biophysical predictions of amagnetite-based magnetoreceptor Other mechanismslike radical pair mechanisms and cryptochromes may alsobe responsible (see ldquoMechanismsrdquo below)

Much has been written about magnetoreceptionmdash theterm used to describe how species sense electromagneticfieldsmdashwhich is well established but not well understoodMany species use information about the Earthrsquos natural

fields for migration mating food-finding homing nest-ing and numerous other activities Migratory bird species[55 56] honey bees [57] fish [58] mammals [59] bats [60]numerous insect species [61] mollusks [62] and evenbacteria [63] are known to sense Earthrsquos magnetic fields invarious ways Magnetoreception may enable some birdspecies to actually see the Earthrsquos fields [64]

Some insect and arachnid species (eg Trichobothria)can detect natural atmospheric electric fields [65] whichtrigger ballooning behaviormdash eg climbing to the highestplace letting out silk and traveling onwind currents usinghair-like Trichobothria that detects airborne vibrationscurrents and electrical charge Some have been found ashigh as 25mi (4 km) in the sky dispersing over hundreds ofkilometers Morley and Robert [65] found that the presenceof a weak natural vertical e-field elicited ballooningbehavior and takeoff in the spiders their mechano-sensoryhairs function as putative sensory receivers which areactivated by natural weak electric-fields in response toboth e-field and air-flow stimuli The researchers hypoth-esized that atmospheric electricity was key to the massmigration patterns of some arthropod fauna

Even soil nematodes (Caenorhabditis elegans) orient toearth-strength magnetic fields in their burrowing behav-iors and a recent study byVidal-Gadea [66] found thatweakstaticfields slightly above Earthrsquos naturalfields determinedstem cell regeneration in flatworms (Planaria) [67]

Large ruminant mammalian species also orient to theEarthrsquos fields Grazing cattle and deer were first observedaligning to geomagnetic field lines by Begall et al [68]Using satellite imagery field observations and measuringldquodeerbedsrdquo in snow they noted that domestic cattle acrossthe globe aswell as grazing and resting red (Cervus alphas)and roe (Capreolus capreolus) deer consistently align theirbody axis in a general northndashsouth direction and that roedeer also orient their heads northward when grazing orresting Burda et al [69] discovered however that man-made ELF-EMF disrupted the north-south alignment withthe geomagnetic field in resting cattle and roe deer whenthey found body orientation was random on pastures un-der or near power lines with the disturbed pattern dimin-ishing with distance from conductors Cattle exposed tovarious magnetic field patterns directly beneath or nearpower lines exhibited distinct patterns of alignment Theyconcluded there was evidence for magnetic sensation inlarge mammals as well as overt behavioral reactions toweak ELF-MF in vertebrates implying cellular and mo-lecular effects Slaby et al [70] also found cattle align alonga north-south axis but suggested that such alignment maydepend on herd density as the affect disappeared in herdswith higher numbers Fedrowitz [71] expanded this to

Levitt et al EMF and wildlife 5

include bovine sensitivity to other weak ELF-EMF frompowerlines but with observed effects due to combinedelectric and magnetic fields rather than the electric fieldexposure alone (see ldquoBovinesrdquobelow)

Cerveny et al [72] found red fox (Vulpes vulpes) usegeomagnetic fields during hunting Even domestic dogswere found by Hart et al [73] to be sensitive to small varia-tions in the Earthrsquos orientation in their excretion habitspreferring a general north-south axis for both defecation andurination depending on geomagnetic field changes AndNieszligner et al [74] found dogs and some other species mayactually ldquoseerdquo geomagneticfields through blue-light sensingphotoreceptor proteins in their eyes called cryptochromes

According to the USUK World Magnetic Model [75]sensitivity to the geomagnetic field may further complicateissues for migratory species (eg some turtles sea ani-mals birds and insects) because the Earthrsquos magneticnorth pole is shifting faster than at any time in humanhistory Compared to the period between 1900 and 1980 ithas greatly accelerated to about 30 mi (50 km) distance peryear mdash moving west from over Canadarsquos Ellesmere Islandits traditional allocation for most of recorded history mdashtoward Russia [76] Magnetic north fluctuates according tochanges in the Earthrsquosmolten core unlike true northwhichaligns according to the Earthrsquos axis This trend may indi-cate a coming pole reversal with north and south tradingplaces something that occurs approximately every400000 yearswith the last being about 780000 years agoSome animalsmaybe capable of recalibrating navigationalcues but that remains to be seen Since somemigratory birdspecies may see geomagnetic fields through special re-ceptor cells in their eyes and via other mechanisms theycould be thrown off course It is unclear how many otherspecies also see geomagnetic fields but some crustaceansand several insect species especially thosewith compoundeye structures consisting of thousands of ommatidiamdash tinyindependent photoreception units with a cornea lens andphotoreceptor cells that orient in different directions anddistinguish brightness and many more bands of color thanhumans mdash are good candidates Compared to single-aperture eyes compound eyes have a very large view anglethat can detect fast movement and in some cases lightpolarization

In aquatic environments some lakes have more than200 species of fish that use some form of electromagnetismto locate food and reproduce Electric eels can deliver a500-V zap to kill prey Sharks have an array of electro-magnetic sensors These include magnetic field receptorsin their mouths eyes that are 10 times more sensitive thanhumans and their perception of tiny electric neuronaldischarges from the moving muscles in prey (including

humans) guides their attackingfeeding behavior (seeldquoFishrdquobelow) Sharks are often attracted by low-levelelectromagnetic fields surrounding underwater electriccables and are sometimes electrocuted when they mistakethe conduit for living prey and bite into it Many fish havelateral lines on either side of their bodies that are composedof magnetite which allows fish to swim in synchronousschools [52]

Many other animals evolved special receptor organs todetect environmental EMF The duck-billed platypus(Ornithorhynchus anatinus) a semi-aquatic primitive egg-laying mammal has thousands of electric sensors on itsbill skin As noted in Lai [77] using these electroreceptorsand interacting with another type of mechanoreceptor aplatypus can detect an electric field of 20 μVcm [78] mdashequivalent to that produced by the muscles of a shrimpThe information is processed by the somatosensory cortexof the platypus to fix the location of prey This type ofelectroreception is common in the three species of mono-tremes platypus and long (Zaglossus bruijni) and short-bill (Tachyglossus aculeatus) echidna Electric fish (elas-mobranchs) emit EMF that covers a distance of severalcentimeters [79 80] This allows location of potential preyby comparing its electrical properties with that in its im-mediate vicinity Their electroreceptors have been shownto detect a field of 5 nVcm Such EMF-sensing systems arehighly sensitive and efficient but also highly vulnerable todisruption by unnatural fields Organisms that use thegeomagnetic field for migration have the capability notonly to detect the field but also the orientation of the field

Anthropogenic light frequencies affect wildlife in wayswe have only recently grasped Ecological studies havefound that artificial light-at-night is disrupting nocturnalanimals in devastating ways including disorientation anddisruption in breeding and migration cycles in turtlesflying insects birds butterflies and a host of other wildlifeincluding mammals [81ndash84] As much as 30 of nocturnalvertebrates and over 60 of invertebrates may be affectedby artificial light [85] Illumination reflected off of cloudsknown as ldquosky glowrdquo can produce unnaturally brightconditions at night from various wavelength spectra thatimpact different species with the potential to alter thebalance of species interactions [86 87] It has been foundthat changing the color of the light can help some speciesyet harm another [88] For instance low-pressure sodiumlights that havemore yellow in their spectrum reducemothdeaths around the bulbs but salamanders cannot navigatefrom one pond to the next under yellow or red light Somefrogs have been observed to freeze for hours even afterlights have been turned off and to suspend both feedingand reproduction [83]

6 Levitt et al EMF and wildlife

One of naturersquos greatmysteries involves ldquonatal homingbehaviorrdquo mdash the ability of some animal species to return totheir original location of birth in order to reproducesometimes over great distances Natal homing behavioris known in sea turtles [89] eels [90] and salmon [91]among other species The underlying mechanism thoughimperfectly understood involves such species ldquoremem-beringrdquo the geomagnetic field configurations of theirbirthplace via a process known as ldquoimprintingrdquo and thuscan locate and return to it even if they are thousands ofmileskilometers away at reproduction time Apparentlynewborns of these species are imprinted with the memoryof the intensity and the inclination angle of the localgeomagnetic field This information is then later used tolocate their place of birth where they return to breed

The question is whether man-made EMF could distortthis imprintingmemory in later locating the site For examplewhat if RFR-emitting facilities are locatednear turtle breedingsites Could that interfere with imprinting There is someevidence from Landler et al [92] of adverse effects in turtlesThe researchers found that RFR could disrupt a naturalorientation establish its own orientation and reversecompletely a natural orientation indicating a need forresearch to further investigate as we simply do not know thefull effects to other species from anthropogenic EMF

Energy conduction in differentspecies unique physiologies andmorphologies

The unique physiology and morphology of non-humanspecies create additional complexities For instancequadrapedal species with four feet on the ground havedifferent and potentially more efficient conductivity thanbipedal species with two feet One example is bovineheightened sensitivity to increased ground current nearhigh tension lines [93 94] and cell towers [95ndash97] Alsobodies that are predominately parallel to the groundwhich includes most four-legged mammals rather than aperpendicular upright gait conduct EMF in different waysthan vertical species like humans apes and other pri-mates Species that hug the ground like snakes sala-manders and frogs have unique exposures to groundcurrents especially on rainy nights when water as aconductivemedium can increase exposures [98] This maymake some species more sensitive to artificial groundcurrent caused by electric utility companies using the Earthas their neutral return back to the substation for excess

alternating current on their lines instead of running addi-tional neutral lines on utility poles [99]

Hair and whiskers and related appendages in variousspecies are known to detect small variations in electro-magnetic fields as well as water and weather alterations[100] In fact ants have been observed to use theirantennae as ldquoEMF antennasrdquo when subjected by re-searchers to external electromagnetic fields aligningthemselves to ldquochannelrdquo RFR away from the colony [7]Species such as birds as well as some insects with com-pound eyes structures can see vastly more colors thanhumans while cats dogs and owls for instance hearmany more sound frequencies at incredibly low levels

Magnetoreception mechanismselectroreceptor cells magnetitecryptochromesradical pairs

According to Lai [77] ldquohellipin order for an environmentalentity to affect the functions of an organism the followingcriteria have to be met the organism should be able todetect the entity the level of the entity should be similar tothose in the normal ambient environment which is gener-ally much lower than the level of the entity used inexperimental studies and the organism must haveresponse mechanisms tuned to certain parameters of theentity that allow immediate detection of the presence andchanges of the entity Thus a variation of the entity wouldbe detected as an aberrant input and trigger a responsereaction In order to understand how man-made EMF af-fects wildlife the above criteria must be consideredincluding multiple sensory mechanisms that vary fromspecies to speciesrdquo

The questions are How do diverse species detect weaknatural geomagnetic signals distinguish the subtle inter-nal microcurrent and magnetic fields inherent to allbiology from external fields then get beyond both internaland external background noise to make use of that elec-tromagnetic information

There are three primary mechanisms used to under-stand magnetoreception(1) Magnetic induction of weak electrical signals in

specialized sensory receptors [101](2) Magnetomechanical interactions with localized de-

posits of single-domain magnetite crystals [52 102103]

(3) Radical-pair photoreceptors which may be the mostplausible [104ndash111]

Levitt et al EMF and wildlife 7

In the induction model (mechanism 1) according to Lin[102] the first category of electrodynamic interactions withweak magnetic fields is epitomized by elasmobranchsincluding sharks rays and skates with heads that containlong jelly-filled canals with high electrical conductivityknown as the Ampullae of Lorenzini As these fish swimthrough the Earthrsquos geomagnetic lines of flux smallvoltage gradients are induced in these canals with electricfield detections as low as 05 μVm [101] The polarity of theinduced field in relation to the geomagnetic field providesdirectional cues for the fish However in birds insects andland-based animals such cells have not been foundindicating this may not be a universal mechanism butrather are environmentspecies-specific factors [111]

The magnetomechanical model (mechanism 2) in-volves the naturally occurring iron-based crystalline min-eral called magnetite found in most species [52] Itsfunction is most simply demonstrated in magnetotacticbacteria [63] with high iron content where biogenicmagnetite is manufactured in 20ndash30 single domain crystalchains [112] Orientation is patterned according to thegeomagnetic field Blakemore et al [113] found that mag-netotactic bacteria in the northern hemisphere migratetoward the north pole of the geomagnetic field whereas thesame strainsmigrate toward the South Pole in the southernhemisphere At the equator they are nearly equally dividedin north- and- south seeking orientations [114] And they allmigrate downward in response to the geomagnetic fieldrsquosvertical component which in aqueous environments maybe essential for their survival in bottom sediments

Among the many species where magnetite has beenfound include the cranium and neck muscles of pigeons[115 116] denticles of mollusks [117 118] and the abdom-inal area of bees [119] Tenforde [103] delineated otherspecies with localized magnetite including dolphinstuna salmon butterflies turtles mice and humans

The third mechanistic model (mechanism 3) gettingresearch attention today involves a complex free-radical-pair reaction and conversion of the forms of electrons(singlet-triplet inter-conversion) in a group of proteincompounds known as cryptochromes Cryptochromeshave been found in the retinas of nocturnal migratorysongbirds by Heyers et al [55] and Moller et al [56]showing complex communication with the brain fororientation when relying on magnetoreception Gegearet al [61] found cryptochromes to be a critical magneto-reception component in fruit flies (Drosophila mela-nogaster) As noted in Lai [77] cryptochrones are alsopresent in the retinas of some animals [120] RFR [121] andoscillating magnetic fields [122] have been reported todisrupt the migratory compass orientation in migratory

birds There are also reports that indicate the presence ofcryptochromes in plants which may be responsible for theeffect of EMF on plant growth [123] Cryptochromes are alsoknown to be involved with circadian rhythms [56 124] Foran excellent review on plausibility theories and com-plexities of cryptochromeradical pairs see Ritz et al [111]

Many species likely use a combination of thesemechanisms as well as more subtle influences as yet un-detected The vector of the geomagnetic field may providethe directional information while intensity andor incli-nation provide the positional information needed fororientation In behavioral studies [125 126]Wiltschko et alfound that birds used both magnetite and cryptochromemechanisms when they responded to a short strongmagnetic pulse capable of changing magnetization ofmagnetite particles while their orientation was light-dependent and easily disrupted by high-frequency mag-netic fields in the MHz range indicating radical pair pro-cesses These findings suggest that along withelectrophysiological and histological studies birds have aradical pair mechanism located in the right eye that pro-vides compass-like directional information while magne-tite in the upper beak senses magnetic intensity thusproviding positional information However Pakhomovet al [122] pointed out that the songbird magnetic compasscan be disrupted by an oscillating 1403-MHz magneticfield of 2ndash3 nT at a level that cannot be explained by theradical-pair mechanism

Light plays a significant role [127] which is of envi-ronmental concern today as more technology moves to-ward using the infrared bands for communications and theincrease of satellites create artificialunfamiliar star-likelights in the night sky that are potentially capable ofimpacting night migration patterns There is other evi-dence that species use a combination of photoreceptorsand magnetite-based magnetoreception As mentionedabove in birds the two mechanisms exist side by sidemediating different types of magnetic information asneeded such as flight on sunny vs cloudy days ornocturnal flights and they can be easily disrupted [106128ndash130] Birds may co-process visual information withmagnetic information and be able to distinguish betweenthe two [131 132] This function likely occurs in the eye orhigher avian brain areas via light-dependent informationprocessing and radical pair cryptochromes [131 133] Birdsrsquomagnetic compass is an inclination compass and RFRfields in the Larmor frequencies near 133 MHz were foundto disrupt birdsrsquo orientation in an extremely sensitiveresonance relationship Blue-light absorbing photopig-ment cryptochromes have been found in the retinas ofbirds RFR appears to directly interfere with the primary

8 Levitt et al EMF and wildlife

processes of magnetoreception and disable the aviancompass as long as the exposure is present [126 128]

Mammals have also demonstrated magnetoreceptionindicating radical-pair mechanisms Malkemper et al [134]found that the surface-dwelling wood mouse (Apodemussylvaticus) built nests in the northern and southern sectors ofa visually symmetrical circular arena using the ambientmagnetic field or in a field rotated by 90deg indicating theanimals usedmagnetic cuesWhen themicewere also testedin the ambient magnetic field with a superimposed radiofrequency magnetic field (100 nT 09 to 5 MHz frequencysweep) they changed preference from north-south to east-west nest building But unlike birds that have been foundsensitive to a constant Larmor frequency exposure at133 MHz that range had no effect on mice orientation In-dividual animal physiology clearly plays a role in howvarious species respondMalewski et al [135] also found thatthe Earthrsquos magnetic field acts as a common directional in-dicator in five species of subterranean digging rodents Andfor the first time research also found that human brainwaves exhibit a strong response to ecologically-relevant ro-tations of Earth-strength magnetic fields [136]

We need far better understanding of magneto-receptionrsquos neural cellular and molecular processesbecause the ultimate question is given our constant risingbackground levels of EMF is this ambient noise reaching atipping point beyond which species simply cannot ldquohearrdquoAre we artificially overwhelming living speciesrsquo ability tofunction with innate natural biological sensors thatevolved over eons in a far more ldquoelectro-silentrdquoworld Theelectroreception mechanisms described above mdash electro-receptors magnetite and cryptochroneradical-pairs mdashenable living organisms to detect the presence and imme-diate changes in environmental fields of very low intensityAnd thus they can be easily disturbed by the presence ofunfamiliar low-intensity man-made fields

Electrohypersensitivity in humans has also showninstantaneous response to EMF at low intensity [137] Ac-cording to Lai [77] one wonders whether the underlyingmechanisms of electrohypersensivity are similar to thosedescribed above Electrohypersensitivity may be a remnantof the evolutionary responses of living organisms to elec-tromagnetic fields mdash particularly magnetic fields mdash in theenvironment Similarities include responsiveness to verylow-field intensity the response is persistent and built intothe physiology of an organism and the response is imme-diate and reacts quickly to the fields Cryptochrome-freeradicalmechanismsmay be involved Some people aremoresensitive than others Perhaps non-sensitive people cantolerate and compensate for effects andor have lostresponsiveness to natural magnetic fields and thus have

becomeevolutionarily aberrant Electrosensitivity is an issuein need of more careful and systematic study and has yet tobe broadly highlightedas a health or publicwelfare concern

One recent theory by Johnsen et al [138] postulates thatmagnetoreception in animal species may be ldquonoisyrdquo mdashmeaning that the magnetic signal is small compared tothermal and other receptor noise for instance They specu-late that magnetoreception may serve as a redundant ldquoas-neededrdquo source of information otherwise animal specieswould use it as their primary source of information Manyspecies they note preferentially exploit non-magnetic cuesfirst if they are available despite the fact that the Earthrsquosgeomagnetic field is pervasive and ever-present Theyspeculate that magnetic receptors may thus be unable toinstantaneously attain highly precise magnetic informationand therefore more extensive time-averaging andor otherhigher-order neural processing of magnetic information isrequired This may render ldquohellipthe magnetic sense inefficientrelative to alternative cues that can be detected faster andwith less effortrdquo Magnetoreception may have been main-tained however they said by natural selection because thegeomagnetic field may sometimes be the only availablesource of directional andor positional information

We already know that some species use variousmechanisms to detect EMFs as noted throughout this pa-per With new environmental factors from anthropogeniccauses such as artificial light-at-night airwater pollutionclimate change impacting visibility as environmental cuesand rising background RFR mdash all of which can obscurenatural information mdash magnetoreception may in factbecomemore necessary as an evolutionary survival tool astime goes on not less

Other mechanisms of biologicalsignificance DNA mdash direct andindirect effects(See Part 2 Supplements 1 and 2for tables of ELF and RFR geneticsstudies)

A significant biological effect in any toxicology researchinvolves the basic genetics of an exposed organism Ge-netic effects consist mainly of gene expression chromatinconformational changes and genotoxicity All such effectscan influence normal physiological functions Relevant tothis paper is the fact that genetic effects are found at EMFlevels similar to those in ambient environments far below

Levitt et al EMF and wildlife 9

levels from communication devices and infrastructure (seePart 1 Supplement 1)

DNA the fundamental building block of all life is amolecular double helix that is coiled twisted and foldedwithin the nucleus of each living cell It is essentiallyidentical among species with variations only in numberand specific genes along chromosomes on DNArsquos twistedchains that distinguish various species and their charac-teristics from one another DNA damage repeatedly seen inone species can therefore be extrapolated to other speciesalthough not all species react the same to external stimuli

Many factors both endogenous and exogenousdamage DNA which is then normally repaired by DNAenzymes But an absence of adequate repair can result inthe accumulation of damaged DNA which will eventuallylead to aging cell death (apotosis) andor cancer DNAbreaks occur as both single and double strand eventsdouble strand breaks are difficult to repair correctly andcan lead to mutations DNA damage from endogenousfactors can include free radical formation from mitochon-drial respiration and metabolism exogenous factorsinclude chemicals ionizing and nonionizing radiationand ultra violet light among others [139]

In several early studies Lai and Singh [140 141] foundboth double and single strandDNAbreaks in the brain cellsof rats exposed to RFR for 2 h at 2450MHz andwhole bodySAR levels of 06 and 12 Wkg The effects were interest-ingly blocked by antioxidants [142] suggesting free radicalinvolvement which could indicate an indirect cause forDNA damage (see below) The low-intensity genetic effectslisted in Part 2 Supplements 1 and 2 are at 01 Wkg andless Therefore the Lai and Singh [140 141] RFR studies arenot included in those Supplements Very similar effectshave also been found by Lai and Singh [143 144] with60-Hz magnetic field exposure

There has also been much study of ELF genetic effectsAs discussed in Phillips et al [139] numerous studiesfound that ELF-EMF leads to DNA damage [143ndash158] Twostudies [159 160] showed that ELF also affects DNA repairmechanisms Sarimov et al [161] found chromatin confor-mational changes in human lymphocytes exposed to a50-Hz magnetic field at 5ndash20 microT EMF-induced changes incellular free radicals are also well studied [77 162]

Others investigated DNA damage early on but withoutthe availability of todayrsquos more sensitive assays Sarkaret al [163] exposed mice to 2450-MHz microwaves at apower density of 1 mWcm2 for 2 hday over 120 150 and200 days They found DNA rearrangement in the testis andbrain of exposed animals that suggested DNA strandbreakage Phillips et al [164] were the first to use the cometassay to study two different forms of cell phone signals mdash

multi-frequency time division multiple access (TDMA) andintegrated digital enhanced network (iDEN) mdash on DNAdamage in Molt-4 human lymphoblastoid cells usingrelatively low intensities of 24ndash26 Wg for 2ndash21 h Theauthors reported seeming conflicting increases and de-creases in DNA damage depending on the type of signalstudied as well as the intensity and duration of exposureThey speculated the fields could affect DNA repair mech-anisms in cells accounting for the conflicting results

In a recent literature review of EMF genetic effects byLai [165] analysis found more research papers reportingeffects than no effects For RFR 224 studies (65) showedgenetic effects while 122 publications (35) found no ef-fects For ELF and static-EMF studies 160 studies (77)found effectswhile in 43 studies (23) no effectswere seen

Research now points to the duration signaling charac-teristics and type of exposure as the determining factors inpotential damage [164 166] not the traditional demarcationbetween ionizing and nonionzing radiation Long-term low-level nonionizing radiation exposures common today arethought to be as detrimental to living cells as are short-termhigh-intensity exposures from ionizing radiation Effectsmay just take longer to manifest [167] Nonionizing EMF atenvironmental levels does cause genetic damage Thesehave also been shown in humans exposed to environmentallevels of EMF in both ELF and RFR ranges [168ndash171]Conceivably similar genetic effects could happen in otherspecies living in similar environments

This body of genetics work goes against the pervasivemyth that low-level low-intensity nonionizing radiationcannot cause detrimental genetic effects That premise is infact the bedrock belief upon which vested interests andgovernment agencies rely in support of current exposurestandards But in fact biological systems are far morecomplex than physics models can ever predict [6 8 172] Anew biological model is needed because todayrsquos exposuresno longer fit that framework [173] for humans and wildlifeEnough research now indicates a reassessment is neededperhaps including the very physics model used to backthose traditional approaches (see Part 1)

Direct mechanisms DNA as fractalantennas cell membranes ionchannels

DNA as fractal antennas

There are several likely mechanisms for DNA damage fromnonionizing radiation far below heating thresholds both

10 Levitt et al EMF and wildlife

direct and indirect intracellular intercellular and extra-cellular Suchmechanisms potentially apply to all wildlifeOne direct mechanism theorizes that DNA itself acts as afractal antenna for EMFRFR [174] capable of receivinginformation from exogenous exposures

According to Blank and Goodman [174] DNA hasinteresting electrical characteristics due to its uniquestructure of intertwined strands connected by rungs ofmolecules called nucleotides (also called bases) with eachrung composed of two nucleotides (one from each strand)in bonded pairs The nucleotides are held together byhydrogen bonds in close proximity that results in a strongattraction between the two strands There are electrons onboth molecular surfaces making the symmetrical nucleo-tides capable of conducting electron current along theentire DNA chain a phenomenon called electron transferThis makes DNA a most efficient electrical conductorsomething not lost on nanotechnology researchers

DNAmay also act as an efficient fractal antenna due toits tightly packed shape within the cell nucleus Blank andGoodman [174] characterized DNA properties in differentfrequency ranges and considered electronic conductionwithin DNArsquos compact construction in the nucleus Theyconcluded that the wide frequency range of observed in-teractions seen with EMF is the functional characteristic ofa fractal antenna and that DNA itself possesses the twostructural characteristics of fractal antennas mdash electronicconduction and self symmetry They noted that theseproperties contribute to greater reactivity of DNAwith EMFin the environment and that direct DNA damage couldaccount for cancer increases as well as the many otherbiological effects seen with EMF exposures

A fractal is a self-repetitive pattern of sometimes geo-metric shapes marked by a larger originating design pro-gressing to small identical designs with a potentiallyunlimited periphery Each part of the shape looks like thewhole shape Fractal designs are quite common in natureeg in snailmollusk shells some deciduous tree leaves andconifer needles pine cones many flowering plants somereptile scales bird feathers and animal fur patterns snow-flakes and crystals forming on cold winter glass windowsMineralsmdash both inert and biologicalmdash can also be fractals

The varying sizes within fractals are what make theminherently multi-frequency By mimicking nature repeti-tive fractal patterns are also designed into mechanicaltransceiver antennas that radiate in multiband frequencieswith more or less efficiency [175] Cell phones WiFi digitalTV and many other transceivers use fractal antennas tooperate

The complex twisted shape and coiled structure ofDNA mdash small coils coiled into larger coils or coiled coils

which Blank and Goodman [174] note that no matter howfar you zoom in or out the shape looks the same mdash is theexact structure of a fractal that maximizes the length of anantenna within a compact space while boosting multi-frequency signals As such DNAmay be acting as a hiddenintracellular biological fractal capable of interacting withexogenous EMF across a range of frequencies In fact oneof DNArsquos fundamental functions may be specifically tointeract with exogenous natural energy and as suchmay bemore sensitive to EMF than other larger protein moleculeswithin any living system Once thought safely tucked awayand protected within the nucleus DNA may be acting as amost efficient electrical conductor at the nexus of all lifeThis interesting theory unfortunately has not been fol-lowed up by others to test its biological validity althoughfractals have been mimicked widely in technology

Cell membranesion channels

Another direct effect from EMF is at the cell membraneitself While DNA is lifersquos fundamental building block cellsare DNArsquos complex electron-coherent architecturalexpression The cellrsquos membrane is far more than just aboundary It is rather the most important ordering tool inthe biological space between intracellular and extracel-lular activities ldquohellip a window through which a unitarybiological element can sense its chemical and electricalenvironmentrdquo [176] And it is replete with microcurrent

The cellrsquos outer surface containsmolecules that receiveinnumerable electrochemical signals from extracellularactivities Specific binding portals on the cell membraneset in motion a sequence leading to phosphorylation ofspecific enzymes that activate proteins for cellular lsquoworkrsquoThat includes everything from information processing inthe central nervous system mechanical functions such asmuscle movements nutrient metabolism and the defensework of the immune system amongmany others includingthe production of enzymes hormones antibodies andneurotransmitters [177] Complex microcurrent signalingpathways exist from the cellrsquos outside to the inside viaprotein intramembraneous particles in the phospholipidplasma membrane These convey information on externalstimuli to the cellrsquos interior to allow cellular function

The cell membrane also has electrical propertiesMicrocurrent constantly moves from the interior to theexterior and vice versa of the cell membrane According toAdey and Sheppard [176] some of these properties influ-ence proteins that form voltage gatedmembrane channelswhich is one way that cells control ion flow andmembraneelectromagnetic potential essential to life There are

Levitt et al EMF and wildlife 11

specific windows that react according to frequencyamplitude and duration differences indicating anonlinear and non-equilibrium character to exogenousexposures on cells [177ndash185]

Some pulsed fields are more biologically active thannon-pulsed fields and different forms of pulsing also createdifferent effects As far back as 1983 Goodman et al [186]found pulsed weak electromagnetic fields modified bio-logical processes via DNA transcription when a repetitivesingle pulse and the repetitive pulse train were used Thesingle pulse increased the specific activity of messengerRNA after 15 and 45 min while the pulse train increasedspecific activity only after 45 min of exposure Digitaltechnology simulates pulsing and is the most commonform of environmental exposure today

Cellular calcium ion channels have long been of in-terest and may be particularly sensitive targets for EMFsdue to possible increased calcium flux through the chan-nels which can lead to secondary responses mediatedthrough Ca2+calmodulin stimulation of nitric oxide syn-thesis calcium signaling elevated nitric oxide (NO) NOsignaling peroxynitrite free radical formation andoxidative stress mdash many with implications to DNA as hy-pothesized by Pall [187] Calcium is essential to signaltransduction between cells and is significant to everythingfrom metabolism bonecellblood regeneration hormoneproduction and neurotransmissions among many othersThese cellular calcium responses to EMF indicate an arti-ficial change in the signaling processes at the cell mem-branemdash considered a switchboard for information betweenthe exterior environment and intracellular activities thatguide cell differentiation and control growth [188]

Pall [187] cited 23 studies of effects to voltage gatedcalcium channels (VGCC) and noted nonthermal mecha-nisms were the most likely since many studies showed ef-fects were blocked by calcium channel blockers (widelyprescribed for heart irregularities having nothing to dowith thermal issues) Pall [189] noted that many otherstudies showed EMF changes in calcium fluxes and intra-cellular calcium signaling He hypothesized that alter-ations in intracellular calciumactivitymay explain some ofthe myriad biological effects seen with EMF exposureincluding oxidative stress DNA breaks some cancersinfertility hormonal alterations cardiac irregularities anddiverse neuropsychiatric effects These end points needfurther study and verification

There is much to be learned about calcium effects asstudies are contradictory Changes in free radicals (seebelow) also affect calcium metabolism There are morestudies showing EMF effects on free radicals than calciumchanges Calcium activates the nitric oxide free radical

pathway but there are only a few studies of this pathwayfollowing EMF exposure mdash less than 5 of EMF-oxidativechange studies are on nitric oxide mechanisms Also ofinterest is the fact that power density and frequency win-dows were seen in early research at rising harmonic in-crements along the electromagnetic spectrum beginning inthe ELF bands [190ndash195] Observed effects were quite dra-matic in what researchers described as calcium efflux orlsquodumpingrsquo from cells The most dramatic effects were seenat 180 Hz in the ELF range This appears to contradict Pallrsquoswork [189] cited above as increased calcium efflux is theopposite of what Pallrsquos hypothesis would predict egcalcium influx Withmore research both calcium influx andefflux effects may be found to be caused by different vari-ables andor EMF exposures

In addition exogenous signaling characteristics arealso important to how cells react to both ELF and RFRranges Building on the work that demonstrated carrierwaves of 50 and 147 MHz when sinusoidally amplitudemodulated at 16 Hz ELF in in vitro chick brain tissue [190191] and in live awake cat brain models [196] that createdfrequency windows for calcium efflux Blackman et al[194] additionally found that signaling characteristicswerealso significant Research showed that calcium effluxoccurred only when tissue samples are exposed to specificintensity ranges of an ELF-modulated carrier wave un-modulated carrier waves did not affect ion efflux Black-man et al [194] further wrote that cells may be capable ofdemodulating signals The authors reported that 16-Hz si-nusoidal fields in the absence of a carrier wave altered theefflux rate of calcium ions and showed a frequency-dependent field-induced enhancement of calcium-ionefflux within the ranges 5ndash75 Vm and 35ndash50 Vm (peak-to-peak incident field in air) with no enhancement withinthe ranges 1ndash2 10ndash30 and 60ndash70 Vm This body of workindicates that living cells interact with and are capable oftaking direction from exogenous fields in far more com-plex ways than ever imagined at intensities barely abovebackground levels This work may be particularly impor-tant to new technology that turns previously wired ELFfrequencies into wireless applications such as ldquowirelesselectricityrdquo to charge electric cars

Blackman et al [197] found for the first time a linkbetween the ELFEMF being studied and the density of thenatural local geomagnetic field (LGF) in the production of abiological response Calcium efflux changes could bemanipulated by controlling the LGF along with ELF andRF-EMF exposures In a local geomagnetic field at a densityof 38 μT 15- and 45-Hz electromagnetic signals had beenshown to induce calcium ion efflux from the exposed tis-sues whereas 1- and- 30-Hz signals did not Bawin and

12 Levitt et al EMF and wildlife

Adey [190] found a reduction in efflux when using anelectric field Blackman et al [194] found an increase whenusing an electromagnetic field thus identifyingisolatingfor the first time the significance of the magnetic fieldcomponent in exposure parameters Building on the win-dow ranges noted above Blackman et al [197] demon-strated that the enhanced calcium efflux field-induced15-Hz signal could be rendered ineffective when the LGF isreduced to 19 μT with Helmholtz coils In addition theineffective 30-Hz signal became effective when the LGFwas altered to k253 μT or to +76 μT The results demon-strated that the net intensity of the local geomagnetic field isan important cofactor in biological response and a poten-tially hidden variable in research The results they notedappear to describe a resonance-like relationship in whichthe frequency of the electromagnetic field can induce achange in calcium efflux proportional to LGF density (seeLiboff [198 199] below for more detail)

The bottom line is that changes of this magnitude atthe cellular levelmdash be it directly to DNAwithin the nucleusor via voltage gated channels at the cellrsquos membranemdash canlead to direct effects on DNAwithin and across species Theevidence cited above illustrates the degree likelihood andvariety of impacts from EMF directly on cellular physiologythat are capable of affecting DNA in all living systems inmyriad ways

Indirect mechanisms free radicalsstress proteins resonance Earthrsquosgeomagnetic fields

Free radicals

An indirect or secondary mechanism for DNA damagewouldbe through free radical formationwithin cellswhich isthe most consistently reported with both ELF and RFR ex-posures under many different conditions in biological sys-tems According to Phillips et al [139] free radicals may alsointeractwithmetals like iron [142 151 152 158] andplay a rolein genotoxic effects from something called the Fenton ef-fect mdash a process ldquohellipcatalyzed by iron in which hydrogenperoxide a product of oxidative respiration in the mito-chondria is converted into hydroxyl free radicals which arevery potent and cytotoxic moleculesrdquo [139]

The significance of free radical processes may even-tually answer some questions regarding how EMF interactswith biological systems There are about 200ndash300 papersshowing EMF effects on free radicals [77 168 200] Free

radicals are important compounds involved in numerousbiological functions that affect many species Increases infree radicals explain effects from damage to macromole-cules such as DNA protein and membrane lipidsincreased heat shock proteins neurodegenerative dis-eases and many more

Yakymenko et al [168] published a review on oxidativestress from low-level RFR and found induced molecular ef-fects in living cells including significant activation of keypathways generating reactive oxygen species (ROS) activa-tion of peroxidation oxidative damage in DNA and changesin the activity of antioxidant enzymes In 100 peer-reviewedstudies 93 confirmed that RFR induced oxidative effects inbiological systems and that their involvement in cellsignaling pathways could explain a high pathogenic rangeof biologicalhealth effects They concluded that low-intensity RFR should be recognized as one of the primarymechanisms of biological activity of nonionizing radiationIn a follow-up study Yakymenko et al [200] investigatedthe oxidative and mutagenic effects of low intensity GSM1800 MHz RFR on developing quail embryos exposed inovo (032 μWcm2 48 s On 12 s Off) during 5 days before and14 days through the incubation period They found statisti-cally significant oxidative effects in embryonic cells thatincluded a 2-fold increase in superoxide generation rate an85 increase in nitrogen oxide generation and oxidativedamage to DNA up to twice the increased levels of 8-oxo-dGin cells of 1-day old chicks RFR exposure almost doubledembryo mortality and was statistically significant Theyconcluded that such exposures should be recognized as arisk factor for living cells including embryonic integrity

Lai [77] focused a review on static magnetic fieldELF-EMF and found that changes in free radical activitiesare one of the most consistent effects Such changes canaffect numerous physiological functions including DNAdamage immune system and inflammatory response cellproliferation and differentiation wound healing neuralelectrical activities and behavior Given that many specieshave proven sensitive to natural static geomagnetic fieldsand use such information in critical survival skills somewildlife species may also be adversely affected via freeradical alterations from anthropogenic exposures But Lai[77] noted the inherent contradictions from EMF-inducedchanges in free radicals particularly on cell proliferationand differentiation since those processes can affect cancerdevelopment as well as growth and development Inducedfree-radical changes may therefore have therapeutic ap-plications in killing cancer cells via the generation of thehighly cytotoxic hydroxyl free radical by the Fenton Re-action (noted above) thereby creating a non-invasive low-side-effect cancer therapy

Levitt et al EMF and wildlife 13

Stress proteins

Another potentially indirect effect to DNA is via proteinsynthesis required by all cells to function A living animalconverts animal and plant proteins that it ingests into otherproteins needed for lifersquos activities mdash antibodies forinstance are a self-manufactured protein DNA is critical toprotein synthesis and can create in humans about 25000different kinds of proteins with which the body can thencreate 2000000 types in order to fully function

There are many different classes of proteins Theseinclude stress proteins stimulated by potentially harmfulenvironmental factors to help cells cope and repair damagedue to factors like acute temperatures changes in oxygenlevels chemicalsheavy metals exposure viralbacterialinfections ultraviolet light and other ionizing andnonionizing radiation exposures [124]

The presence of stress proteins indicates healthy repairaction by an organism and is considered beneficial up to apoint as a protective mechanism According to Blank andGoodman [201] ldquoThe 20 different stress protein families areevolutionarily conserved and act as lsquochaperonesrsquo in the cellwhen they lsquohelprsquo repair and refold damaged proteins andtransport them across cell membranes Induction of thestress response involves activation of DNArdquo Stress proteinsare also considered a yardstick to determine what livingcells experience as stress that requires remediation in thefirst placemdash something not always obvious especiallywithsubtle environmental exposures like low-level EMF barelyabove natural background levels

Whether an effect is thermal or nonthermal adverse orsimply observed biologically has been subject to fiercedebate for decades thus tissue-heating DNA pathways arealso central to this paper Heat as a cellular stressor wasfirst observed in the 1960s by Italian researcher FerruccioRitossa in fruit flies (D melanogaster) when experimentaltemperatures were accidentally raised by a few degreesand he observed enlarged chromosomes at particular sites(Drosophilae are often used in research because they onlyhave four pairs of chromosomes are relatively easy toworkwith have a fast breeding cycle and lay numerous eggs)As cited in Blank [124] as Ritossarsquos observation becamebetter understood with effects subsequently seen overdecades in animals plants and yeast cells it came to becalled the ldquoheat shock responserdquo Extensive researchestablished that the heat shock response lead to the for-mation of a unique protein class mdash heat shock proteins(HSP) that repair other proteins from potentially fataltemperature damage as well as assist cells to be morethermo-tolerant Research has gone on to prove that cells

produce other similar proteins to various stressors nowgenerally called stress proteins but most are still catego-rized as ldquoHSPrdquo from the original demarcation

Goodman and Blank [202 203] found that EMF is acellular stressor even at low intensities in the absence ofelevated temperatures They found the protein distributionpatterns synthesized in response to ELF-EMF resembledthose of heat shock with the same sequence of changes eventhough the energy of the two stimuli differed bymany ordersof magnitude Their results indicated that ELF-EMF stimu-lates a similar gene expression pathway as that of thermalshock and is itself a cellular stressor Of particular signifi-cance is the fact that over-expression of stress genes is foundin a number of human tumors and is characteristic of a va-riety of neoplasia [202] Increased stress proteins are seen innumerous animal model studies pertinent to wildlife

Blank and Goodman [201] further noted that both ELFand RFR activate the cellular stress response despite thelarge energy difference between them that the samecellular pathways respond in both frequency ranges andthat models suggest that EMF can interact directly withelectrons in DNA They note that low energy EMF interactswith DNA to induce the stress response while the increasedenergy in RFR can lead to DNA strand breaks As such thismakes the stress response a frequency-dependent direct andindirect cause of DNA damage mdash a significant finding Theyconcluded that exposure standards should not be based onexposure intensity alone but on biological responses longbefore thermal thresholds are met or crossed

Resonance and geomagnetic fields

There are other important direct and indirect ways that EMFsinteractwith and effect biological systems includingvariousforms of resonance mdash cyclotron electron paramagneticnuclear and stochastic mdash as well as through inherentlyproduced biological materials such as magnetite found inbird brains and many other species (see below)

Resonance is the phenomenon that occurs when acertain aspect of a force (like a frequency wave) matches aphysical characteristic (like a cell or whole living organ-ism) and the power inherent in the force is transferred tothe physical object causing it to resonate or vibrate Withinthe object the resonance is self-perpetuating The classicexample is of an opera singer hitting high C in the presenceof a crystal goblet for a sustained period until it shatters

Following the work of Blackman et al [197] who foundthe Earthrsquos local geomagnetic fields (LGF) could influencecalcium ions moving through membrane channels (see

14 Levitt et al EMF and wildlife

above) Liboff [198 199] proposed that cyclotron resonancewas a plausible mechanism for coupling interactions be-tween the LGM and living cells Liboff found cyclotronresonance consistent with other indications that showedmany membrane channels have helical configurationsthat the model could apply to other circulating chargedcomponents within the cell and that cyclotron resonancecould lead to direct resonant electromagnetic energytransfer to selected cell compartments

All resonance is based on a relationship Cyclotron reso-nance is based on the relationship between a constant mag-netic field and an oscillating (time-varying) electric ormagnetic field that can affect the motion of charged particlessuch as ions some molecules electrons atomic nuclei orDNA in living tissue Living systems are filled with chargedparticles necessary for life including calcium sodiumlithium and potassium ions that all pass through the cellmembrane and are capable of affecting DNA Cyclotronresonance occurs when an ion is exposed to a steady mag-netic field (such as the Earthrsquos) which causes the ion to movein a circular orbit at a right angle to the field The speed of theorbit is determined by the charge andmass of the ion and thestrength of themagnetic field If an electric field is added thatoscillates at exactly the same frequency and that is also at aright angle to the magnetic field energy will be transferredfrom the electric field to the ion causing it tomove faster Thesame effect can be created by applying an additional mag-netic field parallel to the constant magnetic field This isimportant because it provides aplausiblemechanism forhowliving cells interact with both natural and artificial fields andexplainshowvanishingly low levels of EMFs cancreatemajorbiological activity when concentrated on ion particles It alsopoints to living systemsrsquo ability to demodulate mdash or take di-rection frommdash certain aspects of electromagnetic informationfrom both natural and artificial exposures [7] Resonanceshould not be underestimated It applies to all frequenciesand is not based on power density alone

Another subtle energy relationship in biology is calledstochastic resonance that has been determined to be sig-nificant in how various species interact with their naturalenvironments in some instances for their survival Sto-chastic resonance is a phenomenon where a signal belownormal sensing can be boosted by adding wide-spectrumwhite noise signals The frequencies in the white noise thatmatch the original signalrsquos frequencies will resonate witheach other and amplify the original signal while notamplifying the rest of thewhite noise This increase inwhatis called the signal-to-noise ratio makes the original signalmore prominent Some fish for instance can ldquohearrdquopredators better in the noise of running water than in stillwater due to stochastic resonance (see ldquoFishrdquo below)

The signal-to-noise ratio has been a prominent aspectof EMF research with some scientists long holding thatenergy exposures below the bodyrsquos natural signal-to-noiseratio could not possibly damage living tissue But the mostrecent research that finds effects to DNA from lowintensity EMF indicates that many variables affect biolog-ical processes often in nonlinear patterns far below thesignal-to-noise ratio Some of the most cutting edgeresearch mdash with an eye toward treating human in uterobirth defects and adult limb regeneration mdash is being donebymanipulating the electric charge across cell membranes(called membrane potential) via intentional manipulationof genes that form ion channels Pai et al [204] found thatby putting ion channels into cells to raise the voltage up ordown they could control the size and location of the brainin embryonic African clawed frogs (Xenopus laevis) thusdemonstrating the importance of microcurrents on mem-brane potential in growth and development The researchgroup also studied endogenous bioelectricity on clawedfrog brain patterning during embryogenesis noting thatearly frog embryos exhibit a characteristic hyperpolar-ization of cells lining the neural tube Disruption of thisspatial gradient of the transmembrane potential (Vmem)diminished or eliminated the expression of early brainmarkers in frogs causing anatomical mispatterningincluding absent or malformed regions of the brain Thiseffect was mediated by voltage-gated calcium signalingand gap-junctional communication The authors hypoth-esized that voltage modulation is a tractable strategy forintervention in certain classes of birth defects in humansbut they did not make the leap to potential environmentaldamage to other species from such ambient exposures

In general whether direct indirect or synergistic tounderstand ambient effects to wildlife one also needs toknow if effects are cumulative what compensatorymechanisms a species may have and when or if homeo-stasis will deteriorate to the point of no return [205] Inlooking at environmental contaminants we have histor-ically focused on chemicals for both direct and indirecteffects such as endocrine disruption But primary bio-logical manifestation is more physical than chemicalsince the only thing that distinguishes one chemical fromanother on the Periodic Table is the amount of electronsbeing traded up and down on the scale Chemicals areactually secondary manifestations of initial atomic prin-ciples not the other way around Plus the synergisticeffects of the Earthrsquos natural fields can no longer be dis-missed as an interesting artifact that is not biologicallyactive or relevant All living systems are first and foremostexpressions of biological energy in various states ofrelationship

Levitt et al EMF and wildlife 15

For a Table of more low-level effects studies on DNAsee Part 2 Supplements 1 and 2

What the studies show

The literature is voluminous on EMF effects to nonhumanspecies goingbackat least to the1930susingmodernmethodsof inquiry We have after all been using animal plant andmicrobial models in experiments for decades We may in factknow less about effects to humans than to other species

In this paper we focused on exposures common intodayrsquos environment In Part 1 Rising Background Levelswe defined low level RFR as power density of 0001 mWcm2 (1 μWcm2) or a SAR of 0001 Wkg Part 2 Supple-ments 3 and 4 contain extensive tables with pertinentstudies that apply to fauna and flora respectively Thesections that follow in Part 2 on individual species includeselected studies of particular interest to how EMF coupleswith and potentially affects wildlife In most studies asillustrated in Part 2 Supplement 3 the intensity of theincident EMF was provided in μWcm2 or Vm To beconsistent throughout the paper we converted intensity inthe studies to μWcm2 However such conversion (ie Vmto μWcm2) tends to overestimate the exposure level anddoes not represent the full picture Therefore where studiesprovided the amount of energy absorbed eg the specificabsorption rate (SAR) they were also included in Supple-ment 3 (inWkg) Very low levels of energy absorption haveshown effects in all living organisms studied

Levitt and Lai [167] reported numerous biological ef-fects fromRFR at very low intensities and SARs comparableto far-field exposures within 197ndash492 ft (60ndash150 m) fromcell towers Included were in vivo and in vitro low-intensityRFR studies Effects included genetic growth and repro-ductive changes increased permeability of the blood brainbarrier changes in stress proteins behavioral responsesand molecular cellular genetic and metabolic alter-ations All are applicable to migratory birds mammalsreptiles and other wildlife and to plant communities andto far-field exposures in general (An update of that tableappears in Part 2 Supplement 3) It is apparent that envi-ronmental levels of RFR can elicit biologicalhealth effectsin living organisms Although there are not enough data onlow-intensity effects of static ELF-EMF to formulate aseparate table some effects of low-intensity static ELF-EMFare also described throughout this paper ELF genotoxiceffects can be found in Part 2 Supplement 2 and ELF inflora are also listed separately in Part 2 Supplement 4

Effects however do not easily translate from the lab-oratory to the field Cucurachi et al [31] reported on 113

studies with a limited number of ecological studies Themajority were conducted in laboratory settings using birdembryos or eggs small rodents and plants In 65 of thestudies effects from EMF (50 of the animal studies andabout 75 of the plant studies) were found at both highand low intensities indicating broad potential effectsBut lack of standardization among the studies and limitedsampling size made generalizing results from organism toecosystem difficult The researchers concluded that due tothe number of variables no clear dosendashresponse relation-ship could be determined Nevertheless effects from somestudies were well documented and can serve as predictorsfor effects to wild migratory birds and other wildlife

As noted elsewhere throughout this paper living or-ganisms can sense and react to very low-intensity electro-magnetic fields necessary for their survival as seen forinstance in studies by Nicholls and Racey [206 207] onbats andmany others Bats are already in serious trouble inNorth America from white-nosed syndrome and commer-cial wind turbine blade collisions Due to the increased useof tracking radars for bird and bat studies impacts willlikely only increase [22 23] Presence of low levels of RFRfrom tracking radars could adversely affect bat foragingactivity which in turn could affect the composition of in-sect populations in the vicinity Many insects includinghoney bees (Apis mellifera var) and butterflies also dependon the Earthrsquos electromagnetic fields for orientation andforaging Presence of exogenous RFR can disturb thesefunctions This is particularly relevant for pollinator in-sects such as bees and butterflies Pollinators are essentialin producing commercial crops for human consumptionincluding almonds apples pears cherries numerousberry crops citrus fruits melons tomatoes sunflowerssoybeans and much more The strongest disruptive effectto insect pollinators occurs at 12 MHz known as the Larmorfrequency [208] which is related to radical pair resonanceand superoxide radical formation This is an importantindication that effects from RFR are frequency-dependent

Lai [77] citing Shepherd et al [209] noted that EMFcan disrupt the directional sense in insects The fact thatmany animals are able to differentiate the north and southpoles of a magnetic field known as the polarity compass[68 73 134 210 211] indicates they are susceptible tohaving that important sense impaired These polaritycompass traits confer survival competitiveness to organ-isms but are of particular concern since directional cuescan be easily disturbed by man-made EMF [69 134 212]

Bird migration also depends on proper sensing andorientation to natural electromagnetic fields A study byEngels et al [213] showed that magnetic noise at 2 kHzndash9 MHz (within the range of AM radio transmission) could

16 Levitt et al EMF and wildlife

disrupt magnetic compass orientation in migratory Euro-pean Robins (Erithacus rubecula) The disruption can occurat a vanishingly low levelof001Vm or00000265μWcm2Similar effects of RFR interference on magnetoreceptionhave also been reported in a night-migratory songbird [214]and the European Robin [126] Migration is already a taxingand dangerous activity for birds adding another potentialnegative impact to bird survival is troubling

Lai [77] also noted that another consideration is theldquonatal homing behaviorrdquo exhibited in some animals thatreturn to their natal birth places to reproduce Theseinclude sea turtles [89] eels [90] and salmon [91] New-borns of these animals are imprinted with the memory ofthe intensity and the inclination angle of the localgeomagnetic field later used to locate their place of birthwhen they return to breed There are indications that man-made EMF can distort this imprinting memory to locate thesite (see ldquoFishrdquo and ldquoTurtlesrdquobelow) This has importantconsequences to the survival of particular species since itinterrupts their reproductive processes

It is clear that biological effects can occur at levels ofman-made RFR in our present environment therebyconceivably altering delicate ecosystems from a largelyunrecognized danger

Mammals

The majority of EMF laboratory research some going backto the 1800s has been conducted on a variety of mammalspecies using mice rats rabbits monkeys pigs dogs andothers (The second and third most used models are oninsects and yeast respectively) Thus with varying degreesof confidence we know a significant amount about howenergy couples with and affects laboratory mammalianspecies across a range of frequencies However this evi-dence does not automatically transfer at the same confi-dence level regarding how this vast body of researchapplies to wildlife including mammalian species

There is unfortunately a dearth of field research onEMF effects to wildlife Referenced below however aremany potential indicator studies The effects seen includereproductive behavioral mating growth hormonalcellular and others

Rodents

Rodents are the most frequently used mammalian speciesin laboratory research across a range of frequencies andintensities While studies are inconsistent there are

enough troubling indications regarding potential EMFimplications for wildlife

In the RFR range there have been several reviews offertility and other issues in rodentmodelswith citations toonumerous to mention heremdash see La Vignera e al [215] andMerhi [216]mdash but some stand out as potentially pertinent towildlife

Magras and Xenos [217] investigated effects of RFR onprenatal development in mice using RFR measurementsand in vivo experiments at several locations near an an-tenna park with measured RFR power densities between0168 and 1053 μWcm2 Divided into two groups were 12pairs of mice placed in locations of different power den-sities and mated five times One hundred eighteen new-borns were collected measured weighed and examinedmacro- and microscopically With each generation re-searchers found a progressive decrease in the number ofnewborns per dam ending in irreversible infertility How-ever the crown-rump length body weight and number oflumbar sacral and coccygeal vertebrae was improved inprenatal development of some newborns RFR was belowexposure standards and comparable to far-field exposuresthat mice could experience in the wild

Aldad et al [218] in a laboratory setting investigatedcell phoneRFR (800ndash1900MHzSARof 16Wkg) exposuresin in-uteromouse models and effects on neurodevelopmentandbehavior They foundsignificant adult behavioral effectsin prenatally exposed mice vs controls Mice exposed in-uterowere hyperactive had decreasedmemory and anxietyand alteredneuronal developmental programming Exposedmice had dose-response impaired glutamatergic synaptictransmission onto layer V pyramidal neurons of the pre-frontal cortex This was the first evidence of neuropathologyinmice from in-utero RFR at cell phone frequencies now themost prevalent in the environment Effects persisted intoadulthood and were transmissible to next generations Suchchanges can affect survival in wild populations

Meral et al [219] looked at effects in guinea pigs (Caviaparcels) from 900 MHz cell phone frequency exposures onbrain tissue and blood malondialdehyde (MDA) gluta-thione (GSH) retinol (vitamin A) vitamin D(3) andtocopherol (vitamin E) levels as well as catalase (CAT)enzyme activity Fourteenmale guinea pigs were randomlydivided into control and RFR-exposed groups containingseven animals each Animals were exposed to 890- to-915MHz RFR (217 Hz pulse rate 2Wmaximumpeak powerSAR 095 Wkg) from a cellular phone for 12 hday (11 h45 min stand-by and 15 min spiking mode) for 30 daysControls were housed in a separate room without cellphone radiation Blood samples were collected throughcardiac puncture biochemical analysis of brain tissue was

Levitt et al EMF and wildlife 17

done after decapitation at the end of the 30-day periodResults found MDA levels increased (plt005) and GSHlevels and CAT enzyme activity decreased while vitaminsA E and D(3) levels did not change significantly in thebrain tissue of exposed animals In blood samples of theexposed group MDA vitamins A D(3) and E levels andCAT enzyme activity increased (plt005) while GSH levelsdecreased (plt005) They concluded that cell phone radi-ation could cause oxidative stress in brain tissue of guineapigs but more studies were needed to determine if effectsare harmful andor affect neural functions

Lai et al [220] found that Sprague-Dawley rats exposedto RFR during water maze testing showed spatial workingmemory deficits compared to controls But similar studies[221ndash223] did notfindperformance effects in spatial tasks oralterations in brain development after similar exposuresHowever subsequent studies in the last two decades haveshown memory and learning effects in animals andhumans after RFR exposure [224]

Several studies also investigated RFR behavioral effectsin rodent models on learning memory mood disturbancesand anxiety behaviors with contradictory results Danielset al [225] found decreased locomotor activity increasedgrooming and increased basal corticosterone levels in ratsexposed to RFR for 3 h per day at 840MHz but no significantdifferences were seen between controls and test animals inspatial memory testing or morphological brain assessmentThe researchers concluded that RFR exposure may lead toabnormal brain functioning

Lee et al [226 227] looked specifically at effects onpregnant mice and rat testicular function from combinedRFR mobile network signal characteristics used in wide-band code division multiple access (W-CDMA) or CDMAused in 3G mobile communications Experiments showedno observable adverse effects on development reproduc-tion or mutation in tested subjects And no significant ef-fects were seen by Poulletier de Gannes et al [228] in in-utero and post-natal development of rats with wireless fi-delity (WiFi) at 2450 MHz Also Imai et al [229] found notesticular toxicity from 195 GHz W-CDMA

Oneextremelyhigh frequency (EHF) study comparable to5G on a mouse model by Kolomytseva et al [230] looked atleukocyte numbers and the functional activity of peripheralblood neutrophils In healthy mice under whole-body expo-sures to low-intensity extremely-high-frequency electromag-netic radiation (EHF 420 GHz 015 mWcm2 20 min daily)found that the phagocytic activity of peripheral blood neu-trophils was suppressed by about 50 (plt001 as comparedwith the sham-exposed control) in 2ndash3 h after the singleexposure Effects persisted for 1 day and thereafter returned tonormal within 3 days But a significant modification of the

leukocyte blood profile was observed inmice exposed to EHFfor 5 days after exposure cessation Leukocytes increased by44 (plt005 as comparedwith sham-exposed animals) Theyconcluded that EHF effects can be mediated via metabolicsystems and further said results indicated whole-body low-intenstiy EHF exposure of healthymice had a profound effecton the indices of nonspecific immunity These low levels willbe common near 5G infrastructure

In well-designed non-rodent mammal field studiesNicholls and Racey [206 207] found that foraging batsshowed aversive behavioral responses near large air trafficcontrol andweather radars Four civil air traffic control (ATC)radar stations three military ATC radars and three weatherradars were selected each surrounded by heterogeneoushabitat Three sampling points were carefully selected formatched habitats type structure altitude and surroundingland class at increasing distances from each station Radarfield strengthswere taken at three distances from the sourceclose proximity (lt656 ft200 m) with a high EMF strengthgt2 Vm (106 μWcm2) an intermediate line-of sight point(656ndash1312 ft200ndash400 m) with EMF strength lt2 Vm and acontrol location out of radar sight (gt1312 ft400 m) regis-tering 0 Vm Bat activity was recorded three times for a totalof 90 samples 30 within each field strength categoryMeasured from sunset to sunrise they found that bat activitywas significantly reduced in habitats exposed to an EMFgreater than 2 Vm compared to 0 EMF sites but suchreduced activity was not significantly different at lower EMFlevels within 400 m of the radar They concluded that thereduced bat activity was likely due to thermal induction andan increased risk of hyperthermia This was a large fieldstudy near commercial radar installations with mostly highintensity exposures but low-level effects cannot be excludedgiven known magneto-sensitivity in bats

In another field study using a small portable marineradar unit significantly less powerful than their earliermeasured field study Nicholls and Racey [207] found thesmaller signal could also deter batsrsquo foraging behaviorsFirst in summer 2007 bat activity was compared at 20foraging sites in northeast Scotland during experimentaltrials with radar switched on and in controls with no radarsignal After sunset bat activity was recorded for a periodof 30 min with the order of the trials alternating betweennights Then in summer 2008 aerial insects were sampledat 16 of the sites using two small light-suction traps onewith a radar signal the other a control Bat activity andforaging were found significantly reduced when the radarsignal was unidirectional creating a maximized exposureof 1767ndash2624 Vm (83ndash183 μWcm2) The radar had nosignificant effect on the abundance of insects captured bythe traps despite reduced bat activity

18 Levitt et al EMF and wildlife

Balmori [231] also noted significantly reduced bat ac-tivity in a free-tailed bat colony (Tadarida teniotis) wherethe number of bats decreased when several cell towerswere placed 262 ft (80 m) from the colony

In the ELF range Janać et al [232] investigated ELFMFeffects mdash comparable to powerline and stray voltageground currentmdash onmotor behavior patterns inMongoliangerbils (Meriones unguiculatus) and found age-dependentchanges in locomotion stereotypy and immobility in 3-and 10-month-old males Animals were continuouslyexposed to ELF-MF (50 Hz 01 025 and 05 mT) for sevendays with behavior monitored for 60 min in the open fieldafter the 1st 2nd 4th and 7th day (to capture immediateeffects) as well as three days after exposure (to capturedelayed effects) They found that exposure to 3-month-oldgerbils increased motor behavior (locomotion and stereo-typy) and therefore decreased immobility In the 3-monthold gerbils ELFMF also showed a delayed effect (except at025 mT) on stereotypy and immobility In 10-month-oldgerbils ELFMF of 01 025 and 05 mT induced decreasedlocomotion a slight increase in stereotypy and pro-nounced stimulation of motor behavior Increased motorbehavior was observed three days after exposure indi-cating long lasting effects Researchers concluded that in 3-and 10-month-old gerbils specific temporal patterns ofmotor behavior changes were induced by ELFMF due toage-dependent morpho-functional differences in brainareas that control motor behavior

The above is a very small sample of rodent studies SeePart 2 Supplements 1 and 2 for more genetic effects to ro-dents and Supplement 3 for additional studies

Bovines

Due to domestication and easy accessibility there arenumerous studies of dairy cows (Bos taurus) which appearparticularly sensitive to both natural andman-made EMFsFedrowitz [71] published a thorough review with citationstoo numerous to mention here Noted in the review is thefact that bovines although easily accessible are difficult tostudy with precision due to their size which createshandling and dosimetric complexities Also noted are thatbovines today are at their milk- and beef-productionphysiological limits and that the addition of even a weakstressor may be capable of altering a fragile bovine phys-iological balance It is clear in the Fedrowitz review thatcows respond to environmental exposures from a broadrange of frequencies and properties even as some studieslack good exposure assessment RFR exposure createdavoidance behavior reduced ruminating and lying times

and alterations in oxidative stress enzymes among otherproblems while ELF-EMF found contradictory evidenceaffecting milk production fat content hormone imbal-ances and important changes in other physiological pa-rameters Cows have also been found sensitive to strayvoltage and transient harmonics with problematic milkproduction health reproduction and behavioral effects

The question is how much of this body of work couldtranslate to other ruminants and largemammals on-field orin the wild such as deercervids mdash behaviorally repro-ductively and physiologically Stray voltage and ELF-EMFnear powerlines and rural area RFR from both ground-based and satellite transmitters for instance may affectwild migratory herds and large ungulates in remote areasthat go undetected

Bovines and RFR

Loscher and Kas [233] observed abnormal behavior in a dairyherd kept in close proximity to a TV and radio transmitterThey found reduction in milk yield health problems andbehavioral abnormalities After evaluating other factors theyconcluded the high levels of RFR were possibly responsibleThey removed one cow with abnormal behavior to anotherstable 20 km away from the antenna resulting in normali-zation of behavior within five days Symptoms reappearedwhen the cowwas returned to the stablenear theantennas Ina later survey Loscher [234] also found effects of RFR on theproduction health and behavior of farm animals includingavoidance behavior alterations in oxidative stress parame-ters and ruminating duration

Balode [59] obtained blood samples from female browncows from a farm close to and in front of the Skrunda Ra-dar ndash located in Latvia at an early warning radar systemoperating in the 156ndash162MHz frequency rangemdashand samplesfrom cows in a control area They found micronuclei in pe-ripheral erythrocyteswere significantly higher in the exposedcows indicating DNA damage

Staumlrk et al [235] investigated short-wave (3ndash30 MHz)RFR on salivary melatonin levels in dairy cattle with oneherd at a farm located at 1640 ft500 m (consideredhigher exposure) and a second control herd located 13123ft4000 m from the transmitter (considered unexposed)The average nightly magnetic field strength readingswere 21-fold greater on the exposed farm (159 mAm)than on the control farm (0076 mAm) At both farmsafter initially monitoring five cowsrsquo salivary melatoninconcentrations at 2-h intervals during night dark phasefor 10 consecutive days and with the short-wave trans-mitter switched off during three of the 10 days (off phase)samples were analyzed using a radioimmunoassay They

Levitt et al EMF and wildlife 19

reported that mean values of the two initial nights did notshow a statistically significant difference betweenexposed and unexposed cows and concluded thatchronic melatonin reduction was unlikely But on the firstnight of re-exposure after the transmitter had been off forthree days the difference in salivary melatonin concen-tration between the two farms (389 pgml CI 204 741)was statistically significant indicating a two-to-seven-fold increase of melatonin concentration Theyconcluded that a delayed acute effect of EMF on mela-tonin concentration could not be excluded and called forfurther trials to confirm results

Haumlssig et al [95] conducted a cohort study to evaluatethe prevalence of nuclear cataracts in veal calves nearmobilephone base stations with follow-up of each dam and its calffrom conception through fetal development and up toslaughter Particular emphasis was focused on the firsttrimester of gestation (organogenesis) Selected protectiveantioxidants (superoxide dismutase catalase glutathioneperoxidase [GPx]) were assessed in the aqueous humor of theeye to evaluate redox status They found that of 253 calves 79(32) had various degrees of nuclear cataracts but only 9(36)of calveshad severenuclear cataracts Theyconcludedthat a relationship between the location of veal calves withnuclear cataracts in the first trimester of gestation and thestrength of antennas was demonstrated The number of an-tennas within 328ndash653 ft (100ndash199 m) was associated withoxidative stress and there was an association betweenoxidative stress and the distance to the nearest base stationOxidative stress was increased in eyes with cataract (OR perkilometer 080 confidence interval 95 062 093) But theresearchers further concluded that it hadnot been shown thatthe antennas actually affected stress Hosmer-Lemeshowstatistics showed an accuracy of 100 in negative cases withlow radiation andonly 1111accuracy inpositive caseswithhigh radiation This reflected in their opinion that there are alot of other likely causes for nuclear cataracts beside basestations and called for additional studies on EMF duringembryonic development

Haumlssig et al [96] further examined a dairy farm inSwitzerland where a large number of calves were born withnuclear cataractsafter amobilephonebase stationwaserectednear the barn Calves showed a 35 times higher risk for heavycataracts if born there compared to theSwissaverageAll usualcauses for cataracts could be excluded but they neverthelessconcluded that the incidence remained unknown

Bovines and swine ELF-EMF stray electric current

Bovines appear unusually sensitive to ELF-EMF from straycurrent caused by both normal industrial and faulty

grounding methods near high tension transmission linesclose to dairy farms Stray current can cover large areas andoccurs when current flows between the grounded circuitconductor (neutral) of a farm and the Earth through dairyhousing equipment like metal grates It typically involvessmall steady power frequency currents [99] not hightransient shocks although that also can sometimes occurunderwetweather conditions According toHultgren [236]dairy cattle can perceive alternating currents exceeding1 mA between the mouth and all four hooves with behav-ioral effects in cows usually occurring above 3 mA Straycurrent can act as a major physical stressor in cows andother animals [237] This may also be happening in wildmigratory species moving through such areas

At the request of dairymen veterinarians and countyextension agents in Michigan US Kirk et al [238] inves-tigated stray current on 59 Michigan dairy farms On 32farms stray current sources were detected Where voltageexceeded 1 V alternating current increased numbers ofdairy cows showed abnormal behavior in the milking fa-cility and increased prevalence of clinical mastitis Re-covery from the stray current-induced abnormalities wasrelated to the type of abnormality and themagnitude of theexposure voltage

Burchard et al [239] in a small but well-controlledalternating exposure study of non-pregnant lactating Hol-stein cows found a longer estrous cycle in cows exposed to avertical electric field of 10 kVm and a uniform horizontalmagneticfield of 30 μT at 60Hz compared towhen theywerenot exposed Rodriguez et al [240] also found that exposureto EMFmay increase the duration of the bovine estrous cycleBurchard et al [241] evaluated effects on milk production inHolsteins exposed to a vertical electric field of 10 kVm and auniformhorizontalMFof 30μTat 60Hzand foundanaveragedecrease of 497 1378 and 1639 inmilk yield fat correctedmilk yield and milk fat respectively in exposed groups andan increase of 475 in dry matter food intake And Buchardet al [242] in two experiments investigated blood thyroxine(T4) levels in lactating pregnant and non-lactating non-pregnant Holstein cows exposed to 10 kVm 30 microT EMF andfound a significant change depending on the time of bloodsampling in exposed groups They concluded that exposureof dairy cattle to ELF-EMF could moderately affect the bloodlevels of thyroxine

Hillman et al [93 94] reported that harmonic distor-tion and power quality itself could be another variable inbovine sensitivity to stray current They found behaviorhealth and milk production were adversely affected bytransients at the 3rd 5th 7th and triplen harmonic cur-rents on utility power lines after a cell tower was foundcharging the ground neutral with 10+ V causing the

20 Levitt et al EMF and wildlife

distortion After installing a shielded neutral isolationtransformer between the utility and the dairy the distor-tion was reduced to near zero Animal behavior improvedimmediately and milk production which had been sup-pressed for three years gradually returned to normalwithin 18 months

Swine (Sus scrofa domesticus) mdash like rats and mice mdashhave demonstrated aversive behavior to ELF-EMF electricfields Hjeresen et al [243] found miniature pigs exposedto 60‐Hz electric fields (30 kVm for 20 hday 7 daysweekup to 6 months) preferred an absence of the field during a235‐h period by spendingmore time out of the electric fieldthan in it during sleep periods And Sikov et al [244] aspart of a broad study of Hanford Miniature swine onreproductive and developmental toxicology (includingteratology) over three breeding cycles found a strong as-sociation between chronic exposure to a vertical uniformelectric field (60‐Hz 30‐kVm for 20 hday 7 daysweek)and adverse developmental effects vs control Theyconcluded that an association exists between chronicexposure to strong electric fields and adverse develop-mental effects in swine (75malformations in exposed vs29 sham) in first generation with consistent results in twosubsequent generations

Avian

Birds are important indicators of ecosystemwell-being andoverall condition Even subtle effects can be apparent dueto their frequent presence in RFR areas Their hollowfeathers have dielectric and piezoelectric propertiesmeaning they are conductive and capable of acting as awaveguide directing external RFR energy directly anddeeply into avian body cavities [245ndash249] Their thin skullshave both magnetite and radical pair receptors (seeldquoMechanismsrdquo above) and they are highly mobile mdash oftentraveling across great migratory distances of tens to asmuch as a hundred thousand kilometers round-trip peryear resulting in potential multi-frequency cumulativeeffects from chronic near middle and far-field exposuresAvian populations are declining worldwide especiallyamong migratory species This means that birds may beuniquely sensitive to adverse effects from environmentalRFR since their natural habitat is air and they often fly atlateral levels with infrastructure emissions bringing themthat much closer to generating sources

Tower and building construction as direct obstaclesare known hazards to birds One tower at 150 feet (46 m)above ground level is thought to account for as many as3000 songbird deaths per month in migratory pathways

during peak migration [250] and communication towercollisions have been documented to kill more than 10000migratory birds in one night at a TV tower in Wisconsin[251 252] It has been known for years that the songbirdpopulations of North America and Europe are plummetingOnly recently were towers considered a significant factorBut is the problem solely due to obstacles in direct migra-tory pathways or is something else involved

RFR from towers may be acting as an attractant to birdsdue to their singular physiology Avian eyes and beaks areuniquely magnetoreceptive with both magnetite and crypt-chrome radical pair receptors One definitive studybyBeasonand Semm [253] demonstrated that the common cell phonefrequency (900-MHz carrier frequency modulated at 217 Hz)at nonthermal intensities produced firing in several types ofnervous system neurons in Zebra Finches (Taeniopygia gut-tate) Brain neurons of irradiated anesthetized birds showedchanges in neural activity in 76 of responding cells whichincreased their firing rates by an average 35-fold vs controlsOther responding cells exhibited a decrease in rates ofspontaneous activity The Beason and Semm study [253]could explain why birds may be attracted to cell towers atheoretical premise they previously observed with Bobolinks(Dolichonyx oryzivorus [254])

RFR may also act as an avian stressorirritant Earlywork by Wasserman et al [255] in field studies on 12 flocksof migratory birds subjected to various combinations ofmicrowave power density and duration under winter con-ditions at Monomet MA using birds from two additionalflocks as controls showed increased levels of aggression insome of the irradiated birds

Other research indicated a range of effects capable ofbroad adverse environmental outcomes Laboratorystudies by Di Carlo et al [256] found decreases in heatshock protein production in chick embryos The re-searchers used 915-MHz RFR on domestic chicken em-bryos and found that exposure typical of some cell phoneemissions reduced heat shock proteins (HSP-70) andcaused heart attacks and death in some embryos Con-trols were unaffected In replicated experiments similarresults were found by Grigorrsquoev [257] and Xenos andMagras [258] Batellier et al [259] found significantlyelevated embryomortality in exposed vs sham groups ofeggs incubated with a nearby cell phone repeatedlycalling a 10-digit number at 3-min intervals over theentire incubation period Heat shock proteins helpmaintain the conformation of cellular proteins duringperiods of stress A decrease in their productiondiminishes cellular protection possibly leading to can-cer other diseases heart failure and reduction in pro-tection against hypoxia and ultraviolet light

Levitt et al EMF and wildlife 21

Not all results are adverse Tysbulin et al [260 261]investigated both short and prolonged GSM 900 MHz cellphone signal exposure on embryo development in Quail(Coturnix coturnix japonica) irradiating fresh fertilizedeggs during the first 38 h and 14 days of incubation using acell phone in connecting mode continuously activatedthrough a computer systemMaximum intensity of incidentradiation on the eggrsquos surface was 02 mWcm2 Resultsfound a significant (plt0001) increase in differentiatedsomites in 38-h exposed embryos and a significant (plt005)increase in total survival of embryos in eggs after 14 daysexposure They also found the level of thiobarbituric acid(TBA) reactive substances was significantly (p 005ndash0001)higher in the brains and livers of hatchlings from exposedembryos and hypothesized that a facilitating effect existsdue to enhanced metabolism in exposed embryos via per-oxidation mechanisms They concluded low-levelnonthermal effects from GSM 900 MHz to quail embryo-genesis is possible and that effects can be explained via ahormesis effect induced by reactive oxygen species (ROS)

Signaling characteristics such as pulsing vs contin-uous wave are also important Berman et al [262] in amulti-lab study of pulsed ELF magnetic fields found ahighly significant incidence of abnormalities in exposedchick eggs vs controls And Ubeda et al [263] found irre-versible damage to chick embryos from weak pulsedELF-EMF magnetic fields that are common in the environ-ment today Initial studies on freshly fertilized chickeneggs were exposed during the first 48 h of post-laying in-cubation to pulsed magnetic fields (PMFs) with 100 Hzrepetition rate 10 μT peak-to-peak amplitude and 500 μspulse duration Two different pulse waveforms were usedwith rise and fall times of 85 μs or 21 μs A two-day expo-sure found significant increased developmental abnor-malities In follow-up research after exposure eggs wereincubated for an additional nine days without PMFs Em-bryos removed from eggs showed an excess of develop-mental anomalies in the PMF-exposed groups comparedwith the sham-exposed samples There was a high rate ofembryonic death in the 21 μs risefall time Results indicatePMFs can cause irreversible developmental changes con-firming that a pulse waveform can determine embryonicresponse to ELF magnetic fields common today

Between 1999 and 2005 Fernie et al for the first timeinvestigated various potential reproductive effects on acaptive raptor species mdash the American Kestrel (Falcosparverius) mdash from ELF-EMF equivalent to that of wildnesting pairs on power transmission lines In a series ofstudies captive pairs were typically bred under control orEMF exposure over 1ndash3 breeding cycles In 1999 Fernieet al [264] investigated photo phasic plasma melatonin in

reproducing adult and fledgling kestrels finding that EMFsaffected plasma melatonin in adult male kestrels sup-pressing it midway through but elevating it at the end ofthe breeding season In long-term but not short-term EMFexposure of adults plasma melatonin was supressed intheir fledglings too which could affect migratory successMolt happened earlier in adult EMF-exposed males than incontrols EMF exposure had no effect on plasmamelatoninin adult females In avian species melatonin is involved inbody temperature regulation seasonal metabolism loco-motor activity feeding patterns migration and plumagecolor changes important for mate selection Melatonin alsoplays a key role in the growth and development of youngbirds The researchers concluded it is likely that the resultsare relevant to wild raptors nesting within EMF exposures

In 2000 Fernie et al [265] focused on reproductivesuccess in captive American Kestrels exposed to ELF-EMFagain equivalent to that experienced by wild reproducingkestrels Kestrels were bred one season per year for twoyears under EMF or controlled conditions In some yearsbut not others EMF-exposed birds showed a weak asso-ciationwith reduced egg laying higher fertility larger eggswithmore yolk albumen andwater but thinner egg shellsthan control eggs Hatching successwas lower in EMFpairsthan control pairs but fledging success was higher thancontrol pairs in one year They concluded that EMF expo-sure such as what kestrels would experience in the wildwas biologically active in a number of ways leading toreduced hatching success

Also in 2000 Fernie et al [266] further investigatedbehavioral changes in American Kestrels to ELF-EMFagain in captive birds comparable to nesting pairs thatcommonly use electrical transmission structures for nest-ing perching hunting and roosting The amount of EMFexposure time of wild reproducing American Kestrels wasfirst determined at between 25 and 75 of the observedtime On a 24-h basis estimated EMF exposure in wildspecies ranged from 71 during courtship to 90 duringincubation Then effects of EMFs on the behavior of captivereproducing kestrels were examined at comparable expo-sures of 88of a 24-h period Additionally captive kestrelswere exposed to EMF levels experienced by wild kestrelsnesting under 735-kV power lines There appeared to be astimulatorystress effect Captive EMF females were moreactive more alert and perched on the pen roof morefrequently than control females during courtship EMF fe-males preened and rested less often during brood rearingEMF-exposed male kestrels were more active than controlmales during courtship and more alert during incubationThe researchers concluded that the increased activity ofkestrels during courtship may be linked to changes in

22 Levitt et al EMF and wildlife

corticosterone but not to melatonin as found in earlierwork [264] but said the behavioral changes observed wereunlikely to result in previously reported effects inEMF-exposed birds as noted above They added thatbehavioral changes of captive EMF-exposed kestrels mayalso be observed in wild kestrels with uncertain results

In 2001 Fernie and Bird [267] looked at ELF-EMFoxidative stress levels in captive American Kestrels usingthe same test parameters described above to see if ELF-EMFexposure elicited an immune system response In captivemale kestrels bred under control or EMF conditionsequivalent to those experienced by wild kestrels short-term EMF exposure (one breeding season) suppressedplasma total proteins hematocrits and carotenoids in thefirst half of the breeding season It also suppressed eryth-rocyte cells and lymphocyte proportions but elevatedgranulosa proportions at the end of the breeding seasonLong-term EMF exposure (two breeding seasons) alsosuppressed hematocrits in the first half of the reproductiveperiod But results found that only short-termEMF-exposed birds experienced an immune responseparticularly during the early half of the breeding seasonThe elevation of granulocytes and the suppression of ca-rotenoids total proteins and melatonin [264] in the samekestrel species indicated that the short-term EMF-exposedmale kestrels had higher levels of oxidative stress due to animmune response andor EMF exposure The researchersnoted that long-termEMF exposuremay be linked to higherlevels of oxidative stress solely through EMF exposureOxidative stress contributes to cancer neurodegenerativediseases and immune disorders And in 2005 Fernie andReynolds [268] noted most studies of birds and EMF indi-cate changes on behavior reproductive success growthand development physiology and endocrinology andoxidative stress mdash with effects not always consistent or inthe same direction under EMF conditions The entire bodyof work by this research group has implications for all wildspecies that encounter a wide range of EMFs on a regularbasis

In field studies on wild birds in Spain Balmori [269]found strong negative correlations between low levels ofmicrowave radiation and bird breeding nesting roostingand survival in the vicinity of communication towers Hedocumented nest and site abandonment plumage deteri-oration locomotion problems and death in Wood Storks(Mycteria americana) House Sparrows (Passer domes-ticus) Rock Doves (Columba livia) Magpies (Pica pica)Collared Doves (Streptopelia decaocto) and other speciesWhile these species had historically been documented toroost and nest in these areas Balmori [269] did not observethese symptoms prior to construction and operation of the

cell phone towers Results were most strongly negativelycorrelated with proximity to antennas and Stork nestingand survival Twelve nests (40 of his study sample) werelocated within 656 ft (200 m) of the antennas and neversuccessfully raised any chicks while only one nest (33)located further than 984 ft (300 m) never had chicksStrange behaviors were observed at Stork nesting siteswithin 328 ft (100 m) of one or several cell tower antennasBirds impacted directly by the main transmission lobe(ie electric field intensity gt 2 Vm) included young thatdied from unknown causes Within 100 m paired adultsfrequently fought over nest construction sticks and failedto advance nest construction (sticks fell to the ground)Balmori further reported that some nests were nevercompleted and that Storks remained passively in front ofcell site antennas The electric field intensity was higher onnests within 200 m (236 plusmn 082 Vm 148 μWcm2) than onnests further than 300 m (053 plusmn 082 Vm 0074 μWcm2)RF-EMF levels including for nests lt100 m from the an-tennas were not intense enough to be classified as thermalexposures Power densities need to be at least 10 mWcm2

to produce tissue heating of even 05 degC [270] Balmorirsquosresults indicated that RFR could potentially affect one ormore reproductive stages including nest constructionnumber of eggs produced embryonic developmenthatching and mortality of chicks and young in first-growthstages

Balmori and Hallberg [271] and Everaert and Bauwens[272] found similar strong negative correlations amongmale House Sparrows (Passer domestics) throughout mul-tiple sites in Spain and Belgium associated with ambientRFR between 1 MHz and 3 GHz at various proximities toGSM cell base stations House Sparrow declines in Europehave been gradual but cumulative for this species oncehistorically well adapted to urban environments Thesharpest bird density declines were in male House Spar-rows in relatively high electric fields near base stationsindicating that long-term exposure at higher RFR levelsnegatively affected both abundance andor behavior ofwild House Sparrows In another review Balmori [25] re-ported health effects to birds that were continuously irra-diated They suffered long-term effects that includedreduced territorial defense posturing deterioration of birdhealth problems with reproduction and reduction ofuseful territories due to habitat deterioration

Birds have been observed avoiding areas with highand low-intensity EMF in daylight as well as nocturnallyAn early study by Southern in 1975 [273] observed that gullchicks reacted to the US militaryrsquos Project Sanguin ELFtransmitter Tested on clear days in the normal geomag-netic field birds showed significant clustering with

Levitt et al EMF and wildlife 23

predicted bearing corresponding with migration directionbut when the large antenna was energized they dispersedrandomly He concluded that magnetic fields associatedwith such conductors were sufficient to disorient birdsLarkin and Sutherland [274] observed that radar tracking ofindividual nocturnal migrating birds flying over a largealternating-current antenna system caused birds to turn orchange altitude more frequently when the antenna systemwas operating than when it was not The results suggestedthat birds sense low-intensity alternating-current EMFduring nocturnal migratory flight

In a well-designedmulti-year avian study ofmagneto-disruption Engels et al [213] investigated environmentalbroadband electromagnetic lsquonoisersquo emitted everywherehumans use electronics including devices and infra-structure They found migratory birds were unable to usetheir magnetic compass in the presence of a typical urbanenvironment today European Robins (E rubecula)exposed to the background electromagnetic lsquonoisersquo presentin unscreened wooden huts at the University of Oldenburgcampus could not orient using their magnetic compassBut when placed in electrically grounded aluminum-screened huts creating Faraday cages that attenuatedelectromagnetic lsquonoisersquo by approximately two orders ofmagnitude their magnetic orientation returned The re-searchers were able to determine the frequency range from50 kHz to 5 MHz was the most disruptive When groundingwas removed or additional broadband electromagneticlsquonoisersquo was deliberately generated inside the screened andgrounded huts birds again lost magnetic orientationabilities They concluded that RFRrsquos magneto-disruptioneffects are not confined to a narrow frequency band Birdstested far from sources of EMFs required no screening toorientwith theirmagnetic compass Thiswork documenteda reproducible effect of anthropogenic electromagneticambient lsquonoisersquo on the behavior of an intact vertebrate Themagnetic compass is integral to bird movement andmigration Thefindings clearly demonstrated anonthermaleffect on European Robins and serves as a predictor foreffects to othermigratory birds especially those flying overurban areas Such fields are much weaker than minimumlevels expected to produce any effects and far below anyexposure standards

Intensity windows in different species have also beenfound where effects can be more extreme at lower in-tensities than at higher ones due to compensatory mech-anisms such as cell apotosis Panagopoulos andMargaritas[34] found an unexpected intensity window at thermallevels around 10 mWcm2 RFR mdash not uncommon near celltowersmdashwhere effects weremore severe than at intensitieshigher than 200 mWcm2 This window appeared at a

distance of 8ndash12 in (20ndash30 cm) from a cell phone antennacorresponding to a distance of about 66ndash98 ft (20ndash30 m)from a base station antenna This could be considered aclassic nonlinear effect and would apply to far-field expo-sures Since cell base station antennas are frequentlylocated within residential areas where birds nest often atdistances 20ndash30 m from such antennas migratory birdsnon-migratory avifauna and other wildlife may beexposed up to 24-h per day

Concerns also apply to impacts from commercial radiosignals on migratory birds The human anatomy is reso-nant with the FM bands so exposure standards are moststringent in that range High intensity (gt6000 W) com-mercial FM transmitters are typically located on the highestground available to blanket a wider area Low powered FMtransmitters (lt1000 W) can be placed closer to the humanpopulation High intensity locations which can be multi-transmitter sites (colloquially called ldquoantenna farmsrdquo) forother services also provide convenient perches and nestsites formigratory birds FMdigital signals which simulatepulsed waves pose additional health concerns to migra-tory birds This creates a dangerous frequency potential forprotected migratory birds such as Bald Eagles with wing-spans that extend to about 6 ft (183 m)mdash a resonant matchwith the length of the FM signalmdash creating a potential full-body resonant effect for both humans and Bald EaglesBirds could experience both thermal and non-thermaleffects

All migratory birds are potentially at risk includingBald Eagles Golden Eagles birds of conservation concern[275] federal andor state-listed bird species birds na-tionally or regionally in peril as well as birds whose pop-ulations are stable Sadly addressing these concerns mdashbeginning with independent research conducted by sci-entists with no vested interest in the outcomes mdash has notbeen a priority for government agencies or the communi-cations industry

Insects and arachnids

Insects are the most abundant and diverse of all animalgroups with more than one million described speciesrepresenting more than half of all known living speciesand potentially millions more yet to be discovered andidentified They may represent as much as 90 of all lifeforms on Earth Though some are considered pests to farmcrops and others as disease vectors insects remainessential to life and planetary health Found in nearly allenvironments they are the only invertebrates that fly butadults of most insect species walk while some swim

24 Levitt et al EMF and wildlife

Because of these different environmental adaptationsdifferent species will encounter different EMF exposures invarying degrees For instance ground-based walking in-sects may be more susceptible to effects from 60 Hz straycurrent while flying insects may be more susceptible towireless exposures However all species tested have beenaffected across a range of the nonionizing electromagneticbands

Most insects have an exoskeleton three-part bodyconsisting of a head thorax and abdomen three pairs ofjointed legs compound eye structures capable to seeingmany more colors widths and images than humans andone pair of antennae capable of sensing subtle meteoro-logical changes and Earthrsquos geomagnetic fields They livein close harmonywith the natural environment for survivaland mating purposes The most diverse insect groups co-evolved with flowering plants many of which would notsurvive without them Most insect species are highly sen-sitive to temperature variations and climate alterations asthey do not dissipate heat efficiently

Nearly all insects hatch from eggs that are laid inmyriad ways and habitats Growth involves a series ofmolts and stages (called instars) with immature stagesgreatly differing from mature insects in appearancebehavior and preferred habitat Some undergo a four-stage metamorphosis (with a pupal stage) and others athree-stage metamorphosis through a series of nyphalstages

While most insects are solitary some mdash like beestermites and antsmdash evolved into social networks living inldquocooperativerdquo organized colonies that can function as oneunit as evidenced in swarming behaviors Some even showmaternal care over eggs and young They communicatethrough various sounds pheromones light signals andthrough their antennae such as during the beesrsquo ldquowaggledancerdquo (see below)

As far back as the 1800s even though testing methodswere primitive by todayrsquos standards researchers werecurious about electromagnetismrsquos effect on insect devel-opment particularly teratogenicity [276] Research on EMFacross frequencies and insect populations has beenongoing since at least the 1930s with an eye toward usingenergy as an insecticide and anti-contaminant in graintypically at high intensity thermal exposures that wouldnot exist in the natural environment Mckinley and Charles[277] found that wasps die within seconds of high fre-quency exposure But not all early work was strictly highintensity or all effects observed due to thermal factors

There were interesting theories introduced by earlyresearchers regarding how energy couples with variousinsect species Frings [278] found larval stages are more

tolerant to heat than adult insects with appendages thatcan act as conducting pathways to the body and that themore specialized the insect species the more susceptiblethey appear to microwave exposure Carpenter and Liv-ingstone [279] studied effects of 10 GHz continuous-wavemicrowaves at 80 mWcm2 for 20 or 30 min or at 20 mWcm2 for 120 min on pupae of mealworm beetles (Tenebriomolitor)mdash clearlywithin thermal ranges In control groups90 metamorphosed into normal adult beetles whereasonly 24 of exposed groups developed normally 25died and 51 developed abnormally Effects wereassumed to be thermally induced abnormalities until theysimulated the same temperature exposure using radiantheat and found 80 of pupae developed normally Theyconcluded that microwaves were capable of inducingabnormal effects other than through thermal damage

Fruit flies

Insects at all metamorphic stages of development havebeen studied using RFR including egg larva pupa andadult stages Much work has been done on genetic andother effects with fruit flies (D melanogaster) because oftheirwell-described genetic system ease of exposure largebrood size minimal laboratory space needed and fastreproductive rates Over several decades Goodman andBlank using ELF-EMF on Drosophilamodels found effectsto heat shock proteins and several other effects ([201] andsee ldquoMechanismsrdquo above) It is considered a model com-parable to other insects in thewild approximating that sizeD melanogaster may be the most lab-studied insect onEarth although honey and related bee species due to theirdevastating losses over the last decade and significance toagriculture are quickly catching up

Michaelson and Lin [50] noted that RFR-exposed in-sects first react by attempting to escape followed bydisturbance of motor coordination stiffening immobilityand eventually death depending on duration of exposureand insect type For example D melanogaster survivedlonger than 30minwhile certain tropical insects live only afew seconds at the same field intensity Also noted wereconcentration changes in many metabolic products andeffects to embryogenesis mdash the period needed for a but-terfly to complete metamorphosis mdash with acceleratedgastrulation and larval growth [17] Michaelson and Lin[50] cited several negative studies with D melanogasterexposed with continuous-wave RFR between 25 and2450 MHz on larval growth [280 281] and mutagenicity[282] This was after Heller andMickey [283] found a tenfoldrise in sex-linked recessive mutations with pulsed RFR

Levitt et al EMF and wildlife 25

between 30 and 60 MHz It was among the earliest studiesthat found pulsing alone to be a biologically activeexposure

As reported in Michaelson and Lin [50] Tell [284]looked at D melanogasterrsquos physiological absorptionproperties and found that a group of 6-day old male wild-type flies exposed to 2450 MHz for 55 min at an intensefield caused a dramatic 65 reduction in bodyweight Thiswas thought to be from dehydration They then sought tocalculate the fruit flyrsquos absorption properties in relation toplane electromagnetic waves and found that a fly has onlya 11000th effective area of its geometric cross section andthus is an inefficient test species for absorbed microwaveradiation However they concluded that fruit flies wereresponsive to absorbed energy at thermal levels as a blackbody resonator at a power density of 1044 times 104 mWcm2corresponding to a thermal flux density of 0562 times 10minus3 calThese are levels found in close proximity to broadcast fa-cilities and cell phone towers today

More recent investigations of RFR by Weisbrot et al[285] using GSM multiband mobile phones (9001900 MHz SAR approximately 14 Wkg) on D mela-nogaster during the 10-day developmental period from egglaying through pupation found that non-thermal radiationincreased numbers of offspring elevated heat shockprotein-70 levels increased serum response element (SRE)DNA-binding and induced the phosphorylation of the nu-clear transcription factor ELK-1Withinminutes therewasa rapid increase of hsp70 which was apparently not athermal effect Taken together with the identified compo-nents of signal transduction pathways the researchersconcluded the study provided sensitive and reliable bio-markers for realistic RFR safety guidelines

Panagopoulos et al [286] found severe effects in earlyand mid-stage oogenesis in D melanogaster when flieswere exposed in vivo to either GSM 900-MHz or DCS1800-MHz radiation from a common digital cell phone atnon-thermal levels for a few minutes per day during thefirst 6 days of adult life Results suggested that the decreasein oviposition previously reported [287ndash289] was due todegeneration of large numbers of egg chambers after DNAfragmentation of their constituent cells which was inducedby both types of mobile phone radiation Induced celldeath was recorded for the first time in all types of cellsconstituting an egg chamber (follicle cells nurse cells andthe oocyte) and in all stages of early and mid-oogenesisfrom germarium to stage 10 during which programmedcell death does not physiologically occur Germarium andstages 7ndash8 were found to also be the most sensitivedevelopmental stages in response to electromagnetic stressinduced by the GSM and DCS fields Germarium was also

found to be more sensitive than stages 7ndash8 These paperstaken collectively indicate serious potential effects to allinsect species of similar size to fruit flies from cell phonetechnology including from infrastructure and transmittingdevices

Fruit flies have also been found sensitive to ELF-EMFGonet et al [290] found 50 Hz ELF-EMF exposure affectedall developmental stages of oviposition and developmentof D melanogaster females and weakened oviposition insubsequent generations

Savić et al [291] found staticmagneticfields influencedboth development and viability in two species ofDrosophila (D melanogaster and D hydei) Both speciescompleted development (egg-to-adult) in and out of thestatic magnetic field induced by a double horseshoe mag-net Treated vials with eggswere placed in the gap betweenmagnetic poles (47 mm) and exposed to the average mag-netic induction of 60 mT while control groups were keptfar from the magnetic field source They found that expo-sure to the static magnetic field reduced development timein both species but only results for D hydei were statisti-cally significant In addition the average viability of bothspecies was significantly weaker compared to controlsThey concluded a 60 mT static magnetic field could be apotential stressor influencing on different levels bothembryonic and post-embryonic fruit fly development

Beetles

Other insect species also react to both ELF-EMF andRF-EMF Newland et al [292] found behavioral avoidancein cockroaches (Periplaneta americana) to static electricfields pervasive in the environment from both natural andman-made sources Such fields could exist near powerlinesor where utilities ground neutral lines into the Earth Theyfound insect behavioral changes in response to electricfields as tested with a Y-choice chamber with an electricfield generated in one arm of the chamber Locomotorbehavior and avoidance were affected by the magnitude ofthe electric fields with up to 85 of individuals avoidingthe charged arm when the static e-field at the entrance tothe arm was above 8ndash10 kVm Seeking to determinemechanisms of perception and interaction they then sur-gically ablated the antennae and cockroaches were unableto avoid electric fields They concluded that antennae arecrucial in cockroach detection of electric fields that therebyhelps them avoid such fields They also noted that cock-roach ability to detect e-fields is due to long antennaewhich are easily charged and displaced by such fields notbecause of a specialized detection system This leads to the

26 Levitt et al EMF and wildlife

possibility that other insects may also respond to electricfields via antennae alone

Vaacutecha et al [208] found that cockroaches (P americana)were sensitive to weak RFR fields and that the Larmor fre-quency at 12 MHz in particular had a ldquodeafening effectrdquo onmagnetoreception The parameter they studied was the in-crease in locomotor activity of cockroaches induced by peri-odic changes in geomagnetic North positions by 60deg Theonset of the disruptive effect of a 12 MHz field was foundbetween 12 and 18 nT whereas the threshold of a field twicethe frequency (24 MHz) fell between 18 and 44 nT A 7 MHzfield showed no significant effect even at maximal of 44 nTThe results suggested resonance effects and that insects maybe equipped with the same magnetoreception systemas birds

Prolić et al [293] investigated changes in behavior viathe nervous system of cerambycid beetles (Morimus fune-reus) in an open field before and after exposure to a 50 HzELF-MF at 2 mT Experimental groups were divided intoseveral activity categories Results showed activityincreased in the groups with medium and low motor ac-tivity but decreased in highly active individuals High in-dividual variability was found in the experimental groupsas well as differences in motor activities between the sexesboth before and after exposure to ELF‐MF They assumedactivity changes in both sexeswere due to exposure to ELF‐MF Only a detailed analysis of the locomotor activity at 1‐min intervals showed some statistically significant differ-ences in behavior between the sexes

Ants

Ants are another taxa found sensitive to EMF Ants comprisebetween 15 and 25 of the terrestrial animal biomass andthrive in most ecosystems on almost every landmass onEarth By comparison the total estimatedbiomass (weight) ofall ants worldwide equates to the total estimated biomass ofall humans Their complex social organization in colonieswith problem-solving abilities division of labor and bothindividual and whole colony communication via complexbehavioral and pheromone signaling may account for theirsuccess in so many environments Some ant species (egFormica rufa-group) are known to build colonies on activeearthquake faults and have been found to change behaviorhours in advance of earthquakes [294] thus demonstratingpredictive possibilities Ants can modify habitats influencebroad nutrient cycling spread seeds tap resources anddefend themselves Ants co-evolvedwith other specieswhichled to many different kinds of mutual beneficial and antag-onistic relationships

Ants (eg Solenopsis invictus) are long known to besensitive to magnetic fields both natural and manmade[295] Ants (eg Atta colombica) like birds have beenfound to be sensitive to the Earthrsquos natural fields and to useboth a solar compass on sunny days as well as a magneticcompasswhen there is cloud cover [296] Jander and Jander[297] similarly found that the weaver ant (Oecophylla spp)had amore efficient light compass orientation with amuchless efficient magnetic compass orientation suggestingthat they switch from the former to the latter when visualcelestial compass cues become unavailable There is evi-dence from Esquivel et al [298] that such magneto-reception is due to the presence of varying sized magnetiteparticles and paramagnetic resonance in fire ants (Sol-enopsis spp) But Riveros and Srygley [299] found a morecomplex relationship toward a magnetic compass ratherthan the presence of magnetite alone when leafcutter ants(Atta columbica) were subjected to a brief but strongmagnetic pulse which caused complete disorientationregarding nest-finding They found external exposurescould interfere with antsrsquo natural magnetic compass inhome path integration which indicated evidence of acompass based on multi-domain andor super-paramagnetic particles rather than on single-domain par-ticles like magnetite

Acosta-Avalos et al [300] found that fire ants aresensitive to 60 Hz alternating magnetic fields as well asconstant magnetic fields changing their magnetic orien-tation and magnetosensitivity depending on the relationbetween both types of magnetic fields Alternating currenthad the ability to disrupt ant orientation raising thequestion of effects to wild species from underground wir-ing and the common practice of powerline utility com-panies using the Earth as a neutral return pathway tosubstations creating stray current along the way [99]

Camelitepe et al [301] tested black-meadow antsrsquo(Formica pratensis) response under both natural geomag-netic and artificial earth-strength static EMFs (245 μT)They found that under the natural geomagnetic field whenall other orientational cues were eliminated there wassignificant heterogeneity of ant distribution with the ma-jority seeking geomagnetic north in darkness while underlight conditions ants did not discriminate geomagneticnorth Under artificial EMF exposure however ant orien-tation was predominantly on the artificial magnetic NSaxis with significant preference for artificial north in bothlight and dark conditions This indicated EMF abilities toalter ant orientation

Ants are also shown to react to RFR [302 303] Cam-maerts et al [304] found that exposures to GSM 900MHz at00795 μWcm2 significantly inhibited memory and

Levitt et al EMF and wildlife 27

association between food sites and visual and olfactorycues in ants (Myrmica sabuleti) and eventually wiped outmemory altogether Subsequent exposure after a brief re-covery period accelerated memoryolfactory loss within afew hours vs a few days indicating a cumulative effecteven at very low intensity The overall state of the exposedant colonies eventually appeared similar to that exhibitedby honey bee (Apis mellifera) colony collapse disorderAlthough the impact of GSM900MHz radiationwas greateron the visual memory than on the olfactory memory theresearchers concluded that such exposures mdash common tocell phonestowers mdash were capable of a disastrous impacton a wide range of insects using olfactory andor visualmemory including bees Many ant species (eg Lasiusneglectus Nylanderia fulva Camponotus spp Hymenopteraformicidae Solenopsis invicta among others) are attractedto electricity electronic devices and powerlines therebycausing short circuits and fires One hypothesis [305] is thatthe accumulation of ants in electrical equipment may bedue to a few foraging ldquoworker antsrdquo seeking warmth andfinding their way into small spaces completing electricalcontacts which then causes a release of alarm exocrinegland pheromones that attract other ants which then gothrough the same cycle In their study they found thatworkers subjected to a 120 V alternating-current releasedvenom alkaloids alarm pheromones and recruitmentpheromones that elicited both attraction and orientation inants as well as some other unknown behavior-modifyingsubstances But given how ants are affected by EMFs ingeneral it is likely that an attractant factor is also involvednot just warmth and small spaces

There is evidence that ants use their antennae asldquoantennasrdquo in two-way electrochemical communicationsOver 100 hundred years ago Swiss researcher AugusteForel [306] removed the antennae of different species ofants and put them together in one place What would havenormally evoked aggressive behaviors among the differentspecies did not occur and they got along as if belonging tothe same colony To Forel this indicated an ability of antantennae to help different ant species identify each other

Two mechanisms in ants have long been known forchemical receptivity as well as electromagnetic sensitivityRecently Wang et al [307] found evidence that chemicalsignals located specific to antennae vs other body areasdrew more attention from non-nest mates When cuticularhydrocarbons (CHCs) were removed by a solvent fromantennae non-nest mates responded less aggressivelythan to other areas of the body indicating that antennaereveal nest-mate identity conveying and receiving socialsignals Regarding magnetoreception magnetic measure-ments [308ndash310] found the presence of biogenic magnetite

was concentrated in antennae and other body parts of theant Pachycondyla marginata De Oliveira et al [311] alsofound evidence of magnetite and other magnetic materialsimbedded in various locations of antennae tissue inP marginata indicating that antennae function as magne-toreceptors The amount of magnetic material appearedsufficient to produce a magnetic-field-modulated mecha-nosensory output and therefore demonstrated a magneto-receptiontransduction sense in migratory ants

Ticks

Ticks are members of the order Arachnida shared withscorpions and spiders Recent papers in a tick species(Dermacentor reticulates) mirrors an attraction to somefrequencies but not others Vargovaacute et al [312 313] foundthat exposure to RFRmaybe apotential factor altering bothpresence and distribution of ticks in the environmentStudies were conducted to determine potential affinity ofticks for RFR using radiation-shielded tubes (RST) undercontrolled conditions in an electromagnetic compatibilitylaboratory in an anechoic chamber Ticks were irradiatedusing a Double-RidgedWaveguide Horn Antenna to RF-EMFat 900 and 5000 MHz 0 MHz served as control Resultsfound that 900 MHz RFR induced a higher concentration ofticks on the irradiated arm of RSTwhereas at 5000MHz ticksescaped to the shielded arm In addition 900 MHz RFR hadbeen shown to cause unusual specific sudden tick move-ments during exposure manifested as body or leg jerking[312] These studies are the first experimental evidence of RFRpreference and behavioral changes in D reticulates with im-plications forRFR introduced into thenatural environment bydevices and infrastructure In a further study Frątczak et al[314] reported that Ixodes ricinus ticks were attracted to900 MHz RFR at 01 μWcm2 particularly those infected withRickettsia (spotted fever)

RFR may be a new factor in tick distribution alongwith known factors like humidity temperature and hostpresence causing concentrated non-homogenous ormosaic tick distribution in natural habitats Tick preferencefor 900 MHz frequencies common to most cell phones haspossibly important ecological and epidemiological conse-quences Increasing exposures from use of personal de-vices and infrastructure in natural habitats where ticksoccur may increase both tick infestation and diseasetransmission Further studies need to investigate thisworkgiven the ubiquity of ticks today their northward spreaddue to climate change in the Northern Hemisphere and theincreasing and sometimes life-threatening illnesses theytransmit to humans pets and wildlife alike

28 Levitt et al EMF and wildlife

Monarch butterflies

The American Monarch butterfly (D plexippus) has fasci-nated researchers for over 100 years as it is the only insectknown to migrate in multi-generational stages [315ndash319]with the ability to find their exact birthplace on specificmilkweed plants (Asclepias spp) at great distances acrossland and oceans

Monarchs (D plexippus) found across Southern Can-ada the United States and South America are generallydivided by the Rocky Mountains into eastern and westernmigratory groups Their population has precipitouslydeclined by 994 since the 1980s (85 of that since 2017)and by 90 in the past two decades in both western andeastern populations [13 15] These steep declines are fromnumerous anthropogenic causes and may have alreadycrossed extinction thresholds thereby leaving us bereft notonly of their beauty and inspiration but also the perfectmodel for long-distance animalmigration study in general

Monarch butterflies are among North Americarsquos mostbeloved invertebrates They have for centuries navigatedthousands of mileskilometers in an iconic fall migrationfrom southern Canada and the mid- and northeastern USto a small area of about 800 square miles (2072 squarekilometers) in Central Mexico where they once winteredover in the millions in small remote oyamel fir forests Bythe time they reach their final destination some will havetraveled distances exceeded only by some migratoryseabird species The monarch is the only insect known tomigrate annually over 3000miles (4828 km) atsim 250miles(402 km) per day in the fall from the Canadian border toMexico and in the springtime back again Similar to somebird species it is the only butterfly known to have a two-way migration pattern Monarchs are only followed byarmy cutwormmoths (Euxoa auxiliaris) whichmaymigrateseveral thousand kilometers to high elevation sites in theRocky Mountains to escape lowland heat and drought

But monarchs are more interesting than for this oneamazing migrational feat alone How they do this is a long-standing mystery since their entire lifecycle includingtheir two-stage spring return migration is multi-generational indicating genetic factors in directionalmapping since the final return fall migration south cannotbe considered ldquolearnedrdquo Several multifaceted mecha-nisms must come into play as well as little understoodcomplexities in how those mechanisms cooperate andtrade off with each other under different environmentalcircumstances Monarchs also go from solitary insectsduring early developmental stages confined to specificlocations then exhibit social insect behaviors after thethird generation has reached northern latitudes and turned

south during the final fall migration And all of this hap-pens in a brain the size of a grain of sand

Reppert et al [320] published an excellent review in2010 on the complexities of monarch migration noting ldquohelliprecent studies of the fall migration have illuminated themechanisms behind the navigation south using a time-compensated sun compass Skylight cues such as the sunitself and polarized light are processed through both eyesand likely integrated in the brainrsquos central complex thepresumed site of the sun compass Time compensation isprovidedbycircadianclocks thathaveadistinctivemolecularmechanism and that reside in the antennae Monarchs mayalso use a magnetic compass because they possess twocryptochromes that have the molecular capability for light-dependent magnetoreception Multiple genomic approachesare being utilized to ultimately identify navigation genesMonarch butterflies are thus emerging as an excellent modelorganism to study the molecular and neural basis of long-distancemigrationrdquoReppert anddeRoode [321] updated thatinformation in 2018

Although it has been known for some time that mon-archs use a circadian rhythm time-compensated direc-tional sun compass [316 322ndash338] many questions remainabout its dynamics and concerns regarding effects fromradiation

Monarch antennae are known to contain magnetite[339 340] and cryptochromes [335 336 341 342] mdash bothunderstood to play a role in magnetoreception (seeldquoMechanismsrdquoabove) One early study by Jones and Mac-Fadden [343] found magnetic materials located primarilyin the head and thorax areas of dissected monarchs Morerecently Guerra et al [16] found convincing evidence thatmonarchs use a magnetic compass to aid their longest fallmigration back to Mexico Those researchers used flightsimulator studies to show that migrants possess an incli-nation magnetic compass to assist fall migration towardthe equator They found this inclination compass is light-dependent utilizing ultraviolet-Ablue light between 380and 420 nm and noted that the significance of light(lt420 nm) for an inclination compass function had notbeen considered in previous monarch studies They alsonoted that antennae are important for an inclinationcompass since they contain light-sensitive magneto-sensors Like some migratory birds the presence of aninclination compass would serve as an orientation mech-anism when directional daylight cues are impeded bycloudy or inclement weather or during nighttime flight Itmay also augment time-compensated sun compass orien-tation for appropriate directionality throughout migrationThe inclination compass was found to function at earth-strength magnetic fields an important metric

Levitt et al EMF and wildlife 29

The question remains Can the magnetic compass inmonarchs be disrupted by anthropogenic EMF like it doeswithgeomagnetic orientation inmigratorybirds [213] There issome indication this is possible Perez et al [330] foundmonarchs completely disorient after exposure to a strongmagnetic field (04-T MF for 10 s or approximately 15000times the Earthrsquos magnetic field) immediately before releasevs controls This is a high exposure but within range of man-made exposures today very close to powerlines

Bees wasps and others

Pollinators bees in particular are keystone specieswithout which adverse effects would occur throughoutfood webs and the Earthrsquos entire biome were pollinators todisappear Because of their central role and accessibilityfor research bee studies have created a wealth of infor-mation including regarding anthropogenic EMFs

Bees mdash especially honey and bumble bees mdash areanother iconic insect species beloved for their role inpollination honey propolis royal jelly and beeswax pro-duction their critical importance to our food supply andtheir crucial role in global ecological health and stabilityFound on every continent except Anarctica wherever thereare flowering plants requiring insect pollination there areover 16000 known species of bees in seven different bio-logical families consisting of four main branches Somespecies live socially in colonies while others are solitaryThe western honey bee (Apis mellifera) is the best knownand most studied due in part to its central role in agricul-ture Bees feed on nectar for energy and pollen for proteinnutrients and have co-evolved with many plant species inastoundingly complex ways They are also highly sensitiveto both natural and anthropogenic EMFs Beeswax itselfhas electrical properties [50]

Human apiculture has been practiced since the time ofancient Egyptian and Greek cultures and bees have beenclosely studied since the 1800s Almost all bee speciesincluding commercially raised and wild species are underdecades-long multiple assaults These include from pesti-cides herbicides climate change various bacterialviraldiseases infestations from parasitic mite species mdashparticularly Apis cerana Varroa destructor and Varroajacobsoni beginning in the mid-1980s mdash and predationfrom introduced species that attack bees directly (eg theinvasive giant bee-eating hornet Vespa mandarinia) aswell as alter plant ecology over time to adversely affect beefood supply Somehave suggested that vanishing beesmayalso have to do with premature aging due to environmen-tally caused shortened telomeres [344]

Whole colony collapse disorder (CCD) is the mostdramatic manifestation of domesticated bee demise inwhich worker bees abruptly disappear from a hive withouta trace resulting in an empty hive with perhaps aremaining queen and a few worker bees despite ampleresources left behind Few if any dead bees are ever foundnear the hive CCDwas first described in the US in 2006 inFlorida in commercial western honey bee colonies VanEnglesdorp et al [345] quantified bee losses across allbeekeeping operations and estimated that between 075and 100 million honey bee colonies died in the UnitedStates over the winter of 2007ndash2008 Up until that surveyestimates of honey bee population decline had notincluded losses occurring during the wintering periodthus underestimating actual colony mortality

The same phenomenon had been described by bee-keepers in France in 1994 [346] mdash later attributed to thetiming of sunflower blooming and the use of imidacloprid(IMD) a chlorinated nicotine-based insecticide or ldquoneon-icotinoidrdquo being applied to sunflowers for the first time there[347] Similar to DDT but considered safer for mammalsincludinghumans neonicotinoidsare a slow-release class ofneurotoxins that block insect nervous systems via acetyl-choline receptors interferingwith neuronal signaling acrosssynapses Sublethal doses can interfere with bee navigation

Since then similar phenomena have been seenthroughout Europe [348] and some Asian countries Causalhypotheses included all of the above factors with varyingfoci on pesticide classes like neonicotinoids and geneti-cally modified crops but no single agent adequately ex-plains CCD Bromenshenk et al [349] however identifiedpathogen pairingco-infection with two previously unre-ported RNA virusesmdash V destructor-1 and Kakugo virusesand a new irridescent virus (IIV) (Iridoviridae) along withNosema ceranaemdash in North American honey bees that wereassociated with all sampled CCD colonies The pathogenpairing was not seen in non-CCD colonies Later cage trialswith IIV type-6 and N ceranae confirmed that co-infectionwith those two pathogens was more lethal to bees thaneither pathogen alone Still many questions remain

There are two national surveying groups in the USmdashthe US Department of Agriculture (USDA) which begansurveying managed bee populations in 2015 but fundingwas cut in late 2019 and the Bee Informed Partnership(BIP) a non-profit that coordinates with research facilitiesand universities Prior to USDArsquos funding cuts managedcolonies decreased from CCD by 40 [350] with an addi-tional 26 over the same quarter in 2019 [351] BIPrsquos surveyperiod for April 1 2018 through April 1 2019 found USbeekeepers lost an estimated 407 of their managedhoney bee colonies The previous year had similar annual

30 Levitt et al EMF and wildlife

losses of 401 The average annual rate of loss reported bybeekeepers since 2010ndash11 was 378 [352]

Also in theUS for the first time in 2016 seven species ofHawaiian yellow-faced bees (Hylaeus anthracinusHylaeus longiceps Hylaeus assimulans Hylaeus facilisHylaeus hilaris Hylaeus kuakea and Hylaeus mana) wereadded to the federal endangered species list as well as therusty patched bumble bee (Bombus affinis) which prior to thelate 1990s had been widely dispersed across 31 US states[353] Mathiasson and Rehan [354] examined 119 species inmuseum specimens in New Hampshire going back 125 yearsand concluded that 14 species found across New Englandwere on the decline by as much as 90 including the lesserstudied leafcutter and mining bees that nest in the groundunlike honeybees that nest in commercial hives or in treesshrubs and rock crevices in the wild

Worldwide many bee and other pollinator pop-ulations have also declined over the last two decadesManaged honey bee (Apis mellifera) colonies decreased by25over 20 years in Europe and 59over 58 years in NorthAmerica with many wild bumble bee populations inEurope and North America having gone locally extinct[355ndash358] But while dramatic range contractions havebeen seen not all bees in all places are declining somepopulations are growing depending on opportunistic andspecies-adaptability factors Formany species data are stillinsufficient of poor quality or nonexistent [359] In addi-tion bee declines can affect flora survival Miller-Struttmann et al [360] recorded flower declines of 60with 40 years of climate warming in alpine meadows mdashareas largely protected from land-use changes Insects arehighly sensitive to temperature changes

A comprehensive UK survey of pollinator species [361]found that of 353 wild bee and hoverfly species acrossBritain from 1980 to 2013 25 had disappeared from theplaces they had inhabited in 1980 Further estimates foundanet loss of over 27million in 06mi (1 km) grid cells acrossall species Declining pollinator evenness suggested losseswere concentrated in rare species Losses linked to specifichabitats were also identified with a 55 decline amongwild upland species while dominant crop pollinatorsincreased by 12 possibly due to agricultural businessinterventions The general declines found a fundamentaldeterioration in both wider biodiversity and non-croppollination services

There is no question that the huge diversity of polli-nator species across the planet is suffering and that lossescould be catastrophicwith an estimated 90ofwild plantsand 30 of world crops in jeopardy [362]

There is a likelihood that rising EMF background levelsplay a role Bees have been known for decades to have an

astute sense of the Earthrsquos DC magnetic fields [363 364]and rely on that perception for survival For centuriesbeekeepers had noticed curious movements in bee hivesbut Austrian ethologist Karl von Frisch finally interpretedthat activity in the 1940s winning the Nobel Prize in 1973for what came to be known as the honey bee ldquowaggledancerdquo Through complex circles and waggle patternsbees communicate the location of food sources to othermembers of the hive using the orientation of the sun andthe Earthrsquos magnetic fields as a gravity vector ldquodancingrdquoout a map for hive members to follow like naturersquos ownimbeddedGPS Bees also detect the sunrsquos direction throughpolarized light and on overcast days use the Earthrsquos mag-netic fields likely through the presence of magnetite intheir abdominal area and employ complex associativelearning and memory [365]

Building on the earlier work of Gould et al [119]Kobayashi and Kirschvink [52] noted that biogenicmagnetite in honey bees is located primarily in the anteriordorsal abdomen When small magnetized bits of wire wereglued over those areas it interfered with beesrsquo ability tolearn to discriminate magnetic anomalies in conditioningexperiments while nonmagnetized wire used in controlsdid not interfere [366] Kirschvink and Kobayashi [367]found that when pulse-remagnetization techniques wereused on bees trained to exit from a T-maze that north-exiting bees could be converted to a south-exiting directionsimilar to what was observed in magnetobacteria andartificial reorientation by Blakemore [113] Honeybeescould also be trained to respond to very small changes inthe geomagnetic field intensity [368] Valkova and Vacha[369] discussed the possibility that honey bees use acombination of both radical paircryptochromes andmagnetite to detect the geomagnetic field and use it fordirection like many birds

Given these sensitivities bees may be reacting nega-tively through muti-sensory mechanisms to numeroussources of anthropogenic multi-frequency interferenceBumble bees (Bombus terrestris) a solitary species andhoney bees (Apis mellifera) a social hive species areknown to detect weak electric fields in different behavioralcontexts using different sensorymechanisms Bumble beee-field detection is likely through mechanosensory hairs[370ndash372] while honey bees reportedly use their antennae[373] that are electro-mechanically coupled to the sur-rounding e-field taking place in the antennal Johnstonrsquosorgan Greggers et al [373] found that honey bee antennaeoscillate under electric field stimulation that can thenstimulate activity in the antennal nerve The latter occursdue to bees being electrically charged and thus subject toelectrostatic forces Erickson [374] found different surface

Levitt et al EMF and wildlife 31

potentials in bees when leaving or entering hives andColin et al [375] found seasonal variability between posi-tive and negative charges in resting bees It has also beenshown that honey bees with removed or fixed antennae areless able to associate food reward with electric field stimuliand that bees emanate modulated electric fields whenmoving their wings (at about 230 Hz) and body (at about165 Hz) during the waggle dance [373]

Electro-ecological interplay between flowers andpollinators has also been known since the 1960s and iscritical to pollen transfer from flowers to bees [376ndash378]It is known that as bees fly through the air they accu-mulate a positive charge Flowers on the other handwhich are electrically grounded through their root sys-tems tend to have a negative charge in their petalscreated by surrounding air that carries around 100 V forevery meter above ground The accumulating positivecharge around the flower induces a negative charge in itspetals which then interacts with the positive charge inbees In fact bees do not even need to land on flowers forpollen transfer to occur pollen can ldquojumprdquo from theflower to the bee as the bee approaches due to chargedifferentials between the two Thus it appears that beesand flowers have been ldquocommunicatingrdquo via electricfields all along [379] Bees can also learn color discrimi-nation tasks faster when color cues are paired with arti-ficial electric field cues similar to those surroundingnatural flowers but did not learn as readily in an elec-trically neutral environment [370]

This evidence points to floral e-fields being used in aco-evolutionary symbiotic relationship with bees Clarkeet al [370 371] even found that bumblebees can distin-guish between flowers that give off different electric fieldsas floral cues to attract pollinators Like visual cues floralelectric fields exhibit complex variations in pattern andstructure that bumblebees can distinguish contributing tothe myriad complex cues that create a pollinatorrsquos memoryof floral food sources And because floral electric fieldscanmdash and domdash change within seconds of being visited bypollinators this sensory ability likely facilitates rapid anddynamic ldquoinformation exchangerdquo between flowers andtheir pollinators Bumblebees can even amazingly useelectric field information to discriminate between nectar-rewarding and unrewarding flowers [370]

Bees locusts ELF-EMF

Bees are also known to be sensitive to anthropogenicELF-EMF In 1973Wellenstein [380] found that high ten-sion powerlines adversely affected honey bees in woodenhives This in part prompted the Bonneville Power

Administration an American federal agency operating inthe Pacific Northwest under the US Department of Energy(US DOE) to investigate in 1974 [381ndash384] the effects oftransmission lines on people plants and animalsincluding honey bees The industry group Electric PowerResearch Institute also followed up on bee research [385386] Both of those studies confirmed that transmission lineelectric fields can affect honey bees inside wooden hives aswood is a poor insulator and current can be induced whenhives are placed in electric fields whether metal is presentor not The strength of the current inside the hive wasinfluenced by the electric field strength hive height andmoisture conditions with effects noticeable when inducedcurrent exceeded 002ndash004 mA Depending on hiveheight this occurred in field strengths between 2 and 4 kVm Effects included increased motor activity with transientincrease in hive temperature excessive propolis produc-tion (a resinous material used by bees as a hive sealer)decreased colony weight gains increased irritability andmortality abnormal production of queen cells queen lossdecreased seal brood andpoor over-winter colony survival[387] Impacts were most likely caused by electric shocksinside the hives [386 388] Effects were mitigated withgrounded metal screenshielding of hives [385] howeverbees appeared unaffected by magnetic fields whichpermeate metal shielding The authors concluded that theshielding results indicated that bees were unaffected byflying through an external electric field up to 11 kVm butnoted that the study design could not reveal if subtle effectswere occurring

A more recent study of electric fields by Migdał [389]focused on honey bee behavioral effects on walkinggrooming flight stillness contact between individualsand wing movement They found that the selected fre-quency intensity and duration of exposure effects beesrsquobehavioral patterns Bees were exposed for 1 3 and 6 h toE-fields at 50 kVm 115 kVm 230 kVm or 345 kVm(with controls under E-field lt20 kVm) Within theexposed groups results showed that exposure for 3 hcaused decreased time that bees spent on select behaviorsas well as the frequency of behaviors whereas after both 1and 6 h the behavioral parameters increased within thegroups The researchers concluded that a barrier allowingbehavioral patterns to normalize for some periods wasindicated although none of the exposed groups returned toreference values in controls which adhered to normalbehavioral patterns Bees may have compensatory win-dows that appear to be both time and intensity dependentfor E-fields The significance of this study is that bees mustaccomplish certain activities mdash like flight frequency andthe honey bee lsquowaggle dancersquo noted above mdash that are

32 Levitt et al EMF and wildlife

critical for life expectancy and survival Even slightsequential disturbances may have cascading effects

In an early-1988 study Korall et al [390] also foundeffects to bees from magnetic fields (MF) Bursts compa-rable to some of todayrsquos pulsed exposures of artificial MF at250 Hz mdash the frequency of buzzing during the waggledance mdash were applied parallel to natural EMF field linesand induced unequivocal lsquojumpsrsquo of misdirection by up to+10deg in bees during the waggle dance This alone couldcause directional confusion in hives Continuous fields of250 Hz with bursts perpendicular to the static MF howevercaused no effects They concluded that a resonance rela-tionship other than classic resonance models was indi-cated (see ldquoMechanismsrdquo above) This early work hasimplications for subsequent digital pulsing and all wirelessbroadband technology

More recent work on honey bees and ELF-EMF byShepherd et al [209] in 2018 found that acute exposure to50 Hz fields at levels from 20ndash100 μT (at ground level un-derneath powerline conductors) to 1000ndash7000 μT(within 1 m of the conductors) reduced olfactory learningforaging flight success toward food sources and feeding aswell as altered flight dynamics Their results indicated that50 Hz ELF-EMFs from powerlines is an important envi-ronmental honey bee stressor with potential impacts oncognitive and motor abilities

Some wasp species have also been found sensitive toELF-EMF Pereira-Bomfim et al [391] investigated themagnetic sensitivity of the social paper wasp (Polybiapaulista) by analyzing wasp behavior in normal geomag-netic fields and in the presence of external magnetic fieldsaltered by either permanent magnets (DC fields) or byHelmholtz coils (AC fields) They evaluated the change inforaging rhythm and colony behavior as well as the fre-quency of departinghomeward flights and the behavioralresponses of worker wasps located on the outer nest sur-face They found that the alteredmagneticfield from theDCpermanent magnet produced an increase in the frequencyof departing foraging flights and also that wasps groupedtogether on the nest surface in front of the magnet withtheir heads and antennae pointing toward the perturbationsource possibly indicating a response to a potential threatas a defense strategy Controls showed no such groupingbehavior The AC fields created by the Helmholtz coils alsoincreased foraging flights but individuals did not showgrouping behavior The AC fields however induced waspworkers to perform ldquolearning flightsrdquo They concluded thatfor the first time P paulista demonstrated sensitivity to anartificial modification of the local geomagnetic field andthat mechanisms may be due to both cryptochroneradicalpairs and magnetite

Another flying insect model mdash desert locust (Schisto-cerca gregaria)mdashwas found susceptible to entrainment byELF-EMF In a complex study Shepherd et al [392]analyzed acute exposure to sinusoidal AC 50 Hz EMF (fieldstrength range 10 to 10000 μT) vs controls on flights ofindividual locusts tethered between copper wire coilsgenerating EMFs at various frequencies and recorded onhigh-speed video Results found that acute exposure to50 Hz EMFs significantly increased absolute change inwingbeats in a field-strength-dependent manner Applyinga range of ELF-EMF close to normal wingbeat occurancethey found that locusts entrained to the exact frequency ofthe applied EMF They concluded that ELF exposure canlead to small but significant changes in locust wingbeatslikely due to direct acute effects on insect physiology (vscryptochrome ormagnetite-basedmagnetoreception) andor behavioral avoidance responses to molecularphysio-logical stressWyszkowska et al [393] also found effects onlocustsmdash exposure to ELF-EMF above 4mT led to dramaticeffects on behaviour physiology and increased Hsp70protein expression Such higher exposures may be foundnear high tension lines

Bees RF-EMF

The effects of RF-EMF on bees is of increasing interest sincethat is the fastest rising EMF environmental exposure of thepast 30 years [369] Beginning in the early 2000s studies ofcell phones placed in the bottom of hives began to appearHoney bees showed disturbed behavior when returning tohives after foraging and under various RFR exposures[394ndash396] Early methodologies however were not welldesigned or controlled For instance Favre [397] foundincreased piping mdash a distress signal that honey bees giveoff to alert hive mates of threats andor to announce theswarming process Both active and inactive mobile phonehandsetswere placed in close proximity to honey beeswithsounds recorded and analyzed Audiograms and spectro-grams showed that active phone handsets had a dramaticeffect on bee behavior in inducedworker piping This studywas criticized by Darney et al [398] for using music in theactive RFR exposurewhichmay have introduced a variablecapable of affecting bee piping in response to the addedsound alone

In a complex study Darney et al [398] tested highfrequency (HF) and ultra high frequency (UHF) used inRFID technology in order to develop a method to auto-matically record honey bees going in and out of hives Theyglued RFID tags onto individual bee dorsal surfaces thatwere detected at the hive entrance by readers emitting HFradio waves They then looked for possible HF adverse

Levitt et al EMF and wildlife 33

effects on honey beesrsquo survival Eight-day-old honey beeswere exposed to HF 1356 MHz or UHF 868 MHz RFR for 2 hsplit into ON and OFF periods of different durations Deadbees were counted daily with cumulative mortality rates ofexposed and non-exposed honey bees compared sevendays after exposure Two out of five experimental condi-tions found increased mortality once after HF and onceafter UHF exposure with OFF duration of 5 min or moreafter which they recommended limiting honey bee expo-sure to RFR to less than 2 h per day They also curiouslyconcluded that the RFID parameters they used for moni-toring hive activity presented no adverse effects but themultifrequency peak exposures and RFID attachmentsneed further study in light of other works on RFID effects(see Part 1 for discussion of RFID)

In another study using an active cell phone attached tohive frames Odemer and Odemer [399] investigated RFReffects on honey bee queen development and mating suc-cess Control hives had an inactive cell phone attachedAfter exposing honey bee queen larvae to GSM 900 MHzRFR during all stages of pre-adult development (includingpupation) hatching of adult queens was assessed 14 daysafter exposure and mating success after an additional11 days They found that chronic RFR exposure signifi-cantly reduced honey bee queen hatching that mortalitiesoccurred during pupation but not at the larval stages thatmating success was not adversely affected by the irradia-tion and that after exposure surviving queenswere able toestablish intact colonies They therefore determined thatmobile phone radiation had significantly reduced thehatching ratio but not mating success if queens survivedand if treated queens successfully mated colony devel-opment was not adversely affected Even though theyfound strong evidence of mobile phone RFR damage topupal development they cautioned its interpretationnoting that the studyrsquos worst-case exposure scenario wasthe equivalent of a cell phone held to a userrsquos head not at alevel found in typical urban or rural hive settings Theyconcluded that while no acute negative effects on beehealth were seen in the mid-term they also could not ruleout effects on bee health at lower chronic doses such asfound in ambient environments and urgently called forlong term research on sublethal exposures present inmajorcity environments

Sharma andKumar [400] found similar abnormalitiesin honey bee behavior when they compared the perfor-mance of honey bees in RFR exposed and unexposedcolonies Two of four test colonies were designated andeach equipped with two functional cell phones mdash a highexposuremdash placed on two different hive side walls in callmode at GSM 900 MHz The average RFR power density

was measured at 8549 μWcm2 (568 Vm electric field)One control colony had a dummy phone the other had nophone Exposure was delivered in 15 min intervals twiceper day during the period of peak bee activity Theexperiment was performed twice a week during Februaryto April It covered two brood cycles with all aspects ofhive behavior observed including brood area comprisingeggs larvae and sealed brood queen proficiency in egg-laying rate foraging flight behavior returning abilitycolony strength including pollen storage and other var-iables Results included a significant decline in colonystrength and egg laying and reduced foraging to the pointwhere there was no pollen honey brood or bees by theend of the experiment One notable difference in thisstudy was that the number of bees leaving the hivedecreased following exposure There was no immediateexodus of bees as a result of exposure mdash instead beesbecame quiet still andor confused ldquohellipas if unable todecide what to dohelliprdquo the researchers said Such aresponse had not been reported before The authorsconcluded that colony collapse disorder is related to cellphone radiation exposures

Vilić et al [401] investigated RFR and oxidative stressand genotoxicity in honey bees specifically on the activityof catalase superoxide dismutase glutathione S-trans-ferase lipid peroxidation levels and DNA damage Larvaewere exposed to 900 MHz RFR at field levels of 10 23 41and 120 Vmminus1 for 2 h At a field level of 23 Vmminus1 the effect of80AM 1 kHz sinusoidal and 217 Hz modulation were alsoinvestigated They found that catalase activity and the lipidperoxidation levels significantly decreased in larvaeexposed to the unmodulated field at 10 V mminus1 (27 μWcm2)compared to the control Superoxide dismutase andglutathione S-transferase activity in honey bee larvaeexposed to unmodulated fields were not statisticallydifferent compared to the control DNA damage increasedsignificantly in larvae exposed to modulated (80 AM at1 kHz) field at 23 V mminus1 (140 μWcm2) compared to controland all other exposure groups Their results suggested thatRFR effects in honey bee larvae manifested only aftercertain EMF exposure conditions Interestingly they foundthat increased field levels did not cause a linear dose-response in any of the measured parameters whilemodulated RFR produced more negative effects than thecorresponding unmodulated field They concluded thatwhile honey bees in natural environments would not beexposed to the high exposures in their experiments theresults indicated additional intensive research is needed inall stages of honey bee development since the cellular ef-fects seen could affect critical aspects of bee health andsurvival

34 Levitt et al EMF and wildlife

Kumar et al [402] also found biochemical changes inworker honey bees exposed to RFR A wooden box wasdesigned with glass on the front and back and wire gauzefor ventilation on two sides for both exposed bees andcontrols Cell phones (same make model and networkconnection) were kept in listen-talk mode for 40 min Atintervals of 10 20 and 40 min 10 exposed and 10 controlbees were collected at the same times Hemolymph wasthen extracted from the inter-segmental region of bee ab-domens and analyzed Results included increased con-centration of total carbohydrates in exposed bees in the10 min exposure period compared to unexposed beesIncreasing the exposure time to 20min resulted in a furtherincrease in the concentration but exposure at 40min had areverse effect with declines in carbohydrate concentrationalthough it was still higher than controls Hemolymphglycogen and glucose content also showed the sameexposure pattern mdash increase in content up to 20 min afterwhich a slight decline that was still higher than controlsChanges in total lipidscholesterol mdash the major energy re-serves in insects mdash can affect numerous biological pro-cesses Some lipids are crucial membrane structurecomponents while others act as rawmaterials in hormonesand pheromones Changes in these parameters are signif-icant to every biological activity including reproductionAlso of interest in this study was that as exposure timeincreased the bees appeared to have identified the sourceof disturbance There was a large scale movement ofworkers toward the talk-mode (with higher RFR exposureduring transmission function) but not the listening modeBees also showed slight aggression and agitation withwing beating The researchers hypothesized that thisincreased activity could be responsible for increased en-ergy use thereby accounting for the decrease in concen-tration of carbohydrates and lipids in the 40 min exposedsample The researchers concluded that cell phone radia-tion influences honey bee behavior and physiologySharma [403] had also reported increased glycogen andglucose levels in exposed honey bee pupa

It must be pointed out that the cell phone emissionconditions used in some experiments are questionable inparticular where there was no detail regarding how thephones were activated to achieve emission

Not all studies demonstrated adverse effects Mall andKumar [404] found no apparent RFR effects on brood rearinghoney production or foraging behavior in honey bees in hiveswith cell phones inside or near a cell tower and Mixon et al[405] also found no effects of GSM-signal RFR on increasedhoney bee aggression They concluded that RFR did notimpact foraging behavior or honey bee navigation andtherefore was unlikely to impact colony health

Although there are several anectodal reports of insectlosses near communication towers there are only ahandful of ambient RFR field studies conducted on in-vertebrates thus far In the first large survey of wild polli-nating species at varying distances from cell towers Laacutezaroet al [406] found both positive and negative effects fromRFR in a broad range of insects on two islands (Lesvos andLimnos) in the northeastern Aegean Sea near GreeceMeasured ambient RFR levels included all frequencyranges used in cell communications broadcast RFR isabsent on the islands RFR values did not significantlydiffer between islands (Lesvos 027 plusmn 005 Vm Limnos021 plusmn 004 Vm v3 2 = 008 p=0779) and did not decreasewith the distance to the antenna possibly they hypothe-sized because some sampling points near the antennamayhave beenoutside or at the edge of the emission lobes Theymeasured RFR at four distances of 50 100 200 and 400 m(164 328 656 and 1312 ft respectively) from 10 antennas(5 on Lesvos Island and 5 on Limnos Island) and correlatedRFR values with insect abundance (numbers of insects)and richness (general health and vitality)mdash the latter onlyfor wild bees and hoverflies The researchers conductedcareful flowering planttree- and- insect inventories inseveral low-lying grassland areas including for wild beeshoverflies bee flies other remaining flies beetles butter-flies and of various types Honey beeswere not included inthis study as they are a managed species subject tobeekeeper decisions and therefore not a wild species OnLesvos 11547 insects were collected and on Limnos 5544Varied colored pan traps for both nocturnal and diurnalsamples were used Results found all pollinator groupsexcept butterflieswere affected by RFR (both positively andnegatively) and for most pollinator groups effects wereconsistent on both islands Abundance for beetles waspsand hoverflies significantly decreased with RFR but overallabundance of wild bees and bee flies significantlyincreased with exposure Further analysis showed thatonly abundance of underground-nesting wild bees waspositively related to RFR while wild bees nesting aboveground were not affected RFR effects between islandsdiffered only on abundance of remaining flies On speciesrichness RFR tended to only have a negative effect onhoverflies in Limnos Regarding the absence of effects seenin butterflies they hypothesized that the pan trap collec-tion method is not efficient for collecting butterflies (but-terflies accounted for only 13 of total specimens) andthat a different samplingmethodmight produce a differentresult They concluded that with RFRrsquos negative effects oninsect abundance in several groups leading to an alteredcomposition of wild pollinators in natural habitats it waspossible this could affect wild plant diversity and crop

Levitt et al EMF and wildlife 35

production They further said the negative relationshipbetween RFR on the abundance of wasps beetles andhoverflies could indicate higher sensitivity of these insectsto EMFs Potentially more EMF-tolerant pollinators suchas underground-nestingwild bees andbeefliesmayfill thevacant niches left by less tolerant species thus resulting intheir population increases Another possible explanation isthat EMFs may have particularly detrimental effects onmore sensitive larval stages and if so larvae developingabove ground (many beetles wasps hoverflies) may bemore vulnerable than those developing underground sincethe former could be exposed to higher radiation levels

In another field study Taye et al [407] placed fivehives from December to May at varying distances of 1000500 300 200 and 100 m (3280 1640 984 656 and 328 ftrespectively) from a cell tower in India to measure flightactivity returning ability and pollen foraging efficiency inhoney bees (Apis cerana F) They foundmost effects closestto towers with the least returning bees at 100 m distancefrom the tower Maximum foraging and return ability to thecolonies was seen at 500 m followed by 1000 m and indescending order at 300 and 200 m with the fewestreturning bees at 100 m from the tower The study alsofound that if bees returned the pollen load per minute wasnot significantly affected

Vijver et al [408] however challenged the accuracy ofdistance from towers that is often used as a proxy for EMFgradients such as the study above In a field study in TheNetherlands the researchers tested exposure to RFR from acell base station (GSM 900 MHz) on the reproductive ca-pacity of small virgin invertebrates during the most sensi-tive developmental periods spanning preadolescent tomating stages when reproductive effects would most likelybe seen Careful RFR field measurements were taken todetermine null points in order to see if distance fromemitters is a reliable RFR exposure model in field studiesThey exposed four different invertebrate hexapod speciesSpringtails (Folsomia candida) predatory lsquobugsrsquo (Oriuslaevigatus) parasitic wasps (Asobara japonica) and fruit-flies (D melanogaster) were placed in covered pedestalcontainers within the radius of approximately 150 m of a900 MHz mobile phone base station for a 48-h period Sixcontrol groups were placed within 66 ft (2 m) of thetreatment groups and covered in Farady cages Afterexposure all groups were brought to the laboratory tofacilitate reproduction with resulting fecundity and num-ber of offspring then analyzed Results showed that dis-tance was not an adequate proxy to explain dose-responseregressions After complex data synthesis no significantimpact from the exposure conditions measures of centraltendency or temporal variability of EMF on reproductive

endpoints were found although there was some variabilitybetween insect groups As seen in other studies distance isoften used to create a gradient in energy exposures instudies but this study found the intensity of the transmitterand the direction of transmission to be more relevant asdid Bolte andEikelboom [409 410] The direction and tilt ofthe transmitter determines whether the location of interestin field studies is in the main beam In some instances thecloser promixity to the transmitter provided lower readingsthan further away which they found between two loca-tions They also noted that the organisms selected in thestudy were small in size springtails have a body length onaverage of 2 mm wasps are about 3 mm insect sizes from14 to 24 mm with the largest organisms tested being fe-male fruit flies at about 25 mm length and males slightlysmaller Due to size limited absorption and little energyuptake capacity none of these insects are efficient whole-body receptors for 900 MHz waves with a wavelength ofapproximately 13 in (33 cm) But they further noted that thiswas a linear regression study and that biological effects areoften non-linear However finding no distinct effects didnot exclude physiological changes They concluded thatbecause of RFR exposurersquos increasing ubiquity urgentattention to potential effects on biodiversity is needed

The issue of insect size nonlinearity and antenna tiltdirection are factors of critical importance with 5G radia-tion which will create extremely complex near- and- far-field ambient exposures to species in urban and rural en-vironments alike not only fromadensification of small cellantennas close to the ground but also from increased sat-ellite networks circling in low Earth orbits (see Part 1) Therange of frequencies used for wireless telecommunicationsystems will increase from below 6 GHz (2G 3G 4G andWiFi) to frequencies up to 120 GHz for 5G which due tosmaller wavelengths is therefore a better resonant matchfor small insects An alarming study by Thielens et al [411]drawing on numerous robust studies of RFRrsquos decades-long use as a thermal insecticide modeled absorbed RFRin four different types of insects as a function of fre-quency alone from 2 to 120 GHz A set of insect modelswas obtained using novel Micro-CT (computer tomogra-phy) imaging and used for the first time in finite-difference time-domain electromagnetic simulationsAll insects showed frequency-dependent absorbed po-wer and a general increase in absorbed RFR at and above6 GHz in comparison to the absorbed RFR power below6 GHz Their simulations showed that a shift of 10of theincident power density to frequencies above 6 GHzwould lead to an increase in absorbed power between3ndash370 mdash a large differential of serious potentialconsequence to numerous insect species

36 Levitt et al EMF and wildlife

Using a similar approach Thielens et al [412] focusedon the western honey bee (Apis mellifera) with RF-EMFusing a combination of in-situ exposure measurementsnear bee hives in Belgium and numerical simulationsAround five honey bee models were exposed to planewaves at frequencies from 06 to 120 GHz mdash frequenciescarved out for 5G Simulations quantified whole-bodyaveraged RFR absorbed as a function of frequency andfound that the average increased by factors of 16ndash121(depending on the specimen) when frequency increasedfrom 06 to 6 GHz for a fixed incident electric field strengthA relatively small decrease in absorption was observed forall studied honey bees between 12 and 120 GHz due tointerior attenuation RFR measurements were taken at 10bee hive sites near five different locations Results foundaverage total incident RFR field strength of 006 Vm thosevalues were then used to assess absorption and a realisticrate was estimated between 01 and 07 nW Theyconcluded that with an assumed 10 incident powerdensity shift to frequencies higher than 3 GHz this wouldlead to an RFR absorption increase in honey bees between390 and 570 mdash a frequency shift expected with thebuildout of 5G

The two previous studies alone should give pauseregarding environmental effects to invertebrates in thesehigher 5G frequency ranges

Kumar [413] noted that RFR should be included ascausal agents of bee CCD and that test protocols need to bestandardized and established Standardization is criticalsincemany studies conductedwith cell phones in hives areof very uneven quality and only indicative of potential ef-fects Placing cell phones in hives and assuming that RFR isthe only exposure is inaccurate and misleading ELF-EMFsare always present in all telecommunications technologyusing pulsed and modulated signals [414] All of thesecharacteristics have been found to be highly biologicallyactive apart from frequency alone Such studies are likelycapturing ELF effects without identifying them All aspectsof transmission including transmission engineering itselffrom towers need to be considered to determine accurateexposures and delineate causative agents Vibration andheatmust also be consideredmdash cell phones in transmissionmode could raise hive temperature quickly and bees arehighly temperature sensitive Due to ldquowaggle dancerdquo spe-cifics in creating foraging ldquoroadmapsrdquo bees should not beartificially relocated from hives to determine return abilityafter EMF exposure They may be confused by relocationalone adversely affecting their return abilities Such testsalso involve only one stressor when there are multiplestressors on insect species today Understanding such co-factors is critical in determining accurate data and

outcomes [415 416] Translating laboratory studies to fieldrelevance has always been problematic but understandingEMF effects to insects has become urgent with everincreasing low-level ambient exposure from devices andinfrastructure especially in light of the new 5G networksbeing built There are numerous variables that studies haveyet to factor in All of the above indicates a critical need tostandardize experimental protocols and to take electro-ecology far more seriously especially regarding aerialspecies in light of 5G

Aquatic environments

There are fundamental electrical differences in conduc-tivity (how well a material allows electric current to flow)and resistivity (how strongly amaterial opposes the flow ofelectric current) between air and water Through waterEMF propagation is very different than through air becausewater has higher permittivity (ability to form dipoles) andelectrical conductivity Plane wave attenuation (dissipa-tion) is higher in water than air and increases rapidly withfrequency This is one reason that RFR has not traditionallybeen used in underwater communication while ELF hasbeen Conductivity of seawater is typically around 4 Smwhile fresh water varies but typically is in the mSm rangethus making attenuation significantly lower in fresh waterthan in seawater Fresh water however has similarpermittivity as sea water There is little direct effect on themagnetic field component in water mediums propagationloss is mostly caused by conduction on the electric fieldcomponent Energy propagation continually cycles be-tween electric and magnetic fields and higher conductionleads to strong attenuationdissipation of EMF [98]

Because of these essential medium differences electro-receptormechanisms in aquatic speciesmay be very differentthan those previously described in aerial species since air is aless conductive and resistive medium with less attenuationThat is why RFR travels more easily and directly through airIn aquatic species electroreception may be a result of trans-mission via water directly to the nervous system throughunique receptor channels called Ampullae of Lorenzini [371]In frogs amphibians fish some worm species and othersreceptor channels may be through the skin as well as viamechanisms more common in aerial species such as in thepresence of magnetite (see ldquoMechanismsrdquo above) There canbe great variation in electroreceptive sensitivities in speciesinhabiting the two fundamentally different environmentsSome amphibian species however have physical charac-teristics that span both mediums and therefore varied mag-netoreception mechanisms

Levitt et al EMF and wildlife 37

Amphibians frogs salamandersreptiles regeneration abilities

Amphibians are the class of animals that include frogs

toads salamanders newts some reptiles and caecilians

The common term lsquofrogrsquo is used to describe thousands of

tailless amphibian species in theOrderAnura There are over

6300 anuran species recorded thus far with many more

likely disappearing today due to climate change and other

factors before we even knew they existed Informal distinc-

tions are made between frogs (thin-skinned species) and

toads (thick warty skins) but such distinctions are not used

for taxonomic reasons While the greatest concentration of

diverse frog species is in tropical rainforests they are widely

foundall over theworld from the tropics to subarctic regions

Most adult frogs live in fresh water andor on dry land while

some species have adapted to living in trees or underground

Their skin varies in all manner of colors and patterns from

graygreen and brownblack to bright redsyellowsFrog skin is smooth and glandular mdash something of

concern given nascent 5G technology (see Part 1)mdash and cansecrete toxins to ward off predators Frog skin is also semi-permeable which makes them highly susceptible to dehy-dration and pollutants With radical weather shifts due toclimate change and unpredictable swings betweenabnormal droughts followed by flooding in previouslyweather-stable regions environmentally sensitive am-phibians like frogs are considered bell-weather speciesFrequently time may be insufficient for some localregional species to regenerate in between radical weathercycles leading to population collapse

Since the 1950s there has been a significant decline infrog populations with more than one third of species todayconsidered threatened with extinction while over 120 spe-cies are already believed to have gone extinct since the1980s [10 417 418] This amphibian decline is consideredpart of an ongoing global mass extinction with populationcrashes as well as local extinctions creating grave impli-cations for planetary biodiversity [419] Amphibianextinction results are from climate change [420ndash422]habitat lossdestruction [423 424] introduced species[425] pollution [426] parasites [423 427] pesticides her-bicides and fungicides [428ndash430] disease [431ndash435] andincreased ultraviolet-B radiation [436ndash439] among othersAnthropogenic sound pollution may also affect amphibiancall rates and therefore impact reproduction [440] andartificial night lights affectmale green frog (Rana clamitausmelanota) breeding [441] Nonionizing electromagneticfields may also play a role [442]

McCallum [443] calculated that the current extinctionrate of amphibians could be 211 times greater than theirpre-anthropogenic natural ldquobackground extinctionrdquo ratewith the estimate rising 25000ndash45000 times if endan-gered species are also included in the computation Todaydeclining amphibian populations are seen in thousands ofspecies across numerous ecosystems including pristineforested areas [418] and declines are now recognizedamong the most severe impacts of the anthropocene era[417 442]

In addition the number of frogs with severe malfor-mations often incompatible with survival has risensharply Deformities are a complex issue related to physi-ology anatomy reproduction development water qual-ity changing environmental conditions and ecology ingeneral Any time deformities are observed in large seg-ments of wildlife populations there are indications ofserious environmental problems [442] Amphibian mal-formations are presumed due to an aggressive infectiousfungal disease called Chytridiomycosisy caused by thechytrid fungi Batrachochytrium dendrobatodis and Batra-chochytrium salamandrivorans [432ndash435] and by parasiteslike Ribeiroia ondatrae [427] Chytridiomycosis has beenlinked to dramatic amphibian declines and extinctions inNorth Central and South America across sections ofAustralia and Africa and on Caribbean islands likeDominica and Montserrat First identified in the 1970s inColorado US it continues to spread globally at analarming rate Some populations witness sporadic deathswhile others experience 100 mortality There is noeffective measure to control the disease in wild pop-ulations Herbicides like glyphosate used in Rounduptradeand atrazine an endocrine disruptor have also been foundto cause severe malformations in both aquatic and landamphibian species from farmland pesticideherbicidefungicide runoff [428ndash430]

Frogs are known to be highly sensitive to natural andmanmade EMF Much research into the electrophysiologyof frogs has been conducted because they are good labmodels for human nervous system research readilyavailable and easily handled As far back as 1780 theItalian physicist Luigi Galvani discovered what we nowunderstand to be the electrical basis of nerve impulseswhile studying static electricity (the only kind then known)when he accidentally made frog legmuscles contract whileconnected to the spinal cord by two different metal wires[444] Galvani thought he had discovered animalmagnetismrdquo but had actually discovered direct current andwhat later became known as a natural ldquocurrent of injuryrdquomdashthe process by which an injured limb for instance pro-duces a negative charge at the injury site that will later turn

38 Levitt et al EMF and wildlife

to a positive charge at the same site in some species asdiscovered in the 1960s by Robert O Becker [444ndash451] Theearliest curiosity about natural current continuedthroughout the 1800s on various aspects of EMF and laterthroughout the 1920s to 1940s in pioneering researchersElmer J Lund [452ndash454] and Harold Saxon Burr [455ndash457]who worked to establish the first unified electrodynamicfield theory of life using hydra frog and salamandermodels among several others because of their morpho-genic properties [458] While frogs do not regenerate limbsthe way salamanders do both are so similar in taxonomythat curiosity was high in the early pioneers cited abovethroughout the 1960s to 1990s about what fundamentallyallowed limb regeneration in one species by not the otherMuch was learned in the process about amphibian elec-trophysiology and cellular microcurrent in wound healingas well as the electrophysiological properties of cellulardifferentiation and eventually dedifferentiation pertinentto all contemporary stem cell research Today the impli-cations of this early work have gained new interest andtargeted research regarding endogenous microcurrent andlimb regeneration potential in humans as well as dedif-fentiationstem cellmorphogenesis in general for cancertreatment and other healing modalities For a thoroughreview of studies on morphogenesis see Levin [459]

Ubiquitous low-level ambient EMFs today match someof the natural low-level microcurrent found critical to thefundamental processes of amphibian growth reproduc-tion morphogenesis and regeneration lending newmeaning to the early research that defined amphibianelectrophysiology We just need to make far better use of itto understand what role if any todayrsquos ambient exposuresmay be contributing to amphibian losses (To comparetables between rising ambient EMF levels and low leveleffects in wildlife see Part 1 Supplement 1 and Part 2Supplement 3)

Amphibian and reptile magnetoreception

How amphibians perceive natural and manmade EMF issimilar to other species reviewed above and for amphibianmechanism reviews see Phillips et al [460 461] Likemanybird and insect species evidence indicates that amphib-ians perceive the Earthrsquos geomagnetic fields by at least twodifferent biophysical magnetoreception mechanismsnaturally occurring ferromagnetic crystals (magnetite)and light-induced reactions via specialized photo-receptorcells (cryptochromes) that form spin-correlated radicalpairs Like birds both mechanisms are present in someamphibians Cryptochromes provide a directional

lsquocompassrsquo and the non-light-dependent magnetite pro-vides the geographical lsquomaprsquo

In a thorough discussion of many magnetoreceptionstudies in anura and urodela species Diego-Rasilla et al[462] found evidence that Iberian green frog tadpoles(Pelophylax perezi) had a light-dependent magnetic com-pass and Diego-Rasilla et al [463] also found that tadpolesof the European common frog (Rana temporaria) arecapable of using the Earthrsquos magnetic field for orientingalong a learned y-axis In these studies they investigated ifthis orientation is accomplished using a light-dependentmagnetic compass similar to that found in the earlier ex-periments with other species of frogs and newts [460462ndash470] or from some other factor They concluded thatthe magnetic compass provided a reliable source of direc-tional information under a wide range of natural lightingconditions They also compared their findings to studies[470] that showed the pineal organ of newts to be the site ofthe light-dependent magnetic compass as well as to recentneurophysiological evidence showing magnetic fieldsensitivity located in the frog frontal organ which is anoutgrowth of the pineal gland They hypothesized thiswork could indicate a common ancestor as long ago as 294million years

To determine if orientation using Earthrsquos magneticfields changed according to seasonal migration patternsShakhparonov and Ogurtsov [471] tested marsh frogs(Pelophylax ridibundus) in the laboratory to see if frogscould determine migratory direction between the breedingpond and their wintering site according to magnetic cuesAdult frogs (n=32) were tested individually in a T-maze127 cm long inside a three-axis Helmholtz coil system(diameter 3 m) Maze arms were positioned parallel to thenatural migratory route and measured in accordance withthe magnetic field Frogs were tested in the breedingmigratory state and the wintering state mediated by atemperaturelight regime Frog choice in a T-maze wasevident when analyzed according to the magnetic fielddirection They moved along the migratory route to thebreeding pond and followed the reversion of the horizontalcomponent of the magnetic field The preference was seenin both sexes but only during the breeding migratory stateThey concluded that adult frogs obtained directional in-formation from the Earthrsquos magnetic field

Diego-Rasilla et al [472] found similar evidence in twospecies of lacertid lizards (Podarcismuralis and Podarcislilfordi) that exhibited spontaneous longitudinal body axisalignment relative to the Earthrsquos magnetic field during sunbasking periods Both species exhibited a highly signifi-cant bimodal orientation along the north-northeast andsouth-southwest magnetic axis Lizard orientations were

Levitt et al EMF and wildlife 39

significantly correlated over a five-year period withgeomagnetic field values at the time of each observationThis suggested the behavior provides lizards with a con-stant directional reference possibly creating a spacialmental map to facilitate escape This was the first study toprovide spontaneous magnetic alignment behavior in free-living reptiles although studies of terrapins have alsofound such spontaneousmagnetic alignment [92 323 473]Nishimura et al [474 475] also found sensitivity toELF-EMF (sinusoidal 6 and 8 Hz peak magnetic field26 μT peak electric field (10 Vm) in a lizard species(Pogona vitticeps) as demonstrated by significant increasedtail lifting mdash a reproductive behavior Interestingly thistail-lifting response to ELF-EMF disappeared when theparietal eye was covered suggesting that the parietal eyecontributes to light-dependent magnetoreception and thatexposure to ELF-EMFs may increase magnetic-field sensi-tivity in the lizards A further experiment [476] showed thatlight at a wavelength lower than 580 nm was needed toactivate the light-dependent magnetoreception of the pa-rietal eye

Amphibians RF-EMF

Most frogs spend significant time on land but lay eggs inwater where they hatch into tadpoles with tails and inter-nal gills However some species bypass the tadpole stageandor deposit eggs on land Frogs are thus subject to ex-posures from both land-based and aquatic environmentsA frogrsquos life cycle is complete when metamorphosis into anadult form occursMany adverse effects do not appear untilafter metamorphosis is completed but problems have beenfound throughout the entire life cycle after exposures toboth ELF-EMF and RFR

Most early research on frogs (other than the Beckeret al regeneration inquiries noted above) was conducted athigh thermal levels rarely encountered in the environmentbut some are included here because they helped delineateamphibian electrophysiology with effects later supportedin low-level research Some early work did use frog modelsto investigate cardiac effects with lower intensity expo-sures Levitina [477] found that intact frog whole-bodyexposure caused a decrease in heart rate while irradiationof just the head caused an increase Using VHF frequencyRFR at a power density of 60 μWcm2 A=125 cm Levitinaattributed the cardiac changes to peripheral nervous sys-tem effects but according to Frey and Siefert [478] becauseof the wavelengths used in that study little energetic bodypenetration would be expected They said a skin receptorhypothesis was therefore reasonable

Following on Levitinarsquos work Frey and Seifert [478]mdashusing isolated frog hearts UHF frequencies that penetratetissue more efficiently and low intensity pulse modula-tion mdash found that pulsed microwaves at 1425 GHz couldalter frog heart rates depending on the timing of exposurebetween the phase of heart action and themoment of pulseaction Twenty-two isolated frog hearts were irradiatedwith pulses synchronized with the P-wave of the ECGspulses were of 10 s duration triggered at the peak of theP-wave Two control groups were used without RFR ex-posures with no effects noted They found heart rate ac-celeration occurred with pulsing at about 200 ms after theP-wave But if the pulse occurred simultaneously with theP-wave no increases were induced Arrhythmias occurredin half the samples some resulting in cardiac cessationClearly from this study RFR affected frog heart rhythm andcould cause death

A more recent work by Miura and Okada [479] foundsevere vasodilation in frog foot webs from RFR In a seriesof three experiments using 44 anesthetized frogs (X laevis)at thermal and non-thermal intensities researchersexposed foot webs to pulsed RFR in three parameters withthe monitor coil set at 1 V peak-to-peak 100 kHz 582-3 mGand 17476 V cmminus1 10 MHz 73 mG and 219 V cmminus1 1 MHz539 mG and 1611 V cmminus1 They found not only dilated ar-terioles of the web which had already been re-constrictedwith noradrenaline but also dilated arterioles under non-stimulated conditions Vasodilatation increased slowlyand reached a plateau 60 min after radiationrsquos onset Afterradiation ceased vasodilation remained for 10ndash20 minbefore slowly subsiding Vasodilation was optimum whenpulsation was applied 50 of the total time at a 10 kHzburst rate at 10 MHz Effects were non-thermal The patternof vasodilation induced by warm Ringer solution wasdifferent from the vasodilatory effect of weak RFRinvolving the level of intracellular Ca2+ They hypothesizedthat since Ca2+ ATPase is activated by cyclic GMP which isproduced by the enzymatic action of guanylate cyclaseRF-EMF may activate guanylate cyclase to facilitate cyclicGMP production They concluded the study indicates for thefirst time that RFR dilates peripheral resistance vessels byneither pharmacological vasodilator agents nor physicalthermal radiation but that the precise mechanisms of acti-vation of guanylate cyclase by RFR at the molecular levelrequired further study Vasodilation and constriction affectsevery part of the body and can affect all organ systems

Prior to this Schwartz et al [480] found changes incalcium ions in frog hearts in response to a weak VHF fieldthat was modulated at 16 Hz This would be an exposurecommon in the environment Calcium ions are critical toheart function

40 Levitt et al EMF and wildlife

Balmori [24ndash30 442] and Balmori and Hallberg [271]have focused widely on EMF effects to wildlife with twopapers on amphibians Balmori [442] in a review notedthat RFR in the microwave range is a possible cause fordeformations and decline of some amphibian populationsand Balmori [481] in 2010 found increased mortality intadpoles exposed to RFR in an urban environment In the2010 study tadpoles of the common frog (Rana temporaria)were exposed to RFR from severalmobile phone towers at adistance of 459 ft (140 m) Two month exposures lastedthrough egg phase to advanced tadpole growth prior tometamorphosis RF andMW field intensity between 18 and35 Vm (086ndash32 μWcm2) were measured with threedifferent devices Results determined that the exposedgroup (n=70) had low coordination of movements andasynchronous growth that resulted in both large and smalltadpoles aswell as a disturbing 90highmortality rate Inthe control group (n=70) a Faraday cage was used underthe same conditions Controls found movement coordina-tion to be normal and development synchronous withmortality rate at a low 42 These results indicated thatRFR from cell towers in a field situation could affect bothdevelopment and mortality of tadpoles Prior to this studyGrefner et al [482] also found increased death in tadpoles(Rana temporaria L) exposed to EMF as well as highermortality rates and slower less synchronous development

Mortazavi et al [483] found changes in muscle con-tractions in frogs exposed to 900-MHz cell phone radiationfor 30 min gastrocnemimus muscles were then isolatedand exposed to a switched onoff mobile phone radiationfor three 10-min intervals The authors reportedRFR-induced effects on pulse height and latency period ofmuscle contractions SARs of the nerve-muscle preparationwere calculated to be 066 (muscle) and 0407 (nerve)Wkg

Rafati et al [484] investigated the effects of RFR onfrogs frommobile phone jamming equipment emitting RFRin the same frequencies as mobile phones (Althoughillegal inmany countries jammers are nevertheless used tointerfere with signals and stop communication) The studysought to follow up on reports of non-thermal effects ofRFR on amphibians regarding alterations of musclecontraction patterns They focused on three parametersthe pulse height of leg muscle contractions the time in-terval between two subsequent contractions and the la-tency period of frogrsquos isolated gastrocnemius muscle afterstimulation with single square pulses of 1 V (1 Hz) Animalsin the jammer group were exposed to RFR at a distance of1 m from the jammerrsquos antenna for 2 h while the controlfrogs were sham exposed All were then sacrificed andisolated gastrocnemius muscles were exposed to onoff

jammer radiation for three subsequent 10 min intervals(SAR for nerve and muscle of the different forms of jammerradiation was between 001 and 0052 Wkg) Resultsshowed that neither the pulse height of muscle contrac-tions nor the time interval between two subsequent con-tractions were affected but the latency period (timeinterval between stimulus and response) was statisticallysignificantly altered in the RFR-exposed samples Theyconcluded the results supported earlier reports of non-thermal effects of EMF on amphibians including the effectson the pattern of muscle contractions Control shamexposed samples showed no effects

Amphibians reptiles ELF-EMF

Amphibians are highly sensitive to ELF-EMF An early-1969study by Levengood [485] using a magnetic field probefound increased high rates of teratogenesis in frogs (Ranasylvatica) and salamanders (Ambystoma maculatum) Twoidentical probes using different field strengths wereemployed mdash both operated in the kilogauss region withhigh field gradients Amphibian eggs and embryos wereexposed at various stages of development with gross ab-normalities found in developing larvae vs control At thehatching stage severe abnormalities were noted in bothanuran and urodele larvae from probe-treated eggsHatching abnormalities included microcephaly altereddevelopment andmultiple oedematous growths In probe-treated frogs there was a delay in the appearance of a highpercentage of malformations until the climax stage ofmetamorphosis Until that stage the larvae were of thesame appearance as control specimens thus camouflagingthe damage after just a brief treatment of early embryosThe frog abnormalities at metamorphosis differed fromthose in the hatching tadpoles and consisted mainly ofsevere subepidermal blistering and leg malformationsincluding formation of multiple deformed limbs incom-patiblewith life Over 90of themorphological alterationsat metamorphosis climax were also found to be associatedwith deformed kidneys The gastrula stages of develop-ment appeared to be the most sensitive in the delayed-effects category While this was a high-field exposureexperiment it is an intensity that is found in some envi-ronments today especially near high tension lines and inabnormal ground current situations

Neurath [486] also found strongly inhibited early em-bryonic growth of the common leopard frog (Rana pipiens)by a high static magnetic field with a high gradient (1T) mdashan exposure sometimes found in the environmentmdash whileUeno and Iwasaka [487] found abnormal growth and

Levitt et al EMF and wildlife 41

increased incidence of malformations in embryos exposedto magnetic fields up to 8T but exposures that high aretypically near industrial sites and rarely found in nature

Severini et al [488] specifically addressed whetherweak ELF magnetic fields could affect tadpole develop-ment and found delayed maturation in tadpoles Two co-horts of X laevis laevis (Daudin) tadpoles were exposed for60 days during immaturity to a 50 Hz magnetic field of639ndash764 μT rms (root mean square average values)magnetic flux density in a solenoid Controls were twocomparable cohorts remotely located away from the sole-noid The experiment was replicated three times Resultsshowed reduced mean developmental rate of exposed co-horts vs controls (043 vs 048 stagesday plt 0001)beginning from early larval stages exposure increased themean metamorphosis period of tadpoles by 24 days vscontrols (p lt 0001) and during the maturation periodmaturation rates of exposed vs control tadpoles werealtered No increases in mortality malformations or tera-togenic effects were seen in exposed groups The re-searchers concluded that relatively weak 50 Hz magneticfields can cause sub-lethal effects in tadpoles via slowedlarval development and delays in metamorphosis Suchexposures are found in the environment today in somelocations and even though the changes were smallcoupled with climate change such sub-lethal effects mayimpact some wildlife populations in some environments

In similar followup work Severini and Bosco [489]found sensitivity to small variations of magnetic flux den-sity (50 Hz 22-day continuous exposure magnetic fluxdensities between 639 and 764 microT) in tadpoles exposed toa stronger field vs controls exposed to a weaker field Asignificant delay in development of 25 days was found inexposed vs controls They concluded the delaywas causedby the slightly differentmagnetic flux densities with resultssuggesting a field threshold around 70 microT in controlling thetadpole developmental rate

Schlegel in 1997 found European blind cave salaman-ders (Proteus anguinus) and Pyrenean newts (Euproctusasper) to be sensitive to low level electric fields in water[490] And Schlegel and Bulog [491] in followup workfound thresholds of overt avoidance behavior to electricfields as a function of frequency of continuous sine-wavesin water Nine salamanders from different Slovenian pop-ulations of the urodele (P anguinus) that included threespecimens of its lsquoblackrsquo variety (P anguinus parkelj)showed thresholds between 03 mVcm (ca 100 nAcm2)and up to 2 mVcm (670 nAcm2) with the most reactivefrequencies around 30 Hz Sensitivity included a total fre-quency range below 1 Hz (excluding DC) up to 1ndash2 kHzwithup to 40 dB higher thresholds These are ranges that may

be found in the wild near high tension lines and utilitygrounding practices near water by some underwater ca-bling and by some RFR transmitters

Landesman and Douglas in 1990 [492] found somenewt species showed accelerated abnormal limb growthwhen pulsed electromagnetic fields were added to thenormal limb regeneration process While normal limbregeneration found normal regrowth patterns in 72 ofspecimens 28 were abnormal Abnormalities includedloss of a digit fused carpals and long bone defects whichoccurred singly or in combination with one another Whenexposure to a PEMF was added for the first 30 days post-amputation followed by a 3ndash4 month postamputationperiod a group of forelimbs with unique gross defectsincreased by an additional 12 Defects (singly or incombination) included the loss of two or more digits withassociated loss of carpals absence of the entire handpattern and abnormalities associated with the radius andulna The researchers offered no explanation Exposureintensities were similar to those used to facilitate non-juncture fracture healing in humans

Komazaki and Takano in 2007 [493] found acceleratedearly development growth rates with 50 Hz 5ndash30 mTalternating current exposures in the fertilized eggs of Jap-anese newts (Cynops pyrrhogaster) The period of gastru-lation was shortened via EMF-promoted morphogeneticcell movements and increased [Ca2+]i They said their re-sults indicated that EMF specifically increased the [Ca2]i ofgastrula cells thereby accelerating growth This study onlyobserved through the larval stages and they did not see anymalformations under EMF exposures which they attrib-uted to possible differences in the intensity and mode ofEMF

With amphibians and some reptiles demonstratinghigh sensitivity to natural background EMF for importantbreeding and orientation needs amphibians living inaquatic terrestrial and aerial environments (ie tree frogspecies) may be affected from multi-frequency anthropo-genic EMF in ways we do not fully understand There arepotential effects mdash especially from 5G MMW that couplemaximally with skin mdash to all aspects of their developmentand life cycles including secondary effects

Fish marine mammals lobstersand crabs

Aquatic animals are exquisitely sensitive to natural EMFand therefore potentially to anthropogenic disturbanceThe Earthrsquos dipole geomagnetic field yields a consistent

42 Levitt et al EMF and wildlife

though varying source of directional information in bothland and aquatic species for use in homing behaviororientation during navigation and migration This infor-mation is used both as a lsquomaprsquo for positional information aswell as a lsquocompassrsquo for direction [494ndash497] Aquatic speciesare known to be sensitive to static geomagnetic fields at-mospheric changes and sunspot activities [498] For recentcomprehensive reviews onmagnetic field sensitivity in fishand effects on behavior see Tricas and Gill [36] and Krylovet al [33] Some biological lsquomagnetic mapsrsquo may beinherited [499] And for a recent extensive discussion of theEarthrsquos natural fields and magnetoreception in marineanimals with a focus on effects from electromagnetic sur-veys that use localized strong EMFs to map petroleum de-posits under seabeds see Nyqvist et al [498] and below

As mentioned above because of the difference inconductivity of water and other factors the way someaquatic species sense EMF may rely on unique modes ofphysiological perception as well as those employed byterrestrial animals There may also be sensory combina-tions not yet understood in some aquatic and semi-aquaticspecies For instance what role does the neural conduc-tivity of whiskers (vibrissae) in seals sea lions and walrusplay other than for food finding Aquatic speciesrsquo densenetwork of whiskers is larger with greater blood flow thanterrestrial species and can contain 1500 nerves per folliclevs cats at 200 per follicle Seal whiskers also varygeometrically from terrestrial species and the largest partof the seal brain is linked to whisker function Seals usewhiskers to map the size shape and external structure ofobjects and can find prey even when blindfolded Theirwhiskers are also sensitive to weak changes in water mo-tion [100] But are they also using them as a location ordirectional compass in relation to the geomagnetic fieldThat has yet to be studied

Unique sensory differences in aquatic species have longbeen documented Joshberger et al [500] noted that in 1678Stefano Lorenzini [501] was the first to describe a network oforgans in the torpedo ray that became known as the Ampullaeof Lorenzini (AoL) Its purpose was unknown for 300 yearsuntil Murray [502] measured AoLrsquos electrical properties inelasmobranch fishmdash sharks rays and skates Later work [101503ndash508] confirmed and greatly added to this knowledgeResearchers now know that AoL is likely the primary mecha-nism that allows elasmobranch fish to detect and map a po-tential preyrsquos physiology via the very weak changes in electricfields given off by preyrsquos muscle contractions

Individual ampullae are skin pores that open to theaquatic environment with a jelly-filled canal leading to analveolus containing a series of electrosensing cells Withinthe alveolus the electrosensitive cells of the ampullae

communicate with neurons and this integration of signalsfrom multiple ampullae is what allows elasmobranch fish todetect electric field changes as small as 5 nVcm [503 506509 510] TheAoL jelly has been reported as a semiconductorwith temperature-dependence conductivity and thermoelec-tric behavior [500 509 510] as well as a simple ionicconductor with the same electrical properties as the sur-rounding seawater [503 506] Josberger et al [500] attemptedto clarify what AoLrsquos role is in electrosensing by measuringAoLrsquos proton conductivity They found that room-temperature proton conductivity of AoL jelly is very high at2 plusmn 1 mScmmdash only 40-fold lower than some current state-of-the-art manmade proton-conducting polymers That makesAoL the highest conductive biological material reported thusfar They suggested that the polyglycans contained in theAoLjelly may contribute to its high proton conductivity

Other aquatic magneto-sensory mechanisms more inharmony with terrestrial animals include the presence offerromagnetic particles in magnetite mdash tiny naturally pro-duced magnets that align with the Earthrsquos magnetic fieldallowing for speciesrsquo direction and orientation Magnetite ap-pears to transmit necessary information through a connectionwith the central nervous system [340 497 511] A magnetite-based system is plausible for cetaceans [512 513] as magnetitehas been found in the meninges dura mater surrounding thebrains ofwhales anddolphins [514 515] There is also evidencethat local variationsanomalies in the geomagnetic field incertain underwater topographies may play a role in live ceta-cean strandings [516 517]which indicates amagnetic compassbased on magnetite And free-ranging cetaceans have shownevidence of magnetoreception-based navigation eg Finwhale migration routes have been correlated with lowgeomagnetic intensity [513]

Recently Granger et al [518] found correlations in databetween 31 years of gray whale (Eschrichtius robustus)strandings and sunspot activity especially with RF lsquonoisersquoin the 2800 MHz range The 11-year sunspot cycle stronglycorrelateswith the intense releases of high-energy particlesknown as solar storms which can temporarily modify thegeomagnetic field and in turn may modify orientation inmagnetoreceptive species Solar storms also cause an in-crease in natural broadband RF lsquonoisersquo They examinedchanges in both geomagnetic fields and RF lsquonoisersquo andfound RF to be a determinant Further they hypothesizedthat increased strandings during high solar activity is morelikely due to radical pair mechanisms which are morereactive with RFR than magnetite which appears morereactive to ELF-EMF Two previous studies also foundcorrelations with cetacean strandings and solar activities[519 520] Both mechanisms may come into play underdifferent circumstances or act in synergy

Levitt et al EMF and wildlife 43

Kremers et al [512] investigated the spontaneousmagnetoreception response in six captive free-swimmingbottlenose dolphins (Tursiops truncates) to introducedmagnetized and demagnetized devices used as controlsThey found a shorter latency in dolphins that approachedthe device containing a strong magnetized neodymiumblock compared to a control demagnetized block identicalin form and density and therefore indistinguishable withecholocation They concluded that dolphins can discrimi-nate on the basis of magnetic properties mdash a prerequisitefor magnetoreception-based navigation Stafne andManger [521] also observed that captive bottlenose dol-phins in the northern hemisphere swim predominantly in acounter-clockwise directionwhile dolphins in the southernhemisphere swim predominantly in clockwise directionNo speculation was offered for this behavior

How salmon navigate vast distances mdash from theirhatching grounds in freshwater river bottoms to lakesduring juvenile growth then the open ocean duringmaturity and with a final return to their neonatal birthinggrounds to spawn and die (for most anadromous salmo-nids)mdash has fascinated researchers for decades Research in-dicates they may use several magneto-senses to accomplishthis including inherited mechanisms [522] imprinting [499522] a magnetic compass [499 522 523] and biomagneticmaterials Salmon have been found to have crystal chains ofmagnetite [524] One recent study found that strongmagneticpulses were capable of disrupting orientation in salmonmodels [525] indicating a magnetite-based mechanism Insalmon the migration process is complicated by the fact thatthe ability to sense geomagnetic fields can be altered bychanges in salinity between fresh and salt water thuspointing to multi-sensory mechanisms [499]

Speculation that salmon use the geomagnetic field insome capacity for their iconic migration goes back decades[526] Quinn [527] found evidence that sockeye salmon(Oncorhynchus nerka) frey use both a celestial and magneticcompass when migrating from river hatching to lakes Put-man et al [499] whohavewritten extensively on this subjectfocused on how salmon navigate to specific oceanic feedingareas mdash a challenge since juvenile salmon reach feedinghabitats thousands of kilometers from natal locations Theresearchers experimentally found that juvenile Chinooksalmon (Oncorhynchus tshawytscha) responded to magneticfields similar to latitudes of their extreme ocean range byorienting in directions that would lead toward their marinefeeding grounds They further found that fish use the com-bination ofmagnetic intensity and inclination angle to assesstheir geographic location and concluded that the magneticmap of salmon appears to be inherited since the fish had noprior migratory experience These results paired with

findings in sea turtles (see below) indicate that magneticmapsarewidespread in aquatic species and likely explain theextraordinary navigational abilities seen in long-distanceunderwater migrants [499]

It is less likely that light-sensing radical pair crypto-chromes play much of a role in aquatic species thoughsome hypothesize the possibility [528] Krylov et al [33]however noted that there are no anatomical structures orneurophysiological mechanisms presently known forradical pair receptors in the brains of fish and that sincelight decreases with water depth and fish are capable oforienting in complete darkness using the geomagneticfield their opinion was that it is too early to say fish havemagnetoreception mechanisms based on free radicalslight-dependent or otherwise

Fish lobsters crabs ELF-EMF

For several reasons having to do with differences in con-ductivity in water vs air (see above) RFR is of far lessconcern in aquatic environments at present than is ELFWith the ever-increasing number of underwater cablesused for everything from transcontinental datacommu-nications to power supplies for islands marine platformsunderwater observatories off-shore drilling wind facil-ities tidal and wave turbines among others many newsources of both AC and DC electric current are beingcreated in sea and freshwater environments alike Ac-cording to Ardelean and Minnebo writing in 2015 [529]almost 4971 mi (8000 km) of high voltage direct current(HVDC) cables were present on the seabedworldwide 70of which were in European waters and this is only ex-pected to grow dramatically as new sources of renewableenergy are built to replace fossil fuels globally

Curiosity about potential adverse effects from cable-generated ELF-EMF on all phases of fish life has alsogrown especially in benthic and demersal species thatspend significant time near cables in deeper bottom envi-ronments for egg laying larvae growth and developmentfor most if not all of their adult lives

Fey et al [494 495] and Oumlhman et al [530] noted thatthere are two types of anthropogenic exposures created bycables high voltage direct current (HVDC) that emits staticmagnetic fields and three-phase alternating current (ACpower transmission) that emit time-varying electromag-netic fields The density of electric current near underwatercables on the sea floor can vary significantly depending onthe type of cable and whether they are positioned on thesea bottom or buried [36 530] Noticeable magnetic fieldchanges can occur within meters but generally not more

44 Levitt et al EMF and wildlife

than several meters from the cable However Hutchinsonet al [531] in a robust field study and extensive reviewfound surprisingly stronger and more complex exposuresthan anticipated (see below)

Since fish are highly sensitive to static magnetic fields(MF) it is important to delineate static fields from anthro-pogenic alternating current EMF in aquatic studies Infreshwater species under laboratory conditions Fey et al[494] found similar results to those of salmon studies(noted above) in northern pike (Esox lucius) exposed to astatic magnetic field from DC cables (10 mT) during theembryonic phase and in the first six days of post-hatchingNo statistically significant MF effect was seen on hatchingsuccess larvae mortality larvae size at hatching andgrowth rate during the first six days of life However sig-nificant MF effects were seen on hatching time (one dayearlier in a magnetic field than in control) yolk-sac sizewas smaller and yolk-sac absorption rate was faster Theyinterpreted the faster yolk-sac absorption in a magneticfield as an indication of increasedmetabolic rate but addedthat even if some negative consequences were expected asa result that the actual risk for increased northern pikelarvae mortality seemed negligible Though higher than10 mT magnetic field values are hazardous for fish larvaethey added such values do not occur in the natural envi-ronment even along underwater cables

But in follow-up work of longer duration the samegeneral research group reached a different conclusion Feyet al [495] studied effects on eggs and larvae of rainbowtrout (Oncorhynchus mykiss) exposed to a static magneticfield (MF) of 10 mT and a 50 Hz EMF of 1 mT for 36 days(ie from eyed egg stage to approximately 26 days posthatching) They found that while neither the static MF northe 50-Hz EMF had significant effects on embryoniclarvalmortality hatching time larval growth or the time oflarvae swim-up from the bottom both fields did howeverenhance the yolk-sac absorption rates While they said thiswas not directly related to a MF effect it was shown thatlarvaewith absorbed yolk-sacs by the time of swim-upwereless efficient in taking advantage of available food at firstfeeding and gained less weight They concluded that theseexposures could negatively affect the yolk-sac absorptionrate thereby hampering fish in important feeding activitiesneeded for fast weight gain and increased survival In anadditional study Fey et al [532] observed that rainbowtrout reared in a laboratory for 37 days and exposed to astatic MF (10 mT) or a 50-Hz EMF (1 mT) showed defects inotolith of the inner ear which is responsible for hearing andbalance in fish The authors concluded that underwaterconstruction andor cables that emit a MF of 10 mT orhigher can affect living organisms within a few meters

distance especially species like trout in settled life stageson the sediment bottom during early development

Zebrafish (Danio rerio) are often used in EMF research intoxicology and developmental biology investigating effectson humans because the genomes are so similar Li et al [533]studied ELF-MF on the development of fertilized zebrafishembryos divided into seven groups Embryos of experi-mental groups were continuously exposed to 50-Hz sinu-soidal MF with intensities of 30 100 200 400 or 800 μT for96 h The sham group was identical but without ELF-MFexposure Results showed that ELF-MF caused delayedhatching and decreased heart rate at early developmentalstages but no significant differences were seen in embryomortality or abnormality Acridine orange staining assaysshowed notable signs of apoptosis in the ventral fin andspinal column and transcription of apoptosis-related genes(caspase-3 caspase-9) was significantly up-regulated inELF-MF-exposed embryos They concluded that ELF-EMFdemonstrated detrimental effects on zebrafish embryonicdevelopment including on hatching decreased heart rateand induced apoptosis although such effects were not amortal threat The lower range exposures of this study arefound in some aquatic environments

Sedigh et al [534] investigated effects on zebrafishexposed to static magnetic fields Exposures of 1-week acuteand 3-week subacute exposures to different static magneticfields at 25 5 and 75 mT were measured on stress indices(cortisol and glucose) sex steroid hormones (17β-estradioland 17-α hydroxy progesterone) and fecundity They found asignificant change in cortisol glucose 17β-estradiol (E2) and17-α hydroxy progesterone (17-OHP) levels with increasedintensity and duration of exposure and concluded that staticmagnetic fields at higher intensities showed harmful effectson the reproductive biology of zebrafish during both acuteand subacute exposures

Recent laboratory research by Hunt et al [535] used thetransparent glass catfish (Kryptopterus vitreolus) found inslow moving waters in Southeast Asia as a model toinvestigate magnetoreception The study used Y-mazechambers animal tracking software and artificial intelli-gence techniques to quantify effects of magnetic fields onthe swimming direction of catfish They placed a perma-nent Neodymium Rare Earth Magnet (115 times 318 times 22 cm)with a horizontal magnetic flux of 577 mT at the magnetrsquossurface at 10 cm from the endof one of the Y-maze arms andfound that catfish consistently swam away from magneticfields over 20 μT The catfish also showed adaptability tochanging magnetic field direction and location The mag-netic avoidance was not influenced by school behaviorSham exposures produced no avoidance Such exposuresmight be found near some underwater cables

Levitt et al EMF and wildlife 45

To further elucidate findings of species reactions nearunderwater cables and fill in knowledge gaps since the2011 Tricas and Gill review [36] Hutchinson et al [531]conducted both field and laboratory modeling studies ofboth AC and DC fields on the American lobster (Homarusamericanus) and the little skate (Leucoraja erinacea) Theynoted that in previous studies while behavioral responseshad been seen findings were unable to determine if sig-nificant biological effects (eg population changes)occurred TheAmerican lobsterwasmodeled because it is amagnetosensitive species [536] and concern existed thatEMF from cables might restrict movements andor migra-tion Lobsters may migrate up to 50 mi (80 km) one wayfrom deep waters to shallow breeding grounds The littleskate was used as a model for the most electro-sensitivetaxa of the elasmobranchs which may be attracted bytothe EMF of cables particularly for benthic species therebyaltering their foraging or movement behavior Bothmodelswere therefore thought indicative of potential EMF im-pacts In this robust field study the researchers found thatthe American lobster exhibited a statistically significantbut subtle change in behavioral activity when exposed tothe EMF of theHVDC cable (operated at a constant power of330 MW at 1175 Amps) The little skate exhibited a strongbehavioral response to EMF from a cable powered for624 of the study with the most frequently transmittedelectrical current at 16 Amps (at 0 MW 375 of time) 345Amps (100 MW 286) and 1175 Amps (330 MW 152)They concluded that for both species the behavioralchanges have biological relevance regarding how they willmove around and are distributed in a cable-EMF zone butthey noted that the EMF did not constitute a barrier tomovements across the cable for either species

Of interest in this study were the actual field readingsnear cables Unexpected significant ACmagnetic and electricfields did not match computer models and were observed tobe associated with both of the DC power cables studied Themaximum observed AC values along the cable axis were015 μT and 07 mVm for the magnetic and electric fieldsrespectively for one cable and 004 μT and 04 mVmrespectively for the other cable Also the cross section of theEMF peaks exhibited by the DC subsea power cables werebroader than anticipated at both studied The DC and ACmagnetic fields reached background levels on either side ofthe cable on a scale of ca5 and 10m from the peak observedvalue respectively whereas the AC electric fields reachedbackground on a scale of 100 m (328 ft) from the peak valuePeak observed values occurred almost directly above thecable axis location there was an offset of 33 ft (lt1 m) wherethe cable was twisted The researchers noted that thisobservation of AC fields with broad areas of EMF distortion

being associated with DC cables increased the complexity ofinterpreting the studies of EMFrsquos biological effects from DCcables TheACelectricfieldsassociatedwith theACsea2shorecable (1ndash25 mVm) were higher than the unanticipated ACelectricfieldsproducedby theDCcables (04ndash07mVm) Themagnetic field produced by the AC sea2shore cable (range of005ndash03 μT) was sim10 times lower than modeled valuescommissioned by the grid operator indicating that the three-conductor twisted design achieves significant self-cancellation This entire aspect of the study indicates theneed for accurate field assessment not just computermodeling andwell-designed systems since anomalies occur

Nyqvist et al [498] in a thorough review focused onmarine mammals and the use of underwater electromag-netic surveys that map petroleum deposits in seabeds viastrong induced EMFs in varied directional applicationsThey found that EMFs created during such active surveyingwere within the detectable ranges of marine animals andthe fields can potentially affect behavior in electro-perceptive species but they noted that effects should belimited to within a few kilometers as the electric andmagnetic fields created attenuate rapidly They added thatin migrating marine animals exposures are of shortduration and most are close to naturally occurring levelsbut cautioned that lack of studies is a concern especiallyfor the most sensitive elasmobranchs at highest risk fordisturbance to electric fields They also noted that withinduced magnetic fields animals using magnetic cues formigration or local orientation during certain time-windowsfor migration orientation or breeding could be mostaffected by this surveying technology

Taorimina et al [537] studied both static and time-varying magnetic fields on the behavior of juvenile Euro-pean lobsters (Homarus gammarus) Using two differentbehavioral assays day-light conditions to stimulate shel-tering behavior and exposures to an artificial magneticfield gradient (maximum intensity of 200 μT) they foundthat juvenile lobsters did not exhibit any behavioralchanges compared to non-exposed lobsters in the ambientmagnetic field No differences were noted on the lobstersrsquoability to find shelter or modified their exploratorybehavior after one week of exposure to anthropogenicmagnetic fields (225 plusmn 5 μT) which remained similar tobehavior in controls They concluded that neither static nortime-varying anthropogenic magnetic fields at those in-tensities significantly impacted the behavior of juvenileEuropean lobsters in daylight conditions but they notedthat evidence exists showing magnetosensitivity changesduring different life stages in lobster species and that sincetheir modeling was on juveniles their study was thereforean incomplete picture requiring further study

46 Levitt et al EMF and wildlife

Scott et al [538] focused on ELF-EMF effects oncommercially important ediblebrown crab species (Can-cer pagurus) and what they found was startling In labo-ratory tanks they simulated EMF (with Helmholtz coils28 mT evenly distributed assessments during 24 h pe-riods) that would be emitted from sub-sea power cablesnow commonly used at offshore renewable energy facil-ities They measured stress related parameters ((L-lactateD-glucose haemocyanin and respiration rate) along withbehavioral and response parameters (antennal flickingactivity level attractionavoidance shelter preference andtime spent restingroaming) They found that althoughthere was no EMF effect on haemocyanin concentrationsrespiration rate activity level or antennal flicking ratethere were significant changes in haemolymph L-lactateand D-glucose natural circadian rhythms indicating al-terations in hormones Crabs also showed an unusuallyhigh attraction to EMF-exposed shelter areas (69)compared to control shelter areas (9) and significantlyreduced their time roaming by 21 with adverse impli-cations for food foraging mating and overall health Theynoted that EMF clearly altered behavior Crabs spent lesstime roaming around the tank andmore time in a shelter indirect contact with the EMF source indicating naturalroamingfood-or-mate-seeking behavior had been over-ridden by attraction to EMF In fact crabs consistentlychose an EMF-exposed shelter over a non-exposed one andwere always drawn to the EMF The results appear topredict that in benthic areas surrounding EMF-emittingcables there will be an increase in the abundance ofCancer pagurus present They noted that such potentialcrab aggregation around benthic cables and the subse-quent physiological changes in L-lactate and D-glucoselevels caused by EMF exposure is a concern regardingfeeding rates mating and especially egg incubationdirectly in increased EMF environments They concludedthat long term investigations are needed regarding chronicEMF exposure especially on egg development hatchingsuccess and larval fitness and added that EMF emitted inmarine environments from renewable energy devicesmustbe considered as part of the study of cumulative impactsduring the planning stages

Clearly ELF-EMF can affect myriad aquatic species atintensity levels found in proximity to underwater cables atenvironmental intensities

Fish RF-EMF

As mentioned RFR is of minimal environmental concernfor fish since aquatic environments while highly

conductive mediums also highly attenuate EMF at higherfrequencies This may change in the near future as newtechnologies now exist thatmay surpass these obstacles [98]thereby introducing for the first time novel new RFR expo-sures underwater Longer wave wireless ELF with expandedranges are used in anthropogenic sonar (sound navigationranging) primarily for military applications These traveleasily through water and are known to adversely affect ce-taceans and other species that rely on their natural sonar forcommunication migration reproduction and food findingBut soundwaves are not considered ldquoEMFrdquo in the strict senseof the term since the focus of this paper is EMF soundwavesare tangential here But acoustic damage especially to ceta-ceans from military and commercial applications is welldocumented and ELF cables used for underwater militarysubmarine communications can have significant EMF expo-sures near cables Just because this paper does not addressimpacts from sound waves in detail does not mean they arewithout serious effects

There are however three recent studies of RFR onzebrafish included here because it is plausible that suchexposures could exist near shallow aquatic environmentsunder some circumstances Nirwane et al [539] studied900-MHz GSM RFR effects on zebrafish (D rerio) neuro-behavioral changes and brain oxidative stress as a modelfor human exposures to cell phones Exposures wereapplied daily for 1 h 14 days with SAR 134 WKg Theyfound 900-MHz GSM radiation significantly decreased so-cialization and increased anxiety as demonstrated by sig-nificant increased time spent in bottom areas freezingbehaviors and duration and decreased distance travelledas well as decreased average velocity and number of en-tries to the upper half of the tank Exposed zebrafish spentless time in the novel armof a Y-Maze indicating significantimpaired learning compared to the control group Expo-sure also decreased superoxide dismutase (SOD) andcatalase (CAT) activities while increased levels of reducedglutathione (GSH) and lipid peroxidation (LPO) wereencountered indicating compromised antioxidant defensePost-exposure treatment with melatonin in the waterhowever significantly reversed the induced neuro-behavioral and oxidative changes

Piccinettia et al [540] investigated in vivo effects onembryonic development in zebrafish at 100 MHz thermaland nonthermal intensities via a multidisciplinary proto-col Results found 100 MHz RFR affected embryonicdevelopment from 24 to 72 h post fertilization in all theanalyzed pathways Most notably at 48 h post fertilizationreduced growth increased transcription of oxidative stressgenes onset of apoptoticautophagic processes and amodification in cholesterol metabolism were seen EMF

Levitt et al EMF and wildlife 47

affected stress by triggering detoxification mechanisms At72 h post fertilization fish partially recovered and reachedhatching time comparable to controls The researchersconcluded that EMF-RFR unequivocally showed in vivoeffects at non-thermal levels

Dasgupta et al [541] used embryonic zebrafish modelsat 35 GHz SAR asymp 827 Wkg and exposed developingzebrafish from 6 to 48 h post fertilization then measuredmorphological and behavioral endpoints at 120 h postfertilization Results found no significant impacts on mor-tality morphology or photomotor response but noted amodest inhibition of startle response suggesting somelevels of sensorimotor disruptions They concluded thatexposures at low GHz levels are likely benign but never-theless entailed subtle sensorimotor effects Such effectscan affect fish survival in variousways including inhibitedresponse time to predators among others This study wasdone with an eye toward potential human bioeffects atfrequencies used in 4 and 5G technology It was also con-ducted at intensities higher than the focus of this paper

If new technology overcomes the conductivityatten-uation limitations of aquatic environments and introducesmore RFR to aquatic species studies like those cited abovemay soon have more environmental relevance even athigher intensities than explored here

Turtles

Oceanic sea turtle migration joins that of other renownedlong-distance migratory species like salmon and over-landmonarch butterfly treks spanning thousands of kilometersand traversingmultiple complex environments throughouttheir life cycles Sea turtles have long been known to usegeomagnetic fields for orientation [542 543] Freshwaterspecies (eg Chelydra serpentina) have also been shown tohave a magnetic sense capable of artificial disruption [92]as do terrestrial box turtles (Terrapene carolina [544])

Sea turtles demonstrate natal homing behavior mdash theability to return over great distances to their exact birthlocation to reproduce [89] and because of anthropogenicdisruptions of nesting grounds along beaches this repro-ductive homing drive imperils them today The underlyingmechanism is still imperfectly understood but involveslsquoimprintingrsquo of the intensity and inclination angle of thegeomagnetic field at the birth location [545] The informa-tion is then later used in maturity to return to their place oforigin

Sea turtles are by far the most studiedmodels for turtlemagnetoreception especially by the Lohmann Laboratoryat the University of North Carolina US [323 546ndash558]

Irwin and Lohmann [559] discussed the advantagesand disadvantages of various research approaches used toinvestigate magnetic orientation behavior in turtles Theseinclude the use of largemagnetic coil systems in laboratorysettings to generate relatively uniform fields over largeareas [560] which allow the magnetic field to be artificiallyaltered and carefully controlled to determine changes inbehavioral orientation This approach however is un-suited for manipulating exposures around animals innatural environments or for studying localized body mag-netoreceptors which in turtles are still a mystery Anotherapproach is to attach a small magnet or electromagneticcoil to an animal to disrupt magnetic orientationbehavior mdash a far easier approach in hatchlings than injuvenile ormature free-swimming species They note that ifthe imposed field from an attachedmagnet or coil is strongenough to interfere with the Earthrsquos field behavioralorientation changes [116 544 561] and the performance ofa conditioned response [367 562] can be observed Thislatter approach has been used in field studies for the pur-pose of blocking access to normal magnetic information[544 561 563ndash565] and to localize magnetoreceptors bydisrupting the field around a specific terrapin body part[562] This techniquersquos disadvantage however is thatfields rapidly change with distance from the source mak-ing it difficult to quantify the fields that the animal actuallyexperiences

Most sea turtle studies have involved large magneticcoil systems but Irwin and Lohmann [559] attached smallmagnets greater in strength than the Earthrsquos fields to twogroups of loggerhead sea turtle hatchlings (Caretta carettaL) under laboratory conditions in which turtles are knownto orient magnetically [473 546 548ndash550] They found thatmagnetic orientation behavior in hatchling turtles can bedisrupted via small magnets attached to the carapacewhich then create exposures over the entire body Theyconcluded that such an approach can be used to finallydetermine local magnetoreceptors by varying the locationof themagnet and using smaller weakermagnets that alterthe field only around specific anatomical target sites

In loggerhead sea turtles there is evidence of aninclination compass [473 550] that is functionlly similar tothe bird magnetic compass reported in European Robins[566 567] Lohmann and Lohmann [550] investigated aninclination compass in sea turtles and found it was apossible mechanism for determining latitude Also inves-tigated were detection of magnetic intensity [551] naturalregional magnetic fields used as navigational markers forsea turtles [557] and sea turtle hatchlingsrsquo mapping abili-ties [545] Sea turtles are also known to have magnetite intheir heads [104 568] Studies with young sea turtles have

48 Levitt et al EMF and wildlife

shown that a significant portion of their navigationalabilities involve magnetoreception following hatching[569] mdash imprinting with the Earthrsquos magnetic field beingone of several cues hatchlings use as they first migrateoffshore [546 554] The magnetic fields that are unique todifferent areas at sea eventually serve as navigationalmarkers to guide swimming direction to important migra-tory routes As juveniles mature they form topographicalmagnetic maps where they live that direct them to specificregions But it has remained largely unknown if matureturtles specifically nesting females use such mechanismsin open-sea homing as this magneto-sense may changeover time

Field studies are notoriously difficult with large spe-cies at sea but Papi et al [564] studied mature green turtles(Chelonia mydas) during their post-nesting migration over1243 mi (2000 km) from their nesting grounds on Ascen-sion Island in themiddle of the Atlantic Ocean back to theirBrazilian feeding grounds They were investigatingwhether mature female turtles use an inclination compassand geomagnetic fields for direction or by inference (oncethat sense is disturbed) by some other means as yetdetermined Papi et al [564] attached very strong DCmagnets mdash significantly stronger than the Earthrsquos fields mdashto disturb and overcome natural magnetoreception andthereby determine if they could still navigate back to As-cension Island Controls had nonmagnetic brass barsattached and some had transmitters glued to their headsAll had tracking devices that communicatedwith satellitesthus creating strongmulti-frequency static and pulsed RFRexposures Seven turtles were each fitted with six powerfulstatic magnets that produced variable artificial fields sur-rounding the whole turtle making reliance on a geomag-netic map impossible The studyrsquos travel courses were verysimilar to those of eight turtles without magnets that hadbeen tracked via satellite over the same period in the pre-vious year No differences between the magneticallyexposed test turtles and untreated turtles were foundregarding navigational performance and general coursedirection They concluded that magnetic cues were notessential to turtles on the return trip and speculated thatperhaps other factors such as smell or wave current di-rection may come into play

Luschi et al [563] like Papi et al [564] also investi-gated the role of magnetoreception and homing in maturesea turtles but used a different design and found verydifferent results In a large field study in the MozambiqueChannel 20 mature pre-nesting green turtles were alsoequipped with both strong magnets and satellite trackingdevices The turtles were gathered at their nesting beach onMayotte Island before egg-laying and transported to four

open-sea sites 62ndash75 mi (100ndash120 km respectively) awayThere were five releases of four turtles each with threedifferent treatments turtles magnetically lsquodisturbedrsquo onlyduring transportation with magnets removed beforerelease those treated only during the homing trip withmagnets attached just prior to release and controls withnonmagnetic brass discs attached to their heads Treatedturtles had very strongmoveable magnets attached to theirheads to induce varying magnetic fields around themeither at the nesting beach at the start of the relocationjourney or on the boat just prior to release for the homingtrip All groups had satellite transmitters attached to theircarapaces thereby creating in the opinion of the authors ofthis paper an additional exposure that was not consideredas a variable The researchers also included ocean currentsin their assessments estimated by using oceanographicremote sensing measurements All but one turtle eventu-ally returned to Mayotte to complete delayed egg-layingBut treated turtles whether treated during transportationor homing took significantly longer to reach the destina-tion vs controls mdash a surprising finding Most homingroutes showed very long circuitous curved and loopingpatterns before reaching their target Control paths weredirect Both treated turtle groups were clearly impaired bythe MF exposure indicating significant recovery timeneeded between exposure and correcting positionalbehavior The researchers hypothesized the existence of anavigational role for geomagnetic information beinggathered by those turtles in the passive transportationgroup as well as the possibility that magnetic disturbanceduring transportation may have persisted for some timeafter the removal of the magnets in that group thusrendering the two treated groups functionally equivalentduring their homing journeys They also noted that expo-suresmay have physically alteredmagnetite particles thuscreating a longer lasting effect but they said that since long-lasting after-effects of magnet application have not beendescribed this theory could neither be inferred nordismissed

Lohmann [323] reviewed both of the above studies andadded that in addition to the two causal hypotheses ofLuschi et al [563] regarding their unexpected findings ofturtle circuitous migration routes another explanationwould include the positioning of the satellite transmittersin the Papi et al [564] study on turtle heads vs on thecarapace of the Luschi models He added that since satel-lite transmitters also produce magnetic fields capable ofdisrupting magnetoreception and since the Papi groupalso attached satellite transmitters on the heads of severalcontrol turtles that re-analyzing the Papi study using onlyturtles with satellite transmitters placed on the carapace

Levitt et al EMF and wildlife 49

like the Luschi study could show evidence consistent withthe hypothesis that adult turtles exploit magnetic cues innavigation He concluded that sea turtles like all otheranimals studied to date likely exploit multiple cues fornavigation since even with artificial magnetic disturbancecausing impaired performance themagnets in either studydid not prevent turtles from eventually reaching theirtarget beaches This implies that turtles can also rely onother sources of information [570 571] such as celestialcompasses wave direction [572] or olfactory cues likeother species mdash a significant finding

The sum total of the studies mentioned above is thatsea turtle species are highly sensitive to Earthrsquos fields andare capable of adapting to subtle anthropogenicdisruption

Turtles RF-EMF

Turtles may also be senstitive to RFR especially duringincubation while on land andor initial hatchling stages ifthey are exposed to anthopogenic RF-EMF that coulddistort the imprintingmemory they use in later life to locatetheir birthsite beaches again For example if a radar orcommunications base station is installed on or near thebeach of a nesting site could that affect the initialldquoimprintingrdquo process Perhaps augment imprinting andmake return easier Or conversely overwhelm the subtleimprinting process at the start and make return impos-sible If the latter is valid such technology could lead toextinction of sensitive species since it interrupts thereproduction process In the very least in sensitive speciesdisorientation might result as discussed above

To characterize the underlying compass mechanismsin turtles Landler et al [92] studied freshwater juvenilesnapping turtlesrsquo (Chelydra serpentine) ability for sponta-neous magnetic alignment to the Earthrsquos geomagneticfields Using exposure to low-level RFR near the Larmorfrequency (12 MHz) that is related to free radical pair for-mation turtles were first introduced to the testing envi-ronment without the presence of RFR (ldquoRF off RF offrdquo) andthey were found to consistently align toward magneticnorth But when subsequent magnetic testing conditionswere initially free of RFR then included an introducedsignal (ldquoRF off RF onrdquo) they became disoriented Thusintroduction of a RFR field could affect the turtlesrsquo align-ment response to the natural magnetic field The RFR fieldusedwas only 30ndash52 nT (143MHz) In the following reversescenario when the turtles were initially introduced to thetesting environment with RFR present but then removed(ldquoRF on RF offrdquo) they became disoriented when tested

without RFR And with RFR on in both cases (ldquoRF on RFonrdquo) they aligned in the opposite direction toward mag-netic south Clearly test turtles were affected by the expo-sures The researchers concluded that the sensitivity of thespontaneous magnetic alignment response of the turtles toRFR was consistent with a radical pair mechanism (seeldquoMechanismsrdquo above) In addition they concluded that theeffect of RFR appeared to result from a change in thepattern of magnetic input rather than elimination ofmagnetic input altogether Their findings indicated thatturtles when first exposed to a novel environment form alasting association between the pattern of magnetic inputand their surroundings and that they may form a largerinternal GPS-like mapping ability when theymeet any newmagnetic reference framework based on natural magneticcues from multiple sites and localities

They also showed that RFR at or near the Larmor fre-quency (12ndash143 MHz) had the ability to disrupt snappingturtle natural orientation establish its own novel orienta-tion and completely reverse a natural orientation leadingback to the complex questions asked above regardingimprinting and possible reproductive disruption Althoughthe Landler et al study [92] was conducted in a freshwaternon-homing species snapping turtles are long-lived with alow reproduction success rate Even small disruptions tothis species from anthropogenic sources could have anoutsized population effect over time If this freshwaterspecies is any indication of potential RFR effects re-searchers need to further investigate RFR in long-distancemigrating turtle species that imprint on landWe simply donot know the full range of possible effects across fre-quencies with which turtle species come in contact atvulnerable points throughout development and lifetimes

Nematodes and smaller biota

There are reports of sensitivity to EMF in lesser taxa aswellEMF is known to affect numerous other species includingnematodes (Earth and aquatic worms) mollusks (snails)amoeba (single-celled organisms) molds algae pro-tozoans yeast fungi bacteria and viruses (to a limitedextent) mdash with ramifications for creation of antibioticresistant bacteria strains Below are some representativeexamples of observed effects

Nematodes

Common soil-based nematode species like C elegans serveas a useful whole-organism model for genetic and

50 Levitt et al EMF and wildlife

multicellular organism investigations They are routinelyused as a research model to investigate key biologicalprocesses including aging neural system functioning andmuscle degeneration to name a few This speciesrsquo geneticand phenotypic traits are extremely well documented andthey can thus be used as important proxies for quantitativeanalyses [573] Nematodes have a short lifespan are her-maphrodites and demonstrate effects quickly As labmodels they are used primarily for information that can beapplied to humans but we can also glean important in-formation and extrapolate to environmental exposuresunder certain circumstances Healthy soil worm pop-ulations are critical to soil health upon which we alldepend

Hung et al [574] investigated static magnetic field(SMF) effects on life span and premature aging inC elegans Nematodes were grown in SMFs varying from0 to 200 mT They found that SMFrsquos accelerated develop-ment and reduced lifespan in wild-type nematodes Theyalso found increases in heat shock proteins that were se-lective and dose dependent

Vidal-Gadea et al [66] investigated magnetic orienta-tion in C elegans to identify magnetosensory neurons andfound that they orient to the Earthrsquos geomagnetic fieldduring vertical burrowing migrations Well-fed wormsmigrated up while starved worms migrated down Pop-ulations isolated from around the world were found tomigrate at angles to the magnetic vector that would verti-cally translate to their native soil with northern- andsouthern-hemisphere worms displaying opposite migra-tory preferences in conjunction with natural geomagneticfields They also found that magnetic orientation and ver-ticalmigrations required the TAX-4 cyclic nucleotide-gatedion channel in the AFD sensory neuron pair while calciumimaging showed that these neurons respond to magneticfields even without synaptic input They hypothesized thatC elegans may have adapted magnetic orientation tosimplify their vertical burrowingmigration by reducing theorientation task from three dimensions to one

C elegans have also demonstrated sensitivity to elec-tric fields via electrotaxis (also known as galvanotaxis)which is the directed motion of living cells or organismsguided by an electric field or current and often seen inwound healing Sukul and Croll [575] found that nema-todes exposed to an electrical current (002ndash004 mA po-tential differences 2ndash6 V) demonstrated a directionalsensorily-mediated orientation toward the current at firstbut at 2mm from the electrode individualworms increasedreversing behaviors which then remained uniform as theymoved in a constant direction parallel to the exposure Afew which did not reverse direction died (presumably from

electrocution) at 6 V or 04 mA They concluded that adultC elegans move directionally at selected combinations ofvoltage and potential differences and that electrophoresiscould be eliminated

Gabel et al [576] also investigated electric field effectson directionality on C elegans with an eye toward betterunderstanding how the nervous system transforms sensoryinputs into motor outputs They used time-varying electricfields modulated at 100 Hz across an agar surface with adefined direction and amplitude up to 25 Vcm They foundthat the nematodes deliberately crawl toward the negativepole in an electric field at specific angles to the direction ofthe electric field in persistent forward movements with thepreferred angle proportional to field strength They alsofound that the nematodes orient in response to time-varying electric fields by using sudden turns and reversals(normal reorientation maneuvers) They also found thatcertain mutations or laser ablation that disrupt the struc-ture and function of amphid sensory neurons also dis-rupted their electrosensory behavior and that specificneurons are sensitive to the direction and strength ofelectric fields via intracellular calcium dynamics amongthe amphid sensory neurons This study showed thatelectrosensory behavior is crucial to how the C elegansnervous system navigates and can be disrupted at someintensities found in the environment

Maniere et al [573] also found Celegans was sensitiveto electric fields and that when submitted to a moderateelectric field worms move steadily along straight trajec-tories They hypothesized that imposing electric fields inresearch settings was an inexpensive method to measurewormsrsquo crawling velocities and a method to get them toself-sort quickly by taking advantage of their electrotacticskills

An early RFR study of C elegans by Daniells et al [577]found this species to be a useful model for investigatingstress-responses In the majority of investigations theyused 750 MHz with a nominal power of 27 dBm controlswere shielded and all temperatures were strictlycontrolled Stress responses were measured in terms ofbeta-galactosidase (reporter) induction above controllevels Response to continuous microwave radiationshowed significant differences from 25 degrees C in con-trols at 2 and 16 h but not at 4 or 8 h Using a 5 times 5multiwellplate array exposed for 2 h the 25 microwaved samplesshowed highly significant responses compared with asimilar control array Experiments in which the frequencyandor power settings were varied suggested a greaterresponse at 21 than at 27 dBm both at 750 and 300 MHzindicating a nonlinear effect although extremely variableresponses were observed at 24 dBm and 750 MHz Lower

Levitt et al EMF and wildlife 51

power levels tended to induce greater responses mdash theopposite of simple heating effects They concluded thatmicrowave radiation causes measurable stress to trans-genic nematodes via increased levels of protein damagewithin cells at nonthermal levels

Tkalec et al [578] found oxidative and genotoxic ef-fects in earthworms (Eisenia fetida) exposed in vivo to RFRat 900 MHz at 10 23 41 and 120 V m(-1) for 2 h using aGigahertz Transversal Electromagnetic (GTEM) cell Allexposures induced significant effects with modulationincreasing such effects Their results also indicated anti-oxidant stress response induction with enhanced catalaseand glutathione reductase activity indicating lipid andprotein oxidative damage Antioxidant responses anddamage to lipids proteins and DNA differed depending onEMF level modulation and exposure duration

Aquatic and semi-aquatic worm species also showsensitivity to EMF Jakubowska et al [579] investigatedbehavioral and bioenergetic effects of EMF at 50 Hz 1 mTfields (comparable to exposures near underwater cables) inpolychaete ragworms (Hediste diversicolor) that live andburrow in the sandmudof beaches andestuaries in intertidalareas of the North Atlantic While they found no attraction oravoidancebehavior toEMFburrowingactivitywasenhancedwith EMF exposure indicating a stimulatory effect Foodconsumption and respiration rates were unaffected butammonia excretion rate was significantly reduced inEMF-exposed animals compared to control conditions at onlygeomagnetic fields The mechanisms remained unclear Theauthors said this was the first study to demonstrate effects ofenvironmentally realistic EMF values on the behavior andphysiology of marine invertebrates

Van Huizen et al [67] investigated effects of weakmagnetic fields (WMF) on stem-cells and regeneration inan in vivomodel using free-swimming flatworms (Planariassp) that are capable of regenerating all tissues includingthe central nervous system and brain This regenerationability is due to the fact that about 25 of all their cells areadult stem cells (ASC) Injury is followed by a systemicproliferative ASC response that initially peaks at sim 4 hfollowed by ASC migration to the wound site over the first72 h when a second mitotic peak occurs Like salamanderregeneration (see ldquoAmphibiansrdquo above) this activity pro-duces a blastema mdash a group of ASC cell growth that formsthe core of new tissues Full regeneration of damagedplanaria tissues or organs occurs through new tissuegrowth and apototic remodelingscaling of old tissueswithin 2ndash3 weeks Following amputation above and belowthe pharynx (feeding tube) they exposed amputation sitesto 200 μTWMF At three days post-amputation they foundthat 200 μT exposure produced significantly reduced

blastema sizes compared to both untreated and earth-normal 45 μT field strength controls indicating a WMFinterference effect to regeneration They also found that the200 μT exposure was required early and had to be main-tained throughout blastema formation to affect growthand that shorter single-day exposures failed to affect blas-tema size In addition they found weak magnetic fieldsproduced field strengthndashdependent effects These includedsignificant reductions of blastema size observed from 100ndash400 μT but conversely a significant increase in outgrowthoccurred at 500 μT They hypothesized thatWMFeffects werecausedbyaltered reactive oxygen species (ROS) levelswhichpeak at the wound site around 1-h post-amputation and arerequired for planarian blastema formation This study showsthat weak anthropogenic magnetic fields can affect stem cellproliferation and subsequent differentiation in a regenerativespecies and that field strength can increase or decrease newtissue formation in vivo This is a significant finding forregenerating species of all kinds and may affect non-regenerating species as well Sea lamprey eels (Petromyzonmarinus) a fish species are also known to regenerate evenafter multiple amputations [580]

Mollusks amoeba molds algaeprotozoans

Mollusks (marine versions are called chitons) are longknownto manufacture magnetite in their teeth and to use fieldsweaker than the geomagnetic field for kinetic movement anddirection [52 117 340 524] Lowenstam [118] first discoveredthat magnetite was the major mineral in the teeth of marinechitons thought to give teeth their natural hardness ButRatner [62] discovered chitons use magnetite as a magneticcompass when he found a number of chiton species haveradulae (tongues) that are covered by ferro-magnetic(magnetite) denticles The radulae of Acompapleura gran-ulata and Chiton squamosis were also found to be ferro-magnetic but the shells were not Live specimens of a chiton(Chaetopleura apiculata) that also have ferro-magneticradulae were found to rotate more and move farther in amagnetic field weaker than in the Earthrsquos stronger geomag-netic field indicating a nonlinear directionality Ratnerconcluded that chitons are responsive to magnetic fields anddemonstrate kinetic movements within them

Some snails are sensitive to EMFs Nittby et al [581]observed analygesic effects in land snails (Helix pomatia)caused by GSM-1900 RFRs when snails lost sensitivity topain on a hot plate test after nonthernal exposure to RFR

Smaller organisms have also long shown effects fromEMF Goodman et al [582] found delays in mitotic cell

52 Levitt et al EMF and wildlife

division in slime mold (Physarum polycephalum) withELF-EMF exposures Friend et al [583] found perpendic-ular and parallel elongation of the giant amoeba Chaoschaos (Chaos carolinensis) in alternating electric fields overa wide frequency range (1 Hzndash10 MHz) with characteristicchanges as a function of frequency Marron et al [584]found effects on ATP and oxygen levels in another speciesof slime mold (P polycephalum) after exposures to 60 Hzsinusoidal electric and magnetic fields Luchien et al [585]found a stimulating effect on the productivity of the algalbiomass (Chlorella sorokiniana) for a magnetic field of50 Hz but an inhibitory effect at 15 Hz in these microalgae

Protozoans thought to bemore related to animals thanmicrobes also show sensitivity to EMF Protozoans assingle-celled eukaryotes are generally larger than bacteriawhich are classified as prokaryotes The two organisms arestructurally different bacterial cells lack a nucleus whileprotozoa contain organelles such as mitochondria Bacte-ria generally absorb nutrients through their cell wallswhileprotozoa feed on bacteria tissue and organic matter andcan be both infectious and parasitic These protozoainclude human parasites that cause diseases such asamoebic dysentery malaria giardiasis leishmaniasistrichomoniaisis toxoplasmosis and others Animal speciesare also affected by protozoans which can severely weakenand shorten their lifespans

Rodriguez-de la Fuente et al [586] tested ELF-EMF(60 Hz 20 mT for 72 h) on two infectious protozoans Tri-chomonas vaginalis andGiardia lamblia and found growthalterations in both species which they attributed to alter-ations in cell cycle progression and cellular stress Cam-maerts et al [587] used RFR (GSM 900-MHz at 2 W vscontrol) on protozoans (Paramecium caudatum) and foundindividuals moved more slowly and sinuously than usualand that their physiology was affected Paramecia becamebroader pulse vesicles had difficulty expelling content tothe outside of their cells cilia moved less efficiently andtrichocysts became more visible mdash all effects that indicatepoor functioning or cell membrane damage They hy-pothesized that the first impact of RFR could be to cellmembranes

Clearly there are multiple effects at all levels docu-mented in lower taxa from multi-frequency exposures thatare now found in the environment

Yeast and fungi

Yeast is often used in lab models especially since 1996when a complete genomic sequence of Saccharomycescerevisiae was created In fact it is now considered a

ldquopremiermodelrdquo [588] for eukaryotic cell biology as well ashaving helped establishwhole newfields of inquiry such asldquofunctional genomicsrdquo and ldquosystems biologyrdquowhich focuson the interactions of individual genes and proteins toreveal specific properties of living cells and wholeorganisms

EMF research is rich with studies using yeast modelstoo numerous to fully analyze here However we include asmall sample of recent EMF research with potential sig-nificance to environmental exposures

Lin et al [589] investigated glucose uptake and tran-scriptional gene response to ELF-EMF (50 Hz) and RFR(20 GHz) on several strains of budding yeast (S cerevisiae)Results determined that ELF-EMF and RFR exposure canupregulate the expression of genes involved in glucosetransportation and the tricarboxylic acid (TCA) cycle butnot glycolysis pathways thus showing that such exposurescan affect energy metabolism which is closely related withcellular response to environmental stress Glucose meta-bolism is fundamental to all living cellsrsquo need for energywith related significance to many disease states includingmost cancers

In amagnetic field study byMercado-Saenz et al [590]premature aging and cellular instability were found inyeast (S cerevisiae) exposed to low frequency low in-tensity sinusoidal magnetic fields (SMF continuous expo-sure at 245 mT 50 Hz) and pulsed magnetic fields (PMF15 mT 25 Hz 8 hday) Chronological aging was evaluatedduring 40 days and cellular stability was evaluated by aspontaneous mutation count and the index of respiratorycompetence (IRC) They found exposure to PMF producedaccelerated aging while SMF did not and decreasedmitochondrial mutation during aging was also seen withPMF No alterations in respiratory competence wereobserved for either SMF or PMF exposures They concludedthat exposure to PMF accelerated chronological aging andaltered the spontaneous frequency of mitochondrial mu-tation during the aging process whereas the SMF used hadno effect thus showing abnormal effects on cell activityfrom pulsed exposures

Because yeast cells are known to be sensitive to mag-netic fields some industrial and therapeutic applicationsto human health have been investigated These in-vestigations serve to illuminate what we know about yeastand fungal reactions to EMF in general as well as specificuses For industrial applications Wang et al [591] inves-tigated low level static magnetic fields (SMF) on mold(Aspergillus versicolor) growth which can have high im-pacts on metal corrosion in environmental conditionsconducive to mold growth This is especially problematicin fine electronic circuit boards produced today Using a

Levitt et al EMF and wildlife 53

10 mT static magnetic field (SMF) perpendicular to thesurface of printed circuit boards they found the magneticfield inhibited mold growth and surface corrosion whichwere slowed down unlike control boards without appliedmagnetic fields where mold formed a spore-centeredcorrosion pit that then led to macroscopic regional uni-form corrosion This demonstrated changes in cellsporegrowth at a low intensity exposure that can be found in theenvironment

Also with an eye toward commercial possibilities Sunet al [592] found that a polysaccharide of Irpex lacteus (awhite-rot fungus found widely in the environment whichbreaks down organic materials but also is commerciallyused to treat nephritis in humans) was sensitive to low-intensity ELF-EMF as demonstrated by increased biomassand polysaccharide content as well as inducedmalformedtwists on the sample cell surfaces Polysaccharides arecarbohydrates with a large number of sugar moleculesused as energy sources in living cells They identifiedvarying changes in multiple differentially expressed genesafter exposure to alternating current EMF (50 Hz 35 mT3 h per day for 4 days) They found initial sharp increasesin growth rates in exposed samples that were then markedby significant declines in EMFrsquos influence over timealthough there were also important lasting effects Globalgene expression alterations fromEMF indicated pleiotropiceffects (capable of affecting multiple proteins or catalyzingmultiple reactions) were related to transcription cell pro-liferation cell wall and membrane components aminoacid biosynthesis and metabolism Polysaccharidebiosynthesis and metabolism were also significantlyenriched in the EMF-exposed samples They concludedthat EMF significantly increased amino acid contents andwas therefore deemed a suitable method for increasingfermentation of microorganisms presumably for com-mercial use However the significance of this study toenvironmental exposures relates to the multiple ways thatELF alternating current common to electric power gener-ation changed yeast gene expression There is at least oneclinical case of a different strain of I lacteus taking on a rareinfectious and dangerous quality in an immuno-compromised human [593] The question is can now-ubiquitous ELF-EMF contribute to potentially emergingnew forms of yeast contagion

The same question arises with Candida albicans andother pathogenic yeasts that have rapidly developedresistance to antifungal medications C albicans can liveharmlessly in human microflora but certain lifestyle cir-cumstances or immunosuppression can turn it into anopportunistic pathogen It can also infect somenon-humananimals While chronic mucocutaneous candidiasis can

infect the skin nails and oral and genital mucosae underhigh host immunodeficiency C albicans can enter thebloodstream and induce systemic infections withmortalitybetween 30 and 80 [594] There has been increasingresistance of C albicans to traditional antifungal agentssuch as fluconazole and amphotericin B [595 596] Resis-tance mechanisms include overproduction of membranedrug efflux transporters andor changes in gene expression[597]

Two investigations in search of new therapeutic stra-tegies were conducted using EMF Sztafrowski et al [594]investigated the use of staticmagneticfields (SMF 05 T) onC albicans cultures in the presence of two commonly usedantifungal medications Their aim was to assess whetherSMF had any impact on general viability of C albicanshyphal transition and its susceptibility to fluconazole andamphotericin B They found reduction of C albicans hy-phal length in EMF-exposed samples They also found astatistically significant effect on C albicans viability whenSMF was combined with amphotericin B They hypothe-sized that this synergistic effect may be due to the plasmamembrane binding effects of amphotericin B and that SMFcould influence domain orientation in the plasma mem-brane They concluded with caution that the use of a SMFin antifungal therapy could be a new supporting option fortreating candidas infections

Novickij et al [598] also focused on therapeutic pos-sibilities given the multi-drug resistance and side effects toantifungal therapies Their aim was to optimize theelectroporation-mediated induction of apoptosis usingpulses of varied duration (separately and in combinationwith formic acid treatment) and to identify yeast apoptoticphenotypes They focused on nonthermal nanosecondpulsed electric fields (PEF 3 kV 100 ns ndash 1 ms squarewaveand 250 500 750 ns duration 30 kVcm PEF 50 pulses1 kHz) as a therapeutic alternative andor to enhance ef-fects in combinationwith conventional treatments In threeyeast models S cerevisiae (as control) and drug resistantCandida lusitaniae and Candida guilliermondii they foundthat nanosecondPEF induced apoptosis in all three strainsCombining PEF with a weak formic acid solution improvedinduced apotosis and inactivation efficacy in the majorityof the yeast population Yeast cells showed DNA breaksand other changes They concluded that PEF could be auseful newnon-toxic protocol to treat some fungal diseasesand minimize tissue damage

Choe et al [599] studied ion transportation and stressresponse on a yeast strain (K667) to ELF-EMF (60 Hz01 mT sinusoidal or square waves) specifically investi-gating internal ionic homeostasis via the cell membraneinvolving metal ions and cation transports (cations are

54 Levitt et al EMF and wildlife

ionic species of both atoms and molecules with a positivecharge) They found significantly enhanced intracellularcation concentrations as ELF-EMF exposure timeincreased as well as other changes This study has impli-cations for soil health as yeast can be an integral aspect ofhow healthy organic soil matter is formed They concludedthat EMF and yeast could also play a role in the bioreme-diation processes in metal-polluted environments

Lian et al [600] studied effects of ELF-EMF (50 Hz 0ndash70 mT) and RFR (20 GHz 20 Vm temperature at 30 degCaverage SAR single cell012 Wkg) on two budding yeaststrains (NT64C and SB34) and prion generationpropaga-tion They found under both EMF exposures that de novogeneration and propagation of yeast prions (URE3) wereelevated in both yeast strains The prion elevationincreased over time and effects were dose-dependent Thetranscription and expression levels of heat shock proteinsand chaperoneswere not statistically significantly elevatedafter exposure but levels of reactive oxygen species (ROS)as well as superoxide dismutase (SOD) and catalase (CAT)activities were significantly elevated after short-term butnot long-term exposure This work demonstrated for thefirst time that EMF exposure could elevate the de novogeneration and propagation of yeast prions supporting theresearcherrsquos hypothesis that ROS may play a role in theeffects of EMF on protein misfolding ROS levels alsomediate other broad effects of EMF on cell function Theyconcluded that effects of EMF exposure on ROS levels andprotein folding may initiate a cascade of effects negativelyimpacting many biological processes

The effects of EMF on protein folding cannot be over-stated Proteins must fold into proper three-dimensionalconformations to carry out their specific functionsmdash intactproteins are critical to the existence of all life Misfoldingnot only impairs function but leads to disease Foldinginside of cells does not happen spontaneously but ratherdepends on molecular helpers called chaperones Proteinmisfolding has been implicated in Alzheimerrsquos Parkin-sonrsquos and Huntingtonrsquos diseases among others Thedevastating CreutzfeldtndashJakob disease is caused by prionmisfolding in the brain which causes abnormal signalingin neurons that eventually leads to paralysis and deathWildlife can also suffer from prion diseases such as chronicwasting in deer elk and other cervids and cattle can sufferfrom so-called ldquomad-cowrdquo disease The two studies fromabove [599 600] have implications for how such diseasesare spread through soil with possible links to environ-mental EMFs

It is clear from the above that ELF-EMF and RF-EMFusing multiple signaling characteristics are biologicallyactive in both temporary and permanent ways in yeast

fungi species with wide environmental implications acrossnumerous taxa

Bacteria

Strains of bacteria are known to be magnetotactic and usegeomagnetic fields for direction Blakemore [63] was thefirst to suggest in 1973 that bacteria in North Americansaltwater marsh muds use magnetite as a sensor when hediscovered not only that bacteria were highly attracted toan external magnet but they also had magnetite crystalsthat caused them to align with the lines of the Earthrsquosmagnetic fields This was also discovered to be geo-location specific to the North Pole in northern samples andSouth Pole-seeking in southern species [52 63 511] Thebacteria showed ldquomud-uprdquo and ldquomud-downrdquo behavioralong magnetic field gradients when mud was disturbedindicating a magnetic compass Since that early work awhole new field called electromicrobiology has developedwith discoveries that include some electro-active bacteriabeing responsible for magnetite formation with otherscreating their own electric ldquowiresrdquo in mud flats with im-plications for new technologies [601]

Among the more troubling EMF effects are bacterial al-terations with pressing implications for antibiotic resistanceSince the 1940s [602] nonthermal effects were documentedin bacterial viral and tissue cultures with applied low-repetition 20-MHz pulses Most studies spanning the 1940sthough the 1980s focused on EMFrsquos ability to kill microbesand fungi in human food sources at high intensity conse-quently most research was focused on thermal intensitiesThat work still continues today as microwaves have beenshown to be an efficient means for killing microbes [50] Butmicrobes also react to much lower nonlethal intensities andrecent work finds effects from both ELF and RFR

The common bacteria Escherichia coli which can liveharmlessly in the gut of humans and many other animalspecies can also turn virulent and kill through food-borneillnesses E coli comes inmany strains is well studied andnow considered the most genetically and physiologicallycharacterized bacterium E coli encounter varied andnumerous environmental stressors during growth sur-vival and infection including heat cold changes in Phlevels availability of foodwater supplies and EMF Alongwith other bacteria they respond by activating groups ofgenes and heat shock proteins (see ldquoMechanismsrdquo above)which can eventually lead to stress tolerance for survivalpurposes But induced stress tolerance can also lead toincreased virulence as well as enhanced tolerance to otherstressors that confer cross‐protection [603]

Levitt et al EMF and wildlife 55

Salmen and colleagues [604 605] published papers ofEMF effects on bacterial strains documenting the growinginvestigation of microbes related to antibiotic resistancewith many findings stressing responses to EMF [606ndash610]Cellini et al [611] investigated E colirsquos adaptability toenvironmental stress induced by ELF exposures to 50-Hzmagnetic fields at low intensities (01 05 10mT) vs shamcontrols They found exposed samples and controls dis-played similar total and culturable counts but increasedcell viability was observed in exposed samples re-incubated for 24 h outside of the test solenoid comparedto controls Exposure to 50 Hz EMF (20ndash120 min) alsoproduced a significant change in E colimorphotype with apresence of coccoid cells aggregated in clusters after re-incubation of 24 h outside of the magnetic field-solenoidAtypically lengthened bacterial forms were also notedindicating probable alteration during cell division Somedifferences in RNA-AFLP analysis were also seen for allintensities evaluated They concluded that exposure to50-Hz ELF-EMF is a bacterial stressor as evidenced by itsimmediate response in modifying morphology (frombacillary to coccoid) and inducing phenotypical and tran-scriptional changes Despite this stressor effect it was alsoseen that exposed samples significantly increasedviability suggesting the presence of VBNC cells Theyconcluded that further studies were needed to better un-derstand ELF-EMF in bacterial cell organization They didnot extrapolate to the obviousmdash that E coliwas changed inan abnormal way but nevertheless strengthened inviability mdash a recipe for antibiotic resistance

Crabtree et al [612] in a small human study investi-gated the biomic relationship of human bacteria exposed toboth static magnetic fields (SMF) and RFR Using laboratoryculture strains and isolates of skin bacteria collected fromthe hand cheek and chin areas of four volunteers who haddifferent (self-reported) cell phone use histories they foundvaried growth patterns of E coli Pseudomonas aeruginosaand Staphylococcus epidermidis under static magnetic fieldson different bacterial species Isolates of skin microbiotashowed inconsistent growth among the test subjects likelydue to their differing cell phone usage histories (classified asheavymediumand light) andother variables The growthofStaphylococci was increased under RFR in certain in-dividuals while in others growth was suppressed This wascomplicated by the different body areas tested some withhigher chronic exposures such as the hands aswell as othervariables when one test subject used an antibacterial facewash Volunteers in the heavy use category showed lessbacterial growth on the hands possibly due to microbehabituation Overall and despite the small sample theyconcluded RFR can disrupt the balance in skin microbiota

making it more vulnerable to infection by specific opportu-nistic andor other foreign pathogens They noted that bothSMF and RF-EMFs have significant but variable effects onthe growth of common human bacteria that bacterialgrowth was either unaffected increased or suppresseddepending on the species of bacteria and that bacterial re-sponses seemed to be determined by historic exposure toRF-EMF and life style This study even with inherent limi-tations indicates changes in microbes with EMFs and mayprove a novel way to study bacteria with significance forreal-life exposures to humans and animals alike

Salmen et al [605] also found highly variable resultsfromRFR (900 and 1800MHz) effects onDNA growth rateand antibiotic susceptibility in Staphylococcus aureusStaphylococcus epidermidis and P aeruginosa Using anactive cell phone handset they exposed bacteria to 900and 1800 MHz for 2 h then injected samples into a newmedium where growth rate and antibiotic susceptibilitywere evaluated Regarding DNA they found no differencesin S aureus and S epidermidis when exposed to 900 and1800 MHz vs controls but P aeruginosa showed changesinDNAbandpatterns following such exposures Regardinggrowth rates with the exception of a significant decreaseafter 12 h exposure to 900 MHz no significant effects ongrowth of S aureus and S epidermidis were seen But thegrowth of P aeruginosa was significantly reducedfollowing exposure for 10 and 12 h to 900 MHz while nosignificant reduction in growth followed exposure to1800 MHz Regarding antibiotic susceptibility in thedrugs studied (ie amoxicillin 30 mg azithromycin 15 mgchloramphenicol 10 mg and ciprofloxacin 5 mg) with theexception of S aureus treated with amoxicillin (30 mg)EMF-exposure had no significant effect on bacterialsensitivity to antibiotics This study shows variabilityamong bacterial species not only to different frequenciescommon in the environment today but also to changes insensitivity to some antibiotics but not others There mayhave been design problems with this study however

Several studies investigated WiFi signals on bacterialstrains Taheri et al [610] assessed exposure to 900-MHzGSM mobile phone radiation and 24-GHz RFR from com-mon WiFi routers to see if cultures of Listeria mono-cytogenes and E coli resulted in altered susceptibility to 10different antibiotics They found narrowwindows in whichmicrobes became more resistant For L monocytogenes nosignificant changes in antibacterial activity betweenexposed and nonexposed samples mdash except for Tetracy-cline (Doxycycline) mdash were noted For E coli howeverthere was a significant change in antimicrobial activitiessuggesting RFR exposures can influence antibiotic sus-ceptibility of E coli more than in Listeria For window and

56 Levitt et al EMF and wildlife

pronounced effects they found L monocytogenes exhibi-ted different responses to each antibiotic For Doxycyclinethe window occurred after 6 h exposure toWiFi andmobilephone-RFR After 9 h of exposure to WiFi for Ciprofloxacinand Sulfonamide (Tremethoprinsulfamethoxazole) bac-teria tended to become more resistant By contrast thepattern for Levofloxacin and Penicillin (CefotaximeDef-triaxone) showed increased sensitivity For Ecoli thepattern of the response to WiFi and mobile phone RFR wasthe same maximum antibiotic resistance was seen be-tween 6 and 9 h of exposure but after 12 h a stress responselead to a return to preexposure conditions indicating anadaptive reaction Taheri et al [609] found similarnonlinearwindoweffects anddifferences in growth rates inKlebsiella pneumonia while Mortazavi et al [613] foundsimilar window effects in E coli In addition they saw sig-nificant increased growth rates after radiation exposures inboth Gram-negative E coli and Gram-positiveL monocytogenes They concluded that such window ef-fects can be determined by intensity and dose rate thatexposure to RFR within a narrow window can make mi-croorganisms resistant to antibiotics and that this adap-tive phenomenon is a human health threat The same canbe inferred for many non-human species

Said-Salman et al [614] evaluated non-thermal effectsofWiFi at 24 GHz for 24 and 48 h (using aWiFi router as thesource) on the pathogenic bacterial strains E coli 0157H7S aureus and S epidermis for antibiotic resistancemotility metabolic activity and biofilm formation Resultsfound that WiFi exposure altered motility and antibioticsusceptibility of E coli but there was no effect on S aureusand S epidermis However exposed cells (vs unexposedcontrols) showed an increased metabolic activity and bio-film formation ability in E coli S aureus and S epidermisThey concluded that WiFi exposure acted as a bacterialstressor by increasing antibiotic resistance and motility ofE coli as well as enhancing biofilm formation in all strainsstudied They indicated the findingsmay have implicationsfor the management of serious bacterial infections

Movahedi et al [615] also investigated antibioticresistance using short-term exposure to RFR from amobilephone simulator (900 MHz 24 h) on P aeruginosa andS aureus against 11 antibiotics They found significantchanges in structural properties and resistance to thenumerous antibiotics studied P aeruginosa was resistantto all antibiotics after 24 h of exposure vs non-exposedcontrols while S aureus bacteria were resistant to about50 They also found structural changes in all exposedsamples and increased cell wall permeability

In a field study near cell towers Sharma et al [616]looked at changes in microbial diversity and antibiotic

resistance patterns in soil samples taken near four differentbase stations with control samples taken gt300 m awayStenotrophomonas maltophilia Chryseobacterium gleumand Kocuria rosea were isolated and identified in soilsamples collected near the exposed zones They foundgreater antibiotic resistance in microbes from soil nearbase stations compared to controls with a statisticallysignificant difference in the pattern of antibiotic resistancefound with nalidixic acid and cefixime when used asantimicrobial agents They concluded that cell tower ra-diation can significantly alter the vital systems in microbesand make them multi-drug resistant

Researchers have also investigated ELF-EMF effects onbacterial growth and antibiotic sensitivity Segatore et al[608] investigated 2 mT 50 Hz exposures on E coli ATCC25922 and P aeruginosa ATCC 27853 and found EMFsignificantly influenced the growth rate of both strainsnotably at 4 6 and 8 h of incubation The number of cellswas significantly decreased in exposed bacteria vs con-trols And at 24 h incubation the percentage of cellsincreased (P aeruginosa sim 42 E coli sim 5) in treatedgroups vs controls which suggested to the researchers aprogressive adaptive response However they saw noremarkable change in antibiotic sensitivity Potenza at al[617] also found effects at high-intensity static magneticfields at 300 mT on growth and gene expression in Ecolibut that would be a high environmental exposure

Viruses

There is a paucity of research on viral species and EMFlikely due to the fact that viruses lack ferromagnetic ma-terials are difficult to study and donrsquot make good generallab models other than to investigate their direct impact onspecific in vivo end points Virology research thrives in itsown specialized niche and has not been used for basicmodeling like so many other living life forms as notedthroughout this paper There is long-standing debate onwhether viruses are even alive

However one wide-ranging discussion by Zaporozhanand Ponomarenko [618] hypothesized a possible complexmechanistic link between influenza pandemics naturalsun spot cycles and non-thermal effects of weak magneticfields via cryptochromesradical pairs gene expressionpathways and stress-induced host immunological alter-ations favorable to influenza epidemics Noting thatmost mdash though not all mdash major influenza epidemicsoccurred in time intervals starting 2ndash3 years before andending 2ndash3 years after maximum solar activity they hy-pothesized that solar cycles are able to both regulate and

Levitt et al EMF and wildlife 57

entrain processes of biological microevolution in viralspecies (among others) as well as influence human bio-rhythms in synergistic ways that could lead to influenzaepidemics Although others have also noted links betweeninfluenza pandemics and sunspot activity mdash possiblybased on changes in migratory bird patterns as viral vec-tors [619ndash621]mdash and some have linked sun spots with otheradverse human health events these effects remain of in-terest but are still hypothetical UV radiation which is notcovered in this paper is known to suppress cell-mediatedimmunity and is therefore capable of adversely affectingthe course of a viral infection in some mammal speciesAmbient EMF in lower frequency ranges may also bereducing immune viability across species which cantheoretically foster opportunistic virulence Far more EMFresearch needs to be conducted on viruses one fruitfulapproach might be synergistic investigations in virus-infected plant species

The previous studies of microbes show a pattern ofsensitivity inmicroorganisms to EMFwith associations thatencompass a wide range of critical changes includingconsistent stress responses alterations in growth andviability cell membrane alterations and clear patterns ofhow easily antibiotic resistance forms in microbial life tonow ubiquitous EMF levels

Plants (see Part 2 Supplement 4for a table of flora studies ELF RFR)

Plants have evolved in highly sensitive ways to natural andmanmade EMF in all phases of germination growth andmaturation [31] Magnetoreception which is well docu-mented in animals such as birds has also been describedin plants [622] and plant species can respond to subtlechanges in EMF in the environment including in wholeplant communities [623] They may even lsquocommunicatersquoand gather various kinds of lsquoinformationrsquo via electricalsignals in neuron-like cells in root tips and elsewhere [624]Some hypothesize [625] that a form of vibrational andacoustic sensitivity around 220 Hz may play a role in plantlife although not everyone agrees [626]

Almost all vegetation is subject to complex multi-frequency fields due to their soil-based root systems andhigh water content plus above-ground ambient RFR ex-posures makes plants uniquely susceptible to effects neartransmission towers [623 627] Many EMF studies havefound both growth stimulation as well as dieback Thepresence of numerous RFR-emitters in the German andSwiss Alps is thought to have played a role in the

deforestation there [628] The lsquobrowningrsquo of treetops isoften observed near cell towers especially when water isnear tree root bases [25] Treetops with their high moisturecontent and often thick vegetative canopy are known RFRwaveguides In fact military applications utilize thiscapability in treetops for communication signal propaga-tion in remote areas and for guidance of low-flyingweapons systems [629]

How flora interacts with EMF is still a mystery but aclear pattern has emerged in researching the database forthis paper static ELF-EMF has largely been found benefi-cial to plant and seed growth [630] while RFR is detri-mental Plants clearly have magnetoreception in theirstationary condition The normal ground state of magneticfields for plants is the relatively constant naturalgeomagnetic field that averages between 25 and 65 μTdepending on location and seasonal variations [631] At-mospheric changes such as thunderstorms and lightningcan cause intermittent changes in ambient magnetic fieldsThese activities are also generally associated with rain-water critical to virtually all plant life Plants can detectthese changes and prepare for growth using the upcomingrainfall Trees are seen extending their branches skywardlong before rain actually occurs and such changes matchalterations in tree polarities [632]

There are many studies showing an increase in thegrowth rate in plants such as studies of seed germinationexposed to alternatingmagnetic fields Plants also respondsimilarly to high intensity static magnetic fields This maymean that the physiological mechanism in plants thatcauses magnetic field-induced growth is finely tuned to acertain intensity of magnetic flux Any variation in in-tensity or shape of the ambient magnetic field could acti-vate or hinder this growth mechanism

Lightning for instance generates fast and intenseelectromagnetic pulses (EMP) EMP has consistently beenshown to cause biological effects [633] with just one pulsePlants may have mechanisms so sensitive that they candetect the energy of EMP from kilometers away The pulsecauses a transient change in the environmental magneticfield that may be detected by one or more of the mecha-nisms mentioned in the ldquoMechanismsrdquo section above aswell as discussed below EMPhas been closely investigatedfor military applications for its ability at high intensities todisable electronics While much of the military-supportedresearch finds no biological effects from EMP exposurenon-military supported research does show effects Thisparallels the same findings in industry vs non-industryresearch patterns [165 634]

There is a long history on the study of effects of EMFexposure on plant growth notably the work of the Indian

58 Levitt et al EMF and wildlife

scientist Sir Jagadish Bose (1858ndash1937) who proposed theelectric nature of plant responses to environmental stimuliand studied effects of microwaves on plant tissues andmembrane potentials [635] Interestingly Bose investi-gated the effects of millimeter waves [636] now applicableto 5G technology Bose arguably was a pioneer of wirelesscommunication

Another early pioneer in EMF effects on plants wasHarold Saxon Burr (1889ndash1973) at Yale University whoinvestigated the electric potential of trees in two tree spe-cies (a maple and an elm) located on one property andanother maple tree for comparison growing 40 miles(64 km) away Measurements of numerous parameterswere taken using embedded electrodes that recordedhourly from 1953 to 1961 [637] Simultaneous records oftemperature humidity barometric pressure sunlightmoon cycles sunspot activity weather conditionsatmospheric-potential gradients earth-potential gradi-ents and cosmic rays were correlated with tree potentialsBurr also installed equipment that measured the potentialbetween electrodes in the Earth (about 10 miles apart) andthe potential gradient of the air and found that the air andEarth potentials fluctuated exactly with the phase of thetree potentials although the trees were not always syn-chronous Burr ultimately found that the electrical envi-ronment correlated closely with tree potentials in a kind ofentrainment to diurnal lunar and annual cycles Meteo-rological parameters did not correlate in any immediateway other than when passing thunderstorms elicitedanomalous behavior in the trees in direct parallel to mea-surements with the Earth electrodes This follows the the-ory noted above that plants can sense EMP and takeimmediate information from it

There are no other long-term field studies as detailedas Burrrsquos of magnetic field effects on a plant speciesHowever another field study of RFR in Latvia [638]measured effects directly on trees near the Skrunda RadioLocation Station an early warning radar system thatoperated from 1971 to 1998 The systemoperated in the 156ndash162 MHz frequency range transmitting from four pulsedtwo-way antennas that had operated continuously for over20 years by the time of the study In permanent plots in pineforest stands at varying distances from the radar stationand in control areas tree growth changes were measuredand analyzed using retrospective tree ring data Theyfound a statistically significant negative correlation be-tween the relative additional increment in tree growth andthe intensity of the electric field with the radial growth ofpine trees diminished in all plots exposed to RFR Thedecreased growth began after 1970 which coincided withthe initial operation of the station and was subsequently

observed throughout the period of study The effects ofmany other environmental and anthropogenic factors werealso evaluated but no significant effects on tree growthwere correlated This may have been the first detailed fieldstudy of plants and RFR

Many studies of EMFandplants are today conducted inlaboratories and have often focused on growth promotionto create higher yields of food-producing plants Effects ofstatic EMF pulsed EMF ELF-EMF and RF-EMF have beenreported There are in fact over 200 studies on plants andEMF alone mdash too numerous to review here See Part 2Supplement 4 for a Table of studies on plant seedlings anddevelopment based on the types of EMFrsquos tested

As noted in Supplement 4 and in Halgamuge [627]frequently static and ELF-magnetic fields generallyimprove plant growth whereas RFR retards it This is theopposite of results from animal and animal-cell cultureexperiments in which ELF-MF usually produces the sameeffects as RFR It is interesting to note that Hajnorouzi et al[639] and Radhakrishma et al [640] proposed that MF de-creases environmental stress in plants whereas Vian et al[641 642] considered RFR as a systemic stressor A majormorphological difference between animal andplant cells isthat plant cells have a cell wall that is an active physio-logical organelle which regulates growth and cell divisionand controls cellular communications The cell wall con-tains a considerable amount of water [643] Is it possiblethat absorption of RFR by cell-wall water causes a micro-thermal effect that adversely affects plant cell functionsand even causes cell death whereas thermal effects are notlikely to occur with ELF-EMF exposure

Some plant roots have been found sensitive to bothELF and RFR Belyavskaya [644] found a strong cyto-chemical reaction in pea root cells after exposure to lowlevel magnetic fields Kumar et al [645] found cyto- andgenotoxicity in root meristems of Allium cepa with900-MHz and 1800-MHz RFR Chandel et al [646] studiedcytotoxic and genotoxic activity on DNA integrity in rootmeristems of A cepa using 2100-MHz RFR and foundexposure caused DNA damage with a significant decreasein HDNA accompanied by an increase in TDNA while TMand OTM did not change significantly compared to con-trols Biological effects were dependent on the duration ofexposure with maximum changes seen at 4 h

In a series of studies Stefi et al [647ndash649] investigatedthe effects of long termRFR exposure from the base units ofcommon cordless DECT phone systems (pulsed trans-mission mode 1882 MHz 24 hday 7 dweek) on variousplant species (Arabidopsis thaliana Pinus halepensisGossypium hirsutum respectively) and found structural andbiochemical alterations Compared to controls in Faraday

Levitt et al EMF and wildlife 59

cages exposed plant biomass was greatly reduced and leafstructure was only half as thick Leaves were thinner andpossessed greatly reduced chloroplasts which contributedto overall reduced vitality Root systems were alsoadversely affected They concluded that RFR is a stressorandnoxious to plant life A study of similar design [650] didnot find the same effects on maize (Zea mays) which theyattributed to that plantrsquos structural differences althoughchloroplasts were severely affected (see also Kumar et al[651])

Jayasanka and Asaeda [652] published a lengthy re-view that focused on microwave effects in plants Studiesindicate effects depend on the plant family and growthstage involved and exposure duration frequency andpower density among other factors They concluded thateven for short exposure periods (lt15 min to a few hours)nonthermal effects were seen that can persist for long pe-riods even if initial exposures were very short In additionthey noted that since base stations operate 24 hdayneither short exposures nor recovery periods are possiblein natural habitats as plants are continuously exposedthroughout their life cycles They said that variations in thepower density and frequency of microwaves exert complexinfluences on plants and that clearly diverse plant speciesrespond differently to such factors They concluded it isnecessary to rethink the exposure guidelines that currentlydo not take nonthermal effects into consideration

There are numerous reports of adverse RFR effects onmature flora Waldman-Salsam et al [653] reported leafdamage in trees near mobile phone towersmasts In adetailed long-termfieldmonitoring study from2006 to 2015in two German cities they found unusual and unexplain-able tree damage on the sides of trees facing the towers andcorrelated it to RFR measurements vs control areaswithout exposures They found that tree-side differences inmeasured values of power flux density corresponded totree-side differences in damage Controls which consistedof 30 selected trees in low radiation areas without visualcontact to any phone mast and power flux density under50 μWm2 showed no damage They concluded thatnonthermal RFR from mobile phone towers is harmful totrees and that damage that affects one side eventuallyspreads to the whole tree

Vian et al [642] published a review of plant in-teractions with high frequency RFR between 300 MHz and3 GHz and noted that reports at the cellular molecular andwhole plant scale included numerous modified metabolicactivities (reactive oxygen species metabolism α- andβ-amylase Krebs cycle pentose phosphate pathwaychlorophyll content and terpene emission among others)altered gene expression (calmodulin calcium-dependent

protein kinase and proteinase inhibitor) and reducedgrowth (stem elongation and dry weight) after nonthermalRFR exposure They said changes occur in directly exposedtissues as well as systemically in distant tissues and pro-posed that high-frequency RFR be considered a genuineenvironmental factor highly capable of evoking changes inplant metabolism

Halgamuge [627] also published a review that foundweak non-thermal RFR affects living plants The authoranalyzed data from 45 peer-reviewed studies of 29 differentplant species from 1996 to 2016 that described 169 experi-mental observations of physiological and morphologicalchanges The review concluded that the data substantiatedthat RFR showed physiological andor morphological ef-fects (899 plt0001) The results also demonstrated thatmaize roselle pea fenugreek duckweeds tomato onionsand mungbean plants are highly sensitive to RFR and thatplants appear more responsive to certain frequencies be-tween 800 and 1500MHz (plt00001) 1500 and 2400MHz(p 00001) and 3500 and 8000 MHz (p=00161) Hal-gamuge [627] concluded that the literature shows signifi-cant trends of RFR influence on plants

There is particular concern for impacts to flora and 5Gsince millions of small antennas mounted on utility polestransmitting in MMW and other broadband frequenciesalready are mdash or will soon be mdash in very close proximity tovegetation creating both near- and -far field exposures Asnoted in Halgamuge [627] the following are some studiesinvestigating GHz frequencies already in use or planned for5G that found significant effects on plants Tanner andRomero-Sierra [654] on accelerated growth ofMimosa plant(10 GHz 190 mWcm2 5ndash10 min) Scialabba and Tambur-ello [655] on reduced hypocotyls growth rate in radish(Raphanus sativus) (105 GHz 8 mW or 12658 GHz 14 mWfor 96 h) Tafforeau et al [656] induced meristem (activelydividing group of cells) production in Linum usitatissimum(105 GHz for 2 h at 01 mWcm2) and Ragha et al [657](96 GHz 30 min) found germination depended on expo-sure parameters on Vigna radiata Vigna aconitifolia Cicerarietinum and Triticum aestivum plants This is an area inimmediate need of further investigation given the resultsfrom the previous studies

A thorough review of RFR effects to trees and otherplants was published by Czerwinski et al [622] who re-ported that ecological effects on whole plant communitiescould occur at a very low exposure level of 001ndash10 μWcm2 mdash certainly comparable to limits examined in thispaper They focused on frequencies between 07 and18 GHz and includedmultiple complex indicators for planttypes biometrics and environmental factors It was thefirst comprehensive paper that extended beyond using

60 Levitt et al EMF and wildlife

narrower research methods They noted that although theliterature on the effects of RFR on plants is extensive not asingle field study had assessed the biological response atthe level of awhole plant community biome or ecosystembut rather focused mostly on short-term laboratory studiesconducted on single species They said ldquohellipThis disso-nance is particularly striking in view of the fact that alter-ations in a plant communityrsquos structure and compositionhave long been considered to be well founded sensitiveand universal environmental indicatorsrdquo The paper servesas a predictive model for complex future field studies onlarger ecosystems

Interesting EMF synergistic effects were found withstatic magnetic fields and bacteria in plants Seeking non-chemical methods to improve seed germination after pro-longed periods of storage when seed viability can deteri-orate Jovičić-Petrović et al [658] studied the combinedeffects of bacterial inoculation (Bacillus amyloliquefaciensD5 ARV) and static magnetic fields (SMF 90 mT 5 and15 min) on white mustard (Sinapis alba L) seeds Theirresults found that biopriming with the plant growth-promoting B amyloliquefaciens increased seed growth by4043 Seed response to SMF alone was dependent ontreatment duration While SMF at 5 min increased thegermination percentage exposure at 15 min lowered seedgermination compared with the control However thenegative effect at the longer exposure was neutralizedwhen combined with the bacterial inoculation Bothgermination percentages were significantly higher whenSMF was combined with the bacteria (SMF 5 min + D5ARV and SMF 15 min + D5 ARV 4468 and 5320respectively) compared with control They concluded thatbiopriming and SMF treatment gave better results thanbacterial inoculation alone The highest germination per-centagemdash 5320of germinated seedsmdashwas seenwith thebacterium and 15 min exposure to 90 mT demonstrating asynergistic effect They concluded that such techniquescan be used for old seed revitalization and improvedgermination

Even aquatic plants have been found sensitive toartificial electric fields Klink et al [659] assessed electricfield exposures on growth rates and the content of tracemetals of Elodea canadensis Plants were exposed in alaboratory to an electric field of 54 kVm for seven daysPlant length and Fe Mn Ni Pb and Zn were measuredResults showed the applied electric fields slightlyenhanced root growth They also found changes inmineralabsorption Mn and Ni were significantly lower while Pband Zn were significantly higher in exposed plants Fecontent did not differ between control and exposed plantsThey concluded that electric fields had potential use for

phytoremediation in tracemetal contaminatedwaters Thisstudy also has implications for long term aquatic planthealth in general

Alsoworkingwith electric fields Kral et al [660] foundfascinating regeneration in plant root tips inArabidopsis atvarying electric field exposures and time durationswith theweaker exposures producing the most growth They foundthat imposed electric fields can perturb apical root regen-eration and that varying the position of the cut and the timeinterval between excision and stimulation made a differ-ence They also found that a brief pulse of an electric fieldparallel to the root could increase by up to two‐fold theprobability of its regeneration perturb the local distribu-tion of the hormone auxin and alter cell division regula-tion with the orientation of the root towards the anode orthe cathode playing a role

While mechanisms are still unclear regarding howEMFs affect plants oxidative effects appear to play a sig-nificant role Oxidative changes have been reported inmany studies in plants after exposure to EMF [578 639661ndash671] EMF-related stress has been proposed by Vianet al [641 642] Roux et al [672 673] and Radhakrishmaet al [640] Other mechanisms affecting plants such asferromagnetism radical-pairs calcium ions and crypto-chromes have also been proposed [674 675]

It is apparent that plant growth and physiologymdashwiththeir root systems anchored in the ground while theirlsquoheadsrsquo manifest in the air mdash are affected by exposure toEMF in complex synergistic ways and that they are sus-ceptible to multi-frequency exposures throughout their lifespans

Conclusion

Effects from both natural and man-made EMF over a widerange of frequencies intensities wave forms andsignaling characteristics have been observed in all speciesof animals and plants investigated The database is nowvoluminous with in vitro in vivo and field studies fromwhich to extrapolate The majority of studies have foundbiological effects at both high and low-intensityman-madeexposures many with implications for wildlife health andviability It is clear that ambient environmental levels arebiologically active in all non-human species which canhave unique physiological mechanisms that require natu-ral geomagnetic information for their lifersquos most importantactivities Sensitive magnetoreception allows living or-ganisms including plants to detect small variations inenvironmental EMF and react immediately as well as overthe long term but it can also make some organisms

Levitt et al EMF and wildlife 61

exquisitely vulnerable to man-made fields AnthropogenicEMFmay be contributing more than we currently realize tospeciesrsquo diminishment and extinction Exposures continueto escalate without understanding EMF as a potentialcausative andor co-factorial agent It is time to recognizeambient EMF as a potential novel stressor to other speciesdesign technology to reduce exposures to as low asreasonably achievable keep systems wired as much aspossible to reduce ambient RFR and create laws accord-ingly mdash a subject explored more thoroughly in Part 3

Research funding None declaredAuthor contributions All authors have acceptedresponsibility for the entire content of this manuscriptand approved its submissionCompeting interests Authors state no conflict of interestInformed consent Not applicableEthical approval Not applicable

Part 2 supplements

Supplement 1 Genetic Effects of RFR ExposureSupplement 2 Genetic Effects at Low Intensity StaticELF EMF ExposureSupplement 3 Biological Effects in Animals and PlantsExposed to Low Intensity RFRSupplement 4 Effects of EMF on plant growth

References

1 Besser B Synopsis of the historical development of Schumannresonances Radio Sci 200742RS2S02

2 Balser M Wagner CA Measurements of the spectrum of radionoise from 50 to 100 cycles per second 1 J Res Nat Bur Stand DRadio Propag 196064D34ndash42

3 NASA 2021 httpswwwnasagovmission_pagessunearthnewsgalleryschumann-resonancehtml

4 Friedman JS Out of the blue a history of lightening sciencesuperstition and amazing stories of survival NY Delecorte Press2008101 p

5 AdeyWR Electromagnetic fields and the essence of living systemsIn Andersen JB editor Modern radio science New York NY USAOxford University Press 19901ndash37 pp

6 Becker RO Cross currents the perils of electropollution thepromise of electromedicine Los Angeles USA Jeremy Tarcher199067ndash81 pp

7 Levitt BB Electromagnetic fields A consumerrsquos guide to the issuesand how to protect ourselves Orlando FL USA First editionHarcourt Brace and Co 1995 iUniverse Authors GuildBackinprintcom edition 2007 Lincoln NE USA

8 Levitt BB Moving beyond public policy paralysis InClements-Croome D editor Electromagnetic environments and

health in buildings NewYork NY USA Spon Press 2004501ndash18pp

9 Manzella N Bracci M Ciarapica V Staffolani S Strafella ERapisarda V et al Circadian gene expression and extremely low-frequencymagnetic fields an in vitro study Bioelectromagnetics201536294ndash301

10 IUCN 2018 The International Union for Conservation of NatureVersion 2018-1 Red List of Threatened Species 2018

11 Intergovernmental Science and Policy Platform on Biodiversityand Ecosystem Services Paris France (IPBES) In Brondizio ESSettele J Diacuteaz S Ngo HT editors Global assessment report onbiodiversity and ecosystem services of the IntergovernmentalScience-Policy Platform on Biodiversity and Ecosystem ServicesBonn Germany IPBES Secretariat 2019

12 Sanchez-Bayo F Wyckhuys AG Worldwide decline of theentomofauna a review of its drivers Biol Conserv 20192328ndash27

13 Schultz CB Brown LM Pelton E Crone EE Citizen sciencemonitoring demonstrates dramatic declines of monarchbutterflies in western North America Biol Conserv 2017214343ndash6

14 Xerces Society for Invertebrate Conservation 2019Available from httpsxercesorgmonarchs

15 Center for Biological Diversity Monarch butterfly populationdrops by nearly one-third iconic butterfly has declined by morethan 80 percent in recent decades 2017 Available from httpswwwbiologicaldiversityorgnewspress_releases2017monarch-butterfly-02-09-2017php

16 Guerra PA Gegear RJ Reppert SM A magnetic compass aidsmonarch butterfly migration Nat Commun 201454164

17 Marha K Musil J Tuha H Electromagnetic fields and the livingenvironment Praguel Hungary State Health Publishing House1968 (Trans SBN 911302-13-7 San Francisco Press 1971)

18 Ceballos G Garciacutea A Ehrlich PR The sixth extinction crisis lossof animal populations and species J Cosmol 201081821ndash31

19 Ceballos G Ehrlich PR Barnosky AD Garciacutea A Pringle RM PalmerTM Acceleratedmodernhuman-induced species losses enteringthe sixth mass extinction Sci Adv 20151e1400253

20 Ceballos G Ehrlich PR Dirzo R Biological annihilation via theongoing sixth mass extinction signaled by vertebrate populationlosses and declines Proc Natl Acad Sci Unit States Am 2017114E6089ndash96

21 Weimerskirch H Le Bouard F Ryan PG Bost CA Massive declineof the worldrsquos largest king penguin colony at Ile aux CochonsCrozet Anartic Sci 201830236ndash42

22 Manville AM II Impacts to birds and bats due to collisions andelectrocutions from some tall structures in the United States mdashwires towers turbines and solar arrays state of the art inaddressing the problems In Angelici FM editor Problematicwildlife a cross-disciplinary approach New York NY USASpringer International Publishers 2016415ndash42 pp Chap 20

23 Manville AM II Towers turbines power lines and solar arraysthe good the bad and the ugly facing migratory birds and batsmdashsteps to address problems Invited presentation Earth Scienceand Policy Class GEOL 420 GeorgeMasonUniversity 201639 pPowerPoint slides available online

24 Balmori A The effects of microwave radiation on wildlifepreliminary results 2003 Available from httpwwwemrpolicyorglitigationcase_lawbeebe_hillbalmori_wildlife_studypdf

62 Levitt et al EMF and wildlife

largest king penguin colony shrank by 88 in just 35 years[21] due in major part to effects from climate change whileaccording to the International Scientific Committee forTuna and Tuna-like Species in the North Pacific Oceanover 97 of bluefin tuna have disappeared from theworldrsquos oceans primarily due to industrial overfishing butexacerbated by oil spills contamination and climatechange Tree and cave-dwelling bats until recently werecommon including in the Eastern United States Now withthe massive impacts from White-nosed Syndrome (a fatalbat fungal disease) annual wind-turbine bat collisionmortality estimated at nearly 1 million per year in the USalone [22 23] and pesticide use few bats are seen Batsspecies are also sensitive to EMF Impacts fromEMF as nowseen in extensive reviews add only yet another troublingvariable for all wildlife [24ndash36]

Since all food webs are uniquely tied together there arenegative cascading effects across all ecosystems Birds thateat insects are hard hit 8-in-10 partridges have disappearedfrom French farmlands while there has been a 50ndash80reduction in nightingales and turtledoves respectively in theUK Since 1980 the number of birds that typically inhabitEuropersquos farmlands has shrunk by 55 while in the last 17years French farmland-bird counts dropped by a full thirdIntensified agricultural practices are thought responsiblewith loss of insects being the largest contributor [12 37] Inthe United States of the 1027 species of migratory birdscurrently protected under the Migratory Bird Treaty Act of1918 anestimated40are indeclinebasedonbreedingbirdsurveys [38] Christmas Bird Counts [39] and other moni-toring tools [22 23] This trend is comparable to what ishappening globallyWhat role EMFplays in these declines isunclear but remains a disturbing possibility Nor do we un-derstand the limits of tolerance any given species has forenvironmental disturbance mdash some show high flexibilitywhile others thrive only within the narrowest ranges

One estimate of Earthrsquos species finds that since 1970wild animal populations have been reduced on average by60 Popularly called the ldquosixthmass extinctionrdquo [40] theterm connotes the sixth time in the Earthrsquos history thatlarge numbers of species have rapidly disappeared over arelatively short period this time due to human activity notasteroid strikes or volcanic activity Though not officiallyso-designated many now refer to this most recentgeologicecosystem period as the ldquoAnthropocenerdquo mdash theAge of Man [41ndash46]

Insect populations have been especially hard hit withextinctions eight times faster than that of mammals birdsand reptiles [12] Insect total mass is falling by an estimated25 per year suggesting they could vanish by the nextcentury And what affects insect populations affects

everything in the food web in one way or another Loss ofinsect diversity and abundance can cause devastating ef-fects throughout food webs and endanger entire ecosys-tems [12] In Europe Hallmann et al [47] found amore than75 decline over 27 years in total flying insect biomass in63 protected areas many throughout Germany There wasan 82 decline in mid-summer flying insect mass ManyEuropean insect speciesmigrate fromdistances as far awayas Africa The researchers noted that changes in weatherland use and habitat characteristics alone cannot explainthe overall decline and that there may be more than oneunrecognized factor involved in evaluating declines inoverall species abundance That unrecognized factor maybe the steadily rising ambient EMF that directly parallelsthese declines (see Part 1 Supplement 1)

Similar alarming invertebrate declines were discoveredin the Western Hemisphere in 2017 when American ento-mologist Bradford Lister after 40 years revisited the ElYunqueNational Forest in PuertoRico to followupona studybegun in 1976 [48] In the ensuing decades populations ofarthropods including numerous flying insects centipedesand spiders had fallen by 98 in El Yunque a pristinetropical rainforest within the US National Forest SystemInsectivoresmdash including birds lizards and toadsmdash showedsimilar declines with some species vanishing entirely Aftercontrolling for factors like habitat degradation or loss andpesticide use the researchers concluded that climate changewas the primary factor since the average maximum temper-ature in that rainforest had increased by 4 degF during thatperiod They did not factor in the large US military VLFinstallation in Aquada that communicates with submarinesall over the world or the multiple sweeping over-the-horizonphased array radar units aimed at Puerto Rico from coastalsites in the US that irradiate deep into that forest or themultiple NOAADoppler weather radar sites scattered all overthe small island to track hurricanes or the many cell towersthere too

These global declines are truly alarming with impli-cations for planetary health as well as human and wildlifeintegrity Many who study this say that climate changealone is not the only factor and that something new is goingon [47] The question is could steadily rising environ-mental EMF as one of the most ubiquitous but unrecog-nized new environmental genotoxins introduced since the1980s be contributing to these unprecedented specieslosses beginningwith insects but nowmanifesting in otherspecies too The upper microwave bands couple maxi-mally with some insects the size of fruit flies and arecapable of creating devastating resonance and other ef-fects Historically radiofrequency radiation (RFR) impactsto insects were among the first biological effects to be

4 Levitt et al EMF and wildlife

studied [49] with the hope of discovering new forms ofinsect control [50] All insect metamorphic developmentshave been studied including egg larva pupa and adultstages One hypothesis holds that some adult speciesare more sensitive than at larval stages because adultappendages act as conducting pathways to the body(see ldquoInsectsrdquo below)

It is these exact frequency bands between 30 kHz and3 GHz used in telecommunications technology that havebeen on the rise during this period And 5G is on the hori-zon which may specifically target insect populations (seePart 1)

Species sensitivity to EMFs

Other species have vastly more complex electromagneticsensing tools than humans as well as unique physiologiesthat evolved to sense weak fields Many species are highlysensitive to the Earthrsquos natural electromagnetic fields as wellas geographic and seasonal variations In fact it appears thatmost living things mdash including many species of mammalsbirds fish and bacteria mdash are tuned to the Earthrsquos electro-magnetic background in ways once considered as ldquosuper-powersrdquo but are now known to be physiological even asmechanisms are still imperfectly understood For examplemany animals have been observed sensing earthquakes longbeforehuman instrumentsdetect them including snakes andscorpions that seek shelter cattle that stampede birds thatsingat thewrong timesofday and female cats that franticallymove kittens [7]

This ability is likely due in part to numerous speciesreacting to changes in the Earthrsquos magnetic field andelectrostatic charges in the air detected through a naturallyoccurring mineral called magnetite found in many species[51 52] In fact honey bees are able to detect static mag-netic field fluctuations as weak as 26 nT against back-ground earth-strengthmagneticfields that aremuchhigher[53] and to sense weak alternating fields at frequencies of10 and 60 Hz [54] Magnetite reacts a million times morestrongly to external electromagnetic fields than any otherknown magnetic material Authors Kobayshi and Kirch-vink [52] and Kirchvink et al [53 54] hypothesized resultswere consistent with biophysical predictions of amagnetite-based magnetoreceptor Other mechanismslike radical pair mechanisms and cryptochromes may alsobe responsible (see ldquoMechanismsrdquo below)

Much has been written about magnetoreceptionmdash theterm used to describe how species sense electromagneticfieldsmdashwhich is well established but not well understoodMany species use information about the Earthrsquos natural

fields for migration mating food-finding homing nest-ing and numerous other activities Migratory bird species[55 56] honey bees [57] fish [58] mammals [59] bats [60]numerous insect species [61] mollusks [62] and evenbacteria [63] are known to sense Earthrsquos magnetic fields invarious ways Magnetoreception may enable some birdspecies to actually see the Earthrsquos fields [64]

Some insect and arachnid species (eg Trichobothria)can detect natural atmospheric electric fields [65] whichtrigger ballooning behaviormdash eg climbing to the highestplace letting out silk and traveling onwind currents usinghair-like Trichobothria that detects airborne vibrationscurrents and electrical charge Some have been found ashigh as 25mi (4 km) in the sky dispersing over hundreds ofkilometers Morley and Robert [65] found that the presenceof a weak natural vertical e-field elicited ballooningbehavior and takeoff in the spiders their mechano-sensoryhairs function as putative sensory receivers which areactivated by natural weak electric-fields in response toboth e-field and air-flow stimuli The researchers hypoth-esized that atmospheric electricity was key to the massmigration patterns of some arthropod fauna

Even soil nematodes (Caenorhabditis elegans) orient toearth-strength magnetic fields in their burrowing behav-iors and a recent study byVidal-Gadea [66] found thatweakstaticfields slightly above Earthrsquos naturalfields determinedstem cell regeneration in flatworms (Planaria) [67]

Large ruminant mammalian species also orient to theEarthrsquos fields Grazing cattle and deer were first observedaligning to geomagnetic field lines by Begall et al [68]Using satellite imagery field observations and measuringldquodeerbedsrdquo in snow they noted that domestic cattle acrossthe globe aswell as grazing and resting red (Cervus alphas)and roe (Capreolus capreolus) deer consistently align theirbody axis in a general northndashsouth direction and that roedeer also orient their heads northward when grazing orresting Burda et al [69] discovered however that man-made ELF-EMF disrupted the north-south alignment withthe geomagnetic field in resting cattle and roe deer whenthey found body orientation was random on pastures un-der or near power lines with the disturbed pattern dimin-ishing with distance from conductors Cattle exposed tovarious magnetic field patterns directly beneath or nearpower lines exhibited distinct patterns of alignment Theyconcluded there was evidence for magnetic sensation inlarge mammals as well as overt behavioral reactions toweak ELF-MF in vertebrates implying cellular and mo-lecular effects Slaby et al [70] also found cattle align alonga north-south axis but suggested that such alignment maydepend on herd density as the affect disappeared in herdswith higher numbers Fedrowitz [71] expanded this to

Levitt et al EMF and wildlife 5

include bovine sensitivity to other weak ELF-EMF frompowerlines but with observed effects due to combinedelectric and magnetic fields rather than the electric fieldexposure alone (see ldquoBovinesrdquobelow)

Cerveny et al [72] found red fox (Vulpes vulpes) usegeomagnetic fields during hunting Even domestic dogswere found by Hart et al [73] to be sensitive to small varia-tions in the Earthrsquos orientation in their excretion habitspreferring a general north-south axis for both defecation andurination depending on geomagnetic field changes AndNieszligner et al [74] found dogs and some other species mayactually ldquoseerdquo geomagneticfields through blue-light sensingphotoreceptor proteins in their eyes called cryptochromes

According to the USUK World Magnetic Model [75]sensitivity to the geomagnetic field may further complicateissues for migratory species (eg some turtles sea ani-mals birds and insects) because the Earthrsquos magneticnorth pole is shifting faster than at any time in humanhistory Compared to the period between 1900 and 1980 ithas greatly accelerated to about 30 mi (50 km) distance peryear mdash moving west from over Canadarsquos Ellesmere Islandits traditional allocation for most of recorded history mdashtoward Russia [76] Magnetic north fluctuates according tochanges in the Earthrsquosmolten core unlike true northwhichaligns according to the Earthrsquos axis This trend may indi-cate a coming pole reversal with north and south tradingplaces something that occurs approximately every400000 yearswith the last being about 780000 years agoSome animalsmaybe capable of recalibrating navigationalcues but that remains to be seen Since somemigratory birdspecies may see geomagnetic fields through special re-ceptor cells in their eyes and via other mechanisms theycould be thrown off course It is unclear how many otherspecies also see geomagnetic fields but some crustaceansand several insect species especially thosewith compoundeye structures consisting of thousands of ommatidiamdash tinyindependent photoreception units with a cornea lens andphotoreceptor cells that orient in different directions anddistinguish brightness and many more bands of color thanhumans mdash are good candidates Compared to single-aperture eyes compound eyes have a very large view anglethat can detect fast movement and in some cases lightpolarization

In aquatic environments some lakes have more than200 species of fish that use some form of electromagnetismto locate food and reproduce Electric eels can deliver a500-V zap to kill prey Sharks have an array of electro-magnetic sensors These include magnetic field receptorsin their mouths eyes that are 10 times more sensitive thanhumans and their perception of tiny electric neuronaldischarges from the moving muscles in prey (including

humans) guides their attackingfeeding behavior (seeldquoFishrdquobelow) Sharks are often attracted by low-levelelectromagnetic fields surrounding underwater electriccables and are sometimes electrocuted when they mistakethe conduit for living prey and bite into it Many fish havelateral lines on either side of their bodies that are composedof magnetite which allows fish to swim in synchronousschools [52]

Many other animals evolved special receptor organs todetect environmental EMF The duck-billed platypus(Ornithorhynchus anatinus) a semi-aquatic primitive egg-laying mammal has thousands of electric sensors on itsbill skin As noted in Lai [77] using these electroreceptorsand interacting with another type of mechanoreceptor aplatypus can detect an electric field of 20 μVcm [78] mdashequivalent to that produced by the muscles of a shrimpThe information is processed by the somatosensory cortexof the platypus to fix the location of prey This type ofelectroreception is common in the three species of mono-tremes platypus and long (Zaglossus bruijni) and short-bill (Tachyglossus aculeatus) echidna Electric fish (elas-mobranchs) emit EMF that covers a distance of severalcentimeters [79 80] This allows location of potential preyby comparing its electrical properties with that in its im-mediate vicinity Their electroreceptors have been shownto detect a field of 5 nVcm Such EMF-sensing systems arehighly sensitive and efficient but also highly vulnerable todisruption by unnatural fields Organisms that use thegeomagnetic field for migration have the capability notonly to detect the field but also the orientation of the field

Anthropogenic light frequencies affect wildlife in wayswe have only recently grasped Ecological studies havefound that artificial light-at-night is disrupting nocturnalanimals in devastating ways including disorientation anddisruption in breeding and migration cycles in turtlesflying insects birds butterflies and a host of other wildlifeincluding mammals [81ndash84] As much as 30 of nocturnalvertebrates and over 60 of invertebrates may be affectedby artificial light [85] Illumination reflected off of cloudsknown as ldquosky glowrdquo can produce unnaturally brightconditions at night from various wavelength spectra thatimpact different species with the potential to alter thebalance of species interactions [86 87] It has been foundthat changing the color of the light can help some speciesyet harm another [88] For instance low-pressure sodiumlights that havemore yellow in their spectrum reducemothdeaths around the bulbs but salamanders cannot navigatefrom one pond to the next under yellow or red light Somefrogs have been observed to freeze for hours even afterlights have been turned off and to suspend both feedingand reproduction [83]

6 Levitt et al EMF and wildlife

One of naturersquos greatmysteries involves ldquonatal homingbehaviorrdquo mdash the ability of some animal species to return totheir original location of birth in order to reproducesometimes over great distances Natal homing behavioris known in sea turtles [89] eels [90] and salmon [91]among other species The underlying mechanism thoughimperfectly understood involves such species ldquoremem-beringrdquo the geomagnetic field configurations of theirbirthplace via a process known as ldquoimprintingrdquo and thuscan locate and return to it even if they are thousands ofmileskilometers away at reproduction time Apparentlynewborns of these species are imprinted with the memoryof the intensity and the inclination angle of the localgeomagnetic field This information is then later used tolocate their place of birth where they return to breed

The question is whether man-made EMF could distortthis imprintingmemory in later locating the site For examplewhat if RFR-emitting facilities are locatednear turtle breedingsites Could that interfere with imprinting There is someevidence from Landler et al [92] of adverse effects in turtlesThe researchers found that RFR could disrupt a naturalorientation establish its own orientation and reversecompletely a natural orientation indicating a need forresearch to further investigate as we simply do not know thefull effects to other species from anthropogenic EMF

Energy conduction in differentspecies unique physiologies andmorphologies

The unique physiology and morphology of non-humanspecies create additional complexities For instancequadrapedal species with four feet on the ground havedifferent and potentially more efficient conductivity thanbipedal species with two feet One example is bovineheightened sensitivity to increased ground current nearhigh tension lines [93 94] and cell towers [95ndash97] Alsobodies that are predominately parallel to the groundwhich includes most four-legged mammals rather than aperpendicular upright gait conduct EMF in different waysthan vertical species like humans apes and other pri-mates Species that hug the ground like snakes sala-manders and frogs have unique exposures to groundcurrents especially on rainy nights when water as aconductivemedium can increase exposures [98] This maymake some species more sensitive to artificial groundcurrent caused by electric utility companies using the Earthas their neutral return back to the substation for excess

alternating current on their lines instead of running addi-tional neutral lines on utility poles [99]

Hair and whiskers and related appendages in variousspecies are known to detect small variations in electro-magnetic fields as well as water and weather alterations[100] In fact ants have been observed to use theirantennae as ldquoEMF antennasrdquo when subjected by re-searchers to external electromagnetic fields aligningthemselves to ldquochannelrdquo RFR away from the colony [7]Species such as birds as well as some insects with com-pound eyes structures can see vastly more colors thanhumans while cats dogs and owls for instance hearmany more sound frequencies at incredibly low levels

Magnetoreception mechanismselectroreceptor cells magnetitecryptochromesradical pairs

According to Lai [77] ldquohellipin order for an environmentalentity to affect the functions of an organism the followingcriteria have to be met the organism should be able todetect the entity the level of the entity should be similar tothose in the normal ambient environment which is gener-ally much lower than the level of the entity used inexperimental studies and the organism must haveresponse mechanisms tuned to certain parameters of theentity that allow immediate detection of the presence andchanges of the entity Thus a variation of the entity wouldbe detected as an aberrant input and trigger a responsereaction In order to understand how man-made EMF af-fects wildlife the above criteria must be consideredincluding multiple sensory mechanisms that vary fromspecies to speciesrdquo

The questions are How do diverse species detect weaknatural geomagnetic signals distinguish the subtle inter-nal microcurrent and magnetic fields inherent to allbiology from external fields then get beyond both internaland external background noise to make use of that elec-tromagnetic information

There are three primary mechanisms used to under-stand magnetoreception(1) Magnetic induction of weak electrical signals in

specialized sensory receptors [101](2) Magnetomechanical interactions with localized de-

posits of single-domain magnetite crystals [52 102103]

(3) Radical-pair photoreceptors which may be the mostplausible [104ndash111]

Levitt et al EMF and wildlife 7

In the induction model (mechanism 1) according to Lin[102] the first category of electrodynamic interactions withweak magnetic fields is epitomized by elasmobranchsincluding sharks rays and skates with heads that containlong jelly-filled canals with high electrical conductivityknown as the Ampullae of Lorenzini As these fish swimthrough the Earthrsquos geomagnetic lines of flux smallvoltage gradients are induced in these canals with electricfield detections as low as 05 μVm [101] The polarity of theinduced field in relation to the geomagnetic field providesdirectional cues for the fish However in birds insects andland-based animals such cells have not been foundindicating this may not be a universal mechanism butrather are environmentspecies-specific factors [111]

The magnetomechanical model (mechanism 2) in-volves the naturally occurring iron-based crystalline min-eral called magnetite found in most species [52] Itsfunction is most simply demonstrated in magnetotacticbacteria [63] with high iron content where biogenicmagnetite is manufactured in 20ndash30 single domain crystalchains [112] Orientation is patterned according to thegeomagnetic field Blakemore et al [113] found that mag-netotactic bacteria in the northern hemisphere migratetoward the north pole of the geomagnetic field whereas thesame strainsmigrate toward the South Pole in the southernhemisphere At the equator they are nearly equally dividedin north- and- south seeking orientations [114] And they allmigrate downward in response to the geomagnetic fieldrsquosvertical component which in aqueous environments maybe essential for their survival in bottom sediments

Among the many species where magnetite has beenfound include the cranium and neck muscles of pigeons[115 116] denticles of mollusks [117 118] and the abdom-inal area of bees [119] Tenforde [103] delineated otherspecies with localized magnetite including dolphinstuna salmon butterflies turtles mice and humans

The third mechanistic model (mechanism 3) gettingresearch attention today involves a complex free-radical-pair reaction and conversion of the forms of electrons(singlet-triplet inter-conversion) in a group of proteincompounds known as cryptochromes Cryptochromeshave been found in the retinas of nocturnal migratorysongbirds by Heyers et al [55] and Moller et al [56]showing complex communication with the brain fororientation when relying on magnetoreception Gegearet al [61] found cryptochromes to be a critical magneto-reception component in fruit flies (Drosophila mela-nogaster) As noted in Lai [77] cryptochrones are alsopresent in the retinas of some animals [120] RFR [121] andoscillating magnetic fields [122] have been reported todisrupt the migratory compass orientation in migratory

birds There are also reports that indicate the presence ofcryptochromes in plants which may be responsible for theeffect of EMF on plant growth [123] Cryptochromes are alsoknown to be involved with circadian rhythms [56 124] Foran excellent review on plausibility theories and com-plexities of cryptochromeradical pairs see Ritz et al [111]

Many species likely use a combination of thesemechanisms as well as more subtle influences as yet un-detected The vector of the geomagnetic field may providethe directional information while intensity andor incli-nation provide the positional information needed fororientation In behavioral studies [125 126]Wiltschko et alfound that birds used both magnetite and cryptochromemechanisms when they responded to a short strongmagnetic pulse capable of changing magnetization ofmagnetite particles while their orientation was light-dependent and easily disrupted by high-frequency mag-netic fields in the MHz range indicating radical pair pro-cesses These findings suggest that along withelectrophysiological and histological studies birds have aradical pair mechanism located in the right eye that pro-vides compass-like directional information while magne-tite in the upper beak senses magnetic intensity thusproviding positional information However Pakhomovet al [122] pointed out that the songbird magnetic compasscan be disrupted by an oscillating 1403-MHz magneticfield of 2ndash3 nT at a level that cannot be explained by theradical-pair mechanism

Light plays a significant role [127] which is of envi-ronmental concern today as more technology moves to-ward using the infrared bands for communications and theincrease of satellites create artificialunfamiliar star-likelights in the night sky that are potentially capable ofimpacting night migration patterns There is other evi-dence that species use a combination of photoreceptorsand magnetite-based magnetoreception As mentionedabove in birds the two mechanisms exist side by sidemediating different types of magnetic information asneeded such as flight on sunny vs cloudy days ornocturnal flights and they can be easily disrupted [106128ndash130] Birds may co-process visual information withmagnetic information and be able to distinguish betweenthe two [131 132] This function likely occurs in the eye orhigher avian brain areas via light-dependent informationprocessing and radical pair cryptochromes [131 133] Birdsrsquomagnetic compass is an inclination compass and RFRfields in the Larmor frequencies near 133 MHz were foundto disrupt birdsrsquo orientation in an extremely sensitiveresonance relationship Blue-light absorbing photopig-ment cryptochromes have been found in the retinas ofbirds RFR appears to directly interfere with the primary

8 Levitt et al EMF and wildlife

processes of magnetoreception and disable the aviancompass as long as the exposure is present [126 128]

Mammals have also demonstrated magnetoreceptionindicating radical-pair mechanisms Malkemper et al [134]found that the surface-dwelling wood mouse (Apodemussylvaticus) built nests in the northern and southern sectors ofa visually symmetrical circular arena using the ambientmagnetic field or in a field rotated by 90deg indicating theanimals usedmagnetic cuesWhen themicewere also testedin the ambient magnetic field with a superimposed radiofrequency magnetic field (100 nT 09 to 5 MHz frequencysweep) they changed preference from north-south to east-west nest building But unlike birds that have been foundsensitive to a constant Larmor frequency exposure at133 MHz that range had no effect on mice orientation In-dividual animal physiology clearly plays a role in howvarious species respondMalewski et al [135] also found thatthe Earthrsquos magnetic field acts as a common directional in-dicator in five species of subterranean digging rodents Andfor the first time research also found that human brainwaves exhibit a strong response to ecologically-relevant ro-tations of Earth-strength magnetic fields [136]

We need far better understanding of magneto-receptionrsquos neural cellular and molecular processesbecause the ultimate question is given our constant risingbackground levels of EMF is this ambient noise reaching atipping point beyond which species simply cannot ldquohearrdquoAre we artificially overwhelming living speciesrsquo ability tofunction with innate natural biological sensors thatevolved over eons in a far more ldquoelectro-silentrdquoworld Theelectroreception mechanisms described above mdash electro-receptors magnetite and cryptochroneradical-pairs mdashenable living organisms to detect the presence and imme-diate changes in environmental fields of very low intensityAnd thus they can be easily disturbed by the presence ofunfamiliar low-intensity man-made fields

Electrohypersensitivity in humans has also showninstantaneous response to EMF at low intensity [137] Ac-cording to Lai [77] one wonders whether the underlyingmechanisms of electrohypersensivity are similar to thosedescribed above Electrohypersensitivity may be a remnantof the evolutionary responses of living organisms to elec-tromagnetic fields mdash particularly magnetic fields mdash in theenvironment Similarities include responsiveness to verylow-field intensity the response is persistent and built intothe physiology of an organism and the response is imme-diate and reacts quickly to the fields Cryptochrome-freeradicalmechanismsmay be involved Some people aremoresensitive than others Perhaps non-sensitive people cantolerate and compensate for effects andor have lostresponsiveness to natural magnetic fields and thus have

becomeevolutionarily aberrant Electrosensitivity is an issuein need of more careful and systematic study and has yet tobe broadly highlightedas a health or publicwelfare concern

One recent theory by Johnsen et al [138] postulates thatmagnetoreception in animal species may be ldquonoisyrdquo mdashmeaning that the magnetic signal is small compared tothermal and other receptor noise for instance They specu-late that magnetoreception may serve as a redundant ldquoas-neededrdquo source of information otherwise animal specieswould use it as their primary source of information Manyspecies they note preferentially exploit non-magnetic cuesfirst if they are available despite the fact that the Earthrsquosgeomagnetic field is pervasive and ever-present Theyspeculate that magnetic receptors may thus be unable toinstantaneously attain highly precise magnetic informationand therefore more extensive time-averaging andor otherhigher-order neural processing of magnetic information isrequired This may render ldquohellipthe magnetic sense inefficientrelative to alternative cues that can be detected faster andwith less effortrdquo Magnetoreception may have been main-tained however they said by natural selection because thegeomagnetic field may sometimes be the only availablesource of directional andor positional information

We already know that some species use variousmechanisms to detect EMFs as noted throughout this pa-per With new environmental factors from anthropogeniccauses such as artificial light-at-night airwater pollutionclimate change impacting visibility as environmental cuesand rising background RFR mdash all of which can obscurenatural information mdash magnetoreception may in factbecomemore necessary as an evolutionary survival tool astime goes on not less

Other mechanisms of biologicalsignificance DNA mdash direct andindirect effects(See Part 2 Supplements 1 and 2for tables of ELF and RFR geneticsstudies)

A significant biological effect in any toxicology researchinvolves the basic genetics of an exposed organism Ge-netic effects consist mainly of gene expression chromatinconformational changes and genotoxicity All such effectscan influence normal physiological functions Relevant tothis paper is the fact that genetic effects are found at EMFlevels similar to those in ambient environments far below

Levitt et al EMF and wildlife 9

levels from communication devices and infrastructure (seePart 1 Supplement 1)

DNA the fundamental building block of all life is amolecular double helix that is coiled twisted and foldedwithin the nucleus of each living cell It is essentiallyidentical among species with variations only in numberand specific genes along chromosomes on DNArsquos twistedchains that distinguish various species and their charac-teristics from one another DNA damage repeatedly seen inone species can therefore be extrapolated to other speciesalthough not all species react the same to external stimuli

Many factors both endogenous and exogenousdamage DNA which is then normally repaired by DNAenzymes But an absence of adequate repair can result inthe accumulation of damaged DNA which will eventuallylead to aging cell death (apotosis) andor cancer DNAbreaks occur as both single and double strand eventsdouble strand breaks are difficult to repair correctly andcan lead to mutations DNA damage from endogenousfactors can include free radical formation from mitochon-drial respiration and metabolism exogenous factorsinclude chemicals ionizing and nonionizing radiationand ultra violet light among others [139]

In several early studies Lai and Singh [140 141] foundboth double and single strandDNAbreaks in the brain cellsof rats exposed to RFR for 2 h at 2450MHz andwhole bodySAR levels of 06 and 12 Wkg The effects were interest-ingly blocked by antioxidants [142] suggesting free radicalinvolvement which could indicate an indirect cause forDNA damage (see below) The low-intensity genetic effectslisted in Part 2 Supplements 1 and 2 are at 01 Wkg andless Therefore the Lai and Singh [140 141] RFR studies arenot included in those Supplements Very similar effectshave also been found by Lai and Singh [143 144] with60-Hz magnetic field exposure

There has also been much study of ELF genetic effectsAs discussed in Phillips et al [139] numerous studiesfound that ELF-EMF leads to DNA damage [143ndash158] Twostudies [159 160] showed that ELF also affects DNA repairmechanisms Sarimov et al [161] found chromatin confor-mational changes in human lymphocytes exposed to a50-Hz magnetic field at 5ndash20 microT EMF-induced changes incellular free radicals are also well studied [77 162]

Others investigated DNA damage early on but withoutthe availability of todayrsquos more sensitive assays Sarkaret al [163] exposed mice to 2450-MHz microwaves at apower density of 1 mWcm2 for 2 hday over 120 150 and200 days They found DNA rearrangement in the testis andbrain of exposed animals that suggested DNA strandbreakage Phillips et al [164] were the first to use the cometassay to study two different forms of cell phone signals mdash

multi-frequency time division multiple access (TDMA) andintegrated digital enhanced network (iDEN) mdash on DNAdamage in Molt-4 human lymphoblastoid cells usingrelatively low intensities of 24ndash26 Wg for 2ndash21 h Theauthors reported seeming conflicting increases and de-creases in DNA damage depending on the type of signalstudied as well as the intensity and duration of exposureThey speculated the fields could affect DNA repair mech-anisms in cells accounting for the conflicting results

In a recent literature review of EMF genetic effects byLai [165] analysis found more research papers reportingeffects than no effects For RFR 224 studies (65) showedgenetic effects while 122 publications (35) found no ef-fects For ELF and static-EMF studies 160 studies (77)found effectswhile in 43 studies (23) no effectswere seen

Research now points to the duration signaling charac-teristics and type of exposure as the determining factors inpotential damage [164 166] not the traditional demarcationbetween ionizing and nonionzing radiation Long-term low-level nonionizing radiation exposures common today arethought to be as detrimental to living cells as are short-termhigh-intensity exposures from ionizing radiation Effectsmay just take longer to manifest [167] Nonionizing EMF atenvironmental levels does cause genetic damage Thesehave also been shown in humans exposed to environmentallevels of EMF in both ELF and RFR ranges [168ndash171]Conceivably similar genetic effects could happen in otherspecies living in similar environments

This body of genetics work goes against the pervasivemyth that low-level low-intensity nonionizing radiationcannot cause detrimental genetic effects That premise is infact the bedrock belief upon which vested interests andgovernment agencies rely in support of current exposurestandards But in fact biological systems are far morecomplex than physics models can ever predict [6 8 172] Anew biological model is needed because todayrsquos exposuresno longer fit that framework [173] for humans and wildlifeEnough research now indicates a reassessment is neededperhaps including the very physics model used to backthose traditional approaches (see Part 1)

Direct mechanisms DNA as fractalantennas cell membranes ionchannels

DNA as fractal antennas

There are several likely mechanisms for DNA damage fromnonionizing radiation far below heating thresholds both

10 Levitt et al EMF and wildlife

direct and indirect intracellular intercellular and extra-cellular Suchmechanisms potentially apply to all wildlifeOne direct mechanism theorizes that DNA itself acts as afractal antenna for EMFRFR [174] capable of receivinginformation from exogenous exposures

According to Blank and Goodman [174] DNA hasinteresting electrical characteristics due to its uniquestructure of intertwined strands connected by rungs ofmolecules called nucleotides (also called bases) with eachrung composed of two nucleotides (one from each strand)in bonded pairs The nucleotides are held together byhydrogen bonds in close proximity that results in a strongattraction between the two strands There are electrons onboth molecular surfaces making the symmetrical nucleo-tides capable of conducting electron current along theentire DNA chain a phenomenon called electron transferThis makes DNA a most efficient electrical conductorsomething not lost on nanotechnology researchers

DNAmay also act as an efficient fractal antenna due toits tightly packed shape within the cell nucleus Blank andGoodman [174] characterized DNA properties in differentfrequency ranges and considered electronic conductionwithin DNArsquos compact construction in the nucleus Theyconcluded that the wide frequency range of observed in-teractions seen with EMF is the functional characteristic ofa fractal antenna and that DNA itself possesses the twostructural characteristics of fractal antennas mdash electronicconduction and self symmetry They noted that theseproperties contribute to greater reactivity of DNAwith EMFin the environment and that direct DNA damage couldaccount for cancer increases as well as the many otherbiological effects seen with EMF exposures

A fractal is a self-repetitive pattern of sometimes geo-metric shapes marked by a larger originating design pro-gressing to small identical designs with a potentiallyunlimited periphery Each part of the shape looks like thewhole shape Fractal designs are quite common in natureeg in snailmollusk shells some deciduous tree leaves andconifer needles pine cones many flowering plants somereptile scales bird feathers and animal fur patterns snow-flakes and crystals forming on cold winter glass windowsMineralsmdash both inert and biologicalmdash can also be fractals

The varying sizes within fractals are what make theminherently multi-frequency By mimicking nature repeti-tive fractal patterns are also designed into mechanicaltransceiver antennas that radiate in multiband frequencieswith more or less efficiency [175] Cell phones WiFi digitalTV and many other transceivers use fractal antennas tooperate

The complex twisted shape and coiled structure ofDNA mdash small coils coiled into larger coils or coiled coils

which Blank and Goodman [174] note that no matter howfar you zoom in or out the shape looks the same mdash is theexact structure of a fractal that maximizes the length of anantenna within a compact space while boosting multi-frequency signals As such DNAmay be acting as a hiddenintracellular biological fractal capable of interacting withexogenous EMF across a range of frequencies In fact oneof DNArsquos fundamental functions may be specifically tointeract with exogenous natural energy and as suchmay bemore sensitive to EMF than other larger protein moleculeswithin any living system Once thought safely tucked awayand protected within the nucleus DNA may be acting as amost efficient electrical conductor at the nexus of all lifeThis interesting theory unfortunately has not been fol-lowed up by others to test its biological validity althoughfractals have been mimicked widely in technology

Cell membranesion channels

Another direct effect from EMF is at the cell membraneitself While DNA is lifersquos fundamental building block cellsare DNArsquos complex electron-coherent architecturalexpression The cellrsquos membrane is far more than just aboundary It is rather the most important ordering tool inthe biological space between intracellular and extracel-lular activities ldquohellip a window through which a unitarybiological element can sense its chemical and electricalenvironmentrdquo [176] And it is replete with microcurrent

The cellrsquos outer surface containsmolecules that receiveinnumerable electrochemical signals from extracellularactivities Specific binding portals on the cell membraneset in motion a sequence leading to phosphorylation ofspecific enzymes that activate proteins for cellular lsquoworkrsquoThat includes everything from information processing inthe central nervous system mechanical functions such asmuscle movements nutrient metabolism and the defensework of the immune system amongmany others includingthe production of enzymes hormones antibodies andneurotransmitters [177] Complex microcurrent signalingpathways exist from the cellrsquos outside to the inside viaprotein intramembraneous particles in the phospholipidplasma membrane These convey information on externalstimuli to the cellrsquos interior to allow cellular function

The cell membrane also has electrical propertiesMicrocurrent constantly moves from the interior to theexterior and vice versa of the cell membrane According toAdey and Sheppard [176] some of these properties influ-ence proteins that form voltage gatedmembrane channelswhich is one way that cells control ion flow andmembraneelectromagnetic potential essential to life There are

Levitt et al EMF and wildlife 11

specific windows that react according to frequencyamplitude and duration differences indicating anonlinear and non-equilibrium character to exogenousexposures on cells [177ndash185]

Some pulsed fields are more biologically active thannon-pulsed fields and different forms of pulsing also createdifferent effects As far back as 1983 Goodman et al [186]found pulsed weak electromagnetic fields modified bio-logical processes via DNA transcription when a repetitivesingle pulse and the repetitive pulse train were used Thesingle pulse increased the specific activity of messengerRNA after 15 and 45 min while the pulse train increasedspecific activity only after 45 min of exposure Digitaltechnology simulates pulsing and is the most commonform of environmental exposure today

Cellular calcium ion channels have long been of in-terest and may be particularly sensitive targets for EMFsdue to possible increased calcium flux through the chan-nels which can lead to secondary responses mediatedthrough Ca2+calmodulin stimulation of nitric oxide syn-thesis calcium signaling elevated nitric oxide (NO) NOsignaling peroxynitrite free radical formation andoxidative stress mdash many with implications to DNA as hy-pothesized by Pall [187] Calcium is essential to signaltransduction between cells and is significant to everythingfrom metabolism bonecellblood regeneration hormoneproduction and neurotransmissions among many othersThese cellular calcium responses to EMF indicate an arti-ficial change in the signaling processes at the cell mem-branemdash considered a switchboard for information betweenthe exterior environment and intracellular activities thatguide cell differentiation and control growth [188]

Pall [187] cited 23 studies of effects to voltage gatedcalcium channels (VGCC) and noted nonthermal mecha-nisms were the most likely since many studies showed ef-fects were blocked by calcium channel blockers (widelyprescribed for heart irregularities having nothing to dowith thermal issues) Pall [189] noted that many otherstudies showed EMF changes in calcium fluxes and intra-cellular calcium signaling He hypothesized that alter-ations in intracellular calciumactivitymay explain some ofthe myriad biological effects seen with EMF exposureincluding oxidative stress DNA breaks some cancersinfertility hormonal alterations cardiac irregularities anddiverse neuropsychiatric effects These end points needfurther study and verification

There is much to be learned about calcium effects asstudies are contradictory Changes in free radicals (seebelow) also affect calcium metabolism There are morestudies showing EMF effects on free radicals than calciumchanges Calcium activates the nitric oxide free radical

pathway but there are only a few studies of this pathwayfollowing EMF exposure mdash less than 5 of EMF-oxidativechange studies are on nitric oxide mechanisms Also ofinterest is the fact that power density and frequency win-dows were seen in early research at rising harmonic in-crements along the electromagnetic spectrum beginning inthe ELF bands [190ndash195] Observed effects were quite dra-matic in what researchers described as calcium efflux orlsquodumpingrsquo from cells The most dramatic effects were seenat 180 Hz in the ELF range This appears to contradict Pallrsquoswork [189] cited above as increased calcium efflux is theopposite of what Pallrsquos hypothesis would predict egcalcium influx Withmore research both calcium influx andefflux effects may be found to be caused by different vari-ables andor EMF exposures

In addition exogenous signaling characteristics arealso important to how cells react to both ELF and RFRranges Building on the work that demonstrated carrierwaves of 50 and 147 MHz when sinusoidally amplitudemodulated at 16 Hz ELF in in vitro chick brain tissue [190191] and in live awake cat brain models [196] that createdfrequency windows for calcium efflux Blackman et al[194] additionally found that signaling characteristicswerealso significant Research showed that calcium effluxoccurred only when tissue samples are exposed to specificintensity ranges of an ELF-modulated carrier wave un-modulated carrier waves did not affect ion efflux Black-man et al [194] further wrote that cells may be capable ofdemodulating signals The authors reported that 16-Hz si-nusoidal fields in the absence of a carrier wave altered theefflux rate of calcium ions and showed a frequency-dependent field-induced enhancement of calcium-ionefflux within the ranges 5ndash75 Vm and 35ndash50 Vm (peak-to-peak incident field in air) with no enhancement withinthe ranges 1ndash2 10ndash30 and 60ndash70 Vm This body of workindicates that living cells interact with and are capable oftaking direction from exogenous fields in far more com-plex ways than ever imagined at intensities barely abovebackground levels This work may be particularly impor-tant to new technology that turns previously wired ELFfrequencies into wireless applications such as ldquowirelesselectricityrdquo to charge electric cars

Blackman et al [197] found for the first time a linkbetween the ELFEMF being studied and the density of thenatural local geomagnetic field (LGF) in the production of abiological response Calcium efflux changes could bemanipulated by controlling the LGF along with ELF andRF-EMF exposures In a local geomagnetic field at a densityof 38 μT 15- and 45-Hz electromagnetic signals had beenshown to induce calcium ion efflux from the exposed tis-sues whereas 1- and- 30-Hz signals did not Bawin and

12 Levitt et al EMF and wildlife

Adey [190] found a reduction in efflux when using anelectric field Blackman et al [194] found an increase whenusing an electromagnetic field thus identifyingisolatingfor the first time the significance of the magnetic fieldcomponent in exposure parameters Building on the win-dow ranges noted above Blackman et al [197] demon-strated that the enhanced calcium efflux field-induced15-Hz signal could be rendered ineffective when the LGF isreduced to 19 μT with Helmholtz coils In addition theineffective 30-Hz signal became effective when the LGFwas altered to k253 μT or to +76 μT The results demon-strated that the net intensity of the local geomagnetic field isan important cofactor in biological response and a poten-tially hidden variable in research The results they notedappear to describe a resonance-like relationship in whichthe frequency of the electromagnetic field can induce achange in calcium efflux proportional to LGF density (seeLiboff [198 199] below for more detail)

The bottom line is that changes of this magnitude atthe cellular levelmdash be it directly to DNAwithin the nucleusor via voltage gated channels at the cellrsquos membranemdash canlead to direct effects on DNAwithin and across species Theevidence cited above illustrates the degree likelihood andvariety of impacts from EMF directly on cellular physiologythat are capable of affecting DNA in all living systems inmyriad ways

Indirect mechanisms free radicalsstress proteins resonance Earthrsquosgeomagnetic fields

Free radicals

An indirect or secondary mechanism for DNA damagewouldbe through free radical formationwithin cellswhich isthe most consistently reported with both ELF and RFR ex-posures under many different conditions in biological sys-tems According to Phillips et al [139] free radicals may alsointeractwithmetals like iron [142 151 152 158] andplay a rolein genotoxic effects from something called the Fenton ef-fect mdash a process ldquohellipcatalyzed by iron in which hydrogenperoxide a product of oxidative respiration in the mito-chondria is converted into hydroxyl free radicals which arevery potent and cytotoxic moleculesrdquo [139]

The significance of free radical processes may even-tually answer some questions regarding how EMF interactswith biological systems There are about 200ndash300 papersshowing EMF effects on free radicals [77 168 200] Free

radicals are important compounds involved in numerousbiological functions that affect many species Increases infree radicals explain effects from damage to macromole-cules such as DNA protein and membrane lipidsincreased heat shock proteins neurodegenerative dis-eases and many more

Yakymenko et al [168] published a review on oxidativestress from low-level RFR and found induced molecular ef-fects in living cells including significant activation of keypathways generating reactive oxygen species (ROS) activa-tion of peroxidation oxidative damage in DNA and changesin the activity of antioxidant enzymes In 100 peer-reviewedstudies 93 confirmed that RFR induced oxidative effects inbiological systems and that their involvement in cellsignaling pathways could explain a high pathogenic rangeof biologicalhealth effects They concluded that low-intensity RFR should be recognized as one of the primarymechanisms of biological activity of nonionizing radiationIn a follow-up study Yakymenko et al [200] investigatedthe oxidative and mutagenic effects of low intensity GSM1800 MHz RFR on developing quail embryos exposed inovo (032 μWcm2 48 s On 12 s Off) during 5 days before and14 days through the incubation period They found statisti-cally significant oxidative effects in embryonic cells thatincluded a 2-fold increase in superoxide generation rate an85 increase in nitrogen oxide generation and oxidativedamage to DNA up to twice the increased levels of 8-oxo-dGin cells of 1-day old chicks RFR exposure almost doubledembryo mortality and was statistically significant Theyconcluded that such exposures should be recognized as arisk factor for living cells including embryonic integrity

Lai [77] focused a review on static magnetic fieldELF-EMF and found that changes in free radical activitiesare one of the most consistent effects Such changes canaffect numerous physiological functions including DNAdamage immune system and inflammatory response cellproliferation and differentiation wound healing neuralelectrical activities and behavior Given that many specieshave proven sensitive to natural static geomagnetic fieldsand use such information in critical survival skills somewildlife species may also be adversely affected via freeradical alterations from anthropogenic exposures But Lai[77] noted the inherent contradictions from EMF-inducedchanges in free radicals particularly on cell proliferationand differentiation since those processes can affect cancerdevelopment as well as growth and development Inducedfree-radical changes may therefore have therapeutic ap-plications in killing cancer cells via the generation of thehighly cytotoxic hydroxyl free radical by the Fenton Re-action (noted above) thereby creating a non-invasive low-side-effect cancer therapy

Levitt et al EMF and wildlife 13

Stress proteins

Another potentially indirect effect to DNA is via proteinsynthesis required by all cells to function A living animalconverts animal and plant proteins that it ingests into otherproteins needed for lifersquos activities mdash antibodies forinstance are a self-manufactured protein DNA is critical toprotein synthesis and can create in humans about 25000different kinds of proteins with which the body can thencreate 2000000 types in order to fully function

There are many different classes of proteins Theseinclude stress proteins stimulated by potentially harmfulenvironmental factors to help cells cope and repair damagedue to factors like acute temperatures changes in oxygenlevels chemicalsheavy metals exposure viralbacterialinfections ultraviolet light and other ionizing andnonionizing radiation exposures [124]

The presence of stress proteins indicates healthy repairaction by an organism and is considered beneficial up to apoint as a protective mechanism According to Blank andGoodman [201] ldquoThe 20 different stress protein families areevolutionarily conserved and act as lsquochaperonesrsquo in the cellwhen they lsquohelprsquo repair and refold damaged proteins andtransport them across cell membranes Induction of thestress response involves activation of DNArdquo Stress proteinsare also considered a yardstick to determine what livingcells experience as stress that requires remediation in thefirst placemdash something not always obvious especiallywithsubtle environmental exposures like low-level EMF barelyabove natural background levels

Whether an effect is thermal or nonthermal adverse orsimply observed biologically has been subject to fiercedebate for decades thus tissue-heating DNA pathways arealso central to this paper Heat as a cellular stressor wasfirst observed in the 1960s by Italian researcher FerruccioRitossa in fruit flies (D melanogaster) when experimentaltemperatures were accidentally raised by a few degreesand he observed enlarged chromosomes at particular sites(Drosophilae are often used in research because they onlyhave four pairs of chromosomes are relatively easy toworkwith have a fast breeding cycle and lay numerous eggs)As cited in Blank [124] as Ritossarsquos observation becamebetter understood with effects subsequently seen overdecades in animals plants and yeast cells it came to becalled the ldquoheat shock responserdquo Extensive researchestablished that the heat shock response lead to the for-mation of a unique protein class mdash heat shock proteins(HSP) that repair other proteins from potentially fataltemperature damage as well as assist cells to be morethermo-tolerant Research has gone on to prove that cells

produce other similar proteins to various stressors nowgenerally called stress proteins but most are still catego-rized as ldquoHSPrdquo from the original demarcation

Goodman and Blank [202 203] found that EMF is acellular stressor even at low intensities in the absence ofelevated temperatures They found the protein distributionpatterns synthesized in response to ELF-EMF resembledthose of heat shock with the same sequence of changes eventhough the energy of the two stimuli differed bymany ordersof magnitude Their results indicated that ELF-EMF stimu-lates a similar gene expression pathway as that of thermalshock and is itself a cellular stressor Of particular signifi-cance is the fact that over-expression of stress genes is foundin a number of human tumors and is characteristic of a va-riety of neoplasia [202] Increased stress proteins are seen innumerous animal model studies pertinent to wildlife

Blank and Goodman [201] further noted that both ELFand RFR activate the cellular stress response despite thelarge energy difference between them that the samecellular pathways respond in both frequency ranges andthat models suggest that EMF can interact directly withelectrons in DNA They note that low energy EMF interactswith DNA to induce the stress response while the increasedenergy in RFR can lead to DNA strand breaks As such thismakes the stress response a frequency-dependent direct andindirect cause of DNA damage mdash a significant finding Theyconcluded that exposure standards should not be based onexposure intensity alone but on biological responses longbefore thermal thresholds are met or crossed

Resonance and geomagnetic fields

There are other important direct and indirect ways that EMFsinteractwith and effect biological systems includingvariousforms of resonance mdash cyclotron electron paramagneticnuclear and stochastic mdash as well as through inherentlyproduced biological materials such as magnetite found inbird brains and many other species (see below)

Resonance is the phenomenon that occurs when acertain aspect of a force (like a frequency wave) matches aphysical characteristic (like a cell or whole living organ-ism) and the power inherent in the force is transferred tothe physical object causing it to resonate or vibrate Withinthe object the resonance is self-perpetuating The classicexample is of an opera singer hitting high C in the presenceof a crystal goblet for a sustained period until it shatters

Following the work of Blackman et al [197] who foundthe Earthrsquos local geomagnetic fields (LGF) could influencecalcium ions moving through membrane channels (see

14 Levitt et al EMF and wildlife

above) Liboff [198 199] proposed that cyclotron resonancewas a plausible mechanism for coupling interactions be-tween the LGM and living cells Liboff found cyclotronresonance consistent with other indications that showedmany membrane channels have helical configurationsthat the model could apply to other circulating chargedcomponents within the cell and that cyclotron resonancecould lead to direct resonant electromagnetic energytransfer to selected cell compartments

All resonance is based on a relationship Cyclotron reso-nance is based on the relationship between a constant mag-netic field and an oscillating (time-varying) electric ormagnetic field that can affect the motion of charged particlessuch as ions some molecules electrons atomic nuclei orDNA in living tissue Living systems are filled with chargedparticles necessary for life including calcium sodiumlithium and potassium ions that all pass through the cellmembrane and are capable of affecting DNA Cyclotronresonance occurs when an ion is exposed to a steady mag-netic field (such as the Earthrsquos) which causes the ion to movein a circular orbit at a right angle to the field The speed of theorbit is determined by the charge andmass of the ion and thestrength of themagnetic field If an electric field is added thatoscillates at exactly the same frequency and that is also at aright angle to the magnetic field energy will be transferredfrom the electric field to the ion causing it tomove faster Thesame effect can be created by applying an additional mag-netic field parallel to the constant magnetic field This isimportant because it provides aplausiblemechanism forhowliving cells interact with both natural and artificial fields andexplainshowvanishingly low levels of EMFs cancreatemajorbiological activity when concentrated on ion particles It alsopoints to living systemsrsquo ability to demodulate mdash or take di-rection frommdash certain aspects of electromagnetic informationfrom both natural and artificial exposures [7] Resonanceshould not be underestimated It applies to all frequenciesand is not based on power density alone

Another subtle energy relationship in biology is calledstochastic resonance that has been determined to be sig-nificant in how various species interact with their naturalenvironments in some instances for their survival Sto-chastic resonance is a phenomenon where a signal belownormal sensing can be boosted by adding wide-spectrumwhite noise signals The frequencies in the white noise thatmatch the original signalrsquos frequencies will resonate witheach other and amplify the original signal while notamplifying the rest of thewhite noise This increase inwhatis called the signal-to-noise ratio makes the original signalmore prominent Some fish for instance can ldquohearrdquopredators better in the noise of running water than in stillwater due to stochastic resonance (see ldquoFishrdquo below)

The signal-to-noise ratio has been a prominent aspectof EMF research with some scientists long holding thatenergy exposures below the bodyrsquos natural signal-to-noiseratio could not possibly damage living tissue But the mostrecent research that finds effects to DNA from lowintensity EMF indicates that many variables affect biolog-ical processes often in nonlinear patterns far below thesignal-to-noise ratio Some of the most cutting edgeresearch mdash with an eye toward treating human in uterobirth defects and adult limb regeneration mdash is being donebymanipulating the electric charge across cell membranes(called membrane potential) via intentional manipulationof genes that form ion channels Pai et al [204] found thatby putting ion channels into cells to raise the voltage up ordown they could control the size and location of the brainin embryonic African clawed frogs (Xenopus laevis) thusdemonstrating the importance of microcurrents on mem-brane potential in growth and development The researchgroup also studied endogenous bioelectricity on clawedfrog brain patterning during embryogenesis noting thatearly frog embryos exhibit a characteristic hyperpolar-ization of cells lining the neural tube Disruption of thisspatial gradient of the transmembrane potential (Vmem)diminished or eliminated the expression of early brainmarkers in frogs causing anatomical mispatterningincluding absent or malformed regions of the brain Thiseffect was mediated by voltage-gated calcium signalingand gap-junctional communication The authors hypoth-esized that voltage modulation is a tractable strategy forintervention in certain classes of birth defects in humansbut they did not make the leap to potential environmentaldamage to other species from such ambient exposures

In general whether direct indirect or synergistic tounderstand ambient effects to wildlife one also needs toknow if effects are cumulative what compensatorymechanisms a species may have and when or if homeo-stasis will deteriorate to the point of no return [205] Inlooking at environmental contaminants we have histor-ically focused on chemicals for both direct and indirecteffects such as endocrine disruption But primary bio-logical manifestation is more physical than chemicalsince the only thing that distinguishes one chemical fromanother on the Periodic Table is the amount of electronsbeing traded up and down on the scale Chemicals areactually secondary manifestations of initial atomic prin-ciples not the other way around Plus the synergisticeffects of the Earthrsquos natural fields can no longer be dis-missed as an interesting artifact that is not biologicallyactive or relevant All living systems are first and foremostexpressions of biological energy in various states ofrelationship

Levitt et al EMF and wildlife 15

For a Table of more low-level effects studies on DNAsee Part 2 Supplements 1 and 2

What the studies show

The literature is voluminous on EMF effects to nonhumanspecies goingbackat least to the1930susingmodernmethodsof inquiry We have after all been using animal plant andmicrobial models in experiments for decades We may in factknow less about effects to humans than to other species

In this paper we focused on exposures common intodayrsquos environment In Part 1 Rising Background Levelswe defined low level RFR as power density of 0001 mWcm2 (1 μWcm2) or a SAR of 0001 Wkg Part 2 Supple-ments 3 and 4 contain extensive tables with pertinentstudies that apply to fauna and flora respectively Thesections that follow in Part 2 on individual species includeselected studies of particular interest to how EMF coupleswith and potentially affects wildlife In most studies asillustrated in Part 2 Supplement 3 the intensity of theincident EMF was provided in μWcm2 or Vm To beconsistent throughout the paper we converted intensity inthe studies to μWcm2 However such conversion (ie Vmto μWcm2) tends to overestimate the exposure level anddoes not represent the full picture Therefore where studiesprovided the amount of energy absorbed eg the specificabsorption rate (SAR) they were also included in Supple-ment 3 (inWkg) Very low levels of energy absorption haveshown effects in all living organisms studied

Levitt and Lai [167] reported numerous biological ef-fects fromRFR at very low intensities and SARs comparableto far-field exposures within 197ndash492 ft (60ndash150 m) fromcell towers Included were in vivo and in vitro low-intensityRFR studies Effects included genetic growth and repro-ductive changes increased permeability of the blood brainbarrier changes in stress proteins behavioral responsesand molecular cellular genetic and metabolic alter-ations All are applicable to migratory birds mammalsreptiles and other wildlife and to plant communities andto far-field exposures in general (An update of that tableappears in Part 2 Supplement 3) It is apparent that envi-ronmental levels of RFR can elicit biologicalhealth effectsin living organisms Although there are not enough data onlow-intensity effects of static ELF-EMF to formulate aseparate table some effects of low-intensity static ELF-EMFare also described throughout this paper ELF genotoxiceffects can be found in Part 2 Supplement 2 and ELF inflora are also listed separately in Part 2 Supplement 4

Effects however do not easily translate from the lab-oratory to the field Cucurachi et al [31] reported on 113

studies with a limited number of ecological studies Themajority were conducted in laboratory settings using birdembryos or eggs small rodents and plants In 65 of thestudies effects from EMF (50 of the animal studies andabout 75 of the plant studies) were found at both highand low intensities indicating broad potential effectsBut lack of standardization among the studies and limitedsampling size made generalizing results from organism toecosystem difficult The researchers concluded that due tothe number of variables no clear dosendashresponse relation-ship could be determined Nevertheless effects from somestudies were well documented and can serve as predictorsfor effects to wild migratory birds and other wildlife

As noted elsewhere throughout this paper living or-ganisms can sense and react to very low-intensity electro-magnetic fields necessary for their survival as seen forinstance in studies by Nicholls and Racey [206 207] onbats andmany others Bats are already in serious trouble inNorth America from white-nosed syndrome and commer-cial wind turbine blade collisions Due to the increased useof tracking radars for bird and bat studies impacts willlikely only increase [22 23] Presence of low levels of RFRfrom tracking radars could adversely affect bat foragingactivity which in turn could affect the composition of in-sect populations in the vicinity Many insects includinghoney bees (Apis mellifera var) and butterflies also dependon the Earthrsquos electromagnetic fields for orientation andforaging Presence of exogenous RFR can disturb thesefunctions This is particularly relevant for pollinator in-sects such as bees and butterflies Pollinators are essentialin producing commercial crops for human consumptionincluding almonds apples pears cherries numerousberry crops citrus fruits melons tomatoes sunflowerssoybeans and much more The strongest disruptive effectto insect pollinators occurs at 12 MHz known as the Larmorfrequency [208] which is related to radical pair resonanceand superoxide radical formation This is an importantindication that effects from RFR are frequency-dependent

Lai [77] citing Shepherd et al [209] noted that EMFcan disrupt the directional sense in insects The fact thatmany animals are able to differentiate the north and southpoles of a magnetic field known as the polarity compass[68 73 134 210 211] indicates they are susceptible tohaving that important sense impaired These polaritycompass traits confer survival competitiveness to organ-isms but are of particular concern since directional cuescan be easily disturbed by man-made EMF [69 134 212]

Bird migration also depends on proper sensing andorientation to natural electromagnetic fields A study byEngels et al [213] showed that magnetic noise at 2 kHzndash9 MHz (within the range of AM radio transmission) could

16 Levitt et al EMF and wildlife

disrupt magnetic compass orientation in migratory Euro-pean Robins (Erithacus rubecula) The disruption can occurat a vanishingly low levelof001Vm or00000265μWcm2Similar effects of RFR interference on magnetoreceptionhave also been reported in a night-migratory songbird [214]and the European Robin [126] Migration is already a taxingand dangerous activity for birds adding another potentialnegative impact to bird survival is troubling

Lai [77] also noted that another consideration is theldquonatal homing behaviorrdquo exhibited in some animals thatreturn to their natal birth places to reproduce Theseinclude sea turtles [89] eels [90] and salmon [91] New-borns of these animals are imprinted with the memory ofthe intensity and the inclination angle of the localgeomagnetic field later used to locate their place of birthwhen they return to breed There are indications that man-made EMF can distort this imprinting memory to locate thesite (see ldquoFishrdquo and ldquoTurtlesrdquobelow) This has importantconsequences to the survival of particular species since itinterrupts their reproductive processes

It is clear that biological effects can occur at levels ofman-made RFR in our present environment therebyconceivably altering delicate ecosystems from a largelyunrecognized danger

Mammals

The majority of EMF laboratory research some going backto the 1800s has been conducted on a variety of mammalspecies using mice rats rabbits monkeys pigs dogs andothers (The second and third most used models are oninsects and yeast respectively) Thus with varying degreesof confidence we know a significant amount about howenergy couples with and affects laboratory mammalianspecies across a range of frequencies However this evi-dence does not automatically transfer at the same confi-dence level regarding how this vast body of researchapplies to wildlife including mammalian species

There is unfortunately a dearth of field research onEMF effects to wildlife Referenced below however aremany potential indicator studies The effects seen includereproductive behavioral mating growth hormonalcellular and others

Rodents

Rodents are the most frequently used mammalian speciesin laboratory research across a range of frequencies andintensities While studies are inconsistent there are

enough troubling indications regarding potential EMFimplications for wildlife

In the RFR range there have been several reviews offertility and other issues in rodentmodelswith citations toonumerous to mention heremdash see La Vignera e al [215] andMerhi [216]mdash but some stand out as potentially pertinent towildlife

Magras and Xenos [217] investigated effects of RFR onprenatal development in mice using RFR measurementsand in vivo experiments at several locations near an an-tenna park with measured RFR power densities between0168 and 1053 μWcm2 Divided into two groups were 12pairs of mice placed in locations of different power den-sities and mated five times One hundred eighteen new-borns were collected measured weighed and examinedmacro- and microscopically With each generation re-searchers found a progressive decrease in the number ofnewborns per dam ending in irreversible infertility How-ever the crown-rump length body weight and number oflumbar sacral and coccygeal vertebrae was improved inprenatal development of some newborns RFR was belowexposure standards and comparable to far-field exposuresthat mice could experience in the wild

Aldad et al [218] in a laboratory setting investigatedcell phoneRFR (800ndash1900MHzSARof 16Wkg) exposuresin in-uteromouse models and effects on neurodevelopmentandbehavior They foundsignificant adult behavioral effectsin prenatally exposed mice vs controls Mice exposed in-uterowere hyperactive had decreasedmemory and anxietyand alteredneuronal developmental programming Exposedmice had dose-response impaired glutamatergic synaptictransmission onto layer V pyramidal neurons of the pre-frontal cortex This was the first evidence of neuropathologyinmice from in-utero RFR at cell phone frequencies now themost prevalent in the environment Effects persisted intoadulthood and were transmissible to next generations Suchchanges can affect survival in wild populations

Meral et al [219] looked at effects in guinea pigs (Caviaparcels) from 900 MHz cell phone frequency exposures onbrain tissue and blood malondialdehyde (MDA) gluta-thione (GSH) retinol (vitamin A) vitamin D(3) andtocopherol (vitamin E) levels as well as catalase (CAT)enzyme activity Fourteenmale guinea pigs were randomlydivided into control and RFR-exposed groups containingseven animals each Animals were exposed to 890- to-915MHz RFR (217 Hz pulse rate 2Wmaximumpeak powerSAR 095 Wkg) from a cellular phone for 12 hday (11 h45 min stand-by and 15 min spiking mode) for 30 daysControls were housed in a separate room without cellphone radiation Blood samples were collected throughcardiac puncture biochemical analysis of brain tissue was

Levitt et al EMF and wildlife 17

done after decapitation at the end of the 30-day periodResults found MDA levels increased (plt005) and GSHlevels and CAT enzyme activity decreased while vitaminsA E and D(3) levels did not change significantly in thebrain tissue of exposed animals In blood samples of theexposed group MDA vitamins A D(3) and E levels andCAT enzyme activity increased (plt005) while GSH levelsdecreased (plt005) They concluded that cell phone radi-ation could cause oxidative stress in brain tissue of guineapigs but more studies were needed to determine if effectsare harmful andor affect neural functions

Lai et al [220] found that Sprague-Dawley rats exposedto RFR during water maze testing showed spatial workingmemory deficits compared to controls But similar studies[221ndash223] did notfindperformance effects in spatial tasks oralterations in brain development after similar exposuresHowever subsequent studies in the last two decades haveshown memory and learning effects in animals andhumans after RFR exposure [224]

Several studies also investigated RFR behavioral effectsin rodent models on learning memory mood disturbancesand anxiety behaviors with contradictory results Danielset al [225] found decreased locomotor activity increasedgrooming and increased basal corticosterone levels in ratsexposed to RFR for 3 h per day at 840MHz but no significantdifferences were seen between controls and test animals inspatial memory testing or morphological brain assessmentThe researchers concluded that RFR exposure may lead toabnormal brain functioning

Lee et al [226 227] looked specifically at effects onpregnant mice and rat testicular function from combinedRFR mobile network signal characteristics used in wide-band code division multiple access (W-CDMA) or CDMAused in 3G mobile communications Experiments showedno observable adverse effects on development reproduc-tion or mutation in tested subjects And no significant ef-fects were seen by Poulletier de Gannes et al [228] in in-utero and post-natal development of rats with wireless fi-delity (WiFi) at 2450 MHz Also Imai et al [229] found notesticular toxicity from 195 GHz W-CDMA

Oneextremelyhigh frequency (EHF) study comparable to5G on a mouse model by Kolomytseva et al [230] looked atleukocyte numbers and the functional activity of peripheralblood neutrophils In healthy mice under whole-body expo-sures to low-intensity extremely-high-frequency electromag-netic radiation (EHF 420 GHz 015 mWcm2 20 min daily)found that the phagocytic activity of peripheral blood neu-trophils was suppressed by about 50 (plt001 as comparedwith the sham-exposed control) in 2ndash3 h after the singleexposure Effects persisted for 1 day and thereafter returned tonormal within 3 days But a significant modification of the

leukocyte blood profile was observed inmice exposed to EHFfor 5 days after exposure cessation Leukocytes increased by44 (plt005 as comparedwith sham-exposed animals) Theyconcluded that EHF effects can be mediated via metabolicsystems and further said results indicated whole-body low-intenstiy EHF exposure of healthymice had a profound effecton the indices of nonspecific immunity These low levels willbe common near 5G infrastructure

In well-designed non-rodent mammal field studiesNicholls and Racey [206 207] found that foraging batsshowed aversive behavioral responses near large air trafficcontrol andweather radars Four civil air traffic control (ATC)radar stations three military ATC radars and three weatherradars were selected each surrounded by heterogeneoushabitat Three sampling points were carefully selected formatched habitats type structure altitude and surroundingland class at increasing distances from each station Radarfield strengthswere taken at three distances from the sourceclose proximity (lt656 ft200 m) with a high EMF strengthgt2 Vm (106 μWcm2) an intermediate line-of sight point(656ndash1312 ft200ndash400 m) with EMF strength lt2 Vm and acontrol location out of radar sight (gt1312 ft400 m) regis-tering 0 Vm Bat activity was recorded three times for a totalof 90 samples 30 within each field strength categoryMeasured from sunset to sunrise they found that bat activitywas significantly reduced in habitats exposed to an EMFgreater than 2 Vm compared to 0 EMF sites but suchreduced activity was not significantly different at lower EMFlevels within 400 m of the radar They concluded that thereduced bat activity was likely due to thermal induction andan increased risk of hyperthermia This was a large fieldstudy near commercial radar installations with mostly highintensity exposures but low-level effects cannot be excludedgiven known magneto-sensitivity in bats

In another field study using a small portable marineradar unit significantly less powerful than their earliermeasured field study Nicholls and Racey [207] found thesmaller signal could also deter batsrsquo foraging behaviorsFirst in summer 2007 bat activity was compared at 20foraging sites in northeast Scotland during experimentaltrials with radar switched on and in controls with no radarsignal After sunset bat activity was recorded for a periodof 30 min with the order of the trials alternating betweennights Then in summer 2008 aerial insects were sampledat 16 of the sites using two small light-suction traps onewith a radar signal the other a control Bat activity andforaging were found significantly reduced when the radarsignal was unidirectional creating a maximized exposureof 1767ndash2624 Vm (83ndash183 μWcm2) The radar had nosignificant effect on the abundance of insects captured bythe traps despite reduced bat activity

18 Levitt et al EMF and wildlife

Balmori [231] also noted significantly reduced bat ac-tivity in a free-tailed bat colony (Tadarida teniotis) wherethe number of bats decreased when several cell towerswere placed 262 ft (80 m) from the colony

In the ELF range Janać et al [232] investigated ELFMFeffects mdash comparable to powerline and stray voltageground currentmdash onmotor behavior patterns inMongoliangerbils (Meriones unguiculatus) and found age-dependentchanges in locomotion stereotypy and immobility in 3-and 10-month-old males Animals were continuouslyexposed to ELF-MF (50 Hz 01 025 and 05 mT) for sevendays with behavior monitored for 60 min in the open fieldafter the 1st 2nd 4th and 7th day (to capture immediateeffects) as well as three days after exposure (to capturedelayed effects) They found that exposure to 3-month-oldgerbils increased motor behavior (locomotion and stereo-typy) and therefore decreased immobility In the 3-monthold gerbils ELFMF also showed a delayed effect (except at025 mT) on stereotypy and immobility In 10-month-oldgerbils ELFMF of 01 025 and 05 mT induced decreasedlocomotion a slight increase in stereotypy and pro-nounced stimulation of motor behavior Increased motorbehavior was observed three days after exposure indi-cating long lasting effects Researchers concluded that in 3-and 10-month-old gerbils specific temporal patterns ofmotor behavior changes were induced by ELFMF due toage-dependent morpho-functional differences in brainareas that control motor behavior

The above is a very small sample of rodent studies SeePart 2 Supplements 1 and 2 for more genetic effects to ro-dents and Supplement 3 for additional studies

Bovines

Due to domestication and easy accessibility there arenumerous studies of dairy cows (Bos taurus) which appearparticularly sensitive to both natural andman-made EMFsFedrowitz [71] published a thorough review with citationstoo numerous to mention here Noted in the review is thefact that bovines although easily accessible are difficult tostudy with precision due to their size which createshandling and dosimetric complexities Also noted are thatbovines today are at their milk- and beef-productionphysiological limits and that the addition of even a weakstressor may be capable of altering a fragile bovine phys-iological balance It is clear in the Fedrowitz review thatcows respond to environmental exposures from a broadrange of frequencies and properties even as some studieslack good exposure assessment RFR exposure createdavoidance behavior reduced ruminating and lying times

and alterations in oxidative stress enzymes among otherproblems while ELF-EMF found contradictory evidenceaffecting milk production fat content hormone imbal-ances and important changes in other physiological pa-rameters Cows have also been found sensitive to strayvoltage and transient harmonics with problematic milkproduction health reproduction and behavioral effects

The question is how much of this body of work couldtranslate to other ruminants and largemammals on-field orin the wild such as deercervids mdash behaviorally repro-ductively and physiologically Stray voltage and ELF-EMFnear powerlines and rural area RFR from both ground-based and satellite transmitters for instance may affectwild migratory herds and large ungulates in remote areasthat go undetected

Bovines and RFR

Loscher and Kas [233] observed abnormal behavior in a dairyherd kept in close proximity to a TV and radio transmitterThey found reduction in milk yield health problems andbehavioral abnormalities After evaluating other factors theyconcluded the high levels of RFR were possibly responsibleThey removed one cow with abnormal behavior to anotherstable 20 km away from the antenna resulting in normali-zation of behavior within five days Symptoms reappearedwhen the cowwas returned to the stablenear theantennas Ina later survey Loscher [234] also found effects of RFR on theproduction health and behavior of farm animals includingavoidance behavior alterations in oxidative stress parame-ters and ruminating duration

Balode [59] obtained blood samples from female browncows from a farm close to and in front of the Skrunda Ra-dar ndash located in Latvia at an early warning radar systemoperating in the 156ndash162MHz frequency rangemdashand samplesfrom cows in a control area They found micronuclei in pe-ripheral erythrocyteswere significantly higher in the exposedcows indicating DNA damage

Staumlrk et al [235] investigated short-wave (3ndash30 MHz)RFR on salivary melatonin levels in dairy cattle with oneherd at a farm located at 1640 ft500 m (consideredhigher exposure) and a second control herd located 13123ft4000 m from the transmitter (considered unexposed)The average nightly magnetic field strength readingswere 21-fold greater on the exposed farm (159 mAm)than on the control farm (0076 mAm) At both farmsafter initially monitoring five cowsrsquo salivary melatoninconcentrations at 2-h intervals during night dark phasefor 10 consecutive days and with the short-wave trans-mitter switched off during three of the 10 days (off phase)samples were analyzed using a radioimmunoassay They

Levitt et al EMF and wildlife 19

reported that mean values of the two initial nights did notshow a statistically significant difference betweenexposed and unexposed cows and concluded thatchronic melatonin reduction was unlikely But on the firstnight of re-exposure after the transmitter had been off forthree days the difference in salivary melatonin concen-tration between the two farms (389 pgml CI 204 741)was statistically significant indicating a two-to-seven-fold increase of melatonin concentration Theyconcluded that a delayed acute effect of EMF on mela-tonin concentration could not be excluded and called forfurther trials to confirm results

Haumlssig et al [95] conducted a cohort study to evaluatethe prevalence of nuclear cataracts in veal calves nearmobilephone base stations with follow-up of each dam and its calffrom conception through fetal development and up toslaughter Particular emphasis was focused on the firsttrimester of gestation (organogenesis) Selected protectiveantioxidants (superoxide dismutase catalase glutathioneperoxidase [GPx]) were assessed in the aqueous humor of theeye to evaluate redox status They found that of 253 calves 79(32) had various degrees of nuclear cataracts but only 9(36)of calveshad severenuclear cataracts Theyconcludedthat a relationship between the location of veal calves withnuclear cataracts in the first trimester of gestation and thestrength of antennas was demonstrated The number of an-tennas within 328ndash653 ft (100ndash199 m) was associated withoxidative stress and there was an association betweenoxidative stress and the distance to the nearest base stationOxidative stress was increased in eyes with cataract (OR perkilometer 080 confidence interval 95 062 093) But theresearchers further concluded that it hadnot been shown thatthe antennas actually affected stress Hosmer-Lemeshowstatistics showed an accuracy of 100 in negative cases withlow radiation andonly 1111accuracy inpositive caseswithhigh radiation This reflected in their opinion that there are alot of other likely causes for nuclear cataracts beside basestations and called for additional studies on EMF duringembryonic development

Haumlssig et al [96] further examined a dairy farm inSwitzerland where a large number of calves were born withnuclear cataractsafter amobilephonebase stationwaserectednear the barn Calves showed a 35 times higher risk for heavycataracts if born there compared to theSwissaverageAll usualcauses for cataracts could be excluded but they neverthelessconcluded that the incidence remained unknown

Bovines and swine ELF-EMF stray electric current

Bovines appear unusually sensitive to ELF-EMF from straycurrent caused by both normal industrial and faulty

grounding methods near high tension transmission linesclose to dairy farms Stray current can cover large areas andoccurs when current flows between the grounded circuitconductor (neutral) of a farm and the Earth through dairyhousing equipment like metal grates It typically involvessmall steady power frequency currents [99] not hightransient shocks although that also can sometimes occurunderwetweather conditions According toHultgren [236]dairy cattle can perceive alternating currents exceeding1 mA between the mouth and all four hooves with behav-ioral effects in cows usually occurring above 3 mA Straycurrent can act as a major physical stressor in cows andother animals [237] This may also be happening in wildmigratory species moving through such areas

At the request of dairymen veterinarians and countyextension agents in Michigan US Kirk et al [238] inves-tigated stray current on 59 Michigan dairy farms On 32farms stray current sources were detected Where voltageexceeded 1 V alternating current increased numbers ofdairy cows showed abnormal behavior in the milking fa-cility and increased prevalence of clinical mastitis Re-covery from the stray current-induced abnormalities wasrelated to the type of abnormality and themagnitude of theexposure voltage

Burchard et al [239] in a small but well-controlledalternating exposure study of non-pregnant lactating Hol-stein cows found a longer estrous cycle in cows exposed to avertical electric field of 10 kVm and a uniform horizontalmagneticfield of 30 μT at 60Hz compared towhen theywerenot exposed Rodriguez et al [240] also found that exposureto EMFmay increase the duration of the bovine estrous cycleBurchard et al [241] evaluated effects on milk production inHolsteins exposed to a vertical electric field of 10 kVm and auniformhorizontalMFof 30μTat 60Hzand foundanaveragedecrease of 497 1378 and 1639 inmilk yield fat correctedmilk yield and milk fat respectively in exposed groups andan increase of 475 in dry matter food intake And Buchardet al [242] in two experiments investigated blood thyroxine(T4) levels in lactating pregnant and non-lactating non-pregnant Holstein cows exposed to 10 kVm 30 microT EMF andfound a significant change depending on the time of bloodsampling in exposed groups They concluded that exposureof dairy cattle to ELF-EMF could moderately affect the bloodlevels of thyroxine

Hillman et al [93 94] reported that harmonic distor-tion and power quality itself could be another variable inbovine sensitivity to stray current They found behaviorhealth and milk production were adversely affected bytransients at the 3rd 5th 7th and triplen harmonic cur-rents on utility power lines after a cell tower was foundcharging the ground neutral with 10+ V causing the

20 Levitt et al EMF and wildlife

distortion After installing a shielded neutral isolationtransformer between the utility and the dairy the distor-tion was reduced to near zero Animal behavior improvedimmediately and milk production which had been sup-pressed for three years gradually returned to normalwithin 18 months

Swine (Sus scrofa domesticus) mdash like rats and mice mdashhave demonstrated aversive behavior to ELF-EMF electricfields Hjeresen et al [243] found miniature pigs exposedto 60‐Hz electric fields (30 kVm for 20 hday 7 daysweekup to 6 months) preferred an absence of the field during a235‐h period by spendingmore time out of the electric fieldthan in it during sleep periods And Sikov et al [244] aspart of a broad study of Hanford Miniature swine onreproductive and developmental toxicology (includingteratology) over three breeding cycles found a strong as-sociation between chronic exposure to a vertical uniformelectric field (60‐Hz 30‐kVm for 20 hday 7 daysweek)and adverse developmental effects vs control Theyconcluded that an association exists between chronicexposure to strong electric fields and adverse develop-mental effects in swine (75malformations in exposed vs29 sham) in first generation with consistent results in twosubsequent generations

Avian

Birds are important indicators of ecosystemwell-being andoverall condition Even subtle effects can be apparent dueto their frequent presence in RFR areas Their hollowfeathers have dielectric and piezoelectric propertiesmeaning they are conductive and capable of acting as awaveguide directing external RFR energy directly anddeeply into avian body cavities [245ndash249] Their thin skullshave both magnetite and radical pair receptors (seeldquoMechanismsrdquo above) and they are highly mobile mdash oftentraveling across great migratory distances of tens to asmuch as a hundred thousand kilometers round-trip peryear resulting in potential multi-frequency cumulativeeffects from chronic near middle and far-field exposuresAvian populations are declining worldwide especiallyamong migratory species This means that birds may beuniquely sensitive to adverse effects from environmentalRFR since their natural habitat is air and they often fly atlateral levels with infrastructure emissions bringing themthat much closer to generating sources

Tower and building construction as direct obstaclesare known hazards to birds One tower at 150 feet (46 m)above ground level is thought to account for as many as3000 songbird deaths per month in migratory pathways

during peak migration [250] and communication towercollisions have been documented to kill more than 10000migratory birds in one night at a TV tower in Wisconsin[251 252] It has been known for years that the songbirdpopulations of North America and Europe are plummetingOnly recently were towers considered a significant factorBut is the problem solely due to obstacles in direct migra-tory pathways or is something else involved

RFR from towers may be acting as an attractant to birdsdue to their singular physiology Avian eyes and beaks areuniquely magnetoreceptive with both magnetite and crypt-chrome radical pair receptors One definitive studybyBeasonand Semm [253] demonstrated that the common cell phonefrequency (900-MHz carrier frequency modulated at 217 Hz)at nonthermal intensities produced firing in several types ofnervous system neurons in Zebra Finches (Taeniopygia gut-tate) Brain neurons of irradiated anesthetized birds showedchanges in neural activity in 76 of responding cells whichincreased their firing rates by an average 35-fold vs controlsOther responding cells exhibited a decrease in rates ofspontaneous activity The Beason and Semm study [253]could explain why birds may be attracted to cell towers atheoretical premise they previously observed with Bobolinks(Dolichonyx oryzivorus [254])

RFR may also act as an avian stressorirritant Earlywork by Wasserman et al [255] in field studies on 12 flocksof migratory birds subjected to various combinations ofmicrowave power density and duration under winter con-ditions at Monomet MA using birds from two additionalflocks as controls showed increased levels of aggression insome of the irradiated birds

Other research indicated a range of effects capable ofbroad adverse environmental outcomes Laboratorystudies by Di Carlo et al [256] found decreases in heatshock protein production in chick embryos The re-searchers used 915-MHz RFR on domestic chicken em-bryos and found that exposure typical of some cell phoneemissions reduced heat shock proteins (HSP-70) andcaused heart attacks and death in some embryos Con-trols were unaffected In replicated experiments similarresults were found by Grigorrsquoev [257] and Xenos andMagras [258] Batellier et al [259] found significantlyelevated embryomortality in exposed vs sham groups ofeggs incubated with a nearby cell phone repeatedlycalling a 10-digit number at 3-min intervals over theentire incubation period Heat shock proteins helpmaintain the conformation of cellular proteins duringperiods of stress A decrease in their productiondiminishes cellular protection possibly leading to can-cer other diseases heart failure and reduction in pro-tection against hypoxia and ultraviolet light

Levitt et al EMF and wildlife 21

Not all results are adverse Tysbulin et al [260 261]investigated both short and prolonged GSM 900 MHz cellphone signal exposure on embryo development in Quail(Coturnix coturnix japonica) irradiating fresh fertilizedeggs during the first 38 h and 14 days of incubation using acell phone in connecting mode continuously activatedthrough a computer systemMaximum intensity of incidentradiation on the eggrsquos surface was 02 mWcm2 Resultsfound a significant (plt0001) increase in differentiatedsomites in 38-h exposed embryos and a significant (plt005)increase in total survival of embryos in eggs after 14 daysexposure They also found the level of thiobarbituric acid(TBA) reactive substances was significantly (p 005ndash0001)higher in the brains and livers of hatchlings from exposedembryos and hypothesized that a facilitating effect existsdue to enhanced metabolism in exposed embryos via per-oxidation mechanisms They concluded low-levelnonthermal effects from GSM 900 MHz to quail embryo-genesis is possible and that effects can be explained via ahormesis effect induced by reactive oxygen species (ROS)

Signaling characteristics such as pulsing vs contin-uous wave are also important Berman et al [262] in amulti-lab study of pulsed ELF magnetic fields found ahighly significant incidence of abnormalities in exposedchick eggs vs controls And Ubeda et al [263] found irre-versible damage to chick embryos from weak pulsedELF-EMF magnetic fields that are common in the environ-ment today Initial studies on freshly fertilized chickeneggs were exposed during the first 48 h of post-laying in-cubation to pulsed magnetic fields (PMFs) with 100 Hzrepetition rate 10 μT peak-to-peak amplitude and 500 μspulse duration Two different pulse waveforms were usedwith rise and fall times of 85 μs or 21 μs A two-day expo-sure found significant increased developmental abnor-malities In follow-up research after exposure eggs wereincubated for an additional nine days without PMFs Em-bryos removed from eggs showed an excess of develop-mental anomalies in the PMF-exposed groups comparedwith the sham-exposed samples There was a high rate ofembryonic death in the 21 μs risefall time Results indicatePMFs can cause irreversible developmental changes con-firming that a pulse waveform can determine embryonicresponse to ELF magnetic fields common today

Between 1999 and 2005 Fernie et al for the first timeinvestigated various potential reproductive effects on acaptive raptor species mdash the American Kestrel (Falcosparverius) mdash from ELF-EMF equivalent to that of wildnesting pairs on power transmission lines In a series ofstudies captive pairs were typically bred under control orEMF exposure over 1ndash3 breeding cycles In 1999 Fernieet al [264] investigated photo phasic plasma melatonin in

reproducing adult and fledgling kestrels finding that EMFsaffected plasma melatonin in adult male kestrels sup-pressing it midway through but elevating it at the end ofthe breeding season In long-term but not short-term EMFexposure of adults plasma melatonin was supressed intheir fledglings too which could affect migratory successMolt happened earlier in adult EMF-exposed males than incontrols EMF exposure had no effect on plasmamelatoninin adult females In avian species melatonin is involved inbody temperature regulation seasonal metabolism loco-motor activity feeding patterns migration and plumagecolor changes important for mate selection Melatonin alsoplays a key role in the growth and development of youngbirds The researchers concluded it is likely that the resultsare relevant to wild raptors nesting within EMF exposures

In 2000 Fernie et al [265] focused on reproductivesuccess in captive American Kestrels exposed to ELF-EMFagain equivalent to that experienced by wild reproducingkestrels Kestrels were bred one season per year for twoyears under EMF or controlled conditions In some yearsbut not others EMF-exposed birds showed a weak asso-ciationwith reduced egg laying higher fertility larger eggswithmore yolk albumen andwater but thinner egg shellsthan control eggs Hatching successwas lower in EMFpairsthan control pairs but fledging success was higher thancontrol pairs in one year They concluded that EMF expo-sure such as what kestrels would experience in the wildwas biologically active in a number of ways leading toreduced hatching success

Also in 2000 Fernie et al [266] further investigatedbehavioral changes in American Kestrels to ELF-EMFagain in captive birds comparable to nesting pairs thatcommonly use electrical transmission structures for nest-ing perching hunting and roosting The amount of EMFexposure time of wild reproducing American Kestrels wasfirst determined at between 25 and 75 of the observedtime On a 24-h basis estimated EMF exposure in wildspecies ranged from 71 during courtship to 90 duringincubation Then effects of EMFs on the behavior of captivereproducing kestrels were examined at comparable expo-sures of 88of a 24-h period Additionally captive kestrelswere exposed to EMF levels experienced by wild kestrelsnesting under 735-kV power lines There appeared to be astimulatorystress effect Captive EMF females were moreactive more alert and perched on the pen roof morefrequently than control females during courtship EMF fe-males preened and rested less often during brood rearingEMF-exposed male kestrels were more active than controlmales during courtship and more alert during incubationThe researchers concluded that the increased activity ofkestrels during courtship may be linked to changes in

22 Levitt et al EMF and wildlife

corticosterone but not to melatonin as found in earlierwork [264] but said the behavioral changes observed wereunlikely to result in previously reported effects inEMF-exposed birds as noted above They added thatbehavioral changes of captive EMF-exposed kestrels mayalso be observed in wild kestrels with uncertain results

In 2001 Fernie and Bird [267] looked at ELF-EMFoxidative stress levels in captive American Kestrels usingthe same test parameters described above to see if ELF-EMFexposure elicited an immune system response In captivemale kestrels bred under control or EMF conditionsequivalent to those experienced by wild kestrels short-term EMF exposure (one breeding season) suppressedplasma total proteins hematocrits and carotenoids in thefirst half of the breeding season It also suppressed eryth-rocyte cells and lymphocyte proportions but elevatedgranulosa proportions at the end of the breeding seasonLong-term EMF exposure (two breeding seasons) alsosuppressed hematocrits in the first half of the reproductiveperiod But results found that only short-termEMF-exposed birds experienced an immune responseparticularly during the early half of the breeding seasonThe elevation of granulocytes and the suppression of ca-rotenoids total proteins and melatonin [264] in the samekestrel species indicated that the short-term EMF-exposedmale kestrels had higher levels of oxidative stress due to animmune response andor EMF exposure The researchersnoted that long-termEMF exposuremay be linked to higherlevels of oxidative stress solely through EMF exposureOxidative stress contributes to cancer neurodegenerativediseases and immune disorders And in 2005 Fernie andReynolds [268] noted most studies of birds and EMF indi-cate changes on behavior reproductive success growthand development physiology and endocrinology andoxidative stress mdash with effects not always consistent or inthe same direction under EMF conditions The entire bodyof work by this research group has implications for all wildspecies that encounter a wide range of EMFs on a regularbasis

In field studies on wild birds in Spain Balmori [269]found strong negative correlations between low levels ofmicrowave radiation and bird breeding nesting roostingand survival in the vicinity of communication towers Hedocumented nest and site abandonment plumage deteri-oration locomotion problems and death in Wood Storks(Mycteria americana) House Sparrows (Passer domes-ticus) Rock Doves (Columba livia) Magpies (Pica pica)Collared Doves (Streptopelia decaocto) and other speciesWhile these species had historically been documented toroost and nest in these areas Balmori [269] did not observethese symptoms prior to construction and operation of the

cell phone towers Results were most strongly negativelycorrelated with proximity to antennas and Stork nestingand survival Twelve nests (40 of his study sample) werelocated within 656 ft (200 m) of the antennas and neversuccessfully raised any chicks while only one nest (33)located further than 984 ft (300 m) never had chicksStrange behaviors were observed at Stork nesting siteswithin 328 ft (100 m) of one or several cell tower antennasBirds impacted directly by the main transmission lobe(ie electric field intensity gt 2 Vm) included young thatdied from unknown causes Within 100 m paired adultsfrequently fought over nest construction sticks and failedto advance nest construction (sticks fell to the ground)Balmori further reported that some nests were nevercompleted and that Storks remained passively in front ofcell site antennas The electric field intensity was higher onnests within 200 m (236 plusmn 082 Vm 148 μWcm2) than onnests further than 300 m (053 plusmn 082 Vm 0074 μWcm2)RF-EMF levels including for nests lt100 m from the an-tennas were not intense enough to be classified as thermalexposures Power densities need to be at least 10 mWcm2

to produce tissue heating of even 05 degC [270] Balmorirsquosresults indicated that RFR could potentially affect one ormore reproductive stages including nest constructionnumber of eggs produced embryonic developmenthatching and mortality of chicks and young in first-growthstages

Balmori and Hallberg [271] and Everaert and Bauwens[272] found similar strong negative correlations amongmale House Sparrows (Passer domestics) throughout mul-tiple sites in Spain and Belgium associated with ambientRFR between 1 MHz and 3 GHz at various proximities toGSM cell base stations House Sparrow declines in Europehave been gradual but cumulative for this species oncehistorically well adapted to urban environments Thesharpest bird density declines were in male House Spar-rows in relatively high electric fields near base stationsindicating that long-term exposure at higher RFR levelsnegatively affected both abundance andor behavior ofwild House Sparrows In another review Balmori [25] re-ported health effects to birds that were continuously irra-diated They suffered long-term effects that includedreduced territorial defense posturing deterioration of birdhealth problems with reproduction and reduction ofuseful territories due to habitat deterioration

Birds have been observed avoiding areas with highand low-intensity EMF in daylight as well as nocturnallyAn early study by Southern in 1975 [273] observed that gullchicks reacted to the US militaryrsquos Project Sanguin ELFtransmitter Tested on clear days in the normal geomag-netic field birds showed significant clustering with

Levitt et al EMF and wildlife 23

predicted bearing corresponding with migration directionbut when the large antenna was energized they dispersedrandomly He concluded that magnetic fields associatedwith such conductors were sufficient to disorient birdsLarkin and Sutherland [274] observed that radar tracking ofindividual nocturnal migrating birds flying over a largealternating-current antenna system caused birds to turn orchange altitude more frequently when the antenna systemwas operating than when it was not The results suggestedthat birds sense low-intensity alternating-current EMFduring nocturnal migratory flight

In a well-designedmulti-year avian study ofmagneto-disruption Engels et al [213] investigated environmentalbroadband electromagnetic lsquonoisersquo emitted everywherehumans use electronics including devices and infra-structure They found migratory birds were unable to usetheir magnetic compass in the presence of a typical urbanenvironment today European Robins (E rubecula)exposed to the background electromagnetic lsquonoisersquo presentin unscreened wooden huts at the University of Oldenburgcampus could not orient using their magnetic compassBut when placed in electrically grounded aluminum-screened huts creating Faraday cages that attenuatedelectromagnetic lsquonoisersquo by approximately two orders ofmagnitude their magnetic orientation returned The re-searchers were able to determine the frequency range from50 kHz to 5 MHz was the most disruptive When groundingwas removed or additional broadband electromagneticlsquonoisersquo was deliberately generated inside the screened andgrounded huts birds again lost magnetic orientationabilities They concluded that RFRrsquos magneto-disruptioneffects are not confined to a narrow frequency band Birdstested far from sources of EMFs required no screening toorientwith theirmagnetic compass Thiswork documenteda reproducible effect of anthropogenic electromagneticambient lsquonoisersquo on the behavior of an intact vertebrate Themagnetic compass is integral to bird movement andmigration Thefindings clearly demonstrated anonthermaleffect on European Robins and serves as a predictor foreffects to othermigratory birds especially those flying overurban areas Such fields are much weaker than minimumlevels expected to produce any effects and far below anyexposure standards

Intensity windows in different species have also beenfound where effects can be more extreme at lower in-tensities than at higher ones due to compensatory mech-anisms such as cell apotosis Panagopoulos andMargaritas[34] found an unexpected intensity window at thermallevels around 10 mWcm2 RFR mdash not uncommon near celltowersmdashwhere effects weremore severe than at intensitieshigher than 200 mWcm2 This window appeared at a

distance of 8ndash12 in (20ndash30 cm) from a cell phone antennacorresponding to a distance of about 66ndash98 ft (20ndash30 m)from a base station antenna This could be considered aclassic nonlinear effect and would apply to far-field expo-sures Since cell base station antennas are frequentlylocated within residential areas where birds nest often atdistances 20ndash30 m from such antennas migratory birdsnon-migratory avifauna and other wildlife may beexposed up to 24-h per day

Concerns also apply to impacts from commercial radiosignals on migratory birds The human anatomy is reso-nant with the FM bands so exposure standards are moststringent in that range High intensity (gt6000 W) com-mercial FM transmitters are typically located on the highestground available to blanket a wider area Low powered FMtransmitters (lt1000 W) can be placed closer to the humanpopulation High intensity locations which can be multi-transmitter sites (colloquially called ldquoantenna farmsrdquo) forother services also provide convenient perches and nestsites formigratory birds FMdigital signals which simulatepulsed waves pose additional health concerns to migra-tory birds This creates a dangerous frequency potential forprotected migratory birds such as Bald Eagles with wing-spans that extend to about 6 ft (183 m)mdash a resonant matchwith the length of the FM signalmdash creating a potential full-body resonant effect for both humans and Bald EaglesBirds could experience both thermal and non-thermaleffects

All migratory birds are potentially at risk includingBald Eagles Golden Eagles birds of conservation concern[275] federal andor state-listed bird species birds na-tionally or regionally in peril as well as birds whose pop-ulations are stable Sadly addressing these concerns mdashbeginning with independent research conducted by sci-entists with no vested interest in the outcomes mdash has notbeen a priority for government agencies or the communi-cations industry

Insects and arachnids

Insects are the most abundant and diverse of all animalgroups with more than one million described speciesrepresenting more than half of all known living speciesand potentially millions more yet to be discovered andidentified They may represent as much as 90 of all lifeforms on Earth Though some are considered pests to farmcrops and others as disease vectors insects remainessential to life and planetary health Found in nearly allenvironments they are the only invertebrates that fly butadults of most insect species walk while some swim

24 Levitt et al EMF and wildlife

Because of these different environmental adaptationsdifferent species will encounter different EMF exposures invarying degrees For instance ground-based walking in-sects may be more susceptible to effects from 60 Hz straycurrent while flying insects may be more susceptible towireless exposures However all species tested have beenaffected across a range of the nonionizing electromagneticbands

Most insects have an exoskeleton three-part bodyconsisting of a head thorax and abdomen three pairs ofjointed legs compound eye structures capable to seeingmany more colors widths and images than humans andone pair of antennae capable of sensing subtle meteoro-logical changes and Earthrsquos geomagnetic fields They livein close harmonywith the natural environment for survivaland mating purposes The most diverse insect groups co-evolved with flowering plants many of which would notsurvive without them Most insect species are highly sen-sitive to temperature variations and climate alterations asthey do not dissipate heat efficiently

Nearly all insects hatch from eggs that are laid inmyriad ways and habitats Growth involves a series ofmolts and stages (called instars) with immature stagesgreatly differing from mature insects in appearancebehavior and preferred habitat Some undergo a four-stage metamorphosis (with a pupal stage) and others athree-stage metamorphosis through a series of nyphalstages

While most insects are solitary some mdash like beestermites and antsmdash evolved into social networks living inldquocooperativerdquo organized colonies that can function as oneunit as evidenced in swarming behaviors Some even showmaternal care over eggs and young They communicatethrough various sounds pheromones light signals andthrough their antennae such as during the beesrsquo ldquowaggledancerdquo (see below)

As far back as the 1800s even though testing methodswere primitive by todayrsquos standards researchers werecurious about electromagnetismrsquos effect on insect devel-opment particularly teratogenicity [276] Research on EMFacross frequencies and insect populations has beenongoing since at least the 1930s with an eye toward usingenergy as an insecticide and anti-contaminant in graintypically at high intensity thermal exposures that wouldnot exist in the natural environment Mckinley and Charles[277] found that wasps die within seconds of high fre-quency exposure But not all early work was strictly highintensity or all effects observed due to thermal factors

There were interesting theories introduced by earlyresearchers regarding how energy couples with variousinsect species Frings [278] found larval stages are more

tolerant to heat than adult insects with appendages thatcan act as conducting pathways to the body and that themore specialized the insect species the more susceptiblethey appear to microwave exposure Carpenter and Liv-ingstone [279] studied effects of 10 GHz continuous-wavemicrowaves at 80 mWcm2 for 20 or 30 min or at 20 mWcm2 for 120 min on pupae of mealworm beetles (Tenebriomolitor)mdash clearlywithin thermal ranges In control groups90 metamorphosed into normal adult beetles whereasonly 24 of exposed groups developed normally 25died and 51 developed abnormally Effects wereassumed to be thermally induced abnormalities until theysimulated the same temperature exposure using radiantheat and found 80 of pupae developed normally Theyconcluded that microwaves were capable of inducingabnormal effects other than through thermal damage

Fruit flies

Insects at all metamorphic stages of development havebeen studied using RFR including egg larva pupa andadult stages Much work has been done on genetic andother effects with fruit flies (D melanogaster) because oftheirwell-described genetic system ease of exposure largebrood size minimal laboratory space needed and fastreproductive rates Over several decades Goodman andBlank using ELF-EMF on Drosophilamodels found effectsto heat shock proteins and several other effects ([201] andsee ldquoMechanismsrdquo above) It is considered a model com-parable to other insects in thewild approximating that sizeD melanogaster may be the most lab-studied insect onEarth although honey and related bee species due to theirdevastating losses over the last decade and significance toagriculture are quickly catching up

Michaelson and Lin [50] noted that RFR-exposed in-sects first react by attempting to escape followed bydisturbance of motor coordination stiffening immobilityand eventually death depending on duration of exposureand insect type For example D melanogaster survivedlonger than 30minwhile certain tropical insects live only afew seconds at the same field intensity Also noted wereconcentration changes in many metabolic products andeffects to embryogenesis mdash the period needed for a but-terfly to complete metamorphosis mdash with acceleratedgastrulation and larval growth [17] Michaelson and Lin[50] cited several negative studies with D melanogasterexposed with continuous-wave RFR between 25 and2450 MHz on larval growth [280 281] and mutagenicity[282] This was after Heller andMickey [283] found a tenfoldrise in sex-linked recessive mutations with pulsed RFR

Levitt et al EMF and wildlife 25

between 30 and 60 MHz It was among the earliest studiesthat found pulsing alone to be a biologically activeexposure

As reported in Michaelson and Lin [50] Tell [284]looked at D melanogasterrsquos physiological absorptionproperties and found that a group of 6-day old male wild-type flies exposed to 2450 MHz for 55 min at an intensefield caused a dramatic 65 reduction in bodyweight Thiswas thought to be from dehydration They then sought tocalculate the fruit flyrsquos absorption properties in relation toplane electromagnetic waves and found that a fly has onlya 11000th effective area of its geometric cross section andthus is an inefficient test species for absorbed microwaveradiation However they concluded that fruit flies wereresponsive to absorbed energy at thermal levels as a blackbody resonator at a power density of 1044 times 104 mWcm2corresponding to a thermal flux density of 0562 times 10minus3 calThese are levels found in close proximity to broadcast fa-cilities and cell phone towers today

More recent investigations of RFR by Weisbrot et al[285] using GSM multiband mobile phones (9001900 MHz SAR approximately 14 Wkg) on D mela-nogaster during the 10-day developmental period from egglaying through pupation found that non-thermal radiationincreased numbers of offspring elevated heat shockprotein-70 levels increased serum response element (SRE)DNA-binding and induced the phosphorylation of the nu-clear transcription factor ELK-1Withinminutes therewasa rapid increase of hsp70 which was apparently not athermal effect Taken together with the identified compo-nents of signal transduction pathways the researchersconcluded the study provided sensitive and reliable bio-markers for realistic RFR safety guidelines

Panagopoulos et al [286] found severe effects in earlyand mid-stage oogenesis in D melanogaster when flieswere exposed in vivo to either GSM 900-MHz or DCS1800-MHz radiation from a common digital cell phone atnon-thermal levels for a few minutes per day during thefirst 6 days of adult life Results suggested that the decreasein oviposition previously reported [287ndash289] was due todegeneration of large numbers of egg chambers after DNAfragmentation of their constituent cells which was inducedby both types of mobile phone radiation Induced celldeath was recorded for the first time in all types of cellsconstituting an egg chamber (follicle cells nurse cells andthe oocyte) and in all stages of early and mid-oogenesisfrom germarium to stage 10 during which programmedcell death does not physiologically occur Germarium andstages 7ndash8 were found to also be the most sensitivedevelopmental stages in response to electromagnetic stressinduced by the GSM and DCS fields Germarium was also

found to be more sensitive than stages 7ndash8 These paperstaken collectively indicate serious potential effects to allinsect species of similar size to fruit flies from cell phonetechnology including from infrastructure and transmittingdevices

Fruit flies have also been found sensitive to ELF-EMFGonet et al [290] found 50 Hz ELF-EMF exposure affectedall developmental stages of oviposition and developmentof D melanogaster females and weakened oviposition insubsequent generations

Savić et al [291] found staticmagneticfields influencedboth development and viability in two species ofDrosophila (D melanogaster and D hydei) Both speciescompleted development (egg-to-adult) in and out of thestatic magnetic field induced by a double horseshoe mag-net Treated vials with eggswere placed in the gap betweenmagnetic poles (47 mm) and exposed to the average mag-netic induction of 60 mT while control groups were keptfar from the magnetic field source They found that expo-sure to the static magnetic field reduced development timein both species but only results for D hydei were statisti-cally significant In addition the average viability of bothspecies was significantly weaker compared to controlsThey concluded a 60 mT static magnetic field could be apotential stressor influencing on different levels bothembryonic and post-embryonic fruit fly development

Beetles

Other insect species also react to both ELF-EMF andRF-EMF Newland et al [292] found behavioral avoidancein cockroaches (Periplaneta americana) to static electricfields pervasive in the environment from both natural andman-made sources Such fields could exist near powerlinesor where utilities ground neutral lines into the Earth Theyfound insect behavioral changes in response to electricfields as tested with a Y-choice chamber with an electricfield generated in one arm of the chamber Locomotorbehavior and avoidance were affected by the magnitude ofthe electric fields with up to 85 of individuals avoidingthe charged arm when the static e-field at the entrance tothe arm was above 8ndash10 kVm Seeking to determinemechanisms of perception and interaction they then sur-gically ablated the antennae and cockroaches were unableto avoid electric fields They concluded that antennae arecrucial in cockroach detection of electric fields that therebyhelps them avoid such fields They also noted that cock-roach ability to detect e-fields is due to long antennaewhich are easily charged and displaced by such fields notbecause of a specialized detection system This leads to the

26 Levitt et al EMF and wildlife

possibility that other insects may also respond to electricfields via antennae alone

Vaacutecha et al [208] found that cockroaches (P americana)were sensitive to weak RFR fields and that the Larmor fre-quency at 12 MHz in particular had a ldquodeafening effectrdquo onmagnetoreception The parameter they studied was the in-crease in locomotor activity of cockroaches induced by peri-odic changes in geomagnetic North positions by 60deg Theonset of the disruptive effect of a 12 MHz field was foundbetween 12 and 18 nT whereas the threshold of a field twicethe frequency (24 MHz) fell between 18 and 44 nT A 7 MHzfield showed no significant effect even at maximal of 44 nTThe results suggested resonance effects and that insects maybe equipped with the same magnetoreception systemas birds

Prolić et al [293] investigated changes in behavior viathe nervous system of cerambycid beetles (Morimus fune-reus) in an open field before and after exposure to a 50 HzELF-MF at 2 mT Experimental groups were divided intoseveral activity categories Results showed activityincreased in the groups with medium and low motor ac-tivity but decreased in highly active individuals High in-dividual variability was found in the experimental groupsas well as differences in motor activities between the sexesboth before and after exposure to ELF‐MF They assumedactivity changes in both sexeswere due to exposure to ELF‐MF Only a detailed analysis of the locomotor activity at 1‐min intervals showed some statistically significant differ-ences in behavior between the sexes

Ants

Ants are another taxa found sensitive to EMF Ants comprisebetween 15 and 25 of the terrestrial animal biomass andthrive in most ecosystems on almost every landmass onEarth By comparison the total estimatedbiomass (weight) ofall ants worldwide equates to the total estimated biomass ofall humans Their complex social organization in colonieswith problem-solving abilities division of labor and bothindividual and whole colony communication via complexbehavioral and pheromone signaling may account for theirsuccess in so many environments Some ant species (egFormica rufa-group) are known to build colonies on activeearthquake faults and have been found to change behaviorhours in advance of earthquakes [294] thus demonstratingpredictive possibilities Ants can modify habitats influencebroad nutrient cycling spread seeds tap resources anddefend themselves Ants co-evolvedwith other specieswhichled to many different kinds of mutual beneficial and antag-onistic relationships

Ants (eg Solenopsis invictus) are long known to besensitive to magnetic fields both natural and manmade[295] Ants (eg Atta colombica) like birds have beenfound to be sensitive to the Earthrsquos natural fields and to useboth a solar compass on sunny days as well as a magneticcompasswhen there is cloud cover [296] Jander and Jander[297] similarly found that the weaver ant (Oecophylla spp)had amore efficient light compass orientation with amuchless efficient magnetic compass orientation suggestingthat they switch from the former to the latter when visualcelestial compass cues become unavailable There is evi-dence from Esquivel et al [298] that such magneto-reception is due to the presence of varying sized magnetiteparticles and paramagnetic resonance in fire ants (Sol-enopsis spp) But Riveros and Srygley [299] found a morecomplex relationship toward a magnetic compass ratherthan the presence of magnetite alone when leafcutter ants(Atta columbica) were subjected to a brief but strongmagnetic pulse which caused complete disorientationregarding nest-finding They found external exposurescould interfere with antsrsquo natural magnetic compass inhome path integration which indicated evidence of acompass based on multi-domain andor super-paramagnetic particles rather than on single-domain par-ticles like magnetite

Acosta-Avalos et al [300] found that fire ants aresensitive to 60 Hz alternating magnetic fields as well asconstant magnetic fields changing their magnetic orien-tation and magnetosensitivity depending on the relationbetween both types of magnetic fields Alternating currenthad the ability to disrupt ant orientation raising thequestion of effects to wild species from underground wir-ing and the common practice of powerline utility com-panies using the Earth as a neutral return pathway tosubstations creating stray current along the way [99]

Camelitepe et al [301] tested black-meadow antsrsquo(Formica pratensis) response under both natural geomag-netic and artificial earth-strength static EMFs (245 μT)They found that under the natural geomagnetic field whenall other orientational cues were eliminated there wassignificant heterogeneity of ant distribution with the ma-jority seeking geomagnetic north in darkness while underlight conditions ants did not discriminate geomagneticnorth Under artificial EMF exposure however ant orien-tation was predominantly on the artificial magnetic NSaxis with significant preference for artificial north in bothlight and dark conditions This indicated EMF abilities toalter ant orientation

Ants are also shown to react to RFR [302 303] Cam-maerts et al [304] found that exposures to GSM 900MHz at00795 μWcm2 significantly inhibited memory and

Levitt et al EMF and wildlife 27

association between food sites and visual and olfactorycues in ants (Myrmica sabuleti) and eventually wiped outmemory altogether Subsequent exposure after a brief re-covery period accelerated memoryolfactory loss within afew hours vs a few days indicating a cumulative effecteven at very low intensity The overall state of the exposedant colonies eventually appeared similar to that exhibitedby honey bee (Apis mellifera) colony collapse disorderAlthough the impact of GSM900MHz radiationwas greateron the visual memory than on the olfactory memory theresearchers concluded that such exposures mdash common tocell phonestowers mdash were capable of a disastrous impacton a wide range of insects using olfactory andor visualmemory including bees Many ant species (eg Lasiusneglectus Nylanderia fulva Camponotus spp Hymenopteraformicidae Solenopsis invicta among others) are attractedto electricity electronic devices and powerlines therebycausing short circuits and fires One hypothesis [305] is thatthe accumulation of ants in electrical equipment may bedue to a few foraging ldquoworker antsrdquo seeking warmth andfinding their way into small spaces completing electricalcontacts which then causes a release of alarm exocrinegland pheromones that attract other ants which then gothrough the same cycle In their study they found thatworkers subjected to a 120 V alternating-current releasedvenom alkaloids alarm pheromones and recruitmentpheromones that elicited both attraction and orientation inants as well as some other unknown behavior-modifyingsubstances But given how ants are affected by EMFs ingeneral it is likely that an attractant factor is also involvednot just warmth and small spaces

There is evidence that ants use their antennae asldquoantennasrdquo in two-way electrochemical communicationsOver 100 hundred years ago Swiss researcher AugusteForel [306] removed the antennae of different species ofants and put them together in one place What would havenormally evoked aggressive behaviors among the differentspecies did not occur and they got along as if belonging tothe same colony To Forel this indicated an ability of antantennae to help different ant species identify each other

Two mechanisms in ants have long been known forchemical receptivity as well as electromagnetic sensitivityRecently Wang et al [307] found evidence that chemicalsignals located specific to antennae vs other body areasdrew more attention from non-nest mates When cuticularhydrocarbons (CHCs) were removed by a solvent fromantennae non-nest mates responded less aggressivelythan to other areas of the body indicating that antennaereveal nest-mate identity conveying and receiving socialsignals Regarding magnetoreception magnetic measure-ments [308ndash310] found the presence of biogenic magnetite

was concentrated in antennae and other body parts of theant Pachycondyla marginata De Oliveira et al [311] alsofound evidence of magnetite and other magnetic materialsimbedded in various locations of antennae tissue inP marginata indicating that antennae function as magne-toreceptors The amount of magnetic material appearedsufficient to produce a magnetic-field-modulated mecha-nosensory output and therefore demonstrated a magneto-receptiontransduction sense in migratory ants

Ticks

Ticks are members of the order Arachnida shared withscorpions and spiders Recent papers in a tick species(Dermacentor reticulates) mirrors an attraction to somefrequencies but not others Vargovaacute et al [312 313] foundthat exposure to RFRmaybe apotential factor altering bothpresence and distribution of ticks in the environmentStudies were conducted to determine potential affinity ofticks for RFR using radiation-shielded tubes (RST) undercontrolled conditions in an electromagnetic compatibilitylaboratory in an anechoic chamber Ticks were irradiatedusing a Double-RidgedWaveguide Horn Antenna to RF-EMFat 900 and 5000 MHz 0 MHz served as control Resultsfound that 900 MHz RFR induced a higher concentration ofticks on the irradiated arm of RSTwhereas at 5000MHz ticksescaped to the shielded arm In addition 900 MHz RFR hadbeen shown to cause unusual specific sudden tick move-ments during exposure manifested as body or leg jerking[312] These studies are the first experimental evidence of RFRpreference and behavioral changes in D reticulates with im-plications forRFR introduced into thenatural environment bydevices and infrastructure In a further study Frątczak et al[314] reported that Ixodes ricinus ticks were attracted to900 MHz RFR at 01 μWcm2 particularly those infected withRickettsia (spotted fever)

RFR may be a new factor in tick distribution alongwith known factors like humidity temperature and hostpresence causing concentrated non-homogenous ormosaic tick distribution in natural habitats Tick preferencefor 900 MHz frequencies common to most cell phones haspossibly important ecological and epidemiological conse-quences Increasing exposures from use of personal de-vices and infrastructure in natural habitats where ticksoccur may increase both tick infestation and diseasetransmission Further studies need to investigate thisworkgiven the ubiquity of ticks today their northward spreaddue to climate change in the Northern Hemisphere and theincreasing and sometimes life-threatening illnesses theytransmit to humans pets and wildlife alike

28 Levitt et al EMF and wildlife

Monarch butterflies

The American Monarch butterfly (D plexippus) has fasci-nated researchers for over 100 years as it is the only insectknown to migrate in multi-generational stages [315ndash319]with the ability to find their exact birthplace on specificmilkweed plants (Asclepias spp) at great distances acrossland and oceans

Monarchs (D plexippus) found across Southern Can-ada the United States and South America are generallydivided by the Rocky Mountains into eastern and westernmigratory groups Their population has precipitouslydeclined by 994 since the 1980s (85 of that since 2017)and by 90 in the past two decades in both western andeastern populations [13 15] These steep declines are fromnumerous anthropogenic causes and may have alreadycrossed extinction thresholds thereby leaving us bereft notonly of their beauty and inspiration but also the perfectmodel for long-distance animalmigration study in general

Monarch butterflies are among North Americarsquos mostbeloved invertebrates They have for centuries navigatedthousands of mileskilometers in an iconic fall migrationfrom southern Canada and the mid- and northeastern USto a small area of about 800 square miles (2072 squarekilometers) in Central Mexico where they once winteredover in the millions in small remote oyamel fir forests Bythe time they reach their final destination some will havetraveled distances exceeded only by some migratoryseabird species The monarch is the only insect known tomigrate annually over 3000miles (4828 km) atsim 250miles(402 km) per day in the fall from the Canadian border toMexico and in the springtime back again Similar to somebird species it is the only butterfly known to have a two-way migration pattern Monarchs are only followed byarmy cutwormmoths (Euxoa auxiliaris) whichmaymigrateseveral thousand kilometers to high elevation sites in theRocky Mountains to escape lowland heat and drought

But monarchs are more interesting than for this oneamazing migrational feat alone How they do this is a long-standing mystery since their entire lifecycle includingtheir two-stage spring return migration is multi-generational indicating genetic factors in directionalmapping since the final return fall migration south cannotbe considered ldquolearnedrdquo Several multifaceted mecha-nisms must come into play as well as little understoodcomplexities in how those mechanisms cooperate andtrade off with each other under different environmentalcircumstances Monarchs also go from solitary insectsduring early developmental stages confined to specificlocations then exhibit social insect behaviors after thethird generation has reached northern latitudes and turned

south during the final fall migration And all of this hap-pens in a brain the size of a grain of sand

Reppert et al [320] published an excellent review in2010 on the complexities of monarch migration noting ldquohelliprecent studies of the fall migration have illuminated themechanisms behind the navigation south using a time-compensated sun compass Skylight cues such as the sunitself and polarized light are processed through both eyesand likely integrated in the brainrsquos central complex thepresumed site of the sun compass Time compensation isprovidedbycircadianclocks thathaveadistinctivemolecularmechanism and that reside in the antennae Monarchs mayalso use a magnetic compass because they possess twocryptochromes that have the molecular capability for light-dependent magnetoreception Multiple genomic approachesare being utilized to ultimately identify navigation genesMonarch butterflies are thus emerging as an excellent modelorganism to study the molecular and neural basis of long-distancemigrationrdquoReppert anddeRoode [321] updated thatinformation in 2018

Although it has been known for some time that mon-archs use a circadian rhythm time-compensated direc-tional sun compass [316 322ndash338] many questions remainabout its dynamics and concerns regarding effects fromradiation

Monarch antennae are known to contain magnetite[339 340] and cryptochromes [335 336 341 342] mdash bothunderstood to play a role in magnetoreception (seeldquoMechanismsrdquoabove) One early study by Jones and Mac-Fadden [343] found magnetic materials located primarilyin the head and thorax areas of dissected monarchs Morerecently Guerra et al [16] found convincing evidence thatmonarchs use a magnetic compass to aid their longest fallmigration back to Mexico Those researchers used flightsimulator studies to show that migrants possess an incli-nation magnetic compass to assist fall migration towardthe equator They found this inclination compass is light-dependent utilizing ultraviolet-Ablue light between 380and 420 nm and noted that the significance of light(lt420 nm) for an inclination compass function had notbeen considered in previous monarch studies They alsonoted that antennae are important for an inclinationcompass since they contain light-sensitive magneto-sensors Like some migratory birds the presence of aninclination compass would serve as an orientation mech-anism when directional daylight cues are impeded bycloudy or inclement weather or during nighttime flight Itmay also augment time-compensated sun compass orien-tation for appropriate directionality throughout migrationThe inclination compass was found to function at earth-strength magnetic fields an important metric

Levitt et al EMF and wildlife 29

The question remains Can the magnetic compass inmonarchs be disrupted by anthropogenic EMF like it doeswithgeomagnetic orientation inmigratorybirds [213] There issome indication this is possible Perez et al [330] foundmonarchs completely disorient after exposure to a strongmagnetic field (04-T MF for 10 s or approximately 15000times the Earthrsquos magnetic field) immediately before releasevs controls This is a high exposure but within range of man-made exposures today very close to powerlines

Bees wasps and others

Pollinators bees in particular are keystone specieswithout which adverse effects would occur throughoutfood webs and the Earthrsquos entire biome were pollinators todisappear Because of their central role and accessibilityfor research bee studies have created a wealth of infor-mation including regarding anthropogenic EMFs

Bees mdash especially honey and bumble bees mdash areanother iconic insect species beloved for their role inpollination honey propolis royal jelly and beeswax pro-duction their critical importance to our food supply andtheir crucial role in global ecological health and stabilityFound on every continent except Anarctica wherever thereare flowering plants requiring insect pollination there areover 16000 known species of bees in seven different bio-logical families consisting of four main branches Somespecies live socially in colonies while others are solitaryThe western honey bee (Apis mellifera) is the best knownand most studied due in part to its central role in agricul-ture Bees feed on nectar for energy and pollen for proteinnutrients and have co-evolved with many plant species inastoundingly complex ways They are also highly sensitiveto both natural and anthropogenic EMFs Beeswax itselfhas electrical properties [50]

Human apiculture has been practiced since the time ofancient Egyptian and Greek cultures and bees have beenclosely studied since the 1800s Almost all bee speciesincluding commercially raised and wild species are underdecades-long multiple assaults These include from pesti-cides herbicides climate change various bacterialviraldiseases infestations from parasitic mite species mdashparticularly Apis cerana Varroa destructor and Varroajacobsoni beginning in the mid-1980s mdash and predationfrom introduced species that attack bees directly (eg theinvasive giant bee-eating hornet Vespa mandarinia) aswell as alter plant ecology over time to adversely affect beefood supply Somehave suggested that vanishing beesmayalso have to do with premature aging due to environmen-tally caused shortened telomeres [344]

Whole colony collapse disorder (CCD) is the mostdramatic manifestation of domesticated bee demise inwhich worker bees abruptly disappear from a hive withouta trace resulting in an empty hive with perhaps aremaining queen and a few worker bees despite ampleresources left behind Few if any dead bees are ever foundnear the hive CCDwas first described in the US in 2006 inFlorida in commercial western honey bee colonies VanEnglesdorp et al [345] quantified bee losses across allbeekeeping operations and estimated that between 075and 100 million honey bee colonies died in the UnitedStates over the winter of 2007ndash2008 Up until that surveyestimates of honey bee population decline had notincluded losses occurring during the wintering periodthus underestimating actual colony mortality

The same phenomenon had been described by bee-keepers in France in 1994 [346] mdash later attributed to thetiming of sunflower blooming and the use of imidacloprid(IMD) a chlorinated nicotine-based insecticide or ldquoneon-icotinoidrdquo being applied to sunflowers for the first time there[347] Similar to DDT but considered safer for mammalsincludinghumans neonicotinoidsare a slow-release class ofneurotoxins that block insect nervous systems via acetyl-choline receptors interferingwith neuronal signaling acrosssynapses Sublethal doses can interfere with bee navigation

Since then similar phenomena have been seenthroughout Europe [348] and some Asian countries Causalhypotheses included all of the above factors with varyingfoci on pesticide classes like neonicotinoids and geneti-cally modified crops but no single agent adequately ex-plains CCD Bromenshenk et al [349] however identifiedpathogen pairingco-infection with two previously unre-ported RNA virusesmdash V destructor-1 and Kakugo virusesand a new irridescent virus (IIV) (Iridoviridae) along withNosema ceranaemdash in North American honey bees that wereassociated with all sampled CCD colonies The pathogenpairing was not seen in non-CCD colonies Later cage trialswith IIV type-6 and N ceranae confirmed that co-infectionwith those two pathogens was more lethal to bees thaneither pathogen alone Still many questions remain

There are two national surveying groups in the USmdashthe US Department of Agriculture (USDA) which begansurveying managed bee populations in 2015 but fundingwas cut in late 2019 and the Bee Informed Partnership(BIP) a non-profit that coordinates with research facilitiesand universities Prior to USDArsquos funding cuts managedcolonies decreased from CCD by 40 [350] with an addi-tional 26 over the same quarter in 2019 [351] BIPrsquos surveyperiod for April 1 2018 through April 1 2019 found USbeekeepers lost an estimated 407 of their managedhoney bee colonies The previous year had similar annual

30 Levitt et al EMF and wildlife

losses of 401 The average annual rate of loss reported bybeekeepers since 2010ndash11 was 378 [352]

Also in theUS for the first time in 2016 seven species ofHawaiian yellow-faced bees (Hylaeus anthracinusHylaeus longiceps Hylaeus assimulans Hylaeus facilisHylaeus hilaris Hylaeus kuakea and Hylaeus mana) wereadded to the federal endangered species list as well as therusty patched bumble bee (Bombus affinis) which prior to thelate 1990s had been widely dispersed across 31 US states[353] Mathiasson and Rehan [354] examined 119 species inmuseum specimens in New Hampshire going back 125 yearsand concluded that 14 species found across New Englandwere on the decline by as much as 90 including the lesserstudied leafcutter and mining bees that nest in the groundunlike honeybees that nest in commercial hives or in treesshrubs and rock crevices in the wild

Worldwide many bee and other pollinator pop-ulations have also declined over the last two decadesManaged honey bee (Apis mellifera) colonies decreased by25over 20 years in Europe and 59over 58 years in NorthAmerica with many wild bumble bee populations inEurope and North America having gone locally extinct[355ndash358] But while dramatic range contractions havebeen seen not all bees in all places are declining somepopulations are growing depending on opportunistic andspecies-adaptability factors Formany species data are stillinsufficient of poor quality or nonexistent [359] In addi-tion bee declines can affect flora survival Miller-Struttmann et al [360] recorded flower declines of 60with 40 years of climate warming in alpine meadows mdashareas largely protected from land-use changes Insects arehighly sensitive to temperature changes

A comprehensive UK survey of pollinator species [361]found that of 353 wild bee and hoverfly species acrossBritain from 1980 to 2013 25 had disappeared from theplaces they had inhabited in 1980 Further estimates foundanet loss of over 27million in 06mi (1 km) grid cells acrossall species Declining pollinator evenness suggested losseswere concentrated in rare species Losses linked to specifichabitats were also identified with a 55 decline amongwild upland species while dominant crop pollinatorsincreased by 12 possibly due to agricultural businessinterventions The general declines found a fundamentaldeterioration in both wider biodiversity and non-croppollination services

There is no question that the huge diversity of polli-nator species across the planet is suffering and that lossescould be catastrophicwith an estimated 90ofwild plantsand 30 of world crops in jeopardy [362]

There is a likelihood that rising EMF background levelsplay a role Bees have been known for decades to have an

astute sense of the Earthrsquos DC magnetic fields [363 364]and rely on that perception for survival For centuriesbeekeepers had noticed curious movements in bee hivesbut Austrian ethologist Karl von Frisch finally interpretedthat activity in the 1940s winning the Nobel Prize in 1973for what came to be known as the honey bee ldquowaggledancerdquo Through complex circles and waggle patternsbees communicate the location of food sources to othermembers of the hive using the orientation of the sun andthe Earthrsquos magnetic fields as a gravity vector ldquodancingrdquoout a map for hive members to follow like naturersquos ownimbeddedGPS Bees also detect the sunrsquos direction throughpolarized light and on overcast days use the Earthrsquos mag-netic fields likely through the presence of magnetite intheir abdominal area and employ complex associativelearning and memory [365]

Building on the earlier work of Gould et al [119]Kobayashi and Kirschvink [52] noted that biogenicmagnetite in honey bees is located primarily in the anteriordorsal abdomen When small magnetized bits of wire wereglued over those areas it interfered with beesrsquo ability tolearn to discriminate magnetic anomalies in conditioningexperiments while nonmagnetized wire used in controlsdid not interfere [366] Kirschvink and Kobayashi [367]found that when pulse-remagnetization techniques wereused on bees trained to exit from a T-maze that north-exiting bees could be converted to a south-exiting directionsimilar to what was observed in magnetobacteria andartificial reorientation by Blakemore [113] Honeybeescould also be trained to respond to very small changes inthe geomagnetic field intensity [368] Valkova and Vacha[369] discussed the possibility that honey bees use acombination of both radical paircryptochromes andmagnetite to detect the geomagnetic field and use it fordirection like many birds

Given these sensitivities bees may be reacting nega-tively through muti-sensory mechanisms to numeroussources of anthropogenic multi-frequency interferenceBumble bees (Bombus terrestris) a solitary species andhoney bees (Apis mellifera) a social hive species areknown to detect weak electric fields in different behavioralcontexts using different sensorymechanisms Bumble beee-field detection is likely through mechanosensory hairs[370ndash372] while honey bees reportedly use their antennae[373] that are electro-mechanically coupled to the sur-rounding e-field taking place in the antennal Johnstonrsquosorgan Greggers et al [373] found that honey bee antennaeoscillate under electric field stimulation that can thenstimulate activity in the antennal nerve The latter occursdue to bees being electrically charged and thus subject toelectrostatic forces Erickson [374] found different surface

Levitt et al EMF and wildlife 31

potentials in bees when leaving or entering hives andColin et al [375] found seasonal variability between posi-tive and negative charges in resting bees It has also beenshown that honey bees with removed or fixed antennae areless able to associate food reward with electric field stimuliand that bees emanate modulated electric fields whenmoving their wings (at about 230 Hz) and body (at about165 Hz) during the waggle dance [373]

Electro-ecological interplay between flowers andpollinators has also been known since the 1960s and iscritical to pollen transfer from flowers to bees [376ndash378]It is known that as bees fly through the air they accu-mulate a positive charge Flowers on the other handwhich are electrically grounded through their root sys-tems tend to have a negative charge in their petalscreated by surrounding air that carries around 100 V forevery meter above ground The accumulating positivecharge around the flower induces a negative charge in itspetals which then interacts with the positive charge inbees In fact bees do not even need to land on flowers forpollen transfer to occur pollen can ldquojumprdquo from theflower to the bee as the bee approaches due to chargedifferentials between the two Thus it appears that beesand flowers have been ldquocommunicatingrdquo via electricfields all along [379] Bees can also learn color discrimi-nation tasks faster when color cues are paired with arti-ficial electric field cues similar to those surroundingnatural flowers but did not learn as readily in an elec-trically neutral environment [370]

This evidence points to floral e-fields being used in aco-evolutionary symbiotic relationship with bees Clarkeet al [370 371] even found that bumblebees can distin-guish between flowers that give off different electric fieldsas floral cues to attract pollinators Like visual cues floralelectric fields exhibit complex variations in pattern andstructure that bumblebees can distinguish contributing tothe myriad complex cues that create a pollinatorrsquos memoryof floral food sources And because floral electric fieldscanmdash and domdash change within seconds of being visited bypollinators this sensory ability likely facilitates rapid anddynamic ldquoinformation exchangerdquo between flowers andtheir pollinators Bumblebees can even amazingly useelectric field information to discriminate between nectar-rewarding and unrewarding flowers [370]

Bees locusts ELF-EMF

Bees are also known to be sensitive to anthropogenicELF-EMF In 1973Wellenstein [380] found that high ten-sion powerlines adversely affected honey bees in woodenhives This in part prompted the Bonneville Power

Administration an American federal agency operating inthe Pacific Northwest under the US Department of Energy(US DOE) to investigate in 1974 [381ndash384] the effects oftransmission lines on people plants and animalsincluding honey bees The industry group Electric PowerResearch Institute also followed up on bee research [385386] Both of those studies confirmed that transmission lineelectric fields can affect honey bees inside wooden hives aswood is a poor insulator and current can be induced whenhives are placed in electric fields whether metal is presentor not The strength of the current inside the hive wasinfluenced by the electric field strength hive height andmoisture conditions with effects noticeable when inducedcurrent exceeded 002ndash004 mA Depending on hiveheight this occurred in field strengths between 2 and 4 kVm Effects included increased motor activity with transientincrease in hive temperature excessive propolis produc-tion (a resinous material used by bees as a hive sealer)decreased colony weight gains increased irritability andmortality abnormal production of queen cells queen lossdecreased seal brood andpoor over-winter colony survival[387] Impacts were most likely caused by electric shocksinside the hives [386 388] Effects were mitigated withgrounded metal screenshielding of hives [385] howeverbees appeared unaffected by magnetic fields whichpermeate metal shielding The authors concluded that theshielding results indicated that bees were unaffected byflying through an external electric field up to 11 kVm butnoted that the study design could not reveal if subtle effectswere occurring

A more recent study of electric fields by Migdał [389]focused on honey bee behavioral effects on walkinggrooming flight stillness contact between individualsand wing movement They found that the selected fre-quency intensity and duration of exposure effects beesrsquobehavioral patterns Bees were exposed for 1 3 and 6 h toE-fields at 50 kVm 115 kVm 230 kVm or 345 kVm(with controls under E-field lt20 kVm) Within theexposed groups results showed that exposure for 3 hcaused decreased time that bees spent on select behaviorsas well as the frequency of behaviors whereas after both 1and 6 h the behavioral parameters increased within thegroups The researchers concluded that a barrier allowingbehavioral patterns to normalize for some periods wasindicated although none of the exposed groups returned toreference values in controls which adhered to normalbehavioral patterns Bees may have compensatory win-dows that appear to be both time and intensity dependentfor E-fields The significance of this study is that bees mustaccomplish certain activities mdash like flight frequency andthe honey bee lsquowaggle dancersquo noted above mdash that are

32 Levitt et al EMF and wildlife

critical for life expectancy and survival Even slightsequential disturbances may have cascading effects

In an early-1988 study Korall et al [390] also foundeffects to bees from magnetic fields (MF) Bursts compa-rable to some of todayrsquos pulsed exposures of artificial MF at250 Hz mdash the frequency of buzzing during the waggledance mdash were applied parallel to natural EMF field linesand induced unequivocal lsquojumpsrsquo of misdirection by up to+10deg in bees during the waggle dance This alone couldcause directional confusion in hives Continuous fields of250 Hz with bursts perpendicular to the static MF howevercaused no effects They concluded that a resonance rela-tionship other than classic resonance models was indi-cated (see ldquoMechanismsrdquo above) This early work hasimplications for subsequent digital pulsing and all wirelessbroadband technology

More recent work on honey bees and ELF-EMF byShepherd et al [209] in 2018 found that acute exposure to50 Hz fields at levels from 20ndash100 μT (at ground level un-derneath powerline conductors) to 1000ndash7000 μT(within 1 m of the conductors) reduced olfactory learningforaging flight success toward food sources and feeding aswell as altered flight dynamics Their results indicated that50 Hz ELF-EMFs from powerlines is an important envi-ronmental honey bee stressor with potential impacts oncognitive and motor abilities

Some wasp species have also been found sensitive toELF-EMF Pereira-Bomfim et al [391] investigated themagnetic sensitivity of the social paper wasp (Polybiapaulista) by analyzing wasp behavior in normal geomag-netic fields and in the presence of external magnetic fieldsaltered by either permanent magnets (DC fields) or byHelmholtz coils (AC fields) They evaluated the change inforaging rhythm and colony behavior as well as the fre-quency of departinghomeward flights and the behavioralresponses of worker wasps located on the outer nest sur-face They found that the alteredmagneticfield from theDCpermanent magnet produced an increase in the frequencyof departing foraging flights and also that wasps groupedtogether on the nest surface in front of the magnet withtheir heads and antennae pointing toward the perturbationsource possibly indicating a response to a potential threatas a defense strategy Controls showed no such groupingbehavior The AC fields created by the Helmholtz coils alsoincreased foraging flights but individuals did not showgrouping behavior The AC fields however induced waspworkers to perform ldquolearning flightsrdquo They concluded thatfor the first time P paulista demonstrated sensitivity to anartificial modification of the local geomagnetic field andthat mechanisms may be due to both cryptochroneradicalpairs and magnetite

Another flying insect model mdash desert locust (Schisto-cerca gregaria)mdashwas found susceptible to entrainment byELF-EMF In a complex study Shepherd et al [392]analyzed acute exposure to sinusoidal AC 50 Hz EMF (fieldstrength range 10 to 10000 μT) vs controls on flights ofindividual locusts tethered between copper wire coilsgenerating EMFs at various frequencies and recorded onhigh-speed video Results found that acute exposure to50 Hz EMFs significantly increased absolute change inwingbeats in a field-strength-dependent manner Applyinga range of ELF-EMF close to normal wingbeat occurancethey found that locusts entrained to the exact frequency ofthe applied EMF They concluded that ELF exposure canlead to small but significant changes in locust wingbeatslikely due to direct acute effects on insect physiology (vscryptochrome ormagnetite-basedmagnetoreception) andor behavioral avoidance responses to molecularphysio-logical stressWyszkowska et al [393] also found effects onlocustsmdash exposure to ELF-EMF above 4mT led to dramaticeffects on behaviour physiology and increased Hsp70protein expression Such higher exposures may be foundnear high tension lines

Bees RF-EMF

The effects of RF-EMF on bees is of increasing interest sincethat is the fastest rising EMF environmental exposure of thepast 30 years [369] Beginning in the early 2000s studies ofcell phones placed in the bottom of hives began to appearHoney bees showed disturbed behavior when returning tohives after foraging and under various RFR exposures[394ndash396] Early methodologies however were not welldesigned or controlled For instance Favre [397] foundincreased piping mdash a distress signal that honey bees giveoff to alert hive mates of threats andor to announce theswarming process Both active and inactive mobile phonehandsetswere placed in close proximity to honey beeswithsounds recorded and analyzed Audiograms and spectro-grams showed that active phone handsets had a dramaticeffect on bee behavior in inducedworker piping This studywas criticized by Darney et al [398] for using music in theactive RFR exposurewhichmay have introduced a variablecapable of affecting bee piping in response to the addedsound alone

In a complex study Darney et al [398] tested highfrequency (HF) and ultra high frequency (UHF) used inRFID technology in order to develop a method to auto-matically record honey bees going in and out of hives Theyglued RFID tags onto individual bee dorsal surfaces thatwere detected at the hive entrance by readers emitting HFradio waves They then looked for possible HF adverse

Levitt et al EMF and wildlife 33

effects on honey beesrsquo survival Eight-day-old honey beeswere exposed to HF 1356 MHz or UHF 868 MHz RFR for 2 hsplit into ON and OFF periods of different durations Deadbees were counted daily with cumulative mortality rates ofexposed and non-exposed honey bees compared sevendays after exposure Two out of five experimental condi-tions found increased mortality once after HF and onceafter UHF exposure with OFF duration of 5 min or moreafter which they recommended limiting honey bee expo-sure to RFR to less than 2 h per day They also curiouslyconcluded that the RFID parameters they used for moni-toring hive activity presented no adverse effects but themultifrequency peak exposures and RFID attachmentsneed further study in light of other works on RFID effects(see Part 1 for discussion of RFID)

In another study using an active cell phone attached tohive frames Odemer and Odemer [399] investigated RFReffects on honey bee queen development and mating suc-cess Control hives had an inactive cell phone attachedAfter exposing honey bee queen larvae to GSM 900 MHzRFR during all stages of pre-adult development (includingpupation) hatching of adult queens was assessed 14 daysafter exposure and mating success after an additional11 days They found that chronic RFR exposure signifi-cantly reduced honey bee queen hatching that mortalitiesoccurred during pupation but not at the larval stages thatmating success was not adversely affected by the irradia-tion and that after exposure surviving queenswere able toestablish intact colonies They therefore determined thatmobile phone radiation had significantly reduced thehatching ratio but not mating success if queens survivedand if treated queens successfully mated colony devel-opment was not adversely affected Even though theyfound strong evidence of mobile phone RFR damage topupal development they cautioned its interpretationnoting that the studyrsquos worst-case exposure scenario wasthe equivalent of a cell phone held to a userrsquos head not at alevel found in typical urban or rural hive settings Theyconcluded that while no acute negative effects on beehealth were seen in the mid-term they also could not ruleout effects on bee health at lower chronic doses such asfound in ambient environments and urgently called forlong term research on sublethal exposures present inmajorcity environments

Sharma andKumar [400] found similar abnormalitiesin honey bee behavior when they compared the perfor-mance of honey bees in RFR exposed and unexposedcolonies Two of four test colonies were designated andeach equipped with two functional cell phones mdash a highexposuremdash placed on two different hive side walls in callmode at GSM 900 MHz The average RFR power density

was measured at 8549 μWcm2 (568 Vm electric field)One control colony had a dummy phone the other had nophone Exposure was delivered in 15 min intervals twiceper day during the period of peak bee activity Theexperiment was performed twice a week during Februaryto April It covered two brood cycles with all aspects ofhive behavior observed including brood area comprisingeggs larvae and sealed brood queen proficiency in egg-laying rate foraging flight behavior returning abilitycolony strength including pollen storage and other var-iables Results included a significant decline in colonystrength and egg laying and reduced foraging to the pointwhere there was no pollen honey brood or bees by theend of the experiment One notable difference in thisstudy was that the number of bees leaving the hivedecreased following exposure There was no immediateexodus of bees as a result of exposure mdash instead beesbecame quiet still andor confused ldquohellipas if unable todecide what to dohelliprdquo the researchers said Such aresponse had not been reported before The authorsconcluded that colony collapse disorder is related to cellphone radiation exposures

Vilić et al [401] investigated RFR and oxidative stressand genotoxicity in honey bees specifically on the activityof catalase superoxide dismutase glutathione S-trans-ferase lipid peroxidation levels and DNA damage Larvaewere exposed to 900 MHz RFR at field levels of 10 23 41and 120 Vmminus1 for 2 h At a field level of 23 Vmminus1 the effect of80AM 1 kHz sinusoidal and 217 Hz modulation were alsoinvestigated They found that catalase activity and the lipidperoxidation levels significantly decreased in larvaeexposed to the unmodulated field at 10 V mminus1 (27 μWcm2)compared to the control Superoxide dismutase andglutathione S-transferase activity in honey bee larvaeexposed to unmodulated fields were not statisticallydifferent compared to the control DNA damage increasedsignificantly in larvae exposed to modulated (80 AM at1 kHz) field at 23 V mminus1 (140 μWcm2) compared to controland all other exposure groups Their results suggested thatRFR effects in honey bee larvae manifested only aftercertain EMF exposure conditions Interestingly they foundthat increased field levels did not cause a linear dose-response in any of the measured parameters whilemodulated RFR produced more negative effects than thecorresponding unmodulated field They concluded thatwhile honey bees in natural environments would not beexposed to the high exposures in their experiments theresults indicated additional intensive research is needed inall stages of honey bee development since the cellular ef-fects seen could affect critical aspects of bee health andsurvival

34 Levitt et al EMF and wildlife

Kumar et al [402] also found biochemical changes inworker honey bees exposed to RFR A wooden box wasdesigned with glass on the front and back and wire gauzefor ventilation on two sides for both exposed bees andcontrols Cell phones (same make model and networkconnection) were kept in listen-talk mode for 40 min Atintervals of 10 20 and 40 min 10 exposed and 10 controlbees were collected at the same times Hemolymph wasthen extracted from the inter-segmental region of bee ab-domens and analyzed Results included increased con-centration of total carbohydrates in exposed bees in the10 min exposure period compared to unexposed beesIncreasing the exposure time to 20min resulted in a furtherincrease in the concentration but exposure at 40min had areverse effect with declines in carbohydrate concentrationalthough it was still higher than controls Hemolymphglycogen and glucose content also showed the sameexposure pattern mdash increase in content up to 20 min afterwhich a slight decline that was still higher than controlsChanges in total lipidscholesterol mdash the major energy re-serves in insects mdash can affect numerous biological pro-cesses Some lipids are crucial membrane structurecomponents while others act as rawmaterials in hormonesand pheromones Changes in these parameters are signif-icant to every biological activity including reproductionAlso of interest in this study was that as exposure timeincreased the bees appeared to have identified the sourceof disturbance There was a large scale movement ofworkers toward the talk-mode (with higher RFR exposureduring transmission function) but not the listening modeBees also showed slight aggression and agitation withwing beating The researchers hypothesized that thisincreased activity could be responsible for increased en-ergy use thereby accounting for the decrease in concen-tration of carbohydrates and lipids in the 40 min exposedsample The researchers concluded that cell phone radia-tion influences honey bee behavior and physiologySharma [403] had also reported increased glycogen andglucose levels in exposed honey bee pupa

It must be pointed out that the cell phone emissionconditions used in some experiments are questionable inparticular where there was no detail regarding how thephones were activated to achieve emission

Not all studies demonstrated adverse effects Mall andKumar [404] found no apparent RFR effects on brood rearinghoney production or foraging behavior in honey bees in hiveswith cell phones inside or near a cell tower and Mixon et al[405] also found no effects of GSM-signal RFR on increasedhoney bee aggression They concluded that RFR did notimpact foraging behavior or honey bee navigation andtherefore was unlikely to impact colony health

Although there are several anectodal reports of insectlosses near communication towers there are only ahandful of ambient RFR field studies conducted on in-vertebrates thus far In the first large survey of wild polli-nating species at varying distances from cell towers Laacutezaroet al [406] found both positive and negative effects fromRFR in a broad range of insects on two islands (Lesvos andLimnos) in the northeastern Aegean Sea near GreeceMeasured ambient RFR levels included all frequencyranges used in cell communications broadcast RFR isabsent on the islands RFR values did not significantlydiffer between islands (Lesvos 027 plusmn 005 Vm Limnos021 plusmn 004 Vm v3 2 = 008 p=0779) and did not decreasewith the distance to the antenna possibly they hypothe-sized because some sampling points near the antennamayhave beenoutside or at the edge of the emission lobes Theymeasured RFR at four distances of 50 100 200 and 400 m(164 328 656 and 1312 ft respectively) from 10 antennas(5 on Lesvos Island and 5 on Limnos Island) and correlatedRFR values with insect abundance (numbers of insects)and richness (general health and vitality)mdash the latter onlyfor wild bees and hoverflies The researchers conductedcareful flowering planttree- and- insect inventories inseveral low-lying grassland areas including for wild beeshoverflies bee flies other remaining flies beetles butter-flies and of various types Honey beeswere not included inthis study as they are a managed species subject tobeekeeper decisions and therefore not a wild species OnLesvos 11547 insects were collected and on Limnos 5544Varied colored pan traps for both nocturnal and diurnalsamples were used Results found all pollinator groupsexcept butterflieswere affected by RFR (both positively andnegatively) and for most pollinator groups effects wereconsistent on both islands Abundance for beetles waspsand hoverflies significantly decreased with RFR but overallabundance of wild bees and bee flies significantlyincreased with exposure Further analysis showed thatonly abundance of underground-nesting wild bees waspositively related to RFR while wild bees nesting aboveground were not affected RFR effects between islandsdiffered only on abundance of remaining flies On speciesrichness RFR tended to only have a negative effect onhoverflies in Limnos Regarding the absence of effects seenin butterflies they hypothesized that the pan trap collec-tion method is not efficient for collecting butterflies (but-terflies accounted for only 13 of total specimens) andthat a different samplingmethodmight produce a differentresult They concluded that with RFRrsquos negative effects oninsect abundance in several groups leading to an alteredcomposition of wild pollinators in natural habitats it waspossible this could affect wild plant diversity and crop

Levitt et al EMF and wildlife 35

production They further said the negative relationshipbetween RFR on the abundance of wasps beetles andhoverflies could indicate higher sensitivity of these insectsto EMFs Potentially more EMF-tolerant pollinators suchas underground-nestingwild bees andbeefliesmayfill thevacant niches left by less tolerant species thus resulting intheir population increases Another possible explanation isthat EMFs may have particularly detrimental effects onmore sensitive larval stages and if so larvae developingabove ground (many beetles wasps hoverflies) may bemore vulnerable than those developing underground sincethe former could be exposed to higher radiation levels

In another field study Taye et al [407] placed fivehives from December to May at varying distances of 1000500 300 200 and 100 m (3280 1640 984 656 and 328 ftrespectively) from a cell tower in India to measure flightactivity returning ability and pollen foraging efficiency inhoney bees (Apis cerana F) They foundmost effects closestto towers with the least returning bees at 100 m distancefrom the tower Maximum foraging and return ability to thecolonies was seen at 500 m followed by 1000 m and indescending order at 300 and 200 m with the fewestreturning bees at 100 m from the tower The study alsofound that if bees returned the pollen load per minute wasnot significantly affected

Vijver et al [408] however challenged the accuracy ofdistance from towers that is often used as a proxy for EMFgradients such as the study above In a field study in TheNetherlands the researchers tested exposure to RFR from acell base station (GSM 900 MHz) on the reproductive ca-pacity of small virgin invertebrates during the most sensi-tive developmental periods spanning preadolescent tomating stages when reproductive effects would most likelybe seen Careful RFR field measurements were taken todetermine null points in order to see if distance fromemitters is a reliable RFR exposure model in field studiesThey exposed four different invertebrate hexapod speciesSpringtails (Folsomia candida) predatory lsquobugsrsquo (Oriuslaevigatus) parasitic wasps (Asobara japonica) and fruit-flies (D melanogaster) were placed in covered pedestalcontainers within the radius of approximately 150 m of a900 MHz mobile phone base station for a 48-h period Sixcontrol groups were placed within 66 ft (2 m) of thetreatment groups and covered in Farady cages Afterexposure all groups were brought to the laboratory tofacilitate reproduction with resulting fecundity and num-ber of offspring then analyzed Results showed that dis-tance was not an adequate proxy to explain dose-responseregressions After complex data synthesis no significantimpact from the exposure conditions measures of centraltendency or temporal variability of EMF on reproductive

endpoints were found although there was some variabilitybetween insect groups As seen in other studies distance isoften used to create a gradient in energy exposures instudies but this study found the intensity of the transmitterand the direction of transmission to be more relevant asdid Bolte andEikelboom [409 410] The direction and tilt ofthe transmitter determines whether the location of interestin field studies is in the main beam In some instances thecloser promixity to the transmitter provided lower readingsthan further away which they found between two loca-tions They also noted that the organisms selected in thestudy were small in size springtails have a body length onaverage of 2 mm wasps are about 3 mm insect sizes from14 to 24 mm with the largest organisms tested being fe-male fruit flies at about 25 mm length and males slightlysmaller Due to size limited absorption and little energyuptake capacity none of these insects are efficient whole-body receptors for 900 MHz waves with a wavelength ofapproximately 13 in (33 cm) But they further noted that thiswas a linear regression study and that biological effects areoften non-linear However finding no distinct effects didnot exclude physiological changes They concluded thatbecause of RFR exposurersquos increasing ubiquity urgentattention to potential effects on biodiversity is needed

The issue of insect size nonlinearity and antenna tiltdirection are factors of critical importance with 5G radia-tion which will create extremely complex near- and- far-field ambient exposures to species in urban and rural en-vironments alike not only fromadensification of small cellantennas close to the ground but also from increased sat-ellite networks circling in low Earth orbits (see Part 1) Therange of frequencies used for wireless telecommunicationsystems will increase from below 6 GHz (2G 3G 4G andWiFi) to frequencies up to 120 GHz for 5G which due tosmaller wavelengths is therefore a better resonant matchfor small insects An alarming study by Thielens et al [411]drawing on numerous robust studies of RFRrsquos decades-long use as a thermal insecticide modeled absorbed RFRin four different types of insects as a function of fre-quency alone from 2 to 120 GHz A set of insect modelswas obtained using novel Micro-CT (computer tomogra-phy) imaging and used for the first time in finite-difference time-domain electromagnetic simulationsAll insects showed frequency-dependent absorbed po-wer and a general increase in absorbed RFR at and above6 GHz in comparison to the absorbed RFR power below6 GHz Their simulations showed that a shift of 10of theincident power density to frequencies above 6 GHzwould lead to an increase in absorbed power between3ndash370 mdash a large differential of serious potentialconsequence to numerous insect species

36 Levitt et al EMF and wildlife

Using a similar approach Thielens et al [412] focusedon the western honey bee (Apis mellifera) with RF-EMFusing a combination of in-situ exposure measurementsnear bee hives in Belgium and numerical simulationsAround five honey bee models were exposed to planewaves at frequencies from 06 to 120 GHz mdash frequenciescarved out for 5G Simulations quantified whole-bodyaveraged RFR absorbed as a function of frequency andfound that the average increased by factors of 16ndash121(depending on the specimen) when frequency increasedfrom 06 to 6 GHz for a fixed incident electric field strengthA relatively small decrease in absorption was observed forall studied honey bees between 12 and 120 GHz due tointerior attenuation RFR measurements were taken at 10bee hive sites near five different locations Results foundaverage total incident RFR field strength of 006 Vm thosevalues were then used to assess absorption and a realisticrate was estimated between 01 and 07 nW Theyconcluded that with an assumed 10 incident powerdensity shift to frequencies higher than 3 GHz this wouldlead to an RFR absorption increase in honey bees between390 and 570 mdash a frequency shift expected with thebuildout of 5G

The two previous studies alone should give pauseregarding environmental effects to invertebrates in thesehigher 5G frequency ranges

Kumar [413] noted that RFR should be included ascausal agents of bee CCD and that test protocols need to bestandardized and established Standardization is criticalsincemany studies conductedwith cell phones in hives areof very uneven quality and only indicative of potential ef-fects Placing cell phones in hives and assuming that RFR isthe only exposure is inaccurate and misleading ELF-EMFsare always present in all telecommunications technologyusing pulsed and modulated signals [414] All of thesecharacteristics have been found to be highly biologicallyactive apart from frequency alone Such studies are likelycapturing ELF effects without identifying them All aspectsof transmission including transmission engineering itselffrom towers need to be considered to determine accurateexposures and delineate causative agents Vibration andheatmust also be consideredmdash cell phones in transmissionmode could raise hive temperature quickly and bees arehighly temperature sensitive Due to ldquowaggle dancerdquo spe-cifics in creating foraging ldquoroadmapsrdquo bees should not beartificially relocated from hives to determine return abilityafter EMF exposure They may be confused by relocationalone adversely affecting their return abilities Such testsalso involve only one stressor when there are multiplestressors on insect species today Understanding such co-factors is critical in determining accurate data and

outcomes [415 416] Translating laboratory studies to fieldrelevance has always been problematic but understandingEMF effects to insects has become urgent with everincreasing low-level ambient exposure from devices andinfrastructure especially in light of the new 5G networksbeing built There are numerous variables that studies haveyet to factor in All of the above indicates a critical need tostandardize experimental protocols and to take electro-ecology far more seriously especially regarding aerialspecies in light of 5G

Aquatic environments

There are fundamental electrical differences in conduc-tivity (how well a material allows electric current to flow)and resistivity (how strongly amaterial opposes the flow ofelectric current) between air and water Through waterEMF propagation is very different than through air becausewater has higher permittivity (ability to form dipoles) andelectrical conductivity Plane wave attenuation (dissipa-tion) is higher in water than air and increases rapidly withfrequency This is one reason that RFR has not traditionallybeen used in underwater communication while ELF hasbeen Conductivity of seawater is typically around 4 Smwhile fresh water varies but typically is in the mSm rangethus making attenuation significantly lower in fresh waterthan in seawater Fresh water however has similarpermittivity as sea water There is little direct effect on themagnetic field component in water mediums propagationloss is mostly caused by conduction on the electric fieldcomponent Energy propagation continually cycles be-tween electric and magnetic fields and higher conductionleads to strong attenuationdissipation of EMF [98]

Because of these essential medium differences electro-receptormechanisms in aquatic speciesmay be very differentthan those previously described in aerial species since air is aless conductive and resistive medium with less attenuationThat is why RFR travels more easily and directly through airIn aquatic species electroreception may be a result of trans-mission via water directly to the nervous system throughunique receptor channels called Ampullae of Lorenzini [371]In frogs amphibians fish some worm species and othersreceptor channels may be through the skin as well as viamechanisms more common in aerial species such as in thepresence of magnetite (see ldquoMechanismsrdquo above) There canbe great variation in electroreceptive sensitivities in speciesinhabiting the two fundamentally different environmentsSome amphibian species however have physical charac-teristics that span both mediums and therefore varied mag-netoreception mechanisms

Levitt et al EMF and wildlife 37

Amphibians frogs salamandersreptiles regeneration abilities

Amphibians are the class of animals that include frogs

toads salamanders newts some reptiles and caecilians

The common term lsquofrogrsquo is used to describe thousands of

tailless amphibian species in theOrderAnura There are over

6300 anuran species recorded thus far with many more

likely disappearing today due to climate change and other

factors before we even knew they existed Informal distinc-

tions are made between frogs (thin-skinned species) and

toads (thick warty skins) but such distinctions are not used

for taxonomic reasons While the greatest concentration of

diverse frog species is in tropical rainforests they are widely

foundall over theworld from the tropics to subarctic regions

Most adult frogs live in fresh water andor on dry land while

some species have adapted to living in trees or underground

Their skin varies in all manner of colors and patterns from

graygreen and brownblack to bright redsyellowsFrog skin is smooth and glandular mdash something of

concern given nascent 5G technology (see Part 1)mdash and cansecrete toxins to ward off predators Frog skin is also semi-permeable which makes them highly susceptible to dehy-dration and pollutants With radical weather shifts due toclimate change and unpredictable swings betweenabnormal droughts followed by flooding in previouslyweather-stable regions environmentally sensitive am-phibians like frogs are considered bell-weather speciesFrequently time may be insufficient for some localregional species to regenerate in between radical weathercycles leading to population collapse

Since the 1950s there has been a significant decline infrog populations with more than one third of species todayconsidered threatened with extinction while over 120 spe-cies are already believed to have gone extinct since the1980s [10 417 418] This amphibian decline is consideredpart of an ongoing global mass extinction with populationcrashes as well as local extinctions creating grave impli-cations for planetary biodiversity [419] Amphibianextinction results are from climate change [420ndash422]habitat lossdestruction [423 424] introduced species[425] pollution [426] parasites [423 427] pesticides her-bicides and fungicides [428ndash430] disease [431ndash435] andincreased ultraviolet-B radiation [436ndash439] among othersAnthropogenic sound pollution may also affect amphibiancall rates and therefore impact reproduction [440] andartificial night lights affectmale green frog (Rana clamitausmelanota) breeding [441] Nonionizing electromagneticfields may also play a role [442]

McCallum [443] calculated that the current extinctionrate of amphibians could be 211 times greater than theirpre-anthropogenic natural ldquobackground extinctionrdquo ratewith the estimate rising 25000ndash45000 times if endan-gered species are also included in the computation Todaydeclining amphibian populations are seen in thousands ofspecies across numerous ecosystems including pristineforested areas [418] and declines are now recognizedamong the most severe impacts of the anthropocene era[417 442]

In addition the number of frogs with severe malfor-mations often incompatible with survival has risensharply Deformities are a complex issue related to physi-ology anatomy reproduction development water qual-ity changing environmental conditions and ecology ingeneral Any time deformities are observed in large seg-ments of wildlife populations there are indications ofserious environmental problems [442] Amphibian mal-formations are presumed due to an aggressive infectiousfungal disease called Chytridiomycosisy caused by thechytrid fungi Batrachochytrium dendrobatodis and Batra-chochytrium salamandrivorans [432ndash435] and by parasiteslike Ribeiroia ondatrae [427] Chytridiomycosis has beenlinked to dramatic amphibian declines and extinctions inNorth Central and South America across sections ofAustralia and Africa and on Caribbean islands likeDominica and Montserrat First identified in the 1970s inColorado US it continues to spread globally at analarming rate Some populations witness sporadic deathswhile others experience 100 mortality There is noeffective measure to control the disease in wild pop-ulations Herbicides like glyphosate used in Rounduptradeand atrazine an endocrine disruptor have also been foundto cause severe malformations in both aquatic and landamphibian species from farmland pesticideherbicidefungicide runoff [428ndash430]

Frogs are known to be highly sensitive to natural andmanmade EMF Much research into the electrophysiologyof frogs has been conducted because they are good labmodels for human nervous system research readilyavailable and easily handled As far back as 1780 theItalian physicist Luigi Galvani discovered what we nowunderstand to be the electrical basis of nerve impulseswhile studying static electricity (the only kind then known)when he accidentally made frog legmuscles contract whileconnected to the spinal cord by two different metal wires[444] Galvani thought he had discovered animalmagnetismrdquo but had actually discovered direct current andwhat later became known as a natural ldquocurrent of injuryrdquomdashthe process by which an injured limb for instance pro-duces a negative charge at the injury site that will later turn

38 Levitt et al EMF and wildlife

to a positive charge at the same site in some species asdiscovered in the 1960s by Robert O Becker [444ndash451] Theearliest curiosity about natural current continuedthroughout the 1800s on various aspects of EMF and laterthroughout the 1920s to 1940s in pioneering researchersElmer J Lund [452ndash454] and Harold Saxon Burr [455ndash457]who worked to establish the first unified electrodynamicfield theory of life using hydra frog and salamandermodels among several others because of their morpho-genic properties [458] While frogs do not regenerate limbsthe way salamanders do both are so similar in taxonomythat curiosity was high in the early pioneers cited abovethroughout the 1960s to 1990s about what fundamentallyallowed limb regeneration in one species by not the otherMuch was learned in the process about amphibian elec-trophysiology and cellular microcurrent in wound healingas well as the electrophysiological properties of cellulardifferentiation and eventually dedifferentiation pertinentto all contemporary stem cell research Today the impli-cations of this early work have gained new interest andtargeted research regarding endogenous microcurrent andlimb regeneration potential in humans as well as dedif-fentiationstem cellmorphogenesis in general for cancertreatment and other healing modalities For a thoroughreview of studies on morphogenesis see Levin [459]

Ubiquitous low-level ambient EMFs today match someof the natural low-level microcurrent found critical to thefundamental processes of amphibian growth reproduc-tion morphogenesis and regeneration lending newmeaning to the early research that defined amphibianelectrophysiology We just need to make far better use of itto understand what role if any todayrsquos ambient exposuresmay be contributing to amphibian losses (To comparetables between rising ambient EMF levels and low leveleffects in wildlife see Part 1 Supplement 1 and Part 2Supplement 3)

Amphibian and reptile magnetoreception

How amphibians perceive natural and manmade EMF issimilar to other species reviewed above and for amphibianmechanism reviews see Phillips et al [460 461] Likemanybird and insect species evidence indicates that amphib-ians perceive the Earthrsquos geomagnetic fields by at least twodifferent biophysical magnetoreception mechanismsnaturally occurring ferromagnetic crystals (magnetite)and light-induced reactions via specialized photo-receptorcells (cryptochromes) that form spin-correlated radicalpairs Like birds both mechanisms are present in someamphibians Cryptochromes provide a directional

lsquocompassrsquo and the non-light-dependent magnetite pro-vides the geographical lsquomaprsquo

In a thorough discussion of many magnetoreceptionstudies in anura and urodela species Diego-Rasilla et al[462] found evidence that Iberian green frog tadpoles(Pelophylax perezi) had a light-dependent magnetic com-pass and Diego-Rasilla et al [463] also found that tadpolesof the European common frog (Rana temporaria) arecapable of using the Earthrsquos magnetic field for orientingalong a learned y-axis In these studies they investigated ifthis orientation is accomplished using a light-dependentmagnetic compass similar to that found in the earlier ex-periments with other species of frogs and newts [460462ndash470] or from some other factor They concluded thatthe magnetic compass provided a reliable source of direc-tional information under a wide range of natural lightingconditions They also compared their findings to studies[470] that showed the pineal organ of newts to be the site ofthe light-dependent magnetic compass as well as to recentneurophysiological evidence showing magnetic fieldsensitivity located in the frog frontal organ which is anoutgrowth of the pineal gland They hypothesized thiswork could indicate a common ancestor as long ago as 294million years

To determine if orientation using Earthrsquos magneticfields changed according to seasonal migration patternsShakhparonov and Ogurtsov [471] tested marsh frogs(Pelophylax ridibundus) in the laboratory to see if frogscould determine migratory direction between the breedingpond and their wintering site according to magnetic cuesAdult frogs (n=32) were tested individually in a T-maze127 cm long inside a three-axis Helmholtz coil system(diameter 3 m) Maze arms were positioned parallel to thenatural migratory route and measured in accordance withthe magnetic field Frogs were tested in the breedingmigratory state and the wintering state mediated by atemperaturelight regime Frog choice in a T-maze wasevident when analyzed according to the magnetic fielddirection They moved along the migratory route to thebreeding pond and followed the reversion of the horizontalcomponent of the magnetic field The preference was seenin both sexes but only during the breeding migratory stateThey concluded that adult frogs obtained directional in-formation from the Earthrsquos magnetic field

Diego-Rasilla et al [472] found similar evidence in twospecies of lacertid lizards (Podarcismuralis and Podarcislilfordi) that exhibited spontaneous longitudinal body axisalignment relative to the Earthrsquos magnetic field during sunbasking periods Both species exhibited a highly signifi-cant bimodal orientation along the north-northeast andsouth-southwest magnetic axis Lizard orientations were

Levitt et al EMF and wildlife 39

significantly correlated over a five-year period withgeomagnetic field values at the time of each observationThis suggested the behavior provides lizards with a con-stant directional reference possibly creating a spacialmental map to facilitate escape This was the first study toprovide spontaneous magnetic alignment behavior in free-living reptiles although studies of terrapins have alsofound such spontaneousmagnetic alignment [92 323 473]Nishimura et al [474 475] also found sensitivity toELF-EMF (sinusoidal 6 and 8 Hz peak magnetic field26 μT peak electric field (10 Vm) in a lizard species(Pogona vitticeps) as demonstrated by significant increasedtail lifting mdash a reproductive behavior Interestingly thistail-lifting response to ELF-EMF disappeared when theparietal eye was covered suggesting that the parietal eyecontributes to light-dependent magnetoreception and thatexposure to ELF-EMFs may increase magnetic-field sensi-tivity in the lizards A further experiment [476] showed thatlight at a wavelength lower than 580 nm was needed toactivate the light-dependent magnetoreception of the pa-rietal eye

Amphibians RF-EMF

Most frogs spend significant time on land but lay eggs inwater where they hatch into tadpoles with tails and inter-nal gills However some species bypass the tadpole stageandor deposit eggs on land Frogs are thus subject to ex-posures from both land-based and aquatic environmentsA frogrsquos life cycle is complete when metamorphosis into anadult form occursMany adverse effects do not appear untilafter metamorphosis is completed but problems have beenfound throughout the entire life cycle after exposures toboth ELF-EMF and RFR

Most early research on frogs (other than the Beckeret al regeneration inquiries noted above) was conducted athigh thermal levels rarely encountered in the environmentbut some are included here because they helped delineateamphibian electrophysiology with effects later supportedin low-level research Some early work did use frog modelsto investigate cardiac effects with lower intensity expo-sures Levitina [477] found that intact frog whole-bodyexposure caused a decrease in heart rate while irradiationof just the head caused an increase Using VHF frequencyRFR at a power density of 60 μWcm2 A=125 cm Levitinaattributed the cardiac changes to peripheral nervous sys-tem effects but according to Frey and Siefert [478] becauseof the wavelengths used in that study little energetic bodypenetration would be expected They said a skin receptorhypothesis was therefore reasonable

Following on Levitinarsquos work Frey and Seifert [478]mdashusing isolated frog hearts UHF frequencies that penetratetissue more efficiently and low intensity pulse modula-tion mdash found that pulsed microwaves at 1425 GHz couldalter frog heart rates depending on the timing of exposurebetween the phase of heart action and themoment of pulseaction Twenty-two isolated frog hearts were irradiatedwith pulses synchronized with the P-wave of the ECGspulses were of 10 s duration triggered at the peak of theP-wave Two control groups were used without RFR ex-posures with no effects noted They found heart rate ac-celeration occurred with pulsing at about 200 ms after theP-wave But if the pulse occurred simultaneously with theP-wave no increases were induced Arrhythmias occurredin half the samples some resulting in cardiac cessationClearly from this study RFR affected frog heart rhythm andcould cause death

A more recent work by Miura and Okada [479] foundsevere vasodilation in frog foot webs from RFR In a seriesof three experiments using 44 anesthetized frogs (X laevis)at thermal and non-thermal intensities researchersexposed foot webs to pulsed RFR in three parameters withthe monitor coil set at 1 V peak-to-peak 100 kHz 582-3 mGand 17476 V cmminus1 10 MHz 73 mG and 219 V cmminus1 1 MHz539 mG and 1611 V cmminus1 They found not only dilated ar-terioles of the web which had already been re-constrictedwith noradrenaline but also dilated arterioles under non-stimulated conditions Vasodilatation increased slowlyand reached a plateau 60 min after radiationrsquos onset Afterradiation ceased vasodilation remained for 10ndash20 minbefore slowly subsiding Vasodilation was optimum whenpulsation was applied 50 of the total time at a 10 kHzburst rate at 10 MHz Effects were non-thermal The patternof vasodilation induced by warm Ringer solution wasdifferent from the vasodilatory effect of weak RFRinvolving the level of intracellular Ca2+ They hypothesizedthat since Ca2+ ATPase is activated by cyclic GMP which isproduced by the enzymatic action of guanylate cyclaseRF-EMF may activate guanylate cyclase to facilitate cyclicGMP production They concluded the study indicates for thefirst time that RFR dilates peripheral resistance vessels byneither pharmacological vasodilator agents nor physicalthermal radiation but that the precise mechanisms of acti-vation of guanylate cyclase by RFR at the molecular levelrequired further study Vasodilation and constriction affectsevery part of the body and can affect all organ systems

Prior to this Schwartz et al [480] found changes incalcium ions in frog hearts in response to a weak VHF fieldthat was modulated at 16 Hz This would be an exposurecommon in the environment Calcium ions are critical toheart function

40 Levitt et al EMF and wildlife

Balmori [24ndash30 442] and Balmori and Hallberg [271]have focused widely on EMF effects to wildlife with twopapers on amphibians Balmori [442] in a review notedthat RFR in the microwave range is a possible cause fordeformations and decline of some amphibian populationsand Balmori [481] in 2010 found increased mortality intadpoles exposed to RFR in an urban environment In the2010 study tadpoles of the common frog (Rana temporaria)were exposed to RFR from severalmobile phone towers at adistance of 459 ft (140 m) Two month exposures lastedthrough egg phase to advanced tadpole growth prior tometamorphosis RF andMW field intensity between 18 and35 Vm (086ndash32 μWcm2) were measured with threedifferent devices Results determined that the exposedgroup (n=70) had low coordination of movements andasynchronous growth that resulted in both large and smalltadpoles aswell as a disturbing 90highmortality rate Inthe control group (n=70) a Faraday cage was used underthe same conditions Controls found movement coordina-tion to be normal and development synchronous withmortality rate at a low 42 These results indicated thatRFR from cell towers in a field situation could affect bothdevelopment and mortality of tadpoles Prior to this studyGrefner et al [482] also found increased death in tadpoles(Rana temporaria L) exposed to EMF as well as highermortality rates and slower less synchronous development

Mortazavi et al [483] found changes in muscle con-tractions in frogs exposed to 900-MHz cell phone radiationfor 30 min gastrocnemimus muscles were then isolatedand exposed to a switched onoff mobile phone radiationfor three 10-min intervals The authors reportedRFR-induced effects on pulse height and latency period ofmuscle contractions SARs of the nerve-muscle preparationwere calculated to be 066 (muscle) and 0407 (nerve)Wkg

Rafati et al [484] investigated the effects of RFR onfrogs frommobile phone jamming equipment emitting RFRin the same frequencies as mobile phones (Althoughillegal inmany countries jammers are nevertheless used tointerfere with signals and stop communication) The studysought to follow up on reports of non-thermal effects ofRFR on amphibians regarding alterations of musclecontraction patterns They focused on three parametersthe pulse height of leg muscle contractions the time in-terval between two subsequent contractions and the la-tency period of frogrsquos isolated gastrocnemius muscle afterstimulation with single square pulses of 1 V (1 Hz) Animalsin the jammer group were exposed to RFR at a distance of1 m from the jammerrsquos antenna for 2 h while the controlfrogs were sham exposed All were then sacrificed andisolated gastrocnemius muscles were exposed to onoff

jammer radiation for three subsequent 10 min intervals(SAR for nerve and muscle of the different forms of jammerradiation was between 001 and 0052 Wkg) Resultsshowed that neither the pulse height of muscle contrac-tions nor the time interval between two subsequent con-tractions were affected but the latency period (timeinterval between stimulus and response) was statisticallysignificantly altered in the RFR-exposed samples Theyconcluded the results supported earlier reports of non-thermal effects of EMF on amphibians including the effectson the pattern of muscle contractions Control shamexposed samples showed no effects

Amphibians reptiles ELF-EMF

Amphibians are highly sensitive to ELF-EMF An early-1969study by Levengood [485] using a magnetic field probefound increased high rates of teratogenesis in frogs (Ranasylvatica) and salamanders (Ambystoma maculatum) Twoidentical probes using different field strengths wereemployed mdash both operated in the kilogauss region withhigh field gradients Amphibian eggs and embryos wereexposed at various stages of development with gross ab-normalities found in developing larvae vs control At thehatching stage severe abnormalities were noted in bothanuran and urodele larvae from probe-treated eggsHatching abnormalities included microcephaly altereddevelopment andmultiple oedematous growths In probe-treated frogs there was a delay in the appearance of a highpercentage of malformations until the climax stage ofmetamorphosis Until that stage the larvae were of thesame appearance as control specimens thus camouflagingthe damage after just a brief treatment of early embryosThe frog abnormalities at metamorphosis differed fromthose in the hatching tadpoles and consisted mainly ofsevere subepidermal blistering and leg malformationsincluding formation of multiple deformed limbs incom-patiblewith life Over 90of themorphological alterationsat metamorphosis climax were also found to be associatedwith deformed kidneys The gastrula stages of develop-ment appeared to be the most sensitive in the delayed-effects category While this was a high-field exposureexperiment it is an intensity that is found in some envi-ronments today especially near high tension lines and inabnormal ground current situations

Neurath [486] also found strongly inhibited early em-bryonic growth of the common leopard frog (Rana pipiens)by a high static magnetic field with a high gradient (1T) mdashan exposure sometimes found in the environmentmdash whileUeno and Iwasaka [487] found abnormal growth and

Levitt et al EMF and wildlife 41

increased incidence of malformations in embryos exposedto magnetic fields up to 8T but exposures that high aretypically near industrial sites and rarely found in nature

Severini et al [488] specifically addressed whetherweak ELF magnetic fields could affect tadpole develop-ment and found delayed maturation in tadpoles Two co-horts of X laevis laevis (Daudin) tadpoles were exposed for60 days during immaturity to a 50 Hz magnetic field of639ndash764 μT rms (root mean square average values)magnetic flux density in a solenoid Controls were twocomparable cohorts remotely located away from the sole-noid The experiment was replicated three times Resultsshowed reduced mean developmental rate of exposed co-horts vs controls (043 vs 048 stagesday plt 0001)beginning from early larval stages exposure increased themean metamorphosis period of tadpoles by 24 days vscontrols (p lt 0001) and during the maturation periodmaturation rates of exposed vs control tadpoles werealtered No increases in mortality malformations or tera-togenic effects were seen in exposed groups The re-searchers concluded that relatively weak 50 Hz magneticfields can cause sub-lethal effects in tadpoles via slowedlarval development and delays in metamorphosis Suchexposures are found in the environment today in somelocations and even though the changes were smallcoupled with climate change such sub-lethal effects mayimpact some wildlife populations in some environments

In similar followup work Severini and Bosco [489]found sensitivity to small variations of magnetic flux den-sity (50 Hz 22-day continuous exposure magnetic fluxdensities between 639 and 764 microT) in tadpoles exposed toa stronger field vs controls exposed to a weaker field Asignificant delay in development of 25 days was found inexposed vs controls They concluded the delaywas causedby the slightly differentmagnetic flux densities with resultssuggesting a field threshold around 70 microT in controlling thetadpole developmental rate

Schlegel in 1997 found European blind cave salaman-ders (Proteus anguinus) and Pyrenean newts (Euproctusasper) to be sensitive to low level electric fields in water[490] And Schlegel and Bulog [491] in followup workfound thresholds of overt avoidance behavior to electricfields as a function of frequency of continuous sine-wavesin water Nine salamanders from different Slovenian pop-ulations of the urodele (P anguinus) that included threespecimens of its lsquoblackrsquo variety (P anguinus parkelj)showed thresholds between 03 mVcm (ca 100 nAcm2)and up to 2 mVcm (670 nAcm2) with the most reactivefrequencies around 30 Hz Sensitivity included a total fre-quency range below 1 Hz (excluding DC) up to 1ndash2 kHzwithup to 40 dB higher thresholds These are ranges that may

be found in the wild near high tension lines and utilitygrounding practices near water by some underwater ca-bling and by some RFR transmitters

Landesman and Douglas in 1990 [492] found somenewt species showed accelerated abnormal limb growthwhen pulsed electromagnetic fields were added to thenormal limb regeneration process While normal limbregeneration found normal regrowth patterns in 72 ofspecimens 28 were abnormal Abnormalities includedloss of a digit fused carpals and long bone defects whichoccurred singly or in combination with one another Whenexposure to a PEMF was added for the first 30 days post-amputation followed by a 3ndash4 month postamputationperiod a group of forelimbs with unique gross defectsincreased by an additional 12 Defects (singly or incombination) included the loss of two or more digits withassociated loss of carpals absence of the entire handpattern and abnormalities associated with the radius andulna The researchers offered no explanation Exposureintensities were similar to those used to facilitate non-juncture fracture healing in humans

Komazaki and Takano in 2007 [493] found acceleratedearly development growth rates with 50 Hz 5ndash30 mTalternating current exposures in the fertilized eggs of Jap-anese newts (Cynops pyrrhogaster) The period of gastru-lation was shortened via EMF-promoted morphogeneticcell movements and increased [Ca2+]i They said their re-sults indicated that EMF specifically increased the [Ca2]i ofgastrula cells thereby accelerating growth This study onlyobserved through the larval stages and they did not see anymalformations under EMF exposures which they attrib-uted to possible differences in the intensity and mode ofEMF

With amphibians and some reptiles demonstratinghigh sensitivity to natural background EMF for importantbreeding and orientation needs amphibians living inaquatic terrestrial and aerial environments (ie tree frogspecies) may be affected from multi-frequency anthropo-genic EMF in ways we do not fully understand There arepotential effects mdash especially from 5G MMW that couplemaximally with skin mdash to all aspects of their developmentand life cycles including secondary effects

Fish marine mammals lobstersand crabs

Aquatic animals are exquisitely sensitive to natural EMFand therefore potentially to anthropogenic disturbanceThe Earthrsquos dipole geomagnetic field yields a consistent

42 Levitt et al EMF and wildlife

though varying source of directional information in bothland and aquatic species for use in homing behaviororientation during navigation and migration This infor-mation is used both as a lsquomaprsquo for positional information aswell as a lsquocompassrsquo for direction [494ndash497] Aquatic speciesare known to be sensitive to static geomagnetic fields at-mospheric changes and sunspot activities [498] For recentcomprehensive reviews onmagnetic field sensitivity in fishand effects on behavior see Tricas and Gill [36] and Krylovet al [33] Some biological lsquomagnetic mapsrsquo may beinherited [499] And for a recent extensive discussion of theEarthrsquos natural fields and magnetoreception in marineanimals with a focus on effects from electromagnetic sur-veys that use localized strong EMFs to map petroleum de-posits under seabeds see Nyqvist et al [498] and below

As mentioned above because of the difference inconductivity of water and other factors the way someaquatic species sense EMF may rely on unique modes ofphysiological perception as well as those employed byterrestrial animals There may also be sensory combina-tions not yet understood in some aquatic and semi-aquaticspecies For instance what role does the neural conduc-tivity of whiskers (vibrissae) in seals sea lions and walrusplay other than for food finding Aquatic speciesrsquo densenetwork of whiskers is larger with greater blood flow thanterrestrial species and can contain 1500 nerves per folliclevs cats at 200 per follicle Seal whiskers also varygeometrically from terrestrial species and the largest partof the seal brain is linked to whisker function Seals usewhiskers to map the size shape and external structure ofobjects and can find prey even when blindfolded Theirwhiskers are also sensitive to weak changes in water mo-tion [100] But are they also using them as a location ordirectional compass in relation to the geomagnetic fieldThat has yet to be studied

Unique sensory differences in aquatic species have longbeen documented Joshberger et al [500] noted that in 1678Stefano Lorenzini [501] was the first to describe a network oforgans in the torpedo ray that became known as the Ampullaeof Lorenzini (AoL) Its purpose was unknown for 300 yearsuntil Murray [502] measured AoLrsquos electrical properties inelasmobranch fishmdash sharks rays and skates Later work [101503ndash508] confirmed and greatly added to this knowledgeResearchers now know that AoL is likely the primary mecha-nism that allows elasmobranch fish to detect and map a po-tential preyrsquos physiology via the very weak changes in electricfields given off by preyrsquos muscle contractions

Individual ampullae are skin pores that open to theaquatic environment with a jelly-filled canal leading to analveolus containing a series of electrosensing cells Withinthe alveolus the electrosensitive cells of the ampullae

communicate with neurons and this integration of signalsfrom multiple ampullae is what allows elasmobranch fish todetect electric field changes as small as 5 nVcm [503 506509 510] TheAoL jelly has been reported as a semiconductorwith temperature-dependence conductivity and thermoelec-tric behavior [500 509 510] as well as a simple ionicconductor with the same electrical properties as the sur-rounding seawater [503 506] Josberger et al [500] attemptedto clarify what AoLrsquos role is in electrosensing by measuringAoLrsquos proton conductivity They found that room-temperature proton conductivity of AoL jelly is very high at2 plusmn 1 mScmmdash only 40-fold lower than some current state-of-the-art manmade proton-conducting polymers That makesAoL the highest conductive biological material reported thusfar They suggested that the polyglycans contained in theAoLjelly may contribute to its high proton conductivity

Other aquatic magneto-sensory mechanisms more inharmony with terrestrial animals include the presence offerromagnetic particles in magnetite mdash tiny naturally pro-duced magnets that align with the Earthrsquos magnetic fieldallowing for speciesrsquo direction and orientation Magnetite ap-pears to transmit necessary information through a connectionwith the central nervous system [340 497 511] A magnetite-based system is plausible for cetaceans [512 513] as magnetitehas been found in the meninges dura mater surrounding thebrains ofwhales anddolphins [514 515] There is also evidencethat local variationsanomalies in the geomagnetic field incertain underwater topographies may play a role in live ceta-cean strandings [516 517]which indicates amagnetic compassbased on magnetite And free-ranging cetaceans have shownevidence of magnetoreception-based navigation eg Finwhale migration routes have been correlated with lowgeomagnetic intensity [513]

Recently Granger et al [518] found correlations in databetween 31 years of gray whale (Eschrichtius robustus)strandings and sunspot activity especially with RF lsquonoisersquoin the 2800 MHz range The 11-year sunspot cycle stronglycorrelateswith the intense releases of high-energy particlesknown as solar storms which can temporarily modify thegeomagnetic field and in turn may modify orientation inmagnetoreceptive species Solar storms also cause an in-crease in natural broadband RF lsquonoisersquo They examinedchanges in both geomagnetic fields and RF lsquonoisersquo andfound RF to be a determinant Further they hypothesizedthat increased strandings during high solar activity is morelikely due to radical pair mechanisms which are morereactive with RFR than magnetite which appears morereactive to ELF-EMF Two previous studies also foundcorrelations with cetacean strandings and solar activities[519 520] Both mechanisms may come into play underdifferent circumstances or act in synergy

Levitt et al EMF and wildlife 43

Kremers et al [512] investigated the spontaneousmagnetoreception response in six captive free-swimmingbottlenose dolphins (Tursiops truncates) to introducedmagnetized and demagnetized devices used as controlsThey found a shorter latency in dolphins that approachedthe device containing a strong magnetized neodymiumblock compared to a control demagnetized block identicalin form and density and therefore indistinguishable withecholocation They concluded that dolphins can discrimi-nate on the basis of magnetic properties mdash a prerequisitefor magnetoreception-based navigation Stafne andManger [521] also observed that captive bottlenose dol-phins in the northern hemisphere swim predominantly in acounter-clockwise directionwhile dolphins in the southernhemisphere swim predominantly in clockwise directionNo speculation was offered for this behavior

How salmon navigate vast distances mdash from theirhatching grounds in freshwater river bottoms to lakesduring juvenile growth then the open ocean duringmaturity and with a final return to their neonatal birthinggrounds to spawn and die (for most anadromous salmo-nids)mdash has fascinated researchers for decades Research in-dicates they may use several magneto-senses to accomplishthis including inherited mechanisms [522] imprinting [499522] a magnetic compass [499 522 523] and biomagneticmaterials Salmon have been found to have crystal chains ofmagnetite [524] One recent study found that strongmagneticpulses were capable of disrupting orientation in salmonmodels [525] indicating a magnetite-based mechanism Insalmon the migration process is complicated by the fact thatthe ability to sense geomagnetic fields can be altered bychanges in salinity between fresh and salt water thuspointing to multi-sensory mechanisms [499]

Speculation that salmon use the geomagnetic field insome capacity for their iconic migration goes back decades[526] Quinn [527] found evidence that sockeye salmon(Oncorhynchus nerka) frey use both a celestial and magneticcompass when migrating from river hatching to lakes Put-man et al [499] whohavewritten extensively on this subjectfocused on how salmon navigate to specific oceanic feedingareas mdash a challenge since juvenile salmon reach feedinghabitats thousands of kilometers from natal locations Theresearchers experimentally found that juvenile Chinooksalmon (Oncorhynchus tshawytscha) responded to magneticfields similar to latitudes of their extreme ocean range byorienting in directions that would lead toward their marinefeeding grounds They further found that fish use the com-bination ofmagnetic intensity and inclination angle to assesstheir geographic location and concluded that the magneticmap of salmon appears to be inherited since the fish had noprior migratory experience These results paired with

findings in sea turtles (see below) indicate that magneticmapsarewidespread in aquatic species and likely explain theextraordinary navigational abilities seen in long-distanceunderwater migrants [499]

It is less likely that light-sensing radical pair crypto-chromes play much of a role in aquatic species thoughsome hypothesize the possibility [528] Krylov et al [33]however noted that there are no anatomical structures orneurophysiological mechanisms presently known forradical pair receptors in the brains of fish and that sincelight decreases with water depth and fish are capable oforienting in complete darkness using the geomagneticfield their opinion was that it is too early to say fish havemagnetoreception mechanisms based on free radicalslight-dependent or otherwise

Fish lobsters crabs ELF-EMF

For several reasons having to do with differences in con-ductivity in water vs air (see above) RFR is of far lessconcern in aquatic environments at present than is ELFWith the ever-increasing number of underwater cablesused for everything from transcontinental datacommu-nications to power supplies for islands marine platformsunderwater observatories off-shore drilling wind facil-ities tidal and wave turbines among others many newsources of both AC and DC electric current are beingcreated in sea and freshwater environments alike Ac-cording to Ardelean and Minnebo writing in 2015 [529]almost 4971 mi (8000 km) of high voltage direct current(HVDC) cables were present on the seabedworldwide 70of which were in European waters and this is only ex-pected to grow dramatically as new sources of renewableenergy are built to replace fossil fuels globally

Curiosity about potential adverse effects from cable-generated ELF-EMF on all phases of fish life has alsogrown especially in benthic and demersal species thatspend significant time near cables in deeper bottom envi-ronments for egg laying larvae growth and developmentfor most if not all of their adult lives

Fey et al [494 495] and Oumlhman et al [530] noted thatthere are two types of anthropogenic exposures created bycables high voltage direct current (HVDC) that emits staticmagnetic fields and three-phase alternating current (ACpower transmission) that emit time-varying electromag-netic fields The density of electric current near underwatercables on the sea floor can vary significantly depending onthe type of cable and whether they are positioned on thesea bottom or buried [36 530] Noticeable magnetic fieldchanges can occur within meters but generally not more

44 Levitt et al EMF and wildlife

than several meters from the cable However Hutchinsonet al [531] in a robust field study and extensive reviewfound surprisingly stronger and more complex exposuresthan anticipated (see below)

Since fish are highly sensitive to static magnetic fields(MF) it is important to delineate static fields from anthro-pogenic alternating current EMF in aquatic studies Infreshwater species under laboratory conditions Fey et al[494] found similar results to those of salmon studies(noted above) in northern pike (Esox lucius) exposed to astatic magnetic field from DC cables (10 mT) during theembryonic phase and in the first six days of post-hatchingNo statistically significant MF effect was seen on hatchingsuccess larvae mortality larvae size at hatching andgrowth rate during the first six days of life However sig-nificant MF effects were seen on hatching time (one dayearlier in a magnetic field than in control) yolk-sac sizewas smaller and yolk-sac absorption rate was faster Theyinterpreted the faster yolk-sac absorption in a magneticfield as an indication of increasedmetabolic rate but addedthat even if some negative consequences were expected asa result that the actual risk for increased northern pikelarvae mortality seemed negligible Though higher than10 mT magnetic field values are hazardous for fish larvaethey added such values do not occur in the natural envi-ronment even along underwater cables

But in follow-up work of longer duration the samegeneral research group reached a different conclusion Feyet al [495] studied effects on eggs and larvae of rainbowtrout (Oncorhynchus mykiss) exposed to a static magneticfield (MF) of 10 mT and a 50 Hz EMF of 1 mT for 36 days(ie from eyed egg stage to approximately 26 days posthatching) They found that while neither the static MF northe 50-Hz EMF had significant effects on embryoniclarvalmortality hatching time larval growth or the time oflarvae swim-up from the bottom both fields did howeverenhance the yolk-sac absorption rates While they said thiswas not directly related to a MF effect it was shown thatlarvaewith absorbed yolk-sacs by the time of swim-upwereless efficient in taking advantage of available food at firstfeeding and gained less weight They concluded that theseexposures could negatively affect the yolk-sac absorptionrate thereby hampering fish in important feeding activitiesneeded for fast weight gain and increased survival In anadditional study Fey et al [532] observed that rainbowtrout reared in a laboratory for 37 days and exposed to astatic MF (10 mT) or a 50-Hz EMF (1 mT) showed defects inotolith of the inner ear which is responsible for hearing andbalance in fish The authors concluded that underwaterconstruction andor cables that emit a MF of 10 mT orhigher can affect living organisms within a few meters

distance especially species like trout in settled life stageson the sediment bottom during early development

Zebrafish (Danio rerio) are often used in EMF research intoxicology and developmental biology investigating effectson humans because the genomes are so similar Li et al [533]studied ELF-MF on the development of fertilized zebrafishembryos divided into seven groups Embryos of experi-mental groups were continuously exposed to 50-Hz sinu-soidal MF with intensities of 30 100 200 400 or 800 μT for96 h The sham group was identical but without ELF-MFexposure Results showed that ELF-MF caused delayedhatching and decreased heart rate at early developmentalstages but no significant differences were seen in embryomortality or abnormality Acridine orange staining assaysshowed notable signs of apoptosis in the ventral fin andspinal column and transcription of apoptosis-related genes(caspase-3 caspase-9) was significantly up-regulated inELF-MF-exposed embryos They concluded that ELF-EMFdemonstrated detrimental effects on zebrafish embryonicdevelopment including on hatching decreased heart rateand induced apoptosis although such effects were not amortal threat The lower range exposures of this study arefound in some aquatic environments

Sedigh et al [534] investigated effects on zebrafishexposed to static magnetic fields Exposures of 1-week acuteand 3-week subacute exposures to different static magneticfields at 25 5 and 75 mT were measured on stress indices(cortisol and glucose) sex steroid hormones (17β-estradioland 17-α hydroxy progesterone) and fecundity They found asignificant change in cortisol glucose 17β-estradiol (E2) and17-α hydroxy progesterone (17-OHP) levels with increasedintensity and duration of exposure and concluded that staticmagnetic fields at higher intensities showed harmful effectson the reproductive biology of zebrafish during both acuteand subacute exposures

Recent laboratory research by Hunt et al [535] used thetransparent glass catfish (Kryptopterus vitreolus) found inslow moving waters in Southeast Asia as a model toinvestigate magnetoreception The study used Y-mazechambers animal tracking software and artificial intelli-gence techniques to quantify effects of magnetic fields onthe swimming direction of catfish They placed a perma-nent Neodymium Rare Earth Magnet (115 times 318 times 22 cm)with a horizontal magnetic flux of 577 mT at the magnetrsquossurface at 10 cm from the endof one of the Y-maze arms andfound that catfish consistently swam away from magneticfields over 20 μT The catfish also showed adaptability tochanging magnetic field direction and location The mag-netic avoidance was not influenced by school behaviorSham exposures produced no avoidance Such exposuresmight be found near some underwater cables

Levitt et al EMF and wildlife 45

To further elucidate findings of species reactions nearunderwater cables and fill in knowledge gaps since the2011 Tricas and Gill review [36] Hutchinson et al [531]conducted both field and laboratory modeling studies ofboth AC and DC fields on the American lobster (Homarusamericanus) and the little skate (Leucoraja erinacea) Theynoted that in previous studies while behavioral responseshad been seen findings were unable to determine if sig-nificant biological effects (eg population changes)occurred TheAmerican lobsterwasmodeled because it is amagnetosensitive species [536] and concern existed thatEMF from cables might restrict movements andor migra-tion Lobsters may migrate up to 50 mi (80 km) one wayfrom deep waters to shallow breeding grounds The littleskate was used as a model for the most electro-sensitivetaxa of the elasmobranchs which may be attracted bytothe EMF of cables particularly for benthic species therebyaltering their foraging or movement behavior Bothmodelswere therefore thought indicative of potential EMF im-pacts In this robust field study the researchers found thatthe American lobster exhibited a statistically significantbut subtle change in behavioral activity when exposed tothe EMF of theHVDC cable (operated at a constant power of330 MW at 1175 Amps) The little skate exhibited a strongbehavioral response to EMF from a cable powered for624 of the study with the most frequently transmittedelectrical current at 16 Amps (at 0 MW 375 of time) 345Amps (100 MW 286) and 1175 Amps (330 MW 152)They concluded that for both species the behavioralchanges have biological relevance regarding how they willmove around and are distributed in a cable-EMF zone butthey noted that the EMF did not constitute a barrier tomovements across the cable for either species

Of interest in this study were the actual field readingsnear cables Unexpected significant ACmagnetic and electricfields did not match computer models and were observed tobe associated with both of the DC power cables studied Themaximum observed AC values along the cable axis were015 μT and 07 mVm for the magnetic and electric fieldsrespectively for one cable and 004 μT and 04 mVmrespectively for the other cable Also the cross section of theEMF peaks exhibited by the DC subsea power cables werebroader than anticipated at both studied The DC and ACmagnetic fields reached background levels on either side ofthe cable on a scale of ca5 and 10m from the peak observedvalue respectively whereas the AC electric fields reachedbackground on a scale of 100 m (328 ft) from the peak valuePeak observed values occurred almost directly above thecable axis location there was an offset of 33 ft (lt1 m) wherethe cable was twisted The researchers noted that thisobservation of AC fields with broad areas of EMF distortion

being associated with DC cables increased the complexity ofinterpreting the studies of EMFrsquos biological effects from DCcables TheACelectricfieldsassociatedwith theACsea2shorecable (1ndash25 mVm) were higher than the unanticipated ACelectricfieldsproducedby theDCcables (04ndash07mVm) Themagnetic field produced by the AC sea2shore cable (range of005ndash03 μT) was sim10 times lower than modeled valuescommissioned by the grid operator indicating that the three-conductor twisted design achieves significant self-cancellation This entire aspect of the study indicates theneed for accurate field assessment not just computermodeling andwell-designed systems since anomalies occur

Nyqvist et al [498] in a thorough review focused onmarine mammals and the use of underwater electromag-netic surveys that map petroleum deposits in seabeds viastrong induced EMFs in varied directional applicationsThey found that EMFs created during such active surveyingwere within the detectable ranges of marine animals andthe fields can potentially affect behavior in electro-perceptive species but they noted that effects should belimited to within a few kilometers as the electric andmagnetic fields created attenuate rapidly They added thatin migrating marine animals exposures are of shortduration and most are close to naturally occurring levelsbut cautioned that lack of studies is a concern especiallyfor the most sensitive elasmobranchs at highest risk fordisturbance to electric fields They also noted that withinduced magnetic fields animals using magnetic cues formigration or local orientation during certain time-windowsfor migration orientation or breeding could be mostaffected by this surveying technology

Taorimina et al [537] studied both static and time-varying magnetic fields on the behavior of juvenile Euro-pean lobsters (Homarus gammarus) Using two differentbehavioral assays day-light conditions to stimulate shel-tering behavior and exposures to an artificial magneticfield gradient (maximum intensity of 200 μT) they foundthat juvenile lobsters did not exhibit any behavioralchanges compared to non-exposed lobsters in the ambientmagnetic field No differences were noted on the lobstersrsquoability to find shelter or modified their exploratorybehavior after one week of exposure to anthropogenicmagnetic fields (225 plusmn 5 μT) which remained similar tobehavior in controls They concluded that neither static nortime-varying anthropogenic magnetic fields at those in-tensities significantly impacted the behavior of juvenileEuropean lobsters in daylight conditions but they notedthat evidence exists showing magnetosensitivity changesduring different life stages in lobster species and that sincetheir modeling was on juveniles their study was thereforean incomplete picture requiring further study

46 Levitt et al EMF and wildlife

Scott et al [538] focused on ELF-EMF effects oncommercially important ediblebrown crab species (Can-cer pagurus) and what they found was startling In labo-ratory tanks they simulated EMF (with Helmholtz coils28 mT evenly distributed assessments during 24 h pe-riods) that would be emitted from sub-sea power cablesnow commonly used at offshore renewable energy facil-ities They measured stress related parameters ((L-lactateD-glucose haemocyanin and respiration rate) along withbehavioral and response parameters (antennal flickingactivity level attractionavoidance shelter preference andtime spent restingroaming) They found that althoughthere was no EMF effect on haemocyanin concentrationsrespiration rate activity level or antennal flicking ratethere were significant changes in haemolymph L-lactateand D-glucose natural circadian rhythms indicating al-terations in hormones Crabs also showed an unusuallyhigh attraction to EMF-exposed shelter areas (69)compared to control shelter areas (9) and significantlyreduced their time roaming by 21 with adverse impli-cations for food foraging mating and overall health Theynoted that EMF clearly altered behavior Crabs spent lesstime roaming around the tank andmore time in a shelter indirect contact with the EMF source indicating naturalroamingfood-or-mate-seeking behavior had been over-ridden by attraction to EMF In fact crabs consistentlychose an EMF-exposed shelter over a non-exposed one andwere always drawn to the EMF The results appear topredict that in benthic areas surrounding EMF-emittingcables there will be an increase in the abundance ofCancer pagurus present They noted that such potentialcrab aggregation around benthic cables and the subse-quent physiological changes in L-lactate and D-glucoselevels caused by EMF exposure is a concern regardingfeeding rates mating and especially egg incubationdirectly in increased EMF environments They concludedthat long term investigations are needed regarding chronicEMF exposure especially on egg development hatchingsuccess and larval fitness and added that EMF emitted inmarine environments from renewable energy devicesmustbe considered as part of the study of cumulative impactsduring the planning stages

Clearly ELF-EMF can affect myriad aquatic species atintensity levels found in proximity to underwater cables atenvironmental intensities

Fish RF-EMF

As mentioned RFR is of minimal environmental concernfor fish since aquatic environments while highly

conductive mediums also highly attenuate EMF at higherfrequencies This may change in the near future as newtechnologies now exist thatmay surpass these obstacles [98]thereby introducing for the first time novel new RFR expo-sures underwater Longer wave wireless ELF with expandedranges are used in anthropogenic sonar (sound navigationranging) primarily for military applications These traveleasily through water and are known to adversely affect ce-taceans and other species that rely on their natural sonar forcommunication migration reproduction and food findingBut soundwaves are not considered ldquoEMFrdquo in the strict senseof the term since the focus of this paper is EMF soundwavesare tangential here But acoustic damage especially to ceta-ceans from military and commercial applications is welldocumented and ELF cables used for underwater militarysubmarine communications can have significant EMF expo-sures near cables Just because this paper does not addressimpacts from sound waves in detail does not mean they arewithout serious effects

There are however three recent studies of RFR onzebrafish included here because it is plausible that suchexposures could exist near shallow aquatic environmentsunder some circumstances Nirwane et al [539] studied900-MHz GSM RFR effects on zebrafish (D rerio) neuro-behavioral changes and brain oxidative stress as a modelfor human exposures to cell phones Exposures wereapplied daily for 1 h 14 days with SAR 134 WKg Theyfound 900-MHz GSM radiation significantly decreased so-cialization and increased anxiety as demonstrated by sig-nificant increased time spent in bottom areas freezingbehaviors and duration and decreased distance travelledas well as decreased average velocity and number of en-tries to the upper half of the tank Exposed zebrafish spentless time in the novel armof a Y-Maze indicating significantimpaired learning compared to the control group Expo-sure also decreased superoxide dismutase (SOD) andcatalase (CAT) activities while increased levels of reducedglutathione (GSH) and lipid peroxidation (LPO) wereencountered indicating compromised antioxidant defensePost-exposure treatment with melatonin in the waterhowever significantly reversed the induced neuro-behavioral and oxidative changes

Piccinettia et al [540] investigated in vivo effects onembryonic development in zebrafish at 100 MHz thermaland nonthermal intensities via a multidisciplinary proto-col Results found 100 MHz RFR affected embryonicdevelopment from 24 to 72 h post fertilization in all theanalyzed pathways Most notably at 48 h post fertilizationreduced growth increased transcription of oxidative stressgenes onset of apoptoticautophagic processes and amodification in cholesterol metabolism were seen EMF

Levitt et al EMF and wildlife 47

affected stress by triggering detoxification mechanisms At72 h post fertilization fish partially recovered and reachedhatching time comparable to controls The researchersconcluded that EMF-RFR unequivocally showed in vivoeffects at non-thermal levels

Dasgupta et al [541] used embryonic zebrafish modelsat 35 GHz SAR asymp 827 Wkg and exposed developingzebrafish from 6 to 48 h post fertilization then measuredmorphological and behavioral endpoints at 120 h postfertilization Results found no significant impacts on mor-tality morphology or photomotor response but noted amodest inhibition of startle response suggesting somelevels of sensorimotor disruptions They concluded thatexposures at low GHz levels are likely benign but never-theless entailed subtle sensorimotor effects Such effectscan affect fish survival in variousways including inhibitedresponse time to predators among others This study wasdone with an eye toward potential human bioeffects atfrequencies used in 4 and 5G technology It was also con-ducted at intensities higher than the focus of this paper

If new technology overcomes the conductivityatten-uation limitations of aquatic environments and introducesmore RFR to aquatic species studies like those cited abovemay soon have more environmental relevance even athigher intensities than explored here

Turtles

Oceanic sea turtle migration joins that of other renownedlong-distance migratory species like salmon and over-landmonarch butterfly treks spanning thousands of kilometersand traversingmultiple complex environments throughouttheir life cycles Sea turtles have long been known to usegeomagnetic fields for orientation [542 543] Freshwaterspecies (eg Chelydra serpentina) have also been shown tohave a magnetic sense capable of artificial disruption [92]as do terrestrial box turtles (Terrapene carolina [544])

Sea turtles demonstrate natal homing behavior mdash theability to return over great distances to their exact birthlocation to reproduce [89] and because of anthropogenicdisruptions of nesting grounds along beaches this repro-ductive homing drive imperils them today The underlyingmechanism is still imperfectly understood but involveslsquoimprintingrsquo of the intensity and inclination angle of thegeomagnetic field at the birth location [545] The informa-tion is then later used in maturity to return to their place oforigin

Sea turtles are by far the most studiedmodels for turtlemagnetoreception especially by the Lohmann Laboratoryat the University of North Carolina US [323 546ndash558]

Irwin and Lohmann [559] discussed the advantagesand disadvantages of various research approaches used toinvestigate magnetic orientation behavior in turtles Theseinclude the use of largemagnetic coil systems in laboratorysettings to generate relatively uniform fields over largeareas [560] which allow the magnetic field to be artificiallyaltered and carefully controlled to determine changes inbehavioral orientation This approach however is un-suited for manipulating exposures around animals innatural environments or for studying localized body mag-netoreceptors which in turtles are still a mystery Anotherapproach is to attach a small magnet or electromagneticcoil to an animal to disrupt magnetic orientationbehavior mdash a far easier approach in hatchlings than injuvenile ormature free-swimming species They note that ifthe imposed field from an attachedmagnet or coil is strongenough to interfere with the Earthrsquos field behavioralorientation changes [116 544 561] and the performance ofa conditioned response [367 562] can be observed Thislatter approach has been used in field studies for the pur-pose of blocking access to normal magnetic information[544 561 563ndash565] and to localize magnetoreceptors bydisrupting the field around a specific terrapin body part[562] This techniquersquos disadvantage however is thatfields rapidly change with distance from the source mak-ing it difficult to quantify the fields that the animal actuallyexperiences

Most sea turtle studies have involved large magneticcoil systems but Irwin and Lohmann [559] attached smallmagnets greater in strength than the Earthrsquos fields to twogroups of loggerhead sea turtle hatchlings (Caretta carettaL) under laboratory conditions in which turtles are knownto orient magnetically [473 546 548ndash550] They found thatmagnetic orientation behavior in hatchling turtles can bedisrupted via small magnets attached to the carapacewhich then create exposures over the entire body Theyconcluded that such an approach can be used to finallydetermine local magnetoreceptors by varying the locationof themagnet and using smaller weakermagnets that alterthe field only around specific anatomical target sites

In loggerhead sea turtles there is evidence of aninclination compass [473 550] that is functionlly similar tothe bird magnetic compass reported in European Robins[566 567] Lohmann and Lohmann [550] investigated aninclination compass in sea turtles and found it was apossible mechanism for determining latitude Also inves-tigated were detection of magnetic intensity [551] naturalregional magnetic fields used as navigational markers forsea turtles [557] and sea turtle hatchlingsrsquo mapping abili-ties [545] Sea turtles are also known to have magnetite intheir heads [104 568] Studies with young sea turtles have

48 Levitt et al EMF and wildlife

shown that a significant portion of their navigationalabilities involve magnetoreception following hatching[569] mdash imprinting with the Earthrsquos magnetic field beingone of several cues hatchlings use as they first migrateoffshore [546 554] The magnetic fields that are unique todifferent areas at sea eventually serve as navigationalmarkers to guide swimming direction to important migra-tory routes As juveniles mature they form topographicalmagnetic maps where they live that direct them to specificregions But it has remained largely unknown if matureturtles specifically nesting females use such mechanismsin open-sea homing as this magneto-sense may changeover time

Field studies are notoriously difficult with large spe-cies at sea but Papi et al [564] studied mature green turtles(Chelonia mydas) during their post-nesting migration over1243 mi (2000 km) from their nesting grounds on Ascen-sion Island in themiddle of the Atlantic Ocean back to theirBrazilian feeding grounds They were investigatingwhether mature female turtles use an inclination compassand geomagnetic fields for direction or by inference (oncethat sense is disturbed) by some other means as yetdetermined Papi et al [564] attached very strong DCmagnets mdash significantly stronger than the Earthrsquos fields mdashto disturb and overcome natural magnetoreception andthereby determine if they could still navigate back to As-cension Island Controls had nonmagnetic brass barsattached and some had transmitters glued to their headsAll had tracking devices that communicatedwith satellitesthus creating strongmulti-frequency static and pulsed RFRexposures Seven turtles were each fitted with six powerfulstatic magnets that produced variable artificial fields sur-rounding the whole turtle making reliance on a geomag-netic map impossible The studyrsquos travel courses were verysimilar to those of eight turtles without magnets that hadbeen tracked via satellite over the same period in the pre-vious year No differences between the magneticallyexposed test turtles and untreated turtles were foundregarding navigational performance and general coursedirection They concluded that magnetic cues were notessential to turtles on the return trip and speculated thatperhaps other factors such as smell or wave current di-rection may come into play

Luschi et al [563] like Papi et al [564] also investi-gated the role of magnetoreception and homing in maturesea turtles but used a different design and found verydifferent results In a large field study in the MozambiqueChannel 20 mature pre-nesting green turtles were alsoequipped with both strong magnets and satellite trackingdevices The turtles were gathered at their nesting beach onMayotte Island before egg-laying and transported to four

open-sea sites 62ndash75 mi (100ndash120 km respectively) awayThere were five releases of four turtles each with threedifferent treatments turtles magnetically lsquodisturbedrsquo onlyduring transportation with magnets removed beforerelease those treated only during the homing trip withmagnets attached just prior to release and controls withnonmagnetic brass discs attached to their heads Treatedturtles had very strongmoveable magnets attached to theirheads to induce varying magnetic fields around themeither at the nesting beach at the start of the relocationjourney or on the boat just prior to release for the homingtrip All groups had satellite transmitters attached to theircarapaces thereby creating in the opinion of the authors ofthis paper an additional exposure that was not consideredas a variable The researchers also included ocean currentsin their assessments estimated by using oceanographicremote sensing measurements All but one turtle eventu-ally returned to Mayotte to complete delayed egg-layingBut treated turtles whether treated during transportationor homing took significantly longer to reach the destina-tion vs controls mdash a surprising finding Most homingroutes showed very long circuitous curved and loopingpatterns before reaching their target Control paths weredirect Both treated turtle groups were clearly impaired bythe MF exposure indicating significant recovery timeneeded between exposure and correcting positionalbehavior The researchers hypothesized the existence of anavigational role for geomagnetic information beinggathered by those turtles in the passive transportationgroup as well as the possibility that magnetic disturbanceduring transportation may have persisted for some timeafter the removal of the magnets in that group thusrendering the two treated groups functionally equivalentduring their homing journeys They also noted that expo-suresmay have physically alteredmagnetite particles thuscreating a longer lasting effect but they said that since long-lasting after-effects of magnet application have not beendescribed this theory could neither be inferred nordismissed

Lohmann [323] reviewed both of the above studies andadded that in addition to the two causal hypotheses ofLuschi et al [563] regarding their unexpected findings ofturtle circuitous migration routes another explanationwould include the positioning of the satellite transmittersin the Papi et al [564] study on turtle heads vs on thecarapace of the Luschi models He added that since satel-lite transmitters also produce magnetic fields capable ofdisrupting magnetoreception and since the Papi groupalso attached satellite transmitters on the heads of severalcontrol turtles that re-analyzing the Papi study using onlyturtles with satellite transmitters placed on the carapace

Levitt et al EMF and wildlife 49

like the Luschi study could show evidence consistent withthe hypothesis that adult turtles exploit magnetic cues innavigation He concluded that sea turtles like all otheranimals studied to date likely exploit multiple cues fornavigation since even with artificial magnetic disturbancecausing impaired performance themagnets in either studydid not prevent turtles from eventually reaching theirtarget beaches This implies that turtles can also rely onother sources of information [570 571] such as celestialcompasses wave direction [572] or olfactory cues likeother species mdash a significant finding

The sum total of the studies mentioned above is thatsea turtle species are highly sensitive to Earthrsquos fields andare capable of adapting to subtle anthropogenicdisruption

Turtles RF-EMF

Turtles may also be senstitive to RFR especially duringincubation while on land andor initial hatchling stages ifthey are exposed to anthopogenic RF-EMF that coulddistort the imprintingmemory they use in later life to locatetheir birthsite beaches again For example if a radar orcommunications base station is installed on or near thebeach of a nesting site could that affect the initialldquoimprintingrdquo process Perhaps augment imprinting andmake return easier Or conversely overwhelm the subtleimprinting process at the start and make return impos-sible If the latter is valid such technology could lead toextinction of sensitive species since it interrupts thereproduction process In the very least in sensitive speciesdisorientation might result as discussed above

To characterize the underlying compass mechanismsin turtles Landler et al [92] studied freshwater juvenilesnapping turtlesrsquo (Chelydra serpentine) ability for sponta-neous magnetic alignment to the Earthrsquos geomagneticfields Using exposure to low-level RFR near the Larmorfrequency (12 MHz) that is related to free radical pair for-mation turtles were first introduced to the testing envi-ronment without the presence of RFR (ldquoRF off RF offrdquo) andthey were found to consistently align toward magneticnorth But when subsequent magnetic testing conditionswere initially free of RFR then included an introducedsignal (ldquoRF off RF onrdquo) they became disoriented Thusintroduction of a RFR field could affect the turtlesrsquo align-ment response to the natural magnetic field The RFR fieldusedwas only 30ndash52 nT (143MHz) In the following reversescenario when the turtles were initially introduced to thetesting environment with RFR present but then removed(ldquoRF on RF offrdquo) they became disoriented when tested

without RFR And with RFR on in both cases (ldquoRF on RFonrdquo) they aligned in the opposite direction toward mag-netic south Clearly test turtles were affected by the expo-sures The researchers concluded that the sensitivity of thespontaneous magnetic alignment response of the turtles toRFR was consistent with a radical pair mechanism (seeldquoMechanismsrdquo above) In addition they concluded that theeffect of RFR appeared to result from a change in thepattern of magnetic input rather than elimination ofmagnetic input altogether Their findings indicated thatturtles when first exposed to a novel environment form alasting association between the pattern of magnetic inputand their surroundings and that they may form a largerinternal GPS-like mapping ability when theymeet any newmagnetic reference framework based on natural magneticcues from multiple sites and localities

They also showed that RFR at or near the Larmor fre-quency (12ndash143 MHz) had the ability to disrupt snappingturtle natural orientation establish its own novel orienta-tion and completely reverse a natural orientation leadingback to the complex questions asked above regardingimprinting and possible reproductive disruption Althoughthe Landler et al study [92] was conducted in a freshwaternon-homing species snapping turtles are long-lived with alow reproduction success rate Even small disruptions tothis species from anthropogenic sources could have anoutsized population effect over time If this freshwaterspecies is any indication of potential RFR effects re-searchers need to further investigate RFR in long-distancemigrating turtle species that imprint on landWe simply donot know the full range of possible effects across fre-quencies with which turtle species come in contact atvulnerable points throughout development and lifetimes

Nematodes and smaller biota

There are reports of sensitivity to EMF in lesser taxa aswellEMF is known to affect numerous other species includingnematodes (Earth and aquatic worms) mollusks (snails)amoeba (single-celled organisms) molds algae pro-tozoans yeast fungi bacteria and viruses (to a limitedextent) mdash with ramifications for creation of antibioticresistant bacteria strains Below are some representativeexamples of observed effects

Nematodes

Common soil-based nematode species like C elegans serveas a useful whole-organism model for genetic and

50 Levitt et al EMF and wildlife

multicellular organism investigations They are routinelyused as a research model to investigate key biologicalprocesses including aging neural system functioning andmuscle degeneration to name a few This speciesrsquo geneticand phenotypic traits are extremely well documented andthey can thus be used as important proxies for quantitativeanalyses [573] Nematodes have a short lifespan are her-maphrodites and demonstrate effects quickly As labmodels they are used primarily for information that can beapplied to humans but we can also glean important in-formation and extrapolate to environmental exposuresunder certain circumstances Healthy soil worm pop-ulations are critical to soil health upon which we alldepend

Hung et al [574] investigated static magnetic field(SMF) effects on life span and premature aging inC elegans Nematodes were grown in SMFs varying from0 to 200 mT They found that SMFrsquos accelerated develop-ment and reduced lifespan in wild-type nematodes Theyalso found increases in heat shock proteins that were se-lective and dose dependent

Vidal-Gadea et al [66] investigated magnetic orienta-tion in C elegans to identify magnetosensory neurons andfound that they orient to the Earthrsquos geomagnetic fieldduring vertical burrowing migrations Well-fed wormsmigrated up while starved worms migrated down Pop-ulations isolated from around the world were found tomigrate at angles to the magnetic vector that would verti-cally translate to their native soil with northern- andsouthern-hemisphere worms displaying opposite migra-tory preferences in conjunction with natural geomagneticfields They also found that magnetic orientation and ver-ticalmigrations required the TAX-4 cyclic nucleotide-gatedion channel in the AFD sensory neuron pair while calciumimaging showed that these neurons respond to magneticfields even without synaptic input They hypothesized thatC elegans may have adapted magnetic orientation tosimplify their vertical burrowingmigration by reducing theorientation task from three dimensions to one

C elegans have also demonstrated sensitivity to elec-tric fields via electrotaxis (also known as galvanotaxis)which is the directed motion of living cells or organismsguided by an electric field or current and often seen inwound healing Sukul and Croll [575] found that nema-todes exposed to an electrical current (002ndash004 mA po-tential differences 2ndash6 V) demonstrated a directionalsensorily-mediated orientation toward the current at firstbut at 2mm from the electrode individualworms increasedreversing behaviors which then remained uniform as theymoved in a constant direction parallel to the exposure Afew which did not reverse direction died (presumably from

electrocution) at 6 V or 04 mA They concluded that adultC elegans move directionally at selected combinations ofvoltage and potential differences and that electrophoresiscould be eliminated

Gabel et al [576] also investigated electric field effectson directionality on C elegans with an eye toward betterunderstanding how the nervous system transforms sensoryinputs into motor outputs They used time-varying electricfields modulated at 100 Hz across an agar surface with adefined direction and amplitude up to 25 Vcm They foundthat the nematodes deliberately crawl toward the negativepole in an electric field at specific angles to the direction ofthe electric field in persistent forward movements with thepreferred angle proportional to field strength They alsofound that the nematodes orient in response to time-varying electric fields by using sudden turns and reversals(normal reorientation maneuvers) They also found thatcertain mutations or laser ablation that disrupt the struc-ture and function of amphid sensory neurons also dis-rupted their electrosensory behavior and that specificneurons are sensitive to the direction and strength ofelectric fields via intracellular calcium dynamics amongthe amphid sensory neurons This study showed thatelectrosensory behavior is crucial to how the C elegansnervous system navigates and can be disrupted at someintensities found in the environment

Maniere et al [573] also found Celegans was sensitiveto electric fields and that when submitted to a moderateelectric field worms move steadily along straight trajec-tories They hypothesized that imposing electric fields inresearch settings was an inexpensive method to measurewormsrsquo crawling velocities and a method to get them toself-sort quickly by taking advantage of their electrotacticskills

An early RFR study of C elegans by Daniells et al [577]found this species to be a useful model for investigatingstress-responses In the majority of investigations theyused 750 MHz with a nominal power of 27 dBm controlswere shielded and all temperatures were strictlycontrolled Stress responses were measured in terms ofbeta-galactosidase (reporter) induction above controllevels Response to continuous microwave radiationshowed significant differences from 25 degrees C in con-trols at 2 and 16 h but not at 4 or 8 h Using a 5 times 5multiwellplate array exposed for 2 h the 25 microwaved samplesshowed highly significant responses compared with asimilar control array Experiments in which the frequencyandor power settings were varied suggested a greaterresponse at 21 than at 27 dBm both at 750 and 300 MHzindicating a nonlinear effect although extremely variableresponses were observed at 24 dBm and 750 MHz Lower

Levitt et al EMF and wildlife 51

power levels tended to induce greater responses mdash theopposite of simple heating effects They concluded thatmicrowave radiation causes measurable stress to trans-genic nematodes via increased levels of protein damagewithin cells at nonthermal levels

Tkalec et al [578] found oxidative and genotoxic ef-fects in earthworms (Eisenia fetida) exposed in vivo to RFRat 900 MHz at 10 23 41 and 120 V m(-1) for 2 h using aGigahertz Transversal Electromagnetic (GTEM) cell Allexposures induced significant effects with modulationincreasing such effects Their results also indicated anti-oxidant stress response induction with enhanced catalaseand glutathione reductase activity indicating lipid andprotein oxidative damage Antioxidant responses anddamage to lipids proteins and DNA differed depending onEMF level modulation and exposure duration

Aquatic and semi-aquatic worm species also showsensitivity to EMF Jakubowska et al [579] investigatedbehavioral and bioenergetic effects of EMF at 50 Hz 1 mTfields (comparable to exposures near underwater cables) inpolychaete ragworms (Hediste diversicolor) that live andburrow in the sandmudof beaches andestuaries in intertidalareas of the North Atlantic While they found no attraction oravoidancebehavior toEMFburrowingactivitywasenhancedwith EMF exposure indicating a stimulatory effect Foodconsumption and respiration rates were unaffected butammonia excretion rate was significantly reduced inEMF-exposed animals compared to control conditions at onlygeomagnetic fields The mechanisms remained unclear Theauthors said this was the first study to demonstrate effects ofenvironmentally realistic EMF values on the behavior andphysiology of marine invertebrates

Van Huizen et al [67] investigated effects of weakmagnetic fields (WMF) on stem-cells and regeneration inan in vivomodel using free-swimming flatworms (Planariassp) that are capable of regenerating all tissues includingthe central nervous system and brain This regenerationability is due to the fact that about 25 of all their cells areadult stem cells (ASC) Injury is followed by a systemicproliferative ASC response that initially peaks at sim 4 hfollowed by ASC migration to the wound site over the first72 h when a second mitotic peak occurs Like salamanderregeneration (see ldquoAmphibiansrdquo above) this activity pro-duces a blastema mdash a group of ASC cell growth that formsthe core of new tissues Full regeneration of damagedplanaria tissues or organs occurs through new tissuegrowth and apototic remodelingscaling of old tissueswithin 2ndash3 weeks Following amputation above and belowthe pharynx (feeding tube) they exposed amputation sitesto 200 μTWMF At three days post-amputation they foundthat 200 μT exposure produced significantly reduced

blastema sizes compared to both untreated and earth-normal 45 μT field strength controls indicating a WMFinterference effect to regeneration They also found that the200 μT exposure was required early and had to be main-tained throughout blastema formation to affect growthand that shorter single-day exposures failed to affect blas-tema size In addition they found weak magnetic fieldsproduced field strengthndashdependent effects These includedsignificant reductions of blastema size observed from 100ndash400 μT but conversely a significant increase in outgrowthoccurred at 500 μT They hypothesized thatWMFeffects werecausedbyaltered reactive oxygen species (ROS) levelswhichpeak at the wound site around 1-h post-amputation and arerequired for planarian blastema formation This study showsthat weak anthropogenic magnetic fields can affect stem cellproliferation and subsequent differentiation in a regenerativespecies and that field strength can increase or decrease newtissue formation in vivo This is a significant finding forregenerating species of all kinds and may affect non-regenerating species as well Sea lamprey eels (Petromyzonmarinus) a fish species are also known to regenerate evenafter multiple amputations [580]

Mollusks amoeba molds algaeprotozoans

Mollusks (marine versions are called chitons) are longknownto manufacture magnetite in their teeth and to use fieldsweaker than the geomagnetic field for kinetic movement anddirection [52 117 340 524] Lowenstam [118] first discoveredthat magnetite was the major mineral in the teeth of marinechitons thought to give teeth their natural hardness ButRatner [62] discovered chitons use magnetite as a magneticcompass when he found a number of chiton species haveradulae (tongues) that are covered by ferro-magnetic(magnetite) denticles The radulae of Acompapleura gran-ulata and Chiton squamosis were also found to be ferro-magnetic but the shells were not Live specimens of a chiton(Chaetopleura apiculata) that also have ferro-magneticradulae were found to rotate more and move farther in amagnetic field weaker than in the Earthrsquos stronger geomag-netic field indicating a nonlinear directionality Ratnerconcluded that chitons are responsive to magnetic fields anddemonstrate kinetic movements within them

Some snails are sensitive to EMFs Nittby et al [581]observed analygesic effects in land snails (Helix pomatia)caused by GSM-1900 RFRs when snails lost sensitivity topain on a hot plate test after nonthernal exposure to RFR

Smaller organisms have also long shown effects fromEMF Goodman et al [582] found delays in mitotic cell

52 Levitt et al EMF and wildlife

division in slime mold (Physarum polycephalum) withELF-EMF exposures Friend et al [583] found perpendic-ular and parallel elongation of the giant amoeba Chaoschaos (Chaos carolinensis) in alternating electric fields overa wide frequency range (1 Hzndash10 MHz) with characteristicchanges as a function of frequency Marron et al [584]found effects on ATP and oxygen levels in another speciesof slime mold (P polycephalum) after exposures to 60 Hzsinusoidal electric and magnetic fields Luchien et al [585]found a stimulating effect on the productivity of the algalbiomass (Chlorella sorokiniana) for a magnetic field of50 Hz but an inhibitory effect at 15 Hz in these microalgae

Protozoans thought to bemore related to animals thanmicrobes also show sensitivity to EMF Protozoans assingle-celled eukaryotes are generally larger than bacteriawhich are classified as prokaryotes The two organisms arestructurally different bacterial cells lack a nucleus whileprotozoa contain organelles such as mitochondria Bacte-ria generally absorb nutrients through their cell wallswhileprotozoa feed on bacteria tissue and organic matter andcan be both infectious and parasitic These protozoainclude human parasites that cause diseases such asamoebic dysentery malaria giardiasis leishmaniasistrichomoniaisis toxoplasmosis and others Animal speciesare also affected by protozoans which can severely weakenand shorten their lifespans

Rodriguez-de la Fuente et al [586] tested ELF-EMF(60 Hz 20 mT for 72 h) on two infectious protozoans Tri-chomonas vaginalis andGiardia lamblia and found growthalterations in both species which they attributed to alter-ations in cell cycle progression and cellular stress Cam-maerts et al [587] used RFR (GSM 900-MHz at 2 W vscontrol) on protozoans (Paramecium caudatum) and foundindividuals moved more slowly and sinuously than usualand that their physiology was affected Paramecia becamebroader pulse vesicles had difficulty expelling content tothe outside of their cells cilia moved less efficiently andtrichocysts became more visible mdash all effects that indicatepoor functioning or cell membrane damage They hy-pothesized that the first impact of RFR could be to cellmembranes

Clearly there are multiple effects at all levels docu-mented in lower taxa from multi-frequency exposures thatare now found in the environment

Yeast and fungi

Yeast is often used in lab models especially since 1996when a complete genomic sequence of Saccharomycescerevisiae was created In fact it is now considered a

ldquopremiermodelrdquo [588] for eukaryotic cell biology as well ashaving helped establishwhole newfields of inquiry such asldquofunctional genomicsrdquo and ldquosystems biologyrdquowhich focuson the interactions of individual genes and proteins toreveal specific properties of living cells and wholeorganisms

EMF research is rich with studies using yeast modelstoo numerous to fully analyze here However we include asmall sample of recent EMF research with potential sig-nificance to environmental exposures

Lin et al [589] investigated glucose uptake and tran-scriptional gene response to ELF-EMF (50 Hz) and RFR(20 GHz) on several strains of budding yeast (S cerevisiae)Results determined that ELF-EMF and RFR exposure canupregulate the expression of genes involved in glucosetransportation and the tricarboxylic acid (TCA) cycle butnot glycolysis pathways thus showing that such exposurescan affect energy metabolism which is closely related withcellular response to environmental stress Glucose meta-bolism is fundamental to all living cellsrsquo need for energywith related significance to many disease states includingmost cancers

In amagnetic field study byMercado-Saenz et al [590]premature aging and cellular instability were found inyeast (S cerevisiae) exposed to low frequency low in-tensity sinusoidal magnetic fields (SMF continuous expo-sure at 245 mT 50 Hz) and pulsed magnetic fields (PMF15 mT 25 Hz 8 hday) Chronological aging was evaluatedduring 40 days and cellular stability was evaluated by aspontaneous mutation count and the index of respiratorycompetence (IRC) They found exposure to PMF producedaccelerated aging while SMF did not and decreasedmitochondrial mutation during aging was also seen withPMF No alterations in respiratory competence wereobserved for either SMF or PMF exposures They concludedthat exposure to PMF accelerated chronological aging andaltered the spontaneous frequency of mitochondrial mu-tation during the aging process whereas the SMF used hadno effect thus showing abnormal effects on cell activityfrom pulsed exposures

Because yeast cells are known to be sensitive to mag-netic fields some industrial and therapeutic applicationsto human health have been investigated These in-vestigations serve to illuminate what we know about yeastand fungal reactions to EMF in general as well as specificuses For industrial applications Wang et al [591] inves-tigated low level static magnetic fields (SMF) on mold(Aspergillus versicolor) growth which can have high im-pacts on metal corrosion in environmental conditionsconducive to mold growth This is especially problematicin fine electronic circuit boards produced today Using a

Levitt et al EMF and wildlife 53

10 mT static magnetic field (SMF) perpendicular to thesurface of printed circuit boards they found the magneticfield inhibited mold growth and surface corrosion whichwere slowed down unlike control boards without appliedmagnetic fields where mold formed a spore-centeredcorrosion pit that then led to macroscopic regional uni-form corrosion This demonstrated changes in cellsporegrowth at a low intensity exposure that can be found in theenvironment

Also with an eye toward commercial possibilities Sunet al [592] found that a polysaccharide of Irpex lacteus (awhite-rot fungus found widely in the environment whichbreaks down organic materials but also is commerciallyused to treat nephritis in humans) was sensitive to low-intensity ELF-EMF as demonstrated by increased biomassand polysaccharide content as well as inducedmalformedtwists on the sample cell surfaces Polysaccharides arecarbohydrates with a large number of sugar moleculesused as energy sources in living cells They identifiedvarying changes in multiple differentially expressed genesafter exposure to alternating current EMF (50 Hz 35 mT3 h per day for 4 days) They found initial sharp increasesin growth rates in exposed samples that were then markedby significant declines in EMFrsquos influence over timealthough there were also important lasting effects Globalgene expression alterations fromEMF indicated pleiotropiceffects (capable of affecting multiple proteins or catalyzingmultiple reactions) were related to transcription cell pro-liferation cell wall and membrane components aminoacid biosynthesis and metabolism Polysaccharidebiosynthesis and metabolism were also significantlyenriched in the EMF-exposed samples They concludedthat EMF significantly increased amino acid contents andwas therefore deemed a suitable method for increasingfermentation of microorganisms presumably for com-mercial use However the significance of this study toenvironmental exposures relates to the multiple ways thatELF alternating current common to electric power gener-ation changed yeast gene expression There is at least oneclinical case of a different strain of I lacteus taking on a rareinfectious and dangerous quality in an immuno-compromised human [593] The question is can now-ubiquitous ELF-EMF contribute to potentially emergingnew forms of yeast contagion

The same question arises with Candida albicans andother pathogenic yeasts that have rapidly developedresistance to antifungal medications C albicans can liveharmlessly in human microflora but certain lifestyle cir-cumstances or immunosuppression can turn it into anopportunistic pathogen It can also infect somenon-humananimals While chronic mucocutaneous candidiasis can

infect the skin nails and oral and genital mucosae underhigh host immunodeficiency C albicans can enter thebloodstream and induce systemic infections withmortalitybetween 30 and 80 [594] There has been increasingresistance of C albicans to traditional antifungal agentssuch as fluconazole and amphotericin B [595 596] Resis-tance mechanisms include overproduction of membranedrug efflux transporters andor changes in gene expression[597]

Two investigations in search of new therapeutic stra-tegies were conducted using EMF Sztafrowski et al [594]investigated the use of staticmagneticfields (SMF 05 T) onC albicans cultures in the presence of two commonly usedantifungal medications Their aim was to assess whetherSMF had any impact on general viability of C albicanshyphal transition and its susceptibility to fluconazole andamphotericin B They found reduction of C albicans hy-phal length in EMF-exposed samples They also found astatistically significant effect on C albicans viability whenSMF was combined with amphotericin B They hypothe-sized that this synergistic effect may be due to the plasmamembrane binding effects of amphotericin B and that SMFcould influence domain orientation in the plasma mem-brane They concluded with caution that the use of a SMFin antifungal therapy could be a new supporting option fortreating candidas infections

Novickij et al [598] also focused on therapeutic pos-sibilities given the multi-drug resistance and side effects toantifungal therapies Their aim was to optimize theelectroporation-mediated induction of apoptosis usingpulses of varied duration (separately and in combinationwith formic acid treatment) and to identify yeast apoptoticphenotypes They focused on nonthermal nanosecondpulsed electric fields (PEF 3 kV 100 ns ndash 1 ms squarewaveand 250 500 750 ns duration 30 kVcm PEF 50 pulses1 kHz) as a therapeutic alternative andor to enhance ef-fects in combinationwith conventional treatments In threeyeast models S cerevisiae (as control) and drug resistantCandida lusitaniae and Candida guilliermondii they foundthat nanosecondPEF induced apoptosis in all three strainsCombining PEF with a weak formic acid solution improvedinduced apotosis and inactivation efficacy in the majorityof the yeast population Yeast cells showed DNA breaksand other changes They concluded that PEF could be auseful newnon-toxic protocol to treat some fungal diseasesand minimize tissue damage

Choe et al [599] studied ion transportation and stressresponse on a yeast strain (K667) to ELF-EMF (60 Hz01 mT sinusoidal or square waves) specifically investi-gating internal ionic homeostasis via the cell membraneinvolving metal ions and cation transports (cations are

54 Levitt et al EMF and wildlife

ionic species of both atoms and molecules with a positivecharge) They found significantly enhanced intracellularcation concentrations as ELF-EMF exposure timeincreased as well as other changes This study has impli-cations for soil health as yeast can be an integral aspect ofhow healthy organic soil matter is formed They concludedthat EMF and yeast could also play a role in the bioreme-diation processes in metal-polluted environments

Lian et al [600] studied effects of ELF-EMF (50 Hz 0ndash70 mT) and RFR (20 GHz 20 Vm temperature at 30 degCaverage SAR single cell012 Wkg) on two budding yeaststrains (NT64C and SB34) and prion generationpropaga-tion They found under both EMF exposures that de novogeneration and propagation of yeast prions (URE3) wereelevated in both yeast strains The prion elevationincreased over time and effects were dose-dependent Thetranscription and expression levels of heat shock proteinsand chaperoneswere not statistically significantly elevatedafter exposure but levels of reactive oxygen species (ROS)as well as superoxide dismutase (SOD) and catalase (CAT)activities were significantly elevated after short-term butnot long-term exposure This work demonstrated for thefirst time that EMF exposure could elevate the de novogeneration and propagation of yeast prions supporting theresearcherrsquos hypothesis that ROS may play a role in theeffects of EMF on protein misfolding ROS levels alsomediate other broad effects of EMF on cell function Theyconcluded that effects of EMF exposure on ROS levels andprotein folding may initiate a cascade of effects negativelyimpacting many biological processes

The effects of EMF on protein folding cannot be over-stated Proteins must fold into proper three-dimensionalconformations to carry out their specific functionsmdash intactproteins are critical to the existence of all life Misfoldingnot only impairs function but leads to disease Foldinginside of cells does not happen spontaneously but ratherdepends on molecular helpers called chaperones Proteinmisfolding has been implicated in Alzheimerrsquos Parkin-sonrsquos and Huntingtonrsquos diseases among others Thedevastating CreutzfeldtndashJakob disease is caused by prionmisfolding in the brain which causes abnormal signalingin neurons that eventually leads to paralysis and deathWildlife can also suffer from prion diseases such as chronicwasting in deer elk and other cervids and cattle can sufferfrom so-called ldquomad-cowrdquo disease The two studies fromabove [599 600] have implications for how such diseasesare spread through soil with possible links to environ-mental EMFs

It is clear from the above that ELF-EMF and RF-EMFusing multiple signaling characteristics are biologicallyactive in both temporary and permanent ways in yeast

fungi species with wide environmental implications acrossnumerous taxa

Bacteria

Strains of bacteria are known to be magnetotactic and usegeomagnetic fields for direction Blakemore [63] was thefirst to suggest in 1973 that bacteria in North Americansaltwater marsh muds use magnetite as a sensor when hediscovered not only that bacteria were highly attracted toan external magnet but they also had magnetite crystalsthat caused them to align with the lines of the Earthrsquosmagnetic fields This was also discovered to be geo-location specific to the North Pole in northern samples andSouth Pole-seeking in southern species [52 63 511] Thebacteria showed ldquomud-uprdquo and ldquomud-downrdquo behavioralong magnetic field gradients when mud was disturbedindicating a magnetic compass Since that early work awhole new field called electromicrobiology has developedwith discoveries that include some electro-active bacteriabeing responsible for magnetite formation with otherscreating their own electric ldquowiresrdquo in mud flats with im-plications for new technologies [601]

Among the more troubling EMF effects are bacterial al-terations with pressing implications for antibiotic resistanceSince the 1940s [602] nonthermal effects were documentedin bacterial viral and tissue cultures with applied low-repetition 20-MHz pulses Most studies spanning the 1940sthough the 1980s focused on EMFrsquos ability to kill microbesand fungi in human food sources at high intensity conse-quently most research was focused on thermal intensitiesThat work still continues today as microwaves have beenshown to be an efficient means for killing microbes [50] Butmicrobes also react to much lower nonlethal intensities andrecent work finds effects from both ELF and RFR

The common bacteria Escherichia coli which can liveharmlessly in the gut of humans and many other animalspecies can also turn virulent and kill through food-borneillnesses E coli comes inmany strains is well studied andnow considered the most genetically and physiologicallycharacterized bacterium E coli encounter varied andnumerous environmental stressors during growth sur-vival and infection including heat cold changes in Phlevels availability of foodwater supplies and EMF Alongwith other bacteria they respond by activating groups ofgenes and heat shock proteins (see ldquoMechanismsrdquo above)which can eventually lead to stress tolerance for survivalpurposes But induced stress tolerance can also lead toincreased virulence as well as enhanced tolerance to otherstressors that confer cross‐protection [603]

Levitt et al EMF and wildlife 55

Salmen and colleagues [604 605] published papers ofEMF effects on bacterial strains documenting the growinginvestigation of microbes related to antibiotic resistancewith many findings stressing responses to EMF [606ndash610]Cellini et al [611] investigated E colirsquos adaptability toenvironmental stress induced by ELF exposures to 50-Hzmagnetic fields at low intensities (01 05 10mT) vs shamcontrols They found exposed samples and controls dis-played similar total and culturable counts but increasedcell viability was observed in exposed samples re-incubated for 24 h outside of the test solenoid comparedto controls Exposure to 50 Hz EMF (20ndash120 min) alsoproduced a significant change in E colimorphotype with apresence of coccoid cells aggregated in clusters after re-incubation of 24 h outside of the magnetic field-solenoidAtypically lengthened bacterial forms were also notedindicating probable alteration during cell division Somedifferences in RNA-AFLP analysis were also seen for allintensities evaluated They concluded that exposure to50-Hz ELF-EMF is a bacterial stressor as evidenced by itsimmediate response in modifying morphology (frombacillary to coccoid) and inducing phenotypical and tran-scriptional changes Despite this stressor effect it was alsoseen that exposed samples significantly increasedviability suggesting the presence of VBNC cells Theyconcluded that further studies were needed to better un-derstand ELF-EMF in bacterial cell organization They didnot extrapolate to the obviousmdash that E coliwas changed inan abnormal way but nevertheless strengthened inviability mdash a recipe for antibiotic resistance

Crabtree et al [612] in a small human study investi-gated the biomic relationship of human bacteria exposed toboth static magnetic fields (SMF) and RFR Using laboratoryculture strains and isolates of skin bacteria collected fromthe hand cheek and chin areas of four volunteers who haddifferent (self-reported) cell phone use histories they foundvaried growth patterns of E coli Pseudomonas aeruginosaand Staphylococcus epidermidis under static magnetic fieldson different bacterial species Isolates of skin microbiotashowed inconsistent growth among the test subjects likelydue to their differing cell phone usage histories (classified asheavymediumand light) andother variables The growthofStaphylococci was increased under RFR in certain in-dividuals while in others growth was suppressed This wascomplicated by the different body areas tested some withhigher chronic exposures such as the hands aswell as othervariables when one test subject used an antibacterial facewash Volunteers in the heavy use category showed lessbacterial growth on the hands possibly due to microbehabituation Overall and despite the small sample theyconcluded RFR can disrupt the balance in skin microbiota

making it more vulnerable to infection by specific opportu-nistic andor other foreign pathogens They noted that bothSMF and RF-EMFs have significant but variable effects onthe growth of common human bacteria that bacterialgrowth was either unaffected increased or suppresseddepending on the species of bacteria and that bacterial re-sponses seemed to be determined by historic exposure toRF-EMF and life style This study even with inherent limi-tations indicates changes in microbes with EMFs and mayprove a novel way to study bacteria with significance forreal-life exposures to humans and animals alike

Salmen et al [605] also found highly variable resultsfromRFR (900 and 1800MHz) effects onDNA growth rateand antibiotic susceptibility in Staphylococcus aureusStaphylococcus epidermidis and P aeruginosa Using anactive cell phone handset they exposed bacteria to 900and 1800 MHz for 2 h then injected samples into a newmedium where growth rate and antibiotic susceptibilitywere evaluated Regarding DNA they found no differencesin S aureus and S epidermidis when exposed to 900 and1800 MHz vs controls but P aeruginosa showed changesinDNAbandpatterns following such exposures Regardinggrowth rates with the exception of a significant decreaseafter 12 h exposure to 900 MHz no significant effects ongrowth of S aureus and S epidermidis were seen But thegrowth of P aeruginosa was significantly reducedfollowing exposure for 10 and 12 h to 900 MHz while nosignificant reduction in growth followed exposure to1800 MHz Regarding antibiotic susceptibility in thedrugs studied (ie amoxicillin 30 mg azithromycin 15 mgchloramphenicol 10 mg and ciprofloxacin 5 mg) with theexception of S aureus treated with amoxicillin (30 mg)EMF-exposure had no significant effect on bacterialsensitivity to antibiotics This study shows variabilityamong bacterial species not only to different frequenciescommon in the environment today but also to changes insensitivity to some antibiotics but not others There mayhave been design problems with this study however

Several studies investigated WiFi signals on bacterialstrains Taheri et al [610] assessed exposure to 900-MHzGSM mobile phone radiation and 24-GHz RFR from com-mon WiFi routers to see if cultures of Listeria mono-cytogenes and E coli resulted in altered susceptibility to 10different antibiotics They found narrowwindows in whichmicrobes became more resistant For L monocytogenes nosignificant changes in antibacterial activity betweenexposed and nonexposed samples mdash except for Tetracy-cline (Doxycycline) mdash were noted For E coli howeverthere was a significant change in antimicrobial activitiessuggesting RFR exposures can influence antibiotic sus-ceptibility of E coli more than in Listeria For window and

56 Levitt et al EMF and wildlife

pronounced effects they found L monocytogenes exhibi-ted different responses to each antibiotic For Doxycyclinethe window occurred after 6 h exposure toWiFi andmobilephone-RFR After 9 h of exposure to WiFi for Ciprofloxacinand Sulfonamide (Tremethoprinsulfamethoxazole) bac-teria tended to become more resistant By contrast thepattern for Levofloxacin and Penicillin (CefotaximeDef-triaxone) showed increased sensitivity For Ecoli thepattern of the response to WiFi and mobile phone RFR wasthe same maximum antibiotic resistance was seen be-tween 6 and 9 h of exposure but after 12 h a stress responselead to a return to preexposure conditions indicating anadaptive reaction Taheri et al [609] found similarnonlinearwindoweffects anddifferences in growth rates inKlebsiella pneumonia while Mortazavi et al [613] foundsimilar window effects in E coli In addition they saw sig-nificant increased growth rates after radiation exposures inboth Gram-negative E coli and Gram-positiveL monocytogenes They concluded that such window ef-fects can be determined by intensity and dose rate thatexposure to RFR within a narrow window can make mi-croorganisms resistant to antibiotics and that this adap-tive phenomenon is a human health threat The same canbe inferred for many non-human species

Said-Salman et al [614] evaluated non-thermal effectsofWiFi at 24 GHz for 24 and 48 h (using aWiFi router as thesource) on the pathogenic bacterial strains E coli 0157H7S aureus and S epidermis for antibiotic resistancemotility metabolic activity and biofilm formation Resultsfound that WiFi exposure altered motility and antibioticsusceptibility of E coli but there was no effect on S aureusand S epidermis However exposed cells (vs unexposedcontrols) showed an increased metabolic activity and bio-film formation ability in E coli S aureus and S epidermisThey concluded that WiFi exposure acted as a bacterialstressor by increasing antibiotic resistance and motility ofE coli as well as enhancing biofilm formation in all strainsstudied They indicated the findingsmay have implicationsfor the management of serious bacterial infections

Movahedi et al [615] also investigated antibioticresistance using short-term exposure to RFR from amobilephone simulator (900 MHz 24 h) on P aeruginosa andS aureus against 11 antibiotics They found significantchanges in structural properties and resistance to thenumerous antibiotics studied P aeruginosa was resistantto all antibiotics after 24 h of exposure vs non-exposedcontrols while S aureus bacteria were resistant to about50 They also found structural changes in all exposedsamples and increased cell wall permeability

In a field study near cell towers Sharma et al [616]looked at changes in microbial diversity and antibiotic

resistance patterns in soil samples taken near four differentbase stations with control samples taken gt300 m awayStenotrophomonas maltophilia Chryseobacterium gleumand Kocuria rosea were isolated and identified in soilsamples collected near the exposed zones They foundgreater antibiotic resistance in microbes from soil nearbase stations compared to controls with a statisticallysignificant difference in the pattern of antibiotic resistancefound with nalidixic acid and cefixime when used asantimicrobial agents They concluded that cell tower ra-diation can significantly alter the vital systems in microbesand make them multi-drug resistant

Researchers have also investigated ELF-EMF effects onbacterial growth and antibiotic sensitivity Segatore et al[608] investigated 2 mT 50 Hz exposures on E coli ATCC25922 and P aeruginosa ATCC 27853 and found EMFsignificantly influenced the growth rate of both strainsnotably at 4 6 and 8 h of incubation The number of cellswas significantly decreased in exposed bacteria vs con-trols And at 24 h incubation the percentage of cellsincreased (P aeruginosa sim 42 E coli sim 5) in treatedgroups vs controls which suggested to the researchers aprogressive adaptive response However they saw noremarkable change in antibiotic sensitivity Potenza at al[617] also found effects at high-intensity static magneticfields at 300 mT on growth and gene expression in Ecolibut that would be a high environmental exposure

Viruses

There is a paucity of research on viral species and EMFlikely due to the fact that viruses lack ferromagnetic ma-terials are difficult to study and donrsquot make good generallab models other than to investigate their direct impact onspecific in vivo end points Virology research thrives in itsown specialized niche and has not been used for basicmodeling like so many other living life forms as notedthroughout this paper There is long-standing debate onwhether viruses are even alive

However one wide-ranging discussion by Zaporozhanand Ponomarenko [618] hypothesized a possible complexmechanistic link between influenza pandemics naturalsun spot cycles and non-thermal effects of weak magneticfields via cryptochromesradical pairs gene expressionpathways and stress-induced host immunological alter-ations favorable to influenza epidemics Noting thatmost mdash though not all mdash major influenza epidemicsoccurred in time intervals starting 2ndash3 years before andending 2ndash3 years after maximum solar activity they hy-pothesized that solar cycles are able to both regulate and

Levitt et al EMF and wildlife 57

entrain processes of biological microevolution in viralspecies (among others) as well as influence human bio-rhythms in synergistic ways that could lead to influenzaepidemics Although others have also noted links betweeninfluenza pandemics and sunspot activity mdash possiblybased on changes in migratory bird patterns as viral vec-tors [619ndash621]mdash and some have linked sun spots with otheradverse human health events these effects remain of in-terest but are still hypothetical UV radiation which is notcovered in this paper is known to suppress cell-mediatedimmunity and is therefore capable of adversely affectingthe course of a viral infection in some mammal speciesAmbient EMF in lower frequency ranges may also bereducing immune viability across species which cantheoretically foster opportunistic virulence Far more EMFresearch needs to be conducted on viruses one fruitfulapproach might be synergistic investigations in virus-infected plant species

The previous studies of microbes show a pattern ofsensitivity inmicroorganisms to EMFwith associations thatencompass a wide range of critical changes includingconsistent stress responses alterations in growth andviability cell membrane alterations and clear patterns ofhow easily antibiotic resistance forms in microbial life tonow ubiquitous EMF levels

Plants (see Part 2 Supplement 4for a table of flora studies ELF RFR)

Plants have evolved in highly sensitive ways to natural andmanmade EMF in all phases of germination growth andmaturation [31] Magnetoreception which is well docu-mented in animals such as birds has also been describedin plants [622] and plant species can respond to subtlechanges in EMF in the environment including in wholeplant communities [623] They may even lsquocommunicatersquoand gather various kinds of lsquoinformationrsquo via electricalsignals in neuron-like cells in root tips and elsewhere [624]Some hypothesize [625] that a form of vibrational andacoustic sensitivity around 220 Hz may play a role in plantlife although not everyone agrees [626]

Almost all vegetation is subject to complex multi-frequency fields due to their soil-based root systems andhigh water content plus above-ground ambient RFR ex-posures makes plants uniquely susceptible to effects neartransmission towers [623 627] Many EMF studies havefound both growth stimulation as well as dieback Thepresence of numerous RFR-emitters in the German andSwiss Alps is thought to have played a role in the

deforestation there [628] The lsquobrowningrsquo of treetops isoften observed near cell towers especially when water isnear tree root bases [25] Treetops with their high moisturecontent and often thick vegetative canopy are known RFRwaveguides In fact military applications utilize thiscapability in treetops for communication signal propaga-tion in remote areas and for guidance of low-flyingweapons systems [629]

How flora interacts with EMF is still a mystery but aclear pattern has emerged in researching the database forthis paper static ELF-EMF has largely been found benefi-cial to plant and seed growth [630] while RFR is detri-mental Plants clearly have magnetoreception in theirstationary condition The normal ground state of magneticfields for plants is the relatively constant naturalgeomagnetic field that averages between 25 and 65 μTdepending on location and seasonal variations [631] At-mospheric changes such as thunderstorms and lightningcan cause intermittent changes in ambient magnetic fieldsThese activities are also generally associated with rain-water critical to virtually all plant life Plants can detectthese changes and prepare for growth using the upcomingrainfall Trees are seen extending their branches skywardlong before rain actually occurs and such changes matchalterations in tree polarities [632]

There are many studies showing an increase in thegrowth rate in plants such as studies of seed germinationexposed to alternatingmagnetic fields Plants also respondsimilarly to high intensity static magnetic fields This maymean that the physiological mechanism in plants thatcauses magnetic field-induced growth is finely tuned to acertain intensity of magnetic flux Any variation in in-tensity or shape of the ambient magnetic field could acti-vate or hinder this growth mechanism

Lightning for instance generates fast and intenseelectromagnetic pulses (EMP) EMP has consistently beenshown to cause biological effects [633] with just one pulsePlants may have mechanisms so sensitive that they candetect the energy of EMP from kilometers away The pulsecauses a transient change in the environmental magneticfield that may be detected by one or more of the mecha-nisms mentioned in the ldquoMechanismsrdquo section above aswell as discussed below EMPhas been closely investigatedfor military applications for its ability at high intensities todisable electronics While much of the military-supportedresearch finds no biological effects from EMP exposurenon-military supported research does show effects Thisparallels the same findings in industry vs non-industryresearch patterns [165 634]

There is a long history on the study of effects of EMFexposure on plant growth notably the work of the Indian

58 Levitt et al EMF and wildlife

scientist Sir Jagadish Bose (1858ndash1937) who proposed theelectric nature of plant responses to environmental stimuliand studied effects of microwaves on plant tissues andmembrane potentials [635] Interestingly Bose investi-gated the effects of millimeter waves [636] now applicableto 5G technology Bose arguably was a pioneer of wirelesscommunication

Another early pioneer in EMF effects on plants wasHarold Saxon Burr (1889ndash1973) at Yale University whoinvestigated the electric potential of trees in two tree spe-cies (a maple and an elm) located on one property andanother maple tree for comparison growing 40 miles(64 km) away Measurements of numerous parameterswere taken using embedded electrodes that recordedhourly from 1953 to 1961 [637] Simultaneous records oftemperature humidity barometric pressure sunlightmoon cycles sunspot activity weather conditionsatmospheric-potential gradients earth-potential gradi-ents and cosmic rays were correlated with tree potentialsBurr also installed equipment that measured the potentialbetween electrodes in the Earth (about 10 miles apart) andthe potential gradient of the air and found that the air andEarth potentials fluctuated exactly with the phase of thetree potentials although the trees were not always syn-chronous Burr ultimately found that the electrical envi-ronment correlated closely with tree potentials in a kind ofentrainment to diurnal lunar and annual cycles Meteo-rological parameters did not correlate in any immediateway other than when passing thunderstorms elicitedanomalous behavior in the trees in direct parallel to mea-surements with the Earth electrodes This follows the the-ory noted above that plants can sense EMP and takeimmediate information from it

There are no other long-term field studies as detailedas Burrrsquos of magnetic field effects on a plant speciesHowever another field study of RFR in Latvia [638]measured effects directly on trees near the Skrunda RadioLocation Station an early warning radar system thatoperated from 1971 to 1998 The systemoperated in the 156ndash162 MHz frequency range transmitting from four pulsedtwo-way antennas that had operated continuously for over20 years by the time of the study In permanent plots in pineforest stands at varying distances from the radar stationand in control areas tree growth changes were measuredand analyzed using retrospective tree ring data Theyfound a statistically significant negative correlation be-tween the relative additional increment in tree growth andthe intensity of the electric field with the radial growth ofpine trees diminished in all plots exposed to RFR Thedecreased growth began after 1970 which coincided withthe initial operation of the station and was subsequently

observed throughout the period of study The effects ofmany other environmental and anthropogenic factors werealso evaluated but no significant effects on tree growthwere correlated This may have been the first detailed fieldstudy of plants and RFR

Many studies of EMFandplants are today conducted inlaboratories and have often focused on growth promotionto create higher yields of food-producing plants Effects ofstatic EMF pulsed EMF ELF-EMF and RF-EMF have beenreported There are in fact over 200 studies on plants andEMF alone mdash too numerous to review here See Part 2Supplement 4 for a Table of studies on plant seedlings anddevelopment based on the types of EMFrsquos tested

As noted in Supplement 4 and in Halgamuge [627]frequently static and ELF-magnetic fields generallyimprove plant growth whereas RFR retards it This is theopposite of results from animal and animal-cell cultureexperiments in which ELF-MF usually produces the sameeffects as RFR It is interesting to note that Hajnorouzi et al[639] and Radhakrishma et al [640] proposed that MF de-creases environmental stress in plants whereas Vian et al[641 642] considered RFR as a systemic stressor A majormorphological difference between animal andplant cells isthat plant cells have a cell wall that is an active physio-logical organelle which regulates growth and cell divisionand controls cellular communications The cell wall con-tains a considerable amount of water [643] Is it possiblethat absorption of RFR by cell-wall water causes a micro-thermal effect that adversely affects plant cell functionsand even causes cell death whereas thermal effects are notlikely to occur with ELF-EMF exposure

Some plant roots have been found sensitive to bothELF and RFR Belyavskaya [644] found a strong cyto-chemical reaction in pea root cells after exposure to lowlevel magnetic fields Kumar et al [645] found cyto- andgenotoxicity in root meristems of Allium cepa with900-MHz and 1800-MHz RFR Chandel et al [646] studiedcytotoxic and genotoxic activity on DNA integrity in rootmeristems of A cepa using 2100-MHz RFR and foundexposure caused DNA damage with a significant decreasein HDNA accompanied by an increase in TDNA while TMand OTM did not change significantly compared to con-trols Biological effects were dependent on the duration ofexposure with maximum changes seen at 4 h

In a series of studies Stefi et al [647ndash649] investigatedthe effects of long termRFR exposure from the base units ofcommon cordless DECT phone systems (pulsed trans-mission mode 1882 MHz 24 hday 7 dweek) on variousplant species (Arabidopsis thaliana Pinus halepensisGossypium hirsutum respectively) and found structural andbiochemical alterations Compared to controls in Faraday

Levitt et al EMF and wildlife 59

cages exposed plant biomass was greatly reduced and leafstructure was only half as thick Leaves were thinner andpossessed greatly reduced chloroplasts which contributedto overall reduced vitality Root systems were alsoadversely affected They concluded that RFR is a stressorandnoxious to plant life A study of similar design [650] didnot find the same effects on maize (Zea mays) which theyattributed to that plantrsquos structural differences althoughchloroplasts were severely affected (see also Kumar et al[651])

Jayasanka and Asaeda [652] published a lengthy re-view that focused on microwave effects in plants Studiesindicate effects depend on the plant family and growthstage involved and exposure duration frequency andpower density among other factors They concluded thateven for short exposure periods (lt15 min to a few hours)nonthermal effects were seen that can persist for long pe-riods even if initial exposures were very short In additionthey noted that since base stations operate 24 hdayneither short exposures nor recovery periods are possiblein natural habitats as plants are continuously exposedthroughout their life cycles They said that variations in thepower density and frequency of microwaves exert complexinfluences on plants and that clearly diverse plant speciesrespond differently to such factors They concluded it isnecessary to rethink the exposure guidelines that currentlydo not take nonthermal effects into consideration

There are numerous reports of adverse RFR effects onmature flora Waldman-Salsam et al [653] reported leafdamage in trees near mobile phone towersmasts In adetailed long-termfieldmonitoring study from2006 to 2015in two German cities they found unusual and unexplain-able tree damage on the sides of trees facing the towers andcorrelated it to RFR measurements vs control areaswithout exposures They found that tree-side differences inmeasured values of power flux density corresponded totree-side differences in damage Controls which consistedof 30 selected trees in low radiation areas without visualcontact to any phone mast and power flux density under50 μWm2 showed no damage They concluded thatnonthermal RFR from mobile phone towers is harmful totrees and that damage that affects one side eventuallyspreads to the whole tree

Vian et al [642] published a review of plant in-teractions with high frequency RFR between 300 MHz and3 GHz and noted that reports at the cellular molecular andwhole plant scale included numerous modified metabolicactivities (reactive oxygen species metabolism α- andβ-amylase Krebs cycle pentose phosphate pathwaychlorophyll content and terpene emission among others)altered gene expression (calmodulin calcium-dependent

protein kinase and proteinase inhibitor) and reducedgrowth (stem elongation and dry weight) after nonthermalRFR exposure They said changes occur in directly exposedtissues as well as systemically in distant tissues and pro-posed that high-frequency RFR be considered a genuineenvironmental factor highly capable of evoking changes inplant metabolism

Halgamuge [627] also published a review that foundweak non-thermal RFR affects living plants The authoranalyzed data from 45 peer-reviewed studies of 29 differentplant species from 1996 to 2016 that described 169 experi-mental observations of physiological and morphologicalchanges The review concluded that the data substantiatedthat RFR showed physiological andor morphological ef-fects (899 plt0001) The results also demonstrated thatmaize roselle pea fenugreek duckweeds tomato onionsand mungbean plants are highly sensitive to RFR and thatplants appear more responsive to certain frequencies be-tween 800 and 1500MHz (plt00001) 1500 and 2400MHz(p 00001) and 3500 and 8000 MHz (p=00161) Hal-gamuge [627] concluded that the literature shows signifi-cant trends of RFR influence on plants

There is particular concern for impacts to flora and 5Gsince millions of small antennas mounted on utility polestransmitting in MMW and other broadband frequenciesalready are mdash or will soon be mdash in very close proximity tovegetation creating both near- and -far field exposures Asnoted in Halgamuge [627] the following are some studiesinvestigating GHz frequencies already in use or planned for5G that found significant effects on plants Tanner andRomero-Sierra [654] on accelerated growth ofMimosa plant(10 GHz 190 mWcm2 5ndash10 min) Scialabba and Tambur-ello [655] on reduced hypocotyls growth rate in radish(Raphanus sativus) (105 GHz 8 mW or 12658 GHz 14 mWfor 96 h) Tafforeau et al [656] induced meristem (activelydividing group of cells) production in Linum usitatissimum(105 GHz for 2 h at 01 mWcm2) and Ragha et al [657](96 GHz 30 min) found germination depended on expo-sure parameters on Vigna radiata Vigna aconitifolia Cicerarietinum and Triticum aestivum plants This is an area inimmediate need of further investigation given the resultsfrom the previous studies

A thorough review of RFR effects to trees and otherplants was published by Czerwinski et al [622] who re-ported that ecological effects on whole plant communitiescould occur at a very low exposure level of 001ndash10 μWcm2 mdash certainly comparable to limits examined in thispaper They focused on frequencies between 07 and18 GHz and includedmultiple complex indicators for planttypes biometrics and environmental factors It was thefirst comprehensive paper that extended beyond using

60 Levitt et al EMF and wildlife

narrower research methods They noted that although theliterature on the effects of RFR on plants is extensive not asingle field study had assessed the biological response atthe level of awhole plant community biome or ecosystembut rather focused mostly on short-term laboratory studiesconducted on single species They said ldquohellipThis disso-nance is particularly striking in view of the fact that alter-ations in a plant communityrsquos structure and compositionhave long been considered to be well founded sensitiveand universal environmental indicatorsrdquo The paper servesas a predictive model for complex future field studies onlarger ecosystems

Interesting EMF synergistic effects were found withstatic magnetic fields and bacteria in plants Seeking non-chemical methods to improve seed germination after pro-longed periods of storage when seed viability can deteri-orate Jovičić-Petrović et al [658] studied the combinedeffects of bacterial inoculation (Bacillus amyloliquefaciensD5 ARV) and static magnetic fields (SMF 90 mT 5 and15 min) on white mustard (Sinapis alba L) seeds Theirresults found that biopriming with the plant growth-promoting B amyloliquefaciens increased seed growth by4043 Seed response to SMF alone was dependent ontreatment duration While SMF at 5 min increased thegermination percentage exposure at 15 min lowered seedgermination compared with the control However thenegative effect at the longer exposure was neutralizedwhen combined with the bacterial inoculation Bothgermination percentages were significantly higher whenSMF was combined with the bacteria (SMF 5 min + D5ARV and SMF 15 min + D5 ARV 4468 and 5320respectively) compared with control They concluded thatbiopriming and SMF treatment gave better results thanbacterial inoculation alone The highest germination per-centagemdash 5320of germinated seedsmdashwas seenwith thebacterium and 15 min exposure to 90 mT demonstrating asynergistic effect They concluded that such techniquescan be used for old seed revitalization and improvedgermination

Even aquatic plants have been found sensitive toartificial electric fields Klink et al [659] assessed electricfield exposures on growth rates and the content of tracemetals of Elodea canadensis Plants were exposed in alaboratory to an electric field of 54 kVm for seven daysPlant length and Fe Mn Ni Pb and Zn were measuredResults showed the applied electric fields slightlyenhanced root growth They also found changes inmineralabsorption Mn and Ni were significantly lower while Pband Zn were significantly higher in exposed plants Fecontent did not differ between control and exposed plantsThey concluded that electric fields had potential use for

phytoremediation in tracemetal contaminatedwaters Thisstudy also has implications for long term aquatic planthealth in general

Alsoworkingwith electric fields Kral et al [660] foundfascinating regeneration in plant root tips inArabidopsis atvarying electric field exposures and time durationswith theweaker exposures producing the most growth They foundthat imposed electric fields can perturb apical root regen-eration and that varying the position of the cut and the timeinterval between excision and stimulation made a differ-ence They also found that a brief pulse of an electric fieldparallel to the root could increase by up to two‐fold theprobability of its regeneration perturb the local distribu-tion of the hormone auxin and alter cell division regula-tion with the orientation of the root towards the anode orthe cathode playing a role

While mechanisms are still unclear regarding howEMFs affect plants oxidative effects appear to play a sig-nificant role Oxidative changes have been reported inmany studies in plants after exposure to EMF [578 639661ndash671] EMF-related stress has been proposed by Vianet al [641 642] Roux et al [672 673] and Radhakrishmaet al [640] Other mechanisms affecting plants such asferromagnetism radical-pairs calcium ions and crypto-chromes have also been proposed [674 675]

It is apparent that plant growth and physiologymdashwiththeir root systems anchored in the ground while theirlsquoheadsrsquo manifest in the air mdash are affected by exposure toEMF in complex synergistic ways and that they are sus-ceptible to multi-frequency exposures throughout their lifespans

Conclusion

Effects from both natural and man-made EMF over a widerange of frequencies intensities wave forms andsignaling characteristics have been observed in all speciesof animals and plants investigated The database is nowvoluminous with in vitro in vivo and field studies fromwhich to extrapolate The majority of studies have foundbiological effects at both high and low-intensityman-madeexposures many with implications for wildlife health andviability It is clear that ambient environmental levels arebiologically active in all non-human species which canhave unique physiological mechanisms that require natu-ral geomagnetic information for their lifersquos most importantactivities Sensitive magnetoreception allows living or-ganisms including plants to detect small variations inenvironmental EMF and react immediately as well as overthe long term but it can also make some organisms

Levitt et al EMF and wildlife 61

exquisitely vulnerable to man-made fields AnthropogenicEMFmay be contributing more than we currently realize tospeciesrsquo diminishment and extinction Exposures continueto escalate without understanding EMF as a potentialcausative andor co-factorial agent It is time to recognizeambient EMF as a potential novel stressor to other speciesdesign technology to reduce exposures to as low asreasonably achievable keep systems wired as much aspossible to reduce ambient RFR and create laws accord-ingly mdash a subject explored more thoroughly in Part 3

Research funding None declaredAuthor contributions All authors have acceptedresponsibility for the entire content of this manuscriptand approved its submissionCompeting interests Authors state no conflict of interestInformed consent Not applicableEthical approval Not applicable

Part 2 supplements

Supplement 1 Genetic Effects of RFR ExposureSupplement 2 Genetic Effects at Low Intensity StaticELF EMF ExposureSupplement 3 Biological Effects in Animals and PlantsExposed to Low Intensity RFRSupplement 4 Effects of EMF on plant growth

References

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2 Balser M Wagner CA Measurements of the spectrum of radionoise from 50 to 100 cycles per second 1 J Res Nat Bur Stand DRadio Propag 196064D34ndash42

3 NASA 2021 httpswwwnasagovmission_pagessunearthnewsgalleryschumann-resonancehtml

4 Friedman JS Out of the blue a history of lightening sciencesuperstition and amazing stories of survival NY Delecorte Press2008101 p

5 AdeyWR Electromagnetic fields and the essence of living systemsIn Andersen JB editor Modern radio science New York NY USAOxford University Press 19901ndash37 pp

6 Becker RO Cross currents the perils of electropollution thepromise of electromedicine Los Angeles USA Jeremy Tarcher199067ndash81 pp

7 Levitt BB Electromagnetic fields A consumerrsquos guide to the issuesand how to protect ourselves Orlando FL USA First editionHarcourt Brace and Co 1995 iUniverse Authors GuildBackinprintcom edition 2007 Lincoln NE USA

8 Levitt BB Moving beyond public policy paralysis InClements-Croome D editor Electromagnetic environments and

health in buildings NewYork NY USA Spon Press 2004501ndash18pp

9 Manzella N Bracci M Ciarapica V Staffolani S Strafella ERapisarda V et al Circadian gene expression and extremely low-frequencymagnetic fields an in vitro study Bioelectromagnetics201536294ndash301

10 IUCN 2018 The International Union for Conservation of NatureVersion 2018-1 Red List of Threatened Species 2018

11 Intergovernmental Science and Policy Platform on Biodiversityand Ecosystem Services Paris France (IPBES) In Brondizio ESSettele J Diacuteaz S Ngo HT editors Global assessment report onbiodiversity and ecosystem services of the IntergovernmentalScience-Policy Platform on Biodiversity and Ecosystem ServicesBonn Germany IPBES Secretariat 2019

12 Sanchez-Bayo F Wyckhuys AG Worldwide decline of theentomofauna a review of its drivers Biol Conserv 20192328ndash27

13 Schultz CB Brown LM Pelton E Crone EE Citizen sciencemonitoring demonstrates dramatic declines of monarchbutterflies in western North America Biol Conserv 2017214343ndash6

14 Xerces Society for Invertebrate Conservation 2019Available from httpsxercesorgmonarchs

15 Center for Biological Diversity Monarch butterfly populationdrops by nearly one-third iconic butterfly has declined by morethan 80 percent in recent decades 2017 Available from httpswwwbiologicaldiversityorgnewspress_releases2017monarch-butterfly-02-09-2017php

16 Guerra PA Gegear RJ Reppert SM A magnetic compass aidsmonarch butterfly migration Nat Commun 201454164

17 Marha K Musil J Tuha H Electromagnetic fields and the livingenvironment Praguel Hungary State Health Publishing House1968 (Trans SBN 911302-13-7 San Francisco Press 1971)

18 Ceballos G Garciacutea A Ehrlich PR The sixth extinction crisis lossof animal populations and species J Cosmol 201081821ndash31

19 Ceballos G Ehrlich PR Barnosky AD Garciacutea A Pringle RM PalmerTM Acceleratedmodernhuman-induced species losses enteringthe sixth mass extinction Sci Adv 20151e1400253

20 Ceballos G Ehrlich PR Dirzo R Biological annihilation via theongoing sixth mass extinction signaled by vertebrate populationlosses and declines Proc Natl Acad Sci Unit States Am 2017114E6089ndash96

21 Weimerskirch H Le Bouard F Ryan PG Bost CA Massive declineof the worldrsquos largest king penguin colony at Ile aux CochonsCrozet Anartic Sci 201830236ndash42

22 Manville AM II Impacts to birds and bats due to collisions andelectrocutions from some tall structures in the United States mdashwires towers turbines and solar arrays state of the art inaddressing the problems In Angelici FM editor Problematicwildlife a cross-disciplinary approach New York NY USASpringer International Publishers 2016415ndash42 pp Chap 20

23 Manville AM II Towers turbines power lines and solar arraysthe good the bad and the ugly facing migratory birds and batsmdashsteps to address problems Invited presentation Earth Scienceand Policy Class GEOL 420 GeorgeMasonUniversity 201639 pPowerPoint slides available online

24 Balmori A The effects of microwave radiation on wildlifepreliminary results 2003 Available from httpwwwemrpolicyorglitigationcase_lawbeebe_hillbalmori_wildlife_studypdf

62 Levitt et al EMF and wildlife