simberloff_2000_biotic causes, epidemiology global consequences and control

8/6/2019 Simberloff_2000_Biotic Causes, Epidemiology Global Consequences and Control

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Biotic Invasions: Causes, EpidemiologyBiotic Invasions: Causes, EpidemiologyBiotic Invasions: Causes, EpidemiologyBiotic Invasions: Causes, EpidemiologyBiotic Invasions: Causes, EpidemiologyGlobal Consequences and ControlGlobal Consequences and ControlGlobal Consequences and ControlGlobal Consequences and ControlGlobal Consequences and Control

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Issues in EcologyIssues in EcologyIssues in EcologyIssues in EcologyIssues in Ecology Number 5Number 5Number 5Number 5Number 5 Spring 20 00Spring 20 00Spring 20 00Spring 20 00Spring 2000

Biotic Invasions: Causes, EpidemiologyBiotic Invasions: Causes, EpidemiologyBiotic Invasions: Causes, EpidemiologyBiotic Invasions: Causes, EpidemiologyBiotic Invasions: Causes, Epidemiology,,,,,Global Consequences and ControlGlobal Consequences and ControlGlobal Consequences and ControlGlobal Consequences and ControlGlobal Consequences and Control

SUMMARYSUMMARYSUMMARYSUMMARYSUMMARY

Humans have caused an unprecedented redistribut ion of t he earths living things. Both incidentally and deliberately, t hroughmigration, transport, and commerce, humans are continuing to disperse an ever-increasing array of species across previouslyinsurmountable environmental barriers such as oceans, mountain ranges, rivers, and inhospitable climate zones. Among the mostfar-reaching consequences of t his reshuffl ing is a sharp increase in biot ic invaders species that establish new ranges in whichthey proliferate, spread, and persist to the detriment of native species and ecosystems. In a world wit hout borders, few if anyareas remain sheltered from these immigrations, and for some areas, such as oceanic islands, are subject to high rates of invasion

Despite ubiquit ous arr ivals of new plants, animals and microorganisms, the fate of immigrant s is decidedly mixed. Few survive andonly a small fraction become naturalized. Most that do become naturalized exert no demonstrable impact in their new range.However, some naturalized species do become invasive, and these can cause severe environment al damage. There are severapotential reasons why immigrants succeed: Some escape constraints such as predators or parasites, some find vacant niches tooccupy, some are aided by human-caused disturbance that disrupt s nat ive communit ies. Whatever t he cause, successful invaders

can in many cases inflict enormous ecological damage.

The scientific literature reviewed by the panel makes it clear that:

Animal invaders can cause extinctions of vulnerable native species through predation, grazing, competition, and habitatalteration.

Plant invaders can completely alter the fire regime, nutrient cycling, hydrology, and energy budgets in a native ecosystemgreatly diminish the abundance or survival of native species, and even block navigation or enhance flooding.

Many non-native animals and plants can hybridize with native species.

In agriculture, the principle pests of temperate crops are non-native, and the combined expenses of pest control and croplosses const itute a tax on food, f iber, and forage production.

The global cost of virulent plant and animal diseases caused by organisms transported to new ranges and presented with

susceptible new hosts is currently incalculable.

Identifying future invaders and taking effective steps to prevent their dispersal and establishment is a major challenge to ecologyagriculture, aquaculture, horticult ure and pet t rades, conservation, and international commerce. The panel finds that :

Identifying general attributes of future invaders has proven difficult.

Predicting susceptible locales for future invasions seems even more problematic, given the enormous differences in commerceamong various regions and thus in the rate of arrival of potential invaders.

Eradication of an established invader is rare and control efforts vary enormously in their efficacy. Successful control dependsmore on commitment and continuing diligence than the eff icacy of specific t ools themselves (trapping or spraying insecticidesreleasing biological control agents).

Control of biotic invasions is most effective when it employs a long-term, ecosystem-wide strategy rather than a tactica

approach focused on battling individual invaders. Prevention of invasions is much less costly than post-entry control.

Changing nat ional and international quarantine laws by adopting a guilt y unt il proven innocent approach, instead of t hecurrent strategy of denying entry only to species already proven noxious or detr imental, would be a product ive first step. Theglobal consequences of failing to address the issue of invasions effectively would be severe, including wholesale loss of agriculturalforestry and fishery resources in some regions and disruption of the ecological processes that supply natural services on which thehuman enterprise depends. Given their current scale, biotic invasions have also taken their place alongside human-driven atmo-spheric and oceanic change as major agents of global change, and left unchecked, will influence these other forces in profound but

still unpredictable ways.


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by Richard N. M ack, Chair, Daniel Simberlof f, W. M ark Lonsdale,Harry Evans, Michael Clout, and Fakhri Bazzaz

Biotic Invasions: Causes, EpidemiologyBiotic Invasions: Causes, EpidemiologyBiotic Invasions: Causes, EpidemiologyBiotic Invasions: Causes, EpidemiologyBiotic Invasions: Causes, Epidemiology,,,,,Global Consequences and ControlGlobal Consequences and ControlGlobal Consequences and ControlGlobal Consequences and ControlGlobal Consequences and Control

INTRODUCTIONINTRODUCTIONINTRODUCTIONINTRODUCTIONINTRODUCTION

Biotic invasions can occur when organisms aretransported to new, often distant, ranges where theirdescendants proliferate, spread, and persist. In a str ictsense, invasions are neither novel nor exclusively human-driven phenomena. But the geographic scope, f requency,and the number of species involved have grown enor-mously as a direct consequence of expanding transportand commerce in the past 500 years, and especially inthe past 200 years. Few habitats on earth remain free of

species introduced by humans; far fewer can be consid-ered immune from this dispersal. The species involvedrepresent an array of taxonomic categories and geo-graphic orig ins that defy any ready classificat ion.

The adverse consequences of biotic invasions arediverse and inter-connected. Invaders can alter funda-mental ecological properties such as the dominant spe-cies in a community and an ecosystems physical features,nutrient cycling, and plant productivit y. The aggregate

effects of human-caused invasions threaten efforts toconserve biodiversity, maintain productive agriculturasystems, sustain functioning natural ecosystems, and alsoprot ect human health. We out line below the epidemiology of invasions, hypotheses on the causes of invasionsthe environmental and economic toll they take, and toolsand strategies for reducing this toll.

THE EPIDEMIOLTHE EPIDEMIOLTHE EPIDEMIOLTHE EPIDEMIOLTHE EPIDEM IOLOGY OF INVOGY OF INVOGY OF INVOGY OF INVOGY OF INVASIONSASIONSASIONSASIONSASIONS

Biotic invasions constitute only one outcome -

indeed, the least likely outcome - of a multi-stage pro-cess that begins when organisms are t ransported fromtheir nat ive ranges to new regions. First, many, if notmost, perish en route to a new locale. If they succeed inreaching a new site, immigrants are likely to be destroyedquickly by a mult itude of physical or biot ic agents. It isalmost impossible to obt ain data quant ifying t he numbeof species that are actually dispersed from their nativeranges, the number that subsequently perish, and the num

Figure 1Figure 1Figure 1Figure 1Figure 1 - Some invaders, such as the shrub Lantana camara, have been introduced repeatedly in new ranges, the result sof g lobal human colonizat ion and commerce. As the array of est imated years of int roduct ion indicates, lantana wasintroduced throughout the 19 th and early 20 th century in many new sub-t ropical and tropical ranges. In each new rangeit has become highly destructive, both in agricult ural and natural communit ies (Cronk and Fuller 1 995).


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ber of arrivals. But, given the number of species spottedonly once far beyond their native range, local ext inction ofimmigrants soon after their arrival must be enormous.

Despite such wholesale destruct ion either in t ran-sit or soon after arrival, immigrants occasionally surviveto reproduce. Even then, their descendants may survivefor only a few generations before going extinct locally.Again, however, some small fraction of these immigrant

species do persist and become naturalized. At that point ,their persistence does not depend on recurring, frequentre-immigrat ion from the native range, alt hough a greaternumber and frequency of new arrivals do raise the prob-ability that a species will establish permanently.

Among the naturalized species that persist afterthis extremely severe reductive process, a few will go onto become invaders. An analogy is often made betweenepidemics caused by parasites and all other biotic inva-sions because many important factors in disease epidemi-ology have direct parallels in the study of invasions. Be-

low we explore the epidemiology and underlying mecha-nisms, which allow some species to become invaders.

Humans as Dispersal Agents of Potential InvadersHumans have served as both accidental and de-

liberate dispersal agents for millennia, and the increase inplant, animal, and microbial immigrations worldwideroughly t racks the rise in human transport and commerce.Beginning around 1500, Europeans transported OldWorld species to their new settlements in the Western

Hemisphere and elsewhere. The manifests from Columbus second and subsequent voyages, for instance, indicate deliberate transport of species regarded as potent ial crops and livestock. Global commerce has grownmeteorically since then, providing an opportunity for acorresponding growt h in biot ic invasions. As a resultthese biotic invasions can be viewed as predominantlypost-Columbian events. Put in perspective, the human-driven

movement of organisms over the past 200 to 500 yearsdeliberate and accidental, undoubtedly dwarfs in scope, frequency and impact the movement of organisms by naturaforces in any 500-year period in the earths history.

The proport ion of various types of organisms thathave invaded as a result of accidental versus deliberatemovement clearly varies among taxonomic groups. Few, if any, invasive microorganisms have been delib

erately int roduced. Deliberate microbial int roduct ionshave instead most commonly involved yeasts for fermentation or mutualists, such as mycorrhizal fung

that form symbiotic relationships with the roots ofmost plants.

Among insects, some deliberate introductions havehad adverse consequences, including bumblebees inNew Zealand. But the majorit y of invasive insectshave probably been accidentally introduced.

Introductions of marine invertebrates probably mirror insects. A few species have been deliberately introduced, such as the Pacific oyster imported fromJapan to Washington state, but a growing number of

Figure 2Figure 2Figure 2Figure 2Figure 2 - M any invaders occupy newranges at an accelerating rate with pro-nounced lag and log phases of pro-liferation and spread. This init ial slowrate of range occupation may be indis-tinguishable from the rate of spreaddisplayed by non-invasive (but nevert he-

less non-indigenous) species in a newrange, thus hampering the early identi-ficat ion of future invaders. Terrestrialplant invasions most commonly illus-trate this pattern (e.g. the spread ofOpuntia aurantiaca in South Africa)(Moran and Zimmerman 1991 andsources [numbers 1-9] therein). Bycontrast, invaders in other taxonomicgroups may show no lag in range ex-pansion and rapidly occupy new rangeupon entry.


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invaders such as the zebra mussel have arrived asaccidental contaminants in ship ballast.

In contrast, most invasive vert ebrates, pr incipally fish,mammals, and birds, have been deliberately intro-duced. Some of the worst vert ebrate invaders, how-

ever, have been spread accidentally: rats, brown treesnakes, sea lampreys.

Some invasive plants have been accidentally introducedas contaminants among crop seeds and other cargo.Many, if not most, plant invaders have been deliberatelyintroduced, including some of the worst pests: waterhyacinth, melaleuca trees, and tamarisk or salt cedar.

The prominence of deliberately introduced spe-cies that later become biotic invaders emphasizes thatnot all pests arrive unheralded and inconspicuously; manyare the product of deliberate but disastrously flawed hu-

man forethought (Fig. 1).

The Transformation from Immigrant t o InvaderThe progression from immigrant to invader of ten

entails a delay or lag phase, followed by a phase of rapidexponential increase that continues until the speciesreaches the bounds of its new range and its populationgrowt h rate slackens (Fig. 2). This simplified scenario hasmany variants, of course. First, some invasions such asthose by Afr icanized bees in t he Americas and zebra mus-

sels in the Great Lakes may go through only a brief lagphase, or none at all. On t he other hand, many immigrantspecies do not become abundant and widespread for de-cades, during which t ime they may remain inconspicuousBrazilian pepper trees were introduced to Florida in the

nineteenth century but did not become widely noticeableunti l the early 19 60 s. They are now established on morethan 280,000 hectares in south Florida, often in densestands that exclude all other vegetation (Fig. 3).

During the lag phase, it can be difficult to distinguish doomed populations from future invaders. Most extinctions of immigrant populations occur during the lag phaseyet the dynamics of such a population are often indistin-guishable from those of a future invader, which is growingslowly but inexorably larger. This similarit y in the size andrange frustrates attempts to predict future invaders while

they are few in numbers and presumably controllable.Whether most invasions endure lag phases, and

why they occur, remain conjectural. Any lag in the population growth and range expansion for a potential invademost likely results from several forces and factors operating singly or in combination: The number and arrangement of infestations of immi

grants. Usually invasions proceed fastest among manysmall, widely separated infestations compared with asingle larger one.

FFFFFigure 3igure 3igure 3igure 3igure 3 - Invaders often alter drastically the ecosystems they occupy, over-turning native species composition, as well

as changing the fire frequency, soil chemistry and hydrology. The Florida Everglades have been much altered by thecollective effects of invasive plants, including Schinus terebinthifolius(Brazilian pepper). A) The potential natural com-munit ies across much of the Everglades are composed of small forested hammocks in a matrix of marshes. B) Invasionby Brazilian pepper has radically transformed these ecosystems into virtual monocultures of the invasive tree withdevastating effects on the native biota.

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Limits on the detection of a populat ions growth. Alag could be perceived simply t hrough t he inabilit y t odetect still small and isolated but nonetheless grow-ing populations in a new range.

Natural selection that produces novel genetic typesadapted to the new range. The lag phase would re-flect t ime for emergence of newly adapted genotypes,

although proof of this explanation has proven elusive. Habitat alteration. A lag may simply reflect the t ime

between immigrants entry and the later alterat ion ofhabitat (e.g. the fire regime, livestock, hydrology) thatallowed their descendants to proliferate.

The vagaries of environmental forces. The order, tim-ing, and intensity of environmental hazards are crit i-cal for all populations, but the consequences of con-secutive periods of high mortality are most severeamong small populations. Thus, a small immigrantpopulation could persist or perish largely as a conse-

quence of a lottery-like array of forces across timeand generations: that is, whether t he first years in thenew range are benign or severe; whether environmentalforces combine to destroy breeding-age individualsas well as their offspring.

Clearly, some immigrant populations overcomethese long odds and grow to a threshold size such thatextinction from chance events, demographic or environ-mental, becomes unlikely. One great irony about bioticinvasions is that humans, through cultivation and hus-

bandry, of ten enhance the likelihood that immigrants willreach this threshold and become established. This hus-bandry includes activities that protect small, vulnerablepopulations from environmental hazards such as drought ,flooding, frost , parasites, grazers, and compet itors. Withprolonged human effor t , such crops, flocks, or herds cangrow to a size that is not in imminent danger of extinc-t ion. In fact, the populat ion may no longer require humantending to persist . At t his point, the populat ion has be-come naturalized and may eventually become invasive.Thus, humans act to increase the scope and f requency of

invasions by serving as both effective dispersal agentsand also protectors for immigrant populations, helpingfavored non-native species beat the odds that defeat mostimmigrants in a new range.

At some point, whether after years or decades,populations of a future invader may proceed into a phaseof rapid and accelerating growth, in both numbers andareal spread (Fig. 2). This erupt ion oft en occurs rapidly,and there are many first-hand accounts of invasions thatproceeded through this phase, despite concerted efforts

to control them. Eventually, an invasion reaches its envi-ronmental and geographic limits in the new range, and itspopulat ions persist but do not expand.

IDENTIFYING FUTURE INVIDENTIFYING FUTURE INVIDENTIFYING FUTURE INVIDENTIFYING FUTURE INVIDENTIFYING FUTURE INVADERS ANDADERS ANDADERS ANDADERS ANDADERS ANDVULNERABLE COMMUNITIESVULNERABLE COMMUNITIESVULNERABLE COMMUNITIESVULNERABLE COMMUNITIESVULNERABLE COM M UNITIES

Identifying future invaders and predicting theirlikely sites of invasion are of immense scientific and prac-t ical interest . Scient ifically, learning to identify invadersin advance would tell us a great deal about how life his-tory traits evolve and how biotic communities are assembled. In practical terms, it could reveal the most ef-fective means to prevent f uture invasions. Current hypotheses or generalizations about traits that distinguishboth successful invaders and vulnerable communities alconcern some ext raordinary att ributes or circumstancesof t he species or communit ies. Evaluation of t hese gen

eralizations has been difficult because they rely on post-hoc observation, correlation, and classification rather thanexperiments. Probably no invasions (except some invasions of human parasites) have been tracked closely andquantif ied from their inception. Furt hermore, predict ionsof future invaders and vulnerable communities are inex-tricably linked. How can we know whether a communitysustains an invasion because it is intrinsically vulnerableor because the invader possesses extraordinary att ribut es? Do communit ies with f ew current invaders pos

sess intrinsic resistance or have they been reached so faronly by weak immigrants?

At tributes of InvadersBiologists have long sought to explain why so

few naturalized species become invaders. Int riguinglysome species have invaded several widely separated point son the planet (water hyacinth, European starlings, ratslantana, wild oats) which is the ecological equivalent ofwinning repeatedly in a high-stakes lot tery. Such repeatoffenders, or winners, have sparked the obvious ques

tion: do they and other successful invasive species shareattributes that significantly raise their odds for proliferat ion in a new range?

Many attempts have been made to construct listsof common t rait s shared by successful invaders. The hopebehind such efforts is clear: if we can detect a broad listof t raits that, f or example, invading insects, aquatic vascular plants, or birds share as a group, then perhaps wecan predict the identity of future invaders from these taxonomic groups. Some invaders do appear t o have t rait s in


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common, but so far such lists are generally applicable foronly a small group of species, and exceptions abound.

Relatives of invaders, particularly species in thesame genera, seem to be obvious targets of suspicion aspotential invaders. Many of the worlds worst invasiveplants belong to relatively few families and genera:Asteraceae, Poaceae, Acacia, Mimosa, Cyperus. Both

the starling and crow families have several invasive, or atleast widely naturalized, species. But most biot ic invad-ers have few, if any, similarly aggressive relatives (waterhyacinth, for instance, is the only Eichhorniathat is inva-sive). This fact could simply reflect a lack of opport uni-ties for immigration rather than a lack of talent for inva-sion. But the circumstantial evidence suggests otherwise:guilt by (taxonomic) association has proven imprecise atpredict ing invasive potential.

Community Vulnerability to Invasion

As stated above, attempts to predict relative com-munity vulnerability to invasions have also prompted gen-eralizations, including the following. Vacant niches. Some communities such as tropical

oceanic islands appear to be particularly vulnerableto invasions, alt hough the evidence can be equivocal.The vacant niche hypothesis suggests that island com-

munit ies and some others are relat ively impoverishedin numbers of native species and thus cannot provide biological resistance to newcomers. In contrasthowever, many would-be invaders arriving on islandswould find no pollinators, symbionts, or other requiredassociates among the native organisms, a factor thatmight provide island communities with a different form

of resistance to invasion. Yet actual demonstrationof vacant niches anywhere has proven difficult. Escape from biotic constraints. Many immigrants

arrive in new locales as seeds, spores, eggs, or someother resting stage without their native associatesincluding their usual compet itors, predators, grazersand parasites. This great escape can t ranslate intoa powerful advantage for immigrants. All aspects operformance such as growth, longevity, and fitnesscan be much greater for species in new ranges. According to this hypothesis, an invader persists and

proliferates not because it possesses a suite of extraordinary traits but rather because it has fortuitouslyarrived in a new range without virulent or at leastdebilitating associates. For example, the Australianbrushtail possum has become an invader in NewZealand since its int roduct ion 15 0 years ago. In NewZealand it has fewer competitors for food and shel-

Figure 4Figure 4Figure 4Figure 4Figure 4 - Many invasive grasses have greatly expanded their world-wide ranges at the expense of native grasslandsand forests, usually facilitated by human-induced land-clearing, recurr ing f ire, and livestock grazing. On the island ofHawaii, Pennisetum setaceum(fountain grass) from northern Africa has replaced the nat ive M etrosideros polymorphawoodland (see remnant t rees in background). It resprouts readily after it s litt er is burned; nat ive plants are much lesstolerant and are eventually eliminated from these sites.

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ter, no native microparasites, and only 14 species ofmacroparasites, compared wit h 76 in Australia. It spopulation densities in New Zealand forests are ten-fold greater than those prevailing in Australia. It isprobably inevitable on continents that an invader willacquire new foes, especially as it expands its rangeand comes into contact with a wider group of native

species. The idea of escape from biot ic constraints isthe most straightforward hypothesis to explain thesuccess of an invader, and also provides the motiva-tion for researchers to search for biological controlagents among its enemies in its native range.

Community species richness. Charles Elton proposedin 1958 that community resistance to invasions in-creases in proportion to the number of species in thecommunit y it s species richness. To Elton, this fol-lowed from his hypothesis that communities are more stable if t hey are species-rich. This idea is a variant

of the vacant niche hypothesis; that is, a communitywit h many species is unlikely t o have any vacant nichesthat cannot be defended successfully from an immi-grant. On land, however, resistance to plant invasionmay correlate more strongly with the architecture ofthe plant community specifically, t he maintenanceof a multi-t iered plant canopy than with the actualnumber of species wit hin the community. For instance,many forest communities have remained resistant toplant invaders as long as the canopy remained intact.

Here again, exceptions abound. Disturbance before or upon immigration. Humans,or the plants and animals they disperse and domesti-cate, may encourage invasions by causing sudden,radical disturbances in the environment. If native spe-cies can neither acclimatize nor adapt, the subsequentarrival of pre-adapted immigrants can lead swiftly toinvasions. Such disturbances can be provoked by fire,floods, agricult ural practices, or livestock grazing onland, or by drainage of wetlands or alt erat ions of sa-linity, and nutrient levels in streams and lakes. Novel

disturbances, or intensificat ion of natural disturbancessuch as fire, have played a significant role in some ofthe largest biot ic invasions, such as the extensive plantinvasions across vast temperate grasslands in Aus-t ralia and North and South America. Alt ernat ively,recurring natural disturbance may prevent naturaliza-tions, such as non-indigenous species that are con-fined to the boundaries of a fire-prone area.

The diff iculty of predicting community vulnerabilityto invasions is increased greatly by the bias of immigra-

tion, i.e., it is nearly impossible to test critically the rela-tive merits of these hypotheses because of confoundingissues, such as the enormous differences among communit ies in their opport unity to receive immigrants. The likelihood that a community wi ll have received immigrants isinfluenced largely by its proximity to a seaport or othermajor point of entry and also the frequency, speed and

mode of dispersal of the immigrants themselves. For example, for more than 300 years an ever-growing com-merce has both accidentally and deliberately deliverednon-native plant species to the coasts of South Africaand the Northeastern U.S. Not surprisingly, naturalizedfloras in these regions are very large. In contrast, somecontinental interiors, such as Tibet, have minuscule numbers of naturalized plants and few, if any, invaders. Thenative plant and animal communities in such regions maypresent strong barriers to naturalization and invasion, butisolation alone could explain the lack of invaders.

BIOTIC INVBIOTIC INVBIOTIC INVBIOTIC INVBIOTIC INVASIONS AS AGENTSASIONS AS AGENTSASIONS AS AGENTSASIONS AS AGENTSASIONS AS AGENTSOF GLOF GLOF GLOF GLOF GLOBAL CHANGEOBAL CHANGEOBAL CHANGEOBAL CHANGEOBAL CHANGE

Human-driven biotic invasions have alreadycaused wholesale alteration of the earths biota, changing the roles of native species in communities, disruptingevolutionary processes, and causing radical changes inabundance, including extinctions of some species. Thesealterations constitute a threat to global biodiversity sec

ond in impact only to t he direct destruction of habitat .Biotic invaders themselves often destroy habitatfor instance by altering siltation rates in estuaries andalong shorelines. In the past , the scope of t his direct lossof habit at was local or at most regional. Today, howeverwith invasions occurring at an unprecedented pace, invaders are collectively altering global ecosystem processes. Furt hermore, the growing economic toll causedby invasions is not limited by geographic or polit ical boundaries. Invaders are by any criteria major agents of globachange today. We provide below only a brief sketch of

the range of effects that biotic invaders cause tobiodiversity and ecological processes.

Population-Level EffectsInvasions by disease-causing organisms can se

verely impact native species. The American chestnut oncedominated many forests in the eastern U.S, especially inthe Appalachian foothills, until the Asian chestnut blightfungus arrived in New York City on nursery stock early inthe 20th century. Within a few decades, the blight had


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spread throughout the eastern third of the U.S., destroy-ing almost all American chestnuts within it s nat ive range.

The mosquito that carries the avian malaria parasite wasinadvertently introduced to the Hawaiian Islands in 182 6.The parasite itself arrived subsequently, along with theplethora of Eurasian birds that now dominate the Hawai-ian lowlands. Wit h avian malaria rampant in the lowlands,the Eurasian invaders, which are at least somewhat resis-tant t o it , have excluded native Hawaiian birds, which arehighly susceptible to the parasite.

Predation and grazing by invaders can also dev-astate native species. The predatory Nile perch, whichwas introduced into Africas Lake Victoria, has already

eliminated or gravely threatens more than 200 of the300 to 50 0 species of small native cichlid fishes. Feraland domestic cats have been transported to every partof the world and have become devastating predators ofsmall mammals and ground-nest ing or f light less birds. Onmany oceanic islands, feral cats have depleted breedingpopulat ions of seabirds and endemic land birds. In NewZealand, cats have been implicated in the extinction of atleast six species of endemic birds, as well as some 70populat ions of island birds. In Australia, cat predation

takes it s biggest t oll on small nat ive mammals. Cats arestrongly implicated in nineteenth century extinctions of

at least six species of native rodent-like Australian marsupials. Goats int roduced to St . Helena Island in 1513almost cert ainly extinguished more than 50 endemic plantspecies, although only seven were scientifically describedbefore ext inction. Invaders st ill extract a severe toll onSt. Helena. A South American scale insect has recent lythreatened the survival of endemic plants, including thenow rare national tree, Commidendrum robustum. Twoyears after the scale infestation began in 1993, at least25 percent of t he 2,0 00 remaining t rees had been killed

Non-indigenous species may also compete with

natives for resources. The North American gray squirreis replacing the native red squirrel in Britain by foragingmore efficiently. The serial invasion of New Zealandssouthern beech forests by two wasp species has harmednative fauna, including both invertebrates that are preyedon by wasps, and native birds which suffer competitionfor resources. For instance, the threatened kaka, a forestparrot, forages on honeydew produced by a native scaleinsect. But 95 percent of this resource is now claimed byinvasive wasps during the autumn peak of wasp density

Figure 5Figure 5Figure 5Figure 5Figure 5 - Invasive animals as well as invasive plants can radically alter both natural communities and their physicalenvironments. Litt orina litt orea(European periwinkle) was apparently introduced near Pictou, Nova Scotia in the1840s. Since then it has great ly increased the extent of rocky shoreline at t he expense of a marsh-grass dominatedzone along the New England and Canadian At lantic coasts through it s grazing on marine plants that induce silt ationand mud accumulation along wave-protected shorelines.

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and as a result the parrots abandon the beech forestsduring this season. The native biota of the Galapagos Is-lands is threatened by goats and donkeys, not only be-cause of t heir grazing but because they t rample the breed-ing sites of tortoises and land iguanas. They also destroythe forest cover in the highlands, thereby affecting theislands water cycle. Invasive plants have diverse means

of competing with natives. Usurping light and water areprobably the most common tactics. For example, the suc-culent highway ice plant , Carpobrotus edulis, both forms amat over native plants in coastal California and removes scarcewater that the natives would otherwise use.

When a species interferes with or harms anotherin the competition for resources, ecologists call it inter-ference competition, and the tactic has been well demon-strated in invasive species. For example, several widelyint roduced ant species the red fire ant, t he Argentineant, and the big-headed ant all devastate large frac-

t ions of nat ive ant communities by aggression. Report sof interference competition among plants through theirproduction of toxins often spark controversy, althoughQuackgrass, a persistent invader in agriculture, may wellproduce such phytotoxins.

Invasive species can also eliminate natives bymating with them, a particular danger when the nativespecies is rare. For example, hybridization with the int ro-duced North American mallard threatens the existence at least as dist inct species of both the New Zealand

gray duck and the Hawaiian duck. Hybridization betweena non-indigenous species and a native one can even pro-duce a new invasive species. For instance, North Ameri-can cordgrass, carried in shipping ballast to southern En-gland, hybr idized occasionally wit h t he nat ive cordgrassthere. These hybrid individuals were sterile, but one even-tually underwent a genetic change and produced a fer-t ile, highly invasive species of cordgrass. Hybr idizat ioncan threaten a native species even when the hybrids donot succeed, simply because crossbreeding reduces thenumber of new offspring added to the species own popu-

lation. Females of the European mink, already gravelythreatened by habitat deteriorat ion, hybridize with malesof int roduced Nort h American mink. Embryos are invari-ably aborted, but the wastage of eggs exacerbates thedecline of the native species.

Species can evolve after introduction to a newrange. For example, a t ropical seaweed, Caulerpa t axifolia,evolved tolerance for colder temperatures while it wasgrowing at the aquarium of t he Stutt gart Zoo and otherpublic and private aquaria in Europe. Since then it has

escaped into the northwest Mediterranean, and its newtolerance of winter t emperatures has permit ted it to blanket large stretches of the seafloor, threatening nearshoremarine communities. Evolution can also change potentiaimpacts in subtler ways. A parasit ic wasp imported to theU.S. to control the alfalfa weevil was originally ineffective against another insect, the Egyptian alfalfa weevil

The wasps lay their eggs in weevil larvae, providing theiryoung with a source of food. Dissections of larval Egyptian weevils showed that 35 to 40 percent of the waspseggs were destroyed by the immune response of the lar-vae. Fif teen years later, however, only 5 percent of t heeggs were being lost to these weevil defenses.

Communit y- and Ecosystem-Level EffectsThe biggest ecological threat posed by invasive

species is the disruption of entire ecosystems, often byinvasive plants that replace natives. For example, the

Australian paperbark or melaleuca tree, which until recentlywas increasing its range in south Florida by more than 20hectares per day, replaces cypress, sawgrass, and othernative species. It now covers about 16 0,0 00 hectaresoft en in dense stands that exclude virt ually all other vegetation. It provides poor habitat for many nat ive animalsuses huge amounts of water, and intensifies the fire regime. A vine-like perennial shrub from South AmericaChromolaena odorataor Siam weed, is not only an ag-gressive invader in both Asia and Africa, suppressing re

generation of primary forest trees, but also provides feed-ing niches that can sustain other pests. Another highlyinvasive neotropical shrub, Lantana camara, serves as habitat for the normally stream-dwelling t setse fly in East Africa, increasing the incidence of sleeping sickness in bothwild and domesticated animals, as well as in humans (Fig. 1)

M any invasive species wreak havoc on ecosystems by fostering more frequent or int ense fires, t o whichkey native species are not adapted. The paperbark t reehas this effect in Florida, as do numerous invasive grasseswor ldwide. In general, grasses produce a great deal o

flammable standing dead material, they can dry out rapidly, and many resprout quickly aft er f ires (Fig. 4).

An invasion of Hawaii Volcanoes National Parkby a small tree, Myrica faya, native to the Canary Islands, is transforming an entire ecosystem because theinvader is able to fix nit rogen and increase supplies of thisnutrient in the nitrogen-poor volcanic soils at a rate 90fold greater than native plants. Many other non-nativeplants in Hawaii are able to enter only sites with relativelyfertile soils, so Myricapaves the way for further inva


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sions, raising the threat of wholesale changes in theseplant communit ies. Myricaalso attracts the introducedJapanese white-eye, the most destructive invasive bird

species in native Hawaiian forests and a competitor ofseveral nat ive bird species. The whit e-eye, in t urn, dis-perses Myricaseeds.

Ecosystem transformations wrought by invadershave been so complete in some places that even the land-scape it self has been prof oundly alt ered. The BluegrassCountr y of Kentucky invokes images for most Ameri-cans of a pastoral, even pristine, sett ing. But bluegrass isa Eurasian invader that supplanted the regions originalvegetation, an extensive open forest and savanna withwild rye and possibly canes in the understory, after Euro-

pean settlement and land clearing. The European peri-winkle, introduced to Nova Scotia around 1840 , has trans-formed many of the coastal inlets along the northeastcoast of North America from mudflats and salt marshesto a rocky shore (Fig. 5 ). Similar wholesale t ransforma-tions of the landscape have occurred elsewhere, includ-ing the conversion of the Florida Everglades from a sea-sonally flooded marsh to a fire-prone forest of invasivetrees (Fig. 3) and the invasion of the fynbos or shrub com-munities in South Africas Cape Province by eucalyptus,

pines, acacias and other imported trees. Heavy water useby these invasive trees in South Africa has led to majorwater losses, and many rivers now do not flow at all or

flow only infrequent ly. This change, in turn, has reducedagricultural production and also threatened the extinction of many endemic plant species, such as the spec-tacularly flowered Proteas.

Our best estimate is that, left unchecked, thecurrent pace and extent of invasions will influence otheragents of g lobal change including the alteration ogreenhouse gases in the atmosphere in an unpredictable but profound manner. The current t ransformation ofecosystems in the Amazon basin through the burning offorests and their replacement with African grasses pro

vides one of t he most ominous examples. For examplein Brazil the conversion of diverse forest communitiesinto croplands and livestock pastures has often involvedthe deliberate sowing of palatable African grasses. Thespread and proliferation of these grasses has been fostered by fire. Perhaps most signif icant is the fact t hatgrasslands contain much less plant biomass than the nat ive forests and thus sequester less carbon. Given theextent of t he neotropical forests, cont inuing conversionsto grasslands could exacerbate the buildup of carbon di

Figure 6Figure 6Figure 6Figure 6Figure 6 - Invasion of non-indigenous or alien African grasses in the Amazon Basin could eventually cause thepermanent conversion of t his vast forested carbon sink int o grassland or savanna-like areas. Land-clearing, includingwide-ranging fires, create an environment conducive to these grasses at the expense of t he native species. Oncethese grasses occupy a site, their persistence is enhanced through their rapid annual production of highly flammablelit ter. This rat chet-like conversion across such a huge area holds important implications for ecosystem alt eration ata global scale (after DAntonio and Vitousek 1992).


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oxide in the atmosphere, potentially influencing global cli-mate. Alt hough fire and other agents of land-clearinginitiate these changes in the Amazon watershed, the per-sistence of invasive grasses thereafter limits any naturalrecolonization of cleared areas by native forest species(Fig. 6).

Economic ConsequencesAttempts to arouse public and governmental sup-

port for the prevention or control of invasions often failbecause of a lack of understanding of the inextricablelink between nature and economy. But t he threats biot icinvasions pose to biodiversit y and to ecosystem-level pro-cesses translate directly into economic consequences suchas losses in crops, forests, fisheries, and grazing capacity.Yet no other aspect of the study of biotic invasions is aspoorly explored and quantified. Although there are ampleanecdotal examples of local and even regional costs of in-

vaders, we consistently lack clear, comprehensive informa-tion on these costs at national and especially global levels.

Biotic invasions cause two main categories ofeconomic impact. First is loss in potential economic out -put: that is, losses in crop production and reductions indomesticated animal and fisheries survival, fitness, andproduct ion. Second is direct cost of combating invasions,including all forms of quarantine, control, and eradica-t ion. A third category beyond the scope of this report would emphasize costs of combat ing invasive species that

are threats to human health, either as direct agents of dis-ease or as vectors or carriers of disease-causing parasites.These costs form a hidden but onerous tax on

many goods and services. Tallying t hese costs, however,remains a formidable task. One group recently attempted,for example, to tabulate the annual cost of all non-indig-enous species in the U.S. They estimat e that non-indig-enous weeds in crops cost U.S. agriculture about $27billion per year, based on a potent ial crop value of $267billion. Loss of forage and the cost of herbicides appliedto weeds in rangelands, pastures, and lawns cause a fur-

ther $6 billion in losses each year. When the group com-bined these types of direct losses with indirect costs foractivities such as quarantine, the total cost of all non-indigenous species (plants, animals, microbes) exceeded$138 billion per year. By any standard, such costs are aformidable loss, even for a productive industrialized soci-ety such as the U.S.

These estimates illustrate the anecdotal and pre-liminary nature of our current understanding of the eco-nomics of invasions. One solut ion would be a more fre-

quent application of economic tools such as cost-benefitanalyses when considering proposals to import speciesfor perceived economic benefit . When it comes to fut uremovements of species, society needs to be able to con-sider results from the types of analyses economists al-ready provide for other projects with potential environmental consequences, such as construct ion of hydroelec

tric dams, canals, and airport s. We predict that costbenefit analysis of many deliberately introduced invaderswould demonstrate forcefully that their costs to societyswamp any realized or perceived benefits.

PREVENTION AND CONTROL OFPREVENTION AND CONTROL OFPREVENTION AND CONTROL OFPREVENTION AND CONTROL OFPREVENTION AND CONTROL OFBIOTIC INVBIOTIC INVBIOTIC INVBIOTIC INVBIOTIC INVASIONSASIONSASIONSASIONSASIONS

The consequences of biotic invasions are oftenso profound that they must be curbed and new invasionsprevented. This section is divided into two part s: fir st

efforts to prevent the opportunity for invasions by pro-hibit ing t he entry of nonnat ive species into a new rangeand second, concepts for curbing the spread and impactof nonnative species, including invaders, once they haveestablished in a new range.

Preventing Entry of Nonnat ive SpeciesThe use of quarantine, which is intended to pro-

hibit organisms from entering a new range, has a longhistory in combat ing human parasites. Rarely is the say

ing an ounce of prevent ion is worth a pound of cure soapplicable as wit h biot ic invasions. Most invasions beginwith the arrival of a small number of individuals, and thecosts of excluding these is usually t rivial compared t o t hecost and effort of later control after populations havegrown and established. Ident ificat ion of a potential future invader, however dif ficult , could allow marshaling ofresources to bar either it s entry or dispersal or to detecand destroy its founder populations soon after entry.

The ability of a nation to restrict the movementof biotic invaders across its borders is ostensibly gov-

erned by international treaties, key among them beingthe Agreement on the Application of Sanitary andPhytosanitary Measures (SPS). Under this agreement members of the World Trade Organization (WTO) can restrictmovement of species that may pose a threat to human, animal or plant life. The International Plant Protection Convention (IPPC) of 1951 deals with quarantine against crop pestsand the IPPC Secretariat also coordinates phytosanitary standards. The SPS agreement requires WTO members to baseany SPS measures on internationally agreed guidelines.


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In all these instances, three key factors contrib-uted to success. First, part icular aspects of t he biologyof the target species suggested that the means employedmight be effect ive. For example, the host specificit y andpoor dispersal abilit y of the cit rus canker were crucial t oa successful eradicat ion st rategy. Second, suff icient re-sources were devoted for a long enough t ime. If funding

is cut as soon as the immediate threat of an economicimpact lessens, eradication is impossible. Third, there waswidespread support both from the relevant agencies andthe public. Thus, for example, people rigorously heededquarant ines and various sanitary measures.

Even when complete eradication fails, the effortmay well have proven cost-effective and prevented sub-stant ial ecological damage. For example, a long cam-paign to eradicate witchweed, an African root parasite ofseveral crops in the Carolinas, has reduced the infesta-tion from 162,000 to 6,000 hectares. The methods

employed herbicides, soil fumigants to kill seeds, andregulation of seed-contaminated crops and machinery would have been used anyway simply to control this invader.

Other large eradication projects, however, havebeen so unsuccessful that they have engendered publicskepticism about the entire endeavor and have, in some

instances, worsened the problem. The long campaign toeradicate imported fire ants from the southern UnitedStates has been labeled by Harvard ecologist E. O. Wil-son as the Vietnam of entomology and was a $200million disaster. Not only did fire ants reinvade areascleared of ants by insecticides, but also, they returnedfaster than many native ant species. Furt her, many po

tent ial compet itors and predators of fi re ants were killedand traces of the pesticides were found in a wide varietyof non-target organisms, including humans. The int roduced range of fire ants expanded several-fold duringthe 20-year campaign, and sadly, enough was known atthe time about the biology of these ants that the out-come could have been predicted.

Maintenance ControlIf eradication fails, t he goal becomes maintenance

control of a species at acceptable levels. Three main ap

proaches, applied singly or in various combinations, are widelyused: chemical, mechanical, and biological control.

Chemical cont rol probably remains the chief t ooin combating non-indigenous pests in agriculture. As citedabove, chemical control, along wit h regional quarantinehas successfully contained witchweed to a few counties

FFFFFigure 7igure 7igure 7igure 7igure 7 - Mechanical control of invaders can be effect ive, although it usually is not practical over large areas. Insome cases, however, t he environmental damage outweighs the expense of labor-int ensive removal. Stands ofinvasive trees in the Cape Province of South Africa, such as Acacia saligna, are so dense that their removal revealsthe paucity of native plants that survived under the invaders canopy (note cleared strip at far left side of photo).Repeated detection and destruction of surviving invasive plants is essential for prolonged control.

PhotobyRich

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in North Carolina. Chemicals remain the chief t ools forbattling most insect pests, and in North America such

pests are almost invariably of f oreign orig in.Chemical controls, unfor tunately, have too oft encreated health hazards for humans and non-target spe-cies. For example, problems associated wit h DDT arewell known. But t he frequent evolut ion of pest resistance,the high cost, and the necessity of repeated applicationsoft en make cont inued chemical control impossible. If t hegoal were to control an invasive species in a vast naturalarea, the cost of chemical methods alone would be pro-hibit ive. Even when there is no firm evidence of a humanhealth risk from the chemicals involved, however, mas-

sive use of chemicals over heavily populated areas inevi-tably generates enormous public opposition, as demon-strated by the heated responses to recent aerial spraycampaigns using malathion against the medfly in Califor-nia and Florida.

Mechanical methods of cont rolling non-native or-ganisms are sometimes effective and usually do not en-gender public crit icism (Fig. 7). Sometimes they can evenbe used to generate public interest in and support forcontrol of invasive species. In Floridas Blowing Rocks

Preserve, volunt eers helped remove Australian pine, Brazilian pepper, and other invasive plants and to plant more

than 60,000 individuals of 85 native species; the volun-teer t ime to date is valued at more than $1 00 ,000 . And hand picking of g iant Af rican snails was a key component of the successful eradication campaigns in Floridaand Queensland. However, equipment expenses, the difficulty of actually finding the target organisms, and thegeographic scale of some non-indigenous species infes-tations frequently render mechanical control impossible.

Hunting is often cited as an effective method ofmaintenance control of non-indigenous animals, and hunting and trapping were crucial in many of the successfu

mammal eradication campaigns on small islands in NewZealand, as well as in the eradication of the nutria fromBrit ain. In the Galapagos Islands, park off icials have along-established campaign to eradicate non-indigenousmammals, and over the past 30 years goats have beeneliminated from five islands. By contrast , public huntingalone is unlikely to serve as an effective control on aninvasive mammal. Public hunting of Australian brushtaipossums was encouraged in New Zealand from 1951 to1961 through a bounty system and harvesting of ani

FFFFFigure 8igure 8igure 8igure 8igure 8 - Ideally, biological con-trol introduces a species that

voraciously attacks only the tar-get species populations. Even-tually, both target species andthe biocontrol agent becomerare, although usually not ex-t inct, in the new range. Thesmall beetle, Chrysolinaquadrigemina, has proven to be just such an effective agent incontrol of invasive Hypericum

perforatum(St. Johns wort) inthe U.S. and elsewhere.

PhotobyGaryPiper.


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mals for pelts. M ore than 1 million animals each yearwere shot or t rapped in the late 1950s. Nevert heless,the possum continued to spread.

Problems with both chemical and mechanical con-t rols have focused at tention on biological control theint roduct ion of a natural enemy of an invasive species. Ina sense, this is a planned invasion. It aims to establish in

the new set t ing at least part of t he biotic control t he tar-get species experiences in it s nat ive range. Some biologi-cal control projects have succeeded in containing verywidespread, damaging infestations at acceptable levelswit h minimal costs. Examples include the well-known con-trol of invasive prickly pear cactus in Australia by the mothCactoblastis cactorumfrom Argentina; control of SouthAmerican alligator weed in Florida and Georgia by a fleabeetle; and control of the South American cassava mea-lybug in Africa by a South American encyrtid wasp (Fig.8). In each of t hese cases, t he natural enemy has con-

t rolled the pest in perpetuity, wit hout f urther human inter-vent ion. When the pest increases in numbers, the naturalenemy increases correspondingly, causing the pest todecline, which entrains a decline in the natural enemy.Neither player is eliminated; neither becomes common.

Caveats on Biological ControlBiological control has recently been crit ically scru-

tinized on the grounds that non-target species, some ofthem the focus of conservation efforts, have been at-

tacked and even driven to extinction by non-nativebiocontrol agents. The widespread int roduct ion of a NewWorld predatory snail, Euglandina rosea, to control thegiant African snail led to extinction of many endemic snailspecies in the Hawaiian and Society islands. In these cases,the predators attacked many prey species, thus prevent-ing a mutual populat ion control f rom developing betweenthe predator and any single prey species.

Insect biological control agents that have beensubjected to rigorous host-specificity testing have never-theless been known to at tack non-target species. For

example, a Eurasian weevil, introduced to North Americato control invasive musk thistle, is now attacking nativenon-pest t histles. These natives include a federally l istedendangered species and narrowly restr icted endemic spe-cies in at least two Nature Conservancy refuges, threenational parks, and state lands. Controversy about t heextent of such problems focuses primarily on two issues:whether there is suff icient monitor ing t o detect such non-target impacts, and the likelihood that an introduced bio-logical control agent will evolve to attack new hosts. The

fact that biological control agents can disperse and evolveas can any other species introduced to a new range, im-plies that their preliminary evaluation should be extensiveand conducted under extremely secure circumstances.

Exclusion and Control: Socioeconomic IssuesThe difficulties of curbing biotic invasions illus

trate the problem of implement ing scient if ically based recommendations in an arena in which diverse segments ofsociety all have import ant stakes. At every level of prevention and control, the thorny issues are as likely to besocioeconomic as scientific.

A persistent problem with current methods ofexclusion and control is that they largely assume goodwill and cooperat ion on the part of all cit izens. For widelyvarying reasons, large segments of entire industries arecommitted to the introduction, at least in controlled set-tings, of many non-indigenous species and are skeptica

of arguments that they wi ll escape and/ or be problemat icif t hey do escape. Thus, t here is often organized opposition to proposals to stiffen regulations, and there is alsofrequent careless or even willful disregard of exist ing laws

The hort iculture industry is often in the vanguardof opposition to tight control of non-indigenous speciesIt is a large, diverse industry with importers running thegamut from small, family operat ions specializing in a fewspecies to large corporations importing hundreds of taxonomically diverse species. At one extreme, some hort i

culturists generate publications and websites scoffing atthe very existence of ecological problems with introducedspecies. On the other hand, many plant impor ters recognize the dangers and at least support quarantine measures and limited blacklists of species known to be inva-sive. However, as a whole, through trade associat ionsand as individuals, hort icultur ists attempt to influence thepolitical process as it concerns regulation of non-indigenous species. Furthermore, individuals who purchase plantsfrom importers are generally under far less legal obligationand undergo little scrutiny in their use of these plants.

Horticulturists have also been at least loosely al-lied with other interest groups that desire quite unfettered access to the worlds flora. State departments oftransportation, charged with landscaping highways, as welas the U. S. Soil Conservation Service, constituted tobatt le erosion, have traditionally f avored non-indigenousspecies for t hese purposes. At least some state departments of transportation are moving towards use of native plants, but a long history of interaction between thesedepartments and private hort iculturists slows this process


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Agricultural interests and their regulatory agen-cies have had a schizophrenic relationship with int roducedspecies. On t he one hand, they promote the importationof useful and profit able crop plants and livestock. On t heother, they hope to cont rol t he influx of parasites, insectpests, and agricultural weeds. For example, the thistle

weevil discussed above as a biocontrol agent that attacksnon-target species was introduced to North America byAgriculture Canada and spread in the United States bythe U.S. Depart ment of Agr iculture and various stateagricultural agencies.

The pet industry is also often heavily invested innon-native species. As wit h the hort iculture indust ry, itencompasses a tremendous range of operations in termsof size, scope, and degree and nature of specialization,and there is no monolithic stance towards threats posedby non-indigenous species and the prospect of rigorous

control. However, again as wit h hort icultur ists, throughthe political and publicity activities of individuals and tradeorganizations, the general attitude of the pet industrytoward strict regulation of introductions has ranged fromskepticism to outright hostility.

M any domest icated or pet animals have escapedfrom importers and breeders for example, when firesor storms destroyed cages and some have becomeinvasive. In Brit ain, escapees from fur f arms establisheda feral population of nutria, which became the target of a

lengthy eradication campaign. Sometimes, pet dealersor owners deliberately release animals. Again, as withhorticulturists, once a pet is sold, the dealer has no subse-quent control over the owners actions, and the owner maybe less likely than the dealer to obey formal regulations.

Controversies over the management of fera

horses in both the U.S. and New Zealand illustrate theconflicts that readily arise between environmentalists andother segments of society about some widely appreci-ated feral domestic animals. In both countr ies feral horsespose documented threats to native species and ecosystems. Yet some groups contend the horses that escapedfrom Spanish explorers in North America about 500 yearsago belong in the West, merely serving as replacementsfor native equids that became extinct on the continentabout 10,0 00 years ago. In New Zealand, however, therewere no native land mammals, except for bats, before

introduct ions by people. Horses were introduced to NewZealand less than 200 years ago.

In New Zealand, feral horses have occupied thecentral Nort h Island since the 1870s. Land development and hunting progressively reduced their numbers toabout 17 4 animals in 1979 . By 19 81 , however, publiclobbying resulted in creat ion of a protected area for t heremaining horses. Wit h prot ect ion, horses increased to1,576 animals by 1994, essentially doubling their populat ion every four years. In response to damage in native

Figure 9Figure 9Figure 9Figure 9Figure 9 - The detrimental consequences of some invaders are only too apparent. Eichhornia crassipes (water

hyacinth), native to the Amazon, has oft en been considered one of t he worlds worst plant invaders. In many of it snew t ropical ranges, it has rapidly covered the surfaces of lakes and rivers with a t hick, oft en impenetrable, mat.Man Sagar Lake near Jaipur, India

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ecosystems caused by this rapidly growing population,the New Zealand Department of Conservation recom-mended management to retain a herd of about 500 ani-mals. The management plan, which included shoot inghorses, provoked intense public protest . This outcry even-tually resulted in t he overt urning of a scient ifically basedmanagement plan and a 1997 decision to round up as

many horses as possible for sale. Sale of several hundredhorses duly took place, but the long-term fate of the grow-ing herd remains unresolved. The impasse in New Zealandover feral horse control has been mirrored in Nevada,where an int ense dispute has raged between land manag-ers and pro-horse activists about the ecological impactsof feral horses, the size of feral herds, and appropriatemethods of populat ion control. At a pract ical level, theremoval of animals by culling would probably be the sim-plest way of achieving population reduction, but publicresistance precludes this option.

The infusion of strong public sentiment into policyfor feral horses, as well as burros in the U.S., would likelyserve as a mild preview of public reaction to serious ef-for ts to control feral cats. Ample evidence demonstratesthat feral cats are the most serious threat to the persis-tence of many small vert ebrates. One study in Britainestimates that domestic cats alone kill 20 million birdsannually; the toll for feral cats, while unknown, clearlyadds to this tally. The degree to which feral cats in Austra-lia should be eradicated and domestic cats sterilized has

already engendered vituperative debate. Similar discussion,pitt ing environmentalists against the general public, is beingplayed out in the U.S. and Europe. Few biot ic invasions incoming decades will deserve more even-handed commentfrom ecologists than the dilemma caused by feral cats.

Game and fish agencies have traditionally beenmajor importers of non-indigenous species, particularlyfishes, gamebirds, and mammals. Alt hough at least somegame and fish agencies have recently recognized the needfor more regulation of non-indigenous species, the factthat they are still mandated to import new species sug-

gests a conflicted att itude. Furt hermore, many privateindividuals and organizations release game species in newlocat ions. Some releases of game fishes and other ani-mals const itute deliberate flout ing of laws. Groups ofprivate individuals in t he northern Rocky M ountains sur-reptitiously released non-indigenous fish into isolatedmountain lakes, backpacking the fish to ensure that eventhe most isolated alpine lakes received what these indi-viduals deemed as suitable biot a. Even apparently innocu-ous actions can have ecologically catastrophic impacts.

The release of bait fishes by fishermen at the end of the dayhas already led to the extinction of species in the UnitedStates, including t he Pecos pupfish through hybridizat ion.

Long-Term Strategies for Control of Biot ic InvadersEffective prevention and control of biotic inva

sions require a long-term, large-scale strategy rather t han

a tact ical approach focused on bat t ling individual invaders. One of the problems of t aking a tactical view ofinvaders, especially in a region where multiple invasiveorganisms are flourishing, is the prospect of simply t rading one pest f or another. For example, int roduct ion of asuccessful biocont rol agent against only one species maybe ecologically useless unless there is a strategy in placefor dealing wit h the remaining invaders. This may havealready occurred possibly in the ascendance of yellowstarthistle as a plant invader in California as the impact ofbiocontrol on St. Johns wort increased in the 1950s

and it may occur oft en. A st rategic, system-wide approach, rather t han simply destroying the currently mostoppressive invaders, is particularly appropriate for conservation areas; such an approach is seldom undertaken

In some nations, such a broader strategic approach to the control of invaders is being put into placeIn a project of ext raordinary scale, South Af rica is determined to clear all the invasive woody species from itsriver catchments in a 20-year program. The mult i-species, mult i-pronged national strategy involves manual clear

ing of thickets to allow native vegetation to re-establishtreatment of cut stumps with mycoherbicides, and theuse of biological control to prevent reinvasion by exoticwoody species. Although this program will cost US $150million, it is far cheaper than alternatives such as massivedam-building programs to insure the nat ions water supply, and it has the bonus of creating thousands of jobs.

FUTURE RESEARCH AND POLICY PRIORITIESFUTURE RESEARCH AND POLICY PRIORITIESFUTURE RESEARCH AND POLICY PRIORITIESFUTURE RESEARCH AND POLICY PRIORITIESFUTURE RESEARCH AND POLICY PRIORITIES

Extensive research on the ecology of biotic inva-

sions dates back only a few decades. Although much hasbeen learned, too many of the data remain anecdotaland the field still lacks definitive synthesis, generalizat ion, and prediction. The following include a few arenasin which research or new policy initiatives, or both, seemparticularly worthwhile.1. Clearly, we need a much bet ter understanding of t he

epidemiology of invasions. As part of this goal weneed much better areal assessments of on-going in-vasions, for both public policy decisions as well as


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science. Few tools are as effective as t ime-seriesmaps in showing t he public the course of an unfoldinginvasion. An analogy can be made between the needfor current, dynamic maps of invasions and the needmet by modern weather maps. Weather maps allowviewers to recognize instantly source, direction, evenint ensit y and collateral forces. We also emphasize

here the need to collect in a more deliberate mannerinformation about the populat ion biology of immigra-tions that fail, since an understanding of the failureof the vast majorit y of immigrants can eventually helpdiscern the early harbingers of an impending invasion.

2. Experimentat ion in the epidemiology of invasions is alogical extension of (1). So far, the most comprehen-sive data come from observing the fates of insectsreleased in biological control and birds introduced onislands. We need to develop innocuous experimentalreleases of organisms that can be manipulated to ex-

plore the enormous range of chance events to whichall immigrant populations may be subjected.

3. Worthwhile economic est imates of the t rue cost ofbiotic invasions are rare and almost always involvesingle species in small areas. We need comprehensivecost-benefit analyses that accurately and effectivelyhighlight the damage inflicted on the world economyby biot ic invasions. The need is similar to the mandatethe World Health Organization meets by analyzing andreporting the economic toll of human disease.

4. M ost members of society become aware of bioticinvasions only through some first-hand experiencewhich usually involves some type of economic costThese cases often prompt action, or at least publicreaction, that is short -lived and local. We need instead a greater public and governmental awarenessof the chronic and global effects of invasive organ

isms and the tools available to curb their spread andrest rict their ecological and economic impacts. Public outreach about biotic invaders needs to match orexceed current efforts to draw public attention toother ongoing threats to global change.

CONCLCONCLCONCLCONCLCONCLUSIONSUSIONSUSIONSUSIONSUSIONS

Biotic invasions are altering the worlds naturacommunities and their ecological character at an unprecedented rate. If we fail t o implement effective st rategies

to curb the most damaging impacts of invaders, we riskimpoverishing and homogenizing the very ecosystems onwhich we rely to sustain our agriculture, forestry, fisheries and other resources and to supply us with irreplace-able natural services. Given the current scale of invasions and our lack of effective policies to prevent or control t hem, biot ic invasions have joined the ranks of atmospheric and land-use change as major agents of humandriven global change.

Figure 10Figure 10Figure 10Figure 10Figure 10 - Nut ria have caused extensive habitat damage in southern Louisiana, somet imes leading to complete loss ofmarsh wit h conversion to open water. Ariel photo shows the results of vegetative change eight months into a four yearstudy conducted by Lori Randall and Lee Foote through the USGS Nat ional Wetlands Research Center in Lafayette, LA.Experimental exclosures protected marsh vegetation from a 80-90% reduction in standing biomass from nutria (dot-ted white perimeter demarcates unfenced control area grazed by nutria). Such loss of plant biomass leads to a reduc-tion in sediment accumulation and the eventual loss of marsh habitat.

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ACKNOWLEDGMENTSACKNOWLEDGMENTSACKNOWLEDGMENTSACKNOWLEDGMENTSACKNOWLEDGMENTS

The panel thanks David Tilman for his foresight inorganizing the Issues in Ecology series and The Pew Chari-table Trusts for their financial support of the project thatproduced this report . We thank Yvonne Baskin; her editingskills both improved the technical report and produced alucid version of t he report for the general audience. We also

thank G. H. Orians for his comments on an earlier draft ofthe manuscript . We also thank L. Foot e, J. Grace, S. Hacker,G. Piper, and L. Randall for the use of photographs; and L.Hidinger and F. Kearns for their skill in editing, publicationlayout and design.

SUGGESTIONS FOR FURTHER READINGSUGGESTIONS FOR FURTHER READINGSUGGESTIONS FOR FURTHER READINGSUGGESTIONS FOR FURTHER READINGSUGGESTIONS FOR FURTHER READING

Cronk, Q. C. B. and J. L. Fuller. 1995. Plant Invaders.Chapman and Hall, London.

Kaiser, J. 1 999. Stemming t he tide of invading species. Sci-

ence 285: 18 36 -18 41 .Pimentel, D., L. Lach, R. Zuniga and D. Morrison. 2000.

Environmental and economic costs of non-indigenousspecies in the Unit ed States. Bioscience 50(1):53-65 .

Vitousek, P. M., C. M . D Antonio, L. L. Loope, and R.Westbrooks. 1996. Biological invasions as globalenvironmental change. American Scient ist 84 : 46 8-478.

Williamson, M. 1996. Biological Invasions. Chapman andHall, London.

This report summarizes the findings of our panel.Our full report, which is being published in the journal Eco-logical Applications(Volume 10 , Number 3 , June 20 00 ) dis-cusses and cites extensive references to the primary scientificlit erature on this subject. From that list we have chosenthose below as illustrative of the scientific publications andsummaries upon which our report is based.

Bertness, M . D . 1 98 4. Habitat and community modificat ionby an introduced herbivorous snail. Ecology 65: 37 0-

381.Crawley, M. J. 1989. Chance and timing in biological inva-

sions. Pages 407-423 in J. Drake, F. di Castri, R.Groves, F. Kruger, H. A. Mooney, M . Rejmanek, M.Williamson, editors. Biological invasions: a global per-spective. Wiley, New York, New York, USA.

D Antonio, C. M ., and P. M . Vitousek. 1 99 2. Biological in-vasions by exotic grasses, the grass/ fire cycle andglobal change. Annual Review of Ecology and Sys-tematics 23 : 63-87.

Huf faker, C. B. and C. E. Kennet t . A ten-year study ovegetational changes associated with the biologicacontrol of Klamath weed. Journal of Range M anagement 69-82.

M ack, R. N. 1995. Understanding the processes of weedinvasions: The inf luence of envir onmentastochast icity. Pages 65-74 in C. St irt on, editorWeeds in a changing world . British Crop Protec-tion Council, Symposium Proceedings No. 64Brighton, U.K.

Port er, S. D. and D. A. Savignano. 1990. Invasion of polygene fire ants decimates native ants and disruptsarthropod community. Ecology 71: 2095-2106.

M oran, V. C. and H. G. Zimmerman. 19 91 . Biological contro l of jo inted cactus, Opuntia aurant iaca(Cactaceae), in South Africa. Agriculture, Ecosystems and Environment 37: 5-27.

Simberlof f, D., D . C. Schmitz, and T. C. Brown. (editors1997. Strangers in paradise. Island Press, Washington, D.C. USA.

U.S. Congress, Office of Technology Assessment. 1993Harmful non-indigenous species in the United StatesOTA-F-565. U.S. Congress Government PrintingOffice. Washington, D.C., USA.

Weiss, P. W. and S. J. M ilt on. 1 984. Chr ysanthemonoidesmonilifera and Acacia longifolia in Australia andSouth Af rica. Pages 159-160 in B. Dell, editor. Proceedings of the 4th International Conference onM editerranean Ecosystems. University of WesternAustralia, Nedlands, Western Australia.

ABOUT THE PABOUT THE PABOUT THE PABOUT THE PABOUT THE PANEL OF SCIENTISTSANEL OF SCIENTISTSANEL OF SCIENTISTSANEL OF SCIENTISTSANEL OF SCIENTISTS

This report presents a consensus reached by a paneof six scientists chosen to include a broad array of expert isein this area. This report underwent peer review and was approved by the Board of Editors of Issues in Ecology. The affiliations of the members of the panel of scient ists are:

Dr. Richard N. Mack, Panel Chair, School of Biological Sciences, Washington State University, Pullman, WA99164

Dr. Daniel Simberloff, Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxvi lle, TN37996-1610

Dr. W. Mark Lonsdale, CSIRO Entomology and CRC for WeedManagement Systems, GPO Box 1700, CanberraACT 2601, AUSTRALIA

Dr. Harry Evans, CABI BIOSCIENCE, UK Centre (Ascot)Silwood Park, Buckhurst Rd., Ascot, Berkshire SL57TA, UK


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2 0

Dr. M ichael Clout , School of Biological Sciences, Universityof Auckland, Private Bag 92 01 9, Auckland, NEWZEALAND

Dr. Fakhri Bazzaz, Biological Laborator ies, Harvard Univer-sity, 1 6 Divinity Ave., Cambridge, M A 021 38

About the Science WriterYvonne Baskin, a science writer, edited the report of

the panel of scientists to allow it to more effect ively commu-nicate its findings with non-scient ists.

About Issues in EcologyIssues in Ecologyis designed to report , in language

understandable by non-scientists, the consensus of a panel ofscientif ic expert s on issues relevant to t he environment. Is-sues in Ecologyis supported by a Pew Scholars in Conserva-tion Biology grant to David Tilman and by the EcologicalSociety of America. All report s undergo peer review and

must be approved by the editor ial board before publicat ion.

Editorial Board of Issues in EcologyDr. David Tilman, Editor-in-Chief, Department of Ecology,Evolution and Behavior, University of Minnesota, St. Paul,MN 55108-6097. E-mail: [email protected]

Board membersDr. Stephen Carpenter, Center for Limnology, University of

Wisconsin, Madison, WI 53706Dr. Deborah Jensen, The Nature Conservancy, 1 815 Nor th

Lynn Street , Arlingt on, VA 22 20 9Dr. Simon Levin, D epartment of Ecology & Evolut ionary Bi-ology, Princeton University, Princeton, NJ 08 54 4-1003

Dr. Jane Lubchenco, Department of Zoology, O regon StateUniversity, Corvallis, OR 97331-2914

Dr. Judy L. Meyer, Institute of Ecology, University of Geor-gia, Athens, GA 30 60 2-22 02

Dr. Gordon Orians, Department of Zoology, University ofWashington, Seatt le, WA 98 19 5

Dr. Lou Pitelka, Appalachian Environmental Laboratory,

Gunter Hall, Frostburg, MD 21 53 2Dr. William Schlesinger, Departments of Botany and Geol-ogy, Duke University, Durham, NC 27708-0340

Previous ReportsPrevious Issues in Ecologyreports available from the

Ecological Society of America include:

Vit ousek, P.M ., J. Aber, R.W. Howarth, G.E. Likens, P.AMatson, D.W. Schindler, W.H. Schlesinger, and G.DTilman. 19 97 . Human Alteration of the Global Nit rogen Cycle: Causes and Consequences, Issues in EcologyNo. 1.

Daily, G.C. , S. Alexander, P.R. Ehrlich, L. Goulder, JLubchenco, P.A. M atson, H.A. M ooney, S. Postel, S.HSchneider, D. Tilman, and G.M . Woodwell. 199 7. Ecosystem Services: Benefit s Supplied to Human Societiesby Natural Ecosystems, Issues in EcologyNo. 2.

Carpenter, S., N. Caraco, D. L. Correll, R. W. Howarth, AN. Sharpley, and V. H. Smith. 1998. Nonpoint Pollution of Surface Waters with Phosphorus and NitrogenIssues in EcologyNo. 3.

Naeem, S., F.S. Chapin III, R. Costanza, P.R. Ehrlich, F.BGolley, D.U. Hooper, J.H. Lawton, R.V. ONeill, H.AM ooney, O.E. Sala, A.J. Symstad, and D. Tilman. 1999Biodiversity and Ecosystem Functioning: M aintainingNatural Life Support Processes, Issues in EcologyNo. 4

Additional CopiesTo receive additional copies of t his report ($3 each

or previous Issues in Ecology, please contact:

Ecological Society of America

1707 H Street, NW, Suite 400Washington, DC 2000 6(202 ) 833 -8773, esahq@ esa.org

The Issues in Ecologyseries is also availableelectronically at http://esa.sdsc.edu/.

Special t hanks to U.S. Geological Society Biological ResourcesDivision, U.S. Bureau of Land Management, National Oce

anic and Atmospheric Administration, and the U.S. Department of Agr iculture for supporting printing and dist ributionof t his document.

Cover photo: Extensive death of Abies fraseri(Fraser f ir) at Clingmans Dome, Smokey M ountains Nat ional Park. Sincethe arr ival of the lethal insect invader Adelges piceae(balsam woolly adelgid) in the Park less than 30 years ago, almostall of the once prominent A. fraserihave been destroyed. The sparse, surviving arboreal canopy consists primarily ofPicea rubens (red spruce).


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About Issues in EcologyAbout Issues in EcologyAbout Issues in EcologyAbout Issues in EcologyAbout Issues in Ecology

Issues in Ecology is designed to report, in language understandable by non-scientists, theconsensus of a panel of scientific experts on issues relevant to the environment. Issues inEcology is supported by the Pew Scholars in Conservation Biology program and by the Eco-logical Society of America. It is published at ir regular intervals, as reports are completed. Allreports undergo peer review and must be approved by the Editorial Board before publication.

Issues in Ecology is an official publication of the Ecological Society of America, the nationsleading prof essional society of ecologists. Founded in 19 15, ESA seeks to promote the

responsible application of ecological principles to the solut ion of environmental problems. Formore information, contact the Ecological Society of America, 1707 H Street, NW, Suite 400,Washington, DC, 200 06 . ISSN 1092 -898 7

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