are mountain habitats becoming more suitable for …lizards were housed in individual terraria, fed...

Submitted 2 February 2016Accepted 5 May 2016Published 31 May 2016

Corresponding authorZaida Ortega zaidaortegausales

Academic editorCeacuteline Audet

Additional Information andDeclarations can be found onpage 12

DOI 107717peerj2085

Copyright2016 Ortega et al

Distributed underCreative Commons CC-BY 40

OPEN ACCESS

Are mountain habitats becoming moresuitable for generalist than cold-adaptedlizards thermoregulationZaida Ortega AbrahamMenciacutea and Valentiacuten Peacuterez-MelladoDepartment of Animal Biology University of Salamanca Salamanca Spain

ABSTRACTMountain lizards are highly vulnerable to climate change and the continuous warmingof their habitats could be seriously threatening their survival We aim to compare thethermal ecology and microhabitat selection of a mountain lizard Iberolacerta galaniand a widely distributed lizard Podarcis bocagei in a montane area Both speciesare currently in close syntopy in the study area at 1400 m above the sea level Wedetermined the precision accuracy and effectiveness of thermoregulation and thethermal quality of habitat for both species We also compared the selection of thermalmicrohabitats between both species Results show that I galani is a cold-adaptedthermal specialist with a preferred temperature range of 279ndash297 C while P bocageiwould be a thermal generalist with a broader and higher preferred temperature range(301ndash345 C) In addition I galani selects rocky substrates while P bocagei selectswarmer soil and leaf litter substrates The thermal quality of the habitat is higher for Pbocagei than for I galani Finally P bocagei achieves a significantly higher effectivenessof thermoregulation (087) than I galani (080) Therefore these mountain habitatconditions seem currently more suitable for performance of thermophilic generalistlizards than for cold-specialist lizards

Subjects Animal Behavior Biodiversity Conservation Biology Ecology ZoologyKeywords Lizard Climate change Cold-adapted Thermal generalist Temperature LacertidaeIberolacerta Podarcis Mountain habitats Thermal ecology

INTRODUCTIONClimate change has already produced several impacts in the biology and distribution ofmany animal species worldwide (Parmesan 2006 McCain 2010) However some speciesare more vulnerable than others to the impact of global warming (Arauacutejo Thuiller ampPearson 2006 Sinervo et al 2010 Huey et al 2012) Ectotherms are particularly sensitiveto climate warming since they depend on external heat sources for body temperatureupkeep (eg Hertz Huey amp Stevenson 1993 Huey et al 2012) Knowledge on the thermalbiology of ectotherms is necessary to assess their vulnerability to climate change to predictthe future impacts of global warming and to adopt conservation measures to prevent theirextinction (Carvalho et al 2010 Crossman Bryan amp Summers 2012 Groves et al 2012)

High elevation ectotherms would be particularly threatened by the fast increase ofenvironmental temperatures mainly because two reasons (1) the plasticity and evolutionof thermal physiology seem limited to keep pace with the fast environmental warming

How to cite this article Ortega et al (2016 ) Are mountain habitats becoming more suitable for generalist than cold-adapted lizardsthermoregulation PeerJ 4e2085 DOI 107717peerj2085

(eg Muntildeoz et al 2014 Gunderson amp Stillman 2015) and (2) living in mountaintopsthey lack colder areas to migrate (Arauacutejo Thuiller amp Pearson 2006 Berg et al 2010McCain 2010) In addition mountain species tend to be cold-specialists (eg Aguado ampBrantildea 2014) which makes themmore vulnerable because the decline of fitness when bodytemperatures exceed the optimum temperature is greater in narrower thermal reactionnorms (Martin amp Huey 2008 Huey et al 2012 Gunderson amp Stillman 2015) Mountainlizards could also be threatened by potential displacement by thermal generalist specieswith a broader distribution at the surrounding lowlands that may ascend in altitude aswarming increases (Arauacutejo Thuiller amp Pearson 2006 Huey et al 2012 Comas Escorizaamp Moreno-Rueda 2014) An expansion both in altitude and latitude due to climatechange has already been documented for several species (Parmesan 2006 Sinervo et al2010 Chen et al 2011 Moreno-Rueda et al 2012 Bestion Clobert amp Cote 2015) Thesefactors altogether would place high-mountain lizards among the most vulnerable animalsworldwide especially mountain lizards of the Iberian Peninsula due to the higher warmingand drought predicted for these areas (Nogueacutes-Bravo et al 2008 Arauacutejo et al 2011Maiorano et al 2013) The study of the thermal ecology of these mountain lizards aswell as the comparison with their potential competitors would be useful to design theconservation measures required to preserve the species (Urban Tewksbury amp Sheldon2012 Lord amp Whitlatch 2015)

Some studies had assessed thermal ecology of other Iberolacerta lizards (Monasterio etal 2009 Aguado amp Brantildea 2014 Ortega Menciacutea amp Peacuterez-Mellado 2016) We studied thethermal ecology of the Leoacuten rock lizard I galani a mountain lizard living in its historicalrange and the Bocagersquos wall lizard P bocagei that has expanded its altitudinal range to thestudy area in recent years Both are medium-size insectivorous and heliothermic lacertidlizards endemic from the northwestern of Spain Their distribution ranges are considerablydifferent (Fig 1) I galani is restricted to high-mountain climate isolated areas from 1300to 2500 m asl (meters above the sea level Arribas Carranza amp Odierna 2006 MenciacuteaOrtega amp Peacuterez-Mellado 2016) whereas P bocagei inhabits a variety of habitats from thesea level to 1900 m asl habitats (Galaacuten 1994 Peacuterez-Mellado 1998 Galaacuten 2004) Howeverboth live in close syntopy in the study area nowadays fully mixed in the same habitat Wecompared the thermal requirements of the two species in the laboratory and the thermaltraits of their habitat in order to study if mountain habitats are increasingly unsuitable formountain lizards and may be favoring the expansion of thermal generalists instead Wefirst aim to assess and compare the thermal preferences and behavioral thermoregulationof both species (Hertz Huey amp Stevenson 1993 Angilletta 2009) Then we studied theirselection of microhabitats and we compared the thermal suitability of the habitat for bothspecies under the current climatic conditions

MATERIALS amp METHODSStudy areaThe study area was in the Natural Monument lsquolsquoLago de La Bantildearsquorsquo (Leoacuten province Spain4215primeN 629W) It was an area surrounding a glacial lake located at 1400m asl formed by

Ortega et al (2016 ) PeerJ DOI 107717peerj2085 217

Figure 1 Distributional ranges of Iberolacerta galani and Podarcis bocagei I galani is restricted to themountain range of Montes de Leoacuten (Spain) while P bocagei is widely distributed in the northwest of theIberian Peninsula

Table 1 Size andmass of both species Snout-vent length (SLV in mm) and weight (in g) of adult malesand females of Iberolacerta galani and Podarcis bocagei of La Bantildea (Leoacuten Spain) included in the study

SVL Weight

I galani Males (n= 44) 6595plusmn 583 694plusmn 187 Females (n= 53) 6796plusmn 607 702plusmn 183P bocagei Males (n= 48) 5852plusmn 489 490plusmn 127 Females (n= 25) 5538plusmn 466 386plusmn 108

slate rocks meadows and shrubs The area is also circled by mountains peaks of more than2000 m asl on one side and deteriorated slate quarries in the other side (Fuertes-Gutieacuterrezamp Fernaacutendez-Martiacutenez 2010)

Field samplingBody temperatures (Tb) and operative temperatures (Te) were recorded simultaneouslyin the field during August 2011 2012 and 2013 in order to avoid the effect of seasonalvariations Length and weight of the studied animals are provided in Table 1 Operativetemperatures (Te) estimate the temperatures that non-thermoregulating lizards wouldreach if they were distributed randomly in their habitat (Hertz Huey amp Stevenson 1993)For recording Te we employed copper models of the same size of lizards (Bakken ampAngilletta 2014) One thermocouple probe was placed into each hollow model andconnected to a data logger HOBO H8 ( RcopyOnset Computer Corporation) programmed totake a temperature record every five minutes The data loggers with models were placedin different microhabitats rock (in different orientations) soil log leaf litter and grassFor measuring Tb we captured lizards by noosing during their daily activity period from0800 to 1800 h GMT (Greenwich Mean Time) On each capture we measured cloacalbody temperature (Tb) immediately after capture (lt30 s after capture) with a Testo Rcopy 925digital thermometer (plusmn01 C precision) We also registered the time of the day the type ofsubstrate the distance from the nearest potential refuge and the height of the microhabitatfrom the floor


For 30 individual lizards (15 I galani and 15 P bocagei) we also recorded these variables(Ta Ts time of the day type of microhabitat height of the point from the floor anddistance to the nearest potential refuge) at four points associated to each capture placein order to get an approach of the habitat structure Each point was 1 m away from thecapture site in the direction of the main four cardinal points (N S E and W) Thus themeasures at random points represent the availability of all variables in the habitat in orderto compare with the values in the microhabitats used by both species We refer to the valuesof these random points as lsquoavailabilityrsquo in the results section

Lizards were sampled under licences of the Castilla y Leoacuten Environmental Agency(EPCYL3202012) The study was conducted in compliance with all ethical standards andprocedures of the University of Salamanca

Preferred temperature rangeThermal preferences of lizards in the laboratory represent the body temperatures thatlizards would achieve in their habitats in the absence of other ecological restrictionsbut temperature (eg Hertz Huey amp Stevenson 1993 Angilletta 2009) The preferredtemperature range of I galani was measured in August 2011 and the preferred temperaturerange of P bocagei was measured in August 2013 All conditions were replicated for bothspecies field area of capture of lizards laboratory conditions and materials (terrariathermometer and lamp) as well as the methodology (thermal gradient and the protocolof measurement) Lizards were housed in individual terraria fed daily with mealworms(Tenebrio molitor) and crickets (Gryllus assimilis) and provided with water ad libitumThe thermal gradient was built in a glass terrarium (100 times 60 times 60 cm) with a 150 Winfrared lamp over one of the sides obtaining a gradient between 20 and 60 C A data ofa preferred body temperature (Tpref) of a lizard was recorded in the cloaca with a digitalthermometer (Testo Rcopy 925) each hour in the period from 0800 to 1800 h (GMT) We used24 adult lizards (12 males 12 females) from each species with 6 hourly measures of Tpref

of each individual lizard The 50 of central values of preferred body temperatures (thatis the interquartile range) was considered as the preferred temperature range to assessthermoregulation as this is a common metric used to assess thermoregulation (HertzHuey amp Stevenson 1993 Blouin-Demers amp Nadeau 2005) After both experiments lizardswere released completely unharmed at their capture sites

Indexes of thermoregulationTo test the null hypothesis of thermoregulation (that is if lizards use microhabitatsrandomly regarding temperature) we followed the protocol developed by Hertz Hueyamp Stevenson (1993) and calculated three indexes of thermoregulation The first is theindex of accuracy of thermoregulation (db) that is the mean of absolute values of thedeviations between each Tb from the preferred temperature range Thus the values of theindex of accuracy of thermoregulation are counterintuitive higher values of db indicatelower accuracy of thermoregulation and vice-versa The second is the index of thermalquality of habitat (de) calculated as the mean of absolute values mean of the deviationsof each Te from the preferred temperature range Accordingly the values of the index


of thermal quality of the habitat are also counterintuitive higher values of de indicate alower thermal quality of the habitat and vice-versa The third is the index of effectivenessof thermoregulation (E) that is calculated as E = 1minus dbde Hence values of E rangefrom 0 to 1 meaning a higher effectiveness of thermoregulation as higher is the value of E(see Hertz Huey amp Stevenson 1993) The effectiveness of thermoregulation was calculatedwith THERMO a Minitab module written by Richard Brown THERMO has been used inprevious studies of thermal ecology (eg Ortega et al 2014) and uses three kinds of inputdata Tb Te and Tpref of the preferred temperature range and was programed to performbootstraps of 100 iterations building pseudo-distributions of three kinds of output valuesthe arithmetic mean of the index of accuracy of thermoregulation (db) the arithmeticmean of the index of thermal quality of the habitat (de) and the arithmetic mean of theindex of effectiveness of thermoregulation (E)

Data analysisAllmeanswere reportedwith standard deviations (sd) Parametric statistics were performedwhen data followed the assumptions of normality and variance homogeneity If theseassumptions were not fulfilled even after log-transformation non-parametric equivalentswere carried out (Crawley 2012 Sokal amp Rohlf 1995) Analyses were conducted using Rversion 313 (R Core Team 2015) Post-hoc comparisons of KruskalndashWallis tests werecomputed with Nemenyi test with the package PMCMR (Pohlert 2014)

RESULTSTemperatures of the habitatThere were significant differences between the Te offered by the different microhabitats(KruskalndashWallis test H = 2669642df = 15 P lt 00001 n= 6082) According to theresults of the post-hoc comparisons of their Te the microhabitats could be classified intofour groups (1) cold microhabitats that were below the preferred temperature range ofboth species as would be south-facing rock in full sun and flat rock soil and the leaf litterin shade (2) mild microhabitats that provided Te within the preferred temperature rangeof both species as would be under rock microhabitats north-facing and the east-facingrock in full sun and flat rock soil and the leaf litter in filtered sun at some hours of the day(3) warm microhabitats that provided Te that exceeded the preferred temperature range ofI galani but felt within the preferred temperature range of P bocagei during some hours ofthe day as would be the microhabitats of flat east-facing and west-facing rock and log infull sun and (4) very warm microhabitats that exceeded the preferred temperature rangeof both species during all day as is the case of grass log leaf litter and soil in full sun (seeFig 2)

Microhabitat selectionBoth species selected microhabitats not-randomly regarding Ta being the mean Ta ofcapture places of lizards higher than the mean Ta available in the habitat (Fig 3) HoweverTa selected by P bocagei were significantly higher than those selected by I galani (Fig 3)In addition both species selected microhabitats with similar Ts higher than that available


Figure 2 Operative temperatures Boxplots of the operative temperatures of the different microhabi-tats of the study area during the daily activity period of lizards Horizontal bands represent the 50 pre-ferred temperature range of Iberolacerta galani (red band) and Podarcis bocagei (yellow band) The dif-ferent letters indicate significant different operative temperatures among microhabitats in the post-hocpaired comparisons of Kruskal Wallis


Figure 3 Comparison of the environmental temperatures of the selected microhabitats of both speciesand the mean availability of the habitat Boxplots of air and substrate temperature of the capture loca-tions of Iberolacerta galani and Podarcis bocagei and the general availability of the habitat Both species se-lected microhabitats with greater mean air temperature than the mean air temperature randomly availablein the habitat (all post-hoc paired comparisons of KruskalndashWallis are significant for the paired compari-son of I galani-P bocagei regarding substrate temperature) Horizontal bands represent the 50 preferredtemperature range of Iberolacerta galani (red band) and Podarcis bocagei (yellow band)

(Fig 3) Regarding the distance to the nearest potential refuge both species selectedmicrohabitats that were closer to potential refuges than the mean habitat availability(I galani mean distance = 1356 plusmn 1152 cm n= 66 P bocagei mean distance =1604 plusmn 1724cm n= 72 availability mean = 3976 plusmn 3130 cm n= 123 KruskalndashWallistest H = 62198 df = 2 P lt 00001 post-hoc comparisons were significant only for Igalani-availability P lt 00001 and P bocagei- availability P lt 00001) I galani selectedmicrohabitats higher than the mean availability while P bocagei selected microhabitats ofsimilar height of the mean available height (I galani height = 1117 plusmn 1824 cm n= 78P bocagei height = 757 plusmn 1670 cm n= 72 availability = 1030 plusmn 2217 cm n = 123KruskalndashWallis testH = 15824 df = 2 P lt 00001 post-hoc comparisons were significantonly for I galani- availability P = 0009 and I galani-Pbocagei P lt 00001)

Both species clearly selected microhabitats with a significantly different frequencythan the abundance of each type of microhabitat (Fig 4) I galani selected microhabitatswith a smaller presence of grass than the randomly available in the habitat (Fisher exacttest P lt 00001) Meanwhile P bocagei also selected soil microhabitats with a greaterproportion than the randomly available in the habitat (Fisher exact test P lt 00001Fig 4) Finally there were statistically significant differences between the two species in theselection of microhabitats (Fisher exact test P lt 00001) especially regarding the higherselection of rocky areas by I galani (Fig 4) Table 2 shows the proportion of Te of thedifferent types of microhabitat that felt below within and above the preferred temperaturerange of each species

Lizard thermoregulationThere were no differences betweenmales and females in the average preferred temperaturesneither in P bocagei (males Tpref= 329plusmn 163 C n= 12 females Tpref= 318plusmn 244 C


Figure 4 Microhabitat preferences of both speciesMicrohabitats where Iberolacerta galani and Podarcisbocagei lizards occurred and availability of the different types of microhabitats measured though randompoints indicated as percentage of observations for each category The category of lsquoother microhabitatsrsquo in-cludes grass and logs

Table 2 Thermal suitability of studied microhabitats for both species Proportion () of the opera-tive temperatures (Te) of the different studied microhabitats that are lower within of higher than the pre-ferred temperature range (PTR) of Iberolacerta galani and Podarcis bocagei during summer in the studyThe microhabitat category of lsquootherrsquo includes grass and logs All microhabitats were measured under allsun situations (full sun filtered sun and shade) so the sun situation is homogeneous among them mak-ing the proportions comparable

Other Soil Leaf litter Rock Total

I galani Lower 98 525 484 461 469 Within 17 35 62 64 51 Higher 885 440 454 475 480P bocagei Lower 118 567 554 538 529 Within 16 41 43 40 85 Higher 866 392 403 387 386

n= 12 ANOVA F122= 1746 P = 0200) nor in I galani (males Tpref= 289 plusmn 048 Cn= 12 females Tpref = 288 plusmn 049 C n= 12 ANOVA F122 = 0118 P = 0734)Thus data of both genders were combined in subsequent analyses The average preferredtemperatures were lower for I galani than for P bocagei (I galani Tpref= 288 plusmn 047 Cn= 24 P bocagei Tpref = 323 plusmn 211 C n= 24 MannndashWhitney U -test U = 4200P lt 00001) Thus the preferred temperature range of I galani was 279ndash297 C and thepreferred temperature range of P bocagei was 301ndash345 C Furthermore the preferredtemperature range of I galani was significantly narrower than the preferred temperaturerange of P bocagei (Levenersquos test W = 33151 P lt 00001)

In the field I galani exhibited lower Tb than P bocagei (I galani Tb= 309 plusmn 239 Cn= 79 P bocagei Tb = 339 plusmn 303 C n= 72 ANOVA F1149 = 45061 P lt 00001Fig 5) The index of thermal quality of habitat (de) was significantly higher for I galanithan for P bocagei (MannndashWhitney U -test U = 240 P lt 00001 Table 3) In addition


Figure 5 Themoregulation of both speciesHistograms of preferred temperatures body temperaturesand operative temperatures of Iberolacerta galani and Podarcis bocagei lizards Horizontal bands representthe 50 preferred temperature range of Iberolacerta galani (red band) and Podarcis bocagei (yellow band)

I galani showed a higher value of the index of thermoregulation accuracy (db ANOVAF1198= 108686 P lt 00001 Table 3) Finally I galani achieved a lower effectiveness ofthermoregulation (MannndashWhitney U -test U = 770 P lt 00001 Table 3)

DISCUSSIONThe preferred temperature range of a species is assumed to approximately reflect the opti-mum range for fitness (Hertz Huey amp Stevenson 1993Martin amp Huey 2008) I galani hasa low and very narrow preferred temperature range (279ndash297 C) being the lowest found


Table 3 Indexes of thermoregulation of both syntopic populationsMean (plusmnsd) values of the indexesof thermal quality of the habitat (de) accuracy of thermoregulation (db) and effectiveness of thermoregu-lation (E) for Iberolacerta galani and Podarcis bocagei living in close syntopy Values of the 95 CI of eachindex are provided in brackets

de ( C) db ( C) E

I galani 936plusmn 003 (92949419) 188plusmn 002 (18481912) 080plusmn 0002 (07950802)P bocagei 830plusmn 002 (82498347) 105plusmn 002 (10121089) 087plusmn 0002 (08690878)

to date in Lacertidae (Bauwens et al 1995Aguado amp Brantildea 2014Ortega Menciacutea amp Peacuterez-Mellado 2016) By contrast the preferred temperature range of P bocagei (301ndash345 C)is significantly higher and wider than that of I galani and both ranges do not even overlapThus our data suggest that I galani would be a cold-adapted thermal specialist species likeother species of the genus Iberolacerta (Martiacuten amp Salvador 1993 Aguado amp Brantildea 2014Žagar et al 2015 Ortega Menciacutea amp Peacuterez-Mellado 2016) while P bocagei would be athermal generalist with preference for warmer temperatures like other species of the genusPodarcis (Bauwens et al 1995 Bauwens Hertz amp Castilla 1996 Capula et al 2014 Ortegaet al 2014) Environmental temperatures are predicted to continuously rise in the moun-tains of the Iberian Peninsula during the coming years (Arauacutejo Thuiller amp Pearson 2006Nogueacutes-Bravo et al 2008) and the difference between being a thermal specialist or a gener-alist will be crucial when determining the vulnerability of a given species to climate change(Martin amp Huey 2008Huey et al 2012) Thermal reactionnorms of fitness are asymmetricfitness gradually increases from the critical minimum temperature up to the physiologicaloptimum just to decline sharply when body temperature exceeds the physiologicaloptimal temperature (Huey amp Stevenson 1979 Angilletta Huey amp Frazier 2010) Dueto the asymmetry of the thermal reaction norm curve an increase in body temperaturesexceeding the optimal temperature leads to a higher reduction of fitness than a similardecrease in body temperatures as predicted by the Jensenrsquos inequality (Martin amp Huey2008Huey et al 2012)Moreover this negative effect of exceeding the optimal temperatureis higher the more specialized the species is (Huey et al 2012) Consequently not onlyI galani preferred temperature range is lower than that of P bocagei and the increaseof environmental temperatures will exceed it before but also their narrower preferredtemperature range suggest that the negative effects of exceeding their optimal temperatureswould be more detrimental to I galani (Martin amp Huey 2008 Huey et al 2012)

Given a scenario of continued warming there are three alternatives for mountainlizards to adapt to shift their ranges or to extinguish (Berg et al 2010 Gunderson ampStillman 2015) The ability of I galani to disperse is limited by the peaks of mountainsso that sooner or later lizards migrating upwards to avoid overheating would run out ofspace to migrate (Arauacutejo Thuiller amp Pearson 2006Huey et al 2012) Therefore mountainlizards would only avoid extinction by adapting to warmer environments It was recentlydiscovered that the plasticity of the critical temperatures has little capacity for changeeven lesser for the critical thermal maximum so it will probably not be enough to keeppace with the rate of environmental warming (Gunderson amp Stillman 2015) Howeverthe ability of ectotherms to behaviorally buffer environmental temperature changes could


probably mitigate the negative impact of global warming in fitness of mountain lizardsfor a while (Kearney Shine amp Porter 2009 Huey et al 2012) Their high effectiveness ofthermoregulation and their ability to select the most suitable microhabitats suggest that Igalani may have the capacity for behavioral buffering of the impact of climate warmingFurthermore the habitat under study is heterogeneous with a mosaic of microhabitatsoffering different operative temperatures some colder some warmer and some equal tothe preferred temperature range of this species Hence the habitat provides I galani atleast for some time the possibility to use its behavioral adjustments to buffer the impactof global warming (Huey et al 2012 Sears amp Angilletta 2015) It would be also possiblethat the adaptation of the thermal preferences would contribute to the buffering of thetemperature rising at least for a while (eg Gvoždiacutek 2011)

P bocagei select microhabitats of soil and leaf litter with higher frequency than therandomly available in its habitat which are significantly warmer than the rocky substratespreferred by I galani Furthermore the proportion of operative temperatures fitting thepreferred temperature range of P bocagei exceeds nowadays that fitting the preferredtemperature range of I galani In general air temperature diminishes as elevation rises(eg Koumlrner 2007) Nonetheless this montane habitat is at present more suitable forP bocagei than for I galani In addition the warm habitat condition leads I galani lizardsto achieve a lower effectiveness of thermoregulation than P bocagei which may entail lessphysiological performance and fitness for I galani Hence our results indicate that thethermophilic species has taken a better advantage of the current thermal environmentthan the cold-adapted species maybe favoured by climate warming Moreover generalistlizard species can efficiently exploit high-elevation cold habitats by means of differentadaptations (Zamora-Camacho Reguera amp Moreno-Rueda 2015) which in this situationcould increase I galani competitive exclusion risk Monasterio et al (2009) reported ahigher effectiveness of thermoregulation of Iberolacerta cyreni than Podarcis muralis in highmountain areas a situation that should be the usual but maybe reverting as we reporthere given that the mountain habitats are becoming warmer However we do not knowif I galani and P bocagei compete for food refuges or any other resources Thus thegeneralist could expand without the specialist being affected unless the specialist wouldbe compromised by the new conditions and that would not be qualified as displacementinstead the two species would be reacting independently to climate change

Iberolacerta lizards appear to have not adapted to warm conditions in the past after thelast glaciation and consequently they were relegated to areas of higher altitude (CarranzaArnold amp Amat 2004 Crochet et al 2004 Mouret et al 2011) Hence it is unlikely thatthey will be able to cope with the current climatic change which entails faster warming thanthe species have ever met before (Diffenbaugh amp Field 2013) On the contrary P bocageilizards remained in warm refugia during past cold periods and probably colonized theircurrent distribution within last 10000 years (Pinho et al 2011) In short we are probablydocumenting with human induced climate change a remake of past biogeographic spreadof generalist lizard species and the concomitant restriction of cold-adapted species to colderareas


ACKNOWLEDGEMENTSWe thank the people of La Cabrera Baja for their hospitality during the fieldwork periodsWe also thank Mary Trini Menciacutea and Joe McIntyre for linguistic revision and MarioGarrido Ana Peacuterez-Cembranos Gonzalo Rodriacuteguez and Alicia Leoacuten for support duringthe writing process

ADDITIONAL INFORMATION AND DECLARATIONS

FundingFinancial support was provided to ZO and AM by predoctoral grants of the Universityof Salamanca (FPI program) This work was also supported by the research projectsCGL2009-12926-C02-02 and CGL2012-39850-CO2-02 from the Spanish Ministry ofScience and Innovation The funders had no role in study design data collection andanalysis decision to publish or preparation of the manuscript

Grant DisclosuresThe following grant information was disclosed by the authorsUniversity of SalamancaSpanish Ministry of Science and Innovation CGL2009-12926-C02-02 CGL2012-39850-CO2-02

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Zaida Ortega performed the experiments analyzed the data wrote the paper preparedfigures andor tablesbull Abraham Menciacutea performed the experiments reviewed drafts of the paperbull Valentiacuten Peacuterez-Mellado conceived and designed the experiments reviewed drafts of thepaper

Animal EthicsThe following information was supplied relating to ethical approvals (ie approving bodyand any reference numbers)

Lizards were sampled under licences of the Castilla y Leoacuten Environmental Agency(EPCYL3202012)

Data AvailabilityThe following information was supplied regarding data availability

The raw data has been supplied as Supplemental Information

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj2085supplemental-information


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lizard Iberolacerta cyreni) influence of thermal environmentand associated costsCanadian Journal of Zoology 92955ndash964 DOI 101139cjz-2014-0096

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Arribas O Carranza S Odierna G 2006 Description of a new endemic species ofmountain lizard from Northwestern Spain Iberolacerta galani sp nov (squa-matalacertidae) Zootaxa 22401ndash55

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Bauwens D Garland T Castilla AM Van Damme R 1995 Evolution of sprint speed inlacertid lizards morphological physiological and behavioral covariation Evolution49848ndash863 DOI 1023072410408

Bauwens D Hertz PE Castilla AM 1996 Thermoregulation in a lacertid lizard therelative contributions of distinct behavioral mechanisms Ecology 771818ndash1830DOI 1023072265786

BergMp Kiers ET Driessen G Van Der HeijdenM Kooi BW Kuenen F LieftingMVerhoef HA Ellers J 2010 Adapt or disperse understanding species persistence in achanging world Global Change Biology 16587ndash598DOI 101111j1365-2486200902014x

Bestion E Clobert J Cote J 2015 Dispersal response to climate change scaling down tointraspecific variation Ecology Letters 181226ndash1233 DOI 101111ele12502

Blouin-Demers G Nadeau P 2005 The cost-benefit model of thermoregulationdoes not predict lizard thermoregulatory behaviour Ecology 86560ndash566DOI 10189004-1403

Capula M Corti C Lo Cascio P Luiselli L 2014 Thermal ecology of the aeolian walllizard Podarcis raffonei what about body temperatures in microinsular lizards InCapula M Corti C eds Scripta Herpetologica Studies on Amphibians and Reptilesin honour of Benedetto Lanza Monographie della Societas Herpetologica ItalicamdashIII Latina Edizioni Belbedere 39ndash47


Carranza S Arnold NE Amat F 2004 DNA phylogeny of Lacerta (Iberolacerta) andother lacertine lizards (Reptilia Lacertidae) did competition cause long-termmountain restriction Systematics and Biodiversity 257ndash77DOI 101017S1477200004001355

Carvalho SB Brito JC Crespo EJ PossinghamHP 2010 From climate change predic-tions to actionsmdashconserving vulnerable animal groups in hotspots at a regional scaleGlobal Change Biology 163257ndash3270 DOI 101111j1365-2486201002212x

Chen IC Hill JK Ohlemuumlller R Roy DB Thomas CD 2011 Rapid range shifts ofspecies associated with high levels of climate warming Science 3331024ndash1026DOI 101126science1206432

ComasM Escoriza D Moreno-Rueda G 2014 Stable isotope analysis reveals variationin trophic niche depending on altitude in an endemic alpine gecko Basic and AppliedEcology 15362ndash369 DOI 101016jbaae201405005

Crawley MJ 2012 The R book 2nd edition Chichester John Wiley amp SonsCrochet PA Chaline O Surget-Groba Y Debain C CheylanM 2004 Speciation

in mountains phylogeography and phylogeny of the rock lizards genus Ibero-lacerta (Reptilia Lacertidae)Molecular Phylogenetics and Evolution 30860ndash866DOI 101016jympev200307016

Crossman ND Bryan BA Summers DM 2012 Identifying priority areas for reducingspecies vulnerability to climate change Diversity and Distributions 1860ndash72DOI 101111j1472-4642201100851x

Diffenbaugh NS Field CB 2013 Changes in ecologically critical terrestrial climateconditions Science 341486ndash492 DOI 101126science1237123

Fuertes-Gutieacuterrez I Fernaacutendez-Martiacutenez E 2010 Geosites inventory in the LeonProvince (Northwestern Spain) a tool to introduce geoheritage into regionalenvironmental management Geoheritage 257ndash75 DOI 101007s12371-010-0012-y

Galaacuten P 1994 Seleccioacuten del microhaacutebitat en una poblacioacuten de Podarcis bocagei delnoroeste ibeacuterico Dontildeana Acta Vertebrata 21153ndash168

Galaacuten P 2004 Structure of a population of the lizard Podarcis bocagei in northwestSpain variations in age distribution size distribution and sex ratio Animal Biology5457ndash75 DOI 101163157075604323010051

Groves CR Game ET AndersonMG Cross M Enquist C Ferdantildea Z Girvetz EGondor A Hall KR Higgins J Marshall R Popper K Schill S Shafer SL 2012Incorporating climate change into systematic conservation planning BiodiversityConservation 211651ndash1671 DOI 101007s10531-012-0269-3

Gunderson AR Stillman JH 2015 Plasticity in thermal tolerance has limited potential tobuffer ectotherms from global warming Proceedings of the Royal Society of London BBiological Sciences 282 20150401 DOI 101098rspb20150401

Gvoždiacutek L 2011 Plasticity of preferred body temperatures as means of coping withclimate change Biology Letters 8(2)262ndash265 DOI 101098rsbl20110960

Hertz PE Huey RB Stevenson RD 1993 Evaluating temperature regulation by field-active ectothermsthe fallacy of the inappropiate question The American Naturalist142796ndash818 DOI 101086285573


Huey RB KearneyMR Krockenberger A Holtum JA Jess MWilliams SE 2012 Pre-dicting organismal vulnerability to climate warming roles of behaviour physiologyand adaptation Philosophical Transactions of the Royal Society of London B BiologicalSciences 3671665ndash1679 DOI 101098rstb20120005

Huey RB Stevenson RD 1979 Integrating thermal physiology and ecology of ec-totherms a discussion of approaches American Zoologist 19357ndash366DOI 101093icb191357

KearneyM Shine R PorterWP 2009 The potential for behavioral thermoregulationto buffer lsquolsquocold-bloodedrsquorsquo animals against climate warming Proceedings of theNational Academy of Sciences of the United States of America 1063835ndash3840DOI 101073pnas0808913106

Koumlrner C 2007 The use of lsquoaltitudersquo in ecological research Trends in Ecology andEvolution 22569ndash574 DOI 101016jtree200709006

Lord J Whitlatch R 2015 Predicting competitive shifts and responses to climate change-based on latitudinal distributions of species assemblages Ecology 961264ndash1274DOI 10189014-04031

Maiorano L Amori G Capula M Falcucci A Masi M Montemaggiori A Pottier JPsomas A Rondinini C Russo D Zimmermann NE Boitani L Guisan A 2013Threats from climate change to terrestrial vertebrate hotspots in Europe PLoS ONE8e74989 DOI 101371journalpone0074989

Martiacuten J Salvador A 1993 Thermoregulatory behaviour of rock lizards in response totail loss Behaviour 124123ndash136 DOI 101163156853993X00533

Martin TL Huey RB 2008Why lsquolsquosuboptimalrsquorsquo is optimal Jensenrsquos inequalityand ectotherm thermal preferences The American Naturalist 171E102ndashE118DOI 101086527502

McCain CM 2010 Global analysis of reptile elevational diversity Global Ecology andBiogeography 19541ndash553 DOI 101111j1466-8238201000528x

Menciacutea A Ortega Z Peacuterez-Mellado V 2016 Chemical discrimination of sympatricsnakes by the mountain lizard Iberolacerta galani (Squamata Lacertidae) TheHerpetological Journal 26151ndash157

Monasterio C Salvador A Iraeta P Diacuteaz JA 2009 The effects of thermal biologyand refuge availability on the restricted distribution of an alpine lizard Journal ofBiogeography 361673ndash1684 DOI 101111j1365-2699200902113x

Moreno-Rueda G Pleguezuelos JM PizarroMMontori A 2012 Northward shifts ofthe distributions of Spanish reptiles in association with climate change ConservationBiology 26278ndash283 DOI 101111j1523-1739201101793x

Mouret V Guillaumet A CheylanM Pottier G Ferchaud AL Crochet PA 2011The legacy of ice ages in mountain species post-glacial colonization of mountaintops rather than current range fragmentation determines mitochondrial geneticdiversity in an endemic pyrenean rocklizard Journal of Biogeography 381717ndash1731DOI 101111j1365-2699201102514x

MuntildeozMM Stimola MA Algar AC Conover A Rodriguez AJ LandestoyMA BakkenGS Losos JB 2014 Evolutionary stasis and lability in thermal physiology in a group


of tropical lizards Proceedings of the Royal Society of London B Biological Sciences281 20132433 DOI 101098rspb20132433

Nogueacutes-Bravo D ArauacutejoMB Lasanta T Moreno JTL 2008 Climate change inmediterranean mountains during the 21st century AMBIO A Journal of the HumanEnvironment 37280ndash285 DOI 1015790044-7447(2008)37[280CCIMMD]20CO2

Ortega Z Menciacutea A Peacuterez-Mellado V 2016 The peak of thermoregulation effectivenessthermal biology of the Pyrenean rock lizard Iberolacerta bonnali (SquamataLacertidae) Journal of Thermal Biology 5677ndash83DOI 101016jjtherbio201601005

Ortega Z Peacuterez-Mellado V GarridoM Guerra C Villa-Garciacutea A Alonso-FernaacutendezT 2014 Seasonal changes in thermal biology of Podarcis lilfordi (Squamata Lacer-tidae) consistently depend on habitat traits Journal of Thermal Biology 3932ndash39DOI 101016jjtherbio201311006

Parmesan C 2006 Ecological and evolutionary responses to recent climate changeAnnual Review of Ecology Evolution and Systematics 37637ndash669DOI 101146annurevecolsys37091305110100

Peacuterez-Mellado V 1998 Podarcis bocagei (Seoane 1884) In Salvador A coord RamosMA et al eds Fauna Ibeacuterica vol 10 Reptiles Madrid Museo Nacional de CienciasNaturales 243ndash257

Pinho C Kaliontzopoulou A Harris DJ Ferrand N 2011 Recent evolutionary his-tory of the iberian endemic lizards Podarcis bocagei (Seoane 1884) and Podarciscarbonelli Peacuterez-Mellado 1981 (Squamata Lacertidae) revealed by allozyme andmicrosatellite markers Zoological Journal of the Linnean Society 162184ndash200DOI 101111j1096-3642201000669x

Pohlert T 2014 The pairwise multiple comparison of mean ranks package (PMCMR)R package Available at httpscranr-projectorgwebpackagesPMCMRvignettesPMCMRpdf (accessed 30 January 2016)

R Core Team 2015 R a language and environment for statistical computing Vienna RFoundation for Statistical Computing

Sears MW Angilletta MJ 2015 Costs and benefits of thermoregulation revisited boththe heterogeneity and spatial structure of temperature drive energetic costs TheAmerican Naturalist 185E94ndashE102 DOI 101086680008

Sinervo B Meacutendez-de-la Cruz F Miles DB Heulin B Bastiaans E Villagraacuten-Santa CruzM Lara-Resendiz R Martiacutenez-Meacutendez N Calderoacuten-Espinosa MLMeza-Laacutezaro RN Gadsden H Aacutevila LJ MorandoM De la Riva I Sepuacutelveda PVDuarte-Rocha CF Ibarguumlengoytiacutea NR Aguilar-Puntriano C Massot M LepetzV Oksanen TA Chapple DG Bauer AM BranchWR Clobert J Sites JWJ 2010Erosion of lizard diversity by climate change and altered thermal niches Science328894ndash899 DOI 101126science1184695

Sokal RR Rohlf FJ 1995 Biometry the principles and practice of statistics in biologicalresearch New York State University of New York at Stony Brook


UrbanMC Tewksbury JJ Sheldon KS 2012 On a collision course competition anddispersal differences create no-analogue communities and cause extinctions duringclimate change Proceedings of the Royal Society of London B Biological Sciences2792072ndash2080 DOI 101098rspb20112367

Žagar A CarreteroM Osojnik N Sillero N Vrezec A 2015 A place in the suninterspecific interference affects thermoregulation in coexisting lizards BehavioralEcology and Sociobiology 691127ndash1137 DOI 101007s00265-015-1927-8

Zamora-Camacho FJ Reguera S Moreno-Rueda G 2015 Thermoregulationin the lizard Psammodromus algirus along a 2200-m elevational gradient inSierra Nevada (Spain) International Journal of Biometeorology 60687ndash697DOI 101007s00484-015-1063


(eg Muntildeoz et al 2014 Gunderson amp Stillman 2015) and (2) living in mountaintopsthey lack colder areas to migrate (Arauacutejo Thuiller amp Pearson 2006 Berg et al 2010McCain 2010) In addition mountain species tend to be cold-specialists (eg Aguado ampBrantildea 2014) which makes themmore vulnerable because the decline of fitness when bodytemperatures exceed the optimum temperature is greater in narrower thermal reactionnorms (Martin amp Huey 2008 Huey et al 2012 Gunderson amp Stillman 2015) Mountainlizards could also be threatened by potential displacement by thermal generalist specieswith a broader distribution at the surrounding lowlands that may ascend in altitude aswarming increases (Arauacutejo Thuiller amp Pearson 2006 Huey et al 2012 Comas Escorizaamp Moreno-Rueda 2014) An expansion both in altitude and latitude due to climatechange has already been documented for several species (Parmesan 2006 Sinervo et al2010 Chen et al 2011 Moreno-Rueda et al 2012 Bestion Clobert amp Cote 2015) Thesefactors altogether would place high-mountain lizards among the most vulnerable animalsworldwide especially mountain lizards of the Iberian Peninsula due to the higher warmingand drought predicted for these areas (Nogueacutes-Bravo et al 2008 Arauacutejo et al 2011Maiorano et al 2013) The study of the thermal ecology of these mountain lizards aswell as the comparison with their potential competitors would be useful to design theconservation measures required to preserve the species (Urban Tewksbury amp Sheldon2012 Lord amp Whitlatch 2015)

Some studies had assessed thermal ecology of other Iberolacerta lizards (Monasterio etal 2009 Aguado amp Brantildea 2014 Ortega Menciacutea amp Peacuterez-Mellado 2016) We studied thethermal ecology of the Leoacuten rock lizard I galani a mountain lizard living in its historicalrange and the Bocagersquos wall lizard P bocagei that has expanded its altitudinal range to thestudy area in recent years Both are medium-size insectivorous and heliothermic lacertidlizards endemic from the northwestern of Spain Their distribution ranges are considerablydifferent (Fig 1) I galani is restricted to high-mountain climate isolated areas from 1300to 2500 m asl (meters above the sea level Arribas Carranza amp Odierna 2006 MenciacuteaOrtega amp Peacuterez-Mellado 2016) whereas P bocagei inhabits a variety of habitats from thesea level to 1900 m asl habitats (Galaacuten 1994 Peacuterez-Mellado 1998 Galaacuten 2004) Howeverboth live in close syntopy in the study area nowadays fully mixed in the same habitat Wecompared the thermal requirements of the two species in the laboratory and the thermaltraits of their habitat in order to study if mountain habitats are increasingly unsuitable formountain lizards and may be favoring the expansion of thermal generalists instead Wefirst aim to assess and compare the thermal preferences and behavioral thermoregulationof both species (Hertz Huey amp Stevenson 1993 Angilletta 2009) Then we studied theirselection of microhabitats and we compared the thermal suitability of the habitat for bothspecies under the current climatic conditions

MATERIALS amp METHODSStudy areaThe study area was in the Natural Monument lsquolsquoLago de La Bantildearsquorsquo (Leoacuten province Spain4215primeN 629W) It was an area surrounding a glacial lake located at 1400m asl formed by




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are mountain habitats becoming more suitable for …lizards were housed in individual terraria, fed...

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