Thermal physiology of Amazonian lizards (Reptilia: Squamata)

23 Pages·2017·3.33 MB·English

RESEARCHARTICLE
Thermal physiology of Amazonian lizards
(Reptilia: Squamata)
LuisaM.Diele-Viegas1¤a‡*,LaurieJ.Vitt2☯,BarrySinervo3☯,GuarinoR.Colli4☯,Fernanda
P.Werneck5☯,DonaldB.Miles6☯,WilliamE.Magnusson5☯,JuanC.Santos7☯¤b,Carla
M.Sette3☯,GabrielH.O.Caetano3‡,EmersonPontes5‡,TeresaC.S.A´vila-Pires‡1
1 MuseuParaenseEm´ılioGoeldi,Bele´m,Para´,Brazil,2 SamNobleMuseum,UniversityofOklahoma,
Norman,Oklahoma,UnitedStatesofAmerica,3 UniversityofCaliforniaSantaCruz,SantaCruz,California,
UnitedStatesofAmerica,4 UniversidadedeBrasilia,Brasilia,DistritoFederal,Brazil,5 InstitutoNacionalde
PesquisasdaAmazoˆnia,Manaus,Amazonas,Brazil,6 OhioUniversity,Athens,Ohio,UnitedStatesof
a1111111111
America,7 BrighamYoungUniversity,Provo,Utah,UnitedStatesofAmerica
a1111111111
a1111111111 ☯Theseauthorscontributedequallytothiswork.
a1111111111 ¤a Currentaddress:UniversidadedoEstadodoRiodeJaneiro,RiodeJaneiro,RiodeJaneiro,Brazil
a1111111111 ¤b Currentaddress:St.John’sUniversity,Queens,NewYork,UnitedStatesofAmerica
‡GHOCandEPalsocontributedequallytothiswork.LDVandTCSAParejointseniorauthorsonthiswork.
*[email protected]
Abstract
OPENACCESS
Citation:Diele-ViegasLM,VittLJ,SinervoB,Colli Wesummarizethermal-biologydataof69speciesofAmazonianlizards,includingmodeof
GR,WerneckFP,MilesDB,etal.(2018)Thermal
thermoregulationandfield-activebodytemperatures(T ).Wealsoprovidenewdataonpre-
physiologyofAmazonianlizards(Reptilia: b
Squamata).PLoSONE13(3):e0192834.https:// ferredtemperatures(Tpref),voluntaryandthermal-toleranceranges,andthermal-perfor-
doi.org/10.1371/journal.pone.0192834 mancecurves(TPC’s)for27speciesfromninesitesintheBrazilianAmazonia.Wetested
Editor:MichaelSears,ClemsonUniversity,UNITED forphylogeneticsignalandpairwisecorrelationsamongthermaltraits.Wefoundthatspe-
STATES ciesgenerallycategorizedasthermoregulatorshavethehighestmeanvaluesforallthermal
Received:March31,2017 traits,andbroaderrangesforTb,criticalthermalmaximum(CTmax)andoptimal(Topt)tem-
peratures.SpeciesgenerallycategorizedasthermoconformershavelargerangesforT ,
Accepted:January16,2018 pref
criticalthermalminimum(CT ),andminimumvoluntary(VT )temperaturesforperfor-
min min
Published:March7,2018
mance.Despitethesedifferences,ourresultsshowthatallthermalcharacteristicsoverlap
Copyright:©2018Diele-Viegasetal.Thisisan betweenbothgroupsandsuggestthatAmazonianlizardsdonotfitintodiscretethermoreg-
openaccessarticledistributedunderthetermsof
ulatorycategories.Thetraitsareallcorrelated,withtheexceptionsof(1)T ,whichdoes
theCreativeCommonsAttributionLicense,which opt
permitsunrestricteduse,distribution,and notcorrelatewithCTmax,and(2)CTmin,andcorrelatesonlywithTopt.Weakphylogenetic
reproductioninanymedium,providedtheoriginal signalsforT ,T andVT indicatethatthesecharactersmaybeshapedbylocalenvi-
b pref min
authorandsourcearecredited.
ronmentalconditionsandinfluencedbyphylogeny.Wefoundthatopen-habitatspeciesper-
DataAvailabilityStatement:Allrelevantdataare formwellunderpresentenvironmentalconditions,withoutexperiencingdetectablethermal
withinthepaper,itsSupportingInformationfiles,
stressfromhighenvironmentaltemperaturesinducedinlabexperiments.Forforest-dwell-
andavailableatdoi:10.6084/m9.figshare.5293756.
inglizards,weexpectwarmingtrendsinAmazoniatoinducethermalstress,astempera-
Funding:Thisworkwassupportedby
turessurpassthethermaltolerancesforthesespecies.
Coordenac¸ãodeAperfeic¸oamentodePessoalde
N´ıvelSuperior-graduatefellowshiptoLDVand
financialsupporttoGRC(http://www.capes.gov.br/
):Allowedthedevelopmentoftheresearchandthe
datacollection.ConselhoNacionalde
DesenvolvimentoCient´ıficoeTecnolo´gico-
researchfellowshiptoTAPandfinancialsupportto
FPW(475559/2013-4)(http://cnpq.br/):Allowed
PLOSONE|https://doi.org/10.1371/journal.pone.0192834 March7,2018 1/23
ThermalphysiologyofAmazonianlizards
thedatacollection.PVE(PesquisadorVisitante Introduction
Especial)grantfromCNPq(http://cnpq.br/)–BRS:
Bodytemperature(T )inectothermsinfluencesallphysiologicalandbehavioralprocesses
Allowedthedevelopmentoftheresearch. b
Fundac¸ãodeAmparoàPesquisadoAmazonas– [1].Consequently,maintenanceofTbwithinsuitablelimitsisessentialforectothermssurvival
financialsupporttoFPWandWM(FAPEAM, [2].ThermoregulatorsactivelymaintainT withinarestrictedrangeoftemperaturesby
b
062.00665/2015)(http://www.fapeam.am.gov.br/): heliothermy,i.e.,bybaskinginthesun,orbythigmothermy,i.e.,bycontactwithwarmsur-
Allowedthestudydesignanddecisiontopublish.
faces[3].Thermoconformersdonotactivelythermoregulate,sotheirT parallelsfluctuations
PartnershipsforEnhancedEngagementin b
intheenvironmentaltemperature[1,4].However,nolizardspecieshasbeenshowntobea
ResearchfromtheU.S.NationalAcademyof
completethermoconformer;allwillmovetoavoidunfavorableextremetemperatures.This
SciencesandU.S.AgencyofInternational
Development(PEERNAS/USAIDPGA- categoryisoftenusedforspeciesthatselectareaswithrelativelyuniformtemperatures,suchas
2000005316)–financialsupporttoGRCandFPW shadedforest,whereactivethermoregulationisnotneededtomaintainrelativelystablebody
(http://sites.nationalacademies.org/pga/peer/index.
temperatures.Usingastrictlythermoconformingstrategyrequiresthatspecieshavebroad
htm):Allowedthedevelopmentoftheresearchand
thermaltolerances[1],andexperiencehighvariationinT throughouttheday,seasonand
thedecisiontopublish.Fundac¸ãodeAmparoà b
geographicrange.
PesquisadoPara´-ICAAFnumber011/2012
SISBIOTAHerpeto-Helminto–financialsupportto Inthefield,lizardsareusuallyactiveatarestrictedrangeofTb.Itiscommonlyassumed
LDVandTAP(http://www.fapespa.pa.gov.br/): thatthesetemperaturesrepresenttheiractualthermalpreferences[5].However,laboratory
Allowedthedatacollection.(cid:3)Fundac¸ãodeAmparoà experimentsshowthatthevarianceinT rangeobservedinnaturefortropicallizardsexceeds
b
PesquisadoDistritoFederal(FAPDF)-financial
boththepreferredT andthevoluntaryT rangeobservedwhentheanimalsaresubjectedto
supporttoGRC(http://www.fap.df.gov.br/<http:// b b
thermalgradients[6–7].Consequently,tropicallizardsmayalreadybeexperiencingT ’sator
www.fap.df.gov.br/>)(cid:3)-Allowedthedata b
abovetheirphysiologicaloptima[8],puttingthemdangerouslyclosetotheirupperthermal
collection.NationalScienceFoundation–Emerging
Frontiers[grantnumber1241885,Collaborative thresholds.Theseupperthermallimitsarelikelytobeexceededinthenextfewdecadesasa
Research:“QuantifyingClimate-forcedExtinction consequenceofclimatechange[9].AnalternativeinterpretationisthatpreferredT andvol-
b
RisksforLizards,Amphibians,Fishes,andPlants”] untaryT reflectnotonlyphysiologicallimits,butarealsotailoredtospecificactivities,suchas
b
–LDV,BRS,GRCandFPW(https://www.nsf.gov/):
digestion,reproductionandforagingfordifferenttypesofprey[1],andthatlaboratorystudies
Allowedthedatacollection,analysisandreparation
donotfullyreflecttherangeofmotivationalstates.Fieldactivitytemperaturesmayvarysea-
ofthemanuscript.NationalScienceFoundation–
EmergingFrontiers[grantnumber241848]–BRS sonally,independentofvariationinenvironmentaltemperatures(e.g.,[10]).
andDBM:Allowedthedatacollection,analysisand Theinfluenceofambienttemperatureonkeyphysiologicaltraitsisdescribedbythermal
preparationofthemanuscript.ResearchCouncil performancecurves(TPC)[2].Aspecies’thermalsensitivitycanbevisualizedandquantified
viaaGeorgeLynnCrossResearchProfessorship
throughTPCs,whichrevealseveralimportantthermalpropertiesofectotherms.Theseinclude
oftheUniversityofOklahomaandtheSamNoble
theoptimaltemperature(T ),formaximalanimalperformance;thebreadthoftemperatures
MuseumsupporttoLJV(http://samnoblemuseum. opt
ou.edu/):Allowedthedecisiontopublish. thatresultsinaspeciesperformingat(cid:21)80%ofitsoptimalcapacity(B80);andthethermaltol-
erancerange,whichisthedifferencebetweenthecriticalthermalminimumandmaximum
Competinginterests:Theauthorshavedeclared
temperatures(CT andCT ),i.e.,theextremetemperaturesthatanindividualcanmain-
thatnocompetinginterestsexist. min max
tainlocomotorfunction[11].T canvarywithinandamongspeciesandvariesamongphysi-
opt
ologicaltraits,accordingtothehypothesisofmultiplephysiologicaloptima[1,12].Locomotor
performanceisoneofthebest-studiedtraitsinthermalphysiology,becauseitisrelatedtoDar-
winianfitnessandpresumablyreflectstheabilitytoescapefrompredators,captureprey,and
reproduce[13].TPCsarealsousefulinassessingextinctionriskofectotherms.Becauseglobal
warmingmayalterthespatialdistributionofpreferredmicroclimates[14],animalsthatrely
onbehavioralthermoregulationmayexperienceareductioninthetimeavailableforactivity
duringperiodswhenpreferredmicroclimatesbecometooraretolocatewithoutoverheating
[15].Restrictioninactivitytimecanresultinextirpationorextinctioniftheremainingtimeis
insufficienttoperformallthenecessaryfunctionsforsuccessfulbreedingandrecruitment
[16].
Amazoniaisabiogeographicregionpredictedtobestronglyaffectedbyclimatechange
[17–18].ItcoversabouteightmillionsquarekilometersspreadovernineSouthAmerican
countries[19].Currentestimatessuggestthatatleast210speciesoflizardsoccurintheAma-
zon,althoughtheactualdiversityispoorlyknown[20–21].Observedtrendsintheregion’scli-
mateincludeanoverallreductioninprecipitationandincreaseddurationandintensityof
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ThermalphysiologyofAmazonianlizards
droughts,especiallyinsouthernAmazonia[22],whereclimatechangeinteractionswithland-
usechangearestronger[23–24].Recentstudiesindicatealong-termdecreasingtrendofcar-
bonaccumulationinAmazoniaduetoincreasedtreeturnoverandmortalityrates[25].More-
over,increaseddrynessmayresultinlarge-scalereductionsinbiomass,carbonuptakeandnet
primaryproductivity[26].Somemodelssuggestthatthesechangesmayinducebiomeshiftsin
Amazonia,withtheforestbeingreplacedbydriervegetationassociations,suchasseasonalfor-
estsandsavannas[27].Therefore,recentandprojectedclimatetrendsinAmazoniawilllikely
resultinamoreopencanopyandincreasedambienttemperatureforforest-dwellinglizards.
DespitethevastnessandcomplexityofAmazonianhabitats,thermal-physiologydataforAma-
zonianlizardsarelimited,withmoststudiesscatteredamongthemajorgroupsofSquamata.
Mostdataarefocusedonreportsoffield-activeT andtherehavebeenfewcontrolledexperi-
b
mentsonpreferredoroptimalT .
b
Weaimtoprovidethefirstcomprehensivesummaryofthermalphysiologycharacteristics
ofAmazonianlizards,whichisessentialtoenhanceourunderstandingoftheeffectsofglobal
warmingoncurrentandfuturelizarddiversityinthismegadiverseregion.Wefirstcharacter-
izepatternsofvariationinT ofAmazonianlizards(includingsomespeciesthatoccur
bs
peripherally,attheecotonebetweentheAmazonianrainforestandthesavanna-likeCerrado,
anecophysiologicaltensioninterface).Wealsoprovidenewdataonthethermalbiologyof
someofthesespeciesandsummarizetheinformationonlizards’modesofthermoregulation.
Moreover,wenextanalyzeevolutionarytrendsamongthermalandphysiologicaltraitsby
examiningtheconsistencyoftraitvariationwithphylogeny(i.e.,phylogeneticsignal)andthe
correlationsamongtraitsaftercontrollingfortheinfluenceofphylogeny.
Materialandmethods
Literaturereview
WecarriedoutaliteraturesurveyfordataonsevenphysiologicaltraitsofAmazonianlizards:
field-activeT ,preferredtemperature(T ),minimumandmaximumvoluntarytempera-
b pref
tures(VT andVT ),criticalthermalminimumandmaximum(CT ,CT )andthe
min max min max
optimaltemperatureforlocomotorperformance(T ).OnlydataonT wereavailable.
opt b
BecausesomespecieshavedistributionsextendingbeyondAmazoniaintootherbiomes,our
reviewextendedbeyondAmazonia,andincludedspeciesfromtheAtlanticRainforest,Caa-
tinga,andCerradoregionsofBrazil,aswellastheLavrado,asavannaenclaveinnortheastern
Roraima,Brazil.WealsoincludeddatafromlizardsoccurringintropicalforestsofCentral
Americathathavesimilarecophysiologicaltraits.Specieswereclassifiedasthermoregulators
orthermoconformersbasedonwhetherthestudiesindicatedtheywereheliotherms(thermo-
regulators)ornon-heliotherms(definedhereasthermoconformers).Wealsoreviewedthelit-
eraturetosearchforsubstrate(T )andair-temperature(T )dataassociatedwithT ,and
sub air b
obtained45studiesfromthelast50years,withreportedT ’sfrom62speciesoccurringin
b
Amazonia.
Fielddata
Wecompletedourdatasetwithdatacollectedbytheauthorsthroughouttheyear.First,we
includedT dataoneightspeciescollectedfrom1993to1999insevenlocalitiesinAmazonia:
b
Estacio´nBiolo´gicadelaPontif´ıciaUniversidadCato´lica(Quito),withintheReservadePro-
duccio´nFaun´ısticaCuyabeno(Sucumb´ıosProvince,Ecuador,0˚0’N,76˚10’W);Jurua´River
Basin,ca.5kmnorthofPortoWalter(Acre,Brazil,8˚15’S,72˚46’W);ItuxiRiver(Amazonas,
Brazil,8˚20’S,65˚43’W);30kmNWofCaracara´ı(Roraima,Brazil,2˚50’N,60˚40’W);Parque
EstadualGuajara´–Mirim,ontheFormosoRiver(Rondoˆnia,Brazil,10˚19’S,72˚47’W);SEof
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ThermalphysiologyofAmazonianlizards
Fig1.Thermaltraits’samplinglocalities.Body-temperaturedatawerecollectedbetween1993and1999andthermalpreference
andperformancedatawerecollectedbetween2014and2016.Lizardsareillustrativeoftheelevenfamiliesfoundinthefield.
Numbersarerepresentativeofthelocalities,asfollows:1)30kmNWofCaracara´ı(Roraima,Brazil,2˚50’N,60˚40’W);2)Floresta
NacionaldoAmapa´(Amapa´,Brazil,0˚55’N,51˚36’W);3)Estacio´nBiolo´gicadelaPontif´ıciaUniversidadCato´lica(Sucumb´ıos
Province,Quito,Ecuador,0˚0’N,76˚10’W);4)FlorestaNacionaldeCaxiuanã(Para´,Brazil,1˚44’S,51˚27’W);5)YasuniNational
Park(Ecuador,1˚5’S,75˚55’W);6)ReservaFlorestalAdolphoDucke(Manaus,Brazil,2˚57’S,59˚55’W);7)Agropecua´riaTreviso
(Para´,Brazil,3˚9’S,54˚50’W);8)SEofManaus(Amazonas,Brazil,3˚20’S,59˚4’W);9)Jurua´RiverBasin(Acre,Brazil,8˚15’S,72˚
46’W);10)ItuxiRiver(Amazonas,Brazil,8˚20’S,65˚43’W);11)CentrodePesquisasCanguc¸u(Pium,Tocantins,Brazil,9˚56’S,49˚
47’W);12)ParqueEstadualGuajara´–Mirim(Rondoˆnia,Brazil,10˚19’S,72˚47’W);and13)LosAmigosBiologicalStation(Peru,12˚
34’S,70˚6’W).
https://doi.org/10.1371/journal.pone.0192834.g001
Manaus,onthemarginoftheAmazonRiver(Amazonas,Brazil,3˚20’S,59˚4’W);andAgrope-
cua´riaTreviso,101kmSand18kmEofSantare´m,closetoCurua´-UnaRiver(Para´,Brazil,3˚
9’S,54˚50’W)(Fig1).Forthespeciesfromtheselocalities,cloacaltemperaturesweremea-
suredfromadultindividualswithMiller&Weberquickreadingcloacalthermometers(resolu-
tionof0.2˚C).Literatureandempiricaldataprovideinformationonthegeneralthermal
characteristicsofeachspecies,andwedonotaddresswithin-speciesvariationduetofactors
suchasreproduction,digestionandinfection.
Ecophysiologicaldatawerecollectedinstrictaccordancewiththerecommendationsinthe
GuidefortheCareandUseofLaboratoryAnimalsoftheNationalInstitutesofHealth.The
protocolwasapprovedbytheComissãodeE´ticanoUsodeAnimais(CEUA)–INPA(Permit
Number:029/2014),CEUA–MPEG(PermitNumber:01/2015),andCEUAUnB(33716/
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ThermalphysiologyofAmazonianlizards
2016).AllcollectinginBrazilwasdoneunderpertinentIBAMA(073/94-DIFAS)andSISBIO
(13324–1,49241,50381,44832–1)permits.Alleffortsweremadetominimizediscomfortto
researchanimals.
Wecollectedthermal-preferenceandperformancedataon27speciesbetween2014and
2016insixlocalities,fiveinAmazonia—FlorestaNacionaldoAmapa´(Amapa´,Brazil,0˚55’N,
51˚36’W),FlorestaNacionaldeCaxiuanã(Para´,Brazil,1˚44’S,51˚27’W),ReservaFlorestal
AdolphoDucke(Manaus,Brazil,2˚57’S,59˚55’W);LosAmigosBiologicalStation(Peru,
12˚34’S,70˚6’W),andYasuniNationalPark(Ecuador,1˚5’S,75˚55’W),andoneintheAma-
zonia-Cerradoecotone—CentrodePesquisasCanguc¸u(Pium,Tocantins,Brazil,9˚56’S,49˚
47’W)(Fig1).Specimenswerecapturedbyactivesearchorwithpitfalltrapscheckedtwice
daily.Lizardswerekeptincaptivityforaperiodofnomorethanthreedays,andwerereleased
attheirsiteofcaptureafterarecoverytimeofatleastfourhoursafterthelasttrial.Whilein
captivity,animalswerehousedindividuallyinplasticcontainerswithairholesandadamp
clothformoisture,withoutaccesstofood.WemeasuredT ,CT ,CT ,andthermalper-
pref min max
formancecurvesoncaptivelizards.Table1showsthenumberofindividualsusedineachtest
byspecies.Wemeasuredsnout-ventlength(SVL)to0.1mmwithaVerniercaliper.Afew
voucherspecimensofeachspecieswereeuthanizedwithalethaldoseofTiopentalanesthetics,
fixedin10%formalin,andpermanentlystoredin70%ethanol.Voucherspecimenswere
depositedintheHerpetologicalCollectionsofMuseuParaenseEm´ılioGoeldi(MPEG),Para´,
Brazil;InstitutoNacionaldePesquisasdaAmazoˆnia(INPA),Amazonas,Brazil;Universidade
deBras´ılia,DistritoFederal(CHUNB),Brazil;MonteL.BeanLifeScienceMuseum,Utah,
USA;andMuseodeHistoriaNaturaldelaUniversidadNacionalMayordeSanMarcos,Lima,
Peru.
Wecharacterizedthethermalbiologyofcapturedlizardswiththefollowingprotocol.We
measuredthelizards’T byusinginfraredthermometers,focusingthelaseronthemid-por-
b
tionoftheanimal’sventralside,withapproximately15cmbetweenanimalandthermometer.
WevalidatedtheuseofbodytemperaturesbasedoninfraredthermometerswithdataonZoo-
tocavivipara,withhighcorrelationbetweencoreandsurfacetemperatures(0.85;n=34,
P<0.001).Thisspeciesisofsimilarsizetomostofthelizardsinourdataset.Smallerspecies
shouldpresentevenhighercorrelationsbetweencoreandsurfacetemperatures,andwedid
notincludeanylargespeciesinthelaboratorytests.T andvoluntaryupper(VT )and
pref max
lower(VT )temperaturesweremeasuredusingathermalgradient.Lizardswereplacedfor
min
2hoursinplywoodtracks1minlengthand40cmwide,withaphotothermalgradientof15–
40˚Cgeneratedacrosseachtrackusingiceatoneendandaheatinglamp~100Wfullspectrum
attheother(sensu[28]).T wasmeasuredevery3–5minutes,andT wasestimatedasthe
b pref
meanofallT valuesrecorded.Thefirstmeasurementwasmadeafterfiveminutesoftheani-
b
mals’positioninginsidethetrack,toallowlizardstogetacclimatedtothetrackandreachtheir
preference.VT andVT foreachindividualduringthisintervalwereestimatedbythe
max min
interquartilerangeofT [29].WemeasuredT forallindividualscaptured.Diurnallizards
pref pref
weretestedduringtheday,whilenocturnallizardsweretestedaftersunset.Afterwards,lizards
werearbitrarilychosentoundergoeitherthethermaltoleranceorperformancetests.
Criticaltemperaturesweremeasuredon485individualsof26species.Anindividual’sbody
temperaturewasdecreasedorincreasedinachambercooledbyicepacksorheatedbyhot
wateruntiltheanimallostitsrightingresponse.EachanimalwastestedforbothCT and
min
CT ,andheated/cooledtotheirT immediatelyafterthetests.Wealwaysmeasured
max pref
CT beforeCT ,sincethelastmaygettheanimalsmostimpairedandthusneedsthatthe
min max
animalshavealongerrecoverytime.TocalculateT ,wemeasuredlocomotor-capacity
opt
experimentson254individuals.Westimulatedeachindividualtorunonceat2–7randomly-
assignedtemperatures(15˚,20˚,25˚,30˚,35˚,40˚and43˚C).Speciesthatonlyoccurinshady
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ThermalphysiologyofAmazonianlizards
Table1. ThermaltraitsofAmazonianlizards.
Species ActP EAR T T T T VT VT CT CT T SVL SR
b sub air pref min max min max opt
LAR
GEKKONIDAE
Hemidactylusmabouia(cid:3)[75] N - 27.4(116) 25.6 24.9 27.4(10) 26.5(10) 28.7(10) 10.6(9) 36.1(9) - 50.3(10) A,L
20.6–29.6 18.9–33.8
Hemidactyluspalaichthus[76–77] N 18:00h 26.7(76) 25.4 25.2 - - - - - - 48.8(8) A,L
22:00h 24.2–33.2
PHYLLODACTYLIDAE
Gymnodactylusamarali[78–79] N - 30.2(28) 26.8 26.5 - - - - - - 39.5(370) Ce
26.2–34.1
Phyllopezuspollicaris[80–81] C 13:00h 28.9(10) 29.5 28.6 - - - - - - - Ca,Ce
24:00h 27.8–36.6
Thecadactylusrapicauda(cid:3)[75,82–83] N 20:00h 26.9(80) 26.2 26 28.0(7) 26.9(7) 29.4(7) 3.1(2) 38.4(3) - 110.0(7) A
23:00h 24.2–28.6 21.8–33.8
SPHAERODACTYLIDAE
Chatogekkoamazonicus(cid:3)[65] D 09:00h 27.5(36) 27.5 27.9 23.8(117) 22.08(117) 25.3(117) 9.4(37) 38.6(32) 25.8(24) 20.4(112) A
17:30h 24.6–30.2 16.1–39.5
Coleodactylusseptentrionalis[65] D 09:00h 27.4(50) - 27.4 - - - - - - 26.9(1) A
15:00h -
Gonatodesannularis(cid:3)[20] D 12:30h - - - 31.8(1) 31.0(1) 32.5(1) 16.5(1) - - 33(1) A
15:30h 31–32.5
Gonatodesconcinnatus[83] D 09:30h 27.0(156) 25.5 25.9 - - - - - - 43.3(1) A
15:00h 25.2–30.3
Gonatodeshasemani[84] D 07:00h 30.6(22) 27 26.9 - - - - - - 39.9(1) A
19:00h 28.2–33.2
Gonatodeshumeralis(cid:3)[20,84–86] D 07:00h 29.2(110) 27.3 27.3 26.0(212) 24.8(212) 27.2(212) 8.7(68) 40.9(63) 26.0(66) 36.7(186) A
19:00h 24.8–30.4 15.2–33.9
DACTYLOIDAE
Dactyloapunctata(cid:3)[87] D 10:00h 29.2(32) 28.1 28 27.2(4) 23.8(4) 30.7(4) 8.0(2) 39.6(2) - 77.9(5) A
17:00h 25.8–32 24.5–29.6
Dactyloatransversalis(cid:3)[87] D 08:00h 29.0(12) 26 26.3 24.1(1) 24.0(1) 24.3(1) - - - 76.5(2) A
16:00h 25.4–29.7 23.9–24.3
Noropsauratus[76] D 09:00h 33.9(36) 29.9 29.2 - - - - - - 43.9(123) A
17:30h 30.2–37.2
Noropsbrasiliensis[88] D 08:00h 30.6(46) 30.2 31 - - - - - - 65.3(36) Ce
17:00h 26.5–34.6
Noropschrysolepis(cid:3) D 09:30h - - - 29.15(26) 28.1(26) 30.16(26) 9.4(19) 39.7(19) - 46.1(13) A
16:00h 27.2–33.4
Noropsfuscoauratus(cid:3)[89] D 08:30h 28.6(86) 27 27 27.02(105) 25.75(105) 28.23(105) 8.4(48) 39.8(46) 27.8(30) 43.6(122) A
17:30h 25.7–33.8 19.2–33.1
Noropsortonii(cid:3) D 08:30h 30.3(7) 28 27.5 27.8(14) 26.9(14) 28.8(14) 9.7(4) 42.3(3) - 44.0(11) A
16:00h 27.5–31.2 22.9–33.5
Noropsplaniceps(cid:3)[90–91] D - 28.3(19) 26.1 26.2 29.1(16) 27.5(16) 29.3(16) 9.6(11) 40.3(11) - 55.7(13) A
26.3–30.8 23.1–33
Noropsscypheus[20,92–93] D - 27.3(36) 26.6 26.3 - - - - - - - A
24.8–28.8
Noropstandai[94] D 08:00h 27.7(33) 27 26.9 - - - - - - - Ce
17:00h 25.2–31.2
Noropstrachyderma[83,93] D 09:00h 27.8(31) 26.9 26.9 - - - - - - 53.1(1) A
16:00h 25.6–29.8
HOPLOCERCIDAE
Enyalioideslaticeps[88] D 09:00h 25.6(6) 25.3 25.7 - - - - - - 114.0(1) A
15:00h 25–26.1
(Continued)
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ThermalphysiologyofAmazonianlizards
Table1. (Continued)
Species ActP EAR T T T T VT VT CT CT T SVL SR
b sub air pref min max min max opt
LAR
IGUANIDAE
Iguanaiguana[95–96] D - 35.3(6) 28.5 28.5 - - - - - - 387.5(1) C
26.7–42.4
POLYCHROTIDAE
Polychrusacutirostris[81] D 09:00h 35.0(8) 32.6 30.7 - - - - - - 125.1(1) Ca
15:00h 34.2–36.4
Polychrusmarmoratus(cid:3) D - 29.0(1) 26.1 26.2 - - - - - - 127.5(1) A
TROPIDURIDAE
Plicaplica(cid:3)[97–99] D 08:00h 29.1(56) 27.8 27.4 26.2(23) 25.2(23) 27.4(23) 9.3(17) 41.5(17) 27.4(10) 109.1(21) A
18:00h 25.6–33.8 18.4–33
Plicaumbra(cid:3)[83,100] D 09:30h 28.7(38) 27.6 27.6 27.2(15) 25.9(15) 28.3(15) 9.9(10) 39.7(10) - 85.0(19) A
14:00h 24.8–32.0 16.2–31.3
Stenocercusroseiventris(cid:3) D 09:00h 28.2(3) 27.6 28 - - - - - - 85.0(1) A
14:30h 26.2–32.0
Tropidurushispidus(cid:3)[99,101] D 10:30h 34.2(130) 33.1 30.3 29.1(2) 28.8(2) 30.1(2) 13.2(2) 43.1(2) - 96.8(82) A,Ce
17:00h 30.6–39.6 27.8–30.3
Tropidurusinsulanus[79,97] D - 34.5(51) 30 28.1 - - - - - - 75.2(-) Ce
-
Tropidurusoreadicus[102] D 08:30h 32.9(159) 30.4 28.7 - - - - - - - Ce
18:00h 32.0–38.1
Uracentronflaviceps[103] D 08:30h 31.2(22) 27.9 27.6 - - - - - - 107.3(11) A
17:30h 25–36.7
Uranoscodonsuperciliosus(cid:3) D 11:00h 27.8(24) 27.3 27.1 28.3(7) 27.0(7) 29.5(7) 11.3(5) 39.5(5) - 108.9(7) A
16:00h 24.8–30.1 26.8–33.6
SCINCIDAE
Copeoglossumnigropunctatum(cid:3)[100] D 10:00h 33.2(121) 29.9 28.7 29.1(23) 28.0(23) 30.3(23) 10.4(19) 44.3(19) 27.3(11) 92.5(24) A
16:00h 28.0–37.4 22.2–33.5
Notomabuyafrenata[98,104] D 07:00h 31.8(145) 26.2 26.4 - - - - - - 56.7(56) AF
18:00h 21.7–37
Varzeabistriata[105] D 08:00h 32.9(11) - - - - - - - - 87.2(24) A
16:00h 27.6–36.8
GYMNOPHTHALMIDAE
Alopoglossusangulatus(cid:3)[106] D 10:00h 27.3(10) 25.1 25.6 23.8(3) 19.9(3) 25.6(3) 9.0(2) 37.2(2) - 49.0(3) A
17:00h 25.4–33.0 20.3–27.5
Alopoglossusatriventris[20,106–108] D 09:00h 28.2(12) 25.9 26.4 - - - - - - 53(1) A
18:00h 24.9–34.0
Arthrosaurakockii(cid:3)[20] D 10:00h - - - 26.5(43) 25.3(43) 27.4(43) 10.1(29) 43.4(28) 25.2(12) 30.3(42) A
15:00h 20.0–30.1
Arthrosaurareticulata(cid:3)[20] D 09:00h 27.0(34) 25.9 26.1 24.4(39) 23.4(39) 25.6(39) 8.6(19) 36.1(19) 25.6(8) 50.7(39) A
16:30h 23.8–28.2 15.4–27.7
Cercosauraargulus(cid:3)[109] D 09:00h 29.0(13) 27.2 27.3 25.8(1) 25.6(1) 25.8(1) - - - 34.5(1) A
16:00h 26.2–30.8 25.3–28.0
Cercosauraeigenmanni(cid:3)[20,91] D 09:30h 29.7(20) 27.7 27.4 25.3(3) 24.9(3) 25.4(3) - - - 45.5(1) A
15:30h 27.6–31.9 25.0–25.7
Cercosauramanicata[109] D - 29.7(2) 28 28 - - - - - - - A
Cercosauraocellata(cid:3)[20,91] D 09:30h 28.1(13) - - 28.4(3) 27.4(3) 29.6(3) - - - 52.2(2) A
15:00h 24–30.2 26.6–29.8
Cercosauraoshaughnessyi[20,83,91] D 09:00h 29.5(13) 26.7 26.7 - - - - - - 37.4(1) A
15:30h 26.2–30.8
Iphisaelegans(cid:3)[20,109] D 09:00h 28.2(1) 30.2 29.5 25.4(2) 24.6(2) 26.1(2) 3.1(1) 38.4(1) - 46.7(3) A
17:00h 21.3–29.9
(Continued)
PLOSONE|https://doi.org/10.1371/journal.pone.0192834 March7,2018 7/23
ThermalphysiologyofAmazonianlizards
Table1. (Continued)
Species ActP EAR T T T T VT VT CT CT T SVL SR
b sub air pref min max min max opt
LAR
Leposomaguianense(cid:3)[20] D 09:00h - - - 25.6(26) 23.6(26) 28.0(26) 10.4(15) 37.3(11) - 28.5(25) A
17:00h 20.8–28.6
Leposomaosvaldoi(cid:3)[20] D 09:30h - - - 24.3(11) 23.1(11) 25.8(11) 9.9(9) 36.4(8) - 29.6(11) A
15:30h 20.5–32.4
Leposomapercarinatum(cid:3)[20] D 08:00h 29.7(8) 26.7 26.6 24.1(49) 22.3(49) 25.8(49) 9.0(30) 38.7(30) 28.8(17) 32.3(32) A
17:00h 28.2–31.8 13.4–31.9
Micrablepharusmaximiliani[95,98,102] D 10:00h 29.1(4) - - - - - - - - 36(1) Ce
18:00h
Potamitesecpleopus[20,110] D 08:30h 27.0(63) 25.5 26 - - - - - - 61.8(1) A
18:00h 23.8–31.8
Potamitesjuruazensis[110] D 08:30h 26.4(8) 26.1 26 - - - - - - 41.6(1) A
16:30h 25.4–27.8
Tretioscincusagilis(cid:3)[20] D 09:00h - - - 27.8(10) 26.8(10) 29.4(10) 9.3(7) 40.2(7) - 52.2(15) A
14:00h 23.5–33.0
TEIIDAE A
Ameivaameiva(cid:3)[111–112] D 10:00h 37.4(283) 32.2 30.3 29.2(68) 27.7(67) 30.4(67) 11.0(47) 46.1(45) 34.5(20) 127.7(68) A
16:00h 26.2–41.7 18.5–38.3
Ameivaparecis[113] D 09:00h 38.2(54) 34.8 30.9 - - - - - - 64.5(1) A
13:00h 31.0–42.0
Cnemidophoruscryptus(cid:3)[113] D 09:30h 39.4(11) 37.4 32.3 27.6(40) 26.7(40) 28.4(40) 8.4(20) 50.1(20) 30.5(20) 65.4(40) A
16:00h 34.6–44.4 14.5–32
Cnemidophorusgramivagus[79,113] D 09:00h 37.6(42) - - - - - - - - 56(1) A
14:00h 30.4–40.0
Cnemidophoruslemniscatus[76] D 09:00h 37.6(96) 37.2 31.6 - - - - - - 64.2(1) A
16:00h 29.1–40.7
Crocodilurusamazonicus[114] D 11:00h 31.2(30) 30.4 27.6 - - - - - - 220.0(2) A
16:00h 27.4–35.0
Dracaenaguianensis[114] D - 32.2(1) 29 29 - - - - - - 330(1) A
Kentropyxaltamazonica[77] D 09:30h 36.0(66) 30.9 29.4 - - - - - - 85(1) A
15:30h 28–41.2
Kentropyxcalcarata(cid:3)[47] D 10:00h 34.7(99) 30.6 29 34.2(97) 32.9(97) 35.6(97) 11.9(31) 41.7(30) - 100.8(145) A
16:00h 28.7–41.0 23.3–39.1
Kentropyxpelviceps[83,115] D 10:00h 35.1(143) 29.9 28.6 - - - - - - 104.3(32) A
16:00h 26–40.5
Kentropyxstriata[76,116] D 09:00h 35.7(111) 30.3 29.5 - - - - - - 91.6(110) L
17:00h 28.8–41.0
Salvatormerianae[81] D 09:00h 35.0(8) 32.6 31.2 - - - - - - - Ca
15:00h 34.2–36.4
Tupinambislongilineus(cid:3) D - 35.5(3) 29.8 30 - - - - - - 196.0(1) A
33.5–37.2
Tupinambisquadrilineatus(cid:3) D - 37.2(1) - - - - - - - - - A
Tupinambisteguixin[76,117] D 09:30h 33.2(11) 30.4 28.9 - - - - - - 362.1(8) L
15:30h 26.1–37.2
Numberofanalyzedspecimensinparenthesisaftermeanvalues.Speciesinboldareconsiderheliothermsinliterature.Numbersinbracketsarethereferencesforthe
dataobtainedfromliterature,andasterisks((cid:3))representsnewlydataprovidedinthisstudy.ActP=Activityperiod(D=Diurnal,N=Nocturnal,C=Cathemeral);
EAR=EarliestActivityRecord;LAR=LatestActivityRecord;T =bodytemperature(meanandrange);T =substratetemperature(mean);T =airtemperature
b sub air
(mean);T =preferredtemperature(meanandrange);VT =minimumvoluntarytemperature;VT =maximumvoluntarytemperature;CT =critical
pref min max min
thermalminimum;CT =criticalthermalmaximum;T =optimaltemperature;SVL=snout-ventlength;SR=studyregion(A=Amazonianrainforest;
max opt
AF=BrazilianAtlanticForest;C=CentralAmerica;Ca=BrazilianCaatinga;Ce=BrazilianCerrado;L=BrazilianLavrado).
https://doi.org/10.1371/journal.pone.0192834.t001
PLOSONE|https://doi.org/10.1371/journal.pone.0192834 March7,2018 8/23
ThermalphysiologyofAmazonianlizards
environmentsmaysufferatextremetemperatures,andsuchspecieswererunat20˚,25˚,30˚
and35˚C.Lizardswereallowedtorecoveratleastfourhoursbetweentrials.Duringtherecov-
eryperiod,wemonitoredtheirT andactivityinsidetheircontainersatleastonceeveryhour,
b
inordertoassesstheirhealthandwell-beingafterthestresstests.Weonlyreleasedtheanimals
afterweassessedthattheyhadrecoveredtheirnormalactivitypattern.Noanimaldiedpriorto
theendoftheexperiments.
Tomeasureperformance,theexperimentermanuallystimulatedlizardstorunarounda
circulartrack[30].Atrackwitha4mcircumferencewasusedforlizardswithSVL(cid:21)50mm,
andatrackwith1mcircumferencewasusedforlizardsSVL<50mm.Eachtrialendedwhen
thelizardreachedexhaustionandwasunabletorightitselfwhenplacedinasupineposition.
Animalperformancewascalculatedasthevoluntarydistancetraveled(numberoftimes
aroundthetrackxtrackcircumference).T wasthebodytemperaturethatyieldedthehigh-
opt
estvalueoflocomotorperformance.WedeterminedT fromthethermalperformance
opt
curves.
Analysis
WeusedthestatisticalsoftwareenvironmentR3.3.3[31]forallcalculations.Dependence
betweenthermalphysiologyparametersofaprioriclassificationofthermoregulation
modes,SVL,familiesandspecieswereanalyzedbysimplestepwiseregressionandone-way
analysisofvariance.ShapiroandLevene’stestswereused,respectively,totestassumptions
ofnormalityandhomogeneityofvarianceforparametricvariables.WeusedthePearson
correlationcoefficienttodeterminethecorrelationbetweenT ,T andT .Forcompara-
b sub air
tiveanalyses,weusedthechronogramforSquamataestimatedbyZheng&Wiens[32],
whichincludedallofthespeciesforwhichwewereabletoassemblethermophysiological
traits.PhylogeneticsignalwascalculatedbasedonBlomberg’sK[33],whichisanevolution-
arymodel-basedmetricofphylogenetic-signalstrength.AK-valueofoneindicatesthat
thedistributionoftraitvaluesfollowstheexpectationofBrownianmotionmodelofevolu-
tionalongthetree[33].Thisindicatesthattraitvarianceamongspeciesaccumulatesin
directproportiontotheirdivergencetime,asmeasuredbythebranchlengthsseparating
theminaphylogenetictree[34–35].ValuesofK<1indicatethattraitsarelessconserved
thanexpected,anindicationofadaptiveevolution,whereasvaluesofK>1indicatethattrait
valuesaremoreconservedthanexpectedbyBrownianmotionevolution.Weusedphytools
[36]tocalculateBlomberg’sKandtomeasurethephylogeneticpairwisecorrelations
betweenallthermaltraits.
TPC’sweregeneratedforeachspeciesusingthepackagesggplot2[37],grid[31],mgcv[38]
andproc[39]todoaGeneralizedAdditiveMixedModeling(GAMM)[40].Thesemodelsuse
additivenonparametricfunctionstomodelcovariateeffectswhileaccountingforoverdisper-
sionandcorrelation,byaddingrandomeffectstotheadditivepredictor[41].Akaike’sInfor-
mationCriterion(AIC)andBayesianInformationCriterion(BIC)wereusedtoselectthebest
correlationstructurepriortoestimatingtheTPC.AICmeasuresthequalityoffitofthemodel,
penalizedbymodelcomplexity,andBICadditionallyconsidersthenumberofobservations
includedinthemodel[42].Lizardperformanceatdifferenttemperatureswastheresponse
andindividualwasincludedasarandomeffect.Theextremesofthecurvewerefixedatthe
averageCT andCT valuesforthatspecies.Wetestedseveralcorrelationstructuresto
min max
selectthebestfitincluding:temporalcorrelationstructures(autoregressiveprocess[corAR1],
continuousautoregressiveprocess[corCAR1],andautoregressivemovingaverageprocess
[corARMA])andspatialresidualcorrelationstructures(Gaussianspatialcorrelation[cor-
Gaus],exponentialspatialcorrelationstructure[corExp],rationalquadraticsspatial
PLOSONE|https://doi.org/10.1371/journal.pone.0192834 March7,2018 9/23
ThermalphysiologyofAmazonianlizards
Table2. Numberofspecimensandtaxausedassourceofdatareportedhereforthefirsttime.
No.specimens No.species No.families
T 80 8 5
b
T /VR 1010 27 9
pref
PhysiologicalPerformance 254 10 6
ThermalToleranceRange(CT ,CT ) 485 26 8
min max
T =bodytemperature;T =preferredtemperature;VR=voluntaryrange
b pref
https://doi.org/10.1371/journal.pone.0192834.t002
correlation[corRatio]andsphericalspatialcorrelation[corSpher]).Wechosethecorrelation
structurethatyieldedthelowestAICandBICvalues[42].
Results
Weobtainedthermaldatafor69lizardspeciesfromelevenfamilies(Table1),includingnew
dataonfield-activeT ,T ,thermalperformanceandtolerancefrom27species(Table2).
b pref
Amongallspecieswithphysiologicaldata,64arediurnal,oneiscathemeral,andfournoctur-
nal.Basedontheliterature,38speciesareclassifiedasthermoconformers,while31are
thermoregulators.
Lizards’bodytemperaturewaspositivelycorrelatedwithenvironmentaltemperature(T
b
andT r=0.80,P<0.01;T andT :r=0.67,P<0.05).Sevenspeciesgenerallyclassifiedas
sub: b air
thermoconformershadT /T higherthanT ,suggestingthatthesespeciesdonotgainaddi-
sub air b
tionalheatfromtheenvironment,butmaybethermoregulatingbyselectinglowertempera-
turesorusingevaporativecooling.Aone-wayANOVArevealedsignificantdifferencesinall
physiologicaltraitsinrelationtoaprioriclassificationofthermoregulationmode,SVL,family,
andspecies.Fig2showstherangeoftemperaturesforeachevaluatedtraitforeachthermoreg-
ulationmode.Speciesgenerallyclassifiedasthermoregulatorshadhighermeanvaluesforall
thermaltraitsthanthosegenerallyclassifiedasthermoconformers,aswellaslargervariation
inT ,CT andT .VariationinT ,VT andCT waslowerinspeciesclassifiedas
b max opt pref min min
thermoregulatorsandgreaterinspeciesclassifiedasthermoconformers,thoughmeanvalues
wererelativelysimilar(Fig3).Inspiteofthesedifferences,ourresultsshowanoverlapinmost
thermaltraitsbetweenspeciesclassifiedasthermoregulatorsandthoseclassifiedasthermo-
conformers,withsomelizardsconsideredthermoregulatorshavingrangesoftemperatures
similartoothersidentifiedasthermoconformers.Thus,adichotomousclassificationofther-
moregulationmodemaynotbesatisfactory.
Wealsofoundphylogeneticpairwisecorrelationsbetweenallthermaltraitsevaluated(T ,
b
T ,VT ,VT ,CT ,CT ,andT ),exceptbetween(1)T andCT ,and(2)
pref min max min max opt opt max
CT ,whichonlycorrelateswithT (Table3).Thus,selectionononethermalcharacteristic
min opt
affectstheevolutionofallthoseconsideredhere,except,possibly,inthetwocasesmentioned
above.WedetectedsignificantdeparturesfromBrownianmotionevolutionforT (K=0.64,
b
P=0.0001),T (K=0.49,P=0.04),andVT (K=0.5,P=0.01),butnotfortheotherther-
pref min
maltraits(VT ,K=0.39,P=0.21;CT ,K=0.49,P=0.12;CT ,K=0.50,P=0.079;
max min max
T ,K=0.74,P=0.17).LizardsinthefamilyTeiidaearecomprisedonlyofspeciesclassified
opt
asthermoregulators,andhadthehighestvaluesforallthreethermaltraits.ThelowestT was
b
foundinonespeciesofHoplocercidae(forest-dwellinglizards),andthelowestVT was
min
observedinGekkonidae,bothfamiliescontainingonlyspeciesclassifiedasthermoconformers.
GekkonidaeandDactyloidaepresentedthelowestT .AlthoughDactyloidaeisamixed
pref
family,theonlydactyloidspeciesclassifiedasthermoregulatorinthisstudyhasnoT
pref
dataavailable.Thus,allT measurementsforthisfamilyarefromspeciesclassifiedas
pref
PLOSONE|https://doi.org/10.1371/journal.pone.0192834 March7,2018 10/23