Climate change and body size trends in aquatic and terrestrial endotherms: Does habitat matter?

13 Pages·2017·2.225 MB·English

by  Naya, Daniel E., Hugo Naya, and Joseph Cook

RESEARCHARTICLE
Climate change and body size trends in
aquatic and terrestrial endotherms: Does
habitat matter?
DanielE.Naya1*,HugoNaya2,3,JosephCook4
1 DepartamentodeEcolog´ıayEvolucio´n,FacultaddeCiencias,UniversidaddelaRepu´blica,Montevideo,
Uruguay,2 UnidaddeBioinforma´tica,InstitutPasteurdeMontevideo,Montevideo,Uruguay,
3 DepartamentodeProduccio´nAnimalyPasturas,FacultaddeAgronom´ıa,UniversidaddelaRepu´blica,
Montevideo,Uruguay,4 DepartmentofBiologyandtheMuseumofSouthwesternBiology,UniversityofNew
a1111111111 Mexico,Albuquerque,NewMexico,UnitedStatesofAmerica
a1111111111
*[email protected]
a1111111111
a1111111111
a1111111111
Abstract
Severalstudieshaveclaimedthatreductioninbodysizecomprisesanearlyuniversal
responsetoglobalwarming;however,doubtsaboutthevalidityofthispatternforendother-
OPENACCESS micspecieshavebeenraisedrecently.Accordingly,weassessedtemporalchangesin
Citation:NayaDE,NayaH,CookJ(2017)Climate bodymassfor27birdand17mammalspecies,toevaluateifareductioninbodysizeduring
changeandbodysizetrendsinaquaticand the20thcenturyisawidespreadphenomenonamongendothermicvertebrates.Inaddition,
terrestrialendotherms:Doeshabitatmatter?PLoS
wetestediftherearedifferencesinthetemporalchangeinsizebetweenbirdsandmam-
ONE12(8):e0183051.https://doi.org/10.1371/
journal.pone.0183051 mals,aquaticandterrestrialspecies,andthefirstandsecondhalfofthe20thcentury.Over-
all,sixspeciesincreasedtheirbodymass,21speciesshowednosignificantchangesin
Editor:CarlosANavas,UniversityofSaoPaulo,
BRAZIL size,and17speciesdecreasedtheirbodymassduringthe20thcentury.Temporalchanges
inbodymassweresimilarforbirdsandmammals,butstronglydifferbetweenaquaticand
Received:January19,2017
terrestrialspecies:whilemostoftheaquaticspeciesincreasedordidnotchangeinbody
Accepted:July30,2017
mass,mostterrestrialspeciesdecreasedinsize.Inaddition,wefoundthat,atleastinter-
Published:August16,2017
restrialbirds,themeanvalueofthecorrelationbetweenbodymassandyearofcollection
Copyright:©2017Nayaetal.Thisisanopen differsbetweenthefirsthalfandthesecondhalfofthe20thcentury,beingclosetozerofor
accessarticledistributedunderthetermsofthe
theformerperiodbutnegativeforthelaterone.Toourknowledge,thisisthefirststudy
CreativeCommonsAttributionLicense,which
showingthattemporalchangesinbodymassdifferbetweenaquaticandterrestrialspecies
permitsunrestricteduse,distribution,and
reproductioninanymedium,providedtheoriginal inbothmammalsandbirds.
authorandsourcearecredited.
DataAvailabilityStatement:Allrelevantdataare
withinthepaperanditsSupportingInformation
files.
Funding:JACandsomeofthespecimen Introduction
infrastructureusedherewassupportedinpartby
Severalstudieshaveclaimedthatareductioninbodysizecomprisesthethirduniversaleco-
theNationalScienceFoundation(NSF-DEB
125801).Thefundershadnoroleinstudydesign, logicalresponsetoglobalwarming,afterspeciesdistributionalshiftsandphenologicalchanges
datacollectionandanalysis,decisiontopublish,or [1–3].Fortheparticularcaseofendothermicspecies,twonon-mutuallyexclusiveideasare
preparationofthemanuscript. usuallyinvokedtoexplainthisphenomenon[4–7].First,ariseinambienttemperaturemay
Competinginterests:Theauthorshavedeclared causeareductioninbodysizeduetoenergeticconsiderations–i.e.,smallersizeimpliesalarger
thatnocompetinginterestsexist.
PLOSONE|https://doi.org/10.1371/journal.pone.0183051 August16,2017 1/12
Climatechangeandbodysizetrendsinendotherms
surfacetovolumeratioandis“better”forheatdissipationinwarmerclimates–inlinewith
KarlBergmann’sfamousargument[8].Second,adecreaseinresourceavailability(orquality)
couldcauseareductionintherateofgrowththroughoutananimal’sdevelopment,resulting
inasmalleradultsize.Asforthemechanisticbasisofthesechanges,twonon-mutuallyexclu-
siveexplanationsareusuallyadvanced:aplasticresponseattheindividuallevel[9–10]and
geneticchangesatthepopulationlevel[11–12].Eventhoughveryfewstudieshaveevaluated
therelativeweightofthesetwomechanisms,currentevidencesuggeststhatphenotypicplastic-
ityusuallyaccountsforahigherportion,ifnotforall,oftheoverallphenotypicchange[13–
14].
However,leavingasidethepotentialcausesandthemechanisticbasisfortheobserved
changes,doubtshavebeenraisedrecentlyaboutthevalidityofarelationshipbetween
temperatureandbody-sizeinendothermicspecies[5,15–18].Inlinewiththis,oursemi-
quantitativereviewofcurrentevidenceontemporalchangeinbodysizeforendothermic
vertebratessuggeststhatnoclearpatternisevident.Specifically,afteranalyzingdatafrom
46studies,comprisingatotalof369populationsofbirdsandmammals(S1Dataset),we
concludethat:(i)regardlessofthestatisticalsignificanceofthechanges,theproportionof
populationsthatincreasetheirsizeissimilartotheproportionofpopulationsthatdecrease
theirsize(Fig1a),and(ii)whenthestatisticalsignificanceofthechangesistakeninto
account,nearlytwo-thirdsofpopulationsanalyzedtodateshowednosignificanttemporal
changesinbodysize(Fig1b).Inaddition,twointriguingpointsemergefromthissemi-
quantitativeassessment.First,withacoupleofexceptions,allthestudiesanalyzingonlya
singlepopulationreportedsignificanttemporalchangeinsize,whileallthestudiesanalyz-
ingmorethanonepopulation(orspecies)indicatethatnosignificantchangesarecommon.
Suchdifferencesclearlysuggestapublicationbiasthatcouldaffectimpressionsaboutthe
ubiquityoftemporalchangesinbodysize(see[15]).Second,withveryfewexceptions,
studiesanalyzingmorethanonepopulationofthesamespecies,orthecombinationofdif-
ferentstudiesevaluatingdifferentpopulationsofthesamespecies,indicatethatobserved
responsesusuallyvary,inboththesignofthetrendandstatisticalsignificance,fromone
populationtotheother.Thatis,thereissignificantvariationinbodysizechangesfromsite
tosite,whichsuggestthatidiosyncraticresponses,probablylinkedtodifferencesinlocal
conditions[19]oreventodispersaleventsbetweenlocalities[20],arecommon.Insum-
mary,itisclearthatweneedtoevaluatemuchmoredatabeforeacceptingthatareduction
inbodymassassociatedwithglobalwarmingor,moregenerally,withglobalenvironmental
change,comprisesageneralruleforendotherms.Inparticular,weneedtoconductmore
multi-speciescomparativestudies,tounderstandthenaturalvariationinphenotypic
responses,andusesimilarmethods(e.g.,thesamemeasurementofbodysize)acrosslarge
geographicareas,toreducetheincidenceofconfoundingfactorsandtoaccountforpoten-
tialsite-to-sitefluctuations.
Withinthiscontext,weassessedtemporalchangeinbodymassfor27birdand17mammal
speciestoevaluateifareductioninbodysizeduringthe20thcentury,whateveritscausesand
mechanisticbasis,isawidespreadphenomenonamongendothermicvertebrates.Inaddition,
wetestedwhethertherearedifferencesinthetemporalresponsebetween:(1)birdsandmam-
mals,(2)aquaticandterrestrialspecies,and(3)thefirstandsecondhalfofthe20thcentury.To
thebestofourknowledge,thisisthefirststudythat:(i)simultaneouslyassessestemporal
changesinbodysizeforbirdsandmammals,usingthesamemethodologytoanalyzebothtax-
onomicgroupsandaccountingfortheeffectofphylogeny,and(ii)evaluatesdifferencesinthe
temporalresponsesbetweenaquaticandterrestrialspecies.
PLOSONE|https://doi.org/10.1371/journal.pone.0183051 August16,2017 2/12
Climatechangeandbodysizetrendsinendotherms
Fig1.Percentegeofbirdandmammalpopulationsthatshowdifferenttemporalresponsesinbody
size,takingintoaccount(a)onlythesignofthechanges(upperpanels),and(b)thestatistical
significanceofthechanges(lowerpanels).Datawereanalyzedseparatelyfortrendandsignificance
becausestatisticalsignificancedependsonsamplesize(whichvariesfromcasetocase),andalsobecause
somestudiesonlyreportthesignofthetemporaltrend,whileotherstudiesonlyreportthatchangeswerenot
significant(seeS1Datasetfordetails).
https://doi.org/10.1371/journal.pone.0183051.g001
Methods
Databasedescription
Toassesstemporalchangeinbodysize,wedownloadeddataonbodymassforendothermic
vertebrates,withtheexceptionofrodentsandpasserinebirdsduetologisticconstraints(i.e.,
ourinabilitytocuratetwodatasetswithseveralthousandsofrecords)fromArctos,anonline
naturalhistorydatabase(www.arctos.database.museum).Weincludedallspecieswithmore
than100geo-referencedrecordsofsexedindividuals,coveringthelastfourdecadesatleast.
Weexcludedsixspeciesforwhichmostofthedata(>80%)span<10yearsofcollection
(FigureAinS1Appendix),andremoved26outlierrecordscorrespondingtoverysmallindi-
viduals,inwhichbodymasswasclosetozero.Thoseselectioncriteriayieldedatotalof
20,496recordsbelongingto44species(S2Dataset).Thesespecieswerethenclassified,based
oninformationprovidedbyIUCN(http://www.iucnredlist.org/),BirdlifeInternational
(http://www.birdlife.org/),andtheMuseumofZoologyoftheUniversityofMichigan(http://
animaldiversity.org/),asaquatic,iftheyinhabitfreshwaterand/ormarinehabitatsinaddi-
tiontoterrestrialones(birds:n=10,mammals:n=4),orterrestrial,iftheyonlyinhabitter-
restrialhabitats(birds:n=17,mammals:n=13).Byanalyzingmultiplepopulationsofeach
speciesoverbroadgeographicalareas(seeFigureBinS1Appendix),ouranalysisintendedto
PLOSONE|https://doi.org/10.1371/journal.pone.0183051 August16,2017 3/12
Climatechangeandbodysizetrendsinendotherms
identifyresponsesatthespecieslevel,ratherthanlocalresponsesatthepopulationlevel.
Also,ouranalysisassumedthattheeffectsofseveralfactorsthatcouldaffectbodymassand
thatwecannotfilterstatistically(e.g.,ageofeachindividual,seasonoftheyear,timeofthe
dayofcapture,peopletakingthemeasurements)arerandomlydistributedamongyears.
Comparisonbetweentaxonomicgroupsandspecieshabitats
Weestimatedthepartialcorrelationcoefficientbetweenbodymassandtheyearofcollection
(r )foreachspeciesseparately,throughconventionallinearregressionmodels,using(abso-
year
lute)latitude,longitude,andsexascovariatesinthemodels.Then,weevaluateddifferencesin
r betweentaxonomicgroups(i.e.,birdsormammals)andspecieshabitats(i.e.,aquaticor
year
terrestrial)usingatwo-wayANOVA.Thecorrelationcoefficientbetweenbodymassandthe
yearofcollection(r )wasnotcorrelatedwithsamplesize,speciesbodymass,orspeciesdis-
year
tribution,butwascorrelatedwiththelengthofthetimeseries(r=0.36,P=0.02).Hence,in
additiontotheANOVA,wealsorananANCOVAusingthelengthoftimeseriesasacovari-
ate.Intheseanalyses,weusedtheKolmogorov-Smirnovtesttoassessnormality,Levene’stest
toassesshomogeneityofvariance,and(inANCOVA)aparallelismtesttoassesstheinterac-
tionbetweenfactorsandthecovariate.AlltheseanalysesweredonewithStatistica(version
8.0)software[21],withstatisticalsignificanceestablishedattheα=0.05level.
Totakeintoaccountphylogeneticrelationshipsamongspecies,therelationshipbetween
bodymassandtheyearofcollectionwasalsoevaluatedusingaphylogeneticgeneralizedlinear
mixedmodel(PGLMM)[22],withspeciesasarandomfactor,taxonomicgroupandhabitatas
fixedfactors,and(absolute)latitude,longitude,sexandlengthofthetimeseriesascovariates
(modelA).Toconsiderpotentialinteractionsbetweentheyearofcollectionandfixedfactors,
werantwoadditionalmodels:oneincludingtheinteractiontermwithtaxonomicgroup
(modelB)andtheotherincludingtheinteractiontermwithhabitat(modelC).Inallthese
models,speciesbodymasswasstandardizedtoameanequaltozeroandvarianceequalto
one.Thephylogenetictreeusedintheseanalyses(FigureCinS1Appendix)wasbasedon
previouslypublishedpapersforbirds[23]andmammals[24–25].Giventhatbranchlengthis
notknownforthistree,wesetalllengthstoone.Phylogeneticanalyseswererunwiththe
MCMCglmmpackage[26]inthefreesoftwareR[27].Inferencesforeachregressionmodel
werebasedon200,000samples,obtainedafterdiscarding50,000samplesasburnin.Inall
models,defaultpriorswereusedfor“fixed”effects,whileinverseWishartpriorswithscale
parameterequaltohalfofdependentvariablevariance(and3degreesoffreedom)wereused
for“random"effects.Athinningintervalof100wasusedforcomputingfeaturesoftheposte-
riordistribution.Convergencediagnostics,statisticalandgraphicalanalysesofMarkovchain
MonteCarlo(MCMC)samplingoutputwerecarriedoutwiththeCODApackage[28]avail-
ableinR.Finally,thesignificanceofeachregressioncoefficientwasestimatedfromMarkov
chainMonteCarlop-value(pMCMC),whichbasicallyrepresents(2x)theproportionofposte-
riorvaluesthatareoftheoppositesigntotheparameterestimate,whereasthefitofeach
modeltothedatawasassessedthroughDevianceInformationCriterion(DICscores).
Temporalvariationinthetemporalresponses
Becausedataforterrestrialbirdspeciesarefairlyevenlydistributedintimethroughmostof
the20thcentury(seeFigureBinS1Appendix),wedecidedtoevaluatetemporalchangesinthe
relationshipbetweenbodymassandyearofcollectionwiththisgroupofspecies.Forthatpur-
pose,wesplittheseriesofeachspeciesintotwoperiodsoftime:onefromtheearliestdateof
collection(ca.1915)to1950,representingarelativelylowintensityofchangeinenvironmental
conditions,andtheotherfrom1951tothelatestdateofcollection(ca.2013),representinga
PLOSONE|https://doi.org/10.1371/journal.pone.0183051 August16,2017 4/12
Climatechangeandbodysizetrendsinendotherms
relativelyhighintensityofchangeinenvironmentalconditions[29].Notethattheincreasein
globallyaveragedtemperatureovertheperiod1901–2012wasabout0.89˚C,whiletheincrease
overjusttheperiod1951–2012wasabout0.72˚C[29].Thus,therateofchangeinambient
temperatureforoursecondperiod(ca.0.12˚Cperdecade)isalmostfourtimesgreaterthan
forourfirstperiodoftime(ca.0.03˚Cperdecade).Foreachspeciesandperiodoftime,wecal-
culatedthepartialcorrelationfortheyearofcollection(r )using(absolute)latitude,longi-
year
tudeandsexascovariatesintheregressionmodels.Then,weevaluateddifferenceinthemean
valueofr betweenbothperiodsoftime,usingapairedt-testfordependentsamples.These
year
analysesweredonewithStatistica(version8.0)software,andstatisticalsignificancewasestab-
lishedattheα=0.05level.Finally,totakeintoaccountphylogeneticrelationshipsamongspe-
cies,weestimatedtherelationshipbetweenbodymassandtheyearofcollectionseparatelyfor
eachperiodoftime(i.e.,beforeandafter1950),usingphylogeneticgeneralizedlinearmixed
models(PGLMM)[22],with(absolute)latitude,longitude,andsexascovariates.Then,thesig-
nificanceofeachregressioncoefficientwasestimatedfromMarkovchainMonteCarlop-
value(pMCMC).Inaddition,asintheBayesianMCMCcontextitispossibletodirectlyobtain
samplesoftheregressioncoefficientsfromtheposteriordistributionforeachperiodoftime,
wewereabletogenerateanewdistributionfromthedifferencesbetweenregressioncoeffi-
cients(iterationbyiteration)betweenbothperiods(“after1950”minus“before1950”).Based
onthisnew(delta)distribution,weevaluatedatemporalchangeintheeffectofeachfactor
throughthepMCMCvalue.
Results
Comparisonbetweentaxonomicgroupsandspecieshabitats
Overall,sixspeciesincreasedtheirbodymass,21speciesshowednosignificantchangesin
size,and17speciesdecreasedtheirbodymassduringthe20thcentury(TableAinS1Appen-
dix).Thecorrelationbetweenbodymassandyearofcollection(r )wassimilarforbirdsand
year
mammals(ANOVA:F =1.38,P=0.25;ANCOVA:F =0.01,P=0.92;Fig2a),butit
1,40 1,39
stronglydiffersbetweenaquaticandterrestrialspecies(ANOVA:F =27.1,P<0.001;
1,40
ANCOVA:F =14.8,P<0.001;Fig2a).Takentogether,dataforbirdsandmammalsindi-
1,39
catethat:(1)of14aquaticspecies,fiveshowedasignificantincrease,eightshowedanon-sig-
nificantcorrelation,andoneshowedasignificantdecreaseinbodymassduringthe20th
century(Fig2b);(2)of30terrestrialspecies,16showedasignificantdecrease,13showeda
non-significantcorrelation,andoneshowedasignificantincreaseinbodymassduringthe
20thcentury(Fig2b).Thatis,whilemostaquaticspeciesincreasedordidnotchangebody
massthroughthe20thcentury,mostterrestrialspeciesdecreasedinsize.Inlinewiththese
results,phylogeneticanalysesindicatethat,inadditiontolatitudeandsex,thereisasignificant
effectoftheyearofcollectioninallthemodels(Table1).Inaddition,themodelthatincluded
aninteractiontermbetweenyearofcollectionandhabitat(modelC)showedthebestfittothe
data(Table1),andthisinteractionwassignificant,indicatingagainthecontrastingpatternof
variationbetweenaquaticandterrestrialspecies.
Temporalvariationinthetemporalresponse
Asmentionedabove,therateofchangeinglobaltemperaturewasgreaterforthesecondhalf
ofthe20thcenturythanforthefirsthalf(Fig3a).Inlinewiththis,wefoundthatbefore1950
twoterrestrialbirdspeciesshowedasignificantincreaseinbodymass,twelvespeciesshowed
nosignificantchangesinsize,andthreespeciesshowedasignificantdecreaseinbodymass
(Fig3b;TableBinS1Appendix).However,after1950wefoundthateightspeciesshoweda
significantdecreaseinbodymass,whiletheremainingninespeciesshowednosignificant
PLOSONE|https://doi.org/10.1371/journal.pone.0183051 August16,2017 5/12
Climatechangeandbodysizetrendsinendotherms
Fig2.Correlationcoefficientbetweenbodysizeandyearofcollectionfor(a)thefourspeciesgroups
thatwerecompared,and(b)allthespeciesincludedintheanalysis.AqBirds:aquaticbirds,TerBirds:
terrestrialbirds,AqMamm:aquaticmammals,TerMamm:terrestrialmammals.N=numberofspeciesin
eachgroup.Bars:95%confidenceintervals.*denotesP<0.05and§denotesP<0.1.
https://doi.org/10.1371/journal.pone.0183051.g002
PLOSONE|https://doi.org/10.1371/journal.pone.0183051 August16,2017 6/12
Climatechangeandbodysizetrendsinendotherms
Table1. Posteriormeans(X),lowerandupperconfidenceintervals(L95%CIandU95%CI,respectively),andMarkovchainMonteCarlop-value(pMCMC)
obtainedbyphylogeneticgeneralizedlinearmixedmodels,withbodymassasdependentvariable,yearofcollectionastheindependentvariable,speciesas
arandomfactor,taxonomicgroup(class)andhabitatasfixedfactors,and(absolute)latitude,longitude,sexandlengthofthetimeseriesascovariates(model
A).Aninteractiontermbetweentheyearofcollectionandtaxonomicgroup(class)orhabitatwasincludedinmodelBandC,respectively.Foreachmodel,the
DevianceInformationCriterion(DIC)scoreisprovidedinbrackets;andforeachfactor,thelevelthatwasnotdroppedintotheinterceptisgiveninbrackets.
MODELA(DIC=58.051) MODELB(DIC=58.053) MODELC(DIC=57.986)
X L95%CI U95%CI pMCMC X L95%CI U95%CI pMCMC X L95%CI U95%CI pMCMC
Intercept 4.6931 2.9896 6.3192 5.0E-04 5.0874 3.1025 7.1753 5.00E-04 -9.2593 -13.4541 -4.913 5.0E-04
Year -0.0027 -0.0035 -0.0019 5.0E-04 -0.0029 -0.0039 -0.0020 5.00E-04 0.0042 0.0021 0.0063 5.0E-04
Class(Mammals) -0.0782 -0.4126 0.2064 0.622 -1.2422 -4.9069 2.3277 0.514 -0.0104 -0.3210 0.2813 0.947
Habitat(Terrestrial) 0.1188 -0.0755 0.3193 0.252 0.1141 -0.0753 0.3165 0.259 16.7406 12.0595 21.3008 5.0E-04
Latitude 0.0113 0.0091 0.0136 5.0E-04 0.0114 0.0090 0.0136 5.00E-04 0.0112 0.0088 0.0134 5.0E-04
Longitude 7.2E-06 -0.0003 0.0003 0.949 2.1E-05 -0.0004 0.0003 0.900 -0.0002 -0.0005 0.0002 0.327
Sex(male) 0.0462 0.0186 0.0719 0.002 0.0453 0.0172 0.0710 5.00E-04 0.0439 0.0164 0.0698 5.0E-04
Timeserieslength 0.0007 -0.0052 0.0063 0.806 0.0007 -0.0048 0.0064 0.822 0.0030 -0.0028 0.0086 0.307
Interactionterm ----- ----- ----- ----- 0.0006 -0.0011 0.0025 0.529 -0.0084 -0.0108 -0.0061 5.0E-04
https://doi.org/10.1371/journal.pone.0183051.t001
correlationbetweenbodymassandyearofcollection(Fig3b;TableBinS1Appendix).
Accordingly,themeanvalueofr differedbetweenbothperiodsoftime(t =2.46,
year 16
P=0.03),beingveryclosetozeroforthefirsthalfofthe20thcentury(X=-0.01,SD=0.16)
andnegativeforthesecondhalfofthiscentury(X=-0.14,SD=0.12).Inthesamevein,phylo-
geneticanalysesindicatethatregressioncoefficientfortheyearofcollectiondidnotdiffer
fromzeroforthefirsthalfofthe20thcentury,butwasnegativeandhighlysignificantforthe
secondhalfofthatcentury(Table2).Moreover,thedistributionofthedifferenceoftheregres-
sioncoefficientsfortheyearofcollectionbetweenbothperiodsoftime(“after1950”minus
“before1950”)wasnegativeandstatisticallysignificant(Table2).
Discussion
Importantly,nearlyallthedataconsideredinouranalysesarefromspecimensfromthemid-
dleandhighlatitudesalongthewestcoastandwesternNorthAmericansub-continent
(FigureDinS1Appendix).Althoughthisfactmayconstraingeneralizationofourresults,
ambienttemperatureinthisareahasincreasedbetween1˚Cand2˚Cthroughthe20thcentury
[29].Thus,thechangesinbodysizethatwereobservedherecouldbelinked,atleastintheory,
todirectandindirecteffectsofchangesinambienttemperature.Threemajorresultsemerge
fromthepresentstudy.First,onlysubtle(nonsignificant)differencesinthetemporalchanges
inbodymassbetweenbirdsandmammalswereobserved.Second,temporalchangesinbody
massrecordedforaquaticspeciesweredifferentfromthoserecordedforterrestrialspecies.
Third,thetemporalreductioninbodysizeobservedinterrestrialbirdswasgreaterforthesec-
ondhalfofthe20thcenturythanforthefirsthalf.
Thefirstresultisinterestingbecausepreviouslypublisheddatasuggestthatsignificant
reductionsinbodysizeappeartobemorecommoninbirds,whilesignificantincreasesinsize
appeartobemorecommoninmammals[5,13].However,incontrasttoourstudyinwhich
aquaticspeciesrepresent32%ofspecies,previousworkswereconductedalmostexclusivelyon
terrestrialspecies(>95%).Thus,itcouldbepossiblethatthediscrepancybetweenourstudy
andpreviousworksisrelatedtoadifferenceintherelativenumberofspeciesthatoccurin
aquatichabitats.Inthissense,acloseinspectionofourresultsforterrestrialspeciesindicates
thattheproportionofspeciesthatshowedasignificantreductioninbodysizeishigherin
birds(64.7%)thaninmammals(38.5%).Wethinkthatthistaxonomicdifferenceinterrestrial
habitatcouldberelatedtodifferencesinbiologyandespeciallylinkedtotheenergetic
PLOSONE|https://doi.org/10.1371/journal.pone.0183051 August16,2017 7/12
Climatechangeandbodysizetrendsinendotherms
Fig3.(a)Changeinlandsurfacetemperatureforthelastcentury(modifiedfrom[29]),and(b)correlation
coefficientbetweenbodysizeandyearofcollectionforterrestrialbirdspeciesduringthefirst(before
1950)andsecond(after1950)halfofthe20thcentury.*denotesP<0.05and§denotesP<0.1.
https://doi.org/10.1371/journal.pone.0183051.g003
PLOSONE|https://doi.org/10.1371/journal.pone.0183051 August16,2017 8/12
Climatechangeandbodysizetrendsinendotherms
Table2. Posteriormeans(X),lowerandupperconfidenceintervals(L95%CIandU95%CI,respectively),andMarkovchainMonteCarlop-value
(pMCMC)obtainedbyphylogeneticgeneralizedlinearmixedmodelsincludingdatabefore1950,after1950,andcomparingbothperiodsoftime.
Forthefactor“sex”,thelevelthatwasnotdroppedintotheinterceptisprovidedinbrackets.
Before1950 After1950 ΔPeriods
X L95%CI U95%CI pMCMC X L95%CI U95%CI pMCMC X L95%CI U95%CI pMCMC
Intercept -2.9162 -11.4821 5.4466 0.503 11.2687 6.4670 15.9670 0.001 14.1849 5.3003 24.9950 0.008
Year 0.0007 -0.0034 0.0049 0.711 -0.0063 -0.0084 -0.0041 5.0E-04 -0.0070 -0.0121 -0.0025 0.003
Latitude 0.0528 0.0463 0.0592 5.0E-04 0.0402 0.0341 0.0464 5.0E-04 -0.0126 -0.0214 -0.0036 0.007
Longitude 0.0028 -0.0022 0.0079 0.277 0.0017 -0.0007 0.0042 0.185 -0.0011 -0.0069 0.0044 0.724
Sex(male) -0.1321 -0.2111 -0.0574 0.001 -0.0796 -0.1522 -0.0046 0.037 0.0525 -0.0577 0.1571 0.353
https://doi.org/10.1371/journal.pone.0183051.t002
argument.Thatis,becausebirdshavehighermetabolicratesforagivenbodymassthanmam-
mals[30],theselectivepressureforincreasingheatdissipationabilities(i.e.,smallersizes)
couldbehigherintheformergroup.
Thesecondresult,inouropinion,isthemostinterestingoutcomeofthepresentstudy.In
short,wefoundthatwhilemostoftheaquaticspeciesincreasedordidnotchangeinbody
massthroughthe20thcentury,mostterrestrialspeciesdecreasedinsize.Webelievethatthisis
nottheconsequenceofasinglephysiologicalorecologicalfactoractingdifferentiallybetween
thetwohabitats,buttheresultofanimbalanceinthenumberoffactorspromotingincrease
anddecreaseinsizebetweenaquaticandterrestrialsystems.Inaddition,giventhatspecies
classifiedasaquaticinthepresentstudyrangefromsemi-aquatictofullyaquatic,therelevance
ofeachfactorenlistedbelowcouldchangetoagreaterextentaccordingtothebiologyofindi-
vidualspecies.First,thefactthatwaterthermalconductivityisabout23timesgreaterthanair
thermalconductivitymeansthatthermalstabilityismuchgreaterinaquaticthaninterrestrial
systems[31].Consequently,extremeeventsduringwhichambienttemperaturerisesabovethe
upperlimitofthethermoneutralzone–whichusuallyisbetween30˚Cand40˚C[32]–couldbe
fairlycommononlandbutrareinaquatichabitats(andsurelynonexistentinaquatichabitats
athigherlatitudes).Alongtheselines,adecreaseinbodysizeduetotheenergeticargument
depictedbyBergmann[8]isnotexpectedformostaquaticspecies.Interestingly,anincrease
inbodysizerelatedtoariseinthenumberofextremelyhotdays,duetoapositiverelationship
betweensizeandwaterconservationability,alsohasbeenproposedforterrestrialbirds,but
onlyforsomespeciesinhabitingaridenvironments[33–34].Second,thegreaterthermalcon-
ductivityofwater,whencombinedwiththefactthatmeanambienttemperaturesusuallyare
belowthelowerlimitofthethermoneutralzone[32],impliesthatthecostsofmaintenance
usuallyarehigherinaquaticendothermsthaninterrestrialones[30].Then,evenaslightrise
inwatertemperaturecouldrepresentanimportantsavingsintheamountofenergyneeded
forthermoregulation,andthus,anincreaseintheamountofenergythataquaticspeciescould
devotetobodygrowth[35].Third,giventhatgrowthrateinprimaryproducersispositively
relatedtoambienttemperature,globalwarmingisexpectedtoresultinanincreaseinnetpri-
maryproductivity(NPP,aroughproxyofoverallfoodavailabilityinasystem).However,the
realeffectoftemperatureonNPPusuallychangesbetweengeographicareas,dependingon
wateravailabilityinterrestrialsystems[17]andonnutrientavailability(e.g.,nitrogenand
phosphorous)inaquaticsystems[36–37].Inthissense,whileterrestrialspeciesinourdataset
belongtoareasthatstronglydifferinwateravailability(fromdeserttoborealforest),practi-
callyalltheaquaticspeciesoccurinhighlatitudecoastalandinlandsystems,whereapositive
effectoftemperatureonNPPisexpected[37].Thus,atleastinourstudy,temporalchangesin
foodavailabilityprobablydifferedamongterrestrialspecies,butconsistentlyincreasedfor
aquaticspecies.Fourth,thereductioninthemeanbodysizerecentlyrecordedforseveralfish
PLOSONE|https://doi.org/10.1371/journal.pone.0183051 August16,2017 9/12
Climatechangeandbodysizetrendsinendotherms
assemblages,duetosize-at-age,populationage-structure,andspeciescompositionalshifts
[1,3,38],mayhaveledtoanincreaseinthenumberofpreytypesconsumedbyaquaticbirds
andmammals.Inaddition,thereductionintheabundanceoflargerindividualsofsomelarge
speciesoffish,mostlycausedbyhumanexploitation(e.g.,[39]),mayalsoreducetheselective
pressureofcompetitionactingonsomeaquaticendotherms(e.g.,largepredators).Finally,
habitatfragmentationheavilyimpactsterrestrialsystemsandisexpectedtonegativelyaffect
bodysize,becausehomerangedirectlyaffectstheamountofresourcesavailabletoeachspecies
[40].Thus,webelievethatdifferencesinthefactorsfavoringincreasesanddecreasesinbody
sizebetweenaquaticandterrestrialhabitatscouldberesponsibleforthedissimilarpatternof
bodysizechange.However,researchaimedattestingthisideaisnecessary,especiallybecause
relativelyfewaquaticspecieshavebeenanalyzed.
Finally,wefoundthattemporaldecreaseinbodysizeforterrestrialbirdswasnoticeably
greaterduringthesecondhalfthanduringthefirsthalfofthe20thcentury.Ineffect,bothcon-
ventionalandphylogeneticanalysesindicatethatmeanslopevaluebetweenbodymassand
yearofcollectionwasveryclosetozeroforthefirsthalfof20thcentury,butnegativeforthe
secondhalfofthatcentury.Althoughseldomexplored,temporalvariationinbodysize
changesshouldbeexpectedbecauseglobalwarming,aswellasotheranthropogenicmodifica-
tionsofhabitats(fragmentation,pollution,etc),increasednoticeablyafter1950.Thus,our
resultsreinforcetheideathat,atleastforsomegroupsofanimals,humanactivitiesarebehind
therecordedchangesinbodysizepatterns(see[41]).Nevertheless,furtherinvestigationsare
neededtounderstandhowhuman-causedphenotypicchangesarelinkedtopopulationpro-
cess,andhence,toknowiftheyreallycompriseausefulpieceofinformationwhenassessing
“healthstatus”atthepopulationorspecieslevels(see[42]).Thevastdigitalresourceontrait
variabilitynowavailablethroughon-linemuseumdatabasesprovidesopportunitiestoexplore
theeffectsofenvironmentalchangeondiverseorganisms[43].
Supportinginformation
S1Appendix.AppendixwithsupplementaryTablesAandB,andsupplementaryFigures
A,B,CandD.
(DOCX)
S1Dataset.Compilationofdataonbodysizechangefrom46publishedstudies,compris-
ingatotalof369populationsofbirdsandmammals.Studiesreportingthechangesdueto
experimentalmanipulations,colonizationofislands,orspanningover<10yearswere
excluded.
(XLSX)
S2Dataset.Bodymass,yearofcollection,latitude,longitudeandsexforeachindividual
analyzedinthepresentstudy(20,496records).
(XLSX)
Acknowledgments
WearegratefultoJonathanDunnumforhelpingtobuildthedatabase,andtoFelisaSmith,
JamesH.BrownandMatthewSymondsforvaluablecommentsonthedraftmanuscript.The
authorshavenoconflictofinteresttodeclare.
AuthorContributions
Conceptualization:DanielE.Naya,JosephCook.
PLOSONE|https://doi.org/10.1371/journal.pone.0183051 August16,2017 10/12