Warren Porter Mende, 34090Montpellier, France. balance andwintersurvivalprobabilities. predict theimpactofextremeclimaticeventsonanimalenergy energetics modellingandbodyconditionanalysestounderstand spells. Thisstudydemonstratestherelevanceofusingmechanistic strongly suggestthatflamingosstarvedtodeathduringbothcold was primarilydrivenbycoldairtemperatures.Overall,ourfindings and 2012coldspellscomparedwith‘normal’ winters.Thisincrease flamingo energyrequirementswerehighest(+6–7%)duringthe1985 3700 Received 8April2014; Accepted1August2014 ‡ 2 1 climate onspeciesdynamicshavebeenhighlighted,suchas shifts change afterhumanlanduse(Salaetal.,2000).Strongeffects of Climate changeisthesecondmostimportantdriverofbiodiversity Winter stress Fasting, Bodycondition,NicheMapper KEY WORDS:Bioenergetics,Energyrequirements,stores, model NicheMapper requirements offlamingosacross1980–2012usingthemechanistic and/or fasting.Second,weevaluatedthemonthlyenergy them withthosefoundinotherbirdspeciesexposedtocoldspells stores offlamingosfounddeadinFebruary2012,andcompared observed flamingomassmortalities,wefirstassessedtheenergy in theCamargue(southernFrance).To understandthecauseof 2012) ontheenergeticsofgreaterflamingos( we studiedtheeffect oftwocoldspells(January1985andFebruary important tounderstandtheimpactofextremeclimaticevents.Here populations focusongradualtemperaturechanges,yetitisalso Most studiesanalyzingtheeffects ofglobalwarmingonwild Anne-Sophie Deville the Camargue vertebrates: thecaseofgreaterflamingofacingcoldspellsin Impacts ofextremeclimaticeventsontheenergeticslong-lived RESEARCH ARTICLE © 2014.PublishedbyTheCompanyofBiologistsLtd|JournalExperimentalBiology(2014)217,3700-3707doi:10.1242/jeb.106344 *These authors contributed*These equally tothiswork authors 7701, SouthAfrica. Rondebosch CapeTown, Excellence, University of Institute, DST/NRF Centreof Wisconsin, Madison,250N. MillsStreet,Madison,WI53706,USA. CNRS-ULP, 23Rue Becquerel,67087Strasbourg Cedex 2,France. Ecologie, Physiologie etEthologie, UnitéMixtedeRechercheDépartement 7178 Comté, 25030Besançon,France. Chrono-Environnement, UMRUFC/CNRS6249USCINRA,Université deFranche- cold spell(13.0±2%).Further, NicheMapper much lowerthaninwoodcockswhichwerefedthroughoutthissame rusticola body mass,whichisclosetoresultsfoundinwoodcocks( flamingos founddeadin2012correspondedto2.6±0.3%oftotal INTRODUCTION ABSTRACT Author ([email protected]) for correspondence Centre d’EcologieFonctionnelle etEvolutive (CEFE-CNRS),1919Route de Centre deRecherche delaTour duValat, LeSambuc, 13200 Arles, France. ) thatdiedfromstarvationduringacoldspell(1.7±0.1%),and 5 , MeganFitzpatrick TM . Ourresultsshowthatthebodylipidsof 1,2, 5 Department of Zoology, of University of Department *, SophieLabaude 3 Institut Pluridisciplinaire Hubert Curien, Institut PluridisciplinaireHubert TM , Mechanisticmodelling, 5 , PaulMathewson Phoenicopterus roseus TM 1, predicted that *, Jean-PatriceRobin 6 4 FitzPatrick Departement Scolopax 5 ) and DavidGrémillet died inphaseIII likelydiedfromstarvation (Robin etal.,1999). and probablydiedfromhypothermia. Conversely, ananimal that instance, ananimaldeadinphase IIhadremainingenergy reserves which fastingphasetheanimal died(OwenandCook,1977).For from lipidandproteincontents indifferent tissuestodetermine in reserves) andenergy requirements.Bodyconditioncanbe inferred studied throughajointevaluation ofanimalbodycondition(energy (Robin etal.,1988).PhaseIIIisusuallylethal(Cherel protein catabolismandanincreaseinbodymassloss(proteolysis) animal entersphaseIII,whichischaracterizedbyanincrease in net preferential mobilizationoffatstores(lipolysis).Finally, thefasting Phase IIcorrespondstoaprolongedperiodofproteinsparing and organism usesenergy fromitsglycogenreserves(glycogenesis). 1982). Fastingischaracterizedbythreephases.Duringphase I, the undergo afastingperiodleading todeath(DavidsonandEvans, even unavailable(Boosetal.,2007).Animalsmaytherefore andmaintainhomeostasiswhilefoodisscarce or are confrontedwithincreasingenergy requirementstoenhance Stillman andGoss-Custard,2010). helps predictspeciesrangeshifts(KearneyandPorter, 2009; Moreover, forecastinganimalenergetics asafunctionofclimatealso population dynamics(Chownetal.,2010;Bozinovic2011). extreme orgradualclimaticchangescanhelppredictimpactson 2007). Yet, studyingtheenergetic constraints ofspeciesfacing physiological mechanisms(PearsonandDawson,2003;Dormann, species dynamicsarecorrelativeandignoreunderlying et al.,2011). substantially impactinganimalpopulations(Chanetal.,2005;Péron spell dayshasbeenhighforseveraldecades(Vavrus etal.,2006), (e.g. northwesternNorthAmericaandEurope),thenumberofcold Moreover, althoughmanyregionsundergo warmingduringwinter (Bailey, 1955;Welbergen etal.,2008;McKechnieandWolf, 2010). waves havebeenreportedinterrestrialandaquaticecosystems populations. Forinstance,populationcrashesduetosevereheat dynamics, althoughtheycanhavedramaticimpactsonwild climatic eventsareoftenignoredaspotentialdriversofpopulation events (IPCC,2011; RahmstorfandCoumou,2011). Extreme increase inthefrequency, intensityanddurationofextremeclimatic 2010; Mosesetal.,2012).However, climatologistsalsopredictan consequences ofgradualincreaseintemperature(Brittonetal., of climatechangeonspeciesdynamicsprimarilyfocus (Birkhofer etal.,2012;Duriez2012).Studiesontheeffects (Forchhammer etal.,2001)andfluctuationsinpopulationpatterns (Petchey etal.,1999),changesinpopulationlife-historyfeatures in geographicrange(McCarty, 2001),changesinfoodwebstructure The physiologicalimpactsofcoldspellsonorganisms maybe During acoldspell,non-hibernatingandnon-torpidendotherms Most studiesforecastingconsequencesofclimatechangeon 3 , ArnaudBéchet 2,6,‡ 1 , MichelGauthier-Clerc 1,4 ,

The Journal of Experimental Biology energy requirementsofflamingos acrossthe1980–2012period. − (January 1985andFebruary2012).Thelowesttemperatures were Two coldspellswereidentified duringthe1980–2012study and Porter, 2004;Kearneyetal.,2009).NicheMapper range ofspecies(Porteretal.,2000b;Porter2002;Kearney (Porter andMitchell,2006),whichhasbeenvalidatedforalarge colleagues developedathermodynamicmodel,NicheMapper observations ormanipulations(Fortetal.,2011). Porterand energy expenditurewithnoorlimitedneedfortime-consuming 2009). Suchthermodynamicequationsallowtheassessmentof of thermodynamics(KearneyandPorter, 2004;Kearneyetal., of animalsthroughcalculationsbasedonthefundamentalprinciples Mechanistic modellingassessesthetheoreticalenergy requirements modelling (Porteretal.,2000a;Fort2009;2011). heart raterecordings)orbyindirectmethodssuchasmechanistic empirical measures(i.e.doublylabelledwatertechniqueand/or Daily energy expenditurecanbedeterminedeitherbydirect Mapper the 2012coldspell,andusedmechanisticmodelNiche two events,determinedthebodyconditionofbirdsthatdiedduring end, weexaminedthemorphometricsofbirdsthatdiedduring these mortality fromtheCamargue duringthesetwocoldspells.To this accessing food. ponds werenearlycompletelyfrozenover, preventingthebirdsfrom compared withFebruary2012.Duringbothcoldspells,mostofthe the coldspelllastedthreemoredaysandreachedlowertemperatures more than1500flamingos(A.Béchet,unpublisheddata).In1985, 1991). InFebruary2012,anothercoldspellcausedthedeathof caused thedeathofmorethan3000flamingos(Johnsonetal., in theCamargue inJanuary1985(Sanz-Aguilaretal.,2012)that these survivaltrade-offs werestronglymodifiedduringacoldspell southernmost winteringareas(Sanz-Aguilaretal.,2012).However, those winteringfurtheraway, whereasadultssurvivebetterinthe to oratmediumdistancesfromtheirbirthsitesurvivebetterthan experience andenvironmentalfactors.Young birdswinteringclose Cézilly, 2007).Survivalratesforbothstrategiesdependon winter nearthebreedingcolony(Barbraudetal.,2003;Johnsonand western MediterraneanandNorthAfrica,whereasothersspendthe present insummermigratetodistantwinteringareasacrossthe Cézilly, 2007).Inautumn,approximatelyhalfofallindividuals sites intheworld,withanaverageof10,500pairs(Johnsonand (southern France)areoneofthemostimportantflamingobreeding The commercialsaltpansofSalin-de-GiraudintheCamargue invertebrates andseeds(Devilleetal.,2013;Yohannes etal.,2013). (Jenkin, 1957)foragingonadiversifieddietincludingaquatic emblematic ofMediterraneanwetlands.Flamingosarefilterfeeders roseus al., 2002).Here,wefocusonthegreaterflamingo( survival inagivenenvironment(seePorteretal.,2000b; estimate energetic requirementsandtherebyself-maintenance defined morphological,physiologicalandbehaviouralpropertiesto heat andwatermassbalancesofamodelindividualwithuser- RESEARCH ARTICLE collected deadbirds were133femalesand79 males). significantly biasedtowardsfemales ( and 1120 males).In2012thesex ratio wasequalto0.43,so RESULTS χ (number ofdeadmales/overall numberofdeadflamingos=0.63; 2 10.6°C in1985and− =113.13, d.f.=1,P Our objectivewastodeterminethecausesofflamingomass In 1985,thesexratioofdead birdswasbiasedtowardsmales TM Pallas 1811; hereafter‘flamingo’),along-livedbird (Porter andMitchell,2006)toestimatethemonthly <0.005, collecteddeadbirdswere 670females .° n21 Fg 1). 6.6°C in2012(Fig. χ 2 =13.6, d.f.=1,P Phoenicopterus TM computes =0.0002, TM oyms 1766±188 Lipid 1812±177 2056±197 Protein Body mass Plucked bodymass Intact bodymass Body mass,intact bodymassminusfeathersanddigestive tractcontent. 0.003±0.0004% forabdominalfatpadsand0.003±0.001% 0.7±0.1% fortheskin,0.2±0.01%legsandpectoralmuscles, 2.6±0.3% oftotalbodymass(with1.7±0.2%lipidforthecarcass, 1.Average lipidproportionwas spell issummarizedinTable The bodycompositionofsixbirdscollectedduringthe2012cold recordings. cold spells.Source:Tour duValat/Meteo Francestation,basedonhourly Fig. the coldspellofFebruary2012 Table Flamingo bodycondition Flamingo

kn11.8±3.2 30.2±5.4 0.05±0.009 0.06±0.03 3.8±0.4 32.0±4.0 225.9±29.2 30.1±5.4 45.9±8.7 26.0±2.5 Abdominal fatpads Digestive tractfatpads Carcass Pectoral +legs 314.0±39.1 Total lipidmass Carcass Skin Leg Pectoral Total proteinmass Temperature (°C)

.AirtemperaturesduringtheJanuary 1985andFebruary2012 1. –15 –10 –8 –6 –4 –2 –5 10 15 1. Lipidandproteinstoresforsixflamingosfounddeadin 0 2 4 6 0 5 051015 01 20 15 10 5 0 The JournalofExperimentalBiology(2014)doi:10.1242/jeb.106344 January 1985 February 2012 Day Mean (g) Temperature mean Temperature max. Temperature min. 3701

The Journal of Experimental Biology (Wilcoxon, thatdiedin2012.Also,flamingos1985 reference was1.6timeshigherforbirdsthatdiedin1985than W 142 adultflamingoscollectedduringthe2012coldspell(Wilcoxon, flamingos collectedduringthe1985coldspellcomparedwith a sampleof152adultindividualsrandomlypickedamongthe2700 body conditionofthebirds.Residualsweresignificantlysmallerfor 3702 RESEARCH ARTICLE birds. during theFebruary 2012coldspellalongtheRMA regression forreference regression forreferencebirds;squares areresidualsforflamingosthatdied for flamingosthatdiedduringtheJanuary 2015coldspellalongtheRMA represented bythehorizontalline(reference birds).Triangles areresiduals details) for34flamingosingoodcondition thatdiedoutsidecoldspellsis RMA regression betweenlogbodymassandtarsuslength(seetextfor that diedduring/outsidecoldspells. Fig. tarsus length parameters offlamingosingoodcondition[logbodymass=1.85×log 1.5±1.1%, respectively, ofthetotalproteinmass. proteins andpectoralmusclesaccountedfor1.7±0.3% 2).Legmuscle flamingos werebeyondphaseIIoffasting(Fig. woodcocks indifferent phasesoffasting,thisratiosuggeststhat compared withthosefoundformallards( body mass.Thelipid/proteinratioaveraged0.11±0.74. When digestive tractfatpads).Proteinaccountedfor17±0.2%ofthetotal flamingos thatdiedduringtheFebruary2012coldspell. woodcocks [fedordeadduringacoldspell(Péronetal.,2011)] and phases offasting[fed,inphaseIIorIII(Robinetal.,1999)], Fig. =15170.5, Further, theresidualsofanRMA regressioncalculatedwithbody

Lipid/protein ratio (%) .Comparison ofCamargueflamingobodyconditionsforbirds 3. Residuals Comparisonoflipid/proteinratiosformallardsindifferent 2. 100 –0.8 –0.6 –0.4 –0.2 10 20 30 40 50 60 70 80 90 0.4 0.6 0.2 0 0 oto id Coldspellbirds Control birds Woodcock Mallards W − P =4786, 5.23 (R <0.001). Indeed,thedifference fromtheweight 2 P =0.85, February 2012 <0.001) andin2012(Wilcoxon, Phase II of Mallards fasting P <0.001)] allowedustocomparethe The averageoftheresiduals January 1985 Phase III of Mallards fasting Anas platyrhynchos Flamingos Woodcock Reference W =3909.5, ) and (2639 For males,energy requirementsreachedamaximuminJanuary1985 sexes, withvalueshigherthanatanytimeduring1980–2012(Fig. +22.0% forfemales). than thoseprovidedbyNicheMapper males and2178 than males(meanexcludingcoldspells=1785 in July2006.Femaleshadsignificantlylowerenergy requirements males hadameanenergy requirementof2170 both sexes.Overthewholestudyperiod,excludingcoldspells, energy requirementswerelowestinJulyandgreatestJanuaryfor 4).Overall, year, between-yearandintersexualvariability(Fig. Flamingo monthlyenergy requirementsshowedsubstantialwithin- in goodconditionusedasreferenceflamingos(Fig.3). P than thosecalculated withNicheMapper Allometric equationspredicted 24.5%higherenergy requirements during acoldspell(Fig. fasting andclosetothoseofwoodcocksthatdiedfromstarvation with energy storeslowerthan thoseofmallardsinphaseIII that diedinFebruary2012revealedbirdswereextremely lean, caused bystarvation.Specifically, bodycompositionofflamingos flamingo mass-mortalityeventsoccurringduringcoldspells are of flamingosexposedtocoldspells.Ourresultsstronglysuggestthat across a>30 estimations ofmonthlyenergy requirementsinavertebratespecies Our studyprovides,tothebestofourknowledge,first same effect acrosssexes(supplementarymaterialTable energy requirementsofan‘average’ adult.Theseparametershadthe variation ofenergy requirementsgreaterthan1%comparedwiththe material Tables key factorsinfluencingflamingoenergy requirements(supplementary depth, bodydimensions,temperatureandairtemperatureswere considering coldspells.Oursensitivityanalysisshowedthatplumage compared withthemeanvaluesforsamemonthswithout This correspondedtoanincreaseof7%and6.1%,respectively, 2575 Outside coldspells,theirhighestenergy expenditurewas average flamingoenergy requirementsat2763 expenditure was2143 t was 1387 January 1985(2201 spells. Femaleenergy requirementsalsoreachedamaximumin compared withthemeanvaluesforsamemonthsoutsidecold corresponded toanincreaseof6.5%and5.7%,respectively, Niche Mapper Methodological aspects DISCUSSION disproportionately large increasesinmortality. relatively smalldecreases in temperaturearecausing average, flamingosarecloseto theirenergetic limit,suggesting that mortality inJanuary1985.Finally, ourresultsindicatethat,on spell lastingthreemoredays;Fig. 1985 comparedwithFebruary2012(lowertemperaturesanda cold requirements andharsherclimaticconditionsobservedinJanuary flamingos (Fig. energy requirementsduring bothcoldspellsformaleandfemale =3.18, <0.001) hadasignificantlylowerbodyconditionthanflamingos Both coldspellscausedapeakinenergy requirementsforboth kJ kJ day P day <0.001). Outsidecoldspells,theirhighestenergy kJ The JournalofExperimentalBiology(2014)doi:10.1242/jeb.106344 −

− 1 year period,andthefirstbodyconditionmeasurements day 1 in December1980andtheirlowestwas1720 ) andinFebruary2012(2582

TM S3, S4).A 10%variationoftheseparameters ledtoa

kJ

4). Therefore,slightlyhigherlevelsofenergy − 1 modelling day

in July2006.Allometricequationsestimated kJ − kJ day 1

2). Further, ourresultsshowedmaximum for adultfemales.Thesevaluesarehigher day − 1 ) andinFebruary2012(2151 − 1 in December1980andtheirlowest

1) probablyexplainthehigher TM (+23.2% formalesand TM . Similarly, Fort and

kJ kJ

kJ day day kJ day day

− − S3). 1 − 1 , s.d.=208; , s.d.=235. 1

− kJ for adult 1

kJ ). This day day −

4). 1 − ). 1

The Journal of Experimental Biology skewed towardsmalesin1985andfemales2012. more femalesthanmales,withthesexratioofdeadbirds being However, ourresultsshowthatcoldspells didnotsystematicallykill generally mayhavehadslightlymorebodyreservesthanfemales. the onemale,wethereforecannotcompletelyexcludethatmales Although allsixbirdswerefoundtobeextremelylean,including linked tothefactthatmaleflamingosare20%larger thanfemales. sexual differences interms of bodycomposition,whichmaybe flamingo energy requirementsoverextendedtimeperiods. they providethefirstcredibleestimatesoftemporalvariations been validatedusingthedoublylabelledwatermethodinourcase, (Robin etal.,1999). Specifically, theratioof leg proteintopectoral during acoldspellwherefasting wastheprimarycauseofdeath protein tolegwereclose tothoseofwoodcocksfounddead III offasting.Finally, theirbodyconditionandratioof pectoral Further, their bodyconditionwaspoorerthanthatofmallardsinphase significantly lowerthanthoseof flamingosingoodbodycondition. cold spellswasprolongedfasting. Indeed,theirbodymasseswere Our resultssuggestthattheprimarycauseofflamingodeathduring al., 2011). Therefore,althoughNicheMapper which werevalidatedusingthedoublylabelledwatermethod(Fortet provides accurateandreliableestimatesofenergy requirements, contrast, theyshowedthatmechanistic,thermodynamicmodelling and onlyusedbodymassasaninputvalue(Fortetal.,2011). In equations didnotperformwellbecausetheywerespeciesspecific, cormorants (Phalacrocorax carbo).Theyfoundthatallometric overestimated energy requirementsbyalmost21%ingreat colleagues (Fortetal.,2011) showedthatallometricequations RESEARCH ARTICLE What killsflamingosduringcoldspells? What –1

Because ofourlimitedsamplesizewecouldnotexploreinter- Energy requirement (kJ day ) 1700 1800 1900 2000 2100 2200 2300 2400 2500 2600 2700 1400 1500 1600 1700 1800 1900 2000 2100 2200 2300 u u Nov Aug Jul u u o e a e Apr Jun Feb Jan Dec Nov Aug Jul Females Males e a May Mar Sep Oct e a May Mar Sep Oct e Jan Dec e Apr Jun Feb TM outputs havenotyet

Energy requirement Energy requirement (kJ day–1) (kJ day–1) 1850 1950 2050 2150 2250 2200 2300 2400 2500 2600 2700 spell mightalso beimportant,withcoldspells occurringlaterin al., 2001;MathewsonandPorter 2013).Further, thetimingofcold importance offoodavailability (Grémilletetal.,1999;Grémillet with harshenvironmentalconditions, whichalsostressedthe analysing thesurvivalstrategies ofhomeothermicanimalsconfronted but ratherfoodavailability. Thissituationmirrorspolarstudies ultimately controllingwintersurvival wasnotambienttemperature, for alongerperiod.Consequently, onecanspeculatethatthefactor the coldspellofJanuary1985,whenlowertemperatureswerereached temperatures likelyacceleratedenergy storeusage,especiallyduring Energy storesandthenbody temperaturethusdecreaseduntildeath. they probablyalsocouldnotmaintaintheirhomeothermicstatus. temperatures. Asflamingoswereunabletomaintainbodyreserves, own activityandavailabilitymightalsohavebeenreducedby low preventing flamingosfromaccessingtheirinvertebrateprey, whose cold spells,thewatersurfaceofmostpondsCamargue froze, more energy tomaintainaconstant bodytemperature.Duringboth confronted withverylowtemperatures,homeothermsmust use leading todeathbyincreasingflamingoenergy requirements.When Sampled tissuesarecurrentlybeinganalyzed. did notdisplayabnormalparasiteloadsoranyinternaldamage. During the2012mass-mortalityevent,30birdsweredissected.They to detailedautopsiesandscreeningforparasitespathogens. the 1985coldspell,noneofbirdcarcasseswerekeptandsubjected causes otherthanstarvation,includingdisease.Unfortunately, during However, wecannotexcludethepossibilitythatbirdsdiedfrom muscles andsubstantiallycontributedtototalproteindepletion. cold spell(1.8),showingthatthepectoralsweremostdepleted protein (1.2)isclosetothatfoundforwoodcocksdiedduringa Birds diedduringthecoldspells,andnotafterwards.Hence, Overall, coldtemperaturesprobablyacceleratedtheprocess 1986–2011 1980–1984 2012 1985 The JournalofExperimentalBiology(2014)doi:10.1242/jeb.106344 February 2012. requirements inJanuary1985and April 2012. the CamarguefromJanuary1980to for femaleandmaleflamingoslivingin predicted bythemodelNicheMapper Fig.

.Monthlyenergyrequirements 4. The insetsshowtheenergy 3703 TM

The Journal of Experimental Biology 3704 RESEARCH ARTICLE climatic events. Suchacomplementaryapproach iskeytofuture animals energy balancefacingclimaticchanges,including extreme energy requirementsisessentialtoimproveourunderstanding of determination ofboththeamount ofbodyenergy reserves and (Groscolas etal.,2000). mechanism alsoexistsinKing ( catabolism increases(PiersmaandPoot,1993)].A similar when lipidreservesarealmostexhaustedandprotein searching attheonsetoflastphaseenergy catabolism[i.e. undergoing afastingperiod, arefeedingsignaltriggersactivefood many migratorywaders.Forinstance,inknots(Calidriscanutus ) flamingos mayhaveapredeterminedfuel-depletionthreshold, as do either standtheentirewinterorinitiatemigration.Inthiscontext, mortality, afterwhichtheycouldrefuelbodystoressufficiently to see strategy, expectingashortcoldspellthatmaynotcause kilometres, mayleaveimmediatelyattheonsetofcoldspell. have sufficient energy storestomigrateoverthousandsof migrate inordertoescapecoldspells.Thefattestindividuals,who migratory studieswillshowwhetherflamingoshavethecapacityto winter mass-mortalityfor‘resident’ individuals.Forthcoming consequences forthistrade-off, asitmayenhancetheprobabilityof Tank etal.,2002;Cellitti2006;Vavrus et al.,2006)mayhave forecasted increaseinextremeclimaticevents(Walsh etal.,2001; varying proportionofmigratoryandresidentindividuals.The Introduction, Camargue flamingosarepartialmigrantswitha must facenumerousunpredictablewinters.Asmentionedinthe Béchet, unpublisheddata).Also,asalong-livedspecies,flamingos the followingbreedingseason(whichstartedca.3 In flamingos,the2012coldspellmayexplaindelayedlayingduring survival laterinlife(Webster etal.,2002;RungeandMarra,2005). period oftheannualcycle,whichinfluencebreedingsuccessand effects aredefinedasnon-fatalimpactsonindividualsduringone as coldspellshavecarryovereffects onwildpopulations.Those extreme icingeventin1993–1994(Chanetal.,2005). tarandus) underwentan80%reductioninpopulationsizeduring (Péron etal.,2011), andaSvalbardreindeerpopulation( reduced thesurvivalprobabilitiesofwoodcockswinteringinFrance (Brown andBrown,1998).Furthermore,severewinterssignificantly their populationbyapproximately53%insouthwesternNebraska thousands ofcliff swallows( other vertebratespecies.Forinstance,a1996coldspellkilled flamingos intheCamargue (Johnsonetal.,1991)andfornumerous have profoundimpactsonpopulationdynamics.Thisisthecasefor Cold spellskilladultindividualswithinapopulation,andtherefore 1990), whichmayenhancewintersurvivalprobabilities. (Lovvorn, 1994)andintheirmigratorybehaviour(RidgillFox, also showmoreplasticityintheirmanagementofbodyreserves underestimation ofduckmortality(Pain,1991).Nevertheless,ducks but duckcarcassesarelessconspicuous,whichmayleadtoan species suchasducks.Coldspellsalsokillducks(Newton,2007), particularly susceptibletocoldspellscomparedwithotherwaterbird even moreflamingosifithadoccurredinFebruary. Also, onemightconcludethatthe1985coldspellhavekilled the February2012coldspellwasseverebecauseofitstiming(Fig. of depletedenergy stores.Alongtheselines,onemightspeculatethat winter predictedtokillmorebirdsthanearlierinthisseasonbecause Population and migratory implications Population andmigratory To conclude,ourcasestudyhasshownthataccurate Other, leanerindividualsmay, onthecontrary, adoptawait-and- Beyond acutemortality, adverseenvironmentalconditionssuch Further studiesarerequiredtounderstandwhyflamingos Petrochelidon pyrrhonota Aptenodytes patagonicus

weeks later;A. ), reducing Rangifer

4). ) Mapper measurements wereperformedinFebruary2012toparameterizeNiche (Johnson, 1985),andbywinglengthmeasurementin2012.Additional individual (Appendix1).Birdsweresexedbycloacaeanalysisin1985 basic morphologicalmeasurementswasperformedoneachcollected approximately 1500flamingosdied,ofwhich233werecollected.A setof January 1985,ofwhich2700werecollected.InFebruary2012, (between 1and13February).Approximately3000flamingosdiedin environmental parameters experiencedbytheanimal. We usedthelast characteristics oftheanimal,anda microclimatic modelthatcomputeslocal an endothermmodelwithmorphological, physiologicalandbehavioural 2012’ and‘flamingosingoodcondition’. with Wilcoxon testsbetween‘flamingosdeadin1985’, ‘flamingosdeadin allometric functionwerethencalculatedforallflamingosandcompared and birdslivingincaptivity(Gallet,1949).Regressionresidualsalong this combination ofbirdsthatdiedwithgoodbodyconditionoutsidecold spells du Valat (A.Béchet,unpublisheddata).Theremaining25birds were a condition (mostlyduetopowerlinecollision)andwerecollectedatthe Tour 34 flamingosusedasreferences.Nineofthesebirdsdiedwithgood body RMA oflogbodymassandtarsuslengthwasperformedonasample squares linearregression,whichhasbeencriticized(Green,2001). The during bothcoldspells.AnRMA wasusedinsteadofanordinaryleast regression) asempiricalindicesofbodyconditionforflamingosthat died regression typeIImodel(RMA;alsocalledstandardizedmajor axis in duplicateusing1 as nitrogen×6.25(CampbellandLeatherland,1980).Lipidsweredetermined method (CampbellandLeatherland,1980).Proteincontentwascalculated determined intriplicateusing100–150 homogeneous powderforanalysis.Foreachtissue,nitrogencontentwas dried toconstantmassandgroundunderliquidnitrogenobtaina weighed (±0.1 contents. Pectoralmuscles,legsmusclesandskinweredissected cold spellwereweighed(±1 Six deadflamingos(onemaleandfivefemales)collectedduringthe2012 15 et al.,2002).Onlytwocoldspellswereidentified(Fig. in theCamargue foreachcalendardayacrossthe1980–2012period(Tank mean temperaturesbelowthe10thpercentileoftemperaturedistribution We definedacoldspellasperiod ofatleastsixconsecutivedayswithdaily mortality andpopulationdynamicsofwildpopulations. studies predictingtheeffects ofharshweatherconditionsonthe Niche Mapper the woodcocksthatdiedinadvancedphaseIIIduringacoldspell. the ratioofproteinsinpectoralmuscles/proteinslegswiththosefound muscles beforeproteinsfromlegs(Robinetal.,1999),wealsocompared proteins catabolizedduringphaseIIoffastingarethosefrompectoral et al.,1991)(J.-P. Robin,unpublisheddata).Moreover, becausethefirst (Robin etal.,1999)andwithmallardsindifferent phasesoffasting(Robin content withthoseofwinteringwoodcocksthatdiedduringacoldspell condition. We thereforecomparedtheratiooftheirtotalbodylipid/protein experts, wecouldnotfindanydataonenergy storesforflamingosingood measurements was1.1±0.2%(proteins)and0.7±0.1%(lipids). eliminate anyremainingtracesofwater. Reproducibilitybetweenduplicate 24 Flamingo bodycondition Flamingo Study periodanddata collection MATERIALS ANDMETHODS Niche Mapper a 1 Folch andcolleagues(Folchetal.,1957).Total lipidswereextractedfrom by agravimetricmethodon1 masspercentageofbodymass.Ashcontentwasdeterminedinduplicate We usedresiduals( Despite ourefforts atscreeningthroughtheliteratureandconsultingwith days in1985(between3and17January)thesecond13 h. Sampleswerefreeze-driedonceagainpriortoanalysisinorder

g aliquotusingchloroform/methanol(2/1,v/v).Adipositywasthetotal TM (see Tables The JournalofExperimentalBiology(2014)doi:10.1242/jeb.106344 TM

g). Theselattertissuesandtheentirecarcasswerefreeze- TM (US Patent7,155,377B2)isdivided intotwosub-models: modelling

g aliquotsfollowingagravimetricmethodderivedfrom

2, 3;Fig. y -axis deviations)fromaReducedmajoraxis

g drysamplesplacedinamuffle furnacefor

g). Thedigestivetractwasclearedofits A1).

mg aliquotsfollowingtheKjeldahl

1): thefirstlasted days in2012

The Journal of Experimental Biology flamingo shapewasrepresentedbytwoellipsesforthetorsoand head requires parametersrelatedtotheshapeofmodelledanimal.The influences heatexchangewithitsenvironment,theendothermmodelalso Parameter supplementary materialTable information summarizedinTables center ofeachmonthasarepresentativedayfortheentiremonth. solar heatfluxwiththeenvironment).ThemodelusedJuliandayat with thesurroundingmicroclimate(i.e.radiant,convective,evaporativeand required tomaintaintheanimal’s coretemperaturegivenitsheatexchange energy requirementsforeachmonthbycalculatingthemetabolicrate outputs fromthemicroclimatemodelandestimatesflamingo’s daily along thelengthofleg.Briefly, theendothermmodelreceives for speciessuchasflamingositincludesvariationsincoretemperature and Porter(MathewsonPorter, 2013).Thisupdatedversionisadapted of theendothermmodel(Endo2013a)developedbyFitzpatrick,Mathewson version oftheclimaticmodel(Micr2010a)andarecentlyupdated Data aremeans±s.d.Allvaluesfromthepresentstudy. Parameter Physiology andbodycondition RESEARCH ARTICLE Neck Table Table Flight Head Legs Head +neck(seeAppendix Torso length hra odciiyo ls W Thermal conductivityofflesh Plumage depth Feathers length Rachis diameter Feathers length Rachis diameter Rachis diameter Flight Time spentflying Flight altitude Digestive time O Body temperature Body mass Plumage depth Plumage density length Rachis diameter Plumage depth Animal density Flight speed Animal height Plumage density Reflectivity Plumage thickness Reflectivity % Reflectivity Reflectivity Reflectivity Plumage density Plumage density The endothermmodelwasparameterizedusingflamingo-specific 2 extraction efficiency 2. Morphologicalparametersusedintheendothermmodelforflamingos 3. Physiologicalandflightparametersusedintheendotherm model forflamingos

1 formoredetails)

S1). Astheshapeofanimaldirectly mm µm feathers cm mm µm mm µm Units feathers cm mm µm cm % Cm feathers % % % feathers

and3(seealsoAppendices 2 W m days °C kg % cm % Units kg km

cm cm cm cm m m

h –1 –1 –3 – – – – ² ² ² ² °C –1 122.73±42.89 23.04±5.38 573.33±314.35 118.41±38.50 Dorsal 1.64±0.51 108.33±28.23 2.25±0.85 129.07±51.00 20.18±4.73 1.51±0.45 64.80±4.27 1.19±0.33 13.50±3.22 66.5±2.8 2.1±0.8 34.7±9.9 76.5±3.3 21.3±7.3 66.0±16.1 73.00±3.60 Males ( 25.0±2.6 0.125 219 100 Male 39.5 (37.5–45.0) 24.5 2 130 3.579 60 0.5 932.9 Mean value(min–max) n 1, 2,and 9 Females( =9) used inthisstudy(seesupplementarymaterialTable the Tour duValat/Meteo Franceweatherstation(43°30.6 variables (rainfall,humidity, solarradiationandwindspeedat2 on 32adultsfounddeadinFebruary2012(13malesand19females). and threecylindersforthenecklegs.Thesebodypartsweremeasured periods. 1993 andDecember1994asclimaticdatawereunavailableduringthese 2012, exceptbetweenJanuary1987andMarch1988 flamingo energy requirementswereestimatedfromJanuary1980toApril calculated fornon-reproductiveandnon-migrantbirds.Average monthly varied becauseofobservedclimaticfluctuations.Energy requirementswere Flamingo bodycharacteristicswerekeptconstantandenergy requirements standards. Analysesformalesandfemaleswereconductedseparately. study usingthedoublylabelledwatertechnique,time–energy budgetsand Meteorological hourlydataofairtemperatureandstandardmeteorological Niche Mapper All measurementresolutionsandaccuraciescompliedwithinternational 129 eaeReference Female 2.525 110.00±31.62 431.11±159.29 110.00±31.62 19.42±5.04 110.00±31.62 82.47±14.30 Ventral 67.40±4.40 1.48±0.42 2.04±0.80 17.64±4.50 1.40±0.40 1.14±0.17 16.77±22.53 71.7±2.3 1±0.4 37.2±12.7 75.8±3.7 21.3±6.6 74.7±26.9 72.50±3.86 22.6±2.0 The JournalofExperimentalBiology(2014)doi:10.1242/jeb.106344 TM outputs werevalidatedforaquaticbirdsinaprevious MacDonald, 1980 Bech etal.,1979 Present study;SoftwareFlight1.24; Pennycuick,1989; Bruderer andBoldt,2001 Gallet, 1949 ehe l,1979 Bech etal., Galicia andBaldassarre,1997 Cramp andSimmons,1977 mtet al.,2005;BrudererandBoldt,2001 Amat Porter etal.,2006 Cheng andPlewes,2002 Pennycuick, 2008 557.78±358.34 124.82±51.75 22.44±6.25 Dorsal 1.63±0.52 2.45±1.03 20.74±11.14 1.49±0.42 69.8±2.0 3.3±3.2 79.3±3.9 75.70±4.08 25.6±1.6 n =10)

S2) werecollectedat ′ N, 4°41.63′ 413.33±91.95 83.1±16.75 19.38±4.91 18.60±10.20 Ventral 1.58±0.44 2.30±0.86 1.45±0.36 74.3±2.3 1.3±0.4 80.9±2.4 76.90±3.01 23.6

±1.7 m height) E). 3705

The Journal of Experimental Biology were performedinR(RDevelopmentCoreTeam, 2012). parameters (malesandfemalescombined)wereused.Allstatisticalanalyses considering climaticdataduringthesetwoparticularperiods.Meanbird energy requirementsduringcoldspells,weranasecondsensitivityanalysis separately. Additionally, tohighlightthemostcriticalparametersaffecting 2009). Thesensitivityanalysiswasalsoperformedformalesandfemales and maximumvalueswerenotavailable(Grémilletetal.,2003;Fort they weresettoastandardvariabilityof10%theaveragewhenminimum modified accordingtotheirobservedvariation(minimumandmaximum),or input parametersaffecting birdenergy requirements.Inputvalueswereeither and meanbirdparameters(malesfemalesconfounded)toidentifykey Tables mass (g)(Nagy, 2005). 3706 RESEARCH ARTICLE into atriangleand arectangle(11–14) allowedthecalculation ofwingarea. diameter; (17)tarsus length;and(18)tarsusdiameter. Divisionofthewing rectangle length;(13,14)sidesofthe triangle;(15)tibialength;(16) length; (8)torsowidth;(9)wingspan; (10)winglength;(11) wingwidth; (12) beak width;(4)length;(5)neck diameter;(6)necklength;(7)torso following measurementsweretaken: (1)headlength;(2)width;(3) A1.Morphological measurementsofgreaterflamingos. Fig. where fourreplicatesweretaken.Thespectrometerwascalibrated 10 replicateswereperformedforeachbirdarea,exceptthehead, The probewasheldperpendiculartothebirdplumagesurface,and 2500 ASD spectrometerwithawavelengthrangingbetween350and of measurement.Measurementswereperformedusingaportable that wereselectedasthecleanest,andperfectlydryattime per unitarea.Plumagereflectivitywasmeasuredonbirdcarcasses density wasdeterminedforeachareabycountingfeathersplucked area, witharulerplacedperpendiculartotheskin.Finally, plumage central part.Plumagedepthwasalsomeasuredfivetimesforeach binocular microscopetodeterminethediameterofrachisintheir same numberoffeatherswasmeasuredforeachareaundera plucking themusingcallipersforfivefeathersofeacharea.The dorsal andventralsides.Featherlengthsweredeterminedwithout homogeneous area,whereasfortheotherswedistinguished head, neck,torsoandlegs.‘Head’ wasconsideredasone Feather measurementswereconductedforfourdifferent bodyparts: flamingo fieldmetabolicrates(kJ used genericallometricequationsfornon-passerinebirdstoestimate manipulate, andlittleisknownabouttheiryear-round timebudgets.We thus techniques inflamingosbecauseadultsaredifficult tocaptureand allometric equations(Fortetal.,2011). We couldnotusethefirsttwo Mapper Niche sub-model of theendotherm feathers usedtorun flamingosandtheir greater of measurements Morphological APPENDIX 1 We thenperformedtwosensitivity analyses(supplementarymaterial nm, covering97%ofthesolarspectrumatearth’s surface. S3, S4).First,weusedaverageclimaticdataacrossthelast10 14 13 1 TM 5 2 4 3 12 11

day 10 − 1 ) as10.5M 9 17 15 6 b 7 0.681 18 16 8 , whereM The b is body years rto,J . uhrust . ais .D,Gdr,M .adCp,G.H. Copp, and Brown, C.R.andM.B. M.J. Godard, G.D., Davies, J., Cucherousset, J.R., Britton, using Indico oioi,F,Cls,P n pcr J.I. Spicer, and P. Calosi, F., Bozinovic, J.P. Robin, and G. Delacour, T., Zorn, M., Boos, where analyses. A.S.D.,S.L.,D.G.,A.B.andJ.P.R. wrotethepaper. Some parametersinNicheMapper using awhitereferencesurfaceeach10 http://jeb.biologists.org/lookup/suppl/doi:10.1242/jeb.106344/-/DC1 Supplementary materialavailableonlineat French FondUniqueInterministériel(FUI). Salinalgue, theregionProvence-Alpes-Côted’Azur(SouthofFrance)and This studywasfundedbytheFondationMAVA andadoctoralgrantfrom programmed NicheMapper A.S.D., A.B.,D.G.andM.G.C.conceivedtheresearch.W.P., M.F. andP.M. The authorsdeclarenocompetingfinancialinterests. Audusseau substantialinputonNicheMapper birds. MatthieuGuillemainprovidedexpertadviceonwaterfowl,andHélène Marion Vittecoq, MarkGillingham andSébastienMotreuilalsohelpedmeasure Camargue inFebruary2012.AntoineArnaud,Yves Kayser, ThomasBlanchon, We thankthenumerousvolunteers whocollecteddeadflamingosacrossthe 0.7×neck value. was thuscalculatedasfollows:meanvalue=0.3×headvalue+ and theneck70%.Foreachparameter, themeanvalue(head+neck) calculated asfollows: proportions. Theheadwasconsideredasacylinder. Itsareawas the approximateareaofeachparttoconsiderheadandneckinreal area ismuchmoreimportantthantheheadarea.Hence,wecalculated consider theheadandnecktogether. However, inflamingos,theneck abad . ono,A .adBral,G. Bertault, and A.R. Johnson, C., Barbraud, R.M. Bailey, J.M. Ramirez, and A. Garrido, M., Rendon-Martos, M.A., Rendon, J.A., Amat, ikoe,K,Hnce,J n ui,Y. Lubin, and J. Henschel, K., Birkhofer, G.M.O. Maloiy, and K. Johansen, C., Bech, π considered theheadasacylinderandthenanellipsoid:cylinder: mean diameter=0.99 Acknowledgements NicheMapper headandneck for of theareas Calculations of APPENDIX 2 References Supplementary material Funding Author contributions Competing interests formulae: mean=(72+60)/2=66 1.685 and3.31 ×3.4×6.7=72 and tailasymmetryin Cliff Swallowsduringsevere weather. warming temperaturesinatemperateregion. (2010). Non-nativefishesandclimate change:predictingspeciesresponsesto geographic rangeinanimals. in winteringmallards Oecologia on small-scalespatialpatterns:a20-yearstudyofthedistributiondesertspider. condition. fledging dispersalinapopulationofgreaterflamingos:theimportance body of fishesinsouthernMichigan. 183-192. breeding periods:linkingconnectivitytobiologicalprocesses. (2005). Rangingbehaviourofgreaterflamingosduringthebreedingandpost- panting. composition intheflamingo, Hence, theheadrepresented30%oftotalhead+necksurface Two formulaewereusedfortheheadareacalculation.First,we p =1.6 anda Physiol. Zool. J. Anim.Ecol. 170 (1955). Differential mortalityfromhightemperatureinamixedpopulation The JournalofExperimentalBiology(2014)doi:10.1242/jeb.106344 TM , 651-657. TM cm cm, respectively).We thencalculatedameanofboth Pro software. parameterization 2 Anas platyrhynchos , , andellipsoid:4 52, 313-328. b

cm andmeanlength=48.8 72, 246-257. and π TM ×mean diameter×meanlength=152 . A.S.D.,S.L.,J.P.R., A.B.andD.G.performedthe Annu. Rev. Ecol.Evol.Syst. (1998). Intensenaturalselectiononbody sizeandwing Phoenicopterus ruber c Ecology are thesemi-axesofellipsoid(1.685,

cm 36, 526-528. . BirdStudy (2012). Effects ofextremeclimaticevents 2 . Freshw. Biol. TM π (2003). Phenotypiccorrelatesofpost- TM (2011). Physiologicalcorrelatesof ( (1979). Ventilation andexpired gas (2007). Weather andbodycondition modelling. a

p min. Datawereanalyzed (especially forfeathers) b , duringnormalrespirationand 54, 154-159. p + a

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cm 6 cm², =60 2 , with 125 ,

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