the energetic consequences of behavioral variation in a ... · santa cruz, ca, usa 2institute of...

Ecology and Evolution 20181ndash12 emsp|emsp1wwwecolevolorg

Received12December2017emsp |emsp Accepted11February2018DOI 101002ece33983

O R I G I N A L R E S E A R C H

The energetic consequences of behavioral variation in a marine carnivore

Elizabeth A McHuron1 emsp|emspSarah H Peterson12emsp|emspLuis A Huumlckstaumldt1emsp|emsp Sharon R Melin3emsp|emspJeffrey D Harris3emsp|emspDaniel P Costa1

ThisisanopenaccessarticleunderthetermsoftheCreativeCommonsAttributionLicensewhichpermitsusedistributionandreproductioninanymediumprovidedtheoriginalworkisproperlycitedcopy2018TheAuthorsEcology and EvolutionpublishedbyJohnWileyampSonsLtd

1DepartmentofEcologyampEvolutionaryBiologyUniversityofCaliforniaSantaCruzSantaCruzCAUSA2InstituteofMarineSciencesLongMarineLaboratoryUniversityofCaliforniaSantaCruzSantaCruzCAUSA3MarineMammalLaboratoryAlaskaFisheriesScienceCenterNOAASeattleWAUSA

CorrespondenceElizabethAMcHuronDepartmentofEcologyampEvolutionaryBiologyUniversityofCaliforniaSantaCruzSantaCruzCAUSAEmailemchuronucscedu

Funding informationEampPSoundandMarineLifeJointIndustryProgrammeGrantAwardNumber2207-23

AbstractIntraspecificvariabilityinforagingbehaviorhasbeendocumentedacrossarangeoftaxonomicgroupsyettheenergeticconsequencesofthisvariationarenotwellun-derstoodformanyspeciesUnderstandingtheeffectofbehavioralvariationonen-ergy expenditure and acquisition is particularly crucial for mammalian carnivoresbecause theyhavehighenergy requirements that place considerablepressureonpreypopulationsTodeterminetheinfluenceofbehavioronenergyexpenditureandbalance we combined simultaneousmeasurements of at-sea field metabolic rate(FMR)andforagingbehaviorinamarinecarnivorethatexhibitsintraspecificbehav-ioralvariationtheCaliforniasealion(Zalophus californianus)Sealionsexhibitedvari-abilityinat-seaFMRwithsomeindividualsexpendingenergyatamaximumoftwicetherateofothersThisvariationwasinpartattributabletodifferencesindivingbe-haviorthatmayhavebeenreflectiveofdiethoweverthiswasonlytrueforsealionsusingaforagingstrategyconsistingofepipelagic(lt200mwithinthewatercolumn)andbenthicdivesIncontrastsealionsthatusedadeep-divingforagingstrategyallhadsimilarvaluesofat-seaFMRthatwereunrelatedtodivingbehaviorEnergyin-takedidnotdifferbetweenforagingstrategiesandwasunrelatedtoenergyexpendi-tureOur findings suggest that energyexpenditure inCalifornia sea lionsmaybeinfluencedbyinteractionsbetweendietandoxygenconservationstrategiesTherewerenoapparentenergetictrade-offsbetweenforagingstrategiesalthoughtherewas preliminary evidence that foraging strategiesmay differ in their variability inenergybalanceTheenergeticconsequencesofbehavioralvariationmayinfluencethereproductivesuccessoffemalesealionsandresultindifferentialimpactsofindi-vidualsonpreypopulationsThesefindingshighlighttheimportanceofquantifyingtherelationshipsbetweenenergyexpenditureandforagingbehaviorinothercarni-vores forstudiesaddressing fundamentalandappliedphysiologicaland ecologicalquestions

K E Y W O R D S

Californiasealiondoublylabeledwaterfieldmetabolicrateforagingbehaviorintraspecificvariationpinniped

2emsp |emsp emspensp MCHURON et al

1emsp |emspINTRODUC TION

Energy expenditure is central to understanding physiological andecologicalprocessesBodysizeisaninfluentialfactoraffectingen-ergyexpenditurealthoughotherfactorssuchasphylogenytrophiclevelambienttemperatureandbehaviorcanalsocontributetoin-ter-and intraspecificdifferences inenergyexpenditure (Andersonamp Jetz 2005Nagy 2005) Foraging is one of themost energeti-cally expensive behaviors for nonherbivorous species resulting inhighfieldmetabolicrates(FMR)duringsearchpursuitandcaptureof prey (Acevedo-GutieacuterrezCrollampTershy 2002GormanMillsRaathampSpeakman1998Williamsetal2014)Foragingbehaviorsthemselvesarenotnecessarilyenergeticallyequivalentbecauseofpreybehavioralthoughspeciesthatusemorecostlybehaviorsmayexperiencegreaterenergygainsfollowingtheprinciplesofoptimalforagingtheory(AndersonampKarasov1981NagyHueyampBennett1984)Withina species changes in foragingeffort in response tofoodlimitationaffectFMR(BryantampTatner1991Costa2008)butitislesswellunderstoodhowintraspecificvariabilityinforagingbe-haviorinfluencesenergyexpenditureandacquisition

Ecologists have long recognized the existence of intraspecificvariabilityinforagingbehavioryetthisvariationwaslargelyignoredasldquonoiserdquoinecologicalstudiesInthelasttwodecadestheassump-tionthatindividualsareecologicalequivalentshasbeenlargelyin-validatedbystudiesshowingthatindividualdifferencesinforagingbehaviorarewidespreadandcanbeecologicallyimportantevenforspeciesthataregeneralistsatthepopulationlevel(ArauacutejoBolnickampLayman2011Bolnicketal20032011) Intraspecificvariationinforagingbehaviorisoftenmanifestedthroughdietarydifferencesbutalsomayreflectvariation inhabitatusesearchtacticsorfor-agingstrategiesthatareindependentofdiet(CeiaampRamos2015)Becausetheendresultofforagingisenergyexpenditureandacqui-sitiontheabilitytoquantifytherelationshipsbetweenenergyex-penditureandbehaviorisacrucialcomponentinunderstandingthephysiologicalandecologicalconsequencesofvariabilityinforagingbehaviorThisisparticularlyimportantforcarnivoresbecausetheyhavehighenergyrequirementsthatplaceconsiderablepressureonpreypopulations(CarboneTeacherampRowcliffe2007SmithLinkCadrinampPalka2015WilliamsEstesDoakampSpringer2004)andare often important in structuring ecological communities (Rippleetal 2014) Concurrentmeasurements of FMR and behavior arelackingformostlargecarnivoresduetothechallengeofobtainingestimatesofFMRfromfree-ranginganimals

Femalefursealsandsealions(otariids)aregoodmodelspeciestoexaminequestionsabouttheinterplaybetweenenergyexpen-ditureandbehavior in largecarnivoresAll femaleotariidssharesimilar reproductive characteristicsmdashduring lactation they arecentral-placeforagersalternatingshortforagingtripstosea(daystoweeks)withperiodsofonshorenursingattherookery(Costa1991)Thisbehaviormakesthematractablegroupformetabolicstudies as the commonly usedmethod of doubly labeledwaterrequires an individual to be captured twice across a relativelyshorttimeinterval(Speakman1997)Central-placeforagersalso

placeconsiderablepressureonlocalpreypopulationswhichcanresultinresourcelimitationandhighlevelsofcompetition(Elliottetal2009KuhnBakerTowellampReam2014) Individualvari-ation inforagingbehaviorhasbeen increasinglydocumentedforfemaleotariidswhichmaybeamechanismtoreducecompetition(KernaleacuteguenArnouldGuinetampCherel2015Villegas-AmtmannJeglinskiCostaRobinsonampTrillmich2013) Inparticularmanypopulations usemultiple foraging strategies typically character-izedbydifferences indive types (pelagicvsbenthicdives)divedepthand location (Baylisetal2015Kernaleacuteguenetal2016Villegas-AmtmannCostaTremblaySalazarampAurioles-Gamboa2008)withindividualfidelitytoagivenstrategyoftenmaintainedacrossmultiple years (Arthur etal 2015 ChilversampWilkinson2009) Interspecific comparisons of energy expenditure in free-ranging otariids indicate that benthic-diving species often havehigherat-seaFMRsandaremorelikelytoexceedtheircalculatedaerobicdivelimitthanpelagic-foragingspeciesleadingtothehy-pothesisthatbenthicdivingisanenergeticallyexpensivestrategy(CostaKuhnWeiseShafferampArnould2004)Intraspecificvari-ationinspecificbehaviorsalsoappearstoaffectenergyexpendi-tureatseasuchasvariabilityindivedepth(CostaampGales2000)and the proportion of time diving (Arnould Boydamp Speakman1996) Despite the tractability of female otariids for metabolicstudiesthereremainrelativelyfewstudiesthatconcurrentlymea-sureenergyexpenditureandforagingbehavior

Thegoalofourstudywastodeterminehowintraspecificvaria-tionindivingbehavioraffectsenergyexpenditureinCaliforniasealions (Zalophus californianus) an otariid that inhabits the dynamicCalifornia Current Ecosystem and uses foraging strategies thatencompass all three of the diving patterns (epipelagic mesope-lagic andbenthic) characteristicofair-breathingmarinepredators(McHuron etal 2016) Thesediving patterns largely describe thepositionwithinthewatercolumnwheretheanimalforageswhichlargelyreflectpreytypeWeconcurrentlymeasuredFMRandbe-haviorofadultfemaleCaliforniasealionsacrossaforagingtripusingdoublylabeledwaterandanimal-borneinstruments(bio-loggers)to(1) determine the influenceof behavioral variationon at-sea FMRand how foraging strategy influenced these relationships (2) de-terminewhetherat-seaFMRdifferedbetweenforagingstrategiesand (3)examine the relationshipbetweenenergyexpenditureandacquisition

2emsp |emspMATERIAL S AND METHODS

21emsp|emspCapture and instrumentation

Adult female California sea lions were captured at San Nicolas(n = 10SNI) andSanMiguel Islands (n = 6SMI) inNovemberandDecember of 2014 Themajority of femaleswere observed nurs-ingapup(n = 13)theremainingfemaleswerelactatingatthetimeofcapturebutwerenotobservedwithapupOncecaptured inanet females were weighed (plusmn01kg) physically restrained andanesthetizedusinggasanesthesia aloneor in conjunctionwithan

emspensp emsp | emsp3MCHURON et al

intramuscularinjectionofmidazolam(015to020mgkg)adminis-teredwithatropine(002mgkg)

Sealionswereinstrumentedwithsatellitetagsandtime-depthrecorders(TDRWildlifeComputersRedmondWA)andaVHFtag(AdvancedTelemetrySystems IsantiMN)All tagsweremountedon a neoprene base attached to high-tensionmesh netting usingcable ties and affixed to the dorsal midline using a quick-settingepoxyThecombinedpackageweightswerelt1ofbodymassandapproximately2ofthecross-sectionalareaSealionswererecap-turedafteroneforagingtripwhenpossibletoremoveinstrumentsandcollectbloodsamples

22emsp|emspField metabolic rate (FMR)

WeusedthedoublylabeledwatermethodtoestimateFMR(Nagy1980Speakman1997)whichreliesonchangesinoxygenandhy-drogenisotopesinthebloodovertimetoestimateCO2productionThismethodwhichhasbeenvalidatedagainstmeasuresoffoodin-takeandO2consumptionforpinnipeds(Costa1987DaltonRosenamp Trites 2014 Sparling Thompson Fedak Gallon amp Speakman2008)providesanintegratedestimateofenergyexpenditureacrossthemeasurementperiodThesemeasurementscanalsobeusedtocalculatewaterinfluxwhichcanbeusedasaproxyforfoodintakeassealionsgenerallydonotdrinkseawater(Costa1987)

An initial blood sample was collected from the caudal glutealvein into a tube containingnoadditives todeterminebackgroundisotopelevelsThiswasfollowedbyasingleinjectionofaweigheddoseofsterilesalinesolutioncontaining9982Handeither97(~19mlSNI)or1018O(~130mlSMI)Thisresultedingt200ppmenrichmentabovebackground18Olevelsforallindividuals(rangeof207ndash327ppm)whichiswellaboveenrichmentlevelsrecommendedby Speakman (1997) Sea lionswere held for 3ndash4hr postinjectiontoallowtheisotopetoequilibrateinthebodywaterspace(Costa1987) afterwhich a blood samplewas collected todetermine theequilibrationisotopeconcentrationsAfinalbloodsamplewascol-lectedatrecapturetodeterminethefinalisotopeenrichmentSerumandstockisotopesolutionsampleswerestoredfrozenatminus20degCinparafilm-wrappedplasticinternal-threadedcryovialswithanO-ringtopreventevaporation

Serum and stock solution samples were analyzed for isotopeconcentrations by Metabolic Solutions Inc (Nashua NH) Meanisotope concentrations from triplicate measurements were usedinthecalculationofCO2production Isotopedilutionspaceswerecalculated using the plateau (initial) and scaling (final) methods(Speakman1997)ThereareavarietyofequationsthatcanbeusedtocalculateCO2productionandthedifferentequationsaffecten-ergyestimates(SpeakmanampHambly2016)Wechosethetwo-poolSpeakmanNairandGoran(1993)equationbecauseitmostcloselyapproximatesenergyexpenditureofotariids(BoydWoakesButlerDavisampWilliams1995Daltonetal2014)butwealsopresentes-timatescalculatedusing theNagy (1980)equation forcomparisonwithotherstudiesAvalueof236kJLCO2wasusedtoconvertCO2 productiontoenergyconsumption(Costa1987CostaAntonelisamp

Delong1991)Waterinfluxwascalculatedusingequations5and6inNagyandCosta(1980)andthedilutionspacesdeterminedfrom18OAsrecommendedbySpeakman(1997)wealsoestimatedthevariabilityinourestimateofCO2productionasanindicationoftheprecisionofourestimateofFMR(AppendixS1)Theresultingesti-mateofFMRrepresentstimespentatseaandvariableamountsoftimeonshoreweusedtheapproachdescribedinCostaandGales(2003)tocorrectforonshoretimeandestimateat-seaFMR

23emsp|emspAt- sea behavior

SatellitetagscollectedeitherGPSandorARGOSlocationsLocationdatawerefilteredusingacustomspeedandanglefiltertoremoveerroneous locations (gt12kmhr or gt160deg Y Tremblay)Hourly at-sealocationswerepredictedusingacontinuouscorrelatedrandomwalk (Rpackagecrawl JohnsonLondonLeaandDurban (2008)ARGOS)orlinearinterpolation(GPS)Divedatawereanalyzedusinga custom-built program in MATLAB (IKNOS Y Tremblay) Divesweredefinedasanydivege4mthatlastedaminimumof16sDivedatawereusedtocalculate14variables thatdescribedthedivingbehaviorandeffortofeachsealionTheseincludedcharacteristicsofindividualdives(egmeandepth)divebouts(egmeanboutdu-ration) and the foraging trip itself (eg percentage of time spentdivingTableS1)Divedatawerealsousedtoclassifytheforagingtrip(tripsgt6hr)ofeachsealiontooneofthethreeforagingstrate-giesusedbyfemaleCaliforniasealionsusingmethodspresentedinMcHuronetal (2016)which consistedof aprincipal componentsanalysis (PCA) of 14 diving variables followed by a hierarchicalclusteranalysisto identifyforagingstrategies (TableS2)These14variablesweregenerallydifferentfromthosedescribedinTableS1focusingonbehavioralvariationatafinerscalethatdidnotneces-sarily integratebehavioracross theentire foraging trip (egmeandaydepthinsteadofmeandepth)Therewasastrongfocusonvari-ablesthatdescribedthepositionwithinthewatercolumnwhereasea lion foraged (epipelagicmesopelagicbenthic)anddifferencesindayandnightbehaviorasthesevariablesmayreflectdifferencesinpreytypeWecalculatedthese14variablesforeachforagingtripandpredictedthePCAscoresandresultingforagingstrategyusingalineardiscriminantanalysisIfafemalehadmorethanoneforagingtriptoseaweassignedhertoasinglestrategybasedonthedomi-nantstrategyacrossallforagingtrips

24emsp|emspStatistical analyses

Diving variables were strongly correlated with each other pre-cludingtheabilitytoincludemultiplebehavioralvariableswithinthe same regression model Instead we used principal compo-nents regression where the variables of interest are first inputintoaPCAtogenerateareducedsetofuncorrelatedvariablesthatcan then be regressed against at-sea FMR Prior to analysiswereducedourinitial14variablestoasmallersubsetusingexplora-toryplotsofat-seaFMRvseachbehavioralvariable(FigureS2)acoreassumptionofthisapproachisthatthedirection(s)inwhich


the behavioral variables show themost variation is the same asthevariation inat-seaFMRThevariables included in theanaly-sisweremeandivedurationdivedepthboutdurationdescentrateandascentrateVarimaxrotationofthevariableloadingswasusedforinterpretationofeachprincipalcomponentaxisForagingstrategywasincludedasafactorintheregressionanalysistode-termineifforagingstrategyhadanyinfluenceontherelationshipbetweenthesevariablesandat-seaFMR

Meanvaluesofvariablesthatrepresentbehavioracrosstheen-tireforagingtriparegenerallyassumedtobethemostappropriatetoexaminetherelationshipswithat-seaFMRbecausethedoublyla-beledwatermethodproducesasinglevaluethatintegratesallat-seabehaviorAsmentionedabovethesevariablesmaynotcapturefine-scale variation in foraging behavior that has biological relevanceWeexploredwhether therewereanypatterns in at-seaFMRandbehavioralvariation(asquantifiedbytheforagingstrategyanalysis)todetermineifsealionsthatexhibitedsimilarat-seabehavioralsohadsimilarat-seaFMRsToaccomplishthisweusedaManteltesttodeterminethecorrelationbetweendistancematricesofthePCAscoresfromtheforagingstrategyanalysisandat-seaFMR(Rpack-ageveganOksanenetal2017)PCAscoreswereweightedbasedonthevariabilityexplainedbyeachdimensionbeforethedistancematrixwascreated

WeusedPearsonrsquoscorrelationsbetweenat-seaFMRandwaterinfluxratetoassesswhethersealionsthatexpendedmoreenergyobtainedagreaterenergeticgainThereliabilityofwater influxasaproxyforpreyintakeofsealionsinourstudywasassessedusingaPearsonrsquoscorrelationbetweentherateofmasschangeandwaterinfluxrate

AllstatisticalanalyseswereperformedusingRv341 (RCoreGroup2017)MeanvaluesareshownplusmnSDunlessotherwisestated

3emsp |emspRESULTS

MetabolicratemeasurementswereobtainedforninesealionsfromSNIandallsixsealionsfromSMI(Table1)Themeanmeasurementintervalwas95plusmn35days11sealionswererecapturedafteroneforagingtriponeaftertwoforagingtrips(C16)andthreeafter5+trips(SupplementalText)Fieldmetabolicratesrangedfrom152to548Wkgwithmeanvaluesof390plusmn124(SNI)and348plusmn048Wkg (SMI Table1) Females spent between 47 and 83 of themeasurement interval at sea resulting in estimated at-sea FMRsof329to697Wkg(Table2)withsimilarvaluesbetweenthetwoislands (SNI = 545plusmn108Wkg SMI=492plusmn059Wkg one-wayANOVAF113=114p = 31)The largevariabilityamongsea lionsintimespentatseaduringthemeasurementintervalwasbecauseofvariableamountsof timespentashoreat the rookeryand timeashoreatotherhaul-outsitesduringforagingtrips

SealionsfromSNIprimarilyforagedaroundthenorthernChannelIslandswhereasthemajorityofsealionsfromSMIforagednorthoftheChannelIslandsalongorjustoffthemainlandcoast(Figure1)Themajorityofforagingtripsfellintooneoftwoforagingstrategies

amixedstrategyconsistingprimarilyofbenthicandepipelagicdives(31of44 trips) andadeep-diving strategyconsistingprimarilyofdeepepipelagic andmesopelagicdives (11of44 tripsFigureS3)Sealionsthatundertookmultipleforagingtripstoseagenerallyhadsimilarbehavioronall tripsandclearlyhadonedominantforagingstrategyOverall11sealionswereclassifiedasmixedstrategyfor-agerswhereastheremainingfoursealionswereclassifiedasdeep-divingforagers

Thefirsttwoprincipalcomponentsexplained90ofthevari-ance in thedata andwereused in regressionswith at-seaFMRThere was a significant interaction between the first principalcomponentaxisandforagingstrategy(p = 05)thustherelation-shipbetweenat-seaFMRand the firstprincipalcomponentwasevaluatedseparatelyforeachforagingstrategyThefirstprincipalcomponent explained a significant amount of variation in at-seaFMRformixedstrategy(r2 = 49p = 02)butnotdeep-divingfor-agers(r2 = 57p = 24Figure2)Thevariablesthatloadedstronglyonthisaxisweremeandivedepth(054)diveduration(052)andbout duration (066) There was no relationship between at-seaFMRandthesecondprincipalcomponent(r2 = 20p = 09)wherethe remaining two variables ascent and descent rate loadedstronglyWithregardstofine-scalevariationthreeofthefoursealionswith the highest at-sea FMRs clustered together behavior-allyallthreeofthesesealionshadmuchgreaterdaydivingdepthscomparedwithmostoftheothersealionsusingthemixedforag-ingstrategyTherewashowevernocorrelationbetweendistancematricesofat-seaFMRandPCAscores from the foraging strat-egyanalysis(r = minus16psim=081)Thisdidnotchangeifseparatecorrelationswereperformedforeachforagingstrategyindicatingthat sea lionswith similar fine-scale behavior did not necessaryhavesimilarenergyexpenditure(Figure3)

Waterinfluxratesrangedfrom772to1743mlkgminus1dayminus1withmeanvaluesthatweresimilarbetweenislands(SNI = 1317plusmn342mlkgminus1dayminus1 SMI=1321plusmn292mlkgminus1dayminus1 two-way ANOVAF111lt001 p = 96) and foraging strategies (mixed = 1410plusmn143vsdeep = 1285plusmn354mlkgminus1dayminus1two-wayANOVAF111=010p = 55)Water influx rateand the rateofmasschangewereposi-tively correlated (r = 60p = 02 Figure4a) but therewasno cor-relationbetweenat-seaFMRandwaterinfluxrates(r = minus21p = 46Figure4b)

4emsp |emspDISCUSSION

41emsp|emspInfluence of behavior on at- sea FMR

Adult femaleCalifornia sea lionsexhibitedconsiderablevariabilityin at-sea FMR with some individuals spending energy at almosttwice the rateofother individuals For an80kg sea lion this dif-ferenceamounts to consuminganadditional35ndash6kgofpreyperdaydependingontheenergydensityofcommonpreyspeciesWiththeexceptionofGalapagossea lions (Z wollebaeki) thisvariabilityin energy expenditurewhile at sea appears to be relatively com-moninotariidsasnorthernfurseals(Callorhinus ursinus)Antarctic


TABLE 1emspMasspupstatusandpupmassmeasurementintervaltimeatseatotalbodywater(TBW

)waterinfluxandestimatesofCO

2productionandfieldmetabolicrate(FMR)of15

adultfemaleCaliforniasealionsfromSanNicolasandSanMiguelIslands

Sea

lion

IDIn

itial

mas

s (k

g)Fi

nal m

ass (

kg)

Pup

Pup

mas

s (kg

)In

terv

al (d

ays)

Tim

e at

se

a (d

ays)

TBW

()

H2O

influ

x (m

lkg

day

)

CO2 (

mlg

hr)

FMR

(W)

FMR

(Wk

g)

Nag

ySp

eakm

anN

agy

Spea

kman

Nag

ySp

eakm

an

SanNicolas

C2

854

812

Y22

27

241

650

174

0449

023

32453

127

0294

152

C3

780

754

Y-

81

42

647

154

0763

0545

383

72742

500

358

C8

598

634

Y13

09

066

666

172

099

70743

4025

3004

653

488

C12

784

794

U-

171

110

475

129

1045

0836

5406

4326

685

548

C14

862

760

U-

119

84

640

830774

0628

4115

3341

507

412

C16

942

870

Y-

141

88

635

130

088

00678

5227

4029

577

445

C18

860

848

Y-

111

73

651

139

071

30510

399

12856

467

334

C20

828

762

U-

101

48

621

770544

0420

2834

219

0356

275

C22

954

832

Y8

311

27

3630

127

0969

0763

5674

4467

635

500

SanMiguel

WAF2001

845

720

Y19

03

82

2632

850664

0527

3408

270

2435

345

WAF2002

852

798

Y13

09

97

1629

142

0606

0415

327

72243

397

272

WAF2007

818

802

Y148

59

49

636

150

079

10578

4202

3067

519

379

WAF2010

756

740

Y166

48

28

640

124

0756

0571

3706

279

9495

374

WAF2018

869

796

Y19

810

854

644

122

0662

0486

3615

2653

434

318

WAF2025

789

779

Y17

28

158

634

170

0855

0614

4395

3157

561

403

Pupreferstowhetherafemalewasobservednursingapup(Y)orwhetherherpupstatuswasunknown(U)

CO2productionandFMRwerecalculatedusingequationsfromNagy(1980)andSpeakmanetal(1993)


fur seals (Arctocephalus gazella) Australian sea lions (Neophoca ci-nerea)andNewZealandsealions(Phocarctos hookeri)allexhibitedasimilarmagnitudeofrangesinat-seaFMR(CostaCroxallampDuck1989CostaampGales20002003CostaampGentry1986Villegas-Amtmann McDonald Paacuteez-Rosas Aurioles-Gamboa amp Costa2017)DespitethissimilarityCaliforniasealionsexhibitedconsider-ablymore variability in at-sea behavior than these temperate andArcticspeciesexploitingpreyatawiderangeofdepthswithinthewater column and at or near the seafloor This variation in at-seabehaviorofCalifornia sea lionsdidexplain someof thevariabilityinat-seaFMRalthoughtheinfluenceofbehaviorwasaffectedbywhethersealionsusedthemixedordeep-divingforagingstrategy

Thefirstprincipalcomponentexplained49ofthevariationinat-seaFMRforsealionsthatusedthemixedforagingstrategywhichwaspredominantlyduetovariationindivedepthdivedurationandbout duration among sea lions Although all three variables mayhaveinfluencedat-seaFMRdivedepthmayhavebeentheprimarydriver given that (1) dive depth has an influence on dive durationbuttheoppositeisnotnecessarilytrue(ie ittakesmoretimeforsea lions to reachdeeperdepthsbut they canhave longdurationdivesthatare irrespectiveofdepth)and(2)our initialexploratoryplotsbetweenat-seaFMRandeachindividualvariableshowednoapparentrelationshipbetweentheboutdurationofmixedstrategyforagers and at-sea FMR (ie bout duration appearedmore influ-ential for deep-diving sea lions) The finding that at-sea FMR in-creasedwithdivedepthwasunexpectedgivenapreviousstudythatfoundtheoppositerelationship(CostaampGales2000)andbecause

ofenergy-savingswimstrategiesassociatedwithchangesinbuoy-ancythatair-breathingmarinepredatorsuseondeeperdivessuchasstroke-and-glideswimming(CrockerGalesampCosta2001TiftHuumlckstaumldt McDonald Thorson amp Ponganis 2017 WatanukiNiizumaGabrielsenSatoampNaito2003Williamsetal2000)Tiftetal (2017) found that adult female California sea lions primarilyusedpassiveswimmingstrategiesondivesgt100mwhichcomprisedbetweenlt01and63ofalldivesforeachsealionusingthemixedforagingstrategyWhilemixedforagersmayexperiencesomecostsavingsassociatedwithpassiveswimmingstrategiesondeeperfor-agingdivesitappearsthattheyareovershadowedbyotherbehav-iorsondeeperdivesthatresultinincreasedenergyexpenditure

ForCaliforniasealionswesuspectthatchangesindivedeptharerelatedtochangesinpreytypeorpreyageclasssuchthatthesealionsusingthemixedstrategywithhigherat-seaFMRstargeted(orspentmoretimetargeting)preythatwerecostlytofindorcaptureMcHuronetal(2016)hypothesizedthatsealionsusingthisforagingstrategymaytargetspeciesthatarebothdemersalandpelagicsuchasmarketsquid(Doryteuthis opalescens)andPacifichake(Merluccius productus)andscatscollectedfromtheseandother instrumentedsea lions at SanMiguel during our study support this hypothesis(MarineMammal Laboratory unpublished data)Market squid areabundant in thenorthernChannel Islands fromOctober toMarchandareprimarilyfoundwithinthe100misobathwherethemajorityofcommercial fishingoccurs (Maxwelletal2004Zeidbergetal2012)Juvenilehakearetypicallydistributedwithinthewatercol-umn and are frequently consumed by adult female California sea

TABLE 2emspAt-seafieldmetabolicrates(FMR)foradultfemaleCaliforniasealionsandthebehavioralvariablesusedintheprincipalcomponentsregressionValuesforbehavioralvariablesrepresentmeanvaluesforalldivesorboutsacrosstheforagingtrip

Sea lion ID

At- sea FMR (Wkg)

Depth (m) Duration (s) Ascent rate (ms)Descent rate (ms)

Bout duration (hr)Nagy Speakman

Mixed

C2 530 329 545 1193 118 111 13

C8 800 598 933 1850 150 163 15

C12 884 697 1305 2262 144 153 19

C14 672 535 390 1421 115 132 20

C16 785 601 1432 2258 149 153 12

C20 649 495 421 1323 124 143 14

C22 827 644 922 1733 145 144 17

WAF2001 670 521 320 1221 113 121 12

WAF2002 558 393 741 2023 117 133 16

WAF2010 726 547 824 1677 123 131 17

WAF2025 718 520 419 1572 107 106 13

Deep

C3 729 529 1617 2380 144 161 18

C18 656 475 1889 2555 145 159 25

WAF2007 615 451 2030 2652 154 163 33

WAF2018 710 525 1052 1696 102 100 11

At-seaFMRwascalculatedusingequationsfromNagy(1980)andSpeakmanetal(1993)


lionswhereasadulthakearefoundatornearthebottomatdepthscorresponding to thecontinental slope (BaileyFrancisampStevens1982) and are not targeted as frequently as juvenile age classes(Orr VanBlaricom DeLong Cruz-Escalona amp Newsome 2011)Scat samples collected from instrumented females indicated thatadultfemalesconsumedadulthakeduringourstudyperiodandinthe severalmonths following and theat-sea locationsof the foursealionsinthemixedstrategygroupwiththehighestat-seaFMRs

weregenerallyconsistentwithforagingoverthecontinentalslopeThusthepositiverelationshipbetweenat-seaFMRanddepthmayresultfromastrongerdependenceonadulthakethataremoreen-ergeticallyexpensivetocapturethanjuvenilehakeandmarketsquidfoundatshallowerdepthsandorwithinthewatercolumn

Behavioralvariationappeared tohavedifferentenergeticcon-sequences forCaliforniasea lionsdependingon foragingstrategyas indicatedbythesignificant interactionbetweenthefirstprinci-palcomponentandforagingstrategyThismaybeduetosomedif-ferencesinpreytypessuchasmesopelagicfishes(McHuronetal2016)butalsomayreflectagreaterdependenceonpassiveswim-ming strategies and differences in oxygen management betweenthetwoforagingstrategies includingapronounceddiveresponseand lung collapse at deeper depths (Kooyman amp Ponganis 1998McDonaldampPonganis2012)McDonaldandPonganis(2014)foundthediveresponsecharacterizedbyextremebradycardia(lt10beatsmin)ofCaliforniasealionswaspronouncedonlongerdives(68ofdivesgt4minand98ofdivesgt5min)butmorevariableonshortdives(lt3min)whereonly43ofdiveshadheartratesbelowrest-ing Similarly blood flow to swimmingmuscles appears to be re-strictedduringdivesgt100mbutisnotconsistentlyregulatedduringshallowerdivesinthisspecies(Tiftetal2017)Sealionsusingthedeep-diving strategy generally had amuch greater percentage oflong duration dives with an average of 51 of dives gt4min and46gt5mincomparedwithmixedstrategy foragers thatonlyhadanaverageof24ofdivesgt4minand14gt5minTheyalsohadamuchgreaterpercentageofdives todepthsgt200m thanmixedstrategy foragers (46 vs 125) which is the depth associatedwithcompletelungcollapseinthisspecies(McDonaldampPonganis2012)Collectively thissuggests thatbehavioralandphysiological

F IGURE 1emsp Interpolatedat-sealocationsofadultfemaleCaliforniasealionsfromSanNicolasIsland(a)andSanMiguelIsland(b)plottedoverbathymetry

F IGURE 2emspTherelationshipbetweenat-seafieldmetabolicrate(FMR)andthefirstprincipalcomponentforadultfemaleCaliforniasealionsthatusedamixedforagingstrategySealionsthatusedthedeep-divingstrategyareshowningrayforcomparisonThethreebehavioralvariablesthatloadedstrongly(gt03)onthefirstcomponentweredivedepth(054)diveduration(052)andboutduration(066)


mechanisms thatconserveoxygenon longdeepdivesmayaffecttherelationshipsbetweenenergyexpenditureandvariationindiv-ing behaviorWe did not detect any relationships between at-seaFMRandthetwoprincipalcomponentsforsealionsusingthedeep-divingstrategywhichmayhavebeenduetoasmallsamplesizethemitigatingeffectsofoxygenmanagementstrategiesonvariationinat-sea FMR or because the behaviorswemeasured truly did notinfluenceenergyexpenditure

Itisimportanttorecognizethattherewasconsiderablevariationinat-seaFMRthatwasunexplainedbyindividualvariationinbehav-iorparticularly for the11sea lionsusing themixed foragingstrat-egyThe remainingunexplainedvariability couldhavebeendue toa varietyof intrinsic factors such as individual differences in rest-ingmetabolicrates (Broggietal2007LariveacuteeBoutinSpeakmanMcAdamampHumphries2010)differencesinforagingefficiencyduetoexperience(HoskinsCostaWheatleyGibbensampArnould2015McDonald Goebel Crocker Tremblay amp Costa 2009) or individ-ualvariationinmaternalinvestment(McDonaldGoebelCrockerampCosta2012)Italsoispossiblethatwewereunabletocaptureim-portantpredictorvariablesusingthemethodsemployedinthisstudyasweonlymeasuredtwo-dimensionalbehaviorTheuseofadditionalbio-logging devices such as 3-axis accelerometers and video cam-erascanbeattachedtomanylargepredatorsandwouldbehelpfulinfurtherelucidatingbehaviorsthatmayaffectenergyexpenditureparticularlyasitrelatestooverallbodymovementanddiet

42emsp|emspInfluence of foraging strategy on at- sea FMR and prey intake

Therewerenodifferences in themeanat-seaFMRorwater influxratesbetweensealionsusingthemixedanddeep-divingstrategiessuggesting therewere no clear energetic benefits associatedwithusingoneparticularforagingstrategyItislikelyhoweverthattheen-ergeticcostofaforagingstrategyisdynamicthroughtimegiventhatat-seaFMRisaffectedbydivingbehaviorwhichvariesduetotempo-ralvariationinthedistributionofpreyspecies(KuhnampCosta2014MelinDeLongampSiniff2008)Ourfindingsregardingtheenergetictrade-offsbetweenforagingstrategiesshouldthereforenotbeex-trapolated beyond our study year without further measurementsOurdatawerenotconsistentwiththehypothesisthatbenthicdivingisenergeticallyexpensive(Costaetal2004)asindicatedbythesim-ilarityinmeanat-seaFMRsbetweenthetwoforagingstrategiesandthelackofacorrelationbetweenbehavioralandenergeticsimilarityItmaybethatdivingtoorneartheseafloorisnotitselfinherentlyenergetically costly but that the expense is driven by the specificbehaviorsundertakenwhileatdepthThustheremaynotbeclearintra-orinterspecifictrendsforotariidsbecausedifferentindividualsorspeciesmayexpendvariableamountsofenergyonbenthicdivesdependingonthebehaviorsusedandpreytypesthatarepursued

While therewasa lackofenergetic trade-offsbetween forag-ingstrategiessealionsusingthedeep-divingstrategyneitherlost

F IGURE 3emspDendrogramofdistancematrixofthefirstthreeprincipalcomponentsfromtheforagingstrategyanalysisshowinghowindividualsealionsclusteredtogetherinmultivariatespacewithrespecttofine-scalevariationinforagingbehaviorThecolorbarrepresentsat-seaFMRwithvaluesrangingfromlow(yellow)tohigh(red)Therewasnocorrelationbetweenbehavioralandenergeticdistancematricesillustratedherebythelackofdistinctcolorclusters

F IGURE 4emspCorrelationsbetweenwaterinfluxratesandmasschange(a)andat-seafieldmetabolicrate(FMRb)for15adultfemaleCaliforniasealionsColorsrepresentsealionsthatuseddifferentstrategiesontheirforagingtriptosea(mixedforagingstrategy(black)ordeep-divingstrategy(gray))


norwonbigintermsofenergybalanceasevidencedbythesmallerand intermediate ranges of at-sea FMRs water influx rates andmasschangescomparedwithmixedstrategyforagersThispatterndeserves furtherexplorationbecause itmaybean indication thatforagingstrategiesdifferinthevariabilityofenergybalancethatanindividualsealionexperiences

43emsp|emspBalancing energy expenditure and gain

Therewas no evidence that sea lions that expended energy at ahigherratehadagreaterrateofpreyintakewhichiscontradictorytowhatwewouldexpectbasedonpredictionsofoptimalforagingtheoryWaterinfluxrateisnotsynonymouswithpreyorenergyin-takewhenthedietisunknown(Costa1987)butthepositivecor-relationwiththedailyrateofmasschangeforsealionssuggeststhathigherratesofwaterinfluxwerereflectiveofgreaterpreyintakeandthuslikelygreaterenergyintakePreviousstudieshavefoundvari-able resultswithpositive relationshipsdetectedforsomebutnotallotariidspecies(Arnouldetal1996Costa2008CostaampGales2000 2003 Costa amp Gentry 1986 Costa etal 1989 Villegas-Amtmannetal2017)PupmassesandgrowthratesfromSMIwerebelowaveragein2014(Leisingetal2015)andevidencefromourstudysupportsthehypothesisthatforagingconditionsinsouthernandcentralCaliforniawereunfavorableforsealionsThemajorityof our sea lions lostmass across themeasurement period whichisatypicalof thesetypesofstudies (Arnouldetal1996CostaampGales20002003CostaampGentry1986Costaetal19891991)Althoughmostsealionswerestillnursingapuptheir6-month-oldpups weighed considerably less than the long-term average of7-month-oldpups(16vs25ndash28kgSMelinunpublished)andtherewaslargevariationinpupmassamongfemalesConsequentlythelackofapositiverelationshipbetweenat-seaFMRandwaterinfluxmayreflectthedifficultforagingconditionsencounteredbysealionsthatwerebalancingreproductiveandmaintenancecostsduringun-favorableconditionsThewiderangeofpupmassesindicatedtherewas individual variation in the amount of energy being deliveredto pups through lactation Differentialmaternal investment couldexplain some of the variability in energy expenditureprey intakeamongsealions(iesmallpupsrequirelessenergythanlargepups)butalsomayreflectthathighereffortdidnotyieldgreaterpreyyieldandthatthisenergydeficitwastransferredtothepup(iesealionsmayworkharderwhentheyareunsuccessful)

5emsp |emspCONCLUSIONS

Intraspecific variation in behavior has clear energetic conse-quencesforfemaleCaliforniasealionswhichhasimplicationsforreproductivesuccessandpopulationdynamicsVariablesthatin-tegratedbehavioracrosstheentireforagingtripwere importantpredictorsofenergyexpenditurebut foraging strategywasnothowever the classification of individuals to a foraging strategywasimportantinelucidatingthebehaviorsthatinfluencedenergy

expenditureAlthoughsealionshavetheflexibilitytoswitchfor-aging strategies they generally use one dominant strategy andexhibitconsistencyintheirmeandivedepthanddurationacrossforaging trips at least at short temporal scales (1ndash2monthsMcHuron2016)Duringourstudyperiodpupswerestilldepend-ent on their mothers for nutrition and therefore their growthwasdependentonenergyobtainedoneachforagingtripbytheirmothersConsequently even short-term increases in energyex-penditure could negatively impact pup growth particularly asthese increasesarenotnecessarilyoffsetby increases inenergygainforthemother

Thereappearstobeanupperlimitontherangeinat-seaFMRsexhibitedbyotariidswhichmayenableCaliforniasealionstofunc-tioninadynamicenvironmentbyconstrainingenergyexpenditurewhileallowingfortheexploitationofpreyatawiderangeofdepthsandhabitatsWefoundrelationshipsbetweenenergyexpenditureandbehaviorthatdifferednotonlybetweenforagingstrategiesbutalsowithstudiesonotherotariidspecieshighlightingtheneedtobecautious inextrapolatingfindingswithoutabetterunderstand-ingofthemechanismsdrivingtheserelationshipsWehypothesizethattheinfluenceofbehavioralvariationonenergyexpenditureofCaliforniasealionsismodulatedbyinteractionsbetweenpreytypeandphysiologicalmechanismsforoxygenconservationbutfurtherstudyisneededtoprovidesupportforthishypothesis

Theresultsfromourstudyunderscoretheneedtoquantifytheenergeticconsequenceofbehavioralvariationforlargecarnivoresespeciallygiventhedisproportionateinfluenceofcarnivoresoneco-systemdynamicsThesetypesofstudieshaveprimarilybeenlimitedtoasmallrangeofspeciesbuttechnologicaladvancesandpairingofdatafromcaptiveindividualsandwildpopulationsmakeitincreas-inglypossibletoquantifytheserelationshipsforlargecarnivores

ACKNOWLEDG MENTS

Thisresearchwouldnothavebeenpossiblewithoutsupport fromtheUSNavyNationalMarine Fisheries Service Channel IslandsNationalParkChannel IslandsAviation andassistance fromJohnUgoretz Mike Tift Doug Krause Tracey Goldstein Erin BrodieAlexMcHuronDeniseGreigLaurenCampbellandTerrySprakerWewouldalso liketoacknowledgethetwoanonymousreviewerswhosecommentsimprovedthismanuscriptFundingwasprovidedbytheEampPSoundandMarineLifeJointIndustryProgramme(2207-23)AnimalhandlingwaspermittedunderNMFSpermit17952andapprovedbytheUniversityofCaliforniaSantaCruzInstitutionalAnimalCareandUseCommittee

CONFLIC T OF INTERE S T

Nonedeclared

DATA ACCE SSIBILIT Y

AlldataarepresentedintextorasSupplementalMaterial


AUTHOR CONTRIBUTIONS

DPCandEAMconceivedtheideasanddesignedthemethodologyEAMSHPLAHSRMandJDHcollectedthedataEAManalyzedthedataandledthewritingofthemanuscriptAllauthorscontrib-utedcriticallytothedraftsandgavefinalapprovalforpublication

ORCID

Elizabeth A McHuron httporcidorg0000-0003-3147-2628

R E FE R E N C E S

Acevedo-GutieacuterrezACrollDAampTershyBR(2002)HighfeedingcostslimitdivetimeinthelargestwhalesThe Journal of Experimental Biology2051747ndash1753

AndersonK JampJetzW (2005)Thebroad-scaleecologyofenergyexpenditureofendothermsEcology Letters8310ndash318httpsdoiorg101111j1461-0248200500723x

AndersonRampKarasovW(1981)Contrastsinenergyintakeandex-penditure insit-and-waitandwidelyforaging lizardsOecologia4967ndash72httpsdoiorg101007BF00376899

ArauacutejoMSBolnickDIampLaymanCA(2011)TheecologicalcausesofindividualspecialisationEcology Letters14948ndash958httpsdoiorg101111j1461-0248201101662x

Arnould J Boyd I L amp Speakman J R (1996) The relation-ship between foraging behavior and energy expenditure inAntarctic fur seals Journal of Zoology 239 769ndash782 httpsdoiorg101111j1469-79981996tb05477x

ArthurBHindellMBesterMTrathanPJonsenIStanilandIhellipLeaM-A(2015)ReturncustomersForagingsitefidelityandtheeffectofenvironmentalvariabilityinwide-rangingAntarcticfursealsPLoS ONE10e0120888httpsdoiorg101371journalpone0120888

BaileyKMFrancisRCampStevensPR(1982)ThelifehistoryandfisheryofPacificwhitingMerluccius productus CalCOFI ReportsXXIII81ndash98

Baylis A Orben R Arnould J Peters K Knox T Costa D ampStanilandI(2015)Divingdeeperintoindividualforagingspecializa-tionsofalargemarinepredatorthesouthernsealionOecologia1791053ndash1065httpsdoiorg101007s00442-015-3421-4

BolnickD IAmarasekare PArauacutejoM SBuumlrgerR Levine JMNovakMhellipVasseurDA(2011)Whyintraspecifictraitvariationmatters in community ecologyTrends in Ecology and Evolution26183ndash192httpsdoiorg101016jtree201101009

BolnickDISvanbaumlckRFordyceJAYangLHDavisJMHulseyCDampForisterML(2003)TheecologyofindividualsIncidenceandimplicationsofindividualspecializationThe American Naturalist1611ndash28httpsdoiorg101086343878

Boyd I LWoakesA J Butler P JDavis RWampWilliams TM(1995)Validationof heart rate anddoubly labelledwater asmea-suresofmetabolicrateinswimmingCaliforniasealionsFunctional Ecology9151ndash161httpsdoiorg1023072390559

BroggiJHohtolaEKoivulaKOrellMThomsonRLampNilssonJ Aring (2007) Sources of variation in winter basal metabolic ratein the great tit Functional Ecology 21 528ndash533 httpsdoiorg101111j1365-2435200701255x

BryantDMampTatnerP(1991)IntraspeciesvariationinavianenergyexpenditureCorrelatesandconstraintsIbis133236ndash245

Carbone C Teacher A amp Rowcliffe JM (2007) The costs of car-nivoryPLoS Biology5e22

CeiaFRampRamosJA(2015)Individualspecializationintheforag-ingandfeedingstrategiesofseabirdsAreviewMarine Biology1621923ndash1938httpsdoiorg101007s00227-015-2735-4

Chilvers B ampWilkinson I (2009)Diverse foraging strategies in lac-tating New Zealand sea lionsMarine Ecology Progress Series 378299ndash308httpsdoiorg103354meps07846

CostaDP(1987)Isotopicmethodsforquantifyingmaterialandenergyintakeoffree-rangingmarinemammalsInACHuntleyDPCostaGAJWorthyampMACastellini(Eds)Approaches to marine mammal energetics(pp43ndash66)LawrenceKSSocietyforMarineMammalogy

CostaDP(1991)ReproductiveandforagingenergeticsofpinnipedsImplicationsforlifehistorypatternsInDRenouf(Ed)The behaviour of pinnipeds (pp 300ndash344) Dordrecht Netherlands Springerhttpsdoiorg101007978-94-011-3100-1

CostaDP(2008)Aconceptualmodelofthevariationinparentalatten-danceinresponsetoenvironmentalfluctuationForagingenergeticsoflactatingsealionsandfursealsAquatic Conservation Marine and Freshwater Ecosystems17S44ndashS52

Costa D P Antonelis G A amp Delong R L (1991) Effects ofEl Nintildeo on the foraging energetics of the California sea lionIn F Trillmich amp K A Ono (Eds) Pinnipeds and El Nintildeo (pp156ndash165) Berlin Heidelberg Springer-Verlag httpsdoiorg101007978-3-642-76398-4

CostaDPCroxallJPampDuckCD (1989)ForagingenergeticsofAntarcticfursealsinrelationtochangesinpreyavailabilityEcology70596ndash606httpsdoiorg1023071940211

CostaDPampGalesNJ(2000)Foragingenergeticsanddivingbehav-ioroflactatingNewZealandsealionsPhocarctos hookeri Journal of Experimental Biology2033655ndash3665

CostaDPampGalesNJ(2003)EnergeticsofabenthicdiverSeasonalforaging ecology of the Australian sea lion Neophoca cinerea Ecological Monographs7327ndash43httpsdoiorg1018900012-9615(2003)073[0027EOABDS]20CO2

CostaDPampGentryRL(1986)ReproductiveenergeticsofnorthernfursealsInRLGentryampGLKooyman(Eds)Fur seals Maternal strategies on land and at sea (pp 79ndash101) PrincetonNJPrincetonUniversityPress

CostaDPKuhnCEWeiseMJShafferSAampArnouldJPY(2004)Whendoesphysiologylimittheforagingbehaviouroffreelydiving mammals International Congress Series 1275 359ndash366httpsdoiorg101016jics200408058

CrockerDEGalesNJampCostaDP(2001)Swimmingspeedandforaging strategies of New Zealand sea lions (Phocarctos hook-eri) Journal of Zoology 254 267ndash277 httpsdoiorg101017S0952836901000784

DaltonA JM RosenDA SampTritesAW (2014) Season andtime of day affect the ability of accelerometry and the doublylabeledwatermethods tomeasureenergyexpenditure innorth-ern fur seals (Callorhinus ursinus) Journal of Experimental Marine Biology and Ecology 452 125ndash136 httpsdoiorg101016jjembe201312014

ElliottKHWooKJGastonAJBenvenutiSDallrsquoAntoniaLampDavoren G K (2009) Central-place foraging in an Arctic seabirdprovidesevidenceforStorer-AshmolersquosHaloThe Auk126613ndash625httpsdoiorg101525auk200908245

GormanMLMillsMGRaathJPampSpeakmanJR(1998)HighhuntingcostsmakeAfricanwilddogsvulnerabletokleptoparasitismbyhyaenasNature8521992ndash1994

HoskinsAJCostaDPWheatleyKEGibbensJRampArnouldJPY(2015)InfluenceofintrinsicvariationonforagingbehaviourofadultfemaleAustralianfursealsMarine Ecology Progress Series526227ndash239httpsdoiorg103354meps11200

JohnsonDLondonJLeaMampDurbanJ (2008)Continuous-timecorrelatedrandomwalkmodelforanimaltelemetrydataEcology891208ndash1215httpsdoiorg10189007-10321

Kernaleacuteguen L Arnould J P Y Guinet C amp Cherel Y (2015)Determinants of individual foraging specialization in large


marine vertebrates the Antarctic and subantarctic furseals Journal of Animal Ecology 84 1081ndash1091 httpsdoiorg1011111365-265612347

KernaleacuteguenLDorvilleNIerodiaconouDHoskinsAJBaylisAMMHindellMAhellipArnouldJPY(2016)FromvideorecordingstowhiskerstableisotopesAcriticalevaluationoftimescaleinassessingindividual foraging specialisation inAustralian fur sealsOecologia180657ndash670httpsdoiorg101007s00442-015-3407-2

KooymanGLampPonganisPJ(1998)ThephysiologicalbasisofdivingtodepthBirdsandmammalsAnnual Review of Physiology6019ndash32httpsdoiorg101146annurevphysiol60119

KuhnCEBakerJDTowellRGampReamRR(2014)Evidenceoflocalized resourcedepletion followinganatural colonizationeventbyalargemarinepredatorJournal of Animal Ecology831169ndash1177httpsdoiorg1011111365-265612202

KuhnCEampCostaDP(2014)Interannualvariationintheat-seabe-haviorofCaliforniasealions(Zalophus californianus)Marine Mammal Science301297ndash1319httpsdoiorg101111mms12110

Lariveacutee M L Boutin S Speakman J R McAdam A G ampHumphries M M (2010) Associations between over-wintersurvival and resting metabolic rate in juvenile North Americanred squirrels Functional Ecology 24 597ndash607 httpsdoiorg101111j1365-2435200901680x

Leising AW Schroeder I D Bograd S J Abell J Durazo R ampOthersA(2015)StateoftheCaliforniaCurrent2014ndash15Impactsof the warm-water ldquoBlobrdquo California Cooperative Oceanic Fisheries Investigations Report5631ndash68

MaxwellMRHenryAElvidgeCDSafranJHobsonVRNelsonIhellipHunterJR(2004)FisherydynamicsoftheCaliforniamarketsquid (Loligo opalescens) as measured by satellite remote sensingFishery Bulletin102661ndash670

McDonald B I GoebelM E Crocker D E amp Costa D P (2012)Dynamic influence of maternal and pup traits on maternal careduring lactation in an income breeder the Antarctic fur sealPhysiological and Biochemical Zoology 85 243ndash254 httpsdoiorg101086665407

McDonaldBIGoebelMECrockerDETremblayYampCostaDP (2009)Effectsofmaternal traitsand individualbehavioron theforaging strategies and provisioning rates of an income breedertheAntarcticfursealMarine Ecology Progress Series394277ndash288httpsdoiorg103354meps08308

McDonaldBIampPonganisPJ(2012)LungcollapseinthedivingsealionHoldthenitrogenandsavetheoxygenBiology Letters81047ndash1049httpsdoiorg101098rsbl20120743

McDonaldBIampPonganisPJ(2014)Deep-divingsealionsexhibitex-tremebradycardiainlong-durationdivesThe Journal of Experimental Biology2171525ndash1534httpsdoiorg101242jeb098558

McHuronE(2016)An Individual-Based Approach to the Foraging Behavior and Energetics of a Generalist Marine Predator PhD DissertationUniversityofCaliforniaSantaCruzSantaCruzCA

McHuronEARobinsonPWSimmonsSEKuhnCEFowlerMampCostaDP(2016)Foragingstrategiesofageneralistmarinepred-ator inhabiting a dynamic environmentOecologia182 995ndash1005httpsdoiorg101007s00442-016-3732-0

MelinSDeLongRampSiniffD(2008)TheeffectsofElNintildeoontheforagingbehaviorof lactatingCalifornia sea lions (Zalophus califor-nianus californianus)duringthenonbreedingseasonCanadian Journal of Zoology86192ndash206httpsdoiorg101139Z07-132

NagyKA(1980)CO2productioninanimalsAnalysisofpotentialerrorsinthedoubly labeledwatermethodAmerican Journal of Physiology - Regulatory Integrative and Comparative Physiology 7 466ndash473httpsdoiorg101152ajpregu19802385R466

NagyKA(2005)FieldmetabolicrateandbodysizeJournal of Experimental Biology2081621ndash1625httpsdoiorg101242jeb01553

NagyKAampCostaDP(1980)WaterfluxinanimalsAnalysisofpo-tentialerrorsinthetritiatedwatermethodThe American Journal of Physiology238R454ndashR465

NagyKAHueyRBampBennettAF(1984)Fieldenergeticsandfor-agingmodeofKalaharilacertidlizardsEcology65588ndash596httpsdoiorg1023071941421

OksanenJBlanchetFFriendlyMKindtRLegendrePMcGlinnD hellip Wagner H (2017) vegan Community Ecology Package Rpackageversion24-4RetrievedfromhttpsCRANR-projectorgpackage=vegan

Orr A VanBlaricom G DeLong R Cruz-Escalona V amp NewsomeS (2011) Intraspecific comparison of diet of California sea lions(Zalophus californianus) assessed using fecal and stable isotopeanalyses Canadian Journal of Zoology 89 109ndash122 httpsdoiorg101139Z10-101

RCoreTeam(2017)RAlanguageandenvironmentforstatisticalcom-putingRFoundationforStatisticalComputingViennaAustriaURLhttpswwR-projectorg

RippleW JEstes JABeschtaRLWilmersCCRitchieEGHebblewhite M hellip Schmitz O J (2014) Status and ecologicaleffects of the worldrsquos largest carnivores Science 343 1241484httpsdoiorg101126science1241484

SmithLALinkJSCadrinSXampPalkaD(2015)ConsumptionbymarinemammalsontheNortheastUScontinentalshelfEcological Applications25373ndash389httpsdoiorg10189013-16561

SparlingCEThompsonDFedakMAGallonSLampSpeakmanJ R (2008) Estimating fieldmetabolic rates of pinnipedsDoublylabelledwatergetsthesealofapprovalFunctional Ecology22245ndash254httpsdoiorg101111j1365-2435200701368x

SpeakmanJR(1997)Doubly labelled water Theory and practiceLondonUKChapmanampHall

Speakman J R ampHambly C (2016) Using doubly-labelledwater tomeasure free-living energy expenditure Some old things to re-memberandsomenewthingstoconsiderComparative Biochemistry and Physiology Part A Molecular and Integrative Physiology2023ndash9httpsdoiorg101016jcbpa201603017

SpeakmanJRNairKSampGoranMI(1993)Revisedequationsforcalculating CO2 production from doubly labeledwater in humansThe American Journal of Physiology264E912ndashE917

TiftMSHuumlckstaumldtLAMcDonaldBIThorsonPHampPonganisP J (2017) Flipper stroke rate and venous oxygen levels in free-rangingCaliforniasealionsThe Journal of Experimental Biology2201533ndash1540httpsdoiorg101242jeb152314

Villegas-AmtmannSCostaDTremblayYSalazarSampAurioles-GamboaD (2008)Multipleforagingstrategies inamarineapexpredator the Galapagos sea lion Zalophus wollebaeki Marine Ecology Progress Series 363 299ndash309 httpsdoiorg103354meps07457

Villegas-AmtmannSJeglinskiJWECostaDPRobinsonPWampTrillmichF(2013)Individualforagingstrategiesrevealnicheover-lapbetweenendangeredgalapagospinnipedsPLoS ONE8e70748httpsdoiorg101371journalpone0070748

Villegas-AmtmannSMcDonaldBIPaacuteez-RosasDAurioles-GamboaDampCostaDP (2017)Adapted tochangeLowenergy require-mentsinalowandunpredictableproductivityenvironmentthecaseoftheGalapagossealionDeep Sea Research Part II Topical Studies in Oceanography14094ndash104

WatanukiYNiizumaYGabrielsenGWSatoKampNaitoY(2003)Strokeandglideofwing-propelleddiversDeepdivingseabirdsad-just surge frequency to buoyancy changewith depth Proceedings of the Royal Society of London B Biological Sciences270 483ndash488httpsdoiorg101098rspb20022252

Williams T M Davis R W Fuiman L A Francis J Le Boeuf BJHorningMhellipCrollDA (2000) Sink or swim Strategies for


cost-efficient diving by marine mammals Science 288 133ndash136httpsdoiorg101126science2885463133

WilliamsTMEstesJADoakDFampSpringerAM(2004)KillerappetitesAssessingtheroleofpredatorsinecologicalcommunitiesEcology853373ndash3384httpsdoiorg10189003-0696

WilliamsTMWolfeLDavisTKendallTRichterBWangYhellipWilmersCC (2014) Instantaneous energetics of cougar kills re-vealsadvantageoffelidsneakattacksScience34681ndash85httpsdoiorg101126science1254885

Zeidberg L D Butler J L Ramon D Cossio A Stierhoff K L ampHenryA (2012)Estimationof spawninghabitatsofmarket squid(Doryteuthis opalescens) from field surveysof eggsoffCentral andSouthern California Marine Ecology 33 326ndash336 httpsdoiorg101111j1439-0485201100498x

SUPPORTING INFORMATION

AdditionalSupportingInformationmaybefoundonlineinthesup-portinginformationtabforthisarticle

How to cite this articleMcHuronEAPetersonSHHuumlckstaumldtLAMelinSRHarrisJDCostaDPTheenergeticconsequencesofbehavioralvariationinamarinecarnivore

Ecol Evol 2018001ndash12 httpsdoiorg101002ece33983


1emsp |emspINTRODUC TION

Energy expenditure is central to understanding physiological andecologicalprocessesBodysizeisaninfluentialfactoraffectingen-ergyexpenditurealthoughotherfactorssuchasphylogenytrophiclevelambienttemperatureandbehaviorcanalsocontributetoin-ter-and intraspecificdifferences inenergyexpenditure (Andersonamp Jetz 2005Nagy 2005) Foraging is one of themost energeti-cally expensive behaviors for nonherbivorous species resulting inhighfieldmetabolicrates(FMR)duringsearchpursuitandcaptureof prey (Acevedo-GutieacuterrezCrollampTershy 2002GormanMillsRaathampSpeakman1998Williamsetal2014)Foragingbehaviorsthemselvesarenotnecessarilyenergeticallyequivalentbecauseofpreybehavioralthoughspeciesthatusemorecostlybehaviorsmayexperiencegreaterenergygainsfollowingtheprinciplesofoptimalforagingtheory(AndersonampKarasov1981NagyHueyampBennett1984)Withina species changes in foragingeffort in response tofoodlimitationaffectFMR(BryantampTatner1991Costa2008)butitislesswellunderstoodhowintraspecificvariabilityinforagingbe-haviorinfluencesenergyexpenditureandacquisition

Ecologists have long recognized the existence of intraspecificvariabilityinforagingbehavioryetthisvariationwaslargelyignoredasldquonoiserdquoinecologicalstudiesInthelasttwodecadestheassump-tionthatindividualsareecologicalequivalentshasbeenlargelyin-validatedbystudiesshowingthatindividualdifferencesinforagingbehaviorarewidespreadandcanbeecologicallyimportantevenforspeciesthataregeneralistsatthepopulationlevel(ArauacutejoBolnickampLayman2011Bolnicketal20032011) Intraspecificvariationinforagingbehaviorisoftenmanifestedthroughdietarydifferencesbutalsomayreflectvariation inhabitatusesearchtacticsorfor-agingstrategiesthatareindependentofdiet(CeiaampRamos2015)Becausetheendresultofforagingisenergyexpenditureandacqui-sitiontheabilitytoquantifytherelationshipsbetweenenergyex-penditureandbehaviorisacrucialcomponentinunderstandingthephysiologicalandecologicalconsequencesofvariabilityinforagingbehaviorThisisparticularlyimportantforcarnivoresbecausetheyhavehighenergyrequirementsthatplaceconsiderablepressureonpreypopulations(CarboneTeacherampRowcliffe2007SmithLinkCadrinampPalka2015WilliamsEstesDoakampSpringer2004)andare often important in structuring ecological communities (Rippleetal 2014) Concurrentmeasurements of FMR and behavior arelackingformostlargecarnivoresduetothechallengeofobtainingestimatesofFMRfromfree-ranginganimals

Femalefursealsandsealions(otariids)aregoodmodelspeciestoexaminequestionsabouttheinterplaybetweenenergyexpen-ditureandbehavior in largecarnivoresAll femaleotariidssharesimilar reproductive characteristicsmdashduring lactation they arecentral-placeforagersalternatingshortforagingtripstosea(daystoweeks)withperiodsofonshorenursingattherookery(Costa1991)Thisbehaviormakesthematractablegroupformetabolicstudies as the commonly usedmethod of doubly labeledwaterrequires an individual to be captured twice across a relativelyshorttimeinterval(Speakman1997)Central-placeforagersalso

placeconsiderablepressureonlocalpreypopulationswhichcanresultinresourcelimitationandhighlevelsofcompetition(Elliottetal2009KuhnBakerTowellampReam2014) Individualvari-ation inforagingbehaviorhasbeen increasinglydocumentedforfemaleotariidswhichmaybeamechanismtoreducecompetition(KernaleacuteguenArnouldGuinetampCherel2015Villegas-AmtmannJeglinskiCostaRobinsonampTrillmich2013) Inparticularmanypopulations usemultiple foraging strategies typically character-izedbydifferences indive types (pelagicvsbenthicdives)divedepthand location (Baylisetal2015Kernaleacuteguenetal2016Villegas-AmtmannCostaTremblaySalazarampAurioles-Gamboa2008)withindividualfidelitytoagivenstrategyoftenmaintainedacrossmultiple years (Arthur etal 2015 ChilversampWilkinson2009) Interspecific comparisons of energy expenditure in free-ranging otariids indicate that benthic-diving species often havehigherat-seaFMRsandaremorelikelytoexceedtheircalculatedaerobicdivelimitthanpelagic-foragingspeciesleadingtothehy-pothesisthatbenthicdivingisanenergeticallyexpensivestrategy(CostaKuhnWeiseShafferampArnould2004)Intraspecificvari-ationinspecificbehaviorsalsoappearstoaffectenergyexpendi-tureatseasuchasvariabilityindivedepth(CostaampGales2000)and the proportion of time diving (Arnould Boydamp Speakman1996) Despite the tractability of female otariids for metabolicstudiesthereremainrelativelyfewstudiesthatconcurrentlymea-sureenergyexpenditureandforagingbehavior

Thegoalofourstudywastodeterminehowintraspecificvaria-tionindivingbehavioraffectsenergyexpenditureinCaliforniasealions (Zalophus californianus) an otariid that inhabits the dynamicCalifornia Current Ecosystem and uses foraging strategies thatencompass all three of the diving patterns (epipelagic mesope-lagic andbenthic) characteristicofair-breathingmarinepredators(McHuron etal 2016) Thesediving patterns largely describe thepositionwithinthewatercolumnwheretheanimalforageswhichlargelyreflectpreytypeWeconcurrentlymeasuredFMRandbe-haviorofadultfemaleCaliforniasealionsacrossaforagingtripusingdoublylabeledwaterandanimal-borneinstruments(bio-loggers)to(1) determine the influenceof behavioral variationon at-sea FMRand how foraging strategy influenced these relationships (2) de-terminewhetherat-seaFMRdifferedbetweenforagingstrategiesand (3)examine the relationshipbetweenenergyexpenditureandacquisition

2emsp |emspMATERIAL S AND METHODS

21emsp|emspCapture and instrumentation

Adult female California sea lions were captured at San Nicolas(n = 10SNI) andSanMiguel Islands (n = 6SMI) inNovemberandDecember of 2014 Themajority of femaleswere observed nurs-ingapup(n = 13)theremainingfemaleswerelactatingatthetimeofcapturebutwerenotobservedwithapupOncecaptured inanet females were weighed (plusmn01kg) physically restrained andanesthetizedusinggasanesthesia aloneor in conjunctionwithan


















3emsp |emspRESULTS














Sea

lion

IDIn

itial

mas

s (k

g)Fi

nal m

ass (

kg)

Pup

Pup

mas

s (kg

)In

terv

al (d

ays)

Tim

e at

se

a (d

ays)

TBW

()

H2O

influ

x (m

lkg

day

)

CO2 (

mlg

hr)

FMR

(W)

FMR

(Wk

g)

Nag

ySp

eakm

anN

agy

Spea

kman

Nag

ySp

eakm

an

SanNicolas

C2

854

812

Y22

27

241

650

174

0449

023

32453

127

0294

152

C3

780

754

Y-

81

42

647

154

0763

0545

383

72742

500

358

C8

598

634

Y13

09

066

666

172

099

70743

4025

3004

653

488

C12

784

794

U-

171

110

475

129

1045

0836

5406

4326

685

548

C14

862

760

U-

119

84

640

830774

0628

4115

3341

507

412

C16

942

870

Y-

141

88

635

130

088

00678

5227

4029

577

445

C18

860

848

Y-

111

73

651

139

071

30510

399

12856

467

334

C20

828

762

U-

101

48

621

770544

0420

2834

219

0356

275

C22

954

832

Y8

311

27

3630

127

0969

0763

5674

4467

635

500

SanMiguel

WAF2001

845

720

Y19

03

82

2632

850664

0527

3408

270

2435

345

WAF2002

852

798

Y13

09

97

1629

142

0606

0415

327

72243

397

272

WAF2007

818

802

Y148

59

49

636

150

079

10578

4202

3067

519

379

WAF2010

756

740

Y166

48

28

640

124

0756

0571

3706

279

9495

374

WAF2018

869

796

Y19

810

854

644

122

0662

0486

3615

2653

434

318

WAF2025

789

779

Y17

28

158

634

170

0855

0614

4395

3157

561

403









Sea lion ID

At- sea FMR (Wkg)



Mixed

C2 530 329 545 1193 118 111 13

C8 800 598 933 1850 150 163 15

C12 884 697 1305 2262 144 153 19

C14 672 535 390 1421 115 132 20

C16 785 601 1432 2258 149 153 12

C20 649 495 421 1323 124 143 14

C22 827 644 922 1733 145 144 17

WAF2001 670 521 320 1221 113 121 12

WAF2002 558 393 741 2023 117 133 16

WAF2010 726 547 824 1677 123 131 17

WAF2025 718 520 419 1572 107 106 13

Deep

C3 729 529 1617 2380 144 161 18

C18 656 475 1889 2555 145 159 25

WAF2007 615 451 2030 2652 154 163 33

WAF2018 710 525 1052 1696 102 100 11

























ACKNOWLEDG MENTS



Nonedeclared






ORCID


R E FE R E N C E S






























































































3emsp |emspRESULTS














Sea

lion

IDIn

itial

mas

s (k

g)Fi

nal m

ass (

kg)

Pup

Pup

mas

s (kg

)In

terv

al (d

ays)

Tim

e at

se

a (d

ays)

TBW

()

H2O

influ

x (m

lkg

day

)

CO2 (

mlg

hr)

FMR

(W)

FMR

(Wk

g)

Nag

ySp

eakm

anN

agy

Spea

kman

Nag

ySp

eakm

an

SanNicolas

C2

854

812

Y22

27

241

650

174

0449

023

32453

127

0294

152

C3

780

754

Y-

81

42

647

154

0763

0545

383

72742

500

358

C8

598

634

Y13

09

066

666

172

099

70743

4025

3004

653

488

C12

784

794

U-

171

110

475

129

1045

0836

5406

4326

685

548

C14

862

760

U-

119

84

640

830774

0628

4115

3341

507

412

C16

942

870

Y-

141

88

635

130

088

00678

5227

4029

577

445

C18

860

848

Y-

111

73

651

139

071

30510

399

12856

467

334

C20

828

762

U-

101

48

621

770544

0420

2834

219

0356

275

C22

954

832

Y8

311

27

3630

127

0969

0763

5674

4467

635

500

SanMiguel

WAF2001

845

720

Y19

03

82

2632

850664

0527

3408

270

2435

345

WAF2002

852

798

Y13

09

97

1629

142

0606

0415

327

72243

397

272

WAF2007

818

802

Y148

59

49

636

150

079

10578

4202

3067

519

379

WAF2010

756

740

Y166

48

28

640

124

0756

0571

3706

279

9495

374

WAF2018

869

796

Y19

810

854

644

122

0662

0486

3615

2653

434

318

WAF2025

789

779

Y17

28

158

634

170

0855

0614

4395

3157

561

403









Sea lion ID

At- sea FMR (Wkg)



Mixed

C2 530 329 545 1193 118 111 13

C8 800 598 933 1850 150 163 15

C12 884 697 1305 2262 144 153 19

C14 672 535 390 1421 115 132 20

C16 785 601 1432 2258 149 153 12

C20 649 495 421 1323 124 143 14

C22 827 644 922 1733 145 144 17

WAF2001 670 521 320 1221 113 121 12

WAF2002 558 393 741 2023 117 133 16

WAF2010 726 547 824 1677 123 131 17

WAF2025 718 520 419 1572 107 106 13

Deep

C3 729 529 1617 2380 144 161 18

C18 656 475 1889 2555 145 159 25

WAF2007 615 451 2030 2652 154 163 33

WAF2018 710 525 1052 1696 102 100 11

























ACKNOWLEDG MENTS



Nonedeclared






ORCID


R E FE R E N C E S


















































































Sea

lion

IDIn

itial

mas

s (k

g)Fi

nal m

ass (

kg)

Pup

Pup

mas

s (kg

)In

terv

al (d

ays)

Tim

e at

se

a (d

ays)

TBW

()

H2O

influ

x (m

lkg

day

)

CO2 (

mlg

hr)

FMR

(W)

FMR

(Wk

g)

Nag

ySp

eakm

anN

agy

Spea

kman

Nag

ySp

eakm

an

SanNicolas

C2

854

812

Y22

27

241

650

174

0449

023

32453

127

0294

152

C3

780

754

Y-

81

42

647

154

0763

0545

383

72742

500

358

C8

598

634

Y13

09

066

666

172

099

70743

4025

3004

653

488

C12

784

794

U-

171

110

475

129

1045

0836

5406

4326

685

548

C14

862

760

U-

119

84

640

830774

0628

4115

3341

507

412

C16

942

870

Y-

141

88

635

130

088

00678

5227

4029

577

445

C18

860

848

Y-

111

73

651

139

071

30510

399

12856

467

334

C20

828

762

U-

101

48

621

770544

0420

2834

219

0356

275

C22

954

832

Y8

311

27

3630

127

0969

0763

5674

4467

635

500

SanMiguel

WAF2001

845

720

Y19

03

82

2632

850664

0527

3408

270

2435

345

WAF2002

852

798

Y13

09

97

1629

142

0606

0415

327

72243

397

272

WAF2007

818

802

Y148

59

49

636

150

079

10578

4202

3067

519

379

WAF2010

756

740

Y166

48

28

640

124

0756

0571

3706

279

9495

374

WAF2018

869

796

Y19

810

854

644

122

0662

0486

3615

2653

434

318

WAF2025

789

779

Y17

28

158

634

170

0855

0614

4395

3157

561

403









Sea lion ID

At- sea FMR (Wkg)



Mixed

C2 530 329 545 1193 118 111 13

C8 800 598 933 1850 150 163 15

C12 884 697 1305 2262 144 153 19

C14 672 535 390 1421 115 132 20

C16 785 601 1432 2258 149 153 12

C20 649 495 421 1323 124 143 14

C22 827 644 922 1733 145 144 17

WAF2001 670 521 320 1221 113 121 12

WAF2002 558 393 741 2023 117 133 16

WAF2010 726 547 824 1677 123 131 17

WAF2025 718 520 419 1572 107 106 13

Deep

C3 729 529 1617 2380 144 161 18

C18 656 475 1889 2555 145 159 25

WAF2007 615 451 2030 2652 154 163 33

WAF2018 710 525 1052 1696 102 100 11

























ACKNOWLEDG MENTS



Nonedeclared






ORCID


R E FE R E N C E S



















































































Sea lion ID

At- sea FMR (Wkg)



Mixed

C2 530 329 545 1193 118 111 13

C8 800 598 933 1850 150 163 15

C12 884 697 1305 2262 144 153 19

C14 672 535 390 1421 115 132 20

C16 785 601 1432 2258 149 153 12

C20 649 495 421 1323 124 143 14

C22 827 644 922 1733 145 144 17

WAF2001 670 521 320 1221 113 121 12

WAF2002 558 393 741 2023 117 133 16

WAF2010 726 547 824 1677 123 131 17

WAF2025 718 520 419 1572 107 106 13

Deep

C3 729 529 1617 2380 144 161 18

C18 656 475 1889 2555 145 159 25

WAF2007 615 451 2030 2652 154 163 33

WAF2018 710 525 1052 1696 102 100 11

























ACKNOWLEDG MENTS



Nonedeclared






ORCID


R E FE R E N C E S




































































































ACKNOWLEDG MENTS



Nonedeclared






ORCID


R E FE R E N C E S
















































































ORCID


R E FE R E N C E S













































































the energetic consequences of behavioral variation in a ... · santa cruz, ca, usa 2institute of...

Documents