SexdifferencesinthestopoverecologyofCurlewSandpipersCalidrisferrugineaatarefuellingareaduringautumnmigration
JORDIFIGUEROLA*andALBERTBERTOLERODepartmentofAnimalBiology(Vertebrate),FacultyofBiology,UniversityofBarcelona,Avda.Diagonal645,E-08028Barcelona,Spain
WeinvestigatedthestopoverpatternsofmaleandfemaleCurlewSandpipersatastopover areainnortheast Spain.CurlewSandpipers weretrapped andcolour-ringedduringautumnmigrationin1992and1993.Stopoverlengthwassimilartothosereportedpreviouslyforthisandotherwadersthatmigrateusingasmallnumberofwidelyseparatedstagingareas,butweregreaterthanstopovers reported forotherwadersthatmigrate usingalargenumber of stagingareasseparatedbyshortdistances.Thedifferencesinstopoverlengthbetweenthe birdsusingthesetwostrategiescouldbe relatedtothe fuelreservesthathavetobeaccumulatedtoreachthenextstagingarea.Malesstayedlongerin theareathanfemales.Seasonalchangesinpreyavailabilityorsexdifferencesinmoultingandmigratorypatternsdonotaccountforthesedifferencesinstopoverecology.Following atime-selectedmodelofoptimalmigration,sex differencesinstopoverecologycouldberelatedtoadominanceofthelargerfemalesoverthemalesortoahigherforagingefficiencyorashortersearchandsettlingtimeinfemales.Whetherthesedifferencesarerestrictedtothestudiedareaorarewidespreadinotherstagingareasusedbythespeciescouldbe important for assessing the possible differences in the migration speed ofCurlewSandpipers.Thefindingthatmalesleavethebreedinggrounds21—35daysbeforefemalesbutarriveatthestudyareawithonlya10-daydifferencesupportsthehypothesisthatfemalesmigratefasterthanmalesatleastinthefirsthalfoftheirmigration.
uring migration, long-distance migrantshavetoreplenishtheirenergeticreservesseveraltimesatanumberofstagingareas.1Theoveralltimeneededtocompletemigrationislimited by the time necessary to accumulatenewreserves2 (shortperiodsofflightalternatewithlonger onesoffataccumulation)and,toa
lesser extent, by flight speed. Two strategies ofmigrationhavebeendescribedanddocu-mented mainlyinwaders.3Thefirststrategyisusedby‘hoppers’whichmakeshortflightsandusealargenumberofstagingareasalongtheir
*Correspondenceauthor.
Email:
migratory route. The second is used by
‘jumpers’whichflylargedistancesbetweenthe
smallnumberofstagingareastheyuseto com-
pletetheirmigration.
AlerstamLindström2 producedamodel
based on the optimization criteria of the
decisionsfacedbyabirdaccumulatingfatata
staging area.Thesemodelsassumedthatabird
assessedthemomenttoleaveastagingareain
terms of its present fat reserves, rate of fat
accumulationanditsexpectedfuturefatgain.2,4
These authors presented different models to
explainthedecisionsofabirdatastopover
area. The differences between these models
relyonthevariablesthebirdstrytooptimize.
‘Time-selected’ migrants are expected to
maximizemigrationspeedandsoareverysensitivetovariationsintheirfatdepositionrate.Accordingtothismodel,birdswithhigher intake rates or which select habitatswith greater food resources will migratefasterthanotherbirdsthatdonotforageasefficiently or use less favourable habitats.
‘Energy-selected’migrantstrytocompletetheirmigrationwithlowerenergeticcostsbymaximizingtherelationshipbetweenflightrangeandfatload.Theutilityofaccumulatingadditionalfatdecreaseswithincreasingfatreservesbecauseheavybodymassincreasesflightcosts.5 AlerstamLindström’smodelpredictsthatmigrationdecisionsofenergy-selectedmigrantsarelesssensitivetovari-ationsinfatdepositionrate.
Accordingtothetime-selectedmigrationmodel,dominantindividualsormoreefficientforagersshoulddepartearlierand/orwithgreaterfatreservesthansubdominantsbecausedominantswillbeabletoforageinmorefavourableareas.Inspecieswithenergy-selectedmigration,dominantsshoulddepartwithlowerfatloadsthansubdominantsand,accordingtothismodel,nodifferenceinstopoverlengthistobeexpectedbetweenthesetwogroups.Inthismodeltheprimarybenefitfordominantsisareducedcostforsearchandsettling.2Theeffectofsocialstatusondeparturemassandstopoverlengthintime-selectedmigrantscouldexplainthedifferencesinstopoverecologyofyoungandadultsofseveralspeciesduringautumnmigration6,7 andofmalesandfemalesinspring.8,9
Despitethefactthatmoststudiesofthestopoverecologyofwadershavefoundage-relateddifferencesintheresidencepatternsinautumn,7,1Onostudyhasfocusedonthestopoverpatternsofmalesandfemalesatastagingareaduringtheautumnmigration.Suchstudiescouldprovidebasicinformationtodeterminethepossibleintraspecificdiffer-encesinthecostsofmigration,informationnecessarytodeterminethefactorsresponsibleforthewinterdistributionofwaders.11 InthisstudyweanalysethestopoverpatternsofadultmaleandfemaleCurlewSandpipersCalidrisferrugineaatastagingareainautumn.ThestopoverecologyofthisspecieswasexaminedinrelationtotheoptimizationmodelsofAlerstamLindström2totestthehypothesisthatthesexesdifferintheirstopoverlength.
METHODS
Curlew Sandpiper migration was studied atLesSalinesdelaTrinitat(4O°37′NOO°35′E;northeastSpain).Thestudyareaconsistedofanareaofmudandsand-flatsinasaltpannearthesandycoastoftheMediterraneanSea.Littletidaloscillationoccursonthiscoastandthegreatestvariationinwaterlevelinthesaltpanwasproducedbychangesinwindforceanddirection,orwhensaltextractionwasinprogress. Birds were trapped at night bymist-netandbydayusingwalk-in-trapsfrom
27 July to 12 October 1992 and 25 July to
24September1993.Birdswerecolour-ringed
andbodymass,wing,billandtarsuslengthsof
mostbirdsweremeasured.12 Individualswere
aged12 andthesexofadultbirds(morethan
one-year-old)wasdeterminedfromwingand
billlengthusingthediscriminantformulaof
Wymengaetal.13Bodymassatringingwascor-
rectedtoremovetheeffectofwaterlossandthe
emptying of the gut occurring between
captureanddatarecording,assumingarateof
masslossofO.88%perhourofcaptivity.14 Data
from moulting birds were not included in
the analysis because moulting increases the
energeticrequirementsofbirds15,16 andtherate
ofreserveaccumulationatthestudyareawas
lower in moulting than in non-moulting
Curlew Sandpipers.17 Because the rate of
reserveaccumulationwasoneofthevariables
thataffectstopoverdecisions,2 theinclusionof
thesebirdswouldhaveaffectedtheresultsof
ouranalysis.
Estimationofstopoverlength
Approximatelyeveryotherdayatransectof2.2kmwassurveyedtolocateandidentifycolour-ringedbirdspresentinthearea.Fromthistransectwecensused44haofmudandsand-flats,coveringmostofthesuitablehabitatforCurlewSandpipersinthesaltpan.Additionalrecordsofcolour-markedbirdsobtainedfromcasualobservationswerealsoconsidered.Estimatingtruestopoverlengthisdifficultbecausebirdswereusuallynottrappedimme-diatelyafterarrivalnorjustbeforeleavingthestudy area. To estimate stopover length weusedthemethoddescribedinHolmgrenetal.7
Thismethodisbasedonamark—recapturemodelderivedfrom Jolly18 and Seber.19 The
assumptionsofthismodelarethateachindividualhasaconstantprobabilityofstayingintheareaandthattheprobabilityofresightingwasthesameforallbirds.Usingthismodelwecalculatedthemaximumlikelihoodestimateofthestopoverprobability(ϖ)andtheestimateofmeanstopoverlength(τ) separatelyfor eachsexoneachyear(seeHolmgrenetal.7 foradetaileddescriptionofthemodelandparame-terestimation).
Statisticalanalyses
Differencesinstopoverprobabilitiesweretest-edbycalculatingthestandardnormaldeviate(d)andtheassociatedPvalue.7Differencesinbodyconditionamonggroupsweretestedwithsquare-root-transformedbodymassusing a trifactorial ANCOVA. In this analysissex(male/female),control(resighted/notresighted)andyear(1992/1993)wereusedasfactors.Culmenlengthwasintroducedasacovariatetoremovetheeffectofbodysizeonbodymass.WhensignificantinteractionsbetweenthefactorsweredetectedweusedScheffèmultiplerangeteststoexaminethedifferencesbetweenparticularlevelsofthefactors.2O
RESULTS
Relationship ofbodymassandstopoverlength
Althoughfemaleswerelargerthanmales,21differencesinbodymasswerenotsignificantaftercontrollingfortheeffectofbirdsize(three-wayANCOVA,F1,9O1 =O.27,P=O.61)and
noneoftheinteractionsofsexwiththeothertwofactorswassignificant(sex—control:F1,9O1=
2.11,P=O.15;sex—year:F1,9O1 =1.27,P=O.26).Bodymassofmarkedbirdswasgreaterin1992thanin1993(three-wayANCOVA,F1,9O1=17.O7,P
O.OOO1). Bodymassof birds resighted didnotdifferfromthosethatwerenotresighted(three-wayANCOVA,factorcontrol,F1,9O1=1.27,P=O.26).
However,asignificantinteractionwasdetectedbetweentwoofthefactors(control—year,F1,9O1 =4.29,P=O.O4).Thissignificantinteractionappearedbecausebirdsresightedin
1993wereleanerthanbirdstrappedin1992(bothresightedandnotresighted,Scheffètests,PO.OO3forbothcomparisonsandPO.2Ofortherestofcontrast).Therelationshipsbetweenbody mass at ringing and stopover lengthwerealsoanalysedseparatelyforeachsexandyear.Noneofthelinearregressionsbetweenbodymassandstopoverlengthwassignificant(rrangingfrom—O.O5to—O.12andPfromO.3OtoO.71).
Frequencyandlengthofstopover
In1992wecolour-marked517individuals,ofwhich99werelaterresighted(19.1%).In1993,
89outof393markedindividualswereresight-edafterthedateofringing(22.6%).Numbersofmarkedandresightedindividualsdidnotdifferbetweenyears(χ2 =1.67,1df,P=O.2O),norbetweensexes(1992:χ2=1.43,1df,P=O.23;
1993:χ2=O.45,1df,P=O.5O).Theestimatedstopoverlengthofmaleswaslongerthanfemalesin1992(d = 1.84,P O.O5), in1993(d=1.87,PO.O5),andwhendataofbothyearswerecombined(d=2.64,PO.OO5),seeTable1.
Table1.Observedmeanstopoverlengthofmalesandfemalesresightedatleastonce(t)andestimatedmeanstopoverlengthoftheCurlewSandpiperpopulation(τ)bothexpressedindays.Dailystopoverprobability(ϖ)anditsstandarddeviation.
Males / FemalesYear / t / n / τ / ϖ / sd / t / n / τ / ϖ / sd
1992 / 15.O / 56 / 13.O / O.93 / O.OO9 / 1O.8 / 49 / 8.8 / O.9O / O.O1O
1993 / 16.8 / 5O / 14.O / O.93 / O.OO9 / 12.O / 44 / 9.2 / O.9O / O.O1O
Total / 15.9 / 1O6 / 13.5 / O.93 / O.OO6 / 11.4 / 93 / 9.O / O.9O / O.O1O
DISCUSSION
Stopoverlengthandmigrationstrategy
Comparingthestopoverlengthsreportedindifferentstudiesisdifficultbecauseauthorsusuallyusedifferentmethodstoestimatemeanstopoverlength.Accountingforthisshort-coming,thestopoverlengthspresentedinthisstudy were similar to the approximately 14daysreportedatastagingareaontheGermanWaddenseainautumn1992,22andfallwithintherangeof7—21daysforindividualsrefuellingonaBritishestuary.23 SimilarstopoverlengthswerealsoreportedfortheSemipalmatedSandpiperCalidrispusillainNorthAmerica.24,25Bothspecieswereconsid-eredtouseajumpingstrategy.24,26 However,alltheseestimateswerehigherthanthestopoverlengths reported for other waders of similarsizethatwereconsideredtouseahoppingstrategy.1O,27,28AllDunlinsCalidrisalpinamigrat-ingthroughOttenbystayedintheareaforlessthanninedays(ameanofO.55—1.44days7)andveryshortstopoverswerealsoreportedfortheWesternSandpiperCalidrismauriandLeastSandpiperCalidrisminutilladuringautumnmigrationalongthewesterncoastofNorthAmerica.27,29
Thedifferencesinflightdistancebetweenspeciesthatjumpandthosethathopsuggestthatjumpershavetodepartwithhigherlevelsofreservesandhavetostaylongerinthestagingareastoreplenishtheirfatreserves.AlthoughtheoreticalflightrangesofjumpersandhoppersreadytodepartinspringdidnotdifferatawinteringareainMauritania,14thecomparisonofstopoverlengthsofseveralspeciesindifferentareassuggeststhatjumperswillstopforlongerperiodsinthestagingareastoreplenishtheirfatreserves.Theapparentdiscrepancybetweenthesetworesultscouldoccurbecausebothjumpingandhoppingstrategiesmightoccurinthesamespeciesandthusamongtheindividualsusingthesamerefuellingarea.
ThispatternhasbeendemonstratedbySkagenandKnopf3O withtheuseofradio-trackingtodescribetheresidencypatternsofSemi-palmatedSandpipersandWhite-rumpedSandpipersCalidrisfuscicollisatastagingareainspring.Theirstudyshowedthatresidencypatternswereintraspecificallyvariableandalthoughsomebirdsdepartedwithlargefat
loadsandinapositiontocarryoutlongunin-terruptedflights,othersleavewithsmallreservesandwereonlycapableofshorthops.TheoccurrenceinonespeciesofbothmigrationstrategiescouldexplainwhydifferencesinflightrangewerenotfoundbyZwartsetal.14andthatreportedestimatesofstopoverlength(avariableprobablymoreinfluencedbybirdsstayinglongerinthearea)weregreaterinjumpersthaninhoppers.
Optimalmodelsofbirdmigrationpredictthatintime-selectedmigrants,leanerbirdswillmakelongerstopoversthanfatterbirds.Wedidnotfindthisrelationshipinourstudynorinother studies of several species of waderswithtime-selectedmigration7,25,29,31,32 butseeMascher.33 AsHolmgrenetal.7 pointedout,theseapparentlyrandomstopoverscouldappearifbirdstendtowaitforsuitableweatherconditionsinordertoresumemigra-tionandifweatherchangesrandomly.Inthissituationtime-selectedmigrantswouldcontin-uetodepositfat,butenergy-selectedmigrantswouldnot.
Sexdifferences instopoverecology
Ourresultsshowthat,inautumn,maleCurlewSandpipersstayedforlongerthanfemalesatthestudiedstopoverarea.Severalfactorscouldhavecausedthesedifferences.MaleCurlewSandpipersmigrateaheadofthefemaleswhichremaininthebreedinggroundstakingcareofthebrood.21,26 Thedensityofpreyavailableforbirdsatastagingareacouldchangeduringautumnmigrationandpreydepletionbyearlymigrantshasbeenreportedinseveralstudies(reviewedinSzèkelyBamberger34).Malesarrivedatourstudyareatendaysbeforefemalesin1993andpreydensityavailableforeachsexcouldhavechangedinthistime.However, in 1992 the breeding success ofarcticwaderswasverylow35andinthisyearprobablyledtomalesarrivingonlyfourdaysbeforefemales.36
Iftemporalvariationinpreyavailabilitywasthecauseofthedifferencesinstopoverecologyreportedinthisstudy,differencesinstopoverlengthofmalesandfemalesshouldappearin
1993butnotin1992(whenbothsexesmigratedapproximatelyatthesametimeandstayedinthestudyareaunderthesamebioticandabioticconditions).This,however,isnotthe
caseandsowerejectthehypothesisthattem-poralvariationinpreyavailabilitymayhaveproducedthedifferencesinstopoverlengthreportedinthisstudy.
Anotherpossiblesourceofbiasinouresti-matesofstopoverlengthcouldberelatedtotheinclusioninthedatasetofbirdsinactivewingmoult.Althoughwehaveexcludedfromouranalysisbirdstrappedinactivewingmoult,itispossiblethatsomebirdsstartedprimarymoultjustafterbeingringed,therebyincreas-ingourestimatesofstopoverlength.SomestudieshavereportedthatmaleCurlewSandpipersstarttomoultbeforefemales,26,37,38althoughothersfailedtofindanydifference.39,4OMoremalesstartingprimarymoultinourstudyareacouldhaveincreasedtheestimatedstopoverlengthofthissex.However,thenumberofbirdsthatstartedwingmoultinthestudyareawassmall(6.2%oftheadultbirdsringedinautumns1992and1993),andalthoughmoremalesstartedtomoultinthestudyareain1993,nodifferenceinthenumberofmalesandfemalesmoultingintheareawasdetectedin1992.17Longerstopoversofmaleswerereportedinbothyears,sowealsorejectthepossibilitythatdifferencesinmoultpatternswerethecauseofthereportedsexdifferencesinstopoverlength(atleastofthosefoundin1992).
Accordingtothemodelsofoptimalmigra-tion,2 avarietyoffactorscouldexplainthesexdifferencesinstopoverlength.Femalescouldstayforashorterperiodinthestudyareaiftheyleavewithlowerlevelsofaccumulatedreserves.Toexaminethisissue,FiguerolaBertolero41 comparedtheoreticalflightrangesofmalesandfemalesstayingattheEbroDelta.Arrivalbodymasswascalculatedastheaveragebodymassofthe1O%ofleanestbirdstrappedinthearea,anddeparturebodymasswascalculatedastheaveragebodymassofthe
1O%ofheaviestbirds.Theseapproximatecalculationssuggestedthatmalesaccumulatedapproximately3O.4gandfemales32.5gofbodyreserves.Ifthesefiguresreflecttherealsituation, the sexes did not differ greatly intheirestimatedflightrange(3171versus3288km)andthedifferenceswerenotconsistentwiththehypothesisthatfemalesleavewithsmallerfatloadsthanmales.
Thetime-selectedmodelofoptimalmigra-tion suggests that birds with higher fat
depositionratesoralowersearch-settlingtime(timebetweenarrivalattheareaandinitiationofefficientfatdeposition)coulddepartearlierfromthestagingareas.2Thesedifferencesinfatdepositionrateandsearchcostscouldappearifonesexdominatestheotherorifsexesuseecologicallydifferentresources.InafieldexperimentatastagingareainScandinavia,Lindströmetal.42 demonstratedthatdominantBluethroatsLusciniasvecicaaccumulatedfatatahigherratethansubdominantones.AlthoughinformationonthedominancestructureofCurlewSandpiperpopulationsisscarce(butseePuttick43),itiscommonamongbirdsthatthe larger sexdominatesthe smallerone.44,45
FemaleCurlewSandpipersarelargerthanmalessoitisfairtoexpectthattheydominatemales.Sexualdimorphisminbilllengthisalsoacuteandcouldallowfemalestocapturepreyburiedmoredeeplyinthemud.AccordingtothesedifferencesPuttick46 foundinawinteringareainSouthAfricathatthedietofthesexesdifferedandthatfemalesdominatedmales,foraged more successfully and needed lesstimeforagingtocovertheirenergeticrequire-ments.43
Alltheseobservationslendsupporttothehypothesisthatthesexdifferencesinstopoverlengthreportedinthisstudycouldbeproducedbydifferencesbetweensexesinthecapacitytoaccumulatefatinthestudyareaand/orbecausefemalescanstarttodepositfatearlierthanmales(i.e.haveashortersearch-settlingtime).Ourstudyareacouldbeespeciallysuitableforfemales,whereasotherareascouldbemorefavourableformales.
IfthedifferenceswefoundinthestopoverecologyofCurlewSandpiperalsooccurintheotherstagingareasusedbythespecies,thiswouldmeanthatthefemaleshadahigheroverallmigrationspeed,becausethissexwillstayatthestopoverareasforlesstimethanmales.Malesleavebreedinggroundsoverthreeweeksbeforefemales21 butarrivedatourstudyareain1993only1Odaysaheadoffemales.36Thisreductionofthedifferencesinthetimingofpassageforeachsexgivessupporttothehypothesisthatsexesdifferintheirmigrationspeed.Obviously,theresultspresentedheredonotdemonstratethatinCurlewSandpiperssexesdifferintheirmigrationefficiency.However,theyareconsis-tent with this hypothesis. We hope that this
papermightstimulatefurtherresearchonsexdifferencesinstopoverecologyandsearch-settlingpatternsinspecieswithsignificantnormalorreversesexualdimorphisminbodysize.
ACKNOWLEDGEMENTS
ThisworkwasfundedbytheEbroDeltaNaturalPark,DiputaciódeTarragonaandGrupCatalàd‘Anellament.TheGeneralitatdeCatalunya(CatalanAutonomousGovernment)provided the permits necessary for carryingoutthefieldwork.L.M.CopeteandL.Gustamantemadeanindispensablecontribu-tiontothefieldwork.WewouldalsoliketothankJ.M.Arcos,L.Brotons,L.Carrera,D.Escobar(FonotecadelMuseodeZoologiadeBarcelona),M.A.Franch,D.Froelich,S.Galan,R.Marine,R.Marti,A.Martinez,R.Mateo,A.Motis,D.Oró,X.Riera,A.Salmerón,J.Solans,F.VicentsandR.Vidalfortheirhelpandfriend-ship.M.LockwoodimprovedtheEnglishandJ.A.Amat,B.J.Ens,J.D.Goss-Custard,A.Lindström,T.Piersma,J.C.SenarandD.A.Stroudmadevaluablecommentsonearlierdraftsofthismanuscript.
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