Nutritionalconditionandserumbiochemistryforfree-living

Swainson’sHawkswinteringincentralArgentina

Jose´Herna´nSarasolaa,*,JuanJose´Negroa,AlejandroTravainib

aDepartmentofAppliedBiology,Estacio´nBiolo´gicadeDon˜ana,Avda.deMar´ıaLuisasyn,Pabello´ndelPeru´,41013Sevilla,Spain

bCentrodeInvestigacionesdePuertoDeseado(UNPA-CONICET),CC238,9050PuertoDeseadoSantaCruz,Argentina

Abstract

Weassessedthenutritionalconditionandestablishedreferencevaluesforserumchemistryparametersinalong distancemigrantbirdofprey,theSwainson’sHawk(Buteoswainsoni),winteringincentralArgentina.Weanalyzed serumconcentrationofurea,uricacid,cholesterol,andtriglyceridesandassessedageandsexrelateddifferencesin theseparameters.Abodyconditionindexwasobtainedfromtheresultantresidualsoftheregressionofbodymassand amorphometric measure.Nostatisticaldifferences wereobservedamongsexandagegroupsforurea,uricacidand triglycerideserumconcentration.However,cholesterolconcentrationdifferedamongmaleandfemalehawks,which couldberelatedtothegainofbodymassinwinteringgroundsatdifferentialrates.Themeanvaluesofthefour parameterswereintherangeofthoserecordedintheCommonBuzzard(Buteo buteo), indicatinggoodnutritional conditionofthepopulationwestudied.Forearmlengthwasthemorphometric variablethatbettercorrelated withbody mass.Theresultantbodyconditionindexwasonlycorrelatedwithtriglycerideconcentration, suggestingthatthisindex couldbevaluableinfutureworkdealingwiththeassessmentofbodyfatstorageinwinteringandbreedinghawks,as wellasinstopoverpointsonthemigratoryroute.

Keywords: Buteoswainsoni;Cholesterol;Migration;Nutritionalcondition;Serumchemistry;Swainson’sHawk;Triglyceride;Uric acid;Urea;Winteringgrounds

1.Introduction

Referencevaluesforbiochemicalparameters of free-rangingpopulationsarenotonlyimportantfor veterinarians dealingwithcaptiveandrehabilitat- inganimals,butalsoforstudying animals intheir naturalhabitats.Fewstudieshaveattempted to establishreferencevaluesofbiochemical parame- tersforbirdsofprey(Ferrer,1994;Balbont´ın and Ferrer,2002;Casadoetal.,2002)andmostrefer tocaptiveindividualsundercontrolledconditions

*Correspondingauthor.Tel.:q34-954-232340; fax:q34-

954-261125.

E-mailaddress:(J.H.Sarasola).

andnon-naturaldiets (Balaschet al.,1976;Garc´ıa- Rodriguez etal.,1987a,b;Ferreretal.,1987;Polo etal.,1992;Dobado-Berriosetal.,1998).

Swainson’sHawk(Buteoswainsoni)isaneo-

tropicalbirdofpreythatbreeds intheUSAand Canadaandmigrates tosouthernSouthAmerica duringtheborealwinterinatripofapproximately

10000kmeachway(secondindistanceamong raptors,Fulleretal.,1998).Thespecies hasbeen moreextensivelystudiedinNorthAmericathan initssouthernwintering ranges,butthereareno studiesofbiochemicalparametersassociated with bloodin the wild or in captivity.Moreover,no biochemicalparametershavebeenpublishedfor

free-living individuals ofthegenusButeo.The Swainson’s hawkmakesaninteresting modelfor bloodchemistry studiesinraptors. Whileonits breeding grounds, itpreys mainly onsmall mam- mals,whereasitbecameaninsect-eater onits winteringgroundsinArgentina (Jaramillo,1993; Englandetal.,1997). Inaddition,twocomple- mentaryhypotheses aboutnutritional andfeeding strategiesonmigrationhavebeenasserted and largelydebatedforthisspecies. Thefasting hypothesisproposesthatSwainson’sHawksdonot feedduringthemigratorytriptowintering areas andback,usingonlythefatstored during thepre- migrationinterval(Smith etal.,1986), whereas thealternative fathypothesis suggeststhatSwain- son’s Hawksfeed enrouteduringmigration(Kirk- ley,1991).Neitherofthesehypotheses havebeen adequately tested.Thefastingtheoryissupported onlybytheabsenceofregurgitation pelletsand feces under trees of communalroost sites used duringstopoverpointsinCentralAmerica.Studies dealingwiththeassessment ofbodyconditionof hawkscapturedduringstopover inPanama to evaluatetheirnutritionalstatushavebeenlimited todescriptiveandvisualevaluations ofsubcuta- neousfataccumulation (Smithetal.,1986). Although hawks have been reportedarrivingto winteringareainsuchweakcondition thatthey werepickedupbyhand(C.C. OlroginSmith,

1980),nonutritional studieshavebeenconducted forpopulationsofwinteringhawks.

The aim of this work is to report reference valuesofselectedserumbiochemical parameters thatmayservetoevaluatenutritionalcondition of winteringSwainson’sHawksinthewintering sea- son.Theinfluence ofotherfactorsonthesebio- chemicalparameters, suchassexandage,arealso analyzed.Wealsocorrelateserumconcentration ofthebiochemical parameters againstabody condition indexderivedfrombodymassandmor- phometricmeasures.

2.Materialandmethods

Hawks werecaptured inthevicinityofaroost siteinaEucalyptus spp.treegrovenearLas Varillas,Co´rdobaprovince(318589S,628509W), from19to26January 2003(australsummer).We estimated that approximately 600–700 hawks roostedinthissiteduringthetrapping period. Trappingwasconductedinagricultural fieldscon- sistingofcontinuouscroplands,withsoybeansas

theprincipalcrop.Implanted pastures andnatural fieldsoccupiedthe remainingof the open field surfacededicatedtolivestockand milkproduction. Hawkswerecaptured inopenfieldsneartheroost usingbal-chatritraps(BergerandMueller,1959) inearlymorningandduringtheafternoon. Traps weresetinfrontoffencepostsusually usedby hawksforperching, bothwhentheylefttheroosts in the morningand during late afternoonwhen theyreturnedtoroost.Captured hawkswereclas- sifiedasjuveniles oradultsbasedonplumage characteristics,with2-year-oldbirdsgroupedalong withjuveniles(WheelerandClark, 1995).Hawks werebandedandweighed witha1500gPesola scaletothenearesttwograms. Sixmorphometric measurements weretakenfromadultsandjuve- niles.Wemeasured thelengthofwingchordand tailusingaplastic ruletothenearest 1mm,and lengthoftheexposedculmen, tarsusandhallux clawusingcallipers tothenearest0.05mm.We alsomeasured theforearm length,orthelength from thefront ofthefolded wrist totheproximal extremityoftheulna(seeFerrerandDeleCourt,

1992forfurtherdetails)alsousingacalliper.For afewbirds onlysomeofthebodymeasurements wererecorded.

Approximately 2mlofbloodweretakenfrom eachbirdfromthebrachial vein.Thebloodwas placedintubesandkeptinacooler until analysis. Biochemical analyseswereperformed onadigital spectrophotometer within24hafterbloodextrac- tion.Serumconcentration ofurea,uricacid,cho- lesterolandtriglycerides wasmeasuredusing enzymaticmethods(acommercialkit fromWiener Lab,Argentina).Thecellular fraction oftheblood sample wasusedtosexallhawks. Forthisanaly- sis,weusedprimers 2550Fand2718Rtoamplify the W chromosome gene following Ellegren (1996). Thesampleincluded24males(12juve- nilesand12adults)and10females(5juveniles and5adults).

Weusedatwo-wayANOVA (Zar,1996)to comparemeanvaluesofurea,uricacid,cholesterol andtriglycerides amongsexandagegroups,with male–femaleandjuvenile–adultbeingthelevels of the factors. Due to the lack of normality (Shapiro–Wilktest:Ws0.7, P-0.01), ureacon- centrationwaslog-transformedpriortoanalysis. Toassesstheeffectofcircadianrhythms,weused t-tests(Zar,1996)tocompareserumconcentration of metabolitesin birdscapturedinthemorning amongthosecapturedduringtheafternoon.

Anindexofbodyconditionwasobtainedfor thehawkscaptured.BecauseSwainson’sHawks aresexuallysizedimorphic (Englandetal.,1997) andoursampleincludedadultandjuvenilebirds,

Table2

Correlation coefficients betweenbodymassandeachofsix morphometricvariablesmeasuredinSwainson’sHawks(Buteo swainsoni)capturedinArgentina during2002–2003wintering season

the body condition index was obtained by calcu-

latingmassresidualsforallbirdsaccording tothe relationship betweenbodymassandameasureof structuralsize,correcting thusthebodymassfor bodysizedifferences relatedtosexandage.For thatprocedure wecorrelated thenatural logarithm of bird body mass against natural logarithmof eachofthemorphometric variablesmeasuredin hawksbyusingthePearson’scorrelation coeffi- cient.Theresidualsofthegeometric meanregres- sion(SokalandRohlf,1995;seealsoGreen,2001) amongbodymassandthebetter-correlated mor- phometricvariableagainstbodymasswereconsid- eredasabodycondition indexofthebirds. Relationship amongbodyconditionindexand biochemical variableswereanalyzedbythePear- son’scorrelationcoefficient.

3.Results

Thirty-four hawks were captured during the studyperiod. Thetotalsampleincluded 24males and10females ofwhich17wereadultsand17 juveniles.Twenty-sevenhawkswerecapturedin themorning between 06:30and10:00handthe remaining sevenweretrappedintheafternoon between14:00and20:00h.Descriptiveparameters bysexandage,andvaluesforthepooled sample, areshowninTable1.Serumconcentration of metabolites wassimilarforbirdscapturedinthe morningtothosecapturedintheafternoon (t-test forindependentsamples:ureaPs0.77; uricacid

r2NSignificance

Forearmlength / 0.78 / 33 / P-0.01
Wingchord / 0.75 / 33 / P-0.01
Tail / 0.61 / 33 / P-0.01
Culmen / 0.54 / 31 / P-0.01
Halluxclaw / 0.53 / 33 / P-0.01
Tarsuslength / 0.45 / 33 / P-0.01

Ps0.31;triglyceridePs0.91;andcholesterolPs

0.54).Nosignificantdifferences werefound between sexandagegroupsforurea(Fsexs0.27, P)0.60andFages0.50,P)0.82),uric acid (Fsexs0.40, P)0.52 and Fages0.57, P)0.45), andtriglyceridelevels(Fsexs0.52, P)0.47and Fages2.55,P)0.12).Cholesterol concentration wasalsosimilar foradultandjuvenile hawks (Fages0.57,P)0.44),butsignificant differences werefoundbetween meanvaluesofmalesvs. females (Fsexs8.41,P-0.01).Theinteraction betweenageandsexwasnotsignificantforany oftheparameters analyzed(P)0.45inallcases). The variablewiththehighestcorrelationwithbody masswasforearm length(Table2).Thebody conditionindexresultingfromtheresiduals ofthis regressionwaspositivelycorrelated withtriglyc- erides concentration(rs0.38, P-0.05; Fig. 1), butitdidnotcorrelate withuricacid(rs0.15, Ps0.39),urea(rs0.05,Ps0.76),andcholesterol levels(rsy0.16,Ps0.35).

Table1

Concentrationoffourserumparametersandbodymass(g) intheSwainson’sHawk(Buteoswainsoni)whilewinteringincentral

Argentina.Biochemicalparametervaluesareinmilligramperliterandaregivenasmean"S.D.withrangeinthefollowingrow

Males
Ns24 / Females
Ns10 / Juveniles
Ns17 / Adults
Ns17 / Totalsample
Ns34
Urea / 156.6"67.9 / 173.0"173.6 / 175.8"136.8 / 147.0"67.3 / 161.4"107.2
(50.0–290.0) / (40.0–630.0) / (40.0–630.0) / (50.0–280.0) / (40.0–630.0)
Uricacid / 59.0"20.9 / 64.7"27.4 / 64.4"20.3 / 57.0"25.0 / 60.7"22.7
(30.0–94.4) / (21.0–106.0) / (33.0–106.0) / (21.0–97.0) / (21.0–106.0)
Cholesterol / 2999.6"790.8 / 2167.0"628.2 / 2821.2"812.6 / 2688.2"870.1 / 2754.7"831.7
(1640–4780) / (1330–3200) / (1610"4700) / (1330–4780) / (1330–4780)
Triglycerides / 1493.3"478.6 / 1366.0"476.8 / 1303.5"422.9 / 1608.2"485.9 / 1455.8"474.5
(790–2580) / (580–2050) / (790–2580) / (580–2480) / (580–2580)
Bodymass / 960.0"98.0 / 750.0"57.7 / 860.3"126.24 / 764.1"95.08 / 813.6"120.79
(845–1110) / (610–860) / (740–1110) / (610–940) / (610–1110)

Fig.1.Relationshipbetweenserumtriglyceride concentration and the residuals of GM regression betweenbody massyforearmlength(body conditionindex) forSwainson’s Hawks(Buteoswainsoni)winteringinArgentina.

4.Discussion

Weprovideforthefirsttimereferencevalues forfourserumbiochemicalparametersindicative of nutritional condition (Alonso-Alvarez et al.

2002a,b) forfree-livingSwainson’sHawkswin- teringinSouthernSouthAmerica.Wealso consid- eredfactors suchassexandagethatcaninfluence rangeandmeanvaluesoftherespectiveparameters (FerrerandDobado-Berrios,1998).

Highlevelsofureaanduricacidinseveral bird speciesinfooddeprivationexperiments havebeen related to the catabolismof tissue proteinsdue starvation (OkumuraandTasaki,1969;Garc´ıa- Rodriguezetal.,1987b). However,meanvalues ofSwainson’s Hawksforureaanduricacidlevels wereintherangeofthelowervaluesobtained by Garc´ıa-Rodriguezetal.(1987b) intheCommon Buzzard(Buteobuteo),indicating nomobilization ofproteinreservesandgivingevidence ofgood conditionintermsofproteinmetabolism forthe winteringSwainson’s Hawks.Serumtriglycerides tendtorelatetobodyfatcontent(Bacon etal.,

1989;Dabbert etal.,1997).Thus,thepositive correlation we observed between this parameter andthebodycondition indexobtainedfromthe relationship between body massyforearmlength suggests thatthisindexmaybeusedasameasure offat storagein Swainson’sHawksinfutureworks dealingwithfatcontents ofthesebirdsduring migration.

CholesterolconcentrationinYellow-legged

Gulls (Larus cachinnans) has been related to

changes in body mass (Alonso-Alvarez et al.,

2002a).Goldsteinetal.(1999) observedSwain- son’sHawksgainingbodymassthrough thewin- teringseason.Thedifferencesthatweobserved in serumcholesterolconcentration amongadultmale andfemalehawks couldberelatedtodifferential ratesingainofbodymassinmale andfemale hawks.Inbirds,cholesterolandtriglyceride con- centrations arealsoaffectedbythequalitative composition of diet (Yeh and Leveille, 1972; FerrerandDobado-Berrios, 1998).Inthecaseof Swainson’s Hawks,itisunlikelythatthedietary shifttheyundergobetweenbreeding andwintering areascouldbea factorinfluencingtheabsolute referencevaluesofthesetwoparameters, due similarities infatcontentofinsectsandsmall mammals.Forexample,Birdetal.(1982) found meanvalues ofcrudefat(measuredas percentage oftotaldrymatter)of6.03% forthered-legged grasshopper (Melanoplus femurrubrum) and

6.01%forthemeadowvole(Microtuspennsylvan- icus),whichrepresentthetwomainpreyitems of Swainson’s Hawksinwinteringandbreeding grounds,respectively(Englandetal.,1997).

The absence of significantdifferencesamong groupsofSwainson’sHawksmayberelatedto thelackofspatialandtemporalvariations inour sampling.Onthepositiveside,datacollectionin ashortandwell-delimited timeperiodreduces temporalbiasesinnutrientstorage, whichassure ourdatareflectthenutritional conditionforthe entirepopulationstudied.

Alonso-Alvarezetal.(2002b)foundthatbreed- ing producedchangesin bodymassof Yellow- legged Gulls (Larus cachinnans) and also in plasmacomposition duringincubation. Itcouldbe expectedthatSwainson’sHawkbiochemical val- uesinNorthAmericanrangescanbeaffected by sexandageduetodifferentialenergydemands andrequirement ofbirdsaccording tovarying demands duringdifferent stagesofthebreeding cycleandalsodependingonindividual levelsof parentinvestment. Thehawksthatwestudied constituted, onthecontrary,aratherhomogeneous groupintermsofbehavior andenvironmental demands, and,thereforeourresultscouldbecon- sideredasaccurate normal values ofbiochemical parametersforthespecies.

Acknowledgments

WewishtothankStellaMarisBacileandHugo

Bergonzi for conducting lab analysis and Noah

WithemanandRamo´nA.Sosaforhelp intrapping andhandlinghawksduringfieldwork. Wealso thankpersonnelfromEa.LaIndependenciaand theAgenciaCo´rdobaAmbienteofCo´rdobaprov- inceforgivingpermissiontocarryouttrapping in thestudyareas.WethankA.Lanusse andS.Salva fortheirhospitality andlogisticsupportduring fieldwork.J.H.Sarasolahadafellowship fromthe ConsejoNacionaldeInvestigaciones Cient´ıficas y Te´cnicas (CONICET) of Argentina. This study wassupportedbytheWildlifeConservation Soci- ety(USA)andtheUniversity ofLaPampa (Argentina).

References

Alonso-Alvarez, C.,Ferrer,M.,Velando,A.,2002a.The plasmaticindexofbodyconditioninYellow-legged Gulls Laruscachinnans:afood-controlledexperiment.Ibis144,

147–149.

Alonso-Alvarez,C., Velando,A., Ferrer,M., Veira,J.A.R.,

2002b. Changes in plasma biochemistry and body mass duringincubationintheYellow-leggedGull.Waterbirds25,

253–258.

Bacon,W.L.,Nestor,K.E.,Naber,E.C.,1989.Prediction of carcasscompositionofturkeysbybloodlipids.Poult.Sci.

68,1282–1288.

Balasch,J., Musquera,S., Palacios,L., Jimenez,M.,Palo- meque,J.,1976.Comparative hematologyofsomefalconi- forms.Condor78,258–273.

Balbont´ın,J., Ferrer,M.,2002.Plasmachemistryreference valuesinfree-living Bonelli’s Eagle(Hieraaetusfasciatus) nestlings.J.RaptorRes.36,231–235.

Berger,D.D.,Mueller,H.C.,1959.Thebal-chatri:atrapfor thebirdsofprey.Bird-Banding30,18–26.

Bird,D.M.,Shio-Kuen,H.,Pare´,D.,1982.Nutritivevaluesof threecommonpreyitemsoftheAmericanKestrel. Comp. Biochem.Physiol.A73,513–515.

Casado,E.,Balbont´ın,J.,Ferrer,M.,2002.Plasmachemistry inbootedeagle(Hieraaetusfasciatus)during breeding season.Comp.Biochem.Physiol.A131,233–241.

Dabbert, C.B.,Martin,T.E.,Powell, K.C.,1997.Useofbody measurements andserummetabolitestoestimatethenutri- tionalstatusofMallardswinteringintheMississippi Allu- vialValley,USA.J.Wildl.Dis.33,57–63.

Dobado-Berrios,P.M.,Tella,J.L.,Ceballos,O.,Donazar,J.A.,

1998. Effects of age and captivity on plasma chemistry valuesoftheEgyptianVulture.Condor100,719–725.

Ellegren, H.,1996.FirstgeneontheavianWchromosome (CHD) providesa tag for universalsexing of non-ratite birds.Proc.R.Soc.Lond.B.263,1635–1641.

England,A.S.,Bechard,M.J.,Houston,C.S.,1997.Swainson’s Hawk (Buteoswainsoni).in:Poole, A.,Gill,F., (Eds.),The BirdsofNorthAmerica,No.265.TheAcademyofNatural

Sciences, Philadelphia, and The American Ornithologists

Union,Washington,D.C.

Ferrer,M., 1994.Nutritionalconditionof SpanishImperial EaglenestlingsAquilaadalberti.BirdStudy41,120–123. Ferrer,M.,DeleCourt,C.,1992.Sexidentificationinthe

SpanishImperialEagle.J.FieldOrnithol.62,359–364.

Ferrer,M.,Dobado-Berrios,P.,1998.Factorsaffecting plasma chemistryvaluesoftheSpanishImperialEagle, Aquila adalberti.Comp.Biochem.Physiol.A120,209–217.

Ferrer,M.,Garc´ıa-Rodr´ıguez,T.,Carrillo,J.C.,Castroviejo,J.,

1987. Hematocritand blood chemistry values in captive raptors(Gypsfulvus,Buteobuteo,Milvusmigrans, Aquila heliaca).Comp.Biochem.Physiol.A87,1123–1127.

Fuller,M.R.,Seegar,W.S.,Schueck, L.S.,1998.Routes and travelratesofmigratingPeregrine Falcons Falcoperegrinus andSwainson’s HawksButeoswainsoniintheWestern Hemisphere.J.AvianBiol.29,433–440.

Garc´ıa-Rodriguez,T.,Ferrer,M.,Carrillo,J.C.,Castroviejo,J.,

1987a. Metabolicresponsesof Buteo buteo to long-term fasting and refeeding. Comp. Biochem. Physiol. A 87,

381–386.

Garc´ıa-Rodriguez,T., Ferrer, M., Recio, F., Castroviejo,J.,

1987b.Circadianrhythmsofdetermined bloodchemistry valuesinBuzzardsandEagleowls.Comp.Biochem. Phy- siol.A88,663–669.

Goldstein, M.I., Bloom, P.H., Sarasola, J.H., Lacher, T.E.,

1999.Post-migrationweightgainofSwainson’shawksin

Argentina.WilsonBull.111,428–432.

Green,A.J.,2001.Massylength residuals:measuresofbody condition or generators of spurious results? Ecology 82,

1473–1483.

Jaramillo,A.P.,1993.WinteringSwainson’s HawksinArgen- tina:foodandagesegregation.Condor95,475–479.

Kirkley,J.S., 1991. Do migrantSwainson’sHawksfasten routetoArgentina?J.RaptorRes.25,82–86.

Okumura,J.,Tasaki,I.,1969.Effectoffasting,refeeding and dietaryproteinlevelonuricacidandammonia content of bloodliverandkidneyinchickens.J.Nutr.97,316–320.

Polo,F.J.,Celdra´n,J.F.,Peinado,V.I.,Viscor,G.,Palomeque, J.,1992.Hematological valuesforfourspeciesofbirdsof prey.Condor94,1007–1013.

Smith,N.G.,1980.Hawkandvulturemigration ontheNeo- tropics.In:Keast,A.,Morton,E.S.(Eds.), MigrantBirds ontheNeotropics:Ecology,Behavior,Distribution and Conservation. SmithsonianInstitutionPress,Washington, DC,pp.51–65.

Smith,N.G., Goldstein,D.L.,Bartholomew,G.A.,1986.Is long-distancemigrationpossibleusingonlystoredfat?Auk

103,607–611.

Sokal,R.R.,Rohlf,F.J.,1995.Biometry. Thirded.W.H. Freeman,NewYork.

Wheeler,B.K.,Clark,W.S.,1995.APhotographicGuideto NorthAmericanRaptors.AcademicPress,SanDiego,CA. Yeh, J.C., Leveille, G.A., 1972. Cholesteroland fatty acid synthesisinchicksfeddifferentlevelsofprotein.J.Nutr.

102,349–358.

Zar, J.H.,1996.BiostatisticalAnalysis.Thirded.PrenticeHall, Princeton,NJ.