Felineleukaemiavirusoutbreakinthe endangeredIberian lynxandthe roleoffeedingstations:acautionarytale

F.Palomares,J.V.Lo´pez-BaoA.Rodr´ıguez

DepartmentofConservationBiology,Estacio´nBiolo´gicadeDon˜ana(CSIC),Sevilla,Spain

Correspondence

FranciscoPalomares, Departmentof ConservationBiology,Estacio´nBiolo´gicadeDon˜ana (CSIC),Ame´ricoVespucio s/n,IsladelaCartuja,41092

Sevilla,Spain.

Email:

doi:10.1111/j.1469-1795.2010.00403.x

Lopezetal.(2009)reported afelineleukaemiavirus(FeLV) outbreakintheIberian lynxLynxpardinus,andspeculated on the potential negative role of feeding stations (FS) installedforthesupplementaryfeedingoftheDonanalynx populationwith domestic rabbits. Supplementary feeding hasproven tobeusefulinretaining Iberian lynxinareas with extremefoodscarcitywhereotherwisetheywouldbe absent(Lopez-Bao,Rodrıguez & Palomares, 2008,2009; Lopez-Bao etal., 2010).Therefore, misunderstandingthe roleofFSinthetransmissionoftheFeLV might leadto managementrecommendationsregarding the use of FS, withimportantconservation repercussions. Lopezetal. (2009)assumedthat allinfectedlynxbelongedtothesame lynxsubpopulation[CotodelRey(CR)]withintheDonana metapopulation.Thisassumptionwasincorrect andledto faultyinferencesabouttheroleofFSinFeLVtransmission. Here,wediscussthesupposed pro-active roleofFSinthe propagationoftheFeLV outbreak,and therationalityof themeasuresadopted tocontrol thedisease,wecallatten- tiontothelynx subpopulationsthatwereinvolved,andhow theiridentification challengesinferencesaboutthespreadof FeLVandwe propose aplausibleecologicalscenariofor understandingtheoutbreak.

TheFeLVoutbreaklikelybeganwiththeinfectionofan adultmalecalledRoman inhabiting theCRsubpopulation (Fig.1). ThismalewastheonlyFeLV-positiveindividual detected out of18trapped lynxin November–December

2006[10inCR,fiveinVeraandthreeinDehesa deGato- Arrayan (DGA)].Alllynxknowntobeinhabiting CRand Verasubpopulations,andthreeofseveninDGA subpopu- lation weretrapped during that trapping campaign. Cap- turedlynx weretransferredfromthetraptoatransportcage wheretheywereanaesthetized fortagging, ahealth check andcollectionofbiologicalsamplesatthesamelaboratory, whichincluded ultrasonographicalanalysis (Goritz etal.,

2009),andelectroejaculationofadult males(Ganan etal.,

2010).Theindividual that washandled 2.5hafter Roman wasanadultmalecalled UdafromtheDGAsubpopulation.

Between13March and 8May 2007four lynxwerefound dead(Roman,Uda, andtwoother adult malesfromCR). AllofthemwereFeLVviraemic.InApril2007,thecontrol programmereported byLopezetal.(2009)began.Between

9May and 1August 2007,an additionaleightindividuals were found to be FeLV positive, seven of which were captured inCRandoneinDGA(Fig.1).

IfFShadarelevantroleinthetransmission offeline leukaemia,individualssharingFSwith Romanwouldbe expectedtohaveahigherprobabilityofinfectionthanother individuals.However,noneoftheother11lynxpositivefor FeLV shared FSwithRoman, and allthreelynxthat did share FS werefound to beFeLV negative (Fig. 1).The Iberianlynxexhibitsaterritorialspatialorganization,where oneadultmale,oneadultfemaleandtheiroffspringo1–2 years old exhibit a high overlap in their home ranges, whereas little overlap existsbetween the home ranges of adultsofthesamesex(Ferreraset al.,1997;Palomaresetal.,

2001).Somemalesmaysharetheirhomerangeswithmore thanoneadultfemale.FSwereprimarilyplacedinthecore oflynxterritories, inthiswayminimizingpotential aggres- siveinteractions betweenneighbouring lynx.Lynxvisitsto FSweremonitored byautomaticphotographiccamerasto identifytheindividuals that usedthesupplementaryfood, and to record the frequency with which each individual visitedFS.Usingindependent methods, itwasknown that alllynxlivinginterritories containing FSwereinthisway detectedinsidefeedingenclosures;therefore,theprobability ofanundetected individualusingafeedingstation waslow (Lopez-Bao etal.2009).Out of709photographicrecords from15 differentlynxthatusednineFSinsiteswhere neighbouring territorieswere occupied,lynxenteredaFS placedin aneighbouringterritoryonlyonthreeoccasions (0.4%). Twooftheserecords correspondedtovisitsatthe verybeginningofFSoperation,beforeanyterritory holder usedtheenclosure. Onceterritory ownersentered theFS, this intruder did not visit it again. Outside of Roman’s territory, fourlynxthatsharedFSwithinfectedindividuals

Figure1DistributionofIberianlynxLynxpardinustestedagainstFeLVbyLo´pezetal.(2009)during2006and2007.Circlesrepresentknownmale or femaleterritories(whenmalesterritorieswerenotclearlyidentified),andaclusterofcontactingcirclesrepresentsonesubpopulationwithin theDon˜ana metapopulation.During2006and2007,supplementaryfeedingstationswereplacedinterritoriesrepresentedbyboldcircles. NumbersdenoteterritorieswhereatleastonelynxwascaughtbyLo´pezetal.(2009),andcircleswithoutnumbersrepresentterritoriesinhabited bylynxwherenoindividualwascaught.M,Z2-year-oldmale;F,Z2-year-oldfemale;m,about15-month-oldmales;f,about15-month-old

females; fc,femalecub;mc,malecub;*lynx wereFeLVpositive;#anindividualthatarrivedtoRoma´n’sterritoryafterhisdeath.Individualsthat

werecheckedforFeLV infectionduringNovemberandDecember2006areunderlined.

werefound tobeFeLV negative. Ontheother hand, two cubsthatneverusedFSwere infected.Thesedata,in combination,lendlittlesupport tothehypothesis that FS hadadeterministicroleinthetransmissionofFeLVbefore orduringtheoutbreak.

TheIberianlynxoftenkillssmallercarnivores(Palomares

Caro,1999).BecauseFeLVneedsdirectcontact between individuals to be transmitted (Barr Bowman, 2006), Roman could have acquired the virus while killing an infecteddomesticcat(Melietal.,2009).Apossiblewayfor FeLVpropagation through thelynxpopulation couldbe fightsbetweenadultmales duringthematingseason(Ja- nuary–February;Palomaresetal.,2005).Duringthisseason adultmales exploreneighbouringterritoriessearchingfor females, which may result in aggressive encounters with othermales(Ferreras etal.,1997; Lopez-Bao,Rodrıguez & Ales,2008).Woundsexposedtothesalivaofinfectedrivals maybeamechanism ofFeLV transmission.Ifthisisthe case,onemightexpectthat theprobabilityofinfectionfor adult males in the neighbourhoodof Roman’s territory would be higher than that for non-neighbouring males. Indeed, allneighbouring adult males ofRoman werein- fectedwiththedisease,whereastwooutoffive non- neighbouring adultmalesbelongingtoadifferentsubpopu- lation (DGA) werealsoinfected (Fig.1).How didFeLV reachthetwoadultmaleslivinginDGA?Wecannotdiscard the hypothesis that some undetected, infected dispersing

lynx from CR might have transmittedthe virus to DGA males,although thiswasnotsupportedbyintensivemonitor- ingofCRlynx.Also,wecannot discardthatanymalefrom DGAcouldget thevirusafterkilling another domesticcat, although sequencing ofthe envelope surface unit genere- vealedacommon origin for the FeLV found inalllynxes (Melietal.,2010). However,themostparsimoniousexplana- tionmightbethatthemaleUda,handledsoonafterRoman, wasinfectedwithFeLVthrough improper disinfectionofthe equipment usedforlynximmobilizationandhealthchecking, whiletheotherpositivemaleinDGA receivedtheviruslater on through mating fights with Uda. Adult females could receive the virus while mating with infected males, and juvenilescouldbeinfectedthrough sucklingandlickingfrom theirinfectedmothers.Thehypothesisthatsomevirustrans- missioncouldhavetakenplaceduringtheintensivetrapping campaign ofautumn 2006,whennineoutof12positivelynx detected byLopezetal.(2009)werecaptured andhandled, cannotbediscarded.

Finally, Lopezetal.(2009)suggestedthat ameasure to control thespread ofthediseasewouldbetoprovide just onerabbit atatimeinFS,inorder toavoiddifferentlynx feedingonthesameprey.Noevidenceexistsinsupport of thisproposal. Lynxforagealone,andarabbit represents a

‘ration prey’(Delibes, 1980;Aldama, Beltran Delibes,

1991).ThisisalsothecaseinFS,inwhichonly9%of2238 picturesthereweremorethanonelynx recordedwithinaFS

(oftenadultfemaleswiththeiroffspring),andwe never witnessed two lynx sharing a prey (41540h of video recordinginFSexamined).Therefore,we inferthatthe probabilitythat twoormorelynxsharearabbit, inFSor elsewhere,isverysmall(seealsoAldama Delibes,1991), ofcourseexcludingrabbitsbroughttothecubsby their mothers,abehaviour thattakesplacewithrabbitscaughtin FSorelsewhere.

Despitethelackof clearevidencerelatingtheuseof FSwith thetransmission ofFeLVduringtheoutbreak,afurtherissue shouldbeconsidered. Domesticrabbits consumed bylynxin FSmay have indirectlyaffectedtheirresistancetoFeLVand subsequent secondary infections withother pathogens (Meli etal.,2009).The domestic rabbits wesupplied inFS were treatedwithantibioticstopreventgeneralizedinfections,which mayhaveentailedsomehealthrisksforlynx.LemusBlanco (2009)foundthatvultureswithcirculatingantibiotics showed depressed cellular and humoral immune systems compared withindividualswithoutcirculatingantibiotics,whichsuggests that ingestionofantibiotics maydepresstheimmunesystem, temporarily reducing theirresistancetoopportunisticpatho- gens. Therefore,exposuretoantibioticsmayhavehadarolein thefatalFeLVoutbreakamongDonanalynxandshouldbe furtherinvestigated.The impoverishedimmunologicaland geneticcondition oftheDonana lynx,resultingfromhigh inbreeding and lowMHC geneticdiversity (Johnson etal.,

2004;Jimenezetal.,2008;S.Roques,pers.comm.),mightalso explainapotentially highvulnerabilitytodiseases,eveninthe absenceofexposuretoantibiotics.

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