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DietaryresponseoftheEurasian badger,Melesmeles,toadeclineofits main preyintheDonanaNationalPark
J.M.Fedriani*,P.FerrerasandM.Delibes
Estacio’nBiolo’gicadeDonana,CSIC,Apto.1056,41080Sevilla,Spain
INTRODUCTION
TheEurasianbadger(Melesmeles)isconsideredtobea harvesterratherthanahunter(Kruuk,1989),becauseits foodusuallyconsistsofvegetablesandsmallandeasily capturedanimals,suchas worms andinsects,andit rarely capturesmammals(Neal,1986).However,inthe DonanaNational ParkofMediterranean Spainthe badgerapparentlybehaves asafacultative specialistin theconsumptionofyoungrabbits,Oryctolaguscuniculus (Martin,RodriguezDelibes,1995).In1990,anout- breakofRabbitHaemorrhagicDisease(RHD) caused high mortality amongadult rabbits in mostof the Donanaarea(Villafuerteetal.,1994),althoughallsites ofDonanawerenotaffectedtothesameextent.This situationofferedthepossibilityofcomparingthefood habitsof badgersin theDonanaBiologicalReserve (DBR)before(dataofMartinetal.,1995)andafterthe outbreakofRHD,whileusinganothersitewhererabbit densityhaschanged little overthelastfewyears asa controlarea.
*Allcorrespondenceto: DrJ.M.Fedriani,Estacio’nBiolo’gicade
Donana,CSIC,Apto.1056,41080Sevilla,Spain:
email:
Thestudyisrelated tothediscussionaboutwhetheror notEurasianbadgersforageasfoodspecialists(KruukParish,1981;Roper,1994).Theterms‘specialist’and
‘generalist’canbemisleading, astheyarerelativeterms andaffectdifferentdecisions (e.g.beforeor afterto encountera potential prey). We suggestthat the Eurasianbadgercould be considereda specialized foragerwhereandwhenitfocusesitsforagingonone kindoffood,whichwouldbepreferredovertherest.The theoryoffeedingspecializationrequirestheselectedprey tobeprofitableandabundantandpredictsan increaseof
dietarydiversitywhentheselectedpreybecomesscarce (FutuymaMoreno,1988).Hence,wetestthehypoth- esisthatthedietarydiversityofbadgersinDonanais dependentontherelativebiomassofrabbitsinthediet, regardlessoftheremainingconsumedfoods.
STUDYAREA
ThestudywascarriedoutintheDonanaNationalPark (37°10’N,6°23’W).TheParkissituatedonthewest bankofthemouthoftheGuadalquivirRiver(south- westernSpain).TheclimateinDonanaisMediterranean
METHODS
N
0 Km 5
SCRUBLAND
1
2
MARSH
Weanalysed145faecescollected intheDBRinthe2 yearsfollowingthefirstknownoutbreakofRHD(i.e.the period1990—1992)and209faecescollected inMGduring
1992—1994. All sampleswerewelldistributedoverthe year.For purposesofcomparison,weusedthe265latrine contentscollectedinDBRbeforeRHDandreportedby Martinetal.(1995).Becausetheavailabilityofyoung rabbits is higherfrom December toMay (DelibesCaldero’n, 1979;Rogers, Arthur Soriguer,1994), weconsideredseparatelythedietsoftheso-calledwet (Dec.—May)andadry(June—Nov.)periodsateacharea.
Contentsoffaeceswere determined usingmethods described byReynoldsAebischer(1991).Weexcluded infrequentprey(Roper,1994)thatrepresented lessthan
0.5%oftheingestedbiomass.Importanceinthedietof eachpreycategorywasquantifiedby2methods:1) frequencyofoccurrence = numberofoccurrences of eachprey typex100/numberof faecalsamples; 2) estimateofingestedfreshbiomassbyusingcorrection factors(Lockie,1959);theestimatedingestedbiomass= fraction of eachpreytype(estimatedvisually)xdry weightofthefaecalsamplexcorrectionfactorx100/Y
(dryweightofremainsxcorrectionfactors).We used thesamecorrectionfactorsasMartinetal.(1995).
Fig.1.SketchmapoftheDonanaNational Parkwith the
locationofthetwostudyareas:1)DonanaBiologicalReserve;
2)Matasgordas.Parklimitsare shownbyacontinuousline andotherprotectedareasareindicatedbyadashedline. Badgersfromeachareadonot rangeintheother.
sub-humid,withanaverageannualrainfallof500—600 mmfallingmainlyfromNovembertoApril.Twoareas wereselectedwithinthePark:
1.DonanaBiologicalReserve(DBR): describedby Martinetal.(1995)andlocatedinthecentre ofthePark (Fig.1).Threemainbiotopesweredistinguishedwithin thisarea:marsh,dunesandscrubland.Thescrubland wasdominatedbyHalimiumhalimifoliumshrubswith scattered Quercus subertrees,whileScirpusspp.were dominantinthemarsh.AsinthestudybyMartinetal. (1995),wecollectedfaecesin DBR in theecotone scrubland-marsh.Theannualaveragedensityofadult rabbitsin thisareaduring1977—78 wasnot directly measuredbutassumedtobeabout7—9 individuals/ha
(Kufner, 1986).After RHD, annualaveragerabbit abundance in theDBR hasremainedconsistentlyat levelsfiveorsixtimesbelowthoseregisteredbeforethe diseaseoutbreak(VillafuerteMoreno,Inpress).
2.Matasgordas(MG): situatedalsointheecotone scrubland-marshbut15kmnorthfromDBR(Fig.1). ThedominantshrubinthisareawasPistacealentiscus, and Quercus suberand Fraxinus sp.treeswere abundant.Thoughitissituatedonly15kmnorthfrom theDBR,forunknownreasonstheincidenceofRHD inthisareahasbeenlowandaveragerabbit density
hasbeenestimatedas 11—18ind/ha(Palomaresetal.,
1995).
Differencesinoccurrenceofparticularpreycategories amongpairsofcompareddietswereevaluatedbychi- squareanalysisofcontingencytableswiththeBonfer- roniconfidenceintervals(Rice,1989).Dietdiversitywas calculatedusingtheLevinsIndexanddietsimilarities werecalculatedusingtheRenkonen’sIndex(Krebs,
1989).Spearmanrankcorrelationcoefficientswereused torelatetrophicdiversityandtheimportanceofdif- ferentpreycategories.
RESULTS
Youngrabbitswerethemainpreyitemconsumedby badgersinMatasgordas, duringboththewetandthedry period(Table1).Althoughfrequenciesofoccurrenceof rabbitsdifferedbetweenMatasgordasandtheDonana BiologicalReserve beforeRHD (atleastfor thewet period;Table1),theingestedbiomass ofrabbitswas consistentlyhighinbothyearlyperiodsandbothareas (alwaysabove55%;Table 1).Accordingto theRe- nkonenindices,dietarysimilaritieswerehighbetween MGandDBRbeforeRHD(81.3%and75.6%inwetand dryseason,respectively), lowbetweenDBRbeforeand DBRafterRHD (60.2%and46.2%)andintermediate betweenMGandDBRafterRHD(64.0%and62.35%).
Regardingother food categories,somestatistical differencesappearedwhencomparingfrequencies of occurrence,probably relatedto local differences in availability.Forexample,fruitconsumption washigher inMG withregardtoDBRbeforeRHD duringboth seasons(wet:x2=65.3, d.f.=1,P<0.001;dry: x2=24.0, d.f.=1,P<0.001)andwithregardtoDBRafterRHD duringthewetseason(x2 =34.4,d.f. =1;P<0.001),
Table1.Frequencyofoccurrenceandpercentageofbiomassofeachpreytypeineachstudyareaandperiod,anddiversity (LevinsIndexvalues).Inbracketssamplesize.MG =Matasgordas.DBR =DonanaBiologicalReserve.RHD =Rabbit HaemorrhagicDisease
MGDBRafterRHDDBRbeforeRHD
%Occurrence%Biomass%Occurrence%Biomass%Occurrence%Biomass
Wetseason
(n=108)(n=77)(n=162)
Lagomorphs39.862.120.840.967.380.9
Smallmammals10.23.16.53.59.90.9
Birds0.90.19.112.41.80.0
Reptiles7.40.63.90.39.90.4
Amphibians19.44.27.81.19.31.7
Insects96.317.489.640.481.516.0
Fruits38.012.01.30.71.20.0
LevinsIndex2.322.891.47
Dryseason
(n=101)(n=68)(n=103)
Lagomorphs37.655.68.821.656.361.1
Smallmammals4.93.10.00.04.80.8
Birds4.01.34.411.54.81.7
Reptiles11.93.47.37.916.510.3
Amphibians8.91.35.90.526.212.0
Insects86.111.297.113.876.712.0
Fruits53.523.832.342.520.42.0
LevinsIndex2.653.692.45
4.0
3.64
3.2
2.8
2.4
2.0
1.6
1.2
variedsignificantlywithregardtoDBR beforeRHD andtoMG (P<0.001). Nevertheless, youngrabbits continuedtobeanimportant fooditem,particularly duringthewetseason(41%).Youngrabbits werenot replacedbyasinglepreycategoryinthebadger’sdietin anyseason.Alternativefoodsincludedinsectsandbirds inthewetseasonandfruit,insectsandbirdsinthedry
36season(Table 1). Dietary diversity almost doubled duringthewetseasonandincreased1.5timesduringthe
2dryseasonfollowingtheRHDoutbreak(Table1).
5Thepercentage of rabbit biomass in thedietwas negativelycorrelatedwithfooddiversity(rs=—1,n=6, P0.001;Fig.2),suggestingthatdietarydiversitywas relatedtotheavailabilityofyoungrabbitsandrelatively independentoftheavailabilityoffoodtypesotherthan
1rabbits. There wasa significantpositivecorrelation betweendietdiversityandpercentageofbirdbiomass
(P0.05),suggestingthatbirdswereatypicalcomple-
153045607590
% Rabbit biomass
Fig.2.Correlationbetweendietarydiversity(asLevinsIndex) andthepercentageofingestedbiomassofrabbit.1=Donana Biological Reserve(DBR)beforerabbithaemorrhagic disease (RHD)inwetseason.2=DBRbeforeRHDindryseason.3
=DBRafterRHDinwetseason.4=DBRafterRHDindry season.5=MGinwetseason.6=MGindryseason.
while no significant differencesweredetectedwith regardtoDBRafterRHDduringthedryseason.
Ingestedyoungrabbit biomass declinedabout50%
duringthewetperiodand33%duringthedryperiodin theDBRaftertheoutbreakofRHD (Table1).Inboth
wetanddryperiods,frequenciesofoccurrenceofrabbit
mentaryfood.
DISCUSSION
Giventheremarkable geographical,seasonalandindivi- dualvariationsdetectedinEurasianbadgerdiets (e.g. LurpsWandeler,1993),someauthorssupportthe traditionalviewthatthespeciesisanopportunisticfood generalist(e.g.Roper, 1994;Roper Mickevicius,
1995).Otherauthorsdescribetheforagingbehaviourof someEurasianbadgerpopulationsasbeingmorechar- acteristicofspecializedfeeders,relyinglocallyonsingle resources,suchasearthworms (Kruuk Parish,1981),
somefruit (Kruuk deKock,1981),insectsandfruit
(Pigozzi,1991)oryoungrabbits(Martinetal.,1995).
Themore simplisticinterpretationofourresults suggeststhatbadgersintheDonanaareaareopportu- nisticfeeders,becausetheychangedtheirdietinDBR afterrabbitsbecamescarce.However,suchachangein dietdiversityoffacultative specialistswhentheencounter ratewithpreferredpreydeclinesispredictedbymost theoreticalmodelsoffoodspecialization(e.g.StephensKrebs,1986).In fact,oneoftheaxioms ofclassical foragingtheoryisthatdietarydiversityofspecialistsis governedbyencounter ratewith themoreprofitable prey,regardlessofabundanceofotherfoodresources (Futuyma &Moreno,1988).Inourcase,availabilityof rabbitsseemstobethekeytobadger’sdietdiversity(Fig.
2).Despitethechangeinrabbitnumbers,therewasno possibilityofachangeintheavailabilityofrabbitsper individualbadger,ifthenumbersofbadgershadalso decreased.However,wewereunabletodetectashort- termnumericalresponseofpredators,includingbadgers, totherabbitdeclineafterRHD(Delibesetal.,1992).
Ourresultssuggest that,onlywhenrabbit became scarce,in DBR after RHD, wasthe diet diversity increased.Weassumethattheseasonalavailabilityof insectsandfruitinDBRwasnotnoticeablymodifiedby theRHDoutbreak;nevertheless,theseseasonalchanges
insecondarypreyabundance,veryconspicuousinthe DBRbadgerdietafterRHD(Table1),werenotreflected inthedietswhereand whenrabbitswereabundant.
AccordingtoBrownMorgan(1995),theforager’s diet resultsfrom atwo-stepdecisionprocess:select wheretoseekfood,and oncethere,selectwhattoeat. ProbablyDonanabadgerscouldbeconsideredselective predatorsbecausetheystartsearchingforyoungrabbits byforagingongoodrabbitbreedinggrounds,indepen- dentlyof theabundanceof alternativefoodswhich couldbeeateninanopportunisticway,astheywere foundwhilesearchingforrabbits(Martin etal.,1995;
Rodriguez,MartinDelibes,1996).
A questionremainsas to why Eurasianbadgers apparentlybehave asaselectivepredatorindifferent places.Obviously,theycannotbeconsideredmorpholo- gical,physiologicalorevenbehaviouralspecialistsinthe evolutionarysenseofFutuymaMoreno(1988).Para- doxically,it seems theyareopportunisticto apoint which enablesthemtoadapttheirfeedingbehaviourto actlocallyas truespecialists, onsuchdifferentfood resourcesasearthworms orrabbits.
The describeddietary responseof the Donana
badgerstoadeclineinpreferredpreywassimilartothat ofsomeScottishbadgerpopulationswhenearthworms becamescarce(Kruuk, 1989).In thelongterm,we couldexpectachangeintheDonanabadgerpopulation size,althoughwehopethespecieswillnotdisappear, as happenedintheArdnishstudyareaofKruuk (1989) following achange inlandusewhichgaverisetoa decreaseintheavailabilityofearthworms.
Acknowledgments
WeareindebtedtoRafaelLaffitteforhishelpcollecting faeces andtoCristinaZapatafor herhelpanalysing
them.WethankXimCerda’,HansKruuk, TimRoper, LindaM.Ilse,AlejandroRodriguez,EloyRevillaand FranciscoPalomaresfor constructive comments on draft manuscripts.ClaudiaKeller kindly revisedthe Englishversion.ThisstudywassupportedbyDireccio’n GeneraldeInvestigacio’nCientificayTe’cnica(projects PB-87/0405andPB-94/0480)andtheSeniorauthor (JMF) byapredoctoralgrantfromtheMinisterio de Educacio’nyCiencias ofSpain.
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DietoftwospeciesofminkinEstonia:displacementofMustelalutreolaby
M.vison
T. Maran1,3,H.Kruuk2*,D.W.Macdonald3M.Polma1
1TallinnZoo,Tallinn,Estonia
2InstituteofTerrestrialEcology,BanchoryAB314BY,Scotland
3WildlifeConservation ResearchUnit,DepartmentofZoology,OxfordOX13PS,U.K.
Abstract
Duringaperiodinthe1980swhenbothEuropeanminkMustelalutreolaandAmericanminkM.vison werepresentinEstonia,theirfoodwassignificantlydifferent.Europeanminkateagreaterproportionof fishandcrustaceans,whereasAmericanminktookrelativelymoremammalsandfrogs.Thiswasprobably relatedtoadifferenceinhabitatselection.AfterthedisappearanceoftheEuropeanmink,thedietofthe AmericanminkinourmainstudyareawassimilartothatoftheEuropeaninthesameareapreviously. Twoalternativehypothesesarepresentedforthemechanismswhichled tothereplacementofEuropean minkbytheAmericanspecies:(i)thetwospecieshaveadifferentniche,andtheAmericanminkcould replacetheEuropeanminkafterthelatterhaddisappearedforunrelatedreasons,or(ii)theAmerican minkaggressivelyoustedtheEuropeanmink,aprocessstartingintheAmericanmink’spreferredhabitat (slowflowingrivers).Atpresentthereareinsufficientdatatorejecteitherofthesescenarios.
Keywords:diet,mink,habitat,competition,extinction
INTRODUCTION
ThedeclineoftheEuropeanminkMustelalutreolain thesecondhalf of the20thcenturyhasbeencata- strophic,andnowthisspeciesisatriskofbeingthenext mammalianextinctioninEurope.Amongstthehypoth- esesthatseektoexplainthedecline,severalconcernthe relationshipbetweentheendemicEuropeanminkand theintroducedAmericanminkM.vison.Inparticular, questions ariseof evidenceof competitionfor food, nicheoverlapanddisplacement, betweenthespecies. Onewaytotestsuchacompetitionhypothesis is to makeuseofthenaturalexperimentprovidedbythe disappearanceoftheEuropeanmink,andcomparethe Americanmink’sdietbeforeandafter.
In thispaper,weprovidedataonthefoodofthe EuropeanminkandtheAmericanminkoveralarge areaofEstonia.AftertheEuropeanminkdisappeared from thecountry,datawere collectedondietofthe
Americanminkalongoneoftherivers, andtheywere
*Allcorrespondenceto: DrH.Kruuk,Institute ofTerrestrialEcology, BanchoryAB314BY,Scotland
comparedwiththedietofEuropeanminkduringits occupancyofthesameriver inthepreceding period.
Thecourseofthedeclinesincetheearly1970s,and finaldisappearanceoftheEuropeanminkfromEstonia after1992,havebeenwelldocumented(Maran,1991; Maran Henttonen,1995). Itparallelstherapid declineofthespecieselsewhere inEasternEurope,in contrasttoitsperformanceinSpainwherenumbersare
steadyor increasing(Ba’rta, 1956;Szunyoghy, 1974; Schreiberetal.,1989;Romanowski,1990;Palomares,
1991).Despiteour ratherdetailedknowledgeof the EasternEuropeandeclineandenumerationofpossible causes (Maran Henttonen,1995;Maran etal.,In press),nosatisfactorysingleexplanationhasbeenput forward,andnosimplesolutionfortheconservationof Europeanminkisyetavailable.
ThedemiseofEuropeanminkinEstoniacoincided withtheestablishmentthere,intheearly1970s,ofthe Americanmink(Maran,1991),although theEuropean
mink hadbeenin long-termdeclineeven beforethe arrivalofitsexoticcongener.Oneofthepossible,final causes of theEuropeanmink’s disappearance, there- fore,couldbesimplecompetitionforresourceswitha