Winterreproductioninthegreatermouse-earedbat(Myotismyotis)
inSouthIberia
C.IBAFEZ
EstaciónBiológicadeDoflana,Apartado1056,41080Sevilla,Spain
Introduction
One ofthecharacteristicssharedbytemperatezonebatsistheabilitytodelayreproductiveevents (suchasovulationand fertilizationand,morerarely, implantation). Ithasbeensuggestedindifferent vertebrategroupsthatthesedelaysallowthefemalestotimecopulationandbirthoptimallyinorder to obtainthebestqualitymates(BirkheadMØller,1993).Inaccordancewith thishypothesis,mating takesplaceinautumnintemperatezone bats,whenmalesareingoodphysicalcondition.Thistiming furnishestofemalesabetterselectionchoiceandallowsthedeliveryofoffspringinlatespringor summerwhentheavailabilityoffoodresources ismaximal.
Duringastudyofcave-batpopulationsinAndalusia,southern Spain,somecasesofwinter reproductioninacolonyofmouse-earedbats(Myotismyotis)wereobserved andhereinreported.
Methods
Thecolony islocatedinanabandonedmineinLaPuebladelosInfantes(provinceofSeville,Spain)(37°47’N,
5°25’W)at180ma.s.l.Themine consistsofasinglegalleryabout150mlong,2mhighandImbroad. Ithas neitherlateralgalleriesnorshaftsofanysizebutanothercomdor20mlongneartheentrance.Thesurrounding areaconsistsofpastureswithholm-andcork-oaks(Spanish:‘dehesa’),olivegrovesandcerealfields.
Theminewasvisited5timesduringwinterandspring1995(18 and24 January,22February,31Mayand19
June).Populationestimateswerealwaysattempted,althoughestimatesbecamelessaccuratewhenthenumberof individualsofM.myotisexceededathousand.Insomecapturedandringed(metallicrings,LambournesLtd., Birmingham, U.K.)individuals,forearm lengthwasmeasured withdialcallipers(tonearest0.1mm),body
weight,genderandreproductivestatuswererecordedandageestimated(youngoradult,anddegreeofteethwear inadults).Thetotalepiphyseal gapbetweenmetacarpalandproximalphalanxofthefourthdigitoftherightwing wasadditionallymeasuredinyoungindividuals(KunzAnthony,1982)withadialcalliperwhilespreadingthe wingoverasourceoflight.AgeestimationswerebasedontheequationsofpostnatalgrowthofM.myotis, calculatedbyPaz(1986)inGuadalajara,CentralSpain.Allcapturedyoungindividualshadforearmssmallerthan
56mm(age30days).Therefore,totalgaplength(TG)wasusedforageestimationscorrespondingtothe equationofregression:
age=—15.87+0.76TG.
Results
Atthefirstinspection(18 January)wefounda clusteroffiveindividualsofM.myotisattheendof themaingallery.Fourofthemwereyoungwhoseepiphysealgapbetweenmetacarpalandphalanxwas stillapparent.Theyshowedthetypicalgreycolouredfur.Thefifth specimenwasanadultlactating
0
femalewithverywornteeth.Thetemperatureinthiszoneoftheminewas20°C and thebatswerein
shallowtorpor.AnotherclusterinthesmallergallerywasformedbysevenM.myotisandfour Miniopterusschreibersii. AllM.myotis,twomalesandfivefemales,wereadultswithworntovery wornteeth.Threeofthefemaleshadtheir nipplesdevelopedasiftheywerelactating,buthadnomilk atthatmomentandthesubjacentmammaryglandswerenotswollen.Thenipples oftheothertwo femalesweremoderatelydeveloped.Thebatsofthisclusterwereindeeptorpor.Thetemperature inside thegalleryisinfluencedbytheoutsidetemperatureand,thoughitcouldnotbemeasured,itwas notablylowerthanthatin thefirstgallery.Infact,itwasfreezinginpreviousnights,withaminimum recordof—6°Cfourdaysearlier(14January).Onthisoccasion,nomeasuring,weighingorringing couldbecarriedout.
InthesamespotinwhichwehadobservedthefiveyoungM.myotis, some50individualsofthis specieswerefound sixdayslater(24January).Theywereawakebutdidnotshowmuchactivity.The temperaturein thispartoftheminewas22°C.Five adultsand threeyoungindividualsoccupyingthe centre oftheclusterwerecaptured.Themeasurementsoftheyoungandtheirageestimatesareshown inTableI.Theageofthethreeyoungwouldbebetween44and57days(95%confidenceinterval). Accordingtothisestimate,theirbirthwouldhavetakenplaceatthebeginningofDecember1994. Thereappearedtobenomoreyounginthecluster.Threeoftheadultswerefemales,oneinan advancedstageofgestation(bodymass:36g).Theothertwofemaleswerenotapparentlypregnant, althoughtheyweighed28.5gand30g,respectively.Twoofthefemaleshad verywornteeth,while thethirdfemaleandthemalesshowedwornteeth.
On22February,acolonyofmorethanathousandM.myotiswereroostinginthemaingallery. Twenty-oneindividualswerecaptured,18adults(2malesand16females)and3young(2malesand1 femak).ThemeasurementsandageestimatesoftheyoungareshowninTableI.Twooftheyounghad
TABLEI
Characteristicsofyoungbatscapturedatdfferent occasionsduringthestudy.Forearmlength (FA)andtotalepiphysealgaplength(TG)inmm,weightingandageindays. Thefledgingin CentralSpainoccursattheageof43dayswithamassof 23.1ganda forearmlength0161.2mm (Paz,1986)
DateandIndividualSexFAWeightTGAge
24January / M / 58.3 / 18.5 / 4.0 / 53.52 / F / 57.8 / 19.5 / 4.6 / 48.9
3 / F / 56.8 / 21.0 / 4.2 / 52.0
22February
1 / M / 59.0 / 23.5 / 1.0 / 76.9
2 / F / 58.9 / 23.5 / 0.8 / 78.5
4 / M / 59.3 / 21.5 / 4.8 / 47.3
31May
5 / M / 60.3 / 25.0 / 3.4 / 58.2
6 / M / 60.6 / 24.5 / 5.7 / 40.3
7 / M / 62.2 / 23.5 / 4.7 / 48.1
8 / M / 61.5 / 21.0 / 3.6 / 56.7
9 / M / 62.3 / 24.5 / 5.6 / 41.1
10 / F / 59.6 / 21.5 / 6.4 / 34.8
11 / F / 64.5 / 26.5 / 5.5 / 41.9
12 / F / 62.9 / 23.5 / 7.0 / 30.2
beencapturedbefore(specimensNo.1andNo.2inTableI).Theagedifferencesbetweenthetwo estimates(made29daysapart)ontherecapturedindividualswere22and29days,respectively.The otheryoung,estimated47daysold,wasbornatthebeginningofJanuaryandshouldhavebeenaround
20daysoldatthepreviousvisit. Thisyoungwasprobablybornelsewhere,since itspresencewould
havebeencertainlydetectedif ithadbeen inthemineatthepreviousvisit.Noneoftheadultfemales capturedwaslactating.Thetemperatureofthezoneinwhichthecolonywaslocated,variedbetween
20and22°Cinthetwovisits.
On31May,thecolonyconsistedofseveralthousandindividualsofM.myotis,manyofthemyoung. Eightyoungwerecapturedandmeasured.Theageestimatesvariedbetween30and59days(mean44 days,seeTableI),which indicatesthattheywerebornthroughoutApril.
On19June,thecolonyagainconsistedofseveralthousandsofbats,someofthemM.blythii.The
majorityoftheyoungshowedatotalgaplengthoflessthan1 mm,eventhoughallwerestillnon volantsuckling.TheyoungindividualNo.2(ringed inJanuaryand checkedagain inFebruary),was againrecaptured.The temperaturebetweenFebruaryandJunewasconstantintherangeof20—22°C.
Discussion
Myotismyotisisoneoftheearly-breedingbatspecieswhichhasitsyoungduringabroadrange of time(Brosset,1955;BrossetCaubIre,1959;Kowalskietal.,1986).Asan extremecase,afemale carryingtwofoetuseswascapturedinOctoberinTunisia(Bakereta!,,1974).Mouse-earedbats of NorthAfricaareconsideredhereasM.myotis,accordingtoArlettazetal.(1997).Thisearlinesscould beduetotheirfeedingpreferencesonratherbig-sizedterrestrialarthropods(Bauerová,1978;Audet,
1990;Arlettaz,RuediHausser,1993),whoseabundanceislesstemperature-dependent thanfor flyinginsects(Lewis,1993).
Birthtookplaceduring Aprilforthegreaterpartofthecolony.Iftheintra-uterinelifespanisabout
50days(Herlant,1956), ovulationandfertilizationmusthaveoccurredduringFebruary,whenthe colonyarrivedattherefuge.ThereportedbirthdatesaretheearliestknownforEurope(BrossetCaubère,1959;Paz,1986),includingCentralSpain(endofMayand June), andaresimilartothose describedbyKowalskietal.(1986)forAlgeria.OvulationforyoungborninDecembermusthave occurredatthebeginningofOctober.Itmeansthatthesebatsdidnothibernatethatyear,possibly owingtothewarmanddryconditionsofthatautumn(TableII)andthe associatedgreaterprey availability.Thethreefemaleswithdevelopednipplesthatwerefoundon18Januaryinthesmaller galleryprobablyarethemothersofthreeoftheyoungofthemaingallery.Theuseofalternatelow temperaturedayroostsduringcold periodsrelatedwithnoforagingactivityisknownatlactationinM. myotisandMyotisemarginatus(Audet,1990;Krulletal.,1991).Thisbehaviourcontributes toreduce thermoregulatorycostsasbatscouldusedeeptorporinenergeticdeficitperiods(Audet,1990).
Thetimeofbreedingisanimportantfitnessfactorinanimals.Generally,individualsbornfirst withinthebreedingperiodhaveimportantadvantagesregardingsurvivalandsocialdominance.These advantagesaremaintainedfor animportantpartoftheirlives(i.e.Svensson,1995forbirdsand Green
Rothstein,1993formammals).Ithasbeenshownintemperatezonebatsthatyoungbornearlyhave
moreopportunitiestoaccumulatereservesinordertosurvivetheirfirstwinter(Racey,1982).The advantagesofanearlierbirthcanbemaintainedthroughout life.IndividualsofRhinolophus ferrumequinumwhichwerebornduringthesecondhalfofthebreedingperiodhadalowerprobability oflivingformorethan10yearsthanthosewhichwerebornearlier(Ransome,1989).Itisthereforenot surprisingthatfemalestrytohavetheiryoungasearlyaspossible,althoughitmaybethatonly femalesingoodphysical conditionareabletoreproduceearly.InR.ferrumequinum,olderfemales
TABLE II
Meteorologicalvariablesinthestudyarea.Monthlymeanvaluesoftmaximuntemperature(maxT),minimumtemperature
(minT),numberof dayswith minimumtemperaturebelowzero(minT<O°C),numberofdayswithmaximuntemperatureover
25°C(maxT>25°C)andprecipitation(precip).Meantemperaturevaluesoflast10years,andmeanprecipitationvalues oflast
20years.Samevaluesof1994withinparentheses
Month / maxT (°C) / minT (°C) / minT<0°C (days) / maxT>25 °C (days) / precip(mm)
8 / 36.4/(37.5) / 17.1/(17.8) / 01(0) / 31/(31) / 4.41(0)
9 / 32.0/(31.3) / 14.9/(13.4) / 01(0) / 29/(28) / 17.4/(3.5)
10 / 24.0/(26.5) / 11.5/(11.5) / 01(0) / 151(24) / 79.71(45.5)
11 / 18.8/(20.7) / 6,91(6.9) / 21(0) / 11(0) / 121.6/(89.5)
12 / 15.21(15.7) / 4.41(2.3) / 51(10) / 01(0) / 113.91(7.1)
wereinbetterphysicalconditionwithhigherbodymassbothatthebeginningand endofhibernation (Ransome,1968).Milligan &Brigham(1993)foundthatearlyreproductionandagewerecoincident infemalesofMyotisyumanensis.Inthepresentstudy,thefemalesthatgavebirth inwinterwereold too(worntoverywornteeth),andthesurvivalrateoftheyoungseemsnottohavebeen affected,in spiteofthelowtemperatures;which reachedbelowzero during10nights inDecemberand16more nightsinJanuary(onnoneofourvisitsinJanuaryandFebruarywasanycarcassofyoungfound). Althoughasaresultoftheirearlybirthdate,bodymassesandforearmlengthsofthewinter-born youngwerelowerthanthoseborninspringinthiscolonyandintheoneofCentralSpain(TableI) (Paz,1986).Thisfact,atsoshowninlate-bornR.ferrumequinum,appearstobealong-termhandicap tosuccessfulbreeding(Ransome,1989).
IamgratefultoA.Lafuente,L.Lara,E.Migens,J.L.Pérez-Jordáand J.Quetglasforassistanceinfield work.
J.Juste,R.ArlettazandP.Racey providedhelpfulcommentsonthemanuscript.This study wassupportedbythe
AgenciadeMedioAmbiente(JuntadeAndalucIa).
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Aremajorroadsabarriertosmallmammals?
J.H.RICHARDSON, R.F.SHORE’,J.R.TREWEEK
N.E.R.C.,InstituteofTerrestrialEcology,MonksWood,AbbotsRipton,Huntingdon, Cambridgeshire,PEI72LS,U.K.
ANDS.B.C.LARKIN
S.A.F.E.,CranfieldUniversity,SilsoeCampus,Silsoe,Bedford MK454DT
Introduction
Road networks are developing and expanding in many countries. Great Britain alone has approximately365,000km ofroadsandthisfigureisincreasingeachyear(Departmentof Transport,
1995).Althoughvergesassociatedwithroadsmay providesuitablehabitatforsmallmammals(Way,
1977;AdamsGeiss,1983;Perrow,1994;Ardeshiretat.,subm.),roadsthemselvesarelinear featureswhichmayactasabarriertomovement. Thus,roadsmayfragmenthabitats.
Severalstudieshavespecificallyinvestigated theimpactofroadsonthemovementofsmall
mammals.Oxley,FentonCarmody(1974)trappedsmallmammalsadjacenttoroadsofvarying widthandtrafficdensityintheU.S.A.andconcluded thatroadsinhibitmovement,themostimportant factorprobablybeingroadclearance(distance betweenvegetationcoveroneithersideoftheroad).In Canada,white-footedmicePeromyscusleucopuswererecordedcrossinga3.3—6.4mwidegravelroad infrequently,eventhoughtrafficdensitywasonly1—2vehiclesperhour(vph),anditwasconcluded thatsmallforestroadswere inhibitorsofmovementbutnot absolutebarriers(Merriam etat.,1989).
‘Authortowhomcorrespondenceshouldbeaddressed