relatedness structure and kin-biased foraging in the greater horseshoe bat (rhinolophus)

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Relatedness Structure and Kin-Biased Foraging in the Greater Horseshoe Bat (Rhinolophusferrumequinum)Author(s): Stephen J. Rossiter, Gareth Jones, Roger D. Ransome, Elizabeth M. BarrattReviewed work(s):Source: Behavioral Ecology and Sociobiology, Vol. 51, No. 6 (May, 2002), pp. 510-518Published by: SpringerStable URL: http://www.jstor.org/stable/4602086 .

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Behav Ecol Sociobiol (2002) 51:510-518DOI 10.1007/s00265-002-0467-1

ORIGINAL ARTICLE

Stephen J. Rossiter * Gareth Jones

Roger D. Ransome * Elizabeth M. Barratt

Relatedness tructureand kin-biased oraging

in the greaterhorseshoe bat (Rhinolophuserrumequinum)

Received: 15 June2001 / Revised: 24 January2002 / Accepted: 30 January2002 / Publishedonline: 16 March 2002? Springer-Verlag 002

Abstract Female greater horseshoe bats (Rhinolophusferrumequinum) xhibit strong natal philopatry o theirmaternity oost over manyyears,leadingto the aggrega-tion of matrilinealkin. Maternitycolonies may, there-fore, be expectedto comprisehighly related ndividuals,and, as such, provide conditions suitable for the evolu-tion of kin-selectedbehaviours.To test these predictions,we examinedrelatednessand behaviouramongmatrilin-eal kin within a colony in south-west Britain. Geneticanalysisof 15 matrilines, dentifiedfrom microsatellitegenotypingand long-termringing surveys, revealedav-erage relatedness levels of 0.17 to 0.64. In contrast,background elatednessamong colony females approxi-mated o zero (0.03). Theseresultssuggest that nclusive

fitness benefits may only be accruedthroughdiscrimi-nate cooperationwithinmatrilines,and not at the widercolony level. To examinewhether he potential or suchbenefitsis realisedthroughkin-biasedcooperationdur-ing foraging, females from two matrilineswere radio-trackedsimultaneouslyover 3 years. Pairwise home-range overlap correlatedsignificantlywith Hamilton'srelatednesscoefficient.The greatestspatialassociationswere observed between females and their adult daugh-ters, which shared both foraging grounds and nightroosts, sometimes over several years. Tagged females,however, generally foragedand roostedalone, suggest-ing thatkin-biased patialassociationprobablydoes notresult from either information-transferr cooperative

Communicatedby J. Wilkinson

S.J. Rossiter(1) - G. Jones R.D. RansomeSchool of Biological Sciences, Universityof Bristol,WoodlandRoad,BristolBS8 lUG, UKe-mail: [email protected].:+44-207-8827528, Fax:+44-208-9830973

S.J. Rossiter E.M. BarrattInstituteof Zoology, Zoological Society of London,Regent' s Park,LondonNWl 4RY,UK

Presentaddress:

S.J.Rossiter, Queen Mary,Universityof London,LondonEl 4NS, UK

territorial efence. Such patternsmay insteadresult roma mechanismof maternalnheritance f preferredorag-ing androostingsites.

Keywords Coloniality Chiroptera Kinship

Introduction

Coloniality in mammals is widespread,occurringingroups as diverse as rodents,pinnipeds and bats. Yetwhy individuals ive at highdensities s notalways clear(see Danchinand Wagner 1997). Although sometimesenforced,due to limited criticalresourcessuch as suit-

able shelters e.g. Altmann1974),colonialitycommonlypersistswhere such resourcesare plentiful.This is ob-serveddramaticallyn bats, which can form maternitycolonies numberingseveral million individuals,oftenroosting in bodily contact with each other (e.g. GustinandMcCracken 987).

Wherecoloniality s coupledwith female recruitmentinto thenatalgroupand subsequentong-termphilopatry,as observed in many mammals,including bats (e.g.Castellaet al 2001; Kerthet al. 2000), colonies willcomprisegroupsof femalekin originatingrom one ormore matrilines(e.g. Wilkinson 1985b; Kerth et al.2000). Suchmammalian ocial organisationmay favourtheevolutionof cooperativebehaviours ia kin selection(Hamilton1964), andthese behavioursmay play a sub-sequent role in maintainingsocial cohesiveness (e.g.Armitage1987). Indeed,kin-biasedbehaviourhas beenreported n all majoranimalgroups,and is especiallycommon n socialmammals reviewedby Hepper1991).

Todate,thepotentialmportance f kinshipas adriv-ing forceunderlying he evolutionof cooperation n bats,has been most convincinglyrevealed n the vampirebat(Desmodus rotundus), in which both food sharing andsocial groomingamong colony membersare positivelycorrelated with relatedness,and roosting association

(Wilkinson1984, 1986). Most otherformsof coopera-tionrecordedwithinbatcolonies, including ood sharing



511

(e.g. Wilkinson 1984), communal nursing (e.g.Marimuthu ndSelvanayagam1981; Wilkinson 1992a),increasedwarmth e.g. Roverudand Chappell1991), in-formation exchange (e.g. McCracken and Bradbury1981; Wilkinson 1992b), social grooming (Wilkinson1986) and helper-assisted irth (Kunz et al. 1994) havegenerallybeen describedas mutualistic, hough he rela-

tionships of interactantswas not usually assessed. Nocorrelationwas recordedbetween relatednessand roost-ing association n both wild (Kerthand Konig 1999) andcaptive emperate pecies (Kozhurina 993).

An indirectapproach or assessing the importance fkinship n underpinningociality n mammalgroups s tocalculateaveragegenetic relatedness stimates rom mo-lecular markers e.g. Packer et al. 1991; Girmanet al.1997; De Ruiterand Geffen 1998). This methodhas re-vealed surprisinglyow averagerelatedness alues with-in bat colonies (around zero) (e.g. Wilkinson 1992a;Burlandet al. 2001; Storz et al. 2001), even where kin-selected cooperation has been described (Wilkinson

1985b). Findingsto date, therefore, uggest that coloni-ality in bats cannot sufficientlybe ascribed o close ge-netic ties alone (Burland nd WorthingtonWilmer2001).Wilkinson (1985b) attributed ow relatednessvalues inD. rotunduscolonies to immigration, mall litter size,high infant mortality, ow adult mortality, hort haremtenureby males and ncompletemonopolisation f pater-nities; and used computer imulations o show thatrelat-edness levels rapidlyapproach ero over a rangeof im-migration ates.Studiesof social insects revealthatcolo-ny relatednesss rapidlydilutedwith increasingnumbersof female breeders,especiallywhen these are not close

relatives see Ross2001).Low average relatedness evels recordedwithin batcoloniessuggest that, n order o accrue nclusive fitnessbenefits,individualsmust be able to recogniseand dis-criminatebetweencolonymembers. t follows that stud-ies seekingto establish he potential or, andrealisationof, inclusive fitness benefits n bats cannotrelyon colo-ny means, but instead must examine groupsof relativeswithin the colony. Such accuratedelineationof familygroups n coloniescomprisingmultiple ineages requiresdetailedpedigree information, he collection of whichpresents onsiderable racticaldifficulties.

We examinedforaging behaviour,and quantified e-

latedness, within kin groups of the colonial greaterhorseshoe bat (Rhinolophus ferrumequinum), using

matrilinealpedigreesconstructed rom combinedlong-termobservationandparentagedata.We predicted hatrelatednesswithin matrilineswould be higherthan be-tween matrilines,as well as background olony related-ness, which was expectedto be aroundzero. Secondly,we predicted hatany cooperationamong foraging ndi-vidualswould correlatewithclose geneticties. Co-oper-ative foragingis common in animals,and can involvegroup hunting (e.g. wild dogs Lycaonpictus, Malcolmand Marten 1982), joint territorialdefence (e.g. lions

Panthera eo, IHeinsohnnd Packer1995), active or pas-sive informationexchange (e.g. ravens Corvus corax,

Heinrich 1988) and increased vigilance (e.g. ostrichesStruthio amelus,Bertram1980). Furthermore, anyex-amples exist of groupforaging in bats (e.g. Racey andSwift 1985; Brooke 1997).Where oraging s kin-biased,individualsmay gain additional ndirect itness benefitsthroughsharedgenes (e.g. Kaib et al. 1996). Althoughnot studiedpreviously,observations f apparent ommu-

nal foraging among R. ferrumequinum dults suggestthat cooperationmay occur (Duverge1997). If R. fer-rumequinumemale relativesdo engage in kin-directedcooperative oraging, hen they are expected o associateat feeding sites to a greaterextent than non-kin.Evi-dence of relatedness tructurewithinthe colony, coupledwithkin-biasedbehaviour,would support he theory hatkinshipplaysa role in the evolutionand maintenance fcoloniality n this species.

Methods

Study species and background

We studied a colony of R. ferrumequinum (about 40 breeding fe-

males) at WoodchesterMansion in Gloucestershire,UK (51?2' N,2?90' W). Since 1982, most bats at this colony have been ringedasneonates while attachedto their mothers. This species is long-lived, and females are stronglyphilopatricthroughout heir lives.Once mature, females may produce offspring up to the age of29 years (Ransome 1995a). Parentageanalysis shows that severalhalf-sibs, and some full-sibs, exist within the colony, althoughboth maternal half-sibs and full-sibs must be of different ages,since females only produce one offspring each year (Rossiteret al.2000a). The successful establishmentof new matrilineswithin thecolony seems to be rare,withjust two successful immigrationsre-corded in 8 years (Ransome 1989). R. ferrumequinum social orga-

nisation s thuspredicted o resultin multiple groupsof female rel-atives, potentially providingsuitable conditions for the evolutionof kin-selectedbehaviours.

Matrilineconstruction

Matrilinealpedigrees, containingthree or more female kin, wereconstructed from mother-daughter pairs, identified by capturewithin the roost, genetic analysis, or both. Of 70 females born be-tween 1993 and 1997, a group of 49 (70%) were tissue sampledand ringed while attachedto a mature female. Maternityof theseindividuals was confirmed by genotyping at seven polymorphicmicrosatellite loci, which revealed no mismatches between puta-tive mother-offspring pairs, thus providing strong evidence thatattachmentequatesto actualmaternity.Eighteen female offspring(26%), sampledwhile unattached,were matchedup to a solitarylactatingfemale with 95% confidence, using a likelihood methodof parentageanalysis (Marshallet al. 1998). In addition,maternitywas determined or 18 females bornbefore 1993, by eitherparent-age inference (11 individuals), or where tissue sampling was notpossible due to mortality,by observationof attachment ollowingbirth (7 individuals).Full details of parentage nference are pro-vided in Rossiter et al. (2000a).

Relatednessanalysis

Meangenetic relatedness,based on seven polymorphicmicrosatel-lite loci (Rossiteret al. 1999), was calculatedwithin and betweenmatrilines,as well as among all colony females, using the program

RELATEDNESS 5.03 (see Queller and Goodnight 1989). Esti-mates were calculated against background allele frequencies ob-



512

tained from 291 individuals, sampled at four neighbouringcolo-nies characterised by little or no differentiation (Woodchester,Brockley, Mells and Iford;see Rossiteret al. 2000b for details).Toprevent possible underestimationof relatedness,due to the pres-ence of many relatives in the population, known matrilineal kinwere excluded from contributingtowards backgroundallele fre-quencies. Standarderrors were estimatedby jackknifingover loci(Queller and Goodnight 1989).

Permutationwas used to test whether within-matriline elated-

ness levels were significantlyhigherthan those calculatedfor ran-dom groups of colony individuals, and therefore whetherrelated-ness structurewas homogenisedthroughcommon paternity.To il-lustrate the method, which allowed for the non-independenceofpairwise values, consider two matrilines, of sizes n1 and n2. Theaverage of each matrilinewas calculated from its pairwise valuesof R and an overall arithmeticmean was then taken of these twoaverages. Overall means were then compared with distributionsobtained by permutation.Specifically, by combining individualsfrom the first matriline with individuals from the second, a half-matrix (of size nl+n2 by nl+n2) of relatedness values was con-

structed.Fromthis, n1 individuals were selected randomly,and theoverall mean was calculated from the means of the pairwiseR-val-ues of these individuals,and the distributionof the pairwiseR-val-ues of the remaining n2 individuals. This was repeated 1,000

times, using a custom-writtencomputer program.If bats are lessrelated to members of the other matriline than the individualswithin their own, then overall means which include "cross-matri-line" pairwise values are expected to be lower than the observedmean. Observed values were therefore considered significant ifthey fell within the top 5% of values obtainedby randomisation.

Analysis of foraging associations

To determinewhetherforagingmatrilinealkin associate with eachotherto a greaterextent thannon-kin,females (lactating ndividu-als, non-breeding ndividuals, and yearlings) from two matrilineswere radio-tracked for seven sessions over three summers(1997-1999). For each session, 2-5 roosting females from each

matriline were caught and fitted with 1.3 g radio transmitters(Holohil Systems Carp,Ontario, Canada) using surgicaladhesive(Pfizer, Largo, Fla., USA). Eachevening, an individualwas select-ed randomlyand trackedall-night by one or two trackers,using aLotek SRX_400 receiver (Lotek,Newmarket,Canada)attached oa directional three-elementYagi antenna(MarinerRadar)or vehi-cle-mounted aerial (BioTrack, Wareham, UK). Foraging areaswere located by homing-in on highest amplitude signals (seeWhite and Garrott1990) and bats were approachedandcircled, toconfirmtheirprecise locations. R.ferrumequinum emales typical-ly forage at several foragingareas each night, includingwoodlandblocks, pastures or a series of adjoining fields (Duverge 1997).Foraging episodes, identifiedby extendedperiodsof relativelysta-ble signal strength,are separatedby periods of either commuting(to roosts or other foraging sites), or local night-roosting.To esti-mate distances from the receiver to the bat, we pre-calibrated hereceiver's performance,comparing observed signal strengths tolevels obtainedfromholdingradio transmitters t knowndistancesaway, at fixed receiver gain. While within 10-50 m of each focalanimal, the presence/absenceof other tagged bats was recorded,providing information on spatial-temporalassociations. Wherepossible, foragingbats were also observed visually, or, listened toon a bat detector.In addition, throughout he study, night-roostingepisodes were recorded, with the roosting bats circled to deter-mine their exact location. Tracking sessions continued until alltags fell off or failed.

For bats with >30 independentradio-fixes, 95% and 50% ker-nel utilisation distributions(UD) were plotted using ARCVIEWGIS 3.1 (EnvironmentalSystems Research Institute 1996) withANIMAL MOVEMENT2.0 (Hooge and Eichenlaub 1997). Thesmoothing parameterwas derivedusing a "least-squares ross-val-

idation" method (Silverman 1986), which provides a low-biasedestimator (Hooge and Eichenlaub 1997). The 95% kernel repre-

sents the near total home-range size, while the 50% probabilitykernel corresponds o a "corearea",often corresponding o impor-tant resources (Harriset al. 1990).

To quantify UD overlap, area overlapwas calculated (separate-ly for both 95% and 50%contours) using a digitising tablet (Sum-magraphics), inked to a computer,divided separatelyby the rele-vant total UD area of both individualsin the pair, and averaged.To assess whether relatives share feeding grounds, pairwise UDoverlap was correlated with pairwise R-values using a Mantel

Test. This was also repeated substitutingR-values for Hamilton'srelatednesscoefficients based on female relationships,as an alter-native measureof kinship that does not rely on the accuracyof mi-crosatellite-basedvalues of R. Hamilton's relatedness coefficientwas calculated as X(0.5)L,whereL represents he numberof gen-eration inks, summed for all possible pathwaysbetween two indi-viduals. For this correlation,an arbitrary elatednesscoefficient of0.05 was used for between-matrilinepairwise comparisons,whichwas consideredto be a conservativelyhigh estimate.

Results

Relatedness

We combineda historicaldataset,observations, ndmi-crosatellite-basedmaternity nference to construct 15matrilinealpedigrees, comprising3-12 bats (mean =5.75), over ten generations.Severalunattached ffspringbornbefore 1993, which died before tissuesamplingbe-gan, were not assigned mothers. Some matrilinesmaytherefore harecommon emale ancestors.Groupsof justtwo individuals,usually containinga single mother-daughterpair,were excluded from relatednessanalyses.Mean relatedness within matrilines ranged from0.64?0.12 (mean? SE) (n=3) to 0.17?0.09 (n=5), indi-

cating that considerable otential nclusive fitnessbene-fits couldtheoretically esult fromkin-directed oopera-tion.Averagebetween-matrilineelatedness, n the otherhand, approximated o zero (0.03?0.03, n=102), andmeasured he same as the backgroundevel of related-ness calculatedamong all colony females (0.03?0.03,n=115). Relatednessresults are summarisedn Fig. 1.Significant tructurewas detectedamong he five largestmatrilinestested (P<0.001 to P<0.01), indicatingthatthese matrilineswerecorrectly dentified,and that relat-edness levels amongmatrilineswere not homogenisedthroughpaternalnput romsharedmalerelatives.

Radio-tracking

To determinewhetherbatsforageandnight-roost refer-entiallywith kin, 14 females from two matrilineswereselected for radio-tracking Fig. 2). Average within-matriline elatednessvaluesfor these groupsof femaleswere 0.24?0.10 and 0.25?0.10 (membersof matrilines8144 and 7336 respectively),andbetween-matrilinee-latednesswas 0.06?0.11. Individualswere radiotaggedover three summers Radio-transmittersell off after6.3?2.2 nights,and bats were therefore aggedfor multi-

ple sessions, often in separateyears, to obtain adequatefixes for data analysis. On average, individuals were



513

Fig. 1 Comparisonsof meanpairwise relatednesscalculatedfor the whole colony andsepa-rate matrilines.Matrilinenames are based on the identi-ties of the oldest knownfemaleidentified in each family group.Numbers of individuals sam-pled from each matriline s giv-en inparentheses. Standard r-rors were calculatedby jack-knifing over loci (Queller andGoodnight 1989)

colony emales 1 12) -

between-matriline102) _-+1

within-matriline102) -

matiline10038(5) -

matriline 708 (3) I I

matriline 374 (3) I

matriline 701 (3) -

matriline 483 (7) - *

matriline 477 (10) - * I



matriline 677 (3) -I



matriline 635 (5) -


mariline 379 (5) I

matriline 144 (12) -

matriline 336 (8) -

0.0 0.2 0.4 0.6 0.8

relatednessR)

MATRILINE MATRILINE

8144 7336

9160(dead)

yearborn

88 9684 9668

89

90 9837 10034

91 10036

92

93 10361

94 10531 10540

95 10758

96 130 107

97 11182 11155

98 11563

Fig. 2 Matrilinealpedigreesof bats selected for radio-tracking

tagged for 3.7?0.5 sessions, representing 16.2?5.5nights.

Thirteenbats were selectedas focal animalsandfol-lowed to foraging areas (see Table 1). One individualwasnotselectedbecause ts transmitterell off early,andit was absent romthematernity oostfor subsequent e-tagging. Bats often foraged within close proximityto

WoodchesterMansion <200 m) beforeleavingthe area,and again on return.Duringthe first sessions of each

summer, agged bats generallyreturned o WoodchesterMansionat approximately 030 hours,probably o suck-le offspring,and left again at approximately 300 hours.During he second and thirdsessions, this behaviourwasless regular,and bats were increasingly ound at nightroosts.

The number f independentixes (foraging vents) re-corded for each focal bat averaged 21.1?3.9. In total,296 fixes were recorded,averaging1.68?0.09 km fromthe maternity oost (range:0.14-5.52 km). Of these, 274

(92.6%) nvolved no othertaggedbats otherthanthe fo-cal animal.On 22 (7.4%)occasions a second tagged batwas recorded eeding in the same area as the focal bat,18 of which (81.8%) involved two relatives, revealingmarkedspatial-temporal ssociation. Bats were neverobservedto arrive at or leave a foraging area together.Two cases of two bats simultaneously haringa feedingsite were recorded, although these were both near toWoodchesterMansion(<100 m), and thereforemay bean artefactof the close proximity o the maternity oost.An association of more than two tagged animals (twobats from one matrilineandone from the other)was ob-servedon just one occasion.

Home-ranges 95% UD) with core areas (50% UD)were constructed or seven individuals or whom mostfixes were collected (see Table2). Over 3 years, markeddifferences n foragingbehaviourwere observedamongindividuals.Some femaleshabituallyused the same for-agingareasand thereforehadsmallranges(e.g. individ-uals 9684 and9668), while othersexhibited ess fidelityfor feeding grounds e.g. individuals10930 and 10361).Seasonal variationwas also observed,with bats trackedduringlate August travellingfurther o foraging sites,possiblydue to the onset of the matingperiodwhen fe-males visit caves.For this reason,data obtainedafter25

Augustwere not included n the UD calculations.Pair-wise estimatesof home-range verlap, ogetherwith cor-



514

Table I Identitiesof all individualstagged, with the numbersof fixes recordedin each session, and in total. Emptycells indicate thatthe bat was not tagged

Matriline ID 1997 1998 1999 Totalfixes

Session 1 Session 2 Session 3 Session 1 Session 2 Session 3 Session 113/07-19/07 03/08-11/08 24/08-30/08 13/07-19/07 03/08-14/08 14/08-29/08 10/07-18/07

8144 9684 2 3 9 9 2 6 31

10540 3 1 0 2 1 5 1210036 3 4 4 1110930 9 32 2 4311182 3 7 4 1411563 4 49837 3 2 5 10 17 35

10531 0 0

7336 9668 3 17 4 2410034 8 2 1 19 3010361 5 3 5 8 4 5 11 4110758 5 4 0 10 15 3410907 12 1211155 3 2 0 5

Table 2 Summaryof home-range sizes (95%kernel and 50% ker-nel) of seven individualsfor which most datawere collected

ID 95%kernel(kM2) 50% kernel (km2)

9684 5.60 0.659837 10.52 1.38

10930 17.13 1.589668 9.91 1.68

10034 10.84 2.6510361 13.12 1.6510758 12.91 1.16

respondingpairwiseestimates of relatedness,are pre-sented in Table 3. Home-rangeoverlap(95% UD) wasnot significantlycorrelatedwith microsatellite-baseds-timates of relatedness(Pearsoncorrelationcoefficient0.27, P>0.05). Incontrast,a positivecorrelation etweenhome-range verlapand Hamilton's 1964)coefficientofrelatednesswas significant(Pearson correlation oeffi-cient 0.64, P<0.05) (Fig. 3). The discrepancybetweentheseresults s probablydueto thehighmarginsof errorassociatedwith single pairwiserelatednessvalues basedon seven loci. Negativepairwiserelatedness alueswereobtainedbetweenknown relatives n two cases (Table3;for an

explanationsee

McDonaldand Potts

1994;De

RuiterandGeffen1998), despite perfectallelematching

0.7

0~~~~~0.6

o0

0

~0.4E

- 0.4o *x

0.3

0.2

0.0 0.1 0.2 0.3 0.4 0.5 0.6

Hamilton's 1964) coefficient of relatedness

Fig. 3 Plot of pairwise coefficients of relatedness (Hamilton1964) againstvalues of 95%UD overlap.The positive correlationwas found to be significant using a Mantel procedure(Pearsoncorrelationcoefficient 0.64, P<0.05 by permutation)

between all genotypedmother-youngpairs.Indeed,thecontrasting istributions f relatednessvaluescalculatedwithinandbetweenmatrilines evealsconsiderable ver-

lap (Fig. 4), and therefore, n this instance, Hamilton's(1964) coefficient of relatednessbased on identity-by-

Table 3 Pairwise relatedness values based on Queller and Good-night (1989), together with Hamilton's (1964) theoretical coeffi-cients of relatedness (in parentheses),are given above the diago-

nal. Below the diagonal are pairwise estimates of home-rangeoverlapbased on 95% kernels, with cases of 50% kernel overlapshown in parentheses

9684 9837 10930 9668 10034 10361 10758

9684 -0.05 (0.25) 0.28 (0.5) -0.06 (0.05) 0.32 (0.05) 0.38 (0.05) 0.59 (0.05)9837 0.58 0.13 (0.125) 0.14 (0.05) -0.07 (0.05) 0.01 (0.05) -0.38 (0.05)10930 0.61 (0.71) 0.51 -0.24 (0.05) 0.13 (0.05) 0.12 (0.05) 0.41 (0.05)9668 0.31 0.37 0.29 0.68 (0.5) 0.30 (0.25) -0.25 (0.125)10034 0.33 0.38 (0.13) 0.28 0.65 (0.70) 0.32 (0.5) 0.06 (0.25)10361 0.30 0.42 (0.65) 0.42 0.63 (0.11) 0.57 (0.14) 0.40 (0.5)

10758 0.46 0.65 0.54 0.39 0.42 0.45



515

12

10

2

0

-0.60 -0.40 -0.20 0.00 0.20 0.40 0 .60 0.80 1.00

relatedness (R)

Fig. 4 Distribution of within- and between-matrilinepairwise re-latedness values, based on individualpairwise vales calculatedbythe programRELATEDNESS

f I I I I I I I II I t1| I I I

I I I I . I .... .1 ....11....,...I

* iII.'1 1

I I I l I . I ... . l

Fig. 5a-d Utilisation distribution (UD) for two mother-youngpairs. Parts a and b representthe UDs of individuals 9684 and10930, respectively,andpartsc and d represent ndividuals 10034and 9668. 50% and 80% UDs are shown by light and dark shad-

ing, respectively. Woodchester Mansion is representedby a solidblackcircle, and each grid incrementrepresents2 km

maternaldescent may representa moreaccurate ndica-tor of pairwiserelatedness.Although t cannot be ruledout that females from the two matrilines harecommonmaleancestors, he low levels of polygyny detected n R.ferrumequinum (see Rossiter et al. 2000a), suggest thatthisis unlikely.

Core areas(50%UD) overlappedn 6 out of 21 pair-wise home-range omparisons, ndtherefore oo few da-ta were available for a correlationof core-areaoverlap

versus relatedness.Of these cases, fourcorrespondedowithin-matrilineomparisonsand two correspondedobetween-matrilineomparisons.However,most areas ofoverlapwere in close proximityto the maternityroost(<1 km), and are thus probablyuninformative. ndeedonly two cases of core-areaoverlapwererecordedawayfrom WoodchesterMansion(approximately km), bothof whichcorrespondedo mother-daughter airs.Exam-ples of home-range verlapamongthesepairsof relatedbats are shown n Fig. 5.

Night-roosting wayfrom the maternity oost was re-corded on 27 occasions, representing ive individuals,and occurredmost frequently n sessions 2 and 3, when

bats did not always returnto the Mansion during thenight. On average, ndividualsused 2.7?0.5 roostseach,whichwerebuildingssuch as barnsand cattle-sheds.Ofthe five females found night-roosting,four exhibitedstrongwithin-year idelity to at least one roost, whileone individualwas recordednight-roosting nly twice,atnearby, but different, sites. Two females (10034 and

10930) used the same roosts in both years they weretracked,while individual9684 roosted in the same cat-tle-shedin both 1997 and 1998, andalso in 1993, whenit wasradio-trackeduringan earlier tudy(P.L.Duverge,unpublished ata).Unlikenon-kin,threemother-daugh-ter pairssharednightroosts, sometimessimultaneously,or roosted at adjacent sites (<50 m). One pair, bats 9668and 10034,both used neighbouring arns(approx.20 mapart) located over 2 km south-east of WoodchesterMansion, and on one occasion were found roosting to-gether.Specifically,bat 9668 was recorded ive times inone barn and once in the other, while the latter wasfound twice in each roost. Similarly,bats 10034 and

10361roostedtogether n a barn2 km north-westof thematernity oost.Finally,individual10930 was recordednight-roosting2.5 km from WoodchesterMansion, inboth a cattle-shed three times) and barn(twice) located30 m apart.The lattersite was also used by its mother(9684) on five occasions,on one of whichboth batswerepresentat the same time.Throughouthe study,no caseswere recordedof non-relativesnightroostingwithinthesame area <1 kmapart).

Discussion

Relatednessandmatrilineal tructure

Despite exhibiting strong female natal philopatry,andcontainingseveralgroupsof matrilinealkin, the Wood-chesterMansioncolony was, as predicted,characterisedby a low backgroundevel of relatedness,approximatingto zero. Consequently,kin-biased affiliation probablycannotaloneaccount or coloniality n this species.Lowaveragerelatednessvalues previouslyrecorded n bats(see Introduction), s well as other social mammals n-cluding the savannah baboon (Papio cynocephalus,Altmannet al. 1996), bonobo (Panpaniscus,Gerloffetal. 1999) andhairy-nosedwombat(Lasiorhinuskrefftii;Tayloret al. 1997),have often led to similarconclusionsthatsociality in such cases cannot be attributed o kin-ship, but is more likely to representmutualismor reci-procity.By comparison, elatedness alues calculated orseparateR.ferrumequinummatrilineswereconsiderablyhigher,and similar o levels reportedor otherspecies inwhichkin selectionmay occur,suchas the mound-build-ing mouse(Musspicilegus,Garzaet al. 1997) andlong-tailed macaque (Macaca fascicularis, De Ruiter andGeffen 1998). Furthermore, ifferentiationwas detectedamongdifferentmatrilines.Together,hese findingsthussupporthe conclusion hat nclusivefitnessbenefitsmaybe high enough for the evolutionof kin-selectedcooper-



516

ationat the level of the matriline,butprobablynot with-in the widercolony.

Kin-biased ssociations

Although considerable individual variation was ob-

served, relatedness evels among R. ferrumequinume-males correlatedpositively with home-range overlap,with matrilinealkin shared both feeding grounds andnight roosts to a greaterextent thannon-kin.Temporalassociations,also recordedpredominantly mongrelatedbats, probably reflect such spatial associations. Themaintenance f genetic structuring mongfamily groupswithinthe colony may thusresultfrom kin-biased orag-ing, as well as otherpotentiallycooperativebehaviourswithin the roost (see Introduction) ot considered n thisstudy.

What advantagesmight female relatives gain fromsharing foraging and roosting sites? One of the mostcommonly proposedexplanations or group foraging nbats is information ransfer,wherebyindividualsshareknowledgeaboutthe location or qualityof food patches(WardandZahavi 1973).Althoughpreviouslysuggestedfor a numberof species (e.g. Brooke1997),and demon-stratedunequivocallyn Nycticeiushumeralis Wilkinson1992b), several featuresof our findings appear o ruleout this explanation. ndeed, nformationransferoccurspredominantlyn species that rely on ephemeral oodsources that are difficult to locate (e.g. Waltz1982)andis typically characterisedby following behaviour (re-viewed by Wilkinson1995). Althoughseasonalfluctua-

tionsin the distribution ndabundance f R.ferrumequi-numpreyitems do occur(DuvergeandJones 1994),thepresent study was undertakenexclusively during themid- to late-summerperiod, and several females dis-played ong-term idelity for specificareas.Furthermore,most foraging events involved a single tagged female,and no following was observed. Such solitaryforaging,coupledwith largehome-ranges,also suggestthat rela-tives neitherassociateto cooperativelydefendterritories(e.g. Bradburyand Emmons 1974), nor hunt in groups(e.g. BarakandYom-Tov1989).We can, therefore, indno clear evidenceforcooperativeoragingamongR.fer-rumequinumemale relatives.

Withoutobviousshort-term enefitsof sharing orag-ing areas,an alternative xplanation o account for thespatialassociationof some relatives, s a mechanismofhome-rangeinheritance.Indeed, greatest overlap oc-curred between mother-daughter airs, three of whichused common core areas and night roosts. Mother-to-daughternheritancehas also recentlybeenproposedbyKerthet al. (2001), to explainsimilarhome-range ver-lap betweenfemalekin in the temperatebatMyotisbe-chsteinii. M bechsteinii females, like R ferrumequinum

females,maintainpreferencesorhuntingareasover sea-sons,andappearnot to exchange nformation bout ood

patches. The strikingsimilaritybetween the findings ofthese two studies, which, to the best our knowledge,are

the first to examine long-term foraging associationsamongkin in temperatebats, suggeststhathome-rangeinheritancemay occur in otherbatsspecies as well. As-sociations betweenfemale bats and their newly volantoffspringhave been also recordednLaviafrons Vaughanand Vaughan1987) and Eptesicusfuscus (BrighamandBrigham 1989), while Wilkinson(1985a) observed D.

rotundus emales to share both foraging groundsandwound sites with theiryearling daughters.Yet interest-ingly, a study of range-expansionn R. ferrumequinum

offspring at Woodchesterrevealed that mothers andyoungdo not shareforagingareas during he first sum-mer months.In fact, offspring oragingdistancesdo notreach those of adults until 55-60 days (Jones et al.1995), possibly due to constraintsmposed on the off-springby incomplete keletaldevelopment.Consequent-ly, the completion of offspringrange-expansion oin-cides with the dispersalof adult emales to matingsites,probablyprecludingmother-youngassociationsduringthe offspring's irst summer see Jones 2000). We pro-pose thatoffspringbeginto associatewith theirmothersat foragingsites in the following springand summer,when they inherit heirmothers'preferences or particu-lar areas.Therefore,kin recognitionmustoccurin thisspecies.

Possiblematernaluitionabout oragingareas

Althoughno directevidence of maternaluitionexists inR. ferrumequinum,Ransome(1995b) found that post-weanedjuveniles were less likely to survivetheir first

yearif theirmothersdied,suggesting hatfemalesconfersome form of non-nutritionalurvivaladvantage o theiryoung.A mode of information ransmission boutgoodfeedingareasandnight-roosts,rom mother o daughter,couldexplain he observedpatterns f both uvenilemor-tality andkin associations.Such tutoringaboutmaternalfeedingsites wouldsuggestthatcompetitiventeractionsbetweenmothers ndtheirmature aughterse.g.Clutton-BrockandAlbon1985)are notimportantn thisspecies.

Clans of the brownhyena (Hyaenabrunnea)may in-heritfeeding grounds romtheirpredecessors Skinner tal. 1995), while wild post-weanedColombiangroundsquirrels (Spermophilus colombianus) appear to inherit

the abilityto forage optimallyfromtheirmothers,per-haps throughobservationalearningduringbrief interac-tions (Ritchie 1991). R.ferrumequinumemales, by tu-toring offspringabout favourable oragingsites, couldtheoreticallycontribute o the success of descendants,thusincreasing heirown directfitnessin the long-term.Such vertical transmissionof informationdown matri-lines, coupled with extremesite fidelity and longevity(up to 30 years;R.D. Ransome,unpublished ata)indi-cates that coloniality may allow individuals o acquireextensive knowledge about their local environment.McCombet al. (2001) recentlydemonstratedhat Afri-

can elephant Loxodonta fricana) matriarchs ct as re-positoriesof social informationor theirgroup.Although



517

bats are long-lived for theirsize, andfrequently xhibitcomplex social structure, urprisingly ew studieshaveconsideredthe evolution of social learning within thislarge mammalianorder (reviewed by Wilkinson andBoughman1999). We hope thatby highlighting he po-tential importance of kin-biased associations throughmaternal utoring n the evolutionand maintenanceof

coloniality n bats, this study may encourage urther e-search nto thislittle-studied rea.

Acknowledgements We thank the Woodchester Mansion Trustfor access to the mansion, as well as all those who have helpedwith the collection of data at Woodchesterover the years. We alsothank Tamsin Burland for advice on data analysis and Steve LeComber for help with the figures. S.J.R. was fundedby a NERCstudentship,with additional support rom Bat ConservationInter-national andEnglish Nature.Bats were caught and sampledunderlicences from English Nature andthe Home Office, in accordancewith currentBritish law. Helpfulcomments from threeanonymousrefereesimprovedan earlierversion of the manuscript.

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