J. Zool., Lond. (2000) 252,11±17 # 2000 The Zoological Society of London Printed in the United Kingdom

Social and population structure of a gleaning bat, Plecotus auritus

A. C. Entwistle*, P. A. Racey and J. R. Speakman Department of Zoology, University of Aberdeen, Aberdeen AB24 2TZ, U.K. (Accepted 21 September 1999)

Abstract Brown long-eared bats Plecotus auritus occupying 30 summer roosts in north-east Scotland were studied over 15 years. During this time 1365 bats were ringed, and a further 720 recaptures were made. Individual bats showed a high degree of roost ®delity, returning to one main roost site; < 1% of recaptured bats had moved among roost sites, and all recorded movements (n = 5) were < 300 m. Adults of both sexes were loyal to the roost sites at which they were ®rst captured, indicating long-term use of roosts. At least some juveniles (n = 32) of both sexes returned to the natal roost. Mark±recapture estimates indicated that colonies of this species were substantially larger (c. 30±50 individuals) than assumed in previous studies. Plecotus auritus differs from most other temperate zone, vespertilionid species in that there was no evidence of sexual segregation during summer, with males present in all colonies throughout the period of occupancy. Population structure in summer seems to be consistent with a metapopulation model, with discrete sub-populations showing minimal interchange. The group size, colony composition and population structure described in this species may be associated with the wing shape (particularly aspect ratio) and foraging behaviour of P. auritus. It is postulated that relative motility, linked to wing structure, may affect the distribution of individuals, and may have implications for the genetic structure of this species. Correlations between aspect ratio and both colony size and migratory behaviour, across British bat species, indicate that wing shape could be an important factor contributing to patterns of social behaviour and genetic structuring in bats.

Key words: Chiroptera, social structure, metapopulation, wing morphology, philopatry

INTRODUCTION of morphological and ecological specializations. However, surprisingly little information is available The autecology of a species underlies the distribution of about the patterns and variation in dispersal behaviour individuals, their use of space and resources, interplay and social organization of many, even common, bat with conspeci®cs, and consequently population struc- species. In addition, few attempts have been made to ture. The relationship between ecology and social explain distributions and determine the population behaviour within species has been the source of con- structure of these mammals, and to explain how siderable study, particularly with respect to the such variation may relate to morphological factors or formation of groups (Alexander, 1974; Wilson, 1975). ecological specializations. Studies of variation in wing However, it often remains unclear how speci®c eco- morphology have shown it to be closely associated with logical and morphological specializations may affect feeding specializations and community structuring group formation and population structure. (Fenton, 1972; Aldridge & Rautenbach, 1987; Findley, In general, the social and population structure of bats 1993). Furthermore, a relationship between wing shape is not well known. Most of our knowledge of vespertil- (aspect ratio) and foraging range (Jones, Duverge & ionid behaviour is based upon a few well-studied species Ransome, 1995) leads to a prediction that wing such as Pipistrellus pipistrellus and Myotis lucifugus. morphology may affect the dispersal abilities of bats, Overall, the family is ecologically and behaviourally with implications for group formation and distribution diverse (Bradbury, 1977; Kunz, 1982), with a wide range of individual species. It is predicted that wing morphology may have further implications for both social and population structure. *All correspondence to: Dr Abigail Entwistle, Fauna & Flora International, Great Eastern House, Tenison Road, Cambridge In this paper we examine population structure, group CB1 2DT, U.K. E-mail: [email protected] size and composition in the brown long-eared bat 12 A. C. Entwistle, P. A. Racey and J. R. Speakman

Plecotus auritus, L., which differs in both morphology Assessment of colony size and feeding behaviour from most other vespertilionid bat species. This species displays related morphological Previous attempts at determining colony size from and ecological specializations: distinctive short broad emergence counts for this species proved unsuccessful wings and long ears, coupled with low intensity echo- given the low light intensity at the time of emergence. location calls, used to glean prey (predominantly moths) Instead, the number of bats using each roost was directly from foliage (Anderson & Racey, 1991). Flight assessed in 3 ways: is slow, but manoeuvrable, as a result of low wing (1) An average of the number of bats seen in the attic aspect ratio and low wing loading (Norberg, 1976). The on different visits (average colony count), which is relatively short foraging range described in P. auritus comparable between roosts and independent of effort. (Entwistle, Racey & Speakman, 1996) is consistent with (2) The `minimum number alive' (MNA) (Krebs, 1989) lower ranges associated with species with such wing in a given year was calculated from ringing records, and morphology (Jones et al., 1995). In Britain P. auritus can be considered as the lower limit of population size roosts mostly within the attics of houses, which appear (Montgomery, 1987). to be selected on the basis of a suite of characteristics, (3) The Jolly±Seber method (Seber, 1982) was used to including woodland availability, attic structure and provide an upper population estimate which includes an temperature (Entwistle et al., 1997). However, there is estimate of the individuals that might have evaded surprisingly little detailed information about the occu- capture. In this study all assumptions inherent in the pancy of roost sites by this species, social organization Jolly±Seber method were considered to be ful®lled (see of colonies or population structure (but see Burland also Boyd & Stebbings, 1989). et al., in press). The present study examines several components of social organization and population structure in this Interspeci®c comparisons of wing morphology and species. Furthermore, since P. auritus has an unusual behaviour wing morphology (Norberg, 1976), it provides a useful model to examine how morphology and ecological Relationships between wing morphology and both specializations may be linked to social behaviour and colony size and migratory abilities, for British bat population structure. species, were examined using stepwise regressions. Data were collated on maximum colony sizes from the available literature (Greenaway & Hutson, 1990; MATERIALS AND METHODS Nowak, 1994). Classi®cations of migratory and sedentary species among European bats were taken from A ringing programme was conducted in north-east Strelkov (1969). Interspeci®c comparisons were made Scotland between 1978 and 1989, under licence from the between these data and corresponding measures of statutory nature conservation authorities. Between 1991 morphology (mass, wingspan, ear length, aspect ratio and 1993 this study was extended with a more intensive and wing loading) for each species (from Norberg & ringing schedule, when roosts were checked up to 5 Rayner, 1987). times each summer (mean number of visits = 2.2 per roost each year). Efforts were made to identify all roosts in the study area (an area c. 50 by 20 km), and localities RESULTS with a high concentration of roosts were intensively surveyed, so that all extant roosts could be identi®ed. A Roost occupancy total of 30 roosts in buildings was studied, and the distance between these structures ranged from 100 m to All captures took place between April and October, 40 km, although 8 roosts were located within 4 km of with few individuals found after the beginning of each other. October (average = 5 individuals). Across all 30 roosts, Bats were caught either by hand or with a hand net. bats were present on 65% of visits between 1991 and The total number of bats counted on each visit was 1993 (n = 195). The likelihood of bats being located was recorded, including those that were seen but could not not related to the number of visits made to the roost 2 be captured. Information collected from each individual (F1,11 = 0.03, r < 0.01, n = 12, NS). Bats frequently captured included: sex, adult or juvenile (based upon changed roosting position within the roost site through the epiphyseal gap; Anthony, 1988), and reproductive the course of the summer, although movements maturity and status (Racey, 1974; Entwistle et al., appeared unrelated to the timings of capture. 1998). Bats were marked using 3.0 mm (closed internal diameter) aluminium rings (Mammal Society, London), bearing an individual code. A small proportion of bats Ringing and site ®delity (n = 68) were double ringed to assess ring loss (estimated as < 3%). Juveniles were not ringed until the epiphyses Between 1978 and 1993, 2206 bats were caught. Of had fused, and overall there was minimal incidence of these, 1365 bats were ®rst captures which were subse- damage to bats from the rings. quently ringed, 121 were released without ringing and Social structure in the brown long-eared bat 13

Table 1. The numbers of recaptures made after different time and Jolly±Seber were highly correlated with the average intervals, with percentage of total recaptures of adult bats of colony counts across the 12 roosts (regression equation each sex given in parentheses (data from 1978±93) for MNA estimate = 2.35 (colony count) 710.6, r2 = 0.7, Years between captures Females Males F1,11 = 28.3, n =12, P < 0.001; regression equation for Jolly±Seber estimate = 3.21 (colony count) 75.4; 2 <1 94 (26%) 107 (30%) r = 0.6, F1,11 = 17.4, n = 12, P < 0.005). 1 142 (40%) 178 (49%) 2 37 (10%) 78 (7%) 3 11 (3%) 22 (6%) 4 17 (5%) 7 (2%) Colony composition 5 20 (6%) 8 (2%) 6 22 (6%) 4 (1%) Across all bats ringed in all years, 41% of those captured 7 10 (3%) 4 (1%) were male, which differs signi®cantly from a sex ratio of 8 0 ± 2 (1%) unity (w2 = 19.10, n = 1164, d.f. = 1, P < 0.001). How- 9 4 (1%) 4 (1%) ever, the juvenile sex ratio (53% male) did not differ signi®cantly from unity (w2 = 0.12, n = 201, d.f. = 1, NS). Colony composition changed during summer; early in the year the colonies consisted mainly of females, but 720 were recaptured individuals which had previously thereafter the number of males in the colonies increased been marked. The proportion of bats caught which were to a peak after the young were weaned. Over this period already ringed increased progressively between 1991 and the adult sex ratio (expressed as percentage male) 2 1993. Most recaptures (70%) were made within 1 year of increased signi®cantly (F1, 9 = 26.3; r = 0.76; P < 0.001; initial capture and ringing, while the intervals between Fig. 1). Males mixed freely with the females with no successive captures overall (including further recaptures) evidence of sexual segregation in roosting positions, or ranged from a month to 12 years (Table 1). Data from sub-structuring of the colony, during summer. 1991±92 and 1992±93 allowed the proportion of males and females captured in 1 year and recaptured in the following year to be calculated at the 12 most intensively Juvenile recruitment studied roosts. Over these years, 39% of females re- turned the following year, compared to 48% of males Juvenile recruitment was assessed from the number of (w2 = 3.99, n = 413, d.f. = 1, P < 0.05). males and females ringed whilst immature, which were Both males and females had long-term associations subsequently recaptured after at least 1 year. Overall, 22 with the roost site where they were originally ringed. females and 10 males were recaptured at their natal Individuals of both sexes were recaptured on multiple roost at least 1 year after birth. Recapture rates were occasions at the same roost site, and were present over a not signi®cantly different between the sexes (females period of years; for example, two males were captured 0.31 (22/71); males 0.19 (10/52); w2 = 2.16, n = 123, in every year of study for 7 consecutive years (1986±93). d.f. = 1, NS). Juveniles were not recaptured in any other Movements between summer roost sites were recorded roost site, even adjacent roosts, except on one occasion on only ®ve occasions from all bats recaptured between following disturbance of the natal roost. 1978 and 1993. This represents 0.7% of recaptures during the study. Of these movements, four males and one female were recaptured in neighbouring roosts, between 150 m and 280 m distant from the original 0.8 sites. y = 0.0035x 7–125.31125.31 22 0.7 r == 0.7558

Colony size 0.6

Across all roosts and all visits where bats were present, 0.5 the total number of bats seen ranged from one to 74, 0.4 although typical colony counts were between 10 and 20 individuals (mean 1991±93 = 12.0, se = 0.9, n = 140). The 0.3 mean of mean colony sizes from 12 intensively studied roosts was 16.1 (se = 1.8; range from 5.0 to 28.9). Proportion of males in colony 0.2 MNA population estimates for bats from the 12 roosts in the ®nal year for which data were available 0.1 lllllllll (1992, or 1991 for two roosts where no data from 1992 5 May 25 May 14 Jun 4 Jul 24 Jul 13 Aug 2 Sep 22 Sep 12 Oct were available as a result of low captures) ranged from Date ®ve to 70 (mean = 30.1, se = 5.4) and Jolly±Seber esti- Fig. 1. The proportion of adult males present in colonies of mates ranged between four and 88 (mean = 46.2, P. auritus throughout summer (data combined from 3 years, se = 8.1). Estimates of population size using both MNA 1991±93). 14 A. C. Entwistle, P. A. Racey and J. R. Speakman

1100 reported in Germany (Heise & Schmidt, 1988), and we 1000 yy == 401.13x401.13x7 –2282.92282.9 suggest that these may be analogous to shifts in roosting rr22 == 0.65040.6504 900 position within a single complex roost site (e.g. Licht & Leitner, 1967; Valenciuc, 1989). Regular changes in 800 roosting position were observed within the roost sites in 700 the present study, which may re¯ect selection of optimal 600 thermal conditions. Such changes in roost position, 500 involving withdrawal of the bats into tight cavities 400 inaccessible to researchers, may also explain the appar-

Maximum colony size 300 ent absence of the colony on some occasions 200 (Stebbings,1966). 100

0 ll l l lll 5.5 6 6.5 7 7.5 8 8.5 Colony size Aspect ratio Fig. 2. Relationship between aspect ratio and colony size The results from the mark±recapture analysis suggest across 13 British bat species. that previous population estimates, in the same study area, which were based solely on within-roost counts (Speakman et al., 1991) have substantially under- Interspeci®c comparisons estimated colony size for this species, since only a sample of the whole colony using the roost is visible on Comparison of maximum colony size of 13 British bat any visit. Taking the minimum number alive as a species with corresponding data on their wing mor- reliable minimum estimate, population sizes may be phology demonstrated a signi®cant positive relationship nearly twice that previously assumed, being nearer 30 between colony size and aspect ratio (F1,12 = 23.1, than 15 (as estimated by Speakman et al., 1991). Jolly± r2 = 0.65, P < 0.001; Fig. 2), but not with any of the Seber estimates indicate the possible upper boundary of other four morphological characteristics tested. The colony size (up to three times previous estimates, at same relationship is found through use of non- nearer 50 individuals). However, the signi®cant correla- parametric statistics (F = 6.8, rs = 0.62, P < 0.05). tion between average colony count and mark±recapture Comparison of the wing morphologies of different estimates suggests that colony counts produce satis- European bat species, which had been classi®ed as factory data on relative colony sizes, and may be used to migratory or sedentary by Strelkov (1969), demon- predict actual colony size. strated a signi®cant difference in aspect ratio between Even taking into account the higher estimates from these groups (mean aspect ratio (sedentary) = 6.2, mark±recapture, colony size in P. auritus is still much sd= 0.4, n = 9; mean aspect ratio (migratory) = 7.4, smaller than some sympatric bat species such as Pipis- sd= 0.3, n =5;t = 6.2, d.f. = 9, P = 0.0001), but no differ- trellus pipistrellus (average colony count in the same ences in other morphological characteristics tested. region 117 bats; Speakman et al., 1991). The variation Species with low aspect ratios (< 7.0), including in group sizes found among the Chiroptera has been P. auritus were all classi®ed as sedentary, while species explained by such factors as mating systems (e.g. with larger aspect ratios (> 7.0) were all classed as Bradbury, 1977), roost types used and roost availability, migratory. climate (affecting relative bene®ts of clustering) and food distribution (Bradbury & Vehrencamp, 1976). The availability of resources is obviously an impor- DISCUSSION tant factor limiting group size (Alexander, 1974), and this will be affected not only by the area or amount of Roost occupancy resource available, but also by the ability of the species to exploit it. In particular, foraging dispersal is likely to Plecotus auritus is highly selective of the sites in which it affect the overall area of foraging habitat available to roosts (Entwistle et al., 1997). High rates of occupancy bats occupying a central roost. Thus, greater ¯ight during summer in the present study (67%), indicate that distances are likely to reduce the effects of local compe- most summer activity was associated with these speci®c tition, and increase the effective foraging range for the roost sites, and both within- and between-year ®delity to colony (e.g. Hamilton & Watt, 1970), whereas restricted roost sites was high. Supporting evidence for day-to-day dispersal may limit colony size, by restricting the area of individual roost ®delity was provided by a parallel resources available to animals dispersing from a single radio-tracking study (Entwistle, 1994). In general, tem- point. We suggest that colony size generally re¯ects the perate zone bats appear sensitive to environmental differential ¯ight capacities, and foraging ranges, across conditions which in¯uence food sources, and change species. This is supported by the strong positive relation- roost as a means of behavioural thermoregulation ship between aspect ratio and colony size (Fig. 2), since (Audet, 1990). Frequent shifts by P. auritus between aspect ratio has previously been shown to be strongly roost boxes within a restricted `colony area' have been correlated with foraging distance (Jones et al., 1995). Social structure in the brown long-eared bat 15

Plecotus auritus has a restricted foraging range Table 2. The sex ratio during summer (expressed as percentage (< 1 km from roost, Entwistle et al., 1996), which has males) recorded in various studies at different latitudes been attributed to its slow ¯ight ± a consequence of the Latitude (8N) Sex ratio (%) Reference wing shape and wing loading found in species adapted to gleaning (Norberg, 1976). Furthermore, there is a 57.1 44 This study clear correlation between the availability of foraging 53.3 34 Heise & Schmidt, 1988 habitat within this range and colony size between 52.7 29 O'Gorman & Fairley, 1965 different roosts (Entwistle, 1994). We suggest that the 52.4 38 Boyd & Stebbings, 1989 52.3 20 Heise & Schmidt, 1988 relatively small colony size in this species re¯ects its 50.6 33 Stebbings, 1976 wing morphology and foraging dispersal, as a result of 40.9 10 Benzal, 1991 reduced effective foraging range, and consequently greater local intraspeci®c competition.

explained by constraints linked to intrasexual competi- Colony composition tion (for mating opportunities, usually between males in mammals) and intersexual competition (for access to Previously, matrilinear recruitment has been described resources; Greenwood, 1980). within colonies of P. auritus, with females returning to In P. auritus there is little evidence of direct intra- their natal roost (Heise & Schmidt, 1988). In the present sexual competition (Entwistle, 1994; Park, Masters & study there was limited evidence of equal recruitment Altringham, 1998), unlike P. pipistrellus (Lundberg & from both sexes, but it was unclear whether generally Gerell, 1986; Park et al., 1998). This may re¯ect reduced low return rates indicated signi®cant juvenile mortality, bene®ts of autumn mate defence when inseminations or unrecorded dispersal. The recovery of several males continue during hibernation (Strelkov, 1962) in the at their natal roost after a year (after sexual maturity absence of a vaginal plug. In addition, we suggest that had been achieved) and long-term associations of adult the highly restricted foraging areas used by females of males with colonies, would admit the possibility of this species may enable males to use separate, more within-colony matings and kin mating. distant foraging areas (Entwistle et al., 1996) while In the present study both females and males showed a avoiding intersexual competition for resources. Males high level of ®delity to particular roosts within and may accrue additional bene®ts from sharing a roost between years, as inferred in other studies. This con- with females, which may outweigh any competitive trasts markedly with a study of P. auritus carried out in disadvantages. For example, higher temperatures may Germany, where adult males were vagrant, associating facilitate euthermy during spermatogenesis (Kurta & with different colonies from year to year (Heise & Kunz, 1988; Entwistle et al., 1998). The greater associ- Schmidt, 1988). Furthermore, in the present study the ation of P. auritus males with colonies in northern proportion of males recorded in colonies was even latitudes suggests that this behaviour may indeed be higher than previously described for this species (Table related to thermal conditions. 2). Indeed a signi®cant relationship between latitude and the sex ratio of P. auritus is clear from these data 2 (linear regression, F1,6 = 13.1, r = 0.7, n =7, P < 0.02), Population structure with a higher proportion of males associated with maternity colonies at higher latitudes. This relationship In the present study individuals showed long-term could not be explained by differences in the time of year associations with a particular roost site, and used it at which colonies were examined. Instead, it may indi- exclusively, with few movements recorded to neigh- cate that some environmental, perhaps climatic, factor bouring roosts. This suggests that bats do not use roosts in¯uences coloniality in males. In addition, such intra- indiscriminately, but exhibit strong philopatry to par- speci®c variations between studies indicate that social ticular sites over a long period of time. It seems unlikely behaviour of this species is not ®xed, but may vary that the low numbers of intercolonial movements were geographically or temporally (Emlen & Oring, 1977). simply a re¯ection of the use of undocumented roosts, This emphasizes the need for caution in characterizing given the extent of knowledge of roost sites within the the social system of this and other bat species which are area. Instead, the minimal intercolony interchanges distributed over a wide geographical range. indicated that, at least during summer, the colonies at The absence of sexual segregation in P. auritus is different roosts represented discrete groups. The long- clearly anomalous when compared to most other term use of roosts coupled with longevity in this species vespertilionids studied to date (Bradbury, 1977). For (up to 30 years; Lehmann, Jenni & Maumary, 1992) example, in sympatric populations of P. pipistrellus > suggest that roosts can be considered as traditional sites 98% of individuals in colonies were female (Speakman that may be used by a colony over several decades. et al., 1991), while male pipistrelles tend to occur alone A distribution of individuals in discrete colonies with or in small groups during summer (Stebbings, 1968). minimal interchange to spatially close roosts represents Sexual segregation in mammals, such as that displayed a metapopulation model (Hanski & Gilpin, 1997). Such by most temperate zone vespertilionids, is usually a distribution of individuals may have implications for 16 A. C. Entwistle, P. A. Racey and J. R. Speakman population structure and for gene ¯ow, and free mixing enable further comparisons to be made between these of individuals (i.e. panmixia) would be unlikely under parameters in sympatric species. such conditions. However, it is not clear whether the We suggest that fundamental variations in foraging population structure during summer bears any relation specializations (such as gleaning vs high altitude aerial to the distribution of individuals during the mating foraging) and consequent morphological specializa- season (autumn and winter), and hence re¯ects gene tion may underlie some of the observed differences ¯ow between colonies. in colony organization and population structure within The genetic structure of this species is likely to be the Chiroptera. However, these relationships may be affected not only by its high roost philopatry and further complicated by phylogeny, as well as by local limited dispersal in summer, but also by the lack of any factors such as the availability of foraging habitat, the evidence of migration at any point during the year type and availability of roosts, and climatic or other (Strelkov, 1969). Indeed, in the U.K. it has been environmental factors. suggested that P. auritus may use the same roost year round (Hutson, 1987). Such low dispersal is likely to restrict the mixing of individual P. auritus from different Acknowledgements colonies across more than a local scale, and some degree of genetic structure in the population might be expected We acknowledge the help and hospitality of all house- (such as isolation by distance). This hypothesis is sup- holders who allowed us access to bat roosts within their ported by microsatellite analysis (Burland et al., 1999). homes. We thank Tamsin Burland and two anonymous However, the relative lack of genetic differentiation referees for their comments. This work was carried out indicates greater mixing between colonies during the under licence from Scottish Natural Heritage. ACE was mating season than would be expected given the popula- supported by a NERC studentship. tion structure observed in summer (Burland et al., 1999). 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