Social and population structure of a gleaning bat, Plecotus auritus

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

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

3 Social structure in the brown long-eared bat 13 Table 1. The numbers of recaptures made after different time intervals, with percentage of total recaptures of adult bats of each sex given in parentheses (data from 1978±93) Years between captures Females Males <1 94 (26%) 107 (30%) (40%) 178 (49%) 2 37 (10%) 78 (7%) 3 11 (3%) 22 (6%) 4 17 (5%) 7 (2%) 5 20 (6%) 8 (2%) 6 22 (6%) 4 (1%) 7 10 (3%) 4 (1%) 8 0 ± 2 (1%) 9 4 (1%) 4 (1%) 720 were recaptured individuals which had previously been marked. The proportion of bats caught which were already ringed increased progressively between 1991 and Most recaptures (70%) were made within 1 year of initial capture and ringing, while the intervals between successive captures overall (including further recaptures) ranged from a month to 12 years (Table 1). Data from 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 studied roosts. Over these years, 39% of females returned the following year, compared to 48% of males (w 2 = 3.99, n = 413, d.f. = 1, P < 0.05). Both males and females had long-term associations with the roost site where they were originally ringed. Individuals of both sexes were recaptured on multiple occasions at the same roost site, and were present over a period of years; for example, two males were captured in every year of study for 7 consecutive years (1986±93). Movements between summer roost sites were recorded on only ve occasions from all bats recaptured between 1978 and 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 sites. Colony size Across all roosts and all visits where bats were present, the total number of bats seen ranged from one to 74, although typical colony counts were between 10 and 20 individuals (mean 1991±93 = 12.0, se = 0.9, n = 140). The mean of mean colony sizes from 12 intensively studied roosts was 16.1 (se = 1.8; range from 5.0 to 28.9). MNA population estimates for bats from the 12 roosts in the nal year for which data were available (1992, or 1991 for two roosts where no data from 1992 were available as a result of low captures) ranged from ve to 70 (mean = 30.1, se = 5.4) and Jolly±Seber estimates ranged between four and 88 (mean = 46.2, se = 8.1). Estimates of population size using both MNA and Jolly±Seber were highly correlated with the average colony counts across the 12 roosts (regression equation for MNA estimate = 2.35 (colony count) 710.6, r 2 = 0.7, F 1,11 = 28.3, n =12, P < 0.001; regression equation for Jolly±Seber estimate = 3.21 (colony count) 75.4; r 2 = 0.6, F 1,11 = 17.4, n = 12, P < 0.005). Colony composition Across all bats ringed in all years, 41% of those captured were male, which differs signi cantly from a sex ratio of unity (w 2 = 19.10, n = 1164, d.f. = 1, P < 0.001). However, the juvenile sex ratio (53% male) did not differ signi cantly from unity (w 2 = 0.12, n = 201, d.f. = 1, NS). Colony composition changed during summer; early in the year the colonies consisted mainly of females, but thereafter the number of males in the colonies increased to a peak after the young were weaned. Over this period the adult sex ratio (expressed as percentage male) increased signi cantly (F 1, 9 = 26.3; r 2 = 0.76; P < 0.001; Fig. 1). Males mixed freely with the females with no evidence of sexual segregation in roosting positions, or sub-structuring of the colony, during summer. Juvenile recruitment Juvenile recruitment was assessed from the number of males and females ringed whilst immature, which were subsequently recaptured after at least 1 year. Overall, 22 females and 10 males were recaptured at their natal roost at least 1 year after birth. Recapture rates were not signi cantly different between the sexes (females 0.31 (22/71); males 0.19 (10/52); w 2 = 2.16, n = 123, d.f. = 1, NS). Juveniles were not recaptured in any other roost site, even adjacent roosts, except on one occasion following disturbance of the natal roost. Proportion of males in colony y = x r 2 = l l l l l l l l l 5 May 25 May 14 Jun 4 Jul 24 Jul 13 Aug 2 Sep 22 Sep 12 Oct Date Fig. 1. The proportion of adult males present in colonies of P. auritus throughout summer (data combined from 3 years, 1991±93).

4 14 A. C. Entwistle, P. A. Racey and J. R. Speakman Maximum colony size Interspeci c comparisons Comparison of maximum colony size of 13 British bat species with corresponding data on their wing morphology demonstrated a signi cant positive relationship between colony size and aspect ratio (F 1,12 = 23.1, r 2 = 0.65, P < 0.001; Fig. 2), but not with any of the other four morphological characteristics tested. The same relationship is found through use of nonparametric statistics (F = 6.8, r s = 0.62, P < 0.05). Comparison of the wing morphologies of different European bat species, which had been classi ed as migratory or sedentary by Strelkov (1969), demonstrated a signi cant difference in aspect ratio between these groups (mean aspect ratio (sedentary) = 6.2, sd= 0.4, n = 9; mean aspect ratio (migratory) = 7.4, sd= 0.3, n =5;t = 6.2, d.f. = 9, P = ), but no differences in other morphological characteristics tested. Species with low aspect ratios (< 7.0), including P. auritus were all classi ed as sedentary, while species with larger aspect ratios (> 7.0) were all classed as migratory. DISCUSSION Roost occupancy y = x r 2 r = l l l l l l l Aspect ratio Fig. 2. Relationship between aspect ratio and colony size across 13 British bat species. Plecotus auritus is highly selective of the sites in which it roosts (Entwistle et al., 1997). High rates of occupancy during summer in the present study (67%), indicate that most summer activity was associated with these speci c roost sites, and both within- and between-year delity to roost sites was high. Supporting evidence for day-to-day individual roost delity was provided by a parallel radio-tracking study (Entwistle, 1994). In general, temperate zone bats appear sensitive to environmental conditions which in uence food sources, and change roost as a means of behavioural thermoregulation (Audet, 1990). Frequent shifts by P. auritus between roost boxes within a restricted `colony area' have been reported in Germany (Heise & Schmidt, 1988), and we suggest that these may be analogous to shifts in roosting position within a single complex roost site (e.g. Licht & Leitner, 1967; Valenciuc, 1989). Regular changes in roosting position were observed within the roost sites in the present study, which may re ect selection of optimal thermal conditions. Such changes in roost position, involving withdrawal of the bats into tight cavities inaccessible to researchers, may also explain the apparent absence of the colony on some occasions (Stebbings,1966). Colony size The results from the mark±recapture analysis suggest that previous population estimates, in the same study area, which were based solely on within-roost counts (Speakman et al., 1991) have substantially underestimated colony size for this species, since only a sample of the whole colony using the roost is visible on any visit. Taking the minimum number alive as a reliable minimum estimate, population sizes may be nearly twice that previously assumed, being nearer 30 than 15 (as estimated by Speakman et al., 1991). Jolly± Seber estimates indicate the possible upper boundary of colony size (up to three times previous estimates, at nearer 50 individuals). However, the signi cant correlation between average colony count and mark±recapture estimates suggests that colony counts produce satisfactory data on relative colony sizes, and may be used to predict actual colony size. Even taking into account the higher estimates from mark±recapture, colony size in P. auritus is still much smaller than some sympatric bat species such as Pipistrellus pipistrellus (average colony count in the same region 117 bats; Speakman et al., 1991). The variation in group sizes found among the Chiroptera has been explained by such factors as mating systems (e.g. Bradbury, 1977), roost types used and roost availability, climate (affecting relative bene ts of clustering) and food distribution (Bradbury & Vehrencamp, 1976). The availability of resources is obviously an important factor limiting group size (Alexander, 1974), and this will be affected not only by the area or amount of resource available, but also by the ability of the species to exploit it. In particular, foraging dispersal is likely to affect the overall area of foraging habitat available to bats occupying a central roost. Thus, greater ight distances are likely to reduce the effects of local competition, and increase the effective foraging range for the colony (e.g. Hamilton & Watt, 1970), whereas restricted dispersal may limit colony size, by restricting the area of resources available to animals dispersing from a single point. We suggest that colony size generally re ects the differential ight capacities, and foraging ranges, across species. This is supported by the strong positive relationship between aspect ratio and colony size (Fig. 2), since aspect ratio has previously been shown to be strongly correlated with foraging distance (Jones et al., 1995).

5 Social structure in the brown long-eared bat 15 Plecotus auritus has a restricted foraging range (< 1 km from roost, Entwistle et al., 1996), which has been attributed to its slow ight ± a consequence of the wing shape and wing loading found in species adapted to gleaning (Norberg, 1976). Furthermore, there is a clear correlation between the availability of foraging habitat within this range and colony size between different roosts (Entwistle, 1994). We suggest that the relatively small colony size in this species re ects its wing morphology and foraging dispersal, as a result of reduced effective foraging range, and consequently greater local intraspeci c competition. Colony composition Previously, matrilinear recruitment has been described within colonies of P. auritus, with females returning to their natal roost (Heise & Schmidt, 1988). In the present study there was limited evidence of equal recruitment from both sexes, but it was unclear whether generally low return rates indicated signi cant juvenile mortality, or unrecorded dispersal. The recovery of several males at their natal roost after a year (after sexual maturity had been achieved) and long-term associations of adult males with colonies, would admit the possibility of within-colony matings and kin mating. In the present study both females and males showed a high level of delity to particular roosts within and between years, as inferred in other studies. This contrasts markedly with a study of P. auritus carried out in Germany, where adult males were vagrant, associating with different colonies from year to year (Heise & Schmidt, 1988). Furthermore, in the present study the proportion of males recorded in colonies was even higher than previously described for this species (Table 2). Indeed a signi cant relationship between latitude and the sex ratio of P. auritus is clear from these data (linear regression, F 1,6 = 13.1, r 2 = 0.7, n =7, P < 0.02), with a higher proportion of males associated with maternity colonies at higher latitudes. This relationship could not be explained by differences in the time of year at which colonies were examined. Instead, it may indicate that some environmental, perhaps climatic, factor in uences coloniality in males. In addition, such intraspeci c variations between studies indicate that social behaviour of this species is not xed, but may vary geographically or temporally (Emlen & Oring, 1977). This emphasizes the need for caution in characterizing the social system of this and other bat species which are distributed over a wide geographical range. The absence of sexual segregation in P. auritus is clearly anomalous when compared to most other vespertilionids studied to date (Bradbury, 1977). For example, in sympatric populations of P. pipistrellus > 98% of individuals in colonies were female (Speakman et al., 1991), while male pipistrelles tend to occur alone or in small groups during summer (Stebbings, 1968). Sexual segregation in mammals, such as that displayed by most temperate zone vespertilionids, is usually Table 2. The sex ratio during summer (expressed as percentage males) recorded in various studies at different latitudes Latitude (8N) Sex ratio (%) Reference This study Heise & Schmidt, O'Gorman & Fairley, Boyd & Stebbings, Heise & Schmidt, Stebbings, Benzal, 1991 explained by constraints linked to intrasexual competition (for mating opportunities, usually between males in mammals) and intersexual competition (for access to resources; Greenwood, 1980). In P. auritus there is little evidence of direct intrasexual competition (Entwistle, 1994; Park, Masters & Altringham, 1998), unlike P. pipistrellus (Lundberg & Gerell, 1986; Park et al., 1998). This may re ect reduced bene ts of autumn mate defence when inseminations continue during hibernation (Strelkov, 1962) in the absence of a vaginal plug. In addition, we suggest that the highly restricted foraging areas used by females of this species may enable males to use separate, more distant foraging areas (Entwistle et al., 1996) while avoiding intersexual competition for resources. Males may accrue additional bene ts from sharing a roost with females, which may outweigh any competitive disadvantages. For example, higher temperatures may facilitate euthermy during spermatogenesis (Kurta & Kunz, 1988; Entwistle et al., 1998). The greater association of P. auritus males with colonies in northern latitudes suggests that this behaviour may indeed be related to thermal conditions. Population structure In the present study individuals showed long-term associations with a particular roost site, and used it exclusively, with few movements recorded to neighbouring roosts. This suggests that bats do not use roosts indiscriminately, but exhibit strong philopatry to particular sites over a long period of time. It seems unlikely that the low numbers of intercolonial movements were simply a re ection of the use of undocumented roosts, given the extent of knowledge of roost sites within the area. Instead, the minimal intercolony interchanges indicated that, at least during summer, the colonies at different roosts represented discrete groups. The longterm use of roosts coupled with longevity in this species (up to 30 years; Lehmann, Jenni & Maumary, 1992) suggest that roosts can be considered as traditional sites that may be used by a colony over several decades. A distribution of individuals in discrete colonies with minimal interchange to spatially close roosts represents a metapopulation model (Hanski & Gilpin, 1997). Such a distribution of individuals may have implications for

6 16 A. C. Entwistle, P. A. Racey and J. R. Speakman population structure and for gene ow, and free mixing of individuals (i.e. panmixia) would be unlikely under such conditions. However, it is not clear whether the population structure during summer bears any relation to the distribution of individuals during the mating season (autumn and winter), and hence re ects gene ow between colonies. The genetic structure of this species is likely to be affected not only by its high roost philopatry and limited dispersal in summer, but also by the lack of any evidence of migration at any point during the year (Strelkov, 1969). Indeed, in the U.K. it has been 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 colonies across more than a local scale, and some degree of genetic structure in the population might be expected (such as isolation by distance). This hypothesis is supported by microsatellite analysis (Burland et al., 1999). However, the relative lack of genetic differentiation indicates greater mixing between colonies during the mating season than would be expected given the population structure observed in summer (Burland et al., 1999). Both foraging range and migratory patterns are correlated with wing aspect ratio (Jones et al., 1995; this study), and the limited distances travelled (and lack of extensive intercolony exchange) reported in P. auritus are consistent with expectations based upon wing morphology and consequent ight characteristics of this species. The applicability of relationships between wing morphology and dispersal range to the colony size and population structure of other bat faunas still requires examination. However, we predict that species with slow, manoeuvrable, ight which are specialized as gleaners will be more likely to form small groups, with some degree of population structuring, when compared to species specialized for long-range aerial foraging. This can be illustrated by comparing the ight capabilities and ecological specializations of P. auritus (aspect ratio 5.7, ight speed 1.9±2.7 m/s; Norberg, 1976) to those of Tadarida brasiliensis ± one of the few species with similar data on population structure across a regional scale, and species with very different wing morphology (aspect ratio 8.2; Norberg & Rayner, 1987). Tadarida brasilensis is a fast- ying aerial forager ( ight speed c. 11 m/s; Williams, Ireland & Williams, 1973) which undertakes extensive nightly dispersal from its roosts (65 km; Barbour & Davis, 1969), makes long migratory journeys (up to 1600 km; Cockrum, 1969), and forms extensive colonies (thousands, sometimes millions of individuals; Davis, Herreid & Short, 1962). As might be predicted from differences in their relative motility, studies of T. brasiliensis depict genetically panmictic populations (Svoboda, Choate & Chesser, 1985; McCracken, McCracken & Vawter, 1994), in contrast to the population structuring inferred in P. auritus (this paper, Burland et al., 1999). While this is a single illustrative example, it is hoped that further genetic and ecological studies of European bats will enable further comparisons to be made between these parameters in sympatric species. 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