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Bats Swarm Where They Hibernate: Compositional Similarity Between Autumn Swarming and Winter Hibernation Assemblages at Five Underground Sites

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Bats Swarm Where They Hibernate: Compositional Similarity Between Autumn Swarming and Winter Hibernation Assemblages at Five Underground Sites RESEARCH ARTICLE Bats Swarm Where They Hibernate: Compositional Similarity between Autumn Swarming and Winter Hibernation Assemblages at Five Underground Sites Jaap van Schaik1*, René Janssen2, Thijs Bosch3, Anne-Jifke Haarsma4, Jasja J. A. Dekker5¤, Bart Kranstauber6,7 a11111 1 Department of Behavioural Ecology and Evolutionary Genetics, Max Planck Institute for Ornithology, Eberhard-Gwinner-Strasse, 82319, Seewiesen, Germany, 2 Bionet Natuuronderzoek, Valderstraat 39, 6171EL, Stein, The Netherlands, 3 Ad Hoc Zoogdieronderzoek, Oude Velperweg 34, 6824HE, Arnhem, The Netherlands, 4 Animal Ecology & Ecophysiology group, Institute for Water and Wetland Research, Radboud University Nijmegen, P.O. Box 9010, 6500GL, Nijmegen, The Netherlands, 5 Dutch Mammal Society, P.O. Box 6531, 6503GA, Nijmegen, The Netherlands, 6 Department of Migration and Immuno-ecology, Max Planck Institute for Ornithology, Am Obstberg 1, 78315, Radolfzell, Germany, 7 University of Konstanz, Department of Biology, Konstanz, Germany OPEN ACCESS ¤ Current address: Jasja Dekker Dierecologie, Enkhuizenstraat 26, 6843, WZ, Arnhem, The Netherlands * Citation: van Schaik J, Janssen R, Bosch T, [email protected] Haarsma A-J, Dekker JJA, Kranstauber B (2015) Bats Swarm Where They Hibernate: Compositional Similarity between Autumn Swarming and Winter Hibernation Assemblages at Five Underground Sites. Abstract PLoS ONE 10(7): e0130850. doi:10.1371/journal. During autumn in the temperate zone of both the new and old world, bats of many species pone.0130850 assemble at underground sites in a behaviour known as swarming. Autumn swarming Editor: Brock Fenton, University of Western Ontario, behaviour is thought to primarily serve as a promiscuous mating system, but may also be CANADA related to the localization and assessment of hibernacula. Bats subsequently make use of Received: March 17, 2015 the same underground sites during winter hibernation, however it is currently unknown if the Accepted: May 25, 2015 assemblages that make use of a site are comparable across swarming and hibernation sea- Published: July 8, 2015 sons. Our purpose was to characterize the bat assemblages found at five underground Copyright: © 2015 van Schaik et al. This is an open sites during both the swarming and the hibernation season and compare the assemblages access article distributed under the terms of the found during the two seasons both across sites and within species. We found that the rela- Creative Commons Attribution License, which permits tive abundance of individual species per site, as well as the relative proportion of a species unrestricted use, distribution, and reproduction in any that makes use of each site, were both significantly correlated between the swarming and medium, provided the original author and source are credited. hibernation seasons. These results suggest that swarming may indeed play a role in the localization of suitable hibernation sites. Additionally, these findings have important conser- Data Availability Statement: All relevant data regarding swarming captures are within the paper. vation implications, as this correlation can be used to improve monitoring of underground Winter count data are owned by the Dutch Mammal sites and predict the importance of certain sites for rare and cryptic bat species. Society and due to ethical restrictions are available upon request from Maurice La Haye, e-mail: [email protected], mail: Postbus 6531, 6503 GA, Nijmegen. Funding: This project was funded by a grant from Introduction the province of Limburg (Landschap in Uitvoering). Bionet Natuuronderzoek and Ad Hoc Between August and October many temperate-zone bat species in both the new and old world Zoogdieronderzoek provided support in the form of gather at underground sites in a behaviour known as swarming [1]. The assembled bats display PLOS ONE | DOI:10.1371/journal.pone.0130850 July 8, 2015 1/12 Compositional Similarity in Bat Swarming and Hibernation Assemblages salaries for authors RJ and TB respectively, but did intense flight activity, circling in and around the entrance of the site throughout the night, but not have any additional role in the study design, data predominantly do not roost there during the day [2]. Swarming activity is largely limited to collection and analysis, decision to publish, or species that make use of underground sites seasonally, hibernating there in winter but roosting preparation of the manuscript. The specific roles of these authors are articulated in the ‘author elsewhere in summer [3]. Many behavioural and genetic studies have shown that swarming contributions’ section. acts as a promiscuous mating behaviour, facilitating gene flow between otherwise isolated sum- mer colonies (eg. [4, 5, 6]). In addition, its occurrence at underground sites has often led to the Competing Interests: The authors have declared that no competing interests exist. suggestion that swarming also plays an important role in the assessment of the suitability of a hibernaculum [1, 7, 8] and/or the social transfer of information regarding its location [9]. Within the swarming season there is considerable variation in the timing of swarming activ- ity among species, as well as local variation in timing based on altitude [10, 11] and latitude [12, 13]. However, the general pattern is similar for all species. The assemblage of bats is strongly male-biased, with observed sex ratios of around 4:1 [11, 12, 14], and male bats roost closer to the site than females [15]. Genetic analysis has shown that females from multiple colo- nies make use of a swarming site, both throughout the swarming season and on individual nights [eg. 4]. In Myotis nattereri, it has been shown that females from a single colony attend multiple swarming sites, with most individuals swarming at the nearest site [14]. Ringing stud- ies suggest that individuals of both sexes display general site fidelity within and across years, being recaptured most often at the same site [16]. Similarly, individuals radio-tracked at swarming sites were never found to visit other sites [14, 17], although ringed individuals have been found at other sites [eg. 1]. Approximately one to two months after the peak swarming activity of a species, individuals return to underground sites to hibernate [3]. Whether bats have (species-specific) preferences for particular underground sites has been investigated both during swarming and hibernation seasons. Glover & Altringham [13] showed that swarming intensity was highest at underground sites with 1) extensive chamber develop- ment, 2) without hydrological activity, and 3) with a sheltered, horizontally oriented entrance. Randall and Broders [18] also found chamber length and development to be important, while also suggesting that stream length in the surrounding area positively influences swarming behaviour. Contrary to Glover and Altringham [13], Randall and Broders also found that shel- tered entrances negatively influenced swarming, although all sites in their study were consid- ered highly sheltered (21 of 25 were more than 75% sheltered). Finally, Johnson et al. [19] found that swarming bats preferred sites with a single isolated entrance, while also suggesting that a larger cave entrance size was important for several species. During hibernation, bats have similarly been shown to have preferences for certain sites and microclimates [20, 21]. Particularly, areas with adequate and stable humidity which reduce evaporative water loss appear to be critical [22, 23]. Additionally, broad genus and species-spe- cific preferences for temperature have been reported [24]. However, species are often found hibernating at a wide range of temperatures, and temperature preferences may also be sex and age specific [25], vary throughout the season [26–28], or vary depending on the amount of fat reserves possessed by individuals [29]. Moreover, several monitoring efforts have reported that bats frequently move within and between sites throughout the winter [21, 30], especially fol- lowing extreme weather changes, suggesting they may be flexible in relocating to more optimal conditions/locations [31, 32]. Several studies have made inferences as to whether individuals observed at a site during the swarming season are also found there during hibernation (eg. whether preferences for particu- lar swarming and hibernation sites are linked). Fenton [1] suggested that bats tended to hiber- nate where they had been caught during the swarming season. Likewise, Rivers et al.[14] suggested that at least a proportion of individuals remain at a site to hibernate and proposed that characterizing the swarming assemblage may be a suitable alternative for winter surveys, especially in the case of crevice-dwelling bats such as M. nattereri. More recently, Randall and PLOS ONE | DOI:10.1371/journal.pone.0130850 July 8, 2015 2/12 Compositional Similarity in Bat Swarming and Hibernation Assemblages Broders [18] explicitly made the assumption that sites used during swarming were likely to also be hibernacula. Conversely, in several studies no clear relation has been found between swarm- ing and hibernation assemblages suggesting that bats do not exclusively hibernate where they swarm [2, 7], whereas others found generally comparable assemblages but far fewer bats during the hibernation season suggesting that most bats do not use the same site in winter [33]. Finally, several studies investigating which site characteristics are important to swarming bats have concluded that their observations
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