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Extraordinary Range Expansion in a Common Bat: the Potential Roles of Climate Change and Urbanisation

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Extraordinary Range Expansion in a Common Bat: the Potential Roles of Climate Change and Urbanisation Sci Nat (2016) 103:15 DOI 10.1007/s00114-016-1334-7 ORIGINAL PAPER Extraordinary range expansion in a common bat: the potential roles of climate change and urbanisation L. Ancillotto1 & L. Santini2 & N. Ranc3,4 & L. Maiorano2 & D. Russo1,5 Received: 13 August 2015 /Revised: 27 December 2015 /Accepted: 13 January 2016 # Springer-Verlag Berlin Heidelberg 2016 Abstract Urbanisation and climate change are two global P. kuhlii and showed an increasing trend in the study period; change processes that affect animal distributions, posing crit- mean annual precipitation and precipitation seasonality were ical threats to biodiversity. Due to its versatile ecology and also relevant, but to a lower extent. Although urbanisation synurbic habits, Kuhl’s pipistrelle (Pipistrellus kuhlii)offers increased in recently colonised areas, it had little effect on a unique opportunity to explore the relative effects of climate the species’ presence predictability. P.kuhlii expanded its geo- change and urbanisation on species distributions. In a climate graphical range by about 394 % in the last four decades, a change scenario, this typically Mediterranean species is ex- process that can be interpreted as a response to climate pected to expand its range in response to increasing tempera- change. tures. We collected 25,132 high-resolution occurrence records from P. kuhlii European range between 1980 and 2013 and Keywords Chiroptera . Distribution . Global change . modelled the species’ distribution with a multi-temporal ap- Pipistrelle . Model proach, using three bioclimatic variables and one proxy of urbanisation. Temperature in the coldest quarter of the year was the most important factor predicting the presence of Introduction Communicated by: Fritz Geiser L. Ancillotto and L. Santini are co-first authors. Species distribution may change in response to a variety of factors that act at different spatial scales. Climate change and Electronic supplementary material The online version of this article (doi:10.1007/s00114-016-1334-7) contains supplementary material, land cover modifications are two major global change pro- which is available to authorized users. cesses affecting animal distributions worldwide, with critical implications for conservation (Jetz et al. 2007; Van Dyck * D. Russo 2012; Visconti et al. 2015). [email protected] Climate change is expected to impact heavily on European fauna in the near future, with significant loss of diversity— — 1 Wildlife Research Unit, Laboratorio di Ecologia Applicata, Sezione particularly in southern Europe that will not be offset by di Biologia e Protezione dei Sistemi Agrari e Forestali, Dipartimento species shifts, thus producing a continental biological homog- di Agraria, Università degli Studi di Napoli Federico II, via enisation. The same general trend is predicted for the Medi- Università 100, I-80055 Portici, Napoli, Italy terranean basin, with mammalian communities potentially be- 2 Dipartimento di Biologia e Biotecnologie BCharles Darwin^, ing deeply modified by extinctions and range shifts (Maiorano Università degli Studi di Roma La Sapienza, Rome, Italy et al. 2011). Climate-change-related range shifts or reductions 3 Organismic and Evolutionary Biology Department, Harvard have been frequently documented both in latitude (Shoo et al. University, Cambridge, MA, USA 2006;Chenetal.2011) and altitude (Moritz et al. 2008;Rowe 4 Centro Ricerca ed Innovazione, Fondazione Edmund Mach, San et al. 2010), particularly in specialised taxa. By contrast, range Michele all’Adige, Trento, Italy expansions involving generalists or highly adaptable species 5 School of Biological Sciences, University of Bristol, Bristol, UK appear rare. 15 Page 2 of 8 Sci Nat (2016) 103:15 Urbanisation is another global change process potentially temperatures (Rebelo et al. 2010), as regions at higher latitudes influencing the distribution of organisms whose effects may would become suitable for the species. Second, P. kuhlii has not be easily distinguished from those of climate change (e.g. synurbic habits (Dietz et al. 2009; Russo and Ancillotto 2015), Tomassini et al. 2014). Urbanisation is a non-directional pro- roosting frequently in buildings and commonly foraging at cess characterised by the replacement of natural habitats with streetlamps (Barak and Yom-Tov 1989;RussoandJones built-up areas (Antrop 2004). Europe has a long-standing his- 1998; Serangeli et al. 2012). Finally, despite its sedentary be- tory of human-induced landscape modification starting in the haviour (Dietz et al. 2009), P. kuhlii has expanded its range Holocene, 10,000 years ago (Antrop 2004), and landscape northeast in recent years, colonising regions of central and East- transformation has by no means ended: recent trends show ern Europe during the last three decades (Sachanowicz et al. that urbanisation is still taking place in vast areas of the con- 2006). In most cases, the first records of single individuals tinent, particularly in central and eastern regions (Palang et al. (initially regarded as vagrants) have been followed by observa- 2006). This dramatic process is certainly among the most tions of reproductive bats or maternity colonies, indicating suc- powerful drivers of changes in wildlife distribution in the cessful colonisation of the new region. Anthropocene (Steffen et al. 2011). Besides replacing and In this study, we assess the roles of climate change and fragmenting natural habitats, expanding urban areas are also urbanisation as drivers of P. kuhlii range expansion. We apply typically associated with chemical, light and noise pollution species distribution modelling to predict how the species prob- (Antrop 2004; Chace and Walsh 2006; Bradley and Altizer ability of presence changed in Europe since 1970, and com- 2007; Stone et al. 2009; Perugini et al. 2011; Bennie et al. pare the relative contributions of climate and urbanisation. 2014). Although most animal species avoid urban areas, Particularly, we tested two hypotheses, namely whether some, called Bsynurbic^ species, may either tolerate urbanisa- P. kuhlii range expansion is influenced (1) by climate change tion or even successfully exploit human settlements (Patterson only or (2) by a synergic concurrence of climate change and et al. 2003; Chace and Walsh 2006; Baker and Harris 2007). urbanisation. In the former scenario, we predict that P. kuhlii Bats are well-suited models to explore wildlife responses to has been able to colonise areas where the climate has become human-induced habitat modifications. These mammals are in warmer, whereas in the latter scenario, we predict that climate most cases multiple-habitat specialists, which depend on spe- change has combined with an increase in urbanisation to pro- cific roosting and foraging habitats, whose loss or alteration vide more roosting and foraging opportunities. have therefore seriously affected the population status of many species (Van der Meij et al. 2015). Many bat species find few or no foraging and roosting opportunities in urban Materials and methods areas (for a review, see Russo and Ancillotto 2015). In con- trast, other species tolerate or even thrive in urbanised land- Data collection scapes, for instance because they roost in buildings or forage at streetlamps (Kunz 1982; Rydell 1992). Activity patterns of We set up a database of all reliable records of P. kuhlii (based bats are closely linked to climatic conditions, particularly tem- on authors’ direct observation or acoustic identification or peratures, which strongly influence both their daily torpor as provided by bat specialists) for which both point precision well as hibernation (Stawski et al. 2014), and thus may affect and collection date were known, totalling 25,132 occurrence individual survival and reproductive success. points. To assess the extent of P. kuhlii range expansion after Both modelling and empirical studies suggest that climate 1980, we calculated and compared the area of historical extent change influences bat distribution (Rebelo et al. 2010;Sherwin of occurrence (after Stebbings and Griffiths 1986)withthatof et al. 2013; Razgour et al. 2013). Yet, to our best knowledge, no the current extent of occurrence, based on our dataset, and study has attempted to disentangle the genuine effects of cli- obtained a 100 % minimum convex polygon following IUCN mate change from those of land-use modifications to identify (2012). To model species distribution, we employed three bio- the key factors actually driving changes in bat distribution. climatic variables and one variable of urbanisation potentially Urbanisation and climate change may both play a role in induc- influencing P. kuhlii range. To select variables, we considered ing range shifts or expansions. In particular, they may act syn- the thermophilous nature of this bat, the fact that it hibernates ergically on species adapted to warmer climates (e.g. Mediter- in winter (Dietz et al. 2009) and its significant exposure to ranean species) as large urban settlements can act as Bthermal water loss linked to the dry Mediterranean summer (Russo islands^ favouring distributional changes (Arnfield 2003). et al. 2012). Therefore, we selected the environmental predic- Kuhl’s pipistrelle (Pipistrellus kuhlii) offers a unique oppor- tors that were most likely to limit P. kuhlii distribution, i.e. the tunity to investigate the relative effects of climate change and average minimum temperature of the four coldest months, urbanisation on species distributions for a number of reasons. mean precipitation
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