Skip to main content

Advertisement

Log in

Extraordinary range expansion in a common bat: the potential roles of climate change and urbanisation

  • Original Paper
  • Published:
The Science of Nature Aims and scope Submit manuscript

Abstract

Urbanisation and climate change are two global change processes that affect animal distributions, posing critical threats to biodiversity. Due to its versatile ecology and synurbic habits, Kuhl’s pipistrelle (Pipistrellus kuhlii) offers a unique opportunity to explore the relative effects of climate change and urbanisation on species distributions. In a climate change scenario, this typically Mediterranean species is expected to expand its range in response to increasing temperatures. We collected 25,132 high-resolution occurrence records from P. kuhlii European range between 1980 and 2013 and modelled the species’ distribution with a multi-temporal approach, 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 P. kuhlii and showed an increasing trend in the study period; mean annual precipitation and precipitation seasonality were also relevant, but to a lower extent. Although urbanisation increased in recently colonised areas, it had little effect on the species’ presence predictability. P. kuhlii expanded its geographical range by about 394 % in the last four decades, a process that can be interpreted as a response to climate change.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Allouche O, Tsoar A, Kadmon R (2006) Assessing the accuracy of species distribution models: prevalence, kappa and the true skill statistic (TSS). J Appl Ecol 43:1223–1232

    Article  Google Scholar 

  • Ancillotto L, Allegrini C, Serangeli MT, Jones G, Russo D (2015) Sociality across species: spatial proximity of newborn bats promotes heterospecific social bonding. Behav Ecol 26:293–299

    Article  Google Scholar 

  • Ancillotto L, Russo D (2015) Reassessing the breeding range limits for two long-distance migratory vespertilionid bats, Pipistrellus nathusii and Nyctalus leisleri in the Italian Peninsula. Mammalia 79:245–248

    Google Scholar 

  • Antrop M (2004) Landscape change and the urbanisation process in Europe. Landsc Urban Plan 67:9–26

    Article  Google Scholar 

  • Araújo MB, New M (2007) Ensemble forecasting of species distributions. Trends Ecol Evol 22:42–47

    Article  PubMed  Google Scholar 

  • Arlettaz R, Godat S, Meyer H (2000) Competition for food by expanding pipistrelle bat populations (Pipistrellus pipistrellus) might contribute to the decline of lesser horseshoe bats (Rhinolophus hipposideros). Biol Conserv 93:55–60

    Article  Google Scholar 

  • Arnfield AJ (2003) Two decades of urban climate research: a review of turbulence, exchanges of energy and water, and the urban heat island. Int J Climatol 23:1–26

    Article  Google Scholar 

  • Baker PJ, Harris S (2007) Urban mammals: what does the future hold? An analysis of the factors affecting patterns of use of residential gardens in Great Britain. Mamm Rev 37:297–315

    Google Scholar 

  • Barak Y, Yom-Tov Y (1989) The advantages of group hunting in Kuhl’s bat Pipistrellus kuhlii (Microchiroptera). J Zool 219:670–675

    Article  Google Scholar 

  • Barbet‐Massin M, Jiguet F, Albert CH, Thuiller W (2012) Selecting pseudo-absences for species distribution models: how, where and how many? Methods Ecol Evol 3:327–338

    Article  Google Scholar 

  • Bat Conservation Trust (2010) Rarities and vagrants. http://www.bats.org.uk/publications_download.php/749/raritiesvagrants.pdf

  • Benda P, Ivanova T, Horáček I, Hanák V, Červený J, Gaisler J, Gueorguieva A, Petrov B, Vohralík V (2003) Bats (Mammalia: Chiroptera) of the Eastern Mediterranean. Part 3. Review of bat distribution in Bulgaria. Acta Soc Zool Bohem 67:245–357

    Google Scholar 

  • Bennie J, Davies T, Duffy JP, Inger R, Gaston KJ (2014) Contrasting trends in light pollution across Europe based on satellite observed night time lights. Sci Rep 4:3789

    Article  PubMed  PubMed Central  Google Scholar 

  • Berková H, Pokorný M, Zukal J (2014) Selection of buildings as maternity roosts by greater mouse-eared bats (Myotis myotis). J Mammal 95:1011–1017

    Article  Google Scholar 

  • Bradley CA, Altizer S (2007) Urbanisation and the ecology of wildlife diseases. Trends Ecol Evol 22:95–102

    Article  PubMed  Google Scholar 

  • Cel’uch M, Ševčík M (2006) First record of Pipistrellus kuhlii (Chiroptera) from Slovakia. Biologia 61:637–638

    Google Scholar 

  • Chace JF, Walsh JJ (2006) Urban effects on native avifauna: a review. Landsc Urban Plan 74:46–69

    Article  Google Scholar 

  • Chen IC, Hill JK, Ohlemüller R, Roy DB, Thomas CD (2011) Rapid range shifts of species associated with high levels of climate warming. Science 333:1024–1026

    Article  CAS  PubMed  Google Scholar 

  • Danko Š (2007) Reprodukcia Hypsugo savii a Pipistrellus kuhlii na východnom Slovensku: ďalšie dôkazy o ich šírení na sever. Vespertilio 11:13–14

    Google Scholar 

  • Di Salvo I, Russo D, Sarà M (2009) Habitat preferences of bats in a rural area of Sicily determined by acoustic surveys. Hystrix 20:137–146

    Google Scholar 

  • Dietz C, von Helversen O, Nill D (2009) Bats of Britain, Europe and Northwest Africa. A & C Black, London

    Google Scholar 

  • Dragu A, Munteanu I, Olteanu V (2007) First record of Pipistrellus kuhlii Kuhl, 1817 (Chiroptera: Vespertilionidae) from Dobrogea (Romania). Arch Biol Sci 59:243–247

    Article  Google Scholar 

  • Elith J, Kearney M, Phillips S (2010) The art of modelling range‐shifting species. Methods Ecol Evol 1:330–342

    Article  Google Scholar 

  • Fehèr CE (1995) A fehrszlü denev.r (Pipistrellus kuhli) els. magyarorsz.gi adatai [First data of Kuhl’s pipistrelle (Pipistrellus kuhli) from Hungary]. Denevrkutats (Hungarian Bat Research News) 1:16–17

    Google Scholar 

  • Frick WF, Reynolds DS, Kunz TH (2010) Influence of climate and reproductive timing on demography of little brown myotis Myotis lucifugus. J Anim Ecol 79:128–136

    Article  PubMed  Google Scholar 

  • Goiti U, Vecin P, Garin I, Salona M, Aihartza JR (2003) Diet and prey selection in Kuhl’s pipistrelle Pipistrellus kuhlii (Chiroptera: Vespertilionidae) in south-western Europe. Acta Theriol 48:457–468

    Article  Google Scholar 

  • Guillera-Arroita G, Lahoz-Monfort JJ, Elith J, Gordon A, Kujala H, Lentini PE, Wintle BA (2015) Is my species distribution model fit for purpose? Matching data and models to applications. Glob Ecol Biogeog 24:276–292

    Article  Google Scholar 

  • Hersteinsson P, Macdonald DW (1992) Interspecific competition and the geographical distribution of red and arctic foxes Vulpes vulpes and Alopex lagopus. Oikos 64:505–515

    Article  Google Scholar 

  • Ifrim I, Valenciuc N (2006) Pipistrellus kuhlii Kuhl, 1819, a new reported species for the chiropteran fauna of Moldavia (Romania). Travaux du Muséum National d’Histoire Naturelle ‘Grigore Antipa 49:359–363

    Google Scholar 

  • IUCN (2012) IUCN red list categories and criteria: version 3.1., 2nd edn. IUCN, Gland, Switzerland and Cambridge, Available: www.iucnredlist.org/technical-documents/categories-and-criteria

    Google Scholar 

  • Ivanova TJ, Popov VV (1994) First record of Pipistrellus kuhlii (Kuhl, 1819) (Vespertilionidae, Chiroptera, Mammalia) from Bulgaria. Acta Zool Bulg 47:79–81

    Google Scholar 

  • Jetz W, Wilcove DS, Dobson AP (2007) Projected impacts of climate and land-use change on the global diversity of birds. PLoS Biology 5:e157

    Article  PubMed  PubMed Central  Google Scholar 

  • Kedrov BM, Seshurak PN (1999) The first record of the Pipistrellus kuhlii (Chiroptera, Vespertilionidae) in Chernihiv oblast (Ukraine). Vestnik zoologii 33:66

    Google Scholar 

  • Kunz TH (1982) Roosting ecology of bats. In: Kunz TH (ed) Ecology of bats. Plenum Publishing Corporation, USA, pp 1–55

    Chapter  Google Scholar 

  • Leger F (1992) Sur la présence de la Pipistrelle de Kuhl, Pipistrellus kuhli (Kuhl 1819), en Eure-et-Loir, loir-et-Cher et Sarthe. Bulletin scientifique de la Societè des amis du msèum de Chartres et des Naturalistes d’Eure-et-Loir 11:2–5

  • Lundy M, Montgomery I, Russ J (2010) Climate change-linked range expansion of Nathusius’ pipistrelle bat, Pipistrellus nathusii (Keyserling & Blasius, 1839). J Biogeog 37:2232–2242

    Article  Google Scholar 

  • Maiorano L, Cheddadi R, Zimmermann NE, Pellissier L, Petitpierre B, Pottier J, Laborde H, Hurdu BI, Pearman PB, Psomas A, Singarayer JS, Broennimann O, Vittoz P, Dubuis A, Edwards ME, Binney HA, Guisan A (2013) Building the niche through time: using 13,000 years of data to predict the effects of climate change on three tree species in Europe. Global Ecol Biogeogr 22:302–317

    Article  Google Scholar 

  • Maiorano L, Falcucci A, Zimmermann NE, Psomas A, Pottier J, Baisero D, Boitani L (2011) The future of terrestrial mammals in the Mediterranean basin under climate change. Philos Trans R Soc B 366:2681–2692

    Article  Google Scholar 

  • Martinoli A, Preatoni DG, Tosi G (2000) Does Nathusius’ pipistrelle Pipistrellus nathusii (Keyserling & Blasius, 1839) breed in northern Italy? J Zool 250:217–220

    Article  Google Scholar 

  • McKinney ML, Lockwood JL (1999) Biotic homogenization: a few winners replacing many losers in the next mass extinction. Trends Ecol Evol 14:450–453

    Article  PubMed  Google Scholar 

  • Moritz C, Patton JL, Conroy CJ, Parra JL, White GC, Beissinger SR (2008) Impact of a century of climate change on small-mammal communities in Yosemite National Park, USA. Science 322:261–264

    Article  CAS  PubMed  Google Scholar 

  • Palang H, Printsmann A, Gyuró ÉK, Urbanc M, Skowronek E, Woloszyn W (2006) The forgotten rural landscapes of central and eastern Europe. Landsc Ecol 21:347–357

    Article  Google Scholar 

  • Patterson ME, Montag JM, Williams DR (2003) The urbanisation of wildlife management: social science, conflict and decision making. Urban For Urban Greening 1:171–183

    Article  Google Scholar 

  • Paunović M, Marinković S (1998) Kuhl’s pipistrelle Pipistrellus kuhlii Kuhl, 1817 (Chiroptera, Vespertilionidae)—a new species in the mammal fauna of Serbia, with data on its Balkan distribution range, status and ecology. Proceedings of the fauna of Serbia, Natural and Mathematical Sciences 5:167–180

    Google Scholar 

  • Perugini M, Manera M, Grotta L, Abete MC, Tarasco R, Amorena M (2011) Heavy metal (Hg, Cr, Cd, and Pb) contamination in urban areas and wildlife reserves: honeybees as bioindicators. Biological Trace Element Research 140:170–176

    Article  CAS  PubMed  Google Scholar 

  • Popczyk B, Lesiński G, Baumann A, Wojtowicz B (2008) Kuhl’s pipistrelle, Pipistrellus kuhlii (Kuhl, 1817) or Pipistrellus lepidus Blyth, 1845, in Central Poland—accidental record or a result of expansion? Nyctalus 13:279–281

    Google Scholar 

  • Razgour O, Juste J, Ibáñez C, Kiefer A, Rebelo H, Puechmaille SJ, Arlettaz R, Burke T, Dawson DA, Beaumont M, Jones G (2013) The shaping of genetic variation in edge-of-range populations under past and future climate change. Ecol Lett 16:1258–1266

    Article  PubMed  PubMed Central  Google Scholar 

  • Rebelo H, Tarroso P, Jones G (2010) Predicted impact of climate change on European bats in relation to their biogeographic patterns. Global Change Biology 16:561–576

    Article  Google Scholar 

  • Reiter A, Benda P, Hotovy J (2007) First record of the Kuhl’s pipistrelle, Pipistrellus kuhlii (Kuhl, 1817), in the Czech Republic. Lynx 38:47–54

    Google Scholar 

  • Rowe RJ, Finarelli JA, Rickart EA (2010) Range dynamics of small mammals along an elevational gradient over an 80‐year interval. Glob Chang Biol 16:2930–2943

    Google Scholar 

  • Russo D, Ancillotto L (2015) Sensitivity of bats to urbanisation: a review. Mamm Biol 80:205–212

    Google Scholar 

  • Russo D, Jones G (1998) The social calls of Kuhl’s pipistrelles Pipistrellus kuhlii (Kuhl, 1819): structure and variation (Chiroptera: Vespertilionidae). J Zool 249:476–481

    Article  Google Scholar 

  • Russo D, Jones G (2003) Use of foraging habitats by bats in a Mediterranean area determined by acoustic surveys: conservation implications. Ecography 26:197–209

    Article  Google Scholar 

  • Russo D, Cistrone L, Jones G (2012) Sensory ecology of water detection by bats: a field experiment. PLoS ONE 7(10): e48144. doi:10.1371/journal.pone.0048144

  • Rydell J (1992) Exploitation of insects around streetlamps by bats in Sweden. Funct Ecol 6:744–750

    Article  Google Scholar 

  • Sachanowicz K, Wower A, Bashta AT (2006) Further range extension of Pipistrellus kuhlii (Kuhl, 1817) in central and eastern Europe. Acta Chiropterol 8:543–548

    Article  Google Scholar 

  • Serangeli MT, Cistrone L, Ancillotto L, Tomassini A, Russo D (2012) The post-release fate of hand-reared orphaned bats: survival and habitat. Anim Welf 21:9–18

    Article  CAS  Google Scholar 

  • Sherwin HA, Montgomery WI, Lundy MG (2013) The impact and implications of climate change for bats. Mamm Rev 43:171–182

    Article  Google Scholar 

  • Shoo LP, Williams SE, Hero J (2006) Detecting climate change induced range shifts: where and how should we be looking? Austral Ecol 31:22–29

    Article  Google Scholar 

  • Stawski C, Willis CKR, Geiser F (2014) The importance of temporal heterothermy in bats. J Zool 292:86–100

    Article  Google Scholar 

  • Stebbings RE, Griffith F (1986) Distribution and status of bats in Europe. Institute of Terrestrial Ecology, Abbots Ripton, Huntingdon

    Google Scholar 

  • Steffen W, Grinevald J, Crutzen P, McNeill J (2011) The Anthropocene: conceptual and historical perspectives. Philos Trans R Soc A 369:842–867

    Article  Google Scholar 

  • Stone EL, Jones G, Harris S (2009) Street lighting disturbs commuting bats. Curr Biol 19:1123–1127

    Article  CAS  PubMed  Google Scholar 

  • Thomas CD, Cameron ARG et al (2004) Extinction risk from climate change. Nature 427:145–148

    Article  CAS  PubMed  Google Scholar 

  • Thuiller W, Lafourcade B, Engler R, Araújo MB (2009) BIOMOD—a platform for ensemble forecasting of species distributions. Ecography 32:369–373

    Article  Google Scholar 

  • Tomassini A, Colangelo P, Agnelli P, Jones G, \ D (2014) Cranial size has increased over 133 years in a common bat, Pipistrellus kuhlii: a response to changing climate or urbanisation? J Biogeog 41:944–953

    Article  Google Scholar 

  • Tuttle MD (1976) Population ecology of the gray bat (Myotis grisescens): factors influencing growth and survival of newly volant young. Ecology 57:587–595

    Article  Google Scholar 

  • Van der Meij T, Van Strien AJ, Haysom KA, Dekker J, Russ J, Biala K, Vintulis V (2015) Return of the bats? A prototype indicator of trends in European bat populations in underground hibernacula. Mamm Biol 80:170–177

  • Van Dyck H (2012) Changing organisms in rapidly changing anthropogenic landscapes: the significance of the “Umwelt”—concept and functional habitat for animal conservation. Evol Appl 5:144–153

    Article  PubMed  PubMed Central  Google Scholar 

  • Visconti P, Baisero D, Brooks T, Butchart SHM, Joppa L, Alkemade R, Bakkenes M, Di Marco M, Santini L, Hoffmann M, Maiorano L, Pressey RL, Arponen A, Boitani L, Reside A, van Vuuren D, Rondinini C (2015) Projecting global biodiversity indicators under future development scenarios. Conserv Lett (in press) doi:10.1111/conl.12159

Download references

Acknowledgments

We thank the researchers, professionals, NGO representatives or simple participants who helped us to gather all the data necessary to this study. Special thanks go to the French Society for Mammal Study and Protection (SFEPM), the contributing bat local groups (Groupes Chiroptères) of Aquitaine (GCA), Auvergne (Chauve-Souris Auvergne), Corse (GCC), Champagne Ardennes, Ile de France, Languedoc-Rousillon (GCLR), Midi-Pyrénées (CEN-GMCP), Pays de la Loire, Poitou-Charentes, Provence (GCP) and Rhône Alpes as well as the local mammal groups of Alsace (GEPMA), Bretagne (GMB), Limousin (GMHL), Nord (CMNF) and Normandie (GMN). We would also like to thank the LPO and its local groups Anjou and Vendée, as well as the CPIE Loire Anjou and CPIE Vallées de la Sarthe et du Loir, CREN Poitou-Charentes, Faune-Charente-Maritime, Les Naturalistes Vendéens, Mayenne Nature Environnement, Nature Environnement 17 and Picardie Nature. We also received important contributions from the Natural History Museum of Bourges, the French National Forest Office (ONF) and ECO-MED (environmental consultancy), BatLife Österreich (Austria), the Bat Research and Conservation Centre at the National Museum of Natural History, Sofia (Bulgaria), Tel-Aviv University (Israel), RE.NA.TO (Tuscany, Italy), Centro Recupero Fauna Selvatica di Roma (LIPU), the Instituto da Conservação da Natureza e das Florestas (Portugal), the Bat Conservation Switzerland and the Centro protezione chirotteri Ticino (Switzerland). Finally, we would like to thank J.T. Alcalde, B. Allegrini, O. Allenou, E. Amichai, S. Aulagnier, S. Bareille, V. Barret, P. Barros, P. Benda, Y. Bernard, J. Boireau, L. Braz, A. Casadio, G. Caublot, H. Chauvin, G. Coste, JY Courtois, P. Georgiakakis, L. Girard, N. Harter, J. Jemin, P. Jourde, JF. Julien, B. Karapandza, H. Kraettli, M. Lemaire, M. Leuchtmann, S. Lutz, M. Manni Joss, K. Marchesi, M. Mattei-Roesli, S. Meiri, B. Même-Lafond, E. Mori, E. Papadatou, M. Paunovic, R. Pavisse, B. Petrov, P. Presetnik, D. Quekenborn, L. Rodrigues, F. Spitzenberger, G. Testud, P. Théou, M. Thévenot, L. Tillon, S. Vincent A. Vlaschenko and Y. Yovel for their help. N. Ranc was supported by GBIF and Swarovski Optik. We also thank three anonymous reviewers who greatly improved a previous version of this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to D. Russo.

Ethics declarations

Conflict of interests

The authors declare that they have no competing interests.

Additional information

Communicated by: Fritz Geiser

L. Ancillotto and L. Santini are co-first authors.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 1645 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ancillotto, L., Santini, L., Ranc, N. et al. Extraordinary range expansion in a common bat: the potential roles of climate change and urbanisation. Sci Nat 103, 15 (2016). https://doi.org/10.1007/s00114-016-1334-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00114-016-1334-7

Keywords

Navigation