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Different responses of attic-dwelling bat species to landscape naturalness

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Abstract

Although the general role of bats and the tolerance of many species to urbanized areas is well known, the relationship between urban roosts and their surrounding landscapes having different degrees of naturalness still requires our attention, mainly in species that are the most adapted to human-made structures. We used extensive data from attic-dwelling bat surveillance conducted throughout Slovakia to assess species responses to the degree of naturalness of the landscape surrounding their anthropogenic roosts. Using generalized linear mixed-effects modelling, we found that some bats established their nursery colonies in either a habitat with a higher proportion of forests mostly at sub-mountain/mountain altitudes (R. hipposideros, P. auritus, M. emarginatus), or they preferred lowlands with a predominance of arable land (E. serotinus, P. austriacus). Furthermore, higher habitat heterogeneity and the proportion of grassland were positively associated with the occurrence of P. auritus; however, negative associations with these habitat variables were found in E. serotinus. The predicted suitability of an area for bats to establish nursery colonies suggests the existence of two regions with different bat species composition in the study area: a region of the Pannonian Lowlands and a less urbanized mountain region of the Carpathian Mountains. Our study thus showed that landscape naturalness is a determining factor for roost-site selection by bats preferring anthropogenic roosts; however, some bat species did not express specific preferences according to the tested environmental variables, and other ecological traits in the evaluated species should be considered.

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References

  • Ancillotto, L., Tomassini, A., Russo, D., 2016. The fancy city life: Kuhl’s pipistrelle, Pipistrellus kuhlii, benefits from urbanisation. Wildl. Res. 42, 598–606.

    Article  Google Scholar 

  • Arlettaz, R., Christe, P., Lugon, A., Perrin, N., Vogel, P., 2001. Food availability dictates the timing of parturition in insectivorous mouse-eared bats. Oikos 95, 105–111.

    Article  Google Scholar 

  • Arlettaz, R., 1999. Habitat selection as a major resource partitioning mechanism between the two sibling species of bats Myotis myotis and Myotis blythii.J. Anim. Ecol. 68, 460–471.

    Article  Google Scholar 

  • Ashrafi, S., Rutishauser, M., Ecker, K., Obrist, M., Arlettaz, R., Bontadina, F., 2013. Habitat selection of three cryptic Plecotus bat species in the European Alps reveals contrasting implications forconservation. Biodivers. Conserv. 22, 2751–2766.

    Article  Google Scholar 

  • Audet, D., 1990. Foraging behavior and habitat use by a gleaning bat, Myotis myotis (Chiroptera: Vespertilionidae). J. Mammal. 71, 420–427.

    Article  Google Scholar 

  • Baker, P.J., 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 

  • Barton, K., 2016. MuMIn: Multi-Model Inference. R Package Version 1.15-6. https://doi.org/cran.r-project.org/package=MuMIn.

    Google Scholar 

  • Bates, D., Maechler, M., Bolker, B., Walker, S., 2016. lme4: Linear Mixed-Effects Models Using ’Eigen’ and S4. R Package Version 1.1-11. https://doi.org/cran.r-project.org/package=lme4.

    Google Scholar 

  • Bellamy, C., Altringham, J., 2015. Predicting species distributions using record centre data: multi-scale modelling of habitat suitability forbat roosts. PLoS One 10, e0128440.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Blair, R.B., 1996. Land use and avian species diversity along an urban gradient. Ecol. Appl. 6, 506–519.

    Article  Google Scholar 

  • Bontadina, F., Schofield, H., Naef-Daenzer, B., 2002. Radio-tracking reveals that lesser horseshoe bats (Rhinolophus hipposideros) forage in woodland.J. Zool. 258, 281–290.

    Article  Google Scholar 

  • Boughey, K.L.R., Lake, I.R., Haysom, K.A., Dolman, P.M., 2011. Effects of landscape-scale broadleaved woodland configuration and extent on roost location forsixbat species across the UK. Biol. Conserv. 144, 2300–2310.

    Article  Google Scholar 

  • Catto, C.M.C., Hutson, A.M., Raccey, P.A., Stephenson, P.J., 1996. Foraging behaviour and habitat use of the serotine bat (Eptesicus serotinus) in southern England. J. Zool. 238, 623–633.

    Article  Google Scholar 

  • Ciechanowski, M., 2015. Habitat preferences of bats in anthropogenically altered, mosaic landscapes of northern Poland. Eur.J. Wildl. Res. 61, 415–428.

    Article  Google Scholar 

  • Coleman, J.L., Barclay, R.M.R., 2011. Influence of urbanization on demography of little brown bats (Myotis lucifugus) in the prairies of North America. PLoS One 6, e20483.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dekker, J.J.A., Regelink, J.R., Jansen, E.A., Brinkmann, R., Limpens, H.J.G.A., 2013. Habitat use by female Geoffroy’s bats (Myotis emarginatus) at its two northernmost maternity roosts and the implications fortheirconservation. Lutra 56, 111–120.

    Google Scholar 

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

    Google Scholar 

  • Dietz, M., Pir, J., Hillen, J., 2013. Does the survival ofgreater horseshoe bats and Geoffroy’s bats in Western Europe depend on traditional cultural landscapes? Biodivers. Conserv. 22, 3007–3025.

    Google Scholar 

  • Ekman, M., de Jong, J., 1996. Local patterns of distribution and resource utilization of four bat species (Myotis brandti, Eptesicus nilssoni, Plecotus auritus and Pipistrellus pipistrellus) in patchy and continuous environments.J. Zool. 238, 571–580.

    Article  Google Scholar 

  • Entwistle, A.C., Racey, P.A., Speakman, J.R., 1997. Roost selection by the brown long-eared bat Plecotus auritus.J. Appl. Ecol. 34, 399–408.

    Article  Google Scholar 

  • Fabianek, F., Gagnon, D., Delorme, M., 2011. Bat distribution and activity in Montréal Island green spaces: responses to multi-scale habitat effects in a densely urbanized area. Ecoscience 18, 9–17.

    Article  Google Scholar 

  • Fischer, J.D., Schneider, S.C., Ahlers, A.A., Miller, J.R., 2015. Categorizing wildlife responses to urbanization and conservation implications of terminology. Conserv. Biol. 29, 1246–1248.

    Article  PubMed  Google Scholar 

  • Flanders, J., Jones, G., 2009. Roost use, ranging behavior, and diet ofgreater horseshoe bats (Rhinolophus ferrumequinum) using a transitional roost. J. Mammal. 90, 888–896.

    Article  Google Scholar 

  • Fonderflick, J., Azam, C., Brochier, C., Cosson, E., Quékenborn, D., 2015. Testing the relevance of using spatial modelingto predict foraging habitat suitability around bat maternity: a case study in Mediterranean landscape. Biol. Conserv. 192, 120–129.

    Article  Google Scholar 

  • Francis, R.A., Chadwick, M.A., 2012. What makes a species synurbic? Appl. Geogr. 32, 514–521.

    Google Scholar 

  • Frey-Ehrenbold, A., Bontadina, F., Arlettaz, R., Obrist, M.K., 2013. Landscape connectivity, habitat structure and activity of bat guilds in farmland-dominated matrices. J. Appl. Ecol. 50, 252–261.

    Article  Google Scholar 

  • Güttinger, R., Zahn, A., Krapp, F., Schober, W., 2001. Myotis myotis (Borkhausen, 1771) - Großes Mausohr, Großmausohr. In: Krapp, F. (Ed.), Handbuch der Säugetiere Europas. Band 4: Fledertiere. Teil I: Chiroptera I. Rhinolophidae, Vespertilionidae 1. AULA-Verlag, Wiebelsheim, pp. 123–207.

    Google Scholar 

  • Gehrt, S.D., Chelsvig, J.E., 2004. Species-specific patterns of bat activity in an urban landscape. Ecol. Appl. 14, 625–635.

    Article  Google Scholar 

  • Germaine, S.S., Wakeling, B.F., 2001. Lizard species distributions and habitat occupation along an urban gradient in Tucson, Arizona, USA. Biol. Conserv. 97, 229–237.

    Article  Google Scholar 

  • Gorresen, P.M., Willig, M.R., Strauss, R.E., 2005. Multivariate analysis of scale-dependent associations between bats and landscape structure. Ecol. Appl. 15, 2126–2136.

    Article  Google Scholar 

  • Hale, J.D., Fairbrass, A.J., Matthews, T.J., Sádler, J.P., 2012. Habitat composition and connectivity predicts bat presence and activity at foraging sites in a large UK conurbation. PLoS One 7, e33300.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harbusch, C., Racey, P.A., 2006. The sessile serotine: the influence of roost temperature on philopatry and reproductive phenology of Eptesicus serotinus (Schreber, 1774) (Mammalia: Chiroptera). Acta Chiropterol. 8, 213–229.

    Article  Google Scholar 

  • Holzhaider, J., Kriner, E., Rudolph, B.U., Zahn, A., 2002. Radio-tracking a lesser horseshoe bat (Rhinolophus hipposideros) in Bavaria: an experiment to locate roosts and foraging sites. Myotis 40, 47–54.

    Google Scholar 

  • Horáček, I., 1985. Population ecology of Myotis myotis in Central Bohemia (Mammalia: Chiroptera). Acta Univ. Carol. Biol. 1981, 161–267.

    Google Scholar 

  • Jung, K., Threlfall, C., 2016. Urbanisation and its effects onbats - aglobal meta-analysis. In: Voigt, C.C., Kingston, T. (Eds.), Bats in the Anthropocene: Conservation of Bats in a Changing World. Springer, Cham, Heidelberg, New York, Dordrecht, London, pp. 13–33.

    Google Scholar 

  • Kaňuch, P., Danko, Š., Cel’uch, M., Krištín, A., Pjenčák, P., Matis, Š., Šmídt, J., 2008. Relating bat species presence to habitat features in natural forests of Slovakia (Central Europe). Mamm. Biol. 73, 147–155.

    Article  Google Scholar 

  • Kark, S., Iwaniuk, A., Schalimtzek, A., Banker, E., 2007. Living in the city: can anyone become an ’urban exploiter’? J. Biogeogr. 34, 638–651.

    Article  Google Scholar 

  • Kristofík, J., Danko, S., 2012. Cicavce Slovenska. Rozsírenie bionómia a ochrana. Veda, Bratislava, p. 712.

    Google Scholar 

  • Krull, D., Schumm, A., Metzner, W., Neuweiler, G., 1991. Foraging areas and foraging behavior in the notch-eared bat, Myotis emarginatus (Vespertilionidae). Behav. Ecol. Sociobiol. 28, 247–253.

    Article  Google Scholar 

  • Kunz, T.H., 1982. Roosting ecology of bats. In: Kunz, T.H. (Ed.), Ecology of Bats. Plenum Press, New York, pp. 1–55.

    Book  Google Scholar 

  • Li, H., Wilkins, K.T., 2014. Patch or mosaic: bat activity responds to fine-scale urban heterogeneity in a medium-sized city in the United States. Urban Ecosyst. 17, 1013–1031.

    Article  Google Scholar 

  • Lintott, P.R., Bunnefeld, N., Minderman, J., Fuentes-Montemayor, E., Mayhew, R.J., Olley, L., Park, K.J., 2015a. Differential responses to woodland character and landscape context by cryptic bats in urban environments. PLoS One 10, e0126850.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lintott, P.R., Bunnefeld, N., Park, K.J., 2015b. Opportunities for improving the foraging potential of urban waterways for bats. Biol. Conserv. 191, 224–233.

    Article  Google Scholar 

  • Lisón, F., Sánchez-Fernández, D., Calvo, J., 2015. Are species listed inthe Annex II of the Habitats Directive better represented in Natura 2000 network than the remaining species? A test using Spanish bats. Biodivers. Conserv. 24, 2459–2473.

    Article  Google Scholar 

  • Loeb, S.C., Post, C.J., Hall, S.T., 2009. Relationship between urbanization and bat community structure in national parks of the southeastern U.S. Urban Ecosyst. 12, 197–214.

    Article  Google Scholar 

  • Maiorano, L., Amori, G., Montemaggiori, A., Rondinini, C., Santini, L., Saura, S., Boitani, L., 2015. On how much biodiversity is covered in Europe by national protected areas and by the Natura 2000 network: insights from terrestrial vertebrates. Conserv. Biol. 29, 986–995.

    Article  CAS  PubMed  Google Scholar 

  • Maxinová, E., Kipson, M., Nad’o, L., Hradická, P., Uhrin, M., 2016. Foraging strategy of Kuhlás pipistrelle at the northern edge of the species distribution. Acta Chiropterol. 18, 215–222.

    Article  Google Scholar 

  • McKinney, M.L., 2006. Urbanization as a major cause of biotic homogenization. Biol. Conserv. 127, 247–260.

    Article  Google Scholar 

  • McKinney, M.L., 2008. Effects of urbanization on species richness: a review of plants and animals. Urban Ecosyst. 11, 161–176.

    Article  Google Scholar 

  • Mehr, M., Brandl, R., Hothorn, T., Dziock, F., Förster, B., Müller, J., 2011. Land use is more important than climate for species richness and composition of bat assemblages on a regional scale. Mamm. Biol. 76, 451–460.

    Article  Google Scholar 

  • Michaelsen, T.C., Jensen, K.H., Högstedt, G., 2011. Topography is a limiting distributional factor in the soprano pipistrelle at its latitudinal extreme. Mamm. Biol. 76, 295–301.

    Article  Google Scholar 

  • Milne, D.J., Fisher, A., Pavey, C.R., 2006. Models of the habitat associations and distributions of insectivorous bats of the Top End of the Northern Territory, Australia. Biol. Conserv. 130, 370–385.

    Article  Google Scholar 

  • Moussy, C., 2011. Selection of old stone buildings as summerday roost by the brown long-eared bat Plecotus auritus. Acta Chiropterol. 13, 101–111.

    Article  Google Scholar 

  • Neubaum, D.J., Wilson, K.R., ÓiShea, T.J., 2007. Urban maternity-roost selection by big brown bats in Colorado. J. Wildl. Manag. 71, 728–736.

    Article  Google Scholar 

  • Ode, Å., Fry, G., Tveit, M.S., Messager, P., Miller, D., 2009. Indicators of perceived naturalness as drivers of landscape preference. J. Environ. Manage. 90, 375–383.

    Article  PubMed  Google Scholar 

  • Oprea, M., Mendes, P., Vieira, T.B., Ditchfield, A.D., 2009. Do wooded streets provide connectivity forbats in an urban landscape? Biodivers. Conserv. 18, 2361–2371.

    Google Scholar 

  • Park, K.J., 2015. Mitigating the impacts of agriculture on biodiversity: bats and their potential role as bioindicators. Mamm. Biol. 80, 191–204.

    Article  Google Scholar 

  • Puig-Montserrat, X., Torre, I., López-Baucells, A., Guerrieri, E., Monti, M.M., Ràfols-García, R., Ferrer, X., Gisbert, D., Flaquer, C., 2015. Pest control service provided by bats in Mediterranean rice paddies: linking agroecosystems structure to ecological functions. Mamm. Biol. 80, 237–245.

    Article  Google Scholar 

  • QGIS Development Team, 2015. QGIS Geographic Information System. Open Source Geospatial Foundation Project. https://doi.org/qgis.osgeo.org.

    Google Scholar 

  • R Core Team, 2016. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna https://doi.org/www.r-project.org.

    Google Scholar 

  • Razgour, O., Hanmer, J., Jones, G., 2011. Using multi-scale modelling to predict habitat suitability forspecies of conservation concern: thegrey long-eared bat as a case study. Biol. Conserv. 144, 2922–2930.

    Article  Google Scholar 

  • Robinson, M.F., Stebbings, R.E., 1997. Home range and habitat use by the serotine bat, Eptesicus serotinus, in England. J. Zool. 243, 117–136.

    Article  Google Scholar 

  • Rodrigues, L., Zahn, A., Rainho, A., Palmeirim, J.M., 2003. Contrasting the roosting beaviour and phenology of an insectivorous bat (Myotis myotis) in its southern and northern distribution ranges. Mammalia 67, 321–335.

    Article  Google Scholar 

  • Rowse, E.G., Lewanzik, D., Stone, E.L., Harris, S., Jones, G., 2016. Dark matters: the effects of artificial lighting on bats. In: Voigt, C.C., Kingston, T. (Eds.), Bats in the Anthropocene: Conservation of Bats in a Changing World. Springer, Cham, Heidelberg, New York, Dordrecht, London, pp. 187–213.

    Google Scholar 

  • Rudolph, B.U., Liegl, A., von Helversen, O., 2009. Habitat selection and activity patterns in the greater mouse-eared bat Myotis myotis. Acta Chiropterol. 11, 351–361.

    Article  Google Scholar 

  • Russo, D., Ancillotto, L., 2014. Sensitivity of bats to urbanization: a review. Mamm. Biol. 80, 205–212.

    Article  PubMed  PubMed Central  Google Scholar 

  • Russo, D., Jones, G., 2015. Bats as bioindicators: an introduction. Mamm. Biol. 80, 157–158.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Shwartz, A., Turbé, A., Julliard, R., Simon, L., Prévot, A.-C, 2014. Outstanding challenges for urban conservation research and action. Glob. Environ. Change 28, 39–49.

    Article  Google Scholar 

  • Smith, D.A., Gehrt, S.D., 2010. Bat response to woodland restoration within urban forest fragments. Rest. Ecol. 18, 914–923.

    Article  Google Scholar 

  • Stone, E.L., Harris, S., Jones, G., 2015. Impacts of artificial lighting onbats: a review of challenges and solutions. Mamm. Biol. 80, 213–219.

    Article  Google Scholar 

  • Tink, M., Burnside, N.G., Waite, S., 2014. A spatial analysis of serotine bat (Eptesicus serotinus) roost location and landscape structure: a case study in Sussex, UK. Int. J. Biodivers. 2014, Article ID 495307.

    Google Scholar 

  • Topál, G., Ruedi, M., 2001. Myotis blythii (Tomes, 1857) - Kleines Mausohr. In: Krapp, F. (Ed.), Handbuch der Säugetiere Europas. Band 4: Fledertiere. Teil I: Chiroptera I. Rhinolophidae, Vespertilionidae 1. AULA-Verlag, Wiebelsheim, pp. 209–255.

    Google Scholar 

  • Tournant, P., Afonso, E., Roué, S., Giraudoux, P., Foltête, J.-C, 2013. Evaluatingthe effect of habitat connectivity on the distribution of lesserhorseshoe bat maternity roosts using landscape graphs. Biol. Conserv. 164, 39–49.

    Article  Google Scholar 

  • Uhrin, M., Sevcík, M., 2011. Chiropterologická bibliografia Slovenska3. Práce z obdobia 2006–2010 a doplnky z predchádzajúceho obdobia. Vespertilio 15, 121–149.

    Google Scholar 

  • Uhrin, M., Polakovicová, E., 2000. Netopiere (Chiroptera), rozsírenie, pocetnost’ a ochrana na Slovensku. Vyberová bibliografia. Státna vedecká kniznica v Banskej Bystrici, Banská Bystrica.

    Google Scholar 

  • Uhrin, M., Danko, S., Obuch, J., Horácek, I., Pacenovsky, S., Pjencák, P., Fulín, M., 1996. Distributional patterns of bats (Mammalia: Chiroptera) in Slovakia. Part 1, Horseshoe bats (Rhinolophidae). Acta Soc. Zool. Boh. 60, 247–279.

    Google Scholar 

  • Uhrin, M., Kanuch, P., Kristofík, J., Paule, L., 2010. Phenotypic plasticity in the greater mouse-eared bat in extremely different roost conditions. Acta Theriol. 55, 153–164.

    Article  Google Scholar 

  • Uhrin, M., Boldogh, S., Bücs, S., Paunovic, M., Miková, E., Juhász, M., Csosz, I., Estók, P., Fulín, M., Gombköto, P., Jére, C, Barti, L, Karapandza, B., Matis, S., Nagy, Z.L., Szodoray-Paradi, F., Benda, P., 2012. Revision ofthe occurrence ofRhinolophus euryale in the Carpathian region, Central Europe. Vespertilio 16, 289–328.

    Google Scholar 

  • Uhrin, M., 2006. Chiropterologická bibliografia Slovenska 2. Doplnky do roku 1999 a práce z obdobia 2000–2005. Vespertilio 9–10, 193–216.

    Google Scholar 

  • Voigt, C.C., Phelps, K.L., Aguirre, L.F., Schoeman, C.M., Vanitharani, J., Zubaid, A., 2016. Bats and buildings: the conservation of synanthropic bats. In: Voigt, C.C., Kingston, T. (Eds.), Bats in the Anthropocene: Conservation of Bats in a Changing World. Springer, Cham, Heidelberg, New York, Dordrecht, London, pp. 427–462.

    Google Scholar 

  • Wei, T., 2015. corrplot: Visualization of a Correlation Matrix. R Package Version 0.73. https://doi.org/cran.r-project.org/package=corrplot.

    Google Scholar 

  • Williams-Guillén, K., Olimpi, E., Maas, B., Taylor, P.J., Arlettaz, R., 2016. Bats in the anthropogenic matrix: challenges and opportunities for the conservation of Chiroptera and their ecosystem services in agricultural landscapes. In: Voigt, C.C., Kingston, T. (Eds.), Bats in the Anthropocene: Conservation of Bats in a Changing World. Springer, Cham, Heidelberg, New York, Dordrecht, London, pp. 151–186.

    Google Scholar 

  • Zahn, A., Haselbach, H., Güttinger, R., 2005. Foraging activity of central European Myotis myotis in a landscape dominated by spruce monocultures. Mamm. Biol. 70, 265–270.

    Article  Google Scholar 

  • Zahn, A., Rottenwallner, A., Güttinger, R., 2006. Population density ofthe greater mouse-eared bat (Myotis myotis), local diet composition and availability of foraging habitats. J. Zool. 269, 486–493.

    Article  Google Scholar 

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  1. Department of Zoology, Faculty of Science, P.J. Šafárik University in Košice, Moyzesova 11, 040 01, Košice, Slovakia

    Marcel Uhrin & Peter Kaňuch

  2. Department of Forest Protection and Wildlife Management, Faculty of Forestry and Wood Sciences, Czech University of Life Sciences, Kamýcká 1176, 16521, Praha 6, Czechia

    Marcel Uhrin

  3. Department of Zoology, National Museum (Natural History), Václavské náměstí 68, 115 79, Praha 1, Czechia

    Petr Benda

  4. Department ofZoology, Faculty of Science, Charles University in Prague, Viničná 7, 128 44, Praha 2, Czechia

    Petr Benda

  5. Institute ofForest Ecology, Slovak Academy of Sciences, L. Stúra 2, 960 53, Zvolen, Slovakia

    Peter Kaňuch

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Uhrin, M., Benda, P. & Kaňuch, P. Different responses of attic-dwelling bat species to landscape naturalness. Mamm Biol 82, 48–56 (2017). https://doi.org/10.1016/j.mambio.2016.10.001

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