Biodiversity and Conservation

, Volume 22, Issue 12, pp 2751–2766 | Cite as

Habitat selection of three cryptic Plecotus bat species in the European Alps reveals contrasting implications for conservation

  • Sohrab AshrafiEmail author
  • Marianne Rutishauser
  • Klaus Ecker
  • Martin K. Obrist
  • Raphaël Arlettaz
  • Fabio BontadinaEmail author
Original Paper


Assessing the ecological requirements of species coexisting within a community is an essential requisite for developing sound conservation action. A particularly interesting question is what mechanisms govern the stable coexistence of cryptic species within a community, i.e. species that are almost impossible to distinguish. Resource partitioning theory predicts that cryptic species, like other sympatric taxa, will occupy distinct ecological niches. This prediction is widely inferred from eco-morphological studies. A new cryptic long-eared bat species, Plecotus macrobullaris, has been recently discovered in the complex of two other species present in the European Alps, with even evidence for a few mixed colonies. This discovery poses challenges to bat ecologists concerned with planning conservation measures beyond roost protection. We therefore tested whether foraging habitat segregation occurred among the three cryptic Plecotus bat species in Switzerland by radiotracking 24 breeding female bats (8 of each species). We compared habitat features at locations visited by a bat versus random locations within individual home ranges, applying mixed effects logistic regression. Distinct, species-specific habitat preferences were revealed. P. auritus foraged mostly within traditional orchards in roost vicinity, with a marked preference for habitat heterogeneity. P. austriacus foraged up to 4.7 km from the roost, selecting mostly fruit tree plantations, hedges and tree lines. P. macrobullaris preferred patchy deciduous and mixed forests with high vertical heterogeneity in a grassland dominated-matrix. These species-specific habitat preferences should inform future conservation programmes. They highlight the possible need of distinct conservation measures for species that look very much alike.


Cryptic species Heterogeneity Plecotus Radiotracking Resource partitioning Switzerland 



We wish to thank Andres Beck, Annie Ehrenbold, Kathi Märki, Therese Hotz, and Irene Weinberger for field assistance. We are also grateful to Fitsum Abadi, Michael Schaub and Patrick Patthey for their help with data analysis, Silvia Dingwall for English revision, and the respective cantonal authorities for permitting access to the roosts and the captures of individuals.

Supplementary material

10531_2013_551_MOESM1_ESM.pdf (833 kb)
Supplementary material 1 (PDF 833 kb)


  1. Abrams PA (1998) High competition with low similarity and low competition with high similarity: exploitative and apparent competition in consumer-resource systems. Am Nat 152:114–128PubMedCrossRefGoogle Scholar
  2. Alberdi A, Garin I, Aizpurua O, Aihartza J (2012) The foraging ecology of the mountain long-eared bat Plecotus macrobullaris revealed with DNA mini-barcodes. PLoS One 7(4):e35692PubMedCrossRefGoogle Scholar
  3. Arlettaz R (1999) Habitat selection as a major resource partitioning mechanism between the two sympatric sibling bat species Myotis myotis and Myotis blythii. J Anim Ecol 68:460–471CrossRefGoogle Scholar
  4. Arlettaz R, Perrin N, Hausser J (1997) Trophic resource partitioning and competition between the two sibling bat species Myotis myotis and Myotis blythii. J Anim Ecol 66:897–911CrossRefGoogle Scholar
  5. Artuso R, Bovet S, Streilein A (2003) Practical methods for the verification of countrywide terrain and surface models. Int Arch Photogramm Remote Sens and Spat Inf Sci 34:6 (on CD-ROM)Google Scholar
  6. Ashrafi S, Bontadina F, Kiefer A, Pavlinic I, Arlettaz R (2010) Multiple morphological characters needed for field identification of cryptic long-eared bat species around the Swiss Alps. J Zool 281:241–248CrossRefGoogle Scholar
  7. Ashrafi S, Beck A, Rutishauser M, Arlettaz R, Bontadina F (2011) Trophic niche partitioning of cryptic species of long-eared bats in Switzerland: implications for conservation. Eur J Wildl Res 57(4):843–849CrossRefGoogle Scholar
  8. Bazzaz FA (1975) Plant species-diversity in old-filed successional ecosystems in Illinois. Ecology 56:485–488CrossRefGoogle Scholar
  9. Bickford D, Lohman DJ, Sodhi NS, Ng PKL, Meier R, Winker K, Ingram KK, Das I (2007) Cryptic species as a window on diversity and conservation. Trends Ecol Evol 22:148–155PubMedCrossRefGoogle Scholar
  10. Bontadina F, Naef-Daenzer B (1996) Analysing spatial data of different accuracy: the case of greater horseshoe bats foraging. In: Le Maho Y (ed) Wildlife-Biotelemetry, Strassbourg. Accessed 23 Aug 2013
  11. Bontadina F, Schofield H, Naef-Daenzer B (2002) Radio-tracking reveals that lesser horseshoe bats (Rhinolophus hipposideros) forage in woodland. J Zool 258:281–290CrossRefGoogle Scholar
  12. Bontadina F, Schmied SF, Beck A, Arlettaz R (2008) Changes in prey abundance unlikely to explain the demography of a critically endangered Central European bat. J Appl Ecol 45:641–648CrossRefGoogle Scholar
  13. Boughey KL, Lake IR, Haysom KA, Dolman PM (2011) Improving the biodiversity benefits of hedgerows: how physical characteristics and proximity of foraging habitat affect the use of linear features by bats. Biol Conserv 144:1790–1798CrossRefGoogle Scholar
  14. Burnham KP, Anderson DR (2002) Model selection and multimodel inference. Springer, New YorkGoogle Scholar
  15. Davidowitz G, Rosenzweig ML (1998) The latitudinal gradient of species diversity among North American grasshoppers (Acrididae) within a single habitat: a test of the spatial heterogeneity hypothesis. J Biogeog 25:553–560CrossRefGoogle Scholar
  16. Davidson-Watts I, Walls S, Jones G (2006) Differential habitat selection by Pipistrellus pipistrellus and Pipistrellus pygmaeus identifies distinct conservation needs for cryptic species of echolocating bats. Biol Conserv 133:118–127CrossRefGoogle Scholar
  17. Dietrich S, Szameitat DP, Kiefer A, Schnitzler HU, Denzinger A (2006) Echolocation signals of the plecotine bat, Plecotus macrobullaris Kuzyakin, 1965. Acta Chiropterol 8:465–475CrossRefGoogle Scholar
  18. Entwistle AC, Racey PA, Speakman JR (1996) Habitat exploitation by a gleaning bat, Plecotus auritus. Philos Trans Royal Soc B 351:921–931CrossRefGoogle Scholar
  19. Frey-Ehrenbold A, Bontadina F, Arlettaz R, Obrist M (2013) Landscape connectivity, habitat structure and activity of bat guilds in farmland-dominated matrices. J Appl Ecol 50:252–261CrossRefGoogle Scholar
  20. Gonseth Y, Wohlgemuth T, Sansonnes B, Buttler A (2001) Die biogeographischen Regionen der Schweiz. Erläuterungen und Einteilungsstandard. Bundesamt für Umwelt, Wald und Landschaft, BernGoogle Scholar
  21. Hooge PN, Eichenlaub W (1997) Animal movement extension to arcview. ver. 1.1. Alaska Science Center—Biological Science Office, U.S. Geological Survey, AnchorageGoogle Scholar
  22. Hosmer DW, Lemeshow S (1989) Applied logistic regression. Wiley, New YorkGoogle Scholar
  23. Hutchinson GE (1978) An introduction to population ecology. Yale University, New HavenGoogle Scholar
  24. IUCN (2011) IUCN red list of threatened species. Version 2009.2. <>. Accessed 14 May 2012
  25. Johnson CJ, Boyce MS, Case RL, Cluff HD, Gau RJ, Gunn A, Mulders R (2005) Cumulative effects of human developments on arctic wildlife. Wildl Monogr 160:1–36 Google Scholar
  26. Kiefer A, Veith M (2001) A new species of long-eared bat from Europe (Chiroptera: Vespertilionidae). Myotis 39:5–16Google Scholar
  27. Kiefer A, Mayer F, Kosuch J, Von Helversen O, Veith M (2002) Conflicting molecular phylogenies of European long-eared bats (Plecotus) can be explained by cryptic diversity. Mol Phylogenet Evol 25:557–566PubMedCrossRefGoogle Scholar
  28. Krebs CJ (1999) Ecological methodology. Benjamin Cummings, Menlo ParkGoogle Scholar
  29. Kunz TH, Parsons S (2009) Ecological and behavioral methods for the study of bats. Johns Hopkins University Press, BaltimoreGoogle Scholar
  30. Kurta A, Bell GP, Nagy KA, Kunz TH (1989) Energetics of pregnancy and lactation in free-ranging little brown bats (Myotis lucifugus). Physiol Zool 62(3):804–818Google Scholar
  31. Murphy SE, Greenaway F, Hill DA (2012) Patterns of habitat use by female brown long-eared bats presage negative impacts of woodland conservation management. J Zool 288(3):177–183CrossRefGoogle Scholar
  32. Nicholls B, Racey PA (2006) Habitat selection as a mechanism of resource partitioning in two cryptic bat species Pipistrellus pipistrellus and Pipistrellus pygmaeus. Ecography 29:697–708CrossRefGoogle Scholar
  33. Obrist MK, Rathey E, Bontadina F, Martinoli A, Conedera M, Christe P, Moretti M (2011) Response of bat species to sylvo-pastoral abandonment. For Ecol Manag 261:789–798CrossRefGoogle Scholar
  34. Pianka ER (1969) Sympatry of desert lizards (Ctenotus) in western-Australia. Ecology 50:1012CrossRefGoogle Scholar
  35. Preatoni DG, Spada M, Wauters LA, Tosi G, Martinoli A (2011) Habitat use in the female alpine long-eared bat (Plecotus macrobullaris): does breeding make the difference? Acta Chiropterol 13(2):355–364CrossRefGoogle Scholar
  36. Ransome R (1990) The natural history of hibernating bats. Christopher Helm, LondonGoogle Scholar
  37. Razgour O, Hanmer J, Jones G (2011) Using multi-scale modelling to predict habitat suitability for species of conservation concern: the grey long-eared bat as a case study. Biol Conserv 144(12):2922–2930CrossRefGoogle Scholar
  38. R Development Core Team (2009) R: A language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria, ISBN 3-900051-07-0. Accessed 21 Dec 2009
  39. Ricklefs R (1990) Ecology. WH Freeman and Company, New YorkGoogle Scholar
  40. Russo D, Jones G, Migliozzi A (2002) Habitat selection by the Mediterranean horseshoe bat, Rhinolophus euryale (Chiroptera: Rhinolophidae) in a rural area of southern Italy and implications for conservation. Biol Conserv 107:71–81CrossRefGoogle Scholar
  41. Rutishauser MD, Bontadina F, Braunisch V, Ashrafi S, Arlettaz R (2012) The challenge posed by newly discovered cryptic species: disentangling the environmental niches of long-eared bats. Divers Distrib 18(11):1107–1119CrossRefGoogle Scholar
  42. Schnitzler HU, Kalko EKV (2001) Echolocation by insect-eating bats. Bioscience 51:557–569CrossRefGoogle Scholar
  43. Schoener TW (1974) Resource partitioning in ecological communities. Science 185:27–39PubMedCrossRefGoogle Scholar
  44. Schoener TW (1986) Resource partitioning. In: Kikkawa J, Anderson DJ (eds) Community ecology: pattern and process: 91. Blackwell Scientific Publications, MelbourneGoogle Scholar
  45. Schonrogge K, Barr B, Wardlaw JC, Napper E, Gardner MG, Breen J, Elmes GW, Thomas JA (2002) When rare species become endangered: cryptic speciation in myrmecophilous hoverflies. Biol J Linn Soc 75(3):291–300Google Scholar
  46. Spitzenberger F, Strelkov P, Haring E (2003) Morphology and mitochondrial DNA sequences show that Plecotus alpinus Kiefer & Veith, 2002 and Plecotus microdontus Spitzenberger, 2002 are synonyms of Plecotus macrobullaris Kuzjakin, 1965. Nat Croat 12(2):39–53Google Scholar
  47. Spitzenberger F, Strelkov PP, Winkler H, Haring E (2006) A preliminary revision of the genus Plecotus (Chiroptera, Vespertilionidae) based on genetic and morphological results. Zool Scr 35:187–230CrossRefGoogle Scholar
  48. Stebbings RE (1988) The conservation of European bats. Christopher Helm, LondonGoogle Scholar
  49. Swift SM, Racey PA (1983) Resource partitioning in two species of vespertilionid bats (Chiroptera) occupying the same roost. J Zool 200:249–259CrossRefGoogle Scholar
  50. Tews J, Brose U, Grimm V, Tielborger K, Wichmann MC, Schwager M, Jeltsch F (2004) Animal species diversity driven by habitat heterogeneity/diversity: the importance of keystone structures. J Biogeog 31:79–92CrossRefGoogle Scholar
  51. Walsh AL, Harris S (1996a) Foraging habitat preferences of vespertilionid bats in Britain. J Appl Ecol 33:508–518CrossRefGoogle Scholar
  52. Walsh AL, Harris S (1996b) Factors determining the abundance of vespertilionid bats in Britain: geographical, land class and local habitat relationships. J Appl Ecol 33:519–529CrossRefGoogle Scholar
  53. Wang ZL, Zhang DY, Wang G (2005) Does spatial structure facilitates coexistence of identical competitors? Ecol Model 181:17–23CrossRefGoogle Scholar
  54. White GC, Garrott RA (1990) Analysis of wildlife radio-tracking data. Academic Press, Inc., San DiegoGoogle Scholar
  55. Whittingham MJ, Swetnam RD, Wilson JD, Chamberlain DE, Freckleton RP (2005) Habitat selection by yellow hammers Emberiza citrinella on lowland farmland at two spatial scales: implications for conservation management. J Appl Ecol 42:270–280CrossRefGoogle Scholar
  56. Whittingham MJ, Stephens PA, Bradbury RB, Freckleton RP (2006) Why do we still use stepwise modelling in ecology and behaviour? J Anim Ecol 75:1182–1189PubMedCrossRefGoogle Scholar
  57. Wickramasinghe LP, Harris S, Jones G, Jennings NV (2004) Abundance and species richness of nocturnal insects on organic and conventional farms: effects of agricultural intensification on bat foraging. Conserv Biol 18:1283–1292CrossRefGoogle Scholar
  58. Wing MG, Tynon J (2006) Crime mapping and spatial analysis in national forests. J For 104:293–298Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Sohrab Ashrafi
    • 1
    • 2
    Email author
  • Marianne Rutishauser
    • 1
  • Klaus Ecker
    • 3
  • Martin K. Obrist
    • 3
  • Raphaël Arlettaz
    • 1
  • Fabio Bontadina
    • 1
    • 3
    • 4
    Email author
  1. 1.Division of Conservation Biology, Institute of Ecology and EvolutionUniversity of BernBernSwitzerland
  2. 2.Department of Environmental Science, Faculty of Natural ResourcesUniversity of TehranKarajIran
  3. 3.Swiss Federal Institute for Forest, Snow and Landscape Research WSL, Biodiversity and Conservation BiologyBirmensdorfSwitzerland
  4. 4.SWILD—Urban Ecology & Wildlife ResearchZurichSwitzerland

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