Biodiversity and Conservation

, Volume 23, Issue 3, pp 617–631 | Cite as

The trans-boundary importance of artificial bat hibernacula in managed European forests

  • Christian C. Voigt
  • Linn S. Lehnert
  • Ana G. Popa-Lisseanu
  • Mateusz Ciechanowski
  • Péter Estók
  • Florian Gloza-Rausch
  • Tamás Görföl
  • Matthias Göttsche
  • Carsten Harrje
  • Meike Hötzel
  • Tobias Teige
  • Reiner Wohlgemuth
  • Stephanie Kramer-Schadt
Original Paper

Abstract

Many European migratory bat species hibernate in large hollow trees, a decreasing resource in present day silviculture. Here, we report on the importance of man-made hibernacula to support trans-boundary populations of noctule bats (Nyctalus noctula), a species that performs seasonal long distance movements throughout Europe. In winter, we surveyed nine bat roosts (eight artificial and one natural) in Germany and collected small tufts of fur from a total of 608 individuals. We then measured the stable isotope ratios of the non-exchangeable hydrogen in fur keratin and estimated the origin of migrants using a refined isoscape origin model that included information on expected flight distances and migration directions. According to the stable isotope signature, 78 % of hibernating bats originated from local populations. The remaining 22 % of hibernacula occupants originated from distant populations, mostly from places in northern or eastern countries such as Sweden, Poland and Baltic countries. Our results confirm that many noctule bats cross one or several political borders during migration. Data on the breeding origin of hibernating noctule bats also suggest that artificial roosts may not only be important for local but also for distant populations. Protection of natural and artificial hibernacula in managed forests may support the trans-boundary populations of migratory bats when hollow trees are scarce in managed forests.

Keywords

Chiroptera Compensation Conservation Migratory species Isoscape origin model Spatial model GIS 

References

  1. Agostinelli C, Lund U (2011) R package ‘circular’: Circular Statistics version 0.4-3. https://r-forge.r-project.org/projects/circular/. Accessed 10 Oct 2013
  2. Blohm T, Heise G (2008) Großer Abendsegler Nyctalus noctula Schreber, 1774 in: Naturschutz und Landschaftspflege in Brandenburg – Beiträge zu Ökologie, Natur- und Gewässerschutz. Natursch Landschaftspfl Brandenbg 17:153–160Google Scholar
  3. Boehm SM, Wells K, Kalko EKV (2011) Top-down control of herbivory by birds and bats in the canopy of temperate broad-leaved oaks Quercus robur. PLoS ONE 6:e17857CrossRefGoogle Scholar
  4. Boonman M (2000) Roost selection by noctules Nyctalus noctula and Daubenton’s bats Myotis daubentoni. J Zool 251:385–389CrossRefGoogle Scholar
  5. Bowen GJ, Wassenaar LL, Hobson KA (2005) Global application of stable hydrogen and oxygen isotopes to wildlife forensics. Oecologia 143:337–348PubMedCrossRefGoogle Scholar
  6. Ciechanowski M (2005) Utilization of artificial shelters by bats Chiroptera in three different types of forest. Folia Zool 54:31–37Google Scholar
  7. Crampton LH, Barclay RMR (1998) Selection of roosting and foraging habitat by bats in different-aged aspen mixed wood stands. Conserv Biol 12:1347–1358CrossRefGoogle Scholar
  8. Cryan PM, Bogan MA, Rye RO, Landis GP, Kester CL (2004) Stable hydrogen isotope analysis of bat hair as evidence for seasonal molt and long-distance migration. J Mammal 85:995–1001CrossRefGoogle Scholar
  9. Delignette-Muller ML, Pouillot R, Denis J-B, Dutang C (2013) Fitdistrplus: help to fit of a parametric distribution to non-censored or censored data. R package version 2.0-12Google Scholar
  10. Dietz C, von Helversen O, Nill D (2009) Handbook of bats of Europe and Northwest Africa. A C Books, SeattleGoogle Scholar
  11. Erzberger A, Popa-Lisseanu A, Lehmann GUC, Voigt CC (2011) Potential and limits in detecting altitudinal movements of bats using stable hydrogen isotope ratios of fur keratin. Acta Chiropt 13:431–438CrossRefGoogle Scholar
  12. Evans D (2012) Building the European Union’s Natura 2000 network. Nat Conserv 1:11–16CrossRefGoogle Scholar
  13. Fernandez C, Azkona P (1996) Influence of forest structure on the density and distribution of the white-backed woodpecker Dendrocopos leucotos and black woodpecker Dryocopus martius in Quinto Real (Spanish western Pyrenees). Bird Study 43:305–313CrossRefGoogle Scholar
  14. Furmankiewicz J, Kucharska M (2009) Migration of bats along a large river valley in southwestern Poland. J Mammal 90:1310–1317CrossRefGoogle Scholar
  15. Ghanem SJ, Voigt CC (2012) Increasing awareness of ecosystem services provided by bats. Adv Study Behav 44:279–302CrossRefGoogle Scholar
  16. Gossner MM, Lachat T, Brunet J et al (2013) Current near-to-nature forest management effects on functional trait composition of saproxylic beetles in beech forests. Cons Biol 27:605–614CrossRefGoogle Scholar
  17. Gunnarsson G, Latorre-Margelef N, Hobson KA et al (2012) Disease dynamics and bird migration—linking mallards Anas platyrhynchos and subtype diversity of the Influenca A virus in time and space. PLoS ONE 7:e35679PubMedCentralPubMedCrossRefGoogle Scholar
  18. Heise G, Blohm T (2012) Arbeit mit Fledermauskästen—sinnvoll oder nicht? Nyctalus 17:226–239Google Scholar
  19. Hijmans RJ, van Etten J (2012) Raster: Geographic analysis and modelling with raster data. R package version 2.0-12Google Scholar
  20. Hijmans RJ, Williams E, Vennes C (2012) Geosphere: spherical trigonometry. R package version 1.2-28. http://CRAN.R-project.org/package=geosphere
  21. Hobson KA (1999) Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia 120:314–326CrossRefGoogle Scholar
  22. Hutterer R, Ivanova T, Meyer-Cordes C, Rodrigues L (2005) Bat migrations in Europe—a review of banding data and literature. Natursch Biol Vielf 28:41–43Google Scholar
  23. Jung K, Kaiser S, Bohm S, Nieschzlze J, Kalko EKV (2012) Moving in three dimensions: effects of structural complexity on occurance and activity of insectivorous bats in managed forest stands. J Appl Ecol 49:523–531CrossRefGoogle Scholar
  24. Kouki J, Väänänen A (2000) Impoverishment of resident old growth forest bird assemblages along an isolution gradient of protected areas in eastern Finland. Ornis Fennica 77:145–154Google Scholar
  25. Legendre P (2008) lmodel2: Model II Regression. R package version 1.6-3Google Scholar
  26. Marra PP, Hobson KA, Holmes RT (1998) Linking winter and summer events in a migratory bird by using stable-carbon isotopes. Science 282:1884–1886PubMedCrossRefGoogle Scholar
  27. Meschede A, Heller K-G (2000) Ökologie und Schutz von Fledermäusen in Wäldern. Schriftenreihe Landschaftspfl Natursch 66:374Google Scholar
  28. Mikusiński G, Angelstam P (1998) Economic geography, forest distribution, and woodpecker diversity in Central Europe. Conserv Biol 12:200–208CrossRefGoogle Scholar
  29. Moning C, Muller J (2009) Critical forest age thresholds for the diversity of lichens, mollusks and birds in beech (Fagus sylvatica) dominated forests. Ecol Indica 9:922–932CrossRefGoogle Scholar
  30. Niemela J, Young J, Alard D et al (2005) Identifying, managing and monitoring conflicts between forest biodiversity conservation and other human interests in Europe. Forest Policy Econ 7:877–890CrossRefGoogle Scholar
  31. Norris DR, Marra PP, Kyser TK, Sheery TW, Ratcliffe L (2004) Tropical winter habitat limits reproductive success on the temperate breeding grounds in a migratory bird. Proc R Soc Lond B 271:59–64CrossRefGoogle Scholar
  32. Ossa G, Kramer-Schadt S, Peel AJ, Scharf AK, Voigt CC (2012) The movement ecology of the straw-colored fruit bat, Eidolon helvum, in sub-Saharan Africa assessed by stable isotopes ratios. PLoS ONE 7:e37101CrossRefGoogle Scholar
  33. Ostermann OP (1998) The need for management of nature conservation sites designated under Natura 2000. J Appl Ecol 35:968–973CrossRefGoogle Scholar
  34. Petit E, Mayer F (1999) Male dispersal in the noctule bat Nyctalus noctula: where are the limits? Proc R Soc Lond B 266:1717–1722CrossRefGoogle Scholar
  35. Popa-Lisseanu AG, Soergel K, Luckner A et al (2012) A triple isotope approach to predict breeding origins of European bats. PLoS ONE 7:e30388PubMedCentralPubMedCrossRefGoogle Scholar
  36. 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. http://www.R-project.org. Accessed 10 Oct 2013
  37. Robbins CS, Sauer JR, Greenberg RS, Droege S (1989) Population declines in North American birds that migrate to the neotropics. Proc Nat Acad Sci USA 86:7658–7662PubMedCrossRefGoogle Scholar
  38. Ruczyński I, Bogdanowicz W (2005) Roost cavity selection by Nyctalus noctula and L. leisleri Vespertilionidae, Chiroptera in Białowiża primeval forest, eastern Poland. J Mammal 85:921–930CrossRefGoogle Scholar
  39. Russo D, Cistrone L, Garonna AP, Jones G (2010) Reconsidering the importance of harvested forests for the conservation of tree-welling bats. Biodiv Conserv 19:2501–2515CrossRefGoogle Scholar
  40. Rydell J, Bach L, Dubourg-Savage M-J, Green M, Rodriguez L, Hedenström A (2010) Bat mortality at wind turbines in northwestern Europe. Acta Chiropterol 12:261–274CrossRefGoogle Scholar
  41. Schmidt A (2010) Zum Überwinterungsverhalten des Abendseglers Nyctalus noctula in Ostbrandenburg. Nyctalus 15:223–234Google Scholar
  42. Sherry TW, Holmes RT (1996) Winter habitat quality, population limitation, and conservation of Neotropical-nearctic migrant birds. Ecology 77:36–48CrossRefGoogle Scholar
  43. Steffens R, Zöphel U, Brockmann D (2004) 40 Jahre Fledermauskartierungszentrale Dresden—methodische Hinweise und Ergebnisübersicht. Sächsisches Landesamt für Umwelt und GeologieGoogle Scholar
  44. Studds CE, McFarland KP, Aubry Y, Rimmer CC, Hobson KA, Marra PP, Wassenaar LI (2012) Stable-hydrogen isotope measures of natal dispersal reflect observed population declines in a threatened migratory songbird. Div Distr 18:919–930CrossRefGoogle Scholar
  45. Sullivan AR, Bump JK, Kriger LA, Peterson RO (2012) Bat-cave catchment areas: using stable isotopes (δD) to determine the probable origins of hibernating bats. Ecol Appl 22:1428–1434PubMedCrossRefGoogle Scholar
  46. Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, New York. ISBN 0-387-95457-0CrossRefGoogle Scholar
  47. Viana DS, Santamaria L, Michot TC, Figuerola J (2013) Allometric scaling of long-distance seed dispersal by migratory birds. Am Nat 181:649–662PubMedCrossRefGoogle Scholar
  48. Voigt CC, Popa-Lisseanu A, Niermann I, Kramer-Schadt S (2012) The catchment area of wind farms for European bats: a plea for international regulations. Biol Conserv 153:80–86CrossRefGoogle Scholar
  49. Voigt CC, Helbig-Bonitz M, Kramer-Schadt S, Kalko EKV (2013) The third dimension of bat migration: Elevational movements of Miniopterus natalensis at Mount Kilimanjaro. Oecologia. doi:10.1007/s00442-013-2819-0 Google Scholar
  50. Young J, Watt A, Nowicki P, Alard D, Clitherow J, Henle K, Johnson R, Laczko E, McCracken D, Matouch S, Niemela J, Richards C (2005) Towards sustainable land use: identifying and managing the conflicts between human activities and biodiversity conservation in Europe. Biodiv Conserv 14:1641–1661CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Christian C. Voigt
    • 1
  • Linn S. Lehnert
    • 1
  • Ana G. Popa-Lisseanu
    • 1
  • Mateusz Ciechanowski
    • 2
  • Péter Estók
    • 3
  • Florian Gloza-Rausch
    • 4
  • Tamás Görföl
    • 5
    • 6
  • Matthias Göttsche
    • 7
  • Carsten Harrje
    • 7
  • Meike Hötzel
    • 8
  • Tobias Teige
    • 1
  • Reiner Wohlgemuth
    • 9
  • Stephanie Kramer-Schadt
    • 1
  1. 1.Leibniz Institute for Zoo and Wildlife ResearchBerlinGermany
  2. 2.Department of Vertebrate Ecology and ZoologyUniversity of GdańskGdańskPoland
  3. 3.Department of ZoologyEszterházy Károly CollegeEgerHungary
  4. 4.Noctalis, Fledermauszentrum GmbHBad SegebergGermany
  5. 5.Department of ZoologyHungarian Natural History MuseumBudapestHungary
  6. 6.Institute for Veterinary Medical Research, Centre for Agricultural Research, Hungarian Academy of SciencesBudapestHungary
  7. 7.Faunistisch-Ökologische Arbeitsgemeinshaft, AG WirbeltiereÖkologie-Zentrum Der UniversitätKielGermany
  8. 8.WittenGermany
  9. 9.HolzwickedeGermany

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