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Managing anthropogenic driven range expansion behaviourally: Mediterranean bats in desert ecosystems

  • Asael Greenfeld
  • David Saltz
  • Dror Kapota
  • Carmi Korine
Original Article

Abstract

Bat abundance and activity in deserts is affected by the distribution of water sources. Kuhl’s pipistrelle (Pipistrellus kuhlii) is one of several bat species that penetrated the Negev desert from Mediterranean habitats following anthropogenic development, and potentially competes with desert dwelling bats of the same guild. Pipistrellus kuhlii is an obligate drinker requiring a clear ‘swoop zone’ to drink. Thus, to reduce the competitive load that P. kuhlii has on desert dwelling species, we tested the effectiveness of obstructions above water surfaces, which we hypothesised would reduce the drinking ability of P. kuhlii, thus providing desert species a competitive edge. We obstructed the water surface of a swimming pool and successfully prevented P. kuhlii from drinking. Next, we manipulated natural water sources used by bats for foraging. This was done on two spatial and temporal scales: on 11 adjacent ephemeral water pools in Nahal Zin where each treatment was applied for several nights and on eight isolated natural pools in the Negev where treatments were alternated every 20 min. Manipulation of adjacent pools had no effect on activity levels of bats, but in isolated pools, the obstruction reduced the proportion of P. kuhlii activity by up to 15%. Although this tool cannot be used for management without further examination of its long-term effects on other bats and wildlife, this study does demonstrate its feasibility. Conservation schemes aiming to mitigate effects of undesirable species can be designed by identifying ecological differences between competing species, and manipulating the environment accordingly.

Keywords

Competition Conservation Insectivorous bats Mitigation Range expansion Water 

Notes

Acknowledgments

Field work was carried out with the help of many friends including K. Edwards and B. Evans from the University of Bristol, UK. We thank N. Werner and U. Shanas for lending us the equipment. This research was done under permit 34613 from the Israel Nature and National Parks Protection Authority (INPA). We also acknowledge the INPA for the assistance and advice of their rangers and professional staff. This research was funded through grants from Ben-Gurion University Seed Money to C.K and D.S and the Ministry of Technology and Science to C.K. This is publication no. 963 of the Mitrani Department of Desert Ecology.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Human and animal welfare

All applicable international, national and institutional guidelines for the care and use of animals were followed as stated in research permit 34613 from the Israel Nature and National Parks Protection Authority. The field experiments were conducted under licence 34615 given to CK by the Israel Nature and Parks Authority and under the permit BGU-R-2009 to CK from BGU Committee for the Ethical Care and Use of Animals in Experiments. This includes careful choice of study sites to avoid manipulating sensitive water sources that would make water entirely unavailable to wildlife. This article does not contain any studies with human participants performed by any of the authors.

Supplementary material

10344_2018_1182_MOESM1_ESM.docx (16 kb)
ESM 1 (DOCX 16.3 kb)

References

  1. Ancillotto L, Santini L, Ranc N, Maiorano L, Russo D (2016) Extraordinary range expansion in a common bat: the potential roles of climate change and urbanisation. Sci Nat 103:15.  https://doi.org/10.1007/s00114-016-1334-7 CrossRefGoogle Scholar
  2. Arlettaz R (1996) Feeding behaviour and foraging strategy of free-living mouse-eared bats, Myotis myotis and Myotis blythii. Anim Behav 51:1–11.  https://doi.org/10.1006/anbe.1996.0001 CrossRefGoogle Scholar
  3. 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.  https://doi.org/10.1016/S0006-3207(99)00112-3 CrossRefGoogle Scholar
  4. Benda P, Dietz C, Andreas M et al (2008) Bats (Mammalia: Chiroptera) of the eastern Mediterranean and Middle East. Part 6. Bats of Sinai (Egypt) with some taxonomic, ecological and echolocation data on that fauna. Acta Soc Zool Bohemoslov / Bohemicae 72:1–103Google Scholar
  5. Berger-Tal O, Berger-Tal R, Korine C, Holderied MW, Fenton MB (2008) Echolocation calls produced by Kuhl’s pipistrelles in different flight situations. J Zool 274:59–64.  https://doi.org/10.1111/j.1469-7998.2007.00357.x Google Scholar
  6. Berger-Tal O, Polak T, Oron A, Lubin Y, Kotler BP, Saltz D (2011) Integrating animal behavior and conservation biology: a conceptual framework. Behav Ecol 22:236–239.  https://doi.org/10.1093/beheco/arq224 CrossRefGoogle Scholar
  7. Bilushenko AA (2013) The current status of Kuhl’s Pipistrelle, Pipistrellus kuhlii (Chiroptera, Vespertilionidae), in the central forest-steppe of Ukraine. Vestn Zool 47:343–349.  https://doi.org/10.2478/vzoo-2013-0036 Google Scholar
  8. Biscardi S, Russo D, Casciani V, Cesarini D, Mei M, Boitani L (2007) Foraging requirements of the endangered long-fingered bat: the influence of micro-habitat structure, water quality and prey type. J Zool 273:372–381CrossRefGoogle Scholar
  9. Briggs P (2004) Effect of barn conversion on bat roost sites in Hertfordshire, England. Mammalia 68:353–364CrossRefGoogle Scholar
  10. Burnham KP, Anderson DR (2002) Model selection and multi-model inference. Springer, New York, p 2002Google Scholar
  11. Ciechanowski M (2002) Community structure and activity of bats (Chiroptera) over different water bodies. Mamm Biol 67:276–285.  https://doi.org/10.1078/1616-5047-00042 CrossRefGoogle Scholar
  12. Dukes JS, Mooney HA (2004) Disruption of ecosystem processes in western North America by invasive species. Rev Chil Hist Nat 77:411–437.  https://doi.org/10.4067/S0716-078X2004000300003 CrossRefGoogle Scholar
  13. Falk-Petersen J, Bøhn T, Sandlund OT (2006) On the numerous concepts in invasion biology. Biol Invasions 8:1409–1424.  https://doi.org/10.1007/s10530-005-0710-6 CrossRefGoogle Scholar
  14. Feldman R, Whitaker JO Jr, Yom-Tov Y (2000) Dietary composition and habitat use in a desert insectivorous bat community in Israel. Acta Chiropterologica 2:15–22Google Scholar
  15. Fenton MB (1970) A technique for monitoring bat activity with results obtained from different environments in southern Ontario. Can J Zool 48:847–851CrossRefGoogle Scholar
  16. Greenfeld A (2012) Reducing the competitive load on desert bat communities by hampering the drinking ability of an invasive bat species, Kuhl’s pipistrelle (Pipistrellus kuhlii). Dissertation, Ben-Gurion University of the NegevGoogle Scholar
  17. Greif S, Siemers BM (2010) Innate recognition of water bodies in echolocating bats. Nat Commun 1:107.  https://doi.org/10.1038/ncomms1110 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Griffiths SR, Bender R, Godinho LN, Lentini PE, Lumsden LF, Robert KA (2017) Bat boxes are not a silver bullet conservation tool. Mamm Rev 47:261–265.  https://doi.org/10.1111/mam.12097 CrossRefGoogle Scholar
  19. Hackett TD, Korine C, Holderied MW (2013) The importance of Acacia trees for insectivorous bats and arthropods in the Arava desert. PLoS One 8:e52999.  https://doi.org/10.1371/journal.pone.0052999 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Hall LK, Lambert CT, Larsen RT, Knight RN, McMillan BR (2016) Will climate change leave some desert bat species thirstier than others? Biol Conserv 201:284–292.  https://doi.org/10.1016/j.biocon.2016.07.020 CrossRefGoogle Scholar
  21. Hawlena D, Bouskila A (2006) Land management practices for combating desertification cause species replacement of desert lizards. J Appl Ecol 43:701–709.  https://doi.org/10.1111/j.1365-2664.2006.01177.x CrossRefGoogle Scholar
  22. Israel Meteorology Service (2012) Israel Meteorology Service Climate information. In: gov.il. https://ims.data.gov.il/. Accessed 2 Feb 2017
  23. Jackrel SL, Matlack RS (2010) Influence of surface area, water level and adjacent vegetation on bat use of artificial water sources. Am Midl Nat 164:74–79CrossRefGoogle Scholar
  24. Juste J, Paunović M (2016) Pipistrellus kuhlii. The IUCN Red List of Threatened Species. http://www.iucnredlist.org. Accessed 17 Feb 2017
  25. Korine C, Adams AM, Shamir U, Gross A (2015) Effect of water quality on species richness and activity of desert-dwelling bats. Mamm Biol - Zeitschrift für Säugetierkd 80:185–190.  https://doi.org/10.1016/j.mambio.2015.03.009 CrossRefGoogle Scholar
  26. Korine C, Adams R, Russo D, Fisher-Phelps M, Jacobs D (2016) Bats and water: anthropogenic alterations threaten global bat populations. In: Voigt CC, Kingston T (eds) Bats in the Anthropocene: conservation of bats in a changing world. Springer, New York, pp 215–233CrossRefGoogle Scholar
  27. Korine C, Pinshow B (2004) Guild structure, foraging space use, and distribution in a community of insectivorous bats in the Negev desert. J Zool London 262:187–196.  https://doi.org/10.1017/S0952836903004539 CrossRefGoogle Scholar
  28. Lisón F, Calvo JF (2011) The significance of water infrastructures for the conservation of bats in a semiarid Mediterranean landscape. Anim Conserv 14:533–541.  https://doi.org/10.1111/j.1469-1795.2011.00460.x CrossRefGoogle Scholar
  29. Norberg UM, Rayner JMV (1987) Ecological morphology and flight in bats (Mammalia; Chiroptera): wing adaptations, flight performance, foraging strategy and echolocation. Philos Trans R Soc B Biol Sci 316:335–427CrossRefGoogle Scholar
  30. Polak T, Korine C, Yair S, Holderied MW (2011) Differential effects of artificial lighting on flight and foraging behaviour of two sympatric bat species in a desert. J Zool 285. doi:  https://doi.org/10.1111/j.1469-7998.2011.00808.x
  31. Portnov BAA, Safriel UNN (2004) Combating desertification in the Negev: dryland agriculture vs. dryland urbanisation. J Arid Environ 56:659–680.  https://doi.org/10.1016/S0140-1963(03)00087-9 CrossRefGoogle Scholar
  32. Racey PR, Swift SM, Rydell J, Brodie L (1998) Bats and insects over two Scottish rivers with contrasting nitrate status. Anim Conserv 1:195–202.  https://doi.org/10.1111/j.1469-1795.1998.tb00029.x CrossRefGoogle Scholar
  33. R Core Team (2013). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/.
  34. Razgour O, Korine C, Saltz D (2010) Pond characteristics as determinants of species diversity and community composition in desert bats. Anim Conserv 13:505–513.  https://doi.org/10.1111/j.1469-1795.2010.00371.x CrossRefGoogle Scholar
  35. Razgour O, Korine C, Saltz D (2011) Does interspecific competition drive patterns of habitat use in desert bat communities? Oecologia 167:493–502.  https://doi.org/10.1007/s00442-011-1995-z CrossRefPubMedGoogle Scholar
  36. Rebelo H, Brito JC (2007) Bat guild structure and habitat use in the Sahara desert. Afr J Ecol 45:228–230.  https://doi.org/10.1111/j.1365-2028.2006.00721.x CrossRefGoogle Scholar
  37. Russo D, Ancillotto L (2015) Sensitivity of bats to urbanisation: a review. Mamm Biol 80:205–212.  https://doi.org/10.1016/j.mambio.2014.10.003 CrossRefGoogle Scholar
  38. Russo D, Cistrone L, Jones G (2012) Sensory ecology of water detection by bats: a field experiment. PLoS One 7:1–9.  https://doi.org/10.1371/journal.pone.0048144 Google Scholar
  39. Russo D, Cistrone L, Libralato N, Korine C, Jones G, Ancillotto L (2017) Adverse effects of artificial illumination on bat drinking activity. Anim Conserv 20:492–501.  https://doi.org/10.1111/acv.12340 CrossRefGoogle Scholar
  40. Sachanowicz K, Wower A, Bashta A-T (2006) Further range extension of Pipistrellus kuhlii (Kuhl, 1817) in central and eastern Europe. Acta Chiropterologica 8:543–548CrossRefGoogle Scholar
  41. Salvarina I (2016) Bats and aquatic habitats: a review of habitat use and anthropogenic impacts. Mamm Rev 46:131–143.  https://doi.org/10.1111/mam.12059 CrossRefGoogle Scholar
  42. Seibold S, Buchner J, Bässler C, Müller J (2013) Ponds in acidic mountains are more important for bats in providing drinking water than insect prey. J Zool 290:302–308.  https://doi.org/10.1111/jzo.12041 CrossRefGoogle Scholar
  43. Simberloff DS (2010) Invasive species. In: Sodhi NS, Ehrlich PR (eds) Conservation biology for all. Oxford press, Oxford, pp 131–152CrossRefGoogle Scholar
  44. Sirami C, Jacobs DS, Cumming GS (2013) Artificial wetlands and surrounding habitats provide important foraging habitat for bats in agricultural landscapes in the western cape, South Africa. Biol Conserv 164:30–38.  https://doi.org/10.1016/j.biocon.2013.04.017 CrossRefGoogle Scholar
  45. Szewczak JM, Szewczak SM, Morrison ML, Hall LS (1998) Bats of the white and Inyo Mountains of California-Nevada. Gt Basin Nat 58:66–75Google Scholar
  46. Tomassini A, Colangelo P, Agnelli P, Jones G, Russo D (2014) Cranial size has increased over 133 years in a common bat, Pipistrellus kuhlii: a response to changing climate or urbanisation? J Biogeogr 41:944–953.  https://doi.org/10.1111/jbi.12248 CrossRefGoogle Scholar
  47. Tuttle SR, Chambers CL, Theimer TC (2006) Potential effects of livestock water-trough modifications on bats in northern Arizona. Wildl Soc Bull 34:602–608.  https://doi.org/10.2193/0091-7648(2006) CrossRefGoogle Scholar
  48. Vaughan N, Jones G, Harris S (1996) Effects of sewage effluent on the activity of bats (Chiroptera: Vespertilionidae) foraging along rivers. Biol Conserv 78:337–343.  https://doi.org/10.1016/S0006-3207(96)00009-2 CrossRefGoogle Scholar
  49. Welch JN, Leppanen C (2017) The threat of invasive species to bats: a review. Mamm Rev 47:277–290.  https://doi.org/10.1111/mam.12099 CrossRefGoogle Scholar
  50. Whitaker JO, Shalmon B, Kunz TH (1994) Food and feeding-habits of insectivorous bats from Israel. Zeitschrift Fur Saugetierkunde-international J. Mamm Biol 59:74–81Google Scholar
  51. Wittenberg R, Cock MJW (2001) Invasive alien species: a toolkit of best prevention and management practices. CAB Int, OxonCrossRefGoogle Scholar
  52. Yom-Tov Y (1993) Character displacement among the isectivorous bats of the Dead Sea area. J Zool 230:347–356Google Scholar
  53. Yom-Tov Y, Mendelssohn H (1988) Changes in the distribution and abundance of vertebrates in Israel during the twentieth century. Monogr Biol 62:515–547Google Scholar
  54. Zuur AF, Ieno EN, Walker NJ, et al (2013) Mixed effects models and extensions in ecology with R. Springer-Verlag, New YorkGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Mitrani Department of Desert Ecology, Jacob Blaustein Institutes for Desert ResearchBen-Gurion University of the NegevMidreshet Ben-GurionIsrael
  2. 2.Department of Environment and AgricultureCurtin UniversityBentleyAustralia
  3. 3.Department of Economics and ManagementTel Hai CollegeUpper GalileeIsrael

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