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Mammalian Biology

, Volume 80, Issue 3, pp 191–204 | Cite as

Mitigating the impacts of agriculture on biodiversity: bats and their potential role as bioindicators

  • Kirsty J. ParkEmail author
Review
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Abstract

Agriculture is a dominant land use worldwide with approximately 40% of the land’s surface used for farming. In many countries, particularly parts of Europe, this figure is substantially higher and most agricultural land is under intensive practices aimed at maximising the production of food. The intensification and expansion of modern agricultural practices led to the biological simplification of the farmed environment, which has resulted in declines in farmland biodiversity during the last century. As with other taxa, many bat species have suffered severe population declines during the 20th century, with agriculture believed to be one of the main drivers reducing roost availability and foraging habitat. Lower intensity farming methods, and the creation or management of habitat features on farmland could potentially mitigate some of these negative impacts but the effects of this on bats, in comparison to other taxa, have received relatively little attention. Here, I review evidence on the impacts of efforts to increase biodiversity in agricultural landscapes on bat populations, and explore whether responses of bats to agricultural activities are similar to those of other taxa, a necessary requirement if they are to be used as bioindicator species.

There are relatively few studies with which to assess the effects of management interventions on bats in agricultural landscapes, and these are restricted to only a few countries. Nevertheless, there is evidence that bats benefit from lower intensity agricultural systems, specifically organic farming and shaded agroforestry: these systems tend to be associated with higher bat abundance, species richness and diversity, and are more heavily utilised by foraging bats. Whilst very few studies have explicitly tested the utility of bats as bioindicators in agricultural landscapes, overall, the response of bats to lower intensity agricultural systems also reflects responses by other taxa. These studies have been largely restricted to temperate regions, however. The review highlights several major gaps in our knowledge of bats in agricultural landscapes and where future research could be usefully directed including: (1) a broader geographical range of studies examining both the efficacy, and the underlying mechanisms through which lower intensity agricultural systems may benefit bats; (2) the potential for lower intensity systems in key crops such as oil-palm; (3) studies of the demographic effects of conservation management on bats; (4) in order to assess the potential of bats as bioindicators, studies quantifying the response of both bats and other taxa to environmental change in a wider range of biomes and regions are needed.

Keywords

Chiroptera Agriculture Conservation Bioindicator species 

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References

  1. Abensperg-Traun, M., Wrbka, T., Bieringer, G., Hobbs, R., Deininger, F., York, B.M., Milasowszky, N., Sauberer, N., Zulka, K.P., 2004. Ecological restoration inthe slipstream of agricultural policy in the old and new world. Agricul. Ecosys. Environ. 103, 601–611.CrossRefGoogle Scholar
  2. Adams, R.A., Hayes, M.A., 2008. Water availability and successful lactation by bats as related to climate change in arid regions of western North America. J. Anim. Ecol. 6, 1115–1121.CrossRefGoogle Scholar
  3. Altringham, J.D., Senior, P., 2005. Social systems and ecology of bats. In: Ruckstuhl, K.E., Neuhaus, P. (Eds.), Sexual Segregation in Vertebrates. Cambridge University Press, Cambridge, United Kingdom, pp. 280–302.Google Scholar
  4. Altringham, J., 2011. Bats - From Evolution to Conservation. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
  5. Australian State of the Environment Committee, 2001. Australian State of the Environment Committee, CSIRO, Publishing on behalf of the Department of the Environment and Heritage, Available at: http://www.environment.gov.au/topics/science-and-research/state-environment-reporting/soe-2001/soe-2001-report
  6. Barclay, R.M., 1991. Population structure of temperate zone insectivorous bats in relation to foraging behaviour and energy demand. J. Anim. Ecol., 165–178.CrossRefGoogle Scholar
  7. Barlow, J., Gardner, T.A., Araujo, I.S., Avila-Pires, T.C., Bonaldo, A.B., Costa, J.E., Esposito, M.C., Ferreira, L.V., Hawes, M.I.M., Hernandez, M.I.M., Hoogmoed, M.S., Leite, R.N., Lo-Man-Hung, N.F., Malcolm, J.R., Martins, M.B., Mestre, L.A.M., Miranda-Sontos, R., Nunes-Gutjahr, A.L., Overal, W.L., Parry, L., Peters, S.L., Ribeiro-Junior, M.A., da Silva, M.N.F., da Silva Motta, C., Peres, C.A., 2007. Quantifying the biodiversity value of tropical primary, secondary and plantation forest. PNAS 104, 18555–18560.PubMedCrossRefPubMedCentralGoogle Scholar
  8. Barr, C.J., Gillespie, M.K., 2000. Estimating hedgerow length and pattern characteristics in Great Britain using Countryside Survey data. J. Environ. Manag. 60, 23–32.CrossRefGoogle Scholar
  9. Benton, T.G., Vickery, J.A., Wilson, J.D., 2003. Farmland biodiversity: is habitat heterogeneity the key? Trends Ecol. Evol. 18, 182–188.Google Scholar
  10. Berthinussen, A., Richardson, O.C., Altringham, J.D., 2014. Bat Conservation: Global Evidence for Intervention. Pelagic Publishing Ltd, Exeter, UK, pp. 106.Google Scholar
  11. Boughey, K.L., Lake, I.R., Haysom, K.A., Dolman, P.M., 2011a. Improving the biodiversity benefits of hedgerows: how physical characteristics and the proximity of foraging habitat affect the use of linear features by bats. Biol. Conserv. 144, 1790–1798.CrossRefGoogle Scholar
  12. Boughey, K.L., Lake, I.R., Haysom, K.A., Dolman, P.M., 2011b. Effects of landscape-scale broadleaved woodland configuration and extent on roost location for six bat species across the UK. Biol. Conserv. 144, 2300landscape-scale2310.CrossRefGoogle Scholar
  13. Boyles,J.G., Cryan, P.M., McCracken, G.F., Kunz, T.H., 2011. Economic importance of bats in agriculture. Science 332, 41–42.PubMedCrossRefPubMedCentralGoogle Scholar
  14. Carignan, V., Villard, M.A., 2002. Selecting indicator species to monitor ecological integrity: a review. Environ. Monit. Assess. 78, 45–61.PubMedCrossRefPubMedCentralGoogle Scholar
  15. Carson, R., 1962. Silent Spring. Houghton Mifflin Harcourt, Boston.Google Scholar
  16. Castro-Luna, A.A., Galindo-Gonzalez, J., 2012. Enriching agroecosystems with fruit-producing tree species favors the abundance and richness of frugivorous and nectarivorous bats in Veracruz, Mexico. Mamm. Biol. 77, 32–40.CrossRefGoogle Scholar
  17. Castro-Luna, A.A., Sosa, V.J., Castillo-Campos, G., 2007. Quantifying phyllostomid bats at different taxonomic levels as ecological indicators in a disturbed tropical forest. Acta Chirop. 9, 219–228.CrossRefGoogle Scholar
  18. Davy, C.M., Russo, D., Fenton, M.B., 2007. Use of native woodlands and traditional olive groves by foraging bats on a Mediterranean island: consequences for conservation. J. Zool. Lond. 273, 397–405.CrossRefGoogle Scholar
  19. Defra, 2005. Agricultural Practice and Bats: A Review of Current Research Literature and Management Recommendations. Project BD2005, Available at: http://randd.defra.gov.uk/Document.aspx?Document=BD2005_2103_FRP.doc.
  20. Defra, 2008. Agriculture in the United Kingdom. Department for Environment Food and Rural Affairs, Department of Agriculture and Rural Development (Northern Ireland), Welsh Assembly Government ‒ The Department for Rural Affairs and Heritage, The Scottish Government ‒ Rural and Environment Research and Analysis Directorate.Google Scholar
  21. Downs, N.C., Racey, P.A., 2006. The use by bats of habitat features in mixed farmland in Scotland. Acta Chiropterol. 8, 169–185.CrossRefGoogle Scholar
  22. EEA, 2005. Agriculture and Environment in EU-15 - The IRENA Indicator Report. Report No. 6/2005. European Environment Agency, Copenhagen.Google Scholar
  23. Estrada, A., Coates-Estrada, R., 2001. Species composition and reproductive phenology of bats in a tropical landscape at Los Tuxtlas, Mexico. J. Trop. Ecol. 17, 627–646.CrossRefGoogle Scholar
  24. Estrada, A., Coates-Estrada, R., Merritt, D., 1993. Bat species richness and abundance in tropical rain forest fragments and in agricultural habitats at Los Tuxtlas, Mexico. Ecography 16, 309–318.CrossRefGoogle Scholar
  25. Estrada, C.G., Damon, A., Hernández, C.S., Pinto, S.L., Núñez, G.I., 2006. Bat diversity in montane rainforest and shaded coffee under different management regimes in southeastern Chiapas, Mexico. Biol. Conserv. 132, 351–361.CrossRefGoogle Scholar
  26. EU, 2005. Agri-environment Measures - Overview on General Principles, Types of Measures, and Application. European Commission ‒ Directorate General for Agriculture and Rural Development, Available at: http://ec.europa.eu/agriculture/publi/reports/agrienv/rep_en.pdf
  27. Food and Agricultural Organisation, 2010. Progress towards sustainable forest management. In: Global Forest Resources Assessment. Food and Agricultural Organization ofthe United Nations, Rome, pp. 163–186 (Chapter 9), Available at: http://www.fao.org/docrep/013/i1757e/i1757e09.pdf
  28. Faria, D., Laps, R.R., Baumgarten, J., Cetra, M., 2006. Bat and bird assemblages from forests and shade cacao plantations in two contrasting landscapes in the Atlantic Forest of southern Bahia, Brazil. Biodivers. Conserv. 15, 587–612.CrossRefGoogle Scholar
  29. FiBL-IFOAM, 2014. Organic Farming Statistics. Research Institute of Organic Agriculture FiBL, Available at: http://www.fibl.org/en/themen/themen-statistiken.html
  30. Fischer, J., Zerger, A., Gibbons, P., Stott, J., Law, B., 2010a. Tree decline and the future of Australian farmland biodiversity. PNAS 107, 19597–19602.PubMedCrossRefPubMedCentralGoogle Scholar
  31. Fischer, J., Stott, J., Law, B.S., 2010b. The disproportionate value of scattered trees. Biol. Conserv. 143, 1564–1567.CrossRefGoogle Scholar
  32. Fleming, T.H., Sosa, V.J., 1994. Effects of nectarivorous and frugivorous mammals on reproductive success of plants. J. Mammal. 75, 845–851.CrossRefGoogle Scholar
  33. 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.CrossRefGoogle Scholar
  34. Fuentes-Montemayor, E., Goulson, D., Park, K.J., 2011a. Pipistrelle bats and their prey do not benefit from four widely applied agri-environment management prescriptions. Biol. Conserv. 144, 2233–2246.CrossRefGoogle Scholar
  35. Fuentes-Montemayor, E., Goulson, D., Park, K.J., 2011b. The effectiveness of agri-environment schemes for the conservation of farmland moths: assessing the importance of a landscape-scale management approach. J. Appl. Ecol. 48, 532–542.CrossRefGoogle Scholar
  36. Fuentes-Montemayor, E., Goulson, D., Cavin, L., Wallace, J.M., Park, K., 2013. Fragmented woodlands in agricultural landscapes: the influence of woodland character and landscape context on bats and their insect prey. Agric. Ecosyst. Environ. 172, 6–15.CrossRefGoogle Scholar
  37. Fuller, R.J., Norton, L.R., Feber, R.E., Johnson, P.J., Chamberlain, D.E., Joys, A.C., Mathews, F., Stuart, R.C., Townsend, M.C., Manley, W.J., Wolfe, M.S., Macdonald, D.W., Firbank, L.G., 2005. Benefits of organic farming to biodiversity vary among taxa. Biol. Lett. 1, 431–434.PubMedPubMedCentralCrossRefGoogle Scholar
  38. Hanspach, J., Fischer, J., Ikin, K., Stott, J., Law, B.S., 2012. Using trait-based filtering as a predictive framework for conservation: a case study of bats on farms in southeastern Australia. J. Appl. Ecol. 49, 842–850.CrossRefGoogle Scholar
  39. Harvey, C.A., Villalobos, J.A.G., 2007. Agroforestry systems conserve species-rich but modified assemblages of tropical birds and bats. Biodivers. Conserv. 16, 2257–2292.CrossRefGoogle Scholar
  40. Harvey, C.A., Villanueva, C., Villacís, J., Chacón, M., Muñoz, D., López, M., Ibrahim, M., Gómez, R., Taylor, R., Martinez, J., Navas, A., Saenz, J., Sánchez, D., Medina, A., Vilchez, S., Hernández, B., Perez, A., Ruiz, F., López, F., Lang, I., Sinclair, F.L., 2005. Contribution of live fences to the ecological integrity of agricultural landscapes. Agric. Ecosyst. Environ. 111, 200–230.CrossRefGoogle Scholar
  41. Harvey, C.A., Medina, A., Sánchez, D.M., Vílchez, S., Hernández, B., Saenz, J.C., Maes, J.M., Casanoves, F., Sinclair, F.L., 2006. Patterns of animal diversity in different forms of tree cover in agricultural landscapes. Ecol. Appl. 16, 1986–1999.PubMedCrossRefPubMedCentralGoogle Scholar
  42. Henderson, L.E., Broders, H.G., 2008. Movements and resource selection ofthe northern long-eared myotis (Myotis septentrionalis) in a forest-agriculture landscape. J. Mammal. 89, 952–963.CrossRefGoogle Scholar
  43. Hobbs, R., Catling, P.C.,Wombey, J.C, Clayton, M., Atkins, L., Reid, A., 2003. Faunaluse of bluegum (Eucalyptus globulus) plantations in southwestern Australia. Agrofor. Syst. 58, 195–212.CrossRefGoogle Scholar
  44. Hole, D.G., Perkins, A.J., Wilson, J.D., Alexander, I.H., Grice, P.V., Evans, A.D., 2005. Does organic farming benefit biodiversity? Biol. Conserv. 122, 113–130.CrossRefGoogle Scholar
  45. Holt, E.A., Miller, S.W., 2010. Bioindicators: using organisms to measure environmental impacts. Nat. Educ. Knowl. 3 (10), 8.Google Scholar
  46. Jefferies, D.J., 1972. Organochlorine insecticide residues in British bats and their significance. J. Zool. Lond. 166, 245–263.CrossRefGoogle Scholar
  47. Jones, G., Jacobs, D., Kunz, T., Willig, M., Racey, P., 2009. Carpe noctem: the importance of bats as bioindicators. Endanger. Species Res. 8, 93–115.CrossRefGoogle Scholar
  48. Jung, K., Kaiser, S., Bohm, S., Nieschulze, J., Kalko, E.K.V., 2012. Moving in three dimensions: effects of structural complexity on occurrence and activity of insectivorous bats in managed forest stands. J. App. Ecol. 49, 523–531.CrossRefGoogle Scholar
  49. Kırkagac, M.U., Pulatsu, S., Topcu, A., 2009. Trout farm effluent effects on water sediment quality and benthos. Clean - Soil Air Water 37, 386–391.CrossRefGoogle Scholar
  50. Kleijn, D., Rundlo, M., Scheper, J., Smith, H.G., Tscharntke, T., 2011. Does conservation on farmland contribute to halting the biodiversity decline? Trends Ecol. Evol. 26, 474–481.Google Scholar
  51. Korine, C., Adams, R.A., Russo, D., Jacobs, D., 2014. The association between bats and water they use: implications for species distribution, ecology, and management plans. In: Voigt, C.C., Kingston, T. (Eds.), Bats and the Anthro-pocene: Conservation of bats in a changing world. Springer Press, New York, In press.Google Scholar
  52. Krebs, J.R., Wilson, J.D., Bradbury, R.B., Siriwardena, G.M., 1999. The second silent spring? Nature 400, 611–612.CrossRefGoogle Scholar
  53. Kunz, T.H., Braun de Torrez, E., Bauer, D., Lobova, T., Fleming, T.H., 2011. Ecosystem services provided by bats. Ann. N.Y. Acad. Sci. 1223, 1–38.PubMedCrossRefPubMedCentralGoogle Scholar
  54. Law, B., Park, K.J., Lacki, M.J., 2014. Insectivorous bats and silviculture: balancing timber production and bat conservation. In: Voigt, C.C., Kingston, T. (Eds.), Bats and the Anthropocene: Conservation of bats in a changing world. Springer Press, New York, In press.Google Scholar
  55. Law, B.S., Chidel, M., 2006. Eucalypt plantings on farms: use by insectivorous bats in south-eastern Australia. Biol. Conserv. 133, 236–249.CrossRefGoogle Scholar
  56. Lentini, P.E., Gibbons, P., Fischer, J., Law, B., Hanspach, J., Martin, T.G., 2012. Bats in a farming landscape benefit from linear remnants and unimproved pastures. PLoS ONE 7, e48201.PubMedPubMedCentralCrossRefGoogle Scholar
  57. Limpens, H.J., Kapteyn, K., 1991. Bats, their behaviour and linear landscape elements. Myotis 29, 39–48.Google Scholar
  58. Linton, D., Harrington, L.A., Macdonald, D.W., 2014. Habitat use by bats: disentangling local versus landscape scale effects within lowland farmland. In: Macdonald, D.W., Feber, R.E. (Eds.), Wildlife Conservation on Farmland. Oxford University Press, Oxford, United Kingdom (in press).Google Scholar
  59. Lintott, P.R., Bunnefeld, N., Fuentes-Montemayor, E., Minderman, J., Mayhew, R., Olley, L., Park, K.J., 2014. City life makes females fussy: Sex differences in habitat use of temperate bats in urban areas, Royal Society Open Science 1: 140200.PubMedPubMedCentralCrossRefGoogle Scholar
  60. Lison, F., Calvo, J.F., 2011. The significance of water infrastructures for the conservation of bats in a semiardi Mediterranean landscape. Anim. Conserv. 14, 533–541.CrossRefGoogle Scholar
  61. Lumsden, L.F., Bennett, A.F., 2005. Scattered trees in rural landscapes: foraging habitat for insectivorous bats in south-eastern Australia. Biol. Conserv. 122, 205–222.CrossRefGoogle Scholar
  62. Maas, B., Clough, Y., Tscharntke, T., 2013. Bats and birds increase crop yield in tropical agroforestry Landscapes. Ecol. Lett. 16, 1480–1487.PubMedCrossRefGoogle Scholar
  63. MacDonald, M.A., Morris, A.J., Dodd, S., Johnstone, I., Beresford, A., Angell, R., Haysom, K., Langton, S., Tordoff, G.M., Brereton, T., Hobson, R., Shellswell, C., Hutchinson, N., Dines, T., Wilberforce, E.M., Parry, R., Matthews, V., 2012a. Welsh Assembly Government Contract 183/2007/08 to Undertake Agri-environment Monitoring and Services. Lot 2‒ Species Monitoring, Available at: http://wales.gov.uk/docs/drah/publications/130917report2speciesen.pdf
  64. MacDonald, M.A., Cobbold, G., Mathews, F., Denny, M.J.H., Walker, L.K., Grice, P.V., Anderson, G.Q.A., 2012b. Effects of agri-environment management for cirl buntings on other biodiversity. Biodivers. Conserv. 21, 1477–1492.CrossRefGoogle Scholar
  65. McGeogh, M.A., 1998. The selection, testing and application of terrestrial insects as bioindicators. Biol. Rev. 73, 181–201.CrossRefGoogle Scholar
  66. Medina, A., Harvey, C.A., Sanchez Merlo, D., Vílchez, S., Hernández, B., 2007. Bat diversity and movement in an agricultural landscape in Matiguás, Nicaragua. Biotropica 39, 120–128.CrossRefGoogle Scholar
  67. Mickleburgh, S.P., Hutson, A.M., Racey, P.A., 2002. A review of the global conservation status of bats. Oryx 36, 18–34.CrossRefGoogle Scholar
  68. Moguel, P., Toledo, V.M., 1999. A review of the global conservation status of bats. Conserv. Biol. 13, 11–21.CrossRefGoogle Scholar
  69. Murphy, S.E., Greenaway, F., Hill, D.A., 2012. Patterns of habitat use by female brown long-eared bats presage negative impacts of woodland conservation management. J. Zool. Lond. 288, 177–183.CrossRefGoogle Scholar
  70. Numa, C., Verdú, J.R., Sánchez-Palomino, P., 2005. Phyllostomid bat diversity in a variegated coffee landscape. Biol. Conserv. 122, 151–158.CrossRefGoogle Scholar
  71. Pain, D.J., Pienkowski, M.W., 1997. Farming and Birds in Europe. Academic, London.Google Scholar
  72. Park, K.J., Cristinacce, A., 2006. Use of sewage treatment works as foraging sites by insectivorous bats. Anim. Conserv. 9, 259–268.CrossRefGoogle Scholar
  73. Paull, J., 2011. The uptake of organic agriculture: a decade of worldwide development. J. Soc. Dev. Sci. 2, 111–120.Google Scholar
  74. Perfecto, I., Vandermeer, J., 2008. Biodiversity conservation in tropical agroecosystems: a new conservation paradigm. Ann. N.Y. Acad. Sci. 1134, 173–200.PubMedCrossRefPubMedCentralGoogle Scholar
  75. Pineda, E., Moreno, C.E., Escobar, F., Halffter, G., 2005. Frog, bat and dung beetle diversity in the cloud forest and coffee agroecosystems of Veracruz, Mexico. Conserv. Biol. 19, 400–410.CrossRefGoogle Scholar
  76. Pocock, M.J.O., Jennings, N., 2008. Testing biotic indicator taxa: the sensitivity of insectivorous mammals and their prey to the intensification of lowland agriculture. J. Appl. Ecol. 45, 151–160.CrossRefGoogle Scholar
  77. Ramankutty, N., Evan, A.T., Monfreda, C., Foley, J.A., 2008. Farming the planet I: geographic distribution of global agricultural lands in the year 2000. Glob. Bio-geochem. Cycles 22, GB1003, http://dx.doi.org/10.1029/2007GB002952CrossRefGoogle Scholar
  78. Roundtable on Sustainable Palm Oil. Available at: http://www.rspo.org/file/PnC_ RSPO_Rev1.pdf
  79. RSPB, 2013. The RSPB’s views on the Common Agricultural Policy, Available at: http://www.rspb.org.uk/Images/CAP_aug2013_tcm9-353073.pdf
  80. Russo, D., Ancillotto, L., 2015. Sensitivity of bats to urbanization: a review. Mamm. Biol. 80, 205–212.CrossRefGoogle Scholar
  81. Saldaña-Vázquez, R.A., Castro-Luna, A.A., Sandoval-Ruiz, C.A., Hernández-Montero, J.R., Stoner, K.E., 2013. Population composition and Ectoparasite prevalence on bats (Sturnira ludovici; Phyllostomidae) in forest fragments and coffee plantations of Central Veracruz, Mexico. Biotropica 45, 351–356.CrossRefGoogle Scholar
  82. Salsamendi, E., Arostegui, I., Aihartza, J., Almenar, D., Goiti, U., Garin, I., 2012. Foraging ecology in Mehely’s horseshoe bats: influence of habitat structure and water availability. Acta Chirop. 14, 121–132.CrossRefGoogle Scholar
  83. Sirami, C., Jacobs, D.S., Cumming, G.S., 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.CrossRefGoogle Scholar
  84. Spedding, C.R.W., 1988. An Introduction to Agricultural Systems, 2nd ed. Elsevier, London.CrossRefGoogle Scholar
  85. Stahlschmidt, P., Pätzold, A., Ressl, L., Schulz, R., Brühl, C.A., 2012. Constructed wetlands support bats in agricultural landscapes. Basic Appl. Ecol. 13, 196–203.CrossRefGoogle Scholar
  86. Stebbings, R.E., 1988. Conservation of European bats. Christopher Helm, London.Google Scholar
  87. Struebig, M.J., Kingston, T., Zubaid, A., Mohd-Adnan, A., Rossiter, S.J., 2008. Conservation value of forest fragments to Palaeotropical bats. Biol. Conserv. 141, 2112–2126.CrossRefGoogle Scholar
  88. Struebig, M.J., Kingston, T., Petit, E.J., Le Comber, S.C., Zubaid, A., Mohd-Adnan, A., Rossiter, S.J., 2011. Parallel declines in species and genetic diversity in tropical forest fragments. Ecol. Lett. 14, 582–590.PubMedCrossRefPubMedCentralGoogle Scholar
  89. Tilman, D., 1999. Global environmental impacts of agricultural expansion: the need for sustainable and efficient practices. Proc. Natl. Acad. Sci. U.SA 96, 5995–6000.CrossRefGoogle Scholar
  90. Tilman, D., Balzer, C., Hill, J., Befort, B.L., 2011. Global food demand and the sustainable intensification of agriculture. PNAS 108, 20260–20264.PubMedCrossRefPubMedCentralGoogle Scholar
  91. Tscharntke, T., Klein, A.M., Kruess, A., Steffan-Dewenter, I., Thies, C., 2005. Landscape perspectives on agricultural intensification and biodiversity-ecosystem service management. Ecol. Lett. 8, 857–874.CrossRefGoogle Scholar
  92. Vaughan, N., Jones, G., Harris, S., 1997. Habitat use by bats (Chiroptera) assessed by means of a broad-band acoustic method. J. Appl. Ecol. 34, 716–730.CrossRefGoogle Scholar
  93. Verboom, B., Huitema, H., 1997. The importance of linear landscape elements for the pipistrelle Pipistrellus pipistrellus and the serotine bat Eptesicus serotinus. Landsc. Ecol. 12, 117–125.CrossRefGoogle Scholar
  94. Verhoeven, J.T.A., Setter, T.L., 2010. Agricultural use of wetlands: opportunities and limitations. Ann. Bot. 105, 155–163.PubMedCrossRefPubMedCentralGoogle Scholar
  95. Walsh, A., Harris, S., 1996. Foraging habitat preferences of vespertilionid bats in Britain. J. Appl. Ecol. 33, 519–529.CrossRefGoogle Scholar
  96. Wickramasinghe, L.P., Harris, S., Jones, G., Vaughan, N., 2003. Bat activity and species richness on organic and conventional farms: impact of agricultural intensification. J. Appl. Ecol. 40, 984–993.CrossRefGoogle Scholar
  97. Wickramasinghe, L.P., Harris, S., Jones, G., Jennings, N.V., 2004. Abundance and species richness of nocturnal insects on organic and conventional farms: effects of agricultural intensification on bat foraging. Conserv. Biol. 18, 1283–1292.CrossRefGoogle Scholar
  98. Whittingham, M.J., 2007. Will agri-environment schemes deliver substantial biodiversity gain, and if not why not? J. Appl. Ecol. 44, 1–5.Google Scholar
  99. Wilcove, D.S., Koh, L.P., 2010. Addressing the threats to biodiversity from oil-palm Agriculture. Biodivers. Conserv. 19, 999–1007.CrossRefGoogle Scholar
  100. Williams-Guillén, K., Perfecto, I., Vandermeer, J., 2008. Bats limit insects in a neotropical agroforestry system. Science 320, 70.PubMedCrossRefGoogle Scholar
  101. Williams-Guillén, K., Perfecto, I., 2010. Effects of agricultural intensification on the assemblage of leaf-nosed bats (Phyllostomidae) in a coffee landscape in Chiapas, Mexico. Biotropica 42, 605–613.CrossRefGoogle Scholar
  102. Williams-Guillén, K., Perfecto, I., 2011. Ensemble composition and activity levels of insectivorous bats in response to management intensification in coffee agro-forestry systems. PLoS ONE 6, e16502.PubMedPubMedCentralCrossRefGoogle Scholar
  103. Williamson, T.M., 1986. Parish boundaries and early fields: continuity and discontinuity. J. Hist. Geogr. 12, 241–248.CrossRefGoogle Scholar
  104. Womack, K.M., Amelon, S.K., Thompson, F.R., 2013. Resource selection by Indiana bats during the maternity season. J. Wild. Manag. 77, 707–715.CrossRefGoogle Scholar
  105. Zomer, R.J., Trabucco, A., Coe, R., Place, F., 2009. Trees on farm: analysis of global extent and geographical patterns of agroforestry. ICRAF Working Paper no. 89. World Agroforestry Centre, Nairobi, Kenya.Google Scholar

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© Deutsche Gesellschaft für Säugetierkunde, e. V. DGS 2014

Authors and Affiliations

  1. 1.Biological and Environmental SciencesUniversity of StirlingStirlingUK

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