Disease alters macroecological patterns of North American bats

Global Ecology and Biogeography

Volumn 24, Issue 7, 2015, Pages 741-749

  Frick, Winifred F ^a   Puechmaille, Sébastien J ^b,c,d   Hoyt, Joseph R ^a   Nickel, Barry A ^a   Langwig, Kate E ^a   Foster, Jeffrey T ^e,f   Barlow, Kate E ^g   Bartonička, Tomáš ^h   Feller, Dan ⁱ   Haarsma, Anne Jifke ^j   Herzog, Carl ^k   Horáček, Ivan ^l   van der Kooij, Jeroen ^m   Mulkens, Bart ⁿ   Petrov, Boyan ^o   Reynolds, Rick ^p   Rodrigues, Luísa ^q   Stihler, Craig W ^r   Turner, Gregory G ^s   Kilpatrick, A Marm ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF GREIFSWALD   (Germany)

^c UNIVERSITY COLLEGE DUBLIN   (Ireland)

^d Midi Pyrénées Bat Group CREN GCMP   (France)

^e NORTHERN ARIZONA UNIVERSITY   (United States)

^f UNIVERSITY OF NEW HAMPSHIRE   (United States)

^g BAT CONSERVATION TRUST   (United Kingdom)

^h MASARYK UNIVERSITY   (Czech Republic)

ⁱ UNIVERSITY OF MARYLAND CENTER FOR ENVIRONMENTAL SCIENCE   (United States)

^j RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^k NEW YORK STATE DEPARTMENT OF ENVIRONMENTAL CONSERVATION   (United States)

^l CHARLES UNIVERSITY   (Czech Republic)

^m Norwegian Zoological Society   (Norway)

ⁿ Natuurpunt Studie   (Belgium)

^o BULGARIAN ACADEMY OF SCIENCES   (Bulgaria)

^p Virginia Department of Game and Inland Fisheries   (United States)

^q Instituto da Conservacao da Natureza   (Portugal)

^r West Virginia Division of Natural Resources   (United States)

^s Pennsylvania Game Commission   (United States)

more..

Author keywords

Disease ecology; Extinction risk; Macroecology; Population monitoring; Pseudogymnoascus destructans; White nose syndrome

Indexed keywords

ABUNDANCE; BAT; COLONY; EXTINCTION RISK; FUNGAL DISEASE; HIBERNATION; MACROECOLOGY; MONITORING; SPATIAL DISTRIBUTION;

EUROPE; NORTH AMERICA;

MYOTIS SEPTENTRIONALIS; PSEUDOGYMNOASCUS;

EID: 84930378628     PISSN: 1466822X     EISSN: 14668238     Source Type: Journal    
DOI: 10.1111/geb.12290     Document Type: Article

References (50)

1. Akasaka, T., Akasaka, M. & Nakamura, F. (2012) Scale-independent significance of river and riparian zones on three sympatric Myotis species in an agricultural landscape. Biological Conservation, 145, 15-23.
2. Anderson, R.M. & May, R.M. (1979) Population biology of infectious diseases: part I. Nature, 280, 361-367.
3. Bandouchova, H., Bartonicka, T., Berkova, H., Brichta, J., Cerny, J., Kovacova, V., Kolarik, M., Köllner, B., Kulich, P., Martínkova, N., Rehak, Z., Turner, G.G., Zukal, J. & Pikula, J. (2014) Pseudogymnoascus destructans: evidence of virulent skin invasion for bats under natural conditions, Europe. Transboundary and Emerging Diseases, doi:10.1111/tbed.12282.
4. Blehert, D.S., Hicks, A.C., Behr, M., Meteyer, C.U., Berlowski-Zier, B.M., Buckles, E.L., Coleman, J.T.H., Darling, S.R., Gargas, A., Niver, R., Okoniewski, J.C., Rudd, R.J. & Stone, W.B. (2009) Bat white-nose syndrome: an emerging fungal pathogen? Science, 323, 227.
5. Blomberg, S.P., Garland, T. & Ives, A.R. (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution, 57, 717-745.
6. Bolker, B.M. & R Development Core Team (2013) bbmle: tools for general maximum likelihood estimation. Available at: http://cran.r-project.org/package=bbmle (accessed 20 September 2013).
7. Brown, J.H. (1995) Macroecology. University of Chicago Press, Chicago, IL.
8. Brown, J.H. (1999) Macroecology: progress and prospect. Oikos, 87, 3-14.
9. Brown, J.H. & Maurer, B.A. (1989) Macroecology: the division of food and space among species on continents. Science, 243, 1145-1150.
10. de Castro, F. & Bolker, B. (2004) Mechanisms of disease-induced extinction. Ecology Letters, 8, 117-126.
11. Crawley, M.J. (2007) The R book. John Wiley & Sons, Chichester, UK.
12. Daszak, P., Cunningham, A.A. & Hyatt, A.D. (2000) Emerging infectious diseases of wildlife - threats to biodiversity and human health. Science, 287, 443-449.
13. Davis, W.H. & Hitchcock, H.B. (1965) Biology and migration of the bat, Myotis lucifugus, in New England. Journal of Mammalogy, 46, 296-313.
14. Felsenstein, J. (1985) Phylogenies and the comparative method. The American Naturalist, 125, 1-15.
15. Frick, W.F., Pollock, J.F., Hicks, A.C., Langwig, K.E., Reynolds, D.S., Turner, G.G., Butchkoski, C.M. & Kunz, T.H. (2010) An emerging disease causes regional population collapse of a common North American bat species. Science, 329, 679-682.
16. Gaston, K.J. & Blackburn, T.M. (2000) Patterns and process in macroecology. Blackwell Science, Cambridge, UK.
17. Gehrt, S.D. & Chelsvig, J.E. (2003) Bat activity in an urban landscape: patterns at the landscape and microhabitat scale. Ecological Applications, 13, 939-950.
18. Hochachka, W.M. & Dhondt, A.A. (2000) Density-dependent decline of host abundance resulting from a new infectious disease. Proceedings of the National Academy of Sciences USA, 97, 5303-5306.
19. Hudson, P.J., Dobson, A.P. & Newborn, D. (1998) Prevention of population cycles by parasite removal. Science, 282, 2256-2258.
20. Hutterer, R., Ivanova, T., Meyer-Cords, C. & Rodrigues, L. (2005) Bat migrations in Europe: a review of banding data and literature. Federal Agency for Nature Conservation, Bonn.
21. Johnson, C.N. (1998) Species extinction and the relationship between distribution and abundance. Nature, 394, 272-274.
22. Kembel, S.W., Cowan, P.D., Helmus, M.R., Cornwell, W.K., Morlon, H., Ackerly, D.D., Blomberg, S.P. & Webb, C.O. (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics, 26, 1463-1464.
23. Kerr, J.T., Kharouba, H.M. & Currie, D.J. (2007) The macroecological contribution to global change solutions. Science, 316, 1581-1584.
24. Kilpatrick, A.M., Briggs, C.J. & Daszak, P. (2010) The ecology and impact of chytridiomycosis: an emerging disease of amphibians. Trends in Ecology and Evolution, 25, 109-118.
25. Lande, R. (1993) Risks of population extinction from demographic and environmental stochasticity and random catastrophes. The American Naturalist, 142, 911-927.
26. Langwig, K.E., Frick, W.F., Bried, J.T., Hicks, A.C., Kunz, T.H. & Kilpatrick, A.M. (2012) Sociality, density-dependence and microclimates determine the persistence of populations suffering from a novel fungal disease, white-nose syndrome. Ecology Letters, 15, 1050-1057.
27. Langwig, K.E., Frick, W.F., Reynolds, R., Parise, K.L., Drees, K.P., Hoyt, J.R., Cheng, T.L., Kunz, T.H., Foster, J.T. & Kilpatrick, A.M. (2015) Host and pathogen ecology drive the seasonal dynamics of a fungal disease, white-nose syndrome. Proceedings of the Royal Society B: Biological Sciences, 282, 20142335.
28. Lips, K.R., Brem, F., Brenes, R., Reeve, J.D., Alford, R.A., Voyles, J., Carey, C., Livo, L., Pessier, A.P. & Collins, J.P. (2006) Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proceedings of the National Academy of Sciences USA, 103, 3165-3170.
29. McCallum, H. (2012) Disease and the dynamics of extinction. Philosophical Transactions of the Royal Society B: Biological Sciences, 367, 2828-2839.
30. Martínková, N., Bačkor, P., Bartonička, T. etal. (2010) Increasing incidence of Geomyces destructans fungus in bats from the Czech Republic and Slovakia. PLoS ONE, 5, e13853.
31. 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. Mammalian Biology, 76, 451-460.
32. Meteyer, C.U., Buckles, E.L., Blehert, D.S., Hicks, A.C., Green, D.E., Shearn-Bochsler, V., Thomas, N.J., Gargas, A. & Behr, M.J. (2009) Histopathologic criteria to confirm white-nose syndrome in bats. Journal of Veterinary Diagnostic Investigation, 21, 411-414.
33. Nagy, Z.L. & Postawa, T. (2010) Seasonal and geographical distribution of cave-dwelling bats in Romania: implications for conservation. Animal Conservation, 14, 74-86.
34. Nagy, Z.L. & Szántó, L. (2003) The occurrence of hibernating Pipistrellus pipistrellus (Schreber, 1774) in caves of the Carpathian Basin. Acta Chiropterologica, 5, 155-160.
35. Pikula, J., Bandouchova, H., Novotný, L., Meteyer, C.U., Zukal, J., Irwin, N.R., Zima, J. & Martínková, N. (2012) Histopathology confirms white-nose syndrome in bats in Europe. Journal of Wildlife Diseases, 48, 207-211.
36. Puechmaille, S.J., Verdeyroux, P., Fuller, H., Ar Gouilh, M., Bekaert, M. & Teeling, E.C. (2010) White-nose syndrome fungus (Geomyces destructans) in bat, France. Emerging Infectious Diseases, 16, 290-293.
37. Puechmaille, S.J., Wibbelt, G., Korn, V. etal. (2011a) Pan-European distribution of white-nose syndrome fungus (Geomyces destructans) not associated with mass mortality. PLoS ONE, 6, e19167.
38. Puechmaille, S.J., Frick, W.F., Kunz, T.H., Racey, P.A., Voigt, C.C., Wibbelt, G. & Teeling, E.C. (2011b) White-nose syndrome: is this emerging disease a threat to European bats? Trends in Ecology and Evolution, 26, 570-576.
39. Purvis, A., Gittleman, J.L., Cowlishaw, G. & Mace, G.M. (2000) Predicting extinction risk in declining species. Proceedings of the Royal Society B: Biological Sciences, 267, 1947-1952.
40. R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.
41. Ramsey, F.L. & Schafer, D.W. (2002) The statistical sleuth: a course in methods of data analysis, 2nd edn. Duxbury Thomson Learning, Pacific Grove, CA.
42. Skerratt, L.F., Berger, L., Speare, R., Cashins, S., McDonald, K.R., Phillott, A.D., Hines, H.B. & Kenyon, N. (2007) Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth, 4, 125-134.
43. Smith, F.A., Lyons, S.K., Ernest, S.K.M. & Brown, J.H. (2008) Macroecology: more than the division of food and space among species on continents. Progress in Physical Geography, 32, 115-138.
44. Tompkins, D.M., Dunn, A.M., Smith, M.J. & Telfer, S. (2011) Wildlife diseases: from individuals to ecosystems. Journal of Animal Ecology, 80, 19-38.
45. Torchin, M.E., Lafferty, K.D., Dobson, A.P., McKenzie, V.J. & Kuris, A.M. (2003) Introduced species and their missing parasites. Nature, 421, 628-630.
46. Travis, J. (1996) The significance of geographical variation in species interactions. The American Naturalist, 148, S1-S8.
47. Walsh, A.L. & Harris, S. (1996) Factors determining the abundance of vespertilionid bats in Britain: geographical, land class and local habitat relationships. Journal of Applied Ecology, 33, 519-529.
48. Warnecke, L., Turner, J.M., Bollinger, T.K., Lorch, J.M., Misra, V., Cryan, P.M., Wibbelt, G., Blehert, D.S. & Willis, C.K.R. (2012) Inoculation of bats with European Geomyces destructans supports the novel pathogen hypothesis for the origin of white-nose syndrome. Proceedings of the National Academy of Sciences USA, 109, 6999-7003.
49. Wibbelt, G., Puechmaille, S.J., Ohlendorf, B., Mühldorfer, K., Bosch, T., Görföl, T., Passior, K., Kurth, A., Lacremans, D. & Forget, F. (2013) Skin lesions in European hibernating bats associated with Geomyces destructans, the etiologic agent of white-nose syndrome. PLoS ONE, 8, e74105.
50. Zukal, J., Bandouchova, H., Bartonička, T., Berkova, H., Brack, V., Brichta, J., Dolinay, M., Jaron, K.S., Kovacova, V., Kovarik, M., Martínková, N., Ondracek, K., Rehák, Z., Turner, G.G. & Pikula, J. (2014) White-nose syndrome fungus: a generalist pathogen of hibernating bats. PLoS ONE, 9, e97224.