Truly enigmatic declines in terrestrial salamander populations in Great Smoky Mountains National Park

Diversity and Distributions

Volumn 19, Issue 1, 2013, Pages 38-48

  Caruso, Nicholas M ^a   Lips, Karen R ^a  

^a Bldg 142   (United States)

Author keywords

Batrachochytrium dendrobatidis; Climate change; Great Smoky Mountains; Plethodon; Population decline; Salamanders

Indexed keywords

ABUNDANCE; AMPHIBIAN; BIODIVERSITY; COMMUNITY COMPOSITION; FUNGAL DISEASE; HABITAT LOSS; HOST-PATHOGEN INTERACTION; INVASIVE SPECIES; POPULATION DECLINE; POPULATION STRUCTURE; PROTECTED AREA; TERRESTRIAL ENVIRONMENT; WOODLAND;

GREAT SMOKY MOUNTAINS NATIONAL PARK; UNITED STATES;

BATRACHOCHYTRIUM DENDROBATIDIS; PLETHODON; PLETHODON GLUTINOSUS; PLETHODON JORDANI; PLETHODON TEYAHALEE; PLETHODON VENTRALIS; SALAMANDROIDEA;

EID: 84871149412     PISSN: 13669516     EISSN: 14724642     Source Type: Journal    
DOI: 10.1111/j.1472-4642.2012.00938.x     Document Type: Article

References (82)

1. Alford, R.A. & Richards, S.J. (1999) Global amphibian declines: a problem in applied ecology. Annual Review of Ecology, Evolution, and Systematics, 30, 113-165.
2. Bailey, L.L., Simons, T.R. & Pollock, K.H. (2004) Estimating detection probability parameters for Plethodon salamanders using the robust capture-recapture design. Journal of Wildlife Management, 68, 1-13.
3. Bates, D. & Maechler, M. (2010) lme4: Linear mixed-effects models using S4 classes. R package version 0.999375-35.
4. Becker, G. & Zamudio, K. (2011) Tropical amphibian populations experience higher disease risk in natural habitats. Proceedings of the National Academy of Sciences USA, 108, 9893-9989.
5. Berger, L., Speare, R., Daszak, P., Green, D.E., Cunningham, A.A., Goggin, C.L., Slocombe, R., Ragan, M.A., Hyatt, A.D., McDonald, K.R., Hines, H.B., Lips, K.R., Marantelli, G. & Parkes, H. (1998) Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proceedings of the National Academy of Sciences USA, 95, 9031-9036.
6. Bernardo, J. & Spotila, J.R. (2006) Physiological constraints on organismal response to global warming: mechanistic insights from clinally varying populations and implications for assessing endangerment. Biology Letters, 2, 135-139.
7. Bonardi, A., Manenti, R., Corbetta, A., Ferri, V., Fiacchini, D., Giovine, G., Macchi, S., Romanazzi, E., Soccini, C., Bottoni, L., Padoa-Schioppa, E. & Ficetola, G.F. (2011) Usefulness of volunteer data to measure the large sale decline of "common" toad populations. Biological Conservation, 144, 2328-2334.
8. Bosch, J., Martínez-Solano, I. & García-París, M. (2001) Evidence of a chytrid fungus infection involved in the decline of the common midwife toad (Alytes obstetricians) in protected areas of central Spain. Biological Conservation, 97, 331-337.
9. Boyle, D.G., Boyle, D.B., Olsen, V., Morgan, J.A.T. & Hyatt, A.D. (2004) Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Diseases of Aquatic Organisms, 60, 141-148.
10. Burrowes, P.A., Joglar, R.L. & Green, D.E. (2004) Potential causes for amphibian declines in Puerto Rico. Herpetologica, 60, 141-154.
11. Campbell Grant, E., Bailey, L., Ware, J.L. & Duncan, K. (2008) Prevalence of the amphibian pathogen Batrachochytrium dendrobatidis in stream and wetland amphibians in Maryland, USA. Applied Herpetology, 5, 233-241.
12. Cardillo, M., Mace, G.M., Jones, K.E., Bielby, J., Bininda-Emonds, O.R.P., Sechrest, W., Orme, C.D.L. & Purvis, A. (2005) Multiple causes of high extinction risk in large mammal species. Science, 309, 1239-1241.
13. Chatfield, M.W., Rothermel, B.B., Brooks, C.S. & Kay, J.B. (2009) Detection of Batrachochytrium dendrobatidis in amphibians from the Great Smoky Mountains of North Carolina and Tennessee, USA. Herpetological Review, 40, 176-179.
14. Cheng, T.L., Rovito, S.M., Wake, D.B. & Vredenburg, V.T. (2011) Coincident mass extirpation of neotropical amphibians with the emergence of the infectious fungal pathogen Batrachochytrium dendrobatidis Proceedings of the National Academy of Sciences USA, 108, 9502-9507.
15. Chinnadurai, S.K., Cooper, D., Dombrowski, D.S., Poore, M.F. & Levy, M.G. (2009) Experimental infection of native North Carolina salamanders with Batrachochytrium dendrobatidis Journal of Wildlife Diseases, 45, 631-636.
16. Cooper, N., Bielby, J., Thomas, G.H. & Purvis, A. (2007) Macroecology and extinction risk correlates of frogs. Global Ecology and Biogeography, 17, 211-221.
17. Corey, S.J. & Waite, T.A. (2008) Phylogenetic autocorrelation of extinction threat in globally imperiled amphibians. Diversity and Distributions, 14, 614-629.
18. Corser, J.D. (2001) Decline of disjunct green salamander (Aneides aeneus) populations in the southern Appalachians. Biological Conservation, 97, 119-126.
19. Crawford, A.J., Lips, K.R. & Bermingham, E. (2010) Epidemic disease decimates amphibian abundance, species diversity, and evolutionary history in the highlands of central Panama. Proceedings of the National Academy of Sciences USA, 107, 13777-13782.
20. Daszak, P., Scott, D.E., Kilpatrick, A.M., Faggioni, C., Gibbons, J.W. & Porter, D. (2005) Amphibian population declines at Savannah River site are linked to climate, not chytridiomycosis. Ecology, 86, 3232-3237.
21. Davidson, C., Shaffer, H.B. & Jennings, M.R. (2002) Spatial tests of the pesticide drift, habitat destruction, UV-B, and climate-change hypotheses for California amphibian declines. Conservation Biology, 16, 1588-1601.
22. Davis, M.B. (1993) Old-growth in the east: a survey. Wild Earth, Richmond, VT.
23. Dodd, K. (2004) The amphibians of Great Smoky Mountain National Park. University of Tennessee Press, Knoxville, TN.
24. Dunn, E.R. (1926) The salamanders of the family Plethodontidae. Smith College Publications, Northampton, MA, 441 pp. Reissued in 1972 by the Society for the Study of Amphibians and Reptiles.
25. ESRI (2011) ArcGIS 10.0. ESRI Inc., Redlands, CA.
26. Gesch, D., Oimoen, M., Greenlee, S., Nelson, C., Steuck, M. & Tyler, D. (2002) The national elevation dataset. Photogrammetric Engineering and Remote Sensing, 68, 5-11.
27. Girvetz, E.H., Zganjar, C., Raber, G.T., Maurer, E.P., Kareiva, P. & Lawler, J.J. (2009) Applied climate-change analysis: the climate wizard tool. PLoS ONE, 4, e8320.
28. Hairston, N.G. Sr (1981) Evolution under interspecific competition: field experiments on terrestrial salamanders. Evolution, 34, 409-420.
29. Hairston, N.G., Sr & Wiley, R.H. (1993) No decline in salamander (Amphibia: Caudata) populations: a twenty year study in the southern Appalachians. Brimleyana, 18, 59-64.
30. Harris, R.N., James, T.Y., Lauer, A., Simon, M.A. & Patel, A. (2006) Amphibian pathogen Batrachochytrium dendrobatidis is inhibited by the cutaneous bacteria of amphibian species. EcoHealth, 3, 53-56.
31. Hero, J.-M., Williams, S.E. & Magnusson, W.E. (2005) Ecological traits of declining amphibians in upland areas of eastern Australia. Journal of Zoology, 267, 221-232.
32. Highton, R. (2005) Declines of eastern North American woodland salamanders (Plethodon). Status and conservation of U.S. amphibians (ed. by M.J. Lannoo), pp 34-46. University of California Press, Berkeley, CA.
33. Hijmans, R.J., Cameron, S.E., Parra, J.L., Jones, P.G. & Jarvis, A. (2005) Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25, 1965-1978.
34. Hines, J.E. (2006) PRESENCE - software to estimate patch occupancy and related parameters. USGS-PWRC, Available at: http://www.mbr-pwrc.usgs.gov/software.html (accessed September 2011).
35. Hothorn, T. & Hornik, K. (2011) exactRankTests: exact distributions for rank and permutation tests. R package version 0.8-22.
36. Houlahan, J.E., Findlay, C.S., Schmidt, B.R., Meyer, A.H. & Kuzmin, S.L. (2000) Quantitative evidence for global amphibian population declines. Nature, 404, 752-755.
37. Hunsaker, D. & Potter, F.E., Jr (1960) "Red leg" in a natural population of amphibians. Herpetologica, 16, 285-286.
38. Hyatt, A.D., Boyle, D.G., Olsen, V., Boyle, D.B., Berger, L., Obendor, D., Dalton, A., Kriger, K., Hero, M., Hines, H., Phillott, R., Campbell, R., Marantelli, G., Gleason, F. & Colling, A. (2007) Diagnostic assays and sampling protocols for the detection of Batrachochytrium dendrobatidis Diseases of Aquatic Organisms, 73, 175-192.
39. Hyde, E.J. & Simons, T.R. (2001) Sampling plethodontid salamanders: sources of variability. Journal of Wildlife Management, 65, 624-632.
40. Jenkins, M.A. (2007) Vegetation communities of Great Smoky Mountains National Park. Southeastern Naturalist, 6, 35-56.
41. Johnson, P.T.J., McKenzie, V.J., Peterson, A.C., Kerby, J.L., Brown, J., Blaustein, A.R. & Jackson, T. (2011) Regional decline of an iconic amphibian associated with elevation, land-use change, and invasive species. Conservation Biology, 25, 556-566.
42. 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.
43. Kozak, K.H., Weisrock, D.W. & Larson, A. (2006) Rapid lineage accumulation in a non-adaptive radiation: phylogenetic analysis of diversification rates in eastern North American woodland salamanders (Plethodontidae: Plethodon). Proceedings of the Royal Society B: Biological Sciences, 273, 539-546.
44. Lips, K.R. (2011) Museum collections: mining the past to manage the future. Proceedings of the National Academy of Sciences USA, 108, 9323-9324.
45. Lips, K.R., Reeve, J.D. & Witters, L.R. (2003) Ecological traits predicting amphibian population declines in Central America. Conservation Biology, 17, 1078-1088.
46. 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 on a Neotropical amphibian community. Proceedings of the National Academy of Sciences USA, 103, 3165-3170.
47. Lips, K.R., Diffendorfer, J., Mendelson, J.R. III & Sears, M.W. (2008) Riding the wave: reconciling the roles of disease and climate change in amphibian declines. PLoS Biology, 6, 441-454.
48. Mazerolle, M.J. (2012) AICcmodavg: model selection and multimodel inference based on (Q)AIC(c). R package version 1.24.
49. Means, D.B. & Travis, J. (2007) Declines in ravine-inhabiting dusky salamanders of the southeastern US coastal plain. Southeastern Naturalist, 6, 83-96.
50. Milanovich, J.R., Peterman, W.E., Nibbelink, N.P. & Maerz, J.C. (2010) Projected loss of a salamander diversity hotspot as a consequence of projected global climate change. PLoS ONE, 5, 1-10.
51. Murray, K.A., Retallick, R.W.R., Puschendorf, R., Skerratt, L.F., Rosauer, D., McCallum, H.I., Berger, L., Speare, R. & van der Wal, J. (2011) Assessing spatial patterns of disease risk to biodiversity: implications for the management of the amphibian pathogen, Batrachochytrium dendrobatidis Journal of Applied Ecology, 48, 163-173.
52. National Park Service, Great Smoky Mountains National Park. (2007) Vegetation Disturbance History at Great Smoky Mountains National Park, Tennessee and North Carolina. National Park Service, Great Smoky Mountains National Park, Resource Management and Science. Geospatial Dataset-1045868. Available at: https://irma.nps.gov/App/Reference/Profile/1045868 (accessed October 2011).
53. Ouellet, M., Mikaelian, I., Pauli, B.D., Rodrigue, J. & Green, D.M. (2005) Historical evidence of widespread chytrid infection in North American amphibian populations. Conservation Biology, 19, 1431-1440.
54. Parolo, G., Rossi, G. & Ferranrini, A. (2008) Toward improved species niche modeling: Arnica montana in the Alps as a case study. Journal of Applied Ecology, 45, 1410-1418.
55. Pauly, D. (1995) Anecdotes and the shifting baseline syndrome of fisheries. Trends in Ecology and Evolution, 10, 430.
56. Pearson, R.G., Raxworthy, C.J., Nakamura, M. & Peterson, A.T. (2007) Predicting species distributions from small numbers of occurrence records: a test case using cryptic geckos in Madagascar. Journal of Biogeography, 34, 102-117.
57. Pechmann, J.H.K. & Wilbur, H.M. (1994) Putting declining amphibian populations in perspective: natural fluctuations and human impacts. Herpetologica, 50, 65-84.
58. Pechmann, J.H.K., Scott, D.E., Semlitsch, R.D., Caldwell, J.P., Vitt, L.J. & Gibbons, J.W. (1991) Declining amphibian populations: the problem of separating human impacts from natural fluctuations. Science, 253, 892-895.
59. Petranka, J.W., Eldridge, M.E. & Haley, K.E. (1993) Effects of timber harvesting on southern Appalachian salamanders. Conservation Biology, 7, 363-370.
60. Phillips, S.J., Anderson, R.P. & Schapire, R.E. (2006) Maximum entropy modeling of species geographic distributions. Ecological Modeling, 190, 231-259.
61. Pounds, J.A., Fogden, M.P.L., Savage, J.M. & Gorman, G.C. (1997) Tests of null models for amphibian declines on a tropical mountain. Conservation Biology, 11, 1307-1322.
62. Pounds, J.A., Bustamante, M.R., Coloma, L.A., Consuegra, J.A., Fogden, M.P.L., Foster, P.N., La Marca, E., Masters, K.L., Merino-Viteri, A., Puschendorf, R., Santiago, R.G., Sánchez-Azofeifa, A., Still, C.J. & Young, B.E. (2006) Widespread amphibian extinctions from epidemic disease driven by global warming. Nature, 39, 161-167.
63. Qian, S.S., Cuffney, T.F., Alameddine, I., McMahon, G. & Reckhow, K.H. (2010) On the application of multilevel modeling in environmental and ecological studies. Ecology, 91, 355-361.
64. R Development Core Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, Available at: http://www.R-project.org/ (accessed September 2011).
65. Ron, S.R., Duellman, W.E., Coloma, L.A. & Bustamante, M.R. (2003) Population decline of the Jambato toad Atelopus ignescens (Anura: Bufonidae) in the Andes of Ecuador. Journal of Herpetology, 37, 116-126.
66. Rossi, J.-P. (2011) Rich: Species richness estimation and comparison. R package version 0.1.
67. Roulin, A. & Bersier, L.F. (2007) Nestling barn owls beg more intensely in the presence of their mother than in the presence of their father. Animal Behaviour, 74, 1099-1106.
68. Rovito, S.M., Parra-Olea, G., Vásquez-Almazán, C.R., Papenfuss, T.J. & Wake, D.B. (2009) Dramatic declines in Neotropical salamander populations are an important part of the global amphibian crisis. Proceedings of the National Academy of Sciences USA, 106, 3231-3236.
69. Savage, A.E. & Zamudio, K.R. (2011) MHC genotypes associate with resistance to a frog-killing fungus. Proceedings of the National Academy of Sciences USA, 108, 16705-16710.
70. Schmidt, B.R. (2009) Count data, detection probabilities, and the demography, dynamics, distribution, and decline of amphibians. Comptes Rendus Biologies, 326, 119-124.
71. Shaffer, H.B., Fisher, R.N. & Davidson, C. (1997) The role of natural history collections in documenting species declines. Trends in Ecology and Evolution, 13, 27-30.
72. Smith, C.K. & Petranka, J.W. (2000) Monitoring terrestrial salamander populations: repeatability and validity of area-constrained cover object searches. Journal of Herpetology, 34, 547-557.
73. Smith, K.G., Lips, K.R. & Chase, J.M. (2009) Selecting for extinction: nonrandom disease-associated extinction homogenizes amphibian biotas. Ecology Letters, 12, 1069-1078.
74. Stuart, S.N., Chanson, J.S., Cox, N.A., Young, B.E., Rodrigues, A.S.L., Fischman, D.L. & Walker, R.W. (2004) Status and trends of amphibian declines and extinctions worldwide. Science, 306, 1783-1786.
75. Sugiura, N. (1978) Further analysis of the data by Akaike's information criterion and the finite corrections. Communications in Statistics - Theory and Methods, 7, 13-26.
76. Tilley, S.G. (1973) Life histories and natural selection in populations of the salamander Desmognathus ochrophaeus Ecology, 54, 3-17.
77. Travis, J. (1994) Calibrating our expectations in studying amphibian populations. Herpetologica, 50, 104-108.
78. Ver Hoef, J.M. & Boveng, P.L. (2007) Quasi-poisson vs. negative binomial regression: how should we model overdispersed count data? Ecology, 88, 2766-2772.
79. Vredenburg, V.T., Knapp, R.A., Tunstall, T.S. & Briggs, C.J. (2010) Dynamics of an emerging disease drive large-scale amphibian population extinctions. Proceedings of the National Academy of Sciences USA, 107, 9689-9694.
80. Welsh, H.H., Jr & Droege, S. (2000) A case for using plethodontid salamanders for monitoring biodiversity and ecosystem integrity of North American forests. Conservation Biology, 15, 558-569.
81. Whitfield, S.M., Bell, K.E., Philippi, T., Sasa, M., Bolaños, F., Chaves, G., Savage, J.M. & Donnelly, M.A. (2007) Amphibian and reptile declines over 35 years at La Selva, Costa Rica. Proceedings of the National Academy of Sciences USA, 104, 8352-8356.
82. Wyman, R.L. & Jancola, J. (1992) Degree and scale of terrestrial acidification and amphibian community structure. Journal of Herpetology, 26, 392-401.