Disease Risk in Temperate Amphibian Populations Is Higher at Closed-Canopy Sites

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Becker, C Guilherme ^a   Rodriguez, David ^a   Longo, Ana V ^a   Talaba, Amanda L ^a   Zamudio, Kelly R ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHIBIA; ANURA; ARTICLE; CANOPY; CAUSAL ATTRIBUTION; CHYTRIDIOMYCOSIS; CLOSED CANOPY; COVER CROP; DISEASE PREDISPOSITION; DYNAMICS; ENVIRONMENTAL FACTOR; EXPLANATORY VARIABLE; FOREST FRAGMENTATION; HABITAT STRUCTURE; HOST PATHOGEN INTERACTION; INFECTION RATE; LITHOBATES CLAMITANS; MICROCLIMATE; NONHUMAN; POND; PREVALENCE; UNITED STATES; VEGETATION; WATER TEMPERATURE; WILD SPECIES;

ANIMALS; CHYTRIDIOMYCOTA; CLIMATE; CONSERVATION OF NATURAL RESOURCES; ECOSYSTEM; HOST-PATHOGEN INTERACTIONS; MYCOSES; NEW YORK; RANIDAE; TREES;

AMPHIBIA; ANURA; BATRACHOCHYTRIUM DENDROBATIDIS; FUNGI; LITHOBATES;

EID: 84868283434     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0048205     Document Type: Article

References (65)

1. Ostfeld RS, Keesing F, (2000) Biodiversity and disease risk: The case of lyme disease. Conserv Biol 14: 722-728.
2. McCallum H, Dobson A, (2002) Disease, habitat fragmentation and conservation. Source. P Roy Soc Lond B Bio 269: 2041-2049.
3. Keesing F, Belden LK, Daszak P, Dobson A, Harvell CD, et al. (2010) Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468: 647-652.
4. Ostfeld RS, Keesing F, (2012) Effects of host diversity on infectious disease. Annu Rev Ecol Evol Syst 43: 157-182.
5. Meentemeyer RK, Rank NE, Anacker BL, Rizzo DM, Cushman JH, (2008) Influence of land-cover change on the spread of an invasive forest pathogen. Ecol Appl 18: 159-171.
6. Becker CG, Zamudio KR, (2011) Tropical amphibian populations experience higher disease risk in natural habitats. P Natl Acad Sci USA 108: 9893-9898.
7. Arens P, van der Sluis T, van't Westende WPC, Vosman B, Vos CC, et al. (2007) Genetic population differentiation and connectivity among fragmented Moor frog (Rana arvalis) populations in The Netherlands. Landscape Ecol 22: 1489-1500.
8. Andersen LW, Fog K, Damgaard C, (2004) Habitat fragmentation causes bottlenecks and inbreeding in the European tree frog (Hyla arborea). P Roy Soc Lond B Bio 271: 1293-1302.
9. Costa MH, Foley JA, (2000) Combined effects of deforestation and doubled atmospheric CO2 concentrations on the climate of Amazonia. J Climate 13: 18-34.
10. Kapos V, (1989) Effects of isolation on the water status of forest patches in the Brazilian Amazon. J Trop Ecol 5: 173-185.
11. Patz JA, Graczyk TK, Geller N, Vittor AY, (2000) Effects of environmental change on emerging parasitic diseases. Int J Parasitol 30: 1395-1405.
12. Pounds JA, Bustamante MR, Coloma LA, Consuegra JA, Fogden MPL, et al. (2006) Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 439: 161-167.
13. Woodhams DC, Alford RA, Briggs CJ, Johnson M, Rollins-Smith LA, (2008) Life-history trade-offs influence disease in changing climates: Strategies of an amphibian pathogen. Ecology 89: 1627-1639.
14. Ostfeld RS, Glass GE, Keesing F, (2005) Spatial epidemiology: an emerging (or re-emerging) discipline. Trends Ecol Evol 20: 328-336.
15. Kilpatrick AM, Briggs CJ, Daszak P, (2010) The ecology and impact of chytridiomycosis: an emerging disease of amphibians. Trends Ecol Evol 25: 109-118.
16. Cushman SA, (2006) Effects of habitat loss and fragmentation on amphibians: A review and prospectus. Biol Conserv 128: 231-240.
17. Becker CG, Fonseca CR, Haddad CFB, Batista RF, Prado PI, (2007) Habitat split and the global decline of amphibians. Science 318: 1775-1777.
18. Gaston KJ (2003) The Structure and Dynamics of Geographic Ranges. Oxford: Oxford University Press. 266 p.
19. Gibbs JP, (1998) Distribution of woodland amphibians along a forest fragmentation gradient. Landscape Ecol 13: 263-268.
20. Rohr JR, Raffel TR, Romansic JM, McCallum H, Hudson PJ, (2008) Evaluating the links between climate, disease spread, and amphibian declines. P Natl Acad Sci USA 105: 17436-17441.
21. Rohr JR, Raffel TR, (2010) Linking global climate and temperature variability to widespread amphibian declines putatively caused by disease. P Natl Acad Sci USA 107: 8269-8274.
22. Longo AV, Burrowes PA, Joglar RL, (2010) Seasonality of Batrachochytrium dendrobatidis infection in direct-developing frogs suggests a mechanism for persistence. Dis Aquat Organ 92: 253-260.
23. Raffel TR, Michel PJ, Sites EW, Rohr JR, (2010) What drives chytrid infections in newt populations? associations with substrate, temperature, and shade. Ecohealth 7: 526-536.
24. Carey C, Cohen N, Rollins-Smith L, (1999) Amphibian declines: an immunological perspective. Dev Comp Immunol 23: 459-472.
25. Carey C, (2005) How physiological methods and concepts can be useful in conservation biology. Integr Comp Biol 45: 4-11.
26. Wikelski M, Cooke SJ, (2006) Conservation physiology. Trends Ecol Evol 21: 38-46.
27. Navas CA, Otani L, (2007) Physiology, environmental change, and anuran conservation. Phyllomedusa 6: 83-103.
28. Rollins-Smith LA, Ramsey JP, Pask JD, Reinert LK, Woodhams DC, (2011) Amphibian immune defenses against chytridiomycosis: impacts of changing environments. Integr Comp Biol 51: 552-562.
29. Carey C, (1993) Environmental physiology of the amphibians. Science 259: 390-391.
30. Kiesecker JM, (2002) Synergism between trematode infection and pesticide exposure: A link to amphibian limb deformities in nature? P Natl Acad Sci USA 15: 9900-9904.
31. Raffel TR, Rohr JR, Kiesecker JM, Hudson PJ, (2006) Negative effects of changing temperature on amphibian immunity under field conditions. Funct Ecol 20: 819-828.
32. Piotrowski JS, Annis SL, Longcore JE, (2004) Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. Mycologia 96: 9-15.
33. Bustamante HM, Livo LJ, Carey C, (2010) Effects of temperature and hydric environment on survival of the Panamanian Golden Frog infected with a pathogenic chytrid fungus. Integr Zool 5: 143-153.
34. Ryan JM (2008) Adirondack wildlife: a field guide. Hanover: University of New Hampshire Press. 249 p.
35. Olson DM, Dinerstein E, Wikramanayake ED, Burgess ND, Powell GVN, et al. (2001) Terrestrial ecoregions of the worlds: A new map of life on Earth. Bioscience 11: 933-938.
36. Longcore JR, Longcore JE, Pessier AP, Halteman WA, (2007) Chytridiomycosis widespread in anurans of northeastern United States. J Wildlife Manage 71: 435-444.
37. Hecnar SJ, MCloskey RT, (1997) Spatial scale and determination of species status of the Green Frog. Conserv Biol 11: 670-682.
38. IUCN, Conservation International, NatureServe (2012) Global amphibian assessment. Available: www.globalamphibians.org. Accessed 5 Feb 2012.
39. Boyle DG, Boyle DB, Olsen V, Morgan JAT, Hyatt AD, (2004) Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Dis Aquat Organ 60: 141-148.
40. Hyatt AD, Boyle DG, Olsen V, Boyle DB, Berger L, et al. (2007) Diagnostic assays and sampling protocols for the detection of Batrachochytrium dendrobatidis. Dis Aquat Organ 73: 175-192.
41. Simpson EH, (1949) Measurement of Diversity. Nature 163: 688-688.
42. USGS (2010) Orthoimagery 2008-2009 at 30 and 15 cm resolution. Available: http://earthexplorer.usgs.gov. Accessed 2011 Nov 10.
43. Kriger KM, Pereoglou F, Hero JM, (2007) Latitudinal variation in the prevalence and intensity of chytrid (Batrachochytrium dendrobatidis) infection in Eastern Australia. Conserv Biol 21: 1280-1290.
44. Brem FMR, Lips KR, (2008) Batrachochytrium dendrobatidis infection patterns among Panamanian amphibian species, habitats and elevations during epizootic and enzootic. Dis Aquat Organ 81: 189-202.
45. Lemon PE, (1956) A Spherical densitometer for estimating forest overstory density. Forest Sci 2: 314-320.
46. Savage AE, Sredl MJ, Zamudio KR, (2011) Disease dynamics vary spatially and temporally in a North American amphibian. Biol Conserv 144: 1910-1915.
47. Rangel TF, Diniz-Filho JAF, Bini LM, (2010) SAM: a comprehensive application for Spatial Analysis in Macroecology. Ecography 33: 46-50.
48. Systat (2007) SYSTAT for Windows, version 11. (Richmond, California).
49. Regosin JV, Windmiller BS, Reed JM, (2003) Terrestrial habitat use and winter densities of the wood frog (Rana sylvatica). J Herpetol 37: 390-394.
50. Puschendorf R, Hoskin CJ, Cashins SD, McDonald K, Skerratt LF, et al. (2011) Environmental Refuge from Disease-Driven Amphibian Extinction. Conserv Biol 25: 956-964.
51. Puschendorf R, Chaves G, Crawford AJ, Brooks DR, (2005) Eleutherodactylus ranoides (NCN). Dry Forest population, refuge from decline? Herpetol Rev 36: 53.
52. Forrest MJ, Schlaepfer MA, (2011) Nothing a Hot Bath Won't Cure: Infection Rates of Amphibian Chytrid Fungus Correlate Negatively with Water Temperature under Natural Field Settings. PLoS One 6: e28444.
53. Daskin JH, Alford RA, Puschendorf R, (2011) Short-Term Exposure to Warm Microhabitats Could Explain Amphibian Persistence with Batrachochytrium dendrobatidis. PLoS One 6: e26215.
54. Richards-Zawacki CL, (2010) Thermoregulatory behaviour affects prevalence of chytrid fungal infection in a wild population of Panamanian golden frogs. P Roy Soc Lond B Bio 1681: 519-528.
55. Murphy PJ, St-Hilaire S, Corn PS, (2011) Temperature, hydric environment, and prior pathogen exposure alter the experimental severity of chytridiomycosis in boreal toads. Dis Aquat Organ 95: 31-42.
56. Ribas L, Li MS, Doddington BJ, Robert J, Seidel JA, et al. (2009) Expression Profiling the Temperature-Dependent Amphibian Response to Infection by Batrachochytrium dendrobatidis. PLoS One 4: e8408.
57. Knapp RA, Briggs CJ, Smith TC, Maurer JR, (2011) Nowhere to hide: impact of a temperature-sensitive amphibian pathogen along an elevation gradient in the temperate zone. Ecosphere 2: art93.
58. Briggs CJ, Knapp RA, Vredenburg VT, (2010) Enzootic and epizootic dynamics of the chytrid fungal pathogen of amphibians. P Natl Acad Sci USA 107: 9695-9700.
59. Vredenburg VT, Knapp RA, Tunstall TS, Briggs CJ, (2010) Dynamics of an emerging disease drive large-scale amphibian population extinctions. P Natl Acad Sci USA 107: 9689-9694.
60. Searle CL, Biga LM, Spatafora JW, Blaustein AR, (2011) A dilution effect in the emerging amphibian pathogen Batrachochytrium dendrobatidis. P Natl Acad Sci USA 108: 16322-16326.
61. Gahl MK, Longcore JE, Houlahan JE, (2012) Varying Responses of Northeastern North American Amphibians to the Chytrid Pathogen Batrachochytrium dendrobatidis. Conserv Biol 26: 135-141.
62. Hof C, Araujo MB, Jetz W, Rahbek C, (2011) Additive threats from pathogens, climate and land-use change for global amphibian diversity. Nature 480: 516-U137.
63. Lips KR, Diffendorfer J, Mendelson JR III, Sears MW, (2008) Riding the wave: Reconciling the roles of disease and climate change in amphibian declines. PLoS Biol 6: 441-454.
64. Savage AE, Zamudio KR, (2011) MHC genotypes associate with resistance to a frog-killing fungus. P Natl Acad Sci USA 108: 16705-16710.
65. Puschendorf R, Carnaval AC, VanDerWal J, Zumbado-Ulate H, Chaves G, et al. (2009) Distribution models for the amphibian chytrid Batrachochytrium dendrobatidis in Costa Rica: proposing climatic refuges as a conservation tool. Divers Distrib 15: 401-408.