Effects of the amphibian chytrid fungus and four insecticides on pacific treefrogs (Pseudacris regilla)

Journal of Herpetology

Volumn 46, Issue 4, 2012, Pages 625-631

  Kleinhenz, Peter ^a   Boone, Michelle D ^a   Fellers, Gary ^b  

^a MIAMI UNIVERSITY   (United States)

^b U S GEOLOGICAL SURVEY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHIBIA; BATRACHOCHYTRIUM DENDROBATIDIS; FUNGI; HYLA; PSEUDACRIS; PSEUDACRIS REGILLA;

EID: 84871414048     PISSN: 00221511     EISSN: None     Source Type: Journal    
DOI: 10.1670/11-070     Document Type: Article

References (69)

1. ANGERMANN, J. E., G. M. FELLERS, AND F. MATSUMURA. 2002. Polychlorinated biphenyls and toxaphene in Pacific Tree Frog tadpoles (Hyla regilla) from the California Sierra Nevada, USA. Environmental Toxicology and Chemistry 21:2209-2215.
2. BERGER, L., R. SPEARE, P. DASZAK, D. E. GREEN, A. A. CUNNINGHAM, C. L. GOGGIN, R. SLOCOMBE, M. A. RAGAN, A. D. HYATT, K. R. MCDONALD, ET AL. 1998. Chytridiomycosis causes amphibian mortality associated with population declines in the rain forest of Australia and Central America. Proceedings of the National Academy of Science USA 95: 9031-9036. (Pubitemid 28350609)
3. BLAKLEY, B., P. BROUSSEAU, M. FORUNIER, AND I. VOCCIA. 1999. Immunotoxicolgy of pesticides: a review. Toxicology and Industrial Health 15: 119-132.
4. BLAUSTEIN, A. R., J. M. ROMANSIC, E. A. SCHEESSELE, B. A. HAN, A. P. PESSIER, AND J. E. LONGCORE. 2005. Interspecific variation in susceptibility of frog tadpoles to the pathogenic fungus Batrachochytrium dendrobatidis. Conservation Biology 19:1460-1468. (Pubitemid 41721957)
5. BOONE, M. D., AND C. M. BRIDGES. 2003. Impacts of chemical contaminants on amphibian populations. In R. D. Semlitsch (ed.), Amphibian Conservation, pp. 152-167. Smithsonian Press, Washington, DC.
6. BOONE, M. D., AND R. D. SEMLITSCH. 2001. Interactions of insecticide with larval density and predation in experimental amphibian communities. Conservation Biology 15:228-238. (Pubitemid 32180348)
7. BOYLE, D. G., D. B. BOYLE, V. OLSEN, J. A. T. MORGAN, AND A. D. HYATT. 2004. Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Diseases of Aquatic Organisms 60:141-148. (Pubitemid 39588268)
8. BRIDGES, C. M. 2000. Long-term effects of pesticide exposure at various life stages of the Southern Leopard Frog (Rana sphenocephala). Archives of Environmental Contamination and Toxicology 39:91-96. (Pubitemid 30327544)
9. BRIGGS, C. J., V. T. VREDENBURG, R. A. KNAPP, AND L. J. RACHOWICZ. 2005. Investigating the population-level effects of chytridiomycosis: an emerging infectious disease of amphibians. Ecology 86:3149-3159. (Pubitemid 43086888)
10. CAREY, C., AND C. J. BRYANT. 1995. Possible interrelations among environmental toxicants, amphibian development, and decline of amphibian populations. Environmental Health Perspectives 103:13-14.
11. CAREY, C., J. E. BRUZGUL, L. J. LIVO, M. L. WALLING, K. A. KUEHL, B. F. DIXON, A. P. PESSIER, R. A. ALFORD, AND K. B. ROGERS. 2006. Experimental exposures of Boreal Toads (Bufo boreas) to a pathogenic chytrid fungus (Batrachochytrium dendrobatidis). Eco-Health 3:5-21. (Pubitemid 43363639)
12. CHRISTIN, M. S., A. D. GENDRON, P. BROUSSEAU, L. MENARD, D. J. MARCOGLIESE, D. CYR, S. RUBY, AND M. FOURNIER. 2003. Effects of agricultural pesticides on the immune system of Rana pipiens and on its resistance to parasitic infection. Environmental Toxicology and Chemistry 22:1127-1133. (Pubitemid 36438194)
13. COLLINS, J. P., AND M. L. CRUMP. 2010. Extinction in Our Times: Global Amphibian Decline. Oxford University Press, New York.
14. CONLON, J. M. 2011. The contribution of skin antimicrobial peptides to the system of innate immunity in anurans. Cell Tissue Research 343: 201-212.
15. DASZAK, P., A. A. CUNNINGHAM, AND A. D. HYATT. 2003. Infectious disease and amphibian population declines. Diversity and Distributions 9: 141-150. (Pubitemid 36317431)
16. DASZAK, P., D. E. SCOTT, A. M. KILPATRICK, C. FAGGIONI, J.W. GIBBONS, AND D. PORTER. 2005. Amphibian population declines at Savannah River Site are linked to climate not chytridiomycosis. Ecology 86:3232-3237. (Pubitemid 43086897)
17. DAVIDSON, C. 2004. Declining downwind: amphibian population declines in California and historical pesticide use. Ecological Applications 14: 1892-1902. (Pubitemid 40020374)
18. DAVIDSON, C., H. B. SHAFFER, AND M. R. JENNINGS. 2001. Declines of the California Red-Legged Frog: climate, UV-B, habitat, and pesticides hypotheses. Ecological Applications 14:464-479. (Pubitemid 32276736)
19. -. 2002. Spatial tests of the pesticide drift, habitat destruction, UVB, and climate-change hypotheses for California amphibian declines. Conservation Biology 16:1588-1601. (Pubitemid 35456970)
20. DAVIDSON, C., M. F. BENARD, H. B. SHAFFER, J.M. PARKER, C. O'LEARY, J. M. CONLON, AND L. A. ROLLINS-SMITH. 2007. Effects of chytrid and carbaryl exposure on survival, growth, and skin peptide defenses in foothill Yellow-Legged Frogs. Environmental Science and Technology 41:1771-1776. (Pubitemid 46362485)
21. DISTEL, C. A., AND M. D. BOONE. 2010. Effects of aquatic exposure to the insecticide carbaryl are species-specific across life stages and mediated by heterospecific competitors in anurans. Functional Ecology 24:1342-1352.
22. FELLERS, G. M., D. F. BRADFORD, D. PRATT, AND L. L.WOOD. 2007. Demise of repatriated populations of mountain Yellow-Legged Frogs (Rana muscosa) in the Sierra Nevada of California. Herpetological Conservation and Biology 21:5-21.
23. FISHER, M. C., T. W. J. GARNER, AND S. F. WALKER. 2009. Global emergence of Batrachochytrium denderobatidis and amphibian chytridiomycosis in space, time, and host. Annual Review of Microbiology 63:291-310.
24. GAHL, M. K., B. D. PAULI, AND J. E. HOULAHAN. 2011. Effects of chytrid fungus and a glyphosate-based herbicide on survival and growth of Wood Frogs (Lithobates sylvaticus). Ecological Applications doi:10. 1890/10-2319.1.
25. GARCIA, T. S., J. M. ROMANSIC, AND A. R. BLAUSTEIN. 2006. Survival of three species of anuran metamorphs exposed to UV-B radiation and the pathogenic fungus Batrachochytrium dendrobatidis. Disease of Aquatic Organisms 72:163-169. (Pubitemid 44799860)
26. GARNER, T. W., S. WALKER, J. BOSCH, S. LEECH, J. M. ROWCLIFFE, A. A. CUNNINGHAM, AND M. C. FISHER. 2009. Life history tradeoffs influence mortality associated with the amphibian pathogen Batrachochytrium dendrobatidis. Oikos 118:783-791.
27. GENDRON, A. D., D. J. MARCOGLIESE, S. BARBEAU, A. S. CHRISTIN, P. BROUSSEAU, S. RUBY, D. CYR, AND M. FOURNIER. 2003. Exposure of Leopard Frogs to a pesticide mixture affects life history characteristics of the lungworm Rhabdias ranae. Oecologia 135:469-476. (Pubitemid 36639466)
28. GOSNER, N. 1960. A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183-190.
29. HARRIS, R. N., T. Y. JAMES, A. LAUER, M. A. SIMON, AND A. PATEL. 2006. Amphibian pathogen Batrachochytrium dendrobatidis is inhibited by the cutaneous bacteria of amphibian species. EcoHealth 3:53-56. (Pubitemid 43363645)
30. HAYES, T. B., P. CASE, C. CHUI, D. CHUNG, C. HAEFFELE, K. HASTON, M. LEE, V. P. MAI, Y. MARJUOA, J. PARKER, ET AL. 2006. Pesticide mixtures, endocrine disruption, and amphibian declines: are we underestimating the impact? Environmental Health Perspectives 114:40-50.
31. HAYES, T. B., P. FALSO, S. GALLIPEAU, AND M. STICE. 2010. The cause of global amphibian declines: a developmental endocrinologist's perspective. Journal of Experimental Biology 213:921-933.
32. HOULAHAN, J. E., C. S. FINDLAY, B. R. SCHMIDT, A. H. MEYER, AND S. L. KUZMIN. 2000. Quantitative evidence for global amphibian population declines. Nature 404:752-755. (Pubitemid 30212400)
33. KNAPP, R. A., AND J. A. T. MORGAN. 2006. Tadpole mouthpart depigmentation as an accurate indicator of chytridiomycosis, an emerging disease of amphibians. Copeia 2006:188-197. (Pubitemid 43837093)
34. KUIVILA, K. M., AND C. G. FOE. 1995. Concentrations, transport, and biological effects of dormant spray pesticides in the San Francisco Estuary, California. Environmental Toxicology and Chemistry 14: 1141-1150.
35. LIPS, K. R., J. DIFFENDORFER, J. R. MENDELSON III, AND M. W. SEARS. 2008. Riding the wave: reconciling the roles of disease and climate change in amphibian declines. PLoS Biology 6:441-454.
36. LONGCORE, J. R., J. E. LONGCORE, A. P. PESSIER, AND W. A. HALTEMAN. 2007. Chytridiomycosis widespread in anurans of northeastern United States. Journal of Wildlife Management 71:435-444.
37. MCCONNELL, L. L., J. S. LENOIR, S. DATTA, AND J. N. SEIBER. 1998. Wet deposition of current-use pesticides in the Sierra Nevada mountain range, California, USA. Environmental Toxicology and Chemistry 17:1908-1916. (Pubitemid 28449620)
38. MILLS, N. E., AND R. D. SEMLITSCH. 2004. Competition and predation mediate indirect effects of an insecticide on Southern Leopard Frogs. Ecological Applications 14:1041-1054. (Pubitemid 39188055)
39. MUTHS, E., P. S. CORN, A. P. PESSIER, AND D. E. GREEN. 2003. Evidence for disease-related amphibian decline in Colorado. Biological Conservation 110:357-365. (Pubitemid 36238315)
40. PARRIS, M. J., AND D. R. BAUD. 2004. Interactive effects of a heavy metal and chytridiomycosis on Gray Treefrog larvae (Hyla chrysoscelis). Copeia 2004:344-350. (Pubitemid 38611094)
41. PARRIS, M. J., AND T. O. CORNELIUS. 2004. Fungal pathogen causes competitive and developmental stress in larval amphibian communities. Ecology 85:3385-3395. (Pubitemid 40084786)
42. RACHOWICZ, L. J., AND V. T. VREDENBURG. 2004. Transmission of Batrachochytrium dendrobatidis within and between amphibian life stages. Diseases of Aquatic Organisms 61:75-83. (Pubitemid 39588238)
43. RELYEA, R. A. 2003. Predator cues and pesticides: a double dose of danger for amphibians. Ecological Applications 13:1515-1521. (Pubitemid 38362231)
44. -. 2004. Synergistic impacts of malathion and predatory stress on six species of North American tadpoles. Environmental Toxicology and Chemistry 23:1080-1084. (Pubitemid 38418661)
45. -. 2009. A cocktail of contaminants: how mixtures of pesticides at low concentrations affect aquatic communities. Oecologia 159:363-376.
46. RELYEA, R. A., AND J. HOVERMAN. 2006. Assessing the ecology in ecotoxicology: a review and synthesis in freshwater systems. Ecology Letters 9:1157-1171. (Pubitemid 44401587)
47. RELYEA, R. A., AND N. M. MILLS. 2001. Predator-induced stress makes the pesticide carbaryl more deadly to Gray Treefrog tadpoles (Hyla versicolor). Proceedings of the National Academy of Sciences USA 98: 2491-2496. (Pubitemid 32209509)
48. ROHR, J. R., AND T. R. RAFFEL. 2010. Linking global climate and temperature variability to widespread amphibian declines putatively caused by disease. Proceedings of the National Academy of Sciences USA 107:8269-8274.
49. ROMANSIC, J. M., P. T. J. JOHNSON, C. L. SEARLE, J. E. JOHNSON, T. S. TUNSTALL, B. A. HAN, J. R. ROHR, AND A. R. BLAUSTEIN. 2011. Individual and combined effects of multiple pathogens on Pacific Treefrogs. Oecologia 166:1029-1041.
50. ROTHERMEL, B. B., S. C. WALLS, J. C.MITCHELL, C. K. DODD, L. K. IRWIN, D. E. GREEN, V. M. VAZQUEZ, J. W. PETRANKA, AND D. J. STEVENSON. 2008. Widespread occurrence of the amphibian chytrid fungus Batrachochytrium dendrobatidis in the southeastern USA. Diseases of Aquatic Organisms 82:3-18.
51. SCOTT, D. E. 1994. The effect of larval density on adult demographic traits in Ambystoma opacum. Ecology 75:1383-1396.
52. SEMLITSCH, R. D., D. E. SCOTT, AND J. H. K. PECHMANN. 1988. Time and size at metamorphosis related to adult fitness in Ambystoma talpoideum. Ecology 69:184-192. (Pubitemid 19317739)
53. SKELLY, D. K., AND E. E. WERNER. 1990. Behavioral and life-historical responses of larval American Toads to an odonate predator. Ecology 71:2313-2322.
54. SKERRATT, L. F., L. BERGER, R. SPEARE, S. CASHINS, K. R. MCDONALD, A. D. PHILLOTT, H. B. HINES, AND N. KENYON. 2007. Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth 4:125-134. (Pubitemid 47038075)
55. SMITH, D. C. 1987. Adult recruitment in Chorus Frogs: effects of size and date at metamorphosis. Ecology 68:344-350.
56. SPARLING, D. W., AND G. M. FELLERS. 2007. Comparative toxicity of chlorpyrifos, diazinon, malathion, and their oxon derivatives to larval Rana boylii. Environmental Pollution 147:535-539. (Pubitemid 46711131)
57. -. 2009. Toxicity of two insecticides to California, USA, anurans and its relevance to declining amphibian populations. Environmental Toxicology and Chemistry 28:1696-1703.
58. SPARLING, D. W., G. M. FELLERS, AND L. L. MCCONNELL. 2001. Pesticides and amphibian population declines in California, USA. Environmental Toxicology and Chemistry 20:1591-1595. (Pubitemid 32550022)
59. STOCKWELL, M. P., J. CLULOW, AND M. J. MAHONY. 2010. Host species determines whether infection load increases beyond disease-causing thresholds following exposure to the amphibian chytrid fungus. Animal Conservation 13:62-71.
60. STUART, S. N., J. S. CHANSON, N.A.COX, B. E. YOUNG, A. S. L. RODRIGUES, D. FISCHMAN, AND R. W. WALLER. 2004. Status and trends of amphibian declines and extinctions worldwide. Science 306:1783-1786. (Pubitemid 39601397)
61. TAYLOR, S. K., E. S. WILLIAMS, AND K. W. MILLS. 1999. Effects of malathion on disease susceptibility in Woodhouse's Toads. Journal of Wildlife Diseases 25:536-541. (Pubitemid 129552749)
62. TOBLER, U., AND B. R. SCHMIDT. 2010. Within-and among-population variation in chytridiomycosis-induced mortality in the toad Alytes obstetricans. PLos One 5:e10927.
63. VENESKY, M. D. 2011. Dynamics of an Emerging Infectious Disease of Amphibians: From Individuals to Communities. Unpubl. Ph.D. diss., University of Memphis, Memphis, TN.
64. VENESKY, M. D., M. J. PARRIS, AND A. STORFER. 2010a. Impacts of Batrachochytrium dendrobatidis infection on tadpole foraging performance. EcoHealth 6:565-575.
65. VENESKY, M. D., R. J.WASSERSUG, AND M. J. PARRIS. 2010b. Fungal pathogen changes the feeding kinematics of larval anurans. Journal of Parasitology 96:552-557.
66. -. 2010c. How does change in labial tooth row number affect feeding kinematics and foraging performance of a ranid tadpole (Lithobates sphenocehalus)? Biology Bulletin 218:160-168.
67. VREDENBURG, V. T., R. A. KNAPP, T. S. TUNSTALL, AND C. J. BRIGGS. 2010. Dynamics of an emerging disease drive large-scale amphibian population extinction. Proceedings of the National Academy of Sciences USA 107:9689-9694.
68. WIDDER, P. D., AND J. R. BIDWELL. 2008. Tadpole size, cholinesterase activity, and swim speed in four frog species after exposure to sublethal concentrations of chlorpyrifos. Aquatic Toxicology 88: 9-18.
69. WOODHAMS, D. C., K. ARDIPRADJA, R. A. ALFORD, G. MARANTELLI, L. K. REINERT, AND L. A. ROLLINS-SMITH. 2007. Resistance to chytridiomycosis varies among amphibian species and is correlated with skin peptide defenses. Animal Conservation 10:409-417. (Pubitemid 350020088)