Ecological Research

, Volume 26, Issue 5, pp 897–908 | Cite as

Global stressors and the global decline of amphibians: tipping the stress immunocompetency axis

Special Feature Environmental change, pathogens and human linkages


There is a widespread consensus that the earth is experiencing a mass extinction event and at the forefront are amphibians, the most threatened of all vertebrate taxa. A recent assessment found that nearly one-third (32%, 1,856 species) of the world’s amphibian species are threatened. Amphibians have existed on the earth for over 300 million years, yet in just the last two decades there have been an alarming number of extinctions, nearly 168 species are believed to have gone extinct and at least 2,469 (43%) more have populations that are declining. Infectious diseases have been recognized as one major cause of worldwide amphibian population declines. This could be the result of the appearance of novel pathogens, or it could be that exposure to environmental stressors is increasing the susceptibility of amphibians to opportunistic pathogens. Here I review the potential effects of stressors on disease susceptibility in amphibians and relate this to disease emergence in human and other wildlife populations. I will present a series of case studies that illustrate the role of stress in disease outbreaks that have resulted in amphibian declines. First, I will examine how elevated sea-surface temperatures in the tropical Pacific since the mid-1970s have affected climate over much of the world and could be setting the stage for pathogen-mediated amphibian declines in many regions. Finally, I will discuss how the apparently rapid increase in the prevalence of amphibian limb deformities is linked to the synergistic effects of trematode infection and exposure to chemical contaminants.


Global amphibian declines Stress-mediated infection Climate change Pesticide exposure 


  1. Alemayehu T, Ye-ebiyo Y, Ghebreyesus TA, Witten KH, Bosman A, Teklehaimanot A (1998) Malaria, schistosomiasis, and intestinal helminths in relation to microdams in Tigray, northern Ethiopia. Parassitologia 40:259–267PubMedGoogle Scholar
  2. Alford RA, Bradfield KS, Richards SJ (2007) Global warming and amphibian losses. Nature 447:E3–E4PubMedCrossRefGoogle Scholar
  3. Allen CD, Breshears DD (1998) Drought-induced shift of a forest–woodland ecotone: rapid landscape response to climate variation. Proc Natl Acad Sci USA 95:14839–14842PubMedCrossRefGoogle Scholar
  4. Ankley GT, Diamond SA, Tietge JE, Holcombe GW, Jensen KM, Defoe DL et al (2002) Assessment of the risk of solar ultraviolet radiation to amphibians. I. Dose-dependent induction of hindlimb malformations in the northern leopard frog (Rana pipiens). Environ Sci Technol 36:2853–2858PubMedCrossRefGoogle Scholar
  5. Berger L, Speare R, Daszak P, Green DE, Cunningham AA, Goggin CL, Slocombe R, Ragan MA, Hyatt AD, McDonald KR, Hines HB, Lips KR, Marantelli G, Parkes H (1998) Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proc Natl Acad Sci USA 95:9031–9036PubMedCrossRefGoogle Scholar
  6. Blaustein AR, Bancroft BA (2007) Amphibian population declines: evolutionary considerations. Bioscience 57:437–444CrossRefGoogle Scholar
  7. Blaustein AR, Belden LK (2003) Amphibian defenses against ultraviolet-B radiation. Evol Dev 5:89–97PubMedCrossRefGoogle Scholar
  8. Blaustein AR, Johnson PT (2003) Explaining frog deformities. Sci Am 288:60–65PubMedCrossRefGoogle Scholar
  9. Blaustein AR, Kiesecker JM (2002) Complexity in conservation: lessons from the global decline of amphibian populations. Ecol Lett 5:597–608CrossRefGoogle Scholar
  10. Blaustein AR, Wake DB (1990) Declining amphibian populations: a global phenomenon? Trends Ecol Evol 5:203–204CrossRefGoogle Scholar
  11. Blaustein AR, Wake DB, Sousa WP (1994) Amphibian declines: judging stability, persistence, and susceptibility of populations to local and global extinctions. Conserv Biol 8:60–71CrossRefGoogle Scholar
  12. Blaustein AR, Kiesecker JM, Chivers DP, Anthony RG (1998) Ambient UV-B radiation causes deformities in amphibian embryos. Proc Natl Acad Sci USA 94:13735–13737CrossRefGoogle Scholar
  13. Bosch J, Carrascal LM, Durán L, Walker S, Fisher MC (2007) Climate change and outbreaks of amphibian chytridiomycosis in a montane area of central Spain: is there a link? Proc R Soc Lond B 274:253–260CrossRefGoogle Scholar
  14. Colborn T, Thayer K (2000) Aquatic ecosystems: harbingers of endocrine disruption. Ecol Appl 10:949–957CrossRefGoogle Scholar
  15. Collins JP, Storfer A (2003) Global amphibian declines: sorting the hypotheses. Divers Distrib 9:89–98CrossRefGoogle Scholar
  16. Collins JP, Brunner JL, Jancovich JK, Schock DM (2004) A model host-pathogen system for studying infectious disease dynamics in amphibians: tiger salamanders (Ambystoma tigrinum) and Ambystoma tigrinum virus. Herpetol J 14:195–200Google Scholar
  17. Colwell RR (1996) Global climate and infectious disease: the cholera paradigm. Science 274:2025–2031PubMedCrossRefGoogle Scholar
  18. Daily GC (1997) Nature’s services: societal dependence on natural ecosystems. Island Press, Washington, DCGoogle Scholar
  19. Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife: threats to biodiversity and human health. Science 287:443–449PubMedCrossRefGoogle Scholar
  20. Daszak P, Cunningham AA, Hyatt AD (2001) Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Trop 78:103–116PubMedCrossRefGoogle Scholar
  21. Daszak P, Scott DE, Kilpatrick AM, Faggoni C, Gibbons JW, Porter D (2005) Amphibian population declines at Savannah River site are linked to climate, not chytridiomycosis. Ecology 86:3232–3237CrossRefGoogle Scholar
  22. Desowitz RS (1997) Who gave pinta to the Santa Maria? Harcourt Brace & Company, New York, p 256Google Scholar
  23. Di Rosa I, Simoncelli F, Fagotti A, Pascolini R (2007) The proximate cause of frog declines? Nature 447:E4–E5PubMedCrossRefGoogle Scholar
  24. Dobson AP (2000) Raccoon rabies in space and time. Proc Natl Acad Sci USA 97:14014–14063Google Scholar
  25. Dobson AP, Carper ER (1993) Biodiversity. Lancet 342:1096–1099PubMedCrossRefGoogle Scholar
  26. Duffus ALJ, Pauil BD, Wozney K, Brunetti CR, Berrill M (2008) Frog virus 3-like infections in aquatic amphibian communities J. Wildl Dis 44:109–120Google Scholar
  27. Epstein PR (1999) Perspectives: medicine, climate and health. Science 285:347–348PubMedCrossRefGoogle Scholar
  28. Fauci AS (2001) Infectious diseases: considerations for the 21st century. Clin Infect Dis 32:675–685PubMedCrossRefGoogle Scholar
  29. Forson D, Storfer A (2006) Effects of atrazine and iridovirus infection on survival and life-history traits of the long-toed Salamander (Ambystoma macrodactylum). Environ Toxicol Chem 25:168–173PubMedCrossRefGoogle Scholar
  30. Gendron AD, Marcogliese DJ, Barbeau S, Christin MS, Brousseau P, Ruby S, Cyr D, Fournier M (2003) Exposure of leopard frogs to a pesticide mixture affects life history characteristics of the lungworm Rhabdias ranae. Oecologia 135:469–476PubMedGoogle Scholar
  31. Global Amphibian Assessment (GAA) (2004)
  32. Greer AL, Collins JP (2007) Sensitivity of a diagnostic test for amphibian Ranavirus varies with sampling protocol. J Wildl Dis 43:525–532PubMedGoogle Scholar
  33. Han BA, Bradley BW, Blaustein AR (2008) Ancient behaviors of larval amphibians in response to an emerging fungal pathogen, Batrachochytrium dendrobatidis. Behav Ecol Sociobiol. doi:10.1007/s00265-008-0655-8
  34. Hanselmann R, Rodrıguez I, Lampo M, Fajardo-Ramos L, Aguirre AA, Marm Kilpatrick A, Rodrıguez JP, Daszak P (2004) Presence of an emerging pathogen of amphibians in introduced bullfrogs Rana catesbeiana in Venezuela. Biol Conserv 120:115–119CrossRefGoogle Scholar
  35. Hayes T, Haston K, Tsui M, Hoang A, Haeffele C, Vonk A (2002a) Herbicides: feminization of male frogs in the wild. Nature 419:895–896PubMedCrossRefGoogle Scholar
  36. Hayes TB, Collins A, Lee M, Mendoza M, Noriega N, Stuart AA, Vonk A (2002b) Hermaphroditic, demasculinized frogs after exposure to the herbicide atrazine at low ecologically relevant doses. Proc Natl Acad Sci USA 99:5476–5480PubMedCrossRefGoogle Scholar
  37. Hayes T, Haston K, Tsui M, Hoang A, Haefelle C, Vonk A (2003) Atrazine-induced hermaphrodism at 0.1 ppb in American leopard frogs (Rana pipiens): laboratory and field evidence. Environ Health Perspect 111:568–575PubMedCrossRefGoogle Scholar
  38. Houghton JT et al (eds) (2001) Climate change 2001, the scientific basis. Third Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, CambridgeGoogle Scholar
  39. Johnson P, Sutherland D (2003) Amphibian deformities and Ribeiroia infection: an emerging helminthiasis. Trends Parasitol 19:332–335PubMedCrossRefGoogle Scholar
  40. Johnson PTJ, Lunde KB, Haight RW, Bowerman J, Blaustein AR (2001) Ribeiroia ondatrae (Trematoda: Digenea) infection induces severe limb malformations in western toads (Bufo boreas). Can J Zool 79:370–379Google Scholar
  41. Johnson PTJ, Lunde KB, Thurman EM, Ritchie EG, Wray SN, Sutherland DR et al (2002) Parasite (Ribeiroia ondatrae) infection linked to amphibian malformations in the western United States. Ecol Monogr 72:151–168CrossRefGoogle Scholar
  42. Kendall MD, Safieh B, Harwood J, Pomeroy PP (1992) Plasma thymulin concentrations, the thymus and organochlorine contaminant levels in seals infected with phocine distemper virus. Sci Total Environ 115:133–144PubMedCrossRefGoogle Scholar
  43. Kiesecker JM (2002) Synergism between trematode infection and pesticide exposure: a link to amphibian limb deformities in nature? Proc Natl Acad Sci USA 99:9900–9904PubMedCrossRefGoogle Scholar
  44. Kiesecker JM (2003) Invasive species: defining their role in amphibian declines. In: Semlitsch RD (ed) Amphibian conservation. Smithsonian Institution Press, Washington, DC, pp 113–126Google Scholar
  45. Kiesecker JM, Blaustein AR (1995) Synergism between UV-B radiation and a pathogen magnifies amphibian embryo mortality in nature. Proc Natl Acad Sci USA 92:11049–11052PubMedCrossRefGoogle Scholar
  46. Kiesecker JM, Blaustein AR (1997a) Egg laying behavior influences pathogenic infection of amphibian embryos. Conserv Biol 11:214–220CrossRefGoogle Scholar
  47. Kiesecker JM, Blaustein AR (1997b) Population differences in responses of red-legged frogs (Rana aurora) to introduced bullfrogs (Rana catesbeiana). Ecology 78:1752–1760Google Scholar
  48. Kiesecker JM, Blaustein AR (1998) Effects of introduced bullfrogs and smallmouth bass on the microhabitat use, growth and survival of native red-legged frogs. Conserv Biol 12:776–787CrossRefGoogle Scholar
  49. Kiesecker JM, Blaustein AR, Belden LK (2001a) Complex causes of amphibian population declines. Nature 410:681–684PubMedCrossRefGoogle Scholar
  50. Kiesecker JM, Blaustein AR, Miller CL (2001b) The transfer of a pathogen from fish to amphibians. Conserv Biol 15:1064–1070CrossRefGoogle Scholar
  51. Kiesecker JM, Miller CL, Blaustein AR (2001c) Potential mechanisms underlying the displacement of native red-legged frogs by introduced bullfrogs. Ecology 82:1964–1970CrossRefGoogle Scholar
  52. Kiesecker JM, Belden LK, Shea K, Rubbo MJ (2004) Amphibian declines and emerging disease. Am Sci 92:138–147Google Scholar
  53. Kriger KM (2009) Lack of evidence for the drought-linked chytridiomycosis hypothesis. J Wildl Dis 45:537–541PubMedGoogle Scholar
  54. Kutz SJ, Hoberg EP, Nagy J, Polley L, Elkin B (2005) “Emerging” parasitic infections in Arctic ungulates. Proc R Soc Lond B. doi:10.1098/rspb.2005.3285
  55. LaDeau LD, Kilpatrick MD, Marra PP (2007) West Nile virus emergence and large-scale declines of North American bird populations. Nature 447:710–713PubMedCrossRefGoogle Scholar
  56. Lafferty K, Holt RD (2003) How should environmental stress affect the population dynamics of disease? Ecol Lett 6:654–664CrossRefGoogle Scholar
  57. Lannoo MJ (2008) Malformed frogs: the collapse of aquatic ecosystems. University of California Press, Berkeley, CAGoogle Scholar
  58. Lardans V, Dissous C (1998) Snail control strategies for reduction of schistosomiasis transmission. Parasitol Today 14:413–417PubMedCrossRefGoogle Scholar
  59. Laurance WF, McDonald KR, Speare R (1996) Epidemic disease and the catastrophic decline of Australian rain forest frogs. Conserv Biol 10:1–9CrossRefGoogle Scholar
  60. Leibovitz L, Hwang J (1968) Duck plague on the American continent. Avian Dis 12:361–378PubMedCrossRefGoogle Scholar
  61. Lips K, Green DE, Pappendick R (2003) Chytridiomycosis in wild frogs from southern Costa Rica. J Herpetol 37:215–218CrossRefGoogle Scholar
  62. Lips KR, Diffendorfer JE, Mendelson JR, Sears MW (2008) Riding the wave: reconciling the roles of disease and climate change in amphibian declines. PLoS Biol 6:441–454CrossRefGoogle Scholar
  63. McCallum H (2005) Inconclusiveness of chytridiomycosis as the agent in widespread frog declines. Conserv Biol 19:1421–1430CrossRefGoogle Scholar
  64. Molyneux DH (1998) Vectorborne parasitic diseases—an overview of recent changes. Int J Parasitol 28:927–934PubMedCrossRefGoogle Scholar
  65. Mooney HA, Hobbs RJ (eds) (2000) Invasive species in a changing world. Island Press, Washington, DCGoogle Scholar
  66. Morehouse EA, James TY, Ganley ARD, Vilgalys R, Berger L, Murphy PJ, Longcore JE (2003) Multilocus sequence typing suggests that the chytrid pathogen of amphibians is a recently emerged clone. Mol Ecol 12:395–403PubMedCrossRefGoogle Scholar
  67. Nicholls N (1993) El Niño southern oscillation and vector-borne disease. Lancet 342:1284–1285PubMedCrossRefGoogle Scholar
  68. Ostfeld RS, Keesing F (2000a) Biodiversity and disease risk: the case of Lyme disease. Conserv Biol 14:722–728CrossRefGoogle Scholar
  69. Ostfeld RS, Keesing F (2000b) The function of biodiversity in the ecology of vector-borne zoonotic diseases. Can J Zool 78:2061–2078CrossRefGoogle Scholar
  70. Ouellet M, Bonin J, Rodrigue J, DesGranges J, Lair S (1997) Hindlimb deformities (ectromelia, ectrodactyly) in free living anurans from agricultural habitats. J Wildl Dis 33:95–104PubMedGoogle Scholar
  71. Ouellet M, Mikaelian I, Pauli BD, Rodrigue J, Green DM (2005) Historical evidence of widespread chytrid infection in North American amphibian populations. Conserv Biol 19:1431–1440CrossRefGoogle Scholar
  72. Patz JA, Epstein PR, Burke TA, Balbus JM (1996) Global climate change and emerging infectious diseases. JAMA 275:217–223PubMedCrossRefGoogle Scholar
  73. Pounds JA (2001) Climate and amphibian declines. Nature 410:639–640PubMedCrossRefGoogle Scholar
  74. Pounds JA, Crump ML (1994) Amphibian declines and climate disturbance: the case of the golden toad and the harlequin frog. Conserv Biol 8:72–85CrossRefGoogle Scholar
  75. Pounds JA, Fogden MPL, Campbell JH (1999) Biological response to climate change on a tropical mountain. Nature 398:611–615CrossRefGoogle Scholar
  76. Pounds JA, Bustamante MR, Coloma LA, Consuegra JA, Fogden MPL, Foster PN, La Marca E, Masters KL, Merino-Viteri A, Puschendorf R, Ron SR, Sanchez-Azofeifa GA, Still CJ, Young BE (2006) Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 439:161–167PubMedCrossRefGoogle Scholar
  77. Prusiner SB (1997) Prion diseases and the BSE crisis. Science 252:1515–1522CrossRefGoogle Scholar
  78. Puschendorf R, Bolanos F, Chaves G (2006) The amphibian chytrid fungus along an altitudinal transect before the first reported declines in Costa Rica. Biol Conserv 132:136–142CrossRefGoogle Scholar
  79. Rachowicz LJ, Hero JM, Alford RA, Taylor JW, Morgan JAT, Vredenburg VT, Collins JP, Briggs CJ (2005) The novel and endemic pathogen hypotheses: competing explanations for the origin of emerging infectious diseases of wildlife. Conserv Biol 19:1441–1448CrossRefGoogle Scholar
  80. Redmond KT, Koch RW (1991) Surface climate and stream flow variability in the western United States and their relationship to large-scale circulation indexes. Water Resour Res 27:2381–2399CrossRefGoogle Scholar
  81. Reeves WC, Hardy JL, Reisen WK, Milby MM (1994) The potential effect of global warming on mosquito-borne arboviruses. J Med Entomol 31:323–332PubMedGoogle Scholar
  82. Rohr JR, Raffel TR, Romansic JM, McCallum H, Hudson PJ (2008a) Evaluating the links between climate, disease spread, and amphibian declines. Proc Natl Acad Sci USA 105:17436–17441PubMedCrossRefGoogle Scholar
  83. Rohr JR, Schotthoefer AM, Raffel TR, Carrick HJ, Halstead N (2008b) Agrochemicals increase trematode infections in a declining amphibian species. Nature 455:1235–1239PubMedCrossRefGoogle Scholar
  84. Ron SR, Duellman WE, Coloma LA, Bustamante M (2003) Population decline of the Jambato toad Atelopus ignescens (Anura: Bufonidae) in the Andes of Ecuador. J Herpetol 37:116–126CrossRefGoogle Scholar
  85. Semlitsch RD (ed) (2003) Amphibian conservation. Smithsonian Press, Washington, DCGoogle Scholar
  86. Sessions SK, Ruth SB (1990) Explanation for naturally occurring supernumerary limbs in amphibians. J Exp Zool 254:38–47PubMedCrossRefGoogle Scholar
  87. Storfer A (2003) Amphibian declines: future directions. Divers Distrib 9:151–163CrossRefGoogle Scholar
  88. Storrs SI, Kiesecker JM (2004) Survivorship patterns of larval amphibians exposed to low concentrations of atrazine. Environ Health Perspect 112:1054–1057PubMedCrossRefGoogle Scholar
  89. Timmermann A, Oberhuber J, Bacher A, Esch M, Latif M, Roeckner E (1999) Increased El Niño frequency in a climate model forced by future greenhouse warming. Nature 398:694–697CrossRefGoogle Scholar
  90. Vitousek PM, Mooney HA, Lubchenco J, Melillo JM (1997) Human domination of Earth’s ecosystems. Science 277:494–499CrossRefGoogle Scholar
  91. Weinhold R (2004) Infectious disease: the human costs of our environmental errors. Environ Health Perspect 112:A32–A39PubMedCrossRefGoogle Scholar
  92. Whitfield SM, Bell KE, Philippi T, Sasa M, Bolan F, Chaves G, Savage JM, Donnelly MA (2007) Amphibian and reptile declines over 35 years at La Selva, Costa Rica. Proc Natl Acad Sci USA 104:8352–8356PubMedCrossRefGoogle Scholar
  93. Williams ES, Miller MW (2002) Chronic wasting disease in deer and elk in North America. Rev Sci Tech Off Int Epizoot 21:305–316Google Scholar
  94. Yan ND, Keller W, Scully NM, Lean DRS, Dillon PJ (1996) Increased UV-B penetration in a lake owing to drought-induced acidification. Nature 381:141–143CrossRefGoogle Scholar

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© The Ecological Society of Japan 2010

Authors and Affiliations

  1. 1.North America Conservation Region, The Nature ConservancyFort CollinsUSA

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