Advertisement

Amphibia: Global Amphibian Declines Caused by an Emerging Infectious Disease and Inadequate Immune Responses

  • Jonathan Edward Kolby
Chapter

Abstract

There are approximately 7000 described species of amphibians in the world, and many are currently in decline. In today’s rapidly developing world, biodiversity loss represents a growing threat to global health, and highly virulent wildlife diseases are emerging with greater frequency. The amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd) has recently become the first known pathogen to cause wildlife extinction on multiple continents, and its uncontrolled spread now threatens the existence of hundreds, if not thousands, of amphibian species. Most amphibians show little resistance to chytridiomycosis, the disease caused by Bd infection, and many fail to develop an adaptive immune response upon reexposure. The greatest contemporary pathway of continued Bd dispersal is the international wildlife trade. The lack of required disease screening and regulation in most countries has allowed for the rapid global emergence of this pathogen, and naïve amphibian populations remain highly vulnerable to decline from Bd introduction. Improved biosecurity policies are urgently needed to prevent immeasurable biodiversity loss and the continued emergence of novel wildlife pathogens.

Keywords

Amphibians Disease Chytrid, wildlife trade Extinction Frog Chytridiomycosis Emerging infectious disease Batrachochytrium dendrobatidis Animals Fungus 

References

  1. Altig R (2007) Comments on the descriptions and evaluations of tadpole mouthpart anomalies. Herpetol Conserv Biol 2:1–4Google Scholar
  2. Baitchman EJ, Pessier AP (2013) Pathogenesis, diagnosis, and treatment of amphibian chytridiomycosis. Vet Clin North Am Exot Anim Pract 16:669e685CrossRefGoogle Scholar
  3. 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 U S A 95:9031–9036CrossRefGoogle Scholar
  4. Berger L, Hyatt A, Speare R, Longcore JE (2005) Lifecycle stages of Batrachochytrium dendrobatidis, the amphibian chytrid. Dis Aquat Org 68:51e63Google Scholar
  5. Berger L, Roberts A, Voyles J, Longcore J, Murray K, Skerratt L (2016) History and recent progress on chytridiomycosis in amphibians. Fungal Ecol 19:89–99CrossRefGoogle Scholar
  6. Brannelly LA, Richards-Zawacki CL, Pessier AP (2012) Clinical trials with itraconazole as a treatment for chytrid fungal infections in amphibians. Dis Aquat Org 101:95–104CrossRefGoogle Scholar
  7. Brucker RM, Harris RN, Schwantes CR, Gallaher TN, Flaherty DC, Lam BA, Minbiole KPC (2008) Amphibian chemical defense: antifungal metabolites of the microsymbiont Janthinobacterium lividum on the salamander Plethodon cinereus. J Chem Ecol 34:1422–1429CrossRefGoogle Scholar
  8. Carey C, Bruzgul JE, Livo LJ, Walling ML, Kuehl KA, Dixon BF, Pessier AP, Alford RA, Rodgers KB (2006) Experimental exposures of boreal toads (Bufo boreas) to a pathogenic chytrid fungus (Batrachochytrium dendrobatidis). EcoHealth 3:5e21CrossRefGoogle Scholar
  9. Cashins S, Grogan L, McFadden M, Hunter D, Harlow P, Berger L, Skerratt L (2013) Prior infection does not improve survival against the amphibian disease chytridiomycosis. PLoS One 8:e56747CrossRefGoogle Scholar
  10. Daszak P, Berger L, Cunningham AA, Longcore JE, Brown CC, Porter D (2004) Experimental evidence that the bullfrog (Rana catesbeiana) is a potential carrier of chytridiomycosis, an emerging fungal disease of amphibians. Herpetol J 14:201–207Google Scholar
  11. Ellison AR, Savage AE, DiRenzo GV, Langhammer P, Lips KR, Zamudio KR (2014) Fighting a losing battle: vigorous immune response countered by pathogen suppression of host defenses in the chytridiomycosis susceptible frog Atelopus zeteki. G3 Genes Genomes Genet 4:1275–1289Google Scholar
  12. Farrer RA, Weinert LA, Bielby J, Garner TW, Balloux F, Clare F, Bosch J, Cunningham AA, Weldon C, du Preez LH, Anderson L, Pond SL, Shahar-Golan R, Henk DA, Fisher MC (2011) Multiple emergences of genetically diverse amphibian-infecting chytrids include a globalized hypervirulent recombinant lineage. Proc Natl Acad Sci U S A 108:18732–18736CrossRefGoogle Scholar
  13. Fites JS, Ramsey JP, Holden WM, Collier SP, Sutherland DM, Reinert LK, Gayek AS, Dermody TS, Aune TM, Oswald-Richter K, Rollins-Smith LA (2013) The invasive chytrid fungus of amphibians paralyzes lymphocyte responses. Science 342:366–369CrossRefGoogle Scholar
  14. Fites JS, Reinert LK, Chappell TM, Rollins-Smith LA (2014) Inhibition of local immune responses by the frog-killing fungus Batrachochytrium dendrobatidis. Infect Immun 82:4698–4706CrossRefGoogle Scholar
  15. Garmyn A, Van Rooij P, Pasmans F, Hellebuyck T, Van Den Broeck W, Haesebrouck F, Martel A (2012) Waterfowl: potential environmental reservoirs of the chytrid fungus Batrachochytrium dendrobatidis. PLoS One 7:e35038CrossRefGoogle Scholar
  16. Greenspan SE, Longcore JE, Calhoun AJK (2012) Host invasion by Batrachochytrium dendrobatidis: fungal and epidermal ultrastructure in model anurans. Dis Aquat Org 100:201–210CrossRefGoogle Scholar
  17. Holden WM, Ebert AR, Canning PF, Rollins-Smith LA (2014) Evaluation of amphotericin B and chloramphenicol as alternative drugs for treatment of chytridiomycosis and their impacts on innate skin defenses. Appl Environ Microbiol 80:4034–4041CrossRefGoogle Scholar
  18. Johnson ML, Berger L, Phillips L, Speare R (2003) Fungicidal effects of chemical disinfectants, UV light, desiccation and heat on the amphibian chytrid, Batrachochytrium dendrobatidis. Dis Aquat Org 57:255e260CrossRefGoogle Scholar
  19. Kolby JE (2014) Presence of the amphibian chytrid fungus Batrachochytrium dendrobatidis in native amphibians exported from Madagascar. PLoS One 9:e89660. https://doi.org/10.1371/journal.pone.0089660 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Kolby JE, Daszak P (2016) The emerging amphibian fungal disease, chytridiomycosis: a key example of the global phenomenon of wildlife emerging infectious diseases. Microbiol Spectr 4(3):EI10-0004-2015Google Scholar
  21. Kolby JE, Smith KM, Berger L, Karesh WB, Preston A, Pessier AP, Skerratt LF (2014) First evidence of amphibian chytrid fungus (Batrachochytrium dendrobatidis) and ranavirus in Hong Kong amphibian trade. PLoS One 9:e90750CrossRefGoogle Scholar
  22. Kolby JE, Ramirez SD, Berger L, Richards-Hrdlicka KL, Jocque M, Skerratt LF (2015a) Terrestrial dispersal and potential environmental transmission of the amphibian chytrid fungus (Batrachochytrium dendrobatidis). PLoS One 10:e0125386CrossRefGoogle Scholar
  23. Kolby JE, Ramirez SD, Berger L, Griffin DW, Jocque M, Skerratt LF (2015b) Presence of amphibian chytrid fungus (Batrachochytrium dendrobatidis) in rainwater suggests aerial dispersal is possible. Aerobiologia 31:411–419CrossRefGoogle Scholar
  24. Lamirande EW, Nichols DK (2002) Effects of host age on susceptibility to cutaneous chytridiomycosis in blue-and-yellow poison dart frogs (Dendrobates tinctorius). In: McKinnell RG and Carlson DL (eds) Proceeding of the sixth international symposium on the pathology of reptiles and amphibians. Saint PaulGoogle Scholar
  25. Laurance WF, McDonald KR, Speare R (1996) Epidemic disease and the catastrophic decline of Australian rainforest frogs. Conserv Biol 10:406–413CrossRefGoogle Scholar
  26. Longcore JE, Pessier AP, Nichols DK (1999) Batrachochytrium dendrobatidis gen et sp nov, a chytrid pathogenic to amphibians. Mycologia 91:219–227CrossRefGoogle Scholar
  27. Marantelli G, Berger L, Speare R, Keegan L (2004) Distribution of the amphibian chytrid Batrachochytrium dendrobatidis and keratin during tadpole development. Pac Conserv Biol 10:173–179CrossRefGoogle Scholar
  28. Martel A, Van Rooij P, Vercauteren G, Baert K, Van Waeyenberghe L, Debacker P, Garner TW, Woeltjes T, Ducatelle R, Haesebrouck F, Pasmans F (2011) Developing a safe antifungal treatment protocol to eliminate Batrachochytrium dendrobatidis from amphibians. Med Mycol 49:143–149CrossRefGoogle Scholar
  29. McMahon TA, Sears BF, Venesky MD, Bessler SM, Brown JM, Deutsch K et al (2014) Amphibians acquire resistance to live and dead fungus overcoming fungal immunosuppression. Nature 511:224e227CrossRefGoogle Scholar
  30. Olson DH, Aanensen DM, Ronnenberg KL, Powell CI, Walker SF, Bielby J, TWJ G, Weaver G, Fisher MC, Bd Mapping Group (2013) Mapping the global emergence of Batrachochytrium dendrobatidis, the amphibian chytrid fungus. PLoS One 8:e56802CrossRefGoogle Scholar
  31. Poorten TM, Stice-Kishiyama CJB, Rosenblum EB (2016) Mountain yellow-legged frogs (Rana muscosa) did not produce detectable antibodies in immunization experiments with Batrachochytrium dendrobatidis. J Wildl Dis 52:154–158CrossRefGoogle Scholar
  32. Rachowicz LJ, Vredenburg VT (2004) Transmission of Batrachochytrium dendrobatidis within and between amphibian life stages. Dis Aquat Org 61:75–83CrossRefGoogle Scholar
  33. Rollins-Smith LA, Ramsey JP, Reinert LK, Woodhams DC, Livo LJ, Carey C (2009) Immune defenses of Xenopus laevis against Batrachochytrium dendrobatidis. Front Biosci 1:68–91CrossRefGoogle Scholar
  34. Rollins-Smith L, Ramsey J, Pask J, Reinert L, Woodhams D (2011) Amphibian immune defenses against chytridiomycosis: impacts of changing environments. Integr Comp Biol 51:552–562CrossRefGoogle Scholar
  35. Rollins-Smith LA, Fites JS, Reinert LK, Shiakolas AR, Umile TP, Minbiole KP (2015) Immunomodulatory metabolites released by the frog-killing fungus Batrachochytrium dendrobatidis. Infect Immun 83:4565–4570CrossRefGoogle Scholar
  36. Rosenblum EB, James TY, Zamudio KR, Poorten TJ, Ilut D, Rodriguez D, Eastman JM, Richards-Hrdlicka K, Joneson S, Jenkinson TS, Longcore JE, Parra Olea G, Toledo LF, Arellano ML, Medina EM, Restrepo S, Flechas SV, Berger L, Briggs CJ, Stajich JE (2013) Complex history of the amphibian-killing chytrid fungus revealed with genome resequencing data. Proc Natl Acad Sci U S A 110:9385–9390CrossRefGoogle Scholar
  37. Schloegel LM, Picco A, Kilpatrick AM, Hyatt A, Daszak P (2009) Magnitude of the US trade in amphibians and presence of Batrachochytrium dendrobatidis and ranavirus infection I imported North American bullfrogs (Rana catesbeiana). Biol Conserv 142:1420–1426CrossRefGoogle Scholar
  38. Schloegel LM, Daszak P, Cunningham AA, Speare R, Hill B (2010) Two amphibian diseases, chytridiomycosis and ranaviral disease, are now globally notifiable to the World Organization for Animal Health (OIE): an assessment. Dis Aquat Org 92:101–108CrossRefGoogle Scholar
  39. Schloegel LM, Toledo LF, Longcore JE, Greenspan SE, Vieira CA, Lee M, Zhao S, Wangen C, Ferreira CM, Hipolito M, Davies AJ, Cuomo CA, Daszak P, James TY (2012) Novel, panzootic and hybrid genotypes of amphibian chytridiomycosis associated with the bullfrog trade. Mol Ecol 21:5162–5177CrossRefGoogle Scholar
  40. Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues AS, Fischman DL, Waller RW (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306:1783–1786CrossRefGoogle Scholar
  41. Voyles J, Young S, Berger L, Campbell C, Voyles WF, Dinudom A, Cook D, Webb R, Alford RA, Skerratt LF, Speare R (2009) Pathogenesis of chytridiomycosis, a cause of catastrophic amphibian declines. Science 326:582–585CrossRefGoogle Scholar
  42. Vredenburg VT, Briggs CJ, Harris RN (2011) Host pathogen dynamics of amphibian chytridiomycosis: the role of the skin microbiome in health and disease. In: Olson L, Choffnes E, Relman D, Pray L (eds) Fungal diseases: an emerging threat to human, animal, and plant health. National Academy Press, Washington D.C., pp 342–355Google Scholar
  43. Wake DB, Vredenburg VT (2008) Are we in the midst of the sixth mass extinction? A view from the world of amphibians. Proc Natl Acad Sci 105:11466–11473CrossRefGoogle Scholar
  44. Woodhams DC, Bell SC, Bigler L, Caprioli RM, Chaurand P, Lam BA, Reinert LK, Stalder U, Vazquez VM, Schliep K, Hertz A, Rollins-Smith LA (2016) Life history linked to immune investment in developing amphibians. Conserv Physiol 4:1–15CrossRefGoogle Scholar
  45. Woodhams DC, Bosch J, Briggs CJ, Cashins S, Davis LR, Lauer A, et al (2011) Mitigating amphibian disease: strategies to maintain wild populations and control chytridiomycosis. Front Zool 8:8Google Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.One Health Research Group, College of Public Health, Medical, and Veterinary Sciences, James Cook UniversityTownsvilleAustralia
  2. 2.Honduras Amphibian Rescue and Conservation CenterTelaHonduras
  3. 3.The Conservation AgencyJamestownUSA
  4. 4.National Geographic SocietyWashingtonUSA

Personalised recommendations