EcoHealth

, Volume 14, Issue 2, pp 296–302 | Cite as

Survey of Pathogenic Chytrid Fungi (Batrachochytrium dendrobatidis and B. salamandrivorans) in Salamanders from Three Mountain Ranges in Europe and the Americas

  • Joshua Curtis Parrott
  • Alexander Shepack
  • David Burkart
  • Brandon LaBumbard
  • Patrick Scimè
  • Ethan Baruch
  • Alessandro Catenazzi
Original Contribution

Abstract

Batrachochytrium salamandrivorans (Bsal) is a virulent fungal pathogen that infects salamanders. It is implicated in the recent collapse of several populations of fire salamanders in Europe. This pathogen seems much like that of its sister species, Batrachochytrium dendrobatidis (Bd), the agent responsible for anuran extinctions and extirpations worldwide, and is considered to be an emerging global threat to salamander communities. Bsal thrives at temperatures found in many mountainous regions rich in salamander species; because of this, we have screened specimens of salamanders representing 17 species inhabiting mountain ranges in three continents: The Smoky Mountains, the Swiss Alps, and the Peruvian Andes. We screened 509 salamanders, with 192 representing New World salamanders that were never tested for Bsal previously. Bsal was not detected, and Bd was mostly present at low prevalence except for one site in the Andes.

Keywords

Alps Amphibians Andes Appalachia Conservation Caudata Plethodontidae Salamandridae Wildlife disease 

References

  1. AmphibiaWeb (2016). Information on amphibian biology and conservation. www.amphibiaweb.org. Accessed 15 Jan 2016
  2. Blackburn M, Wayland J, Smith WH, McKenna JH, Harry M, Hamed MK, et al. (2015). First report of Ranavirus and Batrachochytrium dendrobatidis in green salamanders (Aneides aeneus) from Virginia, USA. Herpetological Review 46:357–361Google Scholar
  3. Blooi M, Martel A, Haesebrouck F, Vercammen F, Bonte D, Pasmans F (2015). Treatment of urodelans based on temperature dependent infection dynamics of Batrachochytrium salamandrivorans. Scientific Reports 5:8037CrossRefPubMedPubMedCentralGoogle Scholar
  4. Blooi M, Pasmans F, Longcore JE, Spitzen-van der Sluijs A, Vercammen F, Martel A (2016). Duplex real-time PCR for rapid simultaneous detection of Batrachochytrium dendrobatidis and Batrachochytrium salamandrivorans in amphibian samples. Journal of Clinical Microbiology 51:4173–4177CrossRefGoogle Scholar
  5. Brinkman LC, Ray JM, Mathis A, Greene BD (2016). Filling in the gaps: natural history and conservation of Bolitoglossine Salamanders in Central Panama. Copeia 104:140–148CrossRefGoogle Scholar
  6. Caruso NM, Lips KR (2013). Truly enigmatic declines in terrestrial salamander populations in Great Smoky Mountains National Park. Diversity and Distributions 19:38–48CrossRefGoogle Scholar
  7. Catenazzi A, Lehr E, Rodriguez LO, Vredenburg VT (2011). Batrachochytrium dendrobatidis and the collapse of anuran species richness and abundance in the upper Manu National Park, Southeastern Peru. Conservation Biology 25:382–391CrossRefPubMedGoogle Scholar
  8. Catenazzi A, Lehr E, Vredenburg VT (2014). Thermal physiology, disease, and amphibian declines on the eastern slopes of the Andes. Conservation Biology 28:509–517CrossRefPubMedGoogle Scholar
  9. Crawford AJ, Lips KR, 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 107:13777–13782CrossRefGoogle Scholar
  10. Daszak P, Cunningham AA, Hyatt AD (2003). Infectious disease and amphibian population declines. Diversity and Distributions 9:141–150CrossRefGoogle Scholar
  11. Digiacomo RF, Koepsell TD (1986). Sampling for detection of Infectious disease in animal populations. Journal of the American Veterinary Medical Association 189:22–23PubMedGoogle Scholar
  12. Fisher MC, Henk DA, Briggs CJ, Brownstein JS, Madoff LC, McCraw SL, et al. (2012). Emerging fungal threats to animal, plant and ecosystem health. Nature 484:186–194CrossRefPubMedGoogle Scholar
  13. Garner TWJ, Walker S, Bosch J, Hyatt AD, Cunningham AA, Fisher MC (2005). Chytrid fungus in Europe. Emerging Infectious Diseases 11:1639–1641CrossRefPubMedPubMedCentralGoogle Scholar
  14. Gerson H (2012). International trade in amphibians: a customs perspective. Alytes (Paris) 29:103–115Google Scholar
  15. Grant EHC, Muths EL, Katz RA, Canessa S, Adams MJ, Ballard JR, et al. (2015). Salamander chytrid fungus (Batrachochytrium salamandrivorans) in the United States—Developing research, monitoring, and management strategies. U.S. Geological Survey Report 2015-1233, RestonGoogle Scholar
  16. Gray MJ, Lewis JP, Nanjappa P, Klocke B, Pasmans F, Martel A, et al. (2015). Batrachochytrium salamandrivorans: The North American response and a call for action. Plos Pathogens 11(12):e1005251CrossRefPubMedPubMedCentralGoogle Scholar
  17. Hamed MK, Gray MJ, Miller DL (2013). First Report of Ranavirus in Plethodontid Salamanders from the Mount Rogers National Recreation Area, Virginia, USA. Herpetological Review 44:455–457Google Scholar
  18. James TY, Toledo LF, Rodder D, da Silva Leite D, Belasen AM, Betancourt-Roman CM, et al. (2015). Disentangling host, pathogen, and environmental determinants of a recently emerged wildlife disease: lessons from the first 15 years of amphibian chytridiomycosis research. Ecology and Evolution 5:4079–4097CrossRefPubMedPubMedCentralGoogle Scholar
  19. Killeen TJ, Douglas M, Consiglio T, Jorgensen PM, Mejia J (2007). Dry spots and wet spots in the Andean hotspot. Journal of Biogeography 34:1357–1373CrossRefGoogle Scholar
  20. Lotters S, Kielgast J, Sztatecsny M, Wagner N, Schulte U, Werner P, et al. (2012). Absence of infection with the amphibian chytrid fungus in the terrestrial alpine salamander, Salamandra atra. Salamandra 48:58–62Google Scholar
  21. Martel A, Blooi M, Adriaensen C, Van Rooij P, Beukema W, Fisher MC, et al. (2014). Recent introduction of a chytrid fungus endangers Western Palearctic salamanders. Science 346:630–631CrossRefPubMedGoogle Scholar
  22. Martel A, Spitzen-van der Sluijs A, Blooi M, Bert W, Ducatelle R, Fisher MC, et al. (2013). Batrachochytrium salamandrivorans sp. nov. causes lethal chytridiomycosis in amphibians. Proceedings of the National Academy of Sciences USA 110:15325–15329CrossRefGoogle Scholar
  23. Moffitt D, Williams LA, Hastings A, Pugh MW, Gangloff MM, Siefferman L (2015). Low prevelance of the amphibian pathogen Batrachochytrium Dendrobatidis in the Southern Appalachian Mountains. Herpetological Conservation and Biology 10:123–136Google Scholar
  24. Pavlin BI, Schloegel LM, Daszak P (2009). Risk of Importing zoonotic diseases through wildlife trade, United States. Emerging Infectious Diseases 15:1721–1726CrossRefPubMedPubMedCentralGoogle Scholar
  25. Richgels KLD, Russell RE, Adams MJ, White CL, Grant EHC (2016). Spatial variation in risk and consequence of Batrachochytrium salamandrivorans introduction in the USA. Royal Society Open Science 3:150616–150616CrossRefPubMedPubMedCentralGoogle Scholar
  26. Rovito SM, Parra-Olea G, Vasquez-Almazan CR, Papenfuss TJ, Wake DB (2009). Dramatic declines in neotropical salamander populations are an important part of the global amphibian crisis. Proceedings of the National Academy of Sciences USA 106:3231–3236CrossRefGoogle Scholar
  27. Sabino-Pinto J, Bletz M, Perl RGB, Schmeller DS, Mutschmann F, Wagner N, et al. (2015). First detection of the emerging fungal pathogen Batrachochytrium salamandrivorans in Germany. Amphibia-Reptilia 36:411–416CrossRefGoogle Scholar
  28. Schmidt BR (2016). Switzerland bans the importation of all salamander species because of the salamander chytrid. FrogLog 24:13Google Scholar
  29. Skerratt LF, Berger L, Speare R, Cashins S, McDonald KR, Phillott AD, et al. (2007). Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth 4:125–134CrossRefGoogle Scholar
  30. Sleeman JM (2013). Has the time come for big science in wildlife health? EcoHealth 10:335–338CrossRefPubMedGoogle Scholar
  31. Spitzen-van der Sluijs A, An M, Johan A, Emma KB, Wouter B, Molly CB, et al. (2016). Expanding distribution of lethal amphibian fungus Batrachochytrium salamandrivorans in Europe. Emerging Infectious Disease Journal 22(7):1286–1288CrossRefGoogle Scholar
  32. Spitzen-van der Sluijs A, Spikmans F, Bosman W, de Zeeuw M, van der Meij T, Goverse E, et al. (2013). Rapid enigmatic decline drives the fire salamander (Salamandra salamandra) to the edge of extinction in the Netherlands. Amphibia-Reptilia 34:233–239Google Scholar
  33. Sutton WB, Gray MJ, Hoverman JT, Secrist RG, Super PE, Hardman RH, et al. (2015). Trends in Ranavirus prevalence among plethodontid salamanders in the Great Smoky Mountains National Park. EcoHealth 12:320–329CrossRefPubMedGoogle Scholar
  34. Tobler U, Borgula A, and Schmidt BR (2012). Populations of a susceptible amphibian species can grow despite the presence of a pathogenic chytrid fungus. PLoS One 7:e34667CrossRefPubMedPubMedCentralGoogle Scholar
  35. Wake DB, and Vredenburg VT (2008). Are we in the midst of the sixth mass extinction? A view from the world of amphibians. Proceedings of the National Academy of Sciences USA 105 (Suppl 1):11466–11473CrossRefGoogle Scholar
  36. Warne RW, LaBumbard B, LaGrange S, Vredenburg VT, Catenazzi A (2016). Co-Infection by chytrid fungus and Ranaviruses in wild and harvested frogs in the Tropical Andes. PLoS One 11(1):e0145864CrossRefPubMedPubMedCentralGoogle Scholar
  37. Williams LA, Groves JD (2014). Prevalence of the amphibian pathogen Batrachochytrium Dendrobatidis in eastern hellbenders (Cryptobranchus A-Alleganiensis) in western North Carolina, USA. Herpetological Conservation and Biology 9:454–467Google Scholar
  38. Woodhams DC, Brandt H, Baumgartner S, Kielgast J, Kupfer E, Tobler U, et al. (2014). Interacting symbionts and immunity in the amphibian skin mucosome predict disease risk and probiotic effectiveness. PLoS One 9(4):e96375CrossRefPubMedPubMedCentralGoogle Scholar
  39. Yap TA, Koo MS, Ambrose RF, Wake DB, Vredenburg VT (2015). Averting a North American biodiversity crisis. Science 349:481–482CrossRefPubMedGoogle Scholar

Copyright information

© International Association for Ecology and Health 2016

Authors and Affiliations

  • Joshua Curtis Parrott
    • 1
  • Alexander Shepack
    • 1
  • David Burkart
    • 1
  • Brandon LaBumbard
    • 1
    • 2
  • Patrick Scimè
    • 3
  • Ethan Baruch
    • 4
  • Alessandro Catenazzi
    • 1
  1. 1.Zoology DepartmentSouthern Illinois University CarbondaleCarbondaleUSA
  2. 2.University of Massachusetts BostonBostonUSA
  3. 3.BedanoSwitzerland
  4. 4.School of Life SciencesArizona State UniversityTempeUSA

Personalised recommendations