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EcoHealth

, Volume 12, Issue 2, pp 320–329 | Cite as

Trends in Ranavirus Prevalence Among Plethodontid Salamanders in the Great Smoky Mountains National Park

  • William B. Sutton
  • Matthew J. Gray
  • Jason T. Hoverman
  • Richard G. Secrist
  • Paul E. Super
  • Rebecca H. Hardman
  • Jennifer L. Tucker
  • Debra L. Miller
Original Contribution

Abstract

Emerging pathogens are a potential contributor to global amphibian declines. Ranaviruses, which infect ectothermic vertebrates and are common in aquatic environments, have been implicated in die-offs of at least 72 amphibian species worldwide. Most studies on the subject have focused on pool-breeding amphibians, and infection trends in other amphibian species assemblages have been understudied. Our primary study objective was to evaluate hypotheses explaining ranavirus prevalence within a lungless salamander assemblage (Family Plethodontidae) in the Great Smoky Mountains National Park, USA. We sampled 566 total plethodontid salamanders representing 14 species at five sites over a 6-year period (2007–2012). We identified ranavirus-positive individuals in 11 of the 14 (78.6%) sampled species, with salamanders in the genus Desmognathus having greatest infection prevalence. Overall, we found the greatest support for site elevation and sampling year determining infection prevalence. We detected the greatest number of infections in 2007 with 82.5% of sampled individuals testing positive for ranavirus, which we attribute to record drought during this year. Infection prevalence remained relatively high in low-elevation sites in 2008 and 2009. Neither body condition nor aquatic dependence was a significant predictor of ranavirus prevalence. Overall, our results indicate that life history differences among species play a minor role determining ranavirus prevalence compared to the larger effects of site elevation and yearly fluctuations (likely due to environmental stressors) during sampling years.

Keywords

amphibians lotic pathogen surveillance 

Notes

Acknowledgments

We thank R. Brenes, M. Brand, L. Henderson, along with multiple student volunteers from the University of Tennessee Department of Forestry, Wildlife and Fisheries and Pellissippi State Community College for field sampling assistance; and M. Niemiller and K. Hamed for assistance with salamander identification. Funds for this research were provided by the U.S. National Park Service (GSMNP) and the University of Tennessee Institute of Agriculture. We thank the Barrett lab, H. Rothbone, D. Steen, S. Sterrett, and E. Ridell for comments on earlier versions of this manuscript.

References

  1. Acevedo-Whitehouse K, Duffus ALJ (2009) Effects of environmental change on wildlife health. Philisophical Transactions of the Royal Society B 364:3429‒3438.CrossRefGoogle Scholar
  2. Balseiro A, Dalton KP, del Cerro A, Marquez I, Cunningham AA, Parra F, et al. (2009) Pathology, isolation and molecular characterization of a ranavirus from the common midwife toad Alytes obstetricans on the Iberian Peninsula. Diseases of Aquatic Organisms 84:95–104.CrossRefPubMedGoogle Scholar
  3. Barrett, K, Guyer, C (2008) Differential responses of amphibians and reptiles in riparian and stream habitats to land use disturbances in western Georgia, USA. Biol. Conserv. 141:2290–2300.CrossRefGoogle Scholar
  4. Blaustein AR, Gervasi SS, Johnson PTJ, Hoverman JT, Belden LK, Bradley PW, et al. (2012) Ecophysiology meets conservation: understanding the role of disease in amphibian population declines. Philosophical Transactions of the Royal Society B 367:1688‒1707.CrossRefGoogle Scholar
  5. Brunner JL, Schock DM, Davdison EW, Collins JP (2004) Intraspecific reservoirs: complex life history and the persistence of a lethal ranavirus. Ecology 85:560–566.CrossRefGoogle Scholar
  6. Brunner JL, Barnett KE, Gosier CJ, McNulty SA, Rubbo MJ, Kolozsvary MB (2011) Ranavirus infection die-offs of vernal pool amphibians in New York, USA. Herpetological Review 42:76–79.Google Scholar
  7. Bryan LK, Baldwin CA, Gray MJ, Miller DL (2009) Efficacy of select disinfectants at inactivating Ranavirus. Diseases of Aquatic Organisms 84:89–94.CrossRefPubMedGoogle Scholar
  8. Byappanahalli M, Fowler M, Shively D, Whitman R (2003) Ubiquity and persistence of Escherichia coli within a midwestern stream. Applied Environmental Microbiology 69:4549‒4555.CrossRefGoogle Scholar
  9. Burnham KP, Anderson DR (2002) Model selection and multimodel inference. A practical information-theoretic approach, 2nd ed., New York: SpringerGoogle Scholar
  10. Caruso NM, Lips KR (2013) Truly enigmatic declines in terrestrial salamander populations in Great Smoky Mountains National Park. Diversity and Distributions 19:38–48.CrossRefGoogle Scholar
  11. Collins JP, Storfer A (2003) Global amphibian declines: sorting the hypotheses. Diversity and Distributions 9:89–98.CrossRefGoogle Scholar
  12. Corser JD (2001) Decline of disjunct green salamander (Aneides aeneus) populations in the southern Appalachians. Biological Conservation 97:119–126.CrossRefGoogle Scholar
  13. Crother BI (editor) (2012) Scientific and Standard English Names of Amphibians and Reptiles of North America North of Mexico, with Comments Regarding Confidence in our Understanding, 7th ed., SSAR Circular # 39Google Scholar
  14. Davic RD, Welsh HH, Jr (2004) On the ecological roles of salamanders. Annual Review of Ecology and Systematics 35:404–434.Google Scholar
  15. Davis AK, DeVore JL, Milanovich JR, Cecala K, Maerz JC, Yabsley MJ (2009) New findings from an old pathogen: intraerythrocytic bacteria (Family Anaplasmatacea) in red-backed salamanders (Plethodon cinereus). Ecohealth 6:219–228.CrossRefPubMedGoogle Scholar
  16. Feder ME (1983) Integrating the ecology and physiology of plethodontid salamanders. Herpetologica 39:291‒310.Google Scholar
  17. Fox SF, Greer AL, Torres-Cervantes R, Collins JP (2006) First case of ranavirus-associated morbidity and mortality in natural populations of the South American frog Atelognathus patagoncius. Diseases of Aquatic Organisms 72:87–92.CrossRefPubMedGoogle Scholar
  18. Geng Y, Wang KY, Zhou ZY, Li CW, Wang J, He M, et al. (2011) First report of a Ranavirus associated with morbidity and mortality in farmed Chinese giant salamanders (Andrias davidianus). Journal of Comparative Pathology 145:95–102.CrossRefPubMedGoogle Scholar
  19. Gray MJ, Miller DL, Hoverman JT (2009a) Ecology and pathology of amphibian ranaviruses. Diseases of Aquatic Organisms 87:243–266.CrossRefPubMedGoogle Scholar
  20. Gray MJ, Miller DL, Hoverman JT (2009b) First report of Ranavirus infecting lungless salamanders. Herpetological Review 40:316–319.Google Scholar
  21. Gray MJ, Miller DL, Hoverman JT (2012) Reliability of non-lethal surveillance methods for detecting ranavirus infection. Diseases of Aquatic Organisms 99:1–6.CrossRefPubMedGoogle Scholar
  22. Gray MJ, Miller DL (2013) The rise of ranavirus: an emerging pathogen threatens ectothermic vertebrates. Wildlife Professional 7:51-55Google Scholar
  23. Greer AL, Briggs CJ, Collins JP (2008) Testing a key assumption of host-pathogen theory: density and disease transmission. Oikos 117:1667–1673.CrossRefGoogle Scholar
  24. Haislip NA, Gray MJ, Hoverman JT, Miller DL (2011) Development and disease: how susceptibility to an emerging pathogen changes through anuran development. PLoS ONE 6:1–6.CrossRefGoogle Scholar
  25. Hoverman JT, Gray MJ, Miller DL (2010) Anuran susceptibilities to ranaviruses: role of species identity, exposure route, and a novel virus isolate. Diseases of Aquatic Organisms 89:97–107.CrossRefPubMedGoogle Scholar
  26. Hoverman JT, Gray MJ, Haislip NA, Miller DL (2011) Phylogeny, life history, and ecology contribute to differences in anuran susceptibility to ranaviruses. Ecohealth 8:301–319.CrossRefPubMedGoogle Scholar
  27. Hoverman JT, Gray MJ, Miller DL, Haislip NA (2012) Widespread occurrence of ranavirus in pond-breeding amphibian populations. Ecohealth 9:36‒48.CrossRefPubMedGoogle Scholar
  28. Kiesecker JM, Blaustein AR, Belden LK (2001) Complex causes of amphibian populations declines. Nature 410:681–684.CrossRefPubMedGoogle Scholar
  29. Kroschel WA, Sutton WB, McClure CJW, Pauley TK (2014) Decline of the Cheat Mountain salamander over a 32-year period and the potential influence of competition from a sympatric species. Journal of Herpetology 48:415–422.CrossRefGoogle Scholar
  30. Kundzewicz ZW, Mata LJ, Arnell NW, Döll P, Jimenez B, Miller K, et al. (2008) The implications of projected climate change for freshwater resources and their management. Hydrological Sciences Journal 53:3–10.CrossRefGoogle Scholar
  31. Langdon JS (1989) Experimental transmission and pathogenicity of epizootic hematopoietic necrosis virus (EHNV) in redfin perch, Perca fluviatilis L. and 11 other teleosts. Journal of Fish Diseases 12:295–310.CrossRefGoogle Scholar
  32. Lips KR, Brem F, Brenes R, Reeve JD, Alford RA, Voyles J, et al. (2006) Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proceedings of the National Academy of Sciences 103:3165–3170.CrossRefGoogle Scholar
  33. Martel A, Spitzen-van der Sluijs A, Blooi M., Bert W, Ducatelle R, Fisher MC, et al. (2013) Batrachochytrium salamandrivorans sp. nov. causes lethal chytridomycosis in amphibians. Proceedings of the National Academy of Sciences of the USA 110:15325–15329.PubMedCentralCrossRefPubMedGoogle Scholar
  34. Martel A, Blooi M, Adriaensen C, Rooij Van P, Beukema W, Fisher MC, et al. (2014) Recent introduction of a chytrid fungus endangers Western Palearctic salamanders. Science 31:630–631.CrossRefGoogle Scholar
  35. Mendelson JR, Lips KR, Gagliardo RW, Rabb GB, Collins JP, Diffendorfer JE, et al. (2006) Confronting amphibian declines and extinctions. Science 313:48.CrossRefPubMedGoogle Scholar
  36. Miller D, Gray M, Storfer A (2011) Ecopathology of ranaviruses infecting amphibians. Viruses 2011:2351–2373.CrossRefGoogle Scholar
  37. Nazir J, Spengler M, Marschang RE (2012) Environmental persistence of amphibian and reptilian ranaviruses. Diseases of Aquatic Organisms 98:177–184.CrossRefPubMedGoogle Scholar
  38. Petranka JW (1998) Salamanders of the United States and Canada, Washington, DC and London, UK: Smithsonian Institution Press.Google Scholar
  39. Petranka JW, Murray SS (2001) Effectiveness of removal sampling for determining salamander density and biomass: a case study in an Appalachian streamside community. Journal of Herpetology 35:36–44.CrossRefGoogle Scholar
  40. Petranka JW, Murray SS, Kennedy CA (2003) Responses of amphibians to restoration of a southern Appalachian wetland: perturbations confound post-restoration assessment. Wetlands 23:278–290.CrossRefGoogle Scholar
  41. Petranka JW, Harp EM, Holbrook CT, Hamel JA (2007) Long-term persistence of amphibian populations in a restored wetland complex. Biological Conservation 138:371–380.CrossRefGoogle Scholar
  42. Picco AM, Brunner JL, Collins JP (2007) Susceptibility of the endangered California tiger salamander, Ambystoma californiense, to ranavirus infection. Journal of Wildlife Diseases 43:286–290.CrossRefPubMedGoogle Scholar
  43. R Core Team (2013) A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
  44. Rothermel BB, Travis ER, Miller DL, Hill RL, McGuire JL, Yabsley MJ (2013) High occupancy of stream salamanders despite high ranavirus prevalence in a southern Appalachians watershed. EcoHealth DOI:  10.1007/s10393-013-0843-5.PubMedGoogle Scholar
  45. Rovito SM, Parra-Olea G, Vásquez-Almazán 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 of the USA 106:3231–3236.PubMedCentralCrossRefPubMedGoogle Scholar
  46. Schulte-Hostedde A, Zinner B, Millar JS, Hickling GJ (2005) Restitution of mass-size residuals: validating body condition indices. Ecology 86:155–163.CrossRefGoogle Scholar
  47. Sousa MJ, Gray MJ, Colclough P, Miller DL (2012) Prevalence of infection by Batrachochytrium dendrobatidis and ranavirus in eastern hellbenders (Cryptobranchus alleganiensis alleganiensis) in eastern Tennessee. Journal of Wildlife Diseases 48:560–566.CrossRefGoogle Scholar
  48. St-Amour V, Garner TWJ, Shulte-Hostedde AI, Lesbarrères D (2010) Effects of two amphibian pathogens on the developmental stability of green frogs. Conservation Biology 24:788–794.CrossRefPubMedGoogle Scholar
  49. Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues ASL, Fischman DL, et al. (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306:1783–1786.CrossRefPubMedGoogle Scholar
  50. Teacher AGF, Cunningham AA, Garner TWJ (2010) Assessing the long-term impact of Ranavirus infection in wild common frog populations. Animal Conservation 13:514–522.CrossRefGoogle Scholar
  51. Tilley SG, Huheey JE (2001) Reptiles and Amphibians of the Smokies, Gatlinburg, TN: Great Smoky Mountains Natural History Association.Google Scholar
  52. Une Y, Sakuma A, Matsueda H, Nakai K, Murakam M (2009) Ranavirus outbreak in North American bullfrogs (Rana catesbeiana), Japan, 2008. Emerging Infectious Diseases 15:1146–1147.PubMedCentralCrossRefPubMedGoogle Scholar
  53. Wake DB, Vredenburg VT (2009) Are we in the midst of the sixth mass extinction? A view from the world of amphibians. Proceedings of the National Academy of Sciences 105:11466–11473.CrossRefGoogle Scholar
  54. Wells KD (2007) The Ecology and Behavior of Amphibians, Chicago, IL: The University of Chicago Press.CrossRefGoogle Scholar
  55. Welsh HH, Jr, Droege S (2001) A case for using plethodontid salamanders for monitoring biodiversity and ecosystem integrity of North American forests. Conservation Biology 15:558–569.CrossRefGoogle Scholar
  56. Whiles MR, Lips KR, Pringle CM, Kilham SS, Bixby RJ, Brenes R, et al. (2006) The effects of amphibian population declines on the structure and function of Neotropical stream ecosystems. Frontiers in Ecology and the Environment 4:27–34.CrossRefGoogle Scholar
  57. Whitfield SM, Geerdes E, Chacon I, Ballestero Rodriguez E, Jimenez RR, Donnelly MA, Kerby JL (2013) Infection and co-infection by the amphibian chytrid fungus and ranavirus in wild Costa Rican frogs. Diseases of Aquatic Organisms 104:173–178.CrossRefPubMedGoogle Scholar
  58. Whitman RL, Gochee AV, Dustman WA, Kennedy KJ (1995) Use of coliform bacteria in assessing human sewage contamination. Natural Areas Journal 15:227‒233.Google Scholar
  59. Wyman RL (1998) Experimental assessment of salamanders as predators of detrital food webs: effects on invertebrates, decomposition and the carbon cycle. Biodiversity and Conservation 7:641–650.CrossRefGoogle Scholar

Copyright information

© International Association for Ecology and Health 2014

Authors and Affiliations

  • William B. Sutton
    • 1
    • 2
  • Matthew J. Gray
    • 1
  • Jason T. Hoverman
    • 3
  • Richard G. Secrist
    • 4
  • Paul E. Super
    • 5
  • Rebecca H. Hardman
    • 1
  • Jennifer L. Tucker
    • 1
  • Debra L. Miller
    • 1
  1. 1.Center for Wildlife Health, Department of Forestry, Wildlife and FisheriesUniversity of TennesseeKnoxvilleUSA
  2. 2.Department of Agricultural and Environmental SciencesTennessee State UniversityNashvilleUSA
  3. 3.Department of Forestry and Natural ResourcesPurdue UniversityWest LafayetteUSA
  4. 4.Great Smoky Mountains Institute at TremontTownsendUSA
  5. 5.Appalachian Highlands Science Learning CenterGreat Smoky Mountains National ParkLake JunaluskaUSA

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