Abstract
The interactive effects of environmental stressors and emerging infectious disease pose potential threats to stream salamander communities and their headwater stream ecosystems. To begin assessing these threats, we conducted occupancy surveys and pathogen screening of stream salamanders (Family Plethodontidae) in a protected southern Appalachians watershed in Georgia and North Carolina, USA. Of the 101 salamanders screened for both chytrid fungus (Batrachochytrium dendrobatidis) and Ranavirus, only two exhibited low-level chytrid infections. Prevalence of Ranavirus was much higher (30.4% among five species of Desmognathus). Despite the ubiquity of ranaviral infections, we found high probabilities of site occupancy (≥0.60) for all stream salamander species.
References
Annis SL, Dastoor FP, Ziel H, Daszak P, Longcore JE (2004) A DNA-based assay identifies Batrachochytrium dendrobatidis in amphibians. Journal of Wildlife Diseases 40:420–428
Bakkegard KA, Pessier AP (2010) Batrachochytrium dendrobatidis in adult Notophthalmus viridescens in north-central Alabama, USA. Herpetological Review 41:45–47
Becker MH, Harris RN (2010) Cutaneous bacteria of the redback salamander prevent morbidity associated with a lethal disease. PLoS ONE 5:e10957
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 rainforests of Australia and Central America. Proceedings of the National Academy of Sciences 95:9031–9036
Boyle DG, Boyle DB, Olsen V, Morgan JAT, Hyatt AD (2004) Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Diseases of Aquatic Organisms 60:141–148
Chinnadurai SK, Cooper D, Dombrowski DS, Poore MF, Levy MG (2009) Experimental infection of native North Carolina salamanders with Batrachochytrium dendrobatidis. Journal of Wildlife Diseases 45:631–636
Conor Keitzer S, Goforth R, Pessier AP, Johnson AJ (2011) Survey for the pathogenic chytrid fungus Batrachochytrium dendrobatidis in southwestern North Carolina salamander populations. Journal of Wildlife Diseases 47:455–458
Daszak P, Berger L, Cunningham AA, Hyatt AD, Green DE, Speare R (1999) Emerging infectious diseases and amphibian population declines. Emerging Infectious Diseases 5:735–748
Daszak P, Streiby A, 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. Herpetological Journal 14:201–207
Davidson SRA, Chambers DL (2011) Occurrence of Batrachochytrium dendrobatidis in amphibians of Wise County, Virginia, USA. Herpetological Review 42:214–215
Dodd CK Jr (2004) The Amphibians of Great Smoky Mountains National Park, Knoxville: University of Tennessee Press
Donovan TM, Hines J (2007) Exercises in occupancy modeling and estimation. http://www.uvm.edu/envnr/vtcfwru/spreadsheets/occupancy.htm. Accessed May 10, 2011
Garner TWJ, Perkins MW, Govindarajulu P, Seglie D, Walker S, Cunningham AA, Fisher MC (2006) The emerging amphibian pathogen Batrachochytrium dendrobatidis globally infects introduced populations of the North American bullfrog, Rana catesbeiana. Biology Letters 2:455–459
Grant EHC, Bailey LL, Ware JL, Duncan KL (2008) Prevalence of the amphibian pathogen Batrachochytrium dendrobatidis in stream and wetland amphibians in Maryland, USA. Applied Herpetology 5:233–241
Gratwicke B, Evans M, Grant EHC, Greathouse J, McShea WJ, Rotzel N, Fleischer RC (2011) Low prevalence of Batrachochytrium dendrobatidis detected in Appalachian salamanders from Warren County, Virginia, USA. Herpetological Review 42:217–219
Gray MJ, Miller DL, Hoverman JT (2009a) First report of Ranavirus infecting lungless salamanders. Herpetological Review 40:316–319
Gray MJ, Miller DL, Hoverman JT (2009b) Ecology and pathology of amphibian ranaviruses. Diseases of Aquatic Organisms 87:243–266
Gray MJ, Miller DL, Hoverman JT (2012) Reliability of non-lethal surveillance methods for detecting ranavirus infection. Diseases of Aquatic Organisms 99:1-6
Green DE, Converse KA, Schrader AK (2002) Epizootiology of sixty-four amphibian morbidity and mortality events in the USA, 1996-2001. Annals of the New York Academy of Sciences 969:323–339
Hossack BR, Adams MJ, Grant EHC, Pearl CA, Bettaso JB, Barichivich WJ, Lowe WH, True K, Ware JL, Corn PS (2010) Low prevalence of chytrid fungus (Batrachochytrium dendrobatidis) in amphibians of U.S. headwater streams. Journal of Herpetology 44:253–260
Hoverman JT, Gray MJ, Haislip NA, Miller DL (2011) Phylogeny, life history, and ecology contribute to differences in amphibian susceptibility to ranaviruses. EcoHealth 8:301–319
Hoverman JT, Gray MJ, Miller DL, Haislip NA (2012) Widespread occurrence of ranavirus in pond-breeding amphibian populations. EcoHealth 9:36–48
Kiemnec-Tyburczy KM, Eddy SL, Chouinard AJ, Houck LD (2012) Low prevalence of Batrachochytrium dendrobatidis in two plethodontid salamanders from North Carolina, USA. Herpetological Review 43:85–87
Lips KR, Reeve JD, Witters LR (2003) Ecological traits predicting amphibian population declines in Central America. Conservation Biology 17:1078–1088
Longcore JE, Pessier AP, Nichols DK (1999) Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia 91:219–227
Longcore JR, Longcore JE, Pessier AP, Halteman WA (2007) Chytridiomycosis widespread in anurans of northeastern United States. Journal of Wildlife Management 71:435–444
Lowe WH (2012) Climate change is linked to long-term decline in a stream salamander. Biological Conservation 145:48–53
MacKenzie DI, Nichols JD, Lachman GB, Droege S, Royle JA, Langtimm CA (2002) Estimating site occupancy rates when detection probabilities are less than one. Ecology 83:2248–2255
MacKenzie DI, Nichols JD, Royle JA, Pollock K, Bailey LL, Hines JE (2006) Occupancy Estimation and Modeling: Inferring Patterns and Dynamics of Species Occurrence, Burlington: Academic Press
Mao J, Tham TN, Gentry GA, Aubertin A, Chinchar VG (1996) Cloning, sequence analysis, and expression of the major capsid protein of the iridovirus frog virus 3. Virology 216:431–436
Mao J, Hedrick RP, Chinchar VG (1997) Molecular characterization, sequence analysis, and taxonomic position of newly isolated fish iridoviruses. Virology 229:212–220
Milanovich JR, Peterman WE, Nibbelink NP, Maerz JC (2010) Projected loss of a salamander diversity hotspot as a consequence of projected global climate change. PLoS ONE 5:e12189
Petranka JW (1998) Salamanders of the United States and Canada, Washington, DC: Smithsonian Institution Press
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
Rachowicz LJ, Knapp RA, Morgan JAT, Stice MJ, Vredenburg VT, Parker JM, Briggs CJ (2006) Emerging infectious disease as a proximate cause of amphibian mass mortality. Ecology 87:1671–1683
Raffel TR, Rohr JR, Kiesecker JM, Hudson PJ (2006) Negative effects of changing temperature on amphibian immunity under field conditions. Functional Ecology 20:819–828
Rothermel BB, Walls SC, Mitchell JC, Dodd CK Jr, Irwin LK, Green DE, Vazquez VM, Petranka JW, Stevenson DJ (2008) Widespread occurrence of the amphibian chytrid fungus Batrachochytrium dendrobatidis in the southeastern USA. Diseases of Aquatic Organisms 82:3–18
Schock DM, Bollinger TK, Collins JP (2009) Mortality rates among amphibian populations exposed to three strains of a lethal Ranavirus. EcoHealth 6:438–448
Souza 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
Todd-Thompson M, Miller DL, Super PE, Gray MJ (2009) Chytridiomycosis-associated mortality in a Rana palustris collected in Great Smoky Mountains National Park, Tennessee, USA. Herpetological Review 40:321–323
Todd-Thompson MC (2010) Seasonality, variation in species prevalence, and localized disease for Ranavirus in Cades Cove (Great Smoky Mountains National Park) amphibians, Master’s Thesis. Knoxville, TN: University of Tennessee
Vazquez VM, Rothermel BB, Pessier AP (2009) Experimental infection of North American plethodontid salamanders with the fungus Batrachochytrium dendrobatidis. Diseases of Aquatic Organisms 84:1–7
Vredenburg VT, Knapp RA, Tunstall TS, Briggs CJ (2010) Dynamics of an emerging disease drive large-scale amphibian population extinctions. Proceedings of the National Academy of Sciences 107:9689–9694
Wharton CH (1978) The Natural Environments of Georgia. Bulletin 114, Office of Planning and Research, Georgia Department of Natural Resources
Willson JD, Dorcas ME (2003) Effects of habitat disturbance on stream salamanders: Implications for buffer zones and watershed management. Conservation Biology 17:763–771
Acknowledgments
This project was supported by U.S. Fish and Wildlife Service (Georgia State Wildlife Grant T-34-R) and Nongame Wildlife Conservation Funds administered by Georgia Department of Natural Resources. We thank J. McCollum and Georgia Wildlife Federation for access to field sites and significant in-kind support. J. Jensen and C. Camp provided expert assistance with salamander identification and other aspects of the study. We are grateful to the many dedicated volunteers from Georgia Wildlife Federation (especially S. Caster, S. Downing, D. and E. Jennings, A. and M. Levine, E. Minche, J. Shaw), Zoo Atlanta (D. Brothers, E. Kabay, M. Quinn, L. Wyrwich), and University of Georgia (K. Barrett, D. Satterfield) for their assistance with data collection. We also thank E. Campbell Grant and A. Durso for advice regarding occupancy analyses and S. Walls and two anonymous reviewers for their helpful comments. Field research was performed under a special use permit from U.S. Forest Service and collecting permits from Georgia (29-WBH-10-55) and North Carolina (10-SC00015). Use of animals was reviewed and approved by the University of Georgia IACUC (A2007 10-186).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Rothermel, B.B., Travis, E.R., Miller, D.L. et al. High Occupancy of Stream Salamanders Despite High Ranavirus Prevalence in a Southern Appalachians Watershed. EcoHealth 10, 184–189 (2013). https://doi.org/10.1007/s10393-013-0843-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10393-013-0843-5