Ranavirus could facilitate local extinction of rare amphibian species
- 446 Downloads
There is growing evidence that pathogens play a role in population declines and species extinctions. For small populations, disease-induced extinction may be especially probable. We estimated the susceptibility of two amphibian species of conservation concern (the dusky gopher frog [Lithobates sevosus] and boreal toad [Anaxyrus boreas boreas]) to an emerging pathogen (ranavirus) using laboratory challenge experiments, and combined these data with published demographic parameter estimates to simulate the potential effects of ranavirus exposure on extinction risk. We included effects of life stage during pathogen exposure, pathogen exposure interval, hydroperiod of breeding habitat, population carrying capacity, and immigration in simulations. We found that both species were highly susceptible to ranavirus when exposed to the pathogen in water at environmentally relevant concentrations. Dusky gopher frogs experienced 100 % mortality in four of six life stages tested. Boreal toads experienced 100 % mortality when exposed as tadpoles or metamorphs, which were the only life stages tested. Simulations showed population declines, greater extinction probability, and faster times to extinction with ranavirus exposure. These effects were more evident with more frequent pathogen exposure intervals and lower carrying capacity. Immigration at natural rates did little to mitigate effects of ranavirus exposure unless immigration occurred every 2 years. Our results demonstrate that disease-induced extinction by emerging pathogens, such as ranavirus, is possible, and that threat may be especially high for species with small population sizes. For the species in this study, conservation organizations should incorporate ranavirus surveillance into monitoring programs and devise intervention strategies in the event that disease outbreaks occur.
KeywordsAmphibian declines Anaxyrus boreas boreas Endangered species Iridoviridae Lithobates sevosus Matrix model
Funding for this research was provided by the University of Tennessee Institute of Agriculture (UTIA) and for the dusky gopher frog challenges by the Morris Animal Foundation (Grant #D14ZO-055). We thank Bobby Simpson and Roger Long with the UTIA East Tennessee Research and Education Center for providing laboratory space and logistical support. This work was partially conducted while a Postdoctoral Fellow (JEE) at the National Institute for Mathematical and Biological Synthesis, an Institute sponsored by the National Science Foundation, the US Department of Homeland Security, and the US Department of Agriculture through NSF Award #EF-0832858, with additional support from The University of Tennessee, Knoxville. Further postdoctoral support (JEE) was provided by the South Central Climate Science Center. The authors would like to thank the Institute of Museum and Library Services (IMLS) National Leadership Grant LG-25-09-0064-09, for funding the research that produced the captive-bred Mississippi Gopher Frogs and Boreal Toads. Finally, we thank David Lesbarrères and two anonymous referees for comments that improved our manuscript. Laboratory research was approved under the University of Tennessee IACUC protocol #2140 and USFWS permit #TE171493-0 (dusky gopher frogs).
Author contribution statement
JEE and MJG conceived the study and led analyses and manuscript writing, JCC, WBS, and CEL performed the laboratory experiments, AJK, CL, and JK propagated the animals for the experiments, RPW replicated and titrated the virus, RDH and DLM lead the qPCR and histopathology, and all authors contributed to manuscript revision.
- Brenes R (2013) Mechanisms contributing to the emergence of ranavirus in ectothermic vertebrate communities. PhD, Department of Forestry, Fisheries and Wildlife, University of TennesseeGoogle Scholar
- Brunner JL, Storfer A, Gray MJ, Hoverman JT (2015) Ranavirus ecology and evolution: from epidemiology to extinction. In: Gray MJ, Chinchar VG (eds) Ranaviruses: lethal pathogens of ectothermic vertebrates. Springer, SecaucusGoogle Scholar
- Caswell H (2001) Matrix population models: construction, analysis, and interpretation, 2nd edn. Sinauer Associates, SunderlandGoogle Scholar
- Cheng K, Jones MEB, Jancovich JK, Burchell J, Schrenzel MD, Reavill DR, Imai DM, Urban A, Kirkendall M, Woods LW, Chinchar VG, Pessier AP (2014) Isolation of a Bohle-like iridovirus from boreal toads housed within a cosmopolitan aquarium collection. Dis Aquat Org 111:139–152CrossRefPubMedGoogle Scholar
- Converse KA, Green DE (2005) Diseases of tadpoles. In: Majundar SK, Huffman JE, Brenner FJ, Panah AL (eds) Wildlife diseases: landscape epidemiology, spatial distribution, and utilization of remote sensing technology. The Pennsylvania Academy of Science, Easton, pp 72–88Google Scholar
- Duffus ALJ, Waltzek TB, Stöhr AC, Allender MC, Gotesman M, Whittington RJ, Hick P, Hines MK, Marschang RE (2015) Distribution and host range of ranaviruses. In: Gray MJ, Chinchar VG (eds) Ranaviruses: lethal pathogens of ectothermic vertebrates. Springer, SecaucusGoogle Scholar
- Gosner KL (1960) A simple table for staging anuran embryos with notes on identification. Herpetologica 16:183–190Google Scholar
- Gray MJ, Lewis JP, Nanjappa P, Klocke B, Pasmans F, Martel A, Stephen C, Olea GP, Smith SA, Saacerdote-Velat A, Christman MR, Williams JM, Olson DH (2015b) Batrachochytrium salamandrivorans: the North American response and a call for action. PLoS Pathog 11:e1005251CrossRefPubMedPubMedCentralGoogle Scholar
- Grayfer L, Edholm E-S, Andino FD, Chinchar VG, Robert J (2015) Ranavirus host immunity and immune evasion. In: Gray MJ, Chinchar VG (eds) Ranaviruses: lethal pathogens of ectothermic vertebrates. Springer, Secaucus, pp 141–170Google Scholar
- IUCN SSC Amphibian Specialist Group (2015) Lithobates sylvaticus. The IUCN Red List of Threatened Species 2015:e.T58728A78907321Google Scholar
- Jackson T (2008) Report on the status and conservation of the boreal toad Bufo boreas boreas in the Southern Rock Mountains 2006–2007. Wildlife CDo (ed) Colorado Division of Wildlife, Denver, p 134Google Scholar
- Miller DL, Pessier AP, Hick P, Whittington RJ (2015) Comparative pathology of ranaviruses and diagnostic techniques. In: Gray MJ, Chinchar VG (eds) Ranaviruses: lethal pathogens of ectothermic vertebrates. Springer, SecaucusGoogle Scholar
- Muths E, Gallant AL, Grant EHC, Battaglin WA, Green DE, Staiger JS, Walls SC, Gunzburger MS, Kearney RF (2006a) The amphibian research and monitoring initiative (ARMI): 5-year report. Interior UDo, Survey UG (eds) US Geological Survey Scientific Investigations Report 2006-5224, p 77Google Scholar
- R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org
- Switzer JF, Johnson R, Lubinski BA, King TL (2009) Genetic structure in the Anaxyrus boreas species group (Anura, Bufonidae): an evaluation of the Southern Rocky Mountain population. USFWS, p 37Google Scholar
- Wheelwright NT, Gray MJ, Hill RD, Miller DL (2014) Sudden mass die-off of a large population of wood frog (Lithobates sylvaticus) tadpoles in Maine, USA, likely due to ranavirus. Herpetol Rev 45:240–242Google Scholar