Abstract
Ranaviruses are an emerging threat for many amphibian populations, yet their distribution in amphibian communities and the association of infection with possible stressors and species is not fully understood due to historically sparse surveillance. Agricultural practices that reduce the water quality of amphibian breeding habitats (e.g., cattle access to wetlands) and environmental stressors (e.g., lower temperatures) may contribute to ranavirus emergence. We tested larval amphibians for ranavirus infection across four seasons in farm ponds (n = 40) located in Tennessee, USA. Cattle at various densities were allowed access to half of the sampled ponds. Ranavirus infections were detected in nine species and in 33 of the sampled ponds (83%), illustrating widespread occurrence of the pathogen. Species within the family Ranidae were the most frequently infected. In 13 of the ponds containing infected individuals, prevalence exceeded 40% during at least one season. Infections were detected in multiple seasons in 20 of the sampled ponds containing infections, suggesting that ranaviruses are relatively persistent in these systems. Cattle had negative effects on water quality (turbidity and ammonia) and there was a positive association between cattle abundance and ranavirus prevalence in the summer. Counter to previous field studies in North America, we found a significant positive association between water temperature and ranavirus prevalence in the fall sampling events. Despite these findings, the influences of cattle and temperature on ranavirus prevalence were not consistent across seasons. As such, the mechanisms driving high ranavirus prevalence across the landscape and over time remain unclear. Given the widespread occurrence of ranaviruses in wild amphibians, we encourage the implementation of surveillance programs to help identify potential drivers of emergence. Sites with high ranavirus prevalence should be monitored annually for outbreaks, and the long-term effects on population size determined.
References
Bollinger TK, Mao JH, Schock D, Brigham RM, and Chinchar VG (1999). Pathology, isolation, and preliminary molecular characterization of a novel iridovirus from tiger salamanders in Saskatchewan. Journal of Wildlife Diseases 35:413-429.
Brunner JL, Schock DM, and Collins JP (2007). Transmission dynamics of the amphibian ranavirus Ambystoma tigrinum virus. Diseases of Aquatic Organisms 77:87-95.
Bruno JF, Petes LE, Harvell CD, and Hettinger A (2003). Nutrient enrichment can increase the severity of coral diseases. Ecology Letters 6:1056-1061.
Bryan L, Baldwin CA, Gray MJ, and Miller DL (2009). Efficacy of select disinfectants at inactivating Ranavirus. Diseases of Aquatic Organisms 84:89-94.
Burton EC, Gray MJ, Schmutzer AC, and Miller DL (2009). Differential responses of postmetamorphic amphibians to cattle grazing in wetlands. Journal of Wildlife Management 73:269-277.
Carey C, Bradford DE, Brunner JL, Collins JP, et al. (2003) Biotic factors in amphibian declines. In: Linder G, Krest SK, Sparling DW (eds) Amphibian Declines: An Integrated Analysis of Multiple Stressor Effects. Society of Environmental Toxicology and Chemistry, Pensacola, pp 153–208.
Carey C, Cohen N, and Rollins-Smith L (1999). Amphibian declines: an immunological perspective. Developmental And Comparative Immunology 23:459-472.
Cleaveland S, Laurenson MK, and Taylor LH (2001). Diseases of humans and their domestic mammals: pathogen characteristics, host range and the risk of emergence. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 356:991-999.
Converse KA, and Green DE (2005). Diseases of tadpoles. Pages 72-88 in S. K. Majumdar, J. E. Huffman, F. J. Brenner, and A. I. Panah, editors. Wildlife diseases: Landscape epidemiology, spatial distribution and utilization of remote sensing technology. The Pennsylvania Academy of Science, Easton, Pennsylvania.
Cunningham AA, Hyatt AD, Russell P, and Bennett PM (2007). Experimental transmission of a ranavirus disease of common toads (Bufo bufo) to common frogs (Rana temporaria). Epidemiology and Infection 135:1213-1216.
Daszak P, Berger L, Cunningham AA, Hyatt AD, Green DE, and Speare R (1999). Emerging infectious diseases and amphibian population declines. Emerging Infectious Diseases 5:735-748.
Daszak P, Cunningham AA, and Hyatt AD (2000). Wildlife ecology - Emerging infectious diseases of wildlife: threats to biodiversity and human health. Science 287:443-449.
Daszak P, Cunningham AA, and Hyatt AD (2001). Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Tropica 78:103-116.
Dobson A, and Foufopoulos J (2001). Emerging infectious pathogens of wildlife. Philosophical Transactions Of The Royal Society Of London Series B-Biological Sciences 356:1001-1012.
Docherty DE, Meteyer CU, Wang J, Mao JH, Case ST, and Chinchar VG (2003). Diagnostic and molecular evaluation of three iridovirus-associated salamander mortality events. Journal of Wildlife Diseases 39:556-566.
Duffus ALJ, Pauli BD, Wozney K, Brunetti CR, and Berrill M (2008). Frog virus 3-like infections in aquatic amphibian communities. Journal of Wildlife Diseases 44:109-120.
Forbes MR, McRuer DL, and Rutherford PL (2004). Prevalence of Aeromonas hydrophila in relation to timing and duration of breeding in three species of ranid frogs. Ecoscience 11:282-285.
Gahl MK, and Calhoun AJK (2008). Landscape setting and risk of Ranavirus mortality events. Biological Conservation 141:2679-2689.
Gantress J, Maniero GD, Cohen N, and Robert J (2003). Development and characterization of a model system to study amphibian immune responses to iridoviruses. Virology 311:254-262.
Gray MJ, Miller DL, and Hoverman JT (2009). Ecology and pathology of amphibian ranaviruses. Diseases of Aquatic Organisms 87:243-266.
Gray MJ, Miller DL, Schmutzer AC, and Baldwin CA (2007). Frog virus 3 prevalence in tadpole populations inhabiting cattle-access and non-access wetlands in Tennessee, USA. Diseases of Aquatic Organisms 77:97-103.
Green DE, Converse KA, and 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.
Green DE, Gray MJ, and Miller DL (2009). Disease monitoring and biosecurity. Pages 481-505 in C. K. Dodd, editor. Amphibian Ecology and Conservation: A Handbook of Techniques. Oxford University Press, Oxford, UK.
Greer AL, Berrill M, and Wilson PJ (2005). Five amphibian mortality events associated with ranavirus infection in south central Ontario, Canada. Diseases of Aquatic Organisms 67:9-14.
Greer AL, Brunner JL, and Collins JP (2009). Spatial and temporal patterns of Ambystoma tigrinum virus (ATV) prevalence in tiger salamanders Ambystoma tigrinum nebulosum. Diseases of Aquatic Organisms 85:1-6.
Greer AL, and Collins JP (2008). Habitat fragmentation as a result of biotic and abiotic factors controls pathogen transmission throughout a host population. Journal of Animal Ecology 77:364-369.
Harp EM, and Petranka JW (2006). Ranavirus in wood frogs (Rana sylvatica): Potential sources of transmission within and between ponds. Journal of Wildlife Diseases 42:307-318.
Hoverman JT, Gray MJ, Haislip NA, Miller DL (2011). Phylogeny, life history, and ecology contribute to differences in amphibian susceptibility to ranaviruses. Ecohealth. doi:10.1007/s10393-011-0717-7.
Hoverman JT, Gray MJ, and 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.
Jancovich JK, Davidson EW, Morado JF, Jacobs BL, and Collins JP (1997). Isolation of a lethal virus from the endangered tiger salamander Ambystoma tigrinum stebbinsi. Diseases of Aquatic Organisms 31:161-167.
Jofre MB, and Karasov WH (1999). Direct effect of ammonia on three species of North American anuran amphibians. Environmental Toxicology and Chemistry 18:1806-1812.
Johnson PJ, and Lunde KB (2005). Parasite infection and limb malformations: A growing problem in amphibian conservation. Pages 124-138 in M. Lannoo, editor. Amphibian declines: the conservation status of United States species. University of California Press, Berkeley, California.
Lloyd S (1995). Environmental influences on host immunity. Pages 327-361 in B. Grenfell and A. Dobson, editors. Ecology of infectious disease in natural populations. University of Cambridge, New York, New York.
Maniero GD, and Carey C (1997). Changes in selected aspects of immune function in the leopard frog, Rana pipiens, associated with exposure to cold. Journal Of Comparative Physiology B-Biochemical Systemic And Environmental Physiology 167:256-263.
Mao J, Tham TN, Gentry GA, Aubertin A, and Chinchar VG (1996). Cloning, sequence analysis, and expression of the major capsid protein of the iridovirus frog virus 3. Virology 216:431-436.
Mao JH, Hedrick RP, and Chinchar VG (1997). Molecular characterization, sequence analysis, and taxonomic position of newly isolated fish iridoviruses. Virology 229:212–220.
Miller DL, Gray MJ, and Storfer A (2011). Ecopathology of ranaviruses infecting amphibians. Viruses 3:2351–2373.
Miller DL, Rajeev S, Gray MJ, and Baldwin CA (2007). Frog virus 3 infection, cultured American bullfrogs. Emerging Infectious Diseases 13:342-343.
National_Climatic_Data_Center (2008) State of the climate annual review: U.S. drought 2007 http://www.ncdc.noaa.gov/oa/climate/research/2007/ann/drought-summary.html. Accessed 14 Dec 2010.
Petranka JW, Harp EM, Holbrook CT, and Hamel JA (2007). Long-term persistence of amphibian populations in a restored wetland complex. Biological Conservation 138:371-380.
Petranka JW, Murray SS, and Kennedy CA (2003). Responses of amphibians to restoration of a southern appalachian wetland: Perturbations confound post-restoration assessment. Wetlands 23:278-290.
Picco A, Karam A, Collins J (2010) Pathogen host switching in commercial trade with management recommendations. Ecohealth 7:252–256.
Picco AM, Brunner JL, and Collins JP (2007). Susceptibility of the endangered California tiger salamander, Ambystoma californiense, to Ranavirus infection. Journal of Wildlife Diseases 43:286-290.
Raffel TR, Rohr JR, Kiesecker JM, and Hudson PJ (2006). Negative effects of changing temperature on amphibian immunity under field conditions. Functional Ecology 20:819-828.
Redmond WH, and Scott AF (1996). Atlas of amphibians in Tennessee. Austin Peay State University, Clarksville, Tennessee.
Rohr JR, Schotthoefer AM, Raffel TR, Carrick HJ, Halstead N, Hoverman JT, et al. (2008). Agrochemicals increase trematode infections in a declining amphibian species. Nature 455:1235-U1250.
Rojas S, Richards K, Jancovich JK, and Davidson EW (2005). Influence of temperature on Ranavirus infection in larval salamanders Ambystoma tigrinum. Diseases of Aquatic Organisms 63:95-100.
Schmutzer AC, Gray MJ, Burton EC, and Miller DL (2008). Impacts of cattle on amphibian larvae and the aquatic environment. Freshwater Biology 53:2613-2625.
Schock DM, and Bollinger TK (2005). An apparent decline of Northern Leopard Frogs (Rana pipiens) on the Rafferty Dam Mitigation Lands near Estevan, Saskatchewan. Blue Jay 63:144-154.
Schock DM, Bollinger TK, Chinchar VG, Jancovich JK, Collins JP (2008) Experimental evidence that amphibian ranaviruses are multi-host pathogens. Copeia 1:133–143.
Teacher AGF, Cunningham AA, and Garner TWJ (2010). Assessing the long-term impact of Ranavirus infection in wild common frog populations. Animal Conservation 13:514-522.
Torrence SM, Green DE, Benson CJ, Ip HS, Smith LM, and McMurry ST (2010). A New Ranavirus Isolated from Pseudacris clarkii Tadpoles in Playa Wetlands in the Southern High Plains, Texas. Journal of Aquatic Animal Health 22:65-72.
Tweedell K, and Granoff A (1968). Viruses and renal carcinoma of Rana pipiens. V. Effect of Frog Virus 3 on developing frog embryos and larvae. Journal of the National Cancer Institute 40:407-410.
Wellborn GA, Skelly DK, and Werner EE (1996). Mechanisms creating community structure across a freshwater habitat gradient. Annual Review of Ecology and Systematics 27:337-363.
Acknowledgments
The authors thank the Tennessee Wildlife Resources Agency (TWRA) and the University of Tennessee Institute of Agriculture for funding this study. The University of Georgia Veterinary Diagnostic and Investigational Laboratory in Tifton, Georgia, performed all the molecular procedures associated with ranavirus testing. The authors especially thank L. Whittington and N. Hilzinger for their help. Animal euthanasia procedures followed an approved University of Tennessee IACUC protocol (#1755). Collection of animals was approved by the TWRA (Scientific Collection Permit #1990).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Hoverman, J.T., Gray, M.J., Miller, D.L. et al. Widespread Occurrence of Ranavirus in Pond-Breeding Amphibian Populations. EcoHealth 9, 36–48 (2012). https://doi.org/10.1007/s10393-011-0731-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10393-011-0731-9