Skip to main content
Top
Published in: EcoHealth 4/2014

01-12-2014 | Original Contribution

Introduction of Ranavirus to Isolated Wood Frog Populations Could Cause Local Extinction

Authors: Julia E. Earl, Matthew J. Gray

Published in: EcoHealth | Issue 4/2014

Login to get access

Abstract

Amphibian declines and extinction have been attributed to many causes, including disease such as chytridiomycosis. Other pathogens may also contribute to declines, with ranavirus as the most likely candidate given reoccurring die-offs observed in the wild. We were interested in whether it is possible for ranavirus to cause extinction of a local, closed population of amphibians. We used susceptibility data from experimental challenges on different life stages combined with estimates of demographic parameters from a natural population to predict the likelihood of extinction using a stage-structured population model for wood frogs (Lithobates sylvaticus). Extinction was most likely when the larval or metamorph stage was exposed under frequent intervals in smaller populations. Extinction never occurred when only the egg stage was exposed to ranavirus. Under the worst-case scenario, extinction could occur in as quickly as 5 years with exposure every year and 25–44 years with exposure every 2 years. In natural wood frog populations, die-offs typically occur in the larval stage and can reoccur in subsequent years, indicating that our simulations represent possible scenarios. Additionally, wood frog populations are particularly sensitive to changes in survival during the pre-metamorphic stages when ranavirus tends to be most pathogenic. Our results suggest that ranavirus could contribute to amphibian species declines, especially for species that are very susceptible to ranavirus with closed populations. We recommend that ranavirus be considered in risk analyses for amphibian species.
Literature
go back to reference Al-Asuoad N, Anguelov R, Berven KA & Shillor M (2012) Model and simulations of a wood frog population. Biomath 1:1209032CrossRef Al-Asuoad N, Anguelov R, Berven KA & Shillor M (2012) Model and simulations of a wood frog population. Biomath 1:1209032CrossRef
go back to reference Altizer S, Harvell D & Friedle E (2003) Rapid evolutionary dynamics and disease threats to biodiversity. Trends in Ecology & Evolution 18:589-596CrossRef Altizer S, Harvell D & Friedle E (2003) Rapid evolutionary dynamics and disease threats to biodiversity. Trends in Ecology & Evolution 18:589-596CrossRef
go back to reference Balseiro A, Dalton KP, Del Cerro A, Márquez I, Parra F, Prieto JM & Casais R (2010) Outbreak of common midwife toad virus in alpine newts (Mesotriton alpestris cyreni) and common midwife toads (Alytes obstetricans) in Northern Spain: A comparative pathological study of an emerging ranavirus. Veterinary Journal 186:256-258CrossRef Balseiro A, Dalton KP, Del Cerro A, Márquez I, Parra F, Prieto JM & Casais R (2010) Outbreak of common midwife toad virus in alpine newts (Mesotriton alpestris cyreni) and common midwife toads (Alytes obstetricans) in Northern Spain: A comparative pathological study of an emerging ranavirus. Veterinary Journal 186:256-258CrossRef
go back to reference Bayley AE, Hill BJ & Feist SW (2013) Susceptibility of the European common frog Rana temporaria to a panel of ranavirus isolates from fish and amphibian hosts. Diseases of Aquatic Organisms 103:171-183CrossRefPubMed Bayley AE, Hill BJ & Feist SW (2013) Susceptibility of the European common frog Rana temporaria to a panel of ranavirus isolates from fish and amphibian hosts. Diseases of Aquatic Organisms 103:171-183CrossRefPubMed
go back to reference Berrill M, Coulson DR, Mcgillivray L & Pauli BD (1998) Toxicity of endosulfan to aquatic stages of anuran amphibians. Environmental Toxicology and Chemistry 17:1738-1744CrossRef Berrill M, Coulson DR, Mcgillivray L & Pauli BD (1998) Toxicity of endosulfan to aquatic stages of anuran amphibians. Environmental Toxicology and Chemistry 17:1738-1744CrossRef
go back to reference Berven KA (1990) Factors affecting population fluctuations in larval and adult stages of the wood frog (Rana sylvatica). Ecology 71:1599-1608CrossRef Berven KA (1990) Factors affecting population fluctuations in larval and adult stages of the wood frog (Rana sylvatica). Ecology 71:1599-1608CrossRef
go back to reference Berven KA (1995) Population regulation in wood frog, Rana sylvatica, from three diverse geographic localities. Australian Journal of Ecology 20:385-392CrossRef Berven KA (1995) Population regulation in wood frog, Rana sylvatica, from three diverse geographic localities. Australian Journal of Ecology 20:385-392CrossRef
go back to reference Berven KA (2009) Density dependence in the terrestrial stage of wood frogs: Evidence from a 21-year population study. Copeia 2009:328-338CrossRef Berven KA (2009) Density dependence in the terrestrial stage of wood frogs: Evidence from a 21-year population study. Copeia 2009:328-338CrossRef
go back to reference Biek R, Funk WC, Maxwell BA & Mills LS (2002) What is missing in amphibian decline research: insights from ecological sensitivity analysis. Conservation Biology 16:728-734CrossRef Biek R, Funk WC, Maxwell BA & Mills LS (2002) What is missing in amphibian decline research: insights from ecological sensitivity analysis. Conservation Biology 16:728-734CrossRef
go back to reference Blaustein AR, Hokit DG, O’hara RB & Holt RA (1994) Pathogenic fungus contributes to amphibian losses in the Pacific northwest. Biological Conservation 67:251-254CrossRef Blaustein AR, Hokit DG, O’hara RB & Holt RA (1994) Pathogenic fungus contributes to amphibian losses in the Pacific northwest. Biological Conservation 67:251-254CrossRef
go back to reference Brenes R (2013) Mechanisms contributing to the emergence of ranavirus in ectothermic vertebrate communities. Ph.D. Dissertation, University of Tennessee Brenes R (2013) Mechanisms contributing to the emergence of ranavirus in ectothermic vertebrate communities. Ph.D. Dissertation, University of Tennessee
go back to reference Brenes R, Gray MJ, Waltzek TB, Wilkes RP, Miller DL (2014a) Transmission of ranavirus between ectothermic vertebrate hosts. PLoS One 9:e92476 Brenes R, Gray MJ, Waltzek TB, Wilkes RP, Miller DL (2014a) Transmission of ranavirus between ectothermic vertebrate hosts. PLoS One 9:e92476
go back to reference Brenes R, Miller DL, Waltzek TB, Wilkes RP, Tucker JL (2014b) Susceptibility of fish and turtles to three ranaviruses isolated from different ectothermic vertebrate classes. Journal of Aquatic Animal Health 26:118–126 Brenes R, Miller DL, Waltzek TB, Wilkes RP, Tucker JL (2014b) Susceptibility of fish and turtles to three ranaviruses isolated from different ectothermic vertebrate classes. Journal of Aquatic Animal Health 26:118–126
go back to reference Briggs CJ, Vredenburg VT, Knapp RA & Rachowicz LJ (2005) Investigating the population-level effects of chytridiomycosis: an emerging infectious disease of amphibians. Ecology 86:3149-3159CrossRef Briggs CJ, Vredenburg VT, Knapp RA & Rachowicz LJ (2005) Investigating the population-level effects of chytridiomycosis: an emerging infectious disease of amphibians. Ecology 86:3149-3159CrossRef
go back to reference Brunner JL, Barnett KE, Gosier CJ, Mcnulty SA, Rubbo MJ & Kolozsvary MB (2011) Ranavirus infection in die-offs of vernal pool amphibians in New York, USA. Herpetological Review 42:76-79 Brunner JL, Barnett KE, Gosier CJ, Mcnulty SA, Rubbo MJ & Kolozsvary MB (2011) Ranavirus infection in die-offs of vernal pool amphibians in New York, USA. Herpetological Review 42:76-79
go back to reference Brunner JL, Richards K & Collins JP (2005) Dose and host characteristics influence virulence of ranavirus infections. Oecologia 144:399-406CrossRefPubMed Brunner JL, Richards K & Collins JP (2005) Dose and host characteristics influence virulence of ranavirus infections. Oecologia 144:399-406CrossRefPubMed
go back to reference Brunner JL, Schock DM & Collins JP (2007) Transmission dynamics of the amphibian ranavirus Ambystoma tigrinum virus. Diseases of Aquatic Organisms 77:87-95CrossRefPubMed Brunner JL, Schock DM & Collins JP (2007) Transmission dynamics of the amphibian ranavirus Ambystoma tigrinum virus. Diseases of Aquatic Organisms 77:87-95CrossRefPubMed
go back to reference Brunner JL, Schock DM, Davidson EW & Collins JP (2004) Intraspecific reservoirs: Complex life history and the persistence of a lethal ranavirus. Ecology 85:560-566CrossRef Brunner JL, Schock DM, Davidson EW & Collins JP (2004) Intraspecific reservoirs: Complex life history and the persistence of a lethal ranavirus. Ecology 85:560-566CrossRef
go back to reference Bryan LK, Baldwin CA, Gray MJ & Miller DL (2009) Efficacy of select disinfectants at inactivating ranavirus. Diseases of Aquatic Organisms 84:89-94CrossRefPubMed Bryan LK, Baldwin CA, Gray MJ & Miller DL (2009) Efficacy of select disinfectants at inactivating ranavirus. Diseases of Aquatic Organisms 84:89-94CrossRefPubMed
go back to reference Caswell H (2000) Matrix Population Models: Construction, Analysis, and Interpretation, 2nd edn. Sunderland, MA: Sinauer Associates Caswell H (2000) Matrix Population Models: Construction, Analysis, and Interpretation, 2nd edn. Sunderland, MA: Sinauer Associates
go back to reference Collins JP & Crump ML (2009) Extinction in Our Times: Global Amphibian Decline. Oxford: Oxford University Press Collins JP & Crump ML (2009) Extinction in Our Times: Global Amphibian Decline. Oxford: Oxford University Press
go back to reference Collins JP & Storfer A (2003) Global amphibian declines: sorting the hypotheses. Diversity and Distributions 9:89-98CrossRef Collins JP & Storfer A (2003) Global amphibian declines: sorting the hypotheses. Diversity and Distributions 9:89-98CrossRef
go back to reference Cunningham AA & Daszak P (1998) Extinction of a species of land snail due to infection with a microsporidian parasite. Conservation Biology 12:1139-1141CrossRef Cunningham AA & Daszak P (1998) Extinction of a species of land snail due to infection with a microsporidian parasite. Conservation Biology 12:1139-1141CrossRef
go back to reference Cunningham AA, Langton TE, Bennett PM, Drury SE, Gough RE & Kirkwood JK (1993) Unusual mortality associated with poxvirus-like particles in frogs (Rana temporaria). Veterinary Record 133:141-142CrossRefPubMed Cunningham AA, Langton TE, Bennett PM, Drury SE, Gough RE & Kirkwood JK (1993) Unusual mortality associated with poxvirus-like particles in frogs (Rana temporaria). Veterinary Record 133:141-142CrossRefPubMed
go back to reference Daszak P, Cunningham AA & Hyatt AD (2003) Infectious disease and amphibian population declines. Diversity and Distributions 9:141-150CrossRef Daszak P, Cunningham AA & Hyatt AD (2003) Infectious disease and amphibian population declines. Diversity and Distributions 9:141-150CrossRef
go back to reference De Castro F & Bolker BM (2005) Mechanisms of disease-induced extinction. Ecology Letters 8:117-126CrossRef De Castro F & Bolker BM (2005) Mechanisms of disease-induced extinction. Ecology Letters 8:117-126CrossRef
go back to reference Gahl MK & Calhoun AJK (2010) The role of multiple stressors in ranavirus-caused amphibian mortalities in Acadia National Park wetlands. Canadian Journal of Zoology 88:108-121CrossRef Gahl MK & Calhoun AJK (2010) The role of multiple stressors in ranavirus-caused amphibian mortalities in Acadia National Park wetlands. Canadian Journal of Zoology 88:108-121CrossRef
go back to reference Gantress J, Maniero GD, Cohen N & Robert J (2003) Development and characterization of a model system to study amphibian immune responses to iridoviruses. Virology 311:254-262CrossRefPubMed Gantress J, Maniero GD, Cohen N & Robert J (2003) Development and characterization of a model system to study amphibian immune responses to iridoviruses. Virology 311:254-262CrossRefPubMed
go back to reference Gold KK, Reed PD, Bemis DA, Miller DL, Gray MJ & Souza MJ (2013) Efficacy of common disinfectants and terbinafine in inactivating the growth of Batrachochytrium dendrobatidis in culture. Diseases of Aquatic Organisms 107:77-81CrossRefPubMed Gold KK, Reed PD, Bemis DA, Miller DL, Gray MJ & Souza MJ (2013) Efficacy of common disinfectants and terbinafine in inactivating the growth of Batrachochytrium dendrobatidis in culture. Diseases of Aquatic Organisms 107:77-81CrossRefPubMed
go back to reference Gosner KL (1960) A simple table for staging anuran embryos with notes on identification. Herpetologica 16:183-190 Gosner KL (1960) A simple table for staging anuran embryos with notes on identification. Herpetologica 16:183-190
go back to reference Gray MJ & Miller DL (2013) The rise of ranavirus: an emerging pathogen threatens ectothermic vertebrates. Wildlife Professional, 7:51–55 Gray MJ & Miller DL (2013) The rise of ranavirus: an emerging pathogen threatens ectothermic vertebrates. Wildlife Professional, 7:51–55
go back to reference Gray MJ, Miller DL & Hoverman JT (2009) Ecology and pathology of amphibian ranaviruses. Diseases of Aquatic Organisms 87:243-266CrossRefPubMed Gray MJ, Miller DL & Hoverman JT (2009) Ecology and pathology of amphibian ranaviruses. Diseases of Aquatic Organisms 87:243-266CrossRefPubMed
go back to reference Green DE, Converse KA & Schrader AK (2002) Epizootiology of sixty-four amphibian morbidity and motality events in the USA, 1996-2001. Annals of the New York Academy of Sciences 969:323-339CrossRefPubMed Green DE, Converse KA & Schrader AK (2002) Epizootiology of sixty-four amphibian morbidity and motality events in the USA, 1996-2001. Annals of the New York Academy of Sciences 969:323-339CrossRefPubMed
go back to reference Green DE, Gray MJ & Miller DL (2009) Disease monitoring and biosecurity. In: Amphibian Ecology and Conservation. A Handbook of Techniques, CK Dodd Jr (editor), Oxford, UK: Oxford University Press, pp. 481–505 Green DE, Gray MJ & Miller DL (2009) Disease monitoring and biosecurity. In: Amphibian Ecology and Conservation. A Handbook of Techniques, CK Dodd Jr (editor), Oxford, UK: Oxford University Press, pp. 481–505
go back to reference Greer AL, Berrill M & Wilson PJ (2005) Five amphibian mortality events associated with ranavirus in south central Ontario, Canada. Diseases of Aquatic Organisms 67:9-14CrossRefPubMed Greer AL, Berrill M & Wilson PJ (2005) Five amphibian mortality events associated with ranavirus in south central Ontario, Canada. Diseases of Aquatic Organisms 67:9-14CrossRefPubMed
go back to reference Greer AL, Briggs CJ & Collins JP (2008) Testing a key assumption of host-pathogen theory: density and disease transmission. Oikos 117:1667-1673CrossRef Greer AL, Briggs CJ & Collins JP (2008) Testing a key assumption of host-pathogen theory: density and disease transmission. Oikos 117:1667-1673CrossRef
go back to reference Guerry AD & Hunter ML, Jr. (2002) Amphibian distributions in a landscape of forests and agriculture: an examination of landscape composition and configuration. Conservation Biology 16:745-754CrossRef Guerry AD & Hunter ML, Jr. (2002) Amphibian distributions in a landscape of forests and agriculture: an examination of landscape composition and configuration. Conservation Biology 16:745-754CrossRef
go back to reference 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:e22307CrossRefPubMedCentralPubMed 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:e22307CrossRefPubMedCentralPubMed
go back to reference Han Y, Yu H, Yang X, Rees HH, Liu J & Lai R (2008) A serine proteinase inhibitor from frog eggs with bacteriostatic activity. Comparative Biochemistry and Physiology B-Biochemistry & Molecular Biology 149:58-62CrossRef Han Y, Yu H, Yang X, Rees HH, Liu J & Lai R (2008) A serine proteinase inhibitor from frog eggs with bacteriostatic activity. Comparative Biochemistry and Physiology B-Biochemistry & Molecular Biology 149:58-62CrossRef
go back to reference Harp EM & Petranka JW (2006) Ranavirus in wood frogs (Rana sylvatica): Potential sources of transmission within and between ponds. Journal of Wildlife Diseases 42:307-318CrossRefPubMed Harp EM & Petranka JW (2006) Ranavirus in wood frogs (Rana sylvatica): Potential sources of transmission within and between ponds. Journal of Wildlife Diseases 42:307-318CrossRefPubMed
go back to reference Harper EB, Rittenhouse TAG & Semlitsch RD (2008) Demographic consequences of terrestrial habitat loss for pool-breeding amphibians: Predicting extinction risks associated with inadequate size of buffer zones. Conservation Biology 22:1205-1215CrossRefPubMed Harper EB, Rittenhouse TAG & Semlitsch RD (2008) Demographic consequences of terrestrial habitat loss for pool-breeding amphibians: Predicting extinction risks associated with inadequate size of buffer zones. Conservation Biology 22:1205-1215CrossRefPubMed
go back to reference Heard MJ, Smith KF, Ripp KJ, Berger M, Chen J, Dittmeier J, Goter M, Mcgarvey ST & Ryan E (2013) The threat of disease increases as species move toward extinction. Conservation Biology 27:1378-1388CrossRefPubMed Heard MJ, Smith KF, Ripp KJ, Berger M, Chen J, Dittmeier J, Goter M, Mcgarvey ST & Ryan E (2013) The threat of disease increases as species move toward extinction. Conservation Biology 27:1378-1388CrossRefPubMed
go back to reference Hoverman JT, Gray MJ, Haislip NA & Miller DL (2011) Phylogeny, life history, and ecology contribute to differences in amphibian susceptibility to ranaviruses. EcoHealth 8:301-319CrossRefPubMed Hoverman JT, Gray MJ, Haislip NA & Miller DL (2011) Phylogeny, life history, and ecology contribute to differences in amphibian susceptibility to ranaviruses. EcoHealth 8:301-319CrossRefPubMed
go back to reference Huelsenbeck JP, Rannala B & Yang Z (1997) Statistical tests of host-parasite conspeciation. Evolution 51:410-419CrossRef Huelsenbeck JP, Rannala B & Yang Z (1997) Statistical tests of host-parasite conspeciation. Evolution 51:410-419CrossRef
go back to reference IUCN (2013) The IUCN Red List of Threatened Species, Version 2013.1. IUCN (2013) The IUCN Red List of Threatened Species, Version 2013.1.
go back to reference Jancovich JK, Davidson EW, Seiler A, Jacobs BL & Collins JP (2001) Tranmission of the Ambystoma tigrinum virus to alternative hosts. Diseases of Aquatic Organisms 46:159-163CrossRefPubMed Jancovich JK, Davidson EW, Seiler A, Jacobs BL & Collins JP (2001) Tranmission of the Ambystoma tigrinum virus to alternative hosts. Diseases of Aquatic Organisms 46:159-163CrossRefPubMed
go back to reference Johnson PTJ, Lunde KB, Ritchie EG & Launer AE (1999) The effect of trematode infection on amphibian limb development and survivorship. Science 284:802-804CrossRefPubMed Johnson PTJ, Lunde KB, Ritchie EG & Launer AE (1999) The effect of trematode infection on amphibian limb development and survivorship. Science 284:802-804CrossRefPubMed
go back to reference Julian SE & King TL (2003) Novel tetranucleotide microsatellite DNA markers for the wood frog, Rana sylvatica. Molecular Ecology Notes 3:256-258CrossRef Julian SE & King TL (2003) Novel tetranucleotide microsatellite DNA markers for the wood frog, Rana sylvatica. Molecular Ecology Notes 3:256-258CrossRef
go back to reference Kiesecker JM, Blaustein AR & Belden LK (2001) Complex causes of amphibian population declines. Nature 410:681-684CrossRefPubMed Kiesecker JM, Blaustein AR & Belden LK (2001) Complex causes of amphibian population declines. Nature 410:681-684CrossRefPubMed
go back to reference King AMQ, Adams MJ, Carstens EB & Lefkowitz EJ (2012) Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses. Academic Press, London King AMQ, Adams MJ, Carstens EB & Lefkowitz EJ (2012) Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses. Academic Press, London
go back to reference Lande R (1993) Risks of population extinction from demographic and environmental stochasticity and random catastrophes. The American Naturalist 142:911-927CrossRef Lande R (1993) Risks of population extinction from demographic and environmental stochasticity and random catastrophes. The American Naturalist 142:911-927CrossRef
go back to reference Lanoo M (2005) Amphibian declines: the conservation status of United States species. Berkeley, California: University of California PressCrossRef Lanoo M (2005) Amphibian declines: the conservation status of United States species. Berkeley, California: University of California PressCrossRef
go back to reference León-Vizcaíno L, Deybáñez MRR, Cubero MJ, Ortíz JM, Espinosa J, Pérez L, Simón MA & Alonso F (1999) Sarcoptic mange in Spanish ibex from Spain. Journal of Wildlife Diseases 35:647-659CrossRefPubMed León-Vizcaíno L, Deybáñez MRR, Cubero MJ, Ortíz JM, Espinosa J, Pérez L, Simón MA & Alonso F (1999) Sarcoptic mange in Spanish ibex from Spain. Journal of Wildlife Diseases 35:647-659CrossRefPubMed
go back to reference Lips KR, Brem F, Brenes R, Reeve JD, Alford RA, Voyles J, Carey C, Livo L, Pessler AP & Collins JP (2006) Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. PNAS 103:3165-3170CrossRefPubMedCentralPubMed Lips KR, Brem F, Brenes R, Reeve JD, Alford RA, Voyles J, Carey C, Livo L, Pessler AP & Collins JP (2006) Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. PNAS 103:3165-3170CrossRefPubMedCentralPubMed
go back to reference Marsh DM & Trenham PC (2001) Metapopulation dynamics and amphibian conservation. Conservation Biology 15:40-49CrossRef Marsh DM & Trenham PC (2001) Metapopulation dynamics and amphibian conservation. Conservation Biology 15:40-49CrossRef
go back to reference Mccallum H, Barlow N & Hone J (2001) How should pathogen transmission be modeled. Trends in Ecology & Evolution 16:295-300CrossRef Mccallum H, Barlow N & Hone J (2001) How should pathogen transmission be modeled. Trends in Ecology & Evolution 16:295-300CrossRef
go back to reference Muths E, Gallant AL, Grant EHC, Battaglin WA, Green DE, Staiger JS, Walls SC, Gunzburger MS, Kearney RF (2006). In: The Amphibian Research and Monitoring Initiative (ARMI): 5-Year Report, UDo Interior, UG Survey (editors), US Geological Survey Scientific Investigations Report 2006–5224, pp. 77 Muths E, Gallant AL, Grant EHC, Battaglin WA, Green DE, Staiger JS, Walls SC, Gunzburger MS, Kearney RF (2006). In: The Amphibian Research and Monitoring Initiative (ARMI): 5-Year Report, UDo Interior, UG Survey (editors), US Geological Survey Scientific Investigations Report 2006–5224, pp. 77
go back to reference Nazir J, Spengler M & Marschang RE (2012) Environtmental persistence of amphibian and reptilian ranaviruses. Diseases of Aquatic Organisms 98:177-184CrossRefPubMed Nazir J, Spengler M & Marschang RE (2012) Environtmental persistence of amphibian and reptilian ranaviruses. Diseases of Aquatic Organisms 98:177-184CrossRefPubMed
go back to reference Newman RA & Squire T (2001) Microsatellite variation and fine-scale population structure in the wood frog (Rana sylvatica). Molecular Ecology 10:1087-1100CrossRefPubMed Newman RA & Squire T (2001) Microsatellite variation and fine-scale population structure in the wood frog (Rana sylvatica). Molecular Ecology 10:1087-1100CrossRefPubMed
go back to reference Pauli BD, Coulson DR & Berrill M (1999) Senstivity of amphibian embryos to MIMIC 240LV insecticide following single or double exposures. Environmental Toxicology and Chemistry 18:2538-2544CrossRef Pauli BD, Coulson DR & Berrill M (1999) Senstivity of amphibian embryos to MIMIC 240LV insecticide following single or double exposures. Environmental Toxicology and Chemistry 18:2538-2544CrossRef
go back to reference Pearman PB & Garner TWJ (2005) Susceptibility of Italian agile frog populations to an emerging strain of Ranavirus parallels population genetic diversity. Ecology Letters 8:401-408CrossRef Pearman PB & Garner TWJ (2005) Susceptibility of Italian agile frog populations to an emerging strain of Ranavirus parallels population genetic diversity. Ecology Letters 8:401-408CrossRef
go back to reference Peterman WE, Rittenhouse TAG, Earl JE & Semlitsch RD (2013) Demographic network and multi-season occupancy modeling of Rana sylvatica reveals spatial and temporal patterns of population connectivity and persistence. Landscape Ecology 28:1601-1613CrossRef Peterman WE, Rittenhouse TAG, Earl JE & Semlitsch RD (2013) Demographic network and multi-season occupancy modeling of Rana sylvatica reveals spatial and temporal patterns of population connectivity and persistence. Landscape Ecology 28:1601-1613CrossRef
go back to reference Petranka JW, Harp EM, Holbrook CT & Hamel JA (2007) Long-term persistence of amphibian populations in a restored wetland complex. Biological Conservation 138:371-380CrossRef Petranka JW, Harp EM, Holbrook CT & Hamel JA (2007) Long-term persistence of amphibian populations in a restored wetland complex. Biological Conservation 138:371-380CrossRef
go back to reference Petranka JW, Murray SS & Kennedy CA (2003) Responses of amphibians to restoration of a southern Appalachian wetland: perturbations confound post-restoration assessment. Wetlands 23:278-290CrossRef Petranka JW, Murray SS & Kennedy CA (2003) Responses of amphibians to restoration of a southern Appalachian wetland: perturbations confound post-restoration assessment. Wetlands 23:278-290CrossRef
go back to reference Raithel CJ, Paton PWC, Pooler PS & Golet FC (2011) Assessing long-term population trends of wood frogs using egg-mass counts. Journal of Herpetology 45:23-27CrossRef Raithel CJ, Paton PWC, Pooler PS & Golet FC (2011) Assessing long-term population trends of wood frogs using egg-mass counts. Journal of Herpetology 45:23-27CrossRef
go back to reference Redmer M & Trauth SE (2005) Rana sylvatica LeConte, 1825, Wood Frog. In: Amphibian Declines: The Conservation Status of United States Species, M Lanoo (editor), Los Angeles: University of California Press, pp. 590-593 Redmer M & Trauth SE (2005) Rana sylvatica LeConte, 1825, Wood Frog. In: Amphibian Declines: The Conservation Status of United States Species, M Lanoo (editor), Los Angeles: University of California Press, pp. 590-593
go back to reference Ridenhour BJ & Storfer A (2008) A geographically variable selection in Ambystoma tigrinum virus (Iridoviridae) throughout western United States. Journal of Evolutionary Biology 21:1151-1159CrossRefPubMed Ridenhour BJ & Storfer A (2008) A geographically variable selection in Ambystoma tigrinum virus (Iridoviridae) throughout western United States. Journal of Evolutionary Biology 21:1151-1159CrossRefPubMed
go back to reference Robert J, Morales H, Buck W, Cohen N, Marr S & Gantress J (2005) Adaptive immunity and histopathology in frog virus 3-infected Xenopus. Virology 332:667-675CrossRefPubMed Robert J, Morales H, Buck W, Cohen N, Marr S & Gantress J (2005) Adaptive immunity and histopathology in frog virus 3-infected Xenopus. Virology 332:667-675CrossRefPubMed
go back to reference Rojas S, Richards K, Jancovich JK, Davidson EW (2005) Influence of temperature on Ranavirus infection in larval salamanders Ambystoma tigrinum. Diseases of Aquatic Organisms 63:95–100 Rojas S, Richards K, Jancovich JK, Davidson EW (2005) Influence of temperature on Ranavirus infection in larval salamanders Ambystoma tigrinum. Diseases of Aquatic Organisms 63:95–100
go back to reference Ryder JJ, Miller MR, White A, Knell RJ & Boots M (2007) Host-parasite population dynamics under combined frequency- and density-dependent transmission. Oikos 116:2017-2026CrossRef Ryder JJ, Miller MR, White A, Knell RJ & Boots M (2007) Host-parasite population dynamics under combined frequency- and density-dependent transmission. Oikos 116:2017-2026CrossRef
go back to reference Schock DM, Bollinger TK, Chinchar VG, Jancovich JK & Collins JP (2008) Experimental evidence that amphibian ranaviruses are multi-host pathogens. Copeia 2008:133-143CrossRef Schock DM, Bollinger TK, Chinchar VG, Jancovich JK & Collins JP (2008) Experimental evidence that amphibian ranaviruses are multi-host pathogens. Copeia 2008:133-143CrossRef
go back to reference Skerratt LF, Berger U, Speare R, Cashins S, Mcdonald KR, Phillott AD, Hines HB & Kenyon N (2007) Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth 4:125-134CrossRef Skerratt LF, Berger U, Speare R, Cashins S, Mcdonald KR, Phillott AD, Hines HB & Kenyon N (2007) Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth 4:125-134CrossRef
go back to reference Smith KF, Sax DF & Lafferty KD (2006) Evidence for the role of infectious disease in species extinction and endangerment. Conservation Biology 20:1349-1357CrossRefPubMed Smith KF, Sax DF & Lafferty KD (2006) Evidence for the role of infectious disease in species extinction and endangerment. Conservation Biology 20:1349-1357CrossRefPubMed
go back to reference Storfer A, Alfaro ME, Ridenhour BJ, Jancovich JK, Mech SG, Parris MJ & Collins JP (2007) Phylogenetic concordance analysis shows an emerging pathogen is novel and endemic. Ecology Letters 10:1075-1083CrossRefPubMed Storfer A, Alfaro ME, Ridenhour BJ, Jancovich JK, Mech SG, Parris MJ & Collins JP (2007) Phylogenetic concordance analysis shows an emerging pathogen is novel and endemic. Ecology Letters 10:1075-1083CrossRefPubMed
go back to reference Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues ASL, Fischman DL & Waller RW (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306:1783-1786CrossRefPubMed Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues ASL, Fischman DL & Waller RW (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306:1783-1786CrossRefPubMed
go back to reference Teacher AGF, Cunningham AA & Garner TWJ (2010) Assessing the long-term impact of Ranavirus infection in wild common frog populations. Animal Conservation 13:514-522CrossRef Teacher AGF, Cunningham AA & Garner TWJ (2010) Assessing the long-term impact of Ranavirus infection in wild common frog populations. Animal Conservation 13:514-522CrossRef
go back to reference Teacher AGF, Garner TWJ & Nichols RA (2009) Evidence for directional selection at a novel major histocompatability class I marker in wild common frogs (Rana temporaria) exposed to a viral pathogen (Ranavirus). PLoS One 4:e4616CrossRefPubMedCentralPubMed Teacher AGF, Garner TWJ & Nichols RA (2009) Evidence for directional selection at a novel major histocompatability class I marker in wild common frogs (Rana temporaria) exposed to a viral pathogen (Ranavirus). PLoS One 4:e4616CrossRefPubMedCentralPubMed
go back to reference Todd-Thompson M (2010) Seasonality, Variation in Species Prevalence, and Localized Disease for Ranavirus in Cades Cove (Great Smoky Mountains National Park) Amphibians. M.S., University of Tennessee Todd-Thompson M (2010) Seasonality, Variation in Species Prevalence, and Localized Disease for Ranavirus in Cades Cove (Great Smoky Mountains National Park) Amphibians. M.S., University of Tennessee
go back to reference Vonesh JR & De La Cruz O (2002) Complex life cycles and density dependence: assessing the contribution of egg mortality to amphibian declines. Oecologia 133:325-333CrossRef Vonesh JR & De La Cruz O (2002) Complex life cycles and density dependence: assessing the contribution of egg mortality to amphibian declines. Oecologia 133:325-333CrossRef
go back to reference Vredenburg VT, Knapp RA, Tunstall TS & Briggs CJ (2010) Dynamics of an emerging disease drive large-scale amphibian population extinctions. PNAS 107:9684-9694CrossRef Vredenburg VT, Knapp RA, Tunstall TS & Briggs CJ (2010) Dynamics of an emerging disease drive large-scale amphibian population extinctions. PNAS 107:9684-9694CrossRef
go back to reference Vrijenhoek RC (1994) Genetic diversity and fitness in small populations. In: Conservation Genetics, V Loeschcke, SK Jain & J Tomiuk (editors), Basel, Switzerland: Birkhäuser, pp. 37-53CrossRef Vrijenhoek RC (1994) Genetic diversity and fitness in small populations. In: Conservation Genetics, V Loeschcke, SK Jain & J Tomiuk (editors), Basel, Switzerland: Birkhäuser, pp. 37-53CrossRef
Metadata
Title
Introduction of Ranavirus to Isolated Wood Frog Populations Could Cause Local Extinction
Authors
Julia E. Earl
Matthew J. Gray
Publication date
01-12-2014
Publisher
Springer US
Published in
EcoHealth / Issue 4/2014
Print ISSN: 1612-9202
Electronic ISSN: 1612-9210
DOI
https://doi.org/10.1007/s10393-014-0950-y

Other articles of this Issue 4/2014

EcoHealth 4/2014 Go to the issue