Skip to main content
Erschienen in: EcoHealth 3/2011

01.09.2011 | Original Contribution

Phylogeny, Life History, and Ecology Contribute to Differences in Amphibian Susceptibility to Ranaviruses

verfasst von: Jason T. Hoverman, Matthew J. Gray, Nathan A. Haislip, Debra L. Miller

Erschienen in: EcoHealth | Ausgabe 3/2011

Einloggen, um Zugang zu erhalten

Abstract

Research that identifies the potential host range of generalist pathogens as well as variation in host susceptibility is critical for understanding and predicting the dynamics of infectious diseases within ecological communities. Ranaviruses have been linked to amphibian die-off events worldwide with the greatest number of reported mortality events occurring in the United States. While reports of ranavirus-associated mortality events continue to accumulate, few data exist comparing the relative susceptibility of different species. Using a series of laboratory exposure experiments and comparative phylogenetics, we compared the susceptibilities of 19 amphibian species from two salamander families and five anurans families for two ranavirus isolates: frog virus 3 (FV3) and an FV3-like isolate from an American bullfrog culture facility. We discovered that ranaviruses were capable of infecting 17 of the 19 larval amphibian species tested with mortality ranging from 0 to 100%. Phylogenetic comparative methods demonstrated that species within the anuran family Ranidae were generally more susceptible to ranavirus infection compared to species from the other five families. We also found that susceptibility to infection was associated with species that breed in semi-permanent ponds, develop rapidly as larvae, and have limited range sizes. Collectively, these results suggest that phylogeny, life history characteristics, and habitat associations of amphibians have the potential to impact susceptibility to ranaviruses.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
Zurück zum Zitat Begon M (2008) Effects of host diversity on disease dynamics. In: Infectious Disease Ecology: The Effects of Ecosystems on Disease and of Disease on Ecosystems, Ostfeld R, Keesing F, Eviner VT (editors), Princeton, NJ: Princeton University Press, pp 12–29. Begon M (2008) Effects of host diversity on disease dynamics. In: Infectious Disease Ecology: The Effects of Ecosystems on Disease and of Disease on Ecosystems, Ostfeld R, Keesing F, Eviner VT (editors), Princeton, NJ: Princeton University Press, pp 12–29.
Zurück zum Zitat Blomberg SP, Garland T, and Ives AR (2003). Testing for phylogenetic signal in comparative data: Behavioral traits are more labile. Evolution 57:717-745.PubMed Blomberg SP, Garland T, and Ives AR (2003). Testing for phylogenetic signal in comparative data: Behavioral traits are more labile. Evolution 57:717-745.PubMed
Zurück zum Zitat 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.PubMed 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.PubMed
Zurück zum Zitat Brunner JL, Barnett KE, Gosier CJ, McNulty SA, Rubbo MJ, and 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, and Kolozsvary MB (2011). Ranavirus infection in die-offs of vernal pool amphibians in New York, USA. Herpetological Review 42:76-79.
Zurück zum Zitat Brunner JL, Richards K, and Collins JP (2005). Dose and host characteristics influence virulence of ranavirus infections. Oecologia 144:399-406.PubMedCrossRef Brunner JL, Richards K, and Collins JP (2005). Dose and host characteristics influence virulence of ranavirus infections. Oecologia 144:399-406.PubMedCrossRef
Zurück zum Zitat Brunner JL, Schock DM, and Collins JP (2007). Transmission dynamics of the amphibian ranavirus Ambystoma tigrinum virus. Diseases of Aquatic Organisms 77:87-95.PubMedCrossRef Brunner JL, Schock DM, and Collins JP (2007). Transmission dynamics of the amphibian ranavirus Ambystoma tigrinum virus. Diseases of Aquatic Organisms 77:87-95.PubMedCrossRef
Zurück zum Zitat Bryan L, Baldwin CA, Gray MJ, and Miller DL (2009). Efficacy of select disinfectants at inactivating Ranavirus. Diseases of Aquatic Organisms 84:89-94.PubMedCrossRef Bryan L, Baldwin CA, Gray MJ, and Miller DL (2009). Efficacy of select disinfectants at inactivating Ranavirus. Diseases of Aquatic Organisms 84:89-94.PubMedCrossRef
Zurück zum Zitat Carey C, Bradford DE, Brunner JL, Collins JP, et al. (2003) Biotic factors in amphibian declines. In: Amphibian Declines: An Integrated Analysis of Multiple Stressor Effects. Pensacola, FL: Society of Environmental Toxicology and Chemistry, pp 153–208. Carey C, Bradford DE, Brunner JL, Collins JP, et al. (2003) Biotic factors in amphibian declines. In: Amphibian Declines: An Integrated Analysis of Multiple Stressor Effects. Pensacola, FL: Society of Environmental Toxicology and Chemistry, pp 153–208.
Zurück zum Zitat Collinge SK, and Ray C (2006). Disease ecology: community structure and pathogen dynamics. Oxford University Press. Collinge SK, and Ray C (2006). Disease ecology: community structure and pathogen dynamics. Oxford University Press.
Zurück zum Zitat Conant R, and Collins J (1998). A field guide to reptiles and amphibians of eastern and central North America, 3rd edition. Houghton Mifflin, Boston. Conant R, and Collins J (1998). A field guide to reptiles and amphibians of eastern and central North America, 3rd edition. Houghton Mifflin, Boston.
Zurück zum Zitat 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. 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.
Zurück zum Zitat Craft ME, Hawthorne PL, Packer C, and Dobson AP (2008). Dynamics of a multihost pathogen in a carnivore community. Journal of Animal Ecology 77:1257-1264.PubMedCrossRef Craft ME, Hawthorne PL, Packer C, and Dobson AP (2008). Dynamics of a multihost pathogen in a carnivore community. Journal of Animal Ecology 77:1257-1264.PubMedCrossRef
Zurück zum Zitat Cronin JP, Welsh ME, Dekkers MG, Abercrombie ST, and Mitchell CE (2010). Host physiological phenotype explains pathogen reservoir potential. Ecology Letters 13:1221-1232.PubMedCrossRef Cronin JP, Welsh ME, Dekkers MG, Abercrombie ST, and Mitchell CE (2010). Host physiological phenotype explains pathogen reservoir potential. Ecology Letters 13:1221-1232.PubMedCrossRef
Zurück zum Zitat Cunningham AA, Hyatt AD, Russell P, and Bennett PM (2007). Emerging epidemic diseases of frogs in Britain are dependent on the source of ranavirus agent and the route of exposure. Epidemiology and Infection 135:1200-1212.PubMed Cunningham AA, Hyatt AD, Russell P, and Bennett PM (2007). Emerging epidemic diseases of frogs in Britain are dependent on the source of ranavirus agent and the route of exposure. Epidemiology and Infection 135:1200-1212.PubMed
Zurück zum Zitat 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.PubMedCrossRef 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.PubMedCrossRef
Zurück zum Zitat 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.PubMedCrossRef 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.PubMedCrossRef
Zurück zum Zitat 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.CrossRef 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.CrossRef
Zurück zum Zitat 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.PubMed 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.PubMed
Zurück zum Zitat 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.PubMed 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.PubMed
Zurück zum Zitat Elliot L, Gerhardt HC, and Davidson C (2009). The frogs and toads of North America: A comprehensive guide to their identification, behavior, and calls. Houghton Mifflin Company, Boston, MA. Elliot L, Gerhardt HC, and Davidson C (2009). The frogs and toads of North America: A comprehensive guide to their identification, behavior, and calls. Houghton Mifflin Company, Boston, MA.
Zurück zum Zitat Felsenstein J (1985). Phylogenies and the comparative method. American Naturalist 125:1-15.CrossRef Felsenstein J (1985). Phylogenies and the comparative method. American Naturalist 125:1-15.CrossRef
Zurück zum Zitat Gahl MK, and Calhoun AJK (2008). Landscape setting and risk of Ranavirus mortality events. Biological Conservation 141:2679-2689.CrossRef Gahl MK, and Calhoun AJK (2008). Landscape setting and risk of Ranavirus mortality events. Biological Conservation 141:2679-2689.CrossRef
Zurück zum Zitat 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.PubMedCrossRef 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.PubMedCrossRef
Zurück zum Zitat Garland T, Harvey PH, and Ives AR (1992). Procedures for the analysis of comparative data using phylogenetically independent contrasts. Systematic Biology 41:18-32. Garland T, Harvey PH, and Ives AR (1992). Procedures for the analysis of comparative data using phylogenetically independent contrasts. Systematic Biology 41:18-32.
Zurück zum Zitat Gosner KL (1960). A simplified table for staging anuran embryos and larvae with notes and identification. Herpetologica 16:183-190. Gosner KL (1960). A simplified table for staging anuran embryos and larvae with notes and identification. Herpetologica 16:183-190.
Zurück zum Zitat Granoff A, Came PE, and Rafferty KA (1965). The isolation and properties of viruses from Rana pipiens: Their possible relationship to the renal adenocarcinoma of the leopard frog. Annals of the new York Academy of Science 126:237-255.CrossRef Granoff A, Came PE, and Rafferty KA (1965). The isolation and properties of viruses from Rana pipiens: Their possible relationship to the renal adenocarcinoma of the leopard frog. Annals of the new York Academy of Science 126:237-255.CrossRef
Zurück zum Zitat Gray MJ, Miller DL, and Hoverman JT (2009). Ecology and pathology of amphibian ranaviruses. Diseases of Aquatic Organisms 87:243-266.PubMedCrossRef Gray MJ, Miller DL, and Hoverman JT (2009). Ecology and pathology of amphibian ranaviruses. Diseases of Aquatic Organisms 87:243-266.PubMedCrossRef
Zurück zum Zitat 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.PubMedCrossRef 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.PubMedCrossRef
Zurück zum Zitat 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.PubMedCrossRef 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.PubMedCrossRef
Zurück zum Zitat Haislip NA, Gray MJ, Hoverman JT, and Miller DL (2011). Development and disease: How susceptibility to an emerging pathogen changes through anuran development. Plos One 6:e22307.PubMedCrossRef Haislip NA, Gray MJ, Hoverman JT, and Miller DL (2011). Development and disease: How susceptibility to an emerging pathogen changes through anuran development. Plos One 6:e22307.PubMedCrossRef
Zurück zum Zitat 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.PubMed 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.PubMed
Zurück zum Zitat Harvey PH, and Pagel M (1991). The comparative method in evolutionary biology. Oxford University Press, Oxford. Harvey PH, and Pagel M (1991). The comparative method in evolutionary biology. Oxford University Press, Oxford.
Zurück zum Zitat Hedges SB, Dudley J, and Kumar S (2006). TimeTree: a public knowledge-base of divergence times among organisms. Bioinformatics 22:2971-2972.PubMedCrossRef Hedges SB, Dudley J, and Kumar S (2006). TimeTree: a public knowledge-base of divergence times among organisms. Bioinformatics 22:2971-2972.PubMedCrossRef
Zurück zum Zitat Hillis DM, and Wilcox TP (2005). Phylogeny of the New World true frogs (Rana). Molecular Phylogenetics and Evolution 34:299-314.PubMedCrossRef Hillis DM, and Wilcox TP (2005). Phylogeny of the New World true frogs (Rana). Molecular Phylogenetics and Evolution 34:299-314.PubMedCrossRef
Zurück zum Zitat Houlahan JE, Findlay CS, Meyer AH, Kuzmin SL, and Schmidt BR (2001). Ecology - Global amphibian population declines - Reply. Nature 412:500-500.CrossRef Houlahan JE, Findlay CS, Meyer AH, Kuzmin SL, and Schmidt BR (2001). Ecology - Global amphibian population declines - Reply. Nature 412:500-500.CrossRef
Zurück zum Zitat 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.PubMedCrossRef 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.PubMedCrossRef
Zurück zum Zitat 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.CrossRef 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.CrossRef
Zurück zum Zitat Kerby JL, and Storfer A (2009). Combined Effects of Atrazine and Chlorpyrifos on Susceptibility of the Tiger Salamander to Ambystoma tigrinum Virus. Ecohealth 6:91-98.PubMedCrossRef Kerby JL, and Storfer A (2009). Combined Effects of Atrazine and Chlorpyrifos on Susceptibility of the Tiger Salamander to Ambystoma tigrinum Virus. Ecohealth 6:91-98.PubMedCrossRef
Zurück zum Zitat Lannoo M (2005). Amphibian declines: the conservation status of United States species. University of California Press, Berkeley, California. Lannoo M (2005). Amphibian declines: the conservation status of United States species. University of California Press, Berkeley, California.
Zurück zum Zitat Lemmon EM, Lemmon AR, and Cannatella DC (2007). Geological and climatic forces driving speciation in the continentally distributed trilling chorus frogs (Pseudacris). Evolution 61:2086-2103.PubMedCrossRef Lemmon EM, Lemmon AR, and Cannatella DC (2007). Geological and climatic forces driving speciation in the continentally distributed trilling chorus frogs (Pseudacris). Evolution 61:2086-2103.PubMedCrossRef
Zurück zum Zitat Lochmiller RL, and Deerenberg C (2000). Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88:87-98.CrossRef Lochmiller RL, and Deerenberg C (2000). Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88:87-98.CrossRef
Zurück zum Zitat Martins EP (2004) COMPARE, version 4.6b. Computer programs for the statistical analysis of comparative data. Distributed by the author at http://compare.bio.indiana.edu/. Bloomington, IN: Department of Biology, Indiana University. Martins EP (2004) COMPARE, version 4.6b. Computer programs for the statistical analysis of comparative data. Distributed by the author at http://​compare.​bio.​indiana.​edu/​. Bloomington, IN: Department of Biology, Indiana University.
Zurück zum Zitat Miller DL, Rajeev S, Gray MJ, and Baldwin CA (2007a). Frog virus 3 infection, cultured American bullfrogs. Emerging Infectious Diseases 13:342-343.PubMedCrossRef Miller DL, Rajeev S, Gray MJ, and Baldwin CA (2007a). Frog virus 3 infection, cultured American bullfrogs. Emerging Infectious Diseases 13:342-343.PubMedCrossRef
Zurück zum Zitat Miller MR, White A, and Boots M (2007b). Host life span and the evolution of resistance characteristics. Evolution 61:2-14.PubMedCrossRef Miller MR, White A, and Boots M (2007b). Host life span and the evolution of resistance characteristics. Evolution 61:2-14.PubMedCrossRef
Zurück zum Zitat Morales HD, and Robert J (2007). Characterization of primary and memory CD8 T-cell responses against ranavirus (FV3) in Xenopus laevis. Journal Of Virology 81:2240-2248.PubMedCrossRef Morales HD, and Robert J (2007). Characterization of primary and memory CD8 T-cell responses against ranavirus (FV3) in Xenopus laevis. Journal Of Virology 81:2240-2248.PubMedCrossRef
Zurück zum Zitat Muths E, Gallant AL, Campbell EHC, Battaglin WA, Green DE, Staiger JS, et al. (2006) The Amphibian Research and Monitoring Initiative (ARMI): 5-year Report: U.S. Geological Survey Scientific Investigations Report 2006-5224. Muths E, Gallant AL, Campbell EHC, Battaglin WA, Green DE, Staiger JS, et al. (2006) The Amphibian Research and Monitoring Initiative (ARMI): 5-year Report: U.S. Geological Survey Scientific Investigations Report 2006-5224.
Zurück zum Zitat Ord TJ, and Martins EP (2006). Tracing the origins of signal diversity in anole lizards: phylogenetic approaches to inferring the evolution of complex behaviour. Animal Behaviour 71:1411-1429.CrossRef Ord TJ, and Martins EP (2006). Tracing the origins of signal diversity in anole lizards: phylogenetic approaches to inferring the evolution of complex behaviour. Animal Behaviour 71:1411-1429.CrossRef
Zurück zum Zitat Ostfeld R, Keesing F, and Eviner VT (2008). Infectious disease ecology: the effects of ecosystems on disease and of disease on ecosystems. Princeton University Press, Princeton, N.J. Ostfeld R, Keesing F, and Eviner VT (2008). Infectious disease ecology: the effects of ecosystems on disease and of disease on ecosystems. Princeton University Press, Princeton, N.J.
Zurück zum Zitat Pearman PB, and Garner TWJ (2005). Susceptibility of Italian agile frog populations to an emerging strain of Ranavirus parallels population genetic diversity. Ecology Letters 8:401-408.CrossRef Pearman PB, and Garner TWJ (2005). Susceptibility of Italian agile frog populations to an emerging strain of Ranavirus parallels population genetic diversity. Ecology Letters 8:401-408.CrossRef
Zurück zum Zitat Pearman PB, Garner TWJ, Straub M, and Greber UF (2004). Response of the Italian agile frog (Rana latastei) to a Ranavirus, Frog Virus 3: a model for viral emergence in naïve populations. Journal of Wildlife Diseases 40:660-669.PubMed Pearman PB, Garner TWJ, Straub M, and Greber UF (2004). Response of the Italian agile frog (Rana latastei) to a Ranavirus, Frog Virus 3: a model for viral emergence in naïve populations. Journal of Wildlife Diseases 40:660-669.PubMed
Zurück zum Zitat Pedersen AB, and Fenton A (2007). Emphasizing the ecology in parasite community ecology. Trends in Ecology & Evolution 22:133-139.CrossRef Pedersen AB, and Fenton A (2007). Emphasizing the ecology in parasite community ecology. Trends in Ecology & Evolution 22:133-139.CrossRef
Zurück zum Zitat Petranka JW (1998). Salamanders of the United States and Canada. Smithsonian Institution Press, Washington, DC. Petranka JW (1998). Salamanders of the United States and Canada. Smithsonian Institution Press, Washington, DC.
Zurück zum Zitat 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.CrossRef 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.CrossRef
Zurück zum Zitat 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.CrossRef 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.CrossRef
Zurück zum Zitat 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.PubMed 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.PubMed
Zurück zum Zitat Price T, Lovette IJ, Bermingham E, Gibbs HL, and Richman AD (2000). The imprint of history on communities of North American and Asian warblers. American Naturalist 156:354-367.CrossRef Price T, Lovette IJ, Bermingham E, Gibbs HL, and Richman AD (2000). The imprint of history on communities of North American and Asian warblers. American Naturalist 156:354-367.CrossRef
Zurück zum Zitat Pyke DA, and Thompson JN (1986). Statistical analysis of survival and removal expeiments. Ecology 67:240-245.CrossRef Pyke DA, and Thompson JN (1986). Statistical analysis of survival and removal expeiments. Ecology 67:240-245.CrossRef
Zurück zum Zitat R_Development_Core_Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, http://www.R-project.org. R_Development_Core_Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, http://​www.​R-project.​org.
Zurück zum Zitat Relyea RA (2002). Competitor-induced plasticity in tadpoles: Consequences, cues, and connections to predator-induced plasticity. Ecological Monographs 72:523-540.CrossRef Relyea RA (2002). Competitor-induced plasticity in tadpoles: Consequences, cues, and connections to predator-induced plasticity. Ecological Monographs 72:523-540.CrossRef
Zurück zum Zitat Rigaud T, Perrot-Minnot MJ, and Brown MJF (2010). Parasite and host assemblages: embracing the reality will improve our knowledge of parasite transmission and virulence. Proceedings of the Royal Society B-Biological Sciences 277:3693-3702.CrossRef Rigaud T, Perrot-Minnot MJ, and Brown MJF (2010). Parasite and host assemblages: embracing the reality will improve our knowledge of parasite transmission and virulence. Proceedings of the Royal Society B-Biological Sciences 277:3693-3702.CrossRef
Zurück zum Zitat Schock D, Bollinger TK, and Collins JP (2009). Mortality rates differ among amphibian populations exposed to three strains of a lethal ranavirus. Ecohealth 6:438-448.PubMedCrossRef Schock D, Bollinger TK, and Collins JP (2009). Mortality rates differ among amphibian populations exposed to three strains of a lethal ranavirus. Ecohealth 6:438-448.PubMedCrossRef
Zurück zum Zitat 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, 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.
Zurück zum Zitat Schock DM, Bollinger TK, Chinchar VG, Jancovich JK, Collins JP (2008) Experimental evidence that amphibian ranaviruses are multi-host pathogens. Copeia 133–143. Schock DM, Bollinger TK, Chinchar VG, Jancovich JK, Collins JP (2008) Experimental evidence that amphibian ranaviruses are multi-host pathogens. Copeia 133–143.
Zurück zum Zitat Searle CL, Gervasi SS, Hua J, Hammond JI, Relyea RA, Olson DH, et al. (2011). Differential host susceptibility to Batrachochytrium dendrobatidis, an emerging amphibian pathogen. Conservation Biology 25(1):965–974.PubMedCrossRef Searle CL, Gervasi SS, Hua J, Hammond JI, Relyea RA, Olson DH, et al. (2011). Differential host susceptibility to Batrachochytrium dendrobatidis, an emerging amphibian pathogen. Conservation Biology 25(1):965–974.PubMedCrossRef
Zurück zum Zitat Shaffer HB, Clark JM, and Kraus F (1991). When molecules and morphology clash - A phylogenetic analysis of the North American ambystomatid salamanders (Caudata, Ambystomatidae). Systematic Zoology 40:284-303.CrossRef Shaffer HB, Clark JM, and Kraus F (1991). When molecules and morphology clash - A phylogenetic analysis of the North American ambystomatid salamanders (Caudata, Ambystomatidae). Systematic Zoology 40:284-303.CrossRef
Zurück zum Zitat Stephens PR, and Wiens JJ (2004). Convergence, divergence, and homogenization in the ecological structure of emydid turtle communities: the effects of phylogeny and dispersal. American Naturalist 164:244-254.PubMedCrossRef Stephens PR, and Wiens JJ (2004). Convergence, divergence, and homogenization in the ecological structure of emydid turtle communities: the effects of phylogeny and dispersal. American Naturalist 164:244-254.PubMedCrossRef
Zurück zum Zitat Stephens PR, and Wiens JJ (2008). Testing for evolutionary trade-offs in a phylogenetic context: ecological diversification and evolution of locomotor performance in emydid turtles. Journal of Evolutionary Biology 21:77-87.PubMed Stephens PR, and Wiens JJ (2008). Testing for evolutionary trade-offs in a phylogenetic context: ecological diversification and evolution of locomotor performance in emydid turtles. Journal of Evolutionary Biology 21:77-87.PubMed
Zurück zum Zitat 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.PubMedCrossRef 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.PubMedCrossRef
Zurück zum Zitat Telfer S, Birtles R, Bennett M, Lambin X, Paterson S, and Begon M (2008). Parasite interactions in natural populations: insights from longitudinal data. Parasitology 135:767-781.PubMedCrossRef Telfer S, Birtles R, Bennett M, Lambin X, Paterson S, and Begon M (2008). Parasite interactions in natural populations: insights from longitudinal data. Parasitology 135:767-781.PubMedCrossRef
Zurück zum Zitat 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.PubMedCrossRef 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.PubMedCrossRef
Zurück zum Zitat 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.PubMed 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.PubMed
Zurück zum Zitat Wake DB, and Vredenburg VT (2008). 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.CrossRef Wake DB, and Vredenburg VT (2008). 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.CrossRef
Zurück zum Zitat Warne RW, Crespi EJ, and Brunner JL (2011). Escape from the pond: stress and developmental responses to ranavirus infection in wood frog tadpoles. Functional Ecology 25:139-146.CrossRef Warne RW, Crespi EJ, and Brunner JL (2011). Escape from the pond: stress and developmental responses to ranavirus infection in wood frog tadpoles. Functional Ecology 25:139-146.CrossRef
Zurück zum Zitat 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.CrossRef 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.CrossRef
Zurück zum Zitat Wells KD (2007). The ecology and behavior of amphibians. The University of Chicago Press, Chicago. Wells KD (2007). The ecology and behavior of amphibians. The University of Chicago Press, Chicago.
Zurück zum Zitat Werner EE, Skelly DK, Relyea RA, and Yurewicz KL (2007a). Amphibian species richness across environmental gradients. Oikos 116:1697-1712.CrossRef Werner EE, Skelly DK, Relyea RA, and Yurewicz KL (2007a). Amphibian species richness across environmental gradients. Oikos 116:1697-1712.CrossRef
Zurück zum Zitat Werner EE, Yurewicz KL, Skelly DK, and Relyea RA (2007b). Turnover in an amphibian metacommunity: the role of local and regional factors. Oikos 116:1713-1725.CrossRef Werner EE, Yurewicz KL, Skelly DK, and Relyea RA (2007b). Turnover in an amphibian metacommunity: the role of local and regional factors. Oikos 116:1713-1725.CrossRef
Zurück zum Zitat Wiens JJ, Fetzner JW, Parkinson CL, and Reeder TW (2005). Hylid frog phylogeny and sampling strategies for speciose clades. Systematic Biology 54:719-748.CrossRef Wiens JJ, Fetzner JW, Parkinson CL, and Reeder TW (2005). Hylid frog phylogeny and sampling strategies for speciose clades. Systematic Biology 54:719-748.CrossRef
Zurück zum Zitat Woolhouse MEJ, and Gowtage-Sequeria S (2005). Host range and emerging and reemerging pathogens. Emerging Infectious Diseases 11:1842-1847.PubMedCrossRef Woolhouse MEJ, and Gowtage-Sequeria S (2005). Host range and emerging and reemerging pathogens. Emerging Infectious Diseases 11:1842-1847.PubMedCrossRef
Zurück zum Zitat Zuk M, and Stoehr AM (2002). Immune defense and host life history. American Naturalist 160:S9-S22.PubMedCrossRef Zuk M, and Stoehr AM (2002). Immune defense and host life history. American Naturalist 160:S9-S22.PubMedCrossRef
Metadaten
Titel
Phylogeny, Life History, and Ecology Contribute to Differences in Amphibian Susceptibility to Ranaviruses
verfasst von
Jason T. Hoverman
Matthew J. Gray
Nathan A. Haislip
Debra L. Miller
Publikationsdatum
01.09.2011
Verlag
Springer-Verlag
Erschienen in
EcoHealth / Ausgabe 3/2011
Print ISSN: 1612-9202
Elektronische ISSN: 1612-9210
DOI
https://doi.org/10.1007/s10393-011-0717-7

Weitere Artikel der Ausgabe 3/2011

EcoHealth 3/2011 Zur Ausgabe

What's New

What’s New