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Published in: EcoHealth 2/2013

01-06-2013 | Original Contribution

Natural Stressors and Ranavirus Susceptibility in Larval Wood Frogs (Rana sylvatica)

Authors: Brooke C. Reeve, Erica J. Crespi, Christopher M. Whipps, Jesse L. Brunner

Published in: EcoHealth | Issue 2/2013

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Abstract

Chronic exposure to stressors has been shown to suppress immune function in vertebrates, making them more susceptible to pathogens. It is less clear, however, whether many natural stressors are immunosuppressive. Moreover, whether stressors make disease more likely or more severe in populations is unclear because animals respond to stressors both behaviorally and physiologically. We tested whether chronic exposure to three natural stressors of wood frog tadpoles—high-densities, predator-cues, and low-food conditions—influence their susceptibility to a lethal ranavirus both individually in laboratory experiments, and collectively in outdoor mesocosms. Prior to virus exposure, we observed elevated corticosterone only in low-food treatments, although other treatments altered rates of growth and development as well as tadpole behavior. None of the treatments, however, increased susceptibility to ranavirus as measured by the proportion of tadpoles that became infected or died, or the time to death compared to controls. In fact, mortality in the mesocosms was actually lower in the high-density treatment even though most individuals became infected, largely because of increased rates of metamorphosis. Overall we find no support for the hypothesis that chronic exposure to common, ecologically relevant challenges necessarily elevates corticosterone levels in a population or leads to more severe ranaviral disease or epidemics. Conditions may, however, conspire to make ranavirus infection more common in metamorphosing amphibians.
Literature
go back to reference Acevedo-Whitehouse KA, Duffus A (2009) Effects of environmental change on wildlife health. Philosophical Transactions of the Royal Society B 364:3429-3438CrossRef Acevedo-Whitehouse KA, Duffus A (2009) Effects of environmental change on wildlife health. Philosophical Transactions of the Royal Society B 364:3429-3438CrossRef
go back to reference Belden LK, Kiesecker JM (2005) Glucocorticosteroid hormone treatment of larval treefrogs increases infection by Alaria sp. trematode cercariae. Journal of Parasitology 91(3):686-688PubMedCrossRef Belden LK, Kiesecker JM (2005) Glucocorticosteroid hormone treatment of larval treefrogs increases infection by Alaria sp. trematode cercariae. Journal of Parasitology 91(3):686-688PubMedCrossRef
go back to reference Belden LK, Wojdak JM (2011) The combined influence of trematode parasites and predatory salamanders on wood frog (Rana sylvatica) tadpoles. Oecologia 166:1077-1086PubMedCrossRef Belden LK, Wojdak JM (2011) The combined influence of trematode parasites and predatory salamanders on wood frog (Rana sylvatica) tadpoles. Oecologia 166:1077-1086PubMedCrossRef
go back to reference Belden LK, Rubbo MJ, Wingfield JC, Kiesecker JM (2007) Searching for the physiological mechanism of density-dependence: Does corticosterone regulate tadpole responses to density? Physiological and Biochemical Zoology 80(4):444-451PubMedCrossRef Belden LK, Rubbo MJ, Wingfield JC, Kiesecker JM (2007) Searching for the physiological mechanism of density-dependence: Does corticosterone regulate tadpole responses to density? Physiological and Biochemical Zoology 80(4):444-451PubMedCrossRef
go back to reference Boonstra R, Hik D, Singleton GR, Tinnikov A (1998) The impact of predator-induced stress on the snowshoe hare cycle. Ecological Monographs 68: 371–394CrossRef Boonstra R, Hik D, Singleton GR, Tinnikov A (1998) The impact of predator-induced stress on the snowshoe hare cycle. Ecological Monographs 68: 371–394CrossRef
go back to reference Bosch J, Martínez-Solano I, Garcia-Paris M (2001) Evidence of a chytrid fungus infection involved in the decline of the common midwife toad (Alytes obstetricans) in protected areas in central Spain. Biological Conservation 97(3):331-337CrossRef Bosch J, Martínez-Solano I, Garcia-Paris M (2001) Evidence of a chytrid fungus infection involved in the decline of the common midwife toad (Alytes obstetricans) in protected areas in central Spain. Biological Conservation 97(3):331-337CrossRef
go back to reference Brunner JL, Collins JC (2009) Testing assumptions of the trade-off theory of the evolution of parasite virulence. Evolutionary Ecology Research 11:1169–1188 Brunner JL, Collins JC (2009) Testing assumptions of the trade-off theory of the evolution of parasite virulence. Evolutionary Ecology Research 11:1169–1188
go back to reference Brunner JL, Schock DM, Collins JP (2007) Transmission dynamics of the amphibian ranavirus Ambystoma tigrinum virus. Diseases of Aquatic Organisms 77:87-95PubMedCrossRef Brunner JL, Schock DM, Collins JP (2007) Transmission dynamics of the amphibian ranavirus Ambystoma tigrinum virus. Diseases of Aquatic Organisms 77:87-95PubMedCrossRef
go back to reference Brunner JL, Schock DM, Collins JP Davidson EW (2004) The role of an intraspecific reservoir in the persistence of a lethal ranavirus. Ecology 85(2):560-566CrossRef Brunner JL, Schock DM, Collins JP Davidson EW (2004) The role of an intraspecific reservoir in the persistence of a lethal ranavirus. Ecology 85(2):560-566CrossRef
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 Carey C, Cohen N, Rollins-Smith L (1999) Amphibian declines: An immunological perspective. Developmental and Comparative Immunology 23(6):459-472PubMedCrossRef Carey C, Cohen N, Rollins-Smith L (1999) Amphibian declines: An immunological perspective. Developmental and Comparative Immunology 23(6):459-472PubMedCrossRef
go back to reference Chinenov Y, Rogatsky I (2007) Glucocorticoids and the innate immune system: crosstalk with the toll-like receptor signaling network. Molecular and Cellular Endocrinology 275(1-2):30-42PubMedCrossRef Chinenov Y, Rogatsky I (2007) Glucocorticoids and the innate immune system: crosstalk with the toll-like receptor signaling network. Molecular and Cellular Endocrinology 275(1-2):30-42PubMedCrossRef
go back to reference Collins JP, Storfer A (2003) Global amphibian declines: Sorting the hypotheses. Diversity and Distributions 9(2): 89-98CrossRef Collins JP, Storfer A (2003) Global amphibian declines: Sorting the hypotheses. Diversity and Distributions 9(2): 89-98CrossRef
go back to reference Crespi EJ, Denver RJ (2005) Roles of stress hormones in food intake regulation in anuran amphibians throughout the life cycle. Comparative Biochemistry and Physiology 141(4):381-390PubMedCrossRef Crespi EJ, Denver RJ (2005) Roles of stress hormones in food intake regulation in anuran amphibians throughout the life cycle. Comparative Biochemistry and Physiology 141(4):381-390PubMedCrossRef
go back to reference Dahl E, Orizoala G, Winberg S, Laurila A (2012) Geographic variation in corticosterone response to chronic predator stress in tadpoles. Journal of Evolutionary Biology 25:1066–1076PubMedCrossRef Dahl E, Orizoala G, Winberg S, Laurila A (2012) Geographic variation in corticosterone response to chronic predator stress in tadpoles. Journal of Evolutionary Biology 25:1066–1076PubMedCrossRef
go back to reference Daszak P, Cunningham AA, Hyatt AD (2001) Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Tropica 78(2):103-116PubMedCrossRef Daszak P, Cunningham AA, Hyatt AD (2001) Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Tropica 78(2):103-116PubMedCrossRef
go back to reference Davis RL, Lochmiller RL, Warde WD (1995) Spleenocyte subpopulations of weanling cotton rats (Sigmodon hispidus) are influenced by moderate protein intake. Journal of Mammalogy 76(3):912-924CrossRef Davis RL, Lochmiller RL, Warde WD (1995) Spleenocyte subpopulations of weanling cotton rats (Sigmodon hispidus) are influenced by moderate protein intake. Journal of Mammalogy 76(3):912-924CrossRef
go back to reference Demas GE (2010) In vivo but not in vitro leptin enhances lymphocyte proliferation in Siberian hamsters (Phodopus sungorus). General and Comparative Endocrinology 166(2)314-319PubMedCrossRef Demas GE (2010) In vivo but not in vitro leptin enhances lymphocyte proliferation in Siberian hamsters (Phodopus sungorus). General and Comparative Endocrinology 166(2)314-319PubMedCrossRef
go back to reference Denver RJ, Glennemeier KA, Boorse GC (2002) Endocrinology of complex life cycles: Amphibians. In: Hormones, brain and behavior, Pfaff D, Arnold A, Etgen A, Fahrbach S, Moss R, Rubin R (editors), San Diego: Academic Press, Inc., pp 469-513CrossRef Denver RJ, Glennemeier KA, Boorse GC (2002) Endocrinology of complex life cycles: Amphibians. In: Hormones, brain and behavior, Pfaff D, Arnold A, Etgen A, Fahrbach S, Moss R, Rubin R (editors), San Diego: Academic Press, Inc., pp 469-513CrossRef
go back to reference Dhabhar F S (2002) Stress-induced augmentation of immune function—the role of stress hormones, leukocyte trafficking, and cytokines. Brain, Behavior, and Immunity 16(6):785-798PubMedCrossRef Dhabhar F S (2002) Stress-induced augmentation of immune function—the role of stress hormones, leukocyte trafficking, and cytokines. Brain, Behavior, and Immunity 16(6):785-798PubMedCrossRef
go back to reference Dhabhar FS (2009) Enhancing versus suppressive effects of stress on immune function: Implications for immunoprotection and immunopathology. Neuroimmunomodulation 16(5)300-317PubMedCrossRef Dhabhar FS (2009) Enhancing versus suppressive effects of stress on immune function: Implications for immunoprotection and immunopathology. Neuroimmunomodulation 16(5)300-317PubMedCrossRef
go back to reference Echaubard P, Little K, Pauli B, Lesbarrères D (2010) Context-dependent effects of ranaviral infection on northern leopard frog life history traits. PLoS ONE 5(10):e13723PubMedCrossRef Echaubard P, Little K, Pauli B, Lesbarrères D (2010) Context-dependent effects of ranaviral infection on northern leopard frog life history traits. PLoS ONE 5(10):e13723PubMedCrossRef
go back to reference Elenkov IJ, Chrousos GP (1999) Stress hormones, Th1/Th2 patterns, pro/anti-inflammatory cytokines and susceptibility to disease. Trends in Endocrinology and Metabolism 10(9):359-368PubMedCrossRef Elenkov IJ, Chrousos GP (1999) Stress hormones, Th1/Th2 patterns, pro/anti-inflammatory cytokines and susceptibility to disease. Trends in Endocrinology and Metabolism 10(9):359-368PubMedCrossRef
go back to reference Forson DD, Storfer A (2006) Atrazine increases ranavirus susceptibility in the tiger salamander, Ambystoma tigrinum. Ecological Applications 16:2325–2332PubMedCrossRef Forson DD, Storfer A (2006) Atrazine increases ranavirus susceptibility in the tiger salamander, Ambystoma tigrinum. Ecological Applications 16:2325–2332PubMedCrossRef
go back to reference Fraker ME, Hu F, Cuddapah V, McCollum SA, Relyea RA, Hempel J, et al. (2009) Characterization of an alarm pheromone secreted by amphibian tadpoles that induces behavioral inhibition and suppression of the neuroendocrine stress axis. Hormones and Behavior 55(4):520-529PubMedCrossRef Fraker ME, Hu F, Cuddapah V, McCollum SA, Relyea RA, Hempel J, et al. (2009) Characterization of an alarm pheromone secreted by amphibian tadpoles that induces behavioral inhibition and suppression of the neuroendocrine stress axis. Hormones and Behavior 55(4):520-529PubMedCrossRef
go back to reference Glennemeier KA, Denver RJ (2002) Role for corticoids in mediating the response of Rana pipiens tadpoles to intraspecific competition. Journal of Experimental Zoology 292(1):32-40PubMedCrossRef Glennemeier KA, Denver RJ (2002) Role for corticoids in mediating the response of Rana pipiens tadpoles to intraspecific competition. Journal of Experimental Zoology 292(1):32-40PubMedCrossRef
go back to reference Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183-190 Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183-190
go back to reference Gray MJ, Miller DL, Hoverman JT (2009) Ecology and pathology of amphibian ranaviruses. Diseases of Aquatic Organisms 87(3):243-266PubMedCrossRef Gray MJ, Miller DL, Hoverman JT (2009) Ecology and pathology of amphibian ranaviruses. Diseases of Aquatic Organisms 87(3):243-266PubMedCrossRef
go back to reference Haddad J, Saadé N, Safieh-Garabedian B (2002) Cytokines and neuro-immune-endocrine interactions: a role for the hypothalamic-pituitary-adrenal revolving axis. Journal of Neuroimmunology 133:1-19PubMedCrossRef Haddad J, Saadé N, Safieh-Garabedian B (2002) Cytokines and neuro-immune-endocrine interactions: a role for the hypothalamic-pituitary-adrenal revolving axis. Journal of Neuroimmunology 133:1-19PubMedCrossRef
go back to reference Haislip NA, Hoverman JT, Miller DL, Gray MJ (2012) Natural stressors and disease risk: does the threat of predation increase amphibian susceptibility to ranavirus? Canadian Journal of Zoology 90:893-902CrossRef Haislip NA, Hoverman JT, Miller DL, Gray MJ (2012) Natural stressors and disease risk: does the threat of predation increase amphibian susceptibility to ranavirus? Canadian Journal of Zoology 90:893-902CrossRef
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(2):307-318PubMed Harp EM, Petranka JW (2006) Ranavirus in wood frogs (Rana sylvatica): Potential sources of transmission within and between ponds. Journal of Wildlife Diseases 42(2):307-318PubMed
go back to reference Hopkins WA, DuRant SE (2011) Innate immunity and stress physiology of eastern hellbenders (Cryptobranchus alleganiensis) from two stream reaches with differing habitat quality. General and Comparative Endocrinology 174:107-115PubMedCrossRef Hopkins WA, DuRant SE (2011) Innate immunity and stress physiology of eastern hellbenders (Cryptobranchus alleganiensis) from two stream reaches with differing habitat quality. General and Comparative Endocrinology 174:107-115PubMedCrossRef
go back to reference Kerby JL, Hart AJ. Storfer A (2011) Combined effects of virus, pesticide, and predator cue on the larval tiger salamander (Ambystoma tigrinum). EcoHealth, 8(1):46-54PubMedCrossRef Kerby JL, Hart AJ. Storfer A (2011) Combined effects of virus, pesticide, and predator cue on the larval tiger salamander (Ambystoma tigrinum). EcoHealth, 8(1):46-54PubMedCrossRef
go back to reference Koprivnikar J (2010) Interactions of environmental stressors impact survival and development of parasitized larval amphibians. Ecological Applications 20(8):2263-2272PubMedCrossRef Koprivnikar J (2010) Interactions of environmental stressors impact survival and development of parasitized larval amphibians. Ecological Applications 20(8):2263-2272PubMedCrossRef
go back to reference Ledon-Rettig CC, Pfennig DW,Crespi EJ (2009) Stress hormones and the fitness consequences associated with the transition to a novel diet in larval amphibians. The Journal of Experimental Biology 212:3743-3750PubMedCrossRef Ledon-Rettig CC, Pfennig DW,Crespi EJ (2009) Stress hormones and the fitness consequences associated with the transition to a novel diet in larval amphibians. The Journal of Experimental Biology 212:3743-3750PubMedCrossRef
go back to reference Lochmiller RL, Vestey MR, Boren JC (1993) Relationship between protein nutritional status and immunocompetence in Northern bobwhite chicks. The Auk 110(3):503-510CrossRef Lochmiller RL, Vestey MR, Boren JC (1993) Relationship between protein nutritional status and immunocompetence in Northern bobwhite chicks. The Auk 110(3):503-510CrossRef
go back to reference Mao J, Green DE, Fellers G, Chinchar VG (1999) Molecular characterization of iridoviruses isolated from sympatric amphibians and fish. Virus Research 63(1-2):45-52PubMedCrossRef Mao J, Green DE, Fellers G, Chinchar VG (1999) Molecular characterization of iridoviruses isolated from sympatric amphibians and fish. Virus Research 63(1-2):45-52PubMedCrossRef
go back to reference Martin LB (2009) Stress and immunity in wild vertebrates: Timing is everything. General and Comparative Endocrinology 163(1-2):70-76PubMedCrossRef Martin LB (2009) Stress and immunity in wild vertebrates: Timing is everything. General and Comparative Endocrinology 163(1-2):70-76PubMedCrossRef
go back to reference Martin LB, Hopkins WA, Mydlarz LD, Rohr JR (2010) The effects of anthropogenic global changes on immune functions and disease resistance. Annals of the New York Academy of Sciences 1195:129-148PubMedCrossRef Martin LB, Hopkins WA, Mydlarz LD, Rohr JR (2010) The effects of anthropogenic global changes on immune functions and disease resistance. Annals of the New York Academy of Sciences 1195:129-148PubMedCrossRef
go back to reference McCallum H, Barlow N, Hone J (2001) How should pathogen transmission be modelled? Trends in Ecology and Evolution 16(6):295-300PubMedCrossRef McCallum H, Barlow N, Hone J (2001) How should pathogen transmission be modelled? Trends in Ecology and Evolution 16(6):295-300PubMedCrossRef
go back to reference McEwen BS, Wingfield JC (2003) The concept of allostasis in biology and biomedicine. Hormones and Behavior 43:2-15PubMedCrossRef McEwen BS, Wingfield JC (2003) The concept of allostasis in biology and biomedicine. Hormones and Behavior 43:2-15PubMedCrossRef
go back to reference Moore JA (1939) Temperature tolerance and rates of development in the eggs of Amphibia. Ecology 20(4):459-478CrossRef Moore JA (1939) Temperature tolerance and rates of development in the eggs of Amphibia. Ecology 20(4):459-478CrossRef
go back to reference Nain S, Bour A, Chalmers C, Smits J (2011) Immunotoxicity and disease resistance in Japanese quail (Corturnix corturnix japonica) exposed to malathion. Ecotoxicology 20(4):892-900PubMedCrossRef Nain S, Bour A, Chalmers C, Smits J (2011) Immunotoxicity and disease resistance in Japanese quail (Corturnix corturnix japonica) exposed to malathion. Ecotoxicology 20(4):892-900PubMedCrossRef
go back to reference Pickering AD. Pottinger TG (1989) Stress responses and disease resistance in salmonid fish: Effects of chronic elevation of plasma cortisol. Fish Physiology and Biochemistry, 7(1-6):253-258CrossRef Pickering AD. Pottinger TG (1989) Stress responses and disease resistance in salmonid fish: Effects of chronic elevation of plasma cortisol. Fish Physiology and Biochemistry, 7(1-6):253-258CrossRef
go back to reference Plowright RK, Sokolow SK, Gorman ME, Daszak P, Foley JE (2008) Causal inference in disease ecology: Investigating ecological drivers of disease emergence. Frontiers in Ecology and the Environment, 6(8):420-429CrossRef Plowright RK, Sokolow SK, Gorman ME, Daszak P, Foley JE (2008) Causal inference in disease ecology: Investigating ecological drivers of disease emergence. Frontiers in Ecology and the Environment, 6(8):420-429CrossRef
go back to reference Raffel TR, Hoverman JT, Halstead NT, Michel PJ, Rohr JR (2010) Parasitism in a community context: Trait-mediated interactions with competition and predation. Ecology 91(7):1900-1907PubMedCrossRef Raffel TR, Hoverman JT, Halstead NT, Michel PJ, Rohr JR (2010) Parasitism in a community context: Trait-mediated interactions with competition and predation. Ecology 91(7):1900-1907PubMedCrossRef
go back to reference Relyea RA (2002) Competitor-induced plasticity in tadpoles: consequences, cues, and connections to predator-induced plasticity. Ecological Monographs 72(4):523-540CrossRef Relyea RA (2002) Competitor-induced plasticity in tadpoles: consequences, cues, and connections to predator-induced plasticity. Ecological Monographs 72(4):523-540CrossRef
go back to reference Robert J (2010) Emerging ranaviral infectious diseases and amphibian decline. Diversity 2(3):314-330CrossRef Robert J (2010) Emerging ranaviral infectious diseases and amphibian decline. Diversity 2(3):314-330CrossRef
go back to reference Rollins-Smith LA (1998) Metamorphosis and the amphibian immune system. Immunological Reviews 166:221-230PubMedCrossRef Rollins-Smith LA (1998) Metamorphosis and the amphibian immune system. Immunological Reviews 166:221-230PubMedCrossRef
go back to reference Rot-Nikcevic I, Denver RJ, Wassersug RJ (2005) The influence of visual and tactile stimulation on growth and metamorphosis in anuran larvae. Functional Ecology 19:1008-1016CrossRef Rot-Nikcevic I, Denver RJ, Wassersug RJ (2005) The influence of visual and tactile stimulation on growth and metamorphosis in anuran larvae. Functional Ecology 19:1008-1016CrossRef
go back to reference Sambrook J, Russell DW (2001) Molecular Cloning: A laboratory manual, 3rd ed., New York: Cold Spring Harbor Laboratory Press Sambrook J, Russell DW (2001) Molecular Cloning: A laboratory manual, 3rd ed., New York: Cold Spring Harbor Laboratory Press
go back to reference Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews 21(1):55-89PubMedCrossRef Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews 21(1):55-89PubMedCrossRef
go back to reference Sheridan JF, Dobbs C, Brown D, Zwilling B (1994) Psychoneuroimmunology: Stress effects on pathogenesis and immunity during infection. Clinical Microbiology Reviews 7(2):200-212PubMed Sheridan JF, Dobbs C, Brown D, Zwilling B (1994) Psychoneuroimmunology: Stress effects on pathogenesis and immunity during infection. Clinical Microbiology Reviews 7(2):200-212PubMed
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(5):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(5):514-522CrossRef
go back to reference Van Buskirk J (2001) Specific induced responses to different predator species in anuran larvae. Journal of Evolutionary Biology 14:482-489CrossRef Van Buskirk J (2001) Specific induced responses to different predator species in anuran larvae. Journal of Evolutionary Biology 14:482-489CrossRef
go back to reference Venesky MD, Wilcoxen TE, Rensel MA, Rollins-Smith L, Kirby JL, Parris MJ (2012) Dietary protein restriction impairs growth, immunity, and disease resistance in southern leopard frog tadpoles. Oecologia 169:23-31PubMedCrossRef Venesky MD, Wilcoxen TE, Rensel MA, Rollins-Smith L, Kirby JL, Parris MJ (2012) Dietary protein restriction impairs growth, immunity, and disease resistance in southern leopard frog tadpoles. Oecologia 169:23-31PubMedCrossRef
go back to reference Warne RW, Crespi EJ, Brunner JL (2011) Escape from the pond: Stress and developmental responses to ranavirus infection in wood frog tadpoles. Functional Ecology 25(1):139-146CrossRef Warne RW, Crespi EJ, Brunner JL (2011) Escape from the pond: Stress and developmental responses to ranavirus infection in wood frog tadpoles. Functional Ecology 25(1):139-146CrossRef
go back to reference Webster Marketon JI, Glaser R (2008) Stress hormones and immune function. Cellular Immunology 252(1–2):16–26PubMedCrossRef Webster Marketon JI, Glaser R (2008) Stress hormones and immune function. Cellular Immunology 252(1–2):16–26PubMedCrossRef
go back to reference Werner EE (1992) Competitive interactions between wood frog and northern leopard frog larvae: The influence of size and activity. Copeia 1992(1):26–35CrossRef Werner EE (1992) Competitive interactions between wood frog and northern leopard frog larvae: The influence of size and activity. Copeia 1992(1):26–35CrossRef
go back to reference Wingfield JC, Moore MC, Farner DS (1983) Endocrine responses to inclement weather in naturally breeding populations of white-crowned sparrows (Zonotrichia leucophrys pugetensis). The Auk 100:56-62 Wingfield JC, Moore MC, Farner DS (1983) Endocrine responses to inclement weather in naturally breeding populations of white-crowned sparrows (Zonotrichia leucophrys pugetensis). The Auk 100:56-62
Metadata
Title
Natural Stressors and Ranavirus Susceptibility in Larval Wood Frogs (Rana sylvatica)
Authors
Brooke C. Reeve
Erica J. Crespi
Christopher M. Whipps
Jesse L. Brunner
Publication date
01-06-2013
Publisher
Springer-Verlag
Published in
EcoHealth / Issue 2/2013
Print ISSN: 1612-9202
Electronic ISSN: 1612-9210
DOI
https://doi.org/10.1007/s10393-013-0834-6

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