Antipredator behavior of chytridiomycosis-infected northern leopard frog (Rana pipiens) tadpoles

We investigated the effects of Batrachochytrium dendrobatidis Longcore, Pessier & Nichols, a pathogen implicated in global amphibian population declines, on antipredator behavior of northern leopard frog (Rana pipiens Schreber, 1782) tadpoles in response to visual and chemical cues of a fish predator, bluegill sunfish (Lepomis macrochirus Rafinesque, 1819). We placed infected and uninfected tadpoles in containers partitioned with a transparent divider and measured tadpole activity and distance from the center. Infected tadpoles had significantly lower activity levels across all treatments. When exposed to only visual cues, uninfected tadpoles positioned themselves farther from the center divider (and thus the predator) than infected animals. All tadpoles were at similar distances from the center when exposed to chemical cues only, likely because chemical cues alone do not provide spatial information on the location of predators. Infected tadpoles were significantly farther from the center divider than uni...

[1]  M. Parris,et al.  Interactive Effects of a Heavy Metal and Chytridiomycosis on Gray Treefrog Larvae (Hyla chrysoscelis) , 2004, Copeia.

[2]  J. Kiesecker,et al.  EFFECTS OF DISEASE AND POND DRYING ON GRAY TREE FROG GROWTH, DEVELOPMENT, AND SURVIVAL , 2001 .

[3]  D. Skelly.  Activity level and the susceptibility of anuran larvae to predation , 1994, Animal Behaviour.

[4]  R. Vilgalys,et al.  Multilocus sequence typing suggests the chytrid pathogen of amphibians is a recently emerged clone , 2003, Molecular ecology.

[5]  A. Nicieza.  Interacting effects of predation risk and food availability on larval anuran behaviour and development , 2000, Oecologia.

[6]  B. Woodward,et al.  Predator-prey interactions and breeding-pond use of temporary-pond species in a desert anuran community , 1983 .

[7]  C. Carey,et al.  Amphibian declines: an immunological perspective. , 1999, Developmental and comparative immunology.

[8]  E. Werner,et al.  Behavioral and Life‐Historical Responses of Larval American Toads to an Odonate Predator , 1990 .

[9]  A. Sih.  Evolution, Predator Avoidance, and Unsuccessful Predation , 1985, The American Naturalist.

[10]  E. Werner,et al.  Influence of Forest Canopy Cover on the Breeding Pond Distributions of Several Amphibian Species , 1999 .

[11]  A. Dobson,et al.  The Population Biology of Parasite-Induced Changes in Host Behavior , 1988, The Quarterly Review of Biology.

[12]  R. Wassersug,et al.  Patterns and consequences of behavioural responses to predators and parasites in Rana tadpoles , 2000 .

[13]  K. Lips,et al.  Chytridiomycosis in Wild Frogs from Southern Costa Rica , 2003 .

[14]  E. Levri,et al.  Parasite-induced change in host behavior of a freshwater snail: parasitic manipulation or byproduct of infection? , 1999 .

[15]  P. Daszak,et al.  Perspectives Perspectives Perspectives Perspectives Perspectives Amphibian Population Declines Emerging Infectious Diseases and Amphibian Population Declines , 2022 .

[16]  L. Real.  Sustainability and the Ecology of Infectious Disease Diseases and their pathogenic agents must be viewed as important parts of any ecosystem management strategy , 1996 .

[17]  K. Beard,et al.  Behavioral reduction of infection risk. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[18]  P. Daszak,et al.  Infectious disease and amphibian population declines , 2003 .

[19]  M. Parris.  Hybridization in leopard frogs (Rana pipiens complex): terrestrial performance of newly metamorphosed hybrid and parental genotypes in field enclosures , 2001 .

[20]  J. Longcore,et al.  EXPERIMENTAL TRANSMISSION OF CUTANEOUS CHYTRIDIOMYCOSIS IN DENDROBATID FROGS , 2001, Journal of wildlife diseases.

[21]  Raymond D. Semlitsch,et al.  Effects of visual, chemical and tactile cues of fish on the behavioural responses of tadpoles , 1993, Animal Behaviour.

[22]  M. Parris,et al.  Single-host pathogen effects on mortality and behavioral responses to predators in salamanders (Urodela: Ambystomatidae) , 2004 .

[23]  J. Brunner,et al.  INTRASPECIFIC RESERVOIRS: COMPLEX LIFE HISTORY AND THE PERSISTENCE OF A LETHAL RANAVIRUS , 2004 .

[24]  Paul Stephen Corn,et al.  Evidence for disease-related amphibian decline in Colorado , 2003 .

[25]  R. Speare,et al.  Survival of Batrachochytrium dendrobatidis in Water: Quarantine and Disease Control Implications , 2003, Emerging infectious diseases.

[26]  J. Kiesecker,et al.  PATHOGEN REVERSES COMPETITION BETWEEN LARVAL AMPHIBIANS , 1999 .

[27]  M. Anver,et al.  Fever and survival , 1975, Science.

[28]  M. Parris,et al.  Chytridiomycosis impacts predator-prey interactions in larval amphibian communities , 2004, Oecologia.

[29]  M. Fuller,et al.  Cutaneous Chytridiomycosis in Poison Dart Frogs (Dendrobates spp.) and White's Tree Frogs (Litoria Caerulea) , 1999, Journal of veterinary diagnostic investigation : official publication of the American Association of Veterinary Laboratory Diagnosticians, Inc.

[30]  D E Green,et al.  Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[31]  C. Carey,et al.  Infectious disease and worldwide declines of amphibian populations, with comments on emerging diseases in coral reef organisms and in humans. , 2000, Environmental health perspectives.

[32]  G. Bradley,et al.  Chytridiomycosis in Native Arizona Frogs , 2002, Journal of wildlife diseases.

[33]  S. Stearns.  Evolution in Health and Disease , 2008 .

[34]  E. Werner,et al.  MECHANISMS CREATING COMMUNITY STRUCTURE ACROSS A FRESHWATER HABITAT GRADIENT , 1996 .

[35]  D. E. Green,et al.  Diagnostic Histological Findings in Yosemite Toads (Bufo canorus) from a Die-off in the 1970s , 2001 .

[36]  J. Piotrowski,et al.  Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. , 2004, Mycologia.

[37]  J. Longcore,et al.  BATRACHOCHYTRIUM DENDROBATIDIS GEN. ET SP. NOV., A CHYTRID PATHOGENIC TO AMPHIBIANS , 1999 .

[38]  M. Spigelman,et al.  Emerging pathogens : the archaeology, ecology, and evolution of infectious disease , 2003 .

[39]  M. Parris.  Hybrid response to pathogen infection in interspecific crosses between two amphibian species (Anura: Ranidae) , 2004 .

[40]  M. García‐París,et al.  Evidence of a chytrid fungus infection involved in the decline of the common midwife toad (Alytes obstetricans) in protected areas of central Spain , 2001 .

[41]  S. N. Thompson,et al.  Physiological alterations during parasitism and their effects on host behaviour. , 1990 .

[42]  David C. Smith.  ADULT RECRUITMENT IN CHORUS FROGS: EFFECTS OF SIZE AND DATE AT METAMORPHOSIS' , 1987 .

[43]  V. Vredenburg,et al.  Transmission of Batrachochytrium dendrobatidis within and between amphibian life stages. , 2004, Diseases of aquatic organisms.

[44]  E. Werner,et al.  Factors modifying antipredator behavior in larval toads , 1996 .

[45]  D. Pfennig,et al.  Pathogen transmission as a selective force against cannibalism , 1998, Animal Behaviour.

[46]  G. Fellers,et al.  Oral Chytridiomycosis in the Mountain Yellow-Legged Frog (Rana muscosa) , 2001, Copeia.

[47]  S. L. Lima,et al.  Behavioral decisions made under the risk of predation: a review and prospectus , 1990 .

[48]  P. Morin.  Predation, Competition, and the Composition of Larval Anuran Guilds , 1983 .

[49]  S. Lawler.  Behavioural responses to predators and predation risk in four species of larval anurans , 1989, Animal Behaviour.

[50]  Sustainability and the Ecology of Infectious Disease , 2022 .

[51]  D. Chivers,et al.  The use of chemical cues in predator recognition by western toad tadpoles , 1996, Animal Behaviour.

[52]  V. Morell.  Are Pathogens Felling Frogs? , 1999, Science.

[53]  K. Gosner,et al.  A simplified table for staging anuran embryos and larvae with notes on identification , 1960 .

[54]  S. Pledger,et al.  The recent decline of a New Zealand endemic: how and why did populations of Archey's frog Leiopelma archeyi crash over 1996–2001? , 2004 .

[55]  C. Hardy,et al.  The progression of behavioral and pathological effects of the parasite Toxocara canis in the mouse , 1985, Physiology & Behavior.

[56]  S. J. Arnold,et al.  Differential Predation on Metamorphic Anurans by Garter Snakes (Thamnophis): Social Behavior as a Possible Defense , 1978 .

[57]  E. Werner,et al.  Ecological Consequences of the Trade-Off between Growth and Mortality Rates Mediated by Foraging Activity , 1993, The American Naturalist.

[58]  J. Godin,et al.  Risk taking in parasitized sticklebacks under threat of predation: effects of energetic need and food availability , 1988 .

[59]  R. Speare,et al.  Origin of the Amphibian Chytrid Fungus , 2004, Emerging infectious diseases.

[60]  David C. Smith.  Factors Controlling Tadpole Populations of the Chorus Frog (Pseudacris Triseriata) on Isle Royale, Michigan , 1983 .

[61]  R. Brooks,et al.  Effects of the protozoan parasite Sarcocystis rauschorum on open-field behaviour of its intermediate vertebrate host, Dicrostonyx richardsoni. , 1987, The Journal of parasitology.

[62]  B. Young,et al.  Response to Comment on "Status and Trends of Amphibian Declines and Extinctions Worldwide" , 2005, Science.

[63]  R. Greenberg.  Biometry , 1969, The Yale Journal of Biology and Medicine.

[64]  Tommie O. Cornelius,et al.  FUNGAL PATHOGEN CAUSES COMPETITIVE AND DEVELOPMENTAL STRESS IN LARVAL AMPHIBIAN COMMUNITIES , 2004 .

[65]  N. Giles.  Behavioural effects of the parasite Schistocephalus solidus (Cestoda) on an intermediate host, the three-spined stickleback, Gasterosteus aculeatus L. , 1983, Animal Behaviour.

[66]  A. Dobson,et al.  Detecting disease and parasite threats to endangered species and ecosystems. , 1995, Trends in ecology & evolution.

[67]  A. Sih,et al.  Predator-prey interactions among fish and larval amphibians: use of chemical cues to detect predatory fish , 1987, Animal Behaviour.

[68]  D. Ebert.  Virulence and Local Adaptation of a Horizontally Transmitted Parasite , 1994, Science.

[69]  H. Lefcort,et al.  Antipredatory Behaviour of Feverish Tadpoles: Implications for Pathogen Transmission , 1993 .

[70]  K. Lips.  Mass Mortality and Population Declines of Anurans at an Upland Site in Western Panama , 1999 .

[71]  J. Brunner,et al.  Pathogenicity and Transmission of Chytridiomycosis in Tiger Salamanders (Ambystoma tigrinum) , 2003, Copeia.

[72]  J. Mendelson,et al.  Amphibian population declines in montane southern Mexico: resurveys of historical localities , 2004 .

[73]  O. Kaltz,et al.  Local adaptation in host–parasite systems , 1998, Heredity.

[74]  R. D. Semlitsch,et al.  Diversity and structure of turtle assemblages: associations with wetland characters across a floodplain landscape , 2000 .

[75]  A. Blaustein,et al.  Disease, predator avoidance, and vulnerability to predation in tadpoles , 1995 .