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

Canadian Journal of Zoology

Volumn 84, Issue 1, 2006, Pages 58-65

  Parris, Matthew J ^a   Reese, Elisheva ^a   Storfer, Andrew ^b  

^a UNIVERSITY OF MEMPHIS   (United States)

^b WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ECOLOGY; ECOSYSTEMS; FISHERIES; PATHOLOGY;

ANTIPREDATOR RESPONSES; BATRACHOCHYTRIUM DENDROBATIDIS LONGCORE; BLUEGILL SUNFISH; LEPOMIS MACROCHIRUS RAFINESQUE;

BIODIVERSITY;

ANTIPREDATOR DEFENSE; FISH; FROG; HOST; MORTALITY; POPULATION DENSITY; PREDATOR;

AMPHIBIA; ANIMALIA; ANURA; BATRACHOCHYTRIUM DENDROBATIDIS; FELIDAE; LEPOMIS MACROCHIRUS; RANA PIPIENS;

EID: 33645996071     PISSN: 00084301     EISSN: None     Source Type: Journal    
DOI: 10.1139/z05-175     Document Type: Article

References (75)

1. Anholt, B.R., Skelly, D.K., and Werner, E.E. 1996. Factors modifying antipredator behavior in larval toads. Herpetologica, 52: 301-313.
2. Arnold, S.J., and Wassersug, R.J. 1978. Differential predation on metamorphic anurans by garter snakes (Thamnophis): social behavior as a possible defense. Ecology, 52: 1014-1022.
3. Bell, B.D., Carver, S., Mitchell, N.J., and Pledger, S. 2004. The recent decline of a New Zealand endemic: how and why did populations of Archey's frog Leiopelma archeyi crash over 1996-2001? Biol. Conserv. 120: 189-199.
4. Berger, L., Speare, R., Daszak, P., Green, D.E., Cunningham, A.A., Goggin, C.L., Slocombe, R., Ragan, M.A., Hyatt, A.D., McDonald, K.R., Hines, H.B., Lips, K.R., Marantelli, G., and Parkes, H. 1998. Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proc. Natl. Acad. Sci. U.S.A. 95: 9031-9036.
5. Bodie, J.R., Semlitsch, R.D., and Renken, R.B. 2000. Diversity and structure of turtle assemblages: associations with wetland characters across a floodplain landscape. Ecography, 23: 444-456.
6. Bosch, J., Martínez-Solano, I., and García-París, M. 2001. Evidence of a chytrid fungus infection involved in the decline of the common midwife toad (Alytes obstetricans) in protected areas of central Spain. Biol. Conserv. 97: 331-337.
7. Bradley, G.A., Rosen, P.C., Sredl, M.J., Jones, T.R., and Longcore, J.E. 2002. Chytridiomycosis in native Arizona frogs. J. Wildl. Dis. 38: 206-212.
8. Brunner, J.L., Schock, D.M., Davidson, E.W., and Collins, J.P. 2004. Intraspecific reservoirs: complex life history and the persistence of a lethal ranavirus. Ecology, 85: 560-566.
9. Carey, C. 2000. Infectious disease and worldwide declines of amphibian populations, with comments on emerging diseases in coral reef organisms and in humans. Environ. Health Perspect. 108: 143-150.
10. Carey, C., Cohen. N., and Rollins-Smith, L. 1999. Amphibian declines: an immunological perspective. Dev. Comp. Immunol. 23: 459-472.
11. Collins, J.P., Brunner, J.L., Miera, V., Parris, M.J., Schock, D.M., and Storfer, A. 2003. Ecology and evolution of infectious disease. In Amphibian conservation. Edited by R.D. Semlitsch. Smithsonian Institution Press, Washington, D.C. pp. 137-151.
12. Daszak, P., Berger, L., Cunningham, A.A., Hyatt, A.D., Green, D.E., and Speare, R. 1999. Emerging infectious diseases and amphibian population declines. Emerg. Infect. Dis. 5: 735-748.
13. Daszak, P., Cunningham, A.A., and Hyatt, A.D. 2003. Infectious disease and amphibian population declines. Divers. Distrib. 9: 141-150.
14. Davidson, E.W., Parris, M.J., Collins, J.P., Longcore, J.E., Pessier, A.P., and Brunner, J. 2003. Pathogenicity and transmission of chytridiomycosis in tiger salamanders (Ambystoma tigrinum). Copeia, 2003: 601-607.
15. Dobson, A.P. 1988. The population biology of parasite-induced changes in host behavior. Q. Rev. Biol. 63: 139-165.
16. Dolinsky, Z.S., Hardy, C.A., Burright, R.G., and Donovick, P.J. 1985. The progression of behavioral and pathological effects of the parasite Toxocara canis in the mouse. Physiol. Behav. 35: 33-42.
17. Ebert, D. 1994. Virulence and local adaptations of a horizontally transmitted parasite. Science, (Washington, D.C.), 265: 1084-1086.
18. Ebert, D. 1999. The evolution and expression of parasite virulence. In Evolution in health and disease. Edited by S. Stearns. Oxford University Press, Oxford. pp. 161-172.
19. Fellers, G.M., Green, D.E., and Longcore, J.E. 2001. Oral chytridiomycosis in the mountain yellow-legged frog (Rana muscosa). Copeia, 2001: 945-953.
20. Giles, N. 1983. Behavioural effects of the parasite Schistocephalus solidus (Cestoda) on an intermediate host, the three-spined stickleback, Gasterosteus aculeatus L. Anim. Behav. 31: 1192-1194.
21. Godin, J., and Sproul, C.D. 1988. Risk taking in parasitized stickleback under threat of predation: effects of energetic need and food availability. Can. J. Zool. 66: 2360-2367.
22. Gosner, K.L. 1960. A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica, 16: 183-190.
23. Green, D.E., and Kagarise Sherman, C. 2001. Diagnostic histological findings in Yosemite toads (Bufo canorus) from a die-off in the 1970s. J. Herpetol. 35: 92-103.
24. Johnson, M.L., and Speare, R. 2003. Survival of Batrachochytrium dendrobatidis in water: quarantine and disease control implications. Emerg. Infect. Dis. 9: 922-925.
25. Kaltz, O., and Shykoff, J. 1998. Local adaptation in host-parasite systems. Heredity, 81: 361-370.
26. Kiesecker, J.M., and Blaustein, A.R. 1999. Pathogen reverses competition between larval amphibians. Ecology, 80: 2442-2448.
27. Kiesecker, J.M., and Skelly, D.K. 2001. Effects of disease and pond drying on gray tree frog growth, development, and survival. Ecology, 82: 1956-1963.
28. Kiesecker, J.M., Chivers, D.P., and Blaustein, A.R. 1996. The use of chemical cues in predator recognition by western toad tadpoles. Anim. Behav. 52: 1237-1245.
29. Kiesecker, J.M., Skelly, D.K., Beard, K.H., and Preisser, E. 1999. Behavioral reduction of infection risk. Proc. Natl. Acad. Sci. U.S.A. 96: 9165-9168.
30. Kluger, M.J., Ringler, D.H., and Anver, M.R. 1975. Fever and survival. Science (Washington, D.C.), 118: 166-168.
31. Lawler, S.P. 1989. Behavioural responses to predators and predation risk in four species of larval anurans. Anim. Behav. 38: 1039-1047.
32. Lefcort, H., and Blaustein, A.R. 1995. Disease, predator avoidance, and vulnerability to predation in tadpoles. Oikos, 74: 469-474.
33. Lefcort, H., and Eiger, S.M. 1993. Antipredator behaviour of feverish tadpoles: implications for pathogen transmission. Behaviour, 126: 13-27.
34. Levri, E. 1999. Parasite-induced change in host behavior of a freshwater snail: parasitic manipulation or byproduct of infection? Behav. Ecol. 10: 234-241.
35. Lima, S.L., and Dill, L.M. 1990. Behavioral decisions made under the risk of predation: a review and prospectus. Can. J. Zool. 68: 619-640.
36. Lips, K.R. 1999. Mass mortality and population declines of anurans at an upland site in western Panama. Conserv. Biol. 13: 117-125.
37. Lips, K.R., Green, D.E., and Papendick, R. 2003. Chytridiomycosis in wild frogs from southern Costa Rica. J. Herpetol. 37: 215-218.
38. Lips, K.R., Mendelson J.R., Munoz-Alonso, A., Canseco-Marquez, L., and Mulcahy, D.G. 2004. Amphibian population declines in montane southern Mexico: resurveys of historical localities. Biol. Conserv. 119: 555-564.
39. Longcore, J.E., Pessier, A.P., and Nichols, D.K. 1999. Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia, 91: 219-227.
40. McCallum, H., and Dobson, A. 1995. Detecting disease and parasite threats to endangered species and ecosystems. Trends Ecol. Evol. 10: 190-194.
41. Morehouse, E.A., James, T.Y., Ganley, A.R.D., Vilgalys, R., Berger, L., Murphy, P.J., and Longcore, J.E. 2003. Multilocus sequence typing suggests the chytrid pathogen of amphibians is a recently emerged clone. Mol. Ecol. 12: 395-403.
42. Morell, V. 1999. Are pathogens felling frogs? Science (Washington, D.C.), 284: 728-731.
43. Morin, P.J. 1983. Predation, competition, and the composition of larval anuran guilds. Ecol. Monogr. 53: 119-138.
44. Muths, E., Corn, P.S., Pessier, A.P., and Green, D.E. 2003. Evidence for disease related amphibian decline in Colorado. Biol. Conserv. 110: 357-365.
45. Nichols, D.K., Lamirande, E.W., Pessier, A.P., and Longcore, J.E. 2001. Experimental transmission of cutaneous chytridiomycosis in dendrobatid frogs. J. Wildl. Dis. 37: 1-11.
46. Nicieza, A.G. 2000. Interacting effects of predation risk and food availability on larval anuran behaviour and development. Oecologia (Berl), 123: 497-505.
47. Parris, M.J. 2001. Hybridization in leopard frogs (Rana pipiens complex): terrestrial performance of newly metamorphosed hybrid and parental genotypes in field enclosures. Can. J. Zool. 79: 1552-1558.
48. Parris, M.J. 2004. Hybrid response to pathogen infection in interspecific crosses between two amphibian species (Anura: Ranidae). Evol. Ecol. Res. 6: 457-471.
49. Parris, M.J., and Baud, D.R. 2004. Interactive effects of a heavy metal and chytridiomycosis on Gray Treefrog larvae (Hyla chrysoscelis). Copeia, 2004: 343-349.
50. Parris, M.J., and Beaudoin, J.G. 2004. Chytridiomycosis impacts predator-prey interactions in larval amphibian communities. Oecologia (Berl.), 140: 626-632.
51. Parris, M.J., and Cornelius, T.O. 2004. Fungal pathogen causes competitive and developmental stress in larval amphibian communities. Ecology, 85: 3385-3395.
52. Parris, M.J., Davis, A., and Collins, J.P. 2004. Single-host pathogen effects on mortality and behavioral responses to predators in salamanders (Urodela: Ambystomatidae). Can. J. Zool. 82: 1477-1483.
53. Pessier, A.P., Nichols, D.K., Longcore, J.E., and Fuller, M.S. 1999. Cutaneous chytridiomycosis in poison dart frogs (Dendrobates spp.) and White's tree frogs (Litoria caerulea). J. Vet. Diagn. Invest. 11: 194-199.
54. Petranka, J.W., Kats, L.B., and Sih, A. 1987. Predator-prey interactions among fish and larval amphibians: use of chemical cues to detect predatory fish. Anim. Behav. 35: 420-425.
55. Pfennig, D.W., Ho, S., and Hoffman, E.A. 1998. Pathogen transmission as a selective force against cannibalism. Anim. Behav. 55: 1255-1261.
56. Piotrowski, J.S., Annis, S.L., and Longcore, J.E. 2004. Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. Mycologia, 96: 9-15.
57. Quinn, S.A., Brooks, R.J., and Cawthorn, R.J. 1987. Effects of the protozoan parasite Sarcocystis rauschorum on open-field behaviour of its intermediate vertebrate host, Dicrostonyx richardsoni. J. Parasitol. 73: 265-271.
58. Rachowicz, L.J., and Vredenburg, V.T. 2004. Transmission of an emerging fungal disease within and between amphibian life stages. Dis. Aquat. Org. 61: 75-83.
59. Real, L.A. 1996. Sustainability and the ecology of infectious diseases. Bioscience 46: 88-97.
60. SAS Institute, Inc. 1990. SAS STAT user's guide. Version 6. 4th ed. SAS Institute Inc., Cary, N.C.
61. Sih, A. 1985. Evolution, predator avoidance, and unsuccessful predation. Am. Nat. 125: 153-157.
62. Skelly, D.K. 1994. Activity level and the susceptibility of anuran larvae to predation. Anim. Behav. 47: 465-468.
63. Skelly, D.K., and Werner, E.E. 1990. Behavioral and life-historical responses of larval American toads to an odonate predator. Ecology, 71: 2313-2322.
64. Smith, D.C. 1983. Factors controlling tadpole populations of the chorus frog (Pseudacris triseriata) on Isle Royale. Ecology, 64: 501-510.
65. Smith, D.C. 1987. Adult recruitment in chorus frogs: effects of size and date at metamorphosis. Ecology, 68: 344-350.
66. Sokal, R.R., and Rohlf, F.J. 1995. Biometry. 3rd ed. W.H. Freeman and Co., New York.
67. Stauffer, H.-P., and Semlitsch, R.D. 1993. Effects of visual, chemical and tactile cues of fish on the behavioural responses of tadpoles. Anim. Behav. 46: 355-364.
68. Stuart, S.N., Chanson, J.S., Cox, N.A., Young, B.E., Rodrigues, A.S.L., Fischman, D.L., and Waller, R.W 2004. Status and trends of amphibian declines and extinctions worldwide. Science (Washington, D.C.), 306: 1783-1786.
69. Thiemann, G.W., and Wassersug, R.J. 2000. Patterns and consequences of behavioural responses to predators and parasites in Rana tadpoles. Biol. J. Linn. Soc. 71: 513-528.
70. Thompson, S.N. 1990. Physiological alterations during parasitism and their effects on host behavior. In Parasitism and host behaviour. Edited by C.J. Barnard and J.M. Behnke. Taylor and Francis, London. pp. 64-94.
71. Weldon, C., du Preez, L.H., Hyatt, A.D., Muller, R., and Speare, R. 2004. Origin of the amphibian chytrid fungus. Emerg. Infect. Dis. 10: 2100-2105.
72. Wellborn, G.A., Skelly, D.K., and Werner, E.E. 1996. Mechanisms creating community structure across a freshwater habitat gradient. Annu. Rev. Ecol. Syst. 27: 337-363.
73. Werner, E.E., and Anhlot, B.R. 1993. Ecological consequences of the trade-off between growth and mortality rates mediated by foraging activity. Am. Nat. 142: 242-272.
74. Werner, E.E., and Glennemeier, K.S. 1999. Influence of forest canopy cover on the breeding pond distributions of several amphibian species. Copeia, 1999: 1-12.
75. Woodward, B.D. 1983. Predator-prey interactions and breeding pond use of temporary pond species in a desert anuran community. Ecology, 64: 1549-1555.