EcoHealth

, Volume 6, Issue 4, pp 565–575 | Cite as

Impacts of Batrachochytrium dendrobatidis Infection on Tadpole Foraging Performance

  • Matthew D. Venesky
  • Matthew J. Parris
  • Andrew Storfer
Original Contribution

Abstract

Pathogen-induced modifications in host behavior, including alterations in foraging behavior or foraging efficiency, can compromise host fitness by reducing growth and development. Chytridiomycosis is an infectious disease of amphibians caused by the fungus Batrachochytrium dendrobatidis (Bd), and it has played an important role in the worldwide decline of amphibians. In larval anurans, Bd infections commonly result in reduced developmental rates, however, the mechanism(s) responsible are untested. We conducted laboratory experiments to test whether Bd infections reduced foraging performance of Grey Treefrog (Hyla chrysoscelis) and Fowler’s Toad (Anaxyrus [= Bufo] fowleri) tadpoles. In the first experiment, we observed foraging behavior of Bd-infected and uninfected tadpoles to test for differences in foraging activity. In a second experiment, we tested for differences in the ingestion rates of tadpoles by examining the amount of food in their alimentary track after a 3-hour foraging period. We hypothesized that Bd-infected tadpoles would forage less often and less efficiently than uninfected tadpoles. As predicted, Bd-infected larvae forage less often and were less efficient at obtaining food than uninfected larvae. Our results show that Bd infections reduce foraging efficiency in Anaxyrus and Hyla tadpoles, and that Bd differentially affects foraging behavior in these species. Thus, our results provide a potential mechanism of decreased developmental rates of Bd-infected tadpoles.

Keywords

Anaxyrus fowleri Bufo chytridiomycosis foraging behavior Hyla chrysoscelis pathogen 

Reference

  1. Altig R, McDiarmid RW (1999) Body plan: development and morphology. In: McDiarmid RW, Altig R (eds) Tadpoles: the Biology of Anuran Larvae. Chicago: University of Chicago Press, pp 24–51.Google Scholar
  2. Altizer S, Nunn CL, Thrall PH, Gittleman JL, Antonovics J, Cunningham AA, et al. (2003) Social organization and parasite risk in mammals: integrating theory and empirical studies. Annual Review of Ecology, Evolution, and Systematics 34:517–547.CrossRefGoogle Scholar
  3. Anderson RM, May RM (1978) Regulation and stability of host-parasite population interactions—I. Regulatory processes. Journal of Animal Ecology 47:219–247.CrossRefGoogle Scholar
  4. Anholt BR, Skelly DK, Werner EE (1996) Factors modifying antipredator behaviour in larval toads. Herpetologica 52:301–313.Google Scholar
  5. Audo MC, Mann TM, Polk TL, Loudenslager CM, Diehl WJ, Altig R (1995) Food deprivation during different periods of tadpole (Hyla chrysoscelis) ontogeny affects metamorphic performance differently. Oecologia 103:518–522.CrossRefGoogle Scholar
  6. Beiswenger RE (1977) Diel patterns of aggregative behavior in tadpoles of Bufo americanus, in relation to light and temperature. Ecology 58:98–108.CrossRefGoogle Scholar
  7. Berger L, Speare R, Daszak P, Green DE, Cunningham AA, Goggin CL, et al. (1998) Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proceedings of the National Academy of Sciences of the United States of America 95:9031–9036.CrossRefGoogle Scholar
  8. Berven KA (1990) Factors affecting population fluctuations in larval and adult stages of the wood frog (Rana sylvatica). Ecology 71:1599–1608.CrossRefGoogle Scholar
  9. Blaustein AR, Johnson PTJ (2003) Explaining frog deformities. Scientific American 288:60–65.CrossRefGoogle Scholar
  10. Blaustein AR, Romansic JM, Scheessele EA, Han BA, Pessier AP, Longcore JE (2005) Interspecific variation in susceptibility of frog tadpoles to the pathogenic fungus Batrachochytrium dendrobatidis. Conservation Biology 19:1460–1468CrossRefGoogle Scholar
  11. Blouin MS (1992) Comparing bivariate reaction norms among species: time at metamorphosis in three species of Hyla (Anura: Hylidae). Oecologia 90:288–293.Google Scholar
  12. Boyle DC, Boyle DB, Olsen V, Morgan JAT, Hyatt AD (2004) Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Diseases of Aquatic Organisms 60:141–148.CrossRefGoogle Scholar
  13. Carey C, Bruzgul JE, Livo LJ, Walling ML, Kuehl KA, Dixon BF, et al. (2006) Experimental exposures of boreal toads (Bufo boreas) to a pathogenic chytrid fungus (Batrachochytrium dendrobatidis). EcoHealth 3:5–21.CrossRefGoogle Scholar
  14. Collins JP, Storfer A (2003) Amphibian declines: sorting the hypotheses. Diversity and Distributions 9:89–98.CrossRefGoogle Scholar
  15. Crowden AE, Broom DM (1980) Effects of the eye fluke, Diplostomaum spathaceum, on the behaviour of dace (Leuciscus leuciscus). Animal Behaviour 28:287–294.CrossRefGoogle Scholar
  16. Daszak P, Berger L, Cunningham AA, Hyatt AD, Green DE, Speare R (1999) Emerging infectious diseases and amphibian population declines. Emerging Infectious Diseases 5:735–748.CrossRefGoogle Scholar
  17. Daszak P, Cunningham AA, Hyatt AD (2003) Infectious disease and amphibian population declines. Diversity and Distributions 9:141–150.CrossRefGoogle Scholar
  18. de Castro F, Bolker B (2005) Mechanisms of disease induced extinctions. Ecology Letters 8:117–126.CrossRefGoogle Scholar
  19. Dobson AP (1988) The population biology of parasite-induced changes in host behavior. Quarterly Review of Biology 63:139–165.CrossRefGoogle Scholar
  20. Dodd CK, Smith LL (2003) Habitat destruction and alteration: historical trends and future prospects for amphibians. In: Semlitsch R (ed) Amphibian Conservation. Washington DC, Smithsonian Institution, pp. 94–112.Google Scholar
  21. Drake DL, Altig R, Grace JB, Walls SC (2007) Occurrence of oral deformities in larval anurans. Copeia 2007:449–458.CrossRefGoogle Scholar
  22. Fellers GM, Green DE, Longcore JE (2001) Oral chytridiomycosis in the mountain yellow-legged frog (Rana muscosa). Copeia 2001:945–953.CrossRefGoogle Scholar
  23. Forson D, Storfer A (2006) Effects of atrazine and iridovirus infection on survival and life-history traits of the long-toed salamander (A. macrodactylum). Environmental Toxicology and Chemistry 25:168–173.CrossRefGoogle Scholar
  24. Garner TWJ, Walker S, Bosch J, Leech S, Rowcliffe M, Cunningham AA, et al. (2009) Life history tradeoffs influence mortality associated with the amphibian pathogen Batrachochytrium dendrobatidis. Oikos 118:783–791.CrossRefGoogle Scholar
  25. Giles N (1983) Behavioural effects of the parasite Schistocephalus solidus (Cestoda) on an intermediate host, the three-spined stickleback, Gasterosteus aculeatus. Animal Behaviour 31:1192–1194.CrossRefGoogle Scholar
  26. Goater CP (1994) Growth and survival of postmetamorphic toads: interactions among larval history, density, and parasitism. Ecology 75:2264–2274.CrossRefGoogle Scholar
  27. Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190.Google Scholar
  28. Gunn A, Irvine RJ (2003) Subclinical parasitism and ruminant foraging strategies—a review. Wildlife Society Bulletin 31:117–126.Google Scholar
  29. Han BA, Bradley PW, Blaustein AR (2008) Ancient behaviors of larval amphibians in response to an emerging fungal pathogen, Batrachochytrium dendrobatidis. Behavioral Ecology and Sociobiology 63:241–250.CrossRefGoogle Scholar
  30. Hensley FR (1993) Ontogenetic loss of phenotypic plasticity of age at metamorphosis in tadpoles. Ecology 74:2405–2412.CrossRefGoogle Scholar
  31. Johnson ML, Speare R (2003) Survival of Batrachochytrium dendrobatidis in water: quarantine and disease control implications. Emerging Infectious Diseases 9:922–925.Google Scholar
  32. Johnson PTJ, Chase JM (2004) Parasites in the food web: linking amphibian malformations and aquatic eutrophication. Ecology Letters 7:521–526.CrossRefGoogle Scholar
  33. Kiesecker JM, Blaustein AR (1999) Pathogen reverses competition between larval amphibians. Ecology 80:2442–2448.CrossRefGoogle Scholar
  34. Kiesecker JM, Skelly DK (2001) Effects of disease and pond drying on gray tree frog growth, development, and survival. Ecology 82:1956–1963.CrossRefGoogle Scholar
  35. Kluger MJ, Kozak W, Conn CA, Leon LR, Soszynski D (1998) Role of fever in disease. Annals of the New York Academy of Sciences 856:224–233.CrossRefGoogle Scholar
  36. Kohler SL, Wiley MJ (1997) Pathogen outbreaks reveal large-scale effects of competition in stream communities. Ecology 78:2164–2176.CrossRefGoogle Scholar
  37. Kurzava LM (1998) Tests of functional equivalence: complementary roles of salamanders and fish in community organization. Ecology 79:477–489.CrossRefGoogle Scholar
  38. Lafferty KD, Dobson A, Kuris AM (2006) Parasites dominate food web links. Proceedings of the National Academy of Sciences of the United States of America 103:11211–11216.CrossRefGoogle Scholar
  39. Leips J, Travis J (1994) Metamorphic responses to changing food levels in two species of hylid frogs. Ecology 75:1345–1356.CrossRefGoogle Scholar
  40. Levri EP (1999) Parasite-induced change in host behavior of a freshwater snail: parasitic manipulation or byproduct of infection? Behavioral Ecology 10:234–241.CrossRefGoogle Scholar
  41. Levri EP, Lively CM (1996) The effects of size, reproductive condition, and parasitism on foraging behaviour in a freshwater snail, Potamopyrus antipodarum. Animal Behaviour 51:891–901.CrossRefGoogle Scholar
  42. Lips KR, Brem F, Brenes R, Reeve JD, Alford RA, Voyles J, et al. (2006) Emerging infectious disease and the loss of biodiversity in a neotropical amphibian community. Proceedings of the National Academy of Sciences of the United States of America 102:3165–3170.CrossRefGoogle Scholar
  43. Longcore JE, Pessier AP, Nichols DK (1999) Batrachochytrium dendrobatidis gen. et sp. Nov., a chytrid pathogenic to amphibians. Mycologia 91:219–227.CrossRefGoogle Scholar
  44. Marantelli G, Berger L, Speare R, Keegan L (2004) Distribution of the amphibian chytrid Batrachochytrium dendrobatidis and keratin during tadpole development. Pacific Conservation Biology 10:173–179.Google Scholar
  45. McPeek MA (2004) The growth/predation risk trade-off: so what is the mechanism? American Naturalist 163:E88–E111CrossRefGoogle Scholar
  46. Moore J (2002) Parasites and the Behavior of Animals, Oxford, UK: Oxford University Press.Google Scholar
  47. Ottershatter MC, Gegear RJ, Colla SR, Thomson JD (2005) Effects of parasitic mites and protozoa on the flower constancy and foraging rate of bumble bees. Behavioral Ecology and Sociobiology 58:383–389.CrossRefGoogle Scholar
  48. Parris MJ (2004) Hybrid response to pathogen infection in interspecific crosses between two amphibian species (Anura: Ranidae). Evolutionary Ecology Research 6:457–471.Google Scholar
  49. Parris MJ, Baud DR (2004) Interactive effects of a heavy metal and chytridiomycosis on gray treefrog larvae (Hyla chrysosecelis). Copeia 2004:343–349.CrossRefGoogle Scholar
  50. Parris MJ, Cornelius TO (2004) Fungal pathogen causes competitive and developmental stress in larval amphibian communities. Ecology 85:3385–3395.CrossRefGoogle Scholar
  51. Parris MJ, Reese E, Storfer A (2006) Antipredator behavior of chytridiomycosis-infected northern leopard frog (Rana pipiens) tadpoles. Canadian Journal of Zoology 84:58–65.CrossRefGoogle Scholar
  52. Pessier AP, Nichols DK, Longcore JE, Fuller MS (1999) Cutaneous chytridiomycosis in poison dart frogs (Dendrobates spp.) and White’s tree frogs (Litoria caerulea). Journal of Veterinary Diagnostic Investigation 11:194–199.Google Scholar
  53. Pounds A, Bustamante MR, Coloma LA, Consuegra JA, Fogden MPL, Foster PN, et al. (2006) Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 439:161–166.CrossRefGoogle Scholar
  54. Reed JM, Dobson AP (1993) Behavioural constraints and conservation biology: conspecific attraction and recruitment. Trends in Ecology and Evolution 9:108–110.Google Scholar
  55. Relyea RA, Auld JR (2004) Having the guts to compete: how intestinal plasticity explains costs of inducible defences. Ecology Letters 7:869–875.CrossRefGoogle Scholar
  56. Rowe CL, Kinney OM, Fiori AP, Congdon JD (1996) Oral deformities in tadpoles (Rana catesbeiana) associated with coal ash deposition: effects on grazing ability and growth. Freshwater Biology 36:723–730.CrossRefGoogle Scholar
  57. Roy BA, Kirchner JW (2000) Evolutionary dynamics of pathogen resistance and tolerance. Evolution 54:51–63.Google Scholar
  58. Seale DB, Wassersug RJ (1979) Suspension feeding dynamics on anuran larvae related to their functional morphology. Oecologia 39:259–272.CrossRefGoogle Scholar
  59. Semlitsch RD, Caldwell JP (1982) Effects of density on growth, metamorphosis, and survivorship in tadpoles of Scaphiopus holbrooki. Ecology 63:905–911.CrossRefGoogle Scholar
  60. Semlitsch RD, Scott DE, Pechmann JHK (1988) Time and size at metamorphosis related to adult fitness in Ambystoma talpoideum. Ecology 69:184–192.CrossRefGoogle Scholar
  61. Skelly DK (1994) Activity level and the susceptibility of anuran larvae to predation. Animal Behaviour 48:465–468.CrossRefGoogle Scholar
  62. Skelly DK, Werner EE (1990) Behavioral and life-historical responses of larval American toads to an odonate predator. Ecology 71:2313–2322.CrossRefGoogle Scholar
  63. Smith DC (1987) Adult recruitment in chorus frogs: effects of size and date at metamorphosis. Ecology 68:344–350.CrossRefGoogle Scholar
  64. Smith KG, Weldon C, Conradie W, du Preez LH (2007) Relationships among size, development, and Batrachochytrium dendrobatidis infection in African tadpoles. Diseases of Aquatic Organisms 74:159–164.CrossRefGoogle Scholar
  65. Steiner UK (2007) Linking antipredator behaviour, ingestion, gut evacuation and costs of predator-induced responses in tadpoles. Animal Behaviour 74:1473–1479.CrossRefGoogle Scholar
  66. Steiner UK, van Buskirk J (2008) Environmental stress and the costs of whole-organism phenotypic plasticity in tadpoles. Journal of Evolutionary Biology 21:97–103.Google Scholar
  67. Tierney JF, Huntingford FA, Crompton DWT (1993) The relationship between infectivity of Schistocephalus solidus (Cestoda) and anti-predator behaviour of its intermediate host, the three-spined stickleback Gasterosteus aculeatus. Animal Behaviour 46:603–605.CrossRefGoogle Scholar
  68. Wassersug RJ, Yamashita M (2001) Plasticity and constraints on feeding kinematics in anuran larvae. Comparative Biochemistry and Physiology. A: Comparative Physiology 131:183–195.Google Scholar
  69. Werner EE, Anholt BR (1993) Ecological consequences of the trade-off between growth and mortality-rates mediated by foraging activity. American Naturalist 142:242–272.CrossRefGoogle Scholar
  70. Wilbur HM, Alford RA (1985) Priority effects in experimental pond communities: responses of Hyla to Bufo and Rana. Ecology 66:1106–1114.CrossRefGoogle Scholar
  71. Wilbur HM, Collins JP (1973) Ecological aspects of amphibian metamorphosis. Science 182:1305–1314.CrossRefGoogle Scholar
  72. Woodhams DC, Alford RA (2005) Ecology of chytridiomycosis in rainforest stream frog assemblages of tropical Queensland. Conservation Biology 19:1449–1459.CrossRefGoogle Scholar
  73. Woodhams DC, Ardipradja K, Alford RA, Marantelli G, Reinert LK, Rollins-Smith LA (2007) Resistance to chytridiomycosis varies among amphibian species and is correlated with skin peptide defenses. Animal Conservation 10:409–417.CrossRefGoogle Scholar
  74. Wright HA, Wootton RJ, Barber I (2006) The effect of Schistocephalus solidus infection on meal size of three-spined stickleback. Journal of Fish Biology 68:801–809.CrossRefGoogle Scholar

Copyright information

© International Association for Ecology and Health 2010

Authors and Affiliations

  • Matthew D. Venesky
    • 1
  • Matthew J. Parris
    • 1
  • Andrew Storfer
    • 2
  1. 1.Department of BiologyUniversity of MemphisMemphisUSA
  2. 2.School of Biological SciencesWashington State UniversityPullmanUSA

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