Skip to main content

Advertisement

SpringerLink
Log in

Impacts of Batrachochytrium dendrobatidis Infection on Tadpole Foraging Performance

  • Original Contribution
  • Published:
EcoHealth Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

Reference

  • 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 

  • 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.

    Article  Google Scholar 

  • Anderson RM, May RM (1978) Regulation and stability of host-parasite population interactions—I. Regulatory processes. Journal of Animal Ecology 47:219–247.

    Article  Google Scholar 

  • Anholt BR, Skelly DK, Werner EE (1996) Factors modifying antipredator behaviour in larval toads. Herpetologica 52:301–313.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • Beiswenger RE (1977) Diel patterns of aggregative behavior in tadpoles of Bufo americanus, in relation to light and temperature. Ecology 58:98–108.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Berven KA (1990) Factors affecting population fluctuations in larval and adult stages of the wood frog (Rana sylvatica). Ecology 71:1599–1608.

    Article  Google Scholar 

  • Blaustein AR, Johnson PTJ (2003) Explaining frog deformities. Scientific American 288:60–65.

    Article  Google Scholar 

  • 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 19:1460–1468

    Article  Google Scholar 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Collins JP, Storfer A (2003) Amphibian declines: sorting the hypotheses. Diversity and Distributions 9:89–98.

    Article  Google Scholar 

  • Crowden AE, Broom DM (1980) Effects of the eye fluke, Diplostomaum spathaceum, on the behaviour of dace (Leuciscus leuciscus). Animal Behaviour 28:287–294.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Daszak P, Cunningham AA, Hyatt AD (2003) Infectious disease and amphibian population declines. Diversity and Distributions 9:141–150.

    Article  Google Scholar 

  • de Castro F, Bolker B (2005) Mechanisms of disease induced extinctions. Ecology Letters 8:117–126.

    Article  Google Scholar 

  • Dobson AP (1988) The population biology of parasite-induced changes in host behavior. Quarterly Review of Biology 63:139–165.

    Article  CAS  Google Scholar 

  • 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 

  • Drake DL, Altig R, Grace JB, Walls SC (2007) Occurrence of oral deformities in larval anurans. Copeia 2007:449–458.

    Article  Google Scholar 

  • Fellers GM, Green DE, Longcore JE (2001) Oral chytridiomycosis in the mountain yellow-legged frog (Rana muscosa). Copeia 2001:945–953.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Goater CP (1994) Growth and survival of postmetamorphic toads: interactions among larval history, density, and parasitism. Ecology 75:2264–2274.

    Article  Google Scholar 

  • Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190.

    Google Scholar 

  • Gunn A, Irvine RJ (2003) Subclinical parasitism and ruminant foraging strategies—a review. Wildlife Society Bulletin 31:117–126.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • Hensley FR (1993) Ontogenetic loss of phenotypic plasticity of age at metamorphosis in tadpoles. Ecology 74:2405–2412.

    Article  Google Scholar 

  • Johnson ML, Speare R (2003) Survival of Batrachochytrium dendrobatidis in water: quarantine and disease control implications. Emerging Infectious Diseases 9:922–925.

    Google Scholar 

  • Johnson PTJ, Chase JM (2004) Parasites in the food web: linking amphibian malformations and aquatic eutrophication. Ecology Letters 7:521–526.

    Article  Google Scholar 

  • Kiesecker JM, Blaustein AR (1999) Pathogen reverses competition between larval amphibians. Ecology 80:2442–2448.

    Article  Google Scholar 

  • Kiesecker JM, Skelly DK (2001) Effects of disease and pond drying on gray tree frog growth, development, and survival. Ecology 82:1956–1963.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Kohler SL, Wiley MJ (1997) Pathogen outbreaks reveal large-scale effects of competition in stream communities. Ecology 78:2164–2176.

    Article  Google Scholar 

  • Kurzava LM (1998) Tests of functional equivalence: complementary roles of salamanders and fish in community organization. Ecology 79:477–489.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Leips J, Travis J (1994) Metamorphic responses to changing food levels in two species of hylid frogs. Ecology 75:1345–1356.

    Article  Google Scholar 

  • Levri EP (1999) Parasite-induced change in host behavior of a freshwater snail: parasitic manipulation or byproduct of infection? Behavioral Ecology 10:234–241.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Longcore JE, Pessier AP, Nichols DK (1999) Batrachochytrium dendrobatidis gen. et sp. Nov., a chytrid pathogenic to amphibians. Mycologia 91:219–227.

    Article  Google Scholar 

  • 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 

  • McPeek MA (2004) The growth/predation risk trade-off: so what is the mechanism? American Naturalist 163:E88–E111

    Article  Google Scholar 

  • Moore J (2002) Parasites and the Behavior of Animals, Oxford, UK: Oxford University Press.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • Parris MJ, Baud DR (2004) Interactive effects of a heavy metal and chytridiomycosis on gray treefrog larvae (Hyla chrysosecelis). Copeia 2004:343–349.

    Article  Google Scholar 

  • Parris MJ, Cornelius TO (2004) Fungal pathogen causes competitive and developmental stress in larval amphibian communities. Ecology 85:3385–3395.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Reed JM, Dobson AP (1993) Behavioural constraints and conservation biology: conspecific attraction and recruitment. Trends in Ecology and Evolution 9:108–110.

    Google Scholar 

  • Relyea RA, Auld JR (2004) Having the guts to compete: how intestinal plasticity explains costs of inducible defences. Ecology Letters 7:869–875.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Roy BA, Kirchner JW (2000) Evolutionary dynamics of pathogen resistance and tolerance. Evolution 54:51–63.

    CAS  Google Scholar 

  • Seale DB, Wassersug RJ (1979) Suspension feeding dynamics on anuran larvae related to their functional morphology. Oecologia 39:259–272.

    Article  Google Scholar 

  • Semlitsch RD, Caldwell JP (1982) Effects of density on growth, metamorphosis, and survivorship in tadpoles of Scaphiopus holbrooki. Ecology 63:905–911.

    Article  Google Scholar 

  • Semlitsch RD, Scott DE, Pechmann JHK (1988) Time and size at metamorphosis related to adult fitness in Ambystoma talpoideum. Ecology 69:184–192.

    Article  Google Scholar 

  • Skelly DK (1994) Activity level and the susceptibility of anuran larvae to predation. Animal Behaviour 48:465–468.

    Article  Google Scholar 

  • Skelly DK, Werner EE (1990) Behavioral and life-historical responses of larval American toads to an odonate predator. Ecology 71:2313–2322.

    Article  Google Scholar 

  • Smith DC (1987) Adult recruitment in chorus frogs: effects of size and date at metamorphosis. Ecology 68:344–350.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Steiner UK (2007) Linking antipredator behaviour, ingestion, gut evacuation and costs of predator-induced responses in tadpoles. Animal Behaviour 74:1473–1479.

    Article  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Wassersug RJ, Yamashita M (2001) Plasticity and constraints on feeding kinematics in anuran larvae. Comparative Biochemistry and Physiology. A: Comparative Physiology 131:183–195.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Wilbur HM, Alford RA (1985) Priority effects in experimental pond communities: responses of Hyla to Bufo and Rana. Ecology 66:1106–1114.

    Article  Google Scholar 

  • Wilbur HM, Collins JP (1973) Ecological aspects of amphibian metamorphosis. Science 182:1305–1314.

    Article  CAS  Google Scholar 

  • Woodhams DC, Alford RA (2005) Ecology of chytridiomycosis in rainforest stream frog assemblages of tropical Queensland. Conservation Biology 19:1449–1459.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

Download references

Acknowledgments

We thank M. Ferkin, M. Rensel, S. Schoech, and T. Wilcoxen for reviewing previous versions of this manuscript. R. Altig, K. Warkentin, and R. Wassersug provided suggestions on the foraging efficiency experiment. J. Longcore kindly provided the Bd isolate. We thank M. Beck for providing the materials and space for karyotyping Hyla tadpoles. We also thank N. Hobbs, M. Takahashi, L. Venesky, and T. Wilcoxen for assisting in collecting anuran eggs. Collection permits from TN were obtained prior to collecting the animals used in these experiments, and all experimental procedures were approved by the University of Memphis IACUC. All research conforms to the legal requirements of the United States of America. This publication was developed, in part, under a GRO Research Assistance Agreement No. MA-916980 awarded by the U.S. Environmental Protection Agency to M. Venesky. It has not been formally reviewed by the EPA. The views expressed in this document are solely those of the authors and the EPA does not endorse any products or commercial services mentioned in this publication. The University of Memphis Ecological Research Center Grant in Aid of Research also provided financial support to M. Venesky during portions of this study.

Author information

Authors and Affiliations

  1. Department of Biology, University of Memphis, Memphis, TN, 38152, USA

    Matthew D. Venesky & Matthew J. Parris

  2. School of Biological Sciences, Washington State University, Pullman, WA, 99164, USA

    Andrew Storfer

Authors
  1. Matthew D. Venesky
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Matthew J. Parris
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Andrew Storfer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Matthew D. Venesky.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Venesky, M.D., Parris, M.J. & Storfer, A. Impacts of Batrachochytrium dendrobatidis Infection on Tadpole Foraging Performance. EcoHealth 6, 565–575 (2009). https://doi.org/10.1007/s10393-009-0272-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10393-009-0272-7

Keywords

Search

Navigation