Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-08T05:22:20.119Z Has data issue: false hasContentIssue false
  • English
  • Français

Rethinking the role of invertebrate hosts in the life cycle of the amphibian chytridiomycosis pathogen

Published online by Cambridge University Press:  30 August 2016

CLARISSE M. BETANCOURT-ROMÁN ,
COLIN C. O'NEIL  and
TIMOTHY Y. JAMES
CLARISSE M. BETANCOURT-ROMÁN
Affiliation:
Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109, USA
COLIN C. O'NEIL
Affiliation:
Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109, USA
TIMOTHY Y. JAMES*
Affiliation:
Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109, USA
*
*Corresponding author: Department of Ecology and Evolutionary Biology, University of Michigan, 830 N. University, University of Michigan, Ann Arbor, MI 48109, USA. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The amphibian pathogen Batrachochytrium dendrobatidis (Bd) has recently emerged as a primary factor behind declining global amphibian populations. Much about the basic biology of the pathogen is unknown, however, such as its true ecological niche and life cycle. Here we evaluated invertebrates as infection models by inoculating host species that had previously been suggested to be parasitized in laboratory settings: crayfish (Procambarus alleni) and nematodes (Caenorhabditis elegans). We found neither negative effects on either host nor evidence of persistent infection despite using higher inoculum loads and more pathogen genotypes than tested in previous studies. In contrast, addition of Bd to C. elegans cultures had a slight positive effect on host growth. Bd DNA was detected on the carapace of 2/34 crayfish 7 weeks post-inoculation, suggesting some means of persistence in the mesocosm. These results question the role of invertebrates as alternative hosts of Bd and their ability to modulate disease dynamics.

Keywords

virulence modelchytridenvironmental reservoirPCR detectionpathogenicity
Type
Research Article
Information
Parasitology , Volume 143 , Issue 13 , November 2016 , pp. 1723 - 1729
Check for updates
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Brannelly, L. A., McMahon, T. A., Hinton, M., Lenger, D. and Richards-Zawacki, C. L. (2015). Batrachochytrium dendrobatidis in natural and farmed Louisiana crayfish populations: prevalence and implications. Diseases of Aquatic Organisms 112, 229–235.CrossRefGoogle ScholarPubMed
Chestnut, T., Anderson, C., Popa, R., Blaustein, A. R., Voytek, M., Olson, D. H. and Kirshtein, J. (2014). Heterogeneous occupancy and density estimates of the pathogenic fungus Batrachochytrium dendrobatidis in waters of North America. PLoS ONE 9, e106790.CrossRefGoogle ScholarPubMed
Garmyn, A., Van Rooij, P., Pasmans, F., Hellebuyck, T., Van den Broeck, W., Haesebrouck, F. and Martel, A. (2012). Waterfowl: potential environmental reservoirs of the chytrid fungus Batrachochytrium dendrobatidis . PLoS ONE 7, e35038.CrossRefGoogle ScholarPubMed
Johnson, M. L. and Speare, R. (2003). Survival of Batrachochytrium dendrobatidis in water: quarantine and disease control implications. Emerging Infectious Diseases 9, 922–925.CrossRefGoogle ScholarPubMed
Kerby, J. L., Schieffer, A., Brown, J. R. and Whitfield, S. (2013). Utilization of fast qPCR techniques to detect the amphibian chytrid fungus: a cheaper and more efficient alternative method. Methods in Ecology and Evolution 4, 162–166.CrossRefGoogle Scholar
Kilburn, V. L., Ibanez, R. and Green, D. M. (2011). Reptiles as potential vectors and hosts of the amphibian pathogen Batrachochytrium dendrobatidis in Panama. Diseases of Aquatic Organisms 97, 127–134.CrossRefGoogle ScholarPubMed
Kilpatrick, A. M., Briggs, C. J. and Daszak, P. (2010). The ecology and impact of chytridiomycosis: an emerging disease of amphibians. Trends in Ecology & Evolution 25, 109–118.CrossRefGoogle ScholarPubMed
Kolby, J. E., Ramirez, S. D., Berger, L., Griffin, D. W., Jocque, M. and Skerratt, L. F. (2015). Presence of amphibian chytrid fungus (Batrachochytrium dendrobatidis) in rainwater suggests aerial dispersal is possible. Aerobiologia 31, 411–419.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Martel, A., Blooi, M., Adriaensen, C., Van Rooij, P., Beukema, W., Fisher, M. C., Farrer, R. A., Schmidt, B. R., Tobler, U., Goka, K., Lips, K. R., Muletz, C., Zamudio, K. R., Bosch, J., Lötters, S., Wombwell, E., Garner, T. W. J., Cunningham, A. A., Spitzen-van der Sluijs, A., Salvidio, S., Ducatelle, R., Nishikawa, K., Nguyen, T. T., Kolby, J. E., Van Bocxlaer, I., Bossuyt, F. and Pasmans, F. (2014). Recent introduction of a chytrid fungus endangers Western Palearctic salamanders. Science 346, 630–631.CrossRefGoogle ScholarPubMed
McMahon, T. A., Brannelly, L. A., Chatfield, M. W. H., Johnson, P. T. J., Joseph, M. B., McKenzie, V. J., Richards-Zawacki, C. L., Venesky, M. D. and Rohr, J. R. (2013). Chytrid fungus Batrachochytrium dendrobatidis has nonamphibian hosts and releases chemicals that cause pathology in the absence of infection. Proceedings of the National Academy of Sciences of the United States of America 110, 210–215.CrossRefGoogle ScholarPubMed
Mitchell, K. M., Churcher, T. S., Garner, T. W. J. and Fisher, M. C. (2008). Persistence of the emerging pathogen Batrachochytrium dendrobatidis outside the amphibian host greatly increases the probability of host extinction. Proceedings of the Royal Society B - Biological Sciences 275, 329–334.CrossRefGoogle ScholarPubMed
Mylonakis, E., Casadevall, A. and Ausubel, F. M. (2007). Exploiting amoeboid and non-vertebrate animal model systems to study the virulence of human pathogenic fungi. PLoS Pathogens 3, 859–865.CrossRefGoogle Scholar
Olson, D. H., Aanensen, D. M., Ronnenberg, K. L., Powell, C. I., Walker, S. F., Bielby, J., Garner, T. W. J., Weaver, G., Fisher, M. C. and Bd Mapping, G. (2013). Mapping the global emergence of Batrachochytrium dendrobatidis, the amphibian chytrid fungus. PLoS ONE 8, e56802.CrossRefGoogle ScholarPubMed
Schloegel, L. M., Toledo, L. F., Longcore, J. E., Greenspan, S. E., Viera, C. A., Lee, M., Zhao, S., Wangen, C., Ferreira, C. M., Hipolito, M., Davies, A. J., Cuomo, C. A., Daszak, P. and James, T. Y. (2012). Novel, panzootic, and hybrid genotypes of amphibian chytridiomycosis associated with the bullfrog trade. Molecular Ecology 21, 5162–5177.CrossRefGoogle ScholarPubMed
Schmeller, D. S., Blooi, M., Martel, A., Garner, T. W. J., Fisher, M. C., Azemar, F., Clare, F. C., Leclerc, C., Jager, L., Guevara-Nieto, M., Loyau, A. and Pasmans, F. (2014). Microscopic aquatic predators strongly affect infection dynamics of a globally emerged pathogen. Current Biology 24, 176–180.CrossRefGoogle ScholarPubMed
Searle, C. L., Mendelson, J. R., Green, L. E. and Duffy, M. A. (2013). Daphnia predation on the amphibian chytrid fungus and its impacts on disease risk in tadpoles. Ecology and Evolution 3, 4129–4138.CrossRefGoogle ScholarPubMed
Shapard, E. J., Moss, A. S. and San Francisco, M. J. (2012). Batrachochytrium dendrobatidis can infect and cause mortality in the nematode Caenorhabditis elegans . Mycopathologia 173, 121–126.CrossRefGoogle ScholarPubMed