Skip to main content
Log in

Transition of Chytrid Fungus Infection from Mouthparts to Hind Limbs During Amphibian Metamorphosis

  • Short Communication
  • Published:
EcoHealth Aims and scope Submit manuscript

Abstract

The chytrid fungus, Batrachochytrium dendrobatidis (Bd), is implicated in worldwide amphibian declines. Bd has been shown to qualitatively transition from the mouthparts of tadpoles to the hindlimbs during metamorphosis, but we lack evidence of consistency in the timing of this transition across amphibian species. We also do not have predictive functions for the abundance of Bd in mouthparts and limbs as tadpoles develop or for the relationship between keratin and Bd abundance. Hence, researchers presently have little guidance on where to sample developing amphibians to maximize Bd detection, which could affect the accuracy of prevalence and abundance estimates for this deadly pathogen. Here, we show consistency in the timing of the transition of Bd from mouthparts to hind limbs across two frog species (Osteopilus septentrionalis and Mixophyes fasciolatus). Keratin and Bd simultaneously declined from the mouthparts starting at approximately Gosner stage 40. However, keratin on the hindlimbs began to appear at approximately stage 38 but, on average, Bd was not detectable on the hindlimbs until approximately stage 40, suggesting a lag between keratin and Bd arrival. Predictive functions for the relationships between developmental stage and keratin and developmental stage and Bd for mouthparts and hind limbs are provided so that researchers can optimize sampling designs and minimize erroneous conclusions associated with missing Bd infections or misestimating Bd abundance.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

References

  • Altig R (2007). Comments on the descriptions and evaluations of tadpole anomalies. Herpetological Conservation and Biology 2:1-4.

    Google Scholar 

  • Becker CG, and Zamudio KR (2011). Tropical amphibian populations experience higher disease risk in natural habitats. Proceedings of the National Academy of Sciences of the United States of America 108:9893-9898.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Blaustein AR, Romansic JM, Scheessele EA, Han BA, Pessier AP, and Longcore JE (2005). Interspecific variation in susceptibility of frog tadpoles to the pathogenic fungus Batracbochytrium dendrobatidis. Conservation Biology 19:1460-1468.

    Article  Google Scholar 

  • Briggs CJ, Knapp RA, and Vredenburg VT (2010). Enzootic and epizootic dynamics of the chytrid fungal pathogen of amphibians. Proceedings of the National Academy of Sciences of the United States of America 107:9695-9700.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cohen LM, Neimark H, and Eveland LK (1980). Schistomsoma mansoni: Response of cercariae to a thermal gradient. Journal of Parasitology 66:362-364.

    Article  CAS  PubMed  Google Scholar 

  • Fellers GM, Green DE, Longcore JE (2001). Oral chytridiomycosis in the mountain yellow-legged frog (Rana muscosa). Copeia 4:945-953

    Article  Google Scholar 

  • Garner TW, Walker S, Bosch J, Leech S, Rowcliffe JM, Cunningham AA, et al. (2009). Life history tradeoffs influence mortality associated with the amphibian pathogen Batrachochytrium dendrobatidis. Oikos 118:783-791.

    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 

  • Kriger KM, Hero JM, and Ashton KJ (2006a). Cost efficiency in the detection of chytridiomycosis using PCR assay. Diseases of Aquatic Organisms 71:149-154.

    Article  CAS  PubMed  Google Scholar 

  • Kriger KM, Hines HB, Hyatt AD, Boyle DG, and Hero JM (2006b). Techniques for detecting chytridiomycosis in wild frogs: comparing histology with real-time Taqman PCR. Diseases of Aquatic Organisms 71:141-148.

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Rohr JR, and Li YM (2013). Climate, vegetation, introduced hosts and trade shape a global wildlife pandemic. Proceedings of the Royal Society B-Biological Sciences 280:20122506

    Article  PubMed Central  Google Scholar 

  • Luquet E, Garner TWJ, Léna J-P, Bruel C, Joly P, Lengagne T, et al. (2012). Genetic erosion in wild populations makes resistance to a pathogen more costly. The Society for the Study of Evolution 66:1942-1952.

    Google Scholar 

  • Marantelli G, Berger L, Speare R, and Keegan L (2004) Distribution of the amphibian chytrid Batrachochytrium dendrobatidis and keratin during tadpole development. Pacific Conservation Biology 10:173-179.

    Google Scholar 

  • McMahon TA, Brannelly LA, Chatfield MWH, Johnson PTJ, Joseph MB, McKenzie VJ, et al. (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 Science 110:210-215.

    Article  CAS  Google Scholar 

  • McMahon TA, Romansic JM, and Rohr JR (2013) Non-monotonic and monotonic effects of pesticides on the pathogenic fungus Batrachochytrium dendrobatidis in culture and on tadpoles. Environmental Science and Technology 47:7958-7964

    Article  CAS  PubMed  Google Scholar 

  • Murray KA, Retallick RWR, Puschendorf R, Skerratt LF, Rosauer D, McCallum HI, et al. (2011). Assessing spatial patterns of disease risk to biodiversity: implications for the management of the amphibian pathogen, Batrachochytrium dendrobatidis. Journal of Applied Ecology 48:163-173.

    Article  Google Scholar 

  • R Development Core Team (2010) R: A language and environment for statistical computing. R Foundation for Statistical Computing Version 2.8.1.

  • Raffel TR, Halstead NT, McMahon T, Romansic JM, Venesky MD, and Rohr JR (2013). Disease and thermal acclimation in a more variable and unpredictable climate. Nature Climate Change 3:146-151.

    Article  Google Scholar 

  • Raffel TR, Michel PJ, Sites EW, and Rohr JR (2010). What drives chytrid infections in newt populations? Associations with substrate, temperature, and shade. EcoHealth 7:526-536.

    Article  PubMed  Google Scholar 

  • Rohr JR, and Raffel TR (2010). Linking global climate and temperature variability to widespread amphibian declines putatively caused by disease. Proceedings of the National Academy of Sciences of the United States of America 107:8269-8274.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rohr JR, Raffel TR, Romansic JM, McCallum H, and Hudson PJ (2008). Evaluating the links between climate, disease spread, and amphibian declines. Proceedings of the National Academy of Sciences of the United States of America 105:17436-17441.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Venesky MD, Mendelson JR, Sears BF, Stiling PD, and Rohr JR (2012) Selecting for tolerance against pathogens and herbivores to enhance the success of reintroduction and translocation programs. Conservation Biology 26: 586-592

    Article  PubMed  Google Scholar 

  • Venesky MD, Parris MJ, and Storfer A (2009). Impacts of Batrachochytrium dendrobatidis infection on tadpole foraging performance. Ecohealth 6:565-575.

    Article  PubMed  Google Scholar 

  • Venesky MD, Raffel TR, McMahon TA, and Rohr JR (2013) Confronting inconsistencies in the amphibian-chytridiomycosis system: implications for disease management. Biological Reviews 89: 477-483.

    Article  PubMed  Google Scholar 

  • Voyles J, Rosenblum EB, and Berger L (2011). Interactions between Batrachochytrium dendrobatidis and its amphibian hosts: a review of pathogenesis and immunity. Microbes and Infection 13:25-32

    Article  CAS  PubMed  Google Scholar 

  • Vredenburg VT, Knapp RA, Tunstall TS, and Briggs CJ (2010). Dynamics of an emerging disease drive large-scale amphibian population extinctions. Proceedings of the National Academy of Sciences of the United States of America 107:9689-9694.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Woodhams DC, Bosch J, Briggs CJ, Cashins S, Davis LR, Lauer A, Muths E, Puschendorf R, Schmidt BR, Sheafor B, et al. 2011 Mitigating amphibian disease: strategies to maintain wild populations and control chytridiomycosis. Frontiers in Zoology 8:8. doi: 10.1186/1742-9994-8-8

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

We thank V. Vasquez for providing the Bd. Funds were provided by Grants from the National Science Foundation (DEB 0516227 and IOS-1121758), the US Department of Agriculture (NRI 2006-01370 and 2009-35102-0543), and the US Environmental Protection Agency STAR Grant R833835).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Taegan A. McMahon.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

McMahon, T.A., Rohr, J.R. Transition of Chytrid Fungus Infection from Mouthparts to Hind Limbs During Amphibian Metamorphosis. EcoHealth 12, 188–193 (2015). https://doi.org/10.1007/s10393-014-0989-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10393-014-0989-9

Keywords

Navigation