Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Wildlife Research Wildlife Research Society
Ecology, management and conservation in natural and modified habitats
Shopping Cart: ( empty )
You are here: Home > Journals > WR > WR23126
RESEARCH ARTICLE (Open Access)
Contents Vol 51(10)

High chytrid prevalence and infection intensities in tadpoles of Mixophyes fleayi

Matthijs Hollanders https://orcid.org/0000-0003-0796-1018 A * , Laura F. Grogan B C D , Hamish I. McCallum B C and David A. Newell A
+ Author Affiliations
- Author Affiliations

A Faculty of Science and Engineering, Southern Cross University, Lismore, NSW, Australia.

B Centre for Planetary Health and Food Security, Griffith University, Southport, Qld, Australia.

C School of Environment and Science, Griffith University, Southport, Qld, Australia.

D School of the Environment, University of Queensland, St Lucia, Qld, Australia.

* Correspondence to: matthijs.hollanders@gmail.com

Handling Editor: Thomas Prowse

Wildlife Research 51, WR23126 https://doi.org/10.1071/WR23126
Submitted: 7 October 2023  Accepted: 17 August 2024  Published: 30 September 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

Context

The amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd) has caused catastrophic biodiversity loss globally, but species and life stages within species respond differently to the pathogen. Although tadpoles are often reported to be less vulnerable to disease, they can constitute important infection reservoirs in ecosystems.

Aims

We aimed to describe Bd infection patterns of a long-lived tadpole in a species where post-metamorphic animals appear to exhibit limited mortality as a result of chytridiomycosis. We further investigated how oral dekeratinisation can be used as an indicator of infection.

Methods

We conducted surveys of tadpoles of Mixophyes fleayi (Fleay’s barred frog) over 2 years, at two rainforest streams on the east coast of Australia, to assess patterns in Bd infection prevalence and intensity. We developed an integrated hierarchical model propagating pathogen-detection errors and incorporating how Bd infections affect oral dekeratinisation.

Key results

We found that Bd infection prevalence was strongly associated with lower temperatures and a larger body size, consistent with Bd optimal thermal range and a cumulative risk of exposure for tadpoles. The individual probability of a tadpole being infected with Bd was estimated to be 0.58 [95% HPDI: 0.432, 0.713], the odds of which were approximately eight times greater than for adults at the same sites. Tadpoles infected with Bd were 113 [29, 293] times more likely to have oral dekeratinisation than were uninfected tadpoles, where uninfected individuals were estimated to have a 0.05 [95% HPDI: 0.011, 0.11] probability of having mouthpart loss.

Conclusions

Our results showed that M. fleayi tadpoles are more likely to be infected with Bd than are adults, suggesting that tadpoles could contribute to Bd maintenance in streams. We further showed that sites can be rapidly assessed for Bd by visually checking for oral dekeratinisation.

Implications

Long-lived tadpoles, in general, may contribute to Bd maintenance in ecosystems. We suggest continued exploration of Bd immunocompetence across amphibian life stages to further understand the vastly different infection patterns.

Keywords: amphibian, Batrachochytrium dendrobatidis, chytridiomycosis, dekeratinisation, mouthpart loss, pathogen detection, pathogen load, tadpole.

References

Altman KA, Raffel TR (2019) Thermal acclimation has little effect on tadpole resistance to Batrachochytrium dendrobatidis. Diseases of Aquatic Organisms 133, 207-216.
| Crossref | Google Scholar | PubMed |

Altwegg R, Reyer H-U (2003) Patterns of natural selection on size at metamorphosis in water frogs. Evolution 57, 872-882.
| Crossref | Google Scholar | PubMed |

Anstis M (2002) ‘Tadpoles of south-eastern Australia: a guide with keys.’ (New Holland: Sydney, NSW)

Arellano ML, Natale GS, Grilli PG, Barrasso DA, Steciow MM, Lavilla EO (2017) Host–pathogen relationships between the chytrid fungus Batrachochytrium dendrobatidis and tadpoles of five South American anuran species. Herpetological Journal 27, 33-39.
| Google Scholar |

Berger L, Speare R, Daszak P, Green DE, Cunningham AA, Goggin CL, Slocombe R, Ragan MA, Hyatt AD, McDonald KR, Hines HB, Lips KR, Marantelli G, Parkes H (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 95, 9031-9036.
| Crossref | 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.
| Crossref | Google Scholar |

Boyle DG, 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.
| Crossref | Google Scholar | PubMed |

Brannelly LA, Wetzel DP, West M, Richards-Zawacki CL (2020) Optimized Batrachochytrium dendrobatidis DNA extraction of swab samples results in imperfect detection particularly when infection intensities are low. Diseases of Aquatic Organisms 139, 233-243.
| Crossref | Google Scholar | PubMed |

Brannelly LA, McCallum HI, Grogan LF, Briggs CJ, Puig Ribas M, Hollanders M, Sasso T, Familiar López M, Newell DA, Kilpatrick AM (2021) Mechanisms underlying host persistence following amphibian disease emergence determine appropriate management strategies. Ecology Letters 24, 130-148.
| Crossref | Google Scholar | PubMed |

Briggs CJ, Knapp RA, Vredenburg VT (2010) Enzootic and epizootic dynamics of the chytrid fungal pathogen of amphibians. Proceedings of the National Academy of Sciences 107, 9695-9700.
| Crossref | Google Scholar |

Cashins SD (2009) Epidemiology of chytridiomycosis in rainforest stream tadpoles. PhD thesis, James Cook University.

Catenazzi A, von May R, Vredenburg VT (2013) High prevalence of infection in tadpoles increases vulnerability to fungal pathogen in high-Andean amphibians. Biological Conservation 159, 413-421.
| Crossref | Google Scholar |

Cohen JM, Venesky MD, Sauer EL, Civitello DJ, McMahon TA, Roznik EA, Rohr JR (2017) The thermal mismatch hypothesis explains host susceptibility to an emerging infectious disease. Ecology Letters 20, 184-193.
| Crossref | Google Scholar | PubMed |

Courtois EA, Loyau A, Bourgoin M, Schmeller DS (2017) Initiation of Batrachochytrium dendrobatidis infection in the absence of physical contact with infected hosts: a field study in a high altitude lake. Oikos 126, 843-851.
| Crossref | Google Scholar |

das Neves-da-Silva D, Borges-Júnior VNT, Branco CWC, de Carvalho-e-Silva AMPT (2021) Effects of intrinsic and extrinsic factors on the prevalence of the fungus Batrachochytrium dendrobatidis (Chytridiomycota) in stream tadpoles in the Atlantic Forest domain. Aquatic Ecology 55, 891-902.
| Crossref | Google Scholar |

De Castro F, Bolker B (2004) Mechanisms of disease-induced extinction. Ecology Letters 8, 117-126.
| Crossref | Google Scholar |

de Valpine P, Turek D, Paciorek CJ, Anderson-Bergman C, Lang DT, Bodik R (2017) Programming with models: writing statistical algorithms for general model structures with NIMBLE. Journal of Computational and Graphical Statistics 26, 403-413.
| Crossref | Google Scholar |

de Valpine P, Paciorek C, Turek D, Michaud N, Anderson-Bergman C, Obermeyer F, Wehrhahn Cortes C, Rodrìguez A, Temple Lang D, Paganin S (2023) NIMBLE: MCMC, particle filtering, and programmable hierarchical modeling. Manual. Available at https://doi.org/10.5281/zenodo.1211190

DiRenzo GV, Campbell Grant EH, Longo AV, Che-Castaldo C, Zamudio KR, Lips KR (2018) Imperfect pathogen detection from non-invasive skin swabs biases disease inference. Methods in Ecology and Evolution 9, 380-389.
| Crossref | Google Scholar |

Drake DL, Altig R, Grace JB, Walls SC (2007) Occurrence of oral deformities in larval anurans. Copeia 2007, 449-458.
| Crossref | Google Scholar |

Fellers GM, Green DE, Longcore JE (2001) Oral chytridiomycosis in the mountain yellow-legged frog (Rana muscosa). Copeia 2001, 945-953.
| Crossref | Google Scholar |

Fernández-Loras A, Fernández-Beaskoetxea S, Arriero E, Fisher MC, Bosch J (2017) Early exposure to Batrachochytrium dendrobatidis causes profound immunosuppression in amphibians. European Journal of Wildlife Research 63, 99.
| Crossref | Google Scholar |

Garner TWJ, Walker S, Bosch J, Leech S, Marcus Rowcliffe J, Cunningham AA, Fisher MC (2009) Life history tradeoffs influence mortality associated with the amphibian pathogen Batrachochytrium dendrobatidis. Oikos 118, 783-791.
| Crossref | Google Scholar |

Gelman A, Meng X-L, Stern H (1996) Posterior predictive assessment of model fitness via realized discrepancies. Statistica Sinica 6, 733-807.
| Google Scholar |

Gelman A, Jakulin A, Pittau MG, Su Y-S (2008) A weakly informative default prior distribution for logistic and other regression models. The Annals of Applied Statistics 2, 1360-1383.
| Crossref | Google Scholar |

Gog J, Woodroffe R, Swinton J (2002) Disease in endangered metapopulations: the importance of alternative hosts. Proceedings of the Royal Society of London. Series B: Biological Sciences 269, 671-676.
| Crossref | Google Scholar |

Green PJ (1995) Reversible Jump Markov Chain Monte Carlo computation and Bayesian model determination. Biometrika 82, 711-732.
| Crossref | Google Scholar |

Hagman M, Alford RA (2015) Patterns of Batrachochytrium dendrobatidis transmission between tadpoles in a high-elevation rainforest stream in tropical Australia. Diseases of Aquatic Organisms 115, 213-221.
| Crossref | Google Scholar | PubMed |

Harjoe CC, Buck JC, Rohr JR, Roberts CE, Olson DH, Blaustein AR (2022) Pathogenic fungus causes density- and trait-mediated trophic cascades in an aquatic community. Ecosphere 13,.
| Crossref | Google Scholar |

Haydon DT, Cleaveland S, Taylor LH, Laurenson MK (2002) Identifying reservoirs of infection: a conceptual and practical challenge. Emerging Infectious Diseases 8, 1468-1473.
| Crossref | Google Scholar | PubMed |

Hollanders M, Royle JA (2022) Know what you don’t know: Embracing state uncertainty in disease-structured multievent models. Methods in Ecology and Evolution 13, 2827-2837.
| Crossref | Google Scholar |

Hollanders M, Grogan LF, McCallum HI, Brannelly LA, Newell DA (2023a) Limited impact of chytridiomycosis on juvenile frogs in a recovered species. Oecologia 202, 445-454.
| Crossref | Google Scholar |

Hollanders M, Grogan LF, Nock CJ, McCallum HI, Newell DA (2023b) Recovered frog populations coexist with endemic Batrachochytrium dendrobatidis despite load-dependent mortality. Ecological Applications 33, e2724.
| Crossref | Google Scholar | PubMed |

Hyatt AD, Boyle DG, Olsen V, Boyle DB, Berger L, Obendorf D, Dalton A, Kriger K, Hero M, Hines H, Phillott R, Campbell R, Marantelli G, Gleason F, Colling A (2007) Diagnostic assays and sampling protocols for the detection of Batrachochytrium dendrobatidis. Diseases of Aquatic Organisms 73, 175-192.
| Crossref | Google Scholar | PubMed |

Kilpatrick AM, Briggs CJ, Daszak P (2010) The ecology and impact of chytridiomycosis: an emerging disease of amphibians. Trends in Ecology & Evolution 25, 109-118.
| Crossref | Google Scholar | PubMed |

Knapp RA, Morgan JAT (2006) Tadpole mouthpart depigmentation as an accurate indicator of chytridiomycosis, an emerging disease of amphibians. Copeia 2006, 188-197.
| Crossref | Google Scholar |

Kriger KM, Hero J-M (2007) Large-scale seasonal variation in the prevalence and severity of chytridiomycosis. Journal of Zoology 271, 352-359.
| Crossref | 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.
| Crossref | Google Scholar |

McElreath R (2020) Chapter 15. Missing data and other opportunities. In ‘Statistical rethinking: a Bayesian course with examples in R and Stan. CRC texts in statistical science’. (Ed. R McElreath) pp. 489–524. (Taylor and Francis, CRC Press: Boca Raton, FL, USA) https://doi.org/10.1201/9780429029608

McMahon TA, Rohr JR (2015) Transition of chytrid fungus infection from mouthparts to hind limbs during amphibian metamorphosis. EcoHealth 12, 188-193.
| Crossref | Google Scholar | PubMed |

Navarro-Lozano A, Sánchez-Domene D, Rossa-Feres DC, Bosch J, Sawaya RJ (2018) Are oral deformities in tadpoles accurate indicators of anuran chytridiomycosis? PLoS ONE 13, e0190955.
| Crossref | Google Scholar | PubMed |

Ortiz-Santaliestra ME, Rittenhouse TAG, Cary TL, Karasov WH (2013) Interspecific and postmetamorphic variation in susceptibility of three North American anurans to Batrachochytrium dendrobatidis. Journal of Herpetology 47, 286-292.
| Crossref | Google Scholar |

Piotrowski JS, Annis SL, Longcore JE (2004) Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. Mycologia 96, 9-15.
| Crossref | Google Scholar | PubMed |

Rachowicz LJ (2002) Mouthpart pigmentation in Rana muscosa tadpoles: seasonal changes without chytridiomycosis. Herpetological Review 33, 263-265.
| Google Scholar |

Rachowicz LJ, Briggs CJ (2007) Quantifying the disease transmission function: effects of density on Batrachochytrium dendrobatidis transmission in the mountain yellow-legged frog Rana muscosa. Journal of Animal Ecology 76, 711-721.
| Crossref | Google Scholar | PubMed |

Rachowicz LJ, Vredenburg VT (2004) Transmission of Batrachochytrium dendrobatidis within and between amphibian life stages. Diseases of Aquatic Organisms 61, 75-83.
| Crossref | Google Scholar | PubMed |

R Core Team (2023) ‘R: a language and environment for statistical computing.’ Manual. (R Foundation for Statistical Computing: Vienna, Austria) Available at https://www.R-project.org/

Rollins-Smith LA (1998) Metamorphosis and the amphibian immune system. Immunological Reviews 166, 221-230.
| Crossref | Google Scholar | PubMed |

Sapsford SJ, Alford RA, Schwarzkopf L (2018) Disentangling causes of seasonal infection prevalence patterns: tropical tadpoles and chytridiomycosis as a model system. Diseases of Aquatic Organisms 130, 83-93.
| Crossref | Google Scholar | PubMed |

Sauer EL, Cohen JM, Lajeunesse MJ, McMahon TA, Civitello DJ, Knutie SA, Nguyen K, Roznik EA, Sears BF, Bessler S, Delius BK, Halstead N, Ortega N, Venesky MD, Young S, Rohr JR (2020) A meta-analysis reveals temperature, dose, life stage, and taxonomy influence host susceptibility to a fungal parasite. Ecology 101, e02979.
| Crossref | Google Scholar |

Scheele BC, Pasmans F, Skerratt LF, Berger L, Martel A, Beukema W, Acevedo AA, Burrowes PA, Carvalho T, Catenazzi A, De la Riva I, Fisher MC, Flechas SV, Foster CN, Frías-Álvarez P, Garner TWJ, Gratwicke B, Guayasamin JM, Hirschfeld M, Kolby JE, Kosch TA, La Marca E, Lindenmayer DB, Lips KR, Longo AV, Maneyro R, McDonald CA, Mendelson J, III, Palacios-Rodriguez P, Parra-Olea G, Richards-Zawacki CL, Rödel M-O, Rovito SM, Soto-Azat C, Toledo LF, Voyles J, Weldon C, Whitfield SM, Wilkinson M, Zamudio KR, Canessa S (2019) Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity. Science 363, 1459-1463.
| Crossref | Google Scholar | PubMed |

Stevenson LA, Alford RA, Bell SC, Roznik EA, Berger L, Pike DA (2013) Variation in thermal performance of a widespread pathogen, the amphibian chytrid fungus Batrachochytrium dendrobatidis. PLoS ONE 8, e73830.
| Crossref | Google Scholar | PubMed |

Stratford D, Grigg G, McCallum H, Hines H (2010) Breeding ecology and phenology of two stream breeding myobatrachid frogs (Mixophyes fleayi and M. fasciolatus) in south-east Queensland. Australian Zoologist 35, 189-197.
| Crossref | Google Scholar |

Symonds EP, Hines HB, Bird PS, Morton JM, Mills PC (2007) Surveillance for Batrachochytrium dendrobatidis using Mixophyes (Anura: Myobatrachidae) larvae. Journal of Wildlife Diseases 43, 48-60.
| Crossref | Google Scholar | PubMed |

Valencia-Aguilar A, Toledo LF, Vital MVC, Mott T (2016) Seasonality, environmental factors, and host behavior linked to disease risk in stream-dwelling tadpoles. Herpetologica 72, 98-106.
| Crossref | Google Scholar |

Venesky MD, Parris MJ, Storfer A (2009) Impacts of Batrachochytrium dendrobatidis infection on tadpole foraging performance. EcoHealth 6, 565-575.
| Crossref | Google Scholar | PubMed |

Venesky MD, Wilcoxen TE, Rensel MA, Rollins-Smith L, Kerby JL, Parris MJ (2012) Dietary protein restriction impairs growth, immunity, and disease resistance in southern leopard frog tadpoles. Oecologia 169, 23-31.
| Crossref | Google Scholar | PubMed |

Voyles J, Johnson LR, Rohr J, Kelly R, Barron C, Miller D, Minster J, Rosenblum EB (2017) Diversity in growth patterns among strains of the lethal fungal pathogen Batrachochytrium dendrobatidis across extended thermal optima. Oecologia 184, 363-373.
| Crossref | Google Scholar | PubMed |

Wilber MQ, DeMarchi J, Fefferman NH, Silk MJ (2022) High prevalence does not necessarily equal maintenance species: avoiding biased claims of disease reservoirs when using surveillance data. Journal of Animal Ecology 91, 1740-1754.
| Crossref | Google Scholar |