Decoupling the Roles of Corticosterone in Mediating Effects of Methylmercury and Chytrid Fungus (Bd) on Amphibian Survival

Brian J. Tornabene , Morgan P. Kain , Creagh W. Breuner , Collin A. Eagles-Smith , Lisa A. Eby , Ross K. Hinderer , Kelly L. Smalling , Blake R. Hossack

Wildlife Letters ›› 2025, Vol. 3 ›› Issue (4) : 143 -151.

PDF
Wildlife Letters ›› 2025, Vol. 3 ›› Issue (4) :143 -151. DOI: 10.1002/wll2.70015
LETTER
Decoupling the Roles of Corticosterone in Mediating Effects of Methylmercury and Chytrid Fungus (Bd) on Amphibian Survival
Author information +
History +
PDF

Abstract

Amphibians have suffered widespread declines caused by many interacting factors whose effects are often difficult to isolate. We used complementary analyses to decouple effects of methylmercury (MeHg) and amphibian chytrid fungus (Bd) on survival of Columbia Spotted Frogs (Rana luteiventris) during a 5-year capture-mark-recapture study. We also evaluated whether effects on apparent survival were mediated through physiological responses (corticosterone, CORT). While Bd was unrelated to frog survival, geometric mean MeHg bioaccumulation in our population (164 ng/g) reduced survival by ~20%. Baseline CORT was negatively associated, and stress-induced CORT was positively associated with higher MeHg, suggesting that MeHg dysregulated glucocorticoid physiology. Survival was positively associated with higher baseline CORT, whereas survival was negatively associated with higher stress-induced CORT. Our results provide rare evidence linking CORT and long-term survival of wild vertebrates and that environmentally relevant concentrations of MeHg can influence survival of free-ranging amphibians, and these effects may be mediated by CORT.

Keywords

conservation physiology / contaminants / disease / ecotoxicology / endocrinology / frog

Cite this article

Download citation ▾
Brian J. Tornabene, Morgan P. Kain, Creagh W. Breuner, Collin A. Eagles-Smith, Lisa A. Eby, Ross K. Hinderer, Kelly L. Smalling, Blake R. Hossack. Decoupling the Roles of Corticosterone in Mediating Effects of Methylmercury and Chytrid Fungus (Bd) on Amphibian Survival. Wildlife Letters, 2025, 3(4): 143-151 DOI:10.1002/wll2.70015

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Bergeron, C. M., W. A. Hopkins, B. D. Todd, M. J. Hepner, and J. M. Unrine. 2011. “Interactive Effects of Maternal and Dietary Mercury Exposure Have Latent and Lethal Consequences for Amphibian Larvae.” Environmental Science & Technology 45: 3781–3787.

[2]

Breuner, C. W., H. E. Beyl, and J. L. Malisch. 2020. “Corticosteroid-Binding Globulins: Lessons From Biomedical Research.” Molecular and Cellular Endocrinology 514: 110857.

[3]

Breuner, C. W., S. H. Patterson, and T. P. Hahn. 2008. “In Search of Relationships Between the Acute Adrenocortical Response and Fitness.” General and Comparative Endocrinology 157: 288–295.

[4]

Busch, D. S., and L. S. Hayward. 2009. “Stress in a Conservation Context: A Discussion of Glucocorticoid Actions and How Levels Change With Conservation-Relevant Variables.” Biological Conservation 142: 2844–2853.

[5]

Byrne, A. Q., A. W. Waddle, V. Saenz, et al. 2022. “Host Species Is Linked to Pathogen Genotype for the Amphibian Chytrid Fungus (Batrachochytrium dendrobatidis).” PLoS One 17: e0261047.

[6]

Di Cecco, D., M. Di Zio, and B. Liseo. 2020. “Bayesian Latent Class Models for Capture–Recapture in the Presence of Missing Data.” Biometrical Journal 62: 957–969.

[7]

Chételat, J., J. T. Ackerman, C. A. Eagles-Smith, and C. E. Hebert. 2020. “Methylmercury Exposure in Wildlife: A Review of the Ecological and Physiological Processes Affecting Contaminant Concentrations and Their Interpretation.” Science of the Total Environment 711: 135117.

[8]

Collins, J. P., and A. Storfer. 2003. “Global Amphibian Declines: Sorting the Hypotheses.” Diversity and Distributions 9: 89–98.

[9]

Cooke, S. J., L. Sack, C. E. Franklin, et al. 2013. “What Is Conservation Physiology? Perspectives on an Increasingly Integrated and Essential Science.” Conservation Physiology 1: cot001.

[10]

Dickens, M. J., and L. M. Romero. 2013. “A Consensus Endocrine Profile for Chronically Stressed Wild Animals Does Not Exist.” General and Comparative Endocrinology 191: 177–189.

[11]

Eagles-Smith, C. A., J. T. Ackerman, J. J. Willacker, et al. 2016. “Spatial and Temporal Patterns of Mercury Concentrations in Freshwater Fish Across the Western United States and Canada.” Science of the Total Environment 568: 1171–1184.

[12]

Eagles-Smith, C. A., J. J. Willacker, S. J. Nelson, et al. 2020. “A National-Scale Assessment of Mercury Bioaccumulation in United States National Parks Using Dragonfly Larvae as Biosentinels Through a Citizen-Science Framework.” Environmental Science & Technology 54: 8779–8790.

[13]

Emery, C. A., B. J. Tornabene, B. R. Hossack, et al. 2023. Mercury Concentrations in Amphibian Tissues Across the United States, 2016-2021. U.S. Geological Survey Data Release. https://doi.org/10.5066/P9LSR4HY.

[14]

Fisher, M. C., F. Pasmans, and A. Martel. 2021. “Virulence and Pathogenicity of Chytrid Fungi Causing Amphibian Extinctions.” Annual Review of Microbiology 75: 673–693.

[15]

Forsburg, Z. R., C. B. Goff, H. R. Perkins, J. A. Robicheaux, G. F. Almond, and C. R. Gabor. 2019. “Validation of Water-Borne Cortisol and Corticosterone in Tadpoles: Recovery Rate From an Acute Stressor, Repeatability, and Evaluating Rearing Methods.” General and Comparative Endocrinology 281: 145–152.

[16]

Grear, D. A., M. J. Adams, A. R. Backlin, et al. 2025. “Pan-Amphibia Distribution of the Fungal Parasite Batrachochytrium Dendrobatidis Varies With Species and Temperature.” Ecological Monographs 95: e70001.

[17]

Hammond, T. T., Z. A. Au, A. C. Hartman, and C. L. Richards-Zawacki. 2018. “Assay Validation and Interspecific Comparison of Salivary Glucocorticoids in Three Amphibian Species.” Conservation Physiology 6: coy055.

[18]

Hammond, T. T., P. E. Blackwood, S. A. Shablin, and C. L. Richards-Zawacki. 2020. “Relationships Between Glucocorticoids and Infection With Batrachochytrium Dendrobatidis in Three Amphibian Species.” General and Comparative Endocrinology 285: 113269.

[19]

Hontela, A., J. Rasmussen, C. Audet, and G. Chevalier. 1992. “Impaired Cortisol Stress Response in Fish From Environments Polluted by PAHs, PCBs, and Mercury.” Archives of Environmental Contamination and Toxicology 22: 278–283.

[20]

Hossack, B. R., J. M. Davenport, C. K. Mattison, et al. 2025. “Methylmercury in Subarctic Amphibians: Environmental Gradients, Bioaccumulation, and Estimated Flux.” Environmental Toxicology and Chemistry 44: 698–709.

[21]

Hossack, B. R., R. E. Russell, and R. McCaffery. 2020. “Contrasting Demographic Responses of Toad Populations to Regionally Synchronous Pathogen (Batrachochytrium dendrobatidis) Dynamics.” Biological Conservation 241: 108373.

[22]

Hoverman, J. T., J. R. Mihaljevic, K. L. D. Richgels, J. L. Kerby, and P. T. J. Johnson. 2012. “Widespread Co-Occurrence of Virulent Pathogens Within California Amphibian Communities.” EcoHealth 9: 288–292.

[23]

Hu, L., and P. M. Bentler. 1999. “Cutoff Criteria for Fit Indexes in Covariance Structure Analysis: Conventional Criteria Versus New Alternatives.” Structural Equation Modeling: A Multidisciplinary Journal 6: 1–55.

[24]

Jones, D. K., T. D. Dang, J. Urbina, et al. 2017. “Effect of Simultaneous Amphibian Exposure to Pesticides and an Emerging Fungal Pathogen, Batrachochytrium dendrobatidis.” Environmental Science & Technology 51: 671–679.

[25]

Kain, M. P., B. R. Hossack, K. L. Smalling, et al. 2025. “Independent and Interactive Effects of Disease and Methylmercury on Demographic Rates Across Multiple Amphibian Populations.” Scientific Reports 15: 17314. https://doi.org/10.1038/s41598-025-99839-3.

[26]

Madliger, C. L., S. J. Cooke, E. J. Crespi, et al. 2016. “Success Stories and Emerging Themes in Conservation Physiology.” Conservation Physiology 4: cov057.

[27]

McEwen, B. S., and J. C. Wingfield. 2003. “The Concept of Allostasis in Biology and Biomedicine.” Hormones and Behavior 43: 2–15.

[28]

Metts, B. S., K. A. Buhlmann, T. D. Tuberville, D. E. Scott, and W. A. Hopkins. 2013. “Maternal Transfer of Contaminants and Reduced Reproductive Success of Southern Toads (Bufo [Anaxyrus] terrestris) Exposed to Coal Combustion Waste.” Environmental Science & Technology 47: 2846–2853.

[29]

Narayan, E. J., and J. M. Hero. 2013. “Repeatability of Baseline Corticosterone and Acute Stress Responses to Capture, and Patterns of Reproductive Hormones in Vitellogenic and Non-Vitellogenic Female Fijian Ground Frog (Platymantis vitiana).” Journal of Experimental Zoology Part A: Ecological Genetics and Physiology 319: 471–481.

[30]

Papadatou, E., R. Pradel, M. Schaub, et al. 2012. “Comparing Survival Among Species With Imperfect Detection Using Multilevel Analysis of Mark—Recapture Data: A Case Study on Bats.” Ecography 35: 153–161.

[31]

Piggott, J. J., C. R. Townsend, and C. D. Matthaei. 2015. “Reconceptualizing Synergism and Antagonism Among Multiple Stressors.” Ecology and Evolution 5: 1538–1547.

[32]

R Core Team. 2021. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.

[33]

Rosseel, Y., D. Oberski, and J. Byrnes, et al. 2017. Package ‘Lavaan’.

[34]

Rowland, F. E., E. Muths, C. A. Eagles-Smith, et al. 2023. “Complex Life Histories Alter Patterns of Mercury Exposure and Accumulation in a Pond-Breeding Amphibian.” Environmental Science & Technology 57: 4133–4142.

[35]

Russell, R. E., B. J. Halstead, B. A. Mosher, et al. 2019. “Effect of Amphibian Chytrid Fungus (Batrachochytrium dendrobatidis) on Apparent Survival of Frogs and Toads in the Western USA.” Biological Conservation 236: 296–304.

[36]

Scheuhammer, A. M., M. W. Meyer, M. B. Sandheinrich, and M. W. Murray. 2007. “Effects of Environmental Methylmercury on the Health of Wild Birds, Mammals, and Fish.” AMBIO: A Journal of the Human Environment 36: 12–19.

[37]

Skerratt, L. F., L. Berger, R. Speare, et al. 2007. “Spread of Chytridiomycosis Has Caused the Rapid Global Decline and Extinction of Frogs.” EcoHealth 4: 125.

[38]

Stage, F. K., H. C. Carter, and A. Nora. 2004. “Path Analysis: An Introduction and Analysis of a Decade of Research.” Journal of Educational Research 98: 5–13.

[39]

Stan Development Team. 2024a. RStan: The R Interface to Stan. R package version 2.17. 3.

[40]

Stan Development Team. 2024b. Stan Modeling Language User's Guide and Reference Manual, version 2.34, https://mc-stan.org/docs/2_34/reference-manual-2_34.pdf.

[41]

Tan, S. W., J. C. Meiller, and K. R. Mahaffey. 2009. “The Endocrine Effects of Mercury in Humans and Wildlife.” Critical Reviews in Toxicology 39: 228–269.

[42]

Tarlow, E. M., and D. T. Blumstein. 2007. “Evaluating Methods to Quantify Anthropogenic Stressors on Wild Animals.” Applied Animal Behaviour Science 102: 429–451.

[43]

Todd, B. D., C. M. Bergeron, M. J. Hepner, and W. A. Hopkins. 2011. “Aquatic and Terrestrial Stressors in Amphibians: A Test of the Double Jeopardy Hypothesis Based on Maternally and Trophically Derived Contaminants.” Environmental Toxicology and Chemistry 30: 2277–2284.

[44]

Tornabene, B. J. 2023. “Assay Validation of Saliva Glucocorticoids in Columbia Spotted Frogs and Effects of Handling, Marking, and Toe Clipping.” FigShare. https://doi.org/10.6084/m9.figshare.23810727.v1.

[45]

Tornabene, B. J., M. S. Diskin, J. C. Rowe, et al. 2025. Batrachochytrium dendrobatidis Detections and Methylmercury Loads in Amphibians Across the United States. U.S. Geological Survey Data Release. https://doi.org/10.5066/P13LVCYO.

[46]

Tornabene, B. J., B. R. Hossack, and C. W. Breuner. 2023. “Assay Validation of Saliva Glucocorticoids in Columbia Spotted Frogs and Effects of Handling and Marking.” Conservation Physiology 11: coad078.

[47]

Tornabene, B. J., B. R. Hossack, B. J. Halstead, et al. 2023. “Broad-Scale Assessment of Methylmercury in Adult Amphibians.” Environmental Science & Technology 57: 17511–17521.

[48]

Unrine, J. M., C. H. Jagoe, W. A. Hopkins, and H. A. Brant. 2004. “Adverse Effects of Ecologically Relevant Dietary Mercury Exposure in Southern Leopard Frog (Rana sphenocephala) Larvae.” Environmental Toxicology and Chemistry 23: 2964–2970.

[49]

Wilber, M. Q., P. T. J. Johnson, and C. J. Briggs. 2019. “ When Chytrid Fungus Invades: Integrating Theory and Data to Understand Disease-Induced Amphibian Declines.” In Wildlife Disease Ecology: Linking Theory to Data and Application, edited by K. Wilson, A. Fenton, and D. Tompkins, 511–543. Cambridge University Press (Ecological Reviews).

RIGHTS & PERMISSIONS

2025 The Author(s). Wildlife Letters published by Northeast Forestry University and John Wiley & Sons Australia, Ltd.

PDF

3

Accesses

0

Citation

Detail

Sections
Recommended

/