Advertisement

Oecologia

, Volume 186, Issue 2, pp 393–404 | Cite as

Are the adverse effects of stressors on amphibians mediated by their effects on stress hormones?

  • Caitlin R. GaborEmail author
  • Sarah A. Knutie
  • Elizabeth A. Roznik
  • Jason R. Rohr
Physiological ecology - original research

Abstract

Adverse effects of anthropogenic changes on biodiversity might be mediated by their impacts on the stress response of organisms. To test this hypothesis, we crossed exposure to metyrapone, a synthesis inhibitor of the stress hormone corticosterone, with exposure to the herbicide atrazine and the fungal pathogen Batrachochytrium dendrobatidis (Bd) to assess whether the effects of these stressors on tadpoles and post-metamorphic frogs were mediated by corticosterone. Metyrapone countered atrazine- and Bd-induced corticosterone elevations. However, atrazine- and Bd-induced reductions in body size were not mediated by corticosterone because they persisted despite metyrapone exposure. Atrazine lowered Bd abundance without metyrapone but increased Bd abundance with metyrapone for tadpoles and frogs. In contrast, atrazine reduced tolerance of Bd infections because frogs exposed to atrazine as tadpoles had reduced growth with Bd compared to solvent controls; this effect was not countered by metyrapone. Our results suggest that the adverse effects of atrazine and Bd on amphibian growth, development, and tolerance of infection are not mediated primarily by corticosterone. A possible mechanism for these effects is energy lost from atrazine detoxification, defense against Bd, or repair from damage caused by atrazine and Bd. Additional studies are needed to evaluate how often the effects of anthropogenic stressors are mediated by stress hormones.

Keywords

Atrazine Batrachochytrium dendrobatidis Chytrid Contaminants Pathogen 

Notes

Acknowledgements

We thank J. Middlemis Maher for help with using metyrapone, E. Sauer for help with preparing Bd for inoculations, and N. Halstead for help with atrazine methodology, and early discussions with L. Martin and R. Boughton on this topic. We thank R. Earley for helpful discussion on the experimental design. We also thank K. Cunningham for measuring tadpoles, J. Reyes for help running hormone plates, M. Ehrsam for help with feeding and recording behavior, A. Dubour and V. Caponera for help with water-borne hormone collection, D. Pike for help with swabbing tadpoles for Bd, and S. Sehgal and S. Peters for help with animal husbandry.

Author contribution statement

CRG, SAK, and JRR designed the experiments, CRG, SAK, and EAR carried out the research. CRG and JRR conducted the analyses and primarily wrote the manuscript. All authors gave final approval for publication.

Compliance with ethical standards

Funding

C. R. G. was funded by a REP Grant from Texas State University. J. R. R. was funded by the National Science Foundation (EF-1241889), National Institutes of Health (R01GM109499, R01TW010286), US Department of Agriculture (NRI 2006-01370, 2009-35102-0543), and US Environmental Protection Agency (CAREER 83518801).

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable institutional and/or national guidelines for the care and use of animals were followed. This project was approved by the Texas State University Animal Care and Use Committee # 201485314.

Supplementary material

442_2017_4020_MOESM1_ESM.docx (77 kb)
Supplementary material 1 (DOCX 77 kb)

References

  1. Boekelheide K et al (2012) Predicting later-life outcomes of early-life exposures. Environ Health Perspect 120:1353–1361.  https://doi.org/10.1289/ehp.1204934 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Boonstra R (2013) The ecology of stress: a marriage of disciplines. Funct Ecol 27:7–10.  https://doi.org/10.1111/1365-2435.12048 CrossRefGoogle Scholar
  3. Boyle D, Boyle D, Olsen V, Morgan J, Hyatt A (2004) Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Dis Aquat Org 60:141CrossRefPubMedGoogle Scholar
  4. Busch DS, Hayward LS (2009) Stress in a conservation context: a discussion of glucocorticoid actions and how levels change with conservation-relevant variables. Biol Conserv 142:2844–2853.  https://doi.org/10.1016/j.biocon.2009.08.013 CrossRefGoogle Scholar
  5. Cericato L et al (2009) Responsiveness of the interrenal tissue of Jundia (Rhamdia quelen) to an in vivo ACTH test following acute exposure to sublethal concentrations of agrichemicals. Comp Biochem Physiol C Toxicol Pharmacol 149:363–367.  https://doi.org/10.1016/j.cbpc.2008.09.002 CrossRefPubMedGoogle Scholar
  6. Denver RJ (2009) Stress hormones mediate environment-genotype interactions during amphibian development. Gen Comp Endocrinol 164:20–31.  https://doi.org/10.1016/j.ygcen.2009.04.016 CrossRefPubMedGoogle Scholar
  7. Dirzo R, Young HS, Galetti M, Ceballos G, Isaac NJ, Collen B (2014) Defaunation in the Anthropocene. Science 345:401–406.  https://doi.org/10.1126/science.1251817 CrossRefPubMedGoogle Scholar
  8. Dunlap KD, Schall JJ (1995) Hormonal alterations and reproductive inhibition in male fence lizards (Sceloporus occidentalis) infected with the malarial parasite Plasmodium mexicanum. Physiol Zool 68:608–621CrossRefGoogle Scholar
  9. Eggert LMF, Jodice PGR, O’Reilly KM (2010) Stress response of brown pelican nestlings to ectoparasite infestation. Gen Comp Endocrinol 166:33–38.  https://doi.org/10.1016/j.ygcen.2009.08.009 CrossRefPubMedGoogle Scholar
  10. Ellis T, James JD, Stewart C, Scott AP (2004) A non-invasive stress assay based upon measurement of free cortisol released into the water by rainbow trout. J Fish Biol 65:1233–1252.  https://doi.org/10.1111/j.1095-8649.2004.00499.x CrossRefGoogle Scholar
  11. Fisher MC, Garner TWJ, Walker SF (2009) Global emergence of Batrachochytrium dendrobatidis and amphibian chytridiomycosis in space, time, and host. Annu Rev Microbiol 63:291–310.  https://doi.org/10.1146/annurev.micro.091208.073435 CrossRefPubMedGoogle Scholar
  12. Fraites MJP, Cooper RL, Buckalew A, Jayaraman S, Mills L, Laws SC (2009) Characterization of the hypothalamic-pituitary-adrenal axis response to atrazine and metabolites in the female rat. Toxicol Sci 112:88–99.  https://doi.org/10.1093/toxsci/kfp194 CrossRefPubMedGoogle Scholar
  13. Gabor CR, Fisher MC, Bosch J (2015) Elevated corticosterone levels and changes in amphibian behavior are associated with Batrachochytrium dendrobatidis (Bd) infection and Bd lineage. PLoS ONE 10:e0122685.  https://doi.org/10.1371/journal.pone.0122685 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Gabor CR et al (2016) A non-invasive water-borne assay of stress hormones in aquatic salamanders. Copeia 2016:172–181CrossRefGoogle Scholar
  15. Glennemeier KA, Denver RJ (2002a) Small changes in whole-body corticosterone content affect larval Rana pipiens fitness components. Gen Comp Endocrinol 127:16–25CrossRefPubMedGoogle Scholar
  16. Glennemeier KA, Denver RJ (2002b) Role for corticoids in mediating the response of Rana pipiens tadpoles to intraspecific competition. J Exp Zool 292:32–40.  https://doi.org/10.1002/jez.1140 CrossRefPubMedGoogle Scholar
  17. Glennemeier KA, Denver RJ (2002c) Developmental changes in interrenal responsiveness in anuran amphibians. Integr Comp Biol 42:565–573.  https://doi.org/10.1093/icb/42.3.565 CrossRefPubMedGoogle Scholar
  18. Gosner K (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190Google Scholar
  19. Hayes T, Falso P, Gallipeau S, Stice M (2010) The cause of global amphibian declines: a developmental endocrinologist’s perspective. J Exp Biol 213:921–933CrossRefPubMedPubMedCentralGoogle Scholar
  20. Hernandez SE, Sernia C, Bradley AJ (2014) Effect of atrazine and fenitrothion at no-observed-effect-levels (NOEL) on amphibian and mammalian corticosterone-binding-globulin (CBG). Toxicol Lett 230:408–412.  https://doi.org/10.1016/j.toxlet.2014.08.015 CrossRefPubMedGoogle Scholar
  21. Hossie TJ, Ferland-Raymond B, Burness G, Murray DL (2010) Morphological and behavioural responses of frog tadpoles to perceived predation risk: a possible role for corticosterone mediation? Ecoscience 17:100–108.  https://doi.org/10.2980/17-1-3312 CrossRefGoogle Scholar
  22. Jones DK et al (2017) Effect of simultaneous amphibian exposure to pesticides and an emerging fungal pathogen, Batrachochytrium dendrobatidis. Environ Sci Technol 51:671–679.  https://doi.org/10.1021/acs.est.6b06055 CrossRefPubMedGoogle Scholar
  23. Kiely T, Donaldson D, Grube A (2004) Pesticide industry sales and usage: 2000 and 2001 market estimates. U.S Environmental Protection Agency, Washington, D.C.Google Scholar
  24. Kindermann C, Narayan EJ, Hero J-M (2012) Urinary corticosterone metabolites and chytridiomycosis disease prevalence in a free-living population of male Stony Creek frogs (Litoria wilcoxii). Comp Biochem Physiol A 162:171–176CrossRefGoogle Scholar
  25. Knutie SA, Koop JAH, French SS, Clayton DH (2013) Experimental test of the effect of introduced hematophagous flies on corticosterone levels of breeding Darwin’s finches. Gen Comp Endocrinol 193:68–71.  https://doi.org/10.1016/j.ygcen.2013.07.009 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Koakoski G et al (2014) Agrichemicals chronically inhibit the cortisol response to stress in fish. Chemosphere 112:85–91.  https://doi.org/10.1016/j.chemosphere.2014.02.083 CrossRefPubMedGoogle Scholar
  27. Krucken J et al (2005) Testosterone suppresses protective responses of the liver to blood-stage malaria. Infect Immun 73:436–443.  https://doi.org/10.1128/iai.73.1.436-443.2005 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Larson DL, McDonald S, Fivizzani AJ, Newton WE, Hamilton SJ (1998) Effects of the herbicide atrazine on Ambystoma tigrinum metamorphosis: duration, larval growth, and hormonal response. Physiol Zool 71:671–679CrossRefPubMedGoogle Scholar
  29. Lotter H et al (2013) Testosterone increases susceptibility to amebic liver abscess in mice and mediates inhibition of IFN? Secretion in natural killer T cells. PLoS ONE 8:e55694.  https://doi.org/10.1371/journal.pone.0055694 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Martin LB, Hopkins WA, Mydlarz LD, Rohr JR (2010) The effects of anthropogenic global changes on immune functions and disease resistance. In: Ostfeld RS, Schlesinger WH (eds) Year in Ecology and Conservation Biology, vol 1195, pp 129–148Google Scholar
  31. Matthews SG (2002) Early programming of the hypothalamo-pituitary-adrenal axis. Trends Endocrinol Metab 13:373–380CrossRefPubMedGoogle Scholar
  32. McMahon TA, Romansic JM, Rohr JR (2013a) Nonmonotonic and monotonic effects of pesticides on the pathogenic fungus Batrachochytrium dendrobatidis in culture and on tadpoles. Environ Sci Technol 47:7958–7964.  https://doi.org/10.1021/es401725s CrossRefPubMedGoogle Scholar
  33. McMahon TA et al (2013b) Chytrid fungus Batrachochytrium dendrobatidis has nonamphibian hosts and releases chemicals that cause pathology in the absence of infection. P Natl Acad Sci USA 110:210–215.  https://doi.org/10.1073/pnas.1200592110 CrossRefGoogle Scholar
  34. McMahon TA et al (2014) Amphibians acquire resistance to live and dead fungus overcoming fungal immunosuppression. Nature 511:224–227.  https://doi.org/10.1038/nature13491 CrossRefPubMedPubMedCentralGoogle Scholar
  35. McMahon TA, Boughton RK, Martin LB, Rohr JR (2017) Exposure to the herbicide atrazine nonlinearly affects tadpole corticosterone levels. J Herpetol 51:270–273.  https://doi.org/10.1670/16-126 CrossRefGoogle Scholar
  36. Middlemis Maher J, Werner EE, Denver RJ (2013) Stress hormones mediate predator-induced phenotypic plasticity in amphibian tadpoles. Proc R Soc Biol Sci Ser B 280:20123075.  https://doi.org/10.1098/rspb.2012.3075 CrossRefGoogle Scholar
  37. Murone J, DeMarchi JA, Venesky MD (2016) Exposure to corticosterone affects host resistance, but not tolerance, to an emerging fungal pathogen. PLoS ONE 11:e0163736.  https://doi.org/10.1371/journal.pone.0163736 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Neuman-Lee LA, Stokes AN, Greenfield S, Hopkins GR, Brodie ED Jr, French SS (2015) The role of corticosterone and toxicity in the antipredator behavior of the Rough-skinned Newt (Taricha granulosa). Gen Comp Endocrinol 213:59–64.  https://doi.org/10.1016/j.ygcen.2014.12.006 CrossRefPubMedGoogle Scholar
  39. Oppliger Clobert, Lecomte Lorenzon, Boudjemadi John A (1998) Environmental stress increases the prevalence and intensity of blood parasite infection in the common lizard Lacerta vivipara. Ecol Lett 1:129–138.  https://doi.org/10.1046/j.1461-0248.1998.00028.x CrossRefGoogle Scholar
  40. Peterson JD et al (2013) Host stress response is important for the pathogenesis of the deadly amphibian disease, chytridiomycosis, in Litoria caerulea. PLoS ONE 8:e62146.  https://doi.org/10.1371/journal.pone.0062146 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Pruett SB, Fan R, Zheng Q, Schwab C (2009) Patterns of immunotoxicity associated with chronic as compared with acute exposure to chemical or physical stressors and their relevance with regard to the role of stress and with regard to immunotoxicity testing. Toxicol Sci 109:265–275.  https://doi.org/10.1093/toxsci/kfp073 CrossRefPubMedPubMedCentralGoogle Scholar
  42. R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  43. Råberg L, Sim D, Read AF (2007) Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science 318:812CrossRefPubMedGoogle Scholar
  44. Råberg L, Graham AL, Read AF (2009) Decomposing health: tolerance and resistance to parasites in animals. Philos Trans R Soc B 364:37–49.  https://doi.org/10.1098/rstb.2008.0184 CrossRefGoogle Scholar
  45. Riffle BW et al (2014) Novel molecular events associated with altered steroidogenesis induced by exposure to atrazine in the intact and castrate male rat. Reprod Toxicol 47:59–69.  https://doi.org/10.1016/j.reprotox.2014.05.008 CrossRefPubMedGoogle Scholar
  46. Rogers JM et al (2014) Elevated blood pressure in offspring of rats exposed to diverse chemicals during pregnancy. Toxicol Sci 137:436–446.  https://doi.org/10.1093/toxsci/kft248 CrossRefPubMedGoogle Scholar
  47. Rohr JR, McCoy KA (2010) A qualitative meta-analysis reveals consistent effects of atrazine on freshwater fish and amphibians. Environ Health Perspect 118:20–32.  https://doi.org/10.1289/ehp.0901164 CrossRefPubMedGoogle Scholar
  48. Rohr JR, Palmer BD (2013) Climate change, multiple stressors, and the decline of ectotherms. Conserv Biol 27:741–751.  https://doi.org/10.1111/cobi.12086 CrossRefPubMedGoogle Scholar
  49. Rohr JR et al (2004) Multiple stressors and salamanders: effects of an herbicide, food limitation, and hydroperiod. Ecol Appl 14:1028–1040.  https://doi.org/10.2307/4493602 CrossRefGoogle Scholar
  50. Rohr JR, Raffel TR, Hall CA (2010) Developmental variation in resistance and tolerance in a multi-host-parasite system. Funct Ecol 24:1110–1121.  https://doi.org/10.1111/j.1365-2435.2010.01709.x CrossRefGoogle Scholar
  51. Rohr JR et al (2013) Early-life exposure to a herbicide has enduring effects on pathogen-induced mortality. Proc R Soc Biol Sci Ser B 280:20131502.  https://doi.org/10.1098/rspb.2013.1502 CrossRefGoogle Scholar
  52. Rollins-Smith LA (1998) Metamorphosis and the amphibian immune system. Immunol Rev 166:221–230.  https://doi.org/10.1111/j.1600-065X.1998.tb01265.x CrossRefPubMedGoogle Scholar
  53. Rollins-Smith LA, Ramsey JP, Pask JD, Reinert LK, Woodhams DC (2011) Amphibian immune defenses against chytridiomycosis: impacts of changing environments. Integr Comp Biol 51:552–562.  https://doi.org/10.1093/icb/icr095 CrossRefPubMedGoogle Scholar
  54. Searle CL, Belden LK, Du P, Blaustein AR (2014) Stress and chytridiomycosis: exogenous exposure to corticosterone does not alter amphibian susceptibility to a fungal pathogen. J Exp Zool A Ecol Genet Physiol.  https://doi.org/10.1002/jez.1855 PubMedGoogle Scholar
  55. Sheriff MJ, Dantzer B, Delehanty B, Palme R, Boonstra R (2011) Measuring stress in wildlife: techniques for quantifying glucocorticoids. Oecologia 166:869–887.  https://doi.org/10.1007/s00442-011-1943-y CrossRefPubMedGoogle Scholar
  56. Stuart SN et al (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306:1783–1786CrossRefPubMedGoogle Scholar
  57. Tatiersky L et al (2015) Effect of glucocorticoids on expression of cutaneous antimicrobial peptides in northern leopard frogs (Lithobates pipiens). BMC Vet Res 11:1–8.  https://doi.org/10.1186/s12917-015-0506-6 CrossRefGoogle Scholar
  58. Voyles J et al (2009) Pathogenesis of chytridiomycosis, a cause of catastrophic amphibian declines. Science 326:582–585.  https://doi.org/10.1126/science.1176765 CrossRefPubMedGoogle Scholar
  59. Wake DB, Vredenburg VT (2008) Are we in the midst of the sixth mass extinction? A view from the world of amphibians. Proc Natl Acad Sci USA 105:11466–11473.  https://doi.org/10.1073/pnas.0801921105 CrossRefPubMedPubMedCentralGoogle Scholar
  60. Warne RW, Crespi EJ, Brunner JL (2011) Escape from the pond: stress and developmental responses to ranavirus infection in wood frog tadpoles. Funct Ecol 25:139–146.  https://doi.org/10.1111/j.1365-2435.2010.01793.x CrossRefGoogle Scholar
  61. Zuk M (1996) Disease, endocrine-immune interactions, and sexual selection. Ecology 77:1037–1042.  https://doi.org/10.2307/2265574 CrossRefGoogle Scholar
  62. Zuk M, McKean KA (1996) Sex differences in parasite infections: patterns and processes. Int J Parasitol 26:1009–1023.  https://doi.org/10.1016/s0020-7519(96)80001-4 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Department of BiologyTexas State UniversitySan MarcosUSA
  2. 2.Department of Integrative BiologyUniversity of South FloridaTampaUSA
  3. 3.Department of Ecology and Evolutionary BiologyUniversity of ConnecticutStorrsUSA
  4. 4.Department of Research and ConservationMemphis ZooMemphisUSA

Personalised recommendations