Abstract
Increasing evidence suggests that phenotypic plasticity can play a critical role in ecotoxicology. More specifically, induced pesticide tolerance, in which populations exposed to a contaminant show increased tolerance to the contaminants later, has been documented in multiple taxa. However, the physiological mechanisms of induced tolerance remain unclear. We hypothesized that induced pesticide tolerance is the result of a generalized stress response based on previous studies showing that both natural stressors and anthropogenic stressors can induce tolerance to pesticides. We tested this hypothesis by first exposing larval wood frogs (Rana sylvatica) to either an anthropogenic stressor (sublethal carbaryl concentration), a natural stressor (cues from a caged predator), or a simulated stressor via exogenous exposure to the stress hormone corticosterone (125 nM). We also included treatments that inhibited corticosterone synthesis with the compound metyrapone (MTP). We then exposed the larvae to a lethal carbaryl treatment to assess time to death. We found that prior exposure to 125 nM of exogenous CORT and predator cues induced tolerance to a lethal concentration of carbaryl through a slight delay in time to death. Pre-exposure to sublethal carbaryl, as well as MTP alone or in combination with predator cues, did not induce tolerance to the lethal carbaryl concentration relative to the ethanol vehicle control treatment. Our study provides evidence that pesticide tolerance can be induced by a generalized stress response both in the presence and absence (exogenous CORT) of specific cues and highlights the importance of considering physiological ecology and environmental context in ecotoxicology.
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References
ASTM International (2007) Standard guide for conducting acute toxicity tests on test materials with fishes, macroinvertebrates, and amphibians. Report E729–296 (2007). West Conshohocken, PA, USA
Atwood D, Paisley-Jones C (2017) Pesticides industry sales and usage: 2008–2012 Market Estimates
Audet-Walsh E, Auclair-Vincent S, Anderson A (2009) Glucocorticoids and phenobarbital induce murine CYP2B genes by independent mechanisms. Expert Opin Drug Metab Toxicol 5:1501–1511. https://doi.org/10.1517/17425250903234709
Battaglia M, Ogliari A (2005) Anxiety and panic: from human studies to animal research and back. Neurosci Biobehav Rev 29:169–179
Bernhardt ES, Rosi EJ, Gessner MO (2017) Synthetic chemicals as agents of global change. Front Ecol Environ 15:84–90. https://doi.org/10.1002/fee.1450
Blas J, Bortolotti GR, Tella JL et al. (2007) Stress response during development predicts fitness in a wild, long lived vertebrate. Proc Natl Acad Sci 104:8880–8884. https://doi.org/10.1073/pnas.0700232104
Boone MD, Bridges CM (1999) The effect of temperature on the potency of carbaryl for survival of tadpoles of the green frog (rana clamitans). Environ Toxicol Chem 18:1482. https://doi.org/10.1897/1551-5028(1999)0182.3.CO;2
Boonstra R (2013) Reality as the leading cause of stress: Rethinking the impact of chronic stress in nature. Funct Ecol 27:11–23. https://doi.org/10.1111/1365-2435.12008
Brausch JJM, Smith PNPN (2009) Pesticide resistance from historical agricultural chemical exposure in Thamnocephalus platyurus (Crustacea: Anostraca). Environ Pollut 157:481–487. https://doi.org/10.1016/j.envpol.2008.09.010
Bridges CM (2000) Long-term effects of pesticide exposure at various life stages of the southern leopard frog (Rana sphenocephala). Arch Environ Contam Toxicol 39:91–96. https://doi.org/10.1007/s002440010084
Bridges CM, Semlitsch RD (2000) Variation in pesticide tolerance of tadpoles among and within species of ranidae and patterns of amphibian decline. Conserv Biol 14:1490–1499. https://doi.org/10.1046/j.1523-1739.2000.99343.x
Cain DW, Cidlowski JA (2017) Immune regulation by glucocorticoids. Nat Rev Immunol 17:233–247. https://doi.org/10.1038/nri.2017.1
Calow P, Forbes VE (1998) How do physiological responses to stress translate into ecological and evolutionary processes? Comp Biochem Physiol Part A 120:11–16
Čolović MB, Krstić DZ, Lazarević-Pašti TD et al. (2013) Acetylcholinesterase inhibitors: pharmacology and toxicology. Curr Neuropharmacol 11:315–335. https://doi.org/10.2174/1570159X11311030006
Corlett RT (2015) The Anthropocene concept in ecology and conservation. Trends Ecol Evol 30:36–41. https://doi.org/10.1016/j.tree.2014.10.007
Costantini D, Metcalfe NB, Monaghan P (2010) Ecological processes in a hormetic framework. Ecol Lett 13:1435–1447. https://doi.org/10.1111/j.1461-0248.2010.01531.x
Declerck S, De Bie T, Ercken D et al. (2006) Ecological characteristics of small farmland ponds: associations with land use practices at multiple spatial scales. Biol Conserv 131:523–532. https://doi.org/10.1016/j.biocon.2006.02.024
Denholm I, Rowland MW (1992) Tactics for managing pesticide resistance in arthropods: theory and practice. Annu Rev Entomol 37:91–112. https://doi.org/10.1146/annurev.ento.37.1.91
Denver RJ (2009a) 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
Denver RJ (2019b) Structural and functional evolution of vertebrate neuroendocrine stress systems. Ann N Y Acad Sci 1163:1–16. https://doi.org/10.1111/j.1749-6632.2009.04433.x
Denver RJ (1993) Acceleration of anuran amphibian metamorphosis by corticotropin-releasing hormone-like peptides. Gen Comp Endocrinol 91:38–51. https://doi.org/10.1006/gcen.1993.1102
Denver RJ (1998) Hormonal correlates of environmentally induced metamorphosis in the Western spadefoot toad, Scaphiopus hammondii. Gen Comp Endocrinol 110:326–336. https://doi.org/10.1006/gcen.1998.7082
Futuyma DJ, Kirkpatrick M (2017) Evolution, 4th edn. Sinauer Associates, Inc, Sunderland
Gabor CR, Knutie SA, Roznik EA, Rohr JR (2018) Are the adverse effects of stressors on amphibians mediated by their effects on stress hormones? Oecologia 186:393–404. https://doi.org/10.1007/s00442-017-4020-3
Gilliom RJ, Barbash JE, Crawford CG et al. (2007) The quality of our nation’s waters: pesticides in the nation’s streams and ground water 1992–2001. US Geol Surv Circ 1291:172
Glennemeier KA, Denver RJ (2002) Small changes in whole-body corticosterone content affect larval Rana pipiens fitness components. Gen Comp Endocrinol 127:16–25. https://doi.org/10.1016/S0016-6480(02)00015-1
Glennemeier KA, Denver RJ, Glennemeier KA, Denver RJ (2002) Role for corticoids in mediating the response of rana pipiens tadpoles to intraspecific competition. J Exp Zool 292:32–4032. https://doi.org/10.1002/jez.1140
Haddad NM, Brudvig LA, Clobert J et al. (2015) Habitat fragmentation and its lasting impact on Earth’s ecosystems. Sci Adv 1:e1500052. https://doi.org/10.1126/sciadv.1500052
Hoverman JT, Gray MJ, Miller DL (2010) Anuran susceptibilities to ranaviruses: role of species identity, exposure route, and a novel virus isolate. Dis Aquat Organ 89:97–107. https://doi.org/10.3354/dao02200
Hoverman JT, Relyea RA (2009) Survival trade-offs associated with inducible defences in snails: the roles of multiple predators and developmental plasticity. Funct Ecol 23:1179–1188. https://doi.org/10.1111/j.1365-2435.2009.01586.x
Hua J, Jones DK, Mattes BM et al. (2015a) The contribution of phenotypic plasticity to the evolution of insecticide tolerance in amphibian populations. Evol Appl 8:586–596. https://doi.org/10.1111/eva.12267
Hua J, Jones DK, Mattes BM et al. (2015b) Evolved pesticide tolerance in amphibians: Predicting mechanisms based on pesticide novelty and mode of action. Environ Pollut 206:56–63. https://doi.org/10.1016/j.envpol.2015.06.030
Hua J, Jones DK, Relyea RA (2014) Induced tolerance from a sublethal insecticide leads to cross-tolerance to other insecticides. Environ Sci Technol 48:4078–4085. https://doi.org/10.1021/es500278f
Hua J, Morehouse NI, Relyea R (2013) Pesticide tolerance in amphibians: induced tolerance in susceptible populations, constitutive tolerance in tolerant populations. Evol Appl 6:1028–1040. https://doi.org/10.1111/eva.12083
Jasieniuk M, Brûlé-Babel AL, Morrison IM (1996) The evolution and genetics of herbicide resistance in weeds. Weed Sci 44:176–193
Jones DK, Hintz WD, Schuler MS et al. (2017) Inducible tolerance to agrochemicals was paved by evolutionary responses to predators. Environ Sci Technol 51:13913–13919. https://doi.org/10.1021/acs.est.7b03816
Jones DK, Relyea RA (2015) Here today, gone tomorrow: short-term retention of pesticide-induced tolerance in amphibians. Environ Toxicol Chem 34:2295–2301. https://doi.org/10.1002/etc.3056
Kashiwagi K, Furuno N, Kitamura S et al. (2009) Disruption of thyroid hormone function by environmental pollutants. J Heal Sci 55:147–160. https://doi.org/10.1248/jhs.55.147
Köhler HR, Triebskorn R (2013) Wildlife ecotoxicology of pesticides: can we track effects to the population level and beyond? Science (80-) 341:759–765. https://doi.org/10.1126/science.1237591
Konstandi M, Johnson EO, Lang MA (2014) Consequences of psychophysiological stress on cytochrome P450-catalyzed drug metabolism. Neurosci Biobehav Rev 45:149–167. https://doi.org/10.1016/j.neubiorev.2014.05.011
Kopp K, Wachlevski M, Eterovick PC (2006) Environmental complexity reduces tadpole predation by water bugs. Can J Zool 84:136–140. https://doi.org/10.1139/z05-186
Lewis DB, Lewis LAE, Eby DB, Lewis DB (2002) Spatially heterogeneous refugia and predation risk in intertidal salt marshes. Oikos 96:119–129
Liu N (2015) Insecticide resistance in mosquitoes: impact, mechanisms, and research directions. Annu Rev Entomol 60:537–559. https://doi.org/10.1146/annurev-ento-010814-020828
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
McMahon TA, Halstead NT, Johnson S et al. (2011) The fungicide chlorothalonil is nonlinearly associated with corticosterone levels, immunity, and mortality in amphibians. Environ Health Perspect 119:1098–1103. https://doi.org/10.1289/ehp.1002956
Meredith C, Scott MP, Renwick AB et al. (2003) Studies on the induction of rat hepatic CYP1A, CYP2B, CYP3A and CYP4A subfamily form mRNAs in vivo and in vitro using precision-cut rat liver slices. Xenobiotica 33:511–527. https://doi.org/10.1080/0049825031000085960
Middlemis-Maher J, Werner EE, Denver RJ (2013) Stress hormones mediate predator-induced phenotypic plasticity in amphibian tadpoles. Proc R Soc B Biol Sci 280:20123075. https://doi.org/10.5061/dryad.1kf76
Newman MC (2010) Fundementals of Ecotoxicology, Third. CRC Press, Boca Raton, FL, USA, 2010
Norris LA, Lorz HW, Gregory SZ (1983) Influence of forest and range land management on anadromous fish habitat in western North America: forest chemicals
O’connor CM, Norris DR, Crossin GT, Cooke SJ (2014) Biological carryover effects: Linking common concepts and mechanisms in ecology and evolution. Ecosphere 5:art28. https://doi.org/10.1890/ES13-00388.1
Ortiz de Montellano PR (ed) (2005) Cytochrome P450: Structure, mechanism, and biochemistry, Third. Kluwer Academic/Plenum Publishers
Oziolor EM, Howard W, Lavado R, Matson CW (2017) Induced pesticide tolerance results from detoxification pathway priming. Environ Pollut 224:615–621. https://doi.org/10.1016/J.ENVPOL.2017.02.046
Pigliucci M (2001) Phenotypic plasticity: beyond nature and nurture. Johns Hopkins University Press
Poupardin R, Reynaud S, Strode C et al. (2008) Cross-induction of detoxification genes by environmental xenobiotics and insecticides in the mosquito Aedes aegypti: impact on larval tolerance to chemical insecticides. Insect Biochem Mol Biol 38:540–551. https://doi.org/10.1016/j.ibmb.2008.01.004
Pyke DA, Thompson JN (1986) Statistical analysis of survival and removal rate experiments. Ecology 67:240–245. https://doi.org/10.2307/1938523
R Core Team (2018) R software: Version 3.5.1. R Found. Stat. Comput.
Relyea R, Hoverman J (2006) Assessing the ecology in ecotoxicology: A review and synthesis in freshwater systems. Ecol Lett 9:1157–1171. https://doi.org/10.1111/j.1461-0248.2006.00966.x
Relyea RA (2009) A cocktail of contaminants: how mixtures of pesticides at low concentrations affect aquatic communities. Oecologia 159:363–376. https://doi.org/10.1007/s00442-008-1213-9
Relyea RA (2003) Predator cues and pesticides: a double dose of danger for amphibians. Ecol Appl 13:1515–1521. https://doi.org/10.1890/02-5298
Relyea RA, Mills N (2001) Predator-induced stress makes the pesticide carbaryl more deadly to gray treefrog tadpoles (Hyla versicolor). Proc Natl Acad Sci 98:2491–2496. https://doi.org/10.1073/pnas.031076198
Sailaja BS, Cohen-Carmon D, Zimmerman G et al. (2012) Stress-induced epigenetic transcriptional memory of acetylcholinesterase by HDAC4. Proc Natl Acad Sci 109:E3687–E3695. https://doi.org/10.1073/pnas.1209990110
Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21:55–89. https://doi.org/10.1210/er.21.1.55
Schlichting CD, Pigliucci M (1998) Phenotypic evolution: a reaction norm perspective. Sinauer
Schoenle LA, Zimmer C, Vitousek MN (2018) Understanding Context Dependence in Glucocorticoid–Fitness Relationships: The Role of the Nature of the Challenge, the Intensity and Frequency of Stressors, and Life History. Integr Comp Biol 58:777–787. https://doi.org/10.1093/icb/icy046
Schoeppner NM, Relyea RA (2008) Detecting small environmental differences: risk-response curves for predator-induced behavior and morphology. Oecologia 154:743–754. https://doi.org/10.1007/s00442-007-0862-4
Schriever CA, Liess M (2007) Mapping ecological risk of agricultural pesticide runoff. Sci Total Environ 384:264–279. https://doi.org/10.1016/j.scitotenv.2007.06.019
Shi LJ, Liu LA, Cheng XH, Wang CA (2002) Modulation of neuronal nicotinic acetylcholine receptors by glucocorticoids. Acta Pharm Sin 23:237–242
Sih A, Ferrari MCO, Harris DJ (2011) Evolution and behavioural responses to human-induced rapid environmental change. Evol Appl 4:367–387. https://doi.org/10.1111/j.1752-4571.2010.00166.x
Snell-Rood EC, Kobiela ME, Sikkink KL, Shephard AM (2018) Mechanisms of Plastic Rescue in Novel Environments. Annu Rev Ecol Evol Syst 49:331–354. https://doi.org/10.1146/annurev-ecolsys-110617-062622
Srinivasan S, Shariff M, Bartlett SE (2013) The role of the glucocorticoids in developing resilience to stress and addiction. Front Psychiatry 4:1–11. https://doi.org/10.3389/fpsyt.2013.00068
Tang J, Cao Y, Rose RL, Hodgson E (2002) In vitro metabolism of carbaryl by human cytochrome P450 and its inhibition by chlorpyrifos. Chem Biol Interact 141:229–241. https://doi.org/10.1016/S0009-2797(02)00074-1
Tang Y, Horikoshi M (2016) ggfortify: unified interface to visualize statistical result of popular R packages. R J 8:478–489
Therneau T (2015) A package for survival analysis in S
Thorp JH, Bergey EA (1981) Field experiments on responses of a freshwater, benthic macroinvertebrate community to vertebrate predators. Ecology 62:365–375. https://doi.org/10.2307/1936711
Woodward G, Perkins DM, Brown LE (2010) Climate change and freshwater ecosystems: impacts across multiple levels of organization. Philos Trans R Soc Lond B Biol Sci 365:2093–2106. https://doi.org/10.1098/rstb.2010.0055
Wuerthner VP, Jaeger J, Garramone PS et al. (2019) Inducible pesticide tolerance in Daphnia pulex influenced by resource availability. Ecol Evol 9:1182–1190. https://doi.org/10.1002/ece3.4807
Acknowledgements
We thank S. Abercrombie, N. Buss, T. DeBlieux, D. DiGiacopo, M. Gannon, H. Howard, J. Hua, M. Iacchetta, J. Jaeger, and R. Relyea for their invaluable help in executing this study. We also thank T. DeBlieux, R. Flynn, M. Iacchetta, and D. Rackliffe for their comments on earlier drafts of the manuscript.
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This research was funded in part by a National Science Foundation grant (DEB-1655156) to JTH.
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All methods were approved by the Purdue University IACUC (protocol 1701001530). Animals were collected under Pennsylvania Scientific Collector Permit # 2018-01-0083.
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Billet, L.S., Hoverman, J.T. Pesticide tolerance induced by a generalized stress response in wood frogs (Rana sylvatica). Ecotoxicology 29, 1476–1485 (2020). https://doi.org/10.1007/s10646-020-02277-2
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DOI: https://doi.org/10.1007/s10646-020-02277-2