Skip to main content
SpringerLink
Log in

Behave yourself: effects of exogenous-glucocorticoid exposure on larval amphibian anti-parasite behaviour and physiology

  • Original Research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Parasites represent a ubiquitous threat for most organisms, requiring potential hosts to invest in a range of strategies to defend against infection—these include both behavioural and physiological mechanisms. Avoidance is an essential first line of defence, but this behaviour may show a trade-off with host investment in physiological immunity. Importantly, while environmental stressors can lead to elevated hormones in vertebrates, such as glucocorticoids, that can reduce physiological immunity in certain contexts, behavioural defences may also be compromised. Here, we investigate anti-parasite behaviour and immune responses against a trematode (flatworm) parasite by larval amphibians (tadpoles) exposed or not to a simulated general stressor in the form of exogenous corticosterone. Tadpoles that were highly active in the presence of the trematode infectious stage (cercariae) had lower infection loads, and parasite loads from tadpoles treated only with dechlorinated water were significantly lower than those exposed to corticosterone or the solvent control. However, treatment did not affect immunity as measured through white blood-cell profiles, and there was no relationship between the latter and anti-parasite behaviour. Our results suggest that a broad range of stressors could increase host susceptibility to infection through altered anti-parasite behaviours if they elevate endogenous glucocorticoids, irrespective of physiological immunity effects. How hosts defend themselves against parasitism in the context of multiple challenges represents an important topic for future research, particularly as the risk posed by infectious diseases is predicted to increase in response to ongoing environmental change.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Data availability

Data will be archived and available from the figshare repository using the following https://doi.org/10.6084/m9.figshare.25681758.

References

  • Ackerman JM, Hill SE, Murray DR (2018) 2018. The behavioral immune system: current concerns and future directions. Soc Personal Psychol 12:57–70

    Google Scholar 

  • Adelman JS, Martin LB (2009) Vertebrate sickness behaviors: adaptive and integrated neuroendocrine immune responses. Integr Comp Biol 49:202–214

    Article  CAS  PubMed  Google Scholar 

  • Amoroso CR (2021) Integrating concepts of physiological and behavioral resistance to parasites. Front Ecol Evol 9:47

    Article  Google Scholar 

  • Amoroso CR, Antonovics J (2020) Evolution of behavioural resistance in host–pathogen systems. Biol Lett 16:20200508

    Article  PubMed  PubMed Central  Google Scholar 

  • Bartoń K (2018) MuMIn: multi-model inference. CRAN. https://cran.r-project.org/web/packages/MuMIn/MuMIn.pdf

  • Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  • Behringer DC, Butler MJ, Shields JD (2006) Avoidance of disease by social lobsters. Nature 441:421–421

    Article  CAS  PubMed  Google Scholar 

  • Behringer DC, Karvonen A, Bojko J (2018) Parasite avoidance behaviours in aquatic environments. Phil Trans R Soc B Biol Sci 373:20170202

    Article  Google Scholar 

  • Belden LK, Kiesecker JM (2005) Glucocorticosteroid hormone treatment of larval treefrogs increases infection by Alaria sp trematode cercariae. J Parasitol 91:686–688

    Article  CAS  PubMed  Google Scholar 

  • Belden LK, Moore IT, Wingfield JC, Blaustein AR (2005) Corticosterone and growth in Pacific treefrog (Hyla regilla) tadpoles. Copeia 2005(2):424–430

    Article  Google Scholar 

  • Belden LK, Rubbo MJ, Wingfield JC, Kiesecker JM (2007) Searching for the physiological mechanism of density dependence: does corticosterone regulate tadpole responses to density? Physiol Biochem Zool 80:444–451

    Article  CAS  PubMed  Google Scholar 

  • Belden LK, Wingfield JC, Kiesecker JM (2010) Variation in the hormonal stress response among larvae of three amphibian species. J Exp Zool Part A Ecol Genet Physiol 313(8):524–531

    Article  Google Scholar 

  • Bennett AM, Longhi JN, Chin EH, Burness G, Kerr LR, Murray DL (2016) Acute changes in whole body corticosterone in response to perceived predation risk: a mechanism for anti-predator behavior in anurans? Gen Comp Endocrinol 229:62–66

    Article  CAS  PubMed  Google Scholar 

  • Blaustein AR, Gervasi SS, Johnson PT, Hoverman JT, Belden LK, Bradley PW, Xie GY (2012) Ecophysiology meets conservation: understanding the role of disease in amphibian population declines. Philos Trans R Soc B Biol Sci 367:1688–1707

    Article  Google Scholar 

  • Bókony V, Ujhegyi N, Hamow KÁ, Bosch J, Thumsová B, Vörös J, Aspbury AS, Gabor CR (2021) Stressed tadpoles mount more efficient glucocorticoid negative feedback in anthropogenic habitats due to phenotypic plasticity. Sci Total Environ 753:141896

    Article  PubMed  Google Scholar 

  • Bonier F, Martin PR, Moore IT, Wingfield JC (2009) Do baseline glucocorticoids predict fitness? Trends Ecol Evol 24:634–642

    Article  PubMed  Google Scholar 

  • Bonneaud C, Mazuc J, Gonzalez G, Haussy C, Chastel O, Faivre B, Sorci G (2003) Assessing the cost of mounting an immune response. Am Nat 161:367–379

    Article  PubMed  Google Scholar 

  • Buck JC, Weinstein SB, Young HS (2018) Ecological and evolutionary consequences of parasite avoidance. Trends Ecol Evol 33:619–632

    Article  CAS  PubMed  Google Scholar 

  • Burraco P, Miranda F, Bertó A, Vazquez LA, Gomez-Mestre I (2017) Validated flow cytometry allows rapid quantitative assessment of immune responses in amphibians. Amphibia-Reptilia 38:232–237

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Bush SE, Clayton DH (2018) Anti-parasite behaviour of birds. Philos Trans R Soc B Biol Sci 373:20170196

    Article  Google Scholar 

  • Byers JE (2020) Effects of climate change on parasites and disease in estuarine and nearshore environments. PLoS Biol 18:e3000743

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cain DW, Cidlowski JA (2017) Immune regulation by glucocorticoids. Nat Rev Immunol 17(4):233–247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen TH, Wang YH, Wu YH (2011) Developmental exposures to ethanol or dimethylsulfoxide at low concentrations alter locomotor activity in larval zebrafish: implications for behavioral toxicity bioassays. Aquat Toxicol 102(3–4):162–166

    Article  CAS  PubMed  Google Scholar 

  • Chen J, Wang ZZ, Zuo W, Zhang S, Chu SF, Chen NH (2016) Effects of chronic mild stress on behavioral and neurobiological parameters-role of glucocorticoid. Horm Behav 78:150–159

    Article  CAS  PubMed  Google Scholar 

  • Cooke SJ, Bergman JN, Madliger CL, Cramp RL, Beardall J, Burness G, Clark TD, Dantzer B, De La Barrera E, Fangue NA, Franklin CE (2021) One hundred research questions in conservation physiology for generating actionable evidence to inform conservation policy and practice. Conserv Physiol 9:coab009

    Article  PubMed  PubMed Central  Google Scholar 

  • Crespi EJ, Denver RJ (2004) Ontogeny of corticotropin-releasing factor effects on locomotion and foraging in the Western spadefoot toad (Spea hammondii). Horm Behav 46:399–410

    Article  CAS  PubMed  Google Scholar 

  • Crespi EJ, Denver RJ (2005) Roles of stress hormones in food intake regulation in anuran amphibians throughout the life cycle. Comp Biochem Physiol A Mol Integr Physiol 141:381–390

    Article  PubMed  Google Scholar 

  • Cull F, O’Connor CM, Suski CD, Shultz AD, Danylchuk AJ, Cooke SJ (2015) Puff and bite: the relationship between the glucocorticoid stress response and anti-predator performance in checkered puffer (Sphoeroides testudineus). Gen Comp Endocrinol 214:1–8

    Article  CAS  PubMed  Google Scholar 

  • Curtis VA (2014) Infection-avoidance behaviour in humans and other animals. Trends Immunol 35:457–464

    Article  CAS  PubMed  Google Scholar 

  • Daly EW, Johnson PTJ (2011) Beyond immunity: quantifying the effects of host anti-parasite behavior on parasite transmission. Oecologia 165:1043–1050

    Article  PubMed  Google Scholar 

  • Dantzer B, Fletcher QE, Boonstra R, Sheriff MJ (2014) Measures of physiological stress: a transparent or opaque window into the status, management and conservation of species? Conserv Physiol 2:cou023

    Article  PubMed  PubMed Central  Google Scholar 

  • Davis AK (2009) Metamorphosis-related changes in leukocyte profiles of larval bullfrogs (Rana catesbeiana). Comp Clin Pathol 18:181–186

    Article  Google Scholar 

  • Davis AK, Cook KC, Altizer S (2004) Leukocyte profiles in wild house finches with and without mycoplasmal conjunctivitis, a recently emerged bacterial disease. EcoHealth 1:362–373

    Article  Google Scholar 

  • Davis AK, Keel MK, Ferreira A, Maerz JC (2010) Effects of chytridiomycosis on circulating white blood cell distributions of bullfrog larvae (Rana catesbeiana). Comp Clin Pathol 19:49–55

    Article  Google Scholar 

  • Denver RJ (2009) Stress hormones mediate environment–genotype interactions during amphibian development. Gen Comp Endocrinol 164:20–31

    Article  CAS  PubMed  Google Scholar 

  • Durbin MR, Pelcher LR, McClelland SJ, Woodley SK (2021) Effects of early ethanol exposure on Lithobates pipiens tadpole development. J Young Investig 39:38–44

    Google Scholar 

  • Erickson K, Drevets W, Schulkin J (2003) Glucocorticoid regulation of diverse cognitive functions in normal and pathological emotional states. Neurosci Biobehav Rev 27:233–246

    Article  CAS  PubMed  Google Scholar 

  • Fraker ME, Hu F, Cuddapah V, McCollum SA, Relyea RA, Hempel J, Denver RJ (2009) Characterization of an alarm pheromone secreted by amphibian tadpoles that induces behavioral inhibition and suppression of the neuroendocrine stress axis. Horm Behav 55:520–529

    Article  CAS  PubMed  Google Scholar 

  • Fraker ME, Ludsin SA, Luttbeg B, Denver RJ (2021) Stress hormone-mediated antipredator morphology improves escape performance in amphibian tadpoles. Sci Rep 11(1):1–9

    Article  Google Scholar 

  • Gabor CR, Fisher MC, Bosch J (2013) A non-invasive stress assay shows that tadpole populations infected with Batrachochytrium dendrobatidis have elevated corticosterone levels. PLoS ONE 8:e56054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gabor CR, Davis DR, Kim DS, Zabierek KC, Bendik NF (2018) Urbanization is associated with elevated corticosterone in jollyville plateau salamanders. Ecol Ind 85:229–235

    Article  Google Scholar 

  • Gabor CR, Perkins HR, Heitmann AT, Forsburg ZR, Aspbury AS (2019) Roundup™ with corticosterone functions as an infodisruptor to antipredator response in tadpoles. Front Ecol Evol. https://doi.org/10.3389/fevo.2019.00114

    Article  Google Scholar 

  • Gassen J, Prokosch ML, Makhanova A, Eimerbrink MJ, White JD, Proffitt Leyva RP, Peterman JL, Nicolas SC, Reynolds TA, Maner JK, McNulty JK (2018) Behavioral immune system activity predicts downregulation of chronic basal inflammation. PLoS ONE 13:e0203961

    Article  PubMed  PubMed Central  Google Scholar 

  • Gibson AK, Amoroso CR (2022) Evolution and ecology of parasite avoidance. Annu Rev Ecol Evol Syst 53:47–67

    Article  PubMed  PubMed Central  Google Scholar 

  • Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190

    Google Scholar 

  • Hadji-Azimi I, Coosemans V, Canicatti C, Perrenot N (1987) Atlas of adult Xenopus laevis laevis hematology. Dev Comp Immunol 11:807–874

    Article  CAS  PubMed  Google Scholar 

  • Hale R, Piggott JJ, Swearer SE (2016) Describing and understanding behavioral responses to multiple stressors and multiple stimuli. Ecol Evol 7:38–47

    Article  PubMed  PubMed Central  Google Scholar 

  • Hall MD, Bento G, Ebert D (2017) The evolutionary consequences of stepwise infection processes. Trends Ecol Evol 32:612–623

    Article  PubMed  Google Scholar 

  • Harris BN, Carr JA (2016) The role of the hypothalamus–pituitary–adrenal/interrenal axis in mediating predator-avoidance trade-offs. Gen Comp Endocrinol 230:110–142

    Article  PubMed  Google Scholar 

  • Hart BL (1990) Behavioral adaptations to pathogens and parasites-5 Strategies. Neurosci Biobehav Rev 14:273–294

    Article  CAS  PubMed  Google Scholar 

  • Hart BL (1997) Behavioural defence. In: Clayton DH, Moore J (eds) Host-parasite evolution: General principles and avian models. Oxford University Press, pp 59–77

    Chapter  Google Scholar 

  • Hart BL, Hart LA (2018) How mammals stay healthy in nature: the evolution of behaviours to avoid parasites and pathogens. Philos Trans R Soc Lond B Biol Sci 373:20170205

    Article  PubMed  PubMed Central  Google Scholar 

  • Hing S, Narayan EJ, Thompson RA, Godfrey SS (2016) The relationship between physiological stress and wildlife disease: consequences for health and conservation. Wildl Res 43:51–60

    Article  Google Scholar 

  • Holland M, Skelly DK, Kashgarian M, Bolden SR, Harrison LM, Cappello M (2007) Echinostome infection in green frogs (Rana clamitans) is stage and age dependent. Jzool 271:455–462

    Google Scholar 

  • Hopkins WA, Mendonça MT, Congdon JD (1997) Increased circulating levels of testosterone and corticosterone in southern toads, Bufo terrestris, exposed to coal combustion waste. Gen Comp Endocrinol 108:237–246

    Article  CAS  PubMed  Google Scholar 

  • 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? Écoscience 17:100–108

    Article  Google Scholar 

  • Hossie T, Landolt K, Murray DL (2017) Determinants and co-expression of anti-predator responses in amphibian tadpoles: a meta-analysis. Oikos. https://doi.org/10.1111/oik.03305

    Article  Google Scholar 

  • Karvonen A, Seppälä O, Valtonen ET (2004) Parasite resistance and avoidance behaviour in preventing eye fluke infections in fish. Parasitol 129:159–164

    Article  CAS  Google Scholar 

  • Kernbach ME, Hall RJ, Burkett-Cadena ND, Unnasch TR, Martin LB (2018) Dim light at night: physiological effects and ecological consequences for infectious disease. Integr Comp Biol 58:995–1007

    CAS  PubMed  Google Scholar 

  • Kiesecker JM (2002) Synergism between trematode infection and pesticide exposure: a link to amphibian limb deformities in nature? PNAS 99:9900–9904

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kiesecker JM, Skelly DK, Beard KH, Preisser E (1999) Behavioral reduction of infection risk. PNAS 96:9165–9168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim KS, Han PL (2006) Optimization of chronic stress paradigms using anxiety-and depression-like behavioral parameters. J Neurosci Res 83(3):497–507

    Article  CAS  PubMed  Google Scholar 

  • Klemme I, Karvonen A (2016) Vertebrate defense against parasites: interactions between avoidance, resistance, and tolerance. Ecol Evol 7:561–571

    Article  PubMed  PubMed Central  Google Scholar 

  • Klemme I, Hyvärinen P, Karvonen A (2020) Negative associations between parasite avoidance, resistance and tolerance predict host health in salmonid fish populations. Proc R Soc B Biol Sci 287:20200388

    Article  Google Scholar 

  • Koprivnikar J, Penalva L (2015) Lesser of two evils? Foraging choices in response to threats of predation and parasitism. PLoS ONE 10:e0116569

    Article  PubMed  PubMed Central  Google Scholar 

  • Koprivnikar J, Urichuk TMY (2017) Time-lagged effect of predators on tadpole behaviour and parasite infection. Biol Lett 13:20170440

    Article  PubMed  PubMed Central  Google Scholar 

  • Koprivnikar J, Forbes MR, Baker RL (2006) On the efficacy of anti-parasite behaviour: a case study of tadpole susceptibility to cercariae of Echinostoma trivolvis. Can J Zool 84:1623–1629

    Article  Google Scholar 

  • Koprivnikar J, Marcogliese DJ, Rohr JR, Orlofske SA, Raffel TR, Johnson PT (2012a) Macroparasite infections of amphibians: what can they tell us? EcoHealth 9:342–360

    Article  PubMed  Google Scholar 

  • Koprivnikar J, Gibson CH, Redfern JC (2012b) Infectious personalities: behavioural syndromes and disease risk in larval amphibians. Proc R Soc B Biol Sci 279:1544–1550

    Article  Google Scholar 

  • Koprivnikar J, Redfern JC, Mazier HL (2014) Variation in anti-parasite behaviour and infection among larval amphibian species. Oecologia 174:1179–1185

    Article  PubMed  Google Scholar 

  • Koprivnikar J, Hoye BJ, Urichuk TM, Johnson PT (2019) Endocrine and immune responses of larval amphibians to trematode exposure. Parasitol Res 118:275–288

    Article  PubMed  Google Scholar 

  • Kulkarni PS, Gramapurohit NP (2017) Effect of corticosterone on larval growth, antipredator behaviour and metamorphosis of Hylarana indica. Gen Comp Endocrinol 251:21–29

    Article  CAS  PubMed  Google Scholar 

  • LaFonte BE, Johnson PTJ (2013) Experimental infection dynamics: using immunosuppression and in vivo parasite tracking to understand host resistance in an amphibian-trematode system. J Exp Biol 216:3700–3708

    PubMed  Google Scholar 

  • Lopes PC (2017) Why are behavioral and immune traits linked? Horm Behav 88:52–59

    Article  PubMed  Google Scholar 

  • MacDougall-Shackleton SA, Bonier F, Romero LM, Moore IT (2019) Glucocorticoids and “stress” are not synonymous. Integr Comp Biol 1:obz017

    CAS  Google Scholar 

  • Marcogliese DJ, King KC, Salo HM, Fournier M, Brousseau P, Spear P, Champoux L, McLaughlin JD, Boily M (2009) Combined effects of agricultural activity and parasites on biomarkers in the bullfrog, Rana catasbeiana. Aquat Toxicol 91:126–134

    Article  CAS  PubMed  Google Scholar 

  • Martin LB (2009) Stress and immunity in wild vertebrates: timing is everything. Gen Comp Endocrinol 163:70–76

    Article  CAS  PubMed  Google Scholar 

  • Martin TR, Conn DB (1990) The pathogenicity, localization, and cyst structure of echinostomatid metacercariae (trematoda) infecting the kidneys of the frogs Rana clamitans and Rana pipiens. J Parasitol 76:414–419

    Article  CAS  PubMed  Google Scholar 

  • Martin LB, Gilliam J, Han P, Lee K, Wikelski M (2005) Corticosterone suppresses cutaneous immune function in temperate but not tropical house sparrows, Passer domesticus. Gen Comp Endocrinol 140:126–135

    Article  CAS  Google Scholar 

  • McCarthy AM (1999) The influence of temperature on the survival and infectivity of the cercariae of Echinoparyphium recurvatum (Digenea: Echinostomatidae). Parasitol 118(4):383–388

    Article  Google Scholar 

  • McClelland SJ, Woodley SK (2021) Water-borne corticosterone assay is a valid method in some but not all life-history stages in northern leopard frogs. Gen Comp Endocrinol 312:113858

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Milotic D, Milotic M, Koprivnikar J (2017) Effects of road salt on larval amphibian susceptibility to parasitism through behavior and immunocompetence. Aquat Toxicol 189:42–49

    Article  CAS  PubMed  Google Scholar 

  • Munns J (2006) Assessing risks to wildlife populations from multiple stressors: overview of the problem and research needs. Ecol Soc 11:23

    Article  Google Scholar 

  • Myers B, McKlveen JM, Herman JP (2014) Glucocorticoid actions on synapses, circuits, and behavior: Implications for the energetics of stress. Front Neuroendocrinol 35:180–196

    Article  CAS  PubMed  Google Scholar 

  • Narayan EJ, Forsburg ZR, Davis DR, Gabor CR (2019) Non-invasive methods for measuring and monitoring stress physiology in imperiled amphibians. Front Ecol Evol 7:431

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Oppliger A, Clobert J, Lecomte J, Lorenzon P, Boudjemadi K, John-Alder H (1998) Environmental stress increases the prevalence and intensity of blood parasite infection in the common lizard Lacerta vivipara. Ecol Lett 1:129–138

    Article  Google Scholar 

  • Parker BJ, Barribeau SM, Laughton AM, de Roode JC, Gerardo NM (2011) Non-immunological defense in an evolutionary framework. Trends Ecol Evol 26:242–248

    Article  PubMed  Google Scholar 

  • R Core Team (2021) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  • Råberg L, Sim D, Read AF (2007) Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science 318(5851):812–814

    Article  PubMed  Google Scholar 

  • Råberg L, Graham AL, Read AF (2009) Decomposing health: tolerance and resistance to parasites in animals. Philos Trans R Soc Lond B Biol Sci 364(1513):37–49

    Article  PubMed  Google Scholar 

  • Raffel TR, Martin LB, Rohr JR (2008) Parasites as predators: unifying natural enemy ecology. Trends Ecol Evol 23:610–618

    Article  PubMed  Google Scholar 

  • Rollins-Smith LA (2001) Neuroendocrine-immune system interactions in amphibians: implications for understanding global amphibian declines. Immunol Res 23:273–280

    Article  CAS  PubMed  Google Scholar 

  • Rollins-Smith LA (2017) Amphibian immunity–stress, disease, and climate change. Dev Comp Immunol 66:111–119

    Article  CAS  PubMed  Google Scholar 

  • Rollins-Smith LA, Blair PJ (1993) The effects of corticosteroid hormones and thyroid hormones on lymphocyte viability and proliferation during development and metamorphosis of Xenopus laevis. Differentiation 54(3):155–160

    Article  CAS  PubMed  Google Scholar 

  • Romero LM (2004) Physiological stress in ecology: lessons from biomedical research. Trends Ecol Evol 19:249–255

    Article  PubMed  Google Scholar 

  • Romero LM, Beattie UK (2022) Common myths of glucocorticoid function in ecology and conservation. J Exp Zool Part A Ecol Integr Physiol 337(1):7–14

    Article  CAS  Google Scholar 

  • Romero LM, Dickens MJ, Cyr NE (2009) The reactive scope model—a new model integrating homeostasis, allostasis, and stress. Horm Behav 55(3):375–389

    Article  PubMed  Google Scholar 

  • Rosen JB, Donley MP, Gray D, West EA, Morgan MA, Schulkin J (2008) Chronic corticosterone administration does not potentiate unconditioned freezing to the predator odor, trimethylthiazoline. Behav Brain Res 194:32–38

    Article  CAS  PubMed  Google Scholar 

  • RStudio Team (2021) RStudio: integrated development for R. RStudio, Boston, MA. http://www.rstudio.com/

  • 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

    CAS  PubMed  Google Scholar 

  • Schaller M, Park JH (2011) The behavioral immune system (and why it matters). Curr Dir Psychol Sci 20:99–103

    Article  Google Scholar 

  • Schell SC (1985) Handbook of trematodes of North America north of Mexico. University Press of Idaho, Caldwell

    Google Scholar 

  • Schotthoefer AM, Cole RA, Beasley VR (2003) Relationship of tadpole stage to location of echinostome cercariae encystment and the consequences for tadpole survival. J Parasitol 89:475–482

    Article  PubMed  Google Scholar 

  • Schreier K, Grindstaff J (2020) Repeatable behavioural and immune defence strategies against infection are not traded off. Anim Behav 162:11–22

    Article  Google Scholar 

  • Sears BF, Snyder PW, Rohr JR (2013) Infection deflection: hosts control parasite location with behaviour to improve tolerance. Proc R Soc B Biol Sci 280(1762):20130759

    Article  CAS  Google Scholar 

  • Sheriff MJ, Dantzer B, Delehanty B, Palme R, Boonstra R (2011) Measuring stress in wildlife: techniques for quantifying glucocorticoids. Oecologia 166(4):869–887

    Article  PubMed  Google Scholar 

  • Stephenson JF (2019) Parasite-induced plasticity in host social behaviour depends on sex and susceptibility. Biol Lett 15:20190557

    Article  PubMed  PubMed Central  Google Scholar 

  • Strehl C, Ehlers L, Gaber T, Buttgereit F (2019) Glucocorticoids—all-rounders tackling the versatile players of the immune system. Front Immunol 10:1744

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sullivan AM, Kratzer IE, Jobe SC, Lewis JL (2021) Combined effects of experimentally elevated CORT and predation threat on exploratory and foraging behavior of Desmognathus ochrophaeus. J Herpetol 55:208–214

    Article  Google Scholar 

  • Szuroczki D, Richardson JML (2009) The role of trematode parasites in larval anuran communities: an aquatic ecologist’s guide to the major players. Oecologia 161:371–385

    Article  PubMed  Google Scholar 

  • Szuroczki D, Richardson JM (2012) The behavioral response of larval amphibians (Ranidae) to threats from predators and parasites. PLoS ONE 7(11):e49592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor CN, Oseen KL, Wassersug RJ (2004) On the behavioural response of Rana and Bufo tadpoles to echinostomatoid cercariae: implications to synergistic factors influencing trematode infections in anurans. Can J Zool 82:701–706

    Article  Google Scholar 

  • Thaker M, Lima SL, Hews DK (2009) Acute corticosterone elevation enhances antipredator behaviors in male tree lizard morphs. Horm Behav 56:51–57

    Article  CAS  PubMed  Google Scholar 

  • Thompson SN, Kavaliers M (1994) Physiological bases for parasite-induced alterations of host behaviour. Parasitol 109:S119–S138

    Article  Google Scholar 

  • Tornabene BJ, Hossack BR, Crespi EJ, Breuner CW (2021) Evaluating corticosterone as a biomarker for amphibians exposed to increased salinity and ambient corticosterone. Conserv Physiol 9:coab049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vinterstare J, Hegemann A, Nilsson PA, Hulthén K, Brönmark C (2019) Defence versus defence: are crucian carp trading off immune function against predator-induced morphology? J Anim Ecol 88:1510–1521

    Article  PubMed  Google Scholar 

  • Wingfield JC, Sapolsky R (2003) Reproduction and resistance to stress: when and how. Jneuroendocrinol 15:711–724

    Article  CAS  Google Scholar 

  • Wingfield J, Maney DL, Breuner CW, Jacobs JD, Lynn S, Ramenofsky M, Richardson RD (1998) Ecological bases of hormone–behavior interactions: the “emergency life history stage.” Am Zool 38:191–206

    Article  CAS  Google Scholar 

  • Woodley SK, Lacy EL (2010) An acute stressor alters steroid hormone levels and activity but not sexual behavior in male and female ocoee salamanders (Desmognathus ocoee). Horm Behav 58:427–432

    Article  CAS  PubMed  Google Scholar 

  • Zylberberg M, Klasing KC, Hahn TP (2013) House finches (Carpodacus mexicanus) balance investment in behavioural and immunological defences against pathogens. Biol Lett 9:20120856

    Article  PubMed  PubMed Central  Google Scholar 

  • Zylberberg M, Klasing KC, Hahn TP (2014) In house finches, haemorhous mexicanus, risk takers invest more in innate immune function. Anim Behav 89:115–122

    Article  Google Scholar 

Download references

Acknowledgements

The authors wish to thank the following for their contribution to lab work and project data discussions: Lucia Santos, Brad Jacobs and Tsukushi Kamiya.

Funding

This study was funded by a NSERC Discovery Grant to J.K.

Author information

Author notes

  1. Katie O’Dwyer

    Present address: Marine and Freshwater Research Centre, Atlantic Technological University, Old Dublin Road, Co., Galway, Ireland

  2. Dino Milotic & Marin Milotic

    Present address: Harry Butler Institute, Murdoch University, Perth, WA, Australia

Authors and Affiliations

  1. Department of Chemistry and Biology, Toronto Metropolitan University, Toronto, ON, Canada

    Katie O’Dwyer, Dino Milotic, Marin Milotic & Janet Koprivnikar

Authors
  1. Katie O’Dwyer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dino Milotic
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marin Milotic
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Janet Koprivnikar
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

JK and KoD conceived and designed the experiments. KoD performed the experiments. KoD, DM and MM collected the data. KoD analysed the data. KoD and JK wrote the manuscript; other authors provided editorial advice.

Corresponding author

Correspondence to Katie O’Dwyer.

Ethics declarations

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. Animals were used in accordance with the Canadian Council on Animal Care guidelines, and with institutional approval from the animal care committee (AUP 633).

Additional information

Communicated by Bryan Brown.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 176 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

O’Dwyer, K., Milotic, D., Milotic, M. et al. Behave yourself: effects of exogenous-glucocorticoid exposure on larval amphibian anti-parasite behaviour and physiology. Oecologia (2024). https://doi.org/10.1007/s00442-024-05547-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00442-024-05547-6

Keywords

Search

Navigation