An experimental evaluation of the role of the stress axis in mediating predator-prey interactions in wild marine fish

Michael J Lawrence; Erika J Eliason; Jacob W Brownscombe; Kathleen M Gilmour; John W Mandelman; Steven J Cooke

doi:10.1016/j.cbpa.2017.02.001

An experimental evaluation of the role of the stress axis in mediating predator-prey interactions in wild marine fish

Comp Biochem Physiol A Mol Integr Physiol. 2017 May:207:21-29. doi: 10.1016/j.cbpa.2017.02.001. Epub 2017 Feb 7.

Authors

Michael J Lawrence¹, Erika J Eliason², Jacob W Brownscombe³, Kathleen M Gilmour⁴, John W Mandelman⁵, Steven J Cooke³

Affiliations

¹ Fish Ecology and Conservation Physiology Laboratory, Department of Biology, Carleton University, Ottawa, ON K1S 5B6, Canada. Electronic address: m_lawrence27@live.ca.
² Fish Ecology and Conservation Physiology Laboratory, Department of Biology, Carleton University, Ottawa, ON K1S 5B6, Canada; Department of Ecology, Evolution and Marine Biology, University of California at Santa Barbara, Santa Barbara, CA 93106, USA.
³ Fish Ecology and Conservation Physiology Laboratory, Department of Biology, Carleton University, Ottawa, ON K1S 5B6, Canada.
⁴ Department of Biology, University of Ottawa, Ottawa, ON K1N 6N5, Canada.
⁵ School for the Environment, University of New England, Biddeford, ME 04005, USA; John H. Prescott Marine Laboratory, New England Aquarium, Boston, ME 02110, USA.

PMID: 28185867
DOI: 10.1016/j.cbpa.2017.02.001

Abstract

The hypothalamic-pituitary-interrenal (HPI) axis, through corticosteroid secretion, is an integral mechanism regulating internal homeostasis when vertebrates are faced with a stressor. However, continued HPI-axis stimulation can produce homeostatic overload, where corticosteroids are detrimental to organismal function. This overload condition may play an important role in mediating predator-prey interactions, because chronically/previously stressed animals may have higher rates of predator-induced mortality. However, the mechanism(s) underlying this observation are unknown. Using fish as models, we hypothesized that chronic stress would increase predation susceptibility owing to a poor physiological state (e.g. homeostatic overload) with corresponding sub-optimal changes in predator-avoidance behaviour. As cortisol is also required in low quantities to help regulate basic metabolic functions in fish, we expected that a glucocorticoid receptor antagonist (GR; e.g. homeostatic failure) may produce similar effects. Schoolmaster snapper (Lutjanus apodus) were given intraperitoneal implants of cocoa butter impregnated with nothing (sham; 5ml/kg body weight (BW)), cortisol (50mg/kg BW) or the GR antagonist RU486 (100mg/kg BW). At 24-h post-implantation, fish were tethered to the seafloor and observed for behavioural metrics associated with predation. Blood samples were collected from a subset of fish to assess the physiological consequences of the implants. Cortisol- and RU486-implanted fish both had significantly higher plasma cortisol concentrations than sham fish, with blood glucose and plasma urea being elevated only in the former. Further, anti-predator behaviours and predation mortality did not differ significantly among treatments. Despite changes in physiological state, predation susceptibility was unaffected, a finding that may reflect the complex relationships linking the physiology and behaviour of an organism as well as potential tethering artefacts.

Keywords: Cortisol; Homeostatic overload; Lutjanus apodus; Negaprion brevirostris; Predation; RU486.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Hydrocortisone / pharmacology
Hypothalamo-Hypophyseal System / drug effects
Hypothalamo-Hypophyseal System / metabolism*
Mifepristone / pharmacology
Perciformes / physiology*
Predatory Behavior / drug effects
Predatory Behavior / physiology*
Stress, Physiological / drug effects

Substances

Mifepristone
Hydrocortisone