Erika J. Eliason

Ecology of Exercise in Wild Fish: Integrating Concepts of Individual Physiological Capacity, Behavior, and Fitness Through Diverse Case Studies

SYNOPSISnWild animals maximize fitness through certain behaviors (e.g., foraging, mating, predator avoidance) that incur metabolic costs and often require high levels of locomotor activity. Consequently, the ability of animals to achieve high fitness often relies on their physiological capacity for exercise (aerobic scope) and/or their ability to acquire and utilize energy judiciously. Here, we explore how environmental factors and physiological limitations influence exercise and metabolism in fish while foraging, migrating to spawning grounds, and providing parental care. We do so with three case studies that use a number of approaches to studying exercise in wild fish using biologging and biotelemetry platforms. Bonefish (Albula vulpes) selectively use shallow water tropical marine environments to forage when temperatures are near optimal for aerobic scope and exercise capacity. Bonefish energy expenditure at upper thermal extremes is maximal while activity levels diminish, likely caused by reduced aerobic scope. Pacific salmon (Oncorhynchus spp.) reproductive migrations frequently involve passage through hydraulically challenging areas, and their ability to successfully pass these regions is constrained by their physiological capacity for exercise. Aerobic scope and swim performance are correlated with migration difficulty among sockeye salmon (O. nerka) populations; however, depletion of endogenous energy stores can also limit migration success. In another example, male smallmouth bass (Micropterus dolomieu) allocate a significant amount of energy to nest-guarding behaviors to protect their developing brood. Smallmouth bass body size, endogenous energy reserves, and physiological state influence nest-guarding behaviors and reproductive success. We suggest that in some scenarios (e.g., bonefish foraging, Pacific salmon dam passage) metabolic capacity for exercise may be the strongest determinant of biological fitness, while in others (e.g., long distance salmon migration, smallmouth bass parental care) energy stores may be more important. Interactions among environmental and ecological factors, fish behavior, and fish physiology offer important avenues of mechanistic inquiry to explain ecological dynamics and demonstrate how exercise is fundamental to the ecology of fish.

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

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.

Influence of supraphysiological cortisol manipulation on predator avoidance behaviours and physiological responses to a predation threat in a wild marine teleost fish

The stress axis in teleost fish attempts to maintain internal homeostasis in the face of allostatic loading. However, stress axis induction has been associated with a higher predation rate in fish. To date, the physiological and behavioral factors associated with this outcome are poorly understood. The purpose of the present study was to investigate the impact of experimental cortisol elevation on anti-predator behavior and physiological responses to predator presence. We hypothesized that semi-chronic cortisol elevation would increase susceptibility to predation by increasing stress-induced risk-taking behaviors. To test this hypothesis, schoolmaster snapper were given cocoa butter implants without cortisol (sham) or with cortisol (50 mg/kg body weight) and tethered to cover. Fish were exposed to either a lemon shark or control conditions for 15-min. Space use and activity were recorded throughout and fish were terminally sampled for blood. Cortisol implantation, relative to shams, resulted in higher blood glucose and plasma cortisol concentrations with a lower plasma lactate concentration. Shark exposure, relative to controls, elicited higher blood glucose and lactate concentrations but had no effect on plasma cortisol concentration. No interactions were detected between shark exposure and cortisol treatment for any physiological trait. Behavioral metrics, including shelter use and activity, were unaffected by either cortisol implantation or shark exposure. Physiological responses to cortisol implantation likely resulted from enhanced gluconeogenic activity, whereas alterations under predator exposure may have been the product of catecholamine mobilization. Further work should address context-specific influences of stress in mediating behavioral responses to predation.