A Review of the Physiological and Behavioural Consequences of Cold Shock on FishM.R. Donaldson1, S. Yu2 and S.J. Cooke1,21 Ottawa-Carleton Institute of Biology, Carleton University, 1125 Colonel By Drive, Ottawa, ON, Canada, K1S 5B6; 2 Institute of Environmental Science, Carleton University, 1125 Colonel By Drive, Ottawa, ON, Canada, K1S 5B6ABSTRACT A rapid decrease in water temperature, termed cold shock, may result in a number of negative physiological and behavioural consequences for fishes. Sensitivity to different magnitudes of cold shock can be difficult to predict because there is a tendency for interspecific and intraspecific tolerances to vary due to different acclimation temperatures and genetic differences. Physiological responses to cold shock stress can be categorized as: primary (i.e., catecholamine and corticosteroid release into circulation), secondary (i.e., haematological, metabolic, cellular, osmoregulatory and immunologic responses) and tertiary (i.e., growth inhibition, disease susceptibility, reduced fecundity and behavioural changes). Behavioural responses to cold shock include changes in habitat use, foraging, reproduction and migration. We reviewed available cold shock literature to synthesize current knowledge and to identify research gaps. Our objectives were to identify relevant natural and anthropogenic sources of cold shock, document the effects of cold shock on the physiology and behaviour of fish, and evaluate the adverse effects of cold shock on population dynamics, community structure and aquatic ecosystem function. We conclude by discussing management implications and identifying directions for future research. Cold shock is now widely recognized as a significant stressor on fish and fish populations. However, there are still few examples of studies that combine multiple endpoints (e.g., behaviour and physiology) or that link laboratory studies with data collected in field settings.CONTEXT Acute decreases in water temperature from natural or anthropogenic sources can result in cold shock stress for fishes. Natural cold shock sources include thermoclines, abnormal seiches and water movements and rapid changes in seasonal temperatures. Anthropogenic cold shock sources include rapid termination of thermal effluents from industrial and power generation plants or the transfer of harvested fish from ambient temperatures to temporary cold-water storage. Cold shock initiates adaptive primary, secondary and tertiary physiological and behavioural stress responses. The consequences of cold shock are highly variable and depend on the magnitude of temperature change, genetic differences, stage of development, acclimation and thermal history, as well as interspecific and intraspecific physiological and behavioural differences. A cold shock synthesis was last published in the mid- to late- 1970s to examine fish kills at power generating plant thermal discharge canals (Coutant 1977). In recent years, technological and methodological advancements (i.e., HSP techniques, fMRI) have allowed for further characterization of the cold shock response in fishes, but the literature is diffuse and disparate.

GOALS

To synthesize and review relevant and current (i.e., post-1975) cold shock literature. To define cold shock in terms of primary, secondary and tertiary physiological and behavioural stress responses. To consider management implications of cold shock and identify areas of future research.Figure 1: Articles reviewed by decade from 1970 to present (n=201). Although early research on cold shock was fueled by the need to understand the effects of power plant effluents on fish, cold shock is now being used as a convenient and useful stressor for basic research on organismal biology. Figure 2: Primary, secondary and tertiary stress responses to cold shock. Stress responses may be interactive, such that primary and secondary responses may affect secondary and tertiary responses. CONCLUSIONS AND FUTURE DIRECTIONS Cold shock represents a major stressor for fish and is increasingly being recognized as a convenient stressor for basic research on organismal biology. Limited evidence suggests that HSPs may be sensitive to cold shock, but further research is required to determine their specific role in the cold shock stress response. The immune response at low temperatures is generally well understood, but few studies have examined the effects of acute temperature decreases on immune function and susceptibility to disease, particularly for infections of cold-water disease. There is a need for more integrative research that spans disciplines (e.g., behaviour and physiology) and that links laboratory and field research. Many studies have found differences in interspecific and intraspecific responses to cold shock. In the future, these differences must be scrutinized to identify high-risk populations/species in order to inform management strategies. SYNTHESIS OF COLD SHOCK RESEARCHACKNOWLEDGEMENTS

Funding provided by Fisheries and Oceans Canada and Carleton University.0102030405060701970-19741975-19791980-19841985-19891990-19941995-19992000-PresentYearNumber of ArticlesDOW, Washington D.C.Fortum, Finland

Primary Response

Cold shock results in changes in activation states of the hypothalamus and pituitary gland

Sympathetic nerve fibres stimulate catecholamine release from chromaffin tissue

Hypothalamus-pituitary-interrenal axis stimulates the release of cortisol

Release of cortisol is delayed relative to catecholamine release

Cortisol is a sensitive indicator of cold shock but is less sensitive to gradual temperature changesSecondary Response

Hematocrit, leucocrit and plasma concentrations of lactic acid are highly variable and may not be sensitive indicators of acute temperature stress

Heat Shock Proteins (HSPs) are sensitive stress indicators, but are not well understood in relation to cold shock

Cold shock reduces the active influx of ions while diffusional efflux remains constant, resulting in net loss of ions for freshwater fishes

Cold shock may affect immune function, particularly for immune- compromised fishesTertiary Response

Developmental rates and juvenile mortality are increased at low temperatures

Fish preferentially select habitat based on temperature (i.e., selection of power plant thermal plumes in winter)

Cold shock affects swimming behaviour and predation rates

Temperature shock can lead to accelerated cataract development and incidence of cold-water disease

Cold shock does not appear to cause physical damage to gill tissue