A Review of the Physiological and Behavioural Consequences of

1
A Review of the Physiological and Behavioural
Consequences of Cold Shock on Fish
Fortum, Finland
M.R. Donaldson1, S. Yu2 and S.J. Cooke1,2
DOW, Washington D.C.
1 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 5B6
ABSTRACT 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.
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.

• 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.

SYNTHESIS OF COLD SHOCK RESEARCH
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 changes Secondary 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 fishes Tertiary 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

• 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.

70
60
50
40
Number of Articles
30
20
10
0
1970-1974
1975-1979
1980-1984
1985-1989
1990-1994
1995-1999
2000-
Present
Year
Figure 1 Articles reviewed by decade from 1970
to present (n201). 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.
ACKNOWLEDGEMENTS
Funding provided by Fisheries and Oceans Canada
and Carleton University.