Cold shock and fish
TL;DR: This review synthesizes the sublethal physiological and behavioural consequences of cold-shock stress on fishes, identifies natural and anthropogenic sources ofcold shock, discusses the benefits of cold shock to fisheries science and describes mitigation and management efforts.
Abstract: Rapid decreases in water temperature may result in a number of physiological, behavioural and fitness consequences for fishes termed ‘cold shock’. Cold-shock stress occurs when a fish has been acclimated to a specific water temperature or range of temperatures and is subsequently exposed to a rapid decrease in temperature, resulting in a cascade of physiological and behavioural responses and, in some cases, death. Rapid temperature decreases may occur from either natural (e.g. thermocline temperature variation, seiches and storm events) or anthropogenic sources (e.g. varied thermal effluents from power generation and production industries). The magnitude, duration and frequency of the temperature change as well as the initial acclimation temperatures of individuals can influence the extent of the consequences of cold shock on fishes. Early research on cold shock focused on documenting mortality events associated with cold shock. However, in recent years, a shift in research has occurred where the focus of cold-shock studies now involves characterizing the sublethal effects of cold shock in terms of the stress response in fishes. This shift has revealed that cold shock can actually be used as a tool for fisheries science (e.g. to induce polyploidy). The cold-shock stress response offers opportunities to develop many exciting research questions, yet to date, cold-shock research has been largely unfocused. Few studies attempt to link laboratory physiology experiments with ecologically relevant field data on behaviour, growth, bioenergetics and fitness. Additional research will allow for the development of more focused and robust management policies and conservation initiatives. This review synthesizes the sublethal physiological and behavioural consequences of cold-shock stress on fishes, identifies natural and anthropogenic sources of cold shock, discusses the benefits of cold shock to fisheries science and describes mitigation and management efforts. Existing knowledge gaps and opportunities for future cold-shock research are presented.
Citations
More filters
TL;DR: While polyploid fish and amphibians share a number of attributes facilitatingpolyploidy, clear drivers of genome duplication do not emerge from the comparison and the lack of a clear association of sexually reproducing polyploids with range expansion, harsh environments, or risk of extinction could suggest that stronger correlations in plants may be driven by shifts in mating system more than ploidy.
Abstract: Whole genome duplication (leading to polyploidy) is widely accepted as an important evolutionary force in plants, but it is less recognized as a driver of animal diversification. Nevertheless, it occurs across a wide range of animals; this review investigates why it is particularly common in fish and amphibians, while rare among other vertebrates. We review the current geographic, ecological and phylogenetic distributions of sexually reproducing polyploid taxa before focusing more specifically on what factors drive polyploid formation and establishment. In summary, (1) polyploidy is phylogenetically restricted in both amphibians and fishes, although entire fish, but not amphibian, lineages are derived from polyploid ancestors. (2) Although mechanisms such as polyspermy are feasible, polyploid formation appears to occur principally through unreduced gamete formation, which can be experimentally induced by temperature or pressure shock in both groups. (3) External reproduction and fertilization in primarily temperate freshwater environments potentially exposes zygotes to temperature stress, which can promote increased production of unreduced gametes. (4) Large numbers of gametes and group breeding in relatively confined areas could increase the probability of compatible gamete combinations in both groups. (5) Both fish and amphibians have a propensity to form reproductively successful hybrids; although the relative frequency of autopolyploidy versus allopolyploidy is difficult to ascertain, multiple origins involving hybridization have been confirmed for a number of species in both groups. (6) Problems with establishment of polyploid lineages associated with minority cytotype exclusion could be overcome in amphibians via assortative mating by acoustic recognition of the same ploidy level, but less attention has been given to chemical or acoustic mechanisms that might operate in fish. (7) There is no strong evidence that polyploid fish or amphibians currently exist in more extreme environments than their diploid progenitors or have broader ecological ranges. (8) Although pathogens could play a role in the relative fitness of polyploid species, particularly given duplication of genes involved in immunity, this remains an understudied field in both fish and amphibians. (9) As in plants, many duplicate copies of genes are retained for long periods of time, indicative of selective maintenance of the duplicate copies, but we find no physiological or other reasons that could explain an advantage for allelic or genetic complexity. (10) Extant polyploid species do not appear to be more or less prone to extinction than related diploids in either group. We conclude that, while polyploid fish and amphibians share a number of attributes facilitating polyploidy, clear drivers of genome duplication do not emerge from the comparison. The lack of a clear association of sexually reproducing polyploids with range expansion, harsh environments, or risk of extinction could suggest that stronger correlations in plants may be driven by shifts in mating system more than ploidy. However, insufficient data currently exist to provide rigorous tests of these hypotheses and we make a plea for zoologists to also consider polyploidy as a possibility in continuing taxonomic surveys.
222 citations
Cites background from "Cold shock and fish"
...In fishes, although 37 different ways of inducing polyploidy have been described (Pandian &Koteeswaran, 1998), polyploids have most commonly been induced by either temperature or pressure shock, with cold shock typically favoured for warm water species and warm shock favoured for cold water species (Donaldson et al., 2008)....
[...]
...While pressure shock is not relevant to polyploidy formation in wild systems, cold or heat shocks may occur naturally through changes in thermoclines, water movements such as flooding or snow melting, heavy precipitation or rapid changes in seasonal temperatures (Donaldson et al., 2008)....
[...]
...…ways of inducing polyploidy have been described (Pandian &Koteeswaran, 1998), polyploids have most commonly been induced by either temperature or pressure shock, with cold shock typically favoured for warm water species and warm shock favoured for cold water species (Donaldson et al., 2008)....
[...]
TL;DR: Observations of habitat occupation suggest that adult cod will be able to tolerate warming seas, but that climate change will affect cod populations at earlier life-history stages as well as exerting effects on cod prey species.
Abstract: Recent studies in the marine environment have suggested that the limited phenotypic plasticity of cold-adapted species such as Atlantic cod Gadus morhua L. will cause distributions to shift toward the poles in response to rising sea temperatures. Some cod stocks are predicted to collapse, but this remains specu- lative because almost no information is available on the thermal tolerance of cod in its natural environment. We used electronic tags to measure the thermal experience of 384 adult Atlantic cod from 8 different stocks in the northeast Atlantic. Over 100 000 d of data were col- lected in total. The data demonstrate that cod is an adaptable and tolerant species capable of surviving and growing in a wide range of temperate marine climates. The total thermal niche ranged from -1.5 to 19°C; this range was narrower (1 to 8°C) during the spawning season. Cod in each of the stocks studied had a thermal niche of approximately 12°C, but latitudinal differences in water temperature meant that cod in the warmer, southern regions experienced 3 times the degree days (DD; ~4000 DD yr -1 ) than individuals from northern re- gions (~1200 DD yr -1 ). Growth rates increased with temperature, reaching a maximum in those cod with a mean thermal history of between 8 and 10°C. Our di- rect observations of habitat occupation suggest that adult cod will be able to tolerate warming seas, but that climate change will affect cod populations at earlier life-history stages as well as exerting effects on cod prey species.
216 citations
Cites background from "Cold shock and fish"
...…have suggested that the species distributions may be changing rapidly (Rose 2004, Drinkwater 2005, Perry et al. 2005, Parmesan 2006), but empirical data on the response of marine species to different thermal niches and environments is lacking (Pörtner & Knust 2007, Donaldson et al. 2008)....
[...]
...The evidence of the frequency and magnitude of thermal shocks in wild fish is extremely limited (Donaldson et al. 2008), and these data suggest it may be an important factor in understanding the physiological adaptations of large, mobile fish species....
[...]
TL;DR: Understanding of how absolute levels of indicators relate to stressor severity and recovery to date remains limited, and how accurately indicators characterize stress in wild populations naturally exposed to stressors is still an evolving discussion.
Abstract: 1. Why Do We Measure Stress? 2. Quantifying Stress 3. Specific Measures of Fish Stress 3.1. Cellular and Molecular Indicators 3.2. Primary and Secondary Physiological Indicators 3.3. Whole-Organism Indicators 4. Considerations for Measuring and Interpreting Stress 4.1. Interspecific Differences 4.2. Intraspecific Differences 4.3. Context-Specific Differences 4.4. Stressor Severity 4.5. Field Versus Laboratory 4.6. Temporal Aspects 5. From Individual Indicators to Ecosystem Health 6. Stress Indicators of the Future 7. Conclusion A fish is chased with a net in an aquarium before being captured, scooped out of the water, and placed in a nearby testing arena. Is it stressed? How can we tell? Are our indicators reliable? Quantification of stress in fish has evolved from the initial development of radioimmunoassays to measure cortisol in plasma to the rapidly expanding suite of genome-based assays. Indicators range from the intracellular to whole-animal level. Expression of heat shock proteins (HSPs) and activity of metabolic enzymes can be paired with straightforward observations of reflexes and survival. Both traditional and emerging indicators have advantages and disadvantages, and their use is tissue- and context-specific. Ecological, biological, and methodological factors must be considered when selecting, measuring, and interpreting stress indicators. Inter- and intraspecific, sex, life stage, and temporal differences in physiological responses to stressors can confound confirmation of a stressed state. Despite numerous types of indicators, our understanding of how absolute levels of indicators relate to stressor severity and recovery to date remains limited. How accurately indicators characterize stress in wild populations naturally exposed to stressors is still an evolving discussion. The integration of research disciplines and involvement of stakeholders and user groups will aid in filling these knowledge gaps, as well as the translation of individual-level indicators to population- and ecosystem-level processes.
156 citations
Cites background from "Cold shock and fish"
...…and Somero, 1999) HSPs are sensitive to a range of stressors (eg, rapid temperature changes, salinity challenges, handling; Palmisano et al., 2000; Donaldson et al., 2008) Widely studied, wellunderstood function The expression of HSPs is context-dependent since they are sensitive to the magnitude…...
[...]
TL;DR: The transcriptional responses in larval zebrafish exposed to cold or heat stress are characterized using microarray analysis and provide new interesting clues for elucidation of mechanisms underlying the temperature acclimation in fish.
Abstract: Temperature influences nearly all biochemical, physiological and life history activities of fish, but the molecular mechanisms underlying the temperature acclimation remains largely unknown. Previous studies have identified many temperature-regulated genes in adult tissues; however, the transcriptional responses of fish larvae to temperature stress are not well understood. In this study, we characterized the transcriptional responses in larval zebrafish exposed to cold or heat stress using microarray analysis. In comparison with genes expressed in the control at 28 °C, a total of 2680 genes were found to be affected in 96 hpf larvae exposed to cold (16 °C) or heat (34 °C) for 2 and 48h and most of these genes were expressed in a temperature-specific and temporally regulated manner. Bioinformatic analysis identified multiple temperature-regulated biological processes and pathways. Biological processes overrepresented among the earliest genes induced by temperature stress include regulation of transcription, nucleosome assembly, chromatin organization and protein folding. However, processes such as RNA processing, cellular metal ion homeostasis and protein transport and were enriched in genes up-regulated under cold exposure for 48 h. Pathways such as mTOR signalling, p53 signalling and circadian rhythm were enriched among cold-induced genes, while adipocytokine signalling, protein export and arginine and praline metabolism were enriched among heat-induced genes. Although most of these biological processes and pathways were specifically regulated by cold or heat, common responses to both cold and heat stresses were also found. Thus, these findings provide new interesting clues for elucidation of mechanisms underlying the temperature acclimation in fish.
151 citations
Cites background from "Cold shock and fish"
...The body temperature of most fishes equilibrates rapidly with ambient temperature, so water temperature is suggested to be the abiotic master factor which virtually controls and limits all the biochemical, physiological and life history activities [6,7]....
[...]
...The primary response to cold stress in fish is suggested to be a neuroendocrine response that occurs at the CNS, which triggers the release of corticosteroid and catecholamine hormones, and initiates the secondary responses including metabolic, haematological and osmoregulatory changes [6]....
[...]
TL;DR: The objective of this review was to analyze the published data on the thermal biology of the zebrafish and review of the influence of temperature on several physiological variables, including development, growth, metabolism, reproduction, behavior, circadian biology and toxicology.
146 citations
References
More filters
TL;DR: Although the species studied comprise a small and nonrepresentative sample of the almost 20,000 known teleost species, there are many indications that the stress response is variable and flexible in fish, in line with the great diversity of adaptations that enable these animals to live in a large variety of aquatic habitats.
Abstract: The stress response in teleost fish shows many similarities to that of the terrestrial vertebrates These concern the principal messengers of the brain-sympathetic-chromaffin cell axis (equivalent of the brain-sympathetic-adrenal medulla axis) and the brain-pituitary-interrenal axis (equivalent of the brain-pituitary-adrenal axis), as well as their functions, involving stimulation of oxygen uptake and transfer, mobilization of energy substrates, reallocation of energy away from growth and reproduction, and mainly suppressive effects on immune functions There is also growing evidence for intensive interaction between the neuroendocrine system and the immune system in fish Conspicuous differences, however, are present, and these are primarily related to the aquatic environment of fishes For example, stressors increase the permeability of the surface epithelia, including the gills, to water and ions, and thus induce systemic hydromineral disturbances High circulating catecholamine levels as well as structural damage to the gills and perhaps the skin are prime causal factors This is associated with increased cellular turnover in these organs In fish, cortisol combines glucocorticoid and mineralocorticoid actions, with the latter being essential for the restoration of hydromineral homeostasis, in concert with hormones such as prolactin (in freshwater) and growth hormone (in seawater) Toxic stressors are part of the stress literature in fish more so than in mammals This is mainly related to the fact that fish are exposed to aquatic pollutants via the extensive and delicate respiratory surface of the gills and, in seawater, also via drinking The high bioavailability of many chemicals in water is an additional factor Together with the variety of highly sensitive perceptive mechanisms in the integument, this may explain why so many pollutants evoke an integrated stress response in fish in addition to their toxic effects at the cell and tissue levels Exposure to chemicals may also directly compromise the stress response by interfering with specific neuroendocrine control mechanisms Because hydromineral disturbance is inherent to stress in fish, external factors such as water pH, mineral composition, and ionic calcium levels have a significant impact on stressor intensity Although the species studied comprise a small and nonrepresentative sample of the almost 20,000 known teleost species, there are many indications that the stress response is variable and flexible in fish, in line with the great diversity of adaptations that enable these animals to live in a large variety of aquatic habitats
3,722 citations
TL;DR: Fishes display a wide variation in their physiological responses to stress, which is clearly evident in the plasma corticosteroid changes, chiefly cortisol in actinopterygian fishes, that occur following a stressful event.
Abstract: Physical, chemical and perceived stressors can all evoke non-specific responses in fish, which are considered adaptive to enable the fish to cope with the disturbance and maintain its homeostatic state. If the stressor is overly severe or long-lasting to the point that the fish is not capable of regaining homeostasis, then the responses themselves may become maladaptive and threaten the fish's health and well-being. Physiological responses to stress are grouped as primary, which include endocrine changes such as in measurable levels of circulating catecholamines and corticosteroids, and secondary, which include changes in features related to metabolism, hydromineral balance, and cardiovascular, respiratory and immune functions. In some instances, the endocrine responses are directly responsible for these secondary responses resulting in changes in concentration of blood constituents, including metabolites and major ions, and, at the cellular level, the expression of heat-shock or stress proteins. Tertiary or whole-animal changes in performance, such as in growth, disease resistance and behavior, can result from the primary and secondary responses and possibly affect survivorship.Fishes display a wide variation in their physiological responses to stress, which is clearly evident in the plasma corticosteroid changes, chiefly cortisol in actinopterygian fishes, that occur following a stressful event. The characteristic elevation in circulating cortisol during the first hour after an acute disturbance can vary by more than two orders of magnitude among species and genetic history appears to account for much of this interspecific variation. An appreciation of the factors that affect the magnitude, duration and recovery of cortisol and other physiological changes caused by stress in fishes is important for proper interpretation of experimental data and design of effective biological monitoring programs.
2,081 citations
"Cold shock and fish" refers background in this paper
...…corticotrophic cells to secrete adrenocorticotropin hormone, which stimulates kidney interrenal cells and releases corticosteroids into # 2008 The Authors Journal compilation # 2008 The Fisheries Society of the British Isles, Journal of Fish Biology 2008, 73, 1491–1530 circulation (Barton, 2002)....
[...]
...The process of cortisol synthesis and release can take several minutes and varies widely both interspecifically and intraspecifically because of differences in genetic, developmental and environmental factors (Barton & Iwama, 1991; Wendelaar Bonga, 1997; Barton, 2002)....
[...]
...Responses to environmental stress are broadly grouped into three categories (Mazeaud et al., 1977; Barton, 2002): primary (e.g. neuroendocrine response and corticosteroid–catecholamine release), secondary (e.g. metabolic, cellular, haematological, osmoregulatory and immunological changes) and…...
[...]
...The primary stress response in fish is accompanied by rapid changes in plasma concentrations of catecholamine and corticosteroid stress hormones (reviewed in Mazeaud et al., 1977; Barton, 2002)....
[...]
...…in fishes are generally well understood, the primary brain responses to cold temperature stress have not been thoroughly studied (reviewed in Barton 2002), although technology such as fMRI is beginning to allow a more detailed understanding of neural compensatory mechanisms related to…...
[...]
TL;DR: Stress, through the action of corticosteroids, may reduce immunocompetence by influencing lymphocyte numbers and antibody-production capacity, and affect reproduction by altering levels and patterns of reproductive hormones that influence maturation.
1,995 citations
"Cold shock and fish" refers background in this paper
...The process of cortisol synthesis and release can take several minutes and varies widely both interspecifically and intraspecifically because of differences in genetic, developmental and environmental factors (Barton & Iwama, 1991; Wendelaar Bonga, 1997; Barton, 2002)....
[...]
TL;DR: It is concluded that a mechanism of behavioral thermoregulation has evolved which favorably balances daily metabolic expenditures in order to conserve energy when food is limited.
Abstract: SYNOPSIS. Studies on the relation of temperature to tolerance, preference, metabolic rate, performance, circulation, and growth of sockeye salmon all point to a physiological optimum in the region of 15°C. Natural occurrence is limited in time and space at temperatures above 18°C despite being able to tolerate 24°C. Forms of physiological inadequacy can be demonstrated which account for such restrictions in distribution. Predictive power for locating and accounting for concentrations of young fish in thermally stratified lakes appeared to provide “proof” for the controlling influence of the physiological optimum temperature. Early literature on the ecology of sockeye supported this view. Recent studies using midwater trawls and sonar detection reveal a diurnal behavior pattern which points to a more subtle interaction of biotic andabiotic factors governing vertical distribution in which the controlling force appears to be bioenergetic efficiency. It is concluded that a mechanism of behavioral thermoregulation has evolved which favorably balances daily metabolic expenditures in order to conserve energy when food is limited.
1,064 citations
"Cold shock and fish" refers background in this paper
...In fact, water temperature has been described as the ‘abiotic master factor’ for fishes (Brett, 1971)....
[...]
TL;DR: This review has summarized published research concerning the tolerance of North American freshwater fishes to dynamic changes in temperature, i.e., tolerance is tested by methods that gradually change temperatures until biological stress is observed.
Abstract: Traditionally lower and upper temperature tolerances of fishes have been quantified in the laboratory via three different experimental approaches: the Fry or incipient lethal temperature (ILT), critical thermal (CTM) and chronic lethal (CLM) methodologies. Although these three experimental laboratory approaches generate endpoints which are quantitatively expressed as a temperature, are determined experimentally with random samples of fish acclimated to specific temperatures, and involve both time and temperature as major test variables, they do not quantify the same response. All three approaches generate valuable, albeit different, information concerning the temperature tolerance of a species. In this review we have summarized published research concerning the tolerance of North American freshwater fishes to dynamic changes in temperature, i.e., tolerance is tested by methods that gradually change temperatures until biological stress is observed. We found more than 450 individual temperature tolerances listed in 80 publications which present original dynamic temperature tolerance data for 116 species, 7 subspecies and 7 hybrids from 19 families of North American freshwater fishes. This total represents about 1/3 of the families and 1/6 of the known North American freshwater species. Temperature tolerance data were partitioned by experimental approach, i.e., critical thermal method (CTM) and chronic lethal method (CLM), and direction of temperature change. Although both CTM and CLM expose fish to dynamic changes in water temperature, these two methods differ in temperature change rates and test endpoints, and hence measure different aspects of thermal stress. A majority of the 80 studies employed CTM to assess temperature tolerance, in particular determination of CTmaxima. One or more CTmaxima has been reported for 108 fishes. Twenty-two fishes have reported highest CTmaxima of 40°C or higher. Several species in the family Cyprinodontidae have generated some of the highest CTmaxima reported for any ectothermic vertebrate. For a variety of reasons, data concerning tolerance of low temperatures are less plentiful. Low temperature tolerance quantified as either CTminima or CLminima were found for a total of 37 fishes. Acclimation temperature exerts a major effect on the temperature tolerance of most North American fish species and it is usually strongly linearly related to both CTmaxima and CTminima. Although we uncovered dynamic temperature tolerance data for 130 fishes, only a single dynamic, temperature tolerance polygon has been published, that for the sheepshead minnow, Cyprinodon variegatus.
793 citations
"Cold shock and fish" refers background in this paper
...Optimal temperature ranges, as well as upper and lower lethal temperatures, vary widely between and among species and are dependent on genetics, developmental stage and thermal histories (Beitinger et al., 2000; Somero, 2005)....
[...]