Abstract

Similar to that in higher vertebrates, the response of fish to stress follows the pattern of the General Adaptation syndrome, although there are specific exceptions. The major endocrine stress response in fish is characterized by elevations in the blood of the two important stress hormone groups, catecholamines and corticosteroids. Based mainly on studies with salmonid fishes of elevations in plasma cortisol and on metabolic responses, such as alterations in plasma glucose, certain generalizations about stress responses in fish were made. They are: (1) the degree of response depends on the severity and duration of the stressor, (2) responses to stress are cumulative, (3) environmental factors affect stress responses, (4) genetic and ontogenetic factors also influence stress responses, (5) fish habituate to stress, (6) stress responses are not universal, and (7) there is a metabolic cost associated with stress. The endocrine (primary) and metabolic (secondary) responses of fish to stress are considered adaptive, but there is a maladaptive component to the responses that may ultimately affect the fish's survival and general well-being.

The Concept of Stress

"There are few concepts that have evoked as much discussion and disagreement as that of stress when applied to biological system." (Pickering 1981a, p. 1)

"A reliable measurement of stress is critical; however, a reliable, acceptable measurement of stress has not been found, perhaps because the concept is applied to so many different phenomena." (Moberg 1985, p. 28)

These quotes serve to illustrate the past difficulty in attempting to establish the exact nature and boundaries of stress and its effects on the general well-being Of fish. There has been a lot of interest in stress in the last few Years since the Publication of proceedings of the 1980 symposium, "Stress and Fish" (Pickering 1981b). A good definition of stress is elusive and depends, to a large extent, on the context of the investigator. For example, an aquaculturist may have quite a different view of what constitutes stress in fish than what a toxicologist might have. Definitions have ranged from any physiological, biochemical or behavioral response to the various factors of the Physical, chemical and biological environment (Yousef 1985) to only those that extend the adaptive responses beyond the normal range such that the chances of survival are significantly reduced (Brett 1958). In a Physiological context, an acceptable working definition of stress is the nonspecific response of the body to any demand placed upon it such that it causes an extension of a physiological state beyond the normal resting state.

This definition does not imply that stress is necessarily detrimental to the fish. A more widely accepted definition of stress is the nonspecific response of the body to any demand made upon it (Selye 1973a). In Selye I s concept, a stressed organism passes through three distinct phases that he termed the General Adaptation syndrome (GAS) (Selye 1936, 1950). The first stage is an alarm reaction, followed by a stage of resistance. The alarm phase is usually characterized by a rapid physiological response. During the second phase, the organism adapts to or compensates for the altered conditions causing the stress in order to regain homeostasis. This may be evident as a return of physiological conditions to the prestress state or to an altered resting state (Selye 1973b; Schreck 1976; Heath 1987). If the stress is overly severe or long-lasting, compensation may not be possible and the organism enters the final stage of exhaustion. In fish, stress-induced mortality would likely be associated with this phase. More recently, as the role of corticosteroids during stress becomes clearer, the general applicability of the GAS concept has been questioned. In fact, Selye (1950) urged the preliminary nature of his model at the time, although it is still popular. Specifically, the finding that administration of corticosteroids in vivo has anti-inflammatory and immunosuppressive effects contradicted the notion that all physiological responses to stress are adaptive. Munck et al. (1984) proposed a new hypothesis whereby the role of corticosteroid secretions in response to stress, rather than being adaptive per se, is to protect the body from its own defense mechanisms during stress by suppressing those mechanisms. Recent studies (Berkenbosch et al. 1987; Sapolsky et al. 1987) showing that the pyrogenic protein, interleukin-1, also activates the hypothalamic-pituitary-adrenal axis in rats support Munck's view. Regardless of the semantic argument whether or not such inflammatory suppression constitutes an adaptive stress response, it is apparent that continued elevation of corticosteroids would be maladaptive, for example, by lowering disease resistance (Munck et al. 1984). The GAS concept of the stress response is a generalized one and may not be applicable to all stressful situations for fish (Schreck 1981, 1982). Leatherland (1985) noted that not all physiological responses are appropriate for universally evaluating stress in fish, since in some cases, some responses are specific to the type of stressor. Schreck (1981) concluded that a GAS-type of response in fish is only elicited when they experience some form of "fright, discomfort or pain". Thus, because of either the nature of the stressor or the fish's ability to achieve compensation (Schreck 1981), the lack of a detectable physiological response does not necessarily mean that the fish is not stressed. A more recent approach to stress by Moberg (1985) proposed that the stress response is divided into three categories: (1) recognition of a threat to homeostasis, (2) the stress response itself, and (3) the consequences of stress. Each category is comprised of separate biological events that are initiated by perception of the stressor by the central nervous system. The response culminates with the development of a pathological condition if the change in biological function caused by the stress is severe or persistent enough. Thus, the stress response and the consequences of stress represent adaptive and maladaptive phases, respectively, of the overall response of the organism. For example, to summarize Moberg (1985), corticosteroids are released during stress presumably to induce gluconeogenesis to increase glucose availability for metabolism. But increased gluconeogenesis is at the expense of lipid and protein metabolism, thus growth may be reduced. Furthermore, increased corticosteroid levels aver time detrimentally affect immune responses and reproductive processes.

Endocrine Responses to Stress

Corticosteroids

The elevation of plasma corticosteroids, mainly cortisol (Patino et al. 1987), in teleostean fish in response to various types of stressful stimuli has been well documented (Barton and Toth 1980; Donaldson 1981; Schreck 1981) and constitutes one of the important endocrine or primary responses to stress. Cortisol is synthesized and released from the interrenal cells of the head kidney tissue in fish following stimulation by adrenocorticotrophic hormone (ACTH) and is controlled by negative feedback on the hypothalamic-pituitary axis (Fryer and Peter 1977). Recent evidence suggests that this response in fish may be modulated by opioid peptides (Bird et al. 1987; Mukherjee et al. 1987).

The main role of cortisol in fish during stress still remains unclear but it is known that cortisol has both gluconeogenic (Butler 1968; Inui and Yokote 1975; Lidman et al. 1979) and immunosuppressive (Pickering 1984; Grim 1985; Barton et al. 1987; Thomas and Lewis 1987) actions. Based on their experimental results, leach and Taylor (1980) postulated that cortisol may function to sustain elevated levels of circulating glucose during stress after the initial catecholamine-stimulated increase. In fish, cortisol also has an osmoregulatory function (Eddy 1981).

Catecholamines

The other major endocrine response to stress in fish is the secretion of catecholamines, primarily adrenaline (epinephrine), from chromaffin cells following sympathetic stimulation (Mazeaud et al. 1977; Mazeaud and Mazeaud 1981; Nilsson 1984). Because chromaffin tissue is innervated directly with sympathetic ganglionic fibers (Nilsson 1984), the response of catecholamines to stress is much quicker than that for corticosteroids. The model of Mazeaud et al. (1977) implied that the pathways of corticosteroid and catecholamine stress responses in fish were distinct from each other. However, a general review by Axelrod and Reisine (1984) indicates that regulation of these stress hormones is more complex than earlier thought and that neuroendocrine control of both hormonal axes is interrelated.

In response to stress, catecholamines stimulate liver glycogenolysis, the conversion of glycogen stored in hepatocytes to glucose required for energy (Nakano and Tomlinson 1967; Heath 1987). Presumably to facilitate respiration during a stress-induced increase In metabolic rate, catecholamines also stimulate the recruitment of unperfused gill lamellae, reduce blood flow resistance through the gills, and possibly, enhance gill permeability to oxygen (Booth 1979; Butler and Metcalfe 1983).

Other Hormones

Improvements in radioimmunological techniques have allowed the detection and verification of other hormones in fish that are involved in the stress response. Notably, levels of ACTH, the Pituitary hormone responsible for stimulating cortisol release, have been shown to increase markedly in fish Plasma in response to acute stress (Sumpter and Donaldson 1986; Sumpter et al. 1986; Pickering et al. 1987). Similarly, endorphin concentrations in fish blood exhibit elevations following stress (Sumpter et al. 1985).

Although not considered stress hormones per se, other hormones in fish that have been reported to increase in titer following various types of stress are a-melanocyte-stimulating hormone (Gilham and Baker 1985; Sumpter et al. 1985, 1986), thyroxine (Brown et al. 1978), gonadotropin (Leatherland et al. 1982; Pickering et al. 1987), and prolactin (M. Avella, C.B. Schreck*, and P. Prunet, *Personal communication). Stress also suppresses circulating levels of the male reproductive hormones, testosterone and 11-ketotestosterone, in fish (Freeman et, al. 1983; Pickering et al. 1987).

Metabolic Responses to Stress

Carbohydrate Responses

Elevation of circulating levels of glucose (hyperglycemia) following stressful disturbances is a major metabolic response to stress and is also well documented for fish (Love 1980; Wedemeyer et al. 1984). An increase in plasma glucose indicates mobilization of energy reserves such as tissue glycogen through glycogenolysis and may reflect the degree of metabolic activity (Umminger 1977; Love 1980). Presumably, the stress-induced increase in blood glucose is an adaptive response to provide an energy source for the fish during stressful conditions (Love 1980).

In addition to plasma glucose, other secondary responses to stress include changes in plasma lactate, liver glycogen, hydromineral balance, and hematological features, such as hematocrit and circulating lymphocytes (Mazeaud et al. 1977; Wedemeyer and McLeay 1981; Wedemeyer et al. 1984). Although endocrine responses to stress in fish and subsequent secondary responses often covary, this does not mean that there is necessarily a direct cause-effect relationship (Leatherland 1985).

Whole Animal Responses

There are also tertiary or 'whole animal' responses to stress in fish (Wedemeyer and McLeay 1981; Wedemeyer et al. 1984). The most fundamental 'whole animal' response to stress, but one of the least studied, is a change in the metabolic rate. Changes in metabolism or scope for activity have been suggested as possible methods for measuring stress in fish (Brett 1958; Wedemeyer and McLeay 1981). Most investigations with fish, however, have concentrated on measuring stress indicators or changes in individual performances (Schreck 1981).

General Features of Stress Responses in Fish

Based on a review of work mostly examining physically-induced changes in plasma levels of cortisol and glucose, seven generalizations about the nature of stress responses in fish are presented. Such generalizations are important to researchers and managers alike to help both understand the nature of stress and properly interpret experimental results. These generalizations are: (1) the degree of response depends on the severity and duration of the stressor, (2) responses to stress are cumulative, (3) environmental factors affect stress responses, (4) genetic and ontogenetic factors also influence stress responses, (5) fish habituate to stress, (6) stress responses are not universal, and (7) there is a metabolic cost associated with stress.

The genetic, ontogenetic and environmental factors (Table 1) that have been shown to influence the magnitude of corticosteroid and glucose elevations in response to stress may be considered as belonging to three categories: (1) those that are relatively benign, (2) those that exacerbate primary and secondary responses to disturbance, and (3) those that reduce or eliminate these responses. Benign factors, such as species or stock, stage of development, time of day, or nutritional state, may affect the degree of response to stress without necessarily being detrimental to the fish's wellbeing. Nevertheless, it is important that researchers and managers be aware of the differences when they use these indicators to assess stress in fish to ensure correct interpretation of their results. The findings of past investigations are not unanimous. While some studies clearly showed that environmental factors influence the magnitude of these responses, others have either shown little effect of some factors or demonstrated opposite effects.

Quantitative differences in responses to stress under varying environmental conditions underscore the need for appropriate controls in stress investigations. Conflicting published findings do not negate the value of plasma corticosteroids and glucose as indicators of stress. Rather, they point out the importance of being familiar with both the life history and contingent environmental conditions when carrying out stress investigations with fish and interpreting the findings. For example, a high glucose response to a stimulus, relative to a control group, could indicate either an increased sensitivity to stress, suggesting that the fish is "more stressed", or a greater capacity to mobilize energy reserves in response to the stress because of nutritional state.

Factors that exacerbate interrenal or glycemic stress responses are additional stress factors and include poor health and excessively high or low water temperature. An accumulation of responses to these factors nay compromise the fish's realized capacity to perform by increasing the physiological load and thereby reducing the fish's ability to cope with additional changes in the environment. Other response-modifying factors can and are used by fisheries managers to their advantage. The use of salt and anesthetics, when used properly, can suppress stress-induced increases in corticosteroids and glucose, and may improve short-term survival, such as during transport.

The Metabolic Cost of Stress

There is a metabolic cost associated with stress in fish. Performance capacity has an upper limit, delineated genetically and by the environment, to give a realized capacity that is further reduced by stress (Schreck 1981). The reduction in performance capacity is brought about presumably by a shift in energy resources away from other activities, in order to allow the fish to cope with the stress (Schreck 1982). In his classic paper, Fry (1947) provided a basis for description of factors affecting animal activity within its environment and defined the concept of scope for activity. Relative to Schreck's (1981) conceptual model, stress further limits a fish's realized bioenergetic capacity by reducing the energy available within its scope for activity for other performance components. Barton and Schreck (1987b) demonstrated this by comparing oxygen consumption, a measure of metabolic rate, between stressed and unstressed fish subjected to a mild swimming challenge in a respirometer. Stressed fish had more than twice the oxygen consumption rate than unstressed fish when tested under the same experimental protocol. Even though the fish were subjected only to a brief physical disturbance, Barton and Schreck (1987b) estimated that the additional oxygen consumption represented about one-quarter of the fish's scope for activity. Thus, if a portion of the energy budget of fish is needed to deal with stress, the energy available for other, possibly necessary activities will be reduced accordingly.

Adaptive and Maladaptive Aspects of Stress

As our knowledge expands, it becomes increasingly clear that many important biological relationships are more complex and interrelated than earlier thought. The response of fish to stress is of this nature. It is not unreasonable to assume that when a fish is stressed, every physiological system is likely disturbed in some way. The important aspects of the stress response as related specifically to changes in the major stress hormones and their effects on metabolism are summarized in Figure 1. This model represents a synthesis of previously published concepts (Mazeaud. et al. 1977; Schreck 1981; Munck et al. 1984; Moberg 1985) and is supported, either definitively or circumstantially, by experimental results. It is understood that sucha model is overly simple since it does not include the built-in control system such as the negative feedback regulation of corticosteroid output (Fryer and Peter 1977), the interrelation of corticosteroids and catecholamines during stress (Axelrod and Reisine 1984), or the mechanistic components of the pathways such as corticosteroid induction of gluconeogenic enzyme activity (Storer 1967; Freeman and Idler 1973; Inui and Yokote 1975). Nor does it include the multitude of other primary and secondary stress responses and their possible relationships to these pathways such as the effects of catecholamines on gill vasculature and, subsequently, water and ion balance (Mazeaud et al. 1977).

When fish perceive a stressful stimulus, there is a change in biological function (Moberg 1985) as a response of the organism to compensate for the stress, according to the GAS-paradigm of Selye (1950). The ability of fish to respond to stress is part of their adaptive capacity to adjust to perturbations in their surroundings. As discussed earlier, this adaptive response is characterized by the increase in corticosteroids and catecholamines, followed by elevations in plasma glucose and in metabolic rate as energy reserves are mobilized and used to cope with the stress (Figure 1). However, there is a maladaptive component of the overall stress response that can be considered as the "cost of doing business". This is manifested by a reduction of energy availability within the scope for activity, a decline in glycogen reserves, and a decrease in circulating lymphocytes. If the stressor is persistent, these changes could lead to reduced growth as a consequence of both continued gluconeogenesis and reduced metabolic scope, metabolic exhaustion as energy stores are depleted, and increased disease incidence resulting fruit reduced immunocompetence. There is increasing evidence to show that the functional capacity of the immune system of fish is reduced by stress (Ellsaesser and Clem 1986; Fries 1986) and that this effect may be mediated by cortisol (Pickering 1984; Grim 1985; Thomas and Lewis 1987). It follows intuitively that the net result of severe or prolonged stress will be fish that are less capable of functioning optimally in their environment and, thus, have reduced chances of survival (Figure 1).

Figure 1. Adaptive and maladaptive aspects of the major endocrine-metabolic stress response pathways in fish.

Considerations for Research and Management

There is now no question that the normal physiological state of f ish is dramatically disrupted during the response to stress. Even though supported by sound circumstantial evidence, however, the relationship between stress-induced physiological alterations and reduced survival has not yet been clearly established. The challenge for future stress research is clear. Research program need to focus on determining if stress does, in fact, directly affect fish survival and to demonstrate that if by reducing stress, such as in culture and stocking programs, survival could be improved.

For the present, it is unlikely that stress can be eliminated in normal fisheries operations. To this end, much could probably be accomplished by: (1) ensuring that fish used in management programs are in the best possible health and condition, (2) allowing sufficient time in a suitable environment for fish to recover between individual disturbances, (3) avoiding subjecting fish to multiple stressors, simultaneously (e.g., handling and temperature change), and (4) routinely establishing physiological and health or condition profiles of both hatchery and free-ranging fish populations to provide a data base before a stressful event occurs. To meet management objectives, there is more emphasis today on fish quality, than on simply quantity. Improvements in fish quality can be accomplished in a number of ways - genetic manipulation, proper nutrition, or elimination of infectious disease, for example. As managers, we can also help to achieve our objectives through a better understanding of stress and its effects on fish. Stress management has had positive results in human medicine and in domestic livestock production. There is good reason to believe that it can work in fisheries management.

Acknowledgements

I am grateful to Dr. Carl B. Schreck and former colleagues at the Oregon Cooperative Fishery Research Unit, Oregon State University, with whom many discussions helped formulate the ideas presented.

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