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Understanding the adaptive response in vertebrates: The phenomenon of ease and ease response during post-stress acclimation
General and Comparative Endocrinology 181 (2013) 59–64
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Review
Understanding the adaptive response in vertebrates: The phenomenon of ease and ease response during post-stress acclimation M.C. Subhash Peter ⇑ Department of Zoology, University of Kerala, Kariavattom 695581, Thiruvananthapuram, Kerala, India
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Article history: Available online 10 October 2012 Keywords: Ease response Stress response Fish Vertebrate Adaptation Adaptive response Response
a b s t r a c t Vertebrates have evolved mechanisms to perceive stressors that arise either from their body or from the environment. Consequently, a state of stress and stress response occur in fish which is characterized by a disturbed physiological homeostasis. The pattern of stress response becomes complex as a result of neuroendocrine involvement and shows varied magnitudes in fishes depending on the nature and the severity of stressors. The integrated and compensatory physiological modifications in fishes during their early phase of adaptive response favor them to accommodate the imposed stressor through the process of stress acclimation. In contrast, with the direction of neuroendocrine signals, a phase of recovery often called post-stress acclimation occurs if the animal gets away from the stressor exposure. During this late phase of adaptive response, physiological modifications operate in favor of the animal that reduces the magnitude of stress response and finally to a phase of normality as animals possess the urge to correct its disrupted homeostasis. The phenomenon of ease and its response thus reduces the allostatic load, resets the homeostatic state through physiologic processes and corrects the stress-induced homeostatic disturbance with the aid of neuroendocrine signals. Ample evidences are now available to support this novel concept of ease and ease response where mitigation of the intensity of stress response occurs physiologically. Treatment of fish with melatonin or serotonin precursor tryptophan can modify the magnitude of stress response as evident in the pattern of tested physiological indices. In addition to cortisol, thyroid hormone as a major stress modifier hormone is involved in the regulation of ease response in fish probably due to the mechanisms involving inter-hormonal interference. Understanding the mechanisms of adaptive responses in vertebrates thus warranties more studies on the physiology of ease and its response. Ó 2012 Elsevier Inc. All rights reserved.
1. Introduction Perception of stressors and the subsequent physiological and behavioral responses in animals are a major part of stress adaptation that can promote their survival in the dynamic environment. The disturbed homeostatic state in animals often called stress evokes a set of stress responses [55,17,32] and that demands physiological correction. A wide variety of extrinsic or intrinsic stressors impose physiological modifications particularly on the rate of energy utilization, osmotic and metabolic functions which can adversely affect the growth in vertebrates including fishes [2,33,21,32]. For instance, environmental toxicants can modify the pattern of metabolic regulation [12,13,23,43], energy balance [33,55,38] and mineral and water balance in fishes [49,43,23]. Evidence have been presented that neuroendocrine signals that arise from the endocrine axes directs physiological mechanisms leading to stress responses in fishes. These signals can thus play a major ⇑ Fax: +91 471 2597514. E-mail address: [email protected] 0016-6480/$ - see front matter Ó 2012 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ygcen.2012.09.016
role in integrating and modulating the network of physiological processes during stress and post-stress acclimation. As an early phase of adaptive response, stress acclimation demands involvement of neuroendocrine signals that require physiological machinery. The resulting pattern of stress response thus reflects integrated physiological processes including osmotic and metabolic regulations. Extensive studies have indicated that endocrine stress axis is sensitive to both toxic and non-toxic stressors [43,39,44,40,31,32] which are also known as endocrine interrupting agents (EIAs) [19]. For example, fish interrenals are shown to have a higher sensitivity to many biological and environmental stimuli as many EIAs interrupt the cortisol release and its actions in fish [50–53,27]. Unlike stress acclimation that shows stress response, poststress acclimation reveals a recovery response. Moreover, specific neuroendocrine signals are directed to correct the disturbed homeostasis particularly during the phase of post-stress acclimation when the animal gets off from the stressor exposure. Physiological analyses of stressed fish kept for post-stress acclimation have yielded an interesting pattern of recovery response. In this
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late phase of adaptive response, as a result of specific physiological processes a reduction in the intensity of stress response and a reversal of adverse response to normality occur at least in fish. In this review a noval concept of ease has been proposed which could explain the process of post-stress adaptive mechanism in fish. Mitigation of adverse effects of stress response is essential in all animals as it can promote survivalship in challenging environment. Catecholamines and corticosteroids, the important players of endocrine stress axis and thyroid hormone as a major stress modifier hormone are involved in ease response. In addition, specific extrinsic and intrinsic factors have also been identified in the regulation of ease responses in fish models. 2. Stress and post-stress acclimation Extrinsic or intrinsic stimuli evoke physiological and biochemical corrections in animals. Consequently, animals accommodate these challenges with the help of physiological response pattern, which is commonly called stress acclimation [36]. In this phase of adaptive response, animal respond to stressors by showing a classic pattern of stress response because of the disturbed physiological competence. Mounting evidences underscore the role of stress hormones in the modification of physiological processes during stress acclimation particularly in fishes. Hypothalamo-pituitary-interrenal and brain sympathetic chromaffin cell axes are the primary endocrine axes that regulate stress responses in fish. Studies on fish species have yielded a greater complexicity of adaptive responses as these aquatic vertebrates respond to an array of intrinsic and extrinsic stressors which are known for its direct and indirect effects on many physiological processes. For example, evidence is available to suggest that non-toxic stressor like net confinement and its recovery can modify the osmotic and metabolic responses of tilapia and perch [30,42]. In spite of these studies that focus on the physiological mechanisms of adaptive responses during stress acclimation, little is known about the physiological basis of post-stress acclimation which can be seen in the recovery phase of animal after a stressor exposure. For instance, keeping the climbing perch for 96 h recovery in a clean environment can trigger a series of physiological responses that can correct the disturbed homeostasis. Compensatory regulation of Na+ K+ ATPase activity in the organs of this fish would help them to coordinate and correct the disturbed osmotic homeostasis when kept for recovery. Consequently, the process of stress acclimation as the first phase of adaptive response leaves a physiological recovery phase often called post-stress acclimation. During this late phase of adaptive response, animals again rely on their own physiological processes and correct its disturbed homeostatic status [36]. The process of post-stress acclimation can easily be identified physiologically in fish models when they were kept for recovery for varied time slots. With modified neuroendocrine functions these fish regain their basic homeostatic status by triggering compensatory adaptive response. This physiological response pattern in the post-stress acclimation thus clearly accounts for an adaptive phase which appears to be a prerequisite for stress adaptation. 3. Concept of ease and ease response It is a fact that animals possess an urge to overcome the physiological and behavioral disturbances when they are confronted by a stressor or challenge. The response of fish to stressor involves the entire physiological machinery and its complex regulatory network. Consequently, the integrated and compensatory physiological modifications in animals during their early phase of adaptive response favor them to accommodate the imposed stressor
through the process of stress acclimation. On the other hand, with the direction of neuroendocrine signals, a phase of recovery often called post-stress acclimation occurs if the animal gets away from the stressor exposure. During this late phase of adaptive response, the same physiological machinery operate in favor of the animal that can reduce the magnitude of stress response and finally to a phase of normality. This phenomenon of ease and its response can thus reduce the allostatic load, resets the homesostatic status and corrects the stress-induced homeostatic disruption with the help of specific neuroendocrine signals and physiological processes. In other words, ease and ease response are the innate mechanisms that work along with the stress response. 3.1. Physiological implications of ease response Like stress acclimation, post-stress acclimation or recovery phase produces a pattern of physiological responses in fish. Altered physiological and biochemical machineries during stress and poststress acclimation have been identified in fishes [For e.g. [11,13,38,43]. Similarly modifications of energy status in these fish due to modified hormonal actions including THs have also been demonstrated [14,16,22] which may enable them to accommodate the direct effects of stressors particularly during recovery phase [39]. For example, THs have been shown to modify the intermediary and oxidative metabolism in fish challenged by either nimbicidine or rotenone [35,39,44]. The sensitivity of thyroid to non-toxic endocrine interrupting agents (EIAs) like net confinement, air exposure, and high stocking density has been demonstrated in many fish species [20,54,5,55,38,30,32]. A modifier role of THs in stress response has now been well recognized in fish species [36,30,32] and convincing evidence for a role of TH in stress response presented recently in fishes [32]. Modification of physiological processes by THs in stressed fish clearly indicate that the status of thyroid is crucial in stress response as it modifies the stress-induced physiological alteration in fish particularly the osmotic and metabolic regulations [16]. For instance, net confinement and air exposure of perch and tilapia produced declined plasma T3 [30,31], though many toxic stressors can either promote or produce neutral thyroid responses [42]. Many synthetic chemicals, including plant products [42] can produce thyroid disruption in fishes [7]. For example exposure of catfishes to malathion and endosulfan causes disturbances in circulating THs [56,48]. Declined T3 has been found in rainbow trout exposed to acidic water [6]. A role for TH in the compensatory mechanism during recovery phase has been reported in fish. On the contrary, activated thyroid axis as evident in the rise of TH release during acidic water exposure and recovery phase has been demonstrated in air-breathing fish [36]. Similar activated thyroid has also been found in fish when kept for recovery after kerosene exposure [43]. Likewise, keeping the fish for recovery after carbaryl exposure (Peter MCS, unpublished) or exposure to the effluent of coconut husk retting [21,34] can stimulate thyroid activity. These differential TH responses during recovery phase indicate that both THs homeostasis and its actions are essential for the fish to adapt to environmental challenges. Similar to thyroid axis, cortisol axis also shows a greater sensitivity to many environmental contaminants. Many pollutants interfere and act through many sites including receptor levels, transporters, cellular uptake and metabolism [3,46] and adversely affect the endocrine function in fish. Induction of stress by stressors produces substantial rise in plasma cortisol in many fish species [30,32,39]. 3.1.1. TH-Cortisol interference during ease response The differential cortisol and TH responses in fish during stress and post-stress phases strongly indicate its interaction or interference at the physiological level. These hormonal interactions due to
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Fig. 1. Activity pattern of Na+,K+ ATPase and H+-ATPase in the gills and intestine of stressed (net-confined for 1 h) and non-stressed climbing perch in response to melatonin (150 ng g1 for 48 h) pretreatment. Melatonin treatment reduced the magnitude of stress response in this fish probably act through the mechanism of ease response. Columns are means ± SEM for six fish. In Fig. A and B, (P < 0.05) and (P < 0.001) denote significant difference from the control fish, $ (P < 0.05) and $$$ (P < 0.001) shows significant rise in H+ ATPase activity after melatonin treatment in stressed fish. $$$ (P < 0.001) shows significant decline in Na+, K+ ATPase and H+ ATPase activities after melatonin treatment in stressed fish.
the inter-hormonal interference [42] serve as a mechanism of adaptive response in fish. A specific pattern of inter-hormonal interference particularly TH-cortisol interference during ease phase could be found in fish. For example, a decreased T3 after a prolonged net-confinement and a rise in cortisol have been found freshwater tilapia [30,41]. This indicates a lead role of cortisol in the regulation of metabolic and hydromineral actions in this fish where T3 action is less vital. On the other hand, a rise in plasma T4 occurs in climbing perch during the recovery phase after a net confinement and this point to a possibility of THs involvement in this adaptive phase [30]. Similarly a rapid clearance of T3 by cortisol in tilapia can also be considered as one of the adaptive strategies of this fish to combat stress response [54]. Likewise, a decline of plasma T3 in physically-disturbed rainbow trout [16] and in kerosene-treated climbing perch [43] probably indicates an inter-hormonal interference. The plasma levels of T3, T4 and cortisol, the important clues on its availability for actions, are in tune with the body’s physiological demand. A detailed account of these hormone profiles which show varied patterns of specific TH-cortisol interferences has been reported earlier in fish [19]. For example, a temporal and inverse relationship between these hormones during net confinement has been found in tilapia [19], suggesting a lead role of cortisol in acclimation processes in this fish. This cortisol-driven acclimation processes which also show antagonistic interaction with TH appear to be adaptative due to its compensatory nature [19]. The hormonal interaction particularly TH-cortisol interference can thus form the basis of stress adaptation in fish. It appears that inter-hormonal interference can promote ease response in fish. A permissive action of TH can activate TH release during salinity acclimation of climbing perch [19]. A rise in T4 and not T3 during salinity acclimation has been found in tilapia [30]. This varied pattern of inter-hormonal interference further point to the speciesspecificity which may have a role in their salinity acclimation. Post stress-acclimation of climbing perch to 4 day recovery after 2 h airexposure have yielded elevation of plasma T4 and cortisol, indicating active roles of these hormones in both stress and ease response [42]. On the other hand, ease response in fish may not demand a TH-driven physiological machinery during their post-stress as this fish can manage with the existing basal endogenous cortisol avail-
ability or with some unidentified hormonal systems. Similarly, climbing perch does not rely on both THs and cortisol during the acclimation to water-borne nitrate [42]. This varied pattern of hormonal interactions during stress and ease response in fish is not uncommon in fish. Similar absence of TH and cortisol interference during ease response can be found in some fish. For example, climbing perch when kept for post-EIA acclimation i.e., keeping the fish for 4 day recovery after 20 min hypoxic condition [19] or keeping them for recovery after acclimation to water-borne bromide, specifically no deviation in the pattern of TH-cortisol interference exist [19]. In contrast, a pattern of anti-cortisol stati-TH interference can be seen when climbing perch were held for recovery for 4 days after nitrate exposure [19]. Pro-cortisol stati-TH interference occurs in climbing perch when held for recovery after kerosene exposure, where a rise in plasma cortisol without an effect on plasma T3, [19]. Evidence for a permissive interaction of TH with cortisol is available in fish. For example, an upregulated gill cortisol receptors by T3 has been reported in Atlantic salmon [47]. Notwithstanding the mounting evidences that document the involvement of TH and cortisol in osmotic and metabolic regulations in fishes, the role of these hormones in post-stress acclimation or ease response is less understood [36]. Salinity-acclimated climbing perch when kept at hypoxic condition for 20 min and placed for 4 day recovery in clean water shows a remarkable permissive upregulated interaction between TH and cortisol. Similarly, specific anti-TH stati-cortisol interference during ease response could be found in this fish where both these hormones are down regulated [19]. 3.1.2. Role of physiological processes in ease response Like stress response, ease response involves rigorous correction procedure involving compensatory modification of physiological processes. Modifications of acid–base, osmotic and metabolic performances in tune with neuroendocrine signals, drive the compensatory adaptations in fish. Physiological analyses have yielded convincing evidences for the existence of different mechanisms and the involvement of various signaling molecules that may play specific roles in the regulation of ease response. In many instances, several of acid–base, osmotic and metabolic indices show specific response pattern to recovery procedure and that invites ease response in this fish (see figs. 1–4).
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Fig. 3. The schematic chart representing the phenomenon of ease that operates in fish during post-stress acclimation or recovery. The disruption of homeostasis due to sensitization to stressors increases the alloatistic load with characteristic stress response. This allostatic load that accumulates during the disruption of homeostatic state takes a turn to a recovery phase when the animal gets away from the challenge. The characteristic physiological modification that occurs in this late adaptive phase due to desensitization is called a state of ease which produces ease response. Resetting of homeostatic state happens due the ease response which ultimately favors survivalship.
Fig. 2. Activity pattern of Na+, K+ ATPase and H+-ATPase in the intestine of climbing perch fed with control feed (control) or with tryptophan (TRP; 2% for 48 h) and placed for 20 min water immersion (IM) and then kept for one day (1 dR) or four day recovery (4 dR). TRP-fed fish showed a differential and lowered magnitude of stress response due to the involvement of serotonin which could induce ease response in this fish. Columns are means ± SEM for six fish. In Fig. A and B, ⁄⁄ (P < 0.01) and ⁄⁄⁄ (P < 0.001) denote significant difference from the control fish, @@ (P < 0.05) shows significant rise in intestinal H+ ATPase activity after 20 min immersion in TRP fed fish. @@@ (P < 0.001) denote significant difference from 20 min immersed TRP-fed fish.
Despite the diversity of actions of THs and cortisol in fish, these hormones possess certain common actions in fish [15,32]. A direct effect of THs on metabolites and indices of intermediary and oxidative metabolism have been well documented in fishes [29,38,43]. Likewise, cortisol is known for its osmotic and metabolic functions in fish [55,8,1]. In many occasions these hormones interact and interfere each other and can modify each other’s actions in order to fine-tune the homeostasis as many physiological processes work optimally at this state of equilibrium [1,40,32]. A detailed account on the physiological fine-tuning by TH and cortisol has been described elsewhere [32] which mainly accounts for the stress response. It is now clear that similar interference of hormones occurs during ease response that utilizes all physiological machineries in fish [26,18]. Induction of compensatory/adaptive modifications at the level of acid–base, osmotic and metabolic balances thus integrate and promote ease response as evident in their reversed response pattern during recovery phase. Sensitization/desensitization of hormonal receptor activity appears to be one of the target processes that direct ease response.
Alternatively, elevated hormonal status in the blood in conjunction with their receptor system interact each other at the central and peripheral levels resulting in spatial and temporal hormonal actions on its target organs. It is likely that a sort of central interaction occurs between thyroid and interrenal axes at the hypothalamo-pituitary levels. For example, both central and peripheral interactions between TH and cortisol have been reported in common carp [10], though the release of cortisol from carp head kidney fragment does not occur after T4 treatment [9]. On the other hand, release of T4 from kidney of carp occurs after cortisol and ACTH additions [10]. Similarly, an interaction of THs and cortisol occur at the peripheral level as evident in the decreased plasma cortisol in carp after T4 injection [9]. Despite, the specific actions of THs and cortisol on osmotic regulation in fishes [35,40,4,8,1,10,20,25], these hormones can interfere during ease response and alter the osmotic competence of osmoregulatory organs [25,24,1] including mitochondria-rich cell function. [22,55,28,37,40,32]. T4 treatment in tilapia has been shown to exert an additive effect on the stimulatory action of cortisol on osmotic regulation activity, though T4 alone failed to elicit such a response in this fish [30]. These results demonstrate the sensitivity of interrenal axis to TH availability, which has an implication in the ease response of fish mainly because of its modifier role in adaptive response. 3.2. Ecological implications of ease response It is now clear that fish rely on its hormonal and physiological systems to correct its disturbed homeostasis. As a result of interhormonal interference that happens at least between THs and cortisol, the survival capacity of fish increases during the post-stress acclimation phase. For example, during salinity acclimation the interaction of THs and cortisol favor many fish to trigger a complex network of physiological responses which ultimately help them to combat the differing ionoregulatory requirements [19]. Transfer of climbing perch to 20 ppt salinity for a day after transient salinity increments, a rise in plasma T4 but a decline of plasma T3 with
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Fig. 4. The flow chart shows the sequence of events during stress acclimation and post-stress acclimation. Vertebrates with the help of neuroendocrine signals perceive stressors during its exposure and trigger a net work of physiological responses often called stress response. Stress acclimation followed by a phase of post-stress acclimation thus forms the first phase of adaptive response. During recovery or post-stress acclimation, the animals again relay on neuroendocrine signals and physiological machinery to achieve a state of normality by a phenomenon of ease with a characteristic pattern of responses called ease response. Ease response as a second phase of adaptive response thus favors the animal to survive in challenging environment and constitutes the process of stress adaptation.
an unaffected plasma cortisol occur in this fish. However, these hormonal titers returned to basal levels when these fish were kept for a prolonged recovery acclimation of three weeks [45]. In this fish, the physiological response to ease reveals that they depend on TH secretion and the action of cortisol that coordinate the early phase of salinity acclimation is not essential. Consequently, this hormonal interaction, infact make them fully adaptive to brackish water salinity within three weeks. This mode of inter-hormonal interference led by T4 and not cortisol thus directs the ease response of this fish which finally promote a successful salinity adaptation in this fish. Similar examples illustrating the compensatory physiological modifications and interrupting functions of acid–base, osmotic and metabolic processes by TH and cortisol are now available in fishes [1,40,36,32]. Similar to TH and cortisol, hormones like melatonin and serotonin are involved in ease response in fishes. It is found that treatment of melatonin and tryptophan, precursor of serotonin reduced the magnitude of stress response in climbing perch as evident in the activity pattern of Na+, K+ ATPase and H+ ATPase activities in these fish (see Figs. 1 and 2). It is likely that the inter-hormonal interference and subsequent interruption that occur at the hormonal and physiological levels may favor the fish to accommodate the challenge that they perceive during stress acclimation. Fishes, therefore, rely on both neuroendocrine centers and physiological machinery including the mechanism involving inter-hormonal interference particularly TH-cortisol interference during ease response and this makes them more fit to survive in the challenging environment. A schematic model illustrating the details of adaptive responses in fish is presented in Figs. 3 and 4.
4. Conclusions Fishes rely on neuroendocrine signals and their physiological machinery during their survival in the dynamic environment. The physiological analysis shows that the integrated and compensatory modifications that happen in fish during their recovery phase favor them to recover from the adverse effect of stress response. With the direction of neuroendocrine signals, this phase of recovery often called post-stress acclimation, favor them to reduce the magnitude of stress response and finally to a phase of normality. The process of physiological correction that resets the basal homeosta-
sis can be recognized as the phenomenon of ease and ease response which further reduce the allostatic load with the help of specific neuroendocrine signals and physiological processes. This novel concept of ease and ease response thus physiologically mitigate the adverse effect of stress response in fish. Thyroid hormones and cortisol along with other hormones like melatonin and serotonin are found to direct ease response in fish. The mechanism of adaptive responses in fish thus becomes more complex but gives physiological clues on the involvement of ease and its response in stress adaptation. Acknowledgments This work was presented in the International Symposium on Comparative Endocrinology and Stress Physiology (CESP 2012) held in the University of Kerala on 16-18 February 2012. Thanks are due to UGC for financial support (MRP No. F-39-609/2010/SR) and the UGC-SAP facility in the Department of Zoology of the University of Kerala, for some infrastructural support. References [1] G.S. Babitha, M.C.S. Peter, Cortisol promotes and integrates the osmotic competence of the organs in North African catfish (Clarias gariepinus Burchell): evidence from in vivo and in situ approaches, Gen. Comp. Endocrinol. 168 (2010) 14–21. [2] B.A. Barton, Stress in finfish: past, present and future- a historical perspective, in: G.K. Iwama, A.D. Pickering, J.P. Sumpter, C.B. Schreck (Eds.), Fish Stress and Health in Aquaculture, Cambridge University Press, New York, 1997, pp. 1–34. [3] M. Boas, U. Feldt-Rasmussen, N.E. Skakkebaek, K.M. Main, Environmental chemicals and thyroid function, Eur. J. Endocrinol. 154 (2006) 599–611. [4] J.M. Bowers, A. Mustafa, D.J. Speare, G.A. Conboy, M. Brimacombe, D.E. Sims, et al., The physiologicalal response of Atlantic salmon, Salmo salar L., to a single experimental challenge with sea lice, Lepeophtheirus salmonis, J. Fish Dis. 23 (2000) 165–172. [5] J.A. Brown, Endocrine responses to environmental pollutants, in: J.C. Rankin, F.B. Jensen (Eds.), Fish Ecophysiology, Chapman and Hall, London, 1993, pp. 276–296. [6] S.B. Brown, D.L. Maclatchy, T.J. Hara, J.G. Eales, Effects of low ambient pH and aluminium on plasma kinetics of cortisol T3 and T4 in rainbow trout, Oncorhynchus mykiss, Can. J. Zool. 68 (1990) 1537–1543. [7] F. Brucker-Davis, Effects of environmental synthetic chemicals on thyroid function, Thyroid 8 (1998) 827–856. [8] Z.C. Dang, M.H.G. Berntssen, A.K. Lundebye, G. Flik, S.E. Wendelaar Bonga, R.A.C. Lock, Metallothionein and cortisol receptor expression in gills of Atlantic salmon, Salmo salar, exposed to dietary cadmium, Aquat. Toxicol. 53 (2001) 91–101.
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Review
Understanding the adaptive response in vertebrates: The phenomenon of ease and ease response during post-stress acclimation M.C. Subhash Peter ⇑ Department of Zoology, University of Kerala, Kariavattom 695581, Thiruvananthapuram, Kerala, India
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Article history: Available online 10 October 2012 Keywords: Ease response Stress response Fish Vertebrate Adaptation Adaptive response Response
a b s t r a c t Vertebrates have evolved mechanisms to perceive stressors that arise either from their body or from the environment. Consequently, a state of stress and stress response occur in fish which is characterized by a disturbed physiological homeostasis. The pattern of stress response becomes complex as a result of neuroendocrine involvement and shows varied magnitudes in fishes depending on the nature and the severity of stressors. The integrated and compensatory physiological modifications in fishes during their early phase of adaptive response favor them to accommodate the imposed stressor through the process of stress acclimation. In contrast, with the direction of neuroendocrine signals, a phase of recovery often called post-stress acclimation occurs if the animal gets away from the stressor exposure. During this late phase of adaptive response, physiological modifications operate in favor of the animal that reduces the magnitude of stress response and finally to a phase of normality as animals possess the urge to correct its disrupted homeostasis. The phenomenon of ease and its response thus reduces the allostatic load, resets the homeostatic state through physiologic processes and corrects the stress-induced homeostatic disturbance with the aid of neuroendocrine signals. Ample evidences are now available to support this novel concept of ease and ease response where mitigation of the intensity of stress response occurs physiologically. Treatment of fish with melatonin or serotonin precursor tryptophan can modify the magnitude of stress response as evident in the pattern of tested physiological indices. In addition to cortisol, thyroid hormone as a major stress modifier hormone is involved in the regulation of ease response in fish probably due to the mechanisms involving inter-hormonal interference. Understanding the mechanisms of adaptive responses in vertebrates thus warranties more studies on the physiology of ease and its response. Ó 2012 Elsevier Inc. All rights reserved.
1. Introduction Perception of stressors and the subsequent physiological and behavioral responses in animals are a major part of stress adaptation that can promote their survival in the dynamic environment. The disturbed homeostatic state in animals often called stress evokes a set of stress responses [55,17,32] and that demands physiological correction. A wide variety of extrinsic or intrinsic stressors impose physiological modifications particularly on the rate of energy utilization, osmotic and metabolic functions which can adversely affect the growth in vertebrates including fishes [2,33,21,32]. For instance, environmental toxicants can modify the pattern of metabolic regulation [12,13,23,43], energy balance [33,55,38] and mineral and water balance in fishes [49,43,23]. Evidence have been presented that neuroendocrine signals that arise from the endocrine axes directs physiological mechanisms leading to stress responses in fishes. These signals can thus play a major ⇑ Fax: +91 471 2597514. E-mail address: [email protected] 0016-6480/$ - see front matter Ó 2012 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ygcen.2012.09.016
role in integrating and modulating the network of physiological processes during stress and post-stress acclimation. As an early phase of adaptive response, stress acclimation demands involvement of neuroendocrine signals that require physiological machinery. The resulting pattern of stress response thus reflects integrated physiological processes including osmotic and metabolic regulations. Extensive studies have indicated that endocrine stress axis is sensitive to both toxic and non-toxic stressors [43,39,44,40,31,32] which are also known as endocrine interrupting agents (EIAs) [19]. For example, fish interrenals are shown to have a higher sensitivity to many biological and environmental stimuli as many EIAs interrupt the cortisol release and its actions in fish [50–53,27]. Unlike stress acclimation that shows stress response, poststress acclimation reveals a recovery response. Moreover, specific neuroendocrine signals are directed to correct the disturbed homeostasis particularly during the phase of post-stress acclimation when the animal gets off from the stressor exposure. Physiological analyses of stressed fish kept for post-stress acclimation have yielded an interesting pattern of recovery response. In this
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late phase of adaptive response, as a result of specific physiological processes a reduction in the intensity of stress response and a reversal of adverse response to normality occur at least in fish. In this review a noval concept of ease has been proposed which could explain the process of post-stress adaptive mechanism in fish. Mitigation of adverse effects of stress response is essential in all animals as it can promote survivalship in challenging environment. Catecholamines and corticosteroids, the important players of endocrine stress axis and thyroid hormone as a major stress modifier hormone are involved in ease response. In addition, specific extrinsic and intrinsic factors have also been identified in the regulation of ease responses in fish models. 2. Stress and post-stress acclimation Extrinsic or intrinsic stimuli evoke physiological and biochemical corrections in animals. Consequently, animals accommodate these challenges with the help of physiological response pattern, which is commonly called stress acclimation [36]. In this phase of adaptive response, animal respond to stressors by showing a classic pattern of stress response because of the disturbed physiological competence. Mounting evidences underscore the role of stress hormones in the modification of physiological processes during stress acclimation particularly in fishes. Hypothalamo-pituitary-interrenal and brain sympathetic chromaffin cell axes are the primary endocrine axes that regulate stress responses in fish. Studies on fish species have yielded a greater complexicity of adaptive responses as these aquatic vertebrates respond to an array of intrinsic and extrinsic stressors which are known for its direct and indirect effects on many physiological processes. For example, evidence is available to suggest that non-toxic stressor like net confinement and its recovery can modify the osmotic and metabolic responses of tilapia and perch [30,42]. In spite of these studies that focus on the physiological mechanisms of adaptive responses during stress acclimation, little is known about the physiological basis of post-stress acclimation which can be seen in the recovery phase of animal after a stressor exposure. For instance, keeping the climbing perch for 96 h recovery in a clean environment can trigger a series of physiological responses that can correct the disturbed homeostasis. Compensatory regulation of Na+ K+ ATPase activity in the organs of this fish would help them to coordinate and correct the disturbed osmotic homeostasis when kept for recovery. Consequently, the process of stress acclimation as the first phase of adaptive response leaves a physiological recovery phase often called post-stress acclimation. During this late phase of adaptive response, animals again rely on their own physiological processes and correct its disturbed homeostatic status [36]. The process of post-stress acclimation can easily be identified physiologically in fish models when they were kept for recovery for varied time slots. With modified neuroendocrine functions these fish regain their basic homeostatic status by triggering compensatory adaptive response. This physiological response pattern in the post-stress acclimation thus clearly accounts for an adaptive phase which appears to be a prerequisite for stress adaptation. 3. Concept of ease and ease response It is a fact that animals possess an urge to overcome the physiological and behavioral disturbances when they are confronted by a stressor or challenge. The response of fish to stressor involves the entire physiological machinery and its complex regulatory network. Consequently, the integrated and compensatory physiological modifications in animals during their early phase of adaptive response favor them to accommodate the imposed stressor
through the process of stress acclimation. On the other hand, with the direction of neuroendocrine signals, a phase of recovery often called post-stress acclimation occurs if the animal gets away from the stressor exposure. During this late phase of adaptive response, the same physiological machinery operate in favor of the animal that can reduce the magnitude of stress response and finally to a phase of normality. This phenomenon of ease and its response can thus reduce the allostatic load, resets the homesostatic status and corrects the stress-induced homeostatic disruption with the help of specific neuroendocrine signals and physiological processes. In other words, ease and ease response are the innate mechanisms that work along with the stress response. 3.1. Physiological implications of ease response Like stress acclimation, post-stress acclimation or recovery phase produces a pattern of physiological responses in fish. Altered physiological and biochemical machineries during stress and poststress acclimation have been identified in fishes [For e.g. [11,13,38,43]. Similarly modifications of energy status in these fish due to modified hormonal actions including THs have also been demonstrated [14,16,22] which may enable them to accommodate the direct effects of stressors particularly during recovery phase [39]. For example, THs have been shown to modify the intermediary and oxidative metabolism in fish challenged by either nimbicidine or rotenone [35,39,44]. The sensitivity of thyroid to non-toxic endocrine interrupting agents (EIAs) like net confinement, air exposure, and high stocking density has been demonstrated in many fish species [20,54,5,55,38,30,32]. A modifier role of THs in stress response has now been well recognized in fish species [36,30,32] and convincing evidence for a role of TH in stress response presented recently in fishes [32]. Modification of physiological processes by THs in stressed fish clearly indicate that the status of thyroid is crucial in stress response as it modifies the stress-induced physiological alteration in fish particularly the osmotic and metabolic regulations [16]. For instance, net confinement and air exposure of perch and tilapia produced declined plasma T3 [30,31], though many toxic stressors can either promote or produce neutral thyroid responses [42]. Many synthetic chemicals, including plant products [42] can produce thyroid disruption in fishes [7]. For example exposure of catfishes to malathion and endosulfan causes disturbances in circulating THs [56,48]. Declined T3 has been found in rainbow trout exposed to acidic water [6]. A role for TH in the compensatory mechanism during recovery phase has been reported in fish. On the contrary, activated thyroid axis as evident in the rise of TH release during acidic water exposure and recovery phase has been demonstrated in air-breathing fish [36]. Similar activated thyroid has also been found in fish when kept for recovery after kerosene exposure [43]. Likewise, keeping the fish for recovery after carbaryl exposure (Peter MCS, unpublished) or exposure to the effluent of coconut husk retting [21,34] can stimulate thyroid activity. These differential TH responses during recovery phase indicate that both THs homeostasis and its actions are essential for the fish to adapt to environmental challenges. Similar to thyroid axis, cortisol axis also shows a greater sensitivity to many environmental contaminants. Many pollutants interfere and act through many sites including receptor levels, transporters, cellular uptake and metabolism [3,46] and adversely affect the endocrine function in fish. Induction of stress by stressors produces substantial rise in plasma cortisol in many fish species [30,32,39]. 3.1.1. TH-Cortisol interference during ease response The differential cortisol and TH responses in fish during stress and post-stress phases strongly indicate its interaction or interference at the physiological level. These hormonal interactions due to
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Fig. 1. Activity pattern of Na+,K+ ATPase and H+-ATPase in the gills and intestine of stressed (net-confined for 1 h) and non-stressed climbing perch in response to melatonin (150 ng g1 for 48 h) pretreatment. Melatonin treatment reduced the magnitude of stress response in this fish probably act through the mechanism of ease response. Columns are means ± SEM for six fish. In Fig. A and B, (P < 0.05) and (P < 0.001) denote significant difference from the control fish, $ (P < 0.05) and $$$ (P < 0.001) shows significant rise in H+ ATPase activity after melatonin treatment in stressed fish. $$$ (P < 0.001) shows significant decline in Na+, K+ ATPase and H+ ATPase activities after melatonin treatment in stressed fish.
the inter-hormonal interference [42] serve as a mechanism of adaptive response in fish. A specific pattern of inter-hormonal interference particularly TH-cortisol interference during ease phase could be found in fish. For example, a decreased T3 after a prolonged net-confinement and a rise in cortisol have been found freshwater tilapia [30,41]. This indicates a lead role of cortisol in the regulation of metabolic and hydromineral actions in this fish where T3 action is less vital. On the other hand, a rise in plasma T4 occurs in climbing perch during the recovery phase after a net confinement and this point to a possibility of THs involvement in this adaptive phase [30]. Similarly a rapid clearance of T3 by cortisol in tilapia can also be considered as one of the adaptive strategies of this fish to combat stress response [54]. Likewise, a decline of plasma T3 in physically-disturbed rainbow trout [16] and in kerosene-treated climbing perch [43] probably indicates an inter-hormonal interference. The plasma levels of T3, T4 and cortisol, the important clues on its availability for actions, are in tune with the body’s physiological demand. A detailed account of these hormone profiles which show varied patterns of specific TH-cortisol interferences has been reported earlier in fish [19]. For example, a temporal and inverse relationship between these hormones during net confinement has been found in tilapia [19], suggesting a lead role of cortisol in acclimation processes in this fish. This cortisol-driven acclimation processes which also show antagonistic interaction with TH appear to be adaptative due to its compensatory nature [19]. The hormonal interaction particularly TH-cortisol interference can thus form the basis of stress adaptation in fish. It appears that inter-hormonal interference can promote ease response in fish. A permissive action of TH can activate TH release during salinity acclimation of climbing perch [19]. A rise in T4 and not T3 during salinity acclimation has been found in tilapia [30]. This varied pattern of inter-hormonal interference further point to the speciesspecificity which may have a role in their salinity acclimation. Post stress-acclimation of climbing perch to 4 day recovery after 2 h airexposure have yielded elevation of plasma T4 and cortisol, indicating active roles of these hormones in both stress and ease response [42]. On the other hand, ease response in fish may not demand a TH-driven physiological machinery during their post-stress as this fish can manage with the existing basal endogenous cortisol avail-
ability or with some unidentified hormonal systems. Similarly, climbing perch does not rely on both THs and cortisol during the acclimation to water-borne nitrate [42]. This varied pattern of hormonal interactions during stress and ease response in fish is not uncommon in fish. Similar absence of TH and cortisol interference during ease response can be found in some fish. For example, climbing perch when kept for post-EIA acclimation i.e., keeping the fish for 4 day recovery after 20 min hypoxic condition [19] or keeping them for recovery after acclimation to water-borne bromide, specifically no deviation in the pattern of TH-cortisol interference exist [19]. In contrast, a pattern of anti-cortisol stati-TH interference can be seen when climbing perch were held for recovery for 4 days after nitrate exposure [19]. Pro-cortisol stati-TH interference occurs in climbing perch when held for recovery after kerosene exposure, where a rise in plasma cortisol without an effect on plasma T3, [19]. Evidence for a permissive interaction of TH with cortisol is available in fish. For example, an upregulated gill cortisol receptors by T3 has been reported in Atlantic salmon [47]. Notwithstanding the mounting evidences that document the involvement of TH and cortisol in osmotic and metabolic regulations in fishes, the role of these hormones in post-stress acclimation or ease response is less understood [36]. Salinity-acclimated climbing perch when kept at hypoxic condition for 20 min and placed for 4 day recovery in clean water shows a remarkable permissive upregulated interaction between TH and cortisol. Similarly, specific anti-TH stati-cortisol interference during ease response could be found in this fish where both these hormones are down regulated [19]. 3.1.2. Role of physiological processes in ease response Like stress response, ease response involves rigorous correction procedure involving compensatory modification of physiological processes. Modifications of acid–base, osmotic and metabolic performances in tune with neuroendocrine signals, drive the compensatory adaptations in fish. Physiological analyses have yielded convincing evidences for the existence of different mechanisms and the involvement of various signaling molecules that may play specific roles in the regulation of ease response. In many instances, several of acid–base, osmotic and metabolic indices show specific response pattern to recovery procedure and that invites ease response in this fish (see figs. 1–4).
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Fig. 3. The schematic chart representing the phenomenon of ease that operates in fish during post-stress acclimation or recovery. The disruption of homeostasis due to sensitization to stressors increases the alloatistic load with characteristic stress response. This allostatic load that accumulates during the disruption of homeostatic state takes a turn to a recovery phase when the animal gets away from the challenge. The characteristic physiological modification that occurs in this late adaptive phase due to desensitization is called a state of ease which produces ease response. Resetting of homeostatic state happens due the ease response which ultimately favors survivalship.
Fig. 2. Activity pattern of Na+, K+ ATPase and H+-ATPase in the intestine of climbing perch fed with control feed (control) or with tryptophan (TRP; 2% for 48 h) and placed for 20 min water immersion (IM) and then kept for one day (1 dR) or four day recovery (4 dR). TRP-fed fish showed a differential and lowered magnitude of stress response due to the involvement of serotonin which could induce ease response in this fish. Columns are means ± SEM for six fish. In Fig. A and B, ⁄⁄ (P < 0.01) and ⁄⁄⁄ (P < 0.001) denote significant difference from the control fish, @@ (P < 0.05) shows significant rise in intestinal H+ ATPase activity after 20 min immersion in TRP fed fish. @@@ (P < 0.001) denote significant difference from 20 min immersed TRP-fed fish.
Despite the diversity of actions of THs and cortisol in fish, these hormones possess certain common actions in fish [15,32]. A direct effect of THs on metabolites and indices of intermediary and oxidative metabolism have been well documented in fishes [29,38,43]. Likewise, cortisol is known for its osmotic and metabolic functions in fish [55,8,1]. In many occasions these hormones interact and interfere each other and can modify each other’s actions in order to fine-tune the homeostasis as many physiological processes work optimally at this state of equilibrium [1,40,32]. A detailed account on the physiological fine-tuning by TH and cortisol has been described elsewhere [32] which mainly accounts for the stress response. It is now clear that similar interference of hormones occurs during ease response that utilizes all physiological machineries in fish [26,18]. Induction of compensatory/adaptive modifications at the level of acid–base, osmotic and metabolic balances thus integrate and promote ease response as evident in their reversed response pattern during recovery phase. Sensitization/desensitization of hormonal receptor activity appears to be one of the target processes that direct ease response.
Alternatively, elevated hormonal status in the blood in conjunction with their receptor system interact each other at the central and peripheral levels resulting in spatial and temporal hormonal actions on its target organs. It is likely that a sort of central interaction occurs between thyroid and interrenal axes at the hypothalamo-pituitary levels. For example, both central and peripheral interactions between TH and cortisol have been reported in common carp [10], though the release of cortisol from carp head kidney fragment does not occur after T4 treatment [9]. On the other hand, release of T4 from kidney of carp occurs after cortisol and ACTH additions [10]. Similarly, an interaction of THs and cortisol occur at the peripheral level as evident in the decreased plasma cortisol in carp after T4 injection [9]. Despite, the specific actions of THs and cortisol on osmotic regulation in fishes [35,40,4,8,1,10,20,25], these hormones can interfere during ease response and alter the osmotic competence of osmoregulatory organs [25,24,1] including mitochondria-rich cell function. [22,55,28,37,40,32]. T4 treatment in tilapia has been shown to exert an additive effect on the stimulatory action of cortisol on osmotic regulation activity, though T4 alone failed to elicit such a response in this fish [30]. These results demonstrate the sensitivity of interrenal axis to TH availability, which has an implication in the ease response of fish mainly because of its modifier role in adaptive response. 3.2. Ecological implications of ease response It is now clear that fish rely on its hormonal and physiological systems to correct its disturbed homeostasis. As a result of interhormonal interference that happens at least between THs and cortisol, the survival capacity of fish increases during the post-stress acclimation phase. For example, during salinity acclimation the interaction of THs and cortisol favor many fish to trigger a complex network of physiological responses which ultimately help them to combat the differing ionoregulatory requirements [19]. Transfer of climbing perch to 20 ppt salinity for a day after transient salinity increments, a rise in plasma T4 but a decline of plasma T3 with
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Fig. 4. The flow chart shows the sequence of events during stress acclimation and post-stress acclimation. Vertebrates with the help of neuroendocrine signals perceive stressors during its exposure and trigger a net work of physiological responses often called stress response. Stress acclimation followed by a phase of post-stress acclimation thus forms the first phase of adaptive response. During recovery or post-stress acclimation, the animals again relay on neuroendocrine signals and physiological machinery to achieve a state of normality by a phenomenon of ease with a characteristic pattern of responses called ease response. Ease response as a second phase of adaptive response thus favors the animal to survive in challenging environment and constitutes the process of stress adaptation.
an unaffected plasma cortisol occur in this fish. However, these hormonal titers returned to basal levels when these fish were kept for a prolonged recovery acclimation of three weeks [45]. In this fish, the physiological response to ease reveals that they depend on TH secretion and the action of cortisol that coordinate the early phase of salinity acclimation is not essential. Consequently, this hormonal interaction, infact make them fully adaptive to brackish water salinity within three weeks. This mode of inter-hormonal interference led by T4 and not cortisol thus directs the ease response of this fish which finally promote a successful salinity adaptation in this fish. Similar examples illustrating the compensatory physiological modifications and interrupting functions of acid–base, osmotic and metabolic processes by TH and cortisol are now available in fishes [1,40,36,32]. Similar to TH and cortisol, hormones like melatonin and serotonin are involved in ease response in fishes. It is found that treatment of melatonin and tryptophan, precursor of serotonin reduced the magnitude of stress response in climbing perch as evident in the activity pattern of Na+, K+ ATPase and H+ ATPase activities in these fish (see Figs. 1 and 2). It is likely that the inter-hormonal interference and subsequent interruption that occur at the hormonal and physiological levels may favor the fish to accommodate the challenge that they perceive during stress acclimation. Fishes, therefore, rely on both neuroendocrine centers and physiological machinery including the mechanism involving inter-hormonal interference particularly TH-cortisol interference during ease response and this makes them more fit to survive in the challenging environment. A schematic model illustrating the details of adaptive responses in fish is presented in Figs. 3 and 4.
4. Conclusions Fishes rely on neuroendocrine signals and their physiological machinery during their survival in the dynamic environment. The physiological analysis shows that the integrated and compensatory modifications that happen in fish during their recovery phase favor them to recover from the adverse effect of stress response. With the direction of neuroendocrine signals, this phase of recovery often called post-stress acclimation, favor them to reduce the magnitude of stress response and finally to a phase of normality. The process of physiological correction that resets the basal homeosta-
sis can be recognized as the phenomenon of ease and ease response which further reduce the allostatic load with the help of specific neuroendocrine signals and physiological processes. This novel concept of ease and ease response thus physiologically mitigate the adverse effect of stress response in fish. Thyroid hormones and cortisol along with other hormones like melatonin and serotonin are found to direct ease response in fish. The mechanism of adaptive responses in fish thus becomes more complex but gives physiological clues on the involvement of ease and its response in stress adaptation. Acknowledgments This work was presented in the International Symposium on Comparative Endocrinology and Stress Physiology (CESP 2012) held in the University of Kerala on 16-18 February 2012. Thanks are due to UGC for financial support (MRP No. F-39-609/2010/SR) and the UGC-SAP facility in the Department of Zoology of the University of Kerala, for some infrastructural support. References [1] G.S. Babitha, M.C.S. Peter, Cortisol promotes and integrates the osmotic competence of the organs in North African catfish (Clarias gariepinus Burchell): evidence from in vivo and in situ approaches, Gen. Comp. Endocrinol. 168 (2010) 14–21. [2] B.A. Barton, Stress in finfish: past, present and future- a historical perspective, in: G.K. Iwama, A.D. Pickering, J.P. Sumpter, C.B. Schreck (Eds.), Fish Stress and Health in Aquaculture, Cambridge University Press, New York, 1997, pp. 1–34. [3] M. Boas, U. Feldt-Rasmussen, N.E. Skakkebaek, K.M. Main, Environmental chemicals and thyroid function, Eur. J. Endocrinol. 154 (2006) 599–611. [4] J.M. Bowers, A. Mustafa, D.J. Speare, G.A. Conboy, M. Brimacombe, D.E. Sims, et al., The physiologicalal response of Atlantic salmon, Salmo salar L., to a single experimental challenge with sea lice, Lepeophtheirus salmonis, J. Fish Dis. 23 (2000) 165–172. [5] J.A. Brown, Endocrine responses to environmental pollutants, in: J.C. Rankin, F.B. Jensen (Eds.), Fish Ecophysiology, Chapman and Hall, London, 1993, pp. 276–296. [6] S.B. Brown, D.L. Maclatchy, T.J. Hara, J.G. Eales, Effects of low ambient pH and aluminium on plasma kinetics of cortisol T3 and T4 in rainbow trout, Oncorhynchus mykiss, Can. J. Zool. 68 (1990) 1537–1543. [7] F. Brucker-Davis, Effects of environmental synthetic chemicals on thyroid function, Thyroid 8 (1998) 827–856. [8] Z.C. Dang, M.H.G. Berntssen, A.K. Lundebye, G. Flik, S.E. Wendelaar Bonga, R.A.C. Lock, Metallothionein and cortisol receptor expression in gills of Atlantic salmon, Salmo salar, exposed to dietary cadmium, Aquat. Toxicol. 53 (2001) 91–101.
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