The physiological response of the Caribbean reef shark (Carcharhinus perezi) to longline capture

Longline fishing is the most common elasmobranch capture method around the world, yet the physiological consequences of this technique are poorly understood. To quantify the sub-lethal effects of longline capture in the commonly exploited Caribbean reef shark (Carcharhinus perezi), 37 individuals were captured using standard, mid-water longlines. Hook timers provided hooking duration to the nearest minute. Once sharks were landed, blood samples were taken and used to measure a suite of physiological parameters. Control data were obtained by sampling an additional three unrestrained Caribbean reef sharks underwater at an established shark feeding site. The greatest level of physiological disruption occurred after 120-180min of hooking, whereas sharks exposed to minimal and maximal hook durations exhibited the least disturbed blood chemistry. Significant relationships were established between hooking duration and blood pH, pCO(2), lactate, glucose, plasma calcium and plasma potassium. Longline capture appears more benign than other methods assessed to date, causing a shift in the stress response from acute at the onset of capture to a sub-acute regime as the capture event progresses, apparently facilitating a degree of physiological recovery. Continued investigation into the physiological response of elasmobranchs to longline capture is vital for the effective management of such fisheries.     

Sex, seasonal, and stress-related variations in elasmobranch corticosterone concentrations.

Serum corticosterone was previously studied in numerous elasmobranch fishes (sharks, skates and rays), but the role of this steroid, widespread throughout many taxa, has yet to be defined. The goal of this study was to test whether corticosterone varied in response to acute and chronic capture stress, and across the reproductive cycle in the bonnethead shark, Sphyrna tiburo, and Atlantic stingray, Dasyatis sabina. Serum corticosterone in S. tiburo increased following capture and again 24 h post-capture, possibly caused by interference with 1alpha-hydroxycorticosterone, the primary stress hormone in elasmobranchs. Higher serum concentrations in males compared to females were observed in both species. Variations in corticosterone also occurred during the reproductive cycle in both species. Consistent with other taxa, elevations in male bonnethead sharks and stingrays coincided with peak testicular development and mating. Elevations in female bonnethead sharks occurred from the time of mating through sperm storage into early gestation. In contrast, corticosterone levels in female stingrays were low during their protracted mating season, but elevated through late gestation and parturition. These results indicate that corticosterone has a limited role, if any, in acute and chronic stress associated with capture in S. tiburo, but likely has physiological functions associated with its glucocorticoid properties across the reproductive cycle of both species.     

Microbial stress priming: a meta‐analysis

Microbes have to cope with complex and dynamic environments, making it likely that anticipatory responses provide fitness benefits. Mild, previous stressors can prepare microbes (stress priming) to further and potentially damaging stressors (triggering). We here quantitatively summarize the findings from over 250 trials of 34 studies including bacteria and fungi, demonstrating that priming to stress has a beneficial impact on microbial survival. In fact, survival of primed microbes was about 10‐fold higher compared with that in non‐primed microbes. Categorical moderators related to microbial taxonomy and the kind of stress applied as priming or as triggering revealed significant differences of priming effect size among 14 different microbial species, 6 stress categories and stressor combination. We found that priming by osmotic, physiological and temperature stress had the highest positive effect sizes on microbial response. Cross‐protection was evident for physiological, temperature and pH stresses. Microbes are better prepared against triggering by oxidative, temperature and osmotic stress. Our finding of an overall positive mean effect of priming regardless of the microbial system and particular stressor provides unprecedentedly strong evidence of the broad ecological significance of microbial stress priming. These results further suggest that stress priming may be an important factor in shaping microbial communities.     

The cost of chronic stress: impacts of a nonhabituating stress response on metabolic variables and swimming performance in sturgeon

Metabolic scope for activity (MSA) and critical swimming velocity (U(crit)) were measured in green sturgeon exposed to two stressors daily for 28 consecutive days. The results were compared with unstressed fish in an effort to measure the "cost" of chronic stress. Chronic stress was simulated by exposing fish to a randomized order of acute stressors: a 5-min chasing stressor, a 10-min water depth reduction stressor, or a 5-min confinement stressor. The acute cortisol response to each stressor was initially determined, and the maintenance of that response was verified in 7-d intervals during the chronic stress regime. Exposure to the chronic stress regime resulted in a 25% reduction of MSA caused by significantly increased maintenance metabolic rate (0.27+/-0.01 vs. 0.19+/-0.02 mg O(2) h(-1) g(-1), chronic and control fish, respectively) but did not affect the U(crit) of sturgeon. In addition, a 50% reduction in liver glycogen levels and a twofold increase of resting plasma glucose levels were measured in chronically stressed fish. We conclude that our chronic stress regime resulted in a significant maintenance cost to green sturgeon, possibly because of their inability to habituate to the stressors, but did not decrease their swimming performance.     

Low mass-specific brain Na+/K+-ATPase activity in elasmobranch compared to teleost fishes: implications for the large brain size of elasmobranchs

Elasmobranch fishes have long been noted for having unusually large brains for ectotherms, and therefore may be exceptions to the rule that vertebrates in general devote less than 8% of their resting metabolic rate to the central nervous system. The brain mass of sharks, skates and rays is often several times larger than that of teleost fishes of the same size. Still, the underlying reasons for this have remained unclear. Ion pumping by the Na+/K+-ATPase is the single most energy consuming process in the brain. In this study, Na+/K+-ATPase activity was measured in the brain of four species of elasmobranchs and 11 species of teleosts. While the average brain mass of the elasmobranchs examined was approximately three times that of the teleosts, the mean specific Na+/K+-ATPase activity was only about one-third of that of the teleosts. Thus, the total brain Na+/K+-ATPase activity was similar in elasmobranchs and teleosts. This suggests that the large brain size of elasmobranchs is at least partly related to a low mass-specific rate of brain energy use.     

The neural control of feeding in elasmobranchs: A review and working model

A working model of the neural control of feeding in elasmobranchs is presented and summarized in graphic form. The model is based on a review of studies in sharks and batoids augmented by suggestions and comparisons from research in mammals and teleosts. The focal point of the model is a proposed Hypothalamic Feeding Area (HFA) that encompasses the medial periventricular zone in the inferior lobe and a small area immediately dorsal to it. Electrical stimulation in the HFA has evoked feeding in nurse sharks and neuropeptides and neurotransmitters known to influence feeding in mammals and teleosts have been localized immunocytochemically in the region in several elasmobranchs. The HFA of elasmobranchs appears to be analogous to and possibly homologous with ??hypothalamic feeding centers?? in bony fishes and tetrapods. Such ??centers?? are thought to integrate external and internal stimuli and control feeding in relation to available energy stores. The HFA??s strong olfactory connections in elasmobranchs are consistent with smell-induced feeding activities. In elasmobranchs, the HFA has reciprocal connections with the central pallium of the telencephalon, a region that processes visual, acoustic, mechanoreceptive and electroreceptive lateral line and possibly somatosensory information. These pathways may provide multisensory control in feeding. HFA connections with the cerebellum, brainstem and spinal cord most likely mediate hypothalamic co-ordination of the sensorimotor components of elasmobranch feeding. The review and model help to identify areas for suggested research.     

Sex, seasonal, and stress-related variations in elasmobranch corticosterone concentrations

Serum corticosterone was previously studied in numerous elasmobranch fishes (sharks, skates and rays), but the role of this steroid, widespread throughout many taxa, has yet to be defined. The goal of this study was to test whether corticosterone varied in response to acute and chronic capture stress, and across the reproductive cycle in the bonnethead shark, Sphyrna tiburo, and Atlantic stingray, Dasyatis sabina. Serum corticosterone in S. tiburo increased following capture and again 24 h post-capture, possibly caused by interference with 1α-hydroxycorticosterone, the primary stress hormone in elasmobranchs. Higher serum concentrations in males compared to females were observed in both species. Variations in corticosterone also occurred during the reproductive cycle in both species. Consistent with other taxa, elevations in male bonnethead sharks and stingrays coincided with peak testicular development and mating. Elevations in female bonnethead sharks occurred from the time of mating through sperm storage into early gestation. In contrast, corticosterone levels in female stingrays were low during their protracted mating season, but elevated through late gestation and parturition. These results indicate that corticosterone has a limited role, if any, in acute and chronic stress associated with capture in S. tiburo, but likely has physiological functions associated with its glucocorticoid properties across the reproductive cycle of both species.     

Characteristics of the conditioned motor reactions of unrestrained elasmobranches and teleosts

In elasmobranch (Scyllium canicula, Galleus canis) and teleost (Migull capitocum) fishes it is possible to form motor food-searching conditioned reflexes to discrimination of light and darkness. Some differences were revealed in ecological and conditioned motor behavioural activities in higher and lower sharks. Elasmobranch and teleost fishes exhibit significant differences in ecological, feeding and conditioned reflex behaviour. Nervous activity in elasmobranchs is characterized by lower and primitive organization as compared to that in teleosts.     

Alterations in hippocampal antioxidant enzyme activities and sympatho-adrenomedullary system of rats in response to different stress models

The study deals with activity of three antioxidant enzymes, copper, zinc-superoxide dismutase (CuZnSOD), manganese superoxide dismutase (MnSOD), catalase (CAT) in hippocampus of rats, following the exposure to single chronic (individual housing or forced swimming) and acute (immobilization or cold) stress, as well as to combined chronic/acute stress. In addition, plasma noradrenaline (NA) and adrenaline (A) concentrations were measured in the same stress conditions, because their autooxidation can add to the oxidative stress. We observed that i) long-term social isolation and repeated forced swimming had minor effects on plasma catecholamines, but in the long-term pretreated groups, acute stressors caused profound elevation NA and A levels, ii) chronic stressors activate antioxidant enzymes, iii) acute stressors decrease catalase activity, their effects on CuZnSOD appear to be stressor-dependent, whereas MnSOD is not affected by acute stressors, and iv) pre-exposure to chronic stress affects the antioxidant-related effects of acute stressors, but this effect depends to a large extent on the type of the chronic stressor. Based on both metabolic and neuroendocrine data, long-term isolation appears to be a robust psychological stressor and to induce a "priming" effect specifically on the CuZnSOD and CAT activity.     

Counteraction of urea destabilization of protein structure by methylamine osmoregulatory compounds of elasmobranch fishes

Intracellular fluids of marine elasmobranchs (sharks, skates and rays), holocephalans and the coelacanth contain urea at concentrations averaging 0.4m, high enough to significantly affect the structural and functional properties of many proteins. Also present in the cells of these fishes are a family of methylamine compounds, largely trimethylamine N-oxide with some betaine and sarcosine, and certain free amino acids, mainly beta-alanine and taurine, whose total concentration is approx. 0.2m. These methylamine compounds and amino acids have been found to be effective stabilizers of protein structure, and, at a 1:2 molar concentration ratio of these compounds to urea, perturbations of protein structure by urea are largely or fully offset. These counteracting effects of solutes on proteins are seen for: (1) thermal stability of protein secondary and tertiary structure (bovine ribonuclease); (2) the rate and extent of enzyme renaturation after acid denaturation (rabbit and shark lactate dehydrogenases); and (3) the reactivity of thiol groups of an enzyme (bovine glutamate dehydrogenase). Attaining osmotic equilibrium with seawater by these fishes has thus involved the selective accumulation of certain nitrogenous metabolites that individually have significant effects on protein structure, but that have virtually no net effects on proteins when these solutes are present at elasmobranch physiological concentrations. These experiments indicate that evolutionary changes in intracellular solute compositions as well as in protein amino acid sequences can have important roles in intracellular protein function.     

Temperature increase and its effects on fish stress physiology in the context of global warming

The capacity of fishes to cope with environmental variation is considered to be a main determinant of their fitness and is partly determined by their stress physiology. By 2100, global ocean temperature is expected to rise by 1–4°C, with potential consequences for stress physiology. Global warming is affecting animal populations worldwide through chronic temperature increases and an increase in the frequency of extreme heatwave events. As ectotherms, fishes are expected to be particularly vulnerable to global warming. Although little information is available about the effects of global warming on stress physiology in nature, multiple studies describe the consequences of temperature increases on stress physiology in controlled laboratory conditions, providing insight into what can be expected in the wild. Chronic temperature increase constitutes a physiological load that can alter the ability of fishes to cope with additional stressors, which might compromise their fitness. In addition, rapid temperature increases are known to induce acute stress responses in fishes and might be of ecological relevance in particular situations. This review summarizes knowledge about effects of temperature increases on the stress physiology of fishes and discusses these in the context of global warming.     

Does domestication process affect stress response in juvenile Eurasian perch Perca fluviatilis?

The objective was to evaluate the impact of domestication process on the physiological stress response of cultured Eurasian perch confronted to a chronic stress situation. Briefly, F1 and F4 juveniles were submitted to chronic confinement and investigated on days 5, 15 and 30. Capture and 15min-anesthesia were imposed on fish to assess the effect of preceding confinement on acute stress response. On day 30, the fish were finally challenged with Aeromonas hydrophila and sampled after 5 and 10 days for immune parameter measurements. Cortisol and glucose levels were not affected by confinement but increased significantly after acute stressor exposure. Moreover, cortisol rise following capture and anesthesia was higher in F1 confined-fish, suggesting that they have previously been affected by chronic confinement. A higher HSP70 level was also observed on day 30 in F1 confined-juveniles. During bacterial challenge, regardless of confinement level, F4 juveniles displayed higher lysozyme activity and agglutination response than F1 which may indicate a higher immune capacity in domesticated fish. In conclusion, chronic confinement stressor induced few physiological responses but may increase the responsiveness to other aquacultural stressors. Domestication process also seems to improve chronic stress resistance, growth as well as the immune status of the fish.     

Repeated thermal stressor causes chronic elevation of baseline corticosterone and suppresses the physiological endocrine sensitivity to acute stressor in the cane toad (Rhinella marina)

Extreme environmental temperature could impact the physiology and ecology of animals. The stress endocrine axis provides necessary physiological stress response to acute (day–day) stressors. Presently, there are no empirical evidences showing that exposure to extreme thermal stressor could cause chronic stress in amphibians. This could also modulate the physiological endocrine sensitivity to acute stressors and have serious implications for stress coping in amphibians, particularly those living in fragmented and disease prone environments. We addressed this important question using the cane toad (Rhinella marina) model from its introduced range in Queensland, Australia. We quantified their physiological endocrine sensitivity to a standard acute (capture and handling) stressor after exposing the cane toads to thermal shock at 35 °C for 30 min daily for 34 days. Corticosterone (CORT) responses to the capture and handling protocol were measured on three sampling intervals (days 14, 24, and 34) to determine whether the physiological endocrine sensitivity was maintained or modulated over-time. Two control groups (C1 for baseline CORT measurement only and C2 acute handled only) and two temperature treatment groups (T1 received daily thermal shock up to day 14 only and a recovery phase of 20 days and T2 received thermal shock daily for 34 days). Results showed that baseline CORT levels remained high on day 14 (combined effect of capture, captivity and thermal stress) for both T1 and T2. Furthermore, baseline CORT levels decreased for T1 once the thermal shock was removed after day 14 and returned to baseline by day 29. On the contrary, baseline CORT levels kept on increasing for T2 over the 34 days of daily thermal shocks. Furthermore, the magnitudes of the acute CORT responses or physiological endocrine sensitivity were consistently high for both C1 and T1. However, acute CORT responses for T2 toads were dramatically reduced between days 24 and 34. These novel findings suggest that repeated exposure to extreme thermal stressor could cause chronic stress and consequently suppress the physiological endocrine sensitivity to acute stressors (e.g. pathogenic diseases) in amphibians.     

Seasonal modulation in the secondary stress response of a carcharhinid shark, Rhizoprionodon terraenovae

Some animals have the ability to modulate their stress response depending on the type and duration of the stressor. Modulations can initiate behavioral changes that increase fitness during the stressful period. The goal of this study was to determine if Atlantic sharpnose sharks, Rhizoprionodon terraenovae, exhibit seasonal modulations in their secondary stress parameters. Mature, male Atlantic sharpnose sharks were acutely stressed and serially sampled for one-hour, during spring, summer, and fall. An elevated stress response was observed for plasma glucose, lactate and osmolality during summer compared to spring and fall. Glucose also exhibited elevated initial concentrations, followed by a linear response during summer; varying from the asymptotic response during spring and fall. Hematocrit did not show differences over time or season; however, the power of the analysis was low due to the small sample size. When an additional 120 samples were included in the analysis, significantly higher initial hematocrit values were found during summer. Based on these results we suggest that summer is a demanding time for Atlantic sharpnose sharks.     

Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids

Physical, chemical and perceived stressors can all evoke non-specificresponses in fish, which are considered adaptive to enable thefish to cope with the disturbance and maintain its homeostaticstate. If the stressor is overly severe or long-lasting to thepoint that the fish is not capable of regaining homeostasis,then the responses themselves may become maladaptive and threatenthe fish's health and well-being. Physiological responses tostress are grouped as primary, which include endocrine changessuch as in measurable levels of circulating catecholamines andcorticosteroids, and secondary, which include changes in featuresrelated to metabolism, hydromineral balance, and cardiovascular,respiratory and immune functions. In some instances, the endocrineresponses are directly responsible for these secondary responsesresulting 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 orwhole-animal changes in performance, such as in growth, diseaseresistance and behavior, can result from the primary and secondaryresponses and possibly affect survivorship. Fishes display a wide variation in their physiological responsesto stress, which is clearly evident in the plasma corticosteroidchanges, chiefly cortisol in actinopterygian fishes, that occurfollowing a stressful event. The characteristic elevation incirculating cortisol during the first hour after an acute disturbancecan vary by more than two orders of magnitude among speciesand genetic history appears to account for much of this interspecificvariation. An appreciation of the factors that affect the magnitude,duration and recovery of cortisol and other physiological changescaused by stress in fishes is important for proper interpretationof experimental data and design of effective biological monitoringprograms.     

Absence of cellular damage in tropical newly hatched sharks (<Emphasis Type="Italic">Chiloscyllium plagiosum</Emphasis>) under ocean acidification conditions

Sharks have maintained a key role in marine food webs for 400 million years and across varying physicochemical contexts, suggesting plasticity to environmental change. In this study, we investigated the biochemical effects of ocean acidification (OA) levels predicted for 2100 (pCO₂ ~?900 μatm) on newly hatched tropical whitespotted bamboo sharks (Chiloscyllium plagiosum). Specifically, we measured lipid, protein, and DNA damage levels, as well as changes in the activity of antioxidant enzymes and non-enzymatic ROS scavengers in juvenile sharks exposed to elevated CO₂ for 50 days following hatching. Moreover, we also assessed the secondary oxidative stress response, i.e., heat shock response and ubiquitin levels. Newly hatched sharks appear to cope with OA-related stress through a range of tissue-specific biochemical strategies, specifically through the action of antioxidant enzymatic compounds. Our findings suggest that ROS-scavenging molecules, rather than complex enzymatic proteins, provide an effective defense mechanism in dealing with OA-elicited ROS formation. We argue that sharks’ ancient antioxidant system, strongly based on non-enzymatic antioxidants (e.g., urea), may provide them with resilience towards OA, potentially beyond the tolerance of more recently evolved species, i.e., teleosts. Nevertheless, previous research has provided evidence of detrimental effects of OA (interacting with other climate-related stressors) on some aspects of shark biology. Moreover, given that long-term acclimation and adaptive potential to rapid environmental changes are yet experimentally unaccounted for, future research is warranted to accurately predict shark physiological performance under future ocean conditions.     

Social isolation and the inflammatory response: sex differences in the enduring effects of a prior stressor

Numerous epidemiological studies have demonstrated an association between persistent social isolation and "all-cause" morbidity and mortality. To date, no causal mechanism for these findings has been established. Whereas animal studies have often reported short-term effects of social isolation on biological systems, the long-term effects of this adverse psychological state have been understudied. This is the first animal study to examine the effects of long-term social isolation from weaning through young adulthood on an innate inflammatory response linked to numerous disease processes. Results presented here offer a plausible link between vulnerability to disease and social neglect. For socially isolated male and female Sprague-Dawley rats, a naturally gregarious species, formation of a granuloma in response to a subcutaneous injection of carrageenin (seaweed) was significantly delayed compared with the response of animals housed in single-sex groups of five. Significant sex differences, however, emerged when an acute prior stressor was superimposed on the experience of chronic social isolation. In this context, isolated females produced a more robust inflammatory response than isolated males. This sexual dimorphism at the nexus of chronic social isolation, acute stress, and inflammatory processes may account for the observation in humans that men with low levels of social integration are more vulnerable to disease and death than women.     

The Acoustical Biology of Elasmobranchs

A report on the auditory capabilities and their associated functions of elasmobranch fishes along with a brief review of the physics of underwater sound as it relates to hearing by fishes is provided. The inner ears of elasmobranchs possess structures that are no different from other fishes, except for an enlarged macula neglecta, which is unique among fishes. Hearing abilities among sharks (the only elasmobranchs examined) have demonstrated highest sensitivity to low frequency sound (40Hz to approximately 800Hz), which is sensed solely through the particle-motion component of an acoustical field. Free-ranging sharks are attracted to sounds possessing specific characteristics: irregularly pulsed, broad-band (most attractive frequencies: below 80Hz), and transmitted without a sudden increase in intensity. Such sounds are reminiscent of those produced by struggling prey. A sound, even an attractive one, can also result in immediate withdrawal by sharks from a source, if its intensity suddenly increases 20dB [10 times] or more above a previous transmission. Present evidence also shows that the lateral line system does not respond to normal acoustical stimuli. Morphological and physiological evidence suggest that the maculae neglecta possess acoustical relevance and may explain directionality of response despite physical principles that provide still other hypotheses for acoustical directionality. Brain centers controlling acoustical response, particularly among sharks, must be explored in the near future with careful consideration of the habits of subjects based on indications of species-differences regarding the importance of acoustical stimuli to their activities. Numerous facts and ideas about the acoustical biology of elasmobranch fishes make certain that future research will be most rewarding.     

哺乳动物的生理应激反应及其生态适应性

应激反应是哺乳动物的基本生理现象之一。目前,与应激有关的研究主要来自生物医学和神经内分泌学。虽然Hans Selye 提出了个体对应激的普遍性适应综合症概念,但目前的研究还主要集中于应激对个体的负效应以及与应激相关的疾病研究。然而,从进化角度似乎很难理解在数亿年的进化过程中,动物应激反应仅简单地
进化为影响个体健康并导致个体患病的一种生理过程。本文从进化的角度,综述了应激反应与动物繁殖对策的关系以及个体对环境应激源的应对类型,并阐述了动物应激反应的适应和进化意义。