Modern hagfishes are considered to be the most primitive of the living craniates and along with their close jawless agnathan relative, the lamprey, take us back an astonishing 500
million years to ...the base of the vertebrate evolutionary tree. The unique osmoconforming strategy of the hagfish, whereby the osmotic constituents of the blood plasma bear more of a resemblance to marine invertebrates than vertebrates, has been classically depicted in comparative physiology textbooks for many years. Fifty years ago in this journal, Bellamy and Chester Jones Bellamy and Chester Jones, 1961. CBP 3, 173–183 published a paper on the chemical composition of the tissues of the Atlantic hagfish,
Myxine glutinosa. This publication was one of a flurry of papers published in the 50s, 60s and early 70s focused on describing the ionic and osmotic components of this bizarre fish. Here we take a retrospective look at the research that has taken place on these intriguing animals prior to and following the Bellamy and Chester Jones manuscript, focusing on tissue chemical compositions, the possible role of amino acids, and our current view on ion regulation, metabolism and hypoxia tolerance.
Salinity decreases are experienced by many marine elasmobranchs. To understand how these fishes cope with hyposmotic stress on a cellular level, we used the spiny dogfish shark (
Squalus acanthias
) ...as a model to test whether a reciprocal relationship exists between the cell’s two primary protein protection mechanisms, the chemical (e.g., trimethylamine oxide, TMAO) and molecular (e.g., heat shock protein 70, HSP70) chaperone systems. This relationship is interesting given that many elasmobranchs are expected to gain water and lose osmolytes, chemical chaperones, and ions as they osmoconform to new, lowered salinity. Dogfish were cannulated for repeated blood sampling and exposed to 70 % seawater (SW) for 48 h. These hyposmotic conditions had no effect on red blood cell (RBC) and white muscle TMAO concentrations, and did not result in HSP70 induction or signs of protein damage (i.e., increased ubiquitin), suggesting that TMAO levels were sufficiently protective in these tissues. However, in the gill, we observed a significant decrease in TMAO concentration and a significant induction of HSP70 as well as signs of protein damage. In the face of this cellular stress response, gill Na
+
/K
+
-ATPase (NKA) activity significantly increased during hyposmotic conditions, as expected. We suggest that this functional preservation in the gill is partly the result of HSP70 induction with lowered salinity. We conclude a reciprocal relationship between TMAO and HSP70 in the gills of dogfish as a result of in vivo hyposmotic stress. When osmotically induced protein damage surpasses the protective capacity of remaining TMAO, HSP70 is induced to preserve tissue and organismal function.
► Warm-acclimated males exposed EE2 induced more vtg1 than cold-acclimated males. ► Changes in salinity or acute heat shock did not affect vtg1 mRNA induction. ► HSP90 and HSP70 have little to do ...with the increased vtg1 in warm-acclimated fish.
Mummichog (Fundulus heteroclitus), an estuarine fish of the western Atlantic, were acclimated to three salinities (0, 16 or 32ppt) or three temperatures (10, 20 or 26°C) and exposed to nominal 50 or 250ng/L 17α-ethynylestradiol (EE2) for 14 days. In a separate experiment, fish were exposed to the same levels of EE2 and were subjected to a 1h heat shock (20–30°C) on the 14th day and allowed to recover for 20h. We were interested in whether or not susceptibility to EE2 exposure, as indicated by increases in vitellogenin (vtg) gene expression would change with high and low salinity, warm or cold temperature acclimation or acute heat shock. We also investigated the potential role of heat shock proteins (HSPs) under these conditions. Liver vtg1 mRNA was significantly induced in male mummichog exposed to 50 and 250ng/L EE2, but salinity acclimation or acute heat shock did not further affect this induction. Males acclimated to 26°C and exposed to 250ng/L EE2 induced 3.5-fold more vtg1 mRNA than EE2 exposed males acclimated to 10°C. HSP90 and HSP70 protein were largely unaffected by EE2 exposure. Our findings suggest that mummichog are more susceptible to EE2 under sustained temperature increases that may occur seasonally or with warming of coastal waters.
Juvenile salmonid fish readily form dominance hierarchies when faced with limited resources. While these social interactions may result in profound behavioural and physiological stress, it is unknown ...if this social stress is evident at the level of the cellular stress response—specifically, the induction of stress or heat shock proteins (Hsps). Thus, the goal of our study was to determine if Hsps are induced during hierarchy formation in juvenile rainbow trout (Oncorhynchus mykiss). To this end, we measured levels of three Hsps, Hsp70, Hsc (heat shock cognate)70 and Hsp90 in the white muscle, liver and brain of trout that had been interacting for 36 h, 72 h or 6 days. Our data indicate that Hsps are induced in both dominant and subordinate fish in a time- and tissue-specific manner. In further mechanistic experiments on fasted and cortisol-treated fish, we demonstrated that high plasma cortisol does not affect Hsp induction in trout white muscle or liver, but both conditions may be part of the mechanism for Hsp induction with social stress in the brain. We conclude that the behavioural and physiological stress experienced by juvenile rainbow trout in dominance hierarchies can be extended to the induction of Hsps.
The shortfin mako shark (Isurus oxyrinchus) is a species commonly targeted by commercial and recreational anglers in many parts of the developed world. In Australia, the species is targeted by ...recreational anglers only, under the assumption that most of the sharks are released and populations remain minimally impacted. If released sharks do not survive, the current management strategy will need to be revised. Shortfin mako sharks are commonly subjected to lengthy angling events; however, their endothermic physiology may provide an advantage over ectothermic fishes when recovering from exercise. This study assessed the post-release survival of recreationally caught shortfin mako sharks using Survivorship Pop-up Archival Transmitting (sPAT) tags and examined physiological indicators of capture stress from blood samples as well as any injuries that may be caused by hook selection. Survival estimates were based on 30 shortfin mako sharks captured off the south-eastern coast of Australia. Three mortalities were observed over the duration of the study, yielding an overall survival rate of 90%. All mortalities occurred in sharks angled for <30 min. Sharks experienced increasing plasma lactate with longer fight times and higher sea surface temperatures (SSTs), increased plasma glucose at higher SSTs and depressed expression of heat shock protein 70 and β-hydroxybutyrate at higher SSTs. Long fight times did not impact survival. Circle hooks significantly reduced foul hooking when compared with J hooks. Under the conditions of this study, we found that physical injury associated with hook choice is likely to have contributed to an increased likelihood of mortality, whereas the high aerobic scope associated with the species' endothermy probably enabled it to cope with long fight times and the associated physiological responses to capture.
When faced with stress, animals use physiological and cellular strategies to preserve homeostasis. We were interested in how these high-level stress responses are integrated at the level of the whole ...animal. Here, we investigated the capacity of the physiological stress response, and specifically the β-adrenergic response, to affect the induction of the cellular heat shock proteins, HSPs, following a thermal stress in vivo. We predicted that blocking β-adrenergic stimulation during an acute heat stress in the whole animal would result in reduced levels of HSPs in red blood cells (RBCs) of rainbow trout compared to animals where adrenergic signaling remained intact. We first determined that a 1 h heat shock at 25 °C in trout acclimated to 13 °C resulted in RBC adrenergic stimulation as determined by a significant increase in cell swelling, a hallmark of the β-adrenergic response. A whole animal injection with the β
2
-adrenergic antagonist, ICI-118,551, successfully reduced this heat-induced RBC swelling. The acute heat shock caused a significant induction of HSP70 in RBCs of 13 °C-acclimated trout as well as a significant increase in plasma catecholamines. When heat-shocked fish were treated with ICI-118,551, we observed a significant attenuation of the HSP70 response. We conclude that circulating catecholamines influence the cellular heat shock response in rainbow trout RBCs, demonstrating physiological/hormonal control of the cellular stress response.
When faced with stress, animals use physiological and cellular strategies to preserve homeostasis. We were interested in how these high-level stress responses are integrated at the level of the whole ...animal. Here, we investigated the capacity of the physiological stress response, and specifically the beta-adrenergic response, to affect the induction of the cellular heat shock proteins, HSPs, following a thermal stress in vivo. We predicted that blocking beta-adrenergic stimulation during an acute heat stress in the whole animal would result in reduced levels of HSPs in red blood cells (RBCs) of rainbow trout compared to animals where adrenergic signaling remained intact. We first determined that a 1 h heat shock at 25 °C in trout acclimated to 13 °C resulted in RBC adrenergic stimulation as determined by a significant increase in cell swelling, a hallmark of the beta-adrenergic response. A whole animal injection with the beta^sub 2^-adrenergic antagonist, ICI-118,551, successfully reduced this heat-induced RBC swelling. The acute heat shock caused a significant induction of HSP70 in RBCs of 13 °C-acclimated trout as well as a significant increase in plasma catecholamines. When heat-shocked fish were treated with ICI-118,551, we observed a significant attenuation of the HSP70 response. We conclude that circulating catecholamines influence the cellular heat shock response in rainbow trout RBCs, demonstrating physiological/hormonal control of the cellular stress response.PUBLICATION ABSTRACT
Shark nurseries are susceptible to environmental fluctuations in salinity because of their shallow, coastal nature; however, the physiological impacts on resident elasmobranchs are largely unknown. ...Gummy sharks (Mustelus antarcticus) and school sharks (Galeorhinus galeus) use the same Tasmanian estuary as a nursery ground; however, each species has distinct distribution patterns that are coincident with changes in local environmental conditions, such as increases in salinity. We hypothesized that these differences were directly related to differential physiological tolerances to high salinity. To test this hypothesis, we exposed wild, juvenile school and gummy sharks to an environmentally relevant hypersaline (120% SW) event for 48 h. Metabolic rate decreased 20-35% in both species, and gill Na(+)/K(+)-ATPase activity was maintained in gummy sharks but decreased 37% in school sharks. We measured plasma ions (Na(+), K(+), Cl(-)) and osmolytes urea and trimethylamine oxide (TMAO), and observed a 33% increase in plasma Na(+) in gummy sharks with hyperosmotic exposure, while school sharks displayed a typical ureosmotic increase in plasma urea (∼20%). With elevated salinity, gill TMAO concentration increased by 42% in school sharks and by 30% in gummy sharks. Indicators of cellular stress (heat shock proteins HSP70, 90 and 110, and ubiquitin) significantly increased in gill and white muscle in both a species- and a tissue-specific manner. Overall, gummy sharks exhibited greater osmotic perturbation and ionic dysregulation and a larger cellular stress response compared with school sharks. Our findings provide physiological correlates to the observed distribution and movement of these shark species in their critical nursery grounds.
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