Some euryhalinity may be more common than expected in marine elasmobranchs: The example of the South American skate Zapteryx brevirostris (Elasmobranchii, Rajiformes, Rhinobatidae)
Abstract:Elasmobranchs are essentially marine, but ~15% of the species occur in brackish or freshwater. The Brazilian marine coastal skate Zapteryx brevirostris, non-reported in nearby estuaries, was submitted to 35, 25, 15, and 5 psu, for 6 or 12h (n=6). Plasma was assayed for osmolality, urea, and ions (Na(+), Cl(-), K(+), Mg(2+)). Muscle water content was determined, and the rectal gland, kidney and gills were removed for carbonic anhydrase (CA) and Na(+),K(+)-ATPase (NKA) activities. The skate survived to all treat… Show more
“…Therefore lower urea concentrations in the current study may represent ongoing changes in the rate of urea synthesis and retention in response to increased environmental salinity. A similar delay is observed in elasmobranchs acclimating to decreased salinities, in which reported urea concentrations are dependent not only on salinity but also the duration of exposure with longer exposures to hypoosmotic conditions resulting in lower urea levels [23]. Figure 1Plasma components and salinity acclimation.…”
Section: Resultssupporting
confidence: 57%
“…Altered Na + /K + -ATPase activity has also been reported for stenohaline species such as the marine South American skate ( Zapteryx brevirostris ), in which decreased salinity does not affect gill Na + /K + -ATPase but results in lower enzyme activity in the rectal gland [23]. It is likely that changes in enzyme activity occur at several levels, including the potential activation of latent Na + /K + -ATPase protein or translation of steady-state mRNAs, which would facilitate rapid plasticity of the elasmobranch gill and rectal gland in response to frequent changes in environmental salinity.…”
BackgroundThe salt-secreting rectal gland plays a major role in elasmobranch osmoregulation, facilitating ion balance in hyperosmotic environments in a manner analogous to the teleost gill. Several studies have examined the central role of the sodium pump Na+/K+-ATPase in osmoregulatory tissues of euryhaline elasmobranch species, including regulation of Na+/K+-ATPase activity and abundance in response to salinity acclimation. However, while the transcriptional regulation of Na+/K+-ATPase in the teleost gill has been well documented the potential for mRNA regulation to facilitate rectal gland plasticity during salinity acclimation in elasmobranchs has not been examined. Therefore, in this study we acclimated Atlantic stingrays, Dasyatis sabina (Lesueur) from 11 to 34 ppt salinity over 3 days, and examined changes in plasma components as well as gill and rectal gland Na+/K+-ATPase α1 (atp1a1) mRNA expression.ResultsAcclimation to increased salinity did not affect hematocrit but resulted in significant increases in plasma osmolality, chloride and urea. Rectal gland atp1a1 mRNA expression was higher in 34 ppt-acclimated D. sabina vs. controls. There was no significant change in gill atp1a1 mRNA expression, however mRNA expression of this gene in the gill and rectal gland were negatively correlated.ConclusionsThis study demonstrates regulation of atp1a1 in the elasmobranch salt-secreting gland in response to salinity acclimation and a negative relationship between rectal gland and gill atp1a1 expression. These results support the hypothesis that the gill and rectal gland play opposing roles in ion balance with the gill potentially facilitating ion uptake in hypoosmotic environments. Future studies should further examine this possibility as well as potential differences in the regulation of Na+/K+-ATPase gene expression between euryhaline and stenohaline elasmobranch species.
“…Therefore lower urea concentrations in the current study may represent ongoing changes in the rate of urea synthesis and retention in response to increased environmental salinity. A similar delay is observed in elasmobranchs acclimating to decreased salinities, in which reported urea concentrations are dependent not only on salinity but also the duration of exposure with longer exposures to hypoosmotic conditions resulting in lower urea levels [23]. Figure 1Plasma components and salinity acclimation.…”
Section: Resultssupporting
confidence: 57%
“…Altered Na + /K + -ATPase activity has also been reported for stenohaline species such as the marine South American skate ( Zapteryx brevirostris ), in which decreased salinity does not affect gill Na + /K + -ATPase but results in lower enzyme activity in the rectal gland [23]. It is likely that changes in enzyme activity occur at several levels, including the potential activation of latent Na + /K + -ATPase protein or translation of steady-state mRNAs, which would facilitate rapid plasticity of the elasmobranch gill and rectal gland in response to frequent changes in environmental salinity.…”
BackgroundThe salt-secreting rectal gland plays a major role in elasmobranch osmoregulation, facilitating ion balance in hyperosmotic environments in a manner analogous to the teleost gill. Several studies have examined the central role of the sodium pump Na+/K+-ATPase in osmoregulatory tissues of euryhaline elasmobranch species, including regulation of Na+/K+-ATPase activity and abundance in response to salinity acclimation. However, while the transcriptional regulation of Na+/K+-ATPase in the teleost gill has been well documented the potential for mRNA regulation to facilitate rectal gland plasticity during salinity acclimation in elasmobranchs has not been examined. Therefore, in this study we acclimated Atlantic stingrays, Dasyatis sabina (Lesueur) from 11 to 34 ppt salinity over 3 days, and examined changes in plasma components as well as gill and rectal gland Na+/K+-ATPase α1 (atp1a1) mRNA expression.ResultsAcclimation to increased salinity did not affect hematocrit but resulted in significant increases in plasma osmolality, chloride and urea. Rectal gland atp1a1 mRNA expression was higher in 34 ppt-acclimated D. sabina vs. controls. There was no significant change in gill atp1a1 mRNA expression, however mRNA expression of this gene in the gill and rectal gland were negatively correlated.ConclusionsThis study demonstrates regulation of atp1a1 in the elasmobranch salt-secreting gland in response to salinity acclimation and a negative relationship between rectal gland and gill atp1a1 expression. These results support the hypothesis that the gill and rectal gland play opposing roles in ion balance with the gill potentially facilitating ion uptake in hypoosmotic environments. Future studies should further examine this possibility as well as potential differences in the regulation of Na+/K+-ATPase gene expression between euryhaline and stenohaline elasmobranch species.
“…Our results are consistent with the majority of literature regarding elasmobranch branchial NKA activity with changing salinity in that, as salinity decreases, gill NKA activity and abundance increases (Piermarini and Evans 2000;Duncan et al 2009;Reilly et al 2011). It has been suggested, however, that the branchial NKA response to changing salinity is species (Pillans et al 2005) as well as duration specific (Wosnick and Freire 2013). It is likely that the increased NKA activity with decreased salinity observed here and in previous studies (Piermarini and Evans 2000;Duncan et al 2009;Reilly et al 2011) is due to its role in ion uptake (Wright and Wood 2015 for review).…”
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.
“…In marine fish, it occurs through seawater drinking, followed by its absorption by the gastrointestinal tract. Euryhaline sharks and rays display reduction in plasma urea when facing salinity decrease, especially upon acclimation (Wosnick and Freire 2013). To absorb NaCl from freshwater requires an additional pump, the H + -V-ATPase (apical), in addition to the Na + /K + -ATPase (basolateral).…”
This study brings an integrated analysis about the relationship between water deterioration and its physiological consequences in live fish transport. The analysis was focused on the transport water and its deterioration, and physiological challenges imposed on the fish. Usual commercial handling procedures employed to mitigate fish stress during transport were discussed. Future topics of research for the establishment of safer fish transport protocols were proposed. Transport was classified into short (≤8 h) or long transport (>8 h). The main issue in short transports should be the prevention of water pH reduction, while in long transports it is the increase in ammonia. Plasma cortisol is the most employed marker for stress and is acutely elevated upon short episodes of transport, but remains elevated even in long‐transport events. Plasma glucose is perhaps a better marker for handling stress. Plasma lactate, pH, osmolality CO2 and ions should be more often evaluated. Plasma Na+ and Cl‐ are very useful markers of acidosis, due to their respective exchange for H+ and HCO3−, for acid–base regulation. The establishment of species‐specific transport protocols should be preceded by such combined analyses of water and physiological parameters.
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