Age-Dependent Decline in Salinity Tolerance in a Euryhaline Fish (original) (raw)
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Ontogeny of osmoregulation in postembryonic fish: A review
Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 2005
Salinity and its variations are among the key factors that affect survival, metabolism and distribution during the fish development. The successful establishment of a fish species in a given habitat depends on the ability of each developmental stage to cope with salinity through osmoregulation. It is well established that adult teleosts maintain their blood osmolality close to 300 mosM kg À1 due to ion and water regulation effected at several sites: tegument, gut, branchial chambers, urinary organs. But fewer data are available in developing fish. We propose a review on the ontogeny of osmoregulation based on studies conducted in different species. Most teleost prelarvae are able to osmoregulate at hatch, and their ability increases in later stages. Before the occurrence of gills, the prelarval tegument where a high density of ionocytes (displaying high contents of Na + /K +-ATPase) is located appears temporarily as the main osmoregulatory site. Gills develop gradually during the prelarval stage along with the numerous ionocytes they support. The tegument and gill Na + /K +-ATPase activity varies ontogenetically. During the larval phase, the osmoregulatory function shifts from the skin to the gills, which become the main osmoregulatory site. The drinking rate normalized to body weight tends to decrease throughout development. The kidney and urinary bladder develop progressively during ontogeny and the capacity to produce hypotonic urine at low salinity increases accordingly. The development of the osmoregulatory functions is hormonally controlled. These events are interrelated and are correlated with changes in salinity tolerance, which often increases markedly at the metamorphic transition from larva to juvenile. In summary, the ability of ontogenetical stages of fish to tolerate salinity through osmoregulation relies on integumental ionocytes, then digestive tract development and drinking rate, developing branchial chambers and urinary organs. The physiological changes leading to variations in salinity tolerance are one of the main basis of the ontogenetical migrations or movements between habitats of different salinity regimes.
Moorman et al 2015 The Effects of Acute Salinity Challenges on Osmoregulation - JEB.pdf
This study characterizes the differences in osmoregulatory capacity among Mozambique tilapia, Oreochromis mossambicus, reared in freshwater (FW), in seawater (SW) or under tidally driven changes in salinity. This was addressed through the use of an abrupt exposure to a change in salinity. We measured changes in: (1) plasma osmolality and prolactin (PRL) levels; (2) pituitary expression of prolactin (PRL) and its receptors, PRLR1 and PRLR2; (3) branchial expression of PRLR1, PRLR2, Na + /Cl − co-transporter (NCC), Na + /K + /2Cl − co-transporter (NKCC), α1a and α1b isoforms of Na + /K + -ATPase (NKA), cystic fibrosis transmembrane conductance regulator (CFTR), aquaporin 3 (AQP3) and Na + /H + exchanger 3 (NHE3). Mozambique tilapia reared in a tidal environment successfully adapted to SW while fish reared in FW did not survive a transfer to SW beyond the 6 h sampling. With the exception of CFTR, the change in the expression of ion pumps, transporters and channels was more gradual in fish transferred from tidally changing salinities to SW than in fish transferred from FW to SW. Upon transfer to SW, the increase in CFTR expression was more robust in tidal fish than in FW fish. Tidal and SW fish successfully adapted when transferred to FW. These results suggest that Mozambique tilapia reared in a tidally changing salinity, a condition that more closely represents their natural history, gain an adaptive advantage compared with fish reared in FW when facing a hyperosmotic challenge.
Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 2015
a b s t r a c t 6 We investigated the impact of nutritional status on the physiological, metabolic and ion-osmoregulatory 20 performance of European sea bass (Dicentrarchus labrax) when acclimated to seawater (32 ppt), brackish 21 water (20 and 10 ppt) and hyposaline water (2.5 ppt) for 2 weeks. Following acclimation to different salinities, 22 fish were either fed or fasted (unfed for 14 days). Plasma osmolality, [Na + ], [Cl − ] and muscle water content 23 were severely altered in fasted fish acclimated to 10 and 2.5 ppt in comparison to normal seawater-acclimated 24 fish, suggesting ion regulation and acid-base balance disturbance. In contrast to feed-deprived fish, fed fish 25 were able to avoid osmotic perturbation more effectively. This was accompanied by an increase in Na + /K + -26 ATPase expression and activity, transitory activation of H + -ATPase (only at 2.5 ppt) and down-regulation of 27 Na + /K + /2Cl − gene expression. Ammonia excretion rate was inhibited to a larger extent in fasted fish acclimated 28 to low salinities while fed fish were able to excrete much more efficiently. Consequently, the build-up of 29 ammonia in the plasma of fed fish was relatively lower. Energy stores, especially glycogen and lipid, dropped 30 in the fasted fish at low salinities and progression towards the anaerobic metabolic pathway became evident 31 by an increase in plasma lactate level. Overall, the results indicate no osmotic stress in both feeding treatments 32 within the salinity range of 32 to 20 ppt. However, at lower salinities (10-2.5 ppt) feed deprivation tends to 33 reduce physiological, metabolic, ion-osmoregulatory and molecular compensatory mechanisms and thus limits 34 the fish's abilities to adapt to a hypo-osmotic environment. 35
Past seawater experience enhances seawater adaptability in medaka, Oryzias latipes
Zoological Letters, 2016
Background: During the course of evolution, fishes have acquired adaptability to various salinity environments, and acquirement of seawater (SW) adaptability has played important roles in fish evolution and diversity. However, little is known about how saline environments influence the acquirement of SW adaptability. The Japanese medaka Oryzias latipes is a euryhaline species that usually inhabits freshwater (FW), but is also adaptable to full-strength SW when transferred through diluted SW. In the present study, we examined how past SW experience affects hyposmoregulatory ability in Japanese medaka. Results: For the preparation of SW-experienced fish, FW medaka were acclimated to SW after pre-acclimation to 1/2 SW, and the SW-acclimated fish were transferred back to FW. The SW-experienced fish and control FW fish (SW-inexperienced fish) were transferred directly to SW. Whereas control FW fish did not survive direct transfer to SW, 1/4 of SW-experienced fish adapted successfully to SW. Although there were no significant differences in blood osmolality and plasma Na + and Cl − concentrations between SW-experienced and control FW medaka in FW, increments in these parameters following SW transfer were lower in SW-experienced fish than in control FW fish. The gene expression of SW-type Na + , K +-ATPase (NKA) in the gills of SW-experienced medaka increased more quickly after direct SW transfer compared with the expression in control FW fish. Prior to SW transfer, the density of NKA-immunoreactive ionocytes in the gills was higher in SW-experienced fish than in control FW fish. Ionocytes expressing CFTR Cl − channel at the apical membrane and those forming multicellular complexes, both of which were characteristic of SW-type ionocytes, were also increased in SW-experienced fish. Conclusion: These results indicate that past SW experience enhances the capacity of Na + and Cl − secretion in ionocytes and thus hypoosmoregulatory ability of Japanese medaka, suggesting the presence of epigenetic mechanisms involved in seawater adaptation.
PLoS ONE, 2014
Salinity is one of the key factors that affects metabolism, survival and distribution of fish species, as all fish osmoregulate and euryhaline fish maintain osmotic differences between their extracellular fluid and either freshwater or seawater. The threespine stickleback (Gasterosteus aculeatus) is a euryhaline species with populations in both marine and freshwater environments, where the physiological and genomic basis for salinity tolerance adaptation is not fully understood. Therefore, our main objective in this study was to investigate gene expression of three targeted osmoregulatory genes (Na + /K +-ATPase (ATPA13), cystic fibrosis transmembrane regulator (CFTR) and a voltage gated potassium channel gene (KCNH4) and one stress related heat shock protein gene (HSP70)) in gill tissue from marine and freshwater populations when exposed to non-native salinity for periods ranging from five minutes to three weeks. Overall, the targeted genes showed highly plastic expression profiles, in addition the expression of ATP1A3 was slightly higher in saltwater adapted fish and KCNH4 and HSP70 had slightly higher expression in freshwater. As no pronounced changes were observed in the expression profiles of the targeted genes, this indicates that the osmoregulatory apparatuses of both the marine and landlocked freshwater stickleback population have not been environmentally canalized, but are able to respond plastically to abrupt salinity challenges.
Comparative Biochemistry and Physiology A-molecular & Integrative Physiology, 2009
Euryhaline tilapia (Oreochromis mossambicus) survived in brackish water (BW; 20‰) but died in seawater (SW; 35‰) within 6 h when transferred directly from fresh water (FW). The purpose of this study was to clarify responses in gills of FW tilapia to various hyperosmotic shocks induced by BW or SW. In FWacclimated tilapia, scanning electron micrographs of gills revealed three subtypes of MR cell apical surfaces: wavy-convex (subtype I), shallow-basin (subtype II), and deep-hole (subtype III). Density of apical surfaces of mitochondrion-rich (MR) cell in gills of the BW-transfer tilapia decreased significantly within 3 h posttransfer due to disappearance of subtype I cells, but increased from 48 h post-transfer because of increasing density of subtype III cells. SW-transfer individuals, however, showed decreased density of MR cell openings after 1 h post-transfer because subtype I MR cell disappeared. On the other hand, relative branchial Na + /K + -ATPase (NKA) α1-subunit mRNA levels, protein abundance, and NKA activity of the BW-transfer group increased significantly at 6, 12, and 12 h post-transfer, respectively. In the SW-transfer group, relative mRNA and protein abundance of gill NKA α1-subunit did not change while NKA activity declined before dying in 5 h. Upon SW transfer, dramatic increases (nearly 2-fold) of plasma osmolality, [Na + ], and [Cl − ] were found prior to death. For the BW-transfer group, plasma osmolality was eventually controlled by 96 h post-transfer by enhancement of NKA expression and subtype III MR cell. The success or failure of NKA activation from gene to functional protein as well as the development of specific SW subtype in gills were crucial for the survival of euryhaline tilapia to various hyperosmotic shocks.
Evolutionary Ecology Research, 2016
Background: Post-Pleistocene diversification of threespine stickleback in fresh water offers a valuable opportunity to study how changes in environmental salinity shape physiological evolution in fish. In Alaska, the presence of both ancestral oceanic populations and derived landlocked populations, including recent lake introductions, allows us to examine rates and direction of evolution of osmoregulation following halohabitat transition. Hypotheses: Strong selection for enhanced freshwater tolerance will improve survival of recently lake-introduced stickleback in ion-poor conditions compared with their oceanic ancestors. Trade-offs between osmoregulation in fresh water and seawater will allow members of the ancestral population to survive better in response to seawater challenge, as mediated by upregulating salt-secreting transporters in the gill. Poorer hypo-osmoregulatory performance of derived fish will be marked by higher levels of taurine and other organic osmolytes. Methods: ...
Journal of Zoology, 2017
Three-spined sticklebacks (Gasterosteus aculeatus L.) of the Camargue region (Rhone delta, northern Mediterranean Sea) occupy coastal mesohaline lagoons and freshwater canals. In this study, the acclimation capacity to different salinities of a population living in freshwater canals was investigated. Freshwater (FW; 5 &) individuals were compared to fish acclimated for at least 2 weeks to brackish water (BW; 15 &) and seawater (SW; 30 &). Blood osmotic pressure and gill Na + /K +-ATPase (NKA) gene expression of the a1 subunit and a1a and a1b isoforms were determined at these salinities. NKA protein expression in the gill ionocytes and the remodelling of these cells were also investigated through NKA immunolabelling and electron microscopy. Blood osmolalities of fish acclimated to FW, BW and SW were significantly different. Branchial NKA a1a and a1b expressions also differed, with a higher expression of NKA a1b in fish acclimated to SW. Gill ionocytes in fish acclimated to FW were located along the lamellae and at their base and appeared elongated, whereas these cells were restricted to gill filaments in fish acclimated to SW with a round shape. Finally, electron microscopy revealed three different types of apical structures for these ionocytes: a honeycomb-like structure and a dome shape in FW, and deeply encrypted in SW. This study shows that ionocyte cell type and morphology, and gill NKA expression are salinity-dependent. This branchial remodelling is directly linked to the physiological homeostatic status reached by the fish. It also highlights that sticklebacks of the Camargue region can rapidly acclimate to different salinities and can easily migrate between FW canals and mesohaline coastal lagoons.
Mechanisms of seawater acclimation in a primitive, anadromous fish, the green sturgeon
Journal of Comparative Physiology B, 2009
Relatively little is known about salinity acclimation in the primitive groups of fishes. To test whether physiological preparative changes occur and to investigate the mechanisms of salinity acclimation, anadromous green sturgeon, Acipenser medirostris (Chondrostei) of three different ages (100, 170, and 533 dph) were acclimated for 7 weeks to three different salinities (\3, 10, and 33 ppt). Gill, kidney, pyloric caeca, and spiral intestine tissues were assayed for Na ? , K ? -ATPase activity; and gills were analyzed for mitochondria-rich cell (MRC) size, abundance, localization and Na ? , K ? -ATPase content. Kidneys were analyzed for Na ? , K ? -ATPase localization and the gastrointestinal tract (GIT) was assessed for changes in ion and base content. Na ? , K ? -ATPase activities increased in the gills and decreased in the kidneys with increasing salinity. Gill MRCs increased in size and decreased in relative abundance with fish size/age. Gill MRC Na ? , K ? -ATPase content (e.g., ion-pumping capacity) was proportional to MRC size, indicating greater abilities to regulate ions with size/age. Developmental/ontogenetic changes were seen in the rapid increases in gill MRC size and lamellar length between 100 and 170 dph. Na ? , K ? -ATPase activities increased fourfold in the pyloric caeca in 33 ppt, presumably due to increased salt and water absorption as indicated by GIT fluids, solids, and ion concentrations. In contrast to teleosts, a greater proportion of base (HCO 3 and 2CO 3 2-) was found in intestinal precipitates than fluids. Green sturgeon osmo-and ionoregulate with similar mechanisms to more-derived teleosts, indicating the importance of these mechanisms during the evolution of fishes, although salinity acclimation may be more dependent on body size.