Ontogeny of osmoregulation in postembryonic fish: a review

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(-1) 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 inter-related 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.     

Metamorphosis and early larval development of the flatfishes (Pleuronectiformes): an osmoregulatory perspective

Flatfish (Pleuronectiformes) distribution in the environment is influenced by salinity, and varies among species and with developmental stage. Osmoregulatory ability likely plays an important role in defining species and developmental stage-specific distribution. Although the mechanisms of osmoregulation in adult and juvenile teleosts have been widely addressed, far less is known about their larval osmoregulatory physiology. Much of our current understanding of larval fish ion-regulation stems from studies using flatfishes, and this article reviews advances in this field, primarily from the point of view of the developing flatfishes. Addressed here are the ontogeny of salinity tolerance, the development of several important osmoregulatory tissues (the skin, gut, and gill), and the influence of the endocrine system on osmoregulation during early larval development and metamorphosis.     

Evolution of osmoregulatory patterns and gill ion transport mechanisms in the decapod Crustacea: a review

Decapod crustaceans exhibit a wide range of osmoregulatory patterns and capabilities from marine osmoconformers to brackish and freshwater hyperregulators to terrestrial hyporegulators. The principal gill salt transport mechanisms proposed to underlie the ability of the better-known taxa to occupy these specific habitats are examined here. Traditional thinking suggests that a graduated series of successively stronger adaptive mechanisms may have driven the occupation of ever more dilute osmotic niches, culminating in the conquest of freshwater and dry land. However, when habitat and osmoregulatory parameters are analyzed quantitatively against the phylogenies of the taxa examined, as illustrated here using a palaemonid shrimp clade, their association becomes questionable and may hold true only in specific cases. We also propose a putative evolution for gill epithelial ion pump and transporter arrangement in a eubrachyuran crab clade whose lineages occupy distinct osmotic niches. By including the systematics of these selected groups, this review incorporates the notion of a protracted time scale, here termed ??phylophysiology??, into decapod osmoregulation, allowing the examination of putative physiological transformations and their underlying evolutionary processes. This approach assumes that species are temporally linked, a factor that can impart phylogenetic structuring, which must be considered in comparative studies. Future experimental models in decapod osmoregulatory physiology should contemplate the phylogenetic relationships among the taxa chosen to better allow comprehension of the transformations arising during their evolution.     

Effect of salinity on flavin-containing monooxygenase expression and activity in rainbow trout (Oncorhynchus mykiss)

In order to obtain more information about the physiological role(s) of flavin-containing monooxygenases (FMOs) in euryhaline teleost fishes, two experimental series were performed using adult and juvenile rainbow trout (Oncorhynchus mykiss). Cannulated adult trout were exposed to freshwater or 21% seawater for 48 h, whereas juvenile trout were acclimated to one of four different salinities: freshwater, 7%, 14%, or 21% during a 2-week period. FMO expression and activity were determined in red blood cells (RBC), liver, gill, kidney, gut, heart and brain. Furthermore, the content of trimethylamine oxide (TMAO; an FMO metabolite and an osmolyte) as well as urea were determined in various tissues. FMO expression and activity increased significantly and in a salinity dependent manner in osmoregulatory organs (gills, kidney and gut) in both juveniles and adult trout and, furthermore, in RBC in adults. No significant changes were observed in liver or heart. Urea content increased significantly and in a salinity dependent manner in all tissues, whereas TMAO was accumulated primarily in muscle tissue. Salinity dependent adjustment of FMO expression and activity primarily in osmoregulatory organs as well as regulation of TMAO content in muscle is consistent with previous studies showing an association of FMO with osmoregulation in euryhaline teleosts. However, the lack of a parallel increase of TMAO with urea in other tissues of fish at high salinity indicates other mechanisms of protection from intracellular urea may exist in non-muscular tissues.     

A structure-function analysis of ion transport in crustacean gills and excretory organs

Osmotic and ionic regulation in the Crustacea is mostly accomplished by the multifunctional gills, together with the excretory organs. In addition to their role in gas exchange, the gills constitute organs of active, transepithelial, ion transport, an activity of major importance that underlies many essential physiological functions like osmoregulation, calcium homeostasis, ammonium excretion and extracellular pH regulation. This review focuses on structure-function relationships in crustacean gills and excretory effectors, from the organ to molecular levels of organization. We address the diversity of structural architectures encountered in different crustacean gill types, and in constituent cell types, before examining the physiological mechanisms of Na(+), Cl(-), Ca(2+) and NH(4)(+) transport, and of acid-base equivalents, based on findings obtained over the last two decades employing advanced techniques. The antennal and maxillary glands constitute the principal crustacean excretory organs, which have received less attention in functional studies. We examine the diversity present in antennal and maxillary gland architecture, highlighting the structural similarities between both organ types, and we analyze the functions ascribed to each glandular segment. Emphasis is given to volume and osmoregulatory functions, capacity to produce dilute urine in freshwater crustaceans, and the effect of acclimation salinity on urine volume and composition. The microanatomy and diversity of function ascribed to gills and excretory organs are appraised from an evolutionary perspective, and suggestions made as to future avenues of investigation that may elucidate evolutionary and adaptive trends underpinning the invasion and exploitation of novel habitats.     

Neurohormonal Integration of Osmotic and Ionic Regulation

There is evidence in crustaceans that neuroendocrine centers,including the eyestalk, brain, thoracic ganglionic mass, andpericardial organ, produce factors that affect osmotic and ionicregulation. Understanding of the processes responsible for osmoticadjustment in the intact animal, such as regulation of permeability,active uptake of ions, and respiratory and cardiovascular alterations,has increased substantially in the past few years. However,interaction of neuroendocrine factors with the target tissuesand systems is just beginning to be investigated. There is evidencethat content of lipids and activity of enzymes are importantin osmoregulation, and neuroendocrine effects on these metabolicprocesses are worthy of study. In addition, there are some crustaceansin which osmoregulatory ability varies developmentally. Furtherinvestigations of such animals is also necessary. Progress inour understanding of neuroendocrine influences on osmoregulationdepends upon further purification of active factors from neuroendocrinecenters and hemolymph, and upon development of appropriate assayson which to test them.     

Cellular osmoregulation: beyond ion transport and cell volume

All cells are characterized by the expression of osmoregulatory mechanisms, although the degree of this expression is highly variable in different cell types even within a single organism. Cellular osmoregulatory mechanisms constitute a conserved set of adaptations that offset antagonistic effects of altered extracellular osmolality/environmental salinity on cell integrity and function. Cellular osmoregulation includes the regulation of cell volume and ion transport but it does not stop there. We know that organic osmolyte concentration, protein structure, cell turnover, and other cellular parameters are osmoregulated as well. In this brief review two important aspects of cellular osmoregulation are emphasized: 1) maintenance of genomic integrity, and 2) the central role of protein phosphorylation. Novel insight into these two aspects of cellular osmoregulation is illustrated based on two cell models, mammalian kidney inner medullary cells and teleost gill epithelial cells. Both cell types are highly hypertonicity stress-resistant and, therefore, well suited for the investigation of osmoregulatory mechanisms. Damage to the genome is discussed as a newly discovered aspect of hypertonic threat to cells and recent insights on how mammalian kidney cells deal with such threat are presented. Furthermore, the importance of protein phosphorylation as a core mechanism of osmosensory signal transduction is emphasized. In this regard, the potential roles of the 14-3-3 family of phospho-protein adaptor molecules for cellular osmoregulation are highlighted primarily based on work with fish gill epithelial cells. These examples were chosen for the reader to appreciate the numerous and highly specific interactions between stressor-specific and non-specific pathways that form an extensive cellular signaling network giving rise to adaptive compensation of hypertonicity. Furthermore, the example of 14-3-3 proteins illustrates that a single protein may participate in several pathways that are non-specific with regard to the type of stress and, at the same time, in stress-specific pathways to promote cell integrity and function during hypertonicity.     

Influence of salinity and cadmium on the survival and osmoregulation of Callianassa kraussi and Chiromantes eulimene (Crustacea: Decapoda)

This study investigated the influence of salinity and cadmium on the survival and osmoregulatory capability of two decapod crustaceans, Callianassa kraussi and Chiromantes eulimene. Callianassa kraussi was able to survive in salinities of 5–55 over 96 h, whilst C. eulimene survived in 0–55 over the same time period. The 96-hour cadmium LC₅₀ for both species decreased progressively at salinities above and below their respective isosmotic conditions, with the decrease being slightly more pronounced below compared to above isosmotic salinity. A hypo-iso-osmoregulatory strategy was followed by C. kraussi as it hyper-osmoregulated at salinities between 5 and 25 and osmoconformed at salinities greater than 25. Chiromantes eulimene followed a hyper-hypo-osmoregulatory strategy; it hyper-regulated in salinities from 0 up to isosmotic conditions at about 28 (c. 780 mOsm kg^?1), followed by hypo-regulation up to 55. The effect of cadmium exposure on the osmoregulatory capacity of C. kraussi was more pronounced at hyper-regulating salinities (5–25) whilst on C. eulimene the influence was more pronounced at salinities above the isosmotic point (28). The influence of salinity and cadmium on both survival and osmoregulation of the two crustaceans are discussed by outlining the chemical and physiological mechanisms involved.     

Altered expression of Na+/K+–ATPase and other osmoregulatory genes in the gills of euryhaline animals in response to salinity transfer: A meta-analysis of 59 quantitative PCR studies over 10 years

Recent advances in molecular techniques have allowed gene expression in euryhaline animals to be quantified during salinity transfers. As these investigations transition from studying single genes to utilizing genomics-based methodologies, it is an appropriate time to summarize single gene studies. Therefore, a meta-analysis was performed on 59 published studies that used quantitative polymerase chain reaction (qPCR) to examine expression of osmoregulatory genes (the Na⁺/K⁺–ATPase, NKA; the Na⁺/K⁺/2Cl^? cotransporter, NKCC; carbonic anhydrase, CA; the cystic fibrosis transmembrane regulator, CFTR; and the H⁺–ATPase, HAT) in response to salinity transfer. Based on 887 calculated effect sizes, NKA, NKCC, CA, and HAT are up-regulated after salinity transfer, while surprisingly, CFTR is unchanged. Meta-analysis also identified influential factors contributing to these changes. For example, expression was highest: 1) during transfers from higher to lower salinities comprising a physiological transition from osmoconformity to osmoregulation, 2) 1–3 days following transfer, 3) during dissimilar transfers, and 4) in crustaceans rather than teleosts. Methodological characteristics (e.g., types of controls) were not important. Experiments lacking in the current literature were also identified. Meta-analyses are powerful tools for quantitatively synthesizing a large body of literature, and this report serves as a template for their application in other areas of comparative physiology.     

Selected aspects of microbial osmoregulation

Abstract Some salient characteristics of microbial osmoregulation are reviewed, with specific examples drawn from eukaryotes. As well as the need for an osmoregulatory solute to be 'compatible' with cellular processes under all conditions, the importance of the physiological method of regulating the content of the solute as a factor determining xerotolerance is emphasized. The significance of turgor/volume homeostasis is discussed and examples are cited in which, during exponential growth, there is apparently no homeostatic control of the cellular content of the major osmoregulatory solute. Some implications of this for the overall mechanism of osmoregulation are considered.
A recent experiment is described which raises questions about the timing of an osmoregulatory 'signal' in Saccharomyces cerevisiae . Other experiments are summarized which distinguish between osmoregulatory and compatible solutes in yeast. These experiments implicate trehalose as a non-osmoregulatory compatible solute in certain circumstances.     

Salinity tolerance and morphology of the osmoregulation organs in Cladocera with special reference to Cladocera from the Aral sea

The hyperosmotic regulation of adult Cladocera is determined mainly by the amount of salts consumed with the food and by reabsorption of salts in cells of the nuchal (neck) organ. The hypoosmotic regulation both in adults and embryos is determined mainly by excretion of salts in special epipodite cells or in cells of the nuchal (neck) organ. The salinity of the Aral sea for the last 30 years increased from 8–10 to 26–28, which led to changes in the Cladocera fauna. At present only 4 species of Cladocera inhabit the Aral sea instead of 14 species that were previously found. These changes are in agreement with osmoregulation capacities of Cladocera. Note added in proof. Since this paper was accepted for publication, all Cladocera have disappeared from the Aral Sea. This happened when salinity reached 30–32. This disappearance was predicted by and agrees with earlier laboratory experiments with Aral Sea Cladocera (Aladin, 1982b).     

Physiological basis of interactive responses to temperature and salinity in coastal marine invertebrate: Implications for responses to warming

Developing physiological mechanistic models to predict species’ responses to climate‐driven environmental variables remains a key endeavor in ecology. Such approaches are challenging, because they require linking physiological processes with fitness and contraction or expansion in species’ distributions. We explore those links for coastal marine species, occurring in regions of freshwater influence (ROFIs) and exposed to changes in temperature and salinity. First, we evaluated the effect of temperature on hemolymph osmolality and on the expression of genes relevant for osmoregulation in larvae of the shore crab Carcinus maenas. We then discuss and develop a hypothetical model linking osmoregulation, fitness, and species expansion/contraction toward or away from ROFIs. In C. maenas, high temperature led to a threefold increase in the capacity to osmoregulate in the first and last larval stages (i.e., those more likely to experience low salinities). This result matched the known pattern of survival for larval stages where the negative effect of low salinity on survival is mitigated at high temperatures (abbreviated as TMLS). Because gene expression levels did not change at low salinity nor at high temperatures, we hypothesize that the increase in osmoregulatory capacity (OC) at high temperature should involve post‐translational processes. Further analysis of data suggested that TMLS occurs in C. maenas larvae due to the combination of increased osmoregulation (a physiological mechanism) and a reduced developmental period (a phenological mechanisms) when exposed to high temperatures. Based on information from the literature, we propose a model for C. maenas and other coastal species showing the contribution of osmoregulation and phenological mechanisms toward changes in range distribution under coastal warming. In species where the OC increases with temperature (e.g., C. maenas larvae), osmoregulation should contribute toward expansion if temperature increases; by contrast in those species where osmoregulation is weaker at high temperature, the contribution should be toward range contraction.     

A laboratory-based comparison of osmoregulatory ability at different water temperatures and salinities in the stenothermic isopod Saduria entomon (Linnaeus, 1758) and the eurythermic amphipod Corophium volutator (Pallas, 1766) from the Baltic Sea

The aim of the investigation was a comparison of osmoregulatory ability at different water temperatures and salinities by the stenothermic isopod Saduria entomon (Linnaeus, 1758) and the eurythermic amphipod Corophium volutator (Pallas, 1766) from the Baltic Sea. The experiments were performed under laboratory conditions at different water temperatures (5, 10 and 15?°C) and salinities (3, 6.6, 15 and 25 PSU for S. entomon and 3, 6.3, 15 and 25 PSU for C. volutator). The osmotic concentrations of the crustaceans’ haemolymph were determined using the melting point method. Temperature had a statistically significant effect on the osmoregulation in S. entomon, but had generally no statistical influence on the osmoregulation in C. volutator. This physiological information regarding adaptation provides a basis for predicting the distribution of these species in changing environments. The implications of the results for the comparative adaptability of the two species are considered.     

Prolactin osmoregulatory function in fishes and its projection on mammals

Prolactin evolution and key role in fish osmoregulation were reviewed. Comparison of fish and mammalian prolactin was made in respect of its structure, producing tissues, regulation of pituitary secretion. Peculiarities of prolactin receptor structure and prolactin-induced signal cascades, tissue distribution and regulation of prolactin receptor expression were compared in fishes and mammals. Data on mechanisms of prolactin action on ionoconservation in teleost fishes at the level of gills, kidney, intestine, and skin were presented. The facts of prolactin participation in the regulation of water and salt balance in mammals were observed. The existence of fundamentally similar mechanisms of osmoregulatory prolactin action in fishes and mammals was accumed and algorithm of their investigation was suggested.     

Biochemical and physiological adaptations in the estuarine crab Neohelice granulata during salinity acclimation

Neohelice granulata (Chasmagnathus granulatus) is an intertidal crab species living in salt marshes from estuaries and lagoons along the Atlantic coast of South America. It is a key species in these environments because it is responsible for energy transfer from producers to consumers. In order to deal with the extremely marked environmental salinity changes occurring in salt marshes, N. granulata shows important and interesting structural, biochemical, and physiological adaptations at the gills level. These adaptations characterize this crab as a euryhaline species, tolerating environmental salinities ranging from very diluted media to concentrated seawater. These characteristics had led to its use as an animal model to study estuarine adaptations in crustaceans. Therefore, the present review focuses on the influence of environmental salinity on N. granulata responses at the ecological, organismic and molecular levels. Aspects covered include salinity tolerance, osmo- and ionoregulatory patterns, morphological and structural adaptations at the gills, and mechanisms of ion transport and their regulation at the gills level during environmental salinity acclimation. Finally, this review compiles information on the effects of some environmental pollutants on iono- and osmoregulatory adaptations showed by N. granulata.     

Age-specific features in renal response to food intakes and training loads in young professional skiers

The age-specific features of renal functions have been studied in older adolescents and young adults training in ski racing before and after their water and food intake and training loads. Baseline renal functions in the morning demonstrated higher glomerular filtration rate (GFR) and more mature development of the osmoregulatory mechanisms (higher excretion of osmotically active substances, osmotic concentration index, and reabsorption of solute-free liquid) in young adults, compared with adolescents. After food intake, the osmoregulatory mechanisms provided in young adults an adequate renal response—increased excretion of ions in exchange for urea, which preserves osmolality. At the same time, increased excretion of osmotically active substances synchronously with growth in the rate of urine output, higher GFR and reabsorption of solute-free liquid was marked in adolescents, which points to less mature development of the osmoregulatory system. The similar trend of renal homeostatic responses after physical training indicated the activation of volume regulatory mechanisms which did not differ between age groups. Our conclusion is that the definitive volume regulation develops ahead of osmoregulation.     

Some insights into energy metabolism for osmoregulation in fish

A sufficient and timely energy supply is a prerequisite for the operation of iono- and osmoregulatory mechanisms in fish. Measurements of whole-fish or isolated-gill (or other organs) oxygen consumption have demonstrated regulation of the energy supply during acclimation to different osmotic environments, and such regulation is dependent on species, the situation of acclimation or acclimatization, and life habits. Carbohydrate metabolism appears to play a major role in the energy supply for iono- and osmoregulation, and the liver is the major source supplying carbohydrate metabolites to osmoregulatory organs. Compared with carbohydrates, the roles of lipids and proteins remain largely unclear. Energy metabolite translocation was recently found to occur between fish gill ionocytes and neighboring glycogen-rich (GR) cells, indicating the physiological significance of a local energy supply for gill ion regulatory mechanisms. Spatial and temporal relationships between the liver and other osmoregulatory and non-osmoregulatory organs in partitioning the energy supply for ion regulatory mechanisms during salinity challenges were also proposed. A novel glucose transporter was found to specifically be expressed and function in gill ionocytes, providing the first cue for investigating energy translocation among gill cells. Advanced molecular physiological approaches can be used to examine energy metabolism relevant to a particular cell type (e.g., gill ionocytes), and functional genomics may also provide another powerful approach to explore new metabolic pathways related to fish ion regulation.     

Osmoregulation in Elasmobranchs

Osmoregulatory mechanisms were examined in major groups of fishesincluding hagfish, holocephalans, elasmobranchs, the coelacanth,and ray-fin fishes. Four main patterns of body fluid compositionemerged. These represent the three main osmoregulatory processesin the marine environment and the one in fresh water. Some possibleinterrelationships among these four types are discussed. Urearetention in marine elasmobranchs and the coelacanth, althoughsimilar, may have been acquired independently during evolution.The importance of gills and the rectal gland in elasmobranchosmoregulation is discussed. The importance of amino acids inintracellular osmoregulation in elasmobranchs is also reviewed.Recent studies on water and electrolyte regulation in freshwaterstingrays are summarized.     

Energetics of osmoregulation: II. Water flux and osmoregulatory work in the euryhaline fish, Fundulus heteroclitus

Teleost fish experience passive osmotic water influx in fresh water (FW) and water outflux in salt water, which is normally compensated by water flow driven by active ion transport mechanisms. Euryhaline fish may also minimize osmotic energy demand by "behavioral osmoregulation", seeking a medium isotonic with their body fluids. Our goal was to evaluate the energy requirement for osmoregulation by the euryhaline fish Fundulus heteroclitus, to determine whether it is of sufficient magnitude to favor behavioral osmoregulation. We have developed a method of weighing small fish repetitively for long periods without apparent damage, which was used to assess changes in water content following changes in external salinity. We found that cold (4 degrees C) inhibits osmoregulatory active transport mechanisms in fish acclimated to warmer temperatures, leading to a net passive water flux which is reversed by rewarming the fish. A sudden change of salinity at room temperature triggers a transient change in water content and the initial slope can be used to measure the minimum passive flux at that temperature. With some reasonable assumptions as to the stoichiometry of the ion transport and ATP-generating processes, we can calculate the amount of respiration required for ion transport and compare it to the oxygen uptake measured previously under the same conditions. We conclude that osmoregulation in sea water requires from 6% to 10% of the total energy budget in sea water, with smaller percentages in FW, and that this fraction is probably sufficient to be a significant selective driving force favoring behavioral osmoregulation under some circumstances.