Comprehensive Physiology Wiley Online Library

Variations in Salinity, Osmolarity, and Water Availability: Vertebrates and Invertebrates

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Extracellular Fluid
1.1 Extracellular Fluid as a Passive Osmotic Buffer
1.2 Extracellular Fluid as an Active Osmotic Buffer
2 Intracellular Fluid
2.1 Osmoregulation: Osmotic Effectors and Volume Control
2.2 Mechanisms of Cellular Volume Control
2.3 Osmoregulation: Osmotic Effectors and Activity of Macromolecules
3 Conclusion
4 Update
4.1 Note Added in Proof
Figure 1. Figure 1.

Evolution of blood osmolarity during acclimation of the euryhaline Chinese crab Eriocheir sinensis from seawater to fresh water.

Figure 2. Figure 2.

A: Evolution of volume and osmolarity of intracellular (C) and extracellular (B) spaces upon abrupt decrease in osmolarity of external medium (A) from π1 to π2, with π1 > π2. Explanations in text. B: Effect of osmotic shocks of different amplitudes (π12) on volume of a model cell system with different ratios of extracellular to intracellular H2 O. Explanations in text.

Figure 3. Figure 3.

Osmolarity and major osmotic effectors in blood and tissues of animals from marine, limnic, and terrestrial environments. In marine elasmobranchs and Latimeria sp., urea plays a major role among organic substances. **Urea may also become important in sarcopterygian fish, amphibians, and reptiles in different conditions of low water disponibility. *Amino acids are important blood osmotic effectors in different insect groups. Directly inspired by an original drawing of Fredericq (see also Fig. ). See text for details.

Figure 4. Figure 4.

Evolution of blood osmolarity as a function of external medium osmolarity in euryhaline aquatic species. Terrestrial species are not represented; their blood osmolarity may vary between 250 and 400 mOsm, depending on water availability. See text for details.

Figure 5. Figure 5.

Major routes of water (→) and ionic ( movements in animals. B.W., body walls; E.R.O., extrarenal organs of osmoregulation (gills, rectal gland, salt gland); G.I.T., gastrointestinal tract; R.O., renal organs; R.S., respiratory surfaces. Only net movements are considered. At the levels of body walls and respiratory surfaces, movements may go in or out, depending on the species and the medium. Details in Figure and in text.

Figure 6. Figure 6.

Major routes of water and ionic movements in aquatic and terrestrial (facing page) species. HBWP, high body wall permeability; LBWP, low body wall permeability. Note that in some terrestrial or semiterrestrial species, water can go in through the body walls (crustaceans, insects, amphibians). See text for details.

Figure 7. Figure 7.

Water flux in animals, modified from Nagy and Peterson .

Figure 8. Figure 8.

Evolution of body weight of the euryhaline mollusc Modiolus demissus granosissimus abruptly transferred at time 0, valves propped open, from seawater to media of different salinities.

Reproduced from Pierce , with permission
Figure 9. Figure 9.

Changes in glomerular filtration rate (GFR), urine flow, and drinking rate in euryhaline teleost fish acclimated to seawater (SW) or fresh water (FW). Details and references in text.

Figure 10. Figure 10.

Osmotic permeability in aquatic species from different media. Details and references in text.

Figure 11. Figure 11.

Mechanisms implicated in active transepithelial movements of NaCl in gills and salt glands. Black‐bordered systems are concerned with NaCl active extrusion, as in salt glands or gills of teleosts in seawater. They would be inactivated during NaCl active pumping, as in gills of teleosts and crustaceans hyperosmoregulating in diluted media. Cellular processes at the basolateral side would be common to the different structures and always active. See text for details.

Figure 12. Figure 12.

infrastructure of epithelial cells from a posterior, NaC1 transporting gill of the Chinese crab Eriocheir sinensis acclimated to seawater (A) or to fresh water (B). Note the important change in the organization of the apical infolding system, x 13,000. From Péqueux and Gilles, unpublished, refer to Péqueux and Gilles .

Figure 13. Figure 13.

Relative appearance rates of 24 Na+ (radioactivity) in teleosts transferred at time t from seawater (SW) to fresh water (FW).

Compiled from data of Motais et al. and Motais ; reproduced from Gilles , with permission
Figure 14. Figure 14.

22Na+ fluxes in isolated, perfused anterior gills of the euryhaline Chinese crab Eriocheir sinensis acclimated to fresh water. Results are mean values of n experiments ± SD. Modified after Péqueux and Gilles .

Figure 15. Figure 15.

22Na+ fluxes in gills (efflux in anterior, influx in posterior) isolated from Eriocheir sinensis acclimated to fresh water (FW) or seawater (SW) bathed (Na+ out) and perfused (Na+ in) in different conditions. After data of Péqueux and Gilles . See text for details.

Figure 16. Figure 16.

Transepithelial water movement against apparent osmotic gradient in intestine. Osmolarity values at the apical side and in the intercellular space are arbitrary and may vary depending on conditions. After data of Groot and Bakker .

Figure 17. Figure 17.

Relative rates of urea biosynthesis in three lungfish relative to water availability in the environment.

Reproduced from Goldstein , with permission. After data of Funkhouser et al.
Figure 18. Figure 18.

Evolution of water content of the leg muscle of the Chinese crab Eriocheir sinensis during acclimation from seawater to fresh water (○) and from fresh water to seawater (•). Osmolarities given in milliosmoles per kilogram. Modified from Gilles .

Figure 19. Figure 19.

Idealized evolution of the volume of cells submitted to hypo‐ or hyperosmotic shocks at the time marked by the first arrow. At the time marked by the second arrow, cells are replaced in their original medium. RVD, regulatory volume decrease; RVI, regulatory volume increase.

Figure 20. Figure 20.

Maximum volume achieved by PC12 cultured cells submitted to hypo‐ and hyperosmotic shocks of amplitude π12. After Delpire .

Figure 21. Figure 21.

Distribution of osmotic effectors (salts and organic substances) in seawater, blood, and tissues of invertebrates, elasmobranchs, and bony fish. Modified from Fredericq .

Figure 22. Figure 22.

Discrepancy between interstitial and intracellular electrolyte concentrations (calculated by the authors as twice the sum of sodium plus potassium concentration; dotted bars). The “osmotic gap” is filled by organic osmolytes (open bars). GPC, glyceroph‐osphorylcholine; TMA, other trimethylamines; Sorb, sorbitol; Inos, inositol. Modified from Beck et al. .

Figure 23. Figure 23.

Components and mechanisms that could a priori be concerned with cellular volume maintenance and regulation.

Reproduced from Gilles , with permission
Figure 24. Figure 24.

Mechanisms that could a priori be implicated in the control of the pool of inorganic and organic osmolytes during cellular osmoregulation. Modified from Gilles .

Figure 25. Figure 25.

Major mechanisms involved in regulatory volume decrease (RVD) and regulatory volume increase (RVI). Refer to text for details. *The Na+/K+ primary active pumping system is not directly involved in RVI; it replaces by K+ the Na+ taken up by the other mechanisms. **This electroneutral K+/H+ exchange functionally coupled to Cl/ exchange has been proposed only once, in the case of Amphiuma red blood cells.

Figure 26. Figure 26.

Model representing coregulation of Na+/H+ and K–Cl cotransport during volume changes. Model postulates a regulator in equilibrium between two states: a phosphorylated state (A), which turns K‐Cl off and Na+/H+ on, and a dephosphorylated state (B), which turns the K–Cl cotransporter on and the Na+/H+ antiporter off. Phosphorylation is; mediated by an unidentified kinase; dephosphorylation is mediated by phosphatase type I. Note that this model postulates an intermediate regulator; alternatively, the transport proteins themselves can be phosphorylated.

From reference , with permission
Figure 27. Figure 27.

Transamination–amination–deamination pathway controlling the free amino acid pool. (1) Glutamate dehydrogenase, (2) amino acid transaminases, (3) serine hydrolyase. +, 0, and — refer, respectively, to activating effect, no effect, and inhibiting effect of NaCl on enzyme activity. After Gilles .

Reproduced from Gilles , with permission
Figure 28. Figure 28.

Hypothetical analogy between heat shock response and osmotic shock response at genetic level. Based on the model of heat shock response (A), we propose that osmotic shock factors (OSF) are activated (that is, released from complex) during an osmotic perturbation and bind to osmotic shock elements (OSE) located upstream in the regulatory region of several genes, inducing activation of those genes. HSF, heat shock (transcription) factor; HSP, heat shock protein; HSE, heat shock element; OSP, hypothetical osmotic shock protein. Note that since some elements of the heat shock response are activated by osmotic shocks, the two models could be interrelated.

Figure 29. Figure 29.

Genetically controlled regulation of the level of an organic osmolyte in animal cells, a putative model. AE, ancillary element; APR, activating protein; ORE, osmotic response element; P, promoter. Derived from references 60b and 304a.



Figure 1.

Evolution of blood osmolarity during acclimation of the euryhaline Chinese crab Eriocheir sinensis from seawater to fresh water.



Figure 2.

A: Evolution of volume and osmolarity of intracellular (C) and extracellular (B) spaces upon abrupt decrease in osmolarity of external medium (A) from π1 to π2, with π1 > π2. Explanations in text. B: Effect of osmotic shocks of different amplitudes (π12) on volume of a model cell system with different ratios of extracellular to intracellular H2 O. Explanations in text.



Figure 3.

Osmolarity and major osmotic effectors in blood and tissues of animals from marine, limnic, and terrestrial environments. In marine elasmobranchs and Latimeria sp., urea plays a major role among organic substances. **Urea may also become important in sarcopterygian fish, amphibians, and reptiles in different conditions of low water disponibility. *Amino acids are important blood osmotic effectors in different insect groups. Directly inspired by an original drawing of Fredericq (see also Fig. ). See text for details.



Figure 4.

Evolution of blood osmolarity as a function of external medium osmolarity in euryhaline aquatic species. Terrestrial species are not represented; their blood osmolarity may vary between 250 and 400 mOsm, depending on water availability. See text for details.



Figure 5.

Major routes of water (→) and ionic ( movements in animals. B.W., body walls; E.R.O., extrarenal organs of osmoregulation (gills, rectal gland, salt gland); G.I.T., gastrointestinal tract; R.O., renal organs; R.S., respiratory surfaces. Only net movements are considered. At the levels of body walls and respiratory surfaces, movements may go in or out, depending on the species and the medium. Details in Figure and in text.



Figure 6.

Major routes of water and ionic movements in aquatic and terrestrial (facing page) species. HBWP, high body wall permeability; LBWP, low body wall permeability. Note that in some terrestrial or semiterrestrial species, water can go in through the body walls (crustaceans, insects, amphibians). See text for details.



Figure 7.

Water flux in animals, modified from Nagy and Peterson .



Figure 8.

Evolution of body weight of the euryhaline mollusc Modiolus demissus granosissimus abruptly transferred at time 0, valves propped open, from seawater to media of different salinities.

Reproduced from Pierce , with permission


Figure 9.

Changes in glomerular filtration rate (GFR), urine flow, and drinking rate in euryhaline teleost fish acclimated to seawater (SW) or fresh water (FW). Details and references in text.



Figure 10.

Osmotic permeability in aquatic species from different media. Details and references in text.



Figure 11.

Mechanisms implicated in active transepithelial movements of NaCl in gills and salt glands. Black‐bordered systems are concerned with NaCl active extrusion, as in salt glands or gills of teleosts in seawater. They would be inactivated during NaCl active pumping, as in gills of teleosts and crustaceans hyperosmoregulating in diluted media. Cellular processes at the basolateral side would be common to the different structures and always active. See text for details.



Figure 12.

infrastructure of epithelial cells from a posterior, NaC1 transporting gill of the Chinese crab Eriocheir sinensis acclimated to seawater (A) or to fresh water (B). Note the important change in the organization of the apical infolding system, x 13,000. From Péqueux and Gilles, unpublished, refer to Péqueux and Gilles .



Figure 13.

Relative appearance rates of 24 Na+ (radioactivity) in teleosts transferred at time t from seawater (SW) to fresh water (FW).

Compiled from data of Motais et al. and Motais ; reproduced from Gilles , with permission


Figure 14.

22Na+ fluxes in isolated, perfused anterior gills of the euryhaline Chinese crab Eriocheir sinensis acclimated to fresh water. Results are mean values of n experiments ± SD. Modified after Péqueux and Gilles .



Figure 15.

22Na+ fluxes in gills (efflux in anterior, influx in posterior) isolated from Eriocheir sinensis acclimated to fresh water (FW) or seawater (SW) bathed (Na+ out) and perfused (Na+ in) in different conditions. After data of Péqueux and Gilles . See text for details.



Figure 16.

Transepithelial water movement against apparent osmotic gradient in intestine. Osmolarity values at the apical side and in the intercellular space are arbitrary and may vary depending on conditions. After data of Groot and Bakker .



Figure 17.

Relative rates of urea biosynthesis in three lungfish relative to water availability in the environment.

Reproduced from Goldstein , with permission. After data of Funkhouser et al.


Figure 18.

Evolution of water content of the leg muscle of the Chinese crab Eriocheir sinensis during acclimation from seawater to fresh water (○) and from fresh water to seawater (•). Osmolarities given in milliosmoles per kilogram. Modified from Gilles .



Figure 19.

Idealized evolution of the volume of cells submitted to hypo‐ or hyperosmotic shocks at the time marked by the first arrow. At the time marked by the second arrow, cells are replaced in their original medium. RVD, regulatory volume decrease; RVI, regulatory volume increase.



Figure 20.

Maximum volume achieved by PC12 cultured cells submitted to hypo‐ and hyperosmotic shocks of amplitude π12. After Delpire .



Figure 21.

Distribution of osmotic effectors (salts and organic substances) in seawater, blood, and tissues of invertebrates, elasmobranchs, and bony fish. Modified from Fredericq .



Figure 22.

Discrepancy between interstitial and intracellular electrolyte concentrations (calculated by the authors as twice the sum of sodium plus potassium concentration; dotted bars). The “osmotic gap” is filled by organic osmolytes (open bars). GPC, glyceroph‐osphorylcholine; TMA, other trimethylamines; Sorb, sorbitol; Inos, inositol. Modified from Beck et al. .



Figure 23.

Components and mechanisms that could a priori be concerned with cellular volume maintenance and regulation.

Reproduced from Gilles , with permission


Figure 24.

Mechanisms that could a priori be implicated in the control of the pool of inorganic and organic osmolytes during cellular osmoregulation. Modified from Gilles .



Figure 25.

Major mechanisms involved in regulatory volume decrease (RVD) and regulatory volume increase (RVI). Refer to text for details. *The Na+/K+ primary active pumping system is not directly involved in RVI; it replaces by K+ the Na+ taken up by the other mechanisms. **This electroneutral K+/H+ exchange functionally coupled to Cl/ exchange has been proposed only once, in the case of Amphiuma red blood cells.



Figure 26.

Model representing coregulation of Na+/H+ and K–Cl cotransport during volume changes. Model postulates a regulator in equilibrium between two states: a phosphorylated state (A), which turns K‐Cl off and Na+/H+ on, and a dephosphorylated state (B), which turns the K–Cl cotransporter on and the Na+/H+ antiporter off. Phosphorylation is; mediated by an unidentified kinase; dephosphorylation is mediated by phosphatase type I. Note that this model postulates an intermediate regulator; alternatively, the transport proteins themselves can be phosphorylated.

From reference , with permission


Figure 27.

Transamination–amination–deamination pathway controlling the free amino acid pool. (1) Glutamate dehydrogenase, (2) amino acid transaminases, (3) serine hydrolyase. +, 0, and — refer, respectively, to activating effect, no effect, and inhibiting effect of NaCl on enzyme activity. After Gilles .

Reproduced from Gilles , with permission


Figure 28.

Hypothetical analogy between heat shock response and osmotic shock response at genetic level. Based on the model of heat shock response (A), we propose that osmotic shock factors (OSF) are activated (that is, released from complex) during an osmotic perturbation and bind to osmotic shock elements (OSE) located upstream in the regulatory region of several genes, inducing activation of those genes. HSF, heat shock (transcription) factor; HSP, heat shock protein; HSE, heat shock element; OSP, hypothetical osmotic shock protein. Note that since some elements of the heat shock response are activated by osmotic shocks, the two models could be interrelated.



Figure 29.

Genetically controlled regulation of the level of an organic osmolyte in animal cells, a putative model. AE, ancillary element; APR, activating protein; ORE, osmotic response element; P, promoter. Derived from references 60b and 304a.

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Raymond Gllles, Eric Delpire. Variations in Salinity, Osmolarity, and Water Availability: Vertebrates and Invertebrates. Compr Physiol 2011, Supplement 30: Handbook of Physiology, Comparative Physiology: 1523-1586. First published in print 1997. doi: 10.1002/cphy.cp130222