52, No. Recent evidence indicates that individual chloride cells of tilapia in fresh water (that are presumably involved in ion uptake) can rapidly develop the morphology characteristic of seawater chloride cells (Hiroi et al., 1999), suggesting that chloride cells are ‘bifunctional;’ that is, capable of rapidly changing from an ion uptake to an ion secretion mode. Address for reprint requests and other correspondence: D. H. Evans, Dept. Hormonal Control of Metabolism and Ionic Regulation|Osmoregulation in Teleost Fish 1469 characterized in rainbow trout (Oncorhynchus mykiss) and the cichlid (Haplochromis burtoni). Given the great diversity among teleosts and the differing acclimation responses and strategies that have evolved, it should not be surprising to find that not all teleost fishes will conform to a single scheme. Obviously, the emerging “knockdown” techniques (siRNA, morpholinos, etc.) Laurent et al. In superb videomicroscopic studies (130, 135), it was demonstrated that the increase in gill resistance in the gill is secondary to the contraction of pillar cells, which separate the two surfaces of the gill lamellae and produce sheet flow of blood through the gill, which maximizes gas exchange (see Ref. Drakenberg, K., V. R. Sara, S. Falkmer, S. Gammeltoft, C. Maake, and M. Reinecke. Salmo salar, The European flounder spends most of its life in the sea but often migrates into estuaries and rivers. 4, Copyright © 2020 the American Physiological Society, August Krogh Distinguished Lectureship of the APS Comparative and Evolutionary Physiology Section, 2008, American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, https://doi.org/10.1152/ajpregu.90337.2008, This is the final version - click for previous version, http://www.the-aps.org/membership/obituaries/ancel_keys.htm, Exposure to colistin impairs skin keratinocytes and lateral-line hair cells in zebrafish embryos, Comparative transcriptome profiling of selected osmotic regulatory proteins in the gill during seawater acclimation of chum salmon (Oncorhynchus keta) fry, Genome-wide analysis of MicroRNA-messenger RNA interactome in ex-vivo gill filaments, Anguilla japonica, Intestinal response to ocean acidification in the European sea bass (Dicentrarchus labrax), Genomic landscape of reproductive isolation in Indeed, Potts's book with Gwyneth Parry (117) started many of us in this subdiscipline. (1987) found that a single injection of GH in rainbow trout (Oncorhynchus mykiss) followed two days later by exposure to seawater resulted in increased salinity tolerance. (124), modern IHC techniques have localized the Na, K, 2Cl cotransporter (sensitive to furosemide; actually NKCC1) to the basolateral regions of the MRC in the fish gill (e.g., 104, 138) and, as one might expect, the expression of the transporter declines as the salinity is lowered. Geven and Gert Flik 3. Meaning of Osmoregulation:. B. Collette, and D. E. Facey. Knoeppel, S. J., D. L. Atkins, and R. K. Packer. 121). Desert Island Biological Laboratory—still a world-class center for marine physiology and functional genomics. On the other hand, a pendrin-like anion exchanger (Cl−/HCO3−; SLC26) has been immunolocalized in the stingray to cells in the gill that contain basolateral V-type H+-ATPase, distinct from Na+-K+-activated ATPase-expressing cells (9, 112). 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. 1, 11 December 2019 | Communications Biology, Vol. Rankin, J. C., D. K. O. Chan, and I. Chester Jones. This is a key component of their osmoregulatory strategy presenting the challenge of excreting excess salts while achieving a net retention of water. Chloride is exchanged for HCO3− at the apical surface and leaves at the basolateral membrane moving ‘downhill’ on an electrical gradient (the chloride cell being more negative than the blood). Peter, M. S., R. C. Lock, and S. W. Bonga. Marine teleost’s face the opposite problem from that of freshwater teleost’s. 1, No. Rousseau, K., B. N. Le, J. Marchelidon, and S. Dufour. Conversely, low growth hormone and high prolactin will cause cortisol to promote ion uptake. Recent evidence suggests that H+-ATPase and the apical sodium channel are located on the apical surface of pavement cells in Mozambique tilapia (Oreochromis mossambicus), but in both pavement cells and chloride cells in the rainbow trout (Oncorhynchus mykiss) (Hiroi et al., 1998; Wilson et al., 2000). Madsen, S. S., M. K. Jensen, J. Nohr, and K. Kristiansen. 1, 13 July 2011 | Environmental Biology of Fishes, Vol. 10, 16 February 2012 | Water, Air, & Soil Pollution, Vol. Evidence collected in the last 15 yr indicates that the growth hormone/insulin-like growth factor I (GH/IGF-I) axis is also important in the seawater acclimation process of teleosts. 15, 15 August 2018 | Royal Society Open Science, Vol. (1972). 37.]. Trombetti, F., V. Ventrella, A. Pagliarani, R. Ballestrazzi, M. Galeotti, G. Trigari, M. Pirini, and A. R. Borgatti. Recent evidence indicates that the growth hormone/insulin-like growth factor I axis is also important in seawater adaptation in several teleosts of widely differing evolutionary lineages. 27 and 91), suggesting that alternative Na+ pathways might be discovered in some species in the future. Examination of the mechanisms of action of GH and IGF-I to promote salinity tolerance indicates that the gill is an important target tissue. N2 - This chapter focuses on intestinal water absorption that is ultimately linked to salt absorption. (1991b) found that IGF-I increased salinity tolerance in rainbow trout, and this effect was later confirmed in other salmonids (McCormick, 1996; Seidelin et al., 1999). Burgess, D. W., W. S. Marshall, and C. M. Wood. In freshwater, teleost fish gain water across their gills by osmosis, while in seawater they lose it. 318, No. Fish - Fish - Excretory organs: The primary excretory organ in fishes, as in other vertebrates, is the kidney. 2, 22 November 2018 | Conservation Physiology, Vol. B—Biochemistry & Molecular Biology, Comp. (1987), McCormick et al. ACTH increased plasma sodium levels in intact (but not in hypophysectomized) Fundulus kansae in fresh water (Stanley and Fleming, 1967). 1, 26 December 2018 | Revista de la Academia Colombiana de Ciencias Exactas, Físicas y Naturales, Vol. Stanford Libraries' official online search tool for books, media, journals, databases, government documents and more. 10Keys left fish physiology a few years later but went on to a very distinguished career in nutrition, including the formulation of “K rations” during World War II and the first discussion of the link between cardiovascular disease and dietary lipid intake. The gastrointestinal tract was recognized early to play a vital role in marine teleost osmoregulation by absorbing water. Most important, he measured Cl− uptake from a variety of Cl salt solutions (e.g., NaCl, KCl, NH4Cl, and CaCl2) and found that the cation made no difference, indicating that Cl− uptake was independent of Na+ uptake. These potentially disruptive osmotic and ionic movements are compensated for by excretion of relatively large volumes of a dilute urine, and active uptake of NaCl across the gill epithelium. Evidence for the importance of the GH/IGF-I axis in seawater acclimation comes primarily from studies on exogenous hormone treatment, changes in circulating levels, metabolic clearance rate, localization of receptors and production of IGF-I by osmoregulatory tissues (Sakamoto et al., 1993; Mancera and McCormick, 1998a). The European flounder spends most of its life in the sea but often migrates into estuaries and rivers. + Teleost fish osmoregulation: what have we learned since August Krogh, Homer Smith, and Ancel Keys. 4, Brazilian Journal of Biology, Vol. Prunet, P., M. Pisam, J. P. Claireaux, G. Boeuf, and A. Rambourg. Cortisol is also apparently acting to promote the development of the ‘freshwater’ morphology of chloride cells (Perry et al., 1992). In other species (e.g., salmonids), cortisol may have the capacity to simultaneously increase both ion uptake and secretory capacity by increasing the number of chloride cells. 310, No. 3, 1 April 2011 | American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, Vol. 1.Mechanisms of osmoregulation by teleost fishes. Rousseau et al. Thus, it certainly can be said that the basic model for teleost osmoregulation was formulated and published in the 1930s, due to the work of Krogh, Smith, and Keys . It furthers the University's objective of excellence in research, scholarship, and education by publishing worldwide, This PDF is available to Subscribers Only. Bjornsson, and S. Moriyama, unpublished results). In the killifish, endothelin can be localized to lamellar pillar cells and to epithelial cells in the filament that are not the MRC (59). Water absorption occurs as a consequence of Na + and Cl - transport, despite high luminal concentrations of divalent ions and alkaline conditions. Although these represent a small number of the euryhaline species, they are widely separated in the evolution of teleosts, suggesting that the osmoregulatory action of GH and IGF-I may also be widespread among teleosts. 119. Marine teleost fish osmoregulation involves seawater ingestion and intestinal fluid absorption. 318, No. Thus, ironically, it appeared that the “chloride cells” were aptly named by Keys 40 years previously. Edwards has since demonstrated NHE2 immunoreactivity in the killifish gill (20), and the mRNA for that protein is upregulated after acclimation to fresh water (123). }, author={D. H. Evans}, journal={American journal of physiology. 10, 21 June 2019 | Fish Physiology and Biochemistry, Vol. In vivo and in vitro exposure to GH increases the sensitivity of interrenal tissue to ACTH (adrenocorticotrophic hormone) in coho salmon, causing increased release of cortisol (Young, 1988). In Vitro Fish Osmoregulation book 308, 12 March 2020 | Fish Physiology and Biochemistry, Vol. Oncorhynchus masou, The Amphibious Mudskipper: A Unique Model Bridging the Gap of Central Actions of Osmoregulatory Hormones Between Terrestrial and Aquatic Vertebrates, Arsenic Reduces Gene Expression Response to Changing Salinity in Killifish, Influence of environmental salinity and cortisol pretreatment on gill Na+/K+ −ATPase activity and survival and growth rates in Cyprinus carpio, The shark-tuna dichotomy: why tuna lay tiny eggs but sharks produce large offspring, Intestinal FXYD12 and sodium-potassium ATPase: A comparative study on two euryhaline medakas in response to salinity changes, Osmoregulation in the Plotosidae Catfish: Role of the Salt Secreting Dendritic Organ, Salinity reduction benefits European eel larvae: Insights at the morphological and molecular level, Changes to Extender, Cryoprotective Medium, and Laurent, P., S. Dunelerb, C. Chevalier, and J. Lignon. Experiments on Gulf toadfish Opsanus beta demonstrate how feeding impacts osmoregulation in the marine teleost intestine. 3, Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, Vol. Osmoregulation: movement of water and ions in saltwater (marine) fish. Our preliminary studies have confirmed the increase in gill resistance (46) in the longhorn sculpin, and we extended the isolated vascular ring studies to ventral aortic tissue from the elasmobranch spiny dogfish (32), the teleost eel, and two agnathan fishes, the hagfish and marine lamprey (35), so it appears that the vasoconstrictive effects of endothelin are present throughout the vertebrates. 1, 25 September 2015 | Scientific Reports, Vol. Shrimpton, J. M., N. J. Bernier, and D. J. Randall. 36, No. See text for details. Therefore they are always losing water. 220, No. Keys found that the presence of the heart was critical to the hemodynamic success of the preparation, and he suggested that “the perfusion medium derives a hormone, or hormones, from the heart, which acts to preserve capillary tone.” This proposition that the heart might produce a vasoactive substance predates DeBold's discovery of atrial natriuretic peptides by 50 years (15). 1, 18 December 2011 | Journal of Comparative Physiology B, Vol. Physiol, The Society for Integrative and Comparative Biology, Introduction to the Symposium: New Frontiers in Antarctic Marine Biology, Epigenetics of Animal Personality: DNA Methylation Cannot Explain the Heritability of Exploratory Behavior in a Songbird, Comparative study of snake lateral undulation kinematics in model heterogeneous terrain, Molecular Plasticity in Animal Pigmentation: Emerging Processes Underlying Color Changes, Theory, hormones and life history stages: an introduction to the symposium epigenetic variation in endocrine systems, About Integrative and Comparative Biology, About the Society for Integrative and Comparative Biology, THE ROLE OF THE GH/IGF-I AXIS IN ACCLIMATION TO SEAWATER, INTERACTION OF THE GH/IGF-I AXIS WITH CORTISOL. Teleost fish genomes display remarkable features, possibly linked to the impressive biodiversity observed in these animals. Cortisol has been viewed as ‘the’ seawater-adapting hormone in fish and prolactin as ‘the’ fresh water adapting hormone. Thus, in a single publication, Smith proposed the basic outline of marine teleost fish osmoregulation: ingestion of seawater, retrieval of NaCl (and some Mg 2+ and ) and water from the intestine, followed by excretion of the divalents via the urine, and the monovalents across the gills. This represents an unusual regulatory system, since in mammals increased calcium is often associated with increased chloride fluxes, and use of calcium as an intracellular messenger is usually associated with α1 (and not α2) receptors. 3, 2 February 2011 | Acta Physiologica, Vol. The results of studies on catecholamine control of ion uptake are contradictory: studies using the isolated head found that catecholamines stimulate sodium and chloride influx, whereas in vivo approaches found inhibition of ion influx (Mayer-Gostan et al., 1987). The site and mechanims involved in ion uptake in fresh water are less certain. ), Sticklebacks adapted to divergent osmotic environments show differences in plasticity for kidney morphology and candidate gene expression, Di- and tripeptide transport in vertebrates: the contribution of teleost fish models, RNA-Seq analysis of salinity stress–responsive transcriptome in the liver of spotted sea bass (Lateolabrax maculatus), Intestinal response to salinity challenge in the Senegalese sole (Solea senegalensis), Transcriptomic imprints of adaptation to fresh water: parallel evolution of osmoregulatory gene expression in the Alewife, Adaptive genomic divergence under high gene flow between freshwater and brackish-water ecotypes of prickly sculpin ( With the exception of the sodium pump and the apical chloride channel, the sequence and physical structure of transporters involved in ion transport in fish have not been characterized (see Evans et al., 1999). 2001; 41:781–794. Maetz found that the measured K+ influx was identical to the Na+ efflux from the flounder, and that the latter was proportional to the external K+ concentration (85). Thus, it certainly can be said that the basic model for teleost osmoregulation was formulated and published in the 1930s, due to the work of Krogh, Smith, and Keys (Fig. During the same time period, Silva et al. Coregonus lavaretus 4, 1 April 2009 | American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, Vol. Fuentes and Eddy (1997) found that GH treatment increased drinking rate after exposure of Atlantic salmon to seawater, suggesting that GH may affect gut function. 166, No. 50, No. Since the late 1960s, laboratories in the United States and Europe (and more recently, Asia) have produced a substantial body of literature on the mechanisms of fish osmoregulation that were first described by Krogh, Smith, and Keys. Thus, there is still a limited picture of the hormones involved, and examination of other lines of evidence such as changes in local or circulating levels and receptors is needed to establish a more complete picture of the rapid regulation of ion uptake and secretion. 331, No. Seriola lalandi The cells that secrete acid via an apical V-type H+-ATPase, and Na+ via an apical channel may be equivalent to a subpopulation of mitochondrion-rich cell (MRC) from the trout gill (isolated by Percoll gradient) that does not bind to peanut lectin agglutinin (PNA-negative) (43, 47, 109). On the basis of published values for teleost plasma ionic concentrations (reviewed in Refs. He was tragically killed in an automobile accident in 1977. 467, No. The fact that known inhibitors of proton transport (e.g., vanadate or decreased external pH) inhibited H+ extrusion by the trout gill (79) supported the hypothesis of the active, apical proton pump that Avella and Borancin (2) had proposed. 8Cl– was chosen because of the relative ease (compared to Na+) of chemical determination. 185, No. 2). The evidence for an apical anion exchanger is somewhat less conflicting, although relatively scant. The definitive proof that the “chloride cell” was the site of the Cl− extrusion came five years later, when Kevin Foskett showed clear Cl− currents when a microprobe was placed over “chloride cells” in the opercular skin of tilapia, which also has high concentrations of these cells (41). ), Ontogenetic changes in cutaneous and branchial ionocytes and morphology in yellowfin tuna (Thunnus albacares) larvae, Type II Na+-phosphate Cotransporters and Phosphate Balance in Teleost Fish, Emersion and Terrestrial Locomotion of the Northern Snakehead (Channa argus) on Multiple Substrates, Morfología externa del pez parásito Paravandellia phaneronema (Miles 1943) (Siluriformes: Trichomycteridae) observada mediante imágenes de microscopía electrónico de barrido, Benzocaine-induced stress in the euryhaline teleost, Centropomus parallelus and its implications for anesthesia protocols. Endocrine control of osmoregulation in teleost fish. To get around this problem, marine fish drink large quantities of water and restrict urination. 81, No. 9, No. 61 Citations (Scopus) Abstract. 11The grant was funded, for the then grand amount of $50,000 for two years. Ancel Keys was Krogh's postdoctoral student in Copenhagen during the early 1930s and also worked at the Physiological Laboratory in Cambridge, UK, during the same period. Sakamoto and Hirano (1991) found that the occupancy of hepatic, but not branchial and renal, growth hormone receptors increased following exposure to seawater. Angiotensin II has been shown to rapidly increase gill Na+, K+ATPase activity in fresh water and seawater adapted eel (Marsigliante et al., 1979). To some degree with prolactin during acclimation to fresh water adapting hormone J. Nohr, and P..... Furimsky M, Thomas SLY extract NaCl from the National Science Foundation since 1970 ; most recently, 's... & Integrative Physiology, Vol and D. J. Randall freshwater and marine intestine... 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Search tool for books, media, journals, databases, government documents and more Research found growth! And Comparative Physiology B, Vol is continuous with the basolateral membrane occurs a. Salinity acclimation may be one reason that teleosts can be found in his famous “ fish! N. Mayer-Gostan, and A. Rambourg ( external salinity, blood osmolarity, osmolarity. Systems of fish Biology and Fisheries, Vol Donaldson, and AncelKeys, so they face osmotic loss water... Compared to Na+ ) of chemical determination may 2016 | teleost fish osmoregulation of Physiology-Regulatory, Integrative and Comparative B. December 2018 | Frontiers in Genetics, Vol to Mark Mandica for his excellent drawing of chloride secretion in is. The size and salinity tolerance in many salmonid species ( e.g., 84.! Intended to be localized to these same cells ( 58 ), suggesting that alternative Na+ pathways be... Probably in exchange for HCO3− official online search tool for books,,! Will discuss our recent data on endothelin, 4 April 2012 | Journal of Zoology... 27 may 2020 | functional Ecology, Vol 24 October 2018 | Journal of Toxicology and environmental Health Part! A similar capacity to interact one reason that teleosts can be found in almost all aquatic habitats that. Nitrogenous waste in the seawater chloride cells similarly, salts diffuse outwards across the marine teleost ’ drink..., in general, with frequent divergent Evolution in the fishes one third of that of seawater chloride cell and... Tetsuya Hirano increased both the size and salinity tolerance of chum salmon fry of. Cl− concentration88Cl– was chosen because of the seawater chloride cells D. K. O. I.! Experimental Neuroscience, Vol Boeuf, and R. J. Balment flux of Na+ November 2018 | Frontiers in Endocrinology Vol! Stenohaline, living wholly in either fresh water adapting hormone 1960s and 1970s (,! Science Foundation since 1970 ; most recently: IOB-0519579 rather complex working model Na+... ” were aptly named by Keys 40 years previously an increasing body of evidence, however, that cortisol promoting! C. Fenwick to its watery home of Na+-K+-activated ATPase-containing cells in seawater they lose it July... Of goldfish ( Chow, 1997 ) frog skin was published four years later ( 56 ) prolactin antagonistic. }, journal= { American Journal of Physiology, P. M. Piermarini, and T. Hirano suggested that uptake. Signaling in the range 10−12−10−11 M ( 1–100 pg/ml ) in expression in seawater-acclimated eels ( )... At least some of the seawater gill are relatively well accepted physiologic strategies for osmoregulation of that of the.! As ionic regulation ( 14 ) live in freshwater, teleost fish relative... Abstract as the primary link between environmental change and physiological response, the neuroendocrinesystem is a critical Part of adaptations. J. Marchelidon, and S. Moriyama, unpublished results ), 16 2016!