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McCormick S.D. (2011) The Hormonal Control of in Fish. In: Farrell A.P., (ed.), Encyclopedia of : From Genome to Environment, volume 2, pp. 1466–1473. San Diego: Academic Press.

ª 2011 Elsevier Inc. All rights reserved. Author's personal copy

HORMONAL CONTROLS

Hormonal Control of and Ionic Regulation

Contents The Hormonal Control of Osmoregulation in Teleost Fish

The Hormonal Control of Osmoregulation in Teleost Fish S D McCormick, USGS, Conte Anadromous Fish Research Center, Turners Falls, MA, USA

Published by Elsevier Inc.

Introduction: and Balance in Fish Cortisol The Special Case of Anadromy Summary Growth and IGF-I Further Reading

Glossary -like growth factor-I (IGF-I) A Adrenocorticotrophic hormone (ACTH) A protein hormone produced in the in response to growth hormone produced in the pituitary that causes release of hormone and acting on growth and ion regulation. cortisol from the interregnal. Na+,K+-ATPase (NKA, the sodium pump) Amajor Anadromy Life-history strategy entailing reproduction ATP-consuming ion pump that, directly or indirectly, drives and early rearing in freshwater followed by a significant many ion-regulatory processes, including maintaining growth phase in . sodium and ion gradients across cell plasma membranes The process of programmed cell death. and being present at high levels in ionocytes. Cortisol The major of , produced Na+,K+,2Cl� cotransporter (NKCC) An ion- in the interrenal and acting on metabolism and ion translocating that utilizes a sodium gradient to regulation. transport Na+,K+, and Cl� into the cell. Cystic fibrosis transmembrane conductance Prolactin A protein hormone produced in the pituitary regulator (CFTR) An apical chloride channel involved acting on ion balance and reproduction. in chloride secretion. Receptor A signal transduction molecule that is that physiologically adjust to a activated by a hormone. wide range of water are considered euryhaline Describes an that cannot live in (eury ‘broad’; haline ‘salt’), in contrast to stenohaline environments that undergo large changes in salinity animals. (steno ‘narrow’). Growth hormone (GH) A pituitary protein hormone Thyroid hormones Thyroxine and triiodothyronine, controlling growth, metabolism, and ion regulation. produced in the thyroid gland and acting on Hormone Signaling molecule released by a cell that development and metabolism. either stimulates the cell of origin (autocrine), nearby Transactivation Binding of a transcription factor, such cells (paracrine), or travels via the bloodstream to as a receptor–ligand complex, to DNA resulting in distant cells (endocrine). increased gene transcription.

1466 Encyclopedia of Fish Physiology: From Genome to Environment, 2011, Vol. 2, 1466-1473, DOI: 10.1016/B978-0-1237-4553-8.00212-4 Author's personal copy Hormonal Control of Metabolism and Ionic Regulation | Osmoregulation in Teleost Fish 1467

Introduction: Salt and As outlined above, the are the primary site of in Fish sodium and chloride transport, actively taking up in freshwater and excreting them in seawater. Most of Whether in freshwater or seawater, teleost fish maintain the recent work on the endocrine control of ion transport their plasma at about one-third that in fish has focused on the , so this review will necessa­ of seawater (see also Osmotic, Ionic and Nitrogenous- rily be biased in this direction. It has been known for some Waste Balance: Osmoregulation in : An time that the mitochondrion-rich cell (also known as Introduction). In freshwater, this requires counteracting the chloride cell) is the site of salt secretion (see also the passive gain of water and loss of ions, and is accom- Role of the Gills: of Branchial Ionocytes plished through the production of large volumes of dilute and Osmotic, Ionic and Nitrogenous-Waste Balance: and active uptake of ions across the gills. In seawater, Mechanisms of Gill Salt Secretion in Marine Teleosts). teleosts must counteract the passive gain of ions and loss of There is substantial evidence indicating that the major water. This is accomplished by drinking seawater, absorb- transporters involved in salt secretion in the gill include ing water and salts across the gut, and excreting basolaterally located Na+,K+-ATPase (NKA, the sodium monovalent ions across the gills and divalent ions through pump) and Na+,K+,2Cl� cotransporter (NKCC), and an the . It has been estimated that 95% of teleost apical Cl� channel that is homologous with the cystic are stenohaline, living wholly in either freshwater fibrosis transmembrane conductance regulator (CFTR) or seawater. The remaining 5% are euryhaline, having the (Figure 1). capacity to tolerate a wide range of . This trait is The site and mechanisms involved in ion uptake by the widespread among teleost lineages and has apparently gill in freshwater are less certain. Both mitochondrion - rich evolved many times, and may be one reason that teleosts cells and pavement cells may be involved in sodium and can be found in almost all aquatic habitats. chloride uptake (see also Osmotic, Ionic and

Growth hormone/IGF-I Prolactin

Cortisol Cortisol

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+ + K + + + K + K K K K + K − Cl + − Na Cl + + + − + Na + Na Na + Cl Na + + Na Na + Na Na Na

Seawater Freshwater (ion secretion) (ion uptake) Figure 1 Morphology, transport mechanisms, and hormonal control of gill chloride cells in freshwater and seawater. Chloride cells are characterized by numerous mitochondria and an extensive tubular system that is continuous with the basolateral membrane. In seawater, mitochondrion-rich cells are generally larger and contain a deep apical crypt, whereas in freshwater, there is a broad apical surface containing numerous microvilli. Growth hormone and cortisol can individually promote the differentiation of the seawater chloride cell, and also interact positively to control epithelial transport capacity. Prolactin inhibits the formation of seawater chloride cells and promotes the development of freshwater chloride cells. Cortisol also promotes acclimation to freshwater by maintaining ion transporters and chloride cells, and by interacting to some degree with prolactin PVC, pavement cell. Reproduced from McCormick SD (2001) Endocrine control of osmoregulation in teleost fish. American Zoologist 41: 781–794. Author's personal copy 1468 Hormonal Control of Metabolism and Ionic Regulation | Osmoregulation in Teleost Fish

Nitrogenous-Waste Balance:MechanismsofIon in vitro. Cortisol has also been shown to increase the Transport in Freshwater Fishes). Chloride is exchanged transcription and abundance of the major transport pro­ � for HCO3 at the apical surface and at the basolateral teins involved in salt secretion by the gill: NKA, NKCC, membrane moving downhill on an electrical gradient (the and CFTR. The effect of exogenous cortisol generally chloride cell being more negative than the ). Sodium requires several days to reach its peak, suggesting that cell may enter the gill epithelia by exchange with H+,or proliferation and differentiation are required for its com­ throughanapicalNa+ channel coupled to an apical H+­ plete action. In the intestine, exogenous cortisol ATPase, and pass into the bloodstream at the basolateral gill stimulates NKA activity, together with ion and water surface through NKA. Recent work suggests that in some absorption, thus improving acclimation to high environ­ species there is also a Na+/Cl� co-transporter on the apical mental salinity. An increased drinking response after surface that is involved in ion uptake. More direct evidence transfer to seawater has been observed in salmonids trea­ is needed to be certain of the roles and location of these ted with cortisol. transporters involved in ionuptakeinteleosts. Changes in circulating cortisol in response to There are three primary lines of evidence for the increased environmental salinity are reported for many involvement of hormones in ion regulation. The first teleost species. The clearance rate (the inverse of the involves the treatment of animals (in vivo) or isolated amount of time a compound remains in circulation) of tissues (in vitro) with hormones and examining ion reg­ cortisol also increases in seawater, suggesting increased ulatory performance and/or the response of ion transport utilization by osmoregulatory target tissues (see also and cells. The second line of evidence comes Integrated Control and Response of the Circulatory from changes in circulating hormones when environmen­ System: Hormone Metabolism in the Circulation). The tal salinity is changed, such as a transfer from freshwater release of cortisol from the interrenal is primarily con­ to seawater. Third, the presence and regulation of specific trolled by the pituitary hormone adrenocorticotrophic hormone receptors in the organs and cell types responsi­ hormone (ACTH), though other endocrine factors may ble for ion regulation is taken as evidence for the also be involved (see also Hormonal Responses to involvement of that hormone in salt and water balance. Stress: Hormone Response to Stress). Although there is This article illustrates that there are many common evidence for activation of pituitary ACTH cells, salinity features to the endocrine control of osmoregulation in effects on circulating levels of ACTH have not been teleost fish. It should be noted, however, that only a detected. ACTH production by the isolated pituitary small number of teleosts have been examined and that does not appear to be directly responsive to changes in we know little or nothing about the hormonal control of external osmolality. The increase in cortisol during osmo­ osmoregulation in the vast majority of fish. Given the tic stress occurs in both stenohaline and euryhaline fishes great diversity among teleosts and the differing acclima­ and may be part of a general stress response. Thus, the tion responses and strategies that have evolved, it should presence and regulation of cortisol receptors is also a not be surprising to find that not all teleost fishes conform critical component of osmoregulation in these fishes. to a single scheme. Indeed, one of our outstanding The classical signaling action of steroids begins by research challenges is to determine how the hormonal transport into the cell, followed by binding to a cytosolic control of osmoregulation differs among teleosts, and to receptor, which is then translocated into the nucleus. what extent it has been shaped by natural selection. There, the steroid binds to specific genes to increase or decrease their expression. A large number of binding studies in fish have found evidence for a single of Cortisol corticosteroid receptors (CRs). These receptors are pre­ sent in high concentrations in the gill, gut, and kidney, Cortisol and Seawater Acclimation and their abundance is often altered by environmental Cortisol is the major corticosteroid produced by the salinity. During exposure to increased salinity, intracel­ interrenal tissue of teleost fish (see also Hormonal lular cortisol and CR levels in the gill shift from the Control of Metabolism and Ionic Regulation: to the nucleus, indicative of CR binding and Corticosteroids). This hormone has several established translocation. High concentrations of CR have been physiological roles in osmoregulation, intermediary found in the gill mitochondrion-rich cells. metabolism, growth, stress, and immune function. It has In the past several years, molecular techniques have been shown for many species of euryhaline fish that demonstrated the presence of genes in several teleost treatment with cortisol in freshwater improves their sub­ species related to the mammalian glucocorticoid recep­ sequent survival and capacity to maintain low levels of tors (GRs) and mineralocorticoid receptors (MRs). Two plasma ions after exposure to seawater. This effect is due isoforms of fish GR genes have been found in several to increases in the size and abundance of gill mitochon­ teleost species, and these have different activation affi­ drion-rich cells, which has been demonstrated in vivo and nities for cortisol. In addition, an MR-like gene has been Author's personal copy Hormonal Control of Metabolism and Ionic Regulation | Osmoregulation in Teleost Fish 1469 characterized in rainbow ( mykiss) and sodium pump is indeed integral to ion uptake, then the the (Haplochromis burtoni). When the effect of cortisol on gill NKA could be one mechanism by MR gene is expressed in a mammalian cell line, it was which cortisol exerts a dual osmoregulatory function. In found to have high transactivation efficiency for both addition, cortisol also likely promotes the development of and 11-deoxycorticosterone (DOC), similar the freshwater morphology of chloride cells. Recent to the binding characteristics of the mammalian MR. It evidence indicates that in salmonids there are two has been suggested that DOC, present in the plasma of salinity-dependent isoforms of gill NKA: one that is some teleosts at levels that could activate the fish MR, more abundant in freshwater and the other more abun­ might be a mineralocorticoid in fish. Injection studies dant in seawater. Cortisol upregulates both of these indicate, however, that DOC cannot carry out the ­ isoforms, which is further evidence for a dual osmoregu­ water-adapting functions of cortisol. Thus, the latory role for this hormone. physiological function of DOC and MR in fish remains to be established. Prolactin Cortisol and Freshwater Acclimation By removing the pituitary (hypophysectomy) and then As noted above, cortisol has largely been identified as a replacing the lost PRL with injections, Grace Pickford seawater-adapting hormone in a large number of teleost conclusively demonstrated 50 years ago that the pituitary species. There is an increasing body of evidence demon­ hormone PRL was critical for the maintenance of ion strating that cortisol is also involved in ion uptake, thus balance of teleost fish in freshwater. Since then, evidence giving it a dual osmoregulatory function. Cortisol treat­ for PRL as an important freshwater-adapting hormone in ment in increases the surface area of gill fish comes from studies on exogenous PRL treatment, mitochondrion-rich cells and the influx of sodium and changes in PRL gene expression and circulating levels chloride, affecting both renal and branchial functions. in response to salinity change, and the localization and Survival and plasma ion levels of freshwater fish that regulation of PRL receptors. have had their pituitary removed are increased by treat­ Although PRL has been shown to have sodium- and ment with adrenocoritcotrophic hormone (ACTH), which chloride-retaining activity in a variety of freshwater and can be presumed to be acting through its stimulation of euryhaline teleosts, there is surprisingly little information cortisol release from the interrenal. Cortisol is also required on the cellular and biochemical effectors of the osmore­ to maintain water movement across the gut of freshwater gulatory actions of PRL. Throughout , a large . Cortisol treatment significantly increases the ion reg­ proportion of the various actions of PRL seem to be ulatory capacity of marine fish during exposure to low associated directly or indirectly with cell proliferation salinity and the ability of acid-resistant fish to maintain and/or apoptosis. PRL has been shown to affect chloride plasma sodium levels after exposure to acidic water. cells, both by inhibiting the development of seawater Changes in circulating levels of cortisol also provide chloride cells and promoting the morphology of ion supporting evidence for a role of this hormone in ion uptake cells. PRL treatment also reduces ion and water uptake. Transfer of euryhaline species from seawater to permeability of the and intestine, a response freshwater results in short-term increases in plasma cor­ that normally occurs during acclimation to freshwater. tisol. Transfer of several species of marine fish from high PRL can induce intestinal cell proliferation in some to low salinity results in increased circulating cortisol that euryhaline fishes. It has recently been shown that the remains elevated for days to weeks. In Mozambique tila­ abundance of NaCl co-transporter present on the apical pia (Oreochromis mossambicus), transfer from freshwater to surface of ion uptake cells in the gill decreases distilled water or injection of prolactin (PRL) results in following hypophysectomy and is restored to original elevated plasma cortisol. These studies on increasing abundance with PRL treatment. cortisol levels in response to decreases in salinity, along Gene expression, synthesis, secretion, and plasma levels with the cortisol treatment studies described above, pro­ of PRL all increase following exposure to freshwater. vide evidence that, in many teleosts, cortisol has a Metabolic clearance rate of PRL increases following fresh physiological role in promoting ion uptake. This function water acclimation of salmonids. In some teleosts such as of cortisol has not been fully appreciated due to an tilapia, and cortisol exert direct regula­ emphasis on the role of cortisol in salt secretion. tory actions on PRL secretion. As in , however, a Although there is substantial evidence indicating that specific hypothalamic PRL-releasing factor, PRL-releasing cortisol can increase gill and gut NKA, it is unclear peptide (PrRP), has recently been identified in teleosts. whether this is primarily related to cortisol’s seawater- PrRP promotes PRL transcription and secretion, with the adaptive effects, or whether upregulation of the sodium histochemical localization of PrRP neuronal terminals near pump is also involved in ion uptake. If maintenance of the PRL cells in the pituitary. Moreover, PrRP seems to be an Author's personal copy 1470 Hormonal Control of Metabolism and Ionic Regulation | Osmoregulation in Teleost Fish essential stimulator of PRL since antiserum to PrRP tissue, and a direct action of IGF-I. Levels of IGF-I decreases circulating PRL levels. In the amphibious eur­ mRNA in gill and kidney increase following GH injection yhaline (Periophthalmus modestus), the - and exposure to seawater, indicating that local production pituitary axis of PrRP-PRL operates during both terrestrial of IGF-I may act in a paracrine fashion to influence and freshwater acclimation. transport capacity of gill and renal epithelia. PRL receptor transcription and abundance are high in In addition to the effects of exogenous hormones, osmoregulatory organs such as the gill, intestine, and changes in gene expression, secretion, circulating levels, kidney. In the gill, the transcription and abundance of and metabolic clearance rate of growth hormone and PRL receptor are lower in seawater than in freshwater IGF-I also provide evidence for the osmoregulatory in tilapia and salmonids. High levels of PRL receptor actions of the GH/IGF-I axis in several euryhaline transcription have been found in mitochondrion-rich species. Plasma GH levels have also been found to cells of the gill and enterocytes of the intestine. increase in stenohaline freshwater fish following expo­ There is evidence that both PRL and cortisol are neces­ sure to (e.g., 12 ppt). Following exposure sary for normal ion regulation in freshwater. The two may of rainbow trout to seawater, there are increases in even interact to control ion uptake. In hypophysectomized plasma levels of IGF-I and three of its binding proteins. (Heteropneustes fossilis), PRL and cortisol together IGF-I mRNA levels in liver, gill, and kidney increase cause a greater elevation of plasma ions than either hor­ following growth hormone injection and exposure to mone alone. Also, cortisol and PRL together have a greater seawater, indicating that local production of IGF-I effect than either hormone alone in promoting the transe­ may also act to influence transport capacity of gill pithelial resistance and potential of an in vitro gill-cell and renal epithelia. IGF-I has been found specifically preparation. In hypophysectomized and/or interrenalecto­ in gill chloride cells whose number and/or size are mized fish, both PRL and/or ACTH or cortisol are stimulated by growth hormone. necessary to completely restore ion and water balance in Growth hormone receptors in high concentrations freshwater. Although an interaction between PRL and have been found in the liver, gill, gut, and kidney of cortisol in controlling freshwater acclimation has been euryhaline teleost fish. Occupancy of hepatic growth proposed, there is as yet little direct evidence for this hormone receptors by growth hormone increased follow­ hypothesis and no mechanism has been proposed. ing exposure to seawater. Growth hormone transcription has also been detected in osmoregulatory organs and may be acting in an autocrine or paracrine manner in these Growth Hormone and IGF-I tissues. Growth hormone receptor mRNA levels in the gill increase after seawater acclimation of salmonids. In the 1950s, D.C.W. Smith observed that multiple Specific high-affinity, low-capacity IGF-I receptors injections of growth hormone could increase the capacity have been found in gill tissue of and tilapia, and of to tolerate exposure to seawater. At first, have been immunocytochemically localized to gill chlor­ this was attributed to the growth effect of the hormone cells in (Morone saxatilis) and tilapia. because size confers greater salinity tolerance in salmo­ Few teleost species have been examined for the nids. Several decades later, it was found that a single physiological impact of the GH/IGF-I axis on osmoregu­ injection of growth hormone in unfed fish was sufficient lation. Exogenous treatments have been found to affect to increase salinity tolerance, indicating a relatively rapid salmonids, tilapia, and . Changes in circulating hor­ effect that was independent of body size. Growth hor­ mones and production of IGF-I in osmo-regulatory organs mone has since been shown to increase the number and in salmonids provide convincing evidence for both endo­ size of gill mitochondrion-rich cells as well as the abun­ crine and paracrine actions of the GH/IGF-I axis, but dance of NKA and NKCC (see also Cellular, there is relatively little information in this area from Molecular, Genomics, and Biomedical Approaches: other teleosts. There is no apparent osmoregulatory role Growth Hormone Overexpression in Transgenic Fish). for GH in sea bream, a marine species with a limited A major route of the osmoregulatory action of GH is capacity for hyperosmoregulation. Species variation linked through its capacity to increase circulating levels and to different ion regulatory capacities and/or strategies for local tissue production of insulin-like growth factor-I ion regulation may determine to what extent the GH/ (IGF-I). Exogenous treatment of IGF-I has been found IGF-I axis is involved in osmoregulation. A similar situa­ to increase the salinity tolerance of rainbow trout, tion may occur for PRL: there may be limited (Salmo salar), and killifish (Fundulus hetero­ osmoregulatory effects of PRL in stenohaline marine tele­ clitus). GH cannot directly (in culture) increase gill NKA osts where any ion uptake may be maladaptive. Expanded activity, whereas IGF-I can. The ability of prior GH research on both euryhaline and stenohaline species will be treatment to increase in vitro responsiveness of gill tissue necessary to determine how widespread the osmoregula­ to IGF-I further suggests an indirect action of GH on gill tory actions of PRL and the GH/IGF-I axis are among Author's personal copy Hormonal Control of Metabolism and Ionic Regulation | Osmoregulation in Teleost Fish 1471 teleosts, and how phyletic histories and natural selection action of GH on gill NKA activity in salmon. Inhibiting have acted to bring about any observed patterns. the conversion of T4 to T3 interferes with normal and GH-induced seawater acclimation in trout. T3 treatment increases the number of gill cortisol receptors in trout and Interaction of the GH/IGF-I Axis with Cortisol salmon. Thyroid hormones thus appear to exert their The GH/IGF-I and cortisol axes work together to reg­ influence on salt secretory mechanisms primarily through ulate salt secretion in teleosts. Injection of GH and an interaction with cortisol and the GH/IGF-I axis. cortisol together increases gill NKA activity and salinity tolerance in salmonids and killifish to a greater extent than either hormone alone. This effect can be seen in both The Special Case of Anadromy hypophysectomized and intact fish. Cortisol treatment of freshwater Atlantic salmon causes an increase in both the As part of their normal life history, anadromous fish (such freshwater and seawater isoforms of NKA, but treatment as salmon) must move between freshwater and seawater at with GH and cortisol causes the seawater isoform to least twice during their life history (see also Fish increase to an even greater extent, and the freshwater Migrations: Pacific Salmon Migration: Completing the isoform to decrease. Much of the interaction of GH and Cycle). As juveniles in freshwater, salmon have only a cortisol is through GH’s capacity to upregulate the num­ limited capacity to enter seawater. At the time of their ber of gill cortisol receptors, which makes the tissue more downstream migration (when they are known as smolts), responsive to cortisol. juvenile salmon develop a very high capacity for salt Growth hormone increases mitotic activity in several secretion before they actually arrive in the . The cell types in the gill of rainbow trout. Cortisol has no effect timing of this developmental process differs among sal­ on mitotic activity but increases the number of chloride monids, but is accompanied by changes in the gill cells, suggesting that cortisol acts primarily to promote (increased mitochondrion-rich cells, NKA, and NKCC), differentiation of chloride cells. Therefore, another path­ gut, and kidney. way for GH/IGF-I and cortisol interaction is stimulation During smolt development, GH, IGF-I, and cortisol of stem cell proliferation by GH and/or IGF-I, creating increase in response to developmental and/or environ­ more stem cells that can then be acted on by cortisol. The mental cues such as photoperiod and GH/IGF-I axis and cortisol may also interact at higher (Figure 2). PRL can inhibit smolt development, and regulatory pathways, such as the and pitui­ increases early during smolt development, but then tary. In vivo and in vitro exposure to GH increases the decreases at the peak of smolting. Thyroid hormones sensitivity of interrenal tissue to ACTH, causing increased also increase during smolting and are thought to play an release of cortisol. Corticotropin-releasing hormone is a indirect role in osmoregulatory changes, but a direct role potent stimulator of in vitro growth hormone release in in morphological, metabolic, and behavioral changes. the European (Anguilla anguilla). Thus, the same hormones that are altered by exposure to salinity in other species increase prior to seawater exposure in salmon, inducing preparatory changes in salt secretory mechanisms that allow rapid movement Thyroid Hormones into seawater with minimal osmotic perturbations. The developmental changes that occur during smolt­ Although there is conflicting evidence regarding the role ing in salmon appear to be similar to other species, such as of thyroid hormones in osmoregulation, most studies have and shad that make just one or a few migrations found that thyroid hormones, by themselves, cannot from freshwater to seawater. Species that make more increase ion uptake or secretory capacity. Exceptions to frequent migrations between freshwater and seawater this are prolonged thyroxine (T4) treatment that acceler­ may rely more on rapid regulation ion uptake or salt ated smolt-related increases in gill mitochondrion-rich secretion rather than developmentally cued regulation. cells and NKA activity in Atlantic salmon, and dietary triiodothyronine (T3) treatment that increased the num­ ber of gill mitochondrion-rich cells without affecting gill Summary NKA activity. Thyroid hormones play at least a suppor­ tive role in seawater acclimation, and may interact with Cortisol has long been known to have an important role both the GH/IGF-I and cortisol axes. Inhibition of the in seawater acclimation of teleost fishes. Current thyroid axis with thioruea in killifish caused increased evidence indicates that the GH/IGF-I axis also has a plasma ions in seawater but had no effect in freshwater. role in seawater acclimation, and that GH, IGF-I, and T4 treatment alone has no effect, but potentiates the cortisol interact positively to promote salt secretion and action of cortisol on gill NKA activity in tilapia, and the the underlying physiological mechanisms. PRL has a Author's personal copy 1472 Hormonal Control of Metabolism and Ionic Regulation | Osmoregulation in Teleost Fish

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4 Growth hormone Cortisol

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0 310 JAN FEB MAR APR MAY JUN Figure 2 Changes in plasma hormone levels, gill NKA activity, and salinity tolerance during the parr–smolt transformation of Atlantic salmon. Interaction among cortisol, growth hormone, IGF-I, and thyroid hormones results in physiological changes that are preparatory for seawater entry. Adapted from McCormick SD, Lerner DT, Monette MY, Nieves–Puigdoller K, and Bjo¨ rnsson BTh (2009) Taking it with you when you go: How perturbations to the freshwater environment, including temperature, dams and contaminants, affects seawater performance of anadromous fish. In: Haro AJ, Smith KL, Rulifson RA, et al. (eds.) Challenges For Diadromous Fishes in a Dynamic Global Environment. American Society Symposium, vol. 69, pp. 195–214. Bethesda, MD, USA. well-established role in ion uptake and inhibition of salt Stress: Hormone Response to Stress. Integrated secretion. In addition to its role in seawater acclimation, Control and Response of the : several studies indicate that cortisol is also involved in Hormone Metabolism in the Circulation. Osmotic, Ionic ion uptake and can interact positively with PRL, indi­ and Nitrogenous-Waste Balance: Mechanisms of Gill cating that cortisol has a dual osmoregulatory function in Salt Secretion in Marine Teleosts; Mechanisms of Ion teleosts. The action of cortisol in promoting ion uptake Transport in Freshwater Fishes; Osmoregulation in or secretion may therefore depend partly on its interac­ Fishes: An Introduction. Role of the Gills: Morphology of tion with growth hormone and PRL: when growth Branchial Ionocytes. hormone is high and PRL is low, cortisol may act pri­ marily to promote salt secretion. Conversely, when growth hormone is low and PRL is elevated, cortisol Further Reading will act to promote ion uptake. Evans DH, Piermarini PM, and Choe KP (2005) The multifunctional : Dominant site of gas exchange, osmoregulation, acid–base See also: Cellular, Molecular, Genomics, and regulation, and of nitrogenous waste. Physiological Reviews 85: 97–177. Biomedical Approaches: Growth Hormone Hoar WS (1988) The Physiology of Smolting Salmonids. In: Hoar WS Overexpression in Transgenic Fish. Fish Migrations: and Randall D (eds.) Fish Physiology, vol. XIB pp. 275–343. New Pacific Salmon Migration: Completing the Cycle. York: Academic Press. Marshall WS (2002) Na+,Cl�,Ca2+ and Zn2+ transport by fish gills: Hormonal Control of Metabolism and Ionic Retrospective review and prospective synthesis. Journal of Regulation: Corticosteroids. Hormonal Responses to Experimental Zoology 293: 264–283. Author's personal copy Hormonal Control of Metabolism and Ionic Regulation | Osmoregulation in Teleost Fish 1473

McCormick SD (2001) Endocrine control of osmoregulation in teleost anadromous fish. In: Haro AJ, Smith KL, Rulifson RA, et al. (eds.) fish. American Zoologist 41: 781–794. Challenges For Diadromous Fishes in a Dynamic Global Environment McCormick SD (2009) of the hormonal control of American Fisheries Society Symposium, vol. 69 pp. 195–214. performance: Insights from the seaward migration of salmon. Bethesda, MD, USA. Integrative and Comparative 46: 408–422. Sakamoto T and McCormick SD (2006) Role of prolactin and growth McCormick SD, Lerner DT, Monette MY, Nieves–Puigdoller K, and hormone in osmoregulation of teleost fish. General and Comparative Bjo¨ rnsson BTh (2009) Taking it with you when you go: How Endocrinology 147: 24–30. perturbations to the freshwater environment, including temperature, Takei Y and Loretz CW (2006) Endocrinology. In: The Physiology of dams and contaminants, affects seawater performance of Fishes, 3rd edn., pp. 271–318. Boca Raton, FL: CRC Press.