Physiology of salinity tolerance in Tilapia : an update of basic and applied aspects

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Physiology of salinity tolerance in Tilapia : an update of

basic and applied aspects

Patrick Prunet, Michel Bornancin

To cite this version:

Patrick Prunet, Michel Bornancin. Physiology of salinity tolerance in Tilapia : an update of basic and applied aspects. Aquatic Living Resources, EDP Sciences, 1989, 2, pp.91-97. �10.1051/alr:1989011�. �hal-02728039�

Aquat. Licing Resour., 1989, 2.91-97

Physiology of salinity tolerance in tilapia

:

an update of basic and applied aspects

Patrick Prunet

(''

and Michel Bornancin"'

(" IJtfRA, Laboratoire de l'hysiologie des I'oissonr, Campus de Beaulieu, % o p Rennes cedex, Franse.

(') UnicersitC de Aïce, Iaboratoire de Physiologie cel~ulaire et romparte,

FacuW des Sciences et des Techniques, parc L'aIrose, 06034 ,Vice cedex, France. Rcccivcd Scptcmbcr 9, i $8; acceptcd January 9, i 989.

Abstract

Résumé

Runet P., hl. Bornancin. Aquat. Licing Resour., 1989, 2, 91-97.

Tilapia species are generally characterized by a large tolerance to salinity; however, such capacity to adapt to brackish or seawater may be modulated by environmental factors. ï h e major osmoregulatory mechanisms involved in salinity adaptation are presented. Most of the available data concern the role of gills in salt or water exchange. The importance of different factors (environmental or endogenous) in such adaptation is also discussed. ï h e second part presents a survey of the endocrine control of osmoregulation in tilapia. Both fast-acting (e. g. glucagon, urotensins, catecholamines) and long-acting (e. g. prolactin, cortisol) hormones have been studied. In conclusion, several areas of osmoregulatory physiology potentially interesting for aquaculture are discussed.

Keynords : Salinity, tilapia, osmoregulation, hormones.

I'hysiologie de la tolérance à la salinité chez tilapia: aspects fondamentaux et appliqués.

Les tilapias sont caractérisés par une large tolérance à la salinité, cependant cette capacité d'adapta- tion à I'eau saumâtre ou I'eau de mer peut être modulée par des facteurs environnementaux. Les principaux mécanismes osmorégulateurs impliqués dans cette adaptation sont présentés. La plupart des résultats concernent le rôle des branchies dans les échanges d'eau et de sel. L'importance de différents facteurs (environnementaux ou endogènes) est aussi abordée. La seconde partie de cette synthèse est consacrée à I'étude du contrôle endocrinien de I'osmorégulation chez le tilapia. L'étude des hormones à action rapide (ex. ducagon, urotensines, catecholamines) et à action lente (ex.

prolactine, cortisol) a été envisagée. En conclusion, plusieurs domaines de la physiologie de I'osmorégu- lation potentiellement intéressants pour i'aquaculture ont été suggérés.

~lots-clés : Salinité, tilapia, osmorégulation, hormones.

liLTHODUCTlON fishes d o not tolerate temperatures below 12" but are remarkably tolerant t o high temperatures, u p to Fish of the genera Tilapia a n d Sarotherodon a r e 42°C (Chervinski, 1982). Moreover, several tilapia characterized by a general tolerance t o a wide range s ~ e d e s possess a marked euryhalinity and numerous of environmental conditions. n e i r tropical origin is reports have described these species in estuarine o r clearly reflected in their preferred temperature: these coastal areas of Africa (see review by Stickney, 1986). Aqual. Livinx Resour. 89'02 91 7 f 2.70,'Q IFREXIER-Ciauthier-Vlllam

P. I'runet and XI. Bomancin

This tolerancc is not limitcd to saline waters but also includes environmcnts with poor water quality. Among other factors, good growth and prolific brecd- ing have certainly favoured the large development of tilapia aquaculture observed in recent years.

Compctition with agriculture has increased pressure to develop tilapia aquaculture in marginal arcas such as brackish water or seawater (Payne, 1983). Ilowe- ver, salinity tolerancc alone docs no1 necessarily mean suitability for optimal production and tilapia spccies such as O. niloticus which were chosen for their aqua- cultural potentiality (mainly high growth rate) are not particularly euryhaline. Conversely, O. mossambicus which is among the most euryhaline spccics, has been rcjcctcd due to its relatively slow growth. This has Ied to the development of hybrid spccies, such as the rcd tilapia (produced by crossing femalc 0. mossambi- cus x O. ltornorum with male 0. niloticus) as a good candidate for brackish water or scawater aquaculture (Liao and Chang, 1983).

Poor gowth and mortality among diffcrent tilapia spccies culturcd in brackish water have been rcported rccently (Doudct, 1986; hlorissens, 1987). This appears to be in contradiction with the classical pic- ture of salinity tolerance of these tilapia spccics. Ilowcvcr, most of thcse studies on curyhalinity were undcrtakcn in the laboratory and sometimes over a short pcriod of time. In natural brackish water, fish have to face fluctuations during several months of environmental conditions such as salinity, water qual- ity or temperature, which may makc salinity adapta- tion more difficult. Evaluation of the physiological importance of such parameters is still lacking.

In an attempt to acquire a clearcr picture of the adaptation of tilapia to salinity, differcnt aspects of the physiology of osmorcgulation will be presented in this rcview: the first part will deal with major physiological mechanisms involved in salinity adapta- tion and the importance of diffcrcnt modulatory fac- tors for such adaptation. The second part will focus on the current knowledge of endocrine control of osmorcgulation in tilapia.

In terms of thermodynamics, fish, like other aquatic organisms, rcpresent an open system in dynamic equi- librium with aquatic surroundings. Steady state is reached as a result of exchanges betwccn the fish and ils cnvironmcnt: on the one hand, by passive fluxes, such as thermal cxchangcs occurring through the whole body surface in contact with water; on the othcr hand, by regulated fluxes taking placc across specialized membranes such as @Ils, digestive tract or renal tubules.

The branchial cpithclium which is in intimate con- tact with the extcrnal cnvironmcnt is responsible for many complex functions in fish, including respiration,

excretion, acid-base balance, ionic and osmotic rcgu- lations. Although the gill cpithclium area is four times greater that of the body, providing oxygen from a low concentration of oxygcn in the \vater requires a continuous flow of water through the gills. This means that branchial cclls are constantly cxposed to natural and artificial chemicals. Thus, respiratory or osmorcgulatory branchial exchanges mechanisms, vital for the organism, can be modificd by changes in the external environment.

If the energy costs of respiration and osmoregula- tion are low (e. g., when ecophysiological equilibrium with the cxternal medium is ideal), thcn the propor- tion of metabolic energy which is available for growth is greater. For instancc, tcmpcrature and salinity of water are important characteristics which can modify survival, growth and reproduction of fishcs and limit the distribution of the specics. Tilapia salinity tole- rance has often bcen testcd. Ilowcvcr, little is known about the osmorcgulatory mcchanisms of these fish. So we shall first rcvicw the results published on bran- chial salt exchanges and the possible role of Na+, K+-ATPase in these exchanges and then we shall comment on the salt watcr tolerancc of tilapia. This point has bcen rcccntly revicwed (Chervinski, 1982; Stichney, 1986).

Salt exchangrs: branchial role

Previous investigations by Potts et al. (1967) have shown that drinking rate, rate of sodium exchange and total body sodium incrcascd when Oreochromis mossambicus was adapted to scawatcr; the drinking rate accounted for only one quarter of the total sodium influx in seawater, whereas the remaining thrce quartcrs rcsulted from branchial or skin.exchan- Ses. It is generally admittcd that the branchial cpithe- lium is the major salt transport site in fishes both for salt uptakc in frcsh water (Evans, 1980; Payan et al., 1983) and salt excrction in seawater (hlaetz and Bornancin, 1976). In the same spccics (0. mossam- bicus) Dharmamba et al. (1975) studicd scawatcr adaptation. Fish adapted to frcsh watcr, one-third scawatcr and full scawatcr wcre comparcd in regard to their branchial Na' and Cl- influxes and effluxes. Results are presented in table 1. Plasma Na' and Cl- rcmain practically constant in al1 thrce media, showing the good adaptability of the fish. IIowcver, upon adaptation from fresh water Io 113 seawater or full seawater, the rate of effluxes increascd 15 and 206 times respcctively. Similarly, a large increase in Na+ turnover rate was observed after adaptation to one-third seawater and full scawatcr. Thcsc last valucs wcre rcccntly confirmed in 7ïlapia gralianii by Eddy and hlaloiy (1983).

Some parallelism was observed bettveen Na' bran- chial fluxes and Na*, K+-ATPrise activity in gill tissues (see table 1 and Dharmamba et al., 1975). The significant increase in gill ATPase activity in relation to external salinity is similar to those observed in vanous other teleosts (De Kenzis and Uornancin, Aquat I.itinp Resour.

I'hysiology of salinity tolcrance in tilapia 93

Table 1. - lonic changes with seawater adaptation of Oreochromis mossambicus (from Dharmamba et al.. 1975). Adaptation medium

l 3 V 113 SW S W Plasma values (meq,l) Na' 1 5 8 . 5 I 2 . 2 163.2k2.5 1 6 3 . 8 k 2 . 0

(n = 12) (n = 9) (n= 1)

Cl- 139.0+1.0 149.552.2 146.221.7

(n = 12) (n = 9) ( n = l l ) Influx (peq,'h/IOOg) Na+ 1 3 . 6 k 2 . 5 116529 746 + 79 (n = 8) (n = 6) (n = 6)

a-

(n = 6)

Efflux (peq,'h/lOOg) Na+ 8 . 4 I 1 . 3 125+56 1651 I l 7 1 (n = 8) (n = 5) (n = 8)

a-

(pmol Fi,'mg proth) (n=12) (n = 9) ( n = l l )

1983). Similar observations were made by Valverde et al. (1982) on Tilapia rendalli and by Dangé ( 1 9 8 6 ~ ) on Oreochromis mossambicus.

Uptakc of othcr ions have also been ascribed to the gills. Flik et al. (1985) showed that C a 2 + entry was mainly extra-intestinal and presumably through the branchial epithelium. These results obtained on freshwater-adapted Oreochromis mossambicus confirm the important role of ambient water as a source of C a +

+.

Recently it has been shown in trout by Avella et al. (1987) that the external medium (so-called "fresh water") encomtmsses several situations which are quite different in term of pH and Na+, CI- or C a 2 + concentrations. When fishes are exposed long enough to fresh water with different ionic concentrations, morphological modifications of the gill tissues occur and can be related to different physiological perfor- mances of the branchial epithelium. In freshwater trout, sodium uptake \vas rclated to the abun- dance of "mitochondria-rich cells" on the secondary lamcllae (Avella et al., 1987). These cells (chloride cells), large, granular and mitochondrion-rich, nere first observed in the gills of seawater adapted eels (Keys and Willmer, 1932) and have bcen implicated in salt sccrction in scatvatcr (hiaetz and Bornancin,

1976; Foskett and Scheffey, 1982).

In seawater-adapted fish, chloride cells are located on the filaments (primary Iamellae) of the gills, and the number of chloride cells increascs following salt water transfer (hiaetz and IIornancin, 1975). In the case of Oreochromis mossambicus, chloride cells also occur in the opercular membrane, and thus allow physiological studies on chloride cell development during salt water adaptation (Foskett et al., 1981). These authors showed that opercular membranes from seawater-adapted tilapia contain typical large chloride cells which are absent from freshwater tis- sues, although rudimentary chloride cells are prcscnt. Vol. . n O Z - I Y X Y

Following seawater transfer, the number of chloride cclls increased during the first 3 days, and subse- quently hypertrophy of these cells occurred. The most .

interesting conclusion which emerges from this work is the high correlation bctiveen increasing number and differentiation of chloride cells and salt extrusion.

Other parameters should bc taken into considera- tion during the acclimation process of tilapia to salt water. Assem and Hanke (1983) for example, have demonstrated the participation of amino acids such as taurine and glycine in the osmotic adjustment of musclc cclls.

Salinity tolerance

The ability of tilapia to dcvelop the above physio- logical mechanisms allows them to survive after transfer from fresh tvater to brackish water or seawa- ter. Although tilapia species arc broadly euryhaline and can tolerate a wide range of salinity, such ability to tvithstand salinity varies according to the species. Surveys of the existing literature on the salinity tole- rance of the different tilapia species have already been published (sec reviews Philippart and Rutvet, 1982; Cheninski, 1982; Payne, 1983; Stickney, 1986). and it is not our purpose to duplicate suc11 reviews.

i\daptability to salinity ;an bc modulated by seve- ral factors, i.e., environmental or endogenous. In a recent study on the ontogeny of saliniiy tolerance, \Vatanabc et al. ( 1 9 8 5 ~ ) indicated a close relationship with size, larger fish adapting ensier to higher salini- ties. In another study, the same authors 31~0 showed

that salinity tolerancc could be increased by carly exposure to salinity (during spawning or hatching): they observed the best salinity tolerance after the earliest and highest salinity exposure (Watanabe et al., 1985 b). Such results could certainly be of practical importance and more studies should be devoted to the physiology of such adaptnbility during early dcve-

94 1'. I'runct and hl. Dornancin

lopment and to the ontogeny of this phenomenon. Fccding may also modify seawater adaptability, and a high salt diet was shown to improve sumival rate of several Oreochromis species transferred into a hyper- osmotie environment (Al-Amoundi, 1987). Finally, environmental factors, such as temperature, dissolvcd oxygen and ammonia, also modulate salinity acclima- tion (Beanish, 1970; Farghaly et al., 1973; \Vhitfield and Blaber, 1976), but the impact of such factors on hypo-osmoregulatory capacity still needs to be clarified. Thus, although several biological investiga- tions have been devoted to salinity tolcrance of tila- pia, still more physiological studies are necded, and it would be especially interesting to evaluate the importance of different frcshwater pre-acclimations on the capacity to adapt to salt water.

As in other teleost species, studies on hormonal control of tilapia osmoregulation have involved both rapidly-acting hormones (catecholamines, somatosta- lin, glucagon, VIP, urotensins) and slowly acting hor- mones (prolactin, cortisol, thyroid hormones).

Prolactin (PRL) was among the hormones first studied in Oreochromis mossambicus: Ilandin et al. (1964) first showed the inability of hypophysecto- mized tilapia to survive in fresh water, and Dhar- mamba et al. (1967) demonstrated that PRL treat- ment promoted survival of these hypophysectomized fish. Further studies confirmed PRL involvement: treatment of these hypophysectomized fish kept in fresh water with PRL restored the sodium balance by reducing the sodium cfflux (Dharmamba and hlaetz, 1972). hloreover, injections of PRL in seawater- adapted tilapia induced increase in plasma sodium level and osmolarity (Dharmamba et al., 1973). This cffect of PRL was demonstrated mainly to inhibit both total Na' influx and cfflux (Dharmamba and hlaetz, 1976) which resultcd in ri loss of intracellular

water and then an increase in intracellular K + (Loretz, 1979). The osmoregulatory property of PRL is the basis for the devclopment of an in cico bioassay based on plasma Na+ increase after PRL injections in scawa ter-adaptcd Oreochromis mossambicus (Clarke, 1973).

Elcctrophysiological and radiotracer technics were applied to the isolated opercular membrane (contain- ing numerous chloride cells) from Oreochromis mos- sambicus, permitting the study of hormonal control of cellular mechanism involvcd in adaptation to fresh water or to seawater. In seawater-adapted tilapia, PRL appcared to inhibit chloride secretion by the opercular membrane, probably through a dedifferenti- ation effect on the chloride cell population (Foskett et al., 1982 a). Recently, studies in fresh water-adapted tilapia of whole-animal transepithelium potential (TEP) have indicated a significant dccrcase of this

parameter after hypophysectomy (Young et al., 1988). Injections of these fish with tilapia PRL restorcd both T E P and plasma Na' and CI- levels measured in sham-operated fish (Young et al., 1988). hloreover, in the same study, tilapia PRI, appcared to be ineffec- tive on gill Na+, K+-ATPase activity. These results are consistent with an inhibitory effect of PRL on epithelial ion permeability in fresh water, as suggested in other species (Clarke and Rern, 1980). hloreover,

PRL has also been shown to decrease water permea- bility in isolated gills of tilnpia (Wendelaar Bonga and Van der hlcij, 1981).

Purification of tilapia PRL (Farmer et al., 1976) allowcd the devclopmcnt of an homologous radio- immunoassay which was used to measure plasma and pituitary PRL levels. Transfer from seawater to fresh water induccd a 7-12 increase in plasma PRL levels (Nicoll et al., 1981). hforeover pituitary PRL content, estimated by means of histological studies or radio- immunoassay, decreases in seawater compared to freshwater (Dharmamba and Nishioka, 1968; Nicoll et al., 1981). Thcse data are consistent with an impor- tant role of PRL in freshwater osmoregulation. hlore- over, low but consistent Ievcls of PRL in seawater- adapted fish support a possible role of this hormone in seawater osmoregulation, as suggested by Foskett et al. (1983). Reccntly, a second PRL molecule has been characteritcd from the culture medium of tilapia pituitary (Specker et al., 1985). The complete scquences of the two tilapia PRL were detcrmincd (Yamaguchi et al., 1988) and one of thcm appcared to be 11 amino acids longer than the smaller one. In spite of thcse biochcmieal diffcrcnces, both PRL hormones present similar osmoregulatory activity in freshwater-adapted tilapia (Spccker et al., 1985; Young et al., 1988). Further studies are needcd to determine whether each PRL has specific physiologi- cal functions.

The major corticosteroid in fish, cortisol, has long been implicated in seawater adaptation of teleosts (Hirano and hlayer-Gostan, 1978); its involvement in tilapia osmoregulation has not bencfittcd from many investigations. Assem and Ilanke (1981) have mea- sured changes in plasma cortisol levels during transfer experiments. They observcd a temporary increase in cortisol level after each transfer (fresh water to seawa- ter and the converse) and suggested that cortisol may be neccssary for metabolic changes involved in ccll volume regulation. hloreover, cortisol rcduce the intracellular shrinkage observed after seawater transfer (Assem and tlanke, 1981). A more direct involvement of cortisol in tilnpia osmoregulation has bcen shown by Dangé (1986b) who observed an incre- ase of gill Na', Kt-ATPase activity after cortisol treatment. hloreover, Foskett et al. (1981), using iso- lated opercular membrane, showed an increase in chloride cell density after cortisol treatment, but without activation of chloride sccretion. Interestingly, cortisol treatment associated with hypophysectomy still did not stimulate chloride secretion (Foskctt et al., 1983), leading the authors to suggest the involve-

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