Changes of the fatty acid composition in smolts of masu salmon (Oncorhynchus masou), associated with desmoltification and sea-water transfer

Camp. Biothem. Physiot. Printed in Great Britain

Vol. 103A,No. 1, pp. 221-226,

0300-9629192 $5.00 + 0.00 0 1992 Pergamon Press Ltd

1992

CHANGES OF THE FATTY ACID COMPOSITION IN SMOLTS OF MASU SALMON (ONCORHYNCHW MASOU), ASSOCIATED WITH DESMOLTIFICATION AND SEA-WATER TRANSFER . HAI-OU I.9 and JURO YAMADA Laboratory of Physiology and Ecology, Faculty of Fisheries, Hokkaido University, Hakodate, Hokkaido 041, Japan (Received

10 December

1991)

Abstract--l.

Tissue lipid compositions of desmoltified yearlings of masu salmon (Oncorhynchus masou) obtained by keeping smoltified fish in fresh water, were examined and compared to those of smoltified fish before and after transfer to sea-water (SW). 2. Lipid contents of muscle, liver, gut and gills of desmolts tended to increase compared to those of initial smelts. 3. The increased proportion of triacylglycerol (TG) and decreased proportion of phosphoIipids (PL) characterized the tissue lipids of desmolts. 4. Liver and muscle hpids showed no distinct differences both in content and proportion between initial and SW smohs, but gut and gill lipids of SW smelts decreased in content accompanied by a decrease of TG and an increase of FL in proportion. 5. Excepting muscle non-polar lipids, tissue lipids of desmolts contained more mono-unsaturated fatty acids and saturated fatty acids and less polyunsaturated fatty acids (PUFA), especially (n-3) PUFA such as 22:6(n-3) than those of initial and SW smelts. 6. No large differences in fatty acid composition were seen between initial and SW smelts except for the gut. 7. The proportion of (n-3) PUFA in the gut of SW smelts was higher than that of initial smelts. 8. The results indicated that masu salmon smelts can modify their lipid metabolism to adapt to ambient salinity changes. The proportion of (n-3) PUFA particularly in polar lipids, or in osmoregulatory organs such as gut and gills, was seen to be critical in lipid types of freshwater- or sea-water-adapted fish.

lNTRODUCTION

and in the intestinal brushborder membrane of trout (Leray ef al., 1984). Marine fish lipids contain more PUFA, especially long-chain (n-3) series PUFA, with a high ratio of (n-3)/(n-6), compared to those of freshwater fishes (Ackman, 1967; Gruger et al., 1964). Generally, the difference of lipid types has been considered to be caused by their different lipid sources through respective food chains. However, it has become clear that tissue fatty acids of fish are not only derived from food but also formed de norm by biosynthesis (Cowey and Sargent, 1972). Furthe~ore, fish seem to have the ability to modify ingested fatty acids by desaturation and chain elongation (Cowey and Sargent, 1972). Sheridan et al. (1985) demonstrated increases in long-chain (n-3) PUFA and a shift of lipid pattern from the freshwater type to the sea-water type during Parr-smolt transformation of steelhead trout (Sulmo gairdneri), which were continuously reared in freshwater under the same temperature, feeding condition and photoperiod. This suggests that in salmonids a change of lipid metabolism occurs as preadaptation for sea-water entry and that the change is related to the capability of osmoregulation, because smoltification is the process of acquiring adaptability to seawater.

salinity adaptability of fish depends on the regulatory abilities of ionic or osmotic transport and membrane permeabilities of specific organs. Sargent (1976) pointed out that polar lipids of the external membranes of cells of marine organisms engaging in ionic regulation in seawater may have special requirements in terms of their fatty acid composition. There is some evidence available to support this idea: the ionic ~~eabiIity of the intestinal brush border membrane of trout decreases with deficiencies in essential fatty acids (EFA) (Di Costanzo et al., 1983); destruction of the gill epithe~ium in marine fish is induced by dietary polyunsaturated fatty acid (PUFA) deficiencies (Bell er al., 1985a, b; 1986); and transepithelial sodium absorption in perfused intestine decreases by a (n-3)EFA deficiency (Nonnotte et al., 1987). A few research workers have shown an alteration in fatty acid composition at the time of sea-water adaptation, characterized by increases in (n-3) series PUFA such as 22:6(n-3), in different organs and tissues of guppies (Daikoku et al., 1982) The

*To whom ail cor~s~ndence should be addressed at: Institute of Applied ~i~he~stry, Yagi Memorial Park, Mitake, Gifu 505-01, Japan. 221

222

HAI-0~

LI and JUROYAMADA

When smohs of some salmonid species are continuously reared in freshwater preventing them from seaward migration, the fish regain some morphological characteristics of parr and thus lose their adaptability to sea-water; the phenomenon of smolt-parr reversion is called desmoltification (Kubo, 1980; Filmar, 1980; Hoar, 1988). If the lipid PUPA composition changes at smoltification, one wonders whether the reverse change can be seen at desmoltification, and the change, if it occurs, may be elucidated with reference to adaptation to ambient salinity changes. In this study, we examined the lipid composition of desmoltified yearlings of masu salmon (Oncorhynchus masou) obtained by keeping smoltified fish in fresh water, and compared it with those of smoltified fish before and after transfer to sea-water. MATERIALS AND METHODS

Experimental animals

Smoltified yearlings (13-17cm in standard length) of masu salmon (~~co~~y~c~~~ rnu~o~) were obtained from freshwater ponds of Hokkaido Fish Hatchery Kumaishi Branch early in June, and brought to the laboratory in Hakodate. They were acclimatized to freshwater (FW} under a photoperiod of 12L: 12D at 13 & 1°C for I month and fed moistened nellets (No. SC NIPPON HAIGOSHIRYO) at a ration bf 1% of wet body weight a day. Seven fish in FW were sampled as “initial smelts”, and the rest were divided into two groups of 1.5 fish each. The fish of one group were transferred to sea-water (SW, salinity 32%0), and those of the other group were continuously maintained in FW. After rearing for 1 month, the fish were fasted for 24 hr, then, all the fish were sacrificed for collection of blood, liver, lateral musculature, gut and gills. The gut and giils were washed with a 0.9% NaCl solution and stored imm~iately together with other tissues in a freezer at -40°C until use for analyses. Lipid extraction

Lipids were extracted following the method of Bligh and Dyer (1959). Lipids of liver, gut and gills were extracted from seven fish and pooled. Muscle lipids were extracted from one side of the musculature of individual fish. The extracted lipids were quantified gravimetrically after evaporation of solvents. The extracts were sealed with nitrogen gas in glass vessels and stored in a freezer at -40°C. Lipid class analysis

Class analyses of liver, muscle, gut and gill lipids were performed using the thin-layer chromatography-flame ionization detection system (TLC-FID) with an Iatroscan TH-10 analyser and Chromarods (Type S-III, fatron Laboratories, Tokyo), Peak areas were determined with a Shimadzu RA-3 integrator. Responses of TLC-FID to different lipid standards were determined using a set of the same 10 Chromarods. The lipid class was identified by comparing the retention time withihose of the primary standards containinz triacvhtlvcerols (TG). free fatty acids (FFA) and choleste;ols (?S?$ and . the’ secondary standard’ containing sterylesters (SE), FFA and ST.

Fatty acid analysis

The fatty acid samples were prepared by mixing lipids with a 10% acetyl chloride ethanol solution at 100°C for 3 hr for methylation. The methylated esters were extracted with n-hexane and purified by thin-layer chromatography (TLC) on 0.25 mm thick layers of silica gel-60 (Merck). Bands of methyl esters were visualized with Rodamine-6G under UV light, and transferred from the TLC plates to a column, eluted in hexane/diethyl ester and evaporated with stream of nitrogen gas and stored in a freezer at--40°C until analysis. The methylated fatty acid samples of total lipids and non-polar and polar lipids of muscle, gut and gills were analysed by gas-liquid chromatography (GLC) (HewlettPackard 589OA, with a fused silica capillary column, SUPELCO WAX 10, 30 m x 0.32 mm i.d.), using helium gas at a column temperature of 170-225°C and increasing at a rate of l”C/min. The injection temperature was 250°C and the detector temperature was 270°C. Fatty acids were identified using standard and separation factors and peak areas were calculated using a Hewlett-Packard 5890 Integrator. Statistics

The Student’s t-test was used to compare differences in body weight and condition factor between the groups. Significant was accepted at a 5% confidence level. RESULTS

Desmoltification of masu smohs occurred after continuous rearing in FW for approximately 2 months. The fish resumed the external pigmentation pattern of parr marks. No fish were seen to mature. Smolts transferred to SW retained the silvery appearance of initial smolts. A significant increase of condition factor was noted in desmolts compared to the initial and SW smolts, but the body weight was not significantly different among the three groups (Table I). Lipid contexts muscle

and lipid class corn~osit~on~ in tiver and

More lipids were contained in the liver than in the muscle, and phospholipids (PL) were the main component in both tissues (Table 2). In both liver and muscle, lipid contents in desmolts were slightly higher than those of initial and SW smolts. The lipid class composition in the liver was not significantly different among the three groups. In muscle, however, a marked increase of TG and a decrease of PL were noted in desmolts. The class composition in the muscle of SW smoits was similar to that in initial smolts.

In both gut and gills, SW smolts showed a noticeably lower lipid content than FW smolts and Table I. Body weight, condition factor of masu salmon yearlings

used for liaid analvsis (means* f S.E.1 Initial smolt

FW desmolt

SW smelt

45.63 f 2.51 1.09 * 0.03

46.94 k 2.28 I .38 + 0.02.

43.98 +_2.51 0.96 f 0.04

Separation of non-polar and polar lipids in muscle, gut and gills

Body weight (g) Condition factor

Lipids of muscle, gut and gills were separated into non-polar and polar lipids by column chromato~aphy on silica gel-60 (Merck) using chloroform and methanol as solvents. An aliquot of each fraction was used for the following fatty acid analysis.

Values are means f SE. Seven fish were sampled from each group. lSi~ifi~ntly different from other groups (3’ < 0.05). Initial smelt: smoitified fish in Fw, FW desmolt: d~moItifi~ fish induced by keeping initial smelts in FW for 2 months; SW smelt: smelts transferred to and maintained in SW for 1 month.

Fatty

acid composition

Table 2. Contents and class compositions of lipids in liver and muscle

of masu salmon yearlings Liver

Total lipids (%)* TG FFA E

of smelt maw

salmon

223

Table 3. Contents and class compositions of lipids in gut and gills of masu salmon yearlings

Initial smelt

FW

SW

Initial

FW

SW

desmolt

smelt

smelt

desmolt

smelt

3.39 0.61 0.28 1.98 97.13

3.70 1.57 0.41 0.91 97.11

3.46 1.54 Tr. I.95 96.51

I.34 4.75 Tr. 0.48 94.76

1.64 14.02 TX-. 0.86 85.12

I.57 5.05 0.66 1.16 93.10

*Seven fish pooled. Tr., Trace (less than 0. IO%), Initial smelt: smohified fish in FW; FW desmolt: desmoltified fish induced by keeping initial smelts in FW for 2 months; SW smelt: smelts transferred to and maintained in SW for I month.

desmolts; the largest lipid content was seen in desmolts (Table 3). The proportion of TG was smaller than that of PL in both organs of all groups except in gills of desmolts. Much more TG was contained in the gills than in the gut. This may be due to the inclusion of gill archs which contained a lot of deposited fats. The gut of SW smolts showed increased PL and decreased TG compared to that of initial smelts and the reverse was found in FW desmolts. Both FFA and ST contents in gut and gills showed some differences between FW fish and SW smelts but their proportions were generally low and not largely varied, as seen for TG and PL. Fatty acid compositions of liver and muscle lipids

Total liver saturated fatty acids (SFA) and monounsaturated fatty acids (MUFA) in desmolts showed larger values than those in the smolt groups, whereas total PUFA in desmolts showed a markedly low value, owing to a pa~icuIarly lower content of (n-3) series PUPA (Table 4). No obvious differences in the proportions of total and (n-3) PUFA were seen between the smolt groups. Since the proportions of TG and PL of total muscle lipids were different between the desmolt and the smelt groups (Table 2), total muscle lipids were analysed after separating them into non-polar and polar lipids. Similar to the results in total liver lipids, muscle lipids of desmolts showed, though in a less extent, a higher proportion of SFA, and lower proportions of MUFA and PUFA compared to those of initial and SW smolts (Table 4). Such a difference was also seen in muscle polar lipids, excepting that MUFA was slightly higher in desmolts.

Total hpids (%)* TG FFA ST PL

Initial smelt

FW desmolt

SW smelt

Initial smelt

FW desmolt

SW smelt

4.03 12.99 3.51 2.72 80.79

4.69 23.92 3.5 1 2.33 70.24

2.66 1.25 2.59 4.21 91.96

4.87 46.13 0.98 2.18 50.72

6.02 50.94 I .09 3.56 44.35

2.93 44.18 1.35 2.12 52.35

*Seven fish pooled. Initial smelt: smoltified fish in FW; FW desmolt: desmoltificd fish induced by keeping initial smolts in FW for 2 months; SW smelt: smelts transferred and maintained in SW for I month.

The lower proportion of liver PUFA in desmolts was mainly dependent on decreases in the (n-3) series PUFA, particularly of 22 : 6 (Fig. 1). The ratio SFA/PUFA of liver lipids of desmolts was markedly larger compared to those of the two smelt groups, which showed little difference (Table 4). The ratio SFAjPUFA of muscle polar lipids was slightly higher in desmolts than in initial and SW smohs. No obvious difference of the ratio was seen between the two smelt groups, Fatty acid compositions of gut and girt lipi&

Total gut lipids of desmolts showed a large increase of MUFA and a large decrease of PUFA, especially of (n-3) PUFA as compared with those of initial smolts (Table 5). SW smolts showed the reversed trend to desmolts. No difference in total SFA level was seen between smelts and desmolts. The proportion of total (n-6) PUFA was not different between the three groups. Gut polar lipids showed similar, but less pronounced trends to total lipids; a relatively larger proportion of MUFA and a smailer proportion of PUFA in desmofts than in initial smoits, and the reversed situation in SW smolts. Gill total and polar lipids in desmolts contained more MUFA and less PUFA compared to those of initial and SW smolts (Table 5). The differences were more obvious than in gut polar lipids. Total and polar PUFA especially (n-3) PUFA decreased in desmolts and increased in SW smolts. The proportions of (n-6) PUFA were not different among the three fish groups. The (n-3) PUFA content in both gut and gill polar lipids decreased in desmolts mainly due to changes of 22: 6(n-3) (Fig. 2). The proportion of 18: 2(n-6) in gut

Table 4. Compositions of saturated (SFA), mono-unsaturated (MUFA), and polyunsaturated of lipids in liver and muscle of maw salmon yearlings Liver TL Fatty acid

Initial smelt

FW desmolt

SFA MUFA PUFA (n-3) (n-6) SFAiPUFA

22.64 21.82 53.51 44.78 8.08 0.42

40.62 27.63 29.56 22.00 7.11 I.37

Gills

Gut

Muscle

fatty acids (PUFA)

Muscle SW

-~ molt 25.72 18.83 54.02 44.69 8.69 0.48

Initial smolt

FW desmolt

___ SW smelt

19.27 45.24 32.52 17.71 13.91 0.59

24.59 42.23 30.34 18.44 10.98 0.81

12.91 46.85 37.62 21.76 15.12 0.34

-Initial smolt 22.91 14.65 60.78 54.19 5.56 0.38

-.FW desmolt 24.01 17.16 56.29 49.38 6.24 0.43

22.61 14.84 60.68 54.18 6.12 0.37

TL, Total lipids; NL, non-polar lipids; PoL, polar lipids. Initial smelt: smoitified fish in FW; FW desmolt: desmoitifi~ fish induced by keeping initial smelts in FW for 2 months; SW smelt: smelts transferred to and maintained in SW for I month.

224

HAI-OU LI and JUROYAMADA Liver 0

Initial FW desmolt

E

FWdesmolt

Muscle Gill 40-I

20 IO 111 O (n-3) IPUFA

20:5(n-3)

22:6(n-3)

22:5(n-3)

Fatty acid

Fig. I. Proportions of major (n-3) series polyunsaturated fatty acids [(n-3)PUFA] of total lipids in liver (upper) and of polar lipids in muscle (lower) of masu salmon yearlings. Initial, smoltified fish in FW; FW desmolt, desmoltified fish induced by keeping initial smelts in FW for about 2 months; SW smolt, smolts transferred to and maintained in SW for 1 month; 20: S(n-3), eicosapentaenoic acid; 22: 5(n-3), docosapentaenoic acid; 22 : 6(n-3), docosahexaenoic acid.

and gill polar lipids was larger in desmolts than those in initial and SW smelts, but the proportion of

20:4(n-6) was larger in SW smolts than in initial smolts and desmolts (Fig. 3). The ratio SFAjPUFA in both gut and gill polar lipids were larger in desmolts than in initial and SW smolts (Table 5), yet no clear difference in the ratio was observed. DISCUSSION

The desmolts of masu salmon, induced by keeping smoltified yearlings in FW for 1 month, increased body lipids in all the observed tissues including liver, muscle, gut and gills compared to initial and SW transferred smolts. The results agree with Woo et al. (1978), who reported large reserves of body fat and glycogen in coho salmon desmolts which is a characteristic of Parr. The increased amount of lipids in desmolts was consistent with a high content of muscle Table

5. Compositions

of saturated

Fatty acid

Fig. 2. Proportions of major (n-3) series polyunsaturated fatty acids [(n-3)PUFA] of polar lipids in gut (upper) and gills (lower) of masu salmon yearlings. Initial, smoltified fish in FW; FW desmolt, desmoltified fish induced by keeping initial smolts in FW for about 2 months; SW smolt, smelts transferred to and maintained in SW for 1 month; 20: S(n-3), eicosapentaenoic acid; 22 : 5(n-3), docosapentaenoic acid; 22 : 6(n-3), docosahexaenoic acid.

TG. On the other hand, the gut and gills of smolts transferred and maintained in SW showed largely decreased lipid contents accompanied by a marked decrease of TG. This was particularly conspicuous in the gut. It is generally accepted that the total amount of lipids in tissues of cultured fish is directly correlated with the amount of TG (Henderson and Tocher, 1987; Sheridan, 1986). According to Sheridan (1988a, b), changes in contents of total tissue lipids and TG are correlated to the rate of lipid synthesis and lipolytic enzyme activity in tissues, that is regulated by hormones such as thyroxin, growth hormones, cortisol and prolactin. Direct evidence of an alteration in lipid composition from freshwater type to marine type during smoltification of masu salmon parr was not observed in the present study. However, changes in the lipid pattern are highly possible as shown in comparative studies of lipids in wild parr and smolts of masu

(SFA), mono-unsaturated (MUFA), and polyunsaturated fatty acids (PUFA) polar (PoL) lipids in gut and gills of maw salmon yearlings TL

of total

(TL) and

POL Gills

Gut

Gut

Gills

Fatty acid

Initial smelt

FW desmolt

SW smolt

Initial smelt

FW desmolt

SW smelt

Initial smelt

FW desmolt

SW smelt

Initial smelt

FW desmolt

SW smelt

SFA MUFA PUFA (n-3) (n-6) SFA/PUFA

24.30 34.63 31.57 21.98 8.86 0.65

26.98 40.73 29.27 18.62 9.84 0.92

27.88 25.88 43.64 35.20 7.71 0.64

25.20 37.73 34.54 20.69 12.92 0.73

21.80 43.18 31.65 18.05 12.73 0.69

25.10 36.38 34.47 22.98 10.67 0.73

25.36 23.85 47.86 39.98 7.19 0.53

26.82 25.57 44.51 36.17 7.77 0.60

27.28 20.30 49.61 41.61 7.24 0.55

26.29 27.41 42.37 33.73 7.86 0.62

30.88 33.57 31.49 22.54 8.17 0.98

30.88 29.07 46.40 36.62 8.98 0.67

TL, Total Lipids; PoL, polar lipids. Initial smelt: smoltilied fish in FW; FW desmolt: desmoltified transferred to and maintained in SW for I month.

fish induced by keeping initial smelts in FW for 2 months;

SW smelt: smelts

Fatty acid composition of smolt masu salmon

Gut

0

lnltlal

n FWdsrmolt

0

H

225

0

SW smelt

6

6

z

ae

53

54 2

2

0

0 (n-6)PUFA

16:2(n-6)

(n-6)PUFA

20:4(n-6)

l&2(11-6)

20:4(n-6)

Fatty acid

Fig. 3. Proportions of major (n-6) series polyunsaturated fatty acids [(n-6)PUFA] of polar lipids in gut (left) and gills (right) of masu salmon yearlings. Initial, smoltified fish in FW; FW desmolt, desmoltified fish induced by keeping intial smolts in FW for about 2 months; SW smelt, smolts transferred to and maintained in SW for 1 month; 18:2(n-6), linoleic acid; 20:4(n-6), arachidonic acid.

salmon by Ota and Yamada (1974a, b). We observed similar differences in the lipid type between parr and smolts of cultured masu salmon (in preparation). It is interesting to note that a large difference in fatty acid composition of polar lipids was observed between initial smolts and desmolts but little difference between initial and SW smolts. This indicates that polar lipids in smoltified yearlings of masu salmon undergo a qualitative change when they are reared in freshwater for a long time. Therefore, the lipid metabolism in desmolts must have changed to bring back the tissue lipid composition which is characteristic of the freshwater type. Sheridan et al. (1985) explained the shift of lipid type during smoltification as a preadaptive change to seaward migration. Thus, the process of desmoltification is considered to be accompanied by a switchover in lipid metabolism with the reverse occuring in Parr-smolt transformation. The result that smelts transferred to SW maintained the lipid type of initial smolts suggests that the marine type lipids of smolts are needed for adaptation to environmental salinity. This interpretation justifies the hypothesis by Sheridan et al. (1985) that the shift of lipid type occurs as a preadaption to sea-water entry. The present study confirmed that the polyunsaturated lipid pattern in both total and polar lipids of gut and gills changed in company with desmoltification, as shown by large decreases in (n-3) PUFA. Particularly, 22: 6(n-3) was found to have contributed to these decreases. Because phospholipids were prodominant in total liver lipids, the changes in the polyunsaturated lipid pattern of liver lipids may be due to changes in polar lipids. SW-adapted smolts maintained or slightly increased their (n-3) PUFA content including 22 : 6(n-3) as in the liver and muscle. These findings agree with those found in the gut, gills and other tissues of guppies (Daikoku et al., 1982), and in the intestinal brushborder membrane of trout (Leray et al., 1984). PUFA in tissue lipids are generally derived from dietary absorption and bioconversion of ingested linoleic and linolenic acids through the desaturation-elongation enzyme system, the process established in several fish species (see review by Henderson and Tocher, 1987). Tocher et al. (1989) studied the

metabolism of (n-3) and (n-6) PUFA in differentially cultured cells originating from freshwater and marine fish, and demonstrated that (n-3) PUFA, especially 22: 6, were preferentially deposited in marine fish cells with a higher desaturase enzyme activity than in freshwater fish cells. The different proportions of PUFA, especially (n-3) PUFA, between all the examined tissues of SW smolts and FW desmolts are considered to be the result of metabolic modification elicited by different environmental salinities. Deficiencies of essential (n-3) fatty acids such as 22: 6(n-3) have been reported to induce loss or reduction in the capability of ionic regulation in the epitheiia of salt-transporting organs in fishes (Di Costanzo et al., 1983; Bell er al., 1985a-c, 1986; Nonnotte et al., 1987). A great increase in 22:6(n-3) in the intestinal membrane causes increased fluidity of the membrane at the time of sea-water adaptation of trout (Leray et al., 1984). A lower proportion of SFA to PUFA increases fluidity of the biomembranes (Bell et al., 1986). In light of these previous reports, the decreased proportion of (n-3) PUFA and the increased ratio SFA/PUFA in tissue lipids of desmolts seems to suggest lowered fluidities of their biomembranes compared to initial and SW smelts. A loss of sea-water adaptability during desmoltification probably has a close relation with a low fluidity of the membrane system to facilitate normal physiological functions in freshwater. It is noteworthy that the proportion of 20 : 4(n-6) in gut and gill lipids was larger in SW smolts than in initial smolts and desmolts. Bell et ul. (1983, 1986) showed that 20:4(n-6) is the major PUFA in phosphatidylinositol (PI) from marine fish. The activity of salt transporting epithelia in the gills of teleost fish is influenced by the metabolic activity of PI in the chloride cells (Girard et al., 1977). The turnover of PI is important in salt secretory activity of the rectal gland in dogfish (Simpson and Sargent, 1985). The increased 20: 4(n-6) in the gut and gills of SW smelts seems to suggest its role in salt transport activity in seawater. Juvenile masu salmon are considered to adjust their lipid composition of salt-transporting organs to adapt to environmental salinity changes. Dynamics of lipid metabolism in fishes should be investigated

226

HAI-OU LI and JUROYAMADA

further in relation to physiological mechanisms adaptation to environmental salinities.

of

Acknowledgements-We

are indebted to Dr Toru Ota, Faculty of Fisheries, Hokkaido University, and Messrs Shari Hokari and Eiji Hasegawa, Nihon Kagaku Shiryo Co. for their valuable technical advice and assistance in chemical analyses of lipids. REFERENCES

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