Adaptations of Fish

G.E. Shulman    Institute of Biology of the Southern Seas, Sevastopol, Republic of Ukraine

R. Malcolm Love    Formerly Torry Research Station, Abbey Road, Aberdeen, Scotland

The metabolism of marine fish is influenced by the abundance, accessibility and composition of the food, by parasites, intra- and interspecies relationships and by the nature of the surrounding medium – temperature, pressure, illumination, gas content, salts and other substances, and perhaps radiation. The fish in turn influence some of these parameters, such as the quantity of food and the composition of the water. Let us consider how fish adapt to these influences.

2.1 TEMPERATURE

2.1.1 General Effects

Temperature influences the rates of chemical reactions. In theory, the range of temperatures tolerated by life forms is comparatively wide, but, in fact, each species shows characteristic, limited temperature preferences and tolerances.

Many effects of change in temperature are manifested through changes in the activity of metabolic enzymes. For example, Shchepkin (1978) found that the activity of succinate dehydrogenase in muscle and liver of several species of fish increased within the temperature range of 5 °C to about 25 °C, but that above this the activity of the enzyme declined – the heat was causing damage. Similar data were obtained by Emeretli (1994a) on succinate dehydrogenase activity of the mitochondria of the same tissues of round goby, scorpion fish and horse-mackerel from the Black Sea. The last two species, together with whiting and pickerel, show positive correlation between lactate dehydrogenase activity of the cytosol and the temperature. The activities of uricase, allantoicase and allantoinase in the liver of carp increase with a rise in temperature (Vellas, 1965). All enzymes are affected in the same way to some extent.

A rise in temperature accelerates the rate of development of eggs (Forrester and Alderdice, 1966) and reduces the period of gestation in live-bearing species (Kinne and Kinne, 1962). The growth rate of adults increases (Le Cren, 1958), as does the rate of emptying the gut after feeding (Hofer et al.,1982; Eccles, 1986) and the actual absorption of the food (Love, 1988, p. 51). The regeneration of nervous tissue following damage is also accelerated (Gas-Baby et al., 1967). In addition, there are positive correlations between temperature, muscle contraction and swimming velocity (Wardle, 1980; Johnston, 1982).

None of these or similar observations is unexpected, nor are they of primary importance. More interesting are the ways in which fish adapt to changes in temperature.

2.1.2 Adaptation to Temperature

2.1.2.1 Enzymes and Metabolism

The correlation between ambient temperature and enzymatic activity in muscle tissue is governed in some cases by the law of Van’t Hoff and Arrhenius, with activity change with a change of temperature of 10 °C (Q10) approaching 2 (Prosser, 1979; Schmidt-Nielsen, 1979), but in other cases the law is not obeyed. Departure from the Van’t Hoff coefficient in poikilothermic animals has been explained as ‘temperature compensation’, which can be achieved by a variety of mechanisms, each being appropriate to a specific temperature range (Bullock, 1955; Prosser, 1967; Newell, 1970; Brett, 1973; Hochachka and Somero, 1973; Klekowski et al., 1973; Wallace, 1973; Slonim, 1979; Lozina-Lozinsky and Zaar, 1987; Ozernyuk et al., 1993).

The fact that enzymes are heterogeneous and that each isoenzyme displays a characteristic optimum reaction temperature may be one mechanism that allows compensation for temperature change in many poikilo-therms. A classic example is the oxygen consumption (i.e. metabolic rate) of Arctic (Scholander et al., 1953) and Antarctic (Wohlschlag, 1960) species, which is considerably greater than that calculated from the Van’t Hoff relationship. Love (1980, pp. 333-335), reviewing isoenzyme interplay at varying temperatures, concluded that the effect was probably limited to ‘certain enzymes in specific organs of a few species’. Enzymic activity may change because of an increase in the actual amount of enzyme present, changes in its conformation or modification of the interrelation between the enzyme and various physico-chemical factors (Tsukuda, 1975; Hochachka and Somero, 1977, 1984).

The concept of temperature compensation of metabolism at the whole animal level in poikilotherms has been subject to strong criticism by Holeton (1974, 1980) and especially by I.V. Ivleva (1981), who believed that such ‘compensation’ was an artefact arising from inadequate acclimation. However, Ivleva’s own experiments were carried out on aquatic invertebrates, not fish, and the data referred to standard metabolism rather than total or active. Note that total metabolism is that taking place in an animal in nature, active metabolism is that which supplies locomotory activity, standard metabolism is that observed in experiments, and basal metabolism is that in the resting state. Ivlev (1959) found that apparent adaptive reactions of animals are seen mostly in active, not standard or basal, metabolism. However, more recent work (Karamushko and Shatunovsky, 1993; Musatov, 1993) appears rather to favour the concept of I.V. Ivleva, that standard, not active, metabolism illustrates the adaptive reactions.

E.V. Ivleva (1989a) found that, during the winter, Black Sea horse-mackerel displayed increased thyroid activity. This is directly related to the intensity of energy metabolism. Other workers found enhanced growth of the follicular cells of the thyroid gland of brown trout and brook trout during periods of low temperature (Woodhead and Woodhead, 1965a,b; Drury and Eales, 1968), and increased thyroxine levels in the blood plasma (Eales et al., 1982). On the other hand, Leatherland (1994) has demonstrated a close positive correlation between water temperature and the concentrations of both forms of thyroid hormone (thyroxine and tri-iodothyronine) in the plasma of brown bullhead.

Differences between species often dilute the impact of otherwise interesting correlations but, in the case of thyroid hormones, the dose level causes additional complications. Tri-iodothyronine enhances the incorporation of amino acids into tissues or enhances their catabolism, depending on the size of the dose of hormone given. A similar effect on weight gain/weight loss is seen according to the dose of the same hormone. A further difficulty with the conclusions of earlier workers is that the enhanced growth of the thyroid follicular cells does not necessarily mean greater secretion of the hormones into the blood stream. All that one can say is that greater quantities of hormones are being stored in the gland (Leatherland, personal communication). It has been considered that the thyroid hormone stimulates oxygen consumption in fish (Ruhland, 1969; Gabos et al., 1973; Pandey and Mushi, 1976). However, having regard to all the data published so far, Leatherland (1994) has concluded that such an effect, if it exists, is small.

As the temperature falls, the number, volume and enzymatic capacity of mitochondria in the muscle tissues of fish increase (Jankowski and Korn, 1965; Wodtke, 1974; Johnston and Maitland, 1980; Dunn, 1988); the sizes of liver cells and their nuclei also decrease (Campbell and Davis, 1978), while the number of muscle cytochromes increases (Sidell, 1977; Demin et al., 1989). Johnston and Horne (1994) have shown that the proportion of each muscle fibre occupied by mitochondria in herring larvae is greater at lower rearing temperatures. The same finding has been reported in adult carp (Rome et al., 1985). Distinct temperature compensations are observed for glycolytic enzymes (phosphofructokinase, aldolase, lactate dehydrogenase), those in the hexose monophosphate shunt (6-phosphogluconate dehydrogenase), the Krebs cycle and electron transfer (succinate dehydrogenase, malate dehydrogenase, cytochrome oxidase, succinate cytochrome-c-reductase, NADH cytochrome-c-reductase), protein synthesis (aminoacyltransferase) and Na+K+-ATPase (Eckberg, 1962; Krüger, 1962; Freed, 1965; Smith et al., 1968; Somero et al., 1968; Caldwell, 1969; Haschemeyer, 1969; Hazel and Prosser, 1970; Smith and Ellory, 1971; Hazel, 1972; Hochachka and Somero, 1973; Wodtke, 1974; Shaklee et al., 1977; Campbell and Davis, 1978; Tirri et al., 1978; Stegeman, 1979; Sidell, 1980; Jones and Sidell, 1982; Christiansen, 1984; Bilyk, 1989; Romanenko et al., 1991; Klyachko and Ozernyuk, 1991; Yakovenko and Yavonenko, 1991; Karpov and Andreeva, 1992). Other enzymes and authors are listed by Love (1980, Table 20).

Not only do the activities of the enzymes increase, but their catalytic efficiencies (enzyme-substrate affinities, as defined...