Thermal acclimation in fish: conservative and labile properties of swimming muscle

HELGA GUDERLEY AND PIERRE BLIER De'partement de biologie, Universite' Laval, Que'bec (Que'. ), Canada GI K 7P4

Received May 18, 1987

GUDERLEY, H., and BLIER, P. 1988. Thermal acclimation in fish: conservative and labile properties of swimming muscle. Can. J . Zool. 66: 1105- 1115.

Given the rapid thermal equilibration of most fish with their environment, thermal compensation of metabolic and contractile properties is essential for the maintenance of locomotory capacities over a wide range of temperatures. The response of fish swimming performance, contractile properties of isolated fibers, myosin ATPase activity, and metabolic systems for ATP generation to short- and long-term changes in temperature have received sufficient study to allow one to identify certain con- strained and labile properties. Sustained swimming performance and its components generally have their optimal performance and lowest thermal sensitivity within the range of temperatures frequently encountered by the organism. These principles are particularly well established for isolated enzyme systems. Furthermore, swimming performance and most of its components demonstrate thermal compensation on the evolutionary time scale. Temperature acclimation also leads to compensatory responses which, while quite species-specific, consistently increase the capacity for sustained swimming at low temperatures. The position of the thermal optimum for locomotion in relation to the width of a species' tolerance limits aids in predicting the species' capacity for thermal compensation during acclimation. Goldfish (Carassius auratus) and common carp (Cyprinus cap io ) , which tolerate temperatures 25 -30°C below their optimum for locomotion, show thermal compensation in terms of contractile properties, myosin ATPase activity, the proportion of red fibers in their axial musculature, and the levels of aerobic enzymes in their musculature. By contrast, striped bass (Morone saxatilis) and chain pickerel (Esox niger), which have lower optimal temperatures for locomotion, only increase the proportion of red fibers and (or) the levels of aerobic enzymes with cold acclimation. Finally, lake whitefish (Coregonus clupeaformis), which have their optimal temperature for locomotion at 12"C, show none of these responses. Given that when thermal compensation occurs, aerobic enzymes in red muscle generally increase, the capacity of red muscle to generate ATP seems more temperature sensitive than other metabolic or contractile properties. Whether this compensatory response serves to counteract the effect of temperature on diffusive exchange between mitochondria and the cytoplasm or its effect on the catalytic capacity of aerobic metabolism remains to be established.

GUDERLEY, H. , et BLIER, P. 1988. Thermal acclimation in fish: conservative and labile properties of swimming muscle. Can. J. Zool. 66 : 1105- 11 15.

Comme la plupart des poissons sont des poikilothermes obligatoires, la compensation thermique des propriCtCs mktaboliques et contractiles est essentielle a la conservation de leur capacitC locomotrice sur une grande gamme de tempkratures. La sensi- bilitC thermique de la performance de nage, des propriktks contractiles des fibres isolkes, de l'activitk de la myosine ATPase et des enzymes du mktabolisme knCrgetique a kt6 suffisamment etudiCe pour que l'on puisse identifier des propriktks qui sont modifiables et d'autres qui sont fixes. La nage soutenue et les composantes qui la dkterminent ont genkralement leur per- formance optimale et leur thermosensibilitC minimale dans la gamme des tempkratures frkquemment rencontrkes par l'organisme. Ces principes sont particulikrement bien Ctablis dans le cas d'enzymes isolks. Ces propriCtks de la nage dkmon- trent donc une compensation thermique sur l'echelle kvolutive. L'acclimatation thermique peut kgalement conduire a des rCac- tions de compensation. Ces rkponses, bien que relativement spkcifiques aux groupes de poissons Ctudiks, amkliorent gCnCralement la capacitk de nage soutenue a basse tempkrature. La position de l'optimum thermique de la locomotion par rapport a l'amplitude de la gamme de tempkratures tolCrCes semble relike a la capacitk de compensation thermique lors de l'acclimatation thermique. Ainsi, le poisson rouge (Carassius auratus) et la carpe (Cyprinus cap io ) , qui tolkrent des tempCra- tures jusqu'a 30°C en bas de la temperature optimale de locomotion, repondent a l'acclimatation au froid par une compensa- tion thermique de leurs propriktks contractiles, de 1'activitC de la myosine ATPase, de la proportion de fibres rouges et des concentrations des enzymes du mktabolisme akrobie dans leur musculature axiale. Par contre, le Bar raye (Morone saxatilis) et le Brochet mail16 (Esox niger), qui posskdent des tempkratures optimales de locomotion plus faibles que celles du poisson rouge et de la carpe, n'augmentent que la proportion de fibres rouges ou les concentrations des enzymes du mktabolisme akrobie dans leur musculature. Finalement, le Grand Corkgone (Coregonus clupeaformis), dont la temperature optimate de locomotion est de 12"C, ne montre aucune compensation de sa capacitk aCrobie au cours de l'acclimatation au froid. Etant donnk que la compensation thermique semble prioritairement augmenter les concentrations des enzymes du metabolisme akro- bie dans le muscle rouge, la capacitk du muscle rouge a gknkrer de I'ATP semble plus sensible a la temperature que les autres propriktks mCtaboliques ou contractiles. I1 reste encore a dkterminer si cette compensation sert a contrer les effets de la tempkrature sur les kchanges par diffusion entre mitochondries et cytoplasme ou les effets sur la capacitC catalytique du mCta- bolisme akrobie.

Introduction

Temperature is the environmental factor that has the most pervasive effects on the cellular biochemistry of fish. Given the rapid .thermal equilibration across gills and body walls, most fish, with the exception of lamnid sharks and tuna, have body temperatures that are very close to those of their environ- ment (Reynolds and Casterlin 1980; Elliott 1981). Changes in environmental temperature thus have an immediate impact upon cellular temperature.

While fish exploit environments in which temperatures Pnnted in Canada I Imprime au Canada

range from -2°C to above 40°C, most species tolerate only a portion of this range. At the lower extreme are polar fishes, such as Pagothenia borchgrevinki, which produce antifreeze proteins to exploit sub-zero temperatures. Desert pupfish (Cyprinodon spp.), which tolerate temperatures as high as 44°C (Elliott 1981) are at the other extreme. As the metabolic rates of species living at different temperatures are similar, the evidence for temperature compensation on an evolutionary time scale is strong (Brett and Groves 1979). In many fish spe- cies, thermal compensation also occurs during acclimation to different environmental temperatures (Hazel and Prosser 1974;

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1106 CAN. J . ZOOL. VOL. 66, 1988

Reynolds and Casterlin 1980). While thermal acclimation has . ? COREGONIDPT

been characterized in many ways (Hazel and Prosser 1974; -------------_ THYMALLIDAE s tenotherms

Reynolds and Casterlin 1980). generalizations as to the stra- SALMONIDAE r * u - - - - - - - - - - - - - - - - - - - - - I

tegies of thermal acclimation require examination of the ? ESOCIDAE responses of one physiological system in species with differing most

thermal requirements. Given the selective importance of con- ---------------------------+ C Y P R I W

,-----------------------, GASTEROSTEIME Mesotherms servation of locomotor capacities and the variety of excellent ? . I studies examining the responses of the metabolic and contrac- tile components of muscle to thermal acclimation, we will focus upon this aspect to identify constrained and adaptable features in the responses to thermal acclimation.

Thermal sensitivities of fish To understand compensatory responses to thermal acclima-

tion, one must understand the thermal sensitivities of fish on both the holistic and reductionist levels. The differing thermal tolerances and capacities for thermal acclimation of fish have led to their somewhat simplistic classification as eurytherms, mesotherms, and stenotherms (see Magnuson et al. 1979; Rey- nolds and Casterlin 1980; Elliott 198 1). In his review, Elliott (1981) compares the thermal requirements (optimum thermal range and upper and lower critical limits) of certain fish fami- lies in the three classes: the Coregonidae, Thymallidae, and Salmonidae represent cold-water stenotherms; the Esocidae, Gasterosteidae , Percidae , Anguillidae , and most Cyprinidae represent mesotherms; and certain Cyprinidae, i.e., common carp (Cyprinus carpio) , goldfish (Carassius auratus) , and grass carp (Ctenopharyngodon idella), represent warm-water eurytherms (Fig. 1). While the range of temperatures between the upper and lower critical limits of these families varies con- siderably, their optimal thermal ranges are more similar in size. This optimal temperature range is that over which feeding and no external signs of abnormal behavior occur; it is some- what wider than the temperature range for growth and matura- tion and similar to the preferred temperature range (Elliott 198 1). Magnuson et al. (1 979) also show that fish species with widely differing preferred temperatures have similarly sized ranges of preferred temperatures. The range of optimal (pre- ferred) temperatures may be a better indicator of the thermal dependence of metabolic processes than the range of tolerated temperatures. Elliott's (1981) review indicates that the Perci- dae, Anguillidae, and Cyprinidae have wider .thermal optima than the eurythermal Cyprinidae (Fig. 1). This suggests that studies seeking to characterize fish species that show thermal independence of metabolic properties should study such meso- thermal fish rather than the eurythermal fish.

How could fish gain thermal independence? Thermal independence can be conferred upon physiological

processes by several means. One possibility is to engineer the components to function optimally over an organism's entire thermal range. Accordingly, the kinetic parameters of enzymes from organisms that live at stable temperatures show marked thermal sensitivity, while the kinetic parameters of enzymes from organisms that experience a wide range of temperatures show greater thermal independence (Somero and Low 1977; Hochachka and Somero 1984). Furthermore, for organisms living at different temperatures, the thermal optima of their enzymes reflect the median habitat temperatures. For lactate dehydrogenase from four species of barracuda (Sphyraenu spp.) living at different temperatures, the K,,, for pyruvate measured at each species' median habitat temperature was the

common carp I ' ( " ' I ' 1 ' 0 10 20 30 40 42

Temperature ( O C )

FIG. 1 . Thermal requirements of different fish families. Solid bars represent the optimal thermal range; solid lines represent the distance between the upper and lower critical limits. Broken lines indicate the limits for normal egg development. (Modified with permission from Elliott 198 1, 0 198 1 Academic Press).

same (Graves and Somero 1982). However, as evidenced by the responses to thermal acclimation, the limits to the euryther- mality of enzyme function probably prevent organisms with broad thermal ranges from relying solely upon constant levels of their metabolic components. A second possibility is to simultaneously express different forms that function in differ- ent portions of the organism's thermal range. Thirdly, if an organism has sufficient time to acclimate to temperature change, it could vary the amount or type of enzyme expressed, as well as the nature of the proteins or lipids that are in the enzyme's immediate environment (Hochachka and Somero 1984). While these alternatives demonstrate means by which the catalytic processes can achieve thermal independence, dif- fusive processes, essential for the exchange of substrates among metabolic components, are also affected by tempera- ture and may require compensatory adjustments to achieve thermal independence (Sidell 1983 ; Sidell and Hazel 1987).

What mechanisms are employed by fish to maintain their locomotor capacity during thermal acclimation? Muscle is a virtually senlicrystalline array of contractile proteins and of enzymes that liberate ATP. The structural and functional con- straints in such a highly organized tissue may well limit the adaptive flexibility required to maintain locomotor capacity over a broad temperature range. On the other hand, the bene- fits of maintaining locomotor capacity should strongly favor such adaptations. In the following sections we will examine the thermal sensitivity of swimming performance, of contrac- tile properties of isolated fibers, of myosin ATPase activity, of fiber recruitment order, and of metabolic properties to under- stand the changes that these parameters undergo during ther- mal acclimation.

Swimming performance in fish Fish physiologists separate fish swimming performance into

three categories: sustained swimming, i.e., swimming at speeds that fish can maintain indefinitely; prolonged swim- ming, i.e., swimming that fish can maintain from 2 to 200 min; and burst swimming, which fish can maintain for 2 min or less (Beamish 1978; Webb 1978). These types of swimming rely upon different fiber types; sustained swimming is pri- marily supported by aerobic "red" fibers, prolonged swim- ming involves recruitment of some of the white fibers that compose the bulk of the swimming musculature, and burst swimming recruits all fibers (Bone 1966; Bone et al . 1978;

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GUDERLEY AND BLIER 1107

Freadman 1979). The thermal sensitivity of these types of swimming should reflect that of different fiber types, their metabolic activities, and the neural control mechanism that directs their recruitment. Given that these categories of swim- ming are used in different ecological contexts, the selection pressures that bear on their thermal sensitivities may well differ. Migrations are carried out using primarily the sustained swimming capacity assured by the aerobic musculature. Priede (1977, 1985) argues that because the risk of mortality increases exponentially as a fish approaches the limits of its aerobic scope, strong selection pressures constrain organisms to remain within their aerobic scope. Because a good capacity for sustained swimming permits high-speed aerobic migration and prevents fatigue, it decreases the probability of mortality for a migrating fish. By contrast, predator avoidance and prey cap- ture rely principally upon the prolonged or burst swimming speeds (Webb 1984; Sidell and Johnston 1985) assured by the fast, glycolytic muscles. As predicted earlier and shown in the following sections, the thermal sensitivity of these types of swimming differs.

Thermal sensitivity of swimming capacities Sustained swimming is most often quantified by the critical

velocity (U,,,) determined by the incremental swimming speed test of Brett (1964) or by measures of endurance at different swimming speeds. The thermal dependence of U,,, generally follows that of aerobic scope (Beamish 1981). Thus, U,,, increases with temperature to a maximum and then decreases with further increases in temperature. This has been observed for Exodon paradoxus and Leporinus fasciatus (Beamish 198 1 ), sockeye salmon (Oncorhynchus nerka) (Brett 1967), coho salmon (0. kisutch) (Griffiths and Alderdice 1972), gold- fish (Carassius auratus) (Fry and Hochachka 1970), spotfin shiner (Notropis spilopterus), and channel catfish (Ictalurus punctatus) (Hocutt 1973). Generally, the maximum for the U,,, occurs within the organism's preferred temperature range. For two tropical species, Exodon paradoxus and Leporinus fasciatus, the maximum for the U,,, is between 30 and 35°C (Beamish 198 1); for goldfish, largemou th bass (Micropterus salmoides), and smallmouth bass (Micropterus dolomieui L.) it is between 25 and 30°C (Fry and Hart 1948; Beamish 1970; Larimore and Denever 1968); for lake trout (Salvelinus namuy- cush) and sockeye salmon it is between 15 and 20°C (Gibson and Fry 1954; Brett 1964); and for lake whitefish (Coregonus clupeaformis), which are widely distributed in Canadian and arctic waters, the U,,, is maximal at 12°C (Bematchez and Dodson 1985). For the antarctic species Trematomus borch- grevinki, U,,, is maximal at -0.8"C (Wohlschlag 1964). In contrast, for certain flounders U,,, is little affected by changes in temperature (Duthie 1981). Thermal independence of the critical velocity within the range of tolerated temperatures is reported for several species from the Mackenzie River (Jones et al. 1974). Finally, data for goldfish, coho salmon, and common carp (C. calpio) (Fry and Hart 1948; Griffiths and Alderdice 1972; Heap and Goldspink 1986) indicate that at a given temperature the maximum critical velocity is attained when this temperature is the acclimation temperature of the fish. These data indicate that critical swimming speeds are responsive, in both the short and long term, to the thermal environment in which the species is found.

Given the short duration of burst swimming, its thermal sensitivity is more difficult to determine than that of the critical

swimming speeds. Generally, burst swimming speeds seem more independent of temperature than sustained swimming speeds. This tendency was observed for herring (Clupea harengus) , winter flounder (Pseudopleuronectes americanus), and sockeye salmon (Beamish 1966; Brett 1967, 1970). In contrast, an increase in burst swimming speeds with increase in temperature was found for striped mullet (Mugil cephalus), spot (Leiostomus xanthurus), and pinfish (Lagodon rhom- boides) (Rulifson 1977).

Thermal sensitivity of contractile properties Given the complex orientation and short length of fish

muscle fibers (Alexander 1969), systematic study of the con- tractile properties of fish muscle requires sophisticated tech- niques that have only recently become available. Nonetheless, as a result of the zealous application of these techniques by Johnston and his collaborators, several conclusions about the correlation between contractile properties and habitat tempera- ture are now possible. The maximal isometric tension (To) of white muscle fibers from many species is independent of habi- tat temperature (regressions between temperature and To or log To are not significant, p > 0.05). By contrast, the To of red fibers decreases with increase in habitat temperature (Table I). For white and red fibers, the maximal contraction velocity, Vmax, increases directly with habitat temperature (Table 1). For both fiber types, the effects of habitat temperature on To and Vmax differ ( p < 0.05). The increase of Vmax with increasing habitat temperature and the temperature independence of To for white fibers resemble the thermal relationships for these con- tractile properties in amphibian, reptilian, and insect muscles (Bennett 1985; Josephson 1983). For the fish from warm habi- tats, Vmax values are highly variable. While the variability may reflect differences in the locomotor capacities of the species, Vmax for the chain pickerel (Esox niger), a species noted for its excellent capacity for acceleration, is one of the lowest (Sidell and Johnston 1985).

While Vmax at habitat temperature increases with rising habi- tat temperature, the thermal sensitivity of contractile properties in different species suggests that thermal compensation on an evolutionary time scale has decreased the impact of tempera- ture on contractile processes. The Vmax values of isolated fibers from the antarctic fishes Notothenia neglects, Tremutomus hansoni, Chaenocephalus aceratus, and Notothenia rossii, measured at 0 to 5°C (Johnston and Brill 1984; Johnston and Harrison 1985), are 180% of that of flounder fibers measured at 0°C (Johnston and Wokoma 1986). Also, the thermosensi- tivity of Vmax of white fibers on the intraspecific level is greater than that shown by interspecific comparisons of Vmax of white fibers measured at habitat temperatures ( p < 0.05) (Table 1). A similar trend is shown by red fibers. This suggests that ther- mal compensation has occurred on an evolutionary time scale and that the contractile machinery can be adjusted to answer the thermal and locomotor requirements of different species.

Power output is the contractile property that is most directly related to swimming performance (Rome et al. 1984; Sidell and Johnston 1985) and for which thermal compensation would be the most advantageous. The thermal sensitivity of power output reflects that of Vmax and To. On the intraspecific level, the thermal sensitivity of Vmax of white fibers is greater than that of To ( p < 0.05) (Table 1); the same tendency is apparent for red muscle. Power output is thus more indepen- dent of temperature than Vmax, and generally shows QIo values

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TABLE 1. Thermal sensitivities of contractile properties

Q I ~ 95% CI

Interspecific comparisons Red muscle To Red muscle V,,, White muscle T, White muscle V,,,

Intraspecific studies Red muscle T, Red muscle V,,, White muscle T, White muscle Vm,,

NOTE: Thermal sensitivities were evaluated by comparing the y,,, and To of fibers isolated from species with differing thermal habitats and by examining the thermal sensitivity of V,,, and 7;) on the intraspecific level. The interspecific QIo values were obtained from the slopes of the regres- sions of log contractile parameter versus temperature. In these relation- ships, the contractile parameters (To and V,,,) were measured at the habitat temperature for Gadus rnorhua (Altringham and Johnston 1982); Noro- rhenia neglecra, Mugil cephalus, Carangus rnrlampygus, Kursuw~onus pelamis, Eurhynnus af inis , and Coryphaena hippurus (Johnston and Brill 1984); Makaira nigricuns (Johnston and Salamonski 1984); Nororhenia neglecra and Scyliorhinus canicula (Altringham and Johnston 1985); Chaenocephalus aceratus, Nororhrnia rossii, and Tremaromus hansoni (Johnston and Harrison 1985); Esox nigrr (Sidell and Johnston 1985); Cyprinus carpio (Johnston er al. 1985); and P1arichrhy.sfle.su.s L. (Johnston and Wokoma 1986). The intraspecific thermal sensitivities were obtained from the Q,,, values published for the contractile properties of fibers from Mugil cephalus, Carangus melanp-vgus, and Karsuwonus pelamis (Johnston and Brill 1984); Myoxocephalus scorpius L. (Johnston and Sidell 1984); Makaira nigricans (Johnston and Salamonski 1984); Esox niger (Sidell and Johnston 1985); Cyprinus carpio (Johnson er a / . 1985); and Plarichrhys flesus L. (Johnston and Wokoma 1986). CI, confidence interval.

below 2 (Johnston and Salamonski 1984; Sidell and Johnston 1985; Johnston and Wokoma 1986).

Relatively little information is available concerning the effect of thermal acclimation on the contractile properties of fish muscle. Common carp (Cyprinus carpio) show thermal compensation of Vmax, To, force generation, and workIATP hydrolyzed after acclimation to low temperatures (Altringham and Johnston 1985; Johnston et al. 1985). Goldfish fin muscles show compensation of contractile properties after acclimation to low temperature (Heap et al. 1987). Similar changes could explain the thermal compensation of sustained swimming speed after acclimation of goldfish to low tempera- tures (Fry and Hart 1948). By contrast, flounder (Platichthys flesus L.), chain pickerel (Esox niger), and striped bass (Morone saxatilis) show no changes in contractile properties with acclimation to low temperatures (Johnston and Wokoma 1986; Sidell and Johnston 1985; Moerland and Sidell 1986~) . Wardle (1980) found that temperature acclimation of plaice did not alter the relationship between temperature and contraction time of isolated pieces of white muscle.

Thermal sensitivity of myosin ATPase Before direct study of the contractile properties of fish

muscle was possible, the correlation between the activity of myosin ATPase and the maximal velocity of shortening in muscles of various vertebrates (Bartiny 1967) provided a tool with which to probe the thermal sensitivity of contractile prop- erties of fish muscle. The thermal sensitivities of myosin ATPase resemble those of enzymes; its Qlo values range from 2.2 to 1 1 (Hochachka and Somero 1973; Sidell et al. 1983; Sidell and Johnston 1985) and the thermal dependence of cal-

cium sensitivity varies with cell temperature (Johnston and Walesby 1979). Furthermore, fish from cold habitats have myosin ATPases with lower activation enthalpies, lower ther- mal stabilities, and greater catalytic efficiencies than those of fish from warmer habitats (Johnston et al. 1975; Johnston et al. 1977; Johnston and Walesby 1977, 1979). This could explain the thermal compensation of Vmax of isolated fibers on an evolutionary time scale. Thermal denaturation studies sug- gest that myosin ATPases from species from colder habitats are less rigid and have a more open structure (Johnston et al. 1973; Johnston and Goldspink 1975; Johnston et al. 1975; Johnston et al. 1977). These differences seem to reside on the level of the myosin light chains (Johnston 1982).

Despite the numerous indications that thermal compensation of myosin ATPase activity has occurred on an evolutionary time scale, the impact of this thermal compensation on con- tractile properties is less clear. The study of myosin ATPase presupposed that it was correlated with contractile velocity. We could find no clear relationship between myosin ATPase activity and contractile velocity for the few species for which measurements of both parameters at habitat temperatures are available (Altringham and Johnston 1982, 1985, 1986; John- ston and Sidell 1984; Johnston and Brill 1984; Sidell and Johnston 1985; Johnston et al. 1985). However, the lack of correlation may reflect the fact that contractile velocities are expressed for isolated skinned fibers while myosin ATPase is generally measured in isolated myofibrils. Furthermore, the data are taken from separate studies. Nonetheless, in goldfish fin muscle, cold acclimation increased myosin ATPase activity and decreased the time to maximal isometric contraction (Heap et al. 1987), suggesting that these parameters are correlated.

Response of myosin ATPase activity to thermal acclimation In some species, acclimation to low temperatures leads to

compensatory changes in the activity of myosin ATPase, while in others no changes are noted. For goldfish, cold acclimation leads to positive thermal compensation of myofibrillar myosin ATPase activity (Johnston et al. 1975; Johnston 1979; Sidell 1980; Penney and Goldspink 1979; Goldspink 1985; Heap et al. 1987). In goldfish axial muscle, the changes in thermo- dynamic activation parameters during cold acclimation were due to changes in the calcium regulatory proteins, troponin and tropomyosin (Johnston 1979). For common carp, C. carpio, cold acclimation did not increase myosin ATPase activity but increased the "economy" of contraction (i.e., (force x time)/ATP hydrolyzed) (Altringham and Johnston 1985). By contrast, for mummichog (Fundulus heteroclitus), chain pickerel, and striped bass, no thermal compensation was observed (Sidell et al. 1983; Sidell and Johnston 1985; Moerland and Sidell 1986b). Thus, thermal compensation of myosin ATPase activity seems to be used only by certain spe- cies during cold acclimation.

In summary, during evolutionary adaptation to low tempera- ture, organisms have adjusted the properties of the contractile proteins to increase their locomotor capacities at low tempera- tures. The higher myosin ATPase activity in species from cold habitats may partially explain the thermal compensation of the contractile properties of these species. Acclimation to low tem- perature leads to an increase in myosin ATPase activity for goldfish (a warm-water eurytherm) (Sidell 1980; Heap et al. 1987; Goldspink 1985) and to thermal compensation of maxi- mal velocity and maximal isometric tension in muscle from common carp (C. carpio) and goldfish (Altringham and

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TABLE 2. Percentage of red fibers after thermal acclimation

Cold acclimated Warm acclimated Source

Goldfish 4.0k0.23 3.3 10.30 Johnston and Lucking 1978 Goldfish 26 14 Siddell 1980 Striped bass 15.03 k0.72 9.03 10.68 Jones and Side11 1982 Threespine sticklebacka 5 . 0 1 1.0 3.010.4 D. Vezina and H. Guderley, in preparation Lake whitefish 3 .81 1.6 4.8k1.9 Blier 1987

"Percent weight of the pectoral muscle over the weight of the carcass without viscera.

Johnston 1985; Johnston et al. 1985; Heap et al. 1987). By fibers (Jones and Sidell 1982). contrast, thermal acclimation does not change the myosin The strategy of increasing the proportion of red muscle ATPase activity or the contractile properties of muscle from during acclimation to low temperature is more common than several mesothermal species (Sidell et al. 1983; Sidell and that of altering the contractile properties of the swimming Johnston 1985; Moerland and Sidell 1986a, 1986b; Johnston musculature. This may well reflect the structural constraints and Wokoma 1986). placed upon the contractile apparatus. Does the choice of

increasing red fibers reflect a lower energetic cost or limited Fiber type proportions genetic Ilexibility? Cyprinus carpio, the only species currently

Because decreasing temperature decreases the activity of change its propenies with myosin ATPase and the contractile velocity and the power out- is tetraploid (Buth 1984). The doubling of the put of isolated muscle fibers, a fish swimming at low tempera- genome may well provide increased genetic flexibility. A simi- ture has a decreased contractile capacity with which to move lar argument has been used to tetra~lOid itself through more viscous water. To attain equivalent speeds species resort to qualitative changes of their metabolic com- at low and high temperatures, the fish must recruit more fibers POnents during temperature (Somero 1975). at low temperatures. Fish are forced to start recruiting white fibers at lower swimming speeds when swimming in cold than in warm water (Rome et al. 1984). Because increased use of white fibers increases the risk of mortality (Priede 1985), fish desiring to maintain their locomotor capacities at low tempera- tures would benefit from compensatory mechanisms increasing their capacity for sustained swimming. Compensation could take the form of alterations of the contractile properties of red fibers, which would increase their potential for functioning at low temperatures. As outlined above, certain Cyprinidae show such compensatory changes in the properties o f individual fibers. Alternatively, compensation could take a quantitative route, increasing the proportion of red fibers present in the swimming musculature. Such an increase with acclimation to low temperatures has been shown for several eurythermal and mesothermal fish, i.e., goldfish (Smit et al. 1974; Johnston and Lucking 1978; Sidell 1980; Heap et al. 1987), striped bass (Jones and Sidell 1982), and threespine stickleback (Gastero- steus aculeatus) (D. Vkzina and H. Guderley , in preparation) (Table 2). By contrast, lake whitefish (Coregonus clupea- formis), a northern species that, while described as steno- thermal, encounters a wide range of temperatures in its natural habitat, does not change the proportion of red fibers in the knial musculature with long-term cold acclimation (Blier 1987).

Cold acclimation significantly increases the speed at which common carp first recruit white muscle while swimming at low temperatures (Rome et al. 1985). Presumably this is caused by compensatory increases in the aerobic capacity of red muscle as well as in the proportion of red muscle in the axial muscula- ture. Interestingly, as cold-acclimated fish cannot sustain higher speeds than warm-acclimated fish while swimming at warm temperatures, the generation of aerobic power at high temperatures does not seem limited by the available red muscle. For striped bass, cold acclimation increases the speed at which white fibers are first recruited at both low and inter- mediate temperatures (Sisson and Sidell 1987), most likely as a result of a compensatory increase in the proportion of red

Thermal sensitivity of enzymatic reactions For muscle to function as an effective unit, temperature

effects on contractile function should be matched to tempera- ture effects on the metabolic apparatus that supplies ATP. The effect of temperature on metabolic reactions has been well studied and several thorough reviews are available (Hazel and Prosser 1974; Hochachka and Somero 1984). For individual enzymatic reactions, increases in temperature generally increase Km values, although the rate of change is generally low within the range of temperatures frequently encountered by the organism. If substrate concentrations remain constant at different temperatures, thermal effects on Km would offset the kinetic effects of an increase in temperature. However, changes in environmental temperature can change metabolite concentrations. In the case of lactate dehydrogenase, a con- stant ratio of the concentration of pyruvate to the apparent Km for pyruvate is maintained at different temperatures (Walsh and Somero 1982). The constancy of this ratio probably reflects the need to maintain a constant regulatory responsive- ness. Alphastat regulation of the ionization status of histidine groups important in substrate binding by dehydrogenases may minimize the variation of Km with temperature (Somero 1981; Hochachka and Somero 1984). For organisms exposed to a wide range of environmental temperatures, the enzymes show a reduced thermal dependence of the Km and thermal optima that reflect those of the species. The molecular mechanisms that could explain these changes in kinetic parameters are out- lined in Somero and Low (1 977). Finally, homeoviscous adap- tation leads to a maintenance of membrane fluidity which seems instrumental ifi conserving the activity 'of membrane enzymes over a wide range of temperature (Cossins and Prosser 1978). In general, organisms exposed to a wide range of temperatures have enzymes that maintain their functionality over a wider thermal range than those from organisms that are exposed to a small range of temperatures (Hochachka and Somero 1984). Thus, the evidence for long-term thermal adaptation of enzyme function is strong.

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TABLE 3. Effect of thermal acclimation on the levels of mitochondrial enzymes and proteins in red muscle, axial muscle, and pec- toral muscle in different teleosts

Enzyme or protein Species Enzyme activity

ratio Muscle Source

Cytochrome oxidase Goldfish Green sunfish Striped bass Flounder Chain pickerel Common carp* Lake whitefisht

Threespine stickleback$ Cytochrome c Green sunfish Succinate dehydrogenase Goldfish

Green sunfish Citrate synthase Striped bass

Chain pickerel Common carp* Lake whitefish?

Threespine stickleback$

Wilson 1973 Shaklee et al. 1977 Jones and Sidell 1982 Johnston and Wokoma 1986 Kleckner and Sidell 1985 Johnston et al. 1985 Blier 1987 Blier 1987 D. Vezina and H. Guderley , in preparation Sidell 1983 Sidell 1980 Shaklee et al. 1977 Jones and Sidell 1982 Kleckner and Sidell 1985 Johnston et al. 1985 Blier 1987 Blier 1987 D. Vkzina and H. Guderley , in preparation

NOTE: Ratios represent the enzyme activity measured at 15OC in the tissues of fish acclimated to 5 and 25°C. R. red muscle; A, axial muscle; P, pectoral muscle. Adapted from Sidell (1 983).

*Acclimation temperatures were 7 and 23°C and measurements were carried out at 15OC. 'yAcclimation temperatures were 5 and 18°C and measurements were carried out at 5OC. 3Acclimation temperatures were 5 and 22°C and measurements were carried out at 15OC.

Changes in muscle metabolism during thermal acclimation

Thermal acclimation rarely leads to qualitative changes in the forms of enzymes expressed in muscle, but frequently leads to changes in the levels of enzymes. Although cold acclimation seldom changes contractile properties and only sometimes leads to compensation of myosin ATPase activity, increases in enzyme levels occur in several species, such as green sunfish (Lepomis cyanellus R.) (Shaklee et al. 1977; Sidell 1977), chain pickerel (Kleckner and Sidell 1985; Sidell and Johnston 1985), striped bass (Jones and Sidell 1982), flounder (Johnston and Wokoma 1986), and threespine stickle- back (D. Vkzina and H. Guderley , in preparation). Given the similarity of the thermal sensitivities of myosin ATPase and metabolic enzymes, the lack of positive compensation of myosin ATPase activity suggests that compensation of the capacity for ATP generation may not be required. However, both use and generation of ATP depend on catalytic and diffu- sive processes. While the catalytic elements of ATP use and generation may be similarly affected by temperature, the diffu- sive elements may differentiate the thermal sensitivities of ATP use and generation.

The increases in enzyme activities with cold acclimation suggest that decreases in temperature reduce the capacity to generate ATP below that required by the contractile apparatus. The nature of the limitations on ATP generation should become clear upon identification of the changes occurring during thermal acclimation. Given the difficulty of measuring diffusive processes within living systems, changes in the cata- lytic elements with thermal acclimation have received most of the experimental attention. Table 3 shows the changes in activ- ity of aerobic enzymes in response to thermal acclimation in several fish species. These data indicate clearly that in numer- ous'eurythermal and mesothermal species, cold acclimation markedly increases the levels of the enzymes of oxidative metabolism. This is true when the data are expressed in terms

of activity in red muscle and of activity in the entire axial musculature. The latter phenomenon may reflect increases in the proportion of red fibers in the axial musculature (Smit et al. 1974; Johnston and Lucking 1978; Sidell 1980; Jones and Sidell 1982) as well as increases in the activity of aerobic enzymes in white or red muscle (Hazel and Prosser 1974; Van den Thillart and Modderkolk 1978; Sidell 1980). Histological studies indicate that the density of mitochondria in both red and white fibers increases during cold acclimation (Jankowski and Korn 1965; Smit et al. 1974; Johnston and Maitland 1980; Tyler and Sidell 1984). While this increase has often been assumed to compensate for a limitation in catalytic capacity at lower temepratures, Sidell (1983), Tyler and Sidell (1984), and Sidell and Hazel (1987) suggest that mitochondrial density increases with cold acclimation to counteract the effect of temperature on diffusive exchange of oxygen and metabolites between the cytoplasm and mitochondria.

In contrast to the activities of aerobic enzymes, glycolytic enzyme activities in both red and axial muscle generally decrease with acclimation to low temperature (Table 4). This contradictory behavior of the glycolytic and mitochondrial enzymes could support the hypothesis that mitochondrial con- centrations increase to compensate for diffusive limitations, while the catalytic capacity for mobilization of glucose units remains sufficient or even excessive. But the effect of cold acclimation on glycolytic enzyme levels could also reflect a greater thermal independence for the glycolytic pathway or a shift in energy source with cold acclimation. Effectively, cold acclimation can lead to an increased reliance upon lipid oxida- tion (Jones and Sidell 1982; Johnston et al. 1985). An excep- tion to the rule of a general decrease in glycolytic enzyme activities in aerobic muscles is found in G. aculeatus, for which both glycolytic and aerobic enzyme activities in the pec- toral muscle increased with cold acclimation (D. Vkzina and H. Guderley , in preparation).

In contrast to the above species, Coregonus clupeaformis

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GUDERLEY AND BLIER 11 11

TABLE 4. Effect of thermal acclimation on the activity of glycolytic enzymes in red muscle, axial muscle, white muscle, and pectoral muscle of different teleosts

Enzyme Species Enzyme activity

ratio Muscle Source

Glucose phosphate isomerase Green sunfish Phosphofructokinase Striped bass

Threespine stickleback* Lake whitefish?

Glyceraldehyde-3-phosphate dehydrogenase Green sunfish

Pyruvate kinase Green sunfish Striped bass Threespine stickleback* Lake whitefishi-

Common carp*

Lactate dehydrogenase Goldfish Green sunfish Striped bass Threespine stickleback* Lake whitefish?

Common carp*

Shaklee er al. 1977 Jones and Sidell 1982 D. VCzina and H. Guderley, in preparation Blier 1987 Blier 1987

Shaklee er al. 1977 Shaklee er al. 1977 Jones and Sidell 1982 D. VCzina and H. Guderley, in preparation Blier 1987 Blier 1987 Johnston er al. 1985 Johnston et al. 1985 Sidell 1980 Shaklee er al. 1977 Jones and Sidell 1982 D. VCzina and H. Guderley, in preparation Blier 1987 Blier 1987 Johnston er al. 1985 Johnston er al. 1985

NOTE: Ratios represent the enzyme activity measured at 15°C in the tissues of fish acclimated to 5 and 25°C. R, red muscle; A, axial muscle: W, white muscle; P, pectoral muscle. Adapted from Side11 (1 983).

*Acclimation at 5 and 22"C, measurements at 15°C. tAcclimation at 5 and 18"C, measurements at 5°C. $Acclimation at 7 and 23"C, measurements at 15°C.

show no positive thermal compensation of aerobic enzymes in the red, white, or axial musculature (Blier 1987). The acclima- tion temperatures, 5 and 18"C, are near the limits of the thermal range that this species encounters. As Ucit is maximal at 12°C (Bernatchez and Dodson 1985), the optima for the oxygen delivery system and for the contractile and metabolic machinery are probably near 12 "C. By contrast, for the studies examining goldfish, common carp, green sunfish, chain pick- erel, striped bass, and flounder, the thermal optima are near the upper acclimation temperatures. In these studies, the lower acclimation temperatures exposed these species to consider- ably greater limitations on locomotor capacity than the lower acclimation temperatuare used for C. clupeaformis. By having its thermal optimum for locomotion in the center of its thermal range, C. clupeaformis may avoid the energetic expenditures associated with metabolic rearrangement during thermal accli- mation and yet be able to exploit habitats ranging from 2 to 20°C. One could argue that given the harshness of northern habitats, any nlechanisms that decrease the energetic costs would be of selective advantage. However, Bernatchez and Dodson (1985) show that whitefish do not optimize their swimming speeds during the estuarine portion of their upstream migration in the Eastmain River. Their continued feeding during this period, as well as a possible requirement for a period at relatively high temperatures for gamete matura- tion (Dodson et al. 1986), could explain this apparently non- optimal behavior.

what are the limits to the eurythermality of a given metabolic design?

temperature is likely viable only within certain limits, and these may well reflect the limits of the eurythermality of a given metabolic design. The systematic study of organisms from habitats with differing degrees of thermal variation should demonstrate what these limits are. The literature pro- vides a few hints. Somero et al. (1968) found that Trematomus bernacchii had a reduced capacity to acclimate to "warm" temperatures (4°C for this antarctic species). The thermal range experienced by this fish is no greater than 7 "C. A lack of thermal compensation is shown by some of the respiratory enzymes of Drosophila pseudoobscura, D. willistonii, and D. melanogaster (Hazel and Prosser 1974). This could reflect a limited capacity for thermal acclimation in tropical species. Braun et al. (1970) found negative or no thermal compensation for numerous glycolytic, Krebs cycle, and gluconeogenic enzymes in the bitterling (Rhodeus amarus) of central and southern Europe after acclimation to 10 and 20°C. However, as the Krebs cycle enzymes in bitterling muscle showed both positive and negative compensation, interpretation of these data in terms of the thermal variation in the species' habitat is difficult. Our enzymatic profile of swimming muscle in C. clupeaformis suggests that a thermal range of 13 "C can easily be covered by a given metabolic design, particularly if the organism's preferred temperature is in the center of such a range. Whether a given design for muscle metabolism can be fexnctional over a larger range of temperatures remains to be seen.

Another high temperate zone species, the threespine stickle- back (G. aculeatus), provides additional insight into this ques- tion. In North America, G. aculeatus shares the geographic distribution of C. clupeaformis, i.e., both species extend to the

The response of C. clupeaformis to changing acclimation north of Hudson ~ a y ( ~ o o t t o n 1976). AS-sticklebacks spend

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1112 CAN. 1. ZOOL. VOL. 66, 1988

considerable time in shallow pools in which they reproduce, they are exposed to considerably greater thermal variations than C. clupeaformis, which are limited to bays and rivers. Effectively, these pools can fluctuate in a single day between 5 and 30°C (FitzGerald 1983; Reebs et al. 1984). In summariz- ing data from European and North American G. aculeatus, Elliott (1981) indicates that the thermal optimum extends from 4 to 20°C, while the optimum for egg development is from 4 to 28°C (Fig. I). Its optimum range is thus twice that of the Coregonines, for which Elliott (198 1) indicates a thermal opti- mum between 7.5 and 15 "C. Six weeks acclimation of G. acu- leatus (f. trachurus) to 4 and 22°C led to significant thermal compensation for phosphofructokinase, pyruvate kinase, lac- tate dehydrogenase, citrate synthase, and cytochrome oxidase in the pectoral muscles (Table 3) (D. Vkzina and H. Guderley , in preparation), which this species uses for its sustained swim- ming (Taylor and McPhail 1986). Although the acclimation temperatures that we used were both near the thermal opti-

BROWN TROUT COD

MAX f ={::: SWIMMING

STANDARD

STANDAFfD STANDARD

FIG. 2. Estimates of power capacities for brown trout, Salmo trutta, and cod, Gadus morhua. The thickness of the arrows is proportional to the power capacity in mW. SDA, specific dynamic action. (Modi- fied after Priede 1985.)

mum, the marked positive compensation obtained suggests sustained swimming at high temperatures, maintenance of sus- that this range of temperatures (18°C) is too great to be tained swimming capacity during acclimation to. low tempera- covered on a long-term basis by one enzymatic profile. A simi- tures requires compensation of the aerobic capacity of their lar conclusion is indicated by the studies with goldfish, striped swimming musculature, be it an increase in the quantity of red bass, chain pickerel, green sunfish, and crucian carp in which muscle or an increase in the density of mitochondria. the acclimation temperatures Were approximately 20°C apart Faced with a decrease in both temperature and aerobic (Shaklee et al. 1977; Johnston and Maitland 1980; Side11 scope, fish make trade-offs in which certain functions are 1980; Jones and Side11 1982; Kleckner and Side11 1985). diminished while others are maintained. Differences in these

Catalytic limitation versus diffusive limitation of metabolic eurythermality

At what level are the limits to eurythermality of metabolic function expressed? Data for individual enzymes such as lac- tate dehydrogenase from the longjaw mudsucker (Gillichthys mirabilis) suggest that K, variations are minimized between 10 and 30°C (Somero 1981). The responses of more cata- lytically complex, flux-generating enzymes may be more tem- perature dependent. However, the limits to metabolic eurythermality may well lie on another level. As decreases in temperature increase the solubility of oxygen in water, a fish exposed to cold water has the potential for extracting more oxygen. However, for most species, aerobic scope shows a distinct thermal optimum, below which decreases in tempera- ture diminish the aerobic capacity. This decreased aerobic capacity could reflect increased cost of ventilation in a more viscous medium, a decreased branchial capacity for oxygen extraction, as well as reduced rates of diffusive exchange between the mitochondria and the capillaries. Thus, despite the increased availability of oxygen in the environment, the avail- ability of oxygen to the mitochondrion can decrease with drop- ping temperature. Given that the contractile activity of red muscle is supported by aerobic degradation of carbohydrates and lipids, it is sensitive to oxygen availability. Once again, the level at which thermal compensation occurs should identify the general nature of the thermal limitation. Increases in the proportion of red fibers at low temperatures suggest that the cardiovascular transport capacity supports more aerobic muscle at low than at high temperatures. This is supported by data indicating that cold-acclimated common carp (C. carpio) cannot extend their sustained swimming speeds at warm tem- peratures beyond those of warm-acclimated carp (Rome et al. 1985). Short-term decreases in temperature apparently do not reduce the cardiovascular delivery of oxygen and substrate to muscle as much as they reduce the capacity of muscle to use oxygen and substrate. Thus, for fish with their optimum for

temperature-dependent compromises could affect the strategies of thermal acclimation. An interesting example is given in Fig. 2, adapted from Priede (1985), in which the effect of tem- perature on the power capacities of brown trout (Salmo trutta) and cod is compared. Cod reach their maximum oxygen con- sumption through the increase in metabolic rate brought about by digestion ("specific dynamic action" or SDA), while trout reach their maximum through increases in locomotion. A decrease in temperature leads to a similar reduction in the power capacities for SDA and swimming in cod, while trout markedly decrease the power capacity associated with SDA and conserve a greater proportion of the power associated with swimming. Effectively, trout switch off digestion to maintain a greater locomotor capacity at low temperatures. Thus, differ- ent species of fish use radically different strategies in their par- titioning of oxygen at different temperatures. Priede (1985) suggests that the cod strategy should typify fish with little red muscle. For these fish, sustained swimming would be of minor importance. By contrast, the trout strategy would typify fish that conserve their locomotor capacities at low temperatures and that would benefit from compensatory responses in their swimming muscle during acclimation to low temperatures.

Although our review of these studies indicates that certain underlying rules may direct the capacities of fish to acclimate to low temperatures, a careful analysis of the literature indi- cates that the strategies of thermal acclimation may be markedly species-specific. In goldfish and common carp, thermal compensation of locomotor performance involves bio- chemical changes on several levels. Cold acclimation increases myosin ATPase activity, changes the contractile properties of isolated fibers, increases the proportion of red fibers in the swimming musculature, increases the levels of mitochondrial enzymes and mitochondrial density in red and white fibers, and decreases the levels of glycolytic enzymes in red and white fibers. By contrast, for striped bass cold acclimation does not increase myosin ATPase activities, does not change the con- tractile properties of red and white fibers, increases the propor-

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GUDERLEY AND BLIER 1113

tion of red fibers in the axial musculature, increases the aerobic capacity of red fibers, and increases the reliance of red muscle upon lipids. Similarly, for chain pickerel and flounder, cold acclimation does not change the contractile properties but increases the levels of mitochondria1 enzymes in the swimming musculature. Finally, whitefish do not change their metabolic organization or their proportion of red fibers in the swimming musculature with cold acclimation. While one could propose that goldfish and common carp have uniquely high capacities for compensatory changes during thermal acclimation because they are tetraploid, whitefish are tetraploid as well (Buth 1984; Allendorf and Thorgaard 1984). The thermal characteristics of the species' habitat as well as the thermal sensitivities of its locomotor and feeding strategies are most likely much more important than genome size in determining the nature of the compensatory mechanisms used by fish during thermal accli- mation.

Examination of the compensatory responses of these species indicates that the relationship between the thermal optimum for locomotion and the breadth of a species' thermal tolerance limits may well predict the extent of their compensatory responses. The champion compensators, common carp and goldfish, have wide thermal tolerance limits and their thermal optimum for locomotion is towards the upper end of their pre- ferred temperatures. Furthermore, their range of optimal tem- peratures is approximately 17°C (Fig. 1). By contrast, the mesotherms, such as striped bass, chain pickerel, and flounder, generally have narrower thermal tolerance limits and their thermal preferenda are lower than those of carp and gold- fish (Coutant 1977). The optimum temperature for sustained swimming of lake whitefish is in the middle of their rather limited range of tolerated temperatures. If a species has its optimum for locomotion at a high temperature within a broad range of tolerated temperatures, decreasing temperatures will markedly restrict its locomotory capacity. If conservation of locomotory capacity at low temperatures is important for the species, compensation of the metabolic and contractile com- ponents of muscle will be of considerable benefit. By contrast, for a species that has its optimum for locomotion centrally positioned within its range of tolerated temperatures, exposure to low temperatures would not decrease its locomotory capa- city as markedly. Thus, compensation would be of less selec- tive importance. While the width of a species' thermal optimum may be the best indication of the thermal indepen- dence of its metabolic processes, the size of its tolerance limits in relation to the position of the thermal optima of its physio- logical processes may be a better indicator of its capacity for thermal compensation.

ALEXANDER, R. McN. 1969. The orientation of muscle fibres in the myomeres of fishes. J. Mar. Biol. Ass. U.K. 49: 263 -290.

ALLENDORF, F. W., and THORGAARD, G. H. 1984. Tetraploidy and the evolution of salmonid fishes. In Evolutionary genetics of fishes. Edited b y B. J. Turner. Plenum Press, New York. pp. 1-53.

ALTRINGHAM, J. D., and JOHNSTON, I. A. 1982. The pCa-tension and force velocity characteristics of skinned fibres isolated from fish fast and slow muscles. J. Physiol. 333: 42 1 -449.

1985. Changes in tension generation and ATPase activity in skinned muscle fibres of the carp following temperature acclima- tion. Pfliigers Arch. 403: 449 -45 1.

1986. Energy cost of contraction in fast and slow muscle fibres isolated from an elasmobranch and an antarctic teleost fish. J. Exp. Biol. 121: 239-250.

BARANY, M. 1967. The ATPase activity of myosin correlated with

speed of muscle shortening. J. Gen. Physiol. 50: 197 -218. BEAMISH, F. W. H. 1966. Swimming endurance of some Northwest

Atlantic fishes. J. Fish Res. Board. Can. 23: 341 -347. 1970. Oxygen consumption of largemouth bass, Micropterus

salmoides, in relation to swimming speed and temperature. Can. J. Zool. 48: 1221 - 1228.

1978. Swimming capacity. In Fish physiology. Vol. 7. Edited b y W. S. Hoar and D. J. Randall. Academic Press, New York. pp. 101 - 187.

1981. Swimming performance and metabolic rate of three tropical fishes in relation to temperature. Hydrobiologia, 83: 245 - 254.

BENNETT, A. F. 1985. Temperature and muscle. J. Exp. Biol. 115: 333 -344.

BERNATCHEZ, L., and DODSON, J. J. 1985. The influence of tempera- ture and current speed on the swimming capacity of the-lake whitefish (Coregonus clupeaformis) and cisco (C. artedii) . Can. J . Fish. Aquat. Sci. 42: 1522-1529.

BL~ER, P. 1987. Reponse metabolique et structurale du muscle axial du grand coregone h une acclimatation h basse temperature. Memoire de maitrise, Universitk Laval.

BONE, Q. 1966. On the function of the two types of myotomal muscle fibre in elasmobranch fish. J. Mar. Biol. Assoc. U.K. 46: 321 -349.

BONE, Q., KICENIUK, J., and JONES, D. R. 1978. On the role of different fiber types in fish myotomes at intermediate swimming speeds. Fish. Bull. 76: 691 -699.

BRAUN, K., K ~ ~ N N E M A N N , H., and LAUDIEN, H. 1970. Der EinfluR von Temperatureanderungen auf Enzyme der Fischmuskulatur. Versuche mit Rhodeus arnarus. Mar. Biol. (Berlin), 7: 59-70.

BRETT, J. R. 1964. The respiratory metabolism and swimming per- formance of young sockeye salmon. J. Fish. Res. Board Can. 21: 1183- 1226.

1967. Swimming performance of sockeye salmon in relation to fatigue time and temperature. J. Fish. Res. Board Can. 24: 1731 - 1741.

1970. Fishes. In Marine ecology. Vol . 1 . Environmental fac- tors. Edited b y 0 . Kinne. John Wiley and Sons, New York. pp. 5 13 -560.

BRETT, J. R., and GROVES, T. D. D. 1979. Physiological energetics. In Fish physiology. Vol. 8. Bioenergetics and growth. Edited b y W. S. Hoar and D. J. Randall. Academic Press, New York. pp. 279 - 352.

BUTH, D. G. 1984. Allozymes of the cyprinid fishes. In Evolutionary genetics of fish. Edited b y B. J. Turner. Plenum Press, New York. pp. 561 -590.

COSSINS, A. R., and PROSSER, C. L. 1978. Evolutionary adaptation of membranes to temperature. Proc. Natl. Acad. U.S.A. 75: 2040 - 2043.

COUTANT, C. C. 1977. Compilation of temperature preference data. J. Fish. Res. Board Can. 34: 739 -745.

DODSON, J. J., LAMBERT, Y., and BERNATCHEZ, L. 1986. Compara- tive migratory and reproductive strategies of the sympatric anadro- mous coregonine species of James Bay. In Migration: mechanisms and adaptive significance. Edited b y M. A. Rankin. Contrib. Mar. Sci. Suppl. No. 27. pp. 296-315.

DUTHIE, G. 1981. The respiratory metabolism of temperature adapted flatfish at rest and during swimming activity and the use of anaerobic metabolism at moderate swimming speeds. J. Exp. Biol. 97: 359-373.

ELLIOTT, J. M. 198 1. Some aspects of thermal stress on freshwater teleosts. In Stress and fish. Edited b y A. D. Pickering. Academic Press, London. pp. 209 - 245.

FITZGERALD, G. J. 1983. The reproductive ecology and behaviour of three sympatric sticklebacks (Gasterosteidae) in a saltmarsh. Biol. Behav. 8: 67 -79.

FREADMAN, M. A. 1979. Role partitioning of swimming musculature of striped bass, Morone saxatilis Walbaum and bluefish, Poma- tomus saltatrix L. J. Fish Biol. 15: 417 -423.

FRY, F. E. J., and HART, J. S. 1948. Cruising speed of goldfish in

Can.

J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.c

om b

y U

nive

rsité

du

Qué

bec

à Ri

mou

ski o

n 11

/04/

13Fo

r per

sona

l use

onl

y.

1114 CAN. J . ZOOL. VOL. 66. 1988

relation to water temperature. J. Fish. Res. Board Can. 7: 169- 175.

FRY, F. E. J., and HOCHACHKA, P. W. 1970. Fish. In Comparative physiology of thermoregulation. Vol. 1. Invertebrates and non- mammalian vertebrates. Edited by G. Causey Whittow. Academic Press, New York. pp. 79- 134.

GIBSON, E. S., and FRY, F. E. J. 1954. The performance of the lake trout, Salvelinus namaycush, at various levels of temperature and oxygen pressure. Can. J. Zool. 32: 252 -260.

GOLDSPINK, G. 1985. Malleability of the motor system: a compara- tive approach. J. Exp. Biol. 115: 375 - 39 1.

GRAVES, J. E., and SOMERO, G. N. 1982. Electrophoretic and func- tional enzymic evolution in four species of eastern Pacific Barra- cudas from different thermal environments. Evolution (Lawrence, Kans .), 36: 97 - 106.

GRIFFITHS, J. S., and ALDERDICE, D. F. 1972. Effects of acclimation and acute temperature experience on the swimming speed of juvenile coho salmon. J. Fish. Res. Board Can. 29: 25 1 -264.

HAZEL, J. R., and PROSSER, C. L. 1974. Molecular mechanisms of temperature compensation in poikilotherms. Physiol. Rev. 54: 620-677,

HEAP, S. P., and GOLDSPINK, G. 1986. Alterations to the swimming performance of carp, Cyprinus carpio, as a result of temperature acclimation. J. Fish Biol. 29: 747 - 753.

HEAP, S. P, WATT, P. W., and GOLDSPINK, G. 1987. Contractile pro- perties of goldfish fin muscles following temperature acclimation. J. Comp. Physiol. B, 157: 219-225.

HOCHACHKA, P. W., and SOMERO, G. N. 1973. Strategies of bio- chemical adaptation. W. B. Saunders Co., Philadelphia, PA.

1984. Biochemical adaptation. Princeton University Press, Princeton, NJ.

HOCUTT, C. H. 1973. Swimming performance of three warm water fishes exposed to a rapid temperature change. Chesapeake Sci. 14: 11-16.

JANKOWSKI, H. D., and KORN, H. 1965. The influence of tempera- ture on the mitochondria1 content of fish muscle. Naturwissen- schaften, 52: 642.

JOHNSTON, I. A. 1979. Calcium regulatory proteins and temperature acclimation of actomyosin from a eurythermal teleost (Carassius auratus). J. Comp. Physiol. B. 129: 163 - 167.

1982. Biochemistry of myosins and contractile properties of fish skeletal muscle. Mol. Physiol. 2: 15 -29.

JOHNSTON, I. A., and BRILL, R. 1984. Thermal dependence of con- tractile properties of single skinned muscle fibres from Antarctic and various warm water marine fishes including skipjack tuna (Kat- suwonus pelamis) and Kawakawa (Euthynnus aflnis). J. Comp. Physiol. B, 155: 63 -70.

JOHNSTON, I. A., and GOLDSPINK, G. 1975. Thermodynamic activa- tion parameters of fish myofibrillar ATPase enzyme and evolution- ary adaptations to temperature. Nature (London), 257: 620-622.

JOHNSTON, I. A., and HARRISON, P. 1985. Contractile and metabolic characteristics of muscle fibres from Antarctic fish. J. Exp. Biol. 116: 223 -236.

JOHNSTON, 1. A., and LUCKING, M. 1978. Temperature induced variation in the distribution of different types of muscle fibre in the goldfish (Carassius auratus). J. Comp. Physiol. B, 124: 111-116.

JOHNSTON, I. A., and MAITLAND, B. 1980. Temperature acclimation in crucian carp, Carassius carassius L.; morphometric analysis of muscle fibre u;trastructure. J. Fish Biol. 17: 1 13 - 125.

JOHNSTON, I. A., and SALAMONSKI, J. 1984. Power output and force-velocity relationship of red and white muscle fibres from the Pacific blue marlin (Makaira nigricans). J. Exp. Biol. 111: 171 - 177.

JOHNSTON, I. A., and SIDELL, B. D. 1984. Differences in tempera- ture dependence of muscle contractile properties and myofibrillar ATPase activity in a cold-temperate fish. J. Exp. Biol. 111: 179- 189.

JOHNSTON, I. A., and WALESBY, N. J. 1977. Molecular mechanisms

of temperature adaptation in fish myofibrillar adenosine triphospha- tases. J. Comp. Physiol. B, 119: 195 -206.

1979. Evolutionary temperature adaptation and the calcium regulation of fish actomyosin ATPase. J. Comp. Physiol. B, 129: 169- 177.

JOHNSTON, I . A., and WOKOMA, A. 1986. Effects of temperature and thermal acclimation on contractile properties and metabolism of skeletal muscle in the flounder (Platichthysflesus L.) . J. Exp. Biol . 120: 1 19 - 130.

JOHNS~~ON, I . A., FREARSON, N., and GOLDSPINK, G. 1973. The effects of environmental temperature on the properties of myofibril- lar adenosine triphosphatase from various species of fish. Biochem. J. 133: 735-738.

JOHNSTON, I. A., DAVISON, W., and GOLDSPINK, G. 1975. Adapta- tion in Mg2+ activated myofibrillar ATPase activity induced by temperature. FEBS Lett. 50: 293 - 295.

JOHNSTON, I . A., WALESBY, N. J., DAVISON, W., and GOLDSPINK, G. 1977. Further studies on the adaptation of fish myofibrillar ATPase to different cell temperatures. Pfliigers Arch. Gesamte Physiol. Menschen Tiere, 371 : 257 -262.

JOHNSTON, I. A., SIDELL, B. D., and DRIEDZIC, W. R. 1985. Force-velocity characteristics and metabolism of carp muscle fibres following temperature acclimation. J. Exp. Biol. 119: 239-249.

JONES, D. R., KICENIUK, J., and BAMFORD, 0. S. 1974. Evaluation of swimming performance of several fish species from the Mackenzie River. J. Fish. Res. Board Can. 31: 164 1 - 1647.

JONES, P. L., and SIDELL, B. D. 1982. Metabolic responses of striped bass (Morone suxatilis) to temperature acclimation. TI. Alterations in metabolic carbon sources and distributions of fiber types in loco- motory muscle. J. Exp. Zool. 219: 163 - 171.

JOSEPHSON, R. K. 1983. Temperature and the' mechanical perform- ance of insect muscle. In Insect thermoregulation. Edited by B. Heinrich. John Wiley and Sons, New York. pp. 20-44.

KLECKNER, N. W., and SIDELL, B. D. 1985. Comparison of maximal activities of enzymes from tissues of thermally acclimated and naturally acclimatized chain pickerel (Esox niger). Physiol . Zool . 58: 18-28.

LARIMORE, R. W., and DENEVER, M. J. 1968. Effect of temperature acclimation on the swimming ability of smallmouth bass fry. Trans. Am. Fish. Soc. 97: 175 - 184.

MAGNUSON, J. J., CROWDER, L. B., and MEDVICK, P. A. 1979. Temperature as an ecological resource. Am. Zool. 19: 334 -34.3.

MOERLAND, T. S., and SIDELL, B. D. 1986a. Biochemical responses to temperature in the contractile protein complex of striped bass, Morone suxatilis. J. Exp. Zool. 238: 287 -295.

19866. Contractile responses to temperature in the loco- motory musculature of striped bass Morone suxatilis. J. Exp. Zool. 240: 25 - 33.

PENNEY, R. K. , and GOLDSPINK, G. 1979. Compensation limits of fish muscle myofibrillar ATPase enzyme to environmental tem- perature. J. Therm. Biol. 4: 269 -272.

PRIEDE, I. G. 1977. Natural selection for energetic efficiency and relationship between activity level and mortality. Nature (London), 267: 610-61 1.

1985. Metabolic scope in fishes. In Fish energetics. Edited by P. Tytler and P. Calow. Croon Helm, London. pp. 33-64.

REEBS, S. G., WHORISKEY, F. G., JR., and FITZGERALD, G. J. 1984. Die1 patterns of fanning activity, egg respiration, and the nocturnal behavior of male three-spined sticklebacks, Gasterosteus aculeatus L. (f. trachurus). Can. J. 2001. 62: 329-334.

REYNOLDS, W. W., and CASTERLIN, M. E. 1980. 'The role of tem- perature in the environmental physiology of fishes. In Environ- mental physiology of fishes. Edited by M. A. Ali. Plenum Press, New York. pp. 497-518.

ROME, L. C., LOUGHNA, P. T., and GOLDSPINK, G. 1984. Muscle fiber activity in carp as a function of swimming speed and muscle temperature. Am. J. Physiol. 247: R272 - R279.

1985. Temperature acclimation: improved sustained swim-

Can.

J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.c

om b

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GUDERLEY AND BLIER 11 15

ming performance in carp at low temperatures. Science (Washing- ton, D.C.) 228: 194- 196.

RULIFSON, R. A. 1977. Temperature and water velocity effects on the swimming performance of young of the year striped mullet, spot and pinfish. J. Fish. Res. Board Can. 34: 2316-2322.

SHAKLEE, J. B., CHRISTIANSEN, J. A., SIDELL, B. D., PROSSER, C. L., and WHITT, G. S. 1977. Molecular aspects of temperature acclimation in fish: contributions of changes in enzyme activities and isozyme patterns to metabolic reorganization in the green sun- fish. J. Exp. Zool. 201: 1-20.

SIDELL, B. D. 1977. Turnover of cytochrome c in skeletal muscle of green sunfish (Lepomis cyanellus R.) during thermal acclimation. J. Exp. Zool. 199: 233-250.

1980. Responses of goldfish (Carassius auratus L.) muscle to acclimation temperature: alterations in biochemistry and propor- tions of different fiber types. Physiol. Zool. 53: 98 - 107.

1983. Cellular acclimatization to environmental change by quantitative alterations in enzymes and organelles. In Cellular acclimatization to environmental change. Edited by A. R. Cossins and P. Sheterline. Symp. Soc. Exp. Biol. No. 17. pp. 103- 120.

SIDELL, B. D., and HAZEL, J. R. 1987. Temperature affects the diffu- sion of small molecules through cytosol of fish muscle. J. Exp. Biol. 129: 191 -203.

SIDELL, B. D., and JOHNSTON, I. A. 1985. Thermal sensitivity of contractile function in chain pickerel, Exos niger. Can. J. Zool. 63: 81 1-816.

SIDELL, B. D., JOHNSTON, I. A., MOERLAND, T. S., and GOLDSPINK, G. 1983. The eurythermal myofibrillar protein complex of the mummichog (Fundulus heteroclitus) adaptation to a fluctuating thermal environment. J. Comp. Physiol. B, 153: 167 - 173.

SISSON, J. E., and SIDELL, B. D. 1987. Effect of thermal acclimation on muscle fiber recruitment of swimming striped bass (Morone saxatilis). Physiol. Zool. 60: 310-320.

SMIT, H., V A N DEN BERG, R. J., and KIJNE-DEN HARTOG, I. 1974. Some experiments on thermal acclimation in the goldfish (Caras- sius auratus L.). Neth. J. Zool. 24: 32 -49.

SOMERO, G. N. 1975. The role of isozymes in adaptation to varying temperatures. In Isozymes. 11. Physiological function. Edited by C. L. Markert. Academic Press, New York. pp. 221 -234.

198 1. pH - temperature interactions on proteins: principles of optimal pH and buffer system design. Mar. Biol. Lett. 2: 168- 178.

SOMERO, G. N., and Low, P. S. 1977. Eurytolerant proteins: mechanisms for extending the environmental tolerance range of enzyme - ligand interactions. Am. Nat. 111: 527 -538.

SOMERO, G. N., GIESE, A. C. , and WOHLSCHLAG, D. E. 1968. Cold adaptation of the Antarctic fish Tremutomus bernacchii. Comp. Biochem. Physiol. B, 26: 223-233.

TAYLOR, E. B., and MCPHAIL, J. D. 1986. Prolonged and burst swimming in anadromous and freshwater threespine sticklebacks, Gasterosteus aculeatus. Can. J . Zool. 64: 4 16 -420.

TYLER, S., and SIDELL, B. D. 1984. Changes in mitochondria1 dis- tribution and diffusion distances in muscle of goldfish upon acclimation to warm and cold temperatures. J. Exp. Zool. 232: 1-9.

VAN DEN THILLART, G., and MODDERKOLK, J. 1978. The effect of acclimation temperature on the activation energies of state I11 respiration and on the unsaturation of membrane lipids of goldfish mitochondria. Biochim. Biophys. Acta, 510: 38-51.

WALSH, P. J., and SOMERO, G. N. 1982. Interactions among pyruvate concentration, pH, and K, in determining in vivo Q , , values of the lactate dehydrogenase reaction. Can. J. Zool. 60: 1293 - 1299.

WARDLE, C. S. 1980. Effects of temperature on the maximum swim- ming speed of fishes. In Environmental physiology of fishes. Edited by M. A. Ali. Plenum Press, New York. pp. 519-531.

WEBB, P. W. 1978. Hydrodynamique et knergktique de la propulsion des poissons. Bull. Off. P k h . Can. 190F.

1984. Body form, locomotion and foraging in aquatic verte- brates. Am. Zool. 24: 107- 120.

WILSON, F. R. 1973. Enzyme changes in goldfish (Carassius auratus L.) in response to temperature acclimation. Ph.D. thesis, Uni- versity of Illinois, Urbana.

WOHLSCHLAG, D. E. 1964. Respiratory metabolism and ecological characteistics of some fishes in McMurdo Sound, Antarctica. In Biology of the Antarctic seas. Edited by M. 0 . Lee. Antarct. Ser. 1: 33-62.

WOOTTON, R. J. 1976. The biology of sticklebacks. Academic Press, London.

Can.

J. Z

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Dow

nloa

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from

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