BY GARRY G. DUTHIE* Department of Zoology, University of Aberdeen, Scotland, United Kingdom. {Received 24 June 1981) SUMMARY

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1 J. exp. Biol. (1982), 97, JWith 6 figures Wrinted in Great Britain THE RESPIRATORY METABOLISM OF TEMPERATURE-ADAPTED FLATFISH AT REST AND DURING SWIMMING ACTIVITY AND THE USE OF ANAEROBIC METABOLISM AT MODERATE SWIMMING SPEEDS BY GARRY G. DUTHIE* Department of Zoology, University of Aberdeen, Scotland, United Kingdom {Received 24 June 1981) SUMMARY (1) The standard oxygen consumption and the oxygen consumption during measured swimming activity have been determined in three flatfish species at, and 1 C. (2) The relationship between weight and standard oxygen consumption for flatfish conform to the general relationship Y = aw b. On an interspecies basis, standard oxygen consumption offlatfishis significantly lower than that of roundfish. (3) A semilogarithmic model describes the relationship between oxygen consumption and swimming speed for the three species. Values for maximum oxygen consumption, metabolic scopes and critical swimming speeds are low in comparison to salmonids. (4) The optimum swimming speeds and critical swimming speeds of flatfish are similar. It is suggested that, over long distances, flatfish adopt a strategy of swimming at supercritical speeds with periods of intermittent rest to repay the accrued oxygen debt. () Elevated lactic acid levels in flounder white muscle after moderate swimming indicate an additional 1 % anaerobic contribution to the cost of locomotion as calculated from aerobic considerations. INTRODUCTION This study has examined the metabolism of three flatfish species at rest and while swimming in a tunnel respirometer, and has considered the results in terms of metabolic scopes (Fry, 1947) and energetic costs of locomotion. Except for feeding and escape, or during migration, flatfish rest on bottom substrates for prolonged periods. It is likely that there are differences in metabolic costs and swimming strategies between flatfish and more active, well studied, roundfish species. Priede & Holliday (1980) established oxygen consumption-swimming speed relationships for the flatfish plaice, Pleuronectes platessa, at three temperatures and related their results to those of sonic tracking experiments in the North Sea. (Greer- Walker, Harden-Jones & Arnold, 1978). The species used in the present study were Present address: Research Unit for Comparative Animal Respiration, University of Bristol, Road, Bristol BS8 iug, England.

2 360 G. G. DUTHIE the flounder, Platichthys flesus (L), the common dab, Limanda limanda (L) and trfl lemon sole, Microstomus kitt (Walbaum). The standard metabolism (Fry, 1947) or a wide weight range of fish exposed to constant temperatures for prolonged periods was measured. Using a narrow weight range, the effects of adaptation temperature (Alderdice, 1976) on the respiratory metabolism during swimming activity was assessed. Estimates of maximum levels of oxygen consumption (active metabolic rates), maximum sustained swimming speeds (critical swimming speeds) and metabolic costs to traverse a unit distance (Weihs, 1974; Webb, 197; Priede & Holliday, 1980) have been made and the results discussed in terms of swimming strategies flatfish may adopt. Further, the assessment of exercise capability in terms of metabolic costs assumes negligible anaerobic contribution (Jones & Randall, 1978). It was observed that the flatfish invariably showed a gradual decline in oxygen consumption subsequent to swimming at moderate speeds, suggesting that an oxygen debt was incurred. An attempt was made to assess the relative contributions of aerobic and anaerobic metabolism to the total energy expenditure during swimming in the flounder. Lactic acid production was used as an index of anaerobic energy expenditure. MATERIALS AND METHODS (1) Collection and maintenance of fish Large individuals (0-800 g) were trawled off the coast of Aberdeen, Scotland. Smaller specimens (1-0 g) were obtained by beach seine. The fish were maintained in aerated constant temperature tanks for two months prior to experimentation to ensure thermal adaptation. All three species were maintained at ± 0-2 and 1 + c-2 C. In addition, a C regime was introduced for dabs and lemon sole. The fish were fed daily to satiation and starved for 48 hours prior to metabolic determinations. A 12 h L:D photoperiod was maintained. (2) Measurement of oxygen consumption Two types of respirometer were used. That for measuring standard oxygen consumption consisted of a closed system with a flush capacity. Three sizes of perspex boxes were used as respiration chambers, total volumes being 12-4, 7-1, and 0-1. This allowed the use of a wide weight range of fish. A full description of the apparatus and experimental procedures used can be found in Duthie (1980). The respirometer used in the swimming trials is described in Priede & Holliday (1980). It is essentially a Brett-type respirometer mounted on gimballs so that the whole apparatus can be tilted at from the horizontal. Tilting the respirometer overcomes the flatfishes' rheotactic behaviour to a water current (Arnold, 1969). The volume of the respirometer was The fish were left overnight in the respirometer in a flow of cm/s before the first swimming trials were conducted. The water velocity was then increased and the tunnel tilted ( from horizontal) until swimming began. In the assessment of fish swimming performance the usual technique involves stepwise increases in water velocity. It was found that a uniformly swimming flatfish became disorientated if speed was changed. After each run, the water flow was reduced and the fish

3 Respiratory metabolism of temperature-adapted flatfish Flounders e o Live weight (g) Lemon sole 0 Live weight (g) 00 0 Live weight (g) Fig. 1. The relationship between standard oxygen consumption and body weight for the three species of flatfish at various adaptation temperatures. O = S C, = C, # = 1 C. 00 to settle on the bottom of the chamber. Swimming was reinduced after 2 h at a higher test velocity (8 cm s -1 increases). Each discrete run lasted 30 min. Critical swimming speeds were taken as the maximum speeds that could be sustained over a 30 min period. The oxygen consumption at these speeds were used as estimates of active metabolic rates. (3) Determination of lactic acid Immediately on termination of a swimming trial the fish was removed from the respirometer and killed by a blow to the head. Muscle blocks (0- g) were cut from the eyed surface and frozen in liquid nitrogen. 0- ml of blood were sampled via the caudal vein and precipitated in chilled 08 N perchloric acid. Lactic acid in muscle and blood was analysed using the procedures of Horhorst (1963) and Wardle (1978). Controls were resting flounders which had been undisturbed for 2 days. RESULTS (1) Standard oxygen consumption - weight relationships i In Fig. 1, standard oxygen consumption values determined at various adaptation temperatures are plotted against body weight for the three flatfish species. Regression

4 362 G. G. DUTHIE Table 1. Standard oxygen consumption (Y) in relation to weight (W) at different adaptation temperatures for the threeflatfishspecies (The weight range of each population can be seen from Fig. 1. Y is mg O 2 h" 1 and W is g.) Species Platichthys flesus Limanda limanda Microstomus kitt Adaptation temperature ( C) IS IS IO IS Regressions log Y = 0827 log W log Y = log W log Y = log W log y = log w log y = 0634 log w log y = 0680 log W-0-97 log y = log w 0804 log y = 0783 log PF r values Level of significance P < o-oo 1 P < o-ooi P < o-ooi P < o-ooi P < o-ooi P < o-oor P < o-ooi P < o-ooi Table 2. Mea«lengths and weights (± S.E.) 0/ thefishused in the swimming respirometry experiments (Each group consists of 4 individuals except for C dabs where only one individual was used. All fish were adapted to their respective temperatures for at least 2 months prior to the swimming trials.) Adaptation Species temperature ( C) Length (cm) Weight (g) Platichthys flesus Limanda limanda Microstomus kitt IS IS ± ± 'O±o S±i6'97 39O + 3II 3999± 0' O ! lines have been fitted to the data. The equations, correlation coefficients and significance levels are given in Table 1. Interspecific comparison of regressions (Snedecor & Cochran, 1972) between equivalent temperatures in no case show significant differences in slopes or elevations (P > 0-0). (2) Oxygen consumption - swimming speed relationships Mean lengths and weights of the fish used in the swimming trials are given in Table 2. Fig. 2(a)-(c) shows the relationships between oxygen consumption and swimming speed for flounders adapted to and 1 C, and dabs and lemon sole adapted to, and 1 C. Regression equations are given in Table 3. Included in Fig. 2 are standard rates of oxygen consumption calculated forfishof equivalent weight to those used in the swimming trials from the weight-oxygen consumption regressions (Fig. 1). A discrepancy exists between the extrapolated intercepts and the calculated standard rates. Intraspecific comparison between slopes and elevations of pairs of regressions show that there are no significant differences in slopes at the different adaptation^

5 w C 300 r C Respiratory metabolism of temperature-adapted flatfish I 0 a I 0 a E 0- Specific speed (Bis" 1 ) Specific speed (Bis" 1 ) 1- (ft) 1 C C C " " ' I 0 a Specific speed (Bl s" 1 ) (c) 1 C C C T Specific speed (Bis" 1 ) Fig. 2. The relationships between oxygen consumption and swimming speed for the three species of flatfish at various adaptation temperatures. In each graph the points represent determinations on a number of individuals tested for different speeds. The dashed horizontal lines are standard rates calculated from the standard oxygen consumption-weight regressions (Table 1), for fish of equivalent weight, (a) flounders, (6) dabs, (c) lemon sole.

6 Table 3. Results from the swimming respirometry experiments (Swimming speed (X) is specific speed (body lengths s-i). Standard oxygen consumption was calculated from previously established weight-oxygen consumption regressions for equivalent weights of fish (Fig. I). Scope is the difference between standard and active oxygen consumption (Fry, 1947). Intercept is the value derived from extrapolation of the oxygen consumption-swimming speed regression (i.e. antilog of the regression constant). 'Posture effect' is the intercept minus standard oxygen consumption (Priede & Holliday, 1980).) Temperature (T) Critical Standard Active swimming 'Posture rate rate speed Scope Intercept effect' (mg kg-' h-') (mg kg-' h-') (B 1 s-') (mg kg-' h-') (mg kg-' h-') (mg kg-' h-') Swimming regression r P 1. I0 1 I0 1. Platichthys flews '91 Limanda limanda '71 Microstomrrs kitt 3 ' '27 log Y = X+ I ~789 log Y = x+ I ~968 log Y = 0.21 I X+ I.770 log Y = X log Y = X log Y = X log Y = x log Y = X

7 Respiratory metabolism of temperature-adapted flatfish 20 Flounders 2- T 2-0 g 10 o a I 0 (A 8 O Temperature ( C) 20 Lemon sole 2-20 Dabs V I 1 j I % 8. O Temperature ( C) Fig. 3. Effect of adaptation temperature on the active metabolic rate #, critical swimming speed O, intercept of the oxygen consumption-swimming speed regression A, and the standard oxygen consumption, for the three species of flatfish. temperatures (P > 0-0). The elevations between compared pairs differ significantly (P < c-0). Interspecific comparisons of the regressions between equivalent adaptation temperatures show no significant differences in slopes or elevations (P > 0-0). Values for critical swimming speeds and active metabolic rates are presented in Table 3. These values are plotted against temperature in Fig. 3. along with the calculated standard rates and the intercepts of the oxygen consumption-swimming speed regressions. The maximum levels of oxygen consumption for the three species increase with temperature. For dabs and lemon sole there is a relative reduction in ^his value at 1 C. The maximum sustained speed for lemon sole declines at 1 C.

8 366 G. G. DUTHIE 00 r. Flounder 400 o" 300 o o 0 ^, 1 C -. C Specific speed (Bl s" 1 ) Dab 00 Lemon sole ~ O 300 & 8 O C '1 C 0 ^- C.T -" 1 c J"_~J" - C 0 C Specific speed (Bl s" 1 ) Fig. 4. The total cost of swimming per kilometre for different swimming speeds for the three flatfish species at the adaptation temperatures. Cost was calculated from oxygen consumption values obtained from the oxygen consumption-swimming speed regressions (Table 3). The dashed lines indicate where cost has been calculated from extrapolation of the regressions. The arrows indicate the maximum sustained swimming speeds observed in the respirometer. 0 (3) The cost of locomotion Fig. 4. shows the total aerobic cost of swimming (including standard costs) per kilometer at different swimming velocities for the three species. Total cost per unit distance was calculated using the oxygen consumption-swimming speed relationships (Table 3) using the formula: Y(x) C(x) = X where Y(x) is the rate of oxygen consumption at velocity X. Specific speed was converted to km h" 1 using the mean lengths of the fish in each group (Table 2). Fig. 4 shows that the aerobic cost of swimming remains low over a range of swimming speeds. By extrapolating the oxygen consumption-swimming speed regressions beyond the maximum observed speeds, the lowest costs are incurred at speedy around or in excess of the maximum recorded speeds in the respirometer.

9 Respiratory metabolism of temperature-adapted flatfish Muscle M o 2 60 I a Specific speed (Bl s" 1 ) Blood Fig.. Changes in lactic acid in flounder muscle and blood in relation to swimming speed. Trials were conducted at 1 C. Each point represents the mean + s.e. from samples from six individuals. Samples were taken immediately on conclusion of a swimming trial. 1- (4) Lactic acid accumulation Initial experiments showed that blood and muscle lactic acid levels in the flounder rose after handling. Within -8 h values returned to resting levels. In practice, fish were left overnight in the respirometer before swimming trials were conducted. The results of the swimming experiments are shown in Fig.. Each point on the graph represents the mean + S.E. of six individuals. Blood lactic acid levels remain small relative to the increase in muscle lactic acid. The relationship between muscle lactic acid and swimming speed can be described by: log L 0-11 X (r = 0-916, P < o-oi), where L is concentration of lactic acid in mg/0 g tissue and X is swimming speed in body lengths s -1. Assuming that 4 % of the total weight of a flatfish is white muscle, (I. G. Priede, pers. comm.), and that the difference between resting lactic acid levels and levels at any particular swimming speed are a consequence of activity alone, the contribution of aerobic and anaerobic factors to the total energetic mobilisation during activity can be estimated by converting oxygen consumption and lactic acid production to their equivalent of ATP produced. The conversion factors given in Bennett & Licht (1972) were used. Details of calculations are in Duthie (1980). The aerobic and anaerobic expenditure for a standard 20 g flounder at a variety of swimming speeds is given in Table 4. For all speeds considered, the anaerobic contribution to the total energy fcpenditure is relatively constant.

10 368 G. G. DUTHIE Table 4. ATP production (mmol ATP 20 animal* 1 h~ l )from aerobic and anaerobic sources for flounder at selected swimming speeds at 1 C Swimming speed (B 1 s" 1 ) Aerobic ATP production Anaerobic ATP production Total ATP production Anaerobic contribution (%) o-s o-7 I' ' ' i-39 4'49 S'S IS-S DISCUSSION (1) Standard oxygen consumption of flatfish and roundfish Flatfish metabolic rates have been found to be low in comparison to more active species (Wood et al. 1979; Priede & Holliday, 1980). The standard oxygen consumption values of the three species in the present study have been plotted against temperature, along with measurements reported in the literature for otherflatfishand roundfish species, in Fig. 6. In view of the number of records available, only data for salmonids and marine pelagic species have been used as representative of active roundfish. All data have been adjusted to a standard 20 g animal using an exponent of o-8 (Winberg 196), unless values were given in the studies. Assuming a semilogarithmic transformation comes closest to linearising such data (Brett 8c Groves, 1979), the regression equations are Flatfish: log Y = T + o-6oo (r = 0-777, P < o-ooi) Roundfish: log Y = T ( r = '&h P < 0001) where Y is mg 0 2 h" 1 and T is temperature in C. In Fig. 6, values for two species of tropical flatfish (nos 16 & 17) were excluded from the line-fitting procedure. They may show a marked metabolic compensation to temperature (Edwards et al. 1970) in a manner analogous to the reputed phenomenon of cold-adaptation observed in certain high latitude ectotherms (Holeton, 1974). There is no significant difference in slopes of the above regressions (P > 0-0). A significant difference exists between the elevations (P < o-oi). Flatfish have a significantly lower standard metabolism over the temperature range considered. This may reflect the relatively inactive lifestyle of flatfish. During sedentary periods on the sea bottom, a low standard metabolism would allow a saving in basic maintenance costs. (2) Oxygen consumption-swimming speed relationships The range of coefficients describing the rate of increase in the logarithm of oxygen consumption with specific swimming speed for the flatfish in the present study (Table 3) fall within that for other fish species (see Beamish, 1978). Comparison between the coefficients for each flatfish species at different adaptation temperatures and also interspecific comparison between equivalent thermal regimes show qfl

11 Respiratory metabolism of temperature-adapted flatfish 369 I c o E (a) Flatfish species 14 i / (b) / t / / Roundfish species. / i 1 12 j / * Ai ; / I V i Temperature ( C) 2 u Temperature ( C) 2 30 Fig. 6. The standard oxygen consumption of a number of fish species in relation to temperature, (a) flatfish, (6) roundfish. All values are for a 20 g standard animal. Flatfish: (1) Platichthys flesus (present study), (2) Limanda limanda (present study), (3) Microstomus kitt (present study), (4) Platichthys stellatus (Hickman, 199), () Parophrys vetulus (Hickman, 199), (6) Citharichthys stigmaeus (Hickman, 199), (7) Pleuronectes platessa (Priede & Holliday, 1980), (8) Platichthys stellatus (Wood et al. 1979), (9) Pseudopleuronectes americanus (Cech et al. 197), () Platichthys stellatus (Watters & Smith, 1973), (11) Pseudopleuronectes americanus (Voyer & Morrison, 1971), (12) Pleuronectes platessa (Edwards et al. 1969), (13) Pseudopleuronectes americanus (Rowell et al. 197), (14) Pleuronectes platessa (Edwards et al. 1970), (1) Pleuronectes platessa (Edwards, 1971), (16) Cynoglossus sp. (Edwards et al. I97i)» ('7) Brachirus sp. (Edwards et al. 1971), Note, numbers 16 and 17 are marked to indicate exclusion from the line fitting exercise. Roundfish: (1) Oncorhynchus nerka (Brett, 1964)1 (2) Salmo trutta (Beamish, 1964), (3) Salvelinus fontinalis (Beamish, 1964), (4) Salmo gairdneri (Stevens & Randall, 1967), () Salmo gairdneri (Webb, 1971), (6) Pollachius virens (Tytler, 1978), (7) Melanogrammus aeglefinus (Tytler, 1978), (8) F. Cottidae (Holeton, 1974), (9) F. Cyclopteridae (Holeton, 1974), () Boreogadus saida (Holeton, 1974), (11) F. Zoarcidae (Holeton, 1974), (12) Oncorhynchus kisutch (Averett, 1969), (13) Gadus morhua (Edwards et al. 1972). significant differences. The overall oxygen consumption-swimming speed relationships forflatfishare similar and independent of adaptation temperature. The elevations of the regressions are significantly altered. It is energetically more expensive to swim at the higher temperatures. Both standard and active metabolic rates of the flounder approximately double for the C increase in temperature (Table 3). Relatively, the increase in active metabolism is greater and thus scope increases with increase in adaptation temperature. The relative reduction in active metabolic rate in dabs and lemon sole at 1 C (Fig. 3) may indicate the critical temperature for these species, whereby the energy demands of ventilation and associated circulation become excessive, restricting in-

12 370 G. G. DUTHIE creased supply of oxygen to tissues (Jones, 1971) and/or oxygen itself becomes I a respiratory limiting factor (Brett, 1964; Fry, 1971). The relative reduction in critical speed at 1 C may also be due to this. A discrepancy exists between the extrapolated intercepts and standard rates for all three species. Priede & Holliday (1980) found a similar discrepancy for plaice and suggest that it represents the power requirement for lift-off which they term the 'posture effect'. The situation is analogous to that observed in a number of mammals when running is initiated from a resting position (Schmidt-Nielsen, 1972). Baudinette (1978) suggested that such differences also include an 'excitement factor' as well as an increment due to increased power requirements. An excitement component would have a relatively greater effect at the lower swimming speeds, causing a corresponding reduction in the slopes of the oxygen consumption-swimming speed regressions. Although it is not possible to state exactly how the difference between intercept and standard rate is partitioned into the power requirement for lift-off and ' excitement', the data in Fig. 2 (a)-(c) demonstrate that the common method of assessing the standard metabolism of fish, that is the extrapolation of the oxygen consumptionswimming speed relationship to zero swimming speed (Fry & Hochachka, 1970) does not apply to flatfish. (3) The cost of locomotion -possible swimming strategies The cost of locomotion calculations (Fig. 4) indicate that the optimum swimming speeds and the maximum sustainable swimming speeds for the three species correlate closely. By calculating the costs beyond the range of the original oxygen consumptionswimming speed regressions it appears that the most economical speeds may occur at speeds greater than the critical speeds. This implies that the aerobic scope of these flatfish may be insufficient to allow them to swim at what is theoretically their most optimum swimming velocity. To attain these speeds may involve the use of anaerobic metabolism. Plaice have been observed to swim continuously at body lengths s -1 for 0 h with long periods of rest between swimming phases (Greer-Walker et al. 1978). If anaerobic metabolism was being employed, these rest periods would allow the repayment of the oxygen debt. A flounder, for example, swimming at 2-0 body lengths s -1 at 1 C would theoretically consume m g 0 2 kg" 1 h" 1 (from extrapolation of the oxygen consumptionswimming speed relationship). The maximum rate of oxygen consumption that was observed was 214 mg O 2.kg -1 h" 1, leaving a deficit of 6-69 mg 0 2.kg" 1 h -1. Anaerobic swimming involves the metabolism of muscle glycogen to lactic acid, which releases 8 Jg" 1 glycogen (Priede & Holliday, 1980). Fish white muscle contains about 1 g glycogen 0 g" 1 muscle (Wardle, 197). Approximately 4 % of the weight of a flounder is myotomal muscle giving a total glycogen store of 4- g kg" 1, -1 or 211 J energy store. Aerobic metabolism releases 22- J mg 0 2 consumed (Priede & Holliday, 1980), so the deficit represents a power requirement of 1478 J kg" 1 h -1. If the anaerobic metabolism of muscle glycogen was used for this deficit, the fish could swim for 211/1478 = 17 h at 2 body lengths s" 1 before all the glycogen reserve was exhausted. This calculation assumes that the animal in its natural environment cannot increase its oxygen consumption above the maximum recorded^

13 Respiratory metabolism of temperature-adapted flatfish 371 fin the respirometer. However, it does indicate that glycogen stores are sufficient to maintain a low level of anaerobic metabolism for a prolonged period. A similar calculation for the plaice indicates that this fish could swim at 2 body lengths s" 1 for 1-23 h before exhaustion (Priede & Holliday, 1980). It is not unreasonable to assume that as well as the plaice, other flatfish species have movements characterised by alternating swimming and resting phases. Therefore, the use of 'supercritical' swimming speeds with associated build up of oxygen debts is a plausible strategy. (4) Anaerobic metabolism at moderate swimming speeds Priede & Holliday (1980) consider that the white muscle of the plaice works only at high speeds. The elevated lactic acid levels in flounder white muscle (Fig. 6) indicate it is operating anaerobically at moderate speeds. The white muscle of a number of fish species is utilized at swimming velocities other than burst activity (Black et al. 1962; Greer-Walker & Pull, 1973; Hudson, 1973; Johnson & Goldspink, 1973; Wokoma & Johnson, 1981). When the total energy contributions of aerobic and anaerobic processes in the flounder are assessed as ATP produced, the anaerobic contribution is 1% of the total energy expenditure for all speeds examined (Table 4). Comparable data for other fish species is lacking although rainbow trout swimming at 3- body lengths s -1 may initially employ at least a 38% anaerobic contribution (Wokoma & Johnston, 1981). The cost of swimming calculations (Fig. 4), which are based on aerobic considerations alone, would appear to be inadequate indicators of the energy requirements of sustained locomotion in the respirometer. It should be noted that the assessment of aerobic and anaerobic metabolism in the flounder during swimming is based on a number of assumptions: (a) that lactic acid is the only end-product of anaerobic metabolism; (b) that phosphocreatine is not utilized or synthesised during swimming; (c) that the P/O ratio is 3; (d) that lactic acid formed during exercise is neither excreted nor re-utilized during swimming. The first three assumptions have been discussed elsewhere (e.g. Wood et al. 1977; Bennett, 1978; Carey, 1979; Hochachka, 1980; Duthie, 1980). Concerning the last assumption, Wardle (1978) provides evidence for the retention of lactic acid accumulated during strenuous activity by the white muscle of the plaice. The low blood lactic acid levels in the flounder immediately after exercise (Fig. ) suggests a similar phenomenon. It is difficult to extrapolate the results of this laboratory study to what may occur under natural conditions. The increase in lactic acid as speed increases may be an artifact of the experimental apparatus. White muscle may be employed to provide orientation as turbulence increases in the water tunnel. On the other hand, movement over short distances with accumulation of anaerobic end-products would be of little inconvenience to a flounder which spends a large percentage of its time on the substratum, and thus could easily pay off any accrued oxygen debt. Movement over greater distances, e.g. during migration, may be achieved by very rapid burst swimming, with long rest periods to restore depleted glycogen reserves. The use of selective tidal transport may also aid migration (Priede & Holliday, 1980). Periods of rest J^ould occur when the tidal currents are in an adverse direction.

14 372 G. G. DUTHIE In comparison to salmonids the active metabolic rates and critical swimming speeds offlatfishare low. Thus despite the relatively low standard metabolic rates of flatfish (Fig. ), the aerobic scopes are small, e.g. less than 20% of the sockeye salmon in Brett's (1964) study. Thus the total amount of oxygen available to the locomotory muscles of flatfish is relatively small. It is, perhaps, not surprising that during swimming, the aerobic metabolism of flatfish is supplemented by anaerobic metabolism. It may even increase the range of speeds at which the fish is able to swim (Wokoma & Johnston, 1981). My thanks to Dr D. F. Houlihan and Dr I. G. Priede for valuable support and for criticism of the manuscript. This work has been accepted in partial fulfilment for the degree of Ph.D. at the University of Aberdeen. Financial assistance was from the S.R.C. whilst in receipt of a studentship. Professor G. M. Hughes made helpful comments. REFERENCES ALDEIIDICE, D. F. (1976). Some concepts and descriptions of physiological tolerance; rate-temperature curves of poikilotherms as transects of response surfaces. J. Fish. Res. Bd Can. 33, ARNOLD, G. P. (1969). The reactions of plaice {Pleuronectes platessa) to water currents. J. exp. Biol. 1, AVERETT, R. C. (1969). Influence of temperature on energy and material utilisation by juvenile coho salmon. Ph.D. thesis, Oregon State Univ. (Cited in Brett & Groves, 1979). BAUDINETTE, R. V. (1978). Scaling of heart rate during locomotion in mammals. J. comp. Physiol BEAMISH, F. W. H. (1964). Respiration of fishes with special emphasis on standard oxygen consumption. III. influence of weight and temperature on respiration of several species. Can.J. Zool. 42, BEAMISH, F. W. H. (1978). Swimming capacity. In Fish Physiology vol. 7 (ed. W. S. Hoar and D. J. Randall). Academic Press, BENNETT, A. F. (1978). Activity metabolism of the lower vertebrates. A. Rev. Physiol. 40, BENNETT, A. F. & LICHT, P. (1972). Anaerobic metabolism during activity in lizards. J. comp. Physiol. 81, BLACK, E. C, CONNOR, A. R., LAM, K. & CHIU, W. (1962). Changes in glycogen, pyruvate and lactate in rainbow trout (Salmo gairdneri) during and following muscular activity, J. Fish. Res. Bd Can. 19, BRETT, J. R. (1964). The respiratory metabolism and swimming performance of young sockeye salmon. J. Fish. Res. Bd Can. 21, BRETT, J. R. & GROVES, T. D. D. (1979). Physiological energetics. In Fish Physiology, vol. 8 (ed. W. S. Hoar, D. J. Randall and J. R. Brett). Academic Press CAREY, C. (1979). Aerobic and anerobic energy expenditure during rest and activity in montane Bufo b. boreas and Rana pipiens. Oecologia (Berl). 39, CECH, J. J. JR., BRIDGES, D. W. & LAVIGNE, J. R. (197). Cardiovascular responses of the winter flounder, (Pseudopleuronectes americanus) to near-lethal temperature. In Respiration of Marine Organisms (ed. J. J. Cech Jr., D. W. Bridges and D. B. Horton), pp Research Institute of the Gulf of Maine. DUTHIE, G. G. (1980). Physiological responses of flatfish to temperature; a comparative study. Ph.D. thesis, University of Aberdeen. EDWARDS, R. R. C. (1971). An assessment of the energy cost of gill ventilation in the plaice (Pletironectes platessa L.). Comp. Biochem. Physiol. 40A, EDWARDS, R. R. C, BLAXTER, J. H. S., GOPALAN, U. K. & MATHEW, C. V. (1970). A comparison of standard oxygen consumption of temperate and tropical bottom-living marine fish. Comp. Biochem. Physiol. 34, EDWARDS, R. R. C, BLAXTER, J. H. S., GOPALAR, U. K., MATHEW, C. U. & FINLAYSON, D. M. (1971). Feeding, Metabolism and growth of tropical flatfish. J. exp. mar. Biol. Ecol. 6, EDWARDS, R. R. C, FINLAYSON, D. M. & STEELE, J. H. (1969). The ecology of O-group plaice and common dabs in Loch Ewe. II. experimental studies of metabolism, jf. exp. mar. Biol. Ecol. 3, EDWARDS, R. R. C, FINLAYSON, D. M. & STEELE, J. H. (1972). An experimental study of the oxygen consumption, growth and metabolism of the cod (Gadus morlma, L.). J. exp. mar. Biol. Ecol. M

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