Thermal dependence of swimming endurance in juvenile brown trout
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1 Journal of Fish Biology (2000) 56, doi: /jfbi , available online at on Thermal dependence of swimming endurance in juvenile brown trout A. F. OJANGUREN* AND F. BRAÑA Departamento de Biología de Organismos y Sistemas, Universidad de Oviedo, Catedrático R. Uría, s/n 33071, Oviedo, Spain (Received 5 November 1999, Accepted 27 January 2000) The maximum swimming stamina of hatchery reared juvenile brown trout Salmo trutta, swimming against a fixed-velocity water flow of 36 6 cm s 1 (6 97 L s 1 ), was achieved at 16 1 C, and a 90% performance level occurred over a breadth of 7 7 C ( C). The wide range of temperatures at which swimming performance is close to the maximal capacity could be a consequence of the implications for survival of this function The Fisheries Society of the British Isles Key words: temperature; swimming stamina; salmonids; optimal temperature; performance breadth. INTRODUCTION Temperature is perhaps the most important environmental determinant of physiological activity and whole-animal performance of ectothermic vertebrates (Cossins & Bowler, 1987; Huey & Kingsolver, 1989; Bennett, 1990). Unlike reptiles, most fishes do not thermoregulate efficiently (Huey, 1982; Cossins & Bowler, 1987) and being exposed to large daily and seasonal fluctuations should consequently perform near the environmental temperatures (but see Matthews & Berg, 1997 and Stevens & Neill, 1978, for small and large scale exceptions). Temperature has complex interactive effects on swimming activity of fishes which have been recognized for a long time, and some effort has been devoted to establishing both optima and limits of locomotor performance (Beamish, 1978 and references therein). Otherwise, thermal dependence of fish locomotion has been focused from a variety of viewpoints, from the ecological level to the organismal and even cellular physiology approach (Rome et al., 1990; Johnson & Bennett, 1995). Thermal regime has been considered to influence the structure of fish communities through its effects on swimming performance, by affecting survival (Childs & Clarkson, 1996) and particularly predator prey relationships (Taylor & McPhail, 1985; Fuiman, 1991; Fuiman & Batty, 1994). Moreover, the interaction between temperature and swimming capacity is an important determinant of microhabitat use (Taylor, 1988) and migration (Heggenes & Traaen, 1988). This work aimed to assess the effect of temperature on swimming endurance of juvenile brown trout Salmo trutta L., taking into account the wide range of *Author to whom correspondence should be addressed. Tel.: ; fax: ; ojangur@sci.cpd.uniovi.es /00/ $35.00/ The Fisheries Society of the British Isles
2 TEMPERATURE AND SWIMMING ENDURANCE IN TROUT 1343 temperature tolerance of this species, and to establish a response curve, which would allow estimation of the optimal temperature for swimming and the performance breadth for this function. MATERIALS AND METHODS Young-of-the-year individuals were obtained from first generation hatchery fish originating from a wild stock caught in the Nalón-Narcea basin (Asturias, northern Spain). Seven full-sibling families were obtained by fertilizing the eggs of seven females each with the milt of one different male. From the swimming-up stage (April 1997), families were reared in standard hatchery conditions with natural photoperiod and temperature (average of daily mean temperatures S.D C, range C). Swimming stamina trials were carried out in the laboratory from 30 July to 21 August Mean ( S.D.) water temperature in the hatchery during the 10 days before the start of the swimming trials was C (range C). Seven trout from each of the seven families were acutely acclimatized in the laboratory starting from the hatchery temperature and gradually increasing or decreasing until the corresponding test value. Then, fish were kept at the target temperature for 38 h before the start of the swimming trials. Seven experimental temperatures were selected (5 5, 10, 15, 17, 19, 21 and 26 C) covering the range observed in natural conditions, but also trying to approach the upper and lower performance limits. The swimming chamber consisted of a cylindrical transparent tube (550 mm long and 44 mm internal diameter) with both ends closed with mesh (1 mm light). This tunnel was submerged in a cm glass aquarium that received water from a 80-l tank connected to a cooler or heater unit to maintain water temperature within 0 1 Cofthe target value. One fish at a time was placed into the swimming tunnel and maintained during 3 min with a water flow of 14 7 cms 1 (2 8 lengths s 1, calculated from the mean fork length) pumped from the tank. This allowed test fish to orient towards the water inflow and to adjust to light and dimensions of the chamber. Then, the inflow pipes were switched, connecting the tunnel to a pump that produced a water speed of 36 6 cms 1 (6 97 L s 1 ) and time until fatigue was registered. This water speed was selected on the basis of some preliminary trials, because similar sized trout get exhausted within a moderate time period. The fish were exhausted when they were no longer able to continue swimming in spite of mechanical stimulation by gently prodding the downstream mesh. Every fish was used just once and it was measured (fork length, to the nearest 0 01 mm) and weighed (to the nearest g) after each trial. Mean ( S.D.) fork length and weight of the individuals tested were mm and g, respectively. RESULTS Size (log fork length) strongly affected swimming stamina (log endurance time), giving significant positive relationships for 10, 15, 17 and 21 C(Fig. 1, Table I). The test of parallelism did not reveal significant between-temperature differences in the slopes of the regression lines (F 6,206 =1 27, P=0 274). To correct for size-dependence, the effects of temperature and family on swimming stamina were assessed by performing an ANCOVA with fork length as covariate, both variables log transformed to achieve normality (Shapiro Wilk s W test) and homoscedasticity (Bartlett χ 2 test). This analysis revealed highly significant differences in stamina (log time) for temperature (F 6,212 =43 35, P<0 001), but neither family effect (F 6,212 =1 44, P=0 200) nor significant temperature family interaction (F 36,212 =0 74, P=0 861). Since there were no between-family differences, data were pooled from all the families for each temperature to obtain
3 1344 A. F. OJANGUREN AND F. BRAÑA C 19 C Endurance time (s) C 17 C 21 C 26 C 5.5 C Fork length (mm) FIG. 1. Regression lines for the relationship between endurance time (log transformed) and fork length (log transformed) for each water temperature. Solid lines represent significant relationships TABLE I. Parameters from the regressions between endurance time and fork length, both log transformed, for each experimental temperature Temperature ( C) n Slope Intercept r 2 P < < < size-adjusted means of log endurance time. These values, transformed back to a linear scale, are fitted well by a second-order polynomial curve in which temperature accounts for >98% of the variance in swimming stamina (Fig. 2). The regression function gives a maximum for endurance time at 16 1 C, and maintains values above the 90% of maximal performance between 12 2 and 19 9 C. DISCUSSION The positive effect of body size on swimming capacity has been reported widely (Fry & Cox, 1970; Ojanguren et al., 1996, for the same population studied here) and was confirmed in the present study except for extreme temperatures. The lack of significant relationship between stamina and body size at the lower- and uppermost temperatures could be attributable to the poor overall
4 TEMPERATURE AND SWIMMING ENDURANCE IN TROUT Endurance time (s) % Water temperature ( C) FIG. 2. Response curve for the relationship between size-adjusted endurance time (t) and water temperature (T). Arrows depict the range of temperatures within which endurance time is >90% of the maximum. t= 0 282T T ; r 2 =0 985; P< performance in the closeness of the thermal limits for locomotion. At these extreme temperatures, the ability to swim and the interindividual differences were reduced, and thus the effect of size was inevitably weaker. Nevertheless, the slopes of the regression lines were all positive and did not differ significantly between temperatures (Fig. 1). The shape of the relationship between swimming endurance time and temperature is the characteristic performance curve with high values around an optimum and decreasing at upper and lower temperatures (Huey & Kingsolver, 1989). However, apparently the curve does not draw the usual asymmetric skew towards low temperatures, perhaps because juvenile brown trout could still maintain some swimming capacity below the lowermost experimental temperature (5 5 C) but probably not above the uppermost one (26 C). If so, a wider spectrum of experimental temperatures should be necessary to approach the expected function. The maximum obtained from the function could be rather high, according to other performance measures reported for northern populations of the species (Elliott, 1994). However, longer acclimatization periods and trials at different times of the year would be required to fix reference values of optimal temperature for swimming endurance. The wide swimming performance breadth exhibited by our study population (7 7 C, in which performance is >90% of the maximum) reinforces the characterization of brown trout as a moderately eurythermal salmonid (Elliott, 1994). In general, the scope of water temperatures at which a fish can perform is expected to be wider for those functions strongly linked to fitness. Hence, maintenance of swimming ability at a broad range of water temperatures could affect juvenile survival through its relationship with predator avoidance (Fuiman, 1991; Hale, 1996; Watkins, 1996). In particular, swimming stamina might be functionally important for drift-feeding salmonids, which need to be swimming almost continuously to intercept individual prey items while resisting displacement by the water flow (Godin & Rangeley, 1989; McLaughlin &
5 1346 A. F. OJANGUREN AND F. BRAÑA Noakes, 1998). This is consistent with the fact that the limits of 90% performance were within the usual range of temperatures in this area during the growing season (April to October, pers. obs.). However, the thermal limits of muscle contractile properties and enzymatic activities could impose functional constraints on performance that would limit the trend toward thermal insensitivity (Rome et al., 1990; Johnson & Bennett, 1995; Somero et al., 1996). A trade-off between breadth and maximal performance has been demonstrated frequently (Huey & Hertz, 1984; Huey & Kingsolver, 1989) and this would imply that high swimming ability at a wider range of temperatures could occur only at the expense of maximal capacity, which to some extent would limit the performance breadth. Nevertheless, this negative relationship has not been demonstrated empirically in brown trout and further multidisciplinary research on this topic, would be required. We thank V. Au lvarez Faes and R. Rodríguez-Muñoz for their valuable assistance during the experimental work; and the Consejería de Agricultura del Principado de Asturias for providing and maintaining experimental trout. The European Commission under the FAIR program (Contract No. CT ) funded this research. References Beamish, F. W. H. (1978). Swimming capacity. In Fish Physiology, Vol. 7 Locomotion (Hoar, W. S. & Randall, D. J., eds), pp New York: Academic Press. Bennett, A. F. (1990). Thermal dependence of locomotor capacity. American Journal of Physiology 28, R253 R258. Childs, M. R. & Clarkson, R. W. (1996). Temperature effects on swimming performance of larval and juvenile Colorado squawfish: implications for survival and species recovery. Transactions of the American Fisheries Society 125, Cossins, A. R. & Bowler, K. (1987). Temperature Biology of Animals. London: Chapman & Hall. Elliott, J. M. (1994). Quantitative Ecology and the Brown Trout. Oxford: Oxford University Press. Fry, F. E. J. & Cox, E. T. (1970). A relation of size to swimming speed in rainbow trout. Journal of the Fisheries Research Board of Canada 27, Fuiman, L. A. (1991). Influence of temperature on evasive responses of Atlantic herring larvae attacked by yearling, Clupea harengus L. Journal of Fish Biology 39, Fuiman, L. A. & Batty, R. S. (1994). Susceptibility of Atlantic herring and plaice larvae to predation by juvenile cod and herring at two constant temperatures. Journal of Fish Biology 44, Godin, J.-G. J. & Rangeley, R. W. (1989). Living in the fast lane: effects of cost of locomotion on foraging behaviour in juvenile Atlantic salmon. Animal Behaviour 37, Hale, M. E. (1996). The development of fast-start performance in fishes: Escape kinematics of the chinook salmon (Oncorhynchus tshawytscha). American Zoologist 36, Heggenes, J. & Traaen, T. (1988). Downstream migrations and critical water velocities in stream channels for fry of four salmonid species. Journal of Fish Biology 32, Huey, R. B. (1982). Temperature physiology and the ecology of Reptiles. In Biology of the Reptilia, Vol. 12 Physiology C, Physiological Ecology (Gans, C. & Pough, F. H., eds), pp London: Academic Press. Huey, R. B. & Hertz, P. E. (1984). Is a jack-of-all-temperatures a master of none? Evolution 38,
6 TEMPERATURE AND SWIMMING ENDURANCE IN TROUT 1347 Huey, R. B. & Kingsolver, J. G. (1989). Evolution of thermal sensitivity of ectotherm performance. Trends in Ecology and Evolution 4, Johnson, T. P. & Bennett, A. F. (1995). The thermal acclimation of burst escape performance in fish: an integrated study of molecular and cellular physiology and organismal performance. Journal of Experimental Biology 198, Matthews, K. R. & Berg, N. H. (1997). Rainbow trout responses to water temperature and dissolved oxygen stress in two southern California stream pools. Journal of Fish Biology 50, McLaughlin, R. L. & Noakes, D. L. G. (1998). Going against the flow: an examination of the propulsive movements made by young brook trout in streams. Canadian Journal of Fisheries and Aquatic Sciences 55, Ojanguren, A. F., Reyes-Gavilán, F. G. & Braña, F. (1996). Effects of egg size on offspring development and fitness in brown trout, Salmo trutta L. Aquaculture 147, Rome, L. C., Funke, R. P. & McNeill-Alexander, R. (1990). The influence of temperature on muscle velocity and sustained performance in swimming carp. Journal of Experimental Biology 154, Somero, G. N., Dahlhoff, E. & Lin, J. J. (1996). Stenotherms and eurytherms: mechanisms establishing thermal optima and tolerance ranges. In Animals and Temperature: Phenotypic and Evolutionary Adaptation (Johnston, I. A. & Bennett, A. F., eds), pp Cambridge: Cambridge University Press. Stevens, E. D. & Neill, W. H. (1978). Body temperature relations of tunas, especially skipjack. In Fish Physiology, Vol. 7 Locomotion (Hoar, W. S. & Randall, D. J., eds), pp New York: Academic Press. Taylor, E. B. (1988). Water temperature and velocity as determinants of microhabitats of juvenile chinook and coho salmon in a laboratory stream channel. Transactions of the American Fisheries Society 117, Taylor, E. B. & McPhail, J. D. (1985). Burst swimming and size-related predation of newly emerged coho salmon Oncorhynchus kisutch. Transactions of the American Fisheries Society 114, Watkins, T. B. (1996). Predator-mediated selection on burst swimming performance in tadpoles of the Pacific tree frog, Pseudacris regilla. Physiological Zoology 69,
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