Salmo salar - Canadian Science Publishing

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At each temperature, exercise led to decreased white muscle ATP and phosphocreatine concentrations. Phosphocreatine was rapidly restored within 1 h at each.
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Influences of temperature upon the postexercise physiology of Atlantic salmon (Salmo salar) Michael P. Wilkie, Mark A. Brobbel, Kevin Davidson, Leonard Forsyth, and Bruce L. Tufts

Abstract: Atlantic salmon (Salmo salar) were acclimated and exhaustively exercised at 12, 18, or 23°C to determine how temperature influences the magnitude of postexercise physiological disturbances. At each temperature, exercise led to decreased white muscle ATP and phosphocreatine concentrations. Phosphocreatine was rapidly restored within 1 h at each temperature whereas ATP restoration took 1–4 h at 18 and 23°C, but considerably longer at 12°C. Exercise-induced depletions of white muscle glycogen were accompanied by elevations in muscle lactate, which contributed to 0.6 unit decreases in white muscle intracellular pH (pHi) at each temperature. Compared with rates of recovery in warmer water, glycogen resynthesis, lactate catabolism, and pHi correction were slower at 12°C. White muscle REDOX state estimates suggested that slower postexercise recovery at 12°C was not due to oxygen delivery limitations. Marked postexercise elevations in plasma osmolality and lactate concentration were also observed and in each case correction of the disturbance took longer at 12°C. Paradoxically, significant mortality (30%) was observed only at 23°C. We conclude that while warmer water facilitates postexercise recovery of white muscle metabolic and acid–base status in Atlantic salmon, extremely high temperatures may make them more vulnerable to delayed postexercise mortality. Résumé : Des saumons atlantiques (Salmo salar) ont été acclimatés et soumis à un exercice intensif à 12, 18 ou 23°C; l’étude avait pour but de déterminer comment la température influe sur l’ampleur des perturbations physiologiques post-exercice. Pour chaque température, l’exercice a provoqué une baisse des concentrations d’ATP et de phosphocréatine dans le muscle blanc. La concentration de phosphocréatine a rapidement remonté, en moins de 1 h, à chaque température, tandis que le rétablissement de l’ATP a pris de 1 à 4 h à 18 et à 23°C, mais beaucoup plus longtemps à 12°C. Les déplétions de glycogène du muscle blanc induites par l’exercice s’accompagnaient de hausses du lactate musculaire, qui se traduisaient par des baisses de 0,6 unité du pH intracellulaire (pHi) du muscle blanc à chaque température. Par rapport aux taux de récupération en eau plus chaude, la resynthèse du glycogène, le catabolisme du lactate et la correction du pHi étaient plus lents à 12°C. Les estimations de l’état d’oxydoréduction du muscle blanc permettent de penser que la lenteur de la récupération à 12 °C n’était pas due à des limitations de l’apport en oxygène. Des hausses post-exercice marquées de l’osmolalité et de la teneur en lactate du plasma ont aussi été observées et, dans chaque cas, la correction de la perturbation a été plus longue à 12°C. Paradoxalement, une mortalité importante (30%) a été observée à 23°C seulement. Nous en concluons que, si l’eau chaude facilite le rétablissement post-exercice du métabolisme du muscle blanc et du rapport acide-base chez le saumon atlantique, des températures extrêmement élevées peuvent rendre ce poisson plus vulnérable à une mortalité post-exercice à retardement. [Traduit par la Rédaction]

Introduction As a result of the growing popularity of angling, many populations of North American gamefish are under ever increasing pressure from recreational anglers. To reduce angling mortality and conserve gamefish populations, catch and release or nonconsumptive angling has been widely promoted in recent Received September 6, 1995. Accepted August 13, 1996. J13073 M.P. Wilkie,1 M.A. Brobbel, and B.L. Tufts. Department of Biology, Queen’s University, Kingston, ON K7L 3N6, Canada. K. Davidson. Department of Fisheries and Oceans, P.O. Box 5030, Moncton, NB E1C 9B6, Canada. L. Forsyth. Margaree Fish Culture Station, Margaree Valley, NS B0E 2C0, Canada. 1

Author to whom all correspondence should be sent at the following address: Department of Biology, Mount Allison University, Sackville, NB EOA 3C0, Canada.

Can. J. Fish. Aquat. Sci. 54: 503–511 (1997)

years. Indeed, stock declines of Atlantic salmon (Salmo salar) have prompted the Canadian government to enact legislation that makes catch and release of large adults (>63 cm fork length) mandatory in Canada’s Atlantic provinces. However, relatively little is known about the potential impacts that catch and release angling has on these highly prized game fish after their release. The physiological disturbances that fish experience following angling are considerable (Wydoski et al. 1976; Beggs et al. 1980; Gustaveson et al. 1991; Pankhurst and Dedual 1994; Booth et al. 1995; Kieffer et al. 1995) and are often characterized by complete physical exhaustion (Kieffer et al. 1995). It is also well established that exhaustive exercise in the laboratory results in marked disturbances to acid–base, osmotic, and electrolyte balance and reductions in high-energy phosphogen fuels, such as ATP and phosphocreatine (e.g., Milligan and Wood 1986a, 1986b; Dobson et al. 1987; Pearson et al. 1990; Wang et al. 1994a, 1994b). In addition, exhaustive exercise is usually characterized by an almost complete depletion © 1997 NRC Canada

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of muscle glycogen stores and large increases in muscle and blood lactate concentration (Black 1957; Black et al. 1962; Milligan and Wood 1986b; Dobson et al. 1987; Pearson et 1990; Wang et al. 1994a). In some cases, postexercise physiological disturbances may be severe enough to result in delayed postangling–exercise mortality (Black 1958; Bouck and Ball 1966; Beggs et al. 1980; Wood et al. 1983; Ferguson and Tufts 1992). In contrast to Atlantic salmon angled in the late fall at 6°C, we recently found that returning Atlantic salmon angled under midsummer (~20°C) conditions were unable to resynthesize glycogen or fully restore white muscle intracellular pH to resting levels within the experimental recovery period (4 h; Wilkie et al. 1996). Moreover, all of the salmon angled in the late fall survived (Booth et al. 1995), but survival under midsummer conditions was only 60% (Wilkie et al. 1996). Although several factors, such as the duration of freshwater acclimation and degree of starvation, also differed between the salmon angled in the summer and fall, we suggested that environmental temperature may have played an important role in the different postangling physiological responses that were observed. Indeed, angling at elevated water temperatures (e.g., >20°C) is known to exacerbate ionoregulatory and osmotic disturbances in the blood of rainbow trout (Oncorhynchus mykiss; Wydoski et al. 1976) and largemouth bass (Micropterus salmoides; Gustaveson et al. 1991). Accordingly, the objective of the present investigation was to examine the influence of temperature on the postexercise physiology and survival of mature Atlantic salmon that were fully acclimated to fresh water, had identical life histories, and, until just prior (2 weeks) to the experiments, were held at similar water temperatures.

Materials and methods Experimental animals and setup Experiments were conducted at the Margaree Fish Culture Station (MFCS), Margaree Valley, Nova Scotia, in August 1994 on sexually mature hatchery-reared Atlantic salmon (mass 2.03 ± 0.05 kg (mean ± SEM); length 60.7 ± 0.5 cm). Approximately 2 weeks before the experiments, the fish were transferred from outdoor, freshwater holding ponds (pH 7.1; [Ca 2+], 1.4 mequiv.⋅L –1 ; [Mg 2+], 0.3 mequiv.⋅L –1; [Na+], 3.7 mequiv.⋅L–1; [Cl-], 3.8 mequiv.⋅L–1; alkalinity, 14.5 mequiv.⋅L–1) to the MFCS’s indoor facilities, where the salmon were equally distributed (n = 26), to three large fibreglass Swede (holding) tanks (2.4 × 2.4 × 1.0 m) with a water depth of 0.8 m. There was a continual inflow (about 10 L⋅min–1) of brook water, identical in chemical composition to that in the holding ponds, and temperature was initially maintained at 18°C. The fish were allowed to adjust to their new surroundings for 3–5 days, after which water temperatures were adjusted toward the nominal experimental temperatures of 12 or 23°C in two of the three tanks at a rate of 1°C⋅day–1; the remaining tank was regulated at 18°C. The 23°C water was maintained by mixing heated brook water with normal, cooler brook water. The 12oC water was pumped from a well and had a similar composition to the brook water (pH, 7.5; [Ca2+], 2.8 mequiv.⋅L–1; [Mg2+], 1.1 mequiv.⋅L–1; [Na+], 2.6 mequiv.⋅L–1; alkalinity, 1.5 mequiv.⋅L–1). Feeding was terminated after the fish were transported indoors because appetite might have been differentially influenced by the different temperature regimes and because migrating Atlantic salmon naturally stop feeding upon entering fresh water (Scott and Crossman 1973; Tufts et al. 1991). After the experimental temperatures were achieved, the fish were left undisturbed in their tanks for a minimum

Can. J. Fish. Aquat. Sci. Vol. 54, 1997 of 2 weeks before postexercise physiology was assessed, and the total period of starvation approximated 3–5 weeks. The system designed to assess the postexercise physiology of the salmon consisted of two large wooden boxes that contained four individual chambers per box. One day prior to experimentation the salmon were netted, one at a time, from the appropriate holding tanks (12, 18, or 23°C), placed in an individual chamber, and allowed to recover overnight at the appropriate temperature. The covered chambers were large enough to permit the salmon to move about (dimensions 22 cm deep × 27 cm wide × 120 cm long) and contained about 70 L of water. Water was directly pumped to the boxes from the appropriate holding tanks and flow rates into each chamber approximated 2.75 ± 0.25 L⋅min–1. Oxygenation was maintained at 90–100% saturation with air stones connected to a Summit 5 artificial oxygenator (Mountain Medical Equipment Inc., Littleton, Colo.). Experimental protocols This study was divided into two distinct series. In part 1, salmon were exercised to exhaustion and then terminally sampled for analysis of physiological variables, at 12, 18, or 23°C. Resting fish, which were sampled in an identical manner to the exercised animals, served as the controls. In part 2, survival was monitored for 3 days following exhaustive exercise at one of the three temperatures. In both series of experiments, exercised fish were chased manually, one at a time, for 6 min in a 1.5 m diameter circular exercise tank containing 30–40 cm of water at the appropriate temperature. Part 1: postexercise physiology After being allowed to acclimate overnight to the holding boxes, the fish were transferred, one at a time, to the exercise tank where they were exhaustively exercised for 6 min. The fish were then anaesthetized in MS-222 (see below) and immediately sampled (0 h), or returned to their respective holding chambers and allowed to recover for 1 or 4 h. Resting fish, which were also held in the holding boxes and subsequently anaesthetized, served as the controls. Anaesthetization was achieved by directly adding concentrated MS-222 (1 g⋅L–1) solution, buffered with NaHCO3– (2 g⋅L–1) , to the water in each holding chamber. This yielded a final concentration of 0.1 g⋅L–1 MS-222 in each chamber. When the fish were unresponsive (within 1 min) they were quickly transferred to a box containing concentrated MS-222 (0.3 g⋅L–1) for 1 min to ensure complete anaesthetization, after which blood and tissue samples were taken within 30 s. Confinement in fish boxes and subsequent anaesthetization with buffered MS-222 was chosen because it is most effective for preserving muscle and blood metabolite concentrations, such as lactate, ATP, phosphocreatine (PCr), and glycogen, in fishes (Tang and Boutilier 1991; Wang et al. 1994b). After anaesthetization, 10-mL blood samples were withdrawn into heparinized, plastic disposable syringes via caudal puncture and immediately placed on ice until muscle sampling was complete. White muscle was then excised from the dorsal region of the trunk, just anterior to the dorsal fin, and quick frozen with aluminum tongs cooled with liquid N2 and immediately plunged into liquid N2. Blood samples were then centrifuged at 10 000 × g for 3 min, and the resultant supernatant was withdrawn and immediately frozen for later determination of plasma lactate and osmolality. Muscle samples were stored in liquid N2 for future analysis of muscle pHi, water content, glycogen, ATP, PCr, free creatine, lactate, and pyruvate. Immediately following blood and muscle sampling, the fish were killed by a sharp blow to the head. Part 2: postexercise survival This experiment was designed to determine if exercise resulted in any delayed mortality at each of the experimental temperatures. At each temperature, fish (n = 10; experimental) were netted one at a time from their respective holding tanks and were then transferred to the exercise tank and chased for 6 min. Efforts were always made to © 1997 NRC Canada

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Wilkie et al. minimize air exposure (