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Unformatted text preview: Color profile: Generic CMYK printer profile Composite Default screen 1104 Effects of acclimation to brackish water on the growth, respiratory metabolism, and swimming performance of young-of-the-year Adriatic sturgeon (Acipenser naccarii) D.J. McKenzie, E. Cataldi, P. Romano, S.F. Owen, E.W. Taylor, and P. Bronzi Abstract: Specific growth rates, exercise respirometry, and swimming performance were compared in young-of-the-year Adriatic sturgeon (Acipenser naccarii) maintained in freshwater (FW) or acclimated to brackish water (BW) that was slightly hypertonic to sturgeon plasma, at a salinity of 11 g·L–1. Specific growth rate was significantly (17%) lower in BW than in FW. Sturgeon in BW also had a significantly (30%) higher standard metabolic rate than those in FW. In both groups, the relationship between swimming speed and oxygen uptake was described equally well by a linear or exponential equation, with a power relationship between swimming speed and net cost of locomotion and a linear relationship between tailbeat frequency and swimming speed. However, sturgeon in BW exhibited higher mean total oxygen uptake, net costs, and tailbeat frequencies than the FW group at any given swimming speed. There were, however, no differences in aerobic scope or maximum sustainable swimming speed between the FW and BW groups because the BW group exhibited a compensatory increase in active metabolic rate and maximum tailbeat frequency. The results indicate that FW is a more suitable environment than mildly hypertonic BW for young-of-the-year Adriatic sturgeon. Résumé : Nous avons comparé les taux de croissance spécifiques, la respirométrie à l’exercice et la performance de nage chez des jeunes Esturgeons de l’Adriatique (Acipenser naccarii) de l’année gardés en eau douce (ED) ou acclimatés à une eau saumâtre (ES) de salinité de 11 g·L–1, légèrement hypertonique par rapport au plasma d’esturgeon. Le taux de croissance spécifique est significativement plus bas (17%) en ES qu’en ED. Les esturgeons en ES ont aussi un taux métabolique standard significativement plus élevé (30%) que les esturgeons en ED. Chez les deux groupes, la relation entre la vitesse de nage et la consommation d’oxygène se décrit aussi bien par une équation linéaire que par une équation exponentielle, avec une relation exponentielle entre la vitesse de nage et le coût net de la locomotion et une relation linéaire entre la fréquence de battement de la queue et la vitesse de nage. Cependant, quelle que soit vitesse de nage, les esturgeons en ES ont une consommation d’oxygène moyen total, des coûts nets et des fréquences de battements de la queue plus élevés que ceux qui sont en ED. Il n’y a toutefois aucune différence dans l’amplitude aérobique ou la vitesse de nage maximale maintenue entre les deux groupes parce que les esturgeons en ES font montre d’une augmentation compensatoire de leur taux de métabolisme actif et de leur taux de battement de la queue. Il en résulte que, pour les jeunes Esturgeons de l’Adriatique de l’année, l’ED est un milieu plus approprié que l’ES légèrement hypertonique. [Traduit par la Rédaction] McKenzie et al. 1112 Introduction The life cycle of many sturgeon species includes repeated migrations between freshwater (FW) and estuarine or marine habitats (Rochard et al. 1991; Birstein 1993). The Adriatic or Italian sturgeon (Acipenser naccarii) exhibits a diadromous life history: breeding occurs in FW, both juveniles and adults are reported to inhabit brackish estuarine waters (Rossi et al. 1992), and adults have been captured in the Adriatic Sea (Tortonese 1989). There are also anecdotal reports of egg deposition in brackish estuarine waters in this species (Paccagnella 1948). There are very few published studies on the osmoregulatory physiology of acipenserids (e.g., Potts and Rudy Received April 14, 2000. Accepted January 25, 2001. Published on the NRC Research Press Web site on May 3, 2001. J15721 D.J. McKenzie.1 Business Unit Environment, Centro Elettrotecnico Sperimentale Italiano, Via Reggio Emilia 39, 20090 Segrate (MI), Italy, and School of Biosciences, University of Birmingham, Birmingham, U.K. B15 2TT. E. Cataldi. Dipartimento di Biologia, Università di Roma Tor Vergata, Via della Ricerca Scientifica, 00133 Roma, Italy. P. Romano and P. Bronzi. Business Unit Environment, Centro Elettrotecnico Sperimentale Italiano, Via Reggio Emilia 39, 20090 Segrate (MI), Italy. S.F. Owen and E.W. Taylor. School of Biosciences, University of Birmingham, Birmingham, U.K. B15 2TT. 1 Corresponding author (c/o CESI Stazione Idrobiologia Fluviale La Casella, Via Argine del Ballottino, 29010 Sarmato (PC), Italy; e-mail: mckenzie@cesi.it). DOI: 10.1139/cjfas-58-6-1104 © 2001 NRC Canada Can. J. Fish. Aquat. Sci. 58: 1104–1112 (2001) 1 J:\cjfas\cjfas58\cjfas-06\F01-059.vp Wednesday, May 02, 2001 11:14:08 AM Color profile: Generic CMYK printer profile Composite Default screen McKenzie et al. 1105 1972; Natochin et al. 1985; Krayushkina et al. 1996). A preliminary study on A. naccarii by Cataldi et al. (1995) revealed that 1- to 1.5-year-olds were able to tolerate brackish water (BW) at a salinity of 20 g·L–1 and seawater (SW) at 30 g·L–1 for 60 days and regulate plasma osmolality and ions at levels similar to those in sturgeon kept in FW. Nonetheless, there was some evidence of difficulty in long-term adaptation, particularly at 30 g·L–1, with plasma osmolality gradually increasing over time (Cataldi et al. 1995). Subsequent studies have revealed that young-of-the-year (YOY) sturgeon acquire the ability to tolerate hyperosmotic environments once they have completed development of the gills and kidney, but the 96-h LC50 for salinity in such sturgeon (aged 120 days) was approximately 23 g·L–1 (Cataldi et al. 1999). Following a 42-day acclimation to BW at 11 and 23 g·L–1, slightly older animals (aged 150 days) were able to regulate plasma osmolality and ion concentrations at levels similar to those of their siblings in FW, as a consequence of adaptive responses that included an increase in the activity of Na+,K+-ATPase in the gills (McKenzie et al. 1999). The effect of salinity on the growth and metabolic rate of euryhaline teleosts (particularly salmonids) has been the focus of many studies (for a review, see Morgan and Iwama 1991). Although early papers indicated that growth might be promoted in BW at an osmolality similar to that of the plasma, as a consequence of reduced metabolic costs for osmoregulation (Canagataram 1959; Rao 1968), recent theoretical and experimental studies (Kirschner 1995; Morgan and Iwama 1999) indicate that osmoregulatory costs are quite low in teleosts and that growth rates are highest and metabolic rates lowest in the salinity that is appropriate for the life stage of the species under study (Morgan and Iwama 1991). An investigation of the effects of salinity on growth rates of euryhaline chondrosts may provide information about the optimal environment for animals of a particular age and size. A previous study compared the growth of YOY sturgeon in FW with that in BW at a salinity of 20 g·L–1 and osmolality of approximately 565 mosmol·kg–1 (McKenzie et al. 1999). Sturgeon plasma has an osmolality of approximately 280 mosmol·kg–1, so BW at an osmolality of 565 mosmol·kg–1 was as hypertonic to sturgeon plasma as the FW was hypotonic. Therefore, costs for osmoregulation, whatever their absolute magnitude, should have been similar in the two environments (Kirschner 1995; Morgan and Iwama 1999). The BW at 20 g·L–1 caused a profound inhibition of growth (McKenzie et al. 1999), indicating that YOY sturgeon were able to tolerate a requirement for hyperosmoregulation much better than an equal but opposite requirement for hypoosmoregulation. In the wild, migrating sturgeon are known to spend a period in BW prior to moving into the marine environment, and this is particularly true for juveniles, for which the period can last for many months or years (Sulak and Clugston 1999). This may indicate that time spent in BW promotes hypoosmoregulatory adaptations necessary for subsequent tolerance of SW but, presumably, only if the water were hypertonic to sturgeon plasma. The current paper investigated the effects of acclimation to slightly hypertonic BW on growth rates of YOY Adriatic sturgeon, employing water at a salinity of 11 g·L–1 and osmolality of 310 mosmol·kg–1. The current study is linked to a companion paper that investigated whether such prior acclimation to a mildly hypertonic environment promoted tolerance of a further salinity challenge (McKenzie et al. 2001). Swimming respirometry has been used extensively to describe aspects of respiratory metabolism in teleosts (Brett 1964; Fry 1971; Beamish 1978), including estimates of standard metabolic rate (SMR) (Brett 1964; Fry 1971) that might reveal metabolic costs associated with salinity acclimation. Swimming performance is also an integrated index of fitness in fish, and differences in performance have been used to reveal underlying stresses associated with nonoptimal abiotic factors such as salinity (Randall and Brauner 1991) or sublethal exposure to toxicants (Beaumont et al. 1995). Swimming performance of acipenserids has been studied very little (Webb 1986; McKinley 1991; Peake et al. 1997) but is of considerable interest because of the migratory lifestyle of many sturgeon species. In the current study, the growth rates of sturgeon in FW or BW at a salinity of 11 g·L–1 were compared with measures of exercise-related respiratory metabolism and swimming performance to reveal any metabolic costs and consequences for performance of acclimation to mildly hypertonic BW as compared with FW. Materials and methods Experimental animals Fertilised eggs of A. naccarii were obtained from the artificial reproduction of captive broodstock (Arlati et al. 1988) at the Azienda Agricola VIP di Giovannini Giacinto (Orzinuovi (BS), Italy) in July 1997. Eggs were transported to the “La Casella” Experimental Thermal Aquaculture Plant (Sarmato (PC), Italy) and hatched indoors on grid incubators provided with a flow of aerated well water at 15°C. The water had the following ionic composition (millimolar) and characteristics: Ca2+ = 2.3, Mg2+ = 0.6, Na+ = 2.3, Cl– = 0.7, K+ = 0.9, titratable alkalinity to pH 4 = 13.5 mM, total hardness = 240 mg·L–1 as CaCO3, and pH 8.2. First-feeding of the fry was with Artemia nauplii, followed by gradual adaptation to artificial granulated dry feed (Trouvit Storioni, Hendrix SpA, Mozzecane (VR), Italy). Photoperiod was natural via skylights. The fry were subsequently transferred to 1-m2 fiberglass tanks (water volume approximately 250 L) and gradually adapted to a flow of aerated FW at a temperature of 23 ± 1°C within a closedcycle hatchery biofilter (total volume 90 m3), with temperature raised over a 16-day period by proportional mixing of well water and biofilter water at the inflow. The biofilter water had the same chemical characteristics as the well water, from which it was derived, but with a water pH of 8.1. Sturgeon were weighed at 30-day intervals and feeding rate maintained at approximately 2% of mean mass per day, using feed (Trouvit Storioni) of increasing granule size, as required. In December 1997, the sturgeon had achieved a mean (±SE) mass of 14.2 ± 0.7 g and mean fork length of 11.8 ± 0.2 cm (N = 173). It has previously been established that Adriatic sturgeon of this size and age can tolerate salinities up to 23 g·L–1 (Cataldi et al. 1999; McKenzie et al. 1999). Six groups of 15 animals, selected at random and with no differences in resultant mean mass, were transferred into 4-m2 fiberglass tanks (water volume approximately 1000 L). Three of the tanks continued to receive a flow of aerated FW from the closed-cycle biofilter. The remaining three tanks received a flow of aerated BW at a salinity of 11 g·L–1 and temperature of 23 ± 1°C, provided from a closed-cycle biofilter with a total volume of approximately 6 m3. The BW was composed of well water to which marine salts (ProdacMare, Prodac, Citadella (PD), © 2001 NRC Canada 2 J:\cjfas\cjfas58\cjfas-06\F01-059.vp Wednesday, May 02, 2001 11:14:08 AM Color profile: Generic CMYK printer profile Composite Default screen 1106 Italy) were added and had a pH of 8.4. These triplicate groups of sturgeon in FW and BW were the subjects of the growth study. Two further 4-m2 fiberglass tanks were also prepared containing 25 randomly selected animals, one of which received a flow of FW and the other a flow of BW. These tanks provided subjects for the swimming respirometry experiments and the analyses of haematological variables in FW versus BW. All tanks received a similar water flow rate of approximately 5 L·s–1. The sturgeon were allowed approximately 70 days (10 weeks) to acclimate to their respective salinities, with total tank mass measured every 30 days to adjust feeding rates. Feed was provided at 3% wet body mass per day. At the beginning of March 1998, the groups of sturgeon acclimated to FW and BW had achieved a mean mass of approximately 100 g and fork length of 23 cm, a size at which they could be tagged for individual identification. They were anaesthetized (100 mg tricaine methanesulphonate·L–1) and tagged with colored glass beads threaded onto sterilized nylon fishing line sutured to the dorsal fin. All animals recovered within 5 min of replacement into aerated water in their tanks; there was no mortality associated with the procedure. Can. J. Fish. Aquat. Sci. Vol. 58, 2001 bility in water at the experimental temperature and salinity. Only slopes with r 2 > 0.9 were used in the calculations. The respirometer chamber was immersed in a large tank of aerated water. When the PWO 2 in the respirometer chamber declined below 90% saturation, the Labview software activated a flushing pump (1048UHP, Eheim, Germany) that flushed aerated water from the outer tank through the respirometer chamber, bringing the PWO 2 back to 95% saturation, at which point the pump switched off and measurement of oxygen consumption resumed. At the end of each experiment, blank tests were run to measure the proportion of total MO2 that was attributable to bacterial metabolism. The measured rates in the absence of a fish never exceeded 5% of the total MO2 and in most cases were negligible. As such, no corrections were applied. The oxygen electrode was calibrated at the beginning and the end of each experiment; zero current was set by unplugging the electrode from the meter and air saturation was then set by reconnecting the electrode and exposing it to a flow of 100% air-saturated water. Individual sturgeon that had previously been starved for at least 24 h were placed in the respirometer containing water at the appropriate acclimation salinity and forced to swim at a water speed equal to 0.5 bodylength (BL)·s–1 for at least 12 h (overnight). This swimming speed was chosen because it is similar to the speed of spontaneous activity in this species (McKenzie et al. 1995). The following day, the fish were exposed to progressive increments in swimming speed of 0.5 BL·s–1 every 60 min until fatigue. Fish were considered to be fatigued when they were unable to remove themselves from the posterior screen of the swimming chamber despite gentle repeated prodding. Measurements of MO2 were collected at each swimming speed. For each fish, a least squares exponential regression was applied to the relationship between swimming speed and MO2. The y-intercept of the regression equation was taken as the theoretical rate of MO2 of the stationary fish (Brett 1964). This value is considered to be an indicator of metabolic rate in the notional absence of locomotor muscle activity, and hence of maintenance metabolism or SMR (Brett 1964; Fry 1971). Active metabolic rate (AMR) was taken as the maximum MO2 measured during exercise in the last increment entirely completed before fatigue (Fry 1971; Webb 1993). SMR was subtracted from AMR to estimate net aerobic scope (Fry 1971). The value of SMR was also subtracted from the MO2 for each swimming speed to reveal the sturgeon’s net cost of locomotion (Beamish 1978). Mean rates of total and net MO2 were also calculated at each speed for comparison between the two groups. Fish were filmed at each swimming speed (Video 8) to allow counts of tailbeat frequency and gill ventilation frequency. Tailbeat frequency at each speed was used as an index of propulsive muscular power in the two groups, while analysis of ventilation frequency provided insight into the extent to which increases in MO2 were linked to increased ventilatory drive and whether the sturgeon exhibited a transition to ram ventilation during swimming. Mean tailbeat and ventilation frequencies were also calculated for each swimming speed. Maximum sustainable (critical) swimming speed (Ucrit, body lengths per second) was calculated using the equation provided by Brett (1964), which adds the velocity of the most recently completed increment to the product of the incremental increase in velocity (i.e., 0.5 BL·s–1) and the proportion of the final increment completed before fatigue. No correction for the solid blocking effect of the fish was considered, as the total cross-sectional area of the fish did not exceed 5% of that of the swimming chamber (Bell and Terhune 1970). Growth The effects of water salinity on growth were measured on the acclimated animals over a 63-day (9-week) period, during which the sturgeon were fed daily by belt feeder over a 2-h period starting at 17:00 with a ration equivalent to 3% wet body mass. Mass and total fork length of the triplicate groups of tagged individuals in FW and BW were measured at 21-day (3-week) intervals. Cumulative specific growth rate (SGR) was calculated at each interval as percent increase in mass per day. Condition factor (CF) was calculated as 100 × (mass/length3). Swimming respirometry The effects of acclimation to FW or BW on respiratory metabolism and exercise performance were investigated with a Brett-type swim-tunnel respirometer constructed in polyvinyl chloride, acetal, and acrylic material. A circulating flow of water was generated in the tunnel (total volume 49 L) by an acrylic propeller attached to a variable-speed DC permanent magnet motor (Brook Hansen MP 80 115 DH, Bell Electric, Birmingham, U.K.). The voltage delivered to the motor was controlled by a personal computer and Labview software (National Instruments, Austin, Tex.) via a data acquisition interface board (CB 68LP, National Instruments). The voltage was calibrated within Labview in order to deliver controlled water velocities between 10 and 90 cm·s–1. Sturgeon were placed downstream of the propeller in a swimming chamber with a square 225-cm2 cross-sectional area. Vanes were positioned between the propeller and swimming chamber to provide nonturbulent water flow and uniform water velocity across the entire section of the swimming chamber (Steffensen et al. 1984). When sealed, the respirometer permitted measurement of oxygen uptake (MO2) by the sturgeon. A small fraction of the water from the sealed respirometer was siphoned past a Clarke-type polarographic oxygen electrode (model E5041, Radiometer, Copenhagen, Denmark) in a cuvette with the thermostat set to 25°C with a water bath (RCS200, MGW Lauda, Königshofen, Germany). An oxygen meter (model 781, Strathkelvin Instruments, Glasgow, Scotland) displayed the PWO 2 in the respirometer, with the signals recorded by the personal computer and Labview software via the interface board. Information on changes in PWO 2 over time during the period of closed-cycle circulation was stored as text files, and then linear regressions between time and PWO 2 were calculated with a spreadsheet program (Excel 97, Microsoft). The resultant slopes were used to quantify oxygen consumption with appropriate values for fish mass, respirometer water volume, and oxygen solu- Haematological variables To investigate characteristics of osmoregulatory homeostasis in FW versus BW, blood samples (1 mL) were collected from the caudal vein of sturgeon acclimated to the two salinities and plasma © 2001 NRC Canada 3 J:\cjfas\cjfas58\cjfas-06\F01-059.vp Wednesday, May 02, 2001 11:14:09 AM Color profile: Generic CMYK printer profile Composite Default screen McKenzie et al. Table 1. Mean (±SE) mass, length, condition factor (CF), and cumulative SGR in Adriatic sturgeon maintained in either FW or BW at a salinity of 11 g·L–1. Day 0 Mass (g) Length (cm) CF (100 g·cm–3) SGR (%·day–1) FW BW FW BW FW BW FW BW 94±6 112±10 22.6±0.6 23.0±0.7 0.79±0.02 0.86±0.01* Day 21 131±8 163±12 25.1±0.6 26.4±0.7 0.79±0.01 0.83±0.01* 1.64±0.07 2.07±0.15* Day 42 206±12 217±16 28.5±0.6 28.9±0.8 0.85±0.01 0.85±0.02 2.72±0.12 2.26±0.17* Day 63 279±17 290±19 31.9±0.6 32.5±0.7 0.82±0.01 0.81±0.02 2.96±0.11 2.47±0.20* 1107 Note: N = 38 for FW and N = 28 for BW. *Significantly different from the FW group at that time (t test, P < 0.05). Fig. 1. Relationship between swimming speed and MO2 in Adriatic sturgeon acclimated to FW (solid circles) or BW at a salinity of 11 g·L–1 (open circles). For FW, the solid line describes the exponential relationship y = 187e0.308x (R 2 = 0.625, N = 47 observations on eight fish). For BW, the broken line describes the exponential relationship y = 303e0.247x (R 2 = 0.699, N = 43 observations on nine fish). The lines are also described by the linear equations y = 124x + 118 (R 2 = 0.636) and y = 122x + 265 (R 2 = 0.701) for FW and BW, respectively. The asterisks on the abscissa indicate those swimming speeds at which BW sturgeon exhibited a significantly higher mean MO2 than FW fish (t test, P < 0.05). measured with an osmometer (Fiske One-Ten, Fiske Associates, Needham Heights, Mass.); Na+, K+, and Cl– were measured by electrolyte analyser with ion-specific electrodes (SPOTCHEM SE 1510, Menarini, Milan, Italy). Plasma samples were frozen and stored in liquid nitrogen for a maximum of 2 weeks prior to thawing and analysis of lactate with an analytical kit (Sigma Lactate 826B). Following collection of blood samples (and swimming respirometry, as appropriate), the tagged fish were returned to their holding tanks in either FW or BW. There were no mortalities associated with the sampling procedure or swimming experiments. Statistical analysis All statistical analyses were performed with the Sigmastat software package (Jandel Scientific, San Rafael, Calif.). Within the FW or BW group, the changes in meristic variables over time were assessed by one-way analysis of variance (ANOVA) for repeated samples, with a Bonferroni multiple comparisons t test to identify significant differences among means. For any given measurement interval, meristic variables were compared between the FW and BW groups by t test. To describe the relationships between respirometric or performance variables during the exercise protocol, linear, exponential, or power functions were applied and the function with the highest correlation coefficient identified. For any given measurement interval during the exercise protocol, variables were compared between the FW and BW groups by t test. All single variables (e.g., Ucrit) were also compared between the two groups by t test. In all cases, P < 0.05 was taken as the fiducial level of significance. Results During the 70-day period of acclimation to their respective salinities, prior to tagging of the sturgeon and commencement of the growth study, the three tanks of sturgeon in FW exhibited a mean (±SE) cumulative mortality of 15.5 ± 2.2%, significantly lower than the mortality of 37.7 ± 2.3% observed in BW. The mortality was not due to disease but can occur during the early life stages of this species and is presumably a consequence of the paucity of information on optimal husbandry requirements. In particular, the mortality is believed to have been a result of interacting factors related to fry quality following artificial reproduction and the acceptance by fry of artificial feeds. The sturgeon that survive these delicate early stages are extremely robust, and there has been no mortality directly attributable to disease in the populations of A. naccarii currently maintained at La Casella. © 2001 NRC Canada osmolality, Na+, Cl–, and K+ measured. Plasma lactate was also measured to investigate the effects of exercise on anaerobic metabolism. For control samples on fish that had not been exercised, care was taken to avoid any exposure of the sturgeon to air prior to sampling under anaesthesia. Individual fish were gently netted into a bucket underwater, the bucket withdrawn from the tank, 100 mg tricaine methanesulphonate·L–1 added, and the fish then sampled immediately following loss of ventilatory movements. This protocol was followed to ameliorate any confounding effects of acute sampling stress on plasma osmolality and ion concentrations (Di Marco et al. 1999). For animals swum to fatigue, caudal samples were collected immediately following fatigue while the fish were resting passively in the swimming respirometer. Plasma was separated by centrifugation. Plasma osmolality was 4 J:\cjfas\cjfas58\cjfas-06\F01-059.vp Wednesday, May 02, 2001 11:14:10 AM Color profile: Generic CMYK printer profile Composite Default screen 1108 Can. J. Fish. Aquat. Sci. Vol. 58, 2001 Table 2. Mean (±SE) values for selected exercise-related metabolic and performance variables in Adriatic sturgeon acclimated to FW or BW at 11 g·L–1. FW (N = 8) SMR (mg O2·kg–1·h–1) AMR (mg O2·kg–1·h–1) Aerobic scope (mg O2·kg–1·h–1) Maximum tailbeat frequency (Hz) Maximum ventilation rate (beats·min–1) Ucrit (BL·s–1) 216±25 548±61 332±47 3.91±0.14 127±4 3.23±0.24 BW (N = 9) 281±11* 635±22 354±20 4.49±0.17* 146±4* 2.75±0.22 Note: *Significantly different from the FW group (t test, P < 0.05). Fig. 2. Relationship between swimming speed and net cost of locomotion (as MO2) in Adriatic sturgeon acclimated to FW (solid circles) or to BW at a salinity of 11 g·L–1 (open circles). For FW, the solid line describes the power relationship y = 45.8x1.44 (R 2 = 0.656, N = 47 observations on eight fish). For BW, the broken line describes the power relationship y = 93.8x1.22 (R 2 = 0.814, N = 43 observations on nine fish). The asterisks on the abscissa indicate those swimming speeds at which BW sturgeon exhibited a significantly higher mean net cost than FW fish (t test, P < 0.05). Fig. 3. Relationship between tailbeat frequency and swimming speed in Adriatic sturgeon acclimated to FW (solid circles) or to BW at a salinity of 11 g·L–1 (open circles). For FW, the solid line describes the linear relationship y = 1.123x – 1.024 (R 2 = 0.646, N = 49 observations on eight fish). For BW, the broken line describes the linear relationship y = 0.776x – 0.646 (R 2 = 0.714, N = 45 observations on nine fish). The asterisks on the ordinate indicate those swimming speeds at which BW sturgeon exhibited a significantly higher mean tailbeat frequency than FW fish (t test, P < 0.05). Growth At the beginning of the growth study, there were no differences in mean mass, length, or CF among the three FW groups or among the three BW groups. The tagged animals were therefore pooled to represent one group for each salinity. The resultant FW and BW groups had the grand means for mass, length, and CF presented in Table 1. There were no differences in mass or length between fish at the two salinities, but the sturgeon in FW had a significantly lower CF. During the 63-day growth experiment, there were three mortalities in one BW tank and one mortality in each of two FW tanks; mean mortality rate did not differ, therefore, between the salinities. Results reported below only consider those animals that survived the entire growth experiment. Within each salinity group, there were no differences between the three replicate tanks for mean mass, SGR, or CF at any measurement interval during the 63-day growth experiment. Thus, analysis has been restricted to a compari- son of the grand means of all individual FW sturgeon versus all individual BW animals (Table 1). Both groups exhibited significant increases in mass and length; mean mass and length were very similar between the two groups with no significant differences at any measurement interval (Table 1). SGRs were high in both groups, ranging between 1.6 and almost 3%·day–1 (Table 1). At a feeding rate of 3% body mass per day, this represents a feed conversion (i.e., ratio of feed provided to weight gain) of between 0.5 and 1. There were, however, some differences in SGR between the groups, whereby the BW sturgeon grew significantly better than their FW counterparts over the first 21 days, but by 42 days, the FW group exhibited a significantly better growth rate and, when the entire 63-day period was considered, the FW group exhibited a significantly higher overall SGR than the BW fish (Table 1). The difference in CF between FW and BW observed at the beginning of the growth experiment had disappeared by 42 days and, at that time © 2001 NRC Canada 5 J:\cjfas\cjfas58\cjfas-06\F01-059.vp Wednesday, May 02, 2001 11:14:11 AM Color profile: Generic CMYK printer profile Composite Default screen McKenzie et al. Fig. 4. Mean (±SE) gill ventilation rates at increasing swimming speeds in Adriatic sturgeon acclimated to FW (solid circles) or to BW at a salinity of 11 g·L–1 (open circles). For FW, N = 8 from 1 to 3 BL·s–1, N = 5 at 3.5 BL·s–1, and N = 3 at 4 BL·s–1. For BW, N = 9 from 1 to 2.5 BL·s–1, N = 4 at 3 BL·s–1, and N = 3 at 3.5 BL·s–1. The asterisks denote those swimming speeds at which the BW fish had higher ventilation frequencies than FW fish (t test, P < 0.05). 1109 interval and at 63 days, there were no differences in CF among the two salinities (Table 1). Swimming respirometry Effects of salinity acclimation on exercise performance were studied on eight animals from the FW group and nine from the BW group. These had mean (±SE) weights and lengths of 156 ± 12 g and 26.3 ± 0.4 cm and 158 ± 16 g and 26.9 ± 1.0 cm in the FW and BW groups, respectively, with no significant differences between the groups. Stepwise increases in swimming speed elicited an increase in MO2 by the sturgeon from both FW and BW (Fig. 1), with the resultant relationships described almost equally well by a linear or an exponential function. Note that MO2 measured at 0.5 BL·s–1 is not included in the analyses, as data were highly variable at that speed due to differences in spontaneous activity between the sturgeon, which disappeared when current velocity rose to 1 BL·s–1 (Webb 1993). As is clearly visible in Fig. 1, however, there were marked differences in MO2 between the groups, with the BW group showing a curve that was shifted towards higher rates of MO2 at any given swimming speed. Indeed, a comparison between the two groups of mean MO2 at each swimming speed revealed that the fish in BW consumed significantly more oxygen than did those in FW when swimming at all speeds between 1 and 3 BL·s–1 inclusive. Calculation of SMR (Brett 1964) revealed that sturgeon acclimated to BW had a significantly higher SMR than those maintained in FW (Table 2), with an increase of about 30%. AMR was 15% higher in the BW group than in the FW group, but the difference was not statistically significant (P = 0.09) and there were no differences in aerobic scope between the two salinities (Table 2). Figure 2 shows the net cost of locomotion (as MO2) of sturgeon in FW or BW. The relationship between swimming speed and cost of locomotion was best described by a power function in both groups. However, the relationship described by the sturgeon acclimated to BW was shifted noticeably upwards relative to that of the sturgeon maintained in FW, revealing higher net costs for the BW fish when swimming at any given speed. A comparison of mean costs at each speed revealed these to be significantly higher in the BW group when swimming at speeds of 1.5 and 2.0 BL·s–1. Figure 3 shows the relationship between tailbeat frequency and swimming speed in the sturgeon acclimated to the two different salinities. The relationship was best described by a linear function in both FW and BW. As is visible in Fig. 3, however, the relationship described by the sturgeon acclimated to BW is shifted to the right when compared with the relationship for the fish in FW, such that BW sturgeon required higher tailbeat frequencies to achieve any given swimming speed. The mean frequencies were significantly higher in BW fish at all swimming speeds between 1 and 3 BL·s–1 inclusive. The BW group also had a significantly higher maximum tailbeat frequency than that measured in the FW group (Table 2). In both experimental groups, stepwise increases in swimming speed were linked to a significant hyperventilation (Fig. 4). In the FW group, there was a linear increase in ventilation rate with increased swimming speed (Fig. 4). When swimming at low to intermediate speeds, the sturgeon acclimated to BW exhibited significantly higher mean ventilation rates than those in FW (Fig. 4). At the highest speeds, the fish in BW exhibited a decline in ventilatory rate that reflected a partial shift towards ram ventilation (Fig. 4). The change towards ram ventilation at high swimming speeds was, however, only partial, as ventilatory rate remained elevated if compared with the rates measured at the lowest swimming speeds (Fig. 4). The animals of the BW group exhibited a significantly higher maximum ventilation rate than the sturgeon in the FW group (Table 2). Critical swimming speeds for the sturgeon acclimated to the two salinities are presented in Table 2. Although mean Ucrit was 17% higher in FW than in BW, the difference was not statistically significant. Haematological variables Effects of salinity acclimation on haematological variables in sturgeon without exercise (i.e., under resting conditions) were studied on six animals from each of the FW and BW groups. These had mean (±SE) masses of 167 ± 15 and 163 ± 17 g in the FW and BW groups, respectively, with no significant difference between the groups. Plasma osmolality and ion concentrations are presented for the BW and FW sturgeon in Table 3. Plasma osmolality was equal in both groups, but the sturgeon acclimated to BW had slightly but significantly higher plasma Na+ and Cl– concentrations than those in FW. Plasma osmolality in the FW and BW sturgeon following exercise to fatigue was not significantly different from the values measured in resting fish from the same group, but because mean osmolality decreased in FW and increased in BW, osmolality was significantly higher in the BW sturgeon postexercise as compared with the FW fish (Table 3). Exer© 2001 NRC Canada 6 J:\cjfas\cjfas58\cjfas-06\F01-059.vp Wednesday, May 02, 2001 11:14:12 AM Color profile: Generic CMYK printer profile Composite Default screen 1110 Can. J. Fish. Aquat. Sci. Vol. 58, 2001 Table 3. Mean (±SE) plasma osmolality, ion concentrations, and lactate concentration in Adriatic sturgeon acclimated to either FW or BW at 11 g·L–1 at rest and following exercise to fatigue. FW Rest (N = 6) Osmolality (mosmol·kg ) Na+ (mequiv.·L–1) Cl– (mequiv.·L–1) K+ (mequiv.·L–1) Lactate (mmol·L–1) –1 BW Fatigue (N = 8) 267±7 138±2 117±4 3.7±0.2 1.41±0.63# Rest (N = 6) 278±5 146±2* 133±4* 3.8±0.2 0.70±0.03 Fatigue (N = 9) 302±10* 151±2*# 139±4*† 4.1±0.2 1.58±0.48# 277±3 138±1 115±2 4.0±0.2 0.58±0.05 Note: *Significantly different from the FW group under the same conditions; #significantly different from the resting value in the same group; †significantly different from the resting value in the FW group (one-way ANOVA, P < 0.05). cise caused a significant increase in plasma Na+ and Cl– levels in BW sturgeon but not in FW fish. As a consequence, the exercise exacerbated the differences in Na+ and Cl– concentrations between the two groups (Table 3). There were no differences in plasma lactate among the groups under resting conditions, and exercise caused a significant increase in plasma lactate concentrations in both groups (Table 3). Discussion The poorer survival and growth rates of the YOY sturgeon acclimated to a water salinity of 11 g·L–1 as compared with their siblings maintained in FW clearly indicate that mildly hypertonic BW is a less optimal environment than FW for sturgeon of that age and (or) size. A previous growth study on this species at approximately the same age found a marked inhibition of growth in sturgeon acclimated for 2 months to BW at 20 g·L–1, SGR fell by 56% relative to siblings maintained in FW, and the animals in BW exhibited 100% mortality following the use of heavy machinery near their tanks (McKenzie et al. 1999). The current study found a 17% inhibition of SGR in BW at 11 g·L–1, and mortality in BW was over twice that in FW. The reduced growth rate in BW can be attributed to the increased SMR and therefore energetic costs for maintenance metabolism in that environment. The increased SMR may represent the metabolic cost of osmoregulation. There are, however, a number of reasons why this is unlikely to have been the case. The osmolality of the BW in the present study (approximately 310 mosmol·kg–1) only exceeded that of sturgeon plasma by about 10%, so the costs of osmoregulation should in fact have been reduced in the BW relative to FW. YOY sturgeon acclimated for 6 weeks to BW at 11 g·L–1 do not exhibit a significant difference from their FW siblings with regard to the activity of the Na+,K+-ATPase in crude gill homogenates (McKenzie et al. 1999). Furthermore, in teleosts, the costs of osmoregulation may in fact be very low (Kirschner 1995; Morgan and Iwama 1999), and rates of oxygen consumption do not always reflect expected costs of osmoregulation (Morgan and Iwama 1998). Indeed, although early studies reported lower metabolic rates and improved growth in salmonids acclimated to BW at an osmolality approaching that of their body fluids (Canagaratnam 1959; Rao 1968), the consensus to emerge from more recent studies is that salmonid fry and parr will exhibit elevated metabolic rate and poor growth in salinities other than the natural one typical for their life stage at that time, even in salinities almost isotonic with their plasma (Morgan and Iwama 1991). Morgan and Iwama (1991, 1998, 1999) argued that the increased SMR and poor growth that are observed in juvenile salmonids maintained at inappropriate salinities reflect influences on metabolism other than metabolic costs for fluid and ion homeostasis. For example, chronic stress-related activation of the hypothalamic–pituitary axis is known to raise metabolic rate and inhibit growth in teleosts (Wendelaar Bonga 1997). Although the stress of handling and anaesthesia caused a marked increase in plasma cortisol in adult Adriatic sturgeon (Di Marco et al. 1999), YOY sturgeon acclimated for 6 weeks to salinities of 11 and 23 g·L–1 exhibited no differences in plasma cortisol concentrations relative to their siblings in FW (McKenzie et al. 1999). Thus, the increased metabolic rate and reduced growth of the sturgeon in BW may reflect other effects of chronic sublethal stress. Morgan and Iwama (1991) reviewed the literature regarding the effects of salinity on metabolic rate in euryhaline teleosts and proposed that they be grouped into five classes. Class III includes the presmolt stages of anadromous salmonids, for whom metabolic rate is lowest in FW and increases in waters of higher salinities (Morgan and Iwama 1991). The results of the current study would seem to place YOY Adriatic sturgeon in the same class, as BW at a salinity of 11 g·L–1 elicited a significant increase in SMR and inhibition of growth. The estimation of maximum sustainable aerobic swimming speed for the Adriatic sturgeon is the first such report for a chondrost and acipenserid. Critical swimming speed in FW was estimated to be about 15% lower than that of sockeye salmon (Oncorhynchus nerka) of similar length (Brett 1965). Webb (1986) reported that lake sturgeon (Acipenser fulvescens) exhibits swimming kinematics that are similar to those of teleosts but that the thrust generated at cruising speeds is 18% less than in similar-sized trout, presumably as a consequence of the heterocercal acipenserid caudal fin. The lake sturgeon’s capacity for burst exercise, namely exercise fueled by anaerobic processes for short periods at high speeds (Beamish 1978), is significantly inferior to that of similar-sized salmonids (Peake et al. 1997). The shallow relationship between swimming speed and log MO2 in both FW and BW may indicate that sustained aerobic exercise in sturgeon is energetically quite efficient (Beamish 1978). McKinley (1991) reported that the relationship between swimming speed and MO2 was best described by a linear equation in lake sturgeon. Although an exponential relationship should be expected for energetic reasons © 2001 NRC Canada 7 J:\cjfas\cjfas58\cjfas-06\F01-059.vp Wednesday, May 02, 2001 11:14:13 AM Color profile: Generic CMYK printer profile Composite Default screen McKenzie et al. 1111 (Fry 1971; Beamish 1978), this is not necessarily the case for all teleost species (Webb 1993). Nonetheless, when the net cost of locomotion was calculated, it was best described by a power function, which is the expected energetic relationship (Beamish 1978). If confirmed in future studies, the apparent energetic efficiency of sustained aerobic swimming in sturgeon would be of obvious adaptive advantage to species that perform repetitive long annual migrations between FW and saline environments. Salinity acclimation had marked effects on swimming performance and respiratory metabolism in the sturgeon. The increased rates of MO2 during swimming in the fish adapted to BW relative to those in FW will have been, in part, a consequence of the increased SMR in the BW fish. However, the significantly higher net costs of locomotion in the BW sturgeon will also have contributed to the elevated MO2 during swimming in that group. The net costs of locomotion are presumably to be attributed to the costs of muscular work, and, indeed, the fish in BW exhibited significantly higher tailbeat frequencies at all speeds compared with those in FW. The increased tailbeat frequencies of the BW fish must indicate that muscular power is influenced by water salinity, presumably also as a consequence of sublethal stress. Nonetheless, despite the metabolic load imposed by raised SMR, their increased costs of locomotion, and their reduced propulsive power, the BW animals were able to avoid a significant inhibition of Ucrit by increasing their maximum ventilation rate, AMR, and tailbeat frequency above those of their FW siblings. That is, although the difference in AMR between the BW and FW sturgeon was not statistically significant, it could be argued that it was physiologically significant in maintaining aerobic scope and avoiding a decline in maximum performance. This adaptive strategy reveals the importance of swimming performance to the sturgeon in their natural environment. Some portion of the reduced growth rate may have been a consequence of the increased costs of locomotion in the sturgeon in BW, since captive Adriatic sturgeon exhibit constant spontaneous swimming activity at a speed of between 0.2 and 0.5 BL·s–1 (McKenzie et al. 1995). Exercise was linked to a similar increase in plasma lactate concentration in both groups. This indicates that the increased maximum tailbeat frequency of the BW compared with the FW animals may not have been associated with increased reliance on anaerobic metabolism. Indeed, plasma lactate concentrations following exercise to exhaustion were much lower than the concentrations that are measured during exposure to graded hypoxia in this species (McKenzie et al. 1997). Although the BW animals regulated plasma osmolality at levels similar to those of their FW counterparts, they exhibited increased plasma Na+ and Cl– concentrations. This may be another indication that they are in a nonoptimal osmotic environment. It is unknown what other osmolyte was regulated to maintain osmolality unchanged when the ion concentrations increased. Exercise caused a significant increase in plasma osmolality in the BW animals. This may indicate movements of water between plasma and the intracellular compartment or changes in gill permeability during maximal exercise. In conclusion, BW at 11 g·L–1 was clearly a less optimal environment than FW for YOY Adriatic sturgeon, causing an inhibition of growth, increased metabolic rate, and increased costs of swimming. This result is consistent with previous studies indicating only partial adaptation to hyperosmotic environments by juvenile Adriatic sturgeon (Cataldi et al. 1995, 1999; McKenzie et al. 1999). All the evidence collected to date contrasts with the anecdotal reports of egg deposition in brackish estuarine waters in this species (Paccagnella 1948). Nonetheless, that larger sturgeon have been captured in the Adriatic sea (Tortonese 1989) indicates that salinity tolerance may increase with age and size, as is known to be the case for other sturgeon species (MacEnroe and Cech 1985). 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