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First published online September 19, 2006
Journal of Experimental Biology 209, 3940-3951 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02440

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Cardiorespiratory physiology and swimming energetics of a high-energy-demand teleost, the yellowtail kingfish (Seriola lalandi)

T. D. Clark^* and R. S. Seymour

Earth and Environmental Sciences, University of Adelaide, South Australia 5005, Australia

^* Author for correspondence (e-mail: timothy.clark{at}adelaide.edu.au)

Accepted 12 July 2006

	Summary

TOP Summary Introduction Materials and methods Results Discussion References

 
This study utilizes a swimming respirometer to investigate the effects of exercise and temperature on cardiorespiratory function of an active teleost, the yellowtail kingfish (Seriola lalandi). The standard aerobic metabolic rate (SMR) of S. lalandi (mean body mass 2.1 kg) ranges from 1.55 mg min^-1 kg^-1 at 20°C to 3.31 mg min^-1 kg^-1 at 25°C. This 2.1-fold increase in SMR with temperature is associated with a 1.5-fold increase in heart rate from 77 to 117 beats min^-1, while cardiac stroke volume remains constant at 0.38 ml beat^-1 kg^-1 and the difference in oxygen content between arterial and mixed venous blood [(Ca_O2-C_O2)] increases marginally from 0.06 to 0.08 mg ml^-1. During maximal aerobic exercise (2.3 BL s^-1) at both temperatures, however, increases in cardiac output are limited to about 1.3-fold, and increases in oxygen consumption rates (up to 10.93 mg min^-1 kg^-1 at 20°C and 13.32 mg min^-1 kg^-1 at 25°C) are mediated primarily through augmentation of (Ca_O2-C_O2) to 0.29 mg ml^-1 at 20°C and 0.25 mg ml^-1 at 25°C. It seems, therefore, that the heart of S. lalandi routinely works close to its maximum capacity at a given temperature, and changes in aerobic metabolism due to exercise are greatly reliant on high blood oxygen-carrying capacity and (Ca_O2-C_O2). Gross aerobic cost of transport (GCOT) is 0.06 mg kg^-1 BL^-1 at 20°C and 0.09 mg kg^-1 BL^-1 at 25°C at the optimal swimming velocities (U) of 1.2 BL s^-1 _opt and 1.7 BL s^-1, respectively. These values are comparable with those reported for salmon and tuna, implying that the interspecific diversity in locomotor mode (e.g. subcarangiform, carangiform and thunniform) is not concomitant with similar diversity in swimming efficiency. A low GCOT is maintained as swimming velocity increases above U_opt, which may partly result from energy savings associated with the progressive transition from opercular ventilation to ram ventilation.

Key words: cardiac output, cardiac stroke volume, heart rate, aerobic metabolism, rate of oxygen consumption, teleost, temperature, tissue oxygen extraction

	Introduction

TOP Summary Introduction Materials and methods Results Discussion References

 
Metabolic studies of highly active teleost fishes are inherently difficult due to their pelagic life history and often large body mass (M_b). Nevertheless, progressive technological advances have permitted the study of several (usually juvenile) high performance species (Brett, 1965; Brett and Glass, 1973; Sepulveda and Dickson, 2000; Dickson et al., 2002; Lee, C. G. et al., 2003; Dabrowski et al., 2004), including the exceptionally active tunas (Dewar and Graham, 1994; Korsmeyer et al., 1997a; Korsmeyer et al., 1997b). Current data imply that high-energy-demand fish, particularly the tunas, have an enhanced standard aerobic metabolic rate (SMR) when compared with more sedentary species, presumably to support energetically expensive morphological and physiological adaptations and allow an increased aerobic metabolic scope (Brill and Bushnell, 1991; Korsmeyer and Dewar, 2001; Graham and Dickson, 2004).

While we are beginning to obtain a better understanding of the basic metabolic requirements of high-energy-demand teleosts, the necessity to instrument animals for circulatory measurements has resulted in a limited understanding of the cardiorespiratory adaptations that allow such an enhanced metabolic capacity. Aerobic metabolic rate, as indicated by the rate of oxygen consumption (_O2), may be enhanced at the circulatory level by augmentation of any of the variables contributing to the Fick equation:

(1)

where _b is cardiac output [the product of heart rate (f_H) and cardiac stroke volume (V_S)], and (Ca_O2-C_O2) is the difference in oxygen content between arterial (Ca_O2) and mixed venous (C_O2) blood (a measure of tissue oxygen extraction). The initial indication was that, unlike other vertebrates, teleost fish modulate _b primarily through changes in V_S rather than f_H (Stevens and Randall, 1967; Kiceniuk and Jones, 1977; Farrell and Jones, 1992), although the reverse is true for some species, particularly those considered to be of high energy demand (Axelsson et al., 1992; Korsmeyer et al., 1997a; Altimiras and Larsen, 2000; Cooke et al., 2002; Graham and Dickson, 2004; Clark et al., 2005). Some high performance species possess an enhanced blood oxygen-carrying capacity owing to higher levels of haemoglobin, which acts to augment (Ca_O2-C_O2) such that extraordinary increases in _b are not necessary to attain maximum levels of _O2 (Brill and Bushnell, 2001; Graham and Dickson, 2004). Nevertheless, many teleosts utilize similar proportional increases in _b and (Ca_O2-C_O2) to satisfy an increase in _O2 with exercise (Brill and Bushnell, 1991; Bushnell and Jones, 1994; Korsmeyer et al., 1997b).

The genus Seriola (amberfishes, amberjacks, and yellowtails) has a circumglobal distribution and comprises several species of highly active predatory marine fish, which may exceed 2 m in length and M_b of around 80 kg (Gillanders et al., 2001; Poortenaar et al., 2001). Members of this genus utilize a carangiform swimming mode, are facultative ramventilators, and share many specialized morphological adaptations with the tunas, including a fusiform body shape to reduce drag, fin grooves to increase streamlining, a highaspect-ratio tail with a narrow caudal peduncle, and finlets along the trailing edges of the body (Dewar and Graham, 1994). The limited cardiorespiratory data that exist for the Seriola genus have been obtained exclusively from studies on S. quinqueradiata (commonly referred to as `yellowtail'), which is an inhabitant of the northwestern Pacific Ocean. This species has been reported to have a SMR greater than most other high performance fishes and approaching that of the tunas (Yamamoto et al., 1981; Korsmeyer and Dewar, 2001), although these data may have been affected by stress due to heavy instrumentation and confinement to a small static respirometer. Interestingly, the published resting f_H value of this species at 25°C is approximately 90 beats min^-1 (Ishimatsu et al., 1990; Lee, K. S. et al., 2003a), which is quite high for a resting teleost, and may reflect a high maximum f_H considering that a twofold increase during exercise is not uncommon (Bushnell and Jones, 1994; Korsmeyer et al., 1997a; Altimiras and Larsen, 2000; Clark et al., 2005).

Given these previous findings for Seriola, it appears that members of this genus may have enhanced aerobic metabolic capacities and may prove to be useful models for the study of exercise physiology in high-energy-demand teleosts. The present study utilizes a temperate species, S. lalandi (commonly referred to as `yellowtail kingfish'), to investigate cardiorespiratory function at rest and while exercising in a custom-built swimming respirometer. Several hypotheses relating to high-energy-demand teleosts are tested, specifically that S. lalandi has (1) an exceptionally high SMR, (2) an enhanced aerobic metabolic scope, (3) a substantial contribution from f_H to attain the required _O2, and (4) a low cost of transport resulting from specialized adaptations presumed to increase swimming efficiency.

	Materials and methods

TOP Summary Introduction Materials and methods Results Discussion References

 
Animals
Ten yellowtail kingfish Seriola lalandi (Valenciennes 1833) were studied between 10 November 2005 and 10 January 2006. Fish eggs were originally purchased from Clean Seas Aquaculture (Arno Bay, South Australia) in February 2004 and transported to the South Australian Research and Development Institute where they were hatched. The larvae were weaned in larval tanks, and eventually relocated to a 40 000 l holding tank where they were raised on commercial pellets (Skretting, Cambridge, Tasmania) to a body mass of approximately 2 kg. The holding tank was of ample volume and had a mild circular flow, which allowed the fish to form schools and cruise at their desired swimming velocities during this rearing period. At least 3 days prior to commencing experiments, the fish were moved to 1000 l indoor tanks at the same water temperature to which they were exposed outdoors (approximately 20°C), and on a 13 h:11 h light:dark cycle that resembled day length patterns for this time of year. Fish were fed once per day, but were fasted for at least 30 h prior to use in experiments, to eliminate the influence of specific dynamic action on the measurements. All experiments were conducted under project number S-024-2005 with the approval of the University of Adelaide Animal Ethics Committee.

Swimming respirometer
Measurements of _O2 at different swimming velocities were performed in a constant temperature room using an upright Brett-type swimming respirometer (water volume 137 l), which was constructed at La Trobe University in Melbourne, Australia. The respirometer was constructed from Perspex^TM tubing (250 mm internal diameter) and the fish was restricted to an 850 mm long transparent working section at the top. The entire respirometer sat within an aerated waterbath (length 1500 mm, width 300 mm, height 1200 mm; replaced with fresh seawater at 2 l min^-1), which provided thermal stability and a source of oxygenated water to flush the respirometer between measurements. Water velocity through the respirometer was regulated by a 245 mm diameter propeller, which was positioned at one end of the respirometer and connected via a stainless steel shaft to a computer-driven DC motor (Baldor, VPT 34550; interfaced with 0-10 V external Penta Drive Regenerative speed controller) mounted above the waterbath. Voltage to the motor was calibrated against water velocity through the center of the working section using a flow meter (model OSS-PC1, Hydrological Services, Australia), and the maximum attainable water velocity was 1.22 m s^-1. A submersible pump with a one-way valve, positioned at the bottom of the respirometer, provided the only interface between the water in the respirometer and that in the waterbath, and computer control of the submersible pump (using a voltage output from PowerLab; see below) allowed the respirometer to be automatically flushed and sealed continuously at predefined intervals. The volume of water pumped into the respirometer by the submersible pump was released through a pipe at the top of the respirometer that extended above the water line of the waterbath. Water temperature and oxygen saturation in the respirometer were continuously monitored using a calibrated sensor (sc100 LDO, Hach, USA), and outputs from this, and a measure of the voltage supplied to the propeller motor and submersible flushing pump, were collected at 100 Hz (PowerLab/4SP and Chart software, ADInstruments, Sydney, Australia).

Instrumentation
Ventilation rate
Concurrently with measuring _O2, it was of interest to determine how opercular ventilation rate (f_G) changed with swimming speed in this facultative ram-ventilating species. Therefore, before being introduced into the respirometer, each fish (N=6; M_b ± s.e.m.=1.90±0.12 kg; length=543±8 mm) underwent the following procedure in order to measure the electromyographic (EMG) signal produced from the opercular muscles. A fish was caught by dip net and placed in a tub (length 1500 mm, width 700 mm, height 700 mm) containing 100 l seawater and 1 ml l^-1 of anaesthetic (2-phenoxyethanol, Ace Chemicals, Camden Park, SA, Australia) at 20°C. When ventilation became shallow and the fish lost responsiveness to touch (10 min), it was weighed, measured and positioned between two foam pads on an operating bench. Ventilation of the gills with aerated seawater and a lower dose of anaesthetic (0.75 ml l^-1) was continued throughout the procedure by way of a recirculation system and a hose positioned in the mouth of the fish.

Approximately 10 mm of insulation was stripped from the ends of two 1 m lengths of otherwise insulated stainless steel electrode wire (diameter 0.25 mm). These ends were threaded through 18 G hypodermic needles that had been positioned subcutaneously approximately 400 mm apart along the ventral midline between the two gills. The needles were then removed along the length of the wire, which left the two wire electrodes in place. Each length of electrode wire was sutured to the skin at the point of insertion, led up opposite sides of the body and secured beside the first dorsal fin. This procedure took a maximum of 7 min.

The fish was then placed in the respirometer at 20°C at a slow water velocity (0.3-0.7 BL s^-1). Assisted ventilation with aerated seawater was continued until the fish displayed strong opercular movements and began to right itself. The loose ends of the wire electrodes were passed through a small tube at the top of the respirometer that extended above the waterline of the waterbath. The EMG signal was amplified (BioAmp, ADInstruments, Sydney, Australia) and recorded using the PowerLab. Following swimming trials, wire electrodes were removed and the fish released into the holding tank.

Cardiac output
Four different fish (M_b=2.35±0.31 kg; length=569±26 mm), but from the same cohort as those detailed above, were available to measure cardiac output using ventral aortic flow cuffs. Fish were anaesthetized as described above. One operculum and underlying gills were held back with a piece of soft plastic, and the ventral aorta was exposed through a 10 mm incision made on the lateral wall of the isthmus at the ventral base of the first and second gill arches. The ventral aorta was freed of surrounding connective tissue and a silastic Doppler flow cuff (20 MHz, internal diameter 4-5 mm, Indus Industries, Baylor College of Medicine, Houston, TX, USA) secured around the blood vessel. The incision was closed with sutures and the leads from the cuff secured to the skin on the fringe of the opercular cavity, again near the lateral midline, and finally beside the first dorsal fin. The whole procedure was completed within 30-45 min. The fish was then placed in the respirometer at 20°C, where it received the same treatment as detailed above. The leads from the flow cuff were passed through the small tube at the top of the respirometer, connected to an Ultrasonic Flow/Dimension System (Indus Industries) and the signal collected at 100 Hz.

Following swimming trials, fish were euthanised with an overdose of anaesthetic and the flow cuff was calibrated in situ. An 18 G hypodermic needle was inserted into the bulbus arteriosus posterior to the flow cuff and blood was collected in a flask. Another needle was inserted into the ventral aorta just anterior to the flow cuff, then blood was circulated through the needles in an anterior direction at known flow rates using a peristaltic pump (IsmaTec SA, Glattbrugg, Switzerland). The outlet tube connected to the needle in the ventral aorta was raised by 300 mm such that the blood vessel had a back pressure of 3 kPa. Individual calibration equations (mean r²=0.84) were then applied to the data set for that individual, and cardiac output was calculated as ml min^-1 kg^-1. Finally, the heart was excised, then the ventricle was detached, rinsed with saline, and weighed in relation to total body mass.

Swimming protocol
Resting values for each individual at 20±0.5°C were obtained only following at least 24 h of recovery in the respirometer, when all measured variables had stabilized. Rates of oxygen consumption were repeatedly measured as the fish was exposed to incremental changes in water velocity. Some fish instrumented with EMG electrodes were incremented beyond their maximum sustainable swimming velocity (characterized by vigorous burst episodes and subsequent resting against the grid at the posterior end of the respirometer; typically 2.3 BL s^-1), whereas fish instrumented with flow cuffs were exposed only to sustainable velocities so as to minimize the risk of damage to the ventral aorta. Each _O2 measurement was performed over a 10 min period so that oxygen saturation in the respirometer never fell below 75%, and the respirometer was flushed for 20 min between each measurement with oxygenated water from the waterbath. Fish were maintained at each swimming velocity for at least 60 min (i.e. two measurement cycles) to ensure that all variables had reached a steady state (this excludes speeds greater than 2.3 BL s^-1 where fish were unable to maintain position for more than 10 min). Swimming speed was corrected for the solid blocking effect of each individual using the method described elsewhere (Jones et al., 1974), which increased swimming speed measurements by 10-24%. Several fish struggled immediately when water velocity was increased above that used to obtain resting values (i.e. 0.3-0.7 BL s^-1). In such circumstances, water velocity was rapidly increased to a high, yet sustainable level, to encourage a greater level of exercise, and fish were maintained at this velocity until _O2 plateaued. Some individuals swam at intermediate speeds in later attempts (after a sufficient recovery period), but the number of steady state data points able to be obtained from each individual (minimum 3 velocities, maximum 6 velocities) was reliant upon how well they adjusted to swimming in the respirometer (sample sizes are indicated in tables and figures).

Water heating equipment became available towards the end of this study. Thus, to examine the effect of temperature on cardiorespiratory function, two of the fish that had been instrumented with a flow cuff were maintained at 0.3-0.7 BL s^-1 in the respirometer after the 20°C swimming protocol while the water was heated from 20°C to 25±0.5°C (taking approximately 3 h). Fish were given at least 2 h to acclimate to the new temperature (also to ensure complete recovery from the previous swim at 20°C), and then the same swimming protocol was performed as outlined above.

Data analysis and statistics
Rates of oxygen consumption (given as mass-specific values and at STPD) were calculated using the rate of decline in oxygen saturation in the respirometer over the final 7 min of each 10 min measurement. Calculations took account of the effect of temperature on the oxygen capacitance of the water (Dejours, 1975). The respirometer was regularly sealed without containing a fish, to determine background respiration rates and subsequently correct _O2 measurements of the fish, although the reduction in oxygen saturation during these trials was in all cases negligible.

Tissue oxygen extraction was calculated by rearrangement of Eqn 1, such that _O2(mg min^-1 kg^-1)/_b (ml^-1 min^-1 kg^-1)= (Ca_O2-C_O2)(mg ml^-1). Heart rate was obtained by triggering a rate-meter linked with the output from the flow cuff, and cardiac stroke volume was calculated by dividing _b by f_H. Gross aerobic cost of transport (GCOT) was calculated by dividing each _O2 value by the swimming velocity (U) at which the measurement was obtained, and net aerobic cost of transport (NCOT) was calculated from (_O2-SMR)/U.

Least-squares regressions were used where appropriate, and comparisons of slopes and elevations were performed using analysis of covariance (ANCOVA). Significance was considered at P<0.05. Data are presented as mean ± standard error of the mean (s.e.m.). Minimum and maximum values are denoted by the subscripts min and max, respectively. N=number of animals, n=number of data points.

Critique of methods
The automated method of controlling the respirometer and collecting data allowed for long periods of steady state swimming from undisturbed fish. Thus, although the sample size was low (N=2) for fish at 25°C, we believe that the data obtained are representative of the species in general. In support of this, the 25°C data displayed solid trends that were consistent with those obtained from fish at 20°C (Fig. 1), and these data compare favourably to values obtained from the closely related S. quinqueradiata at the same temperature (see Discussion). Although it was not determined if fish at 25°C were capable of sustained swimming at velocities in excess of 2.3 BL s^-1, similar swimming characteristics (e.g. occasional burst-andglide episodes) were displayed by all fish around this speed, irrespective of temperature, and we believe that the acute temperature change utilized in this study has a negligible influence on maximum sustainable swimming velocity.

View larger version (24K): [in this window] [in a new window]   Fig. 1. (A) Rate of oxygen consumption (O2), (B) cardiac output (b), (C) heart rate (fH), (D) cardiac stroke volume (VS), and (E) tissue oxygen extraction [(CaO2-CO2)] as a function of swimming velocity for Seriola lalandi. The triangle, circles and bold regression lines represent animals at 20°C [(A) N=10; (B-E) N=4], while squares and broken regression lines represent animals at 25°C (N=2). Open symbols are from animals instrumented with EMG electrodes, whereas symbols containing crosses are from animals instrumented with a blood flow cuff. The hatched vertical line represents the approximate maximum sustainable swimming velocity (Umax), about 2.3 BL s-1. Given the lack of steady state swimming at speeds greater than 2.3 BL s-1, O2 data from four animals that swam for short periods at velocities in excess of this value were pooled and are presented in A as mean ± s.e.m. (open triangle). Dotted lines are extrapolations of regression lines to the vertical axis. Regression equations are given in Table 1.

	Results

TOP Summary Introduction Materials and methods Results Discussion References

Zero swimming velocity
Two individuals instrumented with EMG electrodes at 20°C opted to rest on the bottom of the respirometer when exposed to a slow water velocity (0.42 BL s^-1 on both occasions), rather than gently swimming against the water flow as did all other individuals. Consequently, the resting _O2 data points from these two animals can be included in the regression as zero swimming velocity at 20°C, thus alleviating the need to extrapolate this regression to the vertical axis, as was the case with all other variables at both temperatures (Fig. 1, Table 1). It should be noted that these two individuals were in perfect health and swam just as well as all other fish when water velocity was increased.

The rate of oxygen consumption at 0 BL s^-1 (i.e. SMR) increased 2.1-fold (Q₁₀=4.5) from 1.55 mg min^-1 kg^-1 at 20°C to 3.31 mg min^-1 kg^-1 at 25°C (Fig. 1A, Table 2). The increase in _O2 with temperature was mediated primarily through a significant 1.5-fold increase in _b (P<0.01), which itself was governed solely by an increase in f_H while V_S remained statistically unchanged. The blood convection requirement (_b/_O2) decreased with an increase in temperature and, correspondingly, (Ca_O2-C_O2) increased by a similar proportion (Fig. 1, Table 2). Opercular ventilation rate (f_G) at 20°C was 72.2±3.8 strokes min^-1 at 0 BL s^-1 (Fig. 2B).

View larger version (22K): [in this window] [in a new window]   Fig. 2. Relationship of (A) rate of oxygen consumption (O2), (B) opercular ventilation rate (fG), (C) net aerobic cost of transport (NCOT), and (D) gross aerobic cost of transport (GCOT) as a function of swimming velocity (up to 2.3 BL s-1) for Seriola lalandi at 20°C and 25°C (symbols as in Fig. 1). In A, the slopes at the tangent to the curves from the origin (bold broken lines) are equal to the optimum swimming velocity (Uopt), which occurs where GCOT is at a minimum (GCOTmin) (illustrated by vertical dotted lines). In B, data have been binned into increments of 0.25 BL s-1 and symbols represent means ± s.e.m. (N=6, n=45).

Effects of exercise
At 20°C, _O2 increased exponentially with swimming velocity up to approximately 2.3 BL s^-1, after which _O2 plateaued (_O2max) and swimming often became more erratic and interspersed with burst episodes. For this reason, it was considered hazardous to expose fish instrumented with flow cuffs to swimming velocities greater than 2.3 BL s^-1, so data at speeds above this are exclusively from animals instrumented with EMG electrodes at 20°C (Fig. 1A). Fish at 25°C displayed a similar exponential pattern of increasing _O2 with swimming velocity; however, this was elevated in comparison with fish at 20°C (P<0.01). Although it was not determined if fish at 25°C were capable of sustained swimming at velocities in excess of 2.3 BL s^-1, behavioural observations indicated that this was unlikely and, consequently, the maximum sustainable swimming velocity (U_max) is considered herein to be 2.3 BL s^-1 at both temperatures.

The absolute aerobic scope (_O2max-SMR) remained essentially unchanged across temperature at approximately 9.5 mg min^-1 kg^-1, hence the factorial aerobic scope (_O2max/SMR) decreased substantially from 7.0 at 20°C to 4.0 at 25°C (Table 2). At both temperatures, a slight (1.3-fold) linear increase in f_H was solely responsible for the linear rise in _b with exercise, although this increase was insufficient (as indicated by a large drop in _b/_O2), and a substantial exponential increase in (Ca_O2-C_O2) (up 4.7-fold at 20°C, up 3.3-fold at 25°C) was necessary to obtain the required level of _O2 (Fig. 1, Table 2). A multiple linear regression analysis revealed that (Ca_O2-C_O2) accounted for 79% of the variability in _O2 (r²=0.79). The addition of f_H (r²=0.98) and V_S (r²=0.99) strengthened the relationship, while the addition of water temperature had no effect. Opercular ventilation rate at 20°C increased linearly with water speed until it reached 88.5 strokes min^-1 at approximately 1 BL s^-1, after which the rate and amplitude of the opercular stroke declined rapidly as the fish became progressively more reliant on ram ventilation (Fig. 2B).

Aerobic cost of transport
The gross aerobic cost of transport (GCOT) was always higher at 25°C, but at both temperatures changed in a somewhat shallow U-shaped relationship with swimming velocity (Fig. 2D). Nevertheless, minimum values of GCOT (GCOT_min) occurred at the optimal swimming velocities (U_opt) of 1.2 BL s^-1 at 20°C and 1.7 BL s^-1 at 25°C. Interestingly, GCOT_min was at the point when f_G was at approximately 50% of its maximum attainable value, and it could be suggested that the energy saved from the transition from one method of ventilation to the other is at least partially causal to the plateaued relationship displayed between GCOT and swimming velocity above U_opt. Some of the variation in GCOT with temperature is likely attributable to the effect of temperature on SMR, although, even when accounting for SMR by calculating the net aerobic cost of transport (NCOT), the efficiency of swimming was still greater at the cooler temperature (Fig. 2C).

	Discussion

TOP Summary Introduction Materials and methods Results Discussion References

 
Many physiological parameters of high performance fish are not well defined due to the logistical constraints in working with them, so a great deal is still to be learnt of the adaptive mechanisms that allow these species to exploit the open oceans. The present study exposed S. lalandi to changes in swimming velocity and temperature in order to investigate several generalizations relating to the cardiorespiratory physiology of high-energy-demand teleosts. It was hypothesized that S. lalandi would have a high SMR, an enhanced aerobic metabolic scope mediated largely through increases in f_H, and a low cost of transport resulting from morphological adaptations to reduce hydrodynamic resistance.

Standard metabolic rate
Standard metabolic rate is defined as the resting and fasting metabolism at a given temperature and is theoretically the minimum sustainable metabolic rate (Dejours, 1975; Korsmeyer and Dewar, 2001). Measurements of SMR in active species of fish are often difficult, if not impossible, because many fish maintain a routine swimming velocity. Nevertheless, several studies have estimated SMR of high-energy-demand species using fish immobilised by neuromuscular or spinal block, or by extrapolating _O2 and swimming velocity relationships to zero swimming speed (Brill, 1987; Graham et al., 1989; Dewar and Graham, 1994; Clark et al., 2005). The present study lends support to the latter method in that the regression used to predict SMR at 20°C gives a value only 6% different when including or excluding the two data points obtained at zero swimming velocity (Fig. 1A).

The mass-specific SMR of S. lalandi at 20°C (1.55 mg min^-1 kg^-1) is lower than that reported previously for the closely related S. quinqueradiata at a similar temperature (2.45 mg min^-1 kg^-1) (Yamamoto et al., 1981). It seems, however, that SMR of the Seriola genus is somewhat enhanced in comparison with that of many other active species, and it thus approaches values reported for tunas (Fig. 3A). Interestingly, if data from all species are standardised to 25°C assuming a Q₁₀ of 2.5, the difference between SMR of tunas and other active teleosts becomes much less evident with increasing M_b (Fig. 3B). Nevertheless, given that members of the Seriola genus share many adaptations with the tunas, but presumably lack the same thermoregulatory capacity (Dewar et al., 1994), these data provide further evidence that fishes can have a high SMR without the elevated tissue temperatures associated with regional endothermy (Korsmeyer and Dewar, 2001; Sepulveda et al., 2003).

View larger version (26K): [in this window] [in a new window]   Fig. 3. Interspecific comparison for teleosts of standard metabolic rate (SMR) versus body mass (Mb) at (A) the temperature at which the measurement was made, and (B) 25°C (corrected using Q10=2.5). Numbers 1-10 and bold regression lines represent non-tuna species considered to be of high performance; numbers 11-21 and broken regression lines represent species of tuna (dotted lines indicate 95% confidence intervals for each regression). 1-3, mackerel Scomer japonicus measured at 124°C (Sepulveda and Dickson, 2000), 218°C (Dickson et al., 2002) and 315°C (Shadwick and Steffensen, 2000); 4-5, salmon Oncorhynchus nerka measured at 424°C (Brett and Glass, 1973) and 515°C (Brett, 1965); 6-7, rainbow trout Oncorhynchus mykiss measured at 6-715°C (Bushnell et al., 1984; Brill, 1987); 8, menhaden Brevoortia tyrannus measured at 20°C (Macy et al., 1999); 9, bluefish Pomatomus saltatrix measured at 15°C (Freadman, 1979); 10, bonito Sarda chiliensis measured at 18°C (Sepulveda et al., 2003); 11-14, yellowfin Thunnus albacares measured at 11-1325°C (Brill, 1987; Dewar and Graham, 1994) and 1424°C (Sepulveda and Dickson, 2000); 15-17, skipjack Katsuwonus pelamis measured at 15-1725°C (Brill, 1979; Dewar and Graham, 1994); 18-20, kawakawa Euthynnus affinis measured at 18-1925°C (Brill, 1987) and 2024°C (Sepulveda and Dickson, 2000); 21, albacore Thunnus alalunga measured at 15°C (Graham et al., 1989). Closed circle represents Seriola quinqueradiata measured at 19°C (Yamamoto et al., 1981), and open symbols represent data for Seriola lalandi from the present study measured at 20°C (open circle) and 25°C (open square). For comparative purposes, data for species of Seriola were not included in formulating the regressions.

Aerobic metabolic scope
It has been widely theorised that the high SMR for pelagic species of fish supports the biochemical and anatomical framework, enabling heightened rate processes and expansion of their aerobic metabolic scope (Dewar and Graham, 1994). Maximum values of _O2 determined for S. lalandi (Fig. 1; Table 2) are in the upper range of other active fish such as salmon (typically <14 mg min^-1 kg^-1) (Brett, 1965; Lee, C. G. et al., 2003), yet they are well below the _O2max predicted for tunas [27-45 mg min^-1 kg^-1 (Brill and Bushnell, 1991; Brill and Bushnell, 2001)]. The absolute aerobic scope of S. lalandi remained at approximately 9.5 mg min^-1 kg^-1 across the temperature range and, subsequently, the factorial aerobic scope decreased 1.8-fold with increasing temperature (Table 2). This contrasts with several other species of teleosts, for which an increase in temperature is associated with an increase in the absolute aerobic scope (Webber et al., 1998; Claireaux et al., 2000; Clark et al., 2005). It is possible that S. lalandi has a bell-shaped relationship between absolute aerobic scope and water temperature, such as that reported for species of salmon and trout (Dickson and Kramer, 1971; Brett and Glass, 1973; Taylor et al., 1996; Farrell, 2002; Lee, C. G. et al., 2003), yet this may only be determined with further experimentation at multiple temperatures. Nevertheless, the data presented for S. lalandi indicate that SMR comprises a smaller proportion of the absolute aerobic scope when the fish is at 20°C as opposed to 25°C, such that a greater fraction of the metabolic scope is available for other aerobic processes (e.g. swimming, digesting) when at the cooler temperature. This may prove beneficial during vertical migrations into deeper, cooler water, such as may occur when diving to obtain prey.

Circulatory contributions to _O2
In teleost fish, the ventricle is composed either entirely of spongy (also referred to as trabecular) myocardium or, generally in the case of high performance species, of an inner spongy myocardium surrounded by an outer compact myocardium (Santer and Greer Walker, 1980; Farrell and Jones, 1992). It may be suggested that the outer compact myocardium acts to reduce compliance of the heart such that high-energy-demand fish have a limited ability to modulate V_S. In agreement with this, the temperature-related increase in SMR of S. lalandi was modulated primarily by an increase in f_H, while V_S and (Ca_O2-C_O2) remained essentially unchanged (Fig. 1; Table 2). In comparison with other active teleosts, _b at zero swimming velocity was within the typically reported range, yet this was the product of a high f_H and a relatively small V_S (Table 3). The majority of the cardiorespiratory variables determined for S. lalandi at zero swimming velocity are within the ranges reported for the only other studied Seriola species, S. quinqueradiata (Table 3). A notable exception is that f_H of S. lalandi at 25°C is somewhat higher than documented values for S. quinqueradiata at this temperature, and this is possibly due to the fact that S. quinqueradiata inhabits more tropical waters and in all studies was acclimated to the experimental temperature for at least 3 days prior to measurements.

In contrast to the primary use of f_H to attain the increase in SMR with temperature, the increase in _O2 during exercise was modulated primarily through an increase in (Ca_O2-C_O2), while f_H increased only moderately and V_S remained unchanged (Fig. 1). Thus, obtaining extremely high values of _O2max, such as those seen in tuna, may be dependent upon a similar (Ca_O2-C_O2) to S. lalandi, but with an increased ability to raise f_H during exercise. Although the negligible scope in V_S would categorise S. lalandi as a cardiac frequency modulator, a limited capacity for increasing _b, in comparison with several other active species (e.g. Gallaugher et al., 2001; Beaumont et al., 2003; Blank et al., 2004), implies that highly regulated blood flows are of secondary importance to an enhanced blood oxygen-carrying capacity and tissue oxygen extraction. In support of this, S. quinqueradiata has haematocrit and haemoglobin concentrations comparable with those of the tunas (Table 3), and increases in both of these variables are causal to a 1.3-fold increase in Ca_O2 with chasing stress (Yamamoto, 1991). Furthermore, it is likely that a large Bohr effect (logP₅₀/pH=-0.74) assists in unloading of oxygen at the tissues (Lee, K. S. et al., 2003a; Lee, K. S. et al., 2003b). If the oxygen content data determined by Yamamoto et al. (Yamamoto et al., 1981) for S. quinqueradiata at 20°C (Table 3) are also representative of S. lalandi at this temperature, it may be predicted that Ca_O2 must increase by at least 1.9-fold (such that Ca_O2=0.33 mg ml^-1, C_O2=0 mg ml^-1) to allow the 4.7-fold increase in (Ca_O2-C_O2) that occurs during exercise. Such changes in Ca_O2 and C_O2 are impossible, which indicates that S. quinqueradiata differs markedly from S. lalandi in terms of tissue oxygen extraction during exercise, or that the values of (Ca_O2-C_O2) determined by Yamamoto et al. were overestimated (Yamamoto et al., 1981), possibly due to experimental stress. Knowledge of the gas exchange characteristics of the blood of S. lalandi is necessary to answer this question.

Aerobic cost of transport
Calculation of U_opt and GCOT_min of high-energy-demand species is arguably of more ecological relevance than SMR or _O2max. Optimum swimming velocity and GCOT_min provide estimates of routine activity levels and energetics in the natural environment. Indeed, U_opt is considered a good predictor for routine swimming speeds in a range of species, suggesting that fish usually swim at speeds at which transport costs are minimal (Videler, 1993; Dewar and Graham, 1994; Tanaka et al., 2001; Lowe, 2002).

As has been found for several other teleosts (Dickson et al., 2002; Sepulveda et al., 2003), an increase in water temperature increased the aerobic cost of transport of S. lalandi, when calculated as either GCOT or NCOT (Fig. 2). Several theories have been proposed to explain the increase in transport costs with increasing temperature but, at present, these remain contentious (Dickson et al., 2002). Dickson et al. proposed that NCOT may be higher at warmer temperatures because of higher swimming support costs, such as higher _b and blood flow to the oxidative locomotor muscles to compensate for the lower oxygen solubility (Dickson et al., 2002). If the same method used to derive NCOT from _O2 is used to calculate the net cost of transport in terms of _b [i.e. (_b-_{b min})/U], the value is indeed higher at 25°C (0.122 ml kg^-1 m^-1) than at 20°C (0.110 ml kg^-1 m^-1); that is, a greater amount of blood is pumped from the heart per metre swum when S. lalandi is swimming at the warmer temperature. It is therefore possible that this 10% difference is at least partly responsible for the 20% difference in NCOT that is evident between temperatures around the optimal swimming velocities (Fig. 2C).

The U_opt for S. lalandi was higher at the warmer temperature than at the cooler temperature, which can be attributed to the thermal effects on SMR causing an increase in GCOT_min at warmer temperatures. In comparison with the prominent U-shaped relationship that is typically documented for other species (Parsons and Sylvester, 1992; Dewar and Graham, 1994; Lee, C. G. et al., 2003), GCOT of S. lalandi at both temperatures followed a shallower U-shaped relationship with swimming velocity (Fig. 2D), such that increases in swimming speed above U_opt were associated with negligible increases in swimming cost [i.e. the oxygen required to swim 1 m remained relatively unchanged from U_opt to U_max, even though GCOT should theoretically increase exponentially with swimming velocity above GCOT_min to overcome the exponential increase in hydrodynamic resistance (Brett, 1964; Videler and Nolet, 1990)]. It is possible that specific aerobic processes within the body (e.g. blood flow to the gut) are shut down at swimming speeds above U_opt in order to divert additional oxygen to the swimming musculature and reduce GCOT. Additionally, energy saved from the progressive transition from opercular ventilation to ram ventilation (Fig. 2B) may offset some of the increasing costs associated with progressively faster swimming; indeed, shifting from opercular ventilation to ram ventilation causes an 8-13% reduction in metabolic rate in rainbow trout (Steffensen, 1985). In this context, it seems that the ability to utilise ram ventilation facultatively, ensures an adequate supply of oxygen at slow swimming speeds when opercular ventilation is adopted, without resulting in compromised streamlining and swimming efficiency at high swimming speeds when ram ventilation ensues.

The length-specific GCOT_min determined for S. lalandi at 25°C compares favourably to values obtained for other high-energy-demand teleosts, including yellowfin tuna at 25°C and sockeye salmon at approximately 15°C (Table 4), although the higher U_opt values determined for S. lalandi and yellowfin tuna indicate a greater overall efficiency of these species over the salmon. In this context, it is interesting to note that the carangiform swimming mode of S. lalandi is comparably efficient with the thunniform swimming mode of the tunas. Thus, rather than evolving to allow more efficient swimming, thunniform locomotion may have developed as a consequence of other features such as myotomal architecture, red muscle position, and its connections with the skin and skeleton (Katz, 2002; Graham and Dickson, 2004). When considering the effect of temperature on GCOT_min mentioned above, it is quite impressive that S. lalandi at 25°C swims with a greater overall efficiency than sockeye salmon at 15°C (Lee, C. G. et al., 2003). At 20°C, S. lalandi displayed remarkable efficiency at U_opt, with the GCOT_min being substantially lower than predicted for a fish of this body mass (Table 4) (Brett, 1964), and lower than values obtained from most other species of high performance teleost (Dewar and Graham, 1994; Lee, C. G. et al., 2003). In comparison with sockeye salmon at 15°C, however, the contribution of SMR to GCOT_min for S. lalandi at 20°C is relatively small, such that values of NCOT at U_opt are similar for the two species (Table 4).

List of symbols and abbreviations

BL

body length

Ca_O2

oxygen content in arterial blood

C_O2

oxygen content in mixed venous blood

EMG

electromyographic

f_G

opercular ventilation rate

f_H

heart rate

GCOT

gross aerobic cost of transport

M_b

body mass

_O2

rate of oxygen consumption

NCOT

net aerobic cost of transport

SMR

standard metabolic rate

Subscripts max, min, opt

maximum, minimum, optimal, respectively

U

swimming velocity

_b

cardiac output

V_S

cardiac stroke volume

	Acknowledgments

 
This project was funded by grants from the Fisheries Research and Development Corporation through the Aquafin Cooperative Research Center, the Australian Research Council and the University of Adelaide. Our appreciation is extended to Arron Strawbridge (South Australian Research and Development Institute) for assistance with surgical procedures and for all aspects of animal husbandry. Quinn Fitzgibbon (University of Adelaide) is thanked for assistance with raising the fish and animal husbandry. Mick Kent, Laurence Durham and Brian Taylor (La Trobe University) are thanked for constructing the swim respirometer, while Peter Frappell (La Trobe University) is thanked for lending the respirometer to the University of Adelaide in order to perform this study. Craig White (University of Birmingham, UK) provided valuable comments relating to statistical analyses. The manuscript benefited from the constructive comments of two anonymous referees.

	References

TOP Summary Introduction Materials and methods Results Discussion References

 

Altimiras, J. and Larsen, E. (2000). Non-invasive recording of heart rate and ventilation rate in rainbow trout during rest and swimming. Fish go wireless! J. Fish Biol. 57,197 -209.[CrossRef]

Axelsson, M., Davison, W., Forster, M. E. and Farrell, A. P. (1992). Cardiovascular responses of the red-blooded Antarctic fishes Pagothenia bernachii and P. borchgrevinki. J. Exp. Biol. 167,179 -201.[Abstract/Free Full Text]

Beaumont, M. W., Butler, P. J. and Taylor, E. W. (2003). Exposure of brown trout Salmo trutta to a sublethal concentration of copper in soft acidic water: effects upon gas exchange and ammonia accumulation. J. Exp. Biol. 206,153 -162.[Abstract/Free Full Text]

Blank, J. M., Morrissette, J. M., Landeira-Fernandez, A. M., Blackwell, S. B., Williams, T. D. and Block, B. A. (2004). In situ cardiac performance of Pacific bluefin tuna hearts in response to acute temperature change. J. Exp. Biol. 207,881 -890.[Abstract/Free Full Text]

Brett, J. R. (1964). The respiratory metabolism and swimming performance of young sockeye salmon. J. Fish. Res. Board Can. 21,1183 -1226.

Brett, J. R. (1965). The relation of size to rate of oxygen consumption and sustained swimming speed of sockeye salmon (Oncorhynchus nerka). J. Fish. Res. Board Can. 22,1491 -1501.

Brett, J. R. and Glass, N. R. (1973). Metabolic rates and critical swimming speeds of sockeye salmon (Oncorhynchus nerka) in relation to size and temperature. Can. Fish. Res. Board J. 30,379 -387.

Brill, R. W. (1979). The effect of body size on the standard metabolic rate of skipjack tuna, Katsuwonus pelamis.Fish. Bull . 77,494 -498.

Brill, R. W. (1987). On the standard metabolic rates of tropical tunas, including the effect of body size and acute temperature change. Fish. Bull. 85, 25-35.

Brill, R. W. and Bushnell, P. G. (1991). Metabolic and cardiac scope of high energy demand teleosts, the tunas. Can. J. Zool. 69,2002 -2009.

Brill, R. W. and Bushnell, P. G. (2001). The cardiovascular system of tunas. In Tuna - Physiology, Ecology, and Evolution (ed. B. A. Block and E. D. Stevens), pp.79 -120. San Diego: Academic Press.

Bushnell, P. G. and Jones, D. R. (1994). Cardiovascular and respiratory physiology of tuna - adaptations for support of exceptionally high metabolic rates. Environ. Biol. Fish. 40,303 -318.[CrossRef]

Bushnell, P. G., Steffensen, J. G. and Johansen, K. (1984). Oxygen consumption and swimming performance in hypoxia-acclimated rainbow trout, Salmo gairdneri. J. Exp. Biol. 13,225 -235.

Bushnell, P. G., Brill, R. W. and Bourke, R. E. (1990). Cardiorespiratory responses of skipjack tuna (Katsuwonus pelamis), yellowfin tuna (Thunnus albacares), and bigeye tuna (Thunnus obesus) to acute reductions of ambient oxygen. Can. J. Zool. 68,1857 -1865.

Claireaux, G., Webber, D. M., Lagardere, J. P. and Kerr, S. R. (2000). Influence of water temperature and oxygenation on the aerobic metabolic scope of Atlantic cod (Gadus morhua). J. Sea Res. 44,257 -265.[CrossRef]

Clark, T. D., Ryan, T., Ingram, B. A., Woakes, A. J., Butler, P. J. and Frappell, P. B. (2005). Factorial aerobic scope is independent of temperature and primarily modulated by heart rate in exercising Murray cod (Maccullochella peelii peelii). Physiol. Biochem. Zool. 78,347 -355.[CrossRef][Medline]

Cooke, S. J., Bunt, C. M., Schreer, J. F. and Philipp, D. P. (2002). Attachment, validation, and preliminary deployment of ultrasonic heart rate transmitters on largemouth bass, Micropterus salmoides. Aquat. Living Resour. 15,155 -162.[CrossRef]

Dabrowski, K., Lee, K. J., Guz, L., Verlhac, V. and Gabaudan, J. (2004). Effects of dietary ascorbic acid on oxygen stress (hypoxia or hyperoxia), growth and tissue vitamin concentrations in juvenile rainbow trout (Oncorhynchus mykiss). Aquaculture 233,383 -392.[CrossRef]

Dejours, P. (1975). Principles of Comparative Respiratory Physiology. Amsterdam: North-Holland.

Dewar, H. and Graham, J. B. (1994). Studies of tropical tuna swimming performance in a large water tunnel. 1. Energetics. J. Exp. Biol. 192,13 -31.[Abstract]

Dewar, H., Graham, J. B. and Brill, R. W. (1994). Studies of tropical tuna swimming performance in a large water tunnel. 2. Thermoregulation. J. Exp. Biol. 192, 33-44.[Abstract]

Dickson, I. W. and Kramer, R. H. (1971). Factors influencing scope for activity and active and standard metabolism of rainbow trout (Salmo gairdneri). Can. Fish. Res. Board J. 28,587 -596.

Dickson, K. A., Donley, J. M., Sepulveda, C. and Bhoopat, L. (2002). Effects of temperature on sustained swimming performance and swimming kinematics of the chub mackerel Scomber japonicus. J. Exp. Biol. 205,969 -980.[Abstract/Free Full Text]

Farrell, A. P. (2002). Cardiorespiratory performance in salmonids during exercise at high temperature: insights into cardiovascular design limitations in fishes. Comp. Biochem. Physiol. 132A,797 -810.[CrossRef]

Farrell, A. P. and Jones, D. R. (1992). The heart. In Fish Physiology. Vol.12A (ed. W. S. Hoar, D. J. Randall and A. P. Farrell), pp. 1-88. San Diego: Academic Press.

Freadman, M. A. (1979). Swimming energetics of striped bass (Morone saxatilis) and bluefish (Pomatomus saltatrix): gill ventilation and swimming metabolism. J. Exp. Biol. 83,217 -230.[Abstract/Free Full Text]

Gallaugher, P., Thorarensen, H. and Farrell, A. P. (1995). Hematocrit in oxygen transport and swimming in rainbow trout (Oncorhynchus mykiss). Respir. Physiol. 102,279 -292.[CrossRef][Medline]

Gallaugher, P., Thorarensen, H., Kiessling, A. and Farrell, A. P. (2001). Effects of high intensity exercise training on cardiovascular function, oxygen uptake, internal oxygen transport and osmotic balance in chinook salmon (Oncorhynchus tshawytscha) during critical speed swimming. J. Exp. Biol. 204,2861 -2872.

Gillanders, B. M., Ferrell, D. J. and Andrew, N. L. (2001). Estimates of movement and life-history parameters of yellowtail kingfish (Seriola lalandi): how useful are data from a cooperative tagging program? Mar. Freshw. Res. 52,179 -192.[CrossRef]

Graham, J. B. and Dickson, K. A. (2004). Tuna comparative physiology. J. Exp. Biol. 207,4015 -4024.[Abstract/Free Full Text]

Graham, J. B., Lowell, W. R., Lai, N. C. and Laurs, R. M. (1989). O₂ tension, swimming-velocity, and thermal effects on the metabolic rate of the Pacific albacore Thunnus alalunga.Exp. Biol . 48,89 -94.[Medline]

Holeton, G. F. and Randall, D. J. (1967). The effect of hypoxia upon the partial pressure of gases in the blood and water afferent and efferent to the gills of rainbow trout. J. Exp. Biol. 46,317 -327.[Abstract/Free Full Text]

Hopkins, T. E. and Cech, J. J. (1994). Effect of temperature on oxygen consumption of the bat ray, Myliobatis californica (Chondrichthyes, Myliobatidae). Copeia 1994,529 -532.

Ishimatsu, A., Maruta, H., Tsuchiyama, T. and Ozaki, M. (1990). Respiratory, ionoregulatory and cardiovascular responses of the yellowtail Seriola quinqueradiata to exposure to the red tide plankton Chattonella. Nippon Suisan Gakkai Shi 56,189 -199.

Ishimatsu, A., Maruta, H., Oda, T. and Ozaki, M. (1997). A comparison of physiological responses in yellowtail to fatal environmental hypoxia and exposure to Chattonella marina.Fish. Sci . 63,557 -562.

Jones, D. R., Kiceniuk, J. W. and Bamford, O. S. (1974). Evaluation of the swimming performance of several fish species from the Mackenzie river. J. Fish. Res. Board Can. 31,1641 -1647.

Jones, D. R., Brill, R. W. and Bushnell, P. G. (1993). Ventricular and arterial dynamics of anaesthetised and swimming tuna. J. Exp. Biol. 182,97 -112.[Abstract]

Katz, S. L. (2002). Design of heterothermic muscle in fish. J. Exp. Biol. 205,2251 -2266.[Abstract/Free Full Text]

Kiceniuk, J. W. and Jones, D. R. (1977). The oxygen transport system in trout (Salmo gairdneri) during sustained exercise. J. Exp. Biol. 69,247 -260.[Abstract/Free Full Text]

Korsmeyer, K. E. and Dewar, H. (2001). Tuna metabolism and energetics. In Tuna - Physiology, Ecology, and Evolution (ed. B. A. Block and E. D. Stevens), pp.35 -78. San Diego: Academic Press.

Korsmeyer, K. E., Lai, N. C., Shadwick, R. E. and Graham, J. B. (1997a). Heart rate and stroke volume contributions to cardiac output in swimming yellowfin tuna: response to exercise and temperature. J. Exp. Biol. 200,1975 -1986.[Abstract]

Korsmeyer, K. E., Lai, N. C., Shadwick, R. E. and Graham, J. B. (1997b). Oxygen transport and cardiovascular responses to exercise in the yellowfin tuna Thunnus albacares. J. Exp. Biol. 200,1987 -1997.[Abstract]

Lee, C. G., Farrell, A. P., Lotto, A., MacNutt, M. J., Hinch, S. G. and Healey, M. C. (2003). The effect of temperature on swimming performance and oxygen consumption in adult sockeye (Oncorhynchus nerka) and coho (O. kisutch) salmon stocks. J. Exp. Biol. 206,3239 -3251.[Abstract/Free Full Text]

Lee, K. S., Ishimatsu, A., Sakaguchi, H. and Oda, T. (2003a). Cardiac output during exposure to Chattonella marina and environmental hypoxia in yellowtail (Seriola quinqueradiata). Mar. Biol. 142,391 -397.

Lee, K. S., Kita, J. and Ishimatsu, A. (2003b). Effects of lethal levels of environmental hypercapnia on cardiovascular and blood-gas status in yellowtail, Seriola quinqueradiata. Zool. Sci. 20,417 -422.[CrossRef][Medline]

Lowe, C. G. (2002). Bioenergetics of free-ranging juvenile scalloped hammerhead sharks (Sphyrna lewini) in Kane'ohe Bay, O'ahu, HI. J. Exp. Mar. Biol. Ecol. 278,141 -156.[CrossRef]

MacNutt, M. J., Hinch, S. G., Farrell, A. P. and Topp, S. (2004). The effect of temperature and acclimation period on repeat swimming performance in cutthroat trout. J. Fish Biol. 65,342 -353.[CrossRef]

Macy, W. K., Durbin, A. G. and Durbin, E. G. (1999). Metabolic rate in relation to temperature and swimming speed and the cost of filter feeding in Atlantic menhaden, Brevoortia tyrannus. Fish. Bull. 97,282 -293.

O'Steen, S. and Bennett, A. F. (2003). Thermal acclimation effects differ between voluntary, maximum, and critical swimming velocities in two cyprinid fishes. Physiol. Biochem. Zool. 76,484 -496.[CrossRef][Medline]

Parsons, G. R. and Sylvester, J. L. (1992). Swimming efficiency of the white crappie, Pomoxis annularis.Copeia 1992,1033 -1038.[CrossRef]

Poortenaar, C. W., Hooker, S. H. and Sharp, N. (2001). Assessment of yellowtail kingfish (Seriola lalandi lalandi) reproductive physiology, as a basis for aquaculture development. Aquaculture 201,271 -286.[CrossRef]

Randall, D. J., Holeton, G. F. and Stevens, E. D. (1967). The exchange of oxygen and carbon dioxide across the gills of rainbow trout. J. Exp. Biol. 46,339 -348.[Abstract/Free Full Text]

Santer, R. M. and Greer Walker, M. (1980). Morphological studies on the ventricle of teleost and elasmobranch hearts. J. Zool. 190,259 -272.

Schmidt-Nielsen, K. (1990). Animal Physiology: Adaptation and Environment. Cambridge: Cambridge University Press.

Sepulveda, C. and Dickson, K. A. (2000). Maximum sustainable speeds and cost of swimming in juvenile kawakawa tuna (Euthynnus affinis) and chub mackerel (Scomber japonicus). J. Exp. Biol. 203,3089 -3101.[Abstract]

Sepulveda, C. A., Dickson, K. A. and Graham, J. B. (2003). Swimming performance studies on the eastern Pacific bonito Sarda chiliensis, a close relative of the tunas (family Scombridae). I. Energetics. J. Exp. Biol. 206,2739 -2748.[Abstract/Free Full Text]

Shadwick, R. E. and Steffensen, J. F. (2000). The cost and efficiency of aerobic locomotion in the chub mackerel (Scomber japonicus). Am. Zool. 40, 2108.

Steffensen, J. F. (1985). The transition between branchial pumping and ram ventilation in fishes: energetic consequences and dependence on water oxygen tension. J. Exp. Biol. 114,141 -150.[Abstract/Free Full Text]

Stevens, E. D. and Randall, D. J. (1967). Changes in gas concentrations in blood and water during moderate swimming activity in trout. J. Exp. Biol. 46,329 -337.[Abstract/Free Full Text]

Tanaka, H., Takagi, Y. and Naito, Y. (2001). Swimming speeds and buoyancy compensation of migrating adult chum salmon Oncorhynchus keta revealed by speed/depth/acceleration data logger. J. Exp. Biol. 204,3895 -3904.

Taylor, S. E., Egginton, S. and Taylor, E. W. (1996). Seasonal temperature acclimatisation of rainbow trout: cardiovascular and morphometric influences on maximal sustainable exercise level. J. Exp. Biol. 199,835 -845.[Abstract]

Videler, J. J. (1993). Fish Swimming. London: Chapman & Hall.

Videler, J. J. and Nolet, N. R. (1990). Cost of swimming measured at optimum speed: scale effects, differences between swimming styles, taxonomic groups, and submerged and surface swimming. Comp. Biochem. Physiol. 97A, 91-99.[Medline]

Webber, D. M., Boutilier, R. G. and Kerr, S. R. (1998). Cardiac output as a predictor of metabolic rate in cod Gadus morhua. J. Exp. Biol. 201,2779 -2789.[Abstract]

Yamamoto, K. I. (1991). Increase of arterial O₂ content in exercised yellowtail (Seriola quinqueradiata). Comp. Biochem. Physiol. 98A, 43-46.[CrossRef]

Yamamoto, K. I., Itazawa, Y. and Kobayashi, H. (1981). Gas exchange in the gills of yellowtail, Seriola quinqueradiata under resting and normoxic condition. Nippon Suisan Gakkai Shi 47,447 -451.

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