Swimming performance studies on the eastern Pacific bonito Sarda chiliensis, a close relative of the tunas (family Scombridae) I. Energetics
1 Center for Marine Biomedicine and Biotechnology and Marine Biology
Research Division, Scripps Institution of Oceanography, University of
California, San Diego, La Jolla, CA 92093-0204, USA
2 Department of Biological Science, California State University Fullerton,
Fullerton, CA 92834, USA
* Author for correspondence (e-mail: csepulve{at}ucsd.edu)
Accepted 7 May 2003
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Summary |
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Key words: energetics, locomotion, swimming, Scombridae, eastern, Pacific bonito, Sarda chiliensis, standard metabolic rate, cost of transport, tuna
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Introduction |
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The functional and structural bases for tuna endothermy and thunniform
swimming reside in the tunas' myotomal architecture. Red myotomal muscle (RM,
the slow-twitch aerobic fibers that power sustained swimming) occurs both more
anterior in the body and closer to the vertebral column in tunas than in other
fishes (Kishinouye, 1923;
Fierstine and Walters, 1968
;
Graham et al., 1983
). Tuna RM
position has been hypothesized to have influenced thunniform locomotion
through effects on body shape (Magnuson,
1978
; Graham and Dickson,
2000
) and on the mechanical linkage between myotomes and the
caudal fin (Westneat et al.,
1993
; Shadwick et al.,
1998
; Ellerby et al.,
2000
; Graham and Dickson,
2000
). In addition, shifts in the pattern of RM vascular supply
may have established the basis for counter-current heat transfer and for the
origin of endothermy (Graham and Dickson,
2000
,
2001
).
Although a unique RM position and regional endothermy occur exclusively in
the tunas, the sequence of evolutionary changes that took place from the
less-derived mackerels and bonitos to the tunas remains unclear. Therefore,
testing or distinguishing among hypotheses about the acquisition sequence of
these features requires phylogenetically appropriate structural and functional
comparisons with nontuna scombrids
(Magnuson, 1973;
Graham, 1975
;
Collette and Chao, 1975
;
Collette, 1978
;
Block et al., 1993
; Graham and
Dickson, 2000
,
2001
).
Several works have compared the swimming performance of mackerels to that
of tunas. In contrast to the thunniform swimming mode of tunas, both chub
(Scomber japonicus) and Atlantic (Scomber scombrus)
mackerels use the carangiform swimming mode
(Videler and Hess, 1984;
Donley and Dickson, 2000
).
Although the chub mackerel is not endothermic, rapid swimming does transiently
elevate both RM and white muscle temperatures
(Roberts and Graham, 1979
).
Finally, and despite similar costs of locomotion, the standard metabolic rate
(SMR, the minimum metabolic rate required for maintenance functions;
Videler, 1993
) of the chub
mackerel is lower than that of the tunas
(Sepulveda and Dickson, 2000
;
Shadwick and Steffensen,
2000
).
Although mackereltuna comparisons identify key differences between
the two groups, most investigators regard the bonitos, which are the tuna
sister group (Collette, 1978;
Block et al., 1993
), as more
appropriate for evolutionary comparisons
(Block and Finnerty, 1994
;
Altringham and Block, 1997
;
Ellerby et al., 2000
;
Graham and Dickson, 2000
).
Relative to mackerels, bonitos have many morphological specializations (i.e.
body shape, gill surface area, growth rate and maximum size) that are more
like those of tunas (Gray,
1954
; Campbell and Collins,
1975
; Collette,
1978
). Bonito RM is also in a more medial position than in the
mackerels (Kishinouye, 1923
;
Graham et al., 1983
;
Ellerby et al., 2000
;
Graham and Dickson, 2000
), and
both bonito myotomal structure and the arrangement of the anterior and
posterior oblique tendons (which transmit force from the myotomal musculature
to the caudal propeller) are more similar to those of tunas
(Ellerby et al., 2000
;
Westneat et al., 1993
;
Westneat and Wainwright, 2001
;
K. A. Dickson and J. B. Graham, unpublished). However, bonitos do not have the
anterior RM position found in tunas and they are not endothermic
(Carey et al., 1971
;
Graham, 1975
;
Graham et al., 1983
;
Altringham and Block, 1997
;
Graham and Dickson, 2000
,
2001
).
While the importance of additional studies with bonitos to increasing our
understanding of the swimming adaptations of tunas has long been recognized
(Godsil, 1954;
Graham, 1975
;
Block and Finnerty, 1994
;
Altringham and Block, 1997
;
Ellerby et al., 2000
;
Graham and Dickson, 2001
),
access to live specimens by laboratories capable of conducting physiological
studies with them has been rare (Altringham
and Block, 1997
; Ellerby et
al., 2000
). The availability of the eastern Pacific bonito
Sarda chiliensis in southern California coastal waters in the summer
of 2000 provided the opportunity to study the swimming energetics and
kinematics of this species using the same water tunnel respirometer that had
been used for the tuna energetics and kinematics studies reported by Dewar and
Graham
(1994a
,b
).
This paper reports on bonito swimming energetics, and the companion paper
(Dowis et al., 2003
) describes
bonito swimming kinematics.
Previous work on bonito energetics includes indirect
O2 estimates
derived from mouth gape and swimming distance
(Mendo and Pauly, 1988
) and
estimates of routine metabolic rate (RMR, which includes both spontaneous
movements and locomotion; Beamish,
1978
) made for bonito swimming inside of a small annular
respirometer, without speed control
(Freund, 1999
). The objectives
of the present study were to quantify bonito swimming energetics and obtain
swimming
O2
data over a range of controlled speeds. We also wanted to compare bonito
swimming to that of its sister group, the tunas, by contrasting the
relationship between
O2 and swimming
speed in similar-sized fish to estimate the cost of transport and SMR. This
approach has provided new insight into two important questions about scombrid
physiology. (1) How do the costs of locomotion compare for tunas and bonitos?
(2) Is the high SMR of the tunas a unique tuna trait or a synapomorphy of the
tribes Sardini and Thunnini?
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Materials and methods |
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The respirometer
The variable-speed water-tunnel respirometer used in this study has been
described previously (Graham et al.,
1990; Dewar and Graham,
1994a
; Graham et al.,
1994
; Bernal et al.,
2001
). It consists of a 2.3 mx6.3 m (lengthxwidth)
oval of 46 cm-diameter polyvinylchloride pipe with an in-series
diffuser-contraction section and a 100 cmx51 cmx42 cm
(lengthxwidthxheight) working section. It has a total volume of
3000 liters and is powered by a 40 hp variable-speed electric motor with a
fixed, low-pitch propeller. Initial flow analyses
(Graham et al., 1990
) using
attached threads, observations of particle motion and dye streaming all
confirmed a uniform speed and laminar flow field in the center and first half
of the working section, which is where swimming fish spend most of their time
(see below).
Experimental protocol
Care was taken not to touch the bonito during all steps involved in capture
and transfer to the water tunnel. Prior to all experiments, food was withheld
from the entire tank for 24 h. The experimental bonito was obtained by fishing
with a baited, barbless hook. The hooked fish was immediately placed in the
cylindrical transport tank containing oxygenated seawater and the
manufacturer's recommended dose of Fritzyme®, a mucus coat protecting
agent. We found that the presence of other fish in the transfer tank minimized
the introduced bonito's swimming speed and the frequency of its collisions
with the tank wall. Standard procedure therefore was to place between one and
five `companion fish' (either chub mackerel Scomber japonicus, or
topsmelt Atherinops affinis) in the tank prior to introducing the
experimental bonito.
After 15 min the bonito and the water around it were scooped up in a soft
plastic bucket liner and transferred into the working section of the
respirometer. We found that the transferred bonito could better orient to the
flow and had fewer erratic movements and bursts if a `companion fish' was also
present in the working section at the time of introduction. Both chub mackerel
and topsmelt, which swim well in water tunnels
(Sepulveda and Dickson, 2000;
C. Sepulveda, personal observation) were used as `working-section companions'.
The companion fish was removed after about 60 min, once the bonito had begun
to swim steadily. Covering the working section with a dark cloth and placing a
light at its front end helped to keep the bonito swimming in the center of the
channel. A mirror positioned at 45° over the working section facilitated
remote observation of the fish for the duration of the study.
The bonito was then given a 4 h period of slow, steady swimming to allow
its recovery from capture and tunnel placement stress. Previous scombrid
respirometry studies have noted a marked change in fish behavior and
O2 after about 2
h in the working section (Dewar and
Graham, 1994a
; Sepulveda and
Dickson, 2000
). During recovery the bonito swam slowly (about 60
cm s-1) while fresh seawater flowed through the tunnel to maintain
temperature and ambient O2 levels.
Following the recovery period, water inflow to the tunnel was stopped and
the system was sealed. Measurements of bonito
O2 were then
made at different swimming speeds by recording water-tunnel O2
declination rate over a 3060 min period of steady swimming. Tunnel
water speeds were determined by calibration with a flow meter (model 2035,
General Oceanics Inc., FL, USA). The respirometer-water O2 level
was monitored with a polarographic O2 electrode (Yellow Springs
Instrument, OH, USA) connected to a model 52 meter. For each bonito energetics
study, ProComm data acquisition software was used to record both water speed
and O2 concentration.
During a given experiment, the respirometer water temperature was maintained within ±1°C of the bonito holding tank, which was supplied with a continuous flow of fresh seawater and subject to subtle environmental fluctuations in temperature (i.e. solar heating, seasonal fluctuation). Collectively for all tests, the experimental temperature was 18±2°C. Respirometer water O2 concentration was maintained at or above 80% saturation. When fish respiration reduced chamber O2 levels to near the 80% saturation limit, the system was re-oxygenated by seawater flow and application of a gentle stream of bubbles from a compressed O2 cylinder.
O2
measurements were made on bonito swimming between 50 and 120 cm
s-1. Tests of each fish began by swimming it at the lowest speed it
could maintain (5060 cm s-1) for 3060 min while
O2 declination was measured. Following this determination, speed
was increased by 10 cm s-1 and
O2 again
measured. This protocol was repeated until the bonito could no longer swim
steadily or maintain position. Most studies terminated at this point. However,
in two cases, replicate
O2 measurements
were repeated at a lower speeds. Video records of the bonito swimming at the
different test speeds were then made for a kinematics analysis
(Dowis et al., 2003
).
After each individual swimming test, the bonito was removed and the empty
respirometer was resealed to measure the background bacterial respiration rate
and instrumental drift. Throughout the background measurements, the
respirometer motor was circulating the water at approximately 50 cm
s-1 and the
O2 was recorded
for approximately 36 h. The mean background
O2 value for all
experiments was 62±2.3 mg O2 h-1 or 614%
of the maximum measured oxygen consumption rate; the percentage was greatest
at lowest speeds. All reported bonito
O2 data are
background-corrected. After each experiment, the water tunnel was bleached and
cleaned with fresh water.
Plasma lactate
Bonito plasma lactate levels were measured to provide an indication of the
level of anaerobic metabolic stress associated with three different phases of
the respirometry study: (1) pre-experiment, just after capture from the
holding tank, (2) at the end of the 15 min period in the transfer tank, (3) at
the end of all swimming tests. Phases 1 and 2 used bonito that, although not
used in the respirometer, were handled in exactly the same way as were the
respirometer fish. Bonito taken directly from the respirometer following the
completion of all swimming studies were used for phase 3 measurements.
Blood samples were taken by quickly grasping the bonito behind the operculum, and holding it firmly while removing approximately 2 ml of blood via cardiac puncture with a 20-gauge needle attached to a 3 ml syringe. Both the needle and syringe had been flushed with heparinized saline, which also filled the dead space. Plasma obtained by immediately centrifuging the blood (5 min at 3000 g) was stored at -80°C. Lactate assays were performed spectrophotometrically using a Sigma Diagnostics kit (Procedure 735). This method did not employ a deproteination step and may thus have indicated slightly higher lactate levels than actually occurred. The tests do nevertheless provide a relative index for the change in plasma lactate concentrations at the different experimental phases.
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Results |
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Energetics
Covariance analysis (ANCOVA; Minitab version 12) indicated a significant
(P<0.05) positive relationship between swimming speed and
O2, but no
effect of either body mass or FL on swimming
O2. Absence of a
body size effect allowed pooling of data for individual bonito and facilitated
comparisons with
O2 values
obtained for tuna (Dewar and Graham,
1994a
).
Fig. 1 shows the expected
exponential increase in
O2 with
increasing speed for each bonito (Videler,
1993
; Webb, 1998
),
but also indicates a trend for bonito
O2 to level off
or even increase at 5060 cm s-1. In fact, five of the six
bonito for which swimming
O2 data were
obtained at 50 cm s-1 actually had a lower
O2 at 60 cm
s-1. The tendency for bonito
O2 to remain
higher than expected at slower speeds is evident in the combined
O2-speed
relationship for all bonito at each test speed
(Fig. 2). This curve is
U-shaped; the mean
O2 at 50 cm
s-1 is higher than the
O2 at 60 cm
s-1, and the value at 60 cm s-1 is only slightly less
than the rate at 70 cm s-1. Two additional features of bonito
low-speed swimming are indicated in Table
1. First, nine of the 12 fish had an elevated
O2 at the lowest
speed tested (either 50 or 60 cm s-1) than at the next higher test
speed. Second, records for these same fish at the time of study all noted
erratic swimming (i.e. bursting, lateral movements and rapid fluttering of the
pectoral fins) at these lower speeds.
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A higher than expected
O2 at low
swimming speeds affects estimates of both cost of transport (determined from
the instantaneous slope of the
O2speed
regression) and SMR (estimated by extrapolation of the regression function to
zero speed) (Videler, 1993
).
It was therefore important to quantify the effect of an elevated
O2 at low speed
by contrasting a semi-logarithmic regression equation for the complete bonito
data set with a `corrected' regression (i.e. calculated after the selective
removal of approximately one
high-
O2,
low-speed data point from each fish). The criteria used to justify the
selective removal of a
high-
O2,
low-speed data point were: occurrence of a lower
O2 at the next
highest test speed and the occurrence, in notes made at the time of study, of
observations of erratic swimming (Table
1).
Fig. 3 shows the effect of
selective data removal: the exponential form of the regression equation for
the complete data set is y=107e0.015x. The corrected data
set regression equation is y=70e0.020x. The corrected
function has a higher correlation coefficient (r=0.84 versus
0.74); however, there is considerable overlap of the 95% confidence intervals
of the slope and y-intercept values of the two functions, indicating
that they are not significantly different. These two functions do nevertheless
demonstrate the marked effect of an elevated
O2 at low speed
both in lowering the regression equation's slope (from 0.02 to 0.15, a 25%
reduction) and increasing its y-intercept, by 53%. Furthermore,
because the y-intercept value at zero speed is an estimate of SMR
(Videler, 1993
), this
selective data removal reduces the calculated bonito SMR from 107 to 70 mg
O2 kg-1 h-1.
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Bonito cost of transport
Although Fig. 3 indicates
differences between the complete and corrected bonito swimming
speedO2
regressions, a valid comparison of the bonito data with published tuna
energetics data necessitated use of the complete bonito data set because no
high-
O2,
low-speed data points were removed in the tuna study.
To calculate gross cost of transport (GCOT), the mass-specific
O2 values were
first converted to weight-specific values (by dividing by 9.8 m
s-2, the acceleration due to gravity), and these were converted
from mg O2 to Joules (J), using the oxycalorific coefficient of
14.1 J mg-1 O2
(Tucker, 1975
;
Videler, 1993
;
Dewar and Graham, 1994a
).
Then, these values were divided by the speed at which the value was
determined, to obtain GCOT in units of J N-1 m-1.
Because J=N m, this expression of GCOT is dimensionless: (mg O2
h-1 kg-1) (9.8 m s-2)-1 (14.1 J
mg-1 O2) (cm s-1)-1 (1 h 3600
s-1) (100 cm m-1) (kg m s-2 N-1) =
J N-1 m-1. The net cost of transport (COTnet)
at each speed was calculated in the same manner, starting with the rate of
oxygen consumption above SMR (mass-specific
O2 at each speed
SMR).
The graph showing bonito GCOT in relation to speed
(Fig. 4A, note speed units are
m s-1), has a U-shaped function. The function's minimum defines the
optimal swimming speed (Uopt, i.e. the speed with the
lowest energy cost per unit distance)
(Videler and Nolet, 1990;
Videler, 1993
;
Korsmeyer and Dewar, 2001
).
The Uopt of the bonito at both 18°C and 24°C is
approximately 0.7 m s-1 (about 1.4 FL s-1). The
corresponding GCOT at Uopt is 0.17 J N-1
m-1 at 18°C and about 0.27 J N-1 m-1 at
24°C. Also shown in Fig. 4A
are regressions describing bonito COTnet at both 18°C and
24°C. These functions are nearly parallel
(y=0.061e0.885x, r=0.99, at 18°C;
y=0.0951e0.916x, r=0.99, at 24°C);
the difference in the y-intercepts reflects the assumed increase in
SMR at 24°C (see below).
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Interspecific comparisons
Most tuna respirometry has been done at 24°C. Because we lacked the
heating and temperature-control equipment required to acclimate bonito to
24°C, the 18°C bonito
O2 data were
adjusted to 24°C, assuming a Q10 of 2.0 (Brill,
1979
,
1987
;
Dewar and Graham, 1994a
), for
comparison with tuna data.
Fig. 4B compares the GCOT
and COTnet values for the bonito and yellowfin tuna at 24°C
(data from Dewar and Graham,
1994a). At all speeds compared, the GCOT is higher in the
yellowfin tuna than in the bonito. Due to its higher SMR
(Korsmeyer and Dewar, 2001
),
the yellowfin also has a higher Uopt, approximately 1 m
s-1 (2.3 FL s-1) versus 0.7 m
s-1 (1.4 FL s-1) for the bonito. The GCOT at
Uopt for the yellowfin tuna is greater than that of the
bonito (0.46 J N-1 m-1 versus 0.27 J
N-1 m-1). The COTnet functions for the bonito
(y=0.0951e0.916x, r=0.99) and yellowfin tuna
(y=0.0375e2.07x, r=0.98) differ, with the
yellowfin having both a greater slope and a lower intercept. However, because
the 95% confidence intervals of these parameters overlap, the two functions
are not significantly different.
The bonito standard metabolic rate (SMR), as determined by the complete
data set (Fig. 3), does not
differ significantly (i.e. there is overlap in the 95% confidence intervals)
from that of similar sized teleosts (Fig.
5), the yellowtail (Seriola quinqueradiata) at 20°C
(Yamamoto et al., 1981) or the
salmon (Oncorhynchus nerka) at 20°C
(Brett and Glass, 1973
).
However, when adjusted for ambient temperature differences, the bonito SMR
(161±33 mg O2 kg-1 h-1) is
significantly lower (P<0.05, t-test) than that of similar
sized yellowfin, skipjack and kawakawa Euthynnus affinis tunas
(Brill, 1979
,
1987
;
Dewar and Graham, 1994a
) and
dolphinfish Coryphaena hippurus
(Benetti et al., 1995
).
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Plasma lactate concentrations
Bonito plasma lactate levels were determined for three phases of this
respirometry study: just after capture from the holding tank, after 15 min in
the round tank with companion fish, and after the swimming tests. The lactate
concentration measured in the post-transfer period (2.84±0.88 mmol
l-1, N=4) was much greater than the pre-experiment
(baseline-control) lactate concentration (0.11±0.03 mmol
l-1, N=2) and significantly higher (two sample
t-test, P<0.05) than the post-swimming experiment levels
(0.26±0.08 mmol l-1, N=4).
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Discussion |
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Validation of the bonito
O2speed
relationship
Both capture and handling stress have the potential to increase fish
metabolic intensity to the point of elevating muscle and plasma lactate
levels, followed by a period of elevated aerobic metabolism required for the
reconversion of lactate to glycogen
(Milligan and Girard, 1993;
Milligan, 1996
). Validation of
the bonito swimming
O2 data
therefore required confirmation that handling and confinement in the
respirometer working section did not result in an excessive build-up of
lactate. Our findings that bonito plasma lactate levels were elevated during
the handling phases of the experiments, but then fell to low levels during the
swimming tests, indicate that the metabolic costs of lactate reconversion were
not a significant component of the bonito
swimming-
O2
determinations.
Unstable swimming
Bonito O2 was
determined over speeds ranging from 50 to 120 cm s-1. Although the
exponential rise in
O2 occurring
with incremental speed increases above 60 cm s-1 is entirely
consistent with theory (Videler,
1993
; Webb, 1998
),
Fig. 2 shows that the mean
O2 for bonito is
minimal at 60 cm s-1 and elevated at 50 cm s-1. Because
erratic fin fluttering and unsteady swimming were documented for slow-swimming
bonito (Table 1), we attribute
the increase in mean
O2 at speeds of
50 cm s-1 (and, to some extent, 60 cm s-1) to the
metabolic costs associated with the additional movements required for
low-speed stability. This interpretation is consistent with findings for other
fishes at low speeds (He and Wardle,
1986
; Lucas et al.,
1993
; Webb, 1998
;
Freund, 1999
;
Sepulveda and Dickson, 2000
),
as well as for other animals (Withers,
1992
; Schmidt-Nielsen,
1993
).
Most scombrids, including bonitos, are negatively buoyant and must swim
continuously, both for hydrodynamic lift
(Magnuson, 1973) and ram
ventilation (Roberts, 1975
).
Magnuson (1973
) used
comparative morphometric and body density data to estimate the minimum speeds
required for bonitos and tunas to maintain hydrostatic equilibrium.
Application of the Magnuson
(1973
) minimum speed equation
to bonito (4555 cm FL) in this study yields a minimum speed of
approximately 1.2 FL s-1 or about 5466 cm
s-1, which corresponds to the range where unsteady motion and
increased swimming costs occurred for the bonito in this study
(Fig. 2).
Unstable swimming and COT and SMR estimates
Comparison of the complete
O2speed
data set to one modified by the selective removal of the ten
high-
O2,
low-speed measurements (Fig. 3)
documents how unsteady swimming artificially increases the SMR estimate and
lowers the estimated swimming cost (regression parameters of the
O2speed
relationship). In the case of the bonito, this data manipulation was warranted
because of our direct observations of unsteady swimming at low speeds
(Table 1) and the known
correspondence between unsteady swimming and the bonito's minimum speed
requirements for hydrostatic equilibrium (Magnuson,
1973
,
1978
). While this correction
did not significantly change the parameters of either regression function
(i.e. there is overlap in the 95% confidence intervals), it did improve the
correlation coefficient for the
O2speed
function. Although the selected data set appeared to be more meaningful
biologically, comparisons with data for other species, for which selective
removal was not done, required that we operate with the complete data set.
Comparisons of
O2 in bonito
Two previous studies provide swimming
O2 estimates for
the eastern Pacific bonito. Mendo and Pauly
(1988
) used the observational
swimming speed data of Magnuson and Prescott
(1966
) to estimate the routine
metabolic rate (RMR) [defined by Beamish
(1978
) as the combination of
normal and spontaneous movements] for a 2.5 kg, 57 cm FL bonito
swimming in a large aquarium at 22°C. By combining mean swimming speed
(1.4 FL s-1) with the estimated volume of water traversing
the gills (based on mouth aperture or gape), and assuming the extraction of
50% of the O2 in the water contacting the gills, these workers
arrived at an estimated RMR of 160 000 cal day-1, or 800 mg
O2 kg-1 h-1. This value is three times the
O2 that we
measured for bonito swimming at 1.4 FL s-1 (260 mg
O2 kg-1 h-1) and doubtlessly reflects the
numerous assumptions underlying the Mendo and Pauly
(1988
)
O2 estimate.
Freund (1999) reported
similar RMR values for bonito and skipjack tuna swimming in an annular
respirometer at 20±1°C. However, speed was not controlled in that
study and unsteady swimming was noted for both species. The mean RMR estimated
for the bonito was 427 mg O2 kg-1 h-1, and a
speed estimate for one bonito was 50 cm s-1
(Freund, 1999
). Although
bonito size and experimental temperature were similar in that study to ours,
it is difficult to compare the two. Inspection of
Fig. 2 shows that 50 cm
s-1 is too slow for stable swimming in bonito of the size studied,
and this may account for the 1.4-fold higher
O2 measured by
Freund (1999
).
Bonito and tuna comparisons
Swimming efficiency
Although much of our understanding of tuna morphology and physiology
suggests that they should swim more efficiently than other fishes, no study,
including this work with the eastern Pacific bonito, has successfully
documented this difference (Sepulveda and
Dickson, 2000; Korsmeyer and
Dewar, 2001
). This is paradoxical because tuna specializations,
including a high degree of body streamlining, a unique RM position, tendon
arrangement, thunniform swimming mode and endothermy, have all been
hypothesized to augment aerobic swimming performance and presumably swimming
efficiency (Carey and Teal,
1966
; Fierstine and Walters,
1968
; Graham,
1975
; Johnston and Brill,
1984
; Westneat et al.,
1993
; Altringham and Block,
1997
; Graham and Dickson,
2000
,
2001
;
Donley and Dickson, 2000
;
Ellerby et al., 2000
;
Altringham and Shadwick, 2001
;
Dowis et al., 2003
).
Studies of tuna swimming efficiency, however, have of necessity been
carried out on juvenile or sub-adult fishes in swimming chambers
(Gooding et al., 1981;
Graham and Laurs, 1982
;
Graham et al., 1989
;
Dewar and Graham, 1994a
;
Freund, 1999
;
Sepulveda and Dickson, 2000
;
Donley and Dickson, 2000
). In
the case of water tunnels, it may be that the requirement to maintain position
by matching swimming thrust production to water flow speed obscures the
utility of structural and physiological specializations for swimming that, in
a more natural setting, increase swimming efficiency. A free-swimming tuna,
for example, has options for turning, gliding and changing depth, as well as
responding behaviorally to physical features in the environment, such as
density gradients and thermal fronts. In addition, schooling may augment
swimming efficiency (Weihs,
1973
). Magnuson's finding
(Magnuson, 1973
) of allometric
changes that lower the minimum speed requirements of larger tunas further
suggests that increased size, in combination with swimming specializations,
increases swimming efficiency in larger tunas.
Standard metabolic rates
Extrapolation of the Fig. 3
regressions to zero speed yields SMR estimates for the bonito that are
comparable to those of the salmon (Brett
and Glass, 1973) and yellowtail
(Yamamoto et al., 1981
), but
significantly lower than both similar-sized yellowfin and skipjack tunas
swimming in the same respirometer system
(Dewar and Graham, 1994a
) and
spinally blocked (paralyzed) yellowfin, skipjack and kawakawa tunas (Brill,
1979
,
1987
) and dolphinfish
(Benetti et al., 1995
)
(Fig. 5). The dolphinfish is
the only fish species shown to have an SMR comparable to that of the tunas
(Benetti et al., 1995
).
Although it lacks an elevated tissue temperature, the dolphinfish is a highly
active species with several specializations (i.e. rapid growth rate, high
heart rate) related to its high-energy-demand, pelagic existence
(Brill, 1996
). Similarity
between the bonito SMR and that of the chub mackerel
(Shadwick and Steffensen,
2000
) suggests that, among the scombrids thus far studied, the
tunas are unique in having a high SMR.
The basis for the tuna's elevated SMR has been the topic of considerable
discussion (Brill, 1979,
1987
,
1996
;
Gooding et al., 1981
;
Dewar and Graham, 1994a
;
Brill et al., 2001
;
Sepulveda and Dickson, 2000
;
Korsmeyer and Dewar, 2001
;
Graham and Dickson, 2001
).
First, an elevated SMR is consistent with higher maintenance costs associated
with the tunas' relatively large gills and heart and with the elevated
metabolic requirements of the tunas' warm muscle and other tissues. In
addition, there may be functional costs requiring a high SMR, such as the
osmoregulatory load imposed by a larger gill surface area (Brill,
1987
,
1996
;
Benetti et al., 1995
;
Brill et al., 2001
). Tunas
also have the added costs associated with the aerobic requirements of a larger
and thicker-walled ventricle that has both a high cardiac output and a high
systolic pressure (Graham et al.,
1983
; Brill and Bushnell,
1991
,
2001
;
Bushnell and Jones, 1994
;
Graham and Dickson, 2000
).
Added to these may be a higher aerobic cost associated with the more aerobic
white muscle of tunas. As in other fishes, white muscle accounts for the
greatest percentage of body mass, and tuna white muscle has a greater aerobic
capacity than in other species (as indicated by the high activity of the
aerobic enzyme, citrate synthase) (Dickson,
1995
,
1996
;
Korsmeyer and Dewar, 2001
).
Finally, there are the additional metabolic costs for processes such as
gastric evacuation, somatic and gonadal growth rates, and lactate processing,
which all appear to be augmented in tunas relative to other scombrids and
other pelagic teleosts (Magnuson,
1969
; Schaefer,
1984
; Perry et al.,
1985
; Weber et al.,
1985
; Hunter et al.,
1986
; Arthur et al.,
1992
; Bushnell and Jones,
1994
; Brill, 1996
;
Korsmeyer and Dewar, 2001
).
The high SMR of tunas therefore appears important in enabling them to sustain
high energy production rates required by the combinations of endothermy and a
high aerobic scope for activity (Priede,
1985
; Bushnell and Jones,
1994
; Brill, 1996
;
Brill et al., 2001
;
Bushnell and Brill, 2001
;
Korsmeyer and Dewar,
2001
).
Conclusions
The objectives of this study were to obtain swimming energetics data for
the eastern Pacific bonito in the same respirometer that has been used to
study tunas, and to compare bonito and tuna locomotor costs and SMR. Because
the bonito is in the scombrid tribe Sardini, which is the sister group of the
tunas (tribe Thunnini), comparisons of tunabonito swimming performance
have the potential to delineate the pattern of character acquisition leading
to tuna locomotor specializations, including endothermy. Although our swimming
performance comparisons necessitated a temperature adjustment (from 18°C
to 24°C) of the bonito
swimmingO2
data, the resulting net cost of transport (COTnet) estimate for the
bonito significantly overlaps with that of the yellowfin tuna and thus
indicates comparable swimming costs over the range of speeds tested.
On the other hand, the finding of a lower SMR in both the bonito and the
chub mackerel relative to tunas implies that, in tuna, elevated SMR is an
apomorphy linked to this group's numerous structures and functions requiring
high metabolic maintenance. It may be that studies on the more basal species
of tunas, for example, the slender tuna, Allothunnus fallai, will
elucidate the linkages between SMR, aerobic function and endothermy.
Allothunnus has less RM than other tunas and some of the circulatory
modifications required for endothermy, but whether or not it is endothermic is
not presently known (Graham and Dickson,
2000).
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