Swimming performance studies on the eastern Pacific bonito Sarda chiliensis, a close relative of the tunas (family Scombridae) Swimming performance studies on the eastern Pacific bonito Sarda chiliensis, a close relative of the tunas (family Scombridae) II. Kinematics
1 Department of Biological Science, California State University Fullerton,
Fullerton, CA 92834-6850, USA
2 Center for Marine Biotechnology and Biomedicine and Marine Biology
Research Division, Scripps Institution of Oceanography, University of
California San Diego, La Jolla, CA 92093-0204, USA
* Author for correspondence (e-mail: kdickson{at}fullerton.edu)
Accepted 7 May 2003
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: locomotion, swimming, kinematics, Scombridae, eastern, Pacific bonito, Sarda chiliensis, thunniform, carangiform, tuna
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Swimming in tunas has been classified as thunniform locomotion,
characterized by minimal lateral undulation of most of the body and thrust
generation by rapid oscillations of the high-aspect-ratio caudal fin
(Fierstine and Walters, 1968;
Lighthill, 1970
;
Webb, 1975
;
Lindsey, 1978
). Many
morphological specializations of tunas are associated with thunniform
swimming. These include the anteriormedial RM, streamlined body shape,
elongated myotomes, RMtendonskeleton connections, and
narrow-necking of the caudal peduncle
(Fierstine and Walters, 1968
;
Lighthill, 1969
,
1970
;
Webb, 1975
;
Magnuson, 1978
;
Ellerby et al., 2000
;
Graham and Dickson, 2000
;
Westneat and Wainwright,
2001
). It has been proposed that the RM position in tunas evolved
to enhance swimming performance by affecting the mechanical transfer of muscle
contractile force to the backbone and caudal propeller
(Westneat et al., 1993
;
Ellerby et al., 2000
;
Graham and Dickson, 2000
). The
transition to thunniform locomotion was hypothesized to have occurred prior to
the evolution of endothermy, in response to changing oceanographic conditions
(Graham and Dickson,
2000
).
Testing and distinguishing among these hypotheses requires knowledge of the
tunas' sister groups and mapping morphological characteristics onto a scombrid
phylogeny (Block and Finnerty,
1994; Graham and Dickson,
2000
). The Scombridae is composed of a monotypic subgroup (the
butterfly mackerel Gasterochisma melampus) and four tribes: Scombrini
(mackerels), Scomberomorini (Spanish mackerels), Sardini (bonitos) and
Thunnini (tunas) (Collette,
1978
; Collette et al.,
2001
). According to phylogenies based on both morphological and
gene-sequence data, the 15 species of tunas form a derived, monophyletic
clade, and their closest relatives are the bonitos
(Collette, 1978
;
Block et al., 1993
;
Finnerty and Block, 1995
;
Carpenter et al., 1995
;
Graham and Dickson, 2000
;
Collette et al., 2001
).
Because of this sister-taxon relationship, examination of the bonitos is
essential for determining the sequence of character state changes that led to
the specializations of the tunas. This study quantifies swimming kinematics in
the eastern Pacific bonito Sarda chiliensis so that the trait of
thunniform locomotion can be mapped precisely onto the scombrid phylogeny.
Studies of scombrid swimming kinematics have focused primarily on mackerels
and tunas (Gray, 1933;
Fierstine and Walters, 1968
;
Magnuson, 1970
;
Videler and Hess, 1984
;
Dewar and Graham, 1994b
;
Shadwick et al., 1998
;
Knower et al., 1999
;
Gibb et al., 1999
;
Donley and Dickson, 2000
;
Nauen and Lauder, 2000
;
Dickson et al., 2002
). Donley
and Dickson (2000
)
distinguished the kinematics of juvenile chub mackerel Scomber
japonicus and kawakawa tuna Euthynnus affinis, and emphasized
the importance of comparing similar-sized fish at comparable speeds. They
found that, at the same speeds, the tuna swam with higher tailbeat
frequencies, lower tailbeat amplitudes, lower stride lengths and less lateral
displacement along most of the body, than did the chub mackerel.
Some kinematics data have been reported for bonitos, but comparisons with
tunas and mackerels led to conflicting conclusions. The relationship between
tailbeat frequency and speed for a 16 cm total length (TL) Atlantic
bonito Sarda sarda derived from data in Pyatetskiy
(1970) was similar to that of
similar sized (14.8 and 16.7 cm TL) chub mackerel, but lower than
that of a 16.2 cm TL kawakawa tuna
(Donley, 1999
;
Donley and Dickson, 2000
). In
contrast, Altringham and Block
(1997
) reported similar
tailbeat frequencies in S. chiliensis and yellowfin tuna Thunnus
albacares swimming in a large, cylindrical tank, but swimming speed and
fish size, which both affect tailbeat frequency, varied interspecifically.
Block (personal observation, cited in Block
and Finnerty, 1994
) indicated that the Atlantic bonito swims in a
more `stiffbodied' (tuna-like) fashion than mackerels do.
The most comprehensive study to date of bonito swimming
(Ellerby et al., 2000) used
sonomicrometry and electromyography to measure RM strain and activity
patterns, which have been correlated with swimming mode
(Wardle et al., 1995
;
Altringham and Ellerby, 1999
;
Knower et al., 1999
;
Altringham and Shadwick, 2001
),
at several positions along the body in S. chiliensis (6071 cm
fork length, FL). Muscle activity patterns in the bonito were found
to be more similar to those of tunas than to those of mackerels. On the other
hand, based on the extent of maximum lateral displacement of five points along
the dorsal midline measured from videotapes of bonito swimming steadily in a
large, open tank, Ellerby et al.
(2000
) concluded that the
bonito swims in the carangiform mode like the mackerel. They found lateral
displacement of the bonito to be similar to that of the Atlantic mackerel
(Scomber scombrus, 3034 cm TL) from Videler and Hess
(1984
) and greater than that
of a 44 cm FL yellowfin tuna derived from Dewar and Graham
(1994b
).
From the existing data, it is not possible to determine unequivocally if
the swimming mode of bonitos is more similar to that of mackerels or tunas, or
if it is intermediate between the two. Therefore, thunniform locomotion cannot
be mapped onto the scombrid phylogeny at a specific position to determine if
that trait evolved before or after the divergence of the tunas and bonitos.
Furthermore, because most kinematic variables vary with swimming speed or fish
size, it is important that interspecific comparisons are made at the same
speeds in similar sized individuals. Thus, the objective of the present study
was to quantify the swimming kinematics of the eastern Pacific bonito at a
range of controlled speeds, and then to compare the bonito to tunas of similar
size that have been swum at similar speeds in the same respirometer
(Dewar and Graham, 1994b;
Knower, 1998
;
Knower et al., 1999
) and to
intervertebral lateral displacement and bending angle data for chub mackerel
and kawakawa tuna (Donley and Dickson,
2000
).
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
A Motus 3.2 motion analysis system (Peak Performance Technologies, Inc., Englewood, CO, USA) was used to analyze videotaped segments that met the following criteria: (i) the fish was positioned in the middle of the chamber, away from the walls and bottom, (ii) the fish was swimming steadily through at least seven complete tailbeat cycles, and did not move forward or backward in the chamber, and (iii) both the head and tail of the fish were in the field of view. Two points, the tip of the upper lobe of the tail and the tip of the snout, were followed through time by digitizing sequential video frames for 714 complete tail beats at each swimming speed. Using the measured total length of the fish, a scaling factor was calculated for each video segment so that pixels could be converted to centimeters.
Using methods described in Donley and Dickson
(2000), kinematic variables
were quantified for each bonito at each test speed. Tailbeat frequency (in Hz)
was calculated by following the tip of the tail through time and dividing the
number of consecutive tail beats by the amount of time, in seconds, that it
took to complete those tail beats. Tailbeat amplitude (cm) and yaw (cm) were
determined by measuring the distance between the lateral-most positions of the
tip of the tail and of the tip of the snout, respectively, during a complete
tailbeat cycle (the excursion of the tail from one side of the body to the
other and back again). Mean tailbeat amplitude and yaw values were computed at
each speed for each fish. Stride length, the distance (cm) that the fish moves
forward in each tailbeat cycle, was calculated by dividing swimming speed by
tailbeat frequency. Relative values (as %FL) of tailbeat amplitude,
yaw and stride length were also determined. The propulsive wavelength (the
length of the wave of undulation that travels down the body of the fish from
snout to tail tip during swimming) was obtained by dividing propulsive wave
velocity by the corresponding tailbeat frequency. Propulsive wave velocity was
determined from the amount of time (s) between the peaks in lateral
displacement at the tip of the snout and the tip of the tail; then the
TL (cm) of each individual (the distance between the two points) was
divided by the mean progression time in order to obtain the propulsive wave
velocity in cm s-1 at each speed. Propulsive wavelength was
measured in both cm and as a percentage of TL (%TL). Based
on the known size of the field of view that was videotaped and the resolution
of 400 horizontal lines for super VHS, the spatial resolution of the
measurements was 0.1250.183 cm, which is equivalent to ranges of
0.250.41%FL and 0.230.38%TL. Depending on
tailbeat frequency, there were 1840 video fields per tail beat.
The lateral displacement and bending angle of each intervertebral joint
during the tailbeat cycle were determined using the techniques of Jayne and
Lauder (1995) and Donley and
Dickson (2000
). With the Peak
Performance Motus system, 32 points approximately equally spaced around the
dorsal outline of each individual were digitized in consecutive frames for one
complete tailbeat cycle at a swimming speed of 90 cm s-1 (relative
speeds of 1.631.85 TL s-1), a speed at which all
bonito swam. The points were converted into complete curves using a cubic
spline function, and a midline was calculated for each frame
(Jayne and Lauder, 1995
).
Lateral view X-rays were taken of each individual, and the lengths of the
skull, each vertebra, and the hypural plate were measured with digital
calipers. Each midline was divided into segments representing the measured
skeletal elements, and the position in each frame of each intervertebral joint
and of the snout and tail tip were calculated. Using a Microsoft Excel macro
written by Jayne and Lauder
(1995
), the lateral
displacement (z, using the terminology of
Jayne and Lauder, 1995
) and
angle of flexion (ß) of each intervertebral joint throughout the tailbeat
cycle were calculated. Then, maximum lateral displacement
(zmax) and maximum bending angle (ßmax)
during the tail beat were determined for each joint along the body for each
bonito. Mean zmax and ßmax values for each
intervertebral joint for the eight bonito studied were compared with data for
all intervertebral joints in the chub mackerel and kawakawa tuna studied by
Donley and Dickson (2000
) at
speeds of 75100 cm s-1. For these comparisons, the maximum
lateral displacement of each joint, measured in cm, was converted to relative
fish length (%TL), and the position along the body of each
intervertebral joint was expressed as %TL. The
zmax at 0%TL is one-half of yaw, and
zmax at 100%TL is one-half of tailbeat amplitude,
as defined above.
Statistical analysis
The bonito kinematic variables were assessed for significant effects of
swimming speed (cm s-1) and fish size (mass in g and length in cm)
and for significant interactions between these factors. Minitab (version 13.1)
was used to create the data file, calculate interaction terms and test for
normality. SAS (version 8.2) was used to perform repeated-measures multiple
regression analyses on tailbeat frequency (in Hz), tailbeat amplitude, yaw and
stride length (in both cm and %FL), propulsive wavelength (in cm and
%TL), and on zmax (in %TL) and
ßmax (in degrees). The initial statistical models for tailbeat
frequency, tailbeat amplitude, yaw, stride length and propulsive wavelength
included the main effects of speed, mass and FL, as well as all
possible interaction terms. The models for zmax and
ßmax included mass, fish total length, position along the
body, and all possible interactions, but did not include swimming speed
because only one speed was used. For each variable, the full model was
subjected to a backward stepwise reduction to fit the best model to the data;
each nonsignificant term was dropped until a final model that included all
significant terms was obtained.
We then determined if tailbeat frequency (in Hz), tailbeat amplitude, yaw
and stride length (all expressed as %FL), and propulsive wavelength
(in %TL) in the bonito differed significantly from published data for
two species of tuna (Thunnus albacares and skipjack Katsuwonus
pelamis). Because there was limited access to the raw data for the tunas,
two-sample t-tests (Dixon and
Massey, 1969) were used to detect significant interspecific
differences in mean values or in the slopes and y-intercepts of
linear regressions reported in the literature.
We tested for significant interspecific differences in mean maximum lateral
displacement of the body midline and mean maximum flexion angles, at all
intervertebral joints along the body, between the bonito and the chub mackerel
and kawakawa tuna from Donley and Dickson
(2000). Repeated-measures
multiple regression analyses were run in SAS to determine if there were any
significant effects of position along the body (%TL), species, or
position x species on zmax and ßmax.
The position term was squared in order to incorporate curvature into the
equation for a more accurate model of the data, but the coefficients of the
squared terms were not interpreted. Significant interspecific differences are
indicated as significant terms in the final regression model, after a backward
stepwise reduction process was completed. A significance level of
P=0.05 was used in all statistical analyses.
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
Tailbeat amplitude, yaw and stride length were assessed for size and speed effects using the absolute values in cm, as well as relative values (%FL). When the effects of fish size were accounted for, both tailbeat amplitude and stride length increased significantly with swimming speed (Figs 2 and 3), but yaw did not vary significantly with speed. When the effects of speed were accounted for, there were no significant effects of FL or mass on tailbeat amplitude, yaw or stride length. When these three kinematics variables were expressed as %FL, no significant size effects were detected. Tailbeat amplitude ranged from 16 to 24%FL, and the range of stride length was 6291%FL. The yaw for the bonito ranged from 5.2 to 6.9%FL (6.0±0.6%FL, mean ± S.D.).
|
|
Propulsive wavelength (in cm and in %TL) did not vary significantly with fish size or with swimming speed (P=0.065) in the bonito. Thus, a mean for each individual and a grand mean for all eight fish were calculated. The propulsive wavelength was 110129%TL (120±6%TL, mean ± S.D.).
Both mean maximum intervertebral lateral displacement (zmax) and mean maximum intervertebral bending angles (ßmax) varied significantly with position along the body (P<0.0001) in the bonito (Figs 4 and 5). Minimum mean zmax occurred at 30%TL (the joint between vertebrae 11 and 12) and maximum zmax occurred at the tail tip. Minimum mean ßmax occurred at 18%TL (the joint between the first and second vertebrae) and maximum mean ßmax was at the joint between the last vertebra and the hypural plate (92%TL). There were no significant effects of fish mass or length on bonito zmax or ßmax.
|
|
Interspecific comparisons
Significant effects of fish size were not detected for any of the
kinematics variables measured in the present study, most likely due to the
small size range of the bonito studied. Therefore, interspecific comparisons
were made using the mean values of yaw, propulsive wavelength, and
zmax and ßmax at different positions along
the body, and the regressions of the other kinematics variables
versus swimming speed for the bonito. In these comparisons, we have
assumed that temperature differences among the studies compared (with reported
temperatures ranging from 18°C to 28°C) do not contribute
significantly to differences in tailbeat frequency, tailbeat amplitude, yaw
and stride length. This assumption is based on a number of studies that have
found little to no effect of temperature on these kinematics variables when
fish are acclimated to the measurement temperature and comparisons are made at
a given speed (for a review, see Dickson
et al., 2002). Temperature does affect swimming performance in
fishes, primarily through changes in water viscosity that significantly impact
swimming at low Reynolds numbers (Fuiman
and Batty, 1997
; Johnson et
al., 1998
) and by affecting muscle power output and patterns of
muscle fiber recruitment, leading to higher maximum sustainable speeds at
higher temperatures (e.g. Rome and Swank,
1992
; Altringham and Block,
1997
; Rome et al.,
2000
).
Tailbeat frequency increased significantly with speed in both yellowfin and
skipjack tunas (Dewar and Graham,
1994b; Knower
1998
; Knower et al.,
1999
), as it did in the bonito
(Fig. 1). The slopes of the
tailbeat frequency versus speed relationships did not differ
significantly (P>0.25) between the bonito and two groups of
yellowfin tuna (FL 42±1.6 cm and 53±3.0 cm, means
± S.D.) (data from Dewar
and Graham, 1994b
) or between the bonito and 4044 cm
FL yellowfin tuna and 3841 cm FL skipjack tuna (data
from Knower et al., 1999
).
Because the slopes did not differ, comparisons were made between the
y-intercepts of these lines. The intercepts of the tailbeat frequency
versus speed relationships for the 42 cm and 53 cm yellowfin tuna
groups did not differ significantly from that of the bonito
(P>0.25) (Fig. 1A),
but the intercepts for the 4044 cm yellowfin and 3841 cm
skipjack tuna were significantly higher than for the bonito
(P<0.0005) (Fig.
1B). Because the original data from Knower et al.
(1999
) were provided to us,
95% confidence intervals for the tailbeat frequency versus speed
relationships were calculated and plotted
(Fig. 1B). The lack of overlap
of the 95% confidence intervals over the range of speeds studied suggests that
the bonito swim at a given speed with significantly lower tailbeat frequencies
than do similar sized yellowfin and skipjack tunas.
The only published data for tailbeat amplitudes and yaw at known speeds in
tunas that are of comparable size to the bonito in the present study are from
yellowfin tuna (Dewar and Graham,
1994b). Tailbeat amplitude did not vary significantly with speed
in the yellowfin tuna, and the values (mean ± S.D.) of Dewar
and Graham (1994b
) are
compared with the bonito data plotted in
Fig. 2. It appears that, at
similar speeds, the tailbeat amplitude of the bonito does not differ
significantly from that of one group of yellowfin (FL 42±1.6
cm, swimming at a speed of 40±2.8 cm s-1; means ±
S.D.) but is higher than that of the larger yellowfin
(48±2.2 cm FL, swimming at 100±6.5 cm s-1).
The yaw for the bonito (6.0±0.6%FL, mean ±
S.D.) is significantly greater (P<0.001) than the
values for both the 42 cm (4.3±0.38%FL) and 48 cm
(2.8±0.15%FL) yellowfin tuna groups
(Table 1). A high yaw value
(5%TL) was also observed for the eastern Pacific bonito by Ellerby et
al. (2000
).
|
Stride length increased significantly with speed in the yellowfin and
skipjack tunas (Dewar and Graham,
1994b; Knower
1998
), as it did in the bonito
(Fig. 3). The slopes of the
stride length versus speed relationships did not differ significantly
(P>0.25) between the bonito and the two groups of yellowfin tuna
from Dewar and Graham (1994b
),
or between the bonito and the yellowfin and skipjack tunas from Knower et al.
(1999
). The
y-intercepts of the four tuna stride length versus speed
regressions were significantly lower than that of the bonito
(P<0.001). Thus, at a given speed, stride length is greater in the
bonito than it is in similar-sized tunas
(Fig. 3).
The range of values for relative propulsive wavelength (as %FL) in
the bonito (Table 1) overlapped
with data for yellowfin tuna from Dewar and Graham
(1994b)
(124±9%FL and 123±17%FL for 42 cm FL
and 48 cm FL groups, respectively; means ± S.E.M.),
but were higher than values reported by Knower
(1998
) (103%FL in
4044 cm FL yellowfin tuna and 97%FL in 3841 cm
FL skipjack tuna).
The patterns of mean maximum intervertebral lateral displacement
(zmax) and mean maximum bending angle
(ßmax) at all intervertebral joints in the bonito were
compared with data from juvenile kawakawa tuna and chub mackerel
(Donley and Dickson, 2000),
the only scombrid species that have been analyzed in this manner. Overall,
mean zmax was significantly higher in the bonito than in
both the tuna (P<0.0001) and the mackerel (P=0.032).
Lateral displacement at the snout and posterior to 40%TL is greater
in the bonito than in the other two species
(Fig. 4). The pattern of
zmax along the body differed between the bonito and the
kawakawa tuna, as indicated by a significant tuna x position interaction
(P=0.0025), but did not vary significantly between the bonito and the
chub mackerel. The minimum mean zmax occurred at
38%TL (between vertebrae 10 and 11) in the chub mackerel and at
41%TL (between vertebrae 15 and 16) in the kawakawa tuna, compared
with 30%TL in the bonito; maximum mean zmax
occurred at the tip of the tail in all three species.
Mean maximum bending angles in the bonito differed significantly from those in both the kawakawa tuna (P=0.0016) and the chub mackerel (P=0.032), as did the pattern of ßmax versus position along the body, as indicated by significant species x position interaction terms (P<0.0001). The mackerel had higher bending angles than the bonito in the anterior third of the body, and the tuna had lower bending angles than the bonito at approximately 6575%TL (Fig. 5). The position of minimum mean ßmax was 40%TL (between vertebrae 11 and 12) in the chub mackerel and 18%TL (between vertebrae 1 and 2) in both the kawakawa tuna and the bonito; maximum mean ßmax occurred at the intervertebral joint anterior to the hypural plate in all three species (at 87, 90 and 92%TL in the mackerel, tuna and bonito, respectively).
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Because the mackerels that have been studied are all less than 35 cm in length, we cannot compare tailbeat frequency, tailbeat amplitude or stride length data for similar sized mackerels and bonitos swimming at comparable speeds. However, interspecific comparisons of the variables that are apparently independent of fish size, yaw and zmax expressed as a percentage of fish length, show that the bonito swims with significantly more lateral displacement along most of the body, including the snout, than do juvenile chub mackerel. Thus, swimming kinematics in the bonito may not be intermediate between that of tunas and mackerels, as would be predicted on the basis of morphological characteristics.
Swimming kinematics variables
Although we concluded that tailbeat frequency at a given speed is
significantly lower in the bonito than it is in similar sized tunas, based on
comparison with data for yellowfin and skipjack tunas from Knower et al.
(1999), the relationships
between tailbeat frequency and speed did not differ significantly between the
bonito and the yellowfin tuna from Dewar and Graham
(1994b
). There was much
greater variability in the Dewar and Graham
(1994b
) data than in that of
Knower et al. (1999
), which
may be due to the methods that were used to record tailbeat frequency. Dewar
and Graham (1994b
) used visual
observations and a stopwatch to determine the time required for a fish to
complete 20 tail beats while swimming steadily, whereas Knower et al.
(1999
) used frame-by-frame
analysis of video footage to calculate tailbeat frequency. The high
variability may also be a consequence of the inclusion of lower swimming
speeds by Dewar and Graham
(1994b
). If a fish swims at a
speed that is below the minimum speed required for hydrostatic equilibrium
(Magnuson, 1978
), it may use
sporadic swimming motions to maintain position, which can lead to high
variability in kinematics data. Consequently, we believe that the values
measured in Knower et al.
(1999
) are a more accurate
representation of tuna tailbeat frequency at steady, sustainable speeds.
However, it should be noted that the tunas used in Knower et al.
(1999
) all were smaller in
FL than the bonito in the present study and thus would be expected to
use higher tailbeat frequencies at a given speed than larger individuals.
Because no size effects were observed in either study, it is not possible to
extrapolate the data sets to a common fish size. When we compared the largest
tuna (44 cm FL yellowfin) from Knower et al.
(1999
) and our smallest bonito
(45 cm FL), tailbeat frequency was higher at a given speed in the
tuna than in the bonito.
Because tailbeat frequencies were lower in the bonito, we expected that
tailbeat amplitudes would be higher in the bonito compared to tunas. The
bonito did swim at a given speed with a higher tailbeat amplitude than the 48
cm yellowfin, but there was no difference between the bonito and 42 cm
yellowfin (Fig. 2). In
addition, the maximum lateral displacement of the tip of the tail (one-half of
the tailbeat amplitude) was significantly greater in the bonito than in the
juvenile tuna of Donley and Dickson
(2000) when expressed as
%TL (Fig. 4). Thus,
the limited tailbeat amplitude data that are available provide some support
for a difference in swimming mode between the bonito and tuna.
Stride length in the bonito was higher than the values reported for tunas
by both Dewar and Graham
(1994b) and Knower et al.
(1999
), indicating that the
bonito moves farther with each tailbeat. Altringham and Block
(1997
) also noted greater
stride lengths in free-swimming bonito (4247 cm TL) compared
with larger yellowfin tuna (5881 cm TL). These data further
support the difference in swimming mode between tunas and the bonito.
Yaw, the result of anterior recoil forces generated by oscillation of the
tail, is minimized in scombrid fishes by narrow necking of the caudal fin, a
large muscle mass and a high body depth
(Lighthill, 1969;
Lindsey, 1978
; Webb,
1978
,
1998
). Magnuson
(1978
) found that maximum body
thickness (the average of maximum height and maximum width) for seven tuna
species ranged between 20.8 and 23.5%FL, but was only
18.4%FL for Sarda chiliensis and 16.0%FL for
Scomber scombrus. Decreased yaw has been used to distinguish
thunniform locomotion from other swimming modes
(Fierstine and Walters, 1968
;
Dewar and Graham, 1994b
;
Ellerby et al., 2000
). In the
present study, the bonito had significantly higher yaw than did similar sized
yellowfin tuna at similar speeds, which supports the hypothesis that tunas
utilize a different swimming mode than do bonitos. Because yaw (as a
percentage of fish length) apparently does not vary significantly with fish
size, we examined yaw values from a number of other scombrid fishes
(Table 1) and also found yaw in
the bonito to exceed that in kawakawa tuna and Atlantic and chub mackerels.
This interspecific difference is reflected in the midline lateral displacement
at the tip of the snout (one-half of yaw)
(Fig. 4). Thus, although
morphological characteristics indicate that yaw in the bonito would be
intermediate between that in mackerels and tunas, yaw was highest in the
bonito.
Propulsive wavelength values (as %FL or %TL) for tunas,
mackerels and the eastern Pacific bonito overlap
(Table 1), and no consistent
pattern was detected. Propulsive wavelength has been used previously to
categorize swimming mode, and should be greater for thunniform than for
carangiform swimmers (Lindsey,
1978). However, Donley and Dickson
(2000
) found that propulsive
wavelength as a percentage of body length was greater in the chub mackerel
than in the kawakawa tuna, and varied with fish size. Although propulsive
wavelength in scombrids is not known to vary with swimming speed, it does vary
with temperature (Dewar and Graham,
1994b
; Donley and Dickson,
2000
; Dickson et al.,
2002
). Studies with other fish species indicate that propulsive
wavelength varies with axial position
(Blight, 1977
) and within a
given species (Long and Nipper,
1996
) suggest that this variable should not be used as a criterion
for distinguishing fish swimming modes (see
Long and Nipper, 1996
;
Donley and Dickson, 2000
).
The intervertebral flexion angles were higher in the chub mackerel than in
the bonito and in the kawakawa tuna (Fig.
5). These angles reflect intervertebral lateral displacement, the
number of vertebrae and vertebral flexibility. The larger angles in the
mackerel can be attributed primarily to the smaller number of vertebrae in the
chub mackerel (31) relative to the kawakawa (39) and the bonito (44); when
there are fewer intervertebral joints, larger angles are required as the body
midline is displaced laterally a given distance. In all three species, low
ßmax values were found for the intervertebral joints just
anterior to the hypural plate, and ßmax values at this
position were highest in the chub mackerel because the mackerel has one
relatively large vertebra in this position, whereas the tuna and bonito have
two or three much shorter vertebrae
(Collette, 1978).
The interspecific differences in vertebral number may also contribute to
differences in yaw and in the pattern of zmax along the
body. Videler (1985) suggested
that a greater number of vertebrae would lead to a greater degree of lateral
flexibility. This may explain why the bonito swims with greater lateral
displacement than do the kawakawa tuna and chub mackerel
(Fig. 4). However, if vertebral
number was the only factor involved, lateral displacement would be lowest in
the chub mackerel, which has the fewest vertebrae of the three species, but
lateral displacement is lowest in the tuna
(Fig. 4).
The lower zmax and ßmax values observed
in the tuna may result from specializations for axial stiffness and/or the
anteriormedial RM position. Relative to other scombrids, tunas have
enlarged neural and hemal spines, larger zygapophyses that link adjacent
vertebrae, more epipleural ribs and more extensive branching of tendons as
they insert onto the backbone within the horizontal septum, and bony caudal
keels which are thought to stiffen the caudal region
(Kishinouye, 1923;
Fierstine and Walters, 1968
;
Collette, 1978
;
Hebrank, 1982
;
Westneat et al., 1993
). Tunas
also have a well developed vertical septum containing collagen fibers in a
crossed-fiber array, and some tuna species possess bony projections (lattices;
Kishinouye, 1923
) that extend
between their hemal spines that may stiffen the skeleton
(Westneat and Wainwright,
2001
). Furthermore, in the tunas Euthynnus, Katsuwonus
and Thunnus, the first vertebra is partially or fully sutured to the
skull (Collette, 1978
). All of
these characteristics may reduce axial flexibility, but their contribution to
differences in swimming kinematics remains to be determined empirically.
Differences in swimming mode between mackerels, bonitos and tunas may also
be related to the position of the RM, its pattern of activation, and how
muscle contractile force is transferred to the skeleton to produce swimming
movements. In bonitos and mackerels, the lateral RM is firmly attached to the
skin and is connected to the backbone via posterior oblique tendons
(POTs) within the horizontal septum that insert onto the backbone at higher
angles than they do in tunas (Westneat et
al., 1993; Graham and Dickson,
2000
; Westneat and Wainwright,
2001
). Contraction of RM therefore results in localized bending in
the chub mackerel (Shadwick et al.,
1998
) and most likely also in the eastern Pacific bonito
(Ellerby et al., 2000
;
Altringham and Shadwick, 2001
).
In the tunas, little of the RM is firmly attached to the skin and the POTs are
longer and insert onto the backbone at a lower angle
(Westneat et al., 1993
;
Graham and Dickson, 2000
).
Tuna RM transfers contractile force further caudally, allowing RM contraction
in tunas to be uncoupled from local bending
(Knower et al., 1999
;
Shadwick et al., 1999
;
Altringham and Shadwick, 2001
).
Because of the POT morphology, muscle contractile force is also transferred
caudally with a higher velocity ratio, but a lower mechanical advantage, in
tunas compared with mackerels and bonitos
(Westneat et al., 1993
;
Graham and Dickson, 2000
), and
this is reflected in the higher tailbeat frequencies and lower tailbeat
amplitudes in tunas. Future studies are needed to test how differences in
vertebral number, structures that affect axial stiffness, total muscle mass,
RM position and connective tissue linkages between the locomotor muscle, skin
and skeleton affect scombrid swimming kinematics.
Conclusions
The results of this kinematics study support the hypothesis that thunniform
locomotion is a derived characteristic of the endothermic tunas associated
with the anterior, medial position of the RM. The traits of
anteriormedial RM, thunniform locomotion and endothermy all map onto
the scombrid phylogeny after the divergence of the bonitos and tunas, and we
cannot determine if the anteriormedial RM evolved initially for a less
flexible swimming mode and secondarily as a way to conserve metabolically
derived heat. However, when combined with the swimming energetics data for the
bonito (Sepulveda et al.,
2003), we have shown that an increase in energetic efficiency is
apparently not associated with thunniform locomotion. Sepulveda et al.
(2003
) found that the net cost
of transport during sustained swimming was similar in the eastern Pacific
bonito and the yellowfin tuna studied by Dewar and Graham
(1994a
), but that total
metabolic costs were higher in the tuna due to a higher standard metabolic
rate. This corresponds with the results of similar size-matched comparisons of
juvenile chub mackerel and kawakawa tuna
(Donley and Dickson, 2000
;
Sepulveda and Dickson, 2000
;
Korsmeyer and Dewar, 2001
).
Thus, there is no evidence that increased swimming efficiency was the
selective advantage leading to the evolution of the thunniform locomotor mode.
It may be that the advantages of endothermy, not swimming efficiency, led to
the evolution of the anteriormedial RM in tunas, because heat loss from
RM across the body surface would be reduced. If so, thunniform locomotion may
simply be a consequence of changes in the biomechanical linkages of the
locomotor muscle with the backbone and caudal propeller necessitated by this
RM position.
The next step in trying to determine at what point thunniform locomotion
evolved within the family Scombridae will require making comparisons among the
15 tuna species. Although it is assumed that all of the tunas use thunniform
locomotion, swimming in many tuna species has not been studied. Efforts should
be directed at describing the swimming mode of the most basal tuna,
Allothunnus fallai. Although this species does not possess all of the
circulatory specializations for endothermy that are found in the other tunas,
its RM is located in an anterior, medial position and a small central heat
exchanger is present (Graham and Dickson,
2000). Characterizing the swimming kinematics of this species and
determining if it is able to elevate RM temperature will establish whether the
anteriormedial RM evolved prior to the evolution of thunniform
locomotion or prior to the evolution of endothermy.
This research was funded by NSF grant #IBN-9973916, the California State University (CSU) Fullerton Departmental Associations Council, an intramural grant from the CSU State Special Fund for Research, Scholarship and Creative Activity, the Scripps Institution of Oceanography Director's Office, and the Birch Aquarium at Scripps. Modifications of the respirometer system were funded by NSF grants IBN-9607699 and IBN-0077502. Bonito were collected under California Department of Fish and Game scientific collecting permits. All experimental protocols were approved by the University of California San Diego and California State University Fullerton Institutional Animal Care and Use Committees. We thank D. Bernal, C. Chan, J. Donley and H. Lee for assistance with fish collection and maintenance and with the experiments, G. Noffal for use of the Peak Motus system, G. Lauder for providing the Excel programs used in the body bending analyses, J. Donley for her generous assistance with those programs and with data analysis, and K. Messer for invaluable statistical assistance. We are indebted to T. Knower for supplying tuna data and H.J. Walker for assistance with the fish X-rays. We also thank M. Horn, S. Murray, J. Videler and an anonymous reviewer who provided useful comments on drafts of the manuscript.
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Altringham, J. D. and Block, B. A. (1997). Why
do tuna maintain elevated slow muscle temperatures? Power output of muscle
isolated from endothermic and ectothermic fish. J. Exp.
Biol. 200,2617
-2627.
Altringham, J. D. and Ellerby, D. J. (1999).
Fish swimming: Patterns in muscle function. J. Exp.
Biol. 202,3397
-3403.
Altringham, J. D. and Shadwick, R. E. (2001). Swimming and muscle function. In Tuna Physiology, Ecology, and Evolution, Fish Physiology, vol. 19 (ed. B. A. Block and E. D. Stevens), pp. 314-341. New York: Academic Press.
Blight, A. R. (1977). The muscular control of vertebrate swimming movements. Biol. Rev. 52,181 -218.
Block, B. A. (1991). Endothermy in fish: thermogenesis, ecology, and evolution. In Biochemistry and Molecular Biology of Fishes, vol. 1 (ed. P. W. Hochachka and T. P. Mommsen), pp. 269-311. New York: Elsevier.
Block, B. A. and Finnerty, J. R. (1994). Endothermy in fishes: A phylogenetic analysis of constraints, predispositions, and selection pressures. Environ. Biol. Fish. 40,283 -302.
Block, B. A., Finnerty, J. R., Stewart, A. F. R. and Kidd, J. (1993). Evolution of endothermy in fish: mapping physiological traits on a molecular phylogeny. Science 260,210 -214.[Medline]
Carey, F. G., Teal, J. M., Kanwisher, J. W., Lawson, K. D. and Beckett, K. S. (1971). Warm bodied fish. Amer. Zool. 11,137 -145.
Carpenter, K. E., Collette, B. B. and Russo, J. L. (1995). Unstable and stable classifications of scombrid fishes. Bull. Mar. Sci. 56,379 -405.
Collette, B. B. (1978). Adaptations and systematics of the mackerels and tunas. In The Physiological Ecology of Tunas (ed. G. D. Sharp and A. E. Dizon), pp.7 -39. New York: Academic Press.
Collette, B. B., Reeb, C. and Block, B. A. (2001). Systematics of the tunas. In Tuna Physiology, Ecology, and Evolution, Fish Physiology, vol.19 (ed. B. A. Block and E. D. Stevens), pp.5 -30. New York: Academic Press.
Dewar, H. and Graham, J. B. (1994a). Studies of
tropical tuna swimming performance in a large water tunnel. I. Energetics.
J. Exp. Biol. 192,13
-31.
Dewar, H. and Graham, J. B. (1994b). Studies of
tropical tuna swimming performance in a large water tunnel. III. Kinematics.
J. Exp. Biol. 192,45
-59.
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.
Dixon, W. J. and Massey, F. J. (1969). Introduction to Statistical Analysis. New York: McGraw-Hill Book Company.
Donley J. M. (1999). Swimming kinematics of two scombrid fishes. MS thesis, California State University, Fullerton, USA.
Donley, J. M. and Dickson, K. A. (2000). Swimming kinematics of juvenile kawakawa tuna (Euthynnus affinis) and chub mackerel (Scomber japonicus). J. Exp. Biol. 203,3103 -3116.[Abstract]
Ellerby, D. J., Altringham, J. D., Williams, T. and Block, B. A. (2000). Slow muscle function of Pacific bonito (Sarda chiliensis) during steady swimming. J. Exp. Biol. 203, 1-13.[Abstract]
Fierstine, H. L. and Walters, V. (1968). Studies in locomotion and anatomy of scombroid fishes. Mem. S. Calif. Acad. Sci. 6,1 -31.
Finnerty, J. R. and Block, B. A. (1995). Evolution of cytochrome b in the Scombroidei (Teleostei): molecular insights into billfish (Istiophoridae and Xiphiidae) relationships. Fish. Bull. US 93,78 -96.
Fuiman, L. A. and Batty, R. S. (1997). What a
drag it is getting cold: Partitioning the physical and physiological effects
of temperature on fish swimming. J. Exp. Biol.
200,1745
-1755.
Gibb, A. C., Dickson, K. A. and Lauder, G. V.
(1999). Tail kinematics of the chub mackerel, Scomber
japonicus: testing the homocercal tail model of fish propulsion.
J. Exp. Biol. 202,2433
-2447.
Graham, J. B. (1973). Heat exchange in the black skipjack and the blood-gas relationship of warm-bodied fishes. Proc. Natl. Acad. Sci. USA 70,1964 -1967.[Abstract]
Graham, J. B., Koehrn, F. J. and Dickson, K. A. (1983). Distribution and relative proportions of red muscle in scombrid fishes: consequences of body size and relationships to locomotion and endothermy. Can. J. Zool. 61,2087 -2096.
Graham, J. B. and Dickson, K. A. (2000). The evolution of thunniform locomotion and heat conservation in scombrid fishes: New insights based on the morphology of Allothunnus fallai. Zool. J. Linn. Soc. 129,419 -466.[CrossRef]
Gray, J. (1933). Studies in Animal Locomotion. I. The movements of fish with special reference to the eel. J. Exp. Biol. 10,88 -104.
Hebrank, M. R. (1982). Mechanical properties of fish backbones in lateral bending and in tension. J. Biomech. 15,85 -89.[Medline]
Jayne, B. C. and Lauder, G. V. (1995). Speed effects on midline kinematics during steady undulatory swimming of largemouth bass, Micropterus salmoides. J. Exp. Biol. 198,585 -602.[Medline]
Johnson, T. P., Cullum, A. J. and Bennett, A. F.
(1998). Partitioning the effects of temperature and kinematic
viscosity on the C-start performance of adult fishes. J. Exp.
Biol. 201,2045
-2051.
Kishinouye, K. (1923). Contributions to the comparative study of the so-called scombroid fishes. Jour. Coll. Agric., Tokyo Imperial Univ. 8,293 -475.
Knower, T. (1998). Biomechanics of thunniform swimming: electromyography, kinematics, and caudal tendon function in the yellowfin tuna and the skipjack tuna. PhD dissertation, Scripps Institution of Oceanography, California, USA.
Knower, T., Shadwick, R. E., Katz, S. L., Graham, J. B. and
Wardle, C. S. (1999). Red muscle activation patterns in
yellowfin (Thunnus albacares) and skipjack (Katsuwonus
pelamis) tunas during steady swimming. J. Exp.
Biol. 202,2127
-2138.
Korsmeyer, K. E. and Dewar, H. (2001). Tuna metabolism and energetics. In Tuna Physiology, Ecology, and Evolution, Fish Physiology, vol. 19 (ed. B. A. Block and E. D. Stevens), pp. 36-71. New York: Academic Press.
Lighthill, M. J. (1969). Hydromechanics of aquatic animal propulsion. Ann. Rev. Fluid Mech. 1, 413-446.[CrossRef]
Lighthill, M. J. (1970). Aquatic animal propulsion of high hydromechanical efficiency. J. Fluid Mech. 44,265 -301.
Lindsey, C. C. (1978). Form, function, and locomotory habits in fish. In Fish Physiology, vol.7 (ed. W. S. Hoar and D. J. Randall), pp.1 -13. New York: Academic Press.
Long, J. H., Jr and Nipper, K. S. (1996). Body stiffness in undulating vertebrates. Amer. Zool. 36,678 -694.
Magnuson, J. J. (1970). Hydrostatic equilibrium of Euthynnus affinis, a pelagic teleost without a swim bladder. Copeia 1970,56 -85.
Magnuson, J. J. (1978). Locomotion by scombrid fishes: Hydromechanics, morphology and behavior. In Fish Physiology, vol. 7 (ed. W. S. Hoar and D. J. Randall), pp. 240-315. New York: Academic Press.
Nauen, J. C. and Lauder, G. V. (2000).
Locomotion in scombrid fishes: morphology and kinematics of the finlets of the
chub mackerel Scomber japonicus. J. Exp.
Biol. 203,2247
-2259.
Pyatetskiy, V. Y. (1970). Kinematic swimming characteristics of some fast marine fish. In `Hydrodynamic problems in Bionics', Bionika, vol. 4, Kiev (translated from Russian, JPRS 52605, pp.12 -23.Natl. Tech. Inf. Serv., Springfield, Virginia, 1971).
Rome, L. C. and Swank, D. (1992). The influence of temperature on power output of scup red muscle during cyclical length changes. J. Exp. Biol. 171,261 -281.[Abstract]
Rome, L. C., Swank, D. M. and Coughlin, D. J.
(2000). The influence of temperature on power production during
swimming. II. Mechanics of red muscle fibres in vivo. J.
Exp. Biol. 203,333
-345.
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., 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.
Shadwick, R. E., Katz, S. L., Korsmeyer, K. E., Knower, T. and
Covell, J. W. (1999). Muscle dynamics in skipjack tuna:
timing of red muscle shortening in relation to activation and body curvature
during steady swimming. J. Exp. Biol.
202,2139
-2150.
Shadwick, R. E., Steffensen, J. F., Katz, S. L. and Knower, T. (1998). Muscle dynamics in fish during steady swimming. Amer. Zool. 38,755 -770.
Videler, J. J. (1985). Fish swimming movements: A study of one element of behaviour. Neth. J. Zool. 35,470 -485.
Videler, J. J. and Hess, F. (1984). Fast continuous swimming of two pelagic predators saithe (Pollachius virens) and mackerel (Scomber scombrus): a kinematics analysis. J. Exp. Biol. 109,209 -228.
Wardle, C. S., Videler, J. J. and Altringham, J. D. (1995). Tuning into fish swimming waves: body form, swimming mode and muscle function. J. Exp. Biol. 198,1629 -1636.[Medline]
Webb, P. W. (1975). Hydrodynamics and energetics of fish propulsion. Bull. Fish. Res. Bd. Can. 190,1 -159.
Webb, P. W. (1978). Hydrodynamics: nonscombroid fish. In Fish Physiology, vol.7 (ed. W. S. Hoar and D. J. Randall), pp.190 -237. New York: Academic Press.
Webb, P. W. (1998). Swimming. In The Physiology of Fishes, 2nd Edition (ed. D. H. Evans), pp.3 -24. Boca Raton: CRC Press.
Westneat, M. W., Hoese W., Pell, C. A. and Wainwright, S. A. (1993). The horizontal septum: Mechanisms of force transfer in locomotion of scombrid fishes (Scombridae, Perciformes). J. Morphol. 217,183 -204.
Westneat, M. W. and Wainwright, S. A. (2001). Mechanical design for swimming: muscle, tendon, and bone. In Tuna Physiology, Ecology, and Evolution, Fish Physiology, vol.19 (ed. B. A. Block and E. D. Stevens), pp.272 -308. New York: Academic Press.