Energetics of median and paired fin swimming, body and caudal fin swimming, and gait transition in parrotfish (Scarus schlegeli) and triggerfish (Rhinecanthus aculeatus)
Marine Biological Laboratory, University of Copenhagen,
Strandpromenaden 5, Helsingør, DK-3000, Denmark
Present address: Department of Environmental Engineering, Institute of Life
Sciences, Aalborg University, Sohngaardsholmsvej 57, DK-9000 Aalborg,
Denmark
* Author for correspondence at present address: Hawaii Pacific University, Marine Sciences Program, 45-045 Kamehameha Hwy, Kaneohe, HI 96744, USA (e-mail: kkorsmeyer{at}hpu.edu )
Accepted 12 February 2002
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Summary |
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Key words: Scaridae, Balistidae, labriform, balistiform, aquatic locomotion, rigid-body swimming, undulatory swimming, respirometry, cost of transport
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Introduction |
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MPF swimming is generally considered to provide greater maneuverability and
stability at slow swimming speeds, while BCF swimming provides greater power
output for higher speeds and accelerations
(Webb, 1998). The features of
MPF swimming are presumably advantageous for movement through structurally
complex habitats, such as coral reefs, where many MPF specialists are found.
Specialization in MPF swimming, however, is considered to come at the cost of
reduced steady or BCF swimming performance in these fishes
(Webb, 1982
). The implication
is that MPF swimming, while more effective for maneuvering behaviors, is
energetically less efficient, and therefore BCF swimming is the ideal swimming
mode for steady swimming at cruise speeds. Thus, fishes requiring slow
maneuvering capabilities should be MPF swimmers, while open-water, cruise
swimmers should use a BCF mode of propulsion.
Alternatively, it has been proposed that swimming with an MPF gait should
have lower energetic costs, through a reduction in drag by keeping the body
rigid (Webb, 1975;
Gordon et al., 1989
;
Lighthill and Blake, 1990
).
Hydrodynamic models of fish swimming, and tracking water flows over both
swimming and non-swimming fish, suggest that the thrust required for
undulatory swimming is 1.5- to 5-fold higher than rigid-body drag
(Lighthill, 1971
;
Webb, 1998
;
Anderson et al., 2001
). The
additional thrust required for undulatory swimming is attributed to increased
friction drag, caused by boundary layer thinning, and energy loss in the
lateral recoil of the body (Lighthill,
1971
; Webb, 1982
;
Webb, 1992
). In this study we
tested the hypothesis that MPF swimming is more efficient than BCF swimming by
measuring total metabolic rate during both steady, rigid-body (MPF) and
undulatory (BCF) swimming in two species of fish specialized for MPF
swimming.
In addition to specialization for certain swimming modes, most fish use a
combination of gaits over their swimming performance range
(Webb, 1998). If one mode of
swimming is most efficient, then why do gait transitions occur? In terrestrial
vertebrates, it has been shown that each gait optimizes transport costs over
different ranges of speed, and that the animal chooses the gait that minimizes
power requirements at their current speed
(Alexander, 1989
). As speed of
locomotion increases, gait transition occurs to minimize energetic costs and
maximize endurance. It has been proposed that the same rationale governs gait
transition in fishes (Alexander,
1989
; Webb, 1998
).
For example, MPF swimming may be more efficient only at slow swimming speeds,
with BCF swimming becoming more efficient at higher speeds
(Blake, 1980
). An alternative
hypothesis is that gait transition occurs because the different
muscle-propulsor systems are effective over a limited range of performance
(Rome, 1994
). For example, MPF
gaits may be more effective for low speeds (providing greater stability and
maneuverability), while BCF swimming allows recruitment of additional muscle
to provide the power needed to achieve higher speeds
(Alexander, 1989
;
Webb, 1998
). We measured
metabolic rate over a range of swimming speeds and gaits, and tested whether
or not the cost of transport decreases after the transition from MPF to BCF
swimming as speed increases.
We studied two species of coral reef fishes considered to be MPF swimming
specialists. Schlegel's parrotfish, Scarus schlegeli (order
Perciformes, family Scaridae), uses labriform locomotion for routine swimming
(named after their sister family Labridae, the wrasses). This MPF swimming
mode involves flapping of the pectoral fins for propulsion. Although there
have been numerous studies of the kinematics of this mode of swimming
(Webb, 1973;
Blake, 1983
;
Gibb et al., 1994
;
Lauder and Jayne, 1996
;
Westneat, 1996
;
Drucker and Jensen, 1997
;
Walker and Westneat, 1997
;
Westneat and Walker, 1997
),
there have been few measurements of the metabolic costs of labriform
locomotion (Webb, 1974
;
Gordon et al., 1989
;
Parsons and Sylvester, 1992
).
The other species used in this study was the Picasso triggerfish,
Rhinecanthus aculeatus (order Tetraodontiformes, family Balistidae),
which is specialized for balistiform locomotion (named for the triggerfish
family). This MPF swimming mode uses undulations of the soft dorsal and anal
fins (Blake, 1978
,
1983
). We are aware of no
previous measurements of swimming metabolic rate in fish using this type of
locomotion. Both species switch gaits to body-caudal fin undulations (BCF
gait) at higher swimming speeds.
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Materials and methods |
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The swimming respirometer
The swimming respirometer, made of transparent Perspex, consisted of a
31-liter recirculation loop with flow generated by a propeller. Rectilinear
flow was promoted by baffle screens and deflectors followed by a honeycomb
flow-straightener (7 mm cell diameter), producing micro-turbulent flow through
the working section (47 cm long, 15 cm wide, 14.5 cm deep). As with any
swim-flume studies, we cannot rule out the possibility that wall effects
influenced fish swimming performance
(Webb, 1993), particularly for
median or paired fin swimming in which the propulsors extend perpendicularly
from the main body axis. Swimming respirometers must balance the need for a
sufficiently small volume (relative to fish mass) for accurate oxygen
consumption measurements with a large enough working section to minimize
hydrodynamic problems. Fish sizes were chosen to minimize these problems, and
data collected when the fish showed significant interactions with the flume
walls were discarded. For the triggerfish, the maximum vertical distance from
the tip of the soft dorsal to the tip of the anal fin ranged from 6.8 to 8.6
cm (flume depth 14.5 cm). For the parrotfish, pectoral fin span at maximal
extension ranged from 9.9 to 12.5 cm (flume width 15.0 cm).
Water flow speed was calibrated according to the voltage output of the propeller's motor controller. The swimming respirometer was submerged in an aerated, flow-through seawater bath (26-27 °C), and could be alternately sealed or flushed with water from the bath via a computer-actuated pump. The working section was covered with a blind to prevent the fish being disturbed by outside movements, and its activity was viewed via a video monitor.
Oxygen partial pressure (PO2) in the respirometer was measured with an oxygen electrode (Radiometer, E 5046) housed in a thermostated cuvette. A continuous flow of seawater from the respirometer was maintained past the electrode by a peristaltic roller pump at a rate of 3.5 ml min-1. The oxygen electrode was calibrated with air-saturated sea water several times a day.
Rate of oxygen consumption
(O2) was
measured using computerized, intermittent-flow respirometry
(Steffensen et al., 1984
). The
respirometer was periodically flushed with clean, aerated sea water from the
bath for 4 min followed by a 1 min closed mixing period and then 5 min of
closed respirometry, during which the decline in
PO2 in the system was recorded every second.
The flushing and measurement periods, and the data recording, were automated
by computer, providing a measure of oxygen uptake every 10 min. This system
has the advantage of providing frequent, high-resolution respirometry
measurements without washout problems, while keeping oxygen levels high
(>17 kPa, 80% saturation) and preventing buildup of metabolic waste
(Steffensen, 1989
).
Experimental protocol
Each fish was introduced into the respirometer the day prior to the
swimming speed test, and allowed to acclimate overnight at a water speed of
7-10 cm s-1. This flow rate maintained adequate water mixing, but
was not enough to induce swimming, and the fish eventually settled on the
bottom of the working section. Oxygen consumption measurements began
immediately, and continued overnight to obtain a measure of standard metabolic
rate (SMR, O2 at
zero swimming speed).
The following day, a critical speed (Ucrit) swimming
test was performed (Brett,
1964; Beamish,
1978
) with step-wise increases in flow speed of approximately 0.5
total length s-1 (L s-1) every 30 min
(3x10 min
O2 measurement
periods) until the fish fatigued, i.e. could no longer maintain its position
away from the downstream screen of the working section. Video recordings (50
fields s-1) were made at each flow speed for analysis of fin-beat
frequencies. Following the experiment, the fish were weighed and body
dimensions were measured. The triggerfish were returned to the wild and the
parrotfish were killed by an overdose of anesthetic (tricaine
methanesulfonate) for subsequent confirmation of species identification. After
each experiment, the oxygen consumption in the empty respirometer was measured
to determine background levels (10.8±7.7 mg O2
h-1, mean ± S.D., N=12), which were subtracted from
the experimental values for
O2.
Data calculations and analysis
Because water flow speed in the flume increases in the presence of a fish
that occupies part of the cross-sectional area of the working section
(solid-blocking effect), swimming speeds were corrected according to the
equations of Bell and Terhune
(1970):
![]() | (1) |
![]() | (2) |
Swimming gait and fin-beat frequencies were measured from video recordings. At each swimming speed and for each gait used, three separate periods of steady swimming were analyzed and the time for 10 complete fin beat cycles determined and averaged to give fin-beat frequency (beats s-1). Each swimming speed was analyzed over a 1 min time interval to determine the percentage of time spent using each gait.
The 30-min critical swimming speed (Ucrit) was
calculated as described by Beamish
(1978):
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Oxygen consumption rate
(O2) was
determined from the slope of a linear regression of the
PO2 decline over time for each measurement
cycle, using the formula:
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SMR was calculated from a frequency histogram of the raw
O2 data
collected overnight, excluding the initially elevated values immediately after
the fish was introduced into the respirometer. Two normal curves were fit to
the
O2 frequency
histogram to separate the SMR peak, when the fish was at rest, from the peak
of elevated metabolism seen during spontaneous activity (routine metabolic
rate) (Steffensen et al.,
1994
).
For the swimming speed test, periods of unsteady swimming (with the
exception of the burst-and-glide swimming mode seen at the highest speeds in
the parrotfish) and swimming against the sides of the flume were eliminated
from analysis. Multiple
O2 measurements
at the same speed were averaged for individual fish.
Two models were used to describe the relationship between
O2 and swimming
speed U. The first is the traditional exponential function
(Brett, 1964
;
Webb, 1975
;
Beamish, 1978
):
![]() | (5) |
![]() | (6) |
The second model is the hydrodynamics-based power function
(Wu, 1977;
Videler, 1993
):
![]() | (7) |
![]() | (8) |
To determine the effects of body mass, swimming gait, and swimming speed on
O2, and to
compare the slopes (analysis of covariance, ANCOVA), we used the General
Linear Model procedures of SYSTAT (version 10, SPSS Inc. 2000). For the
exponential model (equation 6), we used stepwise multiple regression analysis
to test for any significant effects on
log
O2 of
swimming speed, log(mass), gait, and the interaction terms:
log(mass)xspeed and gaitxspeed. Variables and interaction terms
that did not contribute significantly to the multivariate regression were
dropped, one at a time, and a new regression was calculated until only
variables with significant effects on
log
O2 remained.
The same procedure was repeated for the power model (equation 8), except that
effects on
log(
O2-a)
were tested, and log(speed) was substituted for speed. A significance level of
P<0.05 was used in statistical tests unless otherwise noted. Error
values are given as standard deviation (S.D.).
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Results |
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At low swimming speeds, the triggerfish swam using undulations of the
dorsal and anal fins (MPF gait, balistiform swimming). When swimming steadily,
the dorsal and anal fins undulated at the same frequency. The pectoral fins
were used only occasionally for maneuvering at the lowest speed (1.0
L s-1) and were held against the side at higher swimming
speeds. From 25 to 60 cm s-1 (1.5-3.0 L s-1),
body-caudal undulations (BCF gait) were used intermittently for increasing
amounts of time as speed increased, and were used continuously above 65 cm
s-1 (3.5 L s-1)
(Fig. 2A). During body-caudal
swimming, the dorsal and anal fins beat at the same frequency as the caudal
fin, with deflections in the same direction as the adjacent body undulations.
For the triggerfish, Ucrit ranged from 55 to 93 cm
s-1 (mean=76±14 cm s-1, N=5), or 3.2-5.0
L s-1 (mean=4.1±0.7 L s-1,
N=5), although the high end of the range maybe an underestimate, as
this was the maximal flow speed of the swim flume. With one exception,
fin-beat frequencies increased with swimming speed
(Fig. 2B). At the transitional
swimming speeds, when MPF and BCF gaits were used alternately, fin-beat
frequencies were generally lower during body-caudal swimming, than when using
the dorsal and anal fins alone (Fig.
2B).
|
Energetics
After placing the fish in the swimming respirometer,
O2 was typically
slightly elevated for a few hours, but then settled overnight, allowing the
determination of SMR, after excluding occasional increases in
O2 due to
spontaneous activity (Fig. 3).
Mean SMR for parrotfish was 31.5±11.4 mg O2 h-1
(N=7) or 127±27 mg O2 kg-1
h-1 (N=7), and for triggerfish was 10.2±4.4 mg
O2 h-1 (N=5) or 74.7±21.9 mg
O2 kg-1 h-1 (N=5). In both
parrotfish and triggerfish,
O2 increased
significantly with increases in swimming speed (Figs
4A,
5A).
|
|
|
In the parrotfish swimming using the MPF gait,
O2 increased
significantly with swimming speed (Fig.
4A) and was also positively correlated with body mass (scaling
exponent=0.81), but there were too few data to perform a regression for
swimming speed during the burst-and-coast BCF gait.
O2 during BCF
swimming was, however, significantly higher than during MPF swimming (ANCOVA,
Fig. 4A). After subtraction of
SMR from the swimming
O2 values to get
the net cost of swimming,
(
O2a),
the effect of mass was no longer significant
(Fig. 4B). The value
(
O2a)
in proportion to speed increased to the power 1.66 and also increased
significantly with the transition to the BCF gait (ANCOVA,
Fig. 4B).
For the triggerfish, swimming
O2 values were
grouped according to gait use; one set where only the MPF gait was
used, and one where both the MPF and the BCF gaits were used.
O2 increased
with swimming speed in both sets (Fig.
5A). However, the rate of increase (slope of the semi-log
regression) was significantly higher when the BCF gait was used (ANCOVA,
Fig. 5A). The net cost of
swimming also increased at a higher rate (to the power of 2.31) during BCF
swimming compared with MPF swimming (to the power of 1.55), although these
values were not significantly different (P=0.07)
(Fig. 5B). The lower
statistical significance is probably due to the loss of zero speed values
after calculating
(
O2a).
The effect of body mass on either
O2 or
(
O2a)
was not significant for the relatively narrow range of triggerfish body masses
investigated.
The total cost of transport (TCOT, Fig.
6), the amount of oxygen used per unit mass per unit distance, was
calculated for both species from the exponential relationships shown in Figs
4A and
5A. The relationship between
TCOT and swimming speed is typically U-shaped, with the swimming speed where
TCOT is at a minimum defined as the optimal speed (Uopt).
Parrotfish Uopt occurred during MPF swimming at 53 cm
s-1 (approximately 2.3 L s-1), with a minimum
TCOT of 176 mg O2 kg-1 km-1
(Fig. 6). As with total
O2, TCOT during
BCF swimming in the parrotfish was higher than during MPF swimming at the same
speeds. For the triggerfish, Uopt occurred at the highest
speed obtained with the MPF gait alone (25-29 cm s-1, or approx.
1.5 L s-1) at a TCOT of 120 to 128 mg O2
kg-1 km-1 (Fig.
6). Upon switching to the BCF gait, TCOT increased and continued
to increase with swimming speed.
|
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Discussion |
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Although specialized as MPF swimmers, both the parrotfish and triggerfish
could achieve high, prolonged swimming speeds (Ucrit) that
were comparable with similarly sized BCF swimmers (3-4 L
s-1) (Videler,
1993). These two species use different gaits to reach these high
swimming speeds. Parrotfish, and some other labriform swimmers, have replaced
BCF swimming with MPF swimming for cruise swimming, and the body and caudal
fin are only used for short-duration burst swimming
(Fig. 4) (Webb,
1974
,
1982
). At low swimming speeds,
the parrotfish appeared to be unstable, as we were unable to get them to swim
steadily below about 1.5 L s-1. Similar swimming
performance was found in another labriform swimmer, the bird wrasse
Gomphosus varius (family Labridae), which uses MPF swimming at speeds
up to 6 L s-1, but will not swim steadily below 1.2
L s-1 (Westneat,
1996
; Walker and Westneat,
1997
). These fishes are adapted for MPF swimming to obtain high,
sustained swimming speeds, and show poor swimming stability at low speeds,
despite the MPF swimming mode. Labriform swimmers show a range of swimming
capabilities from those that use labriform swimming for low-speed
maneuverability to those capable of high speed, sustained swimming. Drucker
and Lauder (2000
) found a
possible trade-off in pectoral fin morphology and kinematics between designs
that permit high swimming speeds (generation of high posteriorly directed
thrust), and those that permit a high degree of stability and maneuverability
at low speeds (generation of large lateral forces). Similarly, from
simulations of fin mechanics, Walker and Westneat
(2000
) concluded that fish
using the pectorals in a lift-based swimming mode, by `flapping' to generate
thrust on both the upstroke and downstroke, should be more energy efficient,
permitting high sustained swimming speeds, than those that use a drag-based
`rowing' mode. However, labriform swimmers using rowing mechanics should be
more effective at low speeds, although at greater energetic cost, because more
thrust is generated, facilitating maneuvering behaviors
(Walker and Westneat, 2000
).
These two extremes of labriform swimming also correlate with fin morphology;
high-speed lift-based swimmers possess elongate, high aspect-ratio fins, and
those that are slow, drag-based swimmers have more rounded, low aspect-ratio
fins (Webb, 1994b
; Walker and
Westneat, 1997
,
2000
,
Wainwright et al., 1999
).
This correlation between labriform swimming performance and fin morphology
is consistent with analyses of maneuverability and habitat use among coral
reef labriform swimmers. Those fishes with low aspect-ratio pectoral fins are
superior maneuverers, inhabiting low-wave energy areas of the reef or
remaining close to the substratum, while fish with high aspect-ratio fins are
predominant in areas with high water movement and at higher positions in the
water column (Gerstner, 1999;
Bellwood and Wainwright, 2001
;
Fulton et al., 2001
).
Consistent with their high sustainable swimming speeds, the parrotfish S.
schlegeli have high aspect-ratio pectoral fins and are often found above
the reef, swimming over large areas to forage, rather than within the reef
complex where precise maneuverability would be more advantageous
(Bellwood and Wainwright, 2001
;
K. E. Korsmeyer, J. F. Steffensen and J. Herskin, personal observations).
In contrast to the parrotfish, the triggerfish recruited body-caudal
undulations to achieve high, prolonged swimming speeds
(Fig. 5). This high-speed
endurance was particularly surprising because triggerfish are typically
considered to be highly adapted for low speed maneuverability at the expense
of achieving high, sustained swimming speeds
(Blake, 1978; Webb,
1982
,
1998
). Balistids, and the
Tetraodontiforms in general, show a high degree of morphological
specialization (Lauder and Liem,
1983
), including a truncate body with limited flexibility, which
is thought to limit BCF swimming, and development of defensive armor, which is
thought to compensate for lack of high-speed swimming ability to escape
predators (Lighthill and Blake,
1990
; Webb, 1994a
;
Brainerd and Patek, 1998
). The
limited flexibility of tetraodontiform fishes is a result of reduced vertebral
number (Brainerd and Patek,
1998
), which limits maximal body curvature in these fishes, and
probably reduces startle-response escape speeds (C-starts) that involve
extreme bending of the body from a stationary position
(Brainerd and Patek, 1998
). At
slow swimming speeds, triggerfish are clearly highly maneuverable and stable
using balistiform locomotion. The large, flexible dorsal and anal fins can
move independently and produce thrust in many different directions
(Webb, 1998
). These fish can
hover, swim backwards, and turn about their own axis with little lateral
translation of the body (Blake,
1978
). In addition, we found they are capable of sustaining
swimming speeds of about 4 L s-1 (for at least 30 min)
using body-caudal undulations, in addition to the undulations of the dorsal
and anal fins (Figs 2 and
5). For sustainable swimming
speeds at least, there appears to be no reduction in BCF swimming performance
in the triggerfish. Any limitation in body and caudal fin undulation, if
present, might be offset by the simultaneous use of the median fins. This
high-speed swimming ability may be advantageous for the triggerfish to hold
station in strong surge currents produced by wave action on the reef. Other
tetraodontiform MPF specialists, boxfish (family Ostraciidae), puffers (family
Tetraodontidae) and burrfish (family Diodontidae), are also highly
maneuverable at low swimming speeds, and through a combination of gaits using
pectoral, median and caudal fins can reach high, prolonged swimming speeds
(Arreola and Westneat, 1996
;
Gordon et al., 1996
,
2000
;
Walker, 2000
;
Hove et al., 2001
).
It appears that MPF gait specialization does not necessarily limit
sustainable, steady swimming performance, although the gaits used to achieve
high swimming speeds vary. Within a given gait, however, there is a trade-off
for specialization within a certain range of swimming performance, as
discussed above for labriform swimmers. In the parrotfish, the MPF gait
appears to be adapted for moderate to high sustainable swimming speeds,
limiting slow speed maneuverability, but permitting specialization of the BCF
gait for high speed sprints and accelerations
(Webb, 1982). Conversely, in
the triggerfish, the MPF gait allows a high degree of stability and
maneuverability at low speeds, but the fish must rely on BCF swimming to
support high sustainable swimming speeds. Rapid sprints (burst swimming) by
the triggerfish may be limited, however, as predicted for startle-response
maneuvers (Brainerd and Patek,
1998
).
Use of models to predict swimming energetic costs
The exponential equation (equations 5 and 6) is a valid model for relating
total O2 with
swimming speed in numerous fish species
(Webb, 1975
). With only two
constants to derive, it is more robust than the power function, and more
reliable for making predictions beyond the range of measured values. This is
particularly true for estimating SMR by extrapolating the
log
O2 values as
a function of speed to zero speed (Brett,
1964
; Bushnell et al.,
1984
; Dewar and Graham,
1994
).
The slope of the semi-log transformation of the exponential function
(factor b in equation 6; Figs
4A,
5A) indicates how quickly total
energetic costs increase as swimming velocity increases, and has been used as
a comparison of swimming efficiencies among species
(Bernatchez and Dodson, 1985;
Gordon et al., 1989
;
Dewar and Graham, 1994
).
However, this slope can be misleading because it is highly dependent on the
y-intercept, or SMR. Two different fish with the same net cost of
swimming (swimming
O2SMR)
but different SMRs will have different slopes (b)
(Korsmeyer and Dewar, 2001
).
Although suitable for comparing swimming costs among fish of the same or
similar SMR (e.g. among the same group of fish as in
Fig. 5A), the slope of the
exponential relation cannot be used for comparison of swimming costs in fishes
with different SMRs (e.g. different species).
In contrast, the power function (equation 7) takes into account differences
in SMR (factor a in equation 7), so that the power to which velocity
is raised (factor c) can be used to compare incremental swimming
costs among species. However, unlike the exponential function, fitting the
power equation to total
O2 (equation 7)
will overestimate SMR because iterative least-squares regression with this
equation tends to place more weight on the higher speed values
(Videler and Nolet, 1990
). The
transformation of the power equation (equation 8) results in a linear
relationship between the log of the net cost of swimming
(
O2SMR)
and the log of speed (Figs 4B,
5B). Fitting to this linear
form of the power equation (equation 8) is preferable because it avoids
overestimation at the lower values, but it also requires an accurate measure
of SMR in order to calculate
(
O2SMR)
(see Steffensen, 1989
, for a
discussion of common errors in respirometry).
Because it is the energy expended beyond the maintenance metabolism that is
related to the energy to produce thrust, comparison of the net cost of
swimming is more appropriate than of total
O2. In addition,
the power function follows standard hydrodynamic laws, where the log of thrust
(= the power to overcome drag) is directly related to the log of speed
(Brett, 1964
;
Wu, 1977
;
Videler, 1993
). The rate at
which the log of the net swimming cost increases with the log of speed is
found in factor c (the slope, or the power to which speed is raised
in the untransformed form of the equation, equation 7). This value provides
information on the aerobic swimming efficiency
(Wardle et al., 1996
) and best
represents `delta efficiency', the incremental costs above resting, or
maintenance, metabolic costs (Blake,
1991
; Full, 1991
).
It should be noted, however, that this model assumes that maintenance costs
remain the same at different swimming speeds, and this may not be the case
(Farrell and Steffensen,
1987
). Nevertheless, it is the slope from the best-fit power
function (equation 8) that we recommend be used for comparisons of swimming
efficiency among different groups or species of fishes.
Energetics of MPF versus BCF swimming
For the triggerfish and parrotfish, it appears that undulatory BCF swimming
entails a higher cost than rigid-body MPF swimming. When the parrotfish
switched to a BCF gait, they also used a burst-and-coast mode of swimming.
This swimming pattern is associated with use of the fast glycolytic (FG, or
white) muscle (Videler and Weihs,
1982; Rome et al.,
1990
), which is consistent with the fish's rapid fatigue at these
speeds. Other labriform swimmers, including many labrids and the threespined
stickleback (Gasterosteus aculeatus), show the same swimming pattern,
switching from pectoral fin use to BCF bursts at maximal sustained swimming
speeds, and rapid fatigue results because the myotomal muscle lacks slow
oxidative (SO, or red) fibers (te Kronnie
et al., 1983
; Whoriskey and
Wootton, 1987
; Davison,
1988
; Walker and Westneat,
2002
). Swimming costs in the parrotfish, as measured by oxygen
consumption, increased during burst-and-coast swimming compared with that
predicted for MPF swimming at the same swimming speeds
(Fig. 4). Actual swimming costs
were probably much higher, as only aerobic metabolism was measured, and the
additional anaerobic contribution from use of FG muscle is not included in
O2
The triggerfish used BCF swimming at sustainable (aerobic) speeds,
indicating the primary use of SO muscle. It is not surprising that total
O2 and net
swimming costs increased at a faster rate with swimming speed once the muscles
powering body-caudal undulations were recruited in addition to those powering
the undulations of the dorsal and anal fins
(Fig. 5). Although R.
aculeatus has a significant amount of myotomal SO muscle to power
sustained BCF swimming (K. E. Korsmeyer, unpublished observations), in other
balistids SO fibers are only found in the fin muscles, and the body
musculature is composed entirely of FG fibers
(Davison, 1987
). In these
species, sustainable swimming speeds would be limited to those that could be
powered by balistiform locomotion alone. Among balistiform swimmers, there may
be a range of performance specializations within this swimming mode equivalent
to that seen in labriform swimmers (see above).
The power to which net swimming costs increased with speed was similar for
both the parrotfish (1.66) and the triggerfish (1.55) when swimming in an MPF
gait (Figs 4B and
5B). When the triggerfish added
BCF swimming, the rate at which total
O2 increased
nearly doubled, and net swimming costs increased to the power of 2.31
(Fig. 5). Few studies
comparable with this study of fish swimming energetics have used the power
equation (equation 7). In a study of swimming metabolism of the horse
mackerel, Trachurus trachurus (family Carangidae, a BCF carangiform
swimmer), where SMR was also measured, swimming costs increased with speed to
the power 2.56 (Wardle et al.,
1996
). This value is similar to that determined for the
triggerfish during BCF swimming, and much higher than our MPF swimming values
(Figs 4B,
5B).
Gordon et al. (1989)
measured swimming
O2 in two
labriform swimmers, the shiner surfperch Cymatogaster aggregata
(family Embiotocidae) and the señorita wrasse Oxyjulis
californica (family Labridae). The rates of increase in total
O2 with swimming
speed in that study were extremely low, and in many cases not significantly
different from zero. Although this suggests very low costs of swimming, the
authors caution that their results could be due to confounding factors
(Gordon et al., 1989
).
Variability in
O2 was very
high, suggesting that metabolism was elevated due to stress or excitement,
particularly at low swimming speeds. SMR was not measured, and the power
function, which was difficult to fit to their data, gave highly variable
exponents (0.16-5.8), and is therefore difficult to compare with our results.
A previous study using one of the same species (C. aggregata) found
significant increases in
O2 with swimming
speed, and although a power function was not fit to the data, the results show
increases in net swimming costs similar to those we found for the parrotfish
(Webb, 1974
).
In contrast to our results, Parsons and Sylvester
(1992) found that total
O2 decreased
with a switch in swimming gait from MPF (labriform) to BCF swimming in white
crappie Pomoxis annularis (family Centrarchidae). Unlike the
parrotfish, the crappie use labriform swimming only up to about 1 L
s-1, before switching to BCF swimming for higher sustained swimming
speeds (Parsons and Sylvester,
1992
). The higher costs of labriform swimming in these fish may be
due to fin specialization for stability and maneuverability at low speeds,
which is associated with less efficient fin mechanics
(Walker and Westneat, 2000
).
In addition, the costs to control stability increase as speed decreases, often
resulting in elevated metabolic rates at low speeds
(Webb, 1998
). Such elevation
was seen for the labriform swimmer C. aggregata below 1 L
s-1 (Webb, 1974
).
We did not measure
O2 in either the
parrotfish or triggerfish at water speeds below 1 L s-1
because the fish would not swim, or only swam unsteadily, so that we could not
determine swimming speed. It is reasonable to predict that
O2 would be
elevated because, for example, the triggerfish have higher than expected
fin-beat frequencies at very low swimming speeds (<0.5 L
s-1) (Blake, 1978
).
These higher costs for stability at very low speeds may obscure energetic
advantages of MPF swimming.
The apparent energy savings with MPF swimming were similar in both the
parrotfish and triggerfish, which supports the hypothesis that MPF swimming is
more efficient than BCF swimming, possibly due to the reduced drag of
rigid-body swimming (Webb,
1975; Lighthill and Blake,
1990
). In addition, Lighthill
(1990
;
Lighthill and Blake, 1990
)
calculated that balistiform propulsion by median fins attached to a deep,
rigid body would increase the efficiency of thrust production. Among labriform
swimmers, those with high aspect-ratio pectoral fins are also predicted to
benefit from a high mechanical efficiency
(Walker and Westneat,
2000
).
One consequence of a lower increase in swimming costs using an MPF gait is
that the minimum cost of transport occurs at a higher speed
(Fig. 6). Although the
triggerfish change gaits before reaching the minimum, the parrotfish have a
very high Uopt (approximately 2.3 L
s-1) compared to the expected Uopt for fish of
this size (approximately 1.3 L s-1)
(Videler, 1993), which
suggests that they are adapted for relatively high routine swimming speeds.
Also, the parrotfish TCOT-U curve is very flat above 30 cm
s-1 (approximately 1.5 L s-1), meaning that
distance-specific transport costs change little over a broad range of swimming
speeds. A similarly shallow TCOT curve was found for another MPF swimmer, the
boxfish Ostracion meleagris
(Gordon et al., 2000
),
suggesting this may be a common feature of rigid-body MPF swimmers. However,
the minimum TCOTs for the triggerfish and parrotfish, and also the boxfish,
are similar to that of other fishes
(Videler, 1993
;
Gordon et al., 2000
). Using
the minimum TCOT to compare swimming energetics among fishes does include the
costs of SMR, which are not directly related to swimming costs, however, and
differences in Uopt (which are also highly dependent on
SMR) mean that comparisons are made at different relative swimming speeds.
Perhaps as a result of this, most of the variation in TCOT among fishes is
explained by differences in body mass
(Videler, 1993
).
Energetics of gait transition
Unlike terrestrial vertebrates, the change of gait at higher speeds in the
parrotfish and triggerfish does not appear to be a mechanism to reduce costs,
but may occur because of a limitation in achievable thrust in any one
particular gait. The similar rates of increase in MPF swimming costs in the
parrotfish and triggerfish (Figs
4B,
5B) result in similarly shaped
TCOT-U curves (Fig.
6). While the parrotfish is able to achieve high swimming speeds
within the MPF gait, keeping TCOT low, the triggerfish must switch to BCF
swimming, with its higher transport costs
(Fig. 6). Why don't the
triggerfish use MPF swimming at higher speeds, if swimming costs would be
lower?
Minimization of energetic cost is not the only explanation for a change in
gait. There are potential limitations in the amount of muscle and propulsors
for thrust production that accompany use of median or paired fins
(Alexander, 1989;
Webb, 1998
). In addition,
there are several distinct muscle types, ranging from high-endurance,
low-power SO fibers to low-endurance, high-power FG fibers, which also differ
in the contraction rates at which they produce optimal power (Rome et al.,
1988
,
1990
). To achieve the highest
speeds and accelerations, most fish use the large mass of FG axial, myotomal
muscle, which powers body and caudal fin undulations
(Webb, 1998
). Likewise, when
the parrotfish reach maximal prolonged swimming speeds, they must switch to
BCF undulations to recruit a large amount of FG muscle. These burst swimming
speeds are used to escape from predators, where high propulsive efficiency is
not as important as rapid acceleration.
The triggerfish, therefore, may not be able to power higher swimming speeds
using only the dorsal and anal fins, because of limitations in recruitable
muscle mass or fin-propulsive mechanics. Limits in thrust production are
supported by the observed fin-beat frequencies during transitional swimming
speeds. Dorsal and anal fin-beat frequencies were higher when swimming with an
MPF gait than when swimming with the added use of the caudal fin, at the same
swimming speed (Fig. 2). In
other words, the additional fin use permitted a lower fin-beat frequency to
produce the same forward speed. Our results suggest that gait transition does
not occur to minimize power requirements, as is the case for terrestrial
locomotion (Alexander, 1989),
but instead to meet the greater power requirements required at these higher
swimming speeds. For aquatic locomotion, gait transition may have more to do
with generating the rapidly increasing thrust necessary to swim faster in such
a dense and viscous medium.
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