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First published online September 19, 2006
Journal of Experimental Biology 209, 3708-3718 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02449
Pectoral fin coordination and gait transitions in steadily swimming juvenile reef fishes
1 Department of Organismal Biology and Anatomy, The University of Chicago,
1027 E. 57th Street, Chicago, IL 60637, USA
2 Committee on Neurobiology, The University of Chicago, Chicago, IL 60637,
USA
3 Committee on Computational Neuroscience, The University of Chicago,
Chicago, IL 60637, USA
4 Department of Zoology, Field Museum of Natural History, 1400 South
Lakeshore Drive, Chicago, IL 60605, USA
* Author for correspondence (e-mail: mhale{at}uchicago.edu)
Accepted 20 July 2006
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Summary |
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Key words: gait, pectoral fin, development, functional morphology, locomotion, biomechanics
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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). Most often
these characteristics are patterns of movement such as the order of limb
support during terrestrial locomotion (reviewed by
Biewener, 2004), although
discrete differences in control of locomotion, such as use of red muscle or
white muscle to generate movement (e.g.
Webb, 1994;
Alexander, 1989), can also
define gaits even without distinct changes in movement pattern. Animals often
make transitions through several gaits before reaching their peak speed. They
are thought to change gaits in order "to minimize the energy cost of
traveling at their chosen speed"
(Alexander, 2003) or due to
biomechanical and physiological limitations on movement patterns
(Drucker and Jensen, 1996b;
Korsmeyer et al., 2002).
In terrestrial vertebrates, common gaits include walking, running/trotting
and galloping. Limbed gaits can be classified as symmetrical and asymmetrical.
During symmetrical gaits, paired limbs are either actuated synchronously, in
phase with one another, or alternate 180° out of phase. Asymmetrical gaits
encompass all other limb relationships. The speeds at which gait transitions
occur are related to aspects of body size. For terrestrial limb-based
locomotion, the body dimension used is hip height, which is expressed as a
component of the Froude number, a dimensionless number which
"normalizes the forward velocity of a moving animal to its limb
length and gravitational acceleration"
(Biewener, 2004). Gait
transitions tend to occur at about the same Froude number across species
(Alexander and Jayes, 1983;
Alexander, 1989;
Griffin et al., 2004).
In contrast to terrestrial locomotion, in which multiple gaits have been
well studied, the research on gaits during swimming has largely focused on
axial propulsion. During swimming, fishes often go through the following
series of gaits with increasing swimming speed (reviewed by
Alexander, 1989;
Alexander, 2003;
Webb, 1994): (1) fin
propulsion, (2) burst and coast axial locomotion powered by red muscle, (3)
steady swimming with red muscle, (4) burst and coast axial locomotion powered
by white muscle, (5) steady swimming with white muscle. However, the studied
fish from which these gait transitions were proposed, including carp
(Rome et al., 1990), milkfish
(Katz et al., 1999), cod and
saithe (Videler and Weihs,
1982), tend to rely heavily on the axis and caudal fin as their
primary propulsors, rather than the pectoral fins.
Many fish species use the pectoral fins as the primary propulsors, using
axial propulsion only near peak speeds
(Westneat, 1996). Pectoral
fin, or labriform, locomotion is particularly common among reef fishes. In
this form of swimming the pectoral fins are generally actuated synchronously
with one another in forward swimming
(Webb, 1973;
Archer and Johnston, 1989;
Gibb et al., 1994;
Drucker and Jensen, 1996a;
Westneat, 1996;
Walker and Westneat, 1997;
Mussi et al., 2002). Speed can
be increased gradually by increasing fin beat amplitude and/or frequency.
Labriform swimmers change to body-caudal fin swimming near their peak speed.
Recent work (Korsmeyer et al.,
2002) suggested that at least some of these species are not able
to swim steadily at low speeds, below approximately 1.5 L
s-1, due to decreased stability.
While synchronous pectoral fin actuation is the most common fin
coordination pattern, symmetrical alternating fin movements have also been
described. Alternating pectoral fin movements have been shown to function
during station holding, maneuvering and other nonlinear swimming events
(Drucker and Lauder, 2003;
Hove et al., 2001), and
several studies have described alternating fin movements associated with
steady forward locomotion. Burrfish (Chilomycterus shoepfi) maintain
pectoral fin strokes that are approximately 180° out of phase through a
wide range of speeds (Arreola and Westneat,
1996). As with synchronous fin movement, burrfish fin beat
frequency increased with increasing swimming speed. Larval plaice
(Batty, 1981) and zebrafish
(Müller and van Leeuwen,
2004; Thorsen et al.,
2004) have been shown to alternate their pectoral fins during slow
locomotion. In the zebrafish, this behavior is generally lost during the
juvenile stage of development (Thorsen et
al., 2004). In several cases, fishes have been shown to perform a
gait transition from alternating pectoral fin locomotion to axial/caudal
locomotion with an increase in swimming speed
(Müller and van Leeuwen,
2004; Thorsen et al.,
2004) or type of movement
(Drucker and Lauder, 2003).
Sub-adult fish swimming has received little attention compared to that of
adults but data from larval fishes indicate that, in at least some species
such as zebrafish (Thorsen et al.,
2004), fin movement patterns are distinct from ones observed in
adults and that these patterns change markedly through ontogeny.
In this study, we investigated pectoral fin gait transitions of fishes by
examining swimming through a range of speeds in juveniles of the sapphire
damselfish Pomacentrus pavo and an additional 11 reef species from
three families. By examining a range of juveniles from species that are
pectoral fin specialists, we aimed to explore the patterns and performance of
fin swimming in sub-adult fishes and to examine the use of synchronous and
alternating pectoral fin coordination in swimming. We found a discrete
transition from alternating to synchronous fin beats at intermediate speeds,
prior to the pectoral fin to body-caudal fin transition. Informed by studies
of the synchronous fin coordination to body-caudal fin gait transition, we
investigated the alternating to synchronous gait transition and hypotheses for
the cause of the transition, including energy efficiency across speeds,
stability within specific speed ranges
(Korsmeyer et al., 2002;
Arreola and Westneat, 1996) and
mechanical or physiological limits of the observed gait
(Drucker and Jensen, 1996b;
Korsmeyer et al., 2002). We
propose that alternating pectoral fin beats may be a common swim propulsion
mechanism early in development and that the transition from alternating to
synchronous pectoral fin gaits is a common feature of juvenile fish locomotion
in coral reef species that use their pectoral fins as a primary mode of
propulsion as adults.
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Materials and methods |
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To record kinematics at a range of steady swimming speeds, we filmed the animals in a small flow tank (working section 3.5 cmx3.5 cmx12.5 cm) in flow that ranged from 1.12-11.13 cm s. Ventral views provided the clearest images of bilateral fin movement. Because filming directly from ventral view was not possible due to the flow tank structure, a first surface mirror was positioned at a 45° angle under the tank to reflect ventral views so that images could be collected by a camera positioned to the side of the tank. We monitored each fish visually to determine its dorsoventral position in the tank. We used small fish (<4 cm) in our experiments and only analyzed video in which the fishes swam in the center of the tank, in order to minimize wall effects. Fishes were filmed using a Sony digital video camera de-interlacing frames to achieve a frame rate of 60 Hz. This frame rate is too low to capture fine details of fin movements at most of the fin beat frequencies recorded and we focused instead on describing patterns of pectoral fin coordination. After we recorded locomotor kinematics, fish were euthanized and preserved for subsequent morphological analysis and to confirm species identifications.
Video clips were viewed with an Apple Macintosh G4 using Adobe Premiere 6.5. The videos of Pomacentrus pavo were analyzed and cut into clips featuring the fish performing steady swimming for approximately 5 fin beats against a steady current. Clips were then de-interlaced for field-by-field analysis with QuickImage, a NIH Image based program written by Dr Jeff Walker, University of Southern Maine, ME, USA. Coordinate points were digitized on physical landmarks along the central midline of the fish, the base and tip of both pectoral fins, the caudal peduncle, and the tip of the caudal fin, and for each frame of a sequence. Based on the movement of these landmarks, kinematic variables were calculated using a series of algorithms in a custom-written kinematics program (CodeWarrior Pascal, Metrowerks Corporation, Austin, TX, USA) on an Apple Macintosh G5. Variables included pectoral fin frequency, fin angle to the body (amplitude), pectoral fin chord length in ventral projection, axial bending angle at midbody and at the tail base, change in fore-aft (thrust) and left-right (yaw) position of the nose tip, phase lag, advance ratio and reduced frequency.
Kinematic analysis for Pomacentrus pavo
We analyzed trials from three fish at 5-6 swimming speeds per fish. The
number of trials varied among animals: 15, 25 and 19, respectively for fish
1-3 for a total of 59 trials. Of these trials, 21 were of alternate pectoral
fin swimming, 27 of synchronous and 11 included the transition between gaits.
Phase lag between fins during swimming was calculated to identify left-right
oscillation patterns. If two oscillatory waves have the same frequency, then
their phase relations can range from 0° (synchrony) to 180° out of
phase (asynchrony) up to 360° (back to synchrony)
(Denny, 1988). The relative
position of the right and left fins during each fin beat was used to calculate
phase lag by determining the position of the left fin at the time of maximum
right pectoral fin abduction (maximum angle away from the body). Phase lag
thus ranged from 0° (perfectly in phase, with both fins reaching maximum
abducted position synchronously) to 180° (perfectly out of phase,
indicating alternate fin beats, with left fin maximally adducted at the time
of peak right fin abduction). Intermediate values of phase lag
(0>phase>180) were computed by the equation
(abs(Trmax-Tlmax)/Tcycle)x360,
where Trmax=time of peak right angle,
Tlmax=time of peak left angle, and
Tcycle=total fin cycle time. Taking the absolute (abs)
value of timing between right and left peaks ensured that phase lag ranged
from 0 to 180°.
We examined fin beat amplitude and frequency to determine whether, as in adult fishes, these parameters vary with swimming speed and whether there is a discontinuity in either parameter at the transition from asynchronous to synchronous fin beats. The angle of each pectoral fin leading edge to the body was computed and used to determine angular displacement of each fin for each video frame and the time of maximum and minimum fin position. Fin beat frequency (Hz) was computed for each video clip by dividing the number of fin beats by total time of the video sequence. In addition, we determined the speed of the transition from pectoral fin swimming to body and caudal fin swimming (Upc). Caudal fin amplitude was calculated as the angular movement of the tip of the caudal fin relative to the axis of the body rostral to the caudal peduncle.
To examine the efficiency of fin propulsion during alternating and
synchronous forms of pectoral fin locomotion we calculated the advance ratio
(J). The advance ratio is a dimensionless number that relates the
velocity of the body to the velocity of the fin. Thus, higher advance ratios
indicate higher fin beat efficiency. Advance ratio is calculated as:
 | (1) |
where 
=fin angle/180°, U=forward speed (m s),
Lp=pectoral fin length (m), and
Fp=pectoral fin beat frequency (Hz)
(Drucker and Jensen,
1996a).
Oscillating fins accelerate water, particularly at the start and end of a
stroke. A force called the acceleration reaction resists these changes in
velocity of the fluid surrounding the fin. Daniel summarized the importance of
acceleration reaction nicely: "while drag is the resistance to
motion through a fluid, the acceleration reaction is resistance to changes in
velocity of that motion" (Daniel, 1984). The reduced frequency
parameter is a dimensionless number that characterizes the importance of
acceleration reaction in the thrust obtained from an oscillating appendage
(Daniel, 1988;
Vogel, 1994). Reduced
frequencies were calculated for each fin by the following equation:
 | (2) |
where n=fin beat frequency (Hz), c=maximum chord of the
fin perpendicular to the fin rays (in cm), and U=forward velocity (in
cm s-1) (Vogel,
1994). Typically acceleration reaction forces dominate at reduced
frequency numbers above 0.5.
We calculated Reynolds number (Re) to examine whether the change in
pectoral fin gait is associated with changes in the fluid regime experienced
by the fish. Reynolds number is a dimensionless number calculated as:
 | (3) |
where 
=water density (kg m-3), U=swimming speed (m
s-1), L=characteristic length (m), and µ=dynamic
viscosity (kg ms). We used fish body length (BL) as the
characteristic length in our calculations. Although studies differ, frequently
locomotion at Re values <100 is considered to be dominated by viscous
(resistive) forces and >1000 to be dominated by inertial (reactive)
forces.
We assessed the pattern of thrust by tracking the oscillatory motion of the tip of the snout, our most reliable single point that served as a proxy for the center of mass of the fish. Increased snout tip oscillation from left to right (increased yaw) was predicted for alternate fin strokes. In order to estimate thrust oscillations, we calculated the mean excursion of the point digitized at the tip of the snout in the direction flow through each trial. To determine yaw, we calculated the mean excursion of the tip of the snout perpendicular to the direction of flow through each trial.
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Statistics
We used regression analysis to test the significance of the relationship
between swimming velocity and kinematic variables. To test whether variables
such as frequency, amplitude, advance ratio, phase lag, Reynolds number and
thrust oscillation were significantly different when the fish were performing
synchronous versus alternating gaits, we performed simple two-way
analyses of variance (ANOVA) with gait and individual as main effects. All
variables were tested for homogeneity of variance, and for two variables in
which the variance was significantly different between gaits, we report Welch
ANOVA values corrected for unequal variance. Sequential Bonferroni correction
(Rice, 1989) was used to
determine significance of F ratios due to the use of eight ANOVAs on
the data set. For those variables that had a significant overall regression
with swimming speed (such as frequency, amplitude and advance ratio), we asked
whether the relationship with speed was significantly different during use of
the two pectoral fin gaits. For this we applied analyses of covariance
(ANCOVA) to determine whether the slopes or intercept of the velocity
regression were significantly different, using synchronous versus
asynchronous gait as the main effect. All analyses were performed using the
JMP version 3.16 statistical package (SAS Institute, Cary, NC, USA).
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The pectoral fin to axial-caudal fin transition occurred at approximately 8 BL s-1 (Fig. 5). As at the alternating to synchronous pectoral fin transition, fish often switched back and forth between these locomotor gaits at the transition speed. Fig. 5B illustrates a transition from pectoral fin swimming before 0.17 s to axial locomotion and then back to pectoral fin locomotion at approximately 0.25 s. We did not record sustained axial steady swimming in any species examined due to constraints on the maximum flow speeds produced in our tank and rapid fatigue of the fish at the highest speeds recorded.
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Amplitude (Fig. 6B) ranged from 50° to 142° across gaits (mean 98±3.0°), 50-113° (mean: 79.7±3.2°) for alternating fin beats, 87-142° (mean: 112.3±2.9°) for synchronous and was significantly different (P<0.0001, F=56.7) between the two gaits. Across alternating and synchronous gaits there was an overall increase in amplitude with length-specific swimming speed (R2=0.70) with a slope significantly different from zero (P<0.0001) (Table 1). There was a significant difference in the slopes of amplitude with swimming speed for the two gaits (ANCOVA; P<0.038, F=4.52) with amplitude increasing more rapidly with increasing swimming speed during the alternating fin gait (Table 1).
The reduced frequency parameter showed that acceleration reaction was a
dominant force at all speeds for the juvenile fishes
(Fig. 7A). Acceleration
reaction forces dominate at reduced frequencies of greater than 0.5
(Webb, 1988), and all values
for P. pavo were greater than 1.0. Reduced frequency was particularly
high at low swimming velocities where, despite low speeds, the fins were
oscillating rapidly. Values dropped off quickly to below 10 as swimming speed
increases to 2 BL s-1. There was no apparent discontinuity
in reduced frequency at the gait transition speeds
(Fig. 7A).
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Oscillation of the position of the head in the direction of forward movement provided an indicator of thrust oscillations during the fin stroke cycles (Fig. 8). Head oscillation increased linearly with swimming speed (R2=0.64) from a minimum of 0.017 cm to a maximum of 0.076 cm (Fig. 8, Table 1). Overall, oscillations were lower during the alternating fin gait (range: 0.017-0.056 cm, mean: 0.028±0.002 cm) than during the synchronous fin gait (range: 0.031-0.076 cm, mean: 0.0528±0.002 cm) and there was no discrete transition in forward oscillation between the two gaits.
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Reynolds number ranged from 118-3543 (mean: 1243±101), an interval in which fluid conditions are shifting from being dominated by viscous forces to being dominated by inertial forces. Individual fishes showed clear (by definition) trends of increasing Re with increasing speed, but there was no significant correlation between Reynolds number and the transition point between alternating and synchronous fin gaits across individuals (Table 1).
Pectoral fin gaits in juveniles of multiple species
In order to determine whether the alternating to synchronous fin gait
transition observed in P. pavo is a more general phenomenon, we
surveyed gaits in 33 individuals from 10 other coral reef species
(Table 2). Because of the
difficulties in collection and performance of these experiments on small
subadult fishes under field conditions, we had to be opportunistic when
collecting and the numbers of specimens per species varies. In these species
we saw the same pattern of alternating fin beats at low speeds switching to
synchronous fin beats at higher speeds that we observed in P.
pavo.
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Across all species and trials recorded, synchronous fin coordination occurred at a significantly higher length-specific speed than alternating fin coordination [alternating: 2.57±0.12; synchronous: 3.43±0.18 (P<0.0001)]. However, the transition did not occur at a particular length-specific speed. That point is demonstrated by the range of swimming speeds recorded for each gait, which show considerable overlap. Alternating fin coordination occurred at 0.79-7.52 BL s-1 and synchronous fin coordination was observed at 0.89-8.50 BL s-1.
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), these two gaits were distinct with a rapid transition
between fin coordination patterns.
The gait pattern reported here in fishes is similar to that observed in
tetrapod taxa. For example, frogs and toads have been shown to use alternating
hindlimb movements for slow walking but transition to synchronous fin
coordination during faster hopping (e.g.
Anderson et al., 1991;
Nauwelaerts and Aerts, 2002).
A similar transition as been demonstrated for frog swimming, a switch from
alternating to synchronous hindlimb movement with increasing speed
(Nauwelaerts and Aerts,
2002).
Steady pectoral fin swimming in fishes has generally been described as
either synchronous (e.g. Drucker and
Jensen, 1996a; Walker and
Westneat, 1997; Mussi et al.,
2002) or alternating (Arreola
and Westneat, 1996). Fin beat amplitude and frequency increase
with increasing swimming speeds until the fish either switch to an axial gait
or reach peak swimming speed. In the unusual case of the boxfish, alternating
and synchronous pectoral fin coordination patterns are both used
(Hove et al., 2001). The use
of these gaits by boxfish differed strikingly from the patterns we describe in
P. pavo, the other juvenile fishes studied here and terrestrial
vertebrates. First, the use of synchronous fin beats by boxfish occurred at
slow speeds and transitioned to alternating at higher speeds of 1.3-4.5
BL s-1 (Hove et al.,
2001). Second, the transition was not discrete, as observed here
or in other vertebrates. Instead, boxfish appear to combine the movement of
the two pectoral fins asymmetrically and smoothly transition between
synchronous and alternating patterns. Due to this gradual transition,
alternating and synchronous pectoral fin patterns do not fall into typical
definitions of gaits that specify a discontinuity in movement during
transition. Because of the unusual swimming pattern and the extensive use of
unpaired fins during boxfish locomotion, it is not surprising that these
animals may use the pectoral fins in uncommon coordination patterns.
Why a pectoral fin gait transition?
The presence of two distinct pectoral fin gaits raises questions of why
fish use multiple pectoral fin gaits and what determines the transition
between them. More broadly, the diverse representation of taxa that use
alternating fin/limb movement at slow speeds and transition to synchronous
coordination at higher speeds suggests there may be common constraints or
benefits of the use of these fin movement patterns. Based on previous studies,
we raise several possibilities for why fish may use multiple gait transitions.
First, above a given speed, synchronous fin beats may be more efficient than
alternating propulsive strokes. Studies on oxygen consumption of terrestrial
vertebrates, particularly horses, show that animals use the locomotor gait
that is most energy efficient for a particular speed range (e.g.
Hoyt and Taylor, 1981;
Griffin et al., 2004). Second,
particular gaits may be more or less stable at a given speed and fish may
transition between gaits to maintain stability
(Arreola and Westneat, 1996;
Hove et al., 2001). Energy
efficiency and stability of a gait at specific speeds are related to the
hydrodynamics of movement at those speeds, thus we might expect changes in
indicators of locomotor hydrodynamics such as reduced frequency or Reynolds
number at gait transitions. Third, there may be mechanical constraints on the
speed range in which a particular gait can operate
(Drucker and Jensen,
1996b).
Work on the median and paired fin (MPF) to body and caudal fin (BCF)
transition may provide insight into these issues. Examination of oxygen
consumption at the transition between slow MPF swimming and fast BCF swimming
(Korsmeyer et al., 2002) found
that transitioning to the faster gait did not decrease energy costs. In fact,
energy expenditure was greater for BCF swimming than was predicted for MPF
swimming at the same speed. Instead, they believe that the MPF to BCF
transition appears to be due to physical constraints, so that the switch to
axial propulsion occurs when the fin-based mode of locomotion has reached the
limit of thrust production (Korsmeyer et
al., 2002).
The transition from alternating to synchronous fin movement in the juvenile
fish we examined differs from the MPF to BCF transition in that the same
propulsors are used but in a different pattern of coordination. The most
comparable previous study of gait transitions in vertebrates is the switch
from alternating to synchronous limb movement in swimming frogs
(Nauwelaerts and Aerts, 2002).
At slow swimming speeds the frog Rana esculenta used alternating left
and right limb strokes for propulsion. At faster swimming speeds, frogs
switched to a simultaneous hindlimb movement while tucking the forelimbs
against the body. Nauwelaerts and Aerts calculated the work required for these
two gaits and found that the energy requirements for swimming out of phase are
lower than those for in-phase swimming. Thus, as with the MPF to BCF
transition in fishes, the gait transition is likely due to mechanical
constraints on thrust generation.
The difference in efficiency may be due to the relative steadiness of these
locomotor modes (Nauwelaerts and Aerts,
2002). Simultaneous limb movements result in greater accelerations
during a swim bout and thus greater loss of inertial energy at slow speeds
(Nauwelaerts and Aerts, 2002).
At higher swimming speeds, the simultaneous strokes of the hindlimbs may
generate jetting that does not occur at lower speeds and this overcomes the
energy disadvantage of using the in-phase locomotor mode at lower speeds.
Similarly, it has been suggested that the alternating fins of burrfish may
allow more steady thrust and efficient locomotion than synchronous fin beats
(Arreola and Westneat, 1996).
In our study of P. pavo, forward oscillation was considerably lower
for alternating pectoral fin locomotion than for synchronous, supporting the
steadiness hypothesis (Fig. 8).
However, we would expect that if alternating movements reduced these
oscillations at low speeds then the oscillations during synchronous fin
coordination would be highest immediately following the gait transition and
either decrease or remain level with increasing speed. This was not the case
and suggests that, if steadiness is a factor in the gait transition, it is not
the only one or, possibly, that gait transitions are coupled with fine fin
control to prevent fluctuations in thrust excursion after the transition.
Related to the issue of steadiness is that of stability. Reduced stability
has also been suggested as a disadvantage of synchronous pectoral fin beats of
MPF swimmers at low speeds for parrotfish
(Korsmeyer et al., 2002) and
wrasses (Walker and Westneat,
1997). These species would not swim steadily at speeds below
approximately 1.5 BL s-1 and 1.2 BL
s-1, respectively. Flow visualization studies find that fish
swimming steadily with synchronous fin beats at low speeds (0.5 and 1.0
BL s-1) generate unusually high laterally oriented forces
(Drucker and Lauder, 2000) and
suggest that orientation of force may provide increased stability at low
speeds.
There was no significant trend in yaw magnitude with swimming speed (Fig. 8), indicating that either yaw is not a factor in asynchronous fin propulsion or that the fishes are able to compensate for yaw with other fins. As the symmetrical in-phase movements of synchronous fin activity would not be expected to generate yaw, this control would be more important during asymmetric movements. Observation of dorsal, anal and caudal fin coordination during the two pectoral fin gaits may provide insight into this issue, and flow visualization studies to determine the forces generated by these gaits and through the pectoral fin gait transition would help to address some of these issues.
Both energy efficiency and steadiness/stability might be linked closely to changes in the hydrodynamic environment, in particular, reduced frequency and Reynolds number. Reduced frequency values were high at low speeds (Fig. 7) and, although they decreased with speed, did not shift below about 3.0, indicating that acceleration reaction forces dominate throughout the trials examined. Reynolds number ranged from about 200 up to about 2000 for the P. pavo swimming trials we analyzed (Table 2). We found no significant relationship between gait and Re across the individuals examined. Additional testing of fish larvae and juveniles across a broader size range and Re span may clarify the effect of hydrodynamic regime on fin gait.
Mechanical and physiological limits of fin muscle believed to explain the MPF to BCF transition in fishes may also explain the alternating to synchronous fin coordination gait transition. We predicted that amplitude and/or frequency of the fins during alternating strokes would peak immediately before the transition to synchronous fin coordination and be lower for synchronous strokes. While this was not the case in our data, the advance ratio, which reflects both amplitude and frequency (Fig. 7) exhibits the predicted trend. Advance ratio increases with swimming speed through both gaits with the highest ratios calculated for each speed being relatively similar. We suggest that P. pavo reaches a peak in advance ratio for alternating fin swimming then transitions to synchronous swimming, with which the same speed can be achieved with a lower advance ratio, possibly at lower energetic costs. Advance ratio of synchronous fin swimming increases with speed again until it reaches a peak, at which point the fish transitions to BCF swimming. Because fin length does not change across speeds, frequency and amplitude variability determine the denominator of the advance ratio. This suggests that it is a peak in combined amplitude and frequency that provides the upper speed limits of pectoral fin gait use for an individual animal.
Ontogenetic differences in gait use
It is interesting to consider why the gait transition pattern we observed
only seems to occur in young fish. None of the labriform swimmers previously
studied, including several from the same families that we examined (e.g.
Walker and Westneat, 1997;
Walker and Westneat, 2000),
have been shown to use alternating fin beats for steady swimming at adult life
history stages. Our original hypothesis was that the use of alternating fin
strokes was an effect of size and that at low Reynolds numbers or at low
reduced frequency, alternating fin strokes may be advantageous for steady
locomotion. Indeed, the Reynolds numbers for the fish we examined were low
relative to those of adults, suggesting that flow regime is a critical factor
in the fin gaits used by developing fishes. However, the limited range of our
analysis of Reynolds number and reduced frequency across juvenile swimming
emerged with no significant trends with locomotor gait transitions within
juveniles, indicating that other factors may be important.
Comparisons of the swimming speed ranges we recorded to those reported for
adults of other species suggest that younger fish can swim with paired fins at
a considerably greater range of length-specific body speeds than adults. In
fact, the transition between pectoral fin gaits in juveniles of P.
pavo and other species occurs at the same length-specific speed or a
higher speed than the MPF to BCF transition in adults (e.g.
Drucker and Jensen, 1996b;
Mussi et al., 2002). Juvenile
fishes appear to have a high performance capability for sustained swimming.
This has been shown previously for fish larvae
(Stobutzki and Bellwood, 1994)
and with small sized adults as compared to larger ones
(Mussi et al., 2002) and may
be due to changes in size and shape of body and fins or changes in locomotor
physiology.
In this study we have demonstrated that juvenile fishes from a number of species across several major clades exhibit an alternating to synchronous gait transition in pectoral locomotion. This dramatic phase shift in the pattern of propulsive appendages has not been documented widely in aquatic locomotion, but has been observed in a number of tetrapods. It is possible that the low reported occurrence of this transition in fishes is due to the fact that the locomotion of sub-adult fishes has been largely overlooked due to technical issues of acquiring, maintaining and recording these sensitive animals. We suggest that, through the dynamic transition from larval to adult, much locomotor complexity will be evident that is not observed in adults since, during this period, fish often move between environments and alter diets, change in shape, size and physiology, and face new demands of reproduction.
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Acknowledgments |
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Footnotes |
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Present address: The Centre for Marine Studies, University of Queensland,
Brisbane, QLD 4072, Australia 
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References |
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Alexander, R. McN. (1989). Optimization and
gaits in the locomotion of vertebrates. Physiol. Rev.
69,1199
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Alexander, R. McN. (2003). Principles of Animal Locomotion. Princeton: Princeton University Press.
Alexander, R. McN. and Jayes, A. S. (1983). A dynamic similarity hypothesis for the gaits of quadrupedal mammals. J. Zool. 201,135 -152.
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