Constraints on starting and stopping: behavior compensates for reduced pectoral fin area during braking of the bluegill sunfish Lepomis macrochirus
1 Section of Evolution and Ecology, University of California, One Shields
Avenue, Davis, CA 95616, USA
2 Department of Ecology and Evolutionary Biology, University of California,
Irvine, CA 92717, USA
3 Department of Biological Sciences, University of Cincinnati, PO Box
210006, Cincinnati, OH 45221-0006, USA
4 Department of Organismic and Evolutionary Biology, Harvard University,
Cambridge, MA 02138, USA
* Author for correspondence (e-mail: tehigham{at}ucdavis.edu)
Accepted 1 November 2005
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Summary |
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Key words: intermittent locomotion, kinematics, braking, deceleration, Centrarchidae, Lepomis macrochirus, pectoral fin, morphology, acceleration, swimming, stopping, starting, predation, feeding
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Introduction |
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The prominent role played by the pectoral fins for increasing drag during
stopping has long been recognized (Breder,
1926; Harris,
1937a
,b
;
Bainbridge, 1963
), and the size
and shape of pectoral fin morphology varies widely among different species of
ray-finned fishes (Drucker and Lauder,
2002
; Lauder and Drucker,
2004
; Thorsen and Westneat,
2005
; Wainwright et al.,
2002
; Westneat,
1996
). The drag of pectoral fins increases with both increased
area and increased fluid speed. Thus, accounting for both fin morphology and
kinematics is important for understanding variation in stopping performance.
However, no previous study has quantified the kinematics of the pectoral fins
during the stopping of ray-finned fishes.
We studied the bluegill sunfish Lepomis macrochirus, which has the
large pectoral fins and deep body that characterize maneuvering specialists.
Similar to many other predatory species of fish
(Webb, 1984;
Webb and Gerstner, 2000
), our
study species stops during prey capture by actively braking rather than
gliding (Drucker and Lauder,
2002
; Higham et al.,
2005
). This behavior facilitated quantifying the kinematics,
velocity and accelerations of ecologically relevant startstop episodes
over a standard distance. To gain further insights into roles of morphology
and behavior during braking, we experimentally reduced the area of the
pectoral fins. We addressed the following two primary questions. (1) What are
the magnitudes of starting and stopping accelerations, and are they similar
within a single predatory strike? (2) Does reduced pectoral fin area affect
stopping performance and attack speeds? We expected reduced fin area to
decrease the maximal deceleration or at least alter the movements and postures
used by fish during stopping. With a reduced ability to stop, fish also might
use slower attack speeds to avoid overshooting the location of prey.
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Materials and methods |
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Experimental protocol
All tests were performed at water temperatures of 1820°C. The
test arena was a 114 liter tank divided into three sections, which facilitated
obtaining startstop episodes with a standardized predatorprey
distance (Fig. 2). We used a
suture line with a small weight to suspend the prey item (earthworm,
Lumbricus) 10 cm past the second divider, 40 cm from the trap door
holding the fish in the starting compartment and centered in the opening of
the second partition (Fig. 2).
The openings in the two opaque partitions were 14 cmx14 cm. The
investigator hid behind an opaque partition and raised the trap door
via a string to prevent the fish from having extraneous visual
stimuli.
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We tested each individual both with unaltered pectoral fins and when the fins had been trimmed to reduce their area. Following the trials with intact fins, we anesthetized the fish using MS-222 and cut the fin nearly parallel to the distal edge all the way from the most ventral to the most dorsal fin ray. The average (N=4 individuals; N=8 fins) area of an intact pectoral fin (5.01±0.3 cm2) was reduced to approximately 35% (1.76±0.1 cm2) of its original size. After 1 night of recovery, we tested the individuals with partially ablated fins.
The fish were not fed for 1 week prior to the day of testing, and the time between the tests conducted on a single individual with intact and partially ablated fins was 1 week. The time between successive trials of a single individual within a single day was 10 min. With only one exception (one individual tested twice, 1 week apart, after partial ablation), fewer than 10 trials per individual per treatment within a single day were sufficient to obtain 4 or 5 sequences conforming to the criteria below as suitable for detailed kinematic analysis. Preliminary analyses did not reveal any significant correlations between any measures of velocity or acceleration with trial number of an individual within a day. Furthermore, the within-day trial numbers for the subset of 4 or 5 trials used for detailed analysis differed among different individuals. Consequently, our analyses of variance did not include a factor encoding trial number since we were using multiple trials within an individual and day primarily to increase our statistical power for detecting the effects of partial fin ablation, and we had no evidence of any systematic variation in motivation associated with trial number within a day.
Kinematic measurements
For our frame-by-frame analysis of our videotape, we chose only those
trials where the trajectory of the fish was straight, parallel to the long
axis of the tank, beginning from a standstill (velocity=0), lacking pauses
(velocity=0), and coming to a complete stop at the end. For each combination
of individual and fin reduction we analyzed between 4 and 5 trials (total of
37 trials) that met these criteria.
From play-back of the videotapes we determined the durations (±10 ms) of four broad categories of locomotion to provide an overview of the behaviors used by the fish. Propulsion only (P) indicated that all of the movements of axial structures and the pectoral fins appeared to be contributing to forward thrust. Glide (G) indicated forward movement of the fish without any movement or postures that would appear to contribute either to thrust or to actively decelerating the fish. Braking only (B) indicated that any movements or postures of the axial structures or pectoral fins were being used only to decelerate the fish. Propulsion plus braking (PB) indicated that some movements were contributing to forward thrust, while others were simultaneously retarding forward progression. For example, during PB the pectoral fins were often held bilaterally slightly away from the body (creating drag) while the axial structures, body and caudal fins simultaneously undulated in a manner (posteriorly propagated wave) so as to contribute to the forward speed of the fish. We converted all event durations to percentages of the total time from start to stop to facilitate pooling data from different sequences.
We digitized the two-dimensional coordinates of up to 17 anatomical locations, including the left and right paired fins (depending on visibility) in ventral view (Fig. 3). To provide a minimum of 65 time intervals for each of the attack sequences of variable duration, we digitized points at 10 or 20 ms intervals from when the fish initiated movement until the fish came to a complete stop and consumed the food item.
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For each frame, we calculated the forward displacement of the fish using
the average of the x coordinates of the anterior edges of the left
and right eyes (Fig. 3). We
then used the Quicksand algorithm of Walker
(1998) to smooth the
x-displacement data with a quintic spline and used the first and
second derivatives to determine velocities and accelerations,
respectively.
Three variables described attributes of entire movement bouts, including total duration and total forward displacement. We also divided the total displacement per movement by total duration of movement to calculate average forward velocity (Vavg).
From the ventral view coordinates we calculated four fin angles during the
final portion of each feeding event, when at least some portion of the
pectoral fins was visible (Fig.
3). The pectoral and pelvic fin angles were each a two-dimensional
angle calculated between lines from the anterior margin of the base of the fin
to the distal tip of the fin and a point on the body anterior to the fin
(Fig. 3). We also determined
the angles between the x-axis and lines from the base to the most
lateral point of the median fins and to the most lateral point of the trailing
edge of the caudal fin (Fig.
3). The median fins (dorsal and anal fin) of sunfish are located
above each other, and hence often overlapped in ventral view, and are often
moved synchronously to the same side of the fish during braking
(Breder, 1926;
Drucker and Lauder, 2002
). Thus
we refer to `median fin' as the greatest excursion of either of these two
fins. To facilitate pooling values indicating bending to either the left or
the right in different trials, we used the absolute value of the median and
caudal fin angles in the statistical analysis.
We calculated the distance between the anterior tip of the lower jaw and a
reference line connecting the anterior margins of the eyes
(Fig. 3). Maximum jaw
protrusion (MJP) occurred when this distance was maximal. MJP of bluegill
sunfish corresponds closely with the time of prey capture
(Day et al., 2005;
Higham et al., 2005
).
We calculated six variables describing the timing of kinematic events as percentages of the total duration of movement (Table 1). The time of the initial Vmax was defined as the time of the earliest local maximum velocity. The time of Vmax was the time at which the greatest speed was observed for the entire movement (global maximum). All of the remaining values of maximal magnitudes (MJP, and angles of pectoral, pelvic, median and caudal fins) were determined over the time interval from when the tips of the pectoral fins first became clearly visible after Vmax during the final rapid deceleration until the fish came to a complete stop.
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Statistical analyses
We used SYSTAT version 10 for all statistical analyses, and
P<0.05 was the criterion for statistical significance. To
determine the effects of reducing the area of the pectoral fins, we performed
two-way analyses of variance (ANOVAs) with fin area (fixed and crossed factor
with 2 levels) and individual (random and crossed factor with 4 levels) as the
independent categorical variables and values of kinematic variables as the
dependent variables. In order to properly account for our replication of
observations within individuals, the denominator in the F-test for
the main effect of the fin area reduction effect was the two-way interaction
term between fin area and individual (Zar,
1996).
Results are presented as means ± S.E.M., unless stated otherwise.
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Results |
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Rather than accelerating continuously up to a maximal forward speed, every sequence had an early local maximum in forward velocity that preceded the global maximum velocity by approximately 0.2 s (Fig. 4B,F). The maximum accelerations uniformly occurred prior to the first local maximum of forward velocity. Fish always used caudal fin undulation during the initial episode of propulsion, but use of the pectoral fins over the same time interval was variable. In less than one-third (9 of 37) of the sequences, the pectoral fins remained against the body until after Vmax was attained. More commonly (28 of 37) the fish simultaneously used caudal undulations with propulsive movements of the pectoral fins, which could be either bilateral or alternating and unilateral (Fig. 5). Approximately one-third (13 of 37) of the trials had more than one local maximum in forward velocity before Vmax was obtained. Thus, modulation of speed from the start until Vmax resulted mainly from modulating propulsive forces rather than employing braking behaviors.
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When fish performed gliding after Vmax, the duration of the glide was usually so short that the decrease in forward velocity was modest (Fig. 6A). When the pectoral fins remained slightly protracted as the axial structures continued to undulate (PB) after Vmax, the decreases in forward velocity were also usually small (Fig. 6B).
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Contrary to our expectation, reduction of pectoral fin area did not significantly affect any of the major descriptors of modulating velocity including maximum forward velocity (Vmax), maximum acceleration, and maximum deceleration (Table 1). Furthermore, none of the times of landmark kinematic events, such as maximum fin angles or maximum velocities, were affected significantly by reduction of pectoral fin area (Table 1). Vmax occurred slightly before the halfway point (grand mean=45.9±2.2%) of the total movement duration, and the average velocity profiles for both intact fins and trimmed fins were nearly symmetric about the midpoint (Fig. 7).
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Discussion |
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Stopping vs starting
Unlike starting, where fluid drag is an impediment, fluid resistance
facilitates stopping. Indeed, the forces retarding forward progression were
sufficiently large that we commonly observed decreases in forward velocity
both before and after the global maximum in velocity within a sequence as fish
continually undulated their caudal fins with variable intensity. Before
Vmax, decreases in speed resulted only from variable
propulsive effort, but after Vmax all mechanisms for
decreasing speed occurred. For fish with intact and reduced fin areas, a
sizable period after Vmax [15%=average cessation of
initial P (61%)average time of Vmax (46%)] often
involved only decreased propulsive effort. Thereafter, some fish glided or
combined propulsion with braking before performing only braking behaviors, and
these differences in behavior contributed to considerable variation in
accelerations. However, the greatest magnitude acceleration and deceleration
were consistently near the beginning and end of the startstop episode,
respectively.
Disparities in starting and stopping capacities are interesting because of the manner in which they can theoretically constrain the tactics available for modulating speed within a confined space (Fig. 1). The paucity of data on both starting and stopping accelerations leaves open the question of whether or not these capacities are usually matched within individual fish. However, several indirect lines of evidence suggest that many fish have a greater capacity to start than to stop.
The amount of axial vs appendicular musculature and the manner in
which axial structures are used suggest more power can be generated during
starting than in stopping. The mass of axial muscles of most fish species,
which commonly exceeds 40% body mass (Bone,
1978), is huge compared to that of the pectoral fins, which may be
less than 1% body mass (Geerlink,
1983
). During the rapid starting accelerations of escapes, large
amounts of lateral axial bending occur along nearly the entire length of the
fish, as all the red and white musculature is activated along one side and
then along the contralateral side (Jayne
and Lauder, 1993
). We never observed a substantial amount of
lateral bending in the anterior region of bluegill sunfish braking in this
study (Fig. 5), nor during our
previous studies of escape locomotion in this species. Figures of other
species of fish stopping also show little axial bending anteriorly
(Geerlink, 1987
). Thus, many
fish probably have a greater muscle mass that is useful to recruit during
starting compared to stopping.
The limited empirical data for accelerations during starting are much
greater than those for stopping. For diverse species of fishes, maximal
starting accelerations during escape responses determined from kinematic
analysis range from 4050 m s2 (reviewed in
Blake, 2004), whereas the
scanty data available for stopping accelerations are all less than 9 m
s2 (Table 3).
The values of maximum acceleration that we observed for sunfish are low
compared to values in the literature for escape responses of similar size
fish, and by definition all but one of our multiple observations per
individual per experimental treatment were submaximal. Furthermore, the
variability in both stopping and starting accelerations that we observed among
trials within an individual and experimental treatment was high. Thus, most of
the rapid initial accelerations and final decelerations in our study appear
much less than physiological maximums, which could be attained either in
different experimental conditions or in our particular experimental
conditions.
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Although many accelerations that we observed are probably less than those
sunfish can attain physiologically, maximal accelerations and decelerations
within a sequence had some trends that paralleled expectations for a greater
ability to accelerate than decelerate. For example, our data had a mean value
of maximal acceleration nearly 50% greater than that of maximal deceleration
within a sequence (Table 1).
Maximal acceleration exceeded maximal deceleration in most sequences (17 of 19
intact trials; 10 of 18 reduced area trials)
(Fig. 9). Furthermore, with
increased maximal acceleration the probability of a lesser corresponding
maximal deceleration increased (Fig.
9). An unresolved but interesting issue is whether speeds closer
to a physiological maximum would exaggerate apparent differences in
acceleration and braking capacities. However, the sunfish studied here still
showed relatively high braking decelerations relative to literature values
(Table 3). Diverse stimuli
reliably elicit escape responses, which involve a specialized neural circuit
and a high degree of stereotypy (Eaton et
al., 2001), but predictably eliciting a volitional stop poses a
significant technical challenge. If one could establish the maximal
accelerating and stopping capacities, then one could determine whether the
acceleration and deceleration within a single startstop episode were
similar proportions of different maximal capacities.
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The most conspicuous mechanisms for compensating for the reduced pectoral
fin area in our study were greater displacement and faster protraction speeds
of the pectoral fins (Table 2).
Previous work on the stopping of fishes has focused on how a pectoral fin
angle of 90° relative to the body is likely to maximize drag and hence set
an upper limit to braking performance. When the sunfish in our study had
intact fins, they rarely attained angles of 90°. Similarly, other fish
often do not attain pectoral fins angles of 90° during braking, and
Geerlink (1987) suggested that
this may be a result of having pectoral fin abductor muscles that are too
small to generate sufficient force to hold a 90° angle for the pectoral
fins over a wide range of swimming speeds. Since the force of the fluid acting
on the fin is proportional to its area, one reason for the greater pectoral
fin angles we observed in fish with reduced fin area might be that force
production of the abductor muscles is no longer a limiting factor to fin
displacement.
Even if the fin abductors were sufficiently strong to position the base of
the fin perpendicular to the body, the mechanical stiffness of pectoral fin
rays may not be sufficient to maintain a perpendicular position along the
entire length of the fin. Long-axis curvature of the pectoral fins was
conspicuous during braking for the fish in our study with intact fins, whereas
little long-axis bending was apparent for the shortened pectoral fins. Three
factors suggest that much of the decrease in bending of the shortened pectoral
fins results primarily from the properties of the fin rays rather than
differences in the external loads. First, for two cylinders with identical
diameter made of the same material, less force is required to bend the longer
rod a given amount (Wainwright et al.,
1976). Second, the diameter of the rays decreases from proximal to
distal. Finally, the elastic modulus of the fin rays decreases from proximal
to distal (G. V. Lauder, unpublished data; also see
Lauder, 2005
).
Although the partially ablated pectoral fins of our sunfish transiently had angles of 90°, their ultimate position was well beyond this angle and resulted in a sub-maximal frontal area. The substantial amount of forward movement of the pectoral fins of both the intact and reduced area treatments in the final stages of braking also suggests that the generation of reverse thrust contributes to braking forces in addition to static postures, which increase frontal area and drag. The behavior of increasing protraction speed of partially ablated fins is consistent with the expectation for a compensatory mechanism to maintain braking performance because thrust decreases with decreased surface area and increases with increased fluid speed.
In addition to drag, a swimming animal will experience the acceleration
reaction, which resists changes in velocity and thus inhibits deceleration
(Daniel, 1984). The
acceleration reaction is dependent on the shape, size and acceleration of a
body, and thus abducted pectoral fins will increase drag but also increase the
acceleration reaction. By protracting their fins to a greater extent, and thus
achieving a sub-maximal frontal area, the sunfish with reduced pectoral fins
will actually reduce the acceleration reaction and thereby increase braking
performance.
Additional compensation for reduced pectoral fin area was the trend for
fish in our study to have greater excursions of the median and caudal fins
even though these were not statistically significant. A key feature of
locomotor functional design in fishes is the extent to which different
structures have redundant function or can function in a decoupled fashion from
each other (Blake, 2004;
Lauder and Drucker, 2004
;
Webb, 2004
). The redundancy
for braking of median and paired fins was clearly one factor that can
ameliorate the anticipated negative effects of reduced pectoral fin area on
braking performance. Furthermore, sunfish displayed a remarkable capacity to
decouple function of the paired fins and axial structures as they
simultaneously held the pectoral fins in a static braking posture while the
axial structures continued to have propulsive movements. However, we did not
observe any movement of the median fins that suggested they could be used as
braking structures while the caudal fin was generating propulsive forces (as
indicated by a posterior propagation of maximum lateral displacement and
bending).
Although the combined function of the median structures and paired fins in
braking is widely recognized (Breder,
1926; Harris,
1937a
; Jayne et al.,
1996
; Webb and Fairchild,
2001
), the relative contributions of each are not well understood.
Geerlink (1987
) estimated that
the pectoral fins and the body of the fish he studied could contribute no more
than 30% and 15%, respectively, of the total braking force, but he did not
account for either curvature of the median and caudal fins or generation of
reverse thrust by the pectoral fins. Drucker and Lauder
(2003
) found that for a trout
braking from a slow swimming speed (0.5 lengths s1), the
braking force of the pectoral fins was nearly twice that of the dorsal fin,
but the contribution of whole body drag to braking was not determined. The
sunfish in our study have larger pectoral fins than those of both trout and
the species studied by Geerlink
(1987
). Consequently, the
relative contributions of different structures to braking at similar speed
probably vary widely among species. Furthermore, the role of different
structures during braking for a single species probably varies with swimming
speed. For example, we (B. C. Jayne and G. V. Lauder, unpublished) have
observed braking of sunfish after eliciting a rapid escape response
(Jayne and Lauder, 1993
), and
high forward velocity of the fish appeared to bend the tips of the pectoral
fins near the body, which had an extreme displacement of the caudal fin that
probably indicated its increased importance for braking. Consequently, if the
axial structures are better than the pectoral fins at resisting passive
bending that occurs as a result of the resistive forces of the water, then the
axial structures may assume greater importance for braking as speed
increases.
Ecological relevance of stopping
Feeding and avoidance of collisions are two ecological contexts for which
we consider the benefits of an enhanced ability to stop. A related issue is
whether or not the ecological context in which a behavior is performed affects
the extent to which a maximal capacity is used (`ecological performance' of
Irschick and Garland,
2001).
Braking potentially has two key benefits for aquatic suction feeding.
First, generating suction can pull the predator forward and increase the
chances of colliding with the substrate
(Muller et al., 1982), unless
the predator actively brakes to avoid this. Second, swimming fast during
feeding could decrease the fluid speeds generated by suction due to the
hydrodynamic interactions between swimming (ram) and mouth expansion
(Higham et al., 2005
). Braking
immediately before prey capture could alleviate this negative interaction and
thus preserve suction performance. The extent to which fish stop completely
when feeding varies considerably among different species as they use varying
combinations of swimming towards prey (ram) and suction to move the prey
towards the fish (Norton and Brainerd,
1993
; Wainwright et al.,
2001
; Higham et al.,
2005
). Experimentally exploiting these rich sources of behavioral
and morphological variation among fishes in integrated studies of feeding and
locomotion holds great promise for gaining further insights into how animals
modulate speed.
Braking seems likely to be important for preventing collisions for a wide variety of predators besides fish that attack prey close by or attached to solid objects. Avoiding collisions could have consequences for both the attack trajectories of predators and the anti-predator tactics of prey. For example, prey might obtain some protection from predators simply by being very close to a solid object rather than hiding behind it. Predators could compensate for this prey tactic or for their poor braking ability by using an attack trajectory oblique rather than normal to the surface behind the prey in order to increase the distance between the prey and the background along the attack trajectory. A general understanding of the importance of braking behavior could be enhanced by future comparisons of limbed and limbless animals. Limbless animals such as fish risk cranial injury if they collide with an object while traveling forward. Limbed animals theoretically could use their forelimbs to absorb the shock collision for some range of forward speeds, but the extent to which this strategy is used or facilitates prey capture is unknown.
An increasing number of studies of locomotor performance are finding that
animals often move with less than their maximal capacity, even when evading a
predator or capturing prey (Jayne and
Ellis, 1998; reviewed in
Irschick and Garland, 2001
;
Bolnick and Ferry-Graham,
2002
). The maximal speeds that we observed during the 40 cm
predatory attacks of sunfish were substantially lower than the speeds attained
by species under different conditions
(Jayne and Lauder, 1993
), but
starting and stopping ability seem unlikely to be limiting
Vmax. Some of the following alternatives regarding
energetic and environmental influences may help to explain why the values we
observed for attack speeds and accelerations are so low.
Modeling by Bolnick and Ferry-Graham
(2002) suggests that energetic
considerations may cause the effort expended by a predator to capture prey to
vary with the potential benefit of the prey rather than being an all or none
maximal effort. The prey items we used were not elusive, and the elusiveness
of prey affects the attack speeds of some fish
(Nemeth, 1997
). If attack
speed is not significantly correlated with predatory success, then swimming
quickly would have no benefit, but it would incur an extra energetic cost
because of how drag forces increase with swimming speed. Perhaps processing
and integrating sensory information regarding prey location constrains speed
and acceleration to a greater extent than locomotor capacity. Moving
submaximally during a predatory attack might also facilitate changing the
attack trajectory in response to prey movements and thus maintain strike
accuracy (Higham et al.,
2005
). If predatory attack behaviors evolved in cluttered habitats
with such short unobstructed distances that physiologically maximum capacities
could not be used, then animals may not have sufficient behavioral plasticity
to increase their attack speeds when placed in less cluttered surroundings.
Further experimental manipulations of prey type, predatorprey
distances, and distance from the prey to background object could provide many
additional insights into these issues regarding seemingly low attack
speeds.
Although the ecological relevance and pervasiveness of intermittent
locomotion of animals have been increasingly recognized
(Higham et al., 2001;
Kramer and McLaughlin, 2001
;
Weinstein, 2001
), most work on
intermittent locomotion has concentrated on how the pauses affect recovery,
rather than on the functional basis of stopping, which results in a pause.
Despite the current lack of comparative data on modulating velocity between a
start and stop, systems such as the predatory attacks of suction-feeding
fishes and fiddler crabs returning to their home burrows
(Layne et al., 2003
) may prove
to be useful model systems for future investigation of starts and stops in
which experimenters can manipulate distance and have animals come to a stop at
a predictable location.
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Acknowledgments |
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