Strikes and startles of northern pike (Esox lucius): a comparison of muscle activity and kinematics between S-start behaviors
1 Department of Organismal Biology and Anatomy, University of Chicago,
Chicago, IL 60637, USA
2 Committee on Neurobiology, University of Chicago, Chicago, IL 60637,
USA
3 Committee on Computational Neurobiology, University of Chicago, Chicago,
IL 60637, USA
* Author for correspondence (e-mail: mhale{at}uchicago.edu)
Accepted 7 November 2003
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Summary |
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Key words: Esox lucius, pike, strike, startle, prey capture, fast-start, S-start
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Introduction |
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The focal fast-start behavior for research has been the C-start escape
response. C-start behavior generally includes a C-shaped bend away from the
stimulus direction (stage 1) followed by a propulsive tail stroke (stage 2)
and often subsequent swimming (stage 3)
(Weihs, 1973). C-starts have
been examined in a wide range of species (reviewed by
Domenici and Blake, 1997
),
through ontogeny (e.g. Taylor and McPhail,
1985
; Fuiman,
1994
; Hale, 1996
,
1999
) and within ecological
(O'Steen et al., 2002
) and
evolutionary (e.g. Zottoli,
1978
; Hale et al.,
2002
; O'Steen et al.,
2002
) contexts. Because C-start escape behavior is controlled by a
small population of reticulospinal neurons and because of the simplicity and
accessibility of its neural circuits (e.g.
Faber et al., 1989
;
Fetcho, 1991
;
Zottoli and Faber, 2000
;
Eaton et al., 2001
), it has
become a model system for examining the neural control of movement.
While the C-start has been studied from diverse perspectives, a second type
of fast-start behavior called the S-start
(Hoogland et al., 1956;
Webb, 1976
) has been a focus
of research on muscle dynamics (Frith and
Blake, 1995
; Johnston et al.,
1995
; Spierts and Van Leeuwen,
1999
) and kinematics (Harper and Blake,
1990
,
1991
) but has not been studied
across a wide range of taxa nor has its neural basis been established.
However, the fact that the behavior has been identified in taxa as
phylogenetically distant and ecologically distinct as pike (i.e.
Hoogland et al., 1956
;
Webb and Skadsen, 1980
) and
carp (Spierts and Van Leeuwen,
1999
) suggests the behavior may be used by a broad array of
species. S-start behavior has been shown to occur in both feeding strikes and
escape startles (reviewed by Domenici and
Blake, 1997
). During the S-start startle response, the fish forms
an `S' shape with a bend in the tail contralateral to the major rostral body
bend. Recent electromyography data on S-start escape behavior in the Esocidae
species muskellunge (Esox masquinongy) have demonstrated that the
S-start startle is generated through a qualitatively different pattern of
muscle activity than the C-start (Hale,
2002
). This result suggests that the S-start is an independent
type of startle response from the C-start and is not generated by the same
neural circuit.
The S-start type of fast-start behavior has been identified as functioning
in feeding strikes in several esocid species
(Webb and Skadsen, 1980;
Rand and Lauder, 1981
;
Harper and Blake, 1991
). Prior
to the propulsive movement of the strike, the fish's body takes on an S shape
with a major bend to one side rostrally and to the opposite side caudally. The
S-start of the strike has been subdivided into two categories based on the
length of time the S-bend is maintained
(Webb and Skadsen, 1980
).
During type A strikes, the strike begins with the fish in a straight position
and the S-bend occurs as part of the strike. By contrast, during the type B
strike, the strike is initiated from an S-shaped position. Additional
distinctions in S-start strikes have been made according to the acceleration
profiles of the movement and the number of tail strokes following the S-bend
prior to prey capture (Harper and Blake,
1991
).
The role of the S-start fast-start in strike behavior is unique. While
C-starts have been identified in post-feeding turns, in that context they
probably function as a defensive maneuver away from the water surface
(Canfield and Rose, 1993) where
prey is available but the fish are also more vulnerable to predators. By
contrast, during S-start strikes, the S-bend occurs prior to prey capture and
thus is an integral part of the prey capture event.
The presence of two independent roles of the S-start attack and
escape raises questions about the degree of shared versus
independent neural control of these behaviors. We build upon previous studies
on S-start kinematics (Webb and Skadsen,
1980; Rand and Lauder,
1981
; Harper and Blake,
1991
) by examining muscle activity patterns along with kinematics
of S-start strike and startle in order to address the hypothesis that the
S-start strikes and startles are generated by the same patterns of muscle
activity and to examine how a simple movement pattern is controlled in very
different behavioral contexts. Our first objective was to characterize the
kinematics and muscle activity pattern of the S-start feeding strike in the
northern pike (Esox lucius). The axial muscle activity of S-start
feeding strikes had not been examined previously in any species. Our second
objective was to compare the movement and motor pattern of the S-start strike
with that of the S-start startle response of the same species. For both
strikes and startles, we recorded high-speed video and electromyograms from
epaxial muscle in three positions on each side of the body and from the jaw
adductor muscle on one side of the body to examine the coordination of S-start
axial muscle activity and the relationship between jaw and axial activity.
Materials and methods
Northern pike (Esox lucius L. 1758) were obtained from the Jake
Wolf Fish Hatchery, Illinois Department of Natural Resources, IL, USA. Four
fish ranging from 22.8 cm to 24.5 cm total length (mean ±
S.D., 23.7±0.8 cm) and from 20.1 cm to 22.3 cm standard
length (21.2±1.0 cm) were examined. The fish were maintained at the
Field Museum of Natural History, Chicago, IL, USA in tanks at 20°C.
Experiments were conducted at the Field Museum of Natural History and at the
University of Chicago with IACUC approval from both institutions. While in the
laboratory, fish were fed minnows on alternating days. Fish were not fed for
24 h prior to an experiment.
We chose to work on the northern pike because this species and other
members of the Esocidae are considered acceleration specialists and have been
models for strike and startle behaviors. Comparative work on kinematics of
strikes and startles is available for many esocid species (e.g.
Webb, 1976;
Webb and Skadsen, 1980
;
Rand and Lauder, 1981
; Harper
and Blake, 1990
,
1991
;
Frith and Blake, 1995
;
New et al., 2001
;
Hale, 2002
).
Kinematics
Kinematics of strike and startle responses were recorded from ventral view
in a 60 cmx60 cm tank. Startle responses were elicited by touching or
pinching the tail with metal forceps. Fish were near the center of the tank
when startles were elicited. As angular movements during the startle are in
part determined by stimulus direction
(Eaton and Emberley, 1991;
Domenici and Blake, 1993
), we
used a caudal stimulus to minimize the difference in initial movement angles
of strikes and startles and so as not to initiate C-start behavior, which
tends to be generated by more rostral stimuli. Strike responses were obtained
by introducing a free-swimming prey minnow (Pimephales promelas) into
the filming tank. In choosing strikes to analyze, we only examined strikes in
which the prey fish was not next to the tank wall and there was no contact
between the pike and the walls of the tank during the movements analyzed. The
minimum possible distance between the pike and the wall of the tank at the
initiation of the response was approximately 9 cm. This is a conservative
estimate as the tank wall was not always visible in the field of view and so
the distance to the edge of the field of view was used instead. The maximum
distance between the pike and prey upon initiation of the strike was 6 cm.
Fast-starts were recorded at 250 frames s1 with a Redlake
PCI-1000S digital high-speed video camera. Images were viewed and digitized
with NIH Image 1.62. We examined the initial non-propulsive movements and the
first propulsive tail stroke for both strikes and startles. Kinematic
parameters were determined from midline points reconstructed from digitized
outlines of the fish as described by Hale
(2002) using a midline
analysis program designed by Jayne and Lauder
(1995
). The fish images were
digitized along the axis from the tip of the snout to the caudal peduncle. We
did not digitize the caudal fin because it was not always clear in the images
and our primary concern was with the muscular part of the tail. We examined
movement at 5% intervals along the body and at points corresponding to the
longitudinal positions of the axial electrodes and the center of mass, which
was determined for the longitudinal axis of the fish as described by Westneat
et al. (1998
;
Fig. 1;
Table 1). Velocity and
acceleration were calculated with QuickSAND software written by J. A. Walker
(Walker, 1998
). Angles of head
movement during stages 1 and 2 were measured with NIH Image version 1.62.
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Electromyography
Electromyograms (EMGs) were recorded with fine-wire electrodes implanted in
epaxial muscle. Electrodes were made from 0.05 mm-diameter double-stranded,
insulated, stainless steel wire from the California Fine Wire Company as
described by Hale (2002). Fish
were anesthetized with 3-aminobenzoic acid ethyl ester (MS222) in water. Seven
electrodes were used, three on each side of the body in the epaxial white
muscle and a seventh in the jaw adductor on the left side of the body at
approximately 0.51 cm in depth. Longitudinal positions
(Fig. 1;
Table 1) were chosen so that
the EMGs would describe the distribution of muscle activity along the length
of the body. We assumed that the jaw muscles were active bilaterally and that,
at least for the broad-scale analysis of cranial activity in this research,
the left jaw muscle reflected activity patterns on the right. After
experiments, the study animals were euthanised with MS222. Measurements of
total and standard length and the longitudinal positions of the center of mass
and electrodes were recorded (Table
1).
EMGs were amplified with Grass P 511 amplifiers (gain 5000 or 10 000). Data were stored directly to a computer at a sample rate of 5000 points s1 channel1 using National Instruments' analog-to-digital acquisition system and custom LabView Virtual Instrument (VI) software (National Instruments Corporation, Austin, TX, USA). An additional channel collected a square wave signal that was simultaneously recorded by the video system onto the kinematic sequences to synchronize EMGs and behavior. The relative timing of EMG activity to movement as well as the EMG amplitudes and durations were analyzed with LabView software using custom VIs written by M. W. Westneat. In order to align the responses, the first activity of each response is set to zero and the onset and offset of subsequent EMG bursts are determined as time from that zero. In the case of strikes, which always involved activity in caudal muscle first, this results in no standard error for the onset of the first burst of caudal activity as caudal onset was always set to zero.
Statistics
Trials of S-start escape responses and strikes were measured for each of
four fish. In most cases, three trials of each behavior were analyzed;
however, for one fish only two strikes were analyzed and for another only two
S-starts were analyzed. In order to combine trials of tail bending to the
right and left, the data were standardized to the direction of head movement.
We quantified variation between behaviors and among individuals using analysis
of variance (ANOVA) with repeated measures in the program JMP (SAS Institute)
to test for specific differences in kinematics and EMG variables. None of the
variables showed significant inter-individual effects.
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Results |
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The S-start startle involved generally similar kinematics stages. The movement pattern of the startle is characterized by an initial S-shaped bend with the tail bending in the opposite direction to the major body bend (Fig. 2J). The S-bend is followed by movement into a tight caudal L-bend (Fig. 2K). During stage 2 of the startle, a wave of bending is propagated from rostral to caudal along the entire length of the body (Fig. 2LN).
One difference between strike and startle behaviors is the angle of head movement during stage 1 of the response (Fig. 3). The angle of head movement from initiation of the response through the S-bend was lower for the strike response than for the startle [12.7±5.2° (mean ± S.E.M..) compared with 45.7±3.9°, respectively; P<0.0001]. Similarly, change in head angle was significantly lower for the strike from the end of the S-bend to the L-bend at the end of stage 1 (5.0±2.2° compared with 12.8±1.5°; P<0.01). There was no significant difference in the angular head movement between strikes and startles during stage 2 of the response (4.0±2.2° compared with 7.0±1.9°; P=0.31).
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Total duration of stages 1 and 2 was significantly greater (P<0.05) for the strike (100.3±10.3 ms) than for the startle (70.9±6.2 ms) (Fig. 4). The difference in total duration was reflective of a longer duration stage 1 during the strike behavior (72.2±9.7 ms for the strike compared with 42.7±3.1 ms for the startle). Stage 1 duration was highly variable among strikes as reflected in the high standard error (9.7 ms compared with 3.1 ms for the startle). Comparison of strike and startle within stage 1 shows that the difference in duration in stage 1 is a result of a longer initial S-bend for strike behaviors (55.5±9.1 ms for the strike compared with 23.7±2.3 ms for the startle; P<0.005). There was no significant difference (P=0.219) in the duration of the L-bend between the strike (14.7±2.0 ms) and the startle (19.0±2.2 ms) or in the duration of stage 2 of strikes (36.5±8.2 ms) and startles (29.5±4.1 ms; P=0.064).
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The peak linear velocity of the center of mass in stage 2 (Fig. 5A) was not significantly different between strikes and startles (P=0.524). Strikes had a mean velocity of 1.69±0.20 m s1 while startles averaged 1.75±0.24 m s1. Similarly, the peak linear acceleration of the center of mass in stage 2 (Fig. 5B) did not differ among fast-start types (P=0.383). The peak acceleration during the strike was 54.61±10.97 m s2 and during the startle was 80.20±13.84 m s2.
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Electromyography
S-start strikes and startles result from qualitatively different muscle
activity patterns. Fig. 6
illustrates an example of strike and startle EMG responses. While the pattern
of muscle activity for the startle was highly stereotyped, strike responses
were considerably more variable, particularly in the onset of muscle activity.
The strike example shown (Fig.
6A) was chosen because it illustrates the main features of the
response summarized in Fig. 7
and statistically below.
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The most obvious difference between strikes and startles is the relationship of the onset of jaw adduction to the onset of axial muscle activity, which was significantly delayed for the strike relative to the startle (P<0.0001). During the startle response, jaw adductor activity occurred at the initiation of axial muscle activity, on average within 1 ms of axial muscle (0.64±0.39 ms). During the strike, the onset of jaw adductor muscle activity was delayed relative to the first onset of axial muscle activity recorded, occurring on average 43.05±6.04 ms after axial muscle onset. The onset times of adductor muscle activity had non-overlapping distributions when compared between strike and startle trials (Fig. 8). There was no significant difference in the duration of jaw adductor muscle activity (97.1±20.43 ms for the startle and 118.7±10.8 ms for the strike; P=0.22), which was highly variable among trials. Mean amplitudes of the jaw adductor activity were not significantly different between strikes (0.356±0.064 mV) and startles (0.328±0.09 mV; P=0.81).
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The pattern of axial muscle activity also differs between fast-start types. The duration of the initial caudal muscle activity is considerably longer for strikes than startles (26.9±2.2 ms versus 14.4±2.2 ms, respectively; P<0.001) and of lower mean amplitude (0.208±0.07 mV versus 0.596±0.074 mV, respectively; P<0.001). The onset of the initial burst of rostral activity was delayed relative to initial caudal activity of the strike (Fig. 7). The onset of rostral activity occurred, on average, 19.1±5.46 ms after initial caudal activity for the strike; during the startle, initial rostral activity occurred 0.71±0.28 ms following the first burst of activity in either jaw or more caudal axial muscle. The durations of rostral activity differed significantly between behaviors, being longer for the strike than for the startle (61.0±9.9 ms versus 25.5±5.3 ms, respectively; P<0.02). The mean amplitude of the response was not significantly different: 0.252±0.054 mV (strike) and 0.37±0.112 mV (startle) (P=0.08). Similar to the rostral activity, onset of midbody activity for the strike occurred an average of 15.0±4.1 ms after the onset of initial activity. This was significantly after the corresponding activity for the startle, which occurred 1.0±0.35 ms after the onset of initial activity (P<0.002). The high variability in the onset times of both rostral and midbody ipsilateral activity during the strike is evident in high standard error values, both over 4 ms. There was no significant difference in either duration (P=0.83) or mean amplitude (P=0.06) of this activity. For the strike, the duration of midbody activity was 34.3±8.6 ms and mean amplitude was 0.202±0.056 mV, and for the startle the mean duration was 38.4±8.6 ms and the amplitude was 0.372±0.072 mV.
In contrast to the dramatic differences in stage 1 muscle activity patterns, contralateral muscle activity associated with stage 2, determined through comparison of EMGs from the contralateral rostral and midbody electrodes, was similar for strike and startle behaviors. With the exception of the amplitude of midbody activity (P<0.05), there were no significant differences in onset times, durations or mean amplitudes of muscle activity between the strike and the startle behaviors. The anterior electrode onset occurred at 16.1±4.2 ms after the initial burst of muscle activity for the strike and 14.1±1.3 ms for the startle. The durations of strike and escape bursts were, respectively, 49.8±8.7 ms and 31.9±6.3 ms. EMG amplitudes were 0.298±0.062 mV for the strike and 0.252±0.05 mV for the startle. For the midbody electrode, onset occurred at 26.5±4.5 ms for the strike and 15.3±2.7 ms for the startle. The duration of midbody activity was 37.3±6.6 ms for the strike and 30.4±8.3 ms for the startle, and amplitude was 0.234±0.04 mV for the strike and 0.146±0.068 mV for the startle.
Despite similarity in their EMG patterns, the stage 2 contralateral activity appears to differ in function between strike and startle behaviors. During the startle, contralateral rostral and midbody EMG onsets are considerably delayed relative to the onset of rostral and midbody activity on the ipsilateral side (P<0.0001; Figs 6, 7). By contrast, during the strike, rostral and midbody muscle onsets are not significantly different between the ipsilateral and contralateral electrodes [P=0.66 (rostral); P=0.10 (midbody)]. During the strike, the ipsilateral activity and contralateral activity appear to function together in stage 2. Instead of generating a wave of body bending as in startle behavior (Fig. 2LN), the bilateral rostral activity during the strike is associated with minimal bending in the trunk during stage 2 (Fig. 2E,F) while the primary propulsive tail stroke is generated by caudal ipsilateral muscle (relative onset time 19.1±4.0 ms).
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Discussion |
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In previous work on strike behavior, Harper and Blake
(1991) subdivided the strikes
based on acceleration profiles that corresponded to tail strokes subsequent to
the initial S-bend. In all of the trials examined, the northern pike
accomplished prey capture by the end of stage 2, eliminating this type of
variation. Webb and Skadsen
(1980
) subdivided the strike
based on initial patterns of bending. They found that some strikes were
initiated from a straight position and the S-bend was part of the propulsive
movement, while in others the fish initiated the propulsive movement from an
initial, nonpropulsive, S-shaped bend. We did not see the diversity of
responses described in these previous studies. The strikes we recorded were
variable but did not fall into distinct categories and so we did not subdivide
the responses. In several trials, axial movement preceded the activity of the
white muscle recorded during strike behavior. We hypothesize that red axial
muscle activity may be driving this bending. Further investigations of the
role of red muscle in strike behavior and the coordination of red and white
muscle would clarify these observations.
Initiation of the fast-start response
Major differences in the initiation of strikes and startles were found in
kinematics and muscle activity patterns of stage 1. During strike behavior,
the initial bending was for the most part restricted to the caudal region of
the body, with little angular movement observed rostrally during either the
S-bend or the L-bend. The movement pattern was reflected in the muscle
activity pattern in which the onset of rostral and midbody muscle activity was
delayed relative to caudal muscle activity. The angular movement during
startle behavior was much higher; more than four times the angular movement of
the strike for the S-bend. During the startle, the onset of activity among
electrode positions was much closer, with the rostral and midbody activity
occurring early in the behavior, on average 1 ms after caudal activity.
We suggest that minimizing head movement during stage 1 may have advantages
for the feeding strike that are not relevant to the escape startle. First,
minimizing rostral movement decreases the chance of detection by the prey fish
as the tail movement is less likely to generate disturbance felt in front of
the predator. Such tactics have been suggested for muskellunge predatory
behavior. New et al. (2001)
found that when positioning its body for the strike, the muskellunge appeared
to minimize axial movements, relying instead on fin-based locomotion, and
proposed that minimizing axial movement will decrease the chance of predator
detection. Second, maintaining a relatively constant head position facing the
prey may aid in accurately targeting the propulsive movements of stage 2. New
et al. (2001
) demonstrated
that visual orientation prior to the strike provides important sensory
information for successful prey capture.
The timing of S-start behaviors also differed between strikes and startles.
The duration of the S-bend of the strike was significantly longer and
considerably more variable than the S-bend of the startle response. This
difference was due to a longer S-bend during the strike than startle, on
average 55.5 ms for the strike as opposed to 20.9 ms for the startle. During
the startle, minimizing latency to respond and generating a rapid movement
from the onset of the stimulus is advantageous for a successful escape. By
contrast, during strikes, increasing the duration of initial movements may
allow for fine-tuning of the behavior to increase the likelihood of a
successful feeding event. This is critical for feeding as prey movement may be
unpredictable and the relative locations of predator and prey may change
rapidly with prey fish movement prior to the strike. In addition, early fast
movements may alert the prey to the presence of the attacking predator and
allow more time for escape (reviewed by
Domenici and Blake, 1997).
Coordination of jaws and axis
The relative onset of jaw adductor muscle activity also differed markedly
between the strike and startle. The adductor muscle did not contract during
the early movements of the strike; mean onset was 43 ms after initial activity
of axial muscle. This allowed the jaws to remain open as the pike approached
the prey, closing only after the prey entered the pike's mouth. In contrast to
the strike during the S-start, startle behavior jaw adductor muscle was active
nearly simultaneously with axial muscle, on average 3 ms after first
initiation of axial activity. Yasargil and Diamond
(1968) and Diamond
(1971
) found the same pattern
of activity during the Mauthner cell initiated C-start behavior. In addition,
they described concurrent bilateral adduction of the opercula and movement of
the eyes. Other than those initial descriptions and the one here, the
coordination between cranial and axial motor control during startle behaviors
has not been investigated. The function of this activity is also unclear. In
mammals, the startle response generally involves a bilateral protective move,
drawing in extremities and causing contraction of jaw and other cranial
muscles (e.g. Caesar et al.,
1989
). The cranial response in fishes may also serve this
function, protecting the head from attack. Alternative functions are also
possible. For example, cranial muscle activity and closing of the jaws and, at
least during the C-start, shutting the opercula and eyes may streamline the
head, reducing drag during propulsion. Despite differences in the timing of
jaw adduction, the durations and amplitudes of jaw movement did not differ
between strike and startle behaviors. We suggest that jaw muscle is maximally
active during both behaviors, thus generating similar patterns of
contraction.
As with the axial muscle activity, the differences in timing of jaw
activity during S-start startles and strikes suggest there are differences in
how jaw and axial muscle activities are coordinated, although mechanisms for
these differences are unclear. Our study was limited to one cranial muscle;
further study of the coordination of cranial activity in the strike and
startle, following the work of Diamond
(1971), would provide
additional insight into variation in the cranial portions of the response.
Stage 2 propulsion
Despite major differences in the initial movements of the strike and
startle, stage 2 is remarkably similar between the two behaviors. The angle of
head movement in stage 2 and the duration of that movement were not
significantly different between response types. We measured performance of the
startle and strike kinematics by determining the peak linear velocity and
acceleration of the center of mass in stage 2. As with movement angle and
duration, we found no significant differences between strikes and
startles.
To assess muscle activity in stage 2, we examined EMGs from rostral and
midbody muscle on the opposite side of the body to the initial rostral
activity. We found that there was no significant difference in onset times,
durations or rostral electrode amplitude of stage 2 EMGs. Although EMG
parameters are similar for the contralateral rostral and midbody muscle in
strikes and startles, we suggest that this activity is used in very different
ways. During the strike, rostral and midbody muscle onset times do not differ
between the ipsilateral and contralateral sides. We suggest that this
bilateral activity functions to stiffen the body in stage 2. Bilateral
activity has been suggested previously as a mechanism for increasing body
stiffness during the C-start (Diamond,
1971; Foreman and Eaton,
1993
; Westneat et al.,
1998
; Hale et al.,
2002
; Tytell and Lauder,
2002
). During the propulsive movement of the strike, this activity
might prevent rostral bending to improve prey targeting.
Another possible role of bilateral rostral activity may be in cranial
movement during the strike. Thys
(1997) has shown muscle
activity in the rostral epaxial muscle of the largemouth bass (Micropterus
salmoides) during strike behavior and suggests that these muscles are
used to raise the neurocranium when the mouth opens. More detailed examination
of regional activity of rostral myomeres, as performed by Thys
(1997
), may clarify the role
of bilateral rostral muscle activity in the strike behavior.
Categorizing fast-start responses
We conclude that the term S-start subsumes a range of behaviors that share
several general characteristics of muscle activity and movement patterns but
that differ in their neural control in fundamental ways. The S-start startle
of northern pike demonstrates the same pattern of muscle activity as that
described previously for the muskellunge
(Hale, 2002): near
simultaneous rostral muscle activity on one side of the body and caudal muscle
activity on the opposite side of the body. The strike is similar to the
startle in that it involves regional activity along the length of the body
during initial nonpropulsive movements. However, in contrast to the startle,
during the strike caudal muscle is active prior to contralateral rostral
activity and the duration of that activity is longer and more variable. While
it is possible that the two S-start behaviors may involve the same or
overlapping populations of cells in the hindbrain and spinal cords, those
cells must be coordinated by independent mechanisms. We suggest that, like the
Mauthner-elicited C-start startle behavior, the S-start startle involves a
simple neural circuit with relatively few cells. By contrast, we suggest that
there is greater processing of sensory cues during the initial movements of
the strike and thus a more complicated neural circuit is employed.
It is highly unlikely that the Mauthner cell could function during the
S-start startle or strikes. As discussed by Hale
(2002), the Mauthner cell has
been shown to elicit strong muscle contraction along the full length of the
spinal cord and to override conflicting motor patterns to generate a startle
response (Jayne and Lauder,
1993
; Svoboda and Fetcho,
1996
). That such strong neural activity could be inhibited to
generate the regional EMG pattern that characterizes the S-start behaviors is
unlikely. Thus, while Mauthner cell-elicited behaviors can occur in
post-feeding turns (Canfield and Rose,
1993
), as yet they have not been identified as part of the
high-acceleration prey capture portion of the feeding strike.
Domenici and Blake (1997),
in their figure 5, provide a
useful summary diagram of the fast-start types, their roles in behavior and
neural control. The diagram illustrates how little is known about the S-start
type of fast-start. While the neural basis of S-starts has yet to be studied,
our data begin to refine classifications of S-start behaviors.
Fig. 9 adds to Domenici and
Blake's diagram to incorporate recent data on S-start behaviors. In addition
to confirming that S-starts are an independent behavior from the C-start that
functions in escape (see also Hale,
2002
), we suggest that the S-start strikes and startles should be
subdivided based on differences in muscle activity of initial movements and
the implications of those differences for the motor control in stage 1.
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Acknowledgments |
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References |
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Caesar, M., Ostwald, J. and Pils, P. J. (1989). Startle responses measured in muscle innervated by facial and trigeminal nerves show common modulation. Behav. Neurosci. 103,1075 -1081.[CrossRef][Medline]
Canfield, J. G. and Rose, G. J. (1993). Activation of Mauthner neurons during prey capture. J. Comp. Physiol. A 172,611 -618.
Diamond, J. (1971). The Mauthner cell. In Fish Physiology, vol. 5 (ed. W. S. Hoar and D. J. Randall), pp. 265-346. New York: Academic Press.
Domenici, P. and Blake, R. W. (1993). Escape
trajectories in angelfish (Pterophyllum eimekei). J. Exp.
Biol. 177,253
-272.
Domenici, P. and Blake, R. W. (1997). The
kinematics and performance of fish fast-start swimming. J. Exp.
Biol. 200,1165
-1178.
Eaton, R. C. and Emberley, D. S. (1991). How stimulus direction determines the trajectory of the Mauthner-initiated escape response in a teleost fish. J. Exp. Biol. 161,469 -487.[Abstract]
Eaton, R. C., Lee, R. K. K. and Foreman, M. B. (2001). The Mauthner cell and other identified neurons of the brainstem escape network of fish. Prog. Neurobiol. 63,467 -485.[CrossRef][Medline]
Faber, D. S., Fetcho, J. R. and Korn, H. (1989). Neuronal networks underlying the escape response in goldfish: general implications for motor control. Ann. NY Acad. Sci. 563,11 -33.[Medline]
Fernald, R. D. (1975). Fast body turns in a cichlid fish. Nature 258,228 -229.
Fetcho, J. R. (1991). The spinal network of the Mauthner cell. Brain Behav. Evol. 37,298 -316.[Medline]
Foreman, M. B. and Eaton, R. C. (1993). The direction change concept for reticulospinal control of goldfish escape. J. Neurosci. 13,4101 -4133.[Abstract]
Frith, H. R. and Blake, R. W. (1995). The mechanical power output and the hydromechanical efficiency of northern pike (Esox lucius) fast-starts. J. Exp. Biol. 198,1863 -1873.[Medline]
Fuiman, L. A. (1994). The interplay of ontogeny and scaling in the interactions of fish larvae and their predators. J. Fish. Biol. 45 (Supp. A), 55-79.[CrossRef]
Hale, M. E. (1996). The development of fast-start performance in fishes: escape kinematics of the Chinook salmon (Oncorhynchus tshawytscha). Am. Zool. 36,695 -709.
Hale, M. E. (1999). Locomotor mechanics during
early life history: effects of size and ontogeny on fast-start performance of
salmonid fishes. J. Exp. Biol.
202,1465
-1479.
Hale, M. E. (2002). S- and C-start escape responses of the muskellunge (Esox masquinongy) require alternative neuromotor mechanisms. J. Exp. Biol. 205,2005 -2016.[Medline]
Hale, M. E., Long J. H., Jr, McHenry, M. J. and Westneat, M. W. (2002). Evolution of behavior and neural control of the fast-start escape response. Evolution 56,993 -1007.[Medline]
Harper, D. G. and Blake, R. W. (1990). Fast-start performance of rainbow trout Salmo gairdneri and northern pike Esox lucius. J. Exp. Biol. 150,321 -342.
Harper, D. G. and Blake, R. W. (1991). Prey capture and the fast-start performance of northern pike Esox lucius.J. Exp. Biol. 155,175 -192.
Hoogland, R., Morris, D. and Tinbergen, N. (1956). The spines of the stickleback as a means of defense against predators (Perca and Esox). Behaviour 10,88 -104.
Jayne, B. C. and Lauder, G. V. (1993). Red and white muscle activity and kinematics of the escape response of bluegill sunfish during swimming. J. Comp. Physiol. A 173,495 -508.
Jayne, B. C. and Lauder, G. V. (1995). Speed effects on midline kinematics during steady undulatory swimming of largemouth bass, Micropterus salmoides. J. Exp. Biol. 198,585 -602.[Medline]
Johnston, I. A., Van Leeuwen, J. L., Davies, M. L. F. and Bedow, T. (1995). How fish power predation fast-starts. J. Exp. Biol. 198,1851 -1861.[Medline]
New, J. G., Alborg Fewkes, L. and Khan, A. N.
(2001). Strike feeding behavior in the muskellunge, Esox
masquinongy: contributions of the lateral line and visual sensory
systems. J. Exp. Biol.
204,1207
-1221.
O'Steen, S., Cullum, A. J. and Bennett, A. F. (2002). Rapid evolution of escape performance in Trinidad guppies (Poecilia reticulata). Evolution 56,776 -784.[Medline]
Rand, D. M. and Lauder, G. V. (1981). Prey capture in the chain pickerel, Esox niger: correlations between feeding and locomotor behaviour. Can J. Zool. 59,1072 -1078.
Spierts, I. L. and Van Leeuwen, J. L. (1999).
Kinematics and muscle dynamics of C- and S-starts of carp (Cyprinus
carpio L.). J. Exp. Biol.
202,393
-406.
Svoboda, K. R. and Fetcho, J. R. (1996). Interaction between the neural networks for escape and swimming in goldfish. J. Neurophysiol. 16,843 -852.
Taylor, E. B. and McPhail, J. D. (1985). Ontogeny of the startle response in young coho salmon Oncorhynchus kisutch. Trans. Am. Fish. Soc. 114,552 -557.
Thys, T. (1997). Spatial variation in epaxial
muscle activity during prey strike in largemouth bass (Micropterus
salmoides). J. Exp. Biol.
200,3021
-3031.
Tytell, E. D. and Lauder, G. V. (2002). The
C-start escape response of Polypterus senegalus: bilateral muscle
activity and variation during stage 1 and 2. J. Exp.
Biol. 205,2591
-2603.
Walker, J. A. (1998). Estimating velocities and accelerations of animal locomotion: a simulation experiment comparing numerical differentiation algorithms. J. Exp. Biol. 74,211 -266.
Webb, P. W. (1976). The effect of size on the fast-start performance of rainbow trout (Salmo gairdneri). J. Exp. Biol. 65,157 -177.[Abstract]
Webb, P. W. and Skadsen, J. M. (1980). Strike attacks of Esox. Can. J. Zool. 58,1462 -1469.[Medline]
Weihs, D. (1973). The mechanism of rapid starting of slender fish. Biorheology 10,343 -350.[Medline]
Westneat, M. W., Hale, M. E., McHenry, M. J. and Long, J. H.
(1998). Mechanics of the fast-start: muscle function and the role
of intramuscular pressure in the escape behavior of Amia calva and
Polypterus palmas. J. Exp. Biol.
201,3041
-3055.
Yasargil, G. M. and Diamond, J. (1968). Startle response in teleost fish; an elementary circuit for neural discrimination. Nature 220,241 -243.[Medline]
Zottoli, S. J. (1978). Comparative morphology of the Mauthner cell in fish and amphibians. In Neurobiology of the Mauthner Cell (ed. D. S. Faber and H. Korn), pp.13 -45. New York: Raven Press.
Zottoli, S. J. and Faber, D. S. (2000). The Mauthner cell: what has it taught us? Neuroscientist 6, 25-37.