Use of sonomicrometry demonstrates the link between prey capture kinematics and suction pressure in largemouth bass
1 Department of Biology, 114 Hofstra University, Hempstead, NY 11549,
USA
2 Section of Evolution and Ecology, University of California, Davis, CA
95616, USA
* Author for correspondence (e-mail: christopher.p.sanford{at}hofstra.edu)
Accepted 12 August 2002
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Summary |
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Key words: sonomicrometry, kinematics, feeding, buccal pressure, largemouth bass, Micropterus salmoides
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Introduction |
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The teleost skull is highly kinetic and involves some 60 skeletal units
powered by approximately 80 muscles
(Winterbottom, 1974). Suction
feeding is the result of a rapid expansion of the buccal cavity
(Van Leeuwen, 1984
;
Lauder, 1985
) that generates a
pressure gradient, and water is accelerated into the mouth opening to fill the
expanding buccal cavity (Muller et al.,
1982
; Muller and Osse,
1984
; Van Leeuwen,
1984
). Pressure and water motion are intimately related in this
process. Suction pressure is generated by two phenomena
(Muller et al., 1982
).
Expansion of the buccal cavity occurs rapidly and may be the largest cause of
depressed buccal pressure. In addition, the induced water flow generates a
smaller subambient pressure, which is added to that induced by buccal
expansion. Prey are carried into the oral cavity by the flow generated during
the suction process. The velocity of flow entering the mouth, and hence the
magnitude of the pressure drop, are expected to be proportional to rate of
volume change of the fish's mouth (Muller
et al., 1982
; Van Leeuwen and
Muller, 1983
). The induced flow velocity is considered to be a key
component of suction feeding performance, and since flow and pressure are
intimately related, understanding how fish modulate suction pressure is an
important step in one of the fundamental goals of fish feeding biomechanics:
to understand the basis of suction feeding performance.
Several studies have empirically investigated functional correlates of
buccal pressure, including muscle activation patterns
(Lauder et al., 1986;
Grubich and Wainwright, 1997
)
and cranial kinematics (Svanbäck et
al., 2002
). The overall pattern that has emerged from these
studies is one in which muscle activity and cranial kinematics (excluding
significant interindividual effects) typically account for less than 55% of
the variation in pressure patterns among feeding attempts. This moderately
weak relationship is disappointing because the water flow generated by buccal
expansion is mechanically linked to buccal pressure
(Muller et al., 1982
). The
lack of tight relationships between muscle activity patterns (EMGs),
kinematics and buccal pressure may be the result of a faulty understanding of
the mechanical basis of buccal pressure; alternatively, previous attempts to
describe the relevant kinematic events with data derived from video recordings
may not have portrayed key motions accurately. One reason to suspect the
latter is that video recordings offer only an external view, and thus provide
only indirect estimates of buccal cavity expansion. In the present study we
employed sonomicrometry to measure buccal cavity expansion during suction
feeding by largemouth bass. Sonomicrometry uses ultrasound to precisely
measure distances between small (approximately 2.0 mm) piezoelectric crystals.
By attaching these crystals to key structures in the walls of the buccal
cavity we were able to obtain an accurate picture of changes in the dimensions
of the buccal cavity and jaw motion during suction feeding. Kinematic
variables generated from positional data were used in multiple regression
analyses, with dependent variables taken from simultaneous buccal pressure
recordings. There are no studies to date that have attempted to directly
measure internal expansion of the buccal cavity during suction feeding.
Furthermore, empirical investigations of the relationship between kinematics
and pressure suggest that peak gape, for example, precedes minimum subambient
pressure (Lauder, 1980c
).
Our experiments were designed to answer three questions about suction feeding in largemouth bass: (1) what is the temporal relationship between kinematics of the internal surfaces of the buccal cavity and the subambient pressures generated by those movements; (2) what are the temporal relationships between various elements of the buccal cavity during suction feeding; and (3) can kinematics of the internal buccal cavity be used to accurately predict buccal pressures?
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Materials and methods |
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Specimens
The largemouth bass were obtained from a private fish farm in Yolo County,
CA, USA. Specimens were housed individually in 1001 aquaria at 23-25°C and
were fed a mixed diet of goldfish (Carassius auratus), mosquitofish
(Gambusia affinis) and pieces of squid (Loligo opalescens).
The specimens used for this study were identified as Individuals 1-5 and had a
standard length of 235, 242, 249, 257 and 265 mm, respectively. A narrow size
range was used to reduce any scaling effects that have been demonstrated in
this species (Richard and Wainwright,
1995; Wainwright and Richard,
1995
).
Before each experiment, the bass were starved for 2-3 days to increase hunger level. Prior to surgery the bass were gradually anesthetized with a light dose of tricaine methanesulfonate (MS-222). The bass were returned to their home tank following surgery (described below). They were allowed to recover overnight and recording of feeding behavior was started the following day. The bass were fed goldfish (Carassius auratus), and feeding bouts were recorded in succession over a period of 1-2 days, during which strikes representing a wide range of effort were obtained. The number of strikes obtained for analysis ranged from seven (Individual 3) to 25 (Individual 1). The total number of sequences analyzed was 88.
Sonomicrometry
We used an eight-channel digital sonomicrometer (Sonometrics Corp.) to
measure the kinematics of six internal positions on the wall of the buccal
cavity (Fig. 1). These
positions were selected to reflect the major movements related to volumetric
change in the buccal cavity (Lauder,
1985; Muller,
1989
; De Visser and Barel,
1998
). The locations of the crystals were: (1) the posterior roof
of the mouth just ventral to the parasphenoid, and in the same transverse
plane as crystals 3 and 4 (below), (2) the anterior roof of the mouth just
ventral to the vomer, (3) the left suspensorium just dorsal to the
interhyal-suspensorium articulation, (4) the right suspensorium (the same as 3
but on the opposite side), (5) the dorsal surface of the hyoid at the
articulation between the basihyal and the first basibranchial (this position
was chosen because when the hyoid is depressed, during expansion of the buccal
cavity, this crystal will occupy a position approximately in the same plane as
crystals 1, 3 and 4), and (6) the mucosa on the anteroventral-most region of
the buccal cavity, close to the dentary symphasis.
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The piezoelectric crystals used were omnidirectional and either 1 or 2 mm diameter depending on location, although 2 mm crystals gave a more consistent signal. The crystals were sutured to the mucosal layer using surgical thread. Visual inspection ensured that the crystals were securely tied to the mucosal layer. Any crystal showing excessive movement was anchored using a second suture. All crystals were aligned so that the tip of the crystal was pointing anteriorly. The wires from the crystals were run anterior to the gill arches (three on each side) and out through the operculum. All six wires were then bundled together and stabilized by suturing them to the skin just anterior to the first dorsal fin.
Sonometric data were recorded using the software program Sonoview (Sonomicrometrics Corp.) at a sample rate of 500 Hz and a transmit pulse of 500 ns with an inhibit delay of 3 mm. This program records absolute distances between all crystal pairs and we selected those combinations that provided the best signals and were relevant to our analysis (below). These traces were cleaned of outliers and corrected for other signal problems using Sonoview. An ASCII output file was then imported into Biopac Lab Pro V. 3.6.5 for deriving the variables used in our analysis.
Kinematics and variables
The following distances were transduced: posterior hyoid (distance between
crystals 1 and 5; Fig. 1),
anterior hyoid (distance between crystals 2 and 5), suspensorial distance
(distance between crystals 3 and 4) and gape (distance between crystals 2 and
6). During the implantation, crystals 1, 2 and 5 were placed as close to the
midline as possible and we assumed that depression and elevation of the
basihyal and basibranchials was in the mid-sagittal plane. Thus, crystal 5
swung through an arc in the mid-sagittal plane with crystals 1 and 2. This
assumption was verified by examination of feeding profiles from each
individual bass to confirm that the change in distance between crystals 3 and
5, and crystals 4 and 5, was symmetrical. In addition to these kinematic
variables, the buccal cross-sectional area (hereafter abbreviated to buccal
area) was also estimated at approximately the position of crystals 1, 3 and 4.
We used changes in this variable as a metric of the expansion of the buccal
volume because most expansion occurs in the laterallateral and
dorsalventral axes and not in the anteriorposterior axis.
Calculation of buccal area was based on an expanding elliptical model of the
buccal cavity. With distances between crystals 1-2, 1-5 and 2-5 defining a
triangle, it was possible to calculate the vertical distance of the hyoid
relative to the roof of the mouth (axis 1-2) as it moved in the mid-sagittal
plane (Fig. 1). This distance
was used as one axis of the ellipse and suspensorial distance was used as the
other.
From plots of these five variables against time (Fig. 2), we derived displacement, temporal and velocity variables for each capture sequence. The following derived variables were used for further analysis: maximum displacement from onset, onset time (relative to peak subambient pressure = t0), duration, time of peak displacement (relative to t0), time to peak displacement from onset, and velocity of displacement. Velocity of displacement was calculated using 20% of maximum displacement as the onset time. This procedure eliminated the variable initial stages of displacement kinematics. From our calculations of buccal area we derived two additional variables: the time of peak rate of change in buccal area (relative to t0), and the time of peak rate of percentage change in buccal area (relative to t0). For all derived variables we defined the time of minimum buccal pressure as time zero (t0). This point was unambiguously identified in all feeding sequences and was of very short duration (about 2 ms).
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Pressure
During experiments we simultaneously recorded intra-oral buccal pressure
using a Millar SPR-407 microcatheter-tipped pressure transducer. During
surgical implant of the sonomicrometry crystals (see above) we also inserted a
plastic cannula though the mid-dorsal region of the neurocranium between the
nostrils and the eyes. The cannula had an expanded end holding it in place
against the skin inside the buccal cavity, where it emerged just lateral to
the anterior end of the parasphenoid bone. A sleeve of silicon tubing was
fitted flush with the skin of the neurocranium and it stabilized the position
of the cannula. Following recovery from surgery the pressure transducer was
threaded into the cannula so that the tip was flush with the opening of the
cannula in the buccal cavity. The transducer leads were sealed around the head
of the cannula by a plastic sleeve with a soft plastic core. The analog
pressure signal was digitized at 500 Hz through a parallel channel on the
sonomicrometry system, allowing precise synchronization of the two types of
data.
The synchronized pressure recordings were also processed in Sonosoft and Biopac Lab Pro V. 3.6.5. From traces of pressure against time we derived the following variables: peak subambient buccal pressure, onset time of the buccal pressure curve (when the pressure fell below ambient), total buccal pressure duration from onset to when the pressure again reached ambient (offset), time to peak subambient buccal pressure, measured from onset to peak subambient buccal pressure, and rate of buccal pressure drop, measured as the average rate from 20% of peak subambient pressure to peak subambient pressure. Again, the 20% onset value was used to calculate rate due to the variable nature of the pressure profile during the initial stages. Finally, pressure area was calculated as the area between ambient pressure and the pressure in the buccal cavity from the onset to the offset of subambient pressure. All experimental techniques were approved by UC Davis (institutional animal care and use protocol #10168).
Statistical analysis
We used multiple-regression analysis to explore the correlations between
kinematics of the buccal cavity and pressure. In this analysis we used each
pressure variable in turn as the dependent variable and all kinematic
variables as the independent variables, adding individual bass as a
categorical variable. The resulting analysis of covariance (ANCOVA) model
included interaction terms between each kinematic variable and individual
bass. Each model was run in a two-step process. Initially, all kinematic
variables and interaction terms were included in the model. We then removed
variables and interaction terms from the model if their P value was
greater than 0.4 (a very conservative cut-off of significance). The reduced
model was rerun and although it inevitably provided a lower overall
r2, it is the model reported here. Cumulative
r2 values were calculated to provide insight into the
extent to which kinematic variables provided independent explanatory power.
All data were log10 transformed prior to data analysis to normalize
variances and to linearize exponential relationships. Analyses were performed
using Systat for Windows v. 9.
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Results |
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Gape distance was the first kinematic variable to increase during the expansive phase, with a mean onset time of -40.7±2.7 ms (all values are relative to to; Table 1, Fig. 4). Anterior hyoid depression (-26.2±1.8 ms) and posterior hyoid depression (-27.7±2.4 ms) began virtually simultaneously (Table 1). Finally, the suspensorium began to abduct at -19.6±1.8 ms. The drop in buccal pressure started immediately after the onset of hyoid depression at -24.5±2.0 ms. Buccal area showed a detectable increase at -18.4±2.2 ms (Fig. 4). The temporal sequence of mouth opening followed by hyoid depression and then suspensorial abduction was found in 91 % of feeding sequences (N=88).
One notable feature that was revealed by the synchronized recordings was the very early time of peak subambient buccal pressure during the feeding sequence (Figs 2, 3). Pressure was the fastest variable to reach its peak value from onset (24.5±2.0 ms), and peak subambient pressure occurred on average 24 ms before the first kinematic variable (gape) reached its peak (Table 1, Figs 3, 4). Subambient pressure reached its peak prior to any kinematic variable 100% of the time (N=88).
Relative to minimum subambient pressure (t0), the average time of peak rate of change in buccal area was 11.2±0.7 ms (Table 1), and this was significantly different from the peak rate of percentage change in buccal area, which occurred earlier at 0.56±0.47 ms (mixed model analysis of variance, ANOVA; P<0.001, d.f. 1,4) (for example, see Fig. 3C,D). The time of peak values for gape, hyoid and suspensorium followed the same temporal sequence found for onset times, and this sequence occurred in 100% of feedings (N=88) (Fig. 4). During the expansive phase, gape peaked first at 23.9±1.2 ms, followed by the anterior and posterior hyoid measurements, which both peaked at approximately 35 ms. Buccal area peaked at 45.3±2.8 ms and, finally, the suspensoria were maximally abducted at 53.0±1.9 ms (Fig. 4). The early peak of the buccal area relative to suspensorial abduction is a consequence of the hyoid (one of the two axes of buccal area) beginning to elevate before the suspensorium has reached peak displacement, which occurred in 99% of feedings (N=88) (Fig. 5). The temporal sequence of peak values for kinematic variables is also illustrated by superimposing the time of peak values for kinematic variables and pressure onto the displacement of the hyoid crystal with reference to the roof of the mouth (defined by fixed crystals 1 and 2) (Fig. 5).
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The anterior hyoid measurement had the fastest velocity of any kinematic variable during feeding at 528±25 mm s-1 (Table 1), and the correlation of this variable with peak subambient buccal pressure and pressure area is significant (peak subambient buccal pressure, Pearson correlation -0.71, Bonferroni-corrected P<0.001; pressure area correlation 0.48, Bonferroni-corrected P<0.05; also see below). It is important to remember that the displacement of the hyoid is in a posteroventral direction and is not restricted to ventral motion only (Fig. 5).
Kinematics and pressure relationships
The multiple regression models were all able to account for over 90% of the
variation among strikes in pressure (Tables
2,3,4,5,6).
In the reduced multiple-regression models, kinematics accounted for 99.1% of
the variation in peak subambient buccal pressure, 96.7% of the variation in
buccal pressure area, 91.7% of the variation in buccal pressure rate, 91.9% of
the variation in the time to peak buccal pressure, and 96.3% of the variation
in buccal pressure duration (Tables
2,3,4,5,6).
No single variable or class of variables dominated the regressions. In each
multiple regression a large number of variables and interaction terms were
independently significant, and no single kinematic variable or interaction
term accounted for more than 39.5% of the variance in any pressure
variable.
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One striking feature of these analyses was the large contribution of the interaction terms in every model. As a group, interactions accounted for 20-45% of the total variance explained by the model (Tables 2,3,4,5,6), which implies that the influence of kinematic variables on pressure varied between individual bass (Fig. 6). In some cases even the direction of the relationship between the kinematic and pressure variables varied among bass (Fig. 6C), although in none of these cases was the interaction a dominant term in the model.
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Discussion |
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Buccal kinematics during suction feeding
Previous evidence of a preparatory phase has been limited to periods of
superambient pressure prior to suction strikes (Lauder,
1980a,
c
;
Svanbäck et al., 2002
)
and electrical activity of buccal compression muscles at this time
(Liem, 1978
;
Lauder, 1980a
). Gibb
(1995
) reported a compressive
phase in the flatfish Pleuronichthys verticalis. However, this was
based on movements of the operculum and not the suspensorium. Thus, our study
provides the first direct observation of suspensorial adduction and decrease
in buccal volume prior to the expansive phase of suction feeding. In our
recordings, following the preparatory phase, the expansive phase began with
mouth opening, followed by hyoid depression (about 14 ms later), and then
suspensorial abduction (21 ms) (Figs
2A,
4). This kinematic sequence
reflects the general models of skull function described in actinopterygians
(Lauder and Liem, 1980
;
De Visser and Barel, 1998
;
Lauder, 1985
). As found
previously in analyses of film (Lauder,
1980a
,
b
;
De Visser and Barel, 1998
)
mouth opening clearly began before hyoid depression or suspensorial expansion
(Fig. 2A). We saw no motion of
the basihyal crystal relative to the neurocranium (crystals 1 and 2) until 14
ms after the onset of mouth opening, which implies that mouth opening is not
initiated by hyoid retraction, as has been proposed by some workers
(De Visser and Barel, 1998
),
but rather by some other action, such as cranial elevation or opercular
rotation (Lauder, 1980b
;
Wilga et al., 2000
;
Adriaens et al., 2001
).
Our results provide empirical evidence that the onset of hyoid depression
precedes abduction of the suspensoria (Fig.
4), a pattern that was predicted in models of optimal hyoid motion
in cichlids (De Visser and Barel,
1996,
1998
). However, this pattern
seems to contradict previous electromyographic data from largemouth bass
indicating that the levator arcus palatini, a muscle that directly abducts the
suspensorium, is activated before the hyoid-retracting sternohyoideus
(Wainwright and Richard, 1995
;
Grubich and Wainwright,
1997
).
It has been predicted that the initial stages of hyoid movement are
restricted to the longitudinal axis of the body
(Aerts, 1991;
De Visser and Barel, 1998
). By
triangulating the two crystals fixed to the roof of the mouth and crystal 5 on
the hyoid we were able to calculate movement of the hyoid crystal in the
xy reference frame defined by crystals 1 and 2 (x
axis) and crystal 5 (y axis). The resulting pattern shows clearly
that the hyoid crystal swings in an arc and does not show an initial
retraction along the x axis (Fig.
5). Indeed, in no sequence examined (N=76) was there
evidence of an initial retraction of the hyoid crystal.
In Micropterus, buccal cross-sectional area continues to increase
after the hyoid has reached a maximum, the result of continued suspensorial
abduction (Figs 3A,B,
4,
5). Peak buccal area (and
presumably volume) is reached about 86 ms after mouth opening. This is
approximately 20 ms later than peak volume estimated for Oncorhynchus
mykiss (Van Leeuwen,
1984). The shorter time to peak buccal volume estimated for O.
mykiss is unlikely to be related to size, as Van Leeuwen
(1984
) used larger fish.
It is generally assumed in modeling efforts that during suction feeding the
buccal cavity is circular in cross section, thus minimizing the friction
forces by creating the lowest area/circumference ratio
(Muller et al., 1982;
Barel, 1983
;
Muller and Osse, 1984
;
De Visser and Barel, 1998
).
Although the dorsoventral distance between the hyoid and the roof of the
mouth, and the suspensorial distance (Fig.
1), would occasionally be approximately equal, we did not find
strong empirical support for this expectation. In most sequences examined,
throughout the expansive phase, even at peak hyoid depression, the distance
between the hyoid and the roof of the mouth was much less than the distance
between the suspensoria. This suggests that the buccal cavity cross-section is
described better by a dorsoventrally flattened ellipse than a circle. It might
be argued that this inference would depend on the crystals used to calculate
buccal area being in the same region of the buccal cavity. Examination of
Fig. 5 and displacement
patterns of several sequences indicate that, at maximum depression, the hyoid
reaches a position almost directly ventral to crystal 1 (see Figs
1,
5). Care was also taken during
surgery to place the two suspensorial crystals (3 and 4) in the same
transverse plane as crystal 1.
Our discovery of extensive individual variability is common in studies of
this type (Tables
2,3,4,5,6;
see also Wainwright and Lauder,
1986). These differences between individual bass occurred with
both the kinematic variables and the pressure variables.
The relationship between kinematics and pressure
Suction pressure results from the rapid expansion of the buccal cavity in a
highly deterministic way that should permit pressure to be accurately
calculated from kinematic data (Muller et
al., 1982; Muller and Osse,
1984
; Van Leeuwen,
1984
; Muller,
1989
; De Visser and Barel,
1998
). However, previous attempts that employed multiple
regression methods to link buccal pressure with prey capture kinematics
(Svanbäck et al., 2002
)
and muscle activation patterns (Lauder et
al., 1986
; Grubich and
Wainwright, 1997
) in largemouth bass met with only moderate
success. Kinematic variables based on movements of the jaws, hyoid and head
that were generated from high-speed video recordings accounted for 79.7% of
variation in minimum buccal pressure
(Svanbäck et al., 2002
),
although this was reduced to an average of 50% across all pressure variables.
Electromyographic variables accounted for an average of 54.8% of the variation
among strikes in minimum buccal pressure
(Grubich and Wainwright,
1997
). In contrast, regressions calculated in the present study
were able to account for 99% of the variation between strikes in minimum
pressure, and never less than 90% for any pressure variable; these results
strongly support the general nature of the kinematic basis of suction pressure
(Muller et al., 1982
;
Muller, 1989
). We suggest that
one major factor accounting for the statistical resolution of this study
compared to that of Svanbäck et al.
(2002
) was our use of
sonomicrometry. This technique allowed us to measure the changes in internal
dimensions of the buccal cavity, movements that are directly tied to the
increase in buccal volume and hence the flow of water and pressure that are
generated. Standard video recordings provide poorer resolution of these
movements. The poorer performance of EMG variables in accounting for buccal
pressure may reflect the indirect link between muscle electrical activity and
buccal pressure, as compared to a closer link between buccal expansion and
pressure.
Although our results provide solid confirmation of the expected
relationship between pressure and buccal cavity kinematics, it is not possible
to use the multiple regression results to compare the importance of different
variables in generating buccal pressure patterns. Independent variables that
contribute high r2 values to the multiple regression
models can do so either because they are in fact the causal basis for the
buccal pressure dependent variable, or because they are strongly correlated
with the actions that do underlie buccal pressure. Further, patterns of shared
correlation between independent variables and the dependent variable result in
only one of the independent variables making a strong showing in the
regression models, while the effect of other variables are not significant
because of these correlations (James and
McCulloch, 1990). This pattern may actually mask causal
relationships between individual variables and can be misleading. For example,
anterior hyoid velocity had a significant negative correlation with peak
subambient buccal pressure (Fig.
6A). However, we do not regard this as establishing that the
movement of the hyoid relative to the vomer is more important in generating
peak subambient buccal pressures than any other variable. Anterior hyoid
velocity explained approximately 40% of the variation in peak subambient
buccal pressure, but at the same time anterior hyoid rate was also
significantly correlated with 14 of the possible 24 other variables, not all
of which appeared in the reduced multiple regression. Thus, other variables
may play a causal role, but are statistically redundant as predictors of
buccal pressure. In summary, we emphasize the overall explanatory power of the
models, the r2, rather than the contribution of individual
variables.
Although we cannot dissect apart the causal role that individual kinematic
variables play in generating buccal pressure, it is of interest that several
variables were significant factors in each of the multiple regression models
(Tables
2,3,4,5,6).
This pattern indicates that the basis of pressure is complex and involves some
independence among kinematic variables in their influence on buccal pressure.
Svanbäck et al. (2002) in
their kinematic study found a consistent pattern of mouth opening and hyoid
depression dominating the regression models. Unfortunately, the suspensorial
movements were excluded from that study so it is unclear whether these
movements would also have contributed significantly to the regression
analysis. In our study it is clear that kinematic patterns associated with
movements of the hyoid, gape and suspensorium are all contributing at some
level to the magnitude of negative buccal pressure. However, in every multiple
regression the vast majority of the explanatory power of the kinematics was
seen in the first variable. This reflects the strong pattern of coordination,
and thus correlation, among kinematic variables.
A conspicuous aspect of the regression analyses was the important role of interaction terms in accounting for the overall explanatory power of the models. The independent variables were responsible for over half of the variance explained in each multiple regression analysis, but interaction terms accounted for between 20% and 45% of the total variance explained (Tables 2,3,4,5,6). The implication of these interaction terms is that the relationship between individual kinematic variables and pressure often varied among bass (Fig. 6). Unfortunately, it cannot be determined from the regression analyses alone whether this also implies that the kinematic basis of pressure varied among bass. This pattern could also come about if spurious correlations between kinematic variables and pressure are ephemeral and vary among individual fish. However, this result underscores the need for replicated experiments in organismal functional morphology and the pitfalls of relying upon interpretations of results from a single specimen.
Minimum buccal pressure occurred at the time when the rate of percentage volume change in the buccal cavity was highest (Fig. 3D), 11.2 ms before the time of highest rate of increase in buccal area (Table 1). Minimum buccal pressure should occur at the time when the velocity of flow at the pressure transducer is highest. Guided by the principal of continuity we predict that the time of peak subambient pressure would also coincide with the peak flow of water into the mouth. Thus any prey in front of the mouth at the time of peak subambient pressure would be subject to maximum drag generated by the influx of water. We did not directly measure water flow inside the buccal cavity but this flow will be related to the ratio of rate of buccal volume change and the area of the mouth opening. All else being equal, peak flow at the mouth opening will occur when the rate of volume change of the buccal cavity is highest. However, the gape opens during the strike, thus decreasing the relative flow at the mouth opening. The rate of buccal volume change is increasing while the gape is also increasing, which suggests that peak flow may occur at an intermediate point in time, prior to the time of peak volume change, as we observed (Fig. 3).
One implication of this result is that peak subambient buccal pressure was already achieved when many of the kinematic events that were measured occurred. Thus, although variables such as time to peak gape are correlated with minimum pressure, peak gape actually occurs after peak subambient pressure, indicating an indirect mechanical relationship between these variables. The early peak in buccal pressure also indicates that the forces resisting buccal expansion are highest very early in the event and suggest an important role for power production in the expansion muscles of high performance suction events.
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Acknowledgments |
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References |
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