Muscle activation and strain during suction feeding in the largemouth bass Micropterus salmoides
Section of Evolution and Ecology, University of California, One Shields Avenue, Davis, CA 95616, USA
(e-mail: mcqcarroll{at}ucdavis.edu)
Accepted 31 December 2004
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Summary |
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Key words: suction feeding, largemouth bass, Micropterus salmoides, muscle function, sonomicrometry, electromyography, muscle strain
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Introduction |
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The use of sonomicrometry to measure muscle strain in vivo has
vastly increased understanding of muscle function during numerous behaviors,
helping to clarify how the specific kinematic and mechanical demands of a
behavior affect muscle function (Biewener,
2002). Research into muscle function has predominantly focused on
locomotor behaviors. Feeding behavior, although of equal evolutionary and
ecological significance, has not received commensurate attention. In
particular, muscle force and strain during suction feeding have not been
studied despite a considerable history of research into the muscular basis of
this behavior (Alexander, 1969
;
Lauder et al., 1986
;
Osse, 1969
).
To successfully capture evasive prey, suction feeding musculoskeletal
systems must be able to rapidly expand cranial elements against hydrodynamic
pressure gradients of 560 kPa
(Ferry-Graham et al., 2003;
Lauder, 1980b
;
Muller et al., 1982
).
Understanding how muscles meet the kinematic and mechanical demands of suction
feeding is a necessary first step towards understanding the functional
implications of teleost musculoskeletal morphology and may shed light on the
biomechanics of suction feeding, which are poorly understood
(Ferry-Graham et al.,
2003
).
To these ends, one aspect of muscle function, the time course and amplitude
of muscle fascicle strain in relation to activation and kinematics, was
measured in vivo in the sternohyoideus of largemouth bass
Micropterus salmoides feeding on evasive prey. The sternohyoideus
originates on the pectoral girdle and posterior muscle masses to insert on the
hyoid (Figs 1,
2;
Edgeworth, 1935;
Winterbottom, 1974
).
Shortening in the sternohyoideus results directly in ventralcaudal
rotation of the hyoid and indirectly in lower jaw depression and lateral
expansion of the suspensoria (De Visser
and Barel, 1996
; Fig.
1). Lower jaw depression was also measured to relate strain
measurements to relevant skeletal kinematics. This study is the first direct
measurement of muscle strain during suction feeding.
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|
The sternohyoideus is known to be active during suction feeding
(Grubich and Wainwright, 1997;
Lauder et al., 1986
;
Osse, 1969
), but its function
cannot be determined without information on fascicle strain patterns. The
sternohyoideus may shorten during contraction or may contract isometrically,
either to resist action of the epaxial muscles or transmit strain from larger
more posterior muscle masses (Fig.
1). Thus, a primary objective of this study was to understand how
the sternohyoideus functions during feeding. Because generation of both force
and velocity were thought to be important to suction feeding performance, it
was predicted that the sternohyoideus would contract at velocities that permit
muscular power production during some or all of its active period. In the
absence of in vitro data on the velocity at which largemouth bass
white-muscle fibers produce maximal power, it was predicted that the muscle
would contract at approximately 1/3 maximum velocity or about three muscle
lengths per second, assuming a maximum contraction velocity of about ten
muscle lengths per second (Askew and Marsh,
1998
; Hill, 1938
;
Rome, 1998
).
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Materials and methods |
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Surgery
Prior to surgery fish were anaesthetized by emersion in 0.3 g
l1 of MS-222 (tricaine methane sulfonate). Fish were then
moved to a surgical tray containing 0.1 g l1 of MS-222 and
returned to higher concentrations only if they awoke. Surgery lasted less than
30 min and most fish did not awake during surgery.
Sonomicrometry was used to measure gape and muscle strain. In
sonomicrometry, small piezo-electric crystals are used to measure distances.
The crystals work by transmitting and receiving ultrasound, with the time of
sound travel used to measure distance. The utility of using sonomicrometry to
measure distances within muscle tissue and water has been established in
numerous previous studies (Biewener,
2002; Hoffer et al.,
1989
; Sanford and Wainwright,
2002
). The speed of sound in muscle was estimated as 1560 m
s1 (Mol and Breddels,
1982
). This velocity underestimated kinematic measurements because
the velocity of sound in water was overestimated. The timing of lower jaw
depression was the parameter of interest not the absolute distance of lower
jaw depression, so this overestimation did not seriously affect results.
To measure lower jaw depression, two 2 mm omnidirectional sonometric crystals (Sonometrics Corp., London, ON, Canada) were passed beneath the operculum, rostral to the first gill arch, and into the mouth. One crystal was sutured to the lower jaw just inside the mandibular symphysis, while the other was sutured to the palate lateral to the vomer (Fig. 2). Crystal wires were secured to the dorsal skin of the fish leaving enough slack for normal movement of the jaws and head.
To measure fascicle strain, two 1 mm crystals were inserted between fascicles in the lateral surface of the sternohyoideus. A 1 mm incision was made through the skin and fascia of the sternohyoideus and a 5-0 suture passed through the skin on either side of the incision. Muscle fascicles were gently separated with a blunt probe and the crystal was passed between them with a plastic introducer. The suture was tightened, securing the crystal. The introducer was removed and the skin on either side of the cut was sutured tightly around the wire. Crystals secured by these methods moved freely with underlying muscle fascicles and stayed in place until the end of each experiment. Crystal distance varied from 1117 mm between preparations. Crystals were inserted along fascicle lines so that fascicle strain would be accurately recorded. The accuracy of crystal distance was checked with calipers prior to recovery of the fish. The movement of crystals with muscle shortening was also checked prior to recovery. Crystal strain and strain rate were interpreted as fascicle strain and strain rate based on the assumptions that crystals were aligned along parallel fascicles and that changes in crystal distance reflected changes in fascicle length.
Bipolar electrodes were fashioned from 0.002 inch (0.051 mm) bi-filament stainless steel, Teflon-coated wire (California Fine-Wire, Grover Beach, CA, USA) by exposing and spreading the wire tips. The electrode wire was bent into a hook 35 mm before the exposed tip and the whole wire (approximately 2 m) was threaded through a 26-gauge hypodermic needle. After crystal implantation the electrodes were inserted into the sternohyoideus body via the hypodermic needle and kept in place by the hook in the wire. Care was taken to consistently place electrodes between and just under crystals.
Surgery took place the night before experimentation, allowing the fish to recover overnight before experimentation. Data collection took place the next morning as soon as the fish were willing to feed and continued until satiation. During data collection fish were fed live goldfish (approximately 4 cm SL). At the conclusion of data collection fish were re-anesthetized and instrumentation was removed. Surgical wounds were extensively cleaned with commercial povidoneiodide solution and left open to prevent infection. Fish were returned to their home tank after instrument removal and monitored for 68 h. All fish survived experimentation.
Data collection
Crystal signals were digitized with a Sonometrics TRX-8 conversion box
(Sonometrics Corp.) connected to a PC running Sonoview software (Sonometrics
Corp.). The PC and software were also used to collect, digitize and record
amplified EMG signals. EMG signals were amplified with a differential
amplifier (A-M systems, Everett, WA, USA). Using the same software to record
EMG and crystal data allowed more convenient synchronization of activity,
strain and kinematic signals, but required the EMG signal to be digitized at
sampling rates of no more than 500 Hz. One set of data was collected at 700
Hz, but this higher sampling rate markedly increased noise in the strain
signal.
Data analysis
Crystal and EMG data were converted to tab-delimited ASCII text files and
opened as Microsoft Excel spreadsheets. Crystal data were first smoothed by
manually removing obvious outlying points, then with a 3-point rolling
average. These methods were found to produce smooth strain profiles without
altering the relative timing of discrete events at the sampling frequencies
used in this study. The distance between the lower jaw and the neurocranium
was normalized by subtracting the minimum distance for each strike from each
value and then dividing by the maximum distance for the individual. Fascicle
length at each point in time was normalized by subtracting each value from
length at onset and dividing by the resting length for the preparation.
Because crystal distance at feeding onset varied between strikes, resting
length was calculated as the mean crystal distance at onset for each strike in
the preparation. The timing of kinematic events (slow onset of lower jaw
depression, fast onset of lower jaw depression, peak gape and onset of lower
jaw closing), strain events (onset of shortening, onset of fast shortening,
peak strain and return to resting length), and activation events (onset and
offset) were taken manually from kinematic, strain and activation profiles
graphed in Excel. The timing of peak gape was not taken as the time of maximum
gape but rather as the end of fast opening
(Fig. 3). The onset of fast
fascicle shortening was identified by increases to shortening velocities of
1.5 or greater fascicle lengths (FL) s1.
Although this was an arbitrary value, it was found to be a useful way to
demarcate the onset of rapid shortening. The timing of each event was
subtracted from each other event to produce a matrix of latencies. Latencies
were averaged for each individual and individual means were averaged
(Table 1). For events thought
to be simultaneous, the latencies were compared to a predicted mean of zero in
single t-tests. Events were considered simultaneous if their latency
did not significantly differ from zero (P<0.05).
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|
Instantaneous shortening velocity was calculated at each point by subtracting strain at the present time from strain at the previous point and dividing by the time between samples. Two velocities were calculated for each strike: total shortening velocity (the normalized total amplitude of shortening divided by total time to peak strain) and fast shortening velocity (the normalized change in amplitude between the onset of fast shortening and peak strain divided by the latency between these two events).
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Results |
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Muscle activity
Sternohyoideus activity was observed in all feeding events, but the timing
of activation varied among feeding events. For instance, in some strikes
activity was nearly simultaneous with the onset of shortening
(Fig. 3B), while in others
sternohyoideus shortening began 4060 ms before onset of activation
(Fig. 3E). On average,
observable activity began 23±6 ms after the onset of sternohyoideus
strain. The sternohyoideus was always active before the fast shortening
period. The latency between onset activation and onset of fast shortening was
less variable within individuals than the latency between onset of activation
and onset of slow shortening (t-test of latency
S.E.M. values by individual
P<0.01, N=5). Activity in the sternohyoideus usually
ended simultaneously with peak strain and the onset of lower jaw closing
(Fig. 4, Table 1). Sternohyoideus
activity was never observed prior to the onset of muscle shortening, but was
always observed before the onset of fast shortening
(Fig. 4,
Table 1).
Fascicle strain
Sternohyoideus fascicles shortened by an average of 11±0.7% across
individuals. The onset of shortening was nearly simultaneous with the onset of
slow jaw depression (Table 1),
and typically continued smoothly until maximum strain was reached
(Fig. 3). In two fish it was
common for the sternohyoideus to discontinue shortening or lengthen after the
onset of fast lower jaw depression (Fig.
3A,C,D). The sternohyoideus usually began to shorten again about
the time of peak gape. The relationship between sternohyoideus shortening and
peak gape varied among individuals. In three individuals there was
significantly greater strain after peak gape than before peak gape
(Fig. 5); in the other two
individuals there was roughly equivalent strain before and after peak gape. In
all strikes the sternohyoideus continued to shorten after peak gape. On
average, peak strain occurred 28±3 ms after peak gape. The onset of
lower jaw closing was simultaneous with the cessation of fascicle shortening
and muscle activity (Figs 3,
4;
Table 1). The return of
sternohyoideus to its resting length was simultaneous with the return of the
jaw to its closed position (Table
1).
|
Shortening velocity
Averaged velocity profiles for three individuals are shown in
Fig. 6. Shortening started
slowly but increased rapidly near the time of peak gape. This rapid increase
in negative slope of the strain profile marked the onset of the fast
shortening period. Shortening velocity during fast lower jaw depression was
variable between individuals. In most individuals the sternohyoideus
contracted rapidly during fast lower jaw depression, but in two individuals
the sternohyoideus showed little strain or positive strain during most of
rapid lower jaw depression (Figs
3,
6). In all individuals
sternohyoideus shortening was faster after peak gape than before peak gape
(Fig. 5). Instantaneous
shortening velocities during the fast portion of shortening ranged from
2 to 5 FL s1
(Fig. 6). Fast shortening
levels were typically maintained until peak strain. Total velocity of fascicle
shortening for the sternohyoideus averaged 1.3±0.12 FL
s1 across all individuals. Total fast shortening velocities
averaged 2.5±0.40 FL s1
(Fig. 7). In all strikes the
majority of peak strain occurred during the fast period
(Fig. 7).
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Discussion |
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The sternohyoideus consistently shortened after peak gape
(Fig. 5). In three of the five
individuals more strain was observed after peak gape than before. This pattern
is consistent with the multiple functions of the sternohyoideus, including
lower jaw depression, hyoid depression and lateral expansion of the
suspensoria (Fig. 1). Suction
feeding fish in general, and largemouth bass in particular, exhibit an
anterior-to-posterior wave of expansion during suction feeding. Peak gape
precedes hyoid depression, which precedes peak opercular expansion
(Lauder, 1980a;
Osse, 1969
;
Sanford and Wainwright, 2002
).
This kinematic pattern is possible because the linkage between the proximal
hyoid and lower jaw allows the hyoid to continue depression after the lower
jaw has reached its ventral limit (Fig.
1). Shortening after peak gape would continue ventralcaudal
rotation of the hyoid, resulting in continued depression of the buccal floor
and continued lateral expansion of the suspensioria.
In all individuals the sternohyoideus increased shortening velocity after
peak gape (Fig. 5). This
pattern suggests that sternohyoideus loading may be reduced after peak gape.
Loads may be reduced because the lower jaw is no longer rotating, and because
other cranial structures are not accelerating as rapidly as prior to peak
gape, reducing hydrodynamic load (Sanford
and Wainwright, 2002). The major source of loading during suction
feeding appears to be negative internal buccal pressure
(Alexander, 1969
), the
magnitude of which is greatly decreased after peak gape
(Sanford and Wainwright,
2002
). These factors would all contribute to decreased loading and
increased shortening velocity after peak gape.
Individual variation in sternohyoideus function
In two of the five studied individuals the sternohyoideus lengthened
slightly or contracted isometrically during fast lower jaw depression. One
explanation for this observation is that the sternohyoideus was stretched by
rotation of the hyoid away from the pectoral girdle as described above. By
contracting eccentrically the sternohyoideus might be able to generate greater
force than it would be able to during shortening
(Hill, 1938;
Lindstedt et al., 2002
). Why
this pattern was consistently observed in some individuals and not others is
not apparent from this study, but it may have been the result of subtle
differences in muscle activation between individuals. Individual variation is
common in studies of both suction feeding and muscle function (e.g.
Gillis and Biewener, 2000
;
Grubich and Wainwright, 1997
).
Furthermore, jaw opening in teleosts is actuated by multiple complex and
redundant musculoskeletal systems (Adriaens
et al., 2001
; Lauder,
1980a
; Westneat,
1990
), so there is potential for variation in how these systems
are used between individuals.
Activation and strain
In many reported vertebrate behaviors muscle activation precedes shortening
by 2080 ms (e.g. Franklin and
Johnston 1997; Gillis and
Biewener, 2000
; Olson and
Marsh, 1998
; Lutz and Rome,
1994
). In this study measurable activation was not detected until
an average of 23 ms after the onset of the slow fascicle shortening
(Table 1, Fig. 4). The sternohyoideus may
be returning to resting length after being passively stretched by an
antagonistic muscle or be slackening by action of a synergistic muscle.
Elevation of the lower jaw by the adductor mandibulae would stretch the
sternohyoideus, but these muscles are not detectably active prior to expansion
in largemouth bass (Wainwright and
Richard, 1995
).
Passive shortening in the sternohyoideus might also have been caused by
depression of the lower jaw through the opercular linkage
(Lauder, 1980a). A small
muscle, the levator operculi, links the operculum to the neurocranium and is
thought to depress the lower jaw through a linkage involving the opercular
series. This muscle is typically active prior to the sternohyoideus
(Grubich and Wainwright, 1997
;
Lauder et al., 1986
;
Osse, 1969
) and is thought to
actuate the slow phase of lower jaw depression
(Aerts et al., 1987
;
Osse, 1969
). In doing so it
may allow the sternohyoideus to shorten. The onset of shortening and the onset
of activation were variable within individuals, but the sternohyoideus was
never active prior to shortening. However, several strikes showed nearly
simultaneous onset of shortening, jaw depression and activation
(Fig. 3). In these strikes the
levator operculi may have been activated at the same time as the
sternohyoideus.
Muscle function for power production
The shortening velocities measured in this study suggest that the
sternohyoideus functions to generate mechanical power during suction feeding.
In all individuals, the sternohyiodeus actively shortened during part or all
of its active period, generating mechanical power. Shortening velocity
averaged 2.5 FL s1 during fast shortening.
Although it cannot be concluded from in vivo data alone, this
velocity may maximize mass-specific production of muscle velocity. Peak
muscular power production occurs at approximately 1/3 maximal velocity
(Askew and Marsh, 1998;
Hill, 1938
). Maximal
velocities for suction feeding muscles are not known in fish, but maximum
velocities for fish white axial muscle at 22° approximate 710
FL s1 (Aerts et
al., 1987
; Beddow and Johnston,
1995
). Furthermore, the shortening velocities measured in this
study were similar to those of other ectothermic vertebrates performing
power-limited behaviors at similar temperatures
(Ellerby and Altringham, 2001
;
Lutz and Rome, 1994
;
Nelson and Jayne, 2001
;
Olson and Marsh, 1998
).
Without in vitro data, however, it cannot be concluded that the
sternohyoidues contracts at velocities that permit maximal mass-specific power
production.
Maximizing muscular power production may be an important component of
successful suction feeding on evasive prey
(Aerts et al., 1987;
Alexander, 1969
). To be
successful a suction-feeding predator must accelerate a sufficient volume of
water to entrain prey before the prey has a chance to escape. The energetic
cost of doing so equals the pressure resisting expansion multiplied by the
total change in buccal volume (see, for example,
Marsh et al., 1992
). With
variable pressure, the total work (Wtot) equals the
pressure resisting expansion as a function of volume V integrated
from starting volume (V0) to final volume
(Vfinal). The total pressure resisting cranial expansion
(Ptot) is the sum of sub-ambient pressure inside the mouth
(Pout) and the supra-ambient pressure outside expanding
cranial elements (Pin):
![]() | (1) |
![]() | (2) |
The power required for cranial expansion is equal to the total mechanical
work done on the water divided by the total time t of volume
expansion:
![]() | (3) |
The power required for suction feeding would therefore increase linearly
with decreasing duration of cranial expansion
(tfinalt0) even if the incurred
hydrodynamic resistance were independent of strike duration. In fact,
hydrodynamic loading probably increases with increasing speed of volume
expansion. Although the hydrodynamics of suction feeding are extremely complex
and poorly understood, the pressure measured inside the expanding buccal
cavity probably results from the inertia of water entering the mouth
(Muller et al., 1982); it can
therefore be expected that the more rapidly the volume expansion takes place
the more intense the negative pressures that resist expansion. There is
empirical evidence to support this assumption: Sanford and Wainwright
(2002
) found that internal
pressure in largemouth bass increased with increasing acceleration of cranial
expansion.
Similarly, positive pressures outside expanding cranial elements may
increase with increasing suction feeding speed. This pressure is due to the
inertia of water (added or virtual mass) displaced by the expanding cranial
elements and would be expected to increase linearly with increasing cranial
acceleration (Batchelor, 1967;
Daniel, 1984
;
Vogel, 1994
). In a detailed
theoretical analysis of shrimp tail flips, which occur on time scales similar
to suction feeding, Daniel and Meyhofer
(1989
) found that predicted
muscle force increased exponentially with decreasing duration of the tail
flip. Furthermore, differential pressures measured on the tail of swimming cod
Gadus morhua were shown to increase with increasing tail rotational
acceleration (Webber et al.,
2001
).
If the above analysis is correct, increased suction feeding performance, in
an individual fish, is limited by muscular power. Therefore, fish that use
suction feeding to capture evasive prey ought to possess musculoskeletal
morphologies that permit fascicles to shorten at velocities that maximize
their intrinsic power capabilities. In other words, fish that feed on evasive
prey ought to be `geared' for power generation. This study supports this
theoretical prediction: sternohyoideus fascicles contract at velocities
consistent with the production of mechanical power. Whether the shortening
velocities measured in this study approximate the optimal shortening velocity
for power production must be determined by in vitro measurements of
muscle fiber performance, as has been done in other systems
(Lutz and Rome, 1994;
Marsh et al., 1992
;
Peplowski and Marsh, 1997
;
Rome et al., 1993
;
Wakeling and Johnston,
1998
).
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Acknowledgments |
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References |
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![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Adriaens, D., Aerts, P. and Verraes, W. (2001). Ontogenetic shift in mouth opening mechanisms in a catfish (Clariidae, Siluriformes): A response to increasing functional demands. J. Morphol. 247,197 -216.[CrossRef][Medline]
Aerts, P., Osse, J. W. M. and Verraes, W. (1987). Model of jaw depression during feeding in (Astatotilapia elegans: Teleostei Cichlidae): mechanisms for energy storage and triggering. J. Morphol. 194,85 -109.
Alexander, R. M. (1969). Mechanics of the feeding action of a cyprinid fish. J. Zool. (Lond.) 159, 1-15.
Altringham, J. D. and Ellerby, D. J. (1999).
Fish swimming: patterns in muscle function. J. Exp.
Biol. 202,3397
-3403.
Askew, G. N. and Marsh, R. L. (1998). Optimal
shortening velocity V/Vmax) of skeletal muscle
during cyclical contractions: Lengthforce effects and
velocity-dependent activation and deactivation. J. Exp.
Biol. 201,1527
-1540.
Batchelor, G. K. (1967). An Introduction to Fluid Dynamics. Cambridge, England: Cambridge University Press.
Beddow, T. A. and Johnston, I. A. (1995). Plasticity of muscle contractile properties following temperature acclimation in the marine fish Myoxocephalus scorpius. J. Exp. Biol. 198,193 -201.[Medline]
Biewener, A. A. (2002). Future directions for the analysis of musculoskeletal design and locomotor performance. J. Morphol. 252,38 -51.[CrossRef][Medline]
Biewener, A. A., Konieczynski, D. D. and Baudinette, R. V.
(1998). In vivo muscle force-length behavior during
steady-speed hopping in tammar wallabies. J. Exp.
Biol. 201,1681
-1694.
Daniel, T. L. (1984). Unsteady aspects of aquatic locomotion. Am. Zool. 24,121 -134.
Daniel, T. L. and Meyhofer, E. (1989). Size limits in escape locomotion of carridean shrimp. J. Exp. Biol. 143,245 -266.
De Visser, J. and Barel, C. D. N. (1996). Architectonic constraints on the hyoid's optimal starting position for suction feeding of fish. J. Morphol. 228, 1-18.[CrossRef]
Edgeworth, F. H. (1935). The Cranial Muscles of Vertebrates. London, UK: Cambridge University Press.
Ellerby, D. J. and Altringham, J. D. (2001).
Spatial variation in fast muscle function of the rainbow trout,
Oncorhynchus mykiss, during fast-starts and sprinting. J.
Exp. Biol. 204,2239
-2250.
Etnier, D. A. and Starnes, W. C. (1993). The Fishes of Tennessee. Knoxville: University of Tennessee Press.
Ferry-Graham Lara, A., Wainwright, P. C. and Lauder George, V. (2003). Quantification of flow during suction feeding in bluegill sunfish. Zoology 106,159 -168.
Finni, T., Komi Paavo, V. and Lepola, V. (2000). In vivo human triceps surae and quadriceps femoris muscle function in a squat jump and counter movement jump. Eur. J. Appl. Physiol. 83,416 -426.[CrossRef][Medline]
Franklin, C. E. and Johnston, I. A. (1997).
Muscle power output during escape responses in an Antarctic fish.
J. Exp. Biol. 200,703
-712.
Gillis, G. B. and Biewener, A. A. (2000).
Hindlimb extensor muscle function during jumping and swimming in the toad
(Bufo marinus). J. Exp. Biol.
203,3547
-3563.
Grubich, J. R. and Wainwright, P. C. (1997). Motor basis of suction feeding performance in largemouth bass, Micropterus salmoides. J. Exp. Zool. 277, 1-13.[CrossRef]
Hill, A. V. (1938). The heat of shortening and the dynamic constants of muscle. Proc. R. Soc. Lond. B 126,136 -195.
Hoffer, J. A., Caputi, A. A. and Griffiths, R. I. (1989). Roles of muscle activity and load on the relationship between muscle spindle length and whole muscle length in the freely walking cat. Prog. Brain Res. 80, 75-85.[Medline]
Lauder, G. V. (1980a). Evolution of the feeding mechanism in primitive actinopterygian fishes: a functional anatomical analysis of Polypterus, Lepisosteus, and Amia. J. Morphol. 163,283 -317.
Lauder, G. V. (1980b). The suction feeding mechanism in sunfishes (Lepomis) and experimental analysis. J. Exp. Biol. 88,49 -72.
Lauder, G. V., Wainwright, P. C. and Findeis, E. (1986). Physiological mechanisms of aquatic prey capture in sunfishes: Functional determinants of buccal pressure changes. Comp. Biochem. Physiol. 84A,729 -734.
Lindstedt, S., L., Reich, T. E., Keim, P. and LaStayo, P. C.
(2002). Do muscles function as adaptable locomotor springs?
J. Exp. Biol. 205,2211
-2216.
Lutz, G. J. and Rome, L. C. (1994). Built for jumping: The design of the frog muscular system. Science 263,370 -372.[Medline]
Marsh, R. L. (1999). How muscles deal with
real-world loads: the influence of length trajectory on muscle performance.
J. Exp. Biol. 202,3377
-3385.
Marsh, R. L., Olson, J. M. and Guzik, S. K. (1992). Mechanical performance of scallop adductor muscle during swimming. Nature 357,411 -413.[CrossRef][Medline]
Mol, C. R. and Breddels, P. A. (1982). Ultrasound velocity in muscle. J. Acoust. Soc. Am. 71,455 -461.[Medline]
Muller, M., Osse, J. W. M. and Verhagen, J. H. G. (1982). A quantitative hydrodynamical model of suction feeding in fish. J. Theor. Biol. 95, 49-79.
Nelson, F. E. and Jayne, B. C. (2001). The effects of speed on the in vivo activity and length of a limb muscle during the locomotion of the iguanian lizard, Dipsosaurus dorsalis.J. Exp. Biol. 204,3507 -3522.[Medline]
Norton, S. F. and Brainerd, E. L. (1993).
Convergence in the feeding mechanics of ecomorphologically similar species in
the Centrarchidae and Cichlidae. J. Exp. Biol.
176, 11-29.
Nyberg, D. W. (1971). Prey capture in the largemouth bass. Am. Mid. Nat. 86,128 -144.
Olson, J. M. and Marsh, R. L. (1998).
Activation patterns and length changes in hindlimb muscles of the bullfrog
Rana catesbeiana during jumping. J. Exp.
Biol. 201,2763
-2777.
Osse, J. W. M. (1969). Functional morphology of the head of the perch (Perca fluviatis L.): an electromyographic study. Neth. J. Zool. 19,289 -392.
Peplowski, M. M. and Marsh, R. L. (1997). Work
and power output in the hindlimb muscles of cuban tree frogs Osteopilus
septentrionalis during jumping. J. Exp. Biol.
200,2861
-2870.
Richard, B. A. and Wainwright, P. C. (1995). Scaling the feeding mechanism of largemouth bass (Micropterus salmoides): Kinematics of prey capture. J. Exp. Biol. 198,419 -433.[Medline]
Rome, L. C. (1998). Some advances in integrative muscle physiology. Comp. Biochem. Physiol. 120B,51 -72.
Rome, L. C., Swank, D. and Corda, D. (1993). How fish power swimming. Science 261,340 -343.[Medline]
Sanford, C. P. J. and Wainwright, P. C. (2002). Use of sonomicrometry demonstrates the link between prey capture kinematics and suction pressure in largemouth bass. J. Exp. Biol. 205,3445 -3457.[Medline]
Thys, T. (1997). Spatial variation in epaxial
muscle activity during prey strike in largemouth bass (Micropterus
salmoides). J. Exp. Biol.
200,3021
-3031.
Vogel, S. (1994). Life in Moving Fluids: The Physical Biology of Flow, 2nd edition. Princeton, NJ: Princeton University Press.xiii+467p .
Wakeling, J. M. and Johnston, I. A. (1998).
Muscle power output limits fast-start performance in fish. J. Exp.
Biol. 201,1505
-1526.
Wainwright, P. C. and Richard, B. A. (1995). Scaling the feeding mechanism of the largemouth bass (Micropterus salmoides): Motor pattern. J. Exp. Biol. 198,1161 -1171.[Medline]
Wardle, C. S., Videler, J. J. and Altringham, J. D. (1995). Tuning in to fish swimming waves: Body form, swimming mode and muscle function. J. Exp. Biol. 198,1629 -1636.[Medline]
Webber, D. M., Boutilier, R. G., Kerr, S. R. and Smale, M. J. (2001). Caudal differential pressure as a predictor of swimming speed of cod (Gadus morhua). J. Exp. Biol. 204,3561 -3570.[Medline]
Westneat, M. W. (1990). Feeding mechanics of teleost fishes (Labridae: Perciformes): A test of four-bar linkage models. J. Morphol. 205,269 -296.
Winterbottom, R. (1974). A descriptive synonymy of the striated muscles of the Teleostei. Proc. Acad. Nat. Sci. Phil. 125,225 -317.