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First published online February 1, 2008
Journal of Experimental Biology 211, 587-598 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.012096
Speed-dependent intrinsic caudal fin muscle recruitment during steady swimming in bluegill sunfish, Lepomis macrochirus
Museum of Comparative Zoology, Harvard University, 26 Oxford Street, Cambridge, MA 02138, USA
* Author for correspondence (e-mail: bflammang{at}oeb.harvard.edu)
Accepted 3 December 2007
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: fish, swimming, locomotion, kinematics, electromyography, muscle, caudal fin
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Grove and Newell, 1936;
Lauder, 1989;
Nursall, 1958;
Videler, 1975;
Webb and Smith, 1980). A few
three-dimensional kinematic analyses have provided additional information on
complex patterns of motion of the caudal fin
(Ferry and Lauder, 1996;
Gibb et al., 1999;
Tytell, 2006), but there is
virtually no information on how movements of the caudal fin are controlled and
on how caudal fin muscles are recruited during steady swimming in fishes.
Anatomical studies of caudal fin structure
(Lauder, 1982;
Lauder, 1989;
Liem, 1970;
Nag, 1967;
Videler, 1975;
Winterbottom, 1974) have shown
that approximately 50 discrete muscles are present within the caudal fin, and
that these muscles could potentially control tail fin shape during swimming
and generate propulsive waves on the caudal fin itself independently of the
myotomal muscle fibers that generate body bending anterior to the tail.
Intrinsic caudal musculature is derived from the overlying axial body muscles,
but is modified into smaller muscle groups that do not resemble the broad
`w-shaped' myomeres of the axial body musculature in either form or function.
Instead, intrinsic caudal muscles are compartmentalized into small specific
muscle groups that insert onto and are proposed to control specific fin rays
or groups of fin rays (Gemballa,
2004; Lauder,
1982; Nag, 1972;
Winterbottom, 1974). Muscular
activity patterns that could control the shape and orientation of the caudal
fin in teleost fishes have yet to be described [although some preliminary data
have been presented by Lauder (Lauder,
1989) and Videler (Videler,
1975)], and there are effectively no data on recruitment patterns
for intrinsic tail musculature in fishes.
To this end, the overall goal of this work was to establish a baseline
understanding of intrinsic caudal muscle activity patterns in fishes by
examining muscle activity in relation to caudal fin kinematics during steady
swimming at different speeds. Determining activity patterns of intrinsic
caudal muscles will allow for better understanding and linkage of the
anatomical structure of the caudal fin in fishes
(Gemballa, 2004;
Lauder, 1982;
Lauder, 1989;
Lauder and Drucker, 2002;
Liem, 1970;
Nag, 1967;
Videler, 1975;
Winterbottom, 1974) with
kinematic patterns and previous studies of caudal fin wake hydrodynamics
(Bainbridge, 1963;
Breder, 1926;
Gibb et al., 1999;
Nauen and Lauder, 2002;
Tytell, 2006;
Videler, 1975).
This study addresses four specific questions. First, are intrinsic caudal
fin muscles active during steady swimming behaviors in fishes, or are these
muscles only used to modulate tail shape during maneuvers and hovering
behavior where complex tail motions are most evident? We hypothesize that
intrinsic caudal fin muscles will be active during steady swimming, albeit at
lower intensities than muscle activity during complex tail motions. Second, if
intrinsic tail muscles are active during steady rectilinear locomotion, when
are they first recruited as swimming speed increases? We expect that intrinsic
caudal muscle activity will first be prevalent near swimming speeds of one
body length per second, when bluegill sunfish begin to utilize
body–caudal swimming instead of pectoral fin locomotion. Third, are
there differential activity patterns evident among the many intrinsic tail
muscles, or do they tend to be active as a group? We predict that differential
muscle activity will be observed, acting to control modulation of the tail fin
during swimming. Fourth, how does the recruitment pattern of intrinsic caudal
fin musculature compare to patterns previously described for myotomal red and
white fibers? We anticipate that the patterns observed in previous studies on
red and white myotomal muscle in bluegill sunfish will be conserved in the
intrinsic caudal musculature (Jayne and
Lauder, 1994).
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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20°C) in individual 40 l aquariums, where they were fed
three times a week. Fish were placed in the working section of a recirculating
flow tank 2 days before the experiments and were not fed during this time.
After 8 h in the flow tank on the first day, the flow was turned on to
approximately 1 body length per second (L s–1) for
10–15 min to see if fish would be able to orient into the flow and swim
without difficulty. All fish were induced to swim within the center region of
the flow tank, away from the walls, as in our previous studies of fish
locomotion (Drucker and Lauder,
2005; Jayne and Lauder,
1995b; Liao and Lauder,
2000; Standen and Lauder,
2005; Tytell,
2006). On the second day the fish were allowed to rest with the
flow turned off. Experiments were conducted on the third day. A total of seven
fish of similar size were used in this study (17.5±0.80 cm total
length, TL, mean ± s.e.m.), five for kinematic and electromyography
experiments, one for electrical stimulation of caudal fin muscles, and one for
computer microtomography (µCT) scanning.
Kinematic protocol
Experimental data were gathered while each of five sunfish swam in a 600 l
recirculating tank, which had a 26 cmx26 cmx80 cm study area, as
in previous research (Standen and Lauder,
2005; Tytell,
2006). Three high-speed digital video cameras (Photron USA, Inc.,
San Diego, CA, USA) were used to record the lateral, posterior and ventral
views of the fish. Each fish was filmed at 250 frames s–1
(with 1024x1024 pixel resolution) while swimming steadily at speeds of
0.5, 1.2 and 2.0 L s–1.
High-speed video was calibrated using direct linear transformation of a
custom 20-point calibration frame in three dimensions and digitized using a
program written for MATLAB 6.5.1 (MathWorks, Inc., Natick, MA, USA) by Ty
Hedrick (Hatze, 1988;
Hedrick et al., 2002;
Hsieh, 2003;
Standen and Lauder, 2005). A
total of 7 points were digitized from the video in the caudal region of each
fish: (1) the posterior end of the second fin ray, (2) the posterior end of
the sixth fin ray, (3) the posterior end of the ninth fin ray in the fork of
the caudal fin, (4) the posterior end of the twelfth fin ray, (5) the
posterior end of the fifteenth fin ray, (6) at the insertion of the anal fin
on the anterior ventral edge of the caudal peduncle, and (7) at the posterior
ventral edge of the caudal peduncle at the base of the first raylet. A total
of 33 tail beat sequences from three fish with good electrode placement and
consistently steady swimming were used for kinematic analysis: of these seven
were of swimming at 0.5 L s–1, fourteen at 1.2
L s–1, and twelve at 2.0 L
s–1. These speeds were specifically chosen to cover the range
of natural locomotor behaviors in bluegill sunfish
(Drucker, 1996;
Drucker and Lauder, 1999;
Gibb et al., 1999;
Lauder, 2000). At 0.5
L s–1, bluegill use slow pectoral fin swimming with
little to no body undulation and only minor movements within the tail surface
are occasionally visible. At 1.2 L s–1, bluegill
first begin to use regular rhythmic undulatory locomotion involving body
bending (Drucker and Lauder,
2000; Gibb et al.,
1999), although intermittent beats of the pectoral fins also
occur. At 2.0 L s–1, pectoral fin beats are
infrequent, and locomotion occurs by rapid body undulation. This is near the
maximal speed at which bluegill can sustain undulatory locomotion for
1–2 min before tiring noticeably.
Two kinematic variables were used to describe the action of the tail fin: mean lateral excursion (cm) and mean tail height (cm) measured three-dimensionally. Mean lateral excursion was defined as the average lateral distance traveled by the dorsal tip of the tail, as this was the point that moved the most and was the first part of the tail to move during lateral flexion. Mean tail height was calculated in 3D from the dorsal tip to the ventral tip of the posterior edge of the tail fin.
Electromyographic protocol
Bluegill were anaesthetized using tricaine methanesulfonate (MS222)
buffered with potassium hydroxide and actively ventilated using water
oxygenated by an aquarium air pump throughout the procedure, as in previous
research (Jayne and Lauder,
1993; Jayne et al.,
1996; Tytell and Lauder,
2002). Fish were allowed to recuperate fully from the anesthesia
following electrode insertion before any swimming procedures were begun. As a
general rule, fish were fully recuperated after twice the time that they were
under anesthesia had passed.
Electrodes were made from 2 m lengths of 0.05 mm diameter bifilar Teflon-coated steel wire (California Fine Wire Co., Grover Beach, CA, USA). The wires were split apart along 1 mm of their long axis and 0.5 mm of the tip of one wire was removed, so that the tips did not contact each other. The insulation was removed from a 0.5 mm section at the tip of each wire, and the electrode tips was bent back into a hook shape. Electrodes were threaded through a 26-guage needle for subcutaneous surgical implantation into the fish muscle. Care was taken to standardize electrode construction in order to minimize signal variation.
Electrodes were placed bilaterally in a total of 24 muscles of the caudal
peduncle and fin (13 muscles maximum per experiment) to account for any local
muscle activity contributing to tail shape. Muscles studied included the
flexor dorsalis (FD), flexor ventralis (FV), hypochordal longitudinalis (HL),
infracarinalis posterior (IC), nine of the interradialis (IR) muscles, of
which there are 32 in total between all the caudal fin rays, lateralis
superficialis (LS) in the caudal peduncle, dorsal to the lateral red muscle,
supracarinalis posterior (SC), and the lateral red muscle in the myotomes just
anterior to the caudal peduncle (Fig.
1). The electrodes in the caudal peduncle red fibers correspond in
placement to position 7 of Jayne and Lauder
(Jayne and Lauder, 1995a)
(Fig. 1). Electrodes were
inserted on both the left and right sides of the fishes to include activity
throughout an entire tail beat and to minimize the chance that fish would
favor one side.
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Electrical stimulation experiment
Electrical stimulation was performed to initiate contraction and elucidate
the function of each intrinsic tail muscle individually. For the purpose of
the electrical stimulation experiments, a lethal dose of MS222 was
administered to one fish. The skin over the tail was then removed to visually
ensure direct electrode placement in the correct muscles. Electromyographic
electrodes were implanted into the flexor dorsalis (FD), flexor ventralis
(FV), hypochordal longitudinalis (HL), infracarinalis posterior (IC),
interradialis (IR) between each of the caudal fin rays, lateralis
superficialis (LS), and supracarinalis posterior (SC) muscles to determine
what their action upon activation might be. The free ends of the electrodes
were attached to a Grass S44 electrical stimulator, and muscles were
stimulated both separately and in groups at 10–20 V for 1 s duration of
10–30 pulses s–1 with a 1 ms delay between pulses. A
video camera (Sony Digital Handycam DCR-TRV38) was mounted above the fish tail
during the stimulation experiment to capture caudal fin movement for later
analysis.
Data analysis
Electromyographic recordings that corresponded with clear video views of
the caudal fin in all three video cameras simultaneously were used for
analysis of the muscle activity. The EMG results were rectified, integrated
and digitized in Chart 5.4.2 software. We recorded the onset, duration, and
the intensity of each selected section of muscle activity during steady
swimming sequences, where intensity was defined as the area of the integrated
EMG burst.
In an effort to maximize the total number of muscles studied by electromyography, and since we were limited by the equipment to simultaneous recording of only 13 electrodes in any one fish, many of the specific muscles examined were different for each individual and a few of the implantations were not successful. In all individuals, the activity of the red muscle along the midline of the caudal peduncle and the hypochordal longitudinalis (HL) were recorded, and the activity of all other muscles in each fish was analyzed relative to these shared muscles. Owing to the number of muscles studied within the tail and the fact that some recordings from individual muscles did not yield analyzable data, the final data set had missing recordings for different muscles in each of the different individual fish. As a result of the pattern of missing values, it was not possible to perform a single global analysis of variance (ANOVA) amongst all individuals, muscles, and swimming speeds. Analysis of variance of duration and intensity of activity of muscles shared amongst individuals and swimming speeds, where each muscle was recorded in at least three individuals at each speed, showed that there was no significant difference among individuals (FANOVA=0.2662, F0.05(1),11,24=2.22, P>0.25; power=0.878). Therefore, there was only a 12% chance that individuals were different, and so one-way ANOVAs were used to compare muscle activity duration, relative onset of muscle activity, and EMG burst duration by muscle. In addition, principal component analysis (PCA) was implemented on muscle activity duration, relative onset of muscle activity, and EMG burst duration data of each muscle pooled by swimming speeds.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Winterbottom, 1974). The
flexor dorsalis (FD) originates on the dorsal and lateral aspect of the last
few vertebral centra, neural spines and upper hypurals and inserts onto the
seven or eight dorsal-most fin rays. The flexor ventralis (FV) originates on
the hypurapophysis, lower hypurals, and haemal spines of the posterior-most
vertebrae and inserts onto the eight ventral fin rays. The hypochordal
longitudinalis (HL) originates below the FV on the hypurapophysis and lower
hypurals and extends posterodorsally, inserting superficially to the FD onto
the four dorsal-most fin rays. The infracarinalis posterior (IC) and
supracarinalis posterior (SC) are thin paired muscles located at the ventral-
and dorsal-most edges of the caudal peduncle, respectively
(Fig. 1). The IC originates at
the posterior pterygiophore of the anal fin and inserts on the ventral-most
fin ray and raylets. The SC originates from the posterior pterygiophore of the
dorsal fin and inserts on the dorsal-most fin rays and raylets. The
interradialis (IR) muscles are a series of small angled muscles found between
each of the fin rays. Interradialis muscles between fin ray pairs from the
first to the tenth fin rays are oriented posterodorsally, whereas IR muscles
between fin ray pairs from the ninth to the seventeenth fin rays are oriented
posteroventrally (Fig. 1). Overlying the intrinsic caudal musculature in the region of the caudal peduncle are the lateralis superficialis (LS) and a thin segment of red muscle adjacent to the horizontal septum. Anterior to the caudal peduncle, the LS is a thin band of muscle positioned mediolaterally above the connection between the epaxial and hypaxial musculature. Within the caudal peduncle, however, the LS fans out posteriorly into a thin tendinous expanded sheet to cover the majority of the intrinsic caudal musculature and inserts on the caudal fin rays. Embedded superficially in this muscle, along the midline, is a thin strip of red muscle.
Electrical stimulation
The majority of intrinsic caudal muscles tested during the stimulation
experiments caused lateral flexion of the tail, as well as either abduction or
adduction of the dorsal and ventral lobes of the tail fin
(Table 2,
Fig. 1). Lateral flexion of the
tail was produced by the hypochordal longitudinalis (HL), flexor dorsalis (FD)
and flexor ventralis (FV) muscles. Abduction of the fin rays, which created an
increase in the surface area of the caudal fin, was accomplished by the FD,
FV, supracarinalis (SC) and infracarinalis (IC) muscles. Reduction in the
surface area of the fin occurred through adduction of the fin rays by the
contraction of the HL and interradialis muscles (IR). When stimulated, the IR
muscles acted only on the fin rays to which they were inserted; they did not
affect other sections of IR muscles or fin rays elsewhere in the fin.
Simultaneous stimulation of the FD and SC muscles caused greater abduction of
the dorsal fin rays than either muscle had caused independently. Also,
simultaneous stimulation of the FD, FV, SC and IC induced greater abduction of
the fin rays than stimulations of the FD and FV or SC and IC had caused.
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Overview of recruitment pattern
Fish swimming steadily while the speed of the water in the flow tank was
slowly increased from 0 to 2.0 L s–1 exhibited both
changes in the timing and burst intensity of the electromyographic recordings
(Fig. 2). Initially, at zero
flow, no intrinsic caudal fin muscles were active. As flow speed increased to
near 0.5 L s–1, low amplitude irregular rhythmic
bursting in some intrinsic muscles was observed
(Fig. 2A), and similar very low
amplitude activity was seen in the posterior red fibers in the caudal
peduncle. As flow speed increased to near 1.0 L s–1,
higher amplitude bursts were observed in all muscles
(Fig. 2B). At higher speeds
approaching 2.0 L s–1, duration of muscle bursts
decreased while the overall magnitude of the recorded bursts, or intensity,
increased dramatically (compare Fig. 2B and
C). Not all muscles initiated activity at the same speed: the
supracarinalis (SC), hypochordal longitudinalis (HL), infracarinalis (IC), and
red lateral muscle were occasionally active at speeds lower than 0.5
L s–1 whereas other intrinsic muscles were not
active until the fish approached speeds of 1.2 L
s–1.
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Kinematic and EMG analysis
Fish swimming at 0.5 L s–1 primarily used their
pectoral fins for locomotion; therefore only minor tail fin movements and
shape modulation were observed at this speed
(Fig. 3). Mean lateral
excursion of the tail was less than 0.25 cm from the median axis of the fish
and maximum excursion occurred at approximately 10 and 55% of the tail beat
cycle. The average duration of the tail beat cycle, as determined by onset of
red axial myomere activity, was 0.47 s (N=16). Mean tail height was
generally between 4.6 and 4.9 cm from the dorsal tip to the ventral tip of the
tail. Low amplitude, sustained ipsilateral activity of the supracarinalis
(SC), hypochordal longitudinalis (HL), flexor dorsalis (FD) and infracarinalis
(IC) muscles occurred throughout the nominal flexion of the tail. Only two
fish exhibited interradialis (IR) muscle activity at this speed. The IR6
muscle was active at a different proportion of the tail beat cycle for each of
the five sequences in which it was active. Out of phase muscle activity by the
left IR12 that occurred in the first 15% of the tail beat occurred during four
sequences from the same fish at 0.5 L s–1; no other
fish demonstrated this muscle activity and it was most likely a result of the
electrode initially being inserted too deeply and contacting the right IR12
but later being pulled during swimming into the left IR12, where placement was
confirmed post-mortem.
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Muscle activity duration and burst intensity changed with increasing speed; however, the relative time of onset of muscle activity showed no relationship with swimming speed (Fig. 6). The duration of muscle activity decreased with increasing swim speed from 0.5 L s–1 to 1.2 L s–1, decreasing by 50–70% in the cases of the red myomere, HL, FD, SC, IC and LS muscles. However, none of the muscles, with the exception of IR3, had a significant change in muscle activity duration when swimming speed was increased from 1.2 L s–1 to 2.0 L s–1. Thus, muscles were active for a greater proportion of the tail beat cycle at 2.0 L s–1. There was no significant difference in relative time of muscle onset among swimming speeds. Increasing swimming speed resulted in increases of 50–100% of muscle burst intensity. In particular, the burst intensity of the HL, FD, FV, SC, IC and IR9 increased significantly with each speed transition. Analysis of variance determined that muscle activity duration and burst intensity were significantly different amongst all speeds and muscles (F0.05(1),35,536=1.42, P<0.001).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Videler, 1975;
Winterbottom, 1974); however,
they differ greatly in both morphology and function. The posterior vertebral
processes and the uroneural and hypural bony elements in the tail are modified
into broad, laterally compressed plates from which the intrinsic caudal
muscles originate (Lauder,
1989; Lauder,
2000; Lauder and Liem,
1983; Liem, 1970;
Nag, 1967;
Videler, 1975;
Winterbottom, 1974).
Posteriorly, the fin rays, or lepidotrichia, rest on the distal edge of the
uroneurals and hypurals and form the flexible caudal foil. The lepidotrichia
are modified scale rows (Eaton,
1945; Videler,
1975) deep to the intrinsic musculature that inserts onto the rays
and controls their movement. Fish fin rays possess a remarkable bilaminar
structure that permits musculature attachment to the two heads of the half
rays (termed hemitrichs) to actively control the curvature of the fin rays
(Alben et al., 2007;
Geerlink and Videler, 1987;
Lauder et al., 2006). Control
of caudal fin curvature and stiffness thus could be accomplished by activity
of intrinsic tail muscles. Low amplitude thrust forces could also be generated
by alternating activation of intrinsic tail muscles, causing the caudal fin
rays to oscillate at low speeds where there is no active body undulation.
Lateral flexion of fin rays is controlled through the relatively large hypochordal longitudinalis (HL), flexor dorsalis (FD) and flexor ventralis (FV) muscles. Collectively, these muscles insert onto the lateral aspects of all the fin rays; in the case of the four dorsal-most fin rays, both the HL and FD cause lateral flexion. The supracarinalis posterior (SC) and infracarinalis posterior (IC) muscles, in conjunction with the FD and FV muscles, are primarily responsible for the dorsoventral abduction of fin rays from the midline. Adduction of the fin rays towards the midline is accomplished by the interradialis muscles.
Speed effects on intrinsic tail muscle recruitment
Intrinsic caudal fin muscles are active from the very beginning of
undulatory locomotion and even, intermittently, at speeds associated with
paired fin locomotion (Drucker and Lauder,
1999; Gibb et al.,
1994) where the body does not undergo rhythmic oscillatory
patterns. Even at slow speeds between 0.5 and 1.2 L
s–1 where complex conformational changes of the tail do not
occur, some intrinsic tail muscles are active, and as speed increases all
intrinsic muscles are strongly activated. We found no intrinsic muscles that
remained inactive during steady swimming once speeds above 1.0 L
s–1 were achieved. This result indicates that of all muscle
fibers activated by the spinal cord during locomotion, the intrinsic tail
muscles, innervated by the most posterior spinal neurons, are the first to be
recruited. This recruitment occurs even prior to activation of most of the red
muscle fibers in myotomes anterior to the caudal peduncle.
The timing of intrinsic caudal muscle activity during the tail beat
corresponded with the caudal fin kinematics measured. Little to no intrinsic
caudal muscle activity was detected below 0.5 L s–1,
corresponding with the low amplitude caudal fin motion. Electrical activity
identified in the HL, FD, IC and SC muscles at 0.5 L
s–1, which co-occurred with minimally noticeable effect on
tail fin kinematics, may act instead to stiffen the tail; as bluegill sunfish
generally swim with only its pectoral fins at this speed
(Gibb et al., 1994;
Webb, 1973). Stiffening of the
caudal fin via low intensity activity in these intrinsic muscles may
aid in drag reduction by minimizing tail motion caused by the wake produced by
upstream median and paired fins (Tytell,
2006). Sunfish, as well as other fishes, tend to cup the dorsal
and ventral edges of their caudal fin into oncoming flow at moderate steady
swimming speeds (Bainbridge,
1963; Lauder,
2000; Tytell,
2006), an action that would be caused by activation of the HL, FD,
IC and SC muscles. The timing of the activity of these muscles was synchronous
with the caudal fin being slightly cupped to the ipsilateral side, and lateral
fin cupping is most likely caused by the activity of these intrinsic
muscles.
At higher swim speeds of 1.2 and 2.0 L s–1, more muscles are involved in complex activity patterns as tail shape modulation increases compared with swimming at 0.5 L s–1 (Fig. 4). Muscle activity patterns at these two higher swim speeds is very similar in many regards. At both 1.2 and 2.0 L s–1, there was a great deal of contralateral overlap of muscle activity at points of maximum tail excursion. Overall, activity of all intrinsic muscles on each side of the tail showed a high degree of overlap, and only a few interradialis muscles exhibited substantial differences in activity from the other intrinsic caudal muscles. Electromyography detects electrical activity of muscles, which is not necessarily indicative of muscle contraction as muscles can also be electrically active when stretched. Simultaneous electrical activity on contralateral sides at maximum excursion may indicate preloading of the ipsilateral muscles just prior to their contraction, as the caudal fin changes direction and begins to move to that side. The occurrence of EMG activity during muscle lengthening secondary to contralateral activation suggests that force enhancement by pre-stretching the muscle may be used. An additional possibility is that the contralateral activity serves to stiffen the caudal fin by pulling on both hemitrichs of the caudal fin rays as the tail changes direction at maximum excursion.
Alternatively, contralateral co-activation of fin muscles may help to
increase the area of the caudal fin, thereby increasing the added mass and the
force created as a result of an acceleration reaction
(Daniel, 1984;
Denny, 1990). Contralateral
overlap of the IC and SC muscles occurred at the midpoint between points of
maximum excursion, as the caudal fin passed behind the body of the fish. The
direct result of these muscles being simultaneously active on both sides was
an increase in tail height. The minimum caudal fin height occurred at points
of maximum excursion when the transverse velocity of the tail fin is
approximately equal to zero. This is similar to what was found by Bainbridge
(Bainbridge, 1963), who also
determined that a 15% increase in tail height caused a 10% increase in surface
area of the caudal fin and a 30% increase in tail height caused a 21% increase
in surface area. The bluegill sunfish in this study had a 20% increase in
caudal fin height from slow swimming at 0.5 L s–1 to
faster swimming at 1.2 L s–1 and 2.0 L
s–1; this increase in tail height is coincident with greater
activity of the intrinsic caudal muscles and is presumably important in
maximizing surface area for thrust production.
In addition, activity of the ipsilateral FD, FV, HL, IC and SC just after
maximum excursion coincided with cupping of the dorsal and ventral tips of the
tail fin seen here and by Tytell (Tytell,
2006), demonstrating active modulation of the caudal fin during
steady swimming. The kinematic results observed are likely counteracting
passive deformation of the caudal fin by hydrodynamic forces, stiffening the
fin rays on the ipsilateral side of motion, and maximizing fin area through
the stroke to increase thrust as the caudal fin passes behind the fish. If so,
this could reduce momentum lost at the tail tip, increasing the efficiency
E of the caudal fin to 90%
(Tytell, 2006).
Intrinsic caudal fin muscles also underwent a change in duty cycle with
increasing swimming speed (Fig.
6), in contrast to axial body muscles which generally show no
change in duty cycle with increasing speed
(Coughlin, 2000;
Jayne and Lauder, 1995a;
Shadwick et al., 1998). There
was no change in the absolute duration of muscle activity at 1.2 and 2.0
L s–1 but both the amplitude and duration of the
tail beat itself decreased with increasing swimming speed. This means that for
a single tail beat, muscles are active for a longer proportion of the tail
beat at 2.0 L s–1 than at 1.2 L
s–1. As a result of increased muscle activity duration, more
muscles are active at the same time, possibly acting synergistically,
increasing force production and, potentially, power output and tail
stiffness.
Muscle and fiber type recruitment
The increase in EMG burst intensity with increasing swim speed suggests
that a greater number of muscle fibers, perhaps even of different fiber types,
are active at higher speeds. Fish muscles are composed of fibers of different
metabolic types and these muscle fibers are activated at different swimming
speeds (Bone, 1978;
Coughlin and Rome, 1996;
Jayne and Lauder, 1995b;
Rome et al., 1988;
Rome et al., 1993;
Syme, 2006). Although a great
deal of research has been conducted on myotomal muscle fiber development,
anatomy and function, only one study, to our knowledge, has characterized
fiber types in intrinsic caudal fin and posterior caudal peduncular muscles
(Nag, 1972).
Nag (Nag, 1972) studied
rainbow trout (Salmo gairdneri) and showed that intrinsic caudal
muscles such as the superficial and deep flexor dorsalis and ventralis,
hypochordal longitudinalis, and interradialis muscles all possess both red and
white muscle fibers. He made no mention of any spatial segregation of fiber
types within these muscles, and so we believe that each of these individual
muscles in bluegill most likely has a mixed fiber population more
characteristic of mammalian muscle than the spatially segregated fiber type
distribution characteristic of myotomal musculature. Nag
(Nag, 1972) did note that the
caudal peduncle in rainbow trout possessed nearly 13% red fibers by weight, an
amount approximately 13 times greater than that of anterior body myotomes.
This is consistent with our recordings of activity in a number of regions in
the caudal peduncle, and with the onset of electrical activity even at rather
low swimming speeds when there is effectively no anterior body oscillation and
only minor movement of the tail. In particular, the lateralis superficialis
muscle (LS), which is often presumed to be composed of only white muscle, may
in fact also contain considerable numbers of red muscle fibers, as is
evidenced by its activity at slow swimming speeds (Figs
3,
4). Fiber type proportions and
distribution within the caudal peduncle and intrinsic caudal fin musculature
could certainly be different between rainbow trout and bluegill sunfish, but
Nag's (Nag, 1972) study
provides the only current data on fiber type anatomy in the caudal region of
fishes.
The relative proportions of slow-oxidative (red) and fast-glycolytic
(white) muscle fibers increases from anterior to posterior in many fishes
(Nag, 1972;
Patruno et al., 1998). During
larval development, the superficial monolayer of presumptive red muscle tissue
in the caudal region develops independently of the deep muscle layers of the
body, and is the only muscle layer found in some caudal myomeres
(Nag and Nursall, 1972;
Patruno et al., 1998).
Just as the relative composition of red and white muscle fibers in the
axial body musculature is different than that of the posteriormost caudal
regions, the increase in intensity of muscle activity with increasing speed
illustrates a pattern of intrinsic caudal muscle fiber type recruitment that
appears to be different from that reported in axial body musculature. Jayne
and Lauder (Jayne and Lauder,
1994) proposed a model of axial body muscle activity (based on
data from bluegill sunfish) in which red muscle activity predominated at slow
speeds, then both red and white muscle activity increased moderately as speed
increases, and finally red muscle activity decreases until white muscle fibers
are the dominant active fibers. The data in our study suggest, but not
conclusively so, that in the intrinsic caudal musculature, both red and white
muscle fibers are active at slower swimming speeds and continue to increase in
intensity to 2.0 L s–1, the fastest speed at which
fish could consistently swim steadily (Fig.
6). Intrinsic caudal muscles are activated with the onset of the
slowest undulatory swimming speeds, and in some cases intermittent activity is
seen (Figs 2,
3) even before body undulation
begins and myotomal red fibers are active. We interpret this activity as
functioning to stiffen the tail to minimize drag and tail flutter during
pectoral fin locomotion. Although we cannot determine if specific red or white
fibers within a muscle are active or not at each speed from our current data
and the presumed mixed fiber population within each tail muscle, the intrinsic
caudal muscles are certainly exhibiting patterns independent of, and different
from, those described in the axial myomeres from which they are derived
(Gemballa, 2004;
Patruno et al., 1998;
Videler, 1975;
Winterbottom, 1974).
Prospects
This study addressed four specific issues. First, we documented activation
of intrinsic tail muscles during steady locomotion, and showed that intrinsic
tail muscles are active at all steady swimming speeds. Second, these muscles
become active with, and in some cases prior to, the slowest undulatory
swimming speeds and maintain activity, which increases in intensity as speed
increases. Third, the intrinsic muscles as a group show considerable overlap
in activity pattern which suggests that a major feature of intrinsic tail
muscles during steady swimming is to stiffen the tail against hydrodynamic
loads, perhaps using the bilaminar fin ray mechanism, and to alter tail area
rhythmically during lateral caudal oscillation. Fourth, our data suggest that
intrinsic caudal musculature may be recruited in a different pattern than that
observed for myotomal muscle red and white fibers. Activity in the most
posterior muscles in the fish body innervated by the most distal spinal nerves
is the first to occur as swimming speed increases. This indicates that at
least at the slowest swimming speeds, undulatory locomotion is powered by
posterior musculature, and not by anterior myotomal muscles where strains
during slow swimming approach zero (Jayne
and Lauder, 1995b).
The experiments described here focused on steady swimming, but of equal
interest is the possible role of intrinsic tail musculature in maneuvering
locomotion. This paper also does not address the fiber type distribution
within intrinsic tail muscles in fishes, about which adequate data are not
currently available. Also of considerable further interest is understanding
the central spinal connections and projections to the intrinsic musculature of
the caudal fin. How do spinal motor neurons that drive intrinsic caudal
muscles connect centrally, and how do these connections compare with central
myotomal projections from red and white fibers
(Liu and Westerfield, 1988;
McLean et al., 2007)? There is
currently very little information on intrinsic caudal muscle physiology and
neuroanatomy in fishes, and yet progress in this area is of considerable
importance for understanding the diversity of caudal fin morphology and
control in fishes, and the recruitment of muscle to power swimming.
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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