|
| |
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
First published online May 2, 2008
Journal of Experimental Biology 211, 1612-1622 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.013029
The effects of viscosity on the axial motor pattern and kinematics of the African lungfish (Protopterus annectens) during lateral undulatory swimming
Department of Biological Sciences, University of Cincinnati, PO Box 210006, Cincinnati, OH 45221-0006, USA
* Author for correspondence at present address: Department of Biological Sciences, Ohio University, Irvine Hall, Athens, OH 45701, USA (e-mail: ah312505{at}ohio.edu)
Accepted 7 March 2008
 |
Summary |
|---|
 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
Key words: locomotion, lungfish, EMG, kinematics, swimming, viscosity, tetrapod evolution
|
INTRODUCTION |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
;
Gillis, 1998a;
Gillis and Blob, 2001;
Jayne, 1988), how organisms
move through transitional environments is poorly understood. Muds commonly
occur at the interface of water and land and have a wide range of viscosities
that depend on the relative concentration of substrate to water. Clay mud was
probably the first terrestrial substrate the earliest tetrapods encountered
(Clack, 2002). The increased
viscosity of substances such as mud increases the amount of work required to
overcome drag forces. Any lack of a streamlined form, such as extended
appendages, could exacerbate this problem
(Blake, 1983). Similarly,
increased speeds of swimming also increase the amount of work needed to
overcome drag forces. Consequently, just as many fishes abandon the use of
paired appendages when swimming faster
(Webb, 1984), moving through a
high-drag muddy environment may necessitate a reliance on axial
structures.
The practical difficulties of observing locomotion in substances with high
viscosity such as mud are considerable, including low visibility and impeding
respiration via gills. Unlike many other species of fish, lungfish
(Dipnoi: Sarcopterygii) are able to breathe air and they frequently encounter
mud in their natural habitat. For example, lungfish in the genus
Protopterus often encounter harsh seasonal droughts that prompt
burrowing into the increasingly viscous, muddy substrate
(Fishman et al., 1987).
Protopterus, like most modern lungfish, has morphological traits that
are secondarily derived for burrowing, including an elongate body and
diminutive paired fins that have little function in open-water locomotion.
These behavioral and morphological attributes make lungfish a well-suited
taxon for studying how environmental variation affects the locomotor function
of axial musculature. Surprisingly, axial muscle activity has not previously
been studied for the locomotion of any lungfish.
Axial motor patterns during steady undulatory swimming in water are well
documented and share many features in phylogenetically diverse ectothermic
vertebrates. Common features of swimming axial motor patterns in lamprey
(Williams et al., 1989),
sharks (Grillner, 1974),
actinopterygian fishes with diverse morphologies
(Altringham and Ellerby, 1999;
Coughlin, 2002), salamanders
(Bennett et al., 2001;
Frolich and Biewener, 1992)
and snakes (Jayne, 1988)
include a posterior propagation of activity, and at a given longitudinal
location activity is unilateral and alternates between the left and right
sides. Differences commonly occur between the speed of propagation of muscle
activity and the wave of lateral bending
(Grillner and Kashin, 1976;
Jayne, 1988;
van Leeuwen et al., 1990).
These timing differences can result in the activation of muscle fibers during
lengthening, which may stiffen the posterior regions of the organism as they
push against the water (Long and Nipper,
1996; Wardle et al.,
1995) (but see Rome et al.,
1993). In addition to varying longitudinally, the timing of muscle
activity relative to lengthening can vary among species or with changes in
swimming speed (Coughlin,
2000; Jayne and Lauder,
1995a; Syme and Shadwick,
2002). The different waveforms observed during the undulatory
swimming of vertebrates are thus a complicated consequence of how the
intrinsic stiffness of the swimmer interacts with environmental resistance
(Blight, 1977).
Environmental variation affects both the nature and the magnitude of the
forces that facilitate or resist movement, and for diverse types of locomotion
that use lateral undulation of the axial structures the stiffness of the
animal relative to the compliance of the environment is a key determinant in
the relationship between muscle activity and bending. For example, ectothermic
vertebrates use different axial motor patterns in aquatic and terrestrial
environments. In contrast to swimming, snakes undulating on land have equal
speeds of propagating muscle activity and bending that result in activity
during the shortening of muscle fibers
(Jayne, 1988). When
salamanders walk on land epaxial muscles are activated in a standing, rather
than traveling, wave pattern that results in bending the trunk towards the
side of muscle activity (Frolich and
Biewener, 1992). Unlike the terrestrial undulation of both snakes
and salamanders, when eels move on land the timing of axial muscle activity
relative to bending changes longitudinally but more muscle activity occurs
during shortening than when the eels are swimming
(Gillis, 2000). Hence, the
timing of muscle activity and bending during the terrestrial locomotion of
eels becomes more similar to that of snakes crawling on land, although the
phase relationships between muscle activity and bending are not identical to
those of snakes. For a hypothetical animal that is very flexible, a very
viscous solution may create an environment with so little compliance that it
may be nearly equivalent to when an animal pushes against certain terrestrial
substrates. However, the lack of empirical data on animal locomotion in a wide
range of viscosities presently impedes understanding of whether aquatic or
terrestrial motor patterns are most relevant for predicting axial function in
mud.
In this study, we quantified the kinematics and axial muscle activity used by the lungfish Protopterus annectens during lateral undulatory swimming in a wide range of viscosities to understand what may occur in muddy environments. Our primary objectives were (1) to describe lateral undulatory swimming in water in the lungfish and compare the data with those from other vertebrates, and (2) to test whether increased viscosity affects the kinematics and muscle activity of lungfish.
|
MATERIALS AND METHODS |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
We manipulated the viscosity of the medium by using Poly-Bore (Baroid Industrial Drilling Products, Houston, TX, USA), a partially hydrolyzed polyacrylamide polymer commonly used in offshore oil drilling. Poly-Bore was the only transparent, non-toxic material we were able to locate that created viscosities likely to approach those of mud, and the mixtures were clear enough for both lateral and ventral views of the fish. We obtained kinematic viscosities of 1 (water), 10, 100 and 1000 centi-Stokes (cSt; where 1 St is 10–4 m2 s–1) by increasing the concentration of Poly-Bore in a water solution and allowing ample time (4–6 weeks) to obtain a homogeneous mixture. Viscosity was measured with several different sizes of Otswald-style viscometers (Fisher Scientific, Hampton, NH, USA) to accommodate a wide range of viscosities.
A similarity between Poly-Bore and a wide variety of muds is that they are
shear-thinning non-Newtonian fluids, whereas some other thickening agents such
as corn starch are shear-thickening non-Newtonian fluids
(Balmforth and Provenzale,
2001). For the purpose of comparison we created a mud slurry using
a dry smectite clay mixture from a local pottery shop (Starbrick Clay,
Nelsonville, OH, USA) that was suspended in a known volume of water. By using
a rotational viscometer (Brooksfield Service Company, Stoughton, MA, USA) we
determined that a mixture with dry weight of clay equal to 31% of wet weight
of mud had a kinematic viscosity of 929 cSt, which was nearly equivalent to
our highest viscosity Poly-Bore mixture.
After we recorded 3–5 bouts of steady swimming in one viscosity, the lungfish was moved to a small tank of distilled water while the mixture in the experimental tank was filled with a mixture of a different viscosity. The total transition time to the next mixture was 20–30 min. We selected trials with average swimming speeds as similar as possible across all viscosities to reduce the confounding effects of speed. For our analyses we chose trials with steady speeds and straight trajectories, and the analyzed trials had speeds that were not significantly different among subjects and cycles. After each experiment, the lungfish were killed with an overdose of MS222 and fixed in formalin. All individuals were radiographed and dissected to confirm electrode position within the myomere and relative to a vertebra.
Kinematics
The lungfish were videotaped simultaneously from a lateral and ventral view
using a two-camera NAC HSV 500 high-speed video system operating at 250 images
s–1. We used Didge Image Digitizing Software
(Cullum, 1999) to digitize
video images at equal time intervals with at least 20 images per cycle and
50–60 points around the outline of the fish. As described in previous
studies (Jayne and Lauder,
1995a), for each digitized outline, additional software (Stereo
Measurement TV, written by Garr Updegraff, San Clemente, CA, USA;
garru{at}fea.net)
reconstructed the midline and subsequently estimated the angles of lateral
midline bending after partitioning the midline into lengths representing the
head and individual vertebrae, which were obtained from radiographs of each
individual fish (Fig. 1A).
|
Electromyography
After anesthesia, lungfish were implanted percutaneously with a total of 13
finewire (0.051 mm diameter) stainless steel bipolar electrodes (California
Finewire, Grover Beach, CA, USA). The two strands of each electrode were bound
together with cyanoacrylate glue, and approximately 0.5 mm of insulation was
scraped from the tips of the wire to construct hooks, as described previously
(Jayne, 1988). Sutures sewn
into mid-dorsal tissue and the medial fin affixed the electrode wires at each
longitudinal location, and all electrodes were glued into a single main cable
with an average diameter of approximately 1 mm. Although we did not analyze
kinematics quantitatively, the movements and behaviors of lungfish without
electrodes during preliminary experiments appeared similar to those with
electrodes.
|
EMGs were amplified 5000 times using Grass (West Warwick, RI, USA) model P511 K preamplifiers with low- and high-bandpass filter settings of 10 kHz and 30 Hz, respectively, and a 60 Hz notch filter. The analog EMGs were recorded with a TEAC XR-5000 FM data recorder using a tape speed of 9.5 cm s–1. A 100 Hz square-wave was transmitted simultaneously to both the NAC video system and the TEAC data recorder to synchronize the video and EMG data. We converted the analog signal to digital data using an ADInstruments (Colorado Springs, CO, USA) Powerlab 16 channel converter with an effective sampling rate of 8.8 kHz. The digital EMG data were filtered with a 50 Hz high-pass filter.
We used Chart 5 software (ADInstruments) to measure the onset, offset and duration (offset – onset) for each burst of muscle activity. Relative burst duration (or EMG duty factor) was calculated by dividing EMG burst duration by the cycle duration. EMG intensity was calculated by dividing the rectified integrated area of an EMG burst by its duration.
Four variables described the timing differences in absolute (lag times) or relative (phase shift) amounts of time between muscle activity and bending (β) that were either maximally convex (βmax) or maximally concave on the side of the fish with the electrode. On-β lag equaled the time of EMG onset minus the time of βmax at the same longitudinal location, and off-β lag was between the times of EMG offset and when the region was bent maximally concave. On-β shift and off-β shift were the respective lag times divided by cycle duration. Thus, values of zero correspond to muscle activity during lateral flexion (presumed muscle shortening), and negative values indicate that EMG events preceded the relevant bending at a particular location.
We used βmax to estimate the change in muscle length
relative to resting, assuming that the superficial red fibers located at the
widest part of the fish keep pace with the change in curvature of the fish
during swimming (Coughlin et al.,
1996; Jayne and Lauder,
1995b; Katz and Shadwick,
1998; Rome, 1990;
Rome and Sosnicki, 1991;
Rome et al., 1993). Muscle
length change was calculated as the percentage of the ratio of the lateral to
midline radii of curvature:
 |
Statistical analyses
Three to four cycles from each viscosity were analyzed for each individual.
We performed analyses of variance (ANOVA) for both βmax and
estimated muscle strains using data from all eight longitudinal sites. The EMG
data did not conform to a balanced experimental design for which a single
ANOVA could be used with all viscosities and all longitudinal sites. For
example, the anterior muscle sites were often inactive in lower viscosities
and in one individual, electrodes at sites 1 and 8 dislodged before the
experiments were complete (Table
1). Consequently, an ANOVA with all four viscosities was only
possible for most EMG variables for all fish in all viscosities at sites
5–7. Because EMG intensity was equal to zero when no activity was
observed, we were able to perform an ANOVA using sites 2–7. To account
for variation within and among individuals, we used three-way, mixed-model
ANOVA with viscosity (N=4) and longitudinal site (N=3) as
fixed, crossed factors, and individual (N=4) as a random factor. The
error term for the main, fixed effects was the 2-way interaction term of the
fixed and the random factor. All mean values are reported ±s.e.m.
|
RESULTS |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
). The
trunk contains 34–36 vertebrae and the tail contains 34–38
vertebrae. The lengths of the vertebrae in the trunk were nearly constant,
whereas the lengths of those in the tail decreased posteriorly
(Table 2) except for the
terminal vertebrae posterior to the last EMG (site 8). Similarly, the width of
the trunk was nearly constant, whereas the width of the tail decreased more
than 4-fold (Table 2).
|
Kinematics
Although we selected cycles of swimming with speeds as similar as possible,
the swimming speeds tended to increase with increasing viscosity
(Fig. 2A). However, this
variation in speed with viscosity was not statistically significant (2-way
ANOVA, F=0.87, d.f.=3,9, P>0.50). Cycle duration
decreased significantly with increasing viscosity
(Fig. 2B; F=5.79,
d.f.=3,9, P<0.025). The distance traveled per tail-beat
cycle increased with viscosity but the relationship was not statistically
significant (Fig. 2C;
F=2.75, d.f.=3,9, P>0.10). With increasing
viscosity, the distance from nose tip to tail tip usually decreased, and
anterior lateral displacement increased
(Fig. 3). Maximum lateral
flexion increased significantly both posteriorly and with increasing viscosity
(Fig. 4A,
Table 3). Reynolds numbers
ranged from over 40 000 in the lowest viscosity to less than 100 in the
highest viscosity (Table
2).
|
|
|
|
Motor pattern
The overall pattern of red muscle activity consisted of posteriorly
propagated, unilateral EMGs (Fig.
5) that alternated between right and left sides
(Fig. 6) at a given
longitudinal location. All individuals increased anterior muscle recruitment
with increasing viscosity (Fig.
5), and with the exception of one individual, all eight sites were
active in the highest viscosity. As viscosity increased, activity at white
muscle sites increased (Fig.
7).
|
|
|
Burst duration decreased with increasing posterior longitudinal location within one individual among sites 2–8, but no significant effects were evident even when bursts were pooled across individuals for sites 5–7. The absolute duration of EMG bursts decreased significantly with increasing viscosity (Table 3) in sites 5–7 among all individuals and sites 2–8 in one individual. Relative burst duration, or EMG duty factor, did not vary significantly with site or viscosity among individuals in sites 5–7, but it decreased significantly within the single subject with greatest site replication. The intensity of EMGs increased significantly with increased viscosity and for increasingly posterior location (Fig. 4B).
Muscle strain
The estimated muscle strain increased significantly with increasing
viscosity, and differed significantly among sites (Tables
2 and
3). The increase in strain was
greatest in sites 5 and 6, which were the sites closest to the pelvic girdle.
Although site was a significant factor overall, posterior sites increased
strain minimally compared with anterior sites
(Table 2). Muscle strain at
sites 1–5 increased 2-fold from water to the highest viscosity.
Timing of muscle activity and kinematics
The timing of EMGs relative to bending changed longitudinally in a manner
that indicated the EMGs propagated posteriorly faster than the mechanical wave
of bending (Figs 8,
9,
10). If muscle activity
corresponded to shortening of muscle tissue, then the EMG onset would be
synchronous with maximal convexity on the side of the fish with muscle
activity (Fig. 9), and
on-β phase shifts would equal zero
(Fig. 10C,D). When present,
significant differences in lag times among viscosities and among sites
generally paralleled those observed for phase shifts
(Table 3;
Fig. 10A,B). However, large
variance in cycle duration obscured some trends for lag times that were much
more evident in phase shifts. As viscosity increased, the EMG onset at several
longitudinal locations began to precede the timing of maximal convexity,
presumably indicating muscle activity during lengthening (Figs
8,
9,
10). Thus, the phase shift of
EMG onset relative to bending increased significantly
(Table 3) by both viscosity and
site (Figs 8,
9,
10) in sites 5–7 among
all four individuals, as well as sites 2–8 in one individual. Though the
interaction term was not significant (Table
3), on-β phase shifts tended to increase posteriorly with
increasing viscosity (Fig.
10C). The variation in the longitudinal extent of muscle activity
can also be observed in Fig.
7.
|
|
|
|
DISCUSSION |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
Shape, segmentation and axial bending
The anguilliform, sub-carangiform, carangiform and thunniform modes of
swimming via lateral undulations of the axial structures form a
continuum of behavioral variation that has some large scale correlations with
axial morphology (Breder, 1926;
Lindsey, 1978;
Sfakiotakis et al., 1999). At
one extreme, anguilliform swimmers undulate their entire body, creating more
than one complete wave, and they have a relatively uniform longitudinal
distribution of surface area, low values of maximal body depth divided by
total length (snakes: 3%; eels and lampreys 6–7%) and high numbers of
total (body + caudal) vertebrae (snakes 180–300; eels and lampreys
100–200) (Jayne, 1986;
Jayne, 1985;
Wardle et al., 1995;
Ward and Azizi, 2004). At the
other extreme, thunniform swimmers undulate only the posterior portion of a
narrow caudal peduncle and fin, usually with much less than one wave visible
along the length of the body. Non-anguilliform swimmers have relative high
values (20–30%) of relative body depth
(Jayne and Lauder, 1994a;
Wardle et al., 1995), and
except for the trout (Oncorhynchus mykiss), which has 61–65
total vertebrae, most other species of bony fishes (including tuna) for which
EMGs are available have from 34 to 41 total vertebrae
(Donley and Dickson, 2000;
Jayne and Lauder, 1995b;
Syme and Shadwick, 2002;
Ward and Azizi, 2004;
Webb and Johnsrude, 1988).
With a relative body depth slightly exceeding 10%
(Fig. 1B) and 68–74 total
vertebrae, the lungfish in our study are morphologically intermediate to the
classic examples of anguilliform swimmers and most sub-carangiform/carangiform
swimmers.
Although vertebral numbers among diverse taxa do tend to be correlated to
swimming mode, the functional consequences of variation in segmentation are
also mediated by body width and depth, patterns of muscle activity and the
mechanical properties of tissues within the body and of the environment that
may resist bending (Blight,
1977; Jayne, 1985;
Long, 1998;
Long et al., 1996;
Long and Nipper, 1996;
Wainwright, 1983). For
example, the larger surface area per unit length that is associated with
greater body depth will increase the resistance the animal encounters as its
body pushes against the water. Hence, for a given internal bending force when
all other factors are equal, one would expect more lateral bending with
decreased body depth (Blight,
1977). As is the case for nearly all undulatory swimmers, the
amount of lateral vertebral flexion in the lungfish was greatest in the most
posterior regions where the body is most shallow and narrow
(Fig. 4A).
The limited data available suggest that the amount of lateral vertebral
bending during steady undulatory swimming rarely approaches the maximal
capacity for in vivo lateral flexion. For example, the lateral
flexion during the steady swimming of some Centrarchid fishes is approximately
one-third that observed during escape locomotion
(Johnson et al., 1994).
Similarly, the steady swimming of lungfish in this study in water had lateral
vertebral flexion that was only one-half that of the flexion in the most
viscous solution over a large portion of the anterior body
(Fig. 4A). In addition, the
lateral flexion of the lungfish even in the most viscous solution was less
than that observed in preliminary experiments during escape responses (A.M.H.
and B.C.J., personal observation).
Longitudinal variation during steady swimming
In addition to the lungfish in this study having significant longitudinal
variation in morphology, lateral bending, muscle strain (as estimated by
bending), EMG intensity, and the phase shifts between muscle activity and
bending also varied significantly with longitudinal position. A very general
feature of non-anguilliform swimming is that EMG duty factor decreases
posteriorly (Altringham and Ellerby,
1999), but the motor pattern of the lungfish in our study more
closely resembled that of eels (Gillis,
1998b) and snakes (Jayne,
1988), in which the EMG duty factor lacks obvious longitudinal
variation.
During steady swimming, lateral bending increased posteriorly, which is a
nearly universal feature of the undulatory swimming of vertebrates including
fish swimming (reviewed in Altringham and
Ellerby, 1999; Coughlin,
2002), salamanders (Frolich
and Biewener, 1992) and snakes
(Jayne, 1988). When the
lungfish were swimming steadily in the lower viscosities, lateral flexion was
barely discernible in the anterior locations, which closely resembles the slow
steady swimming of eels (Gillis,
1998b). In addition to the strain in axial muscles increasing with
increased lateral flexion, strain also increased with increased distance from
the midline. Thus, even when vertebral flexion is large, muscle strain may be
small if the body is laterally compressed.
Another nearly universal feature of steady undulatory swimming is that
muscle strain in phylogenetically diverse anguilliform and non-anguilliform
bony fishes commonly doubles from a location near mid-body to a posterior
location, but strain in the most posterior locations rarely exceeds 10%
(Coughlin, 2002). The
posterior increase in muscle strain of lungfish swimming in water resembles
that in many other species. However, the lungfish had an unusually large
longitudinal variation in strain (nearly 4-fold), and the magnitudes of the
estimated muscle strain in the three most posterior sites were nearly twice
those reported in the most posterior locations of other bony fishes swimming
steadily in water. The large caudal strains of lungfish swimming in water
occurred despite the fact that these regions were a mere one-fifth of the
width of the trunk of the fish (Table
2).
For the slowest speeds of steady undulatory swimming, both eels
(Gillis, 1998b) and lungfish
lack detectable muscle activity in the more anterior sites. In other species
of undulatory swimmers such as snakes
(Jayne, 1988) and largemouth
bass (Jayne and Lauder,
1995a), muscle activity is present anteriorly during slow speed
sustainable swimming, but the amplitude of activity is smaller than that in
the more posterior locations. This lack of slow speed anterior muscle activity
contradicts some definitions of anguilliform swimming
(Breder, 1926;
Gray, 1953a;
Wardle et al., 1995) that
suggest the entire length of the body actively contributes to propulsion.
For effectively all studied species of undulatory swimmers, the speed of
posterior propagation of muscle activity along the length of the animal
exceeds that of lateral bending of fish (reviewed in
Altringham and Ellerby, 1999;
Coughlin, 2002), salamanders
(Frolich and Biewener, 1992)
and snakes (Jayne, 1988), with
the exception of some thunniform swimmers
(Shadwick et al., 1999).
Consequently, a progressive, posterior increase occurs between the timing of
muscle activity and lateral bending (or muscle strain). In several species the
timing of anterior muscle activity is nearly coincident with shortening of the
muscle fibers. In the most posterior location of the lungfish swimming in
water in this study, EMG onset preceded the beginning of muscle shortening by
18% of a cycle (Fig. 10C),
which is more than twice that of eels (7.5% of a cycle)
(Gillis, 1998b) but within the
range of values reported for swimming snakes (18–30%)
(Jayne, 1988) and a variety of
non-anguilliform fishes (Altringham and
Ellerby, 1999; Coughlin,
2002). Activating muscle earlier in the strain cycle can provide a
mechanism for increasing power production, or, if it is activated much earlier
relative to shortening, the activity is well-suited for stiffening the body
(Altringham et al., 1993;
Johnson et al., 1994;
Long et al., 1994;
Rome et al., 1993). Since many
of the forces most important for the propulsion of undulatory swimmers are
near the trailing edge of the animal, stiffening this region may be
particularly important for improving the transmission of propulsive
forces.
Effects of speed and environment on locomotion
Experimental manipulations of environment are scant compared with those
addressing the mechanical properties within the body of a swimming organism.
For vertebrates that laterally undulate their axial structures during
locomotion, the primary insights gained from manipulating the environment have
been from comparing swimming in water to locomotion on land. Unlike swimming,
the axial muscle activity of eels (Gillis,
2000), snakes (Jayne,
1988) and salamanders (Frolich
and Biewener, 1992) moving on land is nearly confined to when
muscle fibers shorten. In these two environments, however, some important
details of axial function differ among these taxa. On land, eels have a
significant longitudinal phase shift between the timing of muscle activity and
bending (Gillis, 2000),
whereas snakes and salamanders lack such a phase shift
(Frolich and Biewener, 1992;
Jayne, 1988). The waves of
bending and muscle activity of snakes and eels are propagated posteriorly
while moving both in water and on land, whereas salamanders on land have a
standing wave pattern of bending and muscle activity
(Frolich and Biewener, 1992).
However, lungfish swimming in increasingly viscous solutions had increasingly
greater amounts of muscle activity during lengthening rather than
shortening.
Our 1000-fold manipulation of viscosity greatly exceeded that of any
previous experimental study on the effects of viscosity for the aquatic
locomotion of animals, including a 64-fold range in viscosity for swimming
snakes (Gray, 1953b) and an
approximately 3-fold range in viscosity for swimming fishes
(Fuiman and Batty, 1997;
Johnson et al., 1998).
Although none of these previous studies of the effects of viscosity on aquatic
vertebrate locomotion determined muscle activity, some aspects of kinematics
were quantified. For example, in a solution 3.4 times more viscous than water
the maximum velocities attained by guppies during escape responses were 14%
less than those attained in water, but no statistically significant
differences were evident between water and a solution 1.6 times as viscous as
water (Johnson et al.,
1998).
Snakes swimming in water have a large increase in wave amplitude
posteriorly (Gray, 1953b;
Jayne, 1985), which is a very
general feature of the undulatory swimming of vertebrates. However, in a
solution 64 times more viscous than water the amplitude of the anterior wave
greatly exceeds that of the posterior wave, and the maximum amplitude along
the entire length of the snake is only about one-half that of the snake in
water (Gray, 1953b). Similar
to snakes, with increased viscosity the amplitude of the anterior waves of
lungfish increased. In both snakes (Gray,
1953b) and lungfish (Fig.
2C) the distance traveled per cycle decreases with increased
viscosity. Unlike snakes in the highest viscosity, the amplitude of anterior
waves in lungfish never exceeded that of posterior waves regardless of
viscosity, and the amplitude of the most posterior wave changed little with
increased viscosity (Fig. 3).
Overall, for an equivalent range of viscosities the changes in waveform for
swimming lungfish were small compared with those observed in snakes. The
different effects of increased viscosity on the waveforms of snakes and
lungfish may result from snakes being much more flexible anteriorly.
Some additional details of the undulation of snakes and eels led us to
expect that high viscosities might generate similar phase relationships
between muscle activity and bending to that of terrestrial lateral undulation.
Matching of locomotor speed to wave speed and path following are
characteristic of the type of terrestrial lateral undulation in snakes in
which the phase relationships between muscle activity and lateral bending are
constant along the length of the body and the timing of activity is concurrent
with muscle fiber shortening. Furthermore, the same trend was observed in eels
during terrestrial lateral undulation in that they tended to path-follow while
on wet packed sand (Gillis,
1998a), and the phase relationship between white muscle motor
activity and lateral bending was more similar to that of snakes on land than
to eels in water (Gillis,
2000). Whether or not such a motor pattern would occur in lungfish
in viscosities higher than we used, or indeed for any elongate vertebrate at
any viscosity higher than water, remains an open question.
The earlier onset of muscle activity relative to flexion (lower values of
on-β shift) and presumed fiber shortening observed for lungfish with
increased viscosity resembles previously described changes for increased
swimming speed of fishes. For example, with a nearly 4-fold increase in
swimming speed in the largemouth bass, on-β shift of a posterior site is
–17% of a cycle, which is 10% of a cycle earlier than for the slowest
speed (Jayne and Lauder,
1995a). With a 3-fold increase in swimming speed in the rainbow
trout, the onset of muscle activity in a posterior site may occur 25% of a
cycle before fiber shortening, which is 10% of a cycle earlier than for the
slowest speed (Coughlin,
2000). For the most posterior site of lungfish swimming in the
most viscous solution, on-β shift was –34% of a cycle and 13% of a
cycle earlier than the value for water
(Fig. 10). Thus, the magnitude
and directionality of the change in on-β shift with increased viscosity
are similar to those reported for increased speed in other species, but the
timing of muscle activity in lungfish occurs very early in the bending cycle
compared with the values reported for many other species of fish studied using
similar methods (Altringham and Ellerby,
1999). Remarkably, the offset of muscle activity in the most
posterior site in lungfish in the highest viscosity often occurred near or
slightly before the beginning of flexion towards the side having muscle
activity, indicating that muscles ceased motor activity prior to
shortening.
An undulating swimmer theoretically could coordinate its muscle activity to
compensate for the lag time between electrical activation and time to peak
twitch tension so that peak twitch force remains coincident with a key event
in the strain cycle – such as maximal stretch – even when cycle
duration changes. Using such a constant lag time to preserve the absolute time
course of some events would in turn cause a phase shift between EMG and strain
whenever cycle duration changed. However, such a situation does not appear
sufficient to explain the large phase shifts associated with increased
viscosity for the swimming lungfish as values of on-β lag in the most
viscous solution consistently had the greatest magnitude
(Fig. 10A) even though the
large variance of this variable precluded detecting a statistically
significant main effect of viscosity. For aquatic undulatory locomotion both
increased speed and increased viscosity increase the power required to
overcome drag, as well as increasing the tendency of the body to bend when it
is pushing against the fluid (Schultz and
Webb, 2002). Activating muscle earlier in the strain cycle, as was
observed in the lungfish with increased viscosity, is consistent with the
expectation of an increased role in stiffening structures or serving as a
force transmitter (Blight,
1977), and under such conditions muscle theoretically could
perform no mechanical work or even negative work. However, available data
indicate that even when the posterior muscles have considerable early activity
while lengthening, they usually produce large amounts of positive work per
cycle (Coughlin, 2000;
Hammond et al., 1998;
Rome et al., 1993). Rather
than viewing the function of fish muscle as conforming to mutually exclusive
categories of stiffeners or power producers, posterior muscle activity such as
that in the lungfish in high viscosities may provide a good example of
functioning as a stiffener (early in each cycle) while retaining substantial
power production.
The white muscle deep in the posterior region of the lungfish was commonly
active even though swimming was steady and relatively slow, and the threshold
for recruitment for the anterior white muscle was near a viscosity of 100 for
the speeds we studied. In contrast to the lungfish, the threshold for white
muscle activity in many fish in water is near the transition between rapid
steady swimming and irregular rapid tail beats associated with the burst and
coast mode of swimming (Jayne and Lauder,
1994b; Rome et al.,
1985). When eels undulate slowly on land they also have large
amounts of white muscle activity that would otherwise be absent while swimming
at a similar speed in water (Gillis,
2000). Unlike lungfish in the more viscous solutions, eels
undulating on land have more intense recruitment of white muscle anteriorly
than posteriorly (Gillis,
2000). These examples indicate how the in vivo
relationships between recruitment, force and the speed or frequency of
movement can be altered by the environment, which suggests a greater diversity
of motor pattern and control than would have been detected by only studying
steady swimming in water.
Very high viscosities may create a situation for lung fish similar to the
minimum flight speed required by aerial organisms to overcome drag
(Lighthill, 1974). Despite
repeated trials within and among subjects in the highest viscosities, the
subjects simply did not or could not swim slowly at the highest viscosity. In
the most viscous solution, the first few tail beats of the lungfish often
resulted in no forward displacement, but then when forward movement commenced
the minimal forward speeds of swimming usually exceeded those we observed for
swimming in water. The observed threshold effect may be related to the nature
of non-Newtonian fluids. When shear force is applied to a non-Newtonian fluid
such as mud, the viscosity decreases in a non-linear fashion
(Balmforth and Provenzale,
2001). Although this weakens our ability to predict the effects of
viscosity as precisely as would be ideal, our experimental fluid was also
shear-thinning (Ryan Collins, Baroid IDP Chemist, personal communication) and
so responds to shear force in a comparable manner.
In summary, moving through a viscous medium evidently cannot be considered an intermediate between aquatic and terrestrial locomotion, nor does it seem likely that neuromuscular control changes dramatically in very viscous solutions. Instead, increased viscosity dramatically amplified the timing differences between EMGs and bending that: (1) typify aquatic undulatory swimming, (2) are the most pronounced in the posterior regions of fish, and (3) occur to a greater extent with increased swimming speed. Early tetrapods seem likely to have encountered viscous mud before dealing with fully solid surfaces lacking the buoyancy provided by water. Whether mud firm enough to support body weight would elicit a more terrestrial pattern of axial muscle activity in lungfish remains unresolved but very interesting in the light of the pivotal position this taxon has in tetrapod evolution.
|
Acknowledgments |
|---|
|
References |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
Altringham, J. D. and Ellerby, D. J. (1999). Fish swimming: patterns in muscle function. J. Exp. Biol. 202,3397 -3403.[Abstract]
Altringham, J. D., Wardle, C. S. and Smith, C. I. (1993). Myotomal muscle function at different locations in the body of a swimming fish. J. Exp. Biol. 182,191 -206.[Abstract]
Arratia, G., Schultze, H.-P. and Casciotta, J. (2001). Vertebral column and associated elements in dipnoans and comparison with other fishes: development and homology. J. Morphol. 250,101 -172.[CrossRef][Medline]
Ashley-Ross, M. A. and Bechtel, B. F. (2004).
Kinematics of the transition between aquatic and terrestrial locomotion in the
newt Taricha torosa. J. Exp. Biol.
207,461
-474.
Balmforth, N. J. and Provenzale, A. (2001). Geological Fluid Mechanics. Berlin: Springer.
Bennett, W. O., Simons, R. S. and Brainerd, E. L.
(2001). Twisting and bending: the functional role of salamander
lateral hypaxial musculature during locomotion. J. Exp.
Biol. 204,1979
-1989.
Blake, R. W. (1983). Fish Locomotion. Cambridge: Cambridge University Press.
Blight, A. R. (1977). The muscular control of vertebrate swimming movements. Biol. Rev. 52,181 -218.
Breder, C. M. (1926). The locomotion of fishes. Zoologica 4,159 -297.
Clack, J. A. (2002). Gaining Ground: The Origin and Evolution of Tetrapods. Bloomington: Indiana University Press.
Coughlin, D. J. (2000). Power production during steady swimming in largemouth bass and rainbow trout. J. Exp. Biol. 203,617 -629.[Abstract]
Coughlin, D. J. (2002). Aerobic muscle function during steady swimming in fish. Fish Fish. 3, 63-78.
Coughlin, D. J., Valdes, L. and Rome, L. C. (1996). Muscle length changes during swimming in scup: sonomicrometry verifies the anatomical cine technique. J. Exp. Biol. 199,459 -463.[Abstract]
Cullum, A. (1999). Didge: Image Digitizing Software. Omaha, NE: Parthonogenetic Products, Creighton University.
Donley, J. and Dickson, K. (2000). Swimming kinematics of juvenile kawakawa tuna (Euthynnus affinis) and chub mackerel (Scomber japonicus). J. Exp. Biol. 203,3103 -3116.[Abstract]
Fishman, A. P., Pack, A. I., Delaney, R. G. and Galante, R. J. (1987). Estivation in Protopterus. In The Biology and Evolution of Lungfishes (ed. W. E. Bemis, W. W. Burggren and N. E. Kemp), pp. 163-179. New York: Alan R. Liss.
Frolich, L. M. and Biewener, A. A. (1992).
Kinematic and electromyographic analysis of the functional role of the body
axis during terrestrial and aquatic locomotion in the salamander Ambystoma
tigrinum. J. Exp. Biol. 162,107
-130.
Fuiman, L. and Batty, R. (1997). What a drag it is getting cold: partitioning the physical and physiological effects of temperature on fish swimming. J. Exp. Biol. 200,1745 -1755.[Abstract]
Gillis, G. B. (1998a). Environmental effects on undulatory locomotion in the American eel Anguilla rostrata: kinematics in water and on land. J. Exp. Biol. 201,949 -961.[Abstract]
Gillis, G. B. (1998b). Neuromuscular control of angulliform locomotion: patterns of red and white muscle activity during swimming in the American eel Anguilla rostrata. J. Exp. Biol. 201,3245 -3256.[Abstract]
Gillis, G. B. (2000). Patterns of white muscle activity during terrestrial locomotion in the American eel (Anguilla rostrata). J. Exp. Biol. 203,471 -480.[Abstract]
Gillis, G. B. and Blob, R. (2001). How muscles accomodate movement in different physical environments: aquatic vs. terrestrial locomotion in vertebrates. Comp. Biochem. Physiol. 131A,61 -75.
Gray, J. (1953a). The locomotion of fishes. In Essays in Marine Biology (ed. S. M. Marshall and A. P. Orr), pp. 1-16. London: Oliver and Boyd.
Gray, J. (1953b). Undulatory propulsion. Q. J. Microsc. Sci. 94,551 -578.
Grillner, S. (1974). On the generation of locomotion in the spinal dogfish. Exp. Brain Res. 20,459 -470.[Medline]
Grillner, S. and Kashin, S. (1976). On the generation and performance of swimming in fish. In Neural Control of Locomotion (ed. R. M. Herman, S. Grillner, P. S. G. Stein and D. G. Stuart), pp. 181-201. New York: Plenum Press.
Hammond, L., Altringham, J. D. and Wardle, C. S. (1998). Myotomal slow muscle function of rainbow trout Oncorhynchus mykiss during steady swimming. J. Exp. Biol. 201,1659 -1671.[Abstract]
Jayne, B. C. (1985). Swimming in constricting (Elaphe g. guttata) and nonconstricting (Nerodia fasciata pictiventris) colubrid snakes. Copeia 1985,195 -208.[CrossRef]
Jayne, B. C. (1986). Kinematics of terrestrial snake locomotion. Copeia 1986,195 -208.
Jayne, B. C. (1988). Muscular mechanisms of snake locomotion: an electromyographic study of lateral undulation of the Florida banded water snake (Nerodia fasciata) and the yellow rat snake (Elaphe obsoleta). J. Morphol. 197,159 -181.[CrossRef][Medline]
Jayne, B. C. and Lauder, G. V. (1994a). Comparative morphology of the myomeres and axial skeleton in four genera of centrarchid fishes. J. Morphol. 220,185 -205.[CrossRef]
Jayne, B. C. and Lauder, G. V. (1994b). How fish use slow and fast muscle fibers: implications for models of vertebrate muscle recruitment. J. Comp. Physiol. A 175,123 -131.[Medline]
Jayne, B. C. and Lauder, G. V. (1995a). Red muscle motor patterns during steady swimming in largemouth bass: effects of speed and correlations with axial kinematics. J. Exp. Biol. 198,1575 -1587.[Medline]
Jayne, B. C. and Lauder, G. V. (1995b). Speed effects on midline kinematics during steady undulatory swimming of largemouth bass, Micropterus salmoides. J. Exp. Biol. 198,585 -602.[Medline]
Johnson, T. P., Syme, D. A., Jayne, B. C., Lauder, G. V. and Bennett, A. F. (1994). Modeling red muscle power output during steady and unsteady swimming in largemouth bass. Am. J. Physiol. 267,R481 -R488.[Medline]
Johnson, T. P., Cullum, A. J. and Bennett, A. F. (1998). Partitioning the effects of temperature and kinematic viscosity on the c-start performance of adult fishes. J. Exp. Biol. 201,2045 -2051.[Abstract]
Katz, S. L. and Shadwick, R. E. (1998). Curvature of swimming fish midlines as an index of muscle strain suggests swimming muscle produces net positive work. J. Theor. Biol. 193,243 -256.[CrossRef][Medline]
Lighthill, J. (1974). Aerodynamic aspects of animal flight. In Swimming and Flying in Nature (ed. T. Y. T. Wu, C. J. Brokaw and C. Brennen), pp.423 -491. New York: Plenum Press.
Lindsey, C. C. (1978). Form, function, and locomotory habits in fish. In Fish Physiology. Vol.7 (ed. W. S. Hoar and D. J. Randall), pp.1 -100. New York: Academic Press.
Long, J. H. J. (1998). Muscles, elastic energy, and the dynamics of body stiffness in swimming eels. Am. Zool. 38,771 -792.
Long, J. H. J. and Nipper, K. S. (1996). The importance of body stiffness in undulatory propulsion. Am. Zool. 36,678 -694.
Long, J., McHenry, M. and Boetticher, N. (1994). Undulatory swimming: how traveling waves are produced and modulated in sunfish (Lepomis gibbosus). J. Exp. Biol. 192,129 -145.[Abstract]
Long, J. H. J., Hale, M. E., McHenry, M. J. and Westneat, M. W. (1996). Functions of fish skin: flexural stiffness and steady swimming of longnose gar Lepisosteus osseus. J. Exp. Biol. 199,2139 -2151.[Abstract]
Rome, L. C. (1990). Influence of temperature on muscle recruitment and muscle function in vivo. Am. J. Physiol. 28,R210 -R222.
Rome, L. C. and Sosnicki, A. A. (1991). Myofilament overlap in swimming carp II. Sarcomere length changes during swimming. Am. J. Physiol. 260,C289 -C296.[Medline]
Rome, L. C., Loughna, P. T. and Goldspink, G.
(1985). Temperature acclimation: improved sustained swimming
performance in carp at low temperatures. Science
228,194
-196.
Rome, L. C., Swank, D. and Corda, D. (1993).
How fish power swimming. Science
261,340
-343.
Schultz, W. W. and Webb, P. W. (2002). Power requirements of swimming: do new methods resolve old questions? Integr. Comp. Biol. 42,1018 -1025.[CrossRef]
Sfakiotakis, M., Lane, D. M. and Davies, J. B. C. (1999). Review of fish swimming modes for aquatic locomotion. IEEE J. Oceanic Eng. 24,237 -252.[CrossRef]
Shadwick, R., Katz, S., Korsmeyer, K., Knower, T. and Covell, J. (1999). Muscle dynamics in skipjack tuna: timing of red muscle shortening in relation to activation and body curvature during steady swimming. J. Exp. Biol. 202,2139 -2150.[Abstract]
Syme, D. A. and Shadwick, R. E. (2002). Effects
of longitudinal body position and swimming speed on mechanical power of deep
red muscle from skipjack tuna (Katsuwonus pelamis). J.
Exp. Biol. 205,189
-200.
van Leeuwen, J. L., Lankeet, M. J. M., Akster, H. A. and Osse, J. W. M. (1990). Function of red axial muscles of carp (Cyprinus carpio): recruitment and normalized power output during swimming in different modes. J. Zool. 220,123 -145.[CrossRef]
Wainwright, S. A. (1983). To bend a fish. In Fish Biomechanics (ed. P. W. Webb and D. Weihs), pp.68 -91. New York: Praeger Publishers.
Ward, A. B. and Azizi, E. (2004). Convergent evolution of the head retraction escape response in elongate fishes and amphibians. Zoology Jena 107,205 -217.[Medline]
Wardle, C., Videler, J. and Altringham, J. (1995). Tuning in to fish swimming waves: body form, swimming mode and muscle function. J. Exp. Biol. 198,1629 -1636.[Medline]
Webb, P. W. (1984). Form and function in fish swimming. Sci. Am. 251,72 -82.
Webb, P. W. and Johnsrude, C. L. (1988). The effect of size on the mechanical properties of the myotomal-skeletal system of rainbow trout (Salmo gairdneri). Fish Physiol. Biochem. 5,163 -171.[CrossRef]
Williams, T. L., Grillner, S., Smoljaninov, V. V., Wallen, P.,
Kashin, S. and Rossignol, S. (1989). Locomotion in lamprey
and trout: the relative timing of activation and movement. J. Exp.
Biol. 143,559
-566.
CiteULike 
Complore 
Connotea 
Del.icio.us 
Digg 
Reddit 
Technorati 
Twitter What's this?
Related articles in JEB:
This article has been cited by other articles:
|
|
 |
|
  P. C. Wainwright, R. S. Mehta, and T. E. Higham Stereotypy, flexibility and coordination: key concepts in behavioral functional morphology J. Exp. Biol., November 15, 2008; 211(22): 3523 - 3528. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Phillips HOW AFRICAN LUNGFISH SWIM THROUGH MUD J. Exp. Biol., May 15, 2008; 211(10): i - ii. [Full Text] [PDF]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
