Kinematics of the transition between aquatic and terrestrial locomotion in the newt Taricha torosa
Department of Biology, Box 7325, Wake Forest University, Winston-Salem, NC 27109, USA
* Author for correspondence (e-mail: rossma{at}wfu.edu)
Accepted 27 October 2003
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: newt, salamander, Taricha torosa, kinematics, terrestrial locomotion, aquatic locomotion
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
However, in the past 15 years, evidence has emerged that challenges this
view. Edwards (1989) points
out that bottom-dwelling antennariid anglerfishes use their paired pectoral
and pelvic fins to traverse the substrate in a manner analogous to limbs. The
fins of these animals are fleshy and outwardly resemble limbs. Antennariids
even switch between two recognizable tetrapod gaits: the lateral sequence walk
and the transverse gallop (albeit at extremely low speeds;
Edwards, 1989
). Although the
antennariids are fully aquatic and not closely related to the evolutionary
line that gave rise to tetrapods, the submerged gaits are nonetheless
demonstrative of the usefulness of limbs (or limb-like structures) for certain
types of underwater locomotion.
More compelling to a re-thinking of the evolution of the tetrapod limb is
evidence from recent fossil finds, indicating that the appearance of limbs
pre-dates the move onto land (Clack,
2002a,b
).
For instance, Acanthostega, one of the earliest described tetrapods
from the Upper Devonian, has been reconstructed as possessing fully developed
tetrapod limbs but also equipped with fish-like internal gills in an opercular
chamber (Coates and Clack,
1991
). The later-occurring Pederpes (Early Carboniferous)
retains evidence of a lateral line system in the skull, suggesting aquatic
activity, while also possessing limbs resembling those of late Carboniferous
forms thought to be primarily terrestrial (Clack,
2002a
,b
).
Previous studies of limbed locomotion in vertebrates have examined
primarily terrestrial movements (e.g.
Hildebrand, 1985) and
discussed adaptations of particular groups to different modes of locomotion
(e.g. cursorial versus fossorial animals). However, if tetrapod limb
structure indeed evolved in an aquatic environment, then the original function
of the tetrapod limb was to facilitate underwater, not terrestrial,
locomotion. While we have an excellent understanding of aquatic locomotion
via axial propulsion (e.g. Gillis,
1997
,
1998b
;
Hammond et al., 1998
; Jayne
and Lauder, 1994
,
1995
;
Long et al., 1996
), studies of
limb use during aquatic locomotion are few. The existing studies on limb use
in water have examined turtles (Pace et
al., 2001
), toads (Gillis and
Biewener, 2000
) and ducks
(Biewener and Corning, 2001
);
all of these taxa depart significantly from the plesiomorphic tetrapod body
plan. The study of the function of tetrapod limbs in providing aquatic
propulsion is thus of fundamental importance in enhancing our understanding of
the evolution of a major mode of vertebrate locomotion.
While it would be ideal to examine underwater locomotion in primitive
tetrapods, no such species are available to us. Among extant vertebrate
groups, the closest analog to the movement pattern of the earliest tetrapods
is found in the salamanders (Edwards,
1989). Salamanders resemble early tetrapods in general body form,
and salamander morphology has remained essentially unchanged for at least 150
million years (Gao and Shubin,
2001
). Workers in the field of neural circuit modeling have used
salamanders as a surrogate for primitive tetrapods in their endeavors to model
the control of locomotor movements (Ijspeert,
2000
,
2001
). Indeed, Ijspeert
(2001
) has shown that
movements matching the traveling axial waves of swimming and the standing
waves of trotting can be produced by a simple neuronal circuit in the
salamander model and that the switch between these gaits in the model can
likewise be generated by minor changes in the circuit.
Many adult salamanders spend a large proportion of their lives near or in
water (Duellman and Trueb,
1986), and thus their limbs must be able to carry out both aquatic
and terrestrial locomotion effectively. Previous research on salamander
locomotion has tended to focus almost exclusively on terrestrial locomotion
(e.g. Ashley-Ross,
1994a
,b
,
1995
;
Barclay, 1946
;
Daan and Belterman, 1968
;
Edwards, 1977
). Aquatic
locomotion in salamanders has been studied only in reference to the axial
musculoskeletal system (Frolich and
Biewener, 1992
; Gillis,
1997
). Few studies have explicitly dealt with how the same
locomotor structures are used in different environments
(Carrier, 1993
;
Ellerby et al., 2001
; Gillis
1998a
,
2000
;
Gillis and Blob, 2001
) or how
larval and adult structures function in the same (terrestrial) environment
(Ashley-Ross, 1994b
).
In the present study, we quantify the kinematics of the transition between terrestrial walking and aquatic locomotion (submerged walking and/or swimming). We demonstrate that limb and body movement patterns differ with successive strides during the transition and that kinematics differ according to the direction of the transition.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Video recording
Newts were videotaped walking both up and down an acrylic ramp, positioned
with its lower half submerged in water
(Fig. 1). The ramp was set at
an angle of 15° to the horizontal by supporting one end with a solid
block. The surface of the ramp was covered by adhesive plastic panels with a
rough texture, to provide secure footing for the newts, and marked with a
series of dots spaced 1 cm apart. A vertical 1 cm grid was also placed next to
the ramp to allow calibration of lateral images.
|
Two JVC GR-DVL9800 digital camcorders, one placed above the tank to afford a dorsal view and one placed in front of the tank to capture a lateral view, were tilted so that they were aligned perpendicular to the ramp surface and ramp long axis, respectively. Both cameras captured images at a rate of 60 fields s1. Video records from the two cameras were synchronized by a discrete event visible in both the dorsal and lateral views.
Video analysis
Only sequences in which the newt showed continuous, steady-speed motion
were selected for analysis. Sequences where the animal paused or stopped
between successive strides were not used. Five sequences in each direction
(ramp-to-water and water-to-ramp) were obtained from each animal. Video
recordings were captured using Adobe Premiere 6.5 (Adobe Systems, Inc., San
Jose, CA, USA) into a Macintosh computer. Video files were exported as
sequences of TIFF files. DeBabelizer Pro 5 (Equilibrium Technologies, San
Rafael, CA, USA) was used to de-interlace the two fields of each frame and
convert the images to JPEG format. The custom video analysis program Didge
(written by Alistair Cullum of Creighton University and available for download
at
http://biology.creighton.edu/faculty/cullum/Didge/)
was used to determine the (x, y) coordinates for anatomical landmarks
(see below). Sequences of images from the dorsal and lateral views were
digitized independently. From both views, the following points were digitized:
the tip of the snout, the vertebral column midway between the shoulder joints,
the vertebral column midway between the limb girdles, the vertebral column
midway between the hip joints, and the limbs nearest the front tank wall: the
shoulder, elbow, wrist, hip, knee and ankle joints. Additionally, the joints
of the limbs on the side of the newt away from the lateral camera were
digitized in the dorsal view. Artificial marker points were not used in this
study due to practical reasons: painted or glued-on markers simply float away
when the animal is in the water. Tests in which the same sequence of images
was digitized multiple times showed that the anatomic landmarks we chose could
be located accurately.
To reduce digitizing error, the raw coordinates were smoothed by Gaussian filtering in Igor Pro 3.16 (WaveMetrics, Lake Oswego, OR, USA). The smoothed coordinates were then imported into Microsoft Excel (Microsoft Corp., Redmond, WA, USA), which was used to compute the angle variables defined below. For two-dimensional angles, only the coordinates from the dorsal view were used. For three-dimensional angles, the vertical coordinates from the lateral view were used as the z-coordinates. True three-dimensional angles were computed by Maple 6 (Maplesoft, Waterloo, Ontario, Canada). The curves produced by plotting these angle values for each sequence (the `kinematic profile') were smoothed once more in Igor Pro; the smoothed kinematic profiles were then used for determination of minimum and maximum values for each kinematic variable (defined below).
Definition of variables
A `stride' was defined as the time (in s) from foot contact with the ramp
surface to the subsequent contact of the same foot; the left hindfoot was used
as the reference in all analyses. The time during the stride in which the foot
is in contact with the substrate is termed the `stance phase' or `duty
factor', while the time that the foot is elevated and being moved into
position for the start of the next stride is termed the `swing phase'.
Hildebrand-style footfall diagrams (Hildebrand,
1966,
1976
) were generated by
plotting duty factors as a percentage of the stride duration.
The following angles were measured in two dimensions: `pectoral girdle angle' was defined as the angle between the line connecting the shoulder joints (`pectoral girdle line') and the direction of travel (taken as the line connecting the points on the vertebral column at the pectoral and pelvic girdles). `Pelvic girdle angle' was defined as the angle between the line connecting the hip joints (`pelvic girdle line') and the direction of travel. `Trunk angle' was defined as the angle between the lines connecting the point over the vertebral column midway along the trunk to the points centered over the limb girdles. `Pectoral girdlehumerus angle' was measured between the pectoral girdle line and the line connecting the shoulder joint and the elbow. `Pelvic girdlefemur angle' was measured between the pelvic girdle line and the line connecting the hip joint and the knee. These angles were 180° when the humerus/femur was in line with its respective girdle line, less than 180° when the humerus/femur was inclined forward of that line (protracted) and greater than 180° when inclined back of that line (retracted).
The following angles were measured in three dimensions:
`humerusforearm angle' was measured between the line segments
connecting the shoulder to elbow joint (`humerus line') and the elbow to wrist
joint (`forearm line'). `Femurcrus angle' was measured between the line
segments connecting the hip to knee joint (`femur line') and the knee to ankle
joint (`crus line'). Finally, `humerusramp angle', `forearmramp
angle', `emurramp angle' and `crusramp angle' were defined as
the angles between the appropriate limb segment lines and the ramp surface. In
computing three-dimensional angles, Maple 6 is sensitive to the orientation of
the line segment with respect to the reference plane. If the first point
defining the line segment has a higher z-coordinate than the second
point, the returned value is between 0° and 90°; however, if the
second point has a higher z-coordinate than the first, the returned
value is between 360° and 270°. The latter condition (second point
higher than the first) often occurs in the distal limb segments, and we
therefore transformed those values to center around 180° so as to
facilitate comparisons with other accounts of salamander walking (e.g.
Ashley-Ross, 1994a).
Several timing variables were also measured: the durations of contact of the various feet, and the relative timing between the beginning of the stride and the minima and maxima of the angular variables described above. Dividing by the stride cycle duration standardized the timing variables. Each variable is therefore expressed as a percentage of stride.
Because each stride may have differing relative proportions of stance and
swing phase, the variables were further normalized by converting them into the
corresponding values for a standardized stride consisting of 75% stance and
25% swing. This conversion was done following the formula described in
Ashley-Ross (1995). The
standardized strides were then used to generate mean kinematic profiles for
the angular variables. Briefly, a custom-written macro routine in Igor Pro
sorted each standardized stride into 25 bins, each accounting for 4% of the
stride. The values of a given variable within each bin were averaged over all
strides, and, for graphical purposes, the time (percent stride) associated
with that value was taken to be the midpoint of the bin.
Statistical analysis
Direction of travel (up or down) and kinematics for the different strides
within a sequence were analyzed for statistically significant differences in
StatView 5.0 for the Macintosh (SAS Institute, Cary, NC, USA) using
multivariate analysis of variance (MANOVA) that considered direction, stride
within sequence, and individual as the main effects. Direction and stride were
treated as fixed effects, while individual was treated as a random effect. To
avoid missing cells, the statistical analysis was conducted only on the
strides encompassing the actual transition between media (four consecutive
strides: one in which all the four limbs were out of water, one in which all
the four limbs were in water, and two during which the limbs were either
entering or leaving the water). Subsequent three-way analyses of variance
(ANOVAs) identified individual variables that differed according to effect.
Additional three-way ANOVAs tested for differences in velocity, stride length,
stride duration and duty factor. In all tests, direction was tested over the
direction x individual interaction term, stride was tested over the
stride x individual interaction, and direction x stride was tested
over the direction x stride x individual interaction. Other
effects were tested over the residual. Differences were considered significant
at =0.05; due to large numbers of comparisons being made, the
sequential Bonferroni method of Rice
(1989
) was used to establish
the corrected significance level within each table.
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
|
|
In both movement directions, velocity was highest in the water and declined on the ramp (Fig. 4C). This effect may be a result of the slope of the ramp. A second effect of the slope may be the increase in mean stride length with successive steps in the Down direction (Fig. 4B). By contrast, stride duration and length both declined initially in Up sequences but then remained relatively constant over most of the steps. However, none of the variables mentioned showed a significant effect of stride in the three-way ANOVA.
Average gait diagrams for Up and Down sequences are shown in
Fig. 5. During terrestrial
walking, Taricha uses a diagonal-couplets lateral sequence walk
[Hildebrand, 1976; the first
foot to fall after a given hindfoot is the forefoot on the same side of the
body, and the footfalls of a diagonal limb pair (LH+RF, RH+LF) are closely
spaced in time]. The duty factor averages 76% in fully terrestrial strides but
declines with the extent of submersion to a minimum of 44%
(Fig. 5;
Table 1). ANOVA revealed
significant effects of both stride and direction on duty factor
(Table 1). In addition, the
phase relationships of the limbs for Down sequences are altered in the water
such that the forefoot of the diagonal limb pair falls later in the cycle. The
reduction in the proportion of time the feet spend in the stance phase,
coupled with the phase shift, results in a different footfall sequence
underwater; newts use a gait that would be classified as a diagonal sequence
walk (Fig. 5B, leftmost two
strides). Finally, the stance phases of the limbs have a smaller degree of
overlap when the animal is in the water, leading to periods of suspension that
would be impossible for the newt when on land.
|
|
Fig. 6 shows mean kinematic profiles for the rotation of the limb girdles and overall bending of the trunk during both Down and Up sequences. In both directions of movement, the pectoral and pelvic girdle angles oscillate smoothly around 90° (perpendicular to the direction of motion) and are out of phase with each other. The trunk angle oscillates symmetrically around 180° (trunk straight). For all three variables, the angular excursions are highest when the newt is walking on the dry ramp. Angle ranges decrease, and exhibit greater variation, when the animal is submerged (Fig. 6). The reduced girdle rotation and trunk bending in water probably results from transitions to or from the use of traveling waves in the body axis.
|
Mean profiles for the angles between the limb girdles and the proximal limb segments are shown in Fig. 7. In both directions of movement, the pectoral girdlehumerus angle is greater than 180° for most of the strides, indicating that the humerus is retracted relative to the pectoral girdle. Humeral retraction coincides with pectoral girdle rotation that advances the opposite shoulder (Figs 7, 8); thus, the forelimb appears to primarily push, rather than pull, the newt forward during the stride. Maximal retraction of the humerus reaches a sharp peak in terrestrial strides, but this peak is blunted in aquatic steps, indicating a pause before protraction of the limb commences (Fig. 7). In contrast to the humerus and pectoral girdle, the femur shows protraction relative to the pelvic girdle (angle values less than 180°). Retraction of the femur occurs in synchrony with pelvic girdle rotation that advances the opposite hip, and there is a distinct pause during terrestrial strides where the femur is held directly in line with the pelvic girdle (angle=180°; Fig. 7) before further retraction occurs. The kinematic profile of the pectoral girdlehumerus angle shows a high amount of variation during the last two strides of Down sequences, while the pelvic girdlefemur angle shows greatest variation during the first two strides of Up sequences. This pattern results from the fact that the forelimbs often do not touch the ramp during the last stride of the hindlimbs in Down sequences, while the hindlimbs often do not begin stepping motions (they are still held against the body or are being brought forward to contact the ramp) until after the first stride of the forelimbs in Up sequences.
|
|
Fig. 8 illustrates the mean kinematic profiles for the three-dimensional angles between the humerus and forearm (Fig. 8, top traces) and the femur and crus (bottom traces). For both limbs, immediately after the foot is placed on the ground the joint begins to flex and continues this motion until approximately a quarter of the way through the stride. The joint then extends until the swing phase begins, during which the joint first flexes as the limb is protracted, then extends in preparation for placement of the foot for the next stride. For both Up and Down sequences, and both fore- and hindlimbs, the joints are more extended in the water and more flexed in terrestrial locomotion.
Mean profiles for the three-dimensional angles between the limb segments (humerus, femur, forearm and crus) and the ramp surface are shown in Figs 9, 10. For the proximal limb segments, variation in their angle with the ramp is enhanced in the water, although for the majority of the time the humerus and femur are depressed from horizontal (positive angle values in Fig. 9). For distal limb segments, very little time is spent with the wrist/ankle higher than the elbow/knee (values greater in Fig. 10). During Up (but not Down) sequences, than 180° the angular excursions made by the forearm and crus are smaller and the range is displaced higher in aquatic steps than in terrestrial steps (Fig. 10), indicating that the distal limb segments are making greater angles with the substrate (perhaps as a consequence of the limbs being more extended; see above).
|
|
Multivariate comparisons
MANOVA performed on the minimum and maximum angle values and the time to
minimum and maximum angles for the four strides surrounding the transition
(Ramp 2, Ramp 1, Water 1 and Water 2) revealed significant differences due to
direction, stride within sequence, individual and the direction x stride
interaction (indicating that analogous strides in Down and Up trials were, in
fact, different; Table 2).
|
Down and Up sequences differ in their kinematics in several respects. Tables 3 and 4 show the results of univariate ANOVAs performed on angular and timing variables. Few minimum/maximum angles proved significantly different due to direction (Table 3). The mean maximum humerusforearm angle is larger in Down than Up sequences (Table 5), indicating that the elbow joint is more extended when Taricha is descending the ramp (Fig. 8). The minimum humerusramp angle is less negative (indicating that the humerus is less depressed) in Up than Down trials (Table 5; Fig. 9). While not statistically significant when corrected for the number of comparisons being conducted, two additional variables showed trends towards differences due to direction (Table 3): the pectoral girdle angle range and the minimum femurcrus angle were larger in Down than Up sequences (Table 5), suggesting greater pelvic girdle rotation and less knee flexion when descending the ramp. Differences in other angular variables were not significant. The following timing variables occurred earlier in the stride in Up sequences (Figs 7, 8, 9, 10; Table 4):minimum pelvic girdlefemur angle (protraction of the femur), minimum femurramp angle, minimum forearmramp angle, maximum crusramp angle and maximum femurcrus angle (Table 5). The following timing variables occurred significantly earlier in the stride in Down sequences: minimum pectoral girdlehumerus angle, maximum humerusforearm angle, minimum femurcrus angle, minimum humerusramp angle, maximum forearmramp angle and minimum crusramp angle (Table 5). Three additional variables (maximum pectoral girdlehumerus angle, maximum pelvic girdlefemur angle and maximum humerusramp angle) approached significant differences due to direction (Table 5). Other timing variables did not differ significantly with direction (Table 4).
|
|
|
Significant effects of stride indicate kinematic differences due to the physical environment surrounding the newt. The minimum humerusforearm angle is significantly increased in water (Tables 3, 6), indicating that the elbow joint is held in a more extended position. Several other angles showed differences that approached statistical significance (Table 3). The range of motion of the pelvic girdle and the trunk are greater in terrestrial strides (Fig. 6; Table 6). The maximum humerusforearm angle is greater in the water (Fig. 8;Table 6). The humerusramp and femurramp angles show higher (less negative) values in terrestrial strides, suggesting less depression of the proximal limb segments (negative values in Fig. 9; Table 6). In the distal segments, the forearm is most abducted in the water (minimum forearmramp angle; Fig. 10; timing variables occurred significantly earlier in submerged strides: time to maximum trunk angle, and maximum pelvic girdlefemur angle (Tables 4, 6). Additionally, the time to the minimum femurramp Table 6), while the crus is most elevated on the ramp (maximum crusramp angle; Fig. 10; Table 6). The following approached significance, occurring earlier in the water (Table 6). Other timing variables showed no significant effect of stride (Table 4).
|
Few variables demonstrated significant direction angle stride effects (Tables 3, 4); in those cases, examination of mean values showed that the Water 2 stride usually exhibited the anomalous pattern leading to the significant interaction (data not shown). A significant effect of individual was found for most angular variables but few timing variables (data not shown).
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
During terrestrial strides, uphill and downhill sequences showed
differences in the stride length and duration
(Fig. 4A,B) and velocity of
movement (Fig. 4C). Uphill
strides were characterized by greater stride durations, shorter stride lengths
and slower speeds, similar to previous results
(Farley, 1997;
Irschick and Jayne, 1998
;
Hoyt et al., 2000
). Duty
factors were lower in downhill strides
(Table 1), although the values
in both directions are similar to those reported for other salamanders during
level terrestrial walking (Ashley-Ross,
1994a
; Fig. 5). In
the current study, velocities of downhill strides were significantly higher
than uphill strides (see Results); it is likely that the reduced duty factors
in Down strides result at least partially from the increased speed, as has
been reported in earlier work (Ashley-Ross,
1994b
).
In other vertebrates, the kinematics of uphill locomotion are characterized
by increased flexion of the limbs (particularly the knee joint) early in the
stance, greater extension of knee and ankle joints at the end of stance, and
increased femoral retraction (Vilensky et
al., 1994; Carlson-Kuhta et
al., 1998
; Jayne and Irschick,
1999
). Downhill locomotion shows greater extension of the limbs
and greater femoral protraction (Jayne and
Irschick, 1999
). Taricha follows the pattern seen for
other vertebrates in the relative amount of limb (elbow and knee joint)
extension (Fig. 8;
Table 5). Greater limb
extension may be a result of the higher velocities of downhill strides;
however, joint angles have been shown not to change significantly with speed
in salamanders (Ashley-Ross,
1994b
). Contrary to results from lizards, Taricha
demonstrates no significant differences in the extent of humerus/femur
protraction and retraction. It is possible that the angle of inclination used
in the present study (15°) was too small to induce the newts to alter the
extent of limb protraction and retraction [Jayne and Irschick
(1999
) used an angle of
30° for uphill and downhill trials].
Effect of environment on kinematics
Examination of the average gait diagrams in
Fig. 5 reveals a striking
difference between terrestrial and submerged strides: the duty factor declines
significantly (Table 1) with
the degree of immersion of the newt. While the pattern is true for both
directions, it is particularly evident for Down sequences; for terrestrial
strides, each foot is in contact with the ground for approximately
three-quarters of the stride duration, while for submerged strides, the period
of foot contact declines to less than half of the stride
(Fig. 5B). Furthermore, as the
newt walks underwater, the strike of each forefoot is delayed relative to the
diagonal hindfoot. The end result of the reduced duty factor and the phase
shift in the footfalls is a change in gait to a diagonal sequence walk
(Fig. 5B, leftmost two strides;
Hildebrand, 1976).
Taricha walking underwater on a level surface also shows the diagonal
sequence pattern (M.A.A.-R., unpublished data). This footfall pattern is never
seen in salamanders walking on land
(Ashley-Ross, 1994a
). Finally,
an additional novelty of underwater walking is that the buoyant support of the
water makes it possible for newts, with a sprawled posture, to reduce the
period of limb support to such an extent that there are periods of suspension
during the stride, as is seen in anglerfishes
(Edwards, 1989
) and crabs
(Martinez et al., 1998
).
The MANOVA revealed several kinematic differences between strides on land
and in the water, distinct from differences due to the direction of movement
(uphill or downhill). Smaller ranges of motion in the pelvic girdle and trunk
in submerged strides (Fig. 6) may be related to the incipient shift from standing to traveling waves in the
trunk as the animal transitions to swimming. The greater extension the elbow
joint shows in the water (Fig.
8; Tables 3,
6) is similar to results in
turtles when swimming and walking kinematics are compared
(Gillis and Blob, 2001)
although, since the turtles were swimming rather than walking underwater, such
a conclusion must be made with caution. In swimming, a more-extended limb can
function as an improved paddle; however, since the newts were walking
underwater, this is unlikely to have been a goal of the observed limb
posture.
Buoyancy when submerged is likely to have made possible the greater adduction of the proximal limb segments (Fig. 9) and the more flattened angles of the distal segments (Fig. 10). By contrast, the requirements of supporting all of the body weight on the limbs when moving out of the water necessitates the more acute angles of the distal segments (both to orient the bones to take a greater proportion of the load in compression and to raise the body off the ramp surface). The few changes in timing variables from terrestrial to underwater strides suggest that the basic pattern of movement functions well in either environment, and only small alterations in the timing of lateral flexion and the beginning of hindlimb protraction (time to maximum pelvic girdlefemur angle) are necessary. Further studies to quantify the use of the limbs while walking underwater on a level substrate are underway; comparison with transitional locomotion should clarify environmental effects on walking kinematics.
Implications for the neural control of swimming/walking transitions
Most walking salamanders typically generate standing waves in the trunk,
resulting in increased stride length (Daan
and Belterman, 1968; Frolich
and Biewener, 1992
; Carrier,
1993
; Ashley-Ross,
1994a
), although some elongate forms use traveling waves during
terrestrial locomotion, particularly at increased speed
(Daan and Belterman, 1968
). By
contrast, swimming salamanders generate a pattern of traveling waves in the
body axis, which function to propel the animal
(Frolich and Biewener, 1992
;
Gillis, 1997
) by anguilliform
locomotion, with no participation by the limbs.
Neural networks that successfully model the swimming and terrestrial
(trotting) gaits of a salamander also show a separation between locomotion
via traveling waves and standing waves/limbs (Ijspeert,
2000,
2001
). In the model, tonic
input to the central pattern generator (CPG) for the body axis alone produces
traveling waves, while tonic stimulation applied to both the axial and limb
CPGs results in standing waves plus limb oscillations
(Ijspeert, 2001
).
Our results lend support to the separation of swimming and walking patterns. In no case did we observe traveling waves in the body axis coupled with limb movements. However, the aquatic locomotor repertoire of the newt is by no means limited to only swimming; Taricha always walked into the water until fully submerged and is capable of walking underwater. Analysis of the sequence of strides in the ramp-to-water trials showed that there was a smooth, though well-defined, transition between walking and swimming (Fig. 2). Due to the support of the water, the forelimbs would typically lose contact with the ramp surface after two or three underwater strides. At this point, the hindlimbs would go through one more cycle of protraction/retraction, and the transition to traveling waves would always occur after a final push-off from the second hindlimb (see QuickTime movies referenced above). The coordination of the final hindlimb retraction with the beginning of traveling waves argues that the CPGs responsible for the swimming and walking patterns are not totally separate and may be capable of more extensive interaction than previously thought.
We have recorded kinematic patterns for the transitions between swimming and walking; the observed movements may be strongly influenced by the medium surrounding the newt and not necessarily accurate reflections of the motor output of the nervous system. Further research is needed to document the activity patterns of axial and limb muscles during transitional locomotion in order to understand the interaction between the two propulsive systems.
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Ashley-Ross, M. A. (1994a). Hind limb
kinematics during terrestrial locomotion in a salamander (Dicamptodon
tenebrosus). J. Exp. Biol.
193,255
-283.
Ashley-Ross, M. A. (1994b). Metamorphic and
speed effects on hind limb kinematics during terrestrial locomotion in the
salamander Dicamptodon tenebrosus. J. Exp. Biol.
193,285
-305.
Ashley-Ross, M. A. (1995). Patterns of hind limb motor output during walking in the salamander Dicamptodon tenebrosus, with comparisons to other tetrapods. J. Comp. Physiol. A 177,273 -285.
Barclay, O. R. (1946). The mechanics of amphibian locomotion. J. Exp. Biol. 23,177 -203.
Biewener, A. A. and Corning, W. R. (2001).
Dynamics of mallard (Anas platyrynchos) gastrocnemius function during
swimming versus terrestrial locomotion. J. Exp. Biol.
204,1745
-1756.
Biewener, A. A. and Gillis, G. B. (1999).
Dynamics of muscle function during locomotion: accommodating variable
conditions. J. Exp. Biol.
202,3387
-3396.
Campbell, N. A., Reece, J. B. and Mitchell, L. G. (1999). Biology. 5th edition. Menlo Park, CA: Benjamin/Cummings.
Carlson-Kuhta, P., Trank, T. V. and Smith, J. L.
(1998). Forms of forward quadrupedal locomotion. II. A comparison
of posture, hindlimb kinematics, and motor patterns for upslope and level
walking. J. Neurophysiol.
79,1687
-1701.
Carrier, D. R. (1993). Action of the hypaxial
muscles during walking and swimming in the salamander Dicamptodon ensatus.J. Exp. Biol. 180,75
-83.
Clack, J. A. (2002a). An early tetrapod from "Romer's Gap". Nature 418, 72-76.[CrossRef][Medline]
Clack, J. A. (2002b). Gaining Ground: the Origin and Evolution of Tetrapods. Bloomington, IN: Indiana University Press.
Coates, M. I. and Clack, J. A. (1991). Fish-like gills and breathing in the earliest known tetrapod. Nature 352,234 -236.[CrossRef]
Daan, S. and Belterman, T. (1968). Lateral bending in the locomotion of some lower tetrapods. Proc. Ned. Akad. Wetten. C71,245 -266.
Duellman, W. E. and Trueb, L. (1986). Biology of Amphibians. New York: McGraw-Hill.
Edwards, J. L. (1977). The evolution of terrestrial locomotion. In Major Patterns in Vertebrate Evolution (ed. M. K. Hecht, P. C. Goody and B. M. Hecht), pp.553 -576. New York: Plenum.
Edwards, J. L. (1989). Two perspectives on the evolution of the tetrapod limb. Am. Zool. 29,235 -254.
Ellerby, D. J., Spierts, I. L. Y. and Altringham, J. D.
(2001). Fast muscle function in the European eel (Anguilla
anguilla L.) during aquatic and terrestrial locomotion. J.
Exp. Biol. 204,2231
-2238.
Farley, C. T. (1997). Maximum speed and
mechanical power output in lizards. J. Exp. Biol.
200,2189
-2195.
Farley, C. T. and Emshwiller, M. (1996).
Efficiency of uphill locomotion in nocturnal and diurnal lizards.
J. Exp. Biol. 199,587
-592.
Fricke, H., Reinicke, O., Hofer, H. and Nachtigall, W. (1987). Locomotion of the coelacanth Latimeria chalumnae in its natural environment. Nature 329,331 -333.[CrossRef]
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.
Full, R. J. and Tullis, A. (1990). Energetics of ascent: insects on inclines. J. Exp. Biol. 149,307 -317.[Abstract]
Gao, K.-Q. and Shubin, N. H. (2001). Late Jurassic salamanders from northern China. Nature 410,574 -577.[CrossRef][Medline]
Gillis, G. B. (1997). Anguilliform locomotion
in an elongate salamander (Siren intermedia): effects of speed on
axial undulatory movements. J. Exp. Biol.
200,767
-784.
Gillis, G. B. (1998a). Environmental effects on undulatory locomotion in the American eel Anguilla rostrata: kinematics in water and on land. J. Exp. Biol. 20,949 -961.
Gillis, G. B. (1998b). Neuromuscular control of
anguilliform locomotion: patterns of red and white muscle activity during
swimming in the American eel Anguilla rostrata. J. Exp.
Biol. 201,3245
-3256.
Gillis, G. B. (2000). Patterns of white muscle
activity during terrestrial locomotion in the American eel (Anguilla
rostrata). J. Exp. Biol.
203,471
-480.
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.
Gillis, G. B. and Biewener, A. A. (2002).
Effects of surface grade on proximal hindlimb muscle strain and activation
during rat locomotion. J. Appl. Physiol.
93,1731
-1743.
Gillis, G. B. and Blob, R. W. (2001). How muscles accommodate movement in different physical environments: aquatic vs. terrestrial locomotion in vertebrates. Comp. Biochem. Physiol. A 131,61 -75.
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.
Hildebrand, M. (1966). Analysis of the symmetrical gaits of tetrapods. Fol. Biotheor. 6, 9-22.
Hildebrand, M. (1976). Analysis of tetrapod gaits: general considerations and symmetrical gaits. In Neural Control of Locomotion (ed. R. M. Herman, S. Grillner, P. S. G. Stein and D. G. Stuart), pp. 203-236. New York: Plenum Press.
Hildebrand, M. (1985). Walking and running. In Functional Vertebrate Morphology (ed. M. Hildebrand, D. Bramble, K. F. Liem and D. Wake), pp. 38-57. Cambridge, MA: Belknap Press of Harvard University Press.
Hoyt, D. F., Molinari, M., Wickler, S. J. and Cogger, E. A. (2002). Effect of trotting speed, load and incline on hindlimb stance-phase kinematics. Equine Vet. J. Suppl. 34, 330-336.
Hoyt, D. F., Wickler, S. J. and Cogger, E. A.
(2000). Time of contact and step length: the effect of limb
length, running speed, load carrying and incline. J. Exp.
Biol. 203,221
-227.
Ijspeert, A. J. (2000). A 3-D biomechanical model of the salamander. Proc. 2nd Intl. Conf. Virtual Worlds (ed. J.-C. Heudin), pp. 225-234. Heidelberg, Germany: Springer-Verlag.
Ijspeert, A. J. (2001). A connectionist central pattern generator for the aquatic and terrestrial gaits of a simulated salamander. Biol. Cyber. 84,331 -348.[CrossRef][Medline]
Irschick, D. J. and Jayne, B. C. (1998).
Effects of incline on speed, acceleration, body posture and hindlimb
kinematics in two species of lizard Callisaurus draconoides and
Uma scoparia. J. Exp. Biol.
201,273
-287.
Jayne, B. C. and Irschick, D. J. (1999).
Effects of incline and speed on the three-dimensional hindlimb kinematics of a
generalized iguanian lizard (Dipsosaurus dorsalis). J. Exp.
Biol. 202,143
-159.
Jayne, B. C. and Lauder, G. V. (1994). How swimming 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. (1995). 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]
Long, J. H., Jr, Hale, M. E., McHenry, M. J. and Westneat, M.
W. (1996). Functions of fish skin: the mechanics of steady
swimming in longnose gar Lepisosteus osseus. J. Exp.
Biol. 199,2139
-2151.
Martinez, M. M., Full, R. J. and Koehl, M. A.
(1998). Underwater punting by an intertidal crab: a novel gait
revealed by the kinematics of pedestrian locomotion in air versus water.
J. Exp. Biol. 201,2609
-2623.
Pace, C. M., Blob, R. W. and Westneat, M. W.
(2001). Comparative kinematics of the forelimb during swimming in
red-eared slider (Trachemys scripta) and spiny softshell (Apalone
spinifera) turtles. J. Exp. Biol.
204,3261
-3271.
Petranka, J. W. (1998). Salamanders of the United States and Canada. Washington, DC: Smithsonian Institution Press.
Pierotti, D. J., Roy, R. R., Gregor, R. J. and Edgerton, V. R. (1989). Electromyographic activity of cat hindlimb flexors and extensors during locomotion at varying speeds and inclines. Brain Res. 27,57 -66.
Pough, F. H., Janis, C. M. and Heiser, J. B. (2002). Vertebrate Life. 6th edition. Upper Saddle River, NJ: Prentice Hall.
Rice, W. R. (1989). Analyzing tables of statistical tests. Evolution 43,223 -225.
Swanson, S. C. and Caldwell, G. E. (2000). An integrated biomechanical analysis of high speed incline and level treadmill running. Med. Sci. Sports Exerc. 32,1146 -1155.[Medline]
Vilensky, J. A., Moore, A. M. and Libii, J. N. (1994). Squirrel monkey locomotion on an inclined treadmill: implications for the evolution of gaits. J. Human Evol. 26,375 -386.[CrossRef]
Wickler, S. J., Hoyt, D. F., Cogger, E. A. and Hirschbein, M.
H. (2000). Preferred speed and cost of transport: the effect
of incline. J. Exp. Biol.
203,2195
-2200.