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First published online October 19, 2007
Journal of Experimental Biology 210, 3862-3872 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.009050
Effects of perch diameter and incline on the kinematics, performance and modes of arboreal locomotion of corn snakes (Elaphe guttata)
Department of Biological Sciences, University of Cincinnati, PO Box 210006, Cincinnati, OH 45221-0006, USA
* Author for correspondence (e-mail: astleyhc{at}email.uc.edu)
Accepted 28 August 2007
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Key words: arboreal, locomotion, performance, kinematics, snake, Elaphe, grip, balance, posture, concertina, perch, diameter, incline, speed, climbing, tunnel, primates, gait
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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). The diameter
of perches has numerous and important consequences for gripping and fitting
onto the perch during locomotion, and progressively steeper inclines increase
the influence of the animal's weight parallel to the direction of forward
movement. Within vertebrates, arboreal locomotion is best studied for primates
and lizards (Cartmill, 1974;
Losos and Sinervo, 1989), in
which the effects on limb kinematics
(Higham and Jayne, 2004;
Larson and Stern, 2004;
Schmitt, 1998;
Spezzano and Jayne, 2004) and
locomotor performance (Losos and Irschick,
1996; Losos and Sinervo,
1989; Sinervo,
1991) are well known. Large diameters generally allow faster
forward locomotor speed when lizards are moving on top of the perch
(Losos and Sinervo, 1989).
Although many species of snake are arboreal and have convergently evolved
anatomical specializations for arboreal life
(Jayne, 1982;
Lillywhite, 1987;
Lillywhite and Henderson,
1993), no previous study has determined how any species of snake
moves on cylindrical surfaces that typify the branches found in arboreal
habitats.
The arboreal locomotion of snakes is interesting for several reasons. The
limbless form of snakes provides a conspicuously different body plan in which
to examine the effects of various aspects of arboreal habitat structure, with
the variation in behavior and kinematics giving insights into the general
principles underlying all arboreal locomotion. The flexible, elongate bodies
of snakes may allow them to fit onto and conform easily to different sizes of
perches and to use a wide range of postures and movements. However, such a
variety of movements will be restricted by the need to fit on branches.
Similar to primates, snakes use a frictional grip, the strength of which
depends upon the extent to which the grip encircles the perch
(Cartmill, 1974;
Cartmill, 1985). Unlike limbed
animals, whose grasp on a given diameter perch is limited by finger or arm
span, snakes can change the length of their body that encircles the perch.
This ability to modify gripping arc length may allow snakes to increase the
grip force they can apply, but increased gripping arc has the potential cost
of decreasing the number of grips due to the limited length of the snake and
increasing the lateral distance that must be moved.
Additionally, snakes commonly change modes of locomotion in response to
different physical attributes of the environment
(Jayne, 1988a;
Jayne, 1988b). For example,
snakes use concertina locomotion in the laterally restricted spaces of tunnels
(Gray, 1946;
Mosauer, 1932), which resemble
the narrow spaces available on perches. Fitting to narrow surfaces may create
many similar demands for snakes moving in tunnels and on cylindrical perches
despite differences on perches such as the curvature of the surface and
medially directed gripping forces.
Concertina locomotion can be an extremely demanding mode of locomotion and
hence is well suited for gaining insights into how environmental variation
affects organismal performance and musculoskeletal function. Snakes using
concertina locomotion in tunnels periodically form alternating lateral bends
that press against the sides of the tunnel to create a static frictional
anchor point, after which a portion of the body straightens and moves
anteriorly (Gans, 1974;
Gray, 1946;
Jayne, 1986). Overcoming both
sliding and static friction and the numerous changes in momentum during
concertina locomotion probably contribute to decreased endurance and a high
energetic cost, which is almost seven times that of terrestrial lateral
undulation of snakes and of limbed locomotion for an animal of equal mass
(Walton et al., 1990).
Decreased tunnel width reduces the endurance of snakes using concertina
locomotion (Jayne and Davis,
1991), emphasizing that narrower spaces can have important
functional consequences.
The overall goal of the present study was to determine how inclines,
spatial constraints and shapes of surfaces representative of arboreal
environmental structure affect organismal performance and the modulation of
movement. Narrow spaces potentially limit the ability of an animal to modulate
the amplitude of its propulsive movements during locomotion compared to those
that are anatomically and physiologically possible on open ground. In
addition, the narrow surfaces of both perches and tunnels led us to
hypothesize that snakes on cylindrical perches would use a form of concertina
locomotion similar to that used in tunnels. If locomotion on perches resembles
that in tunnels, then increased perch diameter would increase both cycle
duration and forward displacement per cycle with little change in forward
velocity (Jayne and Davis,
1991). Additionally, increased perch diameter would result in
fewer bends of the body that are oriented increasingly perpendicular to the
long axis of the perch. We also expected that the mean velocity would decrease
when moving up steep inclines because of the increased work needed to raise
the center of mass.
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). The snakes were
housed individually in cages (57x59x26 cm), with an incandescent
light bulb creating a temperature gradient of 27–37°C. The animals
had similar snout–vent lengths (mean SVL=106 cm, range=100–110
cm), total lengths (mean TL=125 cm, range=120–133 cm), mid-body lateral
diameters (mean=2.1 cm, range=1.95–2.25 cm) and masses (mean=421 g,
range=369–455 g). All tests were on postabsorptive animals (7 days after
feeding). White paint marks on the head and at 20 vertebrae intervals along
the mid-dorsal line of the body provided landmarks to facilitate digitizing
kinematic data from video images (Fig.
1A).
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Experimental protocol
We used perches with seven diameters (1.6, 2.9, 4.1, 5.7, 8.9, 15.9 and
21.0 cm) and tunnels with seven widths corresponding to the perch diameters
plus two mean mid-body diameters (5.6, 6.9, 8.1, 9.7, 12.9, 19.9 and 25.0 cm),
which allows similar amounts of lateral displacement. The long axes of the
perches were oriented at 0°, 45° and 90° relative to horizontal,
whereas the tunnels were all horizontal.
To provide a standardized surface with sufficient friction and greater
roughness than the underlying material, we covered all surfaces with strips of
duct tape (Nashua 394, Franklin, KY, USA) parallel to the long axis of the
perches and tunnels. The fibers in the duct tape created a grid of ridges
approximately 1.5x3.0 mm. The shorter and more prominent (
0.1 mm
high) ridge within the tape was perpendicular to the long axis of the
apparatus. To determine the ventral coefficient of static friction,
µs, we placed eight live E. guttata (including all of
the experimental animals) on a flat surface covered with duct tape and tilted
the surface uphill or downhill (three times per snake) until the stationary
snake slipped. Values of µs [tangent of the angle relative to
the horizontal when the animal slipped
(Cartmill, 1979)] did not
differ significantly between uphill and downhill trials
(F1,7=3.74, P=0.09), and the grand mean of 0.28
(N=48; s.e.m.=0.005; range 0.23–0.39) is similar to previous
values for snakes on surfaces with a large range in roughness
(Gray and Lissmann, 1950).
We placed each snake onto the perch or into the tunnel and encouraged it to
move at maximum velocity by gently tapping the snake near the tail or using
the presence of a visual target such as the dark area created by holding
cupped hands just out of reach of the snake. The snakes rested for more than
30 min between trials, with individuals performing no more than four trials
per day. The order in which perch diameters and inclines were presented was
randomized. During tests, the body temperatures of the snakes were
approximately 28°C, which is similar to the mean field active body
temperature of congenerics from a similar climate (Elaphe obsoleta)
(Brattstrom, 1965). The top of
the tunnel was covered with a sheet of Plexiglas to contain the snakes.
We videotaped each trial at 30 frames s–1 with a JVC GR-DVL-9800 (JVC, Yokohama, Japan) digital video camera positioned perpendicular to the long axis of the perches and tunnels and dorsal to the snakes. We converted the video sequences to AVI files using Adobe Premier Pro version 7 (Adobe Systems, San Jose, CA, USA) and then used MaxTRAQ software (Innovision Systems, Columbiaville, MI, USA) to perform frame-by-frame motion analysis with a minimum of 30 images at equal time intervals within each cycle. In each video image, points were digitized at all visible paint marks (Fig. 1A). Additionally, pairs of points were digitized to determine the angle of the body relative to the perch or tunnel during static contact at each crossing region (Fig. 1B). Crossing regions were defined as either where the body crossed the midline of the perch (Fig. 1B) or the portion of the snake between successive contact points with the right and left walls of the tunnel. The coordinates of crossing regions were digitized where they intersected the midline of the perch or tunnel. Angles were determined with a line tangential to the midpoint, with 0° representing parallel to the perch. If crossing regions were obscured by the perch, we estimated their location at the intersection of the perch midline and a line between the closest visible portions of the body on either side. Five cycles per visible paint mark per diameter–incline combination were digitized for each snake. The x-axis was parallel to the long axis of the perch or tunnel and the overall direction of travel, and the y-axis was perpendicular to the x-axis and in a horizontal plane (Fig. 1).
Kinematic measurements
We analyzed seven variables describing the motion of individual paint
marks, and the values for each variable were averaged across all paint marks
for each cycle. Durations of events included those of each cycle
(tcycle), the time moving per cycle
(tm) and the time of static contact per cycle
(ts) for locomotion that involved periodic stopping, where
a cycle was the interval between two successive initiations of movement. The
percentage of time in static contact (%stat) was ts
divided by tcycle. The forward displacement per cycle
(
x) was the distance moved during one cycle. Values of %stat
and x are analogous to the duty factors and stride lengths,
respectively, in limbed locomotion. The mean forward velocity per cycle
(Vx) and mean forward velocity while moving
(Vx,m) equaled x divided by
tcycle and by tm, respectively.
Within each cycle we quantified the maximum lengths of the zones of movement and static contact (Fig. 1A), denoted by subscripts of m and s, respectively. These zone lengths were expressed in terms of the anatomical length of the body of the snake (% SVL) within a zone (ls, lm) and the length of the zone along the x-axis (xs, xm).
Six variables were calculated from the crossing regions. We determined the
maximum and minimum number of simultaneous crossing regions
(Ncr,max and Ncr,min) during a cycle,
which indicates the number of potential grips, and the difference between them
(Ncr). For each crossing region over the same time
interval used to calculate Vx, we recorded its x
position and calculated its mean velocity (Vx,cr). For
concertina locomotion in tunnels, Vx,cr could not be
calculated because crossing regions completely straightened and reformed
between cycles. To describe the waveform of the lateral bending of the snakes,
we calculated the mean distance between pairs of successive crossing regions
(dcr) and the angle of the body (
cr)
midline relative to the long axis of the perch
(Fig. 1B). We also noted the
presence of helical wrapping, when the snake's body encircled 360° of the
perch between two successive visible crossing regions without changing the
direction of wrapping (Fig.
1B).
Some methods used for concertina locomotion had to be modified or could not
be used for downhill locomotion, when the snakes did not have distinct cyclic
starting and stopping. Consequently, these sequences were analyzed for the
time interval taken for the mid-body paint mark to move 5 cm. The cumulative
duration within this time interval in which the snake stopped moving was
divided by the total interval duration to give %stat. We measured
cr at the end of each time interval, but
ls, xs, lm and
xm could not be calculated for this type of continuous
movement. For the two widest tunnels, some snakes used lateral undulation,
which was analyzed in cycles defined by the maximum lateral movement of body
points.
Statistical analyses
We analyzed each variable for five cycles per combination of individual,
diameter, surface (tunnel or perch) and incline (total N=20 for all
four individuals except uphill and downhill 45° at 4.1 cm, where total
N=18 and 19, respectively), using three different, mixed-model
ANOVAs. Individual (N=4) was considered a random, crossed factor
whereas diameter, surface and incline were considered fixed, crossed factors.
The variables determined by individual paint marks or crossings were averaged
to give a single value per cycle.
Because of numerous blank cells and incomplete replication for all combinations of perch diameter and incline, we were unable to perform a single ANOVA on the entire data set. Thus, we performed one two-way ANOVA (with diameter and individual as factors) for all diameters during horizontal movement and another two-way ANOVA (with incline and individual as factors) for all perch inclines at the smallest diameter (Tables 1, 2). Neither distance per cycle nor cycle duration was analyzed in the latter ANOVA because of the lack of distinct cycles during downhill locomotion.
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To determine the effects of moving in tunnels vs on horizontal perches, we performed a three-way ANOVA (with width, individual and surface as factors). For the ANOVA, we analyzed only the smallest five tunnel widths and perch diameters because two individuals used lateral undulation in the largest two tunnel widths and another individual failed to move forward.
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Results |
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). In this
arboreal variant of concertina locomotion, each point on the snake cyclically
moved and stopped (Fig. 3B,C),
but some backwards slipping occurred on steep uphill inclines
(Fig. 3B). The initiation of
the movement and the static phases proceeded from anterior to posterior,
resulting in posteriorly shifting or expanding zones of movement and static
contact that were commonly 0.25 SVL or more
(Fig. 2A,B). On horizontal and
uphill perches, each point along the body nearly followed the path of the
points anterior to it (Fig. 2,
Fig. 4B,C).
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For the five smallest tunnel widths, snakes used concertina locomotion as
described in previous work (Jayne,
1986) (Fig. 3A). As
in arboreal concertina locomotion (Fig.
2A,B), the zones of movement and static contact in tunnels
expanded posteriorly, but unlike arboreal concertina locomotion, each point
did not follow the same path of the snake's body
(Fig. 4A). In tunnels, the
crossing regions did not persist between cycles, but rather they were
straightened and re-formed at different locations after each moving phase. In
the two widest tunnels, only one snake used concertina locomotion whereas two
others used lateral undulation with substantial backwards slipping of the
waves, although forward movement was achieved.
Performance
Increased steepness decreased the ability of snakes to move on larger
diameter perches. All four snakes were able to move forward on all seven of
the perch diameters when they were horizontal, the smallest five diameters at
downhill 45°, and the smallest three diameters vertically downhill and
45° uphill. On the vertical uphill perch, four, three, two and no snakes
climbed the diameters of 1.6, 2.9, 4.1 and 
5.7 cm, respectively. In some
of the failures, the snakes used concertina locomotion but had a net backward
movement due to slipping. The only failure to move forward in the tunnels was
a single animal that did not move in either of two largest tunnel widths.
Forward velocity (Vx) decreased significantly with increased
perch incline (Table 1,
Fig. 5D).
The locomotion in all tunnels and on all perches was relatively slow, with velocities rarely exceeding 10% SVL s–1. The most conspicuous differences in Vx were between tunnels and perches (surface factor in ANOVA), as snakes in tunnels moved as much as 12 times faster than snakes on the matching perch diameter (Table 1, Fig. 5D). Vx decreased significantly with increased perch diameter but was unaffected by tunnel width (Table 1, Fig. 5D).
Kinematics of locomotion on perches
The diameter of horizontal perches significantly affected more kinematic
variables than the incline of the smallest perch (12 of 17 vs 8 of
15) (Tables 1,
2). For concertina locomotion
on perches, tcycle usually increased with increased
diameter (Table 1,
Fig. 5A). Both
tm and ts increased significantly with
increasing diameter, but little change in %stat was evident among different
diameters (Table 1,
Fig. 5B). Diameter did not
significantly affect x
(Table 1,
Fig. 5C). Thus, the animals on
larger diameters were slower as a result of taking longer to cover roughly the
same distance per cycle. Increased incline resulted in increased
ts (Table
1) and increased %stat (Fig.
5B). Vx,m decreased with increased perch
diameter but was unaffected by incline
(Table 1). Hence, the decrease
in forward speed with increased incline was mainly associated with longer
times of static contact rather than changes in the speed while moving.
The lengths of the static zones (ls, xs) decreased significantly with increased perch diameter but were unaffected by incline (Table 1, Fig. 6B). The lengths of the moving zones (lm, xm) were not significantly affected by diameter (Table 1, Fig. 6A).
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Ncr) was constant
(Fig. 6D). The angle of the
body at the crossing regions (cr) became nearly
perpendicular to the long axis of the perch as diameter increased
(Fig. 6E,
Fig. 7), which may facilitate
gripping via ventral flexion.
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Ncr and cr were unaffected by
incline (Fig. 6D,E).
Incline had a large effect on the prevalence of helical wraps compared to diameter. For horizontal perches, 0–25% of the sequences analyzed for different diameters had helical wrapping, whereas helical wrapping occurred in 75–100% of the sequences of vertical uphill and downhill locomotion.
Kinematics of locomotion on perches vs. tunnels
For concertina locomotion on perches versus in tunnels of similar
width (smallest five widths) tcycle,
tm, and ts
(Table 1,
Fig. 5A) were all similar. The
values of %stat for the five smallest widths were significantly greater for
perches than for tunnels (Table
1, Fig. 5B). The
forward movement per cycle (x) in tunnels and the resulting
velocity while moving (Vx,m) were significantly greater than
those for perches with similar diameters
(Table 1,
Fig. 5C), and all zone lengths
except ls were significantly longer in tunnels than on
perches (Fig. 6A,B).
Both Ncr,max and Ncr were
significantly greater in tunnels (Fig.
6C,D) compared to perches of equivalent diameter. Unlike the
movement on perches, much of the body periodically straightened during
locomotion in tunnels, resulting in larger values of
Ncr for tunnels compared to perches, in addition to
significant decreases with increased tunnel width
(Table 2,
Fig. 6D). Compared to the
values for perches with equivalent diameter, dcr was
smaller (Fig. 7) and
cr was larger for tunnels
(Fig. 6E). Thus, the lateral
bends used on perches had longer wavelengths relative to their amplitudes
compared to those in equivalent width tunnels
(Fig. 7). The snakes commonly
used lateral bends resembling square waves rather than simple sinusoidal
waves, as indicated in part by many values of cr approaching
90° (Fig. 6E,
Fig. 7).
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).
Definitions of gaits relying on the presence or absence of a trait (such as a
suspended phase or not for a run vs a walk) are likely to emphasize
categorical variation, whereas categories arising from quantitative
descriptors may be quite arbitrary. Most schemes for classifying modes of
limbless locomotion have relied on the presence or absence of traits rather
than creating categories from continuous variation
(Gans, 1974;
Gray, 1946;
Jayne, 1986;
Mosauer, 1932).
Locomotor modes and performance
A key feature described previously for snake locomotion is the extent to
which snakes modify locomotor mode in response to structural features of the
environment. For example, in the presence of solid surfaces with
irregularities that provide anterio-medially directed surfaces, snakes usually
perform terrestrial lateral undulation, whereas in the presence of closely
spaced, parallel vertical surfaces, such as within the confines of a tunnel,
snakes perform concertina locomotion
(Gans, 1974;
Gray, 1946;
Jayne, 1986;
Mosauer, 1932). In terrestrial
lateral undulation, lateral bending and muscle activity are propagated
posteriorly with a constant speed (Jayne,
1988a), the body only has sliding contact with the locomotor
surface, and effectively all of the points along the length of the snake
during lateral undulation travel along the same path
(Gans, 1974;
Gray, 1946;
Jayne, 1986;
Mosauer, 1932). No previous
study of concertina locomotion in tunnels found any posterior propagation of
lateral bending, and different longitudinal locations along the length of the
snake during this mode follow different paths
(Gray, 1946;
Jayne, 1986;
Jayne, 1988b;
Jayne and Davis, 1991).
Much of the locomotion of snakes on perches that we observed did not conform simply to any previously described mode of limbless locomotion. Snakes on perches had three qualitative features resembling tunnel concertina locomotion: alternating bends to the left and right, stopping periodically, and some portion of the body always having static contact with the substrate. Two additional features did not conform to concertina locomotion within a tunnel. First, different longitudinal locations along the lengths of snakes on perches commonly followed the same path (Fig. 4B,C). Second, regions of vertebral flexion propagated posteriorly while the snake was moving (Fig. 2). Both of these features resemble terrestrial lateral undulation; however, the periodic stopping disrupts the steady posterior propagation of a particular bend, which differs from terrestrial lateral undulation. To avoid a proliferation of terms, we refer to these movements on horizontal and uphill perches as `arboreal concertina locomotion', but we emphasize this is a combination of qualitative traits equally distinct as those used previously to describe other modes of limbless locomotion..
When all points of the snake follow a single path, the entire snake can fit through an opening equal to its largest cross-sectional area, whereas other types of movement require a larger area. For example, snakes performing concertina locomotion in tunnels use a swath equal to the width of the tunnel. Consequently, if this tunnel pattern of movement were used on a perch from which branches emerge, then the branches would obstruct forward movement. By contrast, using a mode of concertina that follows a single path readily avoids such potential obstructions.
In addition to obstructions created by branches that arise from a perch,
the unobstructed space available for movement may be reduced by impinging
vegetation. Clearance within arboreal habitats has received less attention
than how fast animals move and fit onto a single perch. For example, within
arboreal lizards, occurrence on narrower perches commonly correlates with
limbs that are shorter (Williams,
1983). However, even on a narrow unobstructed cylinder,
longer-limbed species usually run faster than shorter-limbed species with
similar overall size (Irschick and Losos,
1999; Losos,
1990). Thus, an overlooked benefit of reduced limb length may be
simply to reduce the cross-sectional area needed to move along a perch in
cluttered natural arboreal environments
(Spezzano and Jayne, 2004).
Similarly, a key advantage of the limbless body plan and behaviors used by
snakes in cluttered arboreal habitats may be the small cross-sectional area
required for moving.
Although tunnel width barely affected the maximal speeds of concertina
locomotion in this and other studies
(Jayne and Davis, 1991), perch
diameter and incline had widespread effects on the locomotor performance of
the snakes in our study, as is the case for diverse limbed animals
(Delciellos and Vieira, 2006;
Huey and Hertz, 1982;
Lammers et al., 2006;
Losos and Sinervo, 1989;
Sinervo et al., 1991). One of
our most conspicuous findings was that increased incline reduced the maximum
size of the perch diameters that snakes could traverse. Even when snakes were
able to move on many different surface widths and inclines, the large
variation in the forward speeds attained while doing so created large
differences in the `performance spaces'
(Bennett, 1989;
Wainwright, 1987) that were
associated with different environments
(Fig. 5D).
Perch diameter affects the maximal speed of locomotion of both snakes and
limbed animals, but the directionality of these effects differs. The maximal
speeds of most lizards have large decreases with decreasing perch diameter
(Irschick and Losos, 1999;
Losos, 1990;
Losos and Irschick, 1996;
Sinervo, 1991), but the
effects of perch diameter and round perches versus flat surfaces for
the speeds of mammals are variable
(Delciellos and Vieira, 2006;
Lammers and Biknevicius,
2004). In lizards, kinematic changes associated with decreased
perch diameter include decreased stride length, which may contribute to
decreased maximal speed (Spezzano and
Jayne, 2004). Unlike lizards, the maximal speeds that we observed
for the arboreal concertina locomotion of snakes increased with decreased
perch diameter. When the diameter of horizontal perches decreased for snakes
performing concertina locomotion, x, which is analogous to
stride length, did not change significantly, but an increase in frequency of
movement was sufficiently large so that speed increased. Since snakes
performing arboreal concertina locomotion follow a path, a decreased perch
diameter allows snakes to travel a less circuitous route, which is also
advantageous for attaining a greater forward speed.
For both limbed and limbless animals, certain ranges of perch diameters may
have little or no consequence for locomotion. For example, the maximal speed
and several kinematic variables of some arboreal lizards change asymptotically
rather than linearly with increased perch diameters such that values for
large-diameter perches resemble those for a flat surface
(Spezzano and Jayne, 2004). As
in lizards, the smallest incremental change in maximal speed that we observed
for snakes occurred between the two largest horizontal cylinders. The maximal
speeds of some species of mammals are effectively constant across a wide range
of perch diameters, and some species also have little discernable differences
in speed between moving on cylinders and flat surfaces
(Delciellos and Vieira, 2006).
Above some threshold value of diameter, snakes could not traverse a large
range of inclined perches.
Balance and grip
In addition to coping with the laterally restricted spaces of perches,
snakes as well as limbed animals moving along the length of cylinders must
counter the tendencies to topple and to slide
(Cartmill, 1974). Problems
related to balance seem likely to explain the reduced speeds of snakes on
horizontal perches compared to in tunnels with similar width. The shape and
posture of the animal, the curvature of the cylinder, the orientation of the
long axis of the cylinder relative to gravity, and the coefficient of friction
all affect the ability of an animal to balance on a perch.
Sideways toppling is a problem for any perch that is not vertical
(Fig. 8), and pitching and
sliding down the length of the perch are problems for perches that are not
horizontal. Sideways toppling may occur for two major reasons. Without
sufficient friction between the animal and a round perch, the animal will
simply topple by sliding circumferentially on the perch unless its center of
mass (COM) is located precisely over the center of the perch
(Fig. 8B). With sufficient
friction, if the animal's COM is lateral to its most lateral point of
attachment with the perch, then it will topple by pivoting sideways unless
something is done to counteract this movement
(Fig. 8A). The tendency to
pitch backwards on inclined perches resembles that of toppling by pivoting
sideways; however, the long axis of the animal functions as an analog of the
width of support during sideways toppling
(Cartmill, 1974;
Cartmill, 1979).
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A lower COM relative to the perch (Fig.
8A) will decrease the tendencies to topple sideways and pitch
backwards (Cartmill, 1974;
Cartmill, 1985), and the
tendency to topple sideways over a pivot also can be reduced by increasing the
lateral distance (Fig. 8A) from
the COM to the pivot. However, this lateral distance, L, can be
limited by either perch diameter or anatomy. With h
L–1 approximating one for many species (where h
is the height from the COM to the pivot point when the animal is upright on a
horizontal surface), snakes have a much lower COM than limbed animals of the
same mass (Fig. 8C).
Both limbed animals and snakes have postural variation that is also
associated with maintaining balance and altering the location of COM on
perches. With increased perch diameter, the lateral extent of support,
L, commonly increases in snakes
(Fig. 7) as well as some
mammals (Cartmill, 1974) and
lizards (Spezzano and Jayne,
2004). Limbed mammals commonly adopt a more crouched posture when
moving on top of cylinders compared to flat surfaces, as well as when moving
on cylinders with smaller diameters
(Schmitt, 1999;
Schmitt, 2003). However, such
reductions in height are often small (7%), and values of h
L–1 may be as high as 30 for monkeys
(Schmitt, 2003). When values
of h L–1 are large (>10), even a substantial
reduction in h has a barely noticeable effect on toppling angle,
which illustrates some of the limitations common to limbed body plans
(Fig. 8C).
The alternating loops of snakes on cylinders had wave crests that were much
longer than in tunnels (Fig.
7), which increased the amount of the snake's body below the top
of the perch and hence lowered the COM. Snakes bridging gaps and launching
themselves to glide have large loops that position their COM below the perch
(Jayne and Riley, 2007;
Socha, 2006), and this
mechanism could also enhance stability of moving on top of perches. The only
manner in which arboreal mammals can attain this stable posture where the COM
is below the perch is to use some form of suspensory locomotion
(Cant, 1992;
Cartmill, 1985;
Fleagle and Mittermeier, 1980;
Napier, 1967). By wrapping
around inclined perches, snakes are also theoretically able to place the COM
at the center of the perch, and wrapping around perches became more common as
incline increased. This mechanism for eliminating pitching is not a
possibility for limbed animals.
Friction between the animal and the perch is directly related to both
balance and grip. As friction increases, the tendencies to topple by sliding
and to slip down an inclined perch both decrease, and the ability to grip will
increase for a given grip force. Without actively generating any gripping
force, the weight of the animal can create frictional resistance, but the
magnitude depends upon the orientation of the contact surface. The alternating
loops formed by snakes on perches crossed the top centerline of the perch,
which ensures that all of the snake's weight will contribute to the normal
force on the perch, whereas the feet of limbed animals commonly are placed
lateral to the top centerline of the perch
(Cartmill, 1974;
Spezzano and Jayne, 2004).
Both snakes and primates use frictional gripping rather than claws or
adhesion (Autumn et al., 2000;
Cartmill, 1985;
Emerson and Diehl, 1980);
therefore, generating forces normal to the locomotor surface is important in
these taxa. Increasing grip force always increases normal force. However, for
grips encircling more than 180°, grip forces also push the cylinder
towards rather than away from the surface of the animal, as would be the case
for grips encircling less than 180°. Consequently, an animal will always
be able to squeeze a cylinder harder with gripping arcs of >180° than
those <180°, assuming it has the physiological capacity to do so
(Cartmill, 1979). The opposable
thumb of primates increases the ability to encircle a perch, which can
increase gripping force and normal force
(Cartmill, 1974). Regardless of
incline, snakes commonly used gripping arcs of over 180° for all but the
largest diameters (Fig. 7), and
the tendency to completely encircle the perch with helical wraps increased
with increased incline. Thus, many aspects of the postures that we observed
for snakes involved creating opposable grips, which are most vital on steep
inclines where weight contributes little or nothing to frictional resistance
while creating a tendency to slide downwards. Another advantage of greater
encirclement of steep perches is that the gripping forces can oppose pitching
moments.
Unlike the fixed grip-span of limbed animals such as primates, we observed
an impressive capacity of snakes to modulate the length of the body used for
gripping (Fig. 7A) as well as
the number of grips (Fig. 6C).
The ventral surface of snakes, which was the primary contact surface of the
gripping regions, is extremely smooth
(Gans, 1974), whereas the
volar pads of primates have surface features and mechanical properties well
suited for maximizing friction. Unlike the locomotion of primates, for which
reduced slippage is beneficial, high friction would impede the most common
modes of snake locomotion that use sliding contact with the substrate. Thus,
the skin of arboreal snakes faces a tradeoff not found in primates.
Although snakes and primates are both highly reliant on frictional gripping and face similar demands for moving in arboreal habitats, snakes had several unique and unanticipated responses to perches with varying inclines and diameters. Overall, increased perch diameters impeded the forward speed and the ability of snakes to balance and grip. Snakes on perches used some unique modes of locomotion, including sliding down steep inclines and a form of concertina locomotion that differed significantly from that used in tunnels. Sideways toppling by pivoting poses a significant problem for primates, but snakes on perches seem more likely to topple by sliding as a result of their smooth skin and low COM. Unlike most tetrapodal vertebrates, snakes have elongate bodies that can conform readily to structures in the environment and change their distribution of mass, both of which enhance their ability to move proficiently in arboreal habitats.
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Acknowledgments |
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References |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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,
relative to vertical at which pivot toppling (A) occurs as a function of
animal shape (h L–1), where h and
L are the height and lateral distance, respectively, from the center
of mass to the pivot point when the animal is upright on a horizontal
surface.