Sweeping and striking: a kinematic study of the trunk during prey capture in three thamnophiine snakes
Committee on Evolutionary Biology, 1025 E. 57th Street, University of Chicago, Chicago, IL 60637, USA and Field Museum of Natural History, 1400 South Lake Shore Drive, Chicago, IL 60805, USA
Author for correspondence at present address: Evolution and Ecology, One Shields Avenue, University of California, Davis, CA 95616, USA (e-mail: malfaro{at}ucdavis.edu)
Accepted 2 April 2003
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Summary |
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Key words: strike, functional morphology, snake, Thamnophis, Nerodia, axial kinematics, feeding, prey capture
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Introduction |
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Lineages from most major groups of snakes have reinvaded aquatic habitats
and become piscivores. Workers have noted similarities in fishing behavior
across a diversity of snake groups, including natricines
(Alfaro, 1998;
Braun and Cundall, 1995
;
Drummond, 1983
;
Halloy and Burghardt, 1990
),
homalopsines (Jayne et al.,
1988
; Smith et al.,
1998
), elapids (Voris et al.,
1978
) and viperids (Savitzky,
1992
), the most notable being that aquatic prey are typically
captured using a lateral sweep of the head. Although Cundall and Greene
(2000
) have suggested that
fishing is a 'slow' behavior, some thamnophiines have recently been shown to
strike as quickly as terrestrial colubrids
(Alfaro, 2002
).
The North American colubrid tribe Thamnophiini (garter snakes and water
snakes) contains a number of highly specialized piscivores as well as
generalists that include fish in their diet. Specialists and generalists have
traditionally been thought to use lateral head sweeping to capture prey (e.g.
Cundall and Greene, 2000),
although recent work has shown that prey capture modes have diversified in
homalopsines (Smith et al.,
2002
) and thamnophiines
(Alfaro, 2002
). Of particular
note is the striking behavior of Thamnophis couchii, which uses a
rapid, long-distance, forward attack to capture prey and appears to adopt a
pre-strike posture (Alfaro,
2002
; Drummond,
1983
). Fast, forward striking has also evolved in at least one
other garter snake species (Alfaro,
2002
), suggesting that aquatic prey capture strategies are far
more diverse than previously recognized.
To examine the role of the trunk in aquatic prey capture and to begin to
characterize the diversity of aquatic feeding modes in thamnophiines, a
kinematic analysis of the strike in two garter snakes, Thamnophis
couchii and Thamnophis elegans, and one water snake, Nerodia
rhombifer, was undertaken. The species in this study are phylogenetically
well differentiated from one another and represent at least two and possibly
three independent evolutions of a piscivorous lifestyle
(Fig. 1). T. couchii
is an aquatic specialist on fishes and anuran larvae
(Drummond, 1983;
Rossman et al., 1996
). T.
elegans feeds on a broad range of aquatic and terrestrial prey
(Rossman et al., 1996
). N.
rhombifer is a highly aquatic species that feeds mainly on fish and
anurans (Mushinsky and Hebrard,
1977
). As is typical for the genus, N. rhombifer is
heavy-bodied compared with most garter snakes and thus provides a contrasting
morphology to the other two species in this study. Digital sequences of trunk
movement during 84 prey captures were analyzed to identify patterns associated
with aquatic feeding. Univariate and multivariate statistical comparisons of
kinematic variables were performed within and among species to determine
levels of variation of this behavior and to identify species-specific
characters of the strike.
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Materials and methods |
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Feeding trials occurred over a three-month period starting in August 1999. Animals were placed in a 113.6 l aquarium filled with water to a depth of 8 cm. One end of the arena was filled with gravel, providing a terrestrial refuge (23 cm long) for the animals. Water temperature ranged from 28°C to 30°C. To aid in locating the dorsal midline, snakes were marked with White Out® at approximately 1 cm intervals, beginning at the neck and ending at a point dorsal to the cloaca. Animals were placed in the arena at least two hours prior to the experiment to allow individuals to acclimate.
To initiate feeding trials, 15-20 fathead minnows, obtained from a local
bait store, were added to the arena. Minnows ranged in size from approximately
4 cm to 6 cm standard length, although prey were not measured individually.
Feeding bouts were recorded in dorsal view using a Sony TRV 900 digital video
camera mounted on a tripod approximately 1.5 m above the tank. Prey density
was maintained over the course addition to the position of the tip of the
snout and the center of mass of the prey item. To facilitate comparison, the
strike vector was calculated. Strike vector was defined as the vector from the
starting position of the snout to the position of maximum snout displacement
during the strike. Digitized coordinates were then rotated so that the strike
vector was parallel to the y-axis (C). Segment angle and path angle
calculations treated the body as a series of segments. Segment angle ()
was the angle between each segment and the strike vector (D). Path angle
(ß) was the angle between a vector defined by the midpoint of a segment
in successive frames and the strike vector (E). of the trial by adding minnows
after successful captures. Trials were terminated when the snake stopped
orienting to prey, typically after 4-7 successful captures. Experiments and
animal care were performed in accordance with IACUC protocols (# 70401).
Digitization and analysis
Video sequences were transferred from the camera to a Macintosh G3 450 mHz
computer via an IEEE-1394 interface (Firewire) using Adobe Premiere.
Strike sequences were edited and previewed using Premiere. Sequences that
reflected typical prey capture behaviors (subjectively assessed as being
similar to behaviors observed in the field or during preliminary trials) and
possessed high image quality and clarity of focus were exported as QuickTime
movies for image analysis. The goal of the study was to examine species-level
differences in behavior. Because qualitative observations of snake foraging
behaviors suggested that the effects of success on strike kinematics were
minor relative to differences between species, and since analysis of variances
(ANOVAs) of starting segment angle, minimum path angle and minimum segment
angle for the first three body segments revealed no significant effect of
success on strike kinematics (analyses not shown), data from successful and
unsuccessful strikes were pooled for subsequent analysis.
QuickTime movies were deinterlaced using a version of NIH Image (developed at the US National Institutes of Health and available on the internet at http://www.usm.maine.edu/~walker/software.html), customized by Jeffrey Walker. The resulting 60 Hz sequences were digitized frame-by-frame. The tip of the snout, the beginning of the neck, and points along the midline until the level of the cloaca were digitized at approximately 1-2 cm intervals. In cases where it was apparent that the snake had oriented to a particular prey item, prey position was also recorded at the prey's estimated center of mass. Snakes sometimes initiated strikes while crawling or swimming. The beginning of the strike was defined as the frame prior to the frame showing an obvious increase in head velocity. Sequences were digitized until the end of the strike, recognized by either the successful capture of the prey or the cessation of rapid forward head movement. Using QuicKurve (a custom-written PASCAL program by Jeffrey Walker, available at http://www.usm.maine.edu/~walker/software.html), a quintic spline was fit to the digitized points along the trunk (Fig. 2A). The smoothing parameter for this spline was based on the estimated error variance, which was calculated from a test series digitized three times. 100 points were interpolated along the midline spline, and coordinates for 11 equally spaced points were retained for analysis. The data set consisted of 13 points: the snout tip, 11 midline trunk points and prey position (Fig. 2B).
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Strikes typically exhibited a high degree of variability in posture and direction. To permit comparisons, strikes were standardized by the strike vector. The starting point of the snout and the point of maximum snout displacement defined this vector. A custom computer program transformed snake and prey coordinates so that the strike vector was parallel to the y-axis (Fig. 2C). These rotated coordinates were used to characterize the behavior of the head and trunk during prey capture. Throughout this paper, forward is defined as the direction that is parallel with this strike vector, and lateral is defined as the direction perpendicular to the strike vector.
To characterize the movement of the snake during the strike, I calculated
the segment angle and the path angle
(Gillis, 1997) of the 10 body
segments defined by the 11 spline coordinates, and of the head segment,
defined by the tip of the snout and the beginning of the neck
(Fig. 2D). Segment angle was
the orientation of the segment relative to the calculated strike vector. Path
angle was the angle between a line connecting the midpoints of a segment in
consecutive fields and the strike vector
(Fig. 2E). Path angle reflected
the displacement of the segment while segment angle reflected the rotation of
the segment.
Finally, head velocity and acceleration, together with the parallel and
perpendicular displacements of the 11 trunk points relative to the strike
vector, were calculated. Velocity and acceleration were calculated using the
raw data for the snout tip with QuickSand
(Walker, 1998). Using this
program, a quintic spline was fit to the snout coordinates over the course of
the strike. Calculations of velocity and acceleration were based on the
spline-fitted coordinates to mitigate against the effects of digitizing and
sampling error on parameter estimation
(Walker, 1998
). Sample rate
was potentially problematic for accurate calculation of accelerations, and
reported values should be interpreted cautiously as they may be substantial
underestimates of the truth. However, strike velocity and duration for the
thamnophiines in this study was on the same scale (all peak velocities within
an order of magnitude), so that error in estimated acceleration is expected to
be roughly equal across species. Displacements, velocities and accelerations
were standardized by head length to control for size variation in
specimens.
Statistical analyses
Slow sweeping bouts in T. elegans and N. rhombifer were
excluded from statistical analysis so that only fast prey capture behaviors
were compared among species. Residual analysis revealed that the raw data met
the necessary assumptions for parametric statistics. To determine if there was
a difference in pre-strike posture among species, a twoway ANOVA on starting
segment angle with species, body position, and body position x species
as fixed effects was performed. The effects of species and position on minimum
path and segment angle were also tested using a two-way mixed-model ANOVA. For
all ANOVAs, significant results were followed by Tukey post hoc tests
to determine specifically which levels differed from each other. Finally,
differences in strike performance were tested for with a multivariate ANOVA
(MANOVA) of standardized head velocity and acceleration using species as a
fixed effect and individuals within species as a random effect. Univariate
oneway ANOVAs were then used to explore species-level differences in velocity
and acceleration.
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Results |
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Head acceleration was high (18.1 m s-2), and individuals typically reached peak velocity (86 cm s-1) within 60 ms of strike initiation (Fig. 4). Segment angle was low in the anterior-most segments and decreased across all segments coincident with increasing velocity. Mean path angle dropped sharply in the anterior trunk as velocity increased. In the posterior half of the trunk, path angle decreased after peak velocity was attained. In addition, path angle in these posterior points continued to decrease as path angle slightly increased in the anterior points late in the strike cycle. Segment displacements in the direction of the strike were high for the first four segments. During head acceleration, the last three segments exhibited displacement away from the prey, suggesting that the posterior trunk plays a role in balancing strike forces.
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The western terrestrial garter snake Thamnophis elegans
Two main modes of prey capture, distinguishable by overall trunk kinematic
pattern and speed of the behavior, were observed in this species. Open-mouth
sweeping (Fig. 5)occurred in
all individuals. Essentially, the animal swam forward while using the anterior
one-third of its trunk to sweep the head to either side. This behavior was
usually elicited in response to rapid movement by a nearby prey item but also
followed unsuccessful forward strikes and, occasionally, was initiated without
any obvious prey stimulus.
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A diagram of segment motion based on a representative sweep (Fig. 6) shows that the five most anterior points undergo the most kinematic activity, while the posterior portion of the body largely maintains the same conformation during the bout. Head excursion is relatively slow, with peak forward velocities (velocity parallel to the calculated strike vector) generally below 33 cm s-1. Sweeping bouts were also more sustained relative to strikes, typically lasting 1-3 s. The four anterior-most segments underwent large changes in path and segment angle. Forward velocity was greatest following periods of maximum lateral excursion.
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T. elegans also captured prey by striking forward from rest or while swimming forward. Trunk recruitment was variable in this species: anterior loops were usually straightened during the initial phase of the strike (Fig. 7). In addition, large, posterior loops were sometimes straightened, especially when the strike covered a distance of four or more head lengths. In these instances, the forward strike transitioned into forward swimming and/or sideways sweeping. Prey appeared to be detected visually. Trunk looping was not as pronounced as that seen in T. couchii, and strikes were often initiated with only the anterior one-third of the trunk pointing towards the prey.
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T. elegans strikes reached mean peak velocities of approximately 46 cm s-1 (35 head lengths s-1; Fig. 8), approximately half that of T. couchii. Accelerations were also relatively lower, reaching mean peak values of approximately 9 m s-2 (540 head lengths s-2). Head acceleration was sustained for 80-100 ms before peak velocity was reached. Head segment angle decreased as velocity increased, although not to the same extent as in T. couchii. Segment angle also decreased in the first segment with increasing velocity, but showed little change in more-posterior segments. Path angles of the head and segments 1 and 2 decreased with increasing velocity. Forward displacement was largely restricted to the three anterior-most segments. More-posterior segments experienced a small amount of backwards displacement during the course of the strike.
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The diamond-backed water snake Nerodia rhombifer
This species sometimes used a low-speed, high-amplitude, open-mouth
sweeping behavior that resembled that found in T. elegans. More
commonly, however, N. rhombifer displayed a high-speed strike from an
ambush position (Fig. 9).
During this behavior, the snake remained motionless, often with its head out
of the water. Strikes were elicited by prey swimming close to the head or
sometimes by prey contacting the anterior trunk. Often, these strikes showed a
strong lateral component as the head was swung rapidly to the side to capture
prey. N. rhombifer showed a remarkable ability to bend the neck and
anterior trunk around to capture prey detected behind the head. In some of
these instances, prey were trapped between the head and anterior trunk and
corralled into the open jaws.
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Strikes were relatively rapid, reaching a mean peak velocity of 84 cm s-1 (42 head lengths s-1; Fig. 10). Accelerations were also high relative to T. elegans, reaching mean peak values of 20 m s-2 (1027 head lengths s-2). At the beginning of the strike, the head was oriented 90° relative to the prey item. Head angle and segment angle 1 decreased as the head was accelerated to roughly 20°. More-posterior segments decreased their segment angle to a much lesser degree than the head and segment 1. Path angles also dropped sharply for the head and segment 1 as velocity increased. More-posterior segments generally maintained path angles greater than 90°, indicating that these portions of the trunk were traveling away from the strike.
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The head and segments 1 and 2 showed the greatest forward displacement. More-posterior segments experienced a minor amount of backwards displacement. Looping of the posterior segments resulted in segments with anterior ends pointing in the opposite direction to the strike. As the strike proceeded and the head was displaced forward, these backwards-facing segments were displaced in the opposite direction of the strike as they followed more anterior segments through a postural curve.
Statistical analysis
Species differed significantly in the mean starting segment angle at strike
initiation (Table 1;
Fig. 11). Post hoc
contrasts revealed that T. couchii was significantly different from
T. elegans + N. rhombifer (F=120.72,
P<0.0001). T. elegans was not significantly different
from N. rhombifer (F=2.68, P=0.10). Species and
body position also had significant effects on minimum segment angle and
minimum path angle. Post hoc contrasts revealed that T.
couchii differed significantly in minimum segment angle from T.
elegans + N. rhombifer (F=129.59, P<0.0001)
and that T. elegans was different from N. rhombifer
(F=3.36, P=0.07). T. couchii differed significantly
in minimum path angle from T. elegans + N. rhombifer
(F=80.5, P<0.0001), and T. elegans was different
from N. rhombifer (F=18.55, P<0.0001). MANOVA of
acceleration and velocity revealed a significant species (F=3.44,
P=0.01) and a nearly significant individual (F=1.73,
P=0.6) effect. Univariate ANOVAs showed that species differed
significantly in maximum head velocity, with both T. couchii and
N. rhombifer attaining higher strike speeds than T. elegans
(Table 2). Species also
differed significantly in maximum head acceleration, with T. couchii
and N. rhombifer achieving values roughly twice that of T.
elegans.
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Discussion |
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Results from this study demonstrate that sideways sweeping is an inadequate term to describe the diversity of feeding modes present within snakes at even a relatively low phylogenetic level. Sideways sweeping best describes the bouts of low-velocity, open-mouth, lateral attacks exhibited by T. elegans and N. rhombifer. However, both of these species displayed faster attack behaviors that could be distinguished from slow sweeping by the velocity of the head and duration of the bout.
Predatory strikes in T. couchii have been recognized as
qualitatively distinct from those of generalist garter snakes
(Drummond, 1983) and have been
shown to have unique cranial kinematic characters
(Alfaro, 2002
). This study
reveals that trunk kinematics in this species also differ significantly from
other aquatic-feeding thamnophiines. T. couchii typically lines its
entire body up with the prey prior to striking. By contrast, Thamnophis
rufipunctatus, an independently evolved forward striker, appears to loop
only the anterior half of the body, while the posterior portion is braced
against a rock or other refuge (M. E. Alfaro, unpublished data).
Nonthamnophiines, such as booids (Cundall
and Deufel, 1999
; Frazzetta,
1966
), rattlesnakes (Kardong
and Bels, 1998
), vipers (Janoo
and Gasc, 1992
) and gopher snakes (Greenwald,
1974
,
1978
), strike by straightening
tight loops in the anterior one-third or so of the trunk. The less-active
posterior trunk may be directed away from the prey.
Linear arrangement of the trunk may partially explain the ability of T.
couchii to generate strikes that are both rapid and long. Although mean
maximum strike distances in T. couchii and T. elegans were
very similar (6.8 cm vs 5.3 cm), maximum head displacement occurred
over a shorter interval in T. couchii compared with T.
elegans (100 ms vs 150 ms; Figs
4,
8). Although N.
rhombifer achieved peak strike velocities and accelerations that were
close to those of T. couchii, the mean maximum strike distance of
T. couchii was relatively greater (3.9 head lengths vs 3.0
head lengths). Linear pre-strike looping may also increase the distance of
midwater strikes by increasing the ability of the animal to use the posterior
trunk to resist rearward-directed forces generated by the anterior trunk. This
ability is likely to be important in a species that forages in fast-moving
streams and rivers (Drummond,
1983; Rossman et al.,
1996
). Finally, selective pressures for rapid, long-distance
aquatic strikes may explain the increased length and number of vertebrae found
in this species relative to other garter snakes
(Rossman et al., 1996
).
Although T. elegans takes a wide range of prey, local populations
may be relatively specialized (Arnold,
1981). Populations of T. elegans in this study regularly
capture minnows and tadpoles while swimming in lakes and ponds
(Arnold, 1981
;
Rossman et al., 1996
). In
contrast to Thamnophis sirtalis, another generalist garter snake
capable of capturing aquatic prey, T. elegans appeared comfortable
when fully immersed (i.e. it did not avoid complete submersion and regularly
engaged in sustained bouts of swimming) and appeared to have greater buoyancy
control (Alfaro, 2002
;
Arnold, 1981
). Although peak
head velocities and accelerations were lower in T. elegans than in
T. couchii or N. rhombifer, T. elegans showed substantially
higher strike performance than that reported for T. sirtalis
capturing fish (mean peak head velocity, 34.57 head lengths s-1
vs 11.04 head lengths s-1; mean peak head acceleration,
539.99 head lengths s-2 vs 227.92 head lengths
s-2; Alfaro, 2002
).
Although comparative data on T. sirtalis trunk kinematics are not
available, this study suggests that T. elegans is a more specialized
fish-catcher than other generalist species of garter snake.
The anterior 20-30% of the trunk is most active during the strike of T. elegans. This portion of the body is generally aligned to the direction of the strike, although not to the same degree as in T. couchii. More posteriorly, the trunk may be coiled circularly or looped irregularly, but it is generally not aligned with the strike direction. Head displacement is accomplished by straightening the curves in the anterior part of the trunk and, during longer strikes, by straightening of posterior loops. The long axis of the head becomes nearly parallel with the strike vector as the head is displaced. Thus, while strikes may initially appear to involve a lateral sweep of the head, prey capture is usually accomplished by a frontal attack. The posterior trunk appears to contribute to head displacement by flowing through postural curves rather than by straightening.
Foraging mode and feeding ecology
The differences in axial kinematics observed here clarify our understanding
of the foraging ecology of the three species examined. T. couchii is
recognized as an aquatic specialist on fish
(Alfaro, 2002; Drummond,
1980
,
1985
). The trunk kinematic
behaviors I observed in this species appear to be related to the
high-velocity, high-acceleration, long-distance strike that T.
couchii uses to capture prey. T couchii also possesses
modifications that enhance its underwater vision
(Schaeffel and De Queiroz,
1990
). Together, these traits suggest that T couchii is
primarily a diurnal predator that has evolved a foraging mode for exploiting
prey in deep water and at relatively low densities.
T. elegans does not show extreme trunk recruitment patterns and
has a low-performance strike compared with that of T. couchii.
Furthermore, this species does not possess especially acute underwater vision
relative to other garter snakes (Schaeffel
and De Queiroz, 1990). However, compared with T.
sirtalis, another generalist species, T. elegans shows a greater
capacity for aquatic foraging behavior
(Arnold, 1981
) and possesses a
fast, forward-directed strike (Alfaro,
2002
). These traits suggest that T. elegans is an
intermediate aquatic specialist that may be less able than T couchii
to exploit prey at low densities but is nevertheless adept at capturing fish
in the water.
Nerodia have relatively poor underwater vision
(Schaeffel and De Queiroz,
1990) and appear to rely heavily on tactile cues to direct strikes
(Brown, 1958
). Interestingly,
and as an alternative to some hydrodynamic hypotheses that have been proposed
to explain fishing behavior in Nerodia
(Young, 1991
), lateral
striking may simply reflect the reliance of this species on tactile cues,
since neck bending would be required to capture most prey that contacted the
animal's body. That N. rhombifer is capable of high-velocity and
high-acceleration strikes relative to generalist garter snake species suggests
that prey capture in Nerodia is specialized. Unlike T.
couchii, which relies on acute underwater vision and a long-distance
strike to exploit prey at low densities, N. rhombifer, and probably
also other Nerodia species, utilize tactile cues and a rapid,
short-distance strike. This may allow this genus to efficiently exploit prey
at high densities and may explain the ability of many Nerodia to
become nearly entirely nocturnal (e.g.
Drummond, 1983
).
Models of trunk activity during the strike: open gate vs
tractor-tread model
Two simple models have been proposed to describe the trunk displacement and
head acceleration of the rattlesnake strike
(Kardong and Bels, 1998). In
the open gate model, acute body bends are straightened. In the tractor-tread
model, the body flows through postural curves. The aquatic snakes in this
study appear to make differential use of these modes during feeding. T.
couchii may provide the best example of a species that uses the open gate
mode to strike: straightening of pre-strike coils usually occurs over the
entire body (Fig. 3). This
mechanism may be the most advantageous way to generate high speeds for snakes
able to recruit large portions of the trunk into the strike, since additional
bends should sum to increase resultant head velocity.
T. elegans strikes generally fit the tractor-tread model well, especially in the posterior trunk, where more-posterior points followed the paths of anterior points (Fig. 7). These posterior curves were often in contact with the sides or bottom of the tank and are probably the site of active pushing. Furthermore, force may be generated by pressing trunk segments against the water. It is unclear whether this water reaction force is sufficient to account for the relatively rapid strikes characterized here, although it is almost certainly the means by which forces are generated during sideways sweeping (Figs 5, 6).
N. rhombifer usually struck opportunistically at prey as they
passed near the head rather than orienting its head and body towards a
specific prey. Prey were often captured lateral to the head, exhibiting a
pattern of displacement that does not fit either the tractor-tread or open
gate model. In this behavior (Fig.
9), a strong bend develops in the anterior portion of the trunk
that was initially relatively straight. Displacement in the kinematically
active region follows the direction of the bend. Although initial bending
occurs at a localized point, regions around this bend also become more curved
as the head continues to swing laterally. The posterior trunk is held
relatively static and probably serves as an anchor for the kinematically
active region. This pattern of displacement appears similar to that exhibited
by homalopsines (Jayne et al.,
1988; Smith et al.,
2002
).
The results of this study challenge many popular preconceptions regarding
aquatic prey capture in snakes. Snakes don't all fish in the same way.
Sideways sweeping actually encompasses two distinct behaviors: a slow,
open-mouthed search, apparently undirected and typically lasting several
seconds, and a more rapid strike that is directed at specific prey items.
Furthermore, as suggested by differences in the two lateral-striking species
examined in this study, diversification within this mode can occur at
relatively low phylogenetic levels. This result shows that 'fast'
(Cundall and Greene, 2000)
strike systems have evolved within natricine snakes a number of times and
suggests that other piscivorous lineages might also have evolved rapid
strikes.
In addition to quantifying the diversity of trunk function in aquatic and terrestrial species, future studies should focus on the skeletal and muscular mechanisms of head acceleration during the strike so that kinematic differences can be understood in a biomechanical context. The combined approach of kinematics and biomechanics has the potential to provide functional explanations of the morphology and behaviors that underlie 'fast' and 'slow' strikes, thus greatly improving our understanding of this complex and important behavior.
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Acknowledgments |
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References |
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