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First published online February 27, 2009
Journal of Experimental Biology 212, 768-777 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.026617
Locomotor–feeding coupling during prey capture in a lizard (Gerrhosaurus major): effects of prehension mode
1 UMR 7179 `Mécanismes Adaptatifs: des Organismes aux
Communautés', Muséum National d'Histoire Naturelle,
équipe `Diversité Fonctionnelle et Adaptations',
Département EGB `Ecologie et Gestion de la Biodiversité', 57,
rue Cuvier bp55, F-75231 Paris cedex 5, France
2 Department of Organismic and Evolutionary Biology, Harvard University, 26
Oxford Street, Cambridge, MA 02138, USA
3 INRIA Rhone-Alpes, 655 Avenue de L'Europe, 38330 Montbonnot, France
* Author for correspondence (e-mail: montuelle{at}mnhn.fr)
Accepted 6 January 2009
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: capture, decoupling, tongue, jaw, lizard, feeding
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). For example,
some long-tongued frogs rely predominantly on tongue movements when capturing
small prey, but add a significant lunge component to the capture when prey are
bigger, thus suggesting an intricate coupling between feeding and locomotor
systems (Anderson, 1993;
Valdez and Nishikawa, 1997).
Yet, most functional studies of feeding consider the feeding system in
isolation from other systems (e.g.
Delheusy and Bels, 1992;
Delheusy and Bels, 1999;
Bels et al., 1994;
Urbani and Bels, 1995;
Herrel et al., 1995;
Herrel et al., 1996;
Herrel et al., 1999;
Bels, 2003), and the movements
involved in the approach of a potential prey and the positioning of the head
prior to the strike have rarely been studied from a functional perspective
(but see Kardong and Bels,
1998; Alfaro, 2003;
Higham et al., 2005;
Higham, 2007a;
Montuelle et al., 2008). The
actual integration between feeding and locomotor systems has received even
less attention to date (see Higham,
2007b).
Prey capture performance (i.e. capture success) is dependent on two
elements: (i) the success of the actual capture determined by the adhesive
capacity of the tongue (Bell,
1989; Delheusy et al.,
1994; Herrel et al.,
2000; Deban and Marks,
2002) or the ability of a predator to grasp the prey firmly and
quickly between the jaws (Frazzetta,
1983), and (ii) the actual acceleration or velocity, and the
precision of the predator during the approach
(Webb, 1975;
Webb, 1984;
Webb and Skadsen, 1980;
Higham et al., 2005). The use
of the tongue as a prehension organ may potentially be constrained by the
velocity of the predator, as tongue protrusion often requires time, and is
dependent on precise sensorimotor coordination
(Nishikawa et al., 1992;
Deban, 1997). Indeed, most prey
capture systems characterized by extreme and fast tongue elongation occur in
animals using a slow approach or that remain stationary
(Wainwright et al., 1991;
Deban et al., 1997;
Nishikawa, 1999). Moreover
most animals using rapid tongue movements depend largely on feedforward
modulation of the tongue and jaws (Deban,
1997; Nishikawa,
1999).
Body propulsion towards the prey, when present, is achieved by the action
of the axial system, like in snakes
(Kardong and Bels, 1998;
Cundall and Greene, 2000), or
the combined action of the axial and appendicular systems, especially in
elongate tetrapods with a parasagittal gait like lizards
(Frazzetta, 1983;
Kraklau, 1991;
Montuelle et al., 2008). For
example, the positioning of the head before capture is achieved by extension
of the front limbs and bending at the cranio-cervical joint
(Kraklau, 1991) but may be
dependent on capture mode. Thus, the integration between feeding and locomotor
systems is expected to be strong but may also be dependent on the prey capture
strategy used. A recent study on feeding in lizards demonstrated that the
actual feeding movements (i.e. jaw and hyolingual kinematics) were independent
of the specific approach strategy used, suggesting that a direct coupling
between feeding and locomotor movements may be absent in some cases
(Montuelle et al., 2008).
Squamate lizards may be an ideal model system to explicitly explore the
coupling between locomotor and feeding movements and its dependence on
prehension mode as different prey capture strategies are used by different
species (Bels et al., 1994;
Schwenk, 2000;
Bels, 2003). For example,
whereas iguanian lizards (chameleons, iguanas and agamids) rely predominantly
on their tongue for prey capture, scleroglossans (all other lizards) mainly
use their jaws to apprehend prey (Schwenk,
2000). The use of tongue-based prey capture may potentially allow
a partial decoupling of the two systems, resulting in a lack of association
between the locomotor strategy used during capture and the actual feeding
movements (Montuelle et al.,
2008). Indeed, in its most extreme form, as observed in chameleons
for example, prey capture is completely decoupled from locomotion
(Wainwright et al., 1991). The
use of the jaws for prey capture, on the other hand, may imply a greater
involvement of the locomotor system (i.e. limbs and vertebral axis, especially
the neck) to position the head before the actual strike. Thus, comparisons
between lizards that use different prey capture strategies may be especially
insightful in understanding the role of prehension mode in driving the
coupling between locomotor and feeding movements.
We decided to use Gerrhosaurus major as a model system to test for
locomotor–feeding coupling. Cordyliform lizards like
Gherrosaurus are known to use both lingual and jaw prehension modes
(Urbani and Bels, 1995;
Reilly and McBrayer, 2007),
allowing the role of prehension mode to be tested without potential
confounding effects of phylogenetic history. Animals were offered four
different prey types to elicit different prehension modes. Because the
predator has to initially position and then move its jaws around the prey,
jaw-based prey capture can be expected to involve the elevation of the head by
extension of the forelimbs. So we predicted that during jaw prehension,
coupling and integration of the feeding and locomotor systems will be strong.
During tongue prehension, however, the tongue is the organ contacting and
transporting the prey and may potentially eliminate the need for extensive
forelimb and body involvement during capture. Thus, the integration between
the locomotor and feeding systems may be reduced in the case of tongue
prehension as previously observed for A. carolinensis
(Montuelle et al., 2008).
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Experimental protocol
We offered four different food items that reflect the natural diet of
Gerrhosaurus major (Spawls et
al., 2002): a piece of fruit (banana, length 10.5±2.8 mm),
mealworms (Tenebrio molitor, length 36.8±7.5 mm), grasshoppers
(Locusta migratoria, length 45.0±1.3 mm) and newborn mice
(Mus musculus, length 29.8±3.6 mm). These prey types were
selected to provide the animal with prey of different size, shape and
mobility, and are know to elicit different prehension modes. The experimental
set-up consisted of a 2 m long, 30 cm wide wooden trackway covered with a
non-slip green plastic carpet. Before the experiments, animals were free to
roam across the track to induce naturalistic foraging behaviour. On one side
of the track, three synchronized high-speed cameras (AVT Pike F-032B, Allied
Vision Technologies, Stadtroda, Germany) were set up and used to film the
capture of prey at 200 frames s–1. One camera was set in
frontal view, a second one in lateral view and the third one tilted down in an
oblique dorsal view. During filming, all five animals (marked individually by
paint codes on their backs) were positioned at one side of the track. Food
items were offered at the opposite side of the track and we waited for lizards
to detect the prey and spontaneously initiate an approach and capture
sequence.
Three-dimensional reconstruction
A custom-written Matlab routine (Loco 2.8) was used to digitize the
landmarks (markers painted on the body and head using non-toxic white paint)
on multiple synchronized views. This allowed us to calculate the screen
coordinates of the following landmarks
(Fig. 1): the upper jaw, the
lower jaw, the corner of the mouth, the anterior corner of the eye, the
mid-sagittal point between the eyes, the back of the parietal bones, the
pectoral girdle, the neck mid-way between the back of the parietal bones and
the pectoral girdle, the pelvic girdle, two markers mid-way between the neck
marker and the parietal bones and pectoral girdle markers, respectively, the
left shoulder, the left elbow, the left wrist, and finally one landmark on the
prey. The digitization provided us with three sets of 2-D coordinates (one set
per camera) which were used to calculate the 3-D coordinates using a
DLT-routine (Hartley and Sturm,
1995). A checkerboard composed of nine by nine squares of 1
cmx1 cm was used to calibrate the cameras and scale the images.
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Kinematic variables describing the movements of the cranial system were based on two profiles. First, the gape angle was defined as the angle subtended by the line interconnecting the tip of the upper jaw and the corner of the mouth, and the line interconnecting the tip of the lower jaw and the corner of the mouth (Fig. 1B). From the gape profile we extracted the maximal gape angle, the time to the onset of opening and the time to maximal gape. Second, the head angle was calculated as the angle between the long axis of the head (line O–H, Fig. 1C) and the long axis of the neck (line V1–NE; Fig. 1C). From the changes in head angle over time, the angle at the onset of mouth opening, the head angle at prey contact, the minimal head angle (describing the most flexed position of the head) and the time to the minimal head angle were extracted.
To describe the movements of the post-cranial system we quantified two profiles. First, the elevation of the neck was calculated as the difference between the Z-coordinate of the neck point with the Z-coordinate of the neck at rest position (Fig. 1B). Based on the change in this variable over time we calculated neck elevation at the onset of mouth opening and at prey contact, the maximal elevation of the neck and the time to the maximal elevation of the neck. Second, the elbow angle was defined as the angle subtended by the shoulder, the elbow and the wrist markers (Fig. 1D). From this profile we quantified the elbow angle at the onset of mouth opening, the elbow angle at prey contact, the minimal and maximal elbow angle, and the time to the minimal and the maximal angle. Additionally, we calculated the absolute magnitude of the variation in elbow angle as the difference between the maximal and minimal angles.
The strike features are based on the predator–prey distance profile over time. The predator–prey distance was defined as the distance between the anterior corner of the eye and the anterior point of the prey (Fig. 1D). In this matrix, we include the strike distance, the predator–prey distance at the onset of mouth opening, and the distance run by the lizard between the start of the strike and the onset of mouth opening (% of the total strike distance). Finally, we calculated peak strike velocity and the time to the peak strike velocity.
Data set
Consequently, our data set is divided into three matrices, each of them
representing a different component of prey capture in Gerrhosaurus
major (Table 1). The
cranial matrix is composed of seven variables (three for jaw system and four
for head positioning): time to mouth opening, maximal gape angle and time to
maximal gape; head angle at the onset of mouth opening, head angle at prey
contact, minimal head angle and time to minimal head angle. Next, the
post-cranial matrix is composed of 11 variables (four for neck movements and
seven for elbow angle): neck elevation at the onset of mouth opening, neck
elevation at prey contact, maximal neck elevation and time to maximal neck
elevation; elbow angle at the onset of mouth opening, elbow angle at prey
contact, maximal elbow angle, time to maximal elbow angle, minimal elbow
angle, time to minimal elbow angle and absolute magnitude of elbow angle
variation. Finally the strike matrix comprises five strike variables: strike
distance, predator–prey distance at the onset of mouth opening, distance
run by the lizard at mouth opening, peak strike velocity and time to peak
strike velocity.
For a total of 37 capture sequences, the three synchronized views were digitized and 3-D reconstructions were performed. Overall, the data set is composed of 16 sequences describing the kinematics of jaw prehension and 21 sequences describing tongue prehension. In both prehension modes, all five individuals are represented, and for each prey type the data set includes at least four of the five individuals.
Statistical analysis
All statistical analyses were performed using SPSS 15.0 for Windows (SPSS,
Chicago, IL, USA). All kinematic data were log10 transformed to
fulfil assumptions of normality and homoscedascity. Prior to analysis, we
performed a MANCOVA on the complete data set (cranial, post-cranial and strike
variables) to test for an effect of individual size. Size was not significant
and thus will no longer be considered in our analysis.
First, we performed a factor analysis with varimax rotation on a composite
matrix combining both the cranial and post-cranial matrix to reduce the
dimensionality of the data. Factors with eigenvalues greater than 1 were
extracted and factor scores were saved. Individuals were entered as random
factor, and prehension mode was entered as a fixed factor in a full factorial
two-way MANOVA coupled to univariate F-tests. Non-significant
interaction terms were removed from the final model. Next, we ran a
discriminant function analysis (DFA) on the factor scores to determine which
kinematic variables discriminated best between prehension modes
(Quinn and Keough, 2002).
The strike variables were analysed through two consecutive statistical procedures. First, we tested for a prehension mode effect by performing an ANOVA coupled to univariate F-tests. In this analysis, individuals were set as random factor and prehension modes as fixed factor, and non-significant interaction terms were removed from the final model. Then, we used a correlation matrix to test for associations between the strike variables and the factor scores obtained previously that summarize the kinematics of the cranial and post-cranial movements.
To test for associations and the integration between the cranial and post-cranial systems during prey capture, the data set was split into two data sets, one representing the kinematics for jaw prehension and one representing tongue prehension. For both data sets, the cranial and post-cranial matrix were separately subjected to a factor with varimax rotation, and factors with eigenvalues greater than 1 were extracted. These factors were then introduced into a correlation matrix to test for associations between the kinematics of the cranial and post-cranial systems, and to compare jaw and tongue prehension modes.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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),
Gerrhosaurus major used two prehension modes to capture prey: jaw and
tongue prehension. The selection of prehension mode was strongly influenced by
the type of food captured; jaw prehension was typically used for newborn mice
(78.6%) and grasshoppers (91.3%), whereas tongue prehension was used for
banana (92.9%) and mealworms (100%). In both prey prehension modes, attacks
were highly successful in all individuals, the predator rarely, if ever,
missing the target.
After detecting the prey, individuals oriented and moved towards the prey,
tongue flicking occasionally. In prey capture sequences involving the use of
the tongue, the lizard stopped closer to the prey compared with those
involving the jaws. During the preparatory phase, a distinctive body
configuration was associated with each prehension mode suggesting that the
selection of prehension modes is completed prior to the strike and is based on
sensory stimuli gathered during the approach. During tongue prehension
sequences, the body remained close to the substratum with the vertebral column
in an extended horizontal position; in contrast, during jaw prehension the
forelimbs were extended, thus elevating the head and neck (see supplementary
material Movies 1 and 2, respectively). After the extension of the forelimbs
the head was flexed ventrally and positioned above the prey. Next the mouth
was opened and gape increased rapidly; the speed of mouth opening being
distinctly greater during jaw prehension than during tongue prehension. The
strike itself was also more rapid during jaw prehension and the forward
velocity of the predator was largely determined by the extension and
subsequent flexion of the forelimbs. Occasionally, the vertebral axis was also
curved in an S-shape during the preparatory phase of jaw prehension, and
extended rapidly during the strike, thus providing an additional acceleration
component, similar to that observed previously in snakes
(Kardong and Bels, 1998).
During both jaw and tongue prehension, the head of the predator was typically
oriented perpendicular to the long axis of the prey. Tongue protrusion in
G. major appears to be qualitatively similar to that described for
iguanians and scincids using this capture mode
(Schwenk and Throckmorton,
1989; Kraklau,
1991; Herrel et al.,
1995; Smith et al.,
1999). The tongue is protracted outside the mouth, curls ventrally
and bulges, thus exposing the dorsal surface anteriorly towards the prey.
Next, the tongue contacts the prey and retracts, bringing the prey inside the
mouth. During jaw prehension, however, the tongue is retracted backwards at
the onset of jaw opening. Once the prey has passed the jaw margins, the mouth
closes rapidly, and a power stroke occurs upon prey contact. Given the more
extended initial position of the head and body during tongue prehension
events, the power stroke is performed with the head positioned horizontally,
in contrast to jaw prehension events where the power stroke occurs while the
head is bent ventrally (Table
1).
Variables in the strike matrix were strongly modulated according to prehension mode. Indeed, the prehension mode had a significant effect on the strike distance (F1,31=11.259; P<0.01), indicating jaw prehension is induced further from the prey. The distance of mouth opening (F1,31=5.248; P=0.03) was also affected by prehension mode suggesting the mouth opens further from the prey in jaw prehension than in tongue prehension. Moreover, the prehension mode had a significant effect on the distance run by the lizard between the start of the strike and mouth opening (F1,31=6.098; P=0.02), providing evidence that a predator using jaw prehension has covered a greater portion of the total strike distance when the mouth opens. Finally, the peak strike velocity was greater during jaw prehension than during tongue prehension (F1,31=58.503; P<0.01). No individual effect was detected for any variables. Interaction term was only significant for the time to peak strike velocity, so we treated each of the five individuals separately. The effect of prehension mode was only significant for one individual (F1,3=12.550; P=0.04), not for the others.
Modulation of capture kinematics according to prehension mode
To test for differences in the kinematics of the feeding and locomotor
systems associated with different prehension modes we performed a factor
analysis with varimax rotation on the full kinematic data matrix. Six factors
with eigenvalues greater than 1 were extracted
(Table 2), the first two
factors jointly explaining 35.76% of the total variance. The MANOVA performed
on the factor scores detected significant prehension mode (Wilk's
=0.357; F6,26=7.789; P<0.01) and
individual effects (Wilk's =0.095;
F24,91.913=3.693; P<0.01). Interaction effects
were non-significant, suggesting that all individuals change their kinematics
in a similar fashion when switching from jaw to tongue prehension.
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The first factor was positively correlated with variables describing the movement of the elbow: the elbow angle at mouth opening, the maximal flexion of the elbow (minimal angle), the elbow angle at prey contact, and the maximal extension of the elbow (maximal angle; Table 2). However, neither prehension mode nor individual effects were significant. The maximal elevation of the neck, and the elevation of the neck at prey contact and mouth opening loaded positively on the second factor (Table 2). Only individual effect (F4,31=4.255; P<0.01) was significant on the second factor.
The third factor was associated with head positioning kinematics: minimal head angle (the most flexed position of the head), the head angle at prey contact and the head angle at the onset of mouth opening all loaded positively (Table 2). As for the second factor, individual effect was significant on the third factor (F4,31=6.148; P<0.01). The fourth factor was positively correlated with jaw movements and especially the time to mouth opening and the maximal gape angle (Table 2). Prehension mode effect was strong on the fourth factor (F1,31=12.905; P<0.01; Fig. 2), and so was individual effect (F4,31=3.844; P=0.01). This suggests that jaws open later and wider in jaw prehension events than in tongue prehension events. The timing of cranial system movements (time to minimal head angle and time to maximal gape angle) loaded positively on the fifth factor (Table 2). This factor was strongly affected by prehension mode (F1,31=11.808; P<0.01; Fig. 2), indicating that head flexion is more rapid and maximal gape occurs sooner in jaw prehension. The sixth factor (correlated with the total extension of the elbow) did not discriminate between either individuals or prehension modes.
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A DFA performed on the six factor scores extracted a single discriminant function defined by factors 4 and 5. Consequently, jaw prehension differs from tongue prehension by a more rapid positioning of the head, a retarded opening of the mouth, and a wider maximal gape that occurs earlier. Interestingly, most variables that discriminated between prehension modes were timing-related variables of the cranial system, suggesting that the speed and timing of jaw movements are the dominant features characterizing each prehension mode.
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Functional integration of cranial and post-cranial systems
Given that jaw and tongue prehension are characterized by different
kinematic variables, we split our initial data set into two matrices: one for
the kinematics of jaw prehension, and one for tongue prehension. For each data
set we performed a factor analysis for kinematic features associated with the
cranial and post-cranial systems separately. Factors with eigenvalues greater
than 1 were retained and bi-variate correlations were performed to test for a
functional integration (i.e. co-variation in kinematics) between cranial and
post-cranial systems during jaw and tongue prehension events,
respectively.
For jaw prehension, three factors were extracted for the cranial system (explaining 83.3% of the total variance), and four factors for the post-cranial system (explaining 89.3% of the total variance; Table 3). Loadings of the variables on the factors were similar to those on the factors retained in the factor analysis performed previously (see Tables 2 and 3). Bi-variate correlations between the seven factors indicated one significant and negative correlation: between cranial factor 3 and post-cranial factor 4 (R=–0.49, P=0.05; Fig. 4A). This correlation describes a functional link between the time of the maximal flexion of the head and the elbow. Interestingly, this association is independent of prey type and thus appears to describe the functional coupling between the two systems (Fig. 4A). However, note the correlated factors are the ones that explained the least of the variance (17.1% and 11.15%, respectively) and, consequently, most cranial (e.g. head positioning, jaw movements) and post-cranial movements (e.g. neck elevation) remain independent.
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For tongue prehension, the multivariate analysis performed on the kinematics associated with the cranial system is summarized by two factors (explaining 78.1% of the total variance), whereas the post-cranial kinematics can be summarized by three factors (explaining 80.7% of the total variance; Table 4). Bi-variate correlations of the five factors indicated only one significant correlation: between cranial factor 2 and post-cranial factor 2 (R=–0.56, P<0.01; Fig. 4B). Consequently, tongue prehension events involving a greater elevation of the neck during the preparatory phase are associated with faster jaw movements (both time of mouth opening and maximal gape). Maximal gape also loaded positively on the second cranial factor indicating that tongue prehension events involving a greater lifting of the neck are associated with lower maximal gape angles. Interestingly, tongue prehension cycles involving higher neck elevation, faster strikes and lower gape angles were mostly associated with the capture of mealworms (Fig. 34). Moreover, as for jaw prehension, the correlated factors only represent 35.5% and 28.76% of their respective total variance (Table 4). Indeed, the factors that explain most of the variance were surprisingly not correlated, indicating head positioning and neck elevation are independent.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). Tongue
prehension, on the other hand is slower and is characterized by a tongue
protrusion–retraction cycle and tongue deformation similar to that
observed for iguanian, scincid and gerrhosaurid lizards
(Schwenk and Throckmorton,
1989; Kraklau,
1991; Herrel et al.,
1995; Urbani and Bels,
1995; Smith et al.,
1999; Meyers and Nishikawa,
2000; Schwenk,
2000). Indeed, in most species using tongue prehension, the tongue
deforms and contacts the prey with its dorsal surface
(Delheusy et al., 1994) (but
see Meyers and Herrel, 2005).
The initialization of the strike is also highly different between tongue and
jaw prehension: when using its jaws to capture prey G. major extends
its forelimbs and raises its head and neck to position its jaws dorsal to the
prey, which is crucial for the jaws to be able to grasp the prey
(Frazzetta, 1983;
Delheusy et al., 1995). During
tongue prehension, on the other hand, the head is kept in a more horizontal
position and elbow extension is much smaller.
Head positioning is thus largely dependent on the movements of the elements of the locomotor system. The most important component of the locomotor system included in our data set was the angular change at the elbow. A greater elbow extension during the initial positioning allows rapid extension of the head during jaw prehension, providing a higher acceleration and ultimately a greater strike velocity, which is likely to be crucial in determining prey capture success. In support of this statement is the observation that jaw prehension was associated with the capture of active and mobile prey (grasshoppers, newborn mice) where speed of capture may make the difference between a successful or failed strike. Moreover, tongue-based capture of mealworms involved a greater elevation of the neck and was associated with a more rapid strike compared with the capture of banana. Consequently, neck elevation may be associated with the capture of more evasive prey, regardless of the prehension mode used. The extension of the forelimbs during jaw prehension also resulted in a change in the bending of the vertebral axis and differences in the elevation of the neck. In summary, both prey capture modes are kinematically well characterized by cranial and post-cranial movements and are strongly discriminated by the timing of kinematic events.
As predicted, correlations between movements of the jaws and those
associated with the locomotor system exist, indicating a functional coupling
between the two anatomical systems as observed previously for other
vertebrates (for a review, see Higham,
2007b). However, note the factors summarizing neck elevation and
head positioning were not correlated, suggesting the head movements are
decoupled from the movements of the neck and the rest of the vertebral axis.
Besides, and in support of our prediction, the cranial–post-cranial
coupling is expressed differently depending on the prehension mode used.
During jaw capture, the timings of the head and elbow actions are correlated,
suggesting quick head positioning is associated with late movements of the
elbow. In contrast to our prediction, however, tongue prehension in G.
major also involved integration between the jaw and locomotor systems.
Indeed, the timing of jaw movements during tongue prehension is dependent on
neck elevation, with faster jaw movements and lower gape angles being
associated with greater elevation of the neck. Yet, our data also suggest that
this coupling may be dependent on prey type
(Fig. 3B), with more mobile
prey eliciting faster jaw movements and a faster strike, in turn facilitated
by movements of the post-cranial system.
Previous studies on tongue-based prey capture in other tetrapods suggest
that tongue actions may be decoupled from the locomotor system, especially in
systems characterized by extreme protrusion and projection
(Wainwright et al., 1991;
Deban et al., 1997;
Nishikawa, 1999;
Nishikawa, 2000).
Consequently, tongue prehension may require less integration between the two
anatomical systems but this may come at the cost of a reduced attack speed.
Although tongue protrusion in G. major is qualitatively similar to
that observed in other lizards using their tongue to capture prey, our data
suggest that these movements are clearly coupled to the movements of the
locomotor system. Although this appears to be in contrast to what has been
observed for lizards using lingual prehension (e.g. iguanian lizards like
chameleons or Anolis lizards), tongue prehension in G. major
is slow and consequently may allow feedback between jaw and locomotor systems.
As a true comparative database is still lacking, it remains difficult to
generalize these observations. One notable feature that may be associated with
the difference in coupling between the jaw and locomotor systems between these
different lizards using tongue prehension is that G. major is a more
active forager (Cooper and Steele,
1999) than the iguanian lizards studied previously. Indeed,
iguanians are typically dedicated ambush foragers that use a `sit and wait'
strategy and wait for the prey to come within strike distance and rely on a
rapid strike (Reilly et al.,
2007). Consequently, there may not be enough time for on-line
integration between the jaw and locomotor systems and thus modulation of the
strike in ambush foragers may be largely feedforward.
Cordyliform lizards would be an ideal system in which to further
investigate the coupling of jaw and locomotor systems during prey capture as
this clade contains both sit-and-wait (Cordylus) and active foragers
[Platysaurus, Gherrosaurus (Cooper
and Steele, 1999; Whiting,
2007)]. Moreover, the clade is characterized by species using both
prehension modes like members of the genera Gherrosaurus (this study)
or Zonosaurus (Urbani and Bels,
1995) as well as species that use jaw prehension exclusively like
lizards of the genus Platysaurus (A.H., unpublished observations),
thus allowing us to test for jaw and locomotor coupling in species differing
in foraging mode and prey capture strategy while minimizing historical
effects. Further studies investigating jaw and locomotor coupling in dedicated
active foragers like Varanus or Tupinambis and dedicated
ambush foragers like Pogona are needed, however, to evaluate these
patterns in a broad comparative framework.
In summary, our data show how the integration of jaw and locomotor systems is not reduced to a simple mechanical link. The observed co-variation between the kinematics of the jaw and locomotor system during prey capture suggests the existence of neural pathways between the two systems allowing feedback, which is crucial to ensure an integration and synchronization between the movements of the elements associated with the two systems.
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This work is part of the PhD project of S.J.M. and is supported by the Legs Prévost (MNHN), ANR 06-BLAN-0132-02 and Phymep Corporation. The authors would like to thank ANR project Kameleon (ARA 05-MMSA-0002 `Masse de Données') which provided the opportunity to use the synchronized camera set-up at the Plateau Technique `Biologie des Organismes' (dpt EGB `Ecologie et Gestion de la Biodiversité', MNHN). We also would like to thank Caroline Simonis for her suggestions on data analysis, and two anonymous reviewers for their constructive comments on a previous draft of the manuscript. Finally, S.J.M. would like to thank Prof. J. Losos for welcoming him to the Losos Lab (Harvard University, Cambridge, MA, USA) during the writing of this manuscript.
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
Alfaro, M. E. (2003). Sweeping and striking: a
kinematic study of the trunk during prey capture in three thamnophiine snakes.
J. Exp. Biol. 206,2381
-2389.
Anderson, C. W. (1993). The modulation of feeding behavior in response to prey type in the frog Rana pipiens.J. Exp. Biol. 179,1 -12.[Abstract]
Bell, D. A. (1989). Functional anatomy of the chameleon tongue. Zool. J. Anat. 119,313 -336.
Bels, V. L. (2003). Evaluating the complexity of the trophic system in Reptilia. In Vertebrate Biomechanics and Evolution (ed. V. L. Bels, J. P. Gasc and A. Casinos), pp.185 -202. Oxford: BIOS Scientific Publishers.
Bels, V. L. and Goosse, V. (1990). Comparative kinematic analysis of prey capture in Anolis carolinensis (Iguania) and Lacerta viridis (Scleroglossa). J. Exp. Zool. 255,120 -124.[CrossRef]
Bels, V. L., Chardon, M. and Kardong, K. V. (1994). Biomechanics of the hyolingual system in Squamata. In Biomechanics of Feeding in Vertebrates, vol.18 (ed. V. L. Bels, M. Chardon and P. Vandewalle), pp.197 -240. Berlin: Springer-Verlag.
Cooper, W. E., Jr and Steele, L. J. (1999). Lingually mediated discriminations among prey chemicals and control stimuli in cordyliform lizards: presence in a gerrhosaurid and absence in two cordylids. Herpetologica 55,361 -368.
Cundall, D. and Greene, H. W. (2000). Feeding in snakes. In Feeding: Form, Function and Evolution in Tetrapod Vertebrates (ed. K. Schwenk), pp.293 -333. San Diego, CA: Academic Press.
Deban, S. M. (1997). Modulation of prey-capture behavior in the plethodontid salamander Ensatina eschscholtzii. J. Exp. Biol. 200,1951 -1964.[Abstract]
Deban, S. M. and Marks, S. B. (2002). Metamorphosis and evolution of feeding behavior in salamanders of the family Plethodontidae. Zool. J. Linn. Soc. 134,375 -400.[CrossRef]
Deban, S. M., Wake, D. B. and Roth, G. (1997). Salamander with a ballistic tongue. Nature 389, 27-28.[Medline]
Delheusy, V. and Bels, V. L. (1992). Kinematics
of feeding behaviour in Oplurus cuvieri (Reptilia: Iguanidae).
J. Exp. Biol. 170,155
-186.
Delheusy, V. and Bels, V. L. (1999). Feeding kinematics of Phelsuma madagascariensis (Reptilia: Gekkonidae): testing differences between Iguania and Scleroglossa. J. Exp. Biol. 202,3715 -3730.[Abstract]
Delheusy, V., Toubeau, G. and Bels, V. L. (1994). Tongue structure and function in Oplurus cuvieri (Reptilia: Iguanidae). Anat. Rec. 238,263 -276.[CrossRef][Medline]
Delheusy, V., Brillet, C. and Bels, V. L. (1995). Etude cinématique de la prise de nourriture chez Eublepharis macularius (Reptilia, Gekkonidae) et comparaison au sein des geckos. Amphibia Reptilia 16,185 -201.[CrossRef]
Frazzetta, T. H. (1983). Adaptation and function of cranial kinesis in reptiles: a time-motion analysis of feeding in alligator lizards. In Advances in Herpetology and Evolutionary Biology: Essays in Honor of E. E. Williams (ed. A. G. J. Rhodin and K. Miyata), pp. 222-244. Cambridge: Museum of Comparative Zoology Publication.
Hartley, R. I. and Sturm, P. (1995). Triangulation. 6th International Conference on Computer Analysis of Images and Patterns, pp. 190-197. Prague, Czech Republic.
Herrel, H., Cleuren, J. and De Vree, F. (1995). Prey capture in the lizard Agama stellio. J. Morphol. 224,313 -329.[CrossRef]
Herrel, A., Cleuren, J. and De Vree, F. (1996). Kinematics of feeding in the lizard Agama stellio. J. Exp. Biol. 199,1727 -1742.[Abstract]
Herrel, A., Verstappen, M. and De Vree, F. (1999). Modulatory complexity of the feeding repertoire in scincid lizards. J. Comp. Physiol. A 184,501 -518.[CrossRef]
Herrel, A., Meyers, J. J., Nishikawa, K. C. and Aerts, P. (2000). The mechanics of prey prehension in chameleons. J. Exp. Biol. 203,3255 -3263.[Abstract]
Higham, T. E. (2007a). Feeding, fins and
braking maneuvers: locomotion during prey capture in centrarchid fishes.
J. Exp. Biol. 210,107
-117.
Higham, T. E. (2007b). The integration of
locomotion and prey capture in vertebrates: morphology, behavior and
performance. Integr. Comp. Biol.
47, 82-95.
Higham, T. E., Day, S. W. and Wainwright, P. C.
(2005). Sucking while swimming: evaluating the effects of ram
speed on suction generation in bluegill sunfish Lepomis macrochirus
using digital particle image velocimetry. J. Exp.
Biol. 208,2653
-2660.
Kardong, K. V. and Bels, V. L. (1998). Rattlesnake strike behavior: kinematics. J. Exp. Biol. 201,837 -850.[Abstract]
Kraklau, D. M. (1991). Kinematics of prey capture and chewing in the lizard Agama agama (Squamata: Agamidae). J. Morphol. 210,195 -212.[CrossRef]
Meyers, J. J. and Herrel, A. (2005). Prey
capture kinematics of ant eating lizards. J. Exp.
Biol. 208,113
-127.
Meyers, J. J. and Nishikawa, K. C. (2000). Comparative study of tongue protrusion in three iguanian lizards: Sceloporus undulatus, Pseudotrapelus sinaitus and Chamaeleo jacksoni. J. Exp. Biol. 203,2833 -2849.[Abstract]
Montuelle, S. J., Daghfous, G. and Bels, V. L. (2008). Effect of locomotor approach on feeding kinematics in the green anole (Anolis carolinensis). J. Exp. Zool. 309A,563 -567.
Nishikawa, K. C. (1999). Neuromuscular control
of prey capture in frogs. Philos. Trans. R. Soc. Lond. B Biol.
Sci. 354,941
-954.
Nishikawa, K. C. (2000). Feeding in frogs. In Feeding: Form, Function and Evolution in Tetrapod Vertebrates (ed. K. Schwenk), pp.117 -144. San Diego, CA: Academic Press.
Nishikawa, K. C., Anderson, C. W., Deban, S. M. and O'Reilly, J. C. (1992). The evolution of neural circuits controlling feeding behavior in frogs. Brain Behav. Evol. 40,125 -140.[Medline]
Quinn, G. P. and Keough, M. J. (2002). Experimental Design and Data Analysis for Biologists. Cambridge: Cambridge University Press.
Reilly, S. M. and McBrayer, L. D. (2007). Prey-capture and processing behaviour and the evolution of lingual and sensory characteristics: divergences and convergences in lizard feeding biology. In Lizard Ecology: the Evolutionary Consequences of Foraging Mode (ed. S. M. Reilly, L. D. McBrayer and D. B. Miles), pp.302 -333. Cambridge: Cambridge University Press.
Reilly, S. M., McBrayer, L. D. and Miles, D. B. (2007). Lizard Ecology: The Evolutionary Consequences of Foraging Mode. Cambridge: Cambridge University Press.
Schwenk, K. (2000). Feeding in lepidosaurs. In Feeding: Form, Function and Evolution in Tetrapod Vertebrates (ed. K. Schwenk), pp.175 -291. San Diego, CA: Academic Press.
Schwenk, K. and Throckmorton, G. S. (1989). Functional and evolutionary morphology of lingual feeding in squamate reptiles: phylogenetics and kinematics. J. Zool. Lond. 219,153 -175.[CrossRef]
Smith, T. L., Kardong, K. K. and Bels, V. L. (1999). Prey capture behavior in the blue-tongued skink, Tiliqua scincoides. J. Herpetol. 33,362 -369.[CrossRef]
Spawls, S., Drewes, R., Howell, K. and Ashe, J. (2002). A Field Guide to the Reptiles of East Africa. London: Academic Press.
Urbani, J. M. and Bels, V. L. (1995). Feeding behavior in two scleroglossan lizards: Lacerta viridis (Lacertidae) and Zonosaurus laticaudatus (Cordylidae). J. Zool. Lond. 236,265 -290.[CrossRef]
Valdez, C. M. and Nishikawa, K. C. (1997). Sensory modulation and behavioral choice during feeding in the Australian frog, Cyclorana novaehollandiae. J. Comp. Physiol. A 180,187 -202.[CrossRef][Medline]
Wainwright, P. C., Kraklau, D. M. and Bennett, A. F.
(1991). Kinematics of tongue projection in Chamaeleo
oustaleti. J. Exp. Biol.
159,109
-133.
Webb, P. W. (1975). Acceleration performance of
rainbow trout, Salmo gairdneri, and green sunfish, Lepomis
cyanellus. J. Exp. Biol. 63,451
-465.
Webb, P. W. (1984). Body and fin form and strike tactics of four teleost predators attacking fathead minnow (Pimephales promelas) prey. Can. J. Fish. Aquat. Sci. 41,157 -165.[CrossRef]
Webb, P. W. and Skadsen, J. M. (1980). Strike tactics of Esox. Can. J. Zool. 58,1462 -1469.[Medline]
Whiting, M. J. (2007). Foraging mode in the African cordylids and plasticity of foraging behavior in Platysaurus broadleyi. In Lizard Ecology: The Evolutionary Consequences of Foraging Mode (ed. S. M. Reilly, L. D. McBrayer and D. B. Miles), pp. 405-426. Cambridge: Cambridge University Press.
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