Content uploaded by Anthony Herrel
Author content
All content in this area was uploaded by Anthony Herrel on Feb 24, 2014
Content may be subject to copyright.
3823
INTRODUCTION
In many vertebrate lineages, the function and morphology of the
feeding structures are influenced by the adaptive pressures that stem
from diet. The effects include adaptation of the jaw apparatus (e.g.
Rodriguez-Robles et al., 1999; Ferry-Graham et al., 2002; Van
Cakenberghe et al., 2002; Metzger and Herrel, 2005; Santana et al.,
2010; Hampton, 2011; Perry et al., 2011), teeth (e.g. Hotton, 1955;
Herrel et al., 1997; Herrel et al., 2004; Santana et al., 2011; Kupczik
and Stynder, 2012), hyolingual apparatus (e.g. Bels et al., 1994;
Schwenk, 2000; Bels, 2003; Meyers and Herrel, 2005; Schwenk
and Rubega, 2005; Herrel et al., 2009) and digestive track (O’Grady
et al., 2005; Herrel et al., 2008; Griffen and Mosblack, 2011). From
a functional perspective, feeding movements vary (i.e. are flexible)
(sensu Wainwright et al., 2008) in response to the physical, textural
and mechanical properties of the ingested food item in many
vertebrates (e.g. Deban, 1997; Nemeth, 1997; Valdez and
Nishikawa, 1997; Ferry-Graham, 1998; Dumont, 1999; Ferry-
Graham et al., 2001; Vincent et al., 2006; Reed and Ross, 2010;
Monroy and Nishikawa, 2011). Such variability in feeding
movements has been documented extensively in squamate lizards
during both the capture and intra-oral transport and processing of
food (e.g. Bels and Baltus, 1988; Herrel et al., 1996; Herrel et al.,
1999; Smith et al., 1999; Schaerlaeken et al., 2007; Schaerlaeken
et al., 2008; Sherbrooke and Schwenk, 2008; Metzger, 2009;
Montuelle et al., 2010; Schaerlaeken et al., 2011).
Organisms that feed on a particular food item (i.e. dietary
specialists) face a specific set of physical, mechanical and textural
properties. Consequently, in such organisms, the form and function
as well as the behavioral capabilities of the feeding system are known
to be specialized for handling the particular characteristics of their
diet (e.g. Herrel et al., 1997; Ralston and Wainwright, 1997; Korzoun
et al. 2001; Korzoun et al., 2003; Aguirre et al., 2003; Homberger,
2003; Meyers and Herrel, 2005; Herrel and De Vree, 2009). In
contrast, organisms that typically feed on a wide variety of food
items (i.e. dietary generalists) routinely face variability in food
properties. Thus, in dietary generalists such as omnivorous predators,
flexibility of feeding movements is a key aspect of feeding behavior
(e.g. Liem, 1978; Herrel et al., 1999). Flexibility is defined as the
‘ability of an organism to alter its behavior’ in response to changes
in the applied stimulus (i.e. ‘across experimental treatments’ in
functional and behavioral studies) (sensu Wainwright et al., 2008).
From a neurological perspective, flexibility is based on the ability
to modulate the motor pattern dictating movements (e.g. Deban et
al., 2001). Here, because we used kinematic data, our study focused
on the flexibility of the movements involved during prey capture;
complementary electromyographic data are required to understand
the modulation of the neuromotor control of prey capture. To date,
flexibility of the feeding movements involved during prey capture
has been documented in response to changes in prey size (e.g. Deban,
1997; Ferry-Graham, 1998; Delheusy and Bels, 1999; Vincent et
SUMMARY
Feeding movements are adjusted in response to food properties, and this flexibility is essential for omnivorous predators as food
properties vary routinely. In most lizards, prey capture is no longer considered to solely rely on the movements of the feeding
structures (jaws, hyolingual apparatus) but instead is understood to require the integration of the feeding system with the
locomotor system (i.e. coordination of movements). Here, we investigated flexibility in the coordination pattern between jaw, neck
and forelimb movements in omnivorous varanid lizards feeding on four prey types varying in length and mobility: grasshoppers,
live newborn mice, adult mice and dead adult mice. We tested for bivariate correlations between 3D locomotor and feeding
kinematics, and compared the jaw–neck–forelimb coordination patterns across prey types. Our results reveal that
locomotor–feeding integration is essential for the capture of evasive prey, and that different jaw–neck–forelimb coordination
patterns are used to capture different prey types. Jaw–neck–forelimb coordination is indeed significantly altered by the length and
speed of the prey, indicating that a similar coordination pattern can be finely tuned in response to prey stimuli. These results
suggest feed-forward as well as feed-back modulation of the control of locomotor–feeding integration. As varanids are considered
to be specialized in the capture of evasive prey (although they retain their ability to feed on a wide variety of prey items), flexibility
in locomotor–feeding integration in response to prey mobility is proposed to be a key component in their dietary specialization.
Key words: integration, flexibility, prey properties, Varanus, kinematics, jaw prehension.
Received 5 March 2012; Accepted 7 August 2012
The Journal of Experimental Biology 215, 3823-3835
© 2012. Published by The Company of Biologists Ltd
doi:10.1242/jeb.072074
RESEARCH ARTICLE
Flexibility in locomotor–feeding integration during prey capture in varanid lizards:
effects of prey size and velocity
Stéphane J. Montuelle1,*, Anthony Herrel2, Paul-Antoine Libourel3, Sandra Daillie2and Vincent L. Bels4
1Ohio University, Heritage College of Osteopathic Medicine, Department of Biomedical Sciences, Athens, OH 45701-2979, USA,
2Muséum National dʼHistoire Naturelle, Département Ecologie et Gestion de la Biodiversité, UMR 7179, Paris, France,
3Université Lyon 1, Institut Fédératif des Neurosciences, UMR 5167, Lyon, France and 4Muséum National dʼHistoire Naturelle,
Département Systematics and Evolution, UMR 7205, Paris, France
*Author for correspondence (montuell@ohiou.edu)
THE JOURNAL OF EXPERIMENTAL BIOLOGY
3824
al., 2006; Freeman and Lemen, 2007; Schaerlaeken et al., 2007)
and prey mobility (e.g. Ferry-Graham, 1998; Ferry-Graham et al.,
2001; Montuelle et al., 2010; Monroy and Nishikawa, 2011) in a
wide array of vertebrates.
Recently, prey-capture behavior has been demonstrated to not be
solely based on the movements of the feeding elements (e.g. the
jaws, the hyolingual apparatus) but, rather, to involve the integration
of the feeding and locomotor elements (e.g. Higham, 2007a;
Higham, 2007b; Montuelle et al., 2009a; Kane and Higham, 2011;
Montuelle et al., 2012). Integration is defined as the coordination
of the movements of two or more body parts (Wainwright et al.,
2008). It is thought to be based on a complex motor control which
ensures that their respective movements are coordinated in time (e.g.
synchronized) and space (i.e. position) (Wainwright et al., 2008).
Locomotor–feeding integration has been observed in fishes, with
the movements of the jaw and hyoid (e.g. jaw opening, expansion
of the buccal cavity through the ventral depression of the hyoid)
being coordinated with those of the fins (Rice and Westneat, 2005;
Higham, 2007a). In terrestrial tetrapods, although fewer data are
available, locomotor–feeding integration has been demonstrated in
snakes (e.g. Frazzetta, 1966; Janoo and Gasc, 1992; Kardong and
Bels, 1998; Cundall and Deufel, 1999; Alfaro, 2003; Young, 2010;
Herrel et al., 2011) and lizards (Montuelle et al., 2009a; Montuelle
et al., 2012). Interestingly, in one omnivorous lizard, Gerrhosaurus
major, both feeding and locomotor movements are observed to be
flexible in response to prey size and mobility (Montuelle et al., 2010).
However, flexibility in locomotor–feeding integration in response
to prey properties itself has yet to be investigated. Knowing whether
integrated movements can be flexible is thus of interest for our
understanding of the mechanisms that drive complex behaviors like
feeding.
Similar to some other cordyliform lizards, the prey-capture
behavior in G. major is characterized by a switch between tongue
prehension and jaw prehension depending on prey type (Urbani and
Bels, 1995; Smith et al., 1999; Reilly and McBrayer, 2007;
Montuelle et al., 2009a). From a motor control perspective, each
prey prehension mode stems from two different integrative motor
patterns that coordinate feeding movements (i.e. tongue and jaw
movements) with those of the locomotor elements (e.g. neck and
forelimb movements) (Montuelle et al., 2009a). Therefore, in G.
major, flexibility in locomotor–feeding integration allows the use
of two different prey prehension modes, each being used for
capturing prey of different size: jaw prehension is used to capture
large prey, whereas tongue prehension is used for relatively small
prey (Montuelle et al., 2009a). Thus, flexibility in locomotor–feeding
integration in response to prey properties may be a key adaptation
for animals with an omnivorous diet.
Here, we examined flexibility in locomotor–feeding integration
in organisms that only use a single prey prehension mode. Varanid
lizards were chosen because they are omnivorous predators that use
jaw prehension for catching different types of prey (Schwenk, 2000;
Vitt et al., 2003; Vitt and Pianka, 2005; Montuelle et al., 2012).
Because the success of jaw prehension lies in the positioning of the
skull on the prey, the movements of the anterior elements of the
locomotor system (the forelimbs and the cervical region of the
vertebral column) are expected to be coordinated with jaw
movements, and locomotor–feeding integration is thus likely a key
functional component of jaw prehension (Montuelle et al., 2012).
Our hypothesis was that because jaw prehension is utilized
successfully and efficiently to capture different prey types,
locomotor–feeding integration may be flexible to respond to changes
in prey properties. Alternatively, if locomotor–feeding integration
during jaw prehension is found to be inflexible in response to
variability in prey properties, the motor control of locomotor–feeding
integration may be independent from dietary constraints.
Our primary objective was to compare the jaw–neck–forelimb
coordination patterns associated with the capture of prey varying
in two properties: size and mobility, the effects of these two
properties on feeding movements being well documented in lizards
(e.g. Bels and Baltus, 1988; Herrel et al., 1996; Delheusy and Bels,
1999; Herrel et al., 1999; Schaerlaeken et al., 2007; Schaerlaeken
et al., 2008; Metzger, 2009; Montuelle et al., 2009b; Montuelle et
al., 2010; Schaerlaeken et al., 2011). Regarding prey size (here
represented by prey length), we expected that the larger the prey,
the higher the cranio-cervical system would have to rise.
Consequently, we expected the capture of large prey to be
characterized by a wider gape to accommodate the size of the prey
item to be ingested, and a higher neck elevation, coupled with greater
extension of the forelimbs, to lift the cranio-cervical system of the
predator above the prey. In contrast, we expected the capture of
small prey to be characterized by small maximum gape, as well as
a reduced elevation of the neck (i.e. the neck would remain close
to its rest position) and flexion of the forelimbs so that the head
drops down to the ground to pick up the prey.
Regarding prey mobility, we hypothesized that the quicker the
prey, the quicker the predator would strike. Thus, we expected jaw
movements to be quicker when feeding on evasive prey, i.e. jaw
opening to occur late and maximum gape angle to occur just before
or at the same time as predator–prey contact. Additionally, we
predicted that maximum gape would be greater for the capture of
evasive prey. Indeed, evasive prey change position in space
constantly and in an unpredictable manner; therefore, wider jaw
opening is necessary to encompass the range of potential prey
positioning during the strike. According to recent data on prey
capture in lizards (Montuelle et al., 2012), quick strikes are based
on a jaw–neck coordination pattern that supports a lunge onto the
prey; thus, maximum neck elevation would occur just before or at
the same time as jaw opening (i.e. at the start of the strike), and the
neck would subsequently lower as the predator lunges on its prey.
In contrast, the capture of immobile prey may not need a quick
strike; thus, we would expect maximum neck elevation to occur
later in the jaw-opening phase, i.e. closer to maximum gape and
predator–prey contact. Alternatively, because a quick strike is not
required, feeding on immobile prey may not require the precise
coordination of jaw movements with those of the neck and forelimbs,
which might lead to variability in the timing of neck elevation and
forelimb flexion–extension with respect to jaw opening. Finally, we
expected the forelimbs to support the strike by extending during
jaw opening to thrust the head forward onto the evasive prey. For
the capture of immobile prey, the extension of the forelimb may
not be as great as it merely supports the elevation of the cranio-
cervical system.
MATERIALS AND METHODS
Animal husbandry
Two adult individuals of Varanus ornatus (Daudin 1803) and one
adult individual of Varanus niloticus (Linnaeus 1758) (snout–vent
length 480±11mm) were purchased from a commercial animal
dealer. Varanus niloticus and V. ornatus are closely related (Böhme,
2003) and used to be considered different subspecies (e.g. Luiselli
et al., 1999). Because their feeding morphology and behavior are
similar, individuals of both species were grouped in the analysis.
They were maintained individually in large vivaria (1.5m
long⫻1.5m deep⫻30cm high) on a 12h:12h light/dark cycle.
The Journal of Experimental Biology 215 (21)
THE JOURNAL OF EXPERIMENTAL BIOLOGY
3825Flexible locomotor–feeding integration
Temperature was set at 24–30°C during the day, with a basking
spot at the higher temperature, and a temperature of no lower than
24°C during the night. Water was available ad libitum and the lizards
were fed mice and grasshoppers twice a week.
Experimental set-up
A trackway (420⫻60cm) covered with non-slip green plastic
flooring was used for the experiments. At one end, a wooden box
(60⫻60⫻60cm) with a sliding door provided the animal with a place
to rest between trials. A heating lamp provided a basking spot in
front of the box. At the other end, a Plexiglas box (60⫻60⫻60cm)
covered the area filmed by the cameras. Each individual was
maintained for 1week, during which recording sessions were
organized daily. After enough data were recorded for the first
individual, the second individual was brought in for 1week and
subjected to daily recording sessions, followed by the third. The
trackway was cleaned between trials. At the beginning of each
recording session, the individual was allowed to walk along the
trackway to become familiar with the experimental set-up. Between
trials, the individual was kept in the wooden box with the door shut.
During trials, the prey item was placed in the area covered by the
cameras. All prey items were oriented with their long axis
perpendicular to the long axis of the predator’s head. For mobile
prey, as their orientation varied during the approach of the predator,
only strikes on perpendicularly oriented prey were analyzed. The
door of the box was subsequently opened and we then waited for
the animal to spontaneously initiate foraging along the trackway
and strike on the prey item.
Prey capture was recorded at 200framess–1 using four
synchronized high-speed cameras (Prosilica GE680, Allied Vision
Technologies GmbH, Stadtroda, Germany). Two cameras were set
up in dorsal view, filming through the Plexiglas sheet above the
trackway. One camera was set up in oblique frontal view, filming
through the Plexiglas sheet placed at the end of the trackway. The
fourth camera was installed in lateral view. In this way, the
anatomical points of interest were visible in at least three of the
four views during the whole sequence recorded. Cameras were
calibrated and scaled using a DLT routine based on the digitization
of a black-and-white checkerboard composed of ten by ten 1⫻1cm
squares.
Data set
Four prey types were offered during the recording session:
grasshoppers (Locusta migratoria, 44±1mm), live newborn mice
(Mus musculus, 39±1mm), adult mice (M. musculus, 90±1mm) and
dead adult mice (M. musculus, 87±3mm). The length of every prey
item was measured using a pair of calipers before being offered.
To quantify prey mobility, the maximum speed of the prey during
the approach of the predator was extracted from the displacement
of the prey point over time. These four prey types were chosen as
they represent prey of different length and mobility (Fig.1):
grasshoppers are small and evasive prey, newborn mice are small
prey with reduced mobility, adult mice are large and mobile prey,
and dead adult mice are large and immobile prey. This allowed us
to assess the effect of prey length in mobile (grasshoppers versus
adult mice) and immobile prey (newborn mice versus dead adult
mice), and the effect of mobility in two length categories (small
prey: grasshoppers versus newborn mice; large prey: adult mice
versus dead adult mice).
Twenty sequences representing the successful capture of
grasshoppers were analyzed (eight, seven and five sequences for
each individual, respectively; Fig.2A), seven sequences for newborn
mice (four and three sequences for the two V. ornatus individuals
only; Fig.2B), 12 sequences for adult mice (five, four and three for
each individual, respectively; Fig.2C), and nine sequences for dead
adult mice (three for each individual; Fig.2D). Note that during the
recording sessions, prey types were offered in random order to avoid
learning effects.
Kinematic analysis
Seven markers were painted on the body: the tip of the lower and
upper jaws, the corner of the mouth, on a point halfway between
the occipital and the pectoral girdle, and on the shoulder, the elbow
and the wrist joints (Fig.2). These markers were digitized on each
frame for each camera view. Screen coordinates of the digitized
markers were extracted for each of the four camera views and their
position in 3D over time was calculated using the calibration. The
position of the prey (point at the insertion of the head on the
prothorax or the trunk) and the position of the eye of the predator
were also digitized to quantify movements of the predator relative
to the prey during the strike. Quantifying movements of skeletal
elements based on external markers must be performed carefully
because of the movements of the skin, but here we believe that
potential error is reduced because of the small amount of soft tissue
between the skin and the actual skeletal elements of interest. We
acknowledge this as a limitation in our study. Additionally, although
we recognize that the hindlimbs are important for propulsion during
the lunge, our study focuses on the movements of the forelimbs and
the cervical portion of the vertebral column because the requirements
for sufficient resolution in reconstructing movements in 3D based
on a multiple-camera set-up constrained the field of view.
Three kinematic profiles were constructed and variables were
extracted to quantify movements of the jaws, neck and forelimbs.
In these profiles, time was set at t0 at the instant of predator–prey
contact so that events occurring before contact are characterized by
negative time values, and events occurring after are characterized
by positive values. First, gape angle was calculated between the tip
of the upper jaw, the corner of the mouth and the tip of the lower
jaw (Fig.3A). From this profile, we extracted the time of the start
Prey length (mm)
20 40 60 80 100
Maximum prey velocity (cm s–1)
0
100
200
300
400
Fig.1. Prey properties of the four prey types tested in this study. The
length of each prey item was measured prior to being offered using a
digital caliper. Prey mobility is represented by the maximum velocity of
the prey item during the predatorʼs approach. Maximum prey velocity
was extracted from the 3D displacement of the point digitized at the
insertion of the head of the prey on the prothorax or the trunk, during
the predatorʼs approach. Prey types are represented by different colored
symbols: grasshoppers, green circles; newborn mice, yellow diamonds;
adult mice, red triangles; and dead adult mice, blue squares.
THE JOURNAL OF EXPERIMENTAL BIOLOGY
3826
of jaw opening, the time of maximum gape angle, and the amplitude
of maximum gape angle (Table1). Second, neck elevation was
calculated as the difference in the Z-coordinate of the point on the
neck with respect to its position at rest (Fig.3B). Maximum neck
elevation and the time to maximum neck elevation were extracted
(Table1). Variation of neck height between the instant of jaw
opening and the instant of predator–prey contact was also calculated,
with negative values representing the neck being lowered during
the strike and positive values representing neck elevation. Finally,
elbow angle was calculated between the shoulder point, the elbow
point and the wrist point (Fig.3C). From this profile, four variables
were extracted: maximum elbow angle (representing maximum
extension of the forelimb at the elbow joint), minimum elbow angle
(representing maximum flexion of the forelimb at the elbow joint),
and the timing of both (Table1). Variation of elbow flexion between
the instant of jaw opening and the instant of predator–prey contact
was also calculated, with negative values indicating forelimb flexing
during the strike and positive values indicating forelimb extension.
Additionally, the distance between the predator and the prey was
calculated as the difference in position between the predator’s eye
and the position of the prey. From this, we extracted the
predator–prey distance at the onset of jaw opening to quantify how
far from the prey the predator initiates the strike (Table1). Finally,
based on the displacement of the eye of the predator over time, we
calculated the speed of the head during the strike, and extracted
maximum head velocity (Table1).
To estimate integration among jaw–neck–forelimb movements
at the functional level, we calculated the latency of maximum neck
elevation, maximum forelimb extension and maximum forelimb
flexion with respect to jaw opening. Latency was defined as the
difference between the time of occurrence of one event of interest
(i.e. maximum neck elevation, minimum and maximum elbow
angle) and the time to jaw opening (Fig.4). A latency value close
to 0 represents a movement being synchronized with jaw opening
(Fig.4A). A negative latency value represents a movement occurring
before the start of jaw opening (Fig.4B), whereas a positive value
represents a movement occurring after jaw opening (Fig.4C).
Statistical analysis
Normality was verified using histograms of frequency of
observations and Shapiro–Wilk’s tests for each variable. First,
ANOVA coupled to univariate F-tests considering the effects of
prey type (fixed factor) and individual (random factor), and the
corresponding interaction effects, were performed on the speed of
the head during the strike, as well as on the predator–prey distance
at the onset of jaw opening to identify significant differences in the
The Journal of Experimental Biology 215 (21)
t=–240
t=–90
t=–25
t=0
t=+25
A B C D
t=–350
t=–180
t=–35
t=0 t=0 t=0
t=+25 t=+25 t=+70
t=–325
t=–220
t=–20
t=–350
t=–250
t=–30
Fig.2. Frame sequences illustrating prey-capture behavior in Varanus ornatus feeding on four prey items varying in length and mobility: grasshoppers
(small/mobile; A), newborn mice (small/immobile; B), live adult mice (large/mobile; C) and dead adult mice (large/immobile; D). Each frame
corresponds to an event of interest, from top to bottom: preparation for the strike, start of jaw opening, instant of maximum gape, predator–prey
contact, bite. Time values are indicated, with time t0 being set at the instant of predator–prey contact.
THE JOURNAL OF EXPERIMENTAL BIOLOGY
3827Flexible locomotor–feeding integration
characteristics of the strike itself. Note that non-significant
interaction effects were removed from the final design of the
ANOVA. Bonferroni post hoc tests were used to test differences
among the four prey-types tested, and among the three individuals.
Factor analyses were performed on jaw variables, neck variables
and forelimb variables separately to reduce the dimensionality of
the data set. Multivariate factors with eigenvalues greater than 1
were retained for the rest of the analysis. Jaw factors, neck factors
and forelimb factors were submitted to ANOVA coupled to
univariate F-tests with prey type entered as a fixed factor, and
individual as a random factor. Non-significant interaction terms were
removed from the final model, and Bonferroni post hoc tests were
used to test differences among the four prey types tested. To
determine the pattern of coordination between jaw, neck and
forelimb movements, the bivariate correlations between the jaw
factors with the neck factors and with the forelimb factors were
tested for each prey type separately. To assess the flexibility of the
jaw–neck–forelimb coordination pattern in response to prey types,
the characteristics of the significant correlations (i.e. the Pearson’s
coefficient r, the slope and the intercept) were compared between
prey types. The Pearson’s correlation coefficients were compared
between prey types using Fisher’s z-test (Fisher, 1921), whereas the
slopes and the intercepts were compared using Student’s t-tests.
To investigate the flexibility of jaw–neck–forelimb
synchronization, the latency of neck elevation, forelimb flexion and
forelimb extension with respect to jaw opening were submitted to
ANOVA coupled to univariate F-tests. Prey type was entered as a
fixed factor and individuals as a random factor, and non-significant
interaction terms were removed from the final model. Bonferroni
post hoc tests were performed on the prey-type factor to test which
prey type differs from the others. To quantify the extent to which
synchronization between jaws and neck movements is altered in
response to prey size, bivariate correlations between the latency of
neck elevation with respect to jaw opening and prey size were tested
for each of the four prey types separately. Similarly, bivariate
correlations between the latency of neck elevation with respect to
jaw opening and the maximum velocity of the prey during the
predator’s approach was tested for mobile prey (i.e. grasshoppers
and mice) to determine the effect of prey mobility on jaw–neck
synchronization. Latency of forelimb flexion and of forelimb
extension were submitted to the same procedure. The characteristics
of the significant correlations were compared between prey types:
the Pearson’s correlation coefficients using Fisher’s z-test (Fisher,
1921), the slopes and the intercepts using Student’s t-tests.
RESULTS
Prey-capture behavior in varanid lizards
Similar to other varanid lizards, V. ornatus and V. niloticus make
use of extensive tongue-flicking while approaching prey, suggesting
that chemoreception is used to detect and locate different prey items
(see Cooper, 1989; Kaufman et al., 1996; Cooper and Habegger,
2001). Typically, V. ornatus and V. niloticus stop between 7 and
12cm from the prey (see Table1), then the jaws open and the strike
is initiated (see Montuelle et al., 2012). As expected, jaw prehension
was always used during prey capture (Schwenk, 2000; Vitt et al.,
2003; Vitt and Pianka, 2005; Montuelle et al., 2012). For both types
of evasive prey, the successful/missed trials ratio was greater than
50%: 30 successful captures of live grasshoppers out of the 51
sequences observed (63.8% of success), 11 successful captures of
adult mice out of the 16 sequences observed (68.8% of success);
no missed trial was observed when feeding on immobile prey (i.e.
newborn mice and dead adult mice).
–300 –200 –100 0 100
Gape angle (deg)
0
10
20
30 Open
Close
A
–300 –200 –100 0 100
Neck height (cm)
7
8
9
10
11 Rises
Rest position
B
Time (ms)
–300 –200 –100 0 100
Elbow angle (deg)
80
100
120
140
160
Extension
Flexion
C
Fig.3. Representative kinematic profiles associated with
the movement of the feeding (jaws) and locomotor
(vertebral column and forelimb) systems during prey
capture in Varanus niloticus and V. ornatus. (A)Gape
angle is calculated as the angle between the upper and
lower jaw, representing the opening–closing movements
of the jaw. (B)Neck height is extracted from the Z-
coordinate of the point digitized on the neck, illustrating
the rise of the neck above the ground with respect to its
rest position. (C)Elbow angle is calculated as the angle
between the shoulder point, the elbow point and the wrist
point, quantifying the flexion–extension movements of the
forelimb. Time t0 was set at the instant of predator–prey
contact (dashed line) so that negative time values
represent events occurring before predator–prey contact,
whereas positive time values represents events occurring
afterwards. Prey types are represented by colored
symbols: grasshoppers, green circles; newborn mice,
yellow diamonds; adult mice, red triangles; and dead adult
mice, blue squares.
THE JOURNAL OF EXPERIMENTAL BIOLOGY
3828
The strike consists of a lunge on the prey with the jaws opened.
Maximum gape occurs shortly before predator–prey contact
(Fig.3A), suggesting that jaw closing is initiated without any sensory
feedback from the prey. The lunge on the prey is characterized by
the neck height dropping down during the strike, but the neck
movements involved during prey capture vary between the prey
types investigated here (Fig.3B). The neck remains high above its
resting position all along the strike when feeding on large prey items
(adult mice; Fig.2C, Fig.3B), whereas the neck is lowered further
to bring the skull closer to the ground so that the jaws can pick up
small prey items such as grasshoppers and newborn mice (Fig.2A,B,
Fig.3B). Similarly, the forelimb angular configuration at the elbow
joint is different between prey types (Fig.3C). During the capture
of dead adult mice, the forelimb extends continuously while the
jaws open (Fig.2D, Fig.3C). In contrast, the forelimb flexes during
jaw opening when feeding on adult mice (Fig.2C, Fig.3C). Forelimb
flexion also occurs early in the strike on grasshoppers, but the
forelimb extends quickly during jaw opening (Fig.2A, Fig.3C).
Finally, forelimb movements are limited during the capture of small
motionless prey like newborn mice (Fig.2B, Fig.3C).
Varability in strike in response to prey type
Maximum velocity of the head during the strike is also significantly
different among prey types (F3,4213.339, P<0.001; see Table1).
Post hoc tests demonstrate that strikes on grasshoppers are
significantly quicker than on newborn mice (P0.006) and dead adult
mice (P<0.001). Strikes on live adult mice are also significantly
quicker than on newborn mice (P0.021) and dead adult mice
(P<0.001). These results show that strikes are faster when feeding
on evasive prey. Head velocity is different among individuals
(F2,4215.800, P<0.001), indicating that the strikes of both
individuals of V. ornatus are quicker than those of the one individual
of V. niloticus (P<0.001 for both post hoc tests between individuals).
Prey type ⫻individual interaction effects are not significant.
Predator–prey distance at the onset of jaw opening is significantly
different among the four prey types (F3,427.264, P<0.001), and
post hoc tests reveal that jaw opening is initiated at a greater distance
from the prey when striking on grasshoppers (see Fig.2A, Table1)
than when striking on newborn mice (P0.013; Fig.2B, Table1),
adult mice (P0.036; Fig.2C, Table1) or dead adult mice (P0.027;
Fig.2D, Table1). This suggests that varanids stop further away from
the prey when preparing a strike on small evasive prey like
grasshoppers, probably to avoid eliciting anti-predator behavior from
the prey. Significant individual differences are also observed in the
predator–prey distance at the onset of jaw opening (F2,4212.108,
P<0.001), with post hoc tests indicating that the one individual of
V. niloticus moves closer to the prey before initiating a strike
compared with the two individuals of V. ornatus (P<0.001 and
P0.004, respectively). Prey type ⫻individual interaction effects
are not significant.
Variability in jaw, neck and forelimb movements in response
to prey types
One multivariate factor was defined by the factor analysis,
representing 50.9% of the variance of jaw kinematics. The jaw factor
is correlated with time to jaw opening and maximum gape angle
(Table2). In the ANOVA of jaw factor, the prey type ⫻individual
interaction term is significant, indicating individuals respond
differently to changes in prey type. Prey-type effect is significant
for each individual (F3,168.546, P0.001; F3,1314.481, P<0.001;
F2,84.921, P0.04); see Table3 for the individual results of the
post hoc tests.
The Journal of Experimental Biology 215 (21)
Table1. Summary of the kinematic variables associated with jaw movements, neck elevation and forelimb flexion–extension at the elbow
joint during prey capture behavior of Varanus niloticus and Varanus ornatus
Grasshopper N20 Newborn mice N7 Adult mice N12 Dead adult mice N9
Prey
Length (cm) 4.37±0.79 3.86±1.37 9.04±1.30 87.06±2.86
Length category Small Small Large Large
Maximum speed (cms–1) 195.9±21.8 1.7±1.5 41.5±10.5 0
Mobility category Mobile Immobile Mobile Immobile
Jaw movements
Time of the start of jaw opening (ms) –176±15 –226±26 –195±27 –288±30
Maximum gape angle (deg) 32.8±0.7 19.6±1.5 28.3±1.0 24.4±1.1
Time of maximum gape angle (ms) –23±4 –35±7 –28±4 –12±7
Neck movements
Maximum neck elevation (cm) 4.74±0.39 5.44±0.13 5.68±0.58 4.68±0.56
Time of maximum neck elevation (ms) –154±18 –244±34 –163±34 –154±31
Latency of maximum neck elevation (ms)* 22±15 –19±40 32±29 133±32
Variation of neck elevation during the strike (cm) –2.22±0.23 –1.28±0.26 –0.87±0.19 –0.59±0.17
Forelimb movements
Minimum elbow angle (deg) 82.9±1.6 113.2±6.6 105.9±6.9 91.2±8.1
Time of minimum elbow angle (ms) –102±27 –97±49 –67±32 –291±48
Latency of minimum elbow angle (ms)* 74±32 128±67 128±46 –3±36
Maximum elbow angle (deg) 108.0±3.0 127.2±8.2 124.4±6.6 112.6±10.0
Time of maximum elbow angle (ms) –72±27 –208±49 –128±40 –64±26
Latency of maximum elbow angle (ms)* 104±28 18±37 68±31 223±43
Variation of elbow angle during the strike (deg) 0.9±3 –2.6±2.6 –4.2±3.4 6.8±7.1
Strike performance
Predator–prey distance at jaw opening (cm) 12.84±1.39 7.68±0.32 9.05±0.78 8.52±0.62
Maximum head velocity during the strike (cms–1) 103.3±8.9 61.4±8.0 101.7±11.8 47.0±6.0
The capture of four different prey types varying in length and mobility was recorded (see Fig.2).
Nrepresents the number of sequences analyzed. Table entries are means ± s.e.m.
*Standardized with respect to jaw opening.
THE JOURNAL OF EXPERIMENTAL BIOLOGY
3829Flexible locomotor–feeding integration
Two multivariate factors represent 71.8% of the total variance of
the kinematics associated with neck elevation. Neck factor 1 represents
37.7% of the total variance and is correlated with maximum neck
elevation (positively) and variation in neck height during the strike
(negatively; Table2). ANOVA reveals that prey-type effects are
significant on neck factor 1 (F3,425.285, P0.003) with neck lowering
when striking on grasshoppers, whereas it is kept at rest position during
the capture of dead mice (P0.001; Fig.5A, Table1). Individual
differences are also significant (F2,4233.841, P<0.001) revealing that
the neck of both individuals of V. ornatus elevates higher than in the
one individual of V. niloticus. Neck factor 2 represents 34.1% of the
total variance and is correlated with the time to maximum elevation
of the neck (Table2). No prey-type or individual effects are found
on neck factor 2.
Two multivariate factors represent 85.1% of the total variance
of the kinematics describing forelimb movements at the elbow joint.
Elbow factor 1 represents 48.3% and is correlated positively with
variation of elbow angle during the strike and the time to maximum
elbow angle, and negatively with the time to minimum elbow angle
(Table2). Prey-type effects approach significance on elbow factor
1 (F3,422.769, P0.053; Fig.5B), but individual effects are not
significant. Elbow factor 2 represents 36.8% and is correlated with
Table2. Summary of the factor analysis performed on the kinematic variables associated with jaw movements, neck elevation and forelimb
flexion–extension at the elbow joint during prey-capture behavior of Varanus niloticus and Varanus ornatus
Jaw factor (50.85%)
Time to jaw opening 0.865
Maximum gape angle 0.845
Time to maximum gape angle 0.251
Neck factor 1 (37.71%) Neck factor 2 (34.08%)
Maximum neck elevation 0.776 0.304
Time to maximum elevation of the neck –0.001 0.934
Variation of neck height during the strike –0.724 0.304
Elbow factor 1 (48.27%) Elbow factor 2 (36.82%)
Minimum elbow angle –0.24 0.969
Time to minimum elbow angle –0.883 –0.045
Maximum elbow angle 0.098 0.965
Time to maximum elbow angle 0.876 –0.072
Variation of elbow angle during the strike 0.895 0.135
Values in bold are loadings greater than 0.70 (Velicer and Fava, 1998).
0 deg
(jaws are
closed)
Time of
maximum gape angle
Time
Rest
position
Time Time of maximum
elevation of the neck
Opening duration
0 deg
(jaws are
closed)
Time of
maximum gape angle
Time
Gape
Angle
Neck
Elevation
Rest
position
Time Time of maximum
elevation of the neck
Opening duration
B
0 deg
(jaws are
closed)
Time
Rest
position
Time Time of maximum
elevation of the neck
Opening duration
A
Time of
jaw opening
C
Maximum neck elevation is synchronized with jaw opening:
latency of maximum neck elevation with respect to jaw
opening =0.
Maximum neck elevation occurs before jaw opening: latency
of maximum neck elevation with respect to jaw opening <0.
Maximum neck elevation occurs after jaw opening: latency
of maximum neck elevation with respect to jaw opening >0.
Gape
Angle
Neck
Elevation
Gape
Angle
Neck
Elevation
Fig.4. Schematic diagrams illustrating the calculation of latency of maximum neck elevation with respect to jaw opening, which is used to determine
the jaw–neck coordination pattern. First, both neck elevation (top) and gape angle (bottom) profiles are synchronized in time according to t0 at the
instant of predator–prey contact. Then, the difference in time between maximum neck elevation (blue dotted arrow) and jaw opening (black dashed
line) is calculated. Three cases are illustrated. (A)Maximum neck elevation is synchronized with jaw opening: latency with respect to jaw opening is
zero. (B)Maximum neck elevation occurs before jaw opening: latency with respect to jaw opening is represented by a negative value. (C)Maximum
neck elevation occurs later in the jaw-opening phase (e.g. close to maximum gape angle): latency with respect to jaw opening is represented by a
positive value. Latency of forelimb flexion at the elbow joint and latency of forelimb extension at the elbow joint were calculated using the same
procedure (modified from Montuelle et al., 2012).
THE JOURNAL OF EXPERIMENTAL BIOLOGY
3830
minimum and maximum elbow angle (Table2). The prey type ⫻
individual interaction term is significant on elbow factor 2, so prey-
type effects were tested for each individual separately. Prey-type
effects are significant in the two V. ornatus individuals (F3,169.675,
P0.001 and F3,165.124, P0.015, respectively), but not in the V.
niloticus individual. Specifically, in both individuals of V. ornatus,
the elbow joint is more extended during the capture of mice than
during the capture of grasshoppers (Table3).
Variability in jaw–neck–forelimb integration in response to
prey types
To investigate jaw–neck–forelimb integration, correlations between
jaw factor and the neck and elbow factors were tested for each prey
type separately. No correlations were significant during the capture
of newborn mice and of dead adult mice. In contrast, the jaw factor
is positively correlated with neck factor 2 during the capture of
grasshoppers and adult mice (r0.639, P0.002 and r0.658,
P0.02, respectively; Fig.6A) illustrating the integration of jaw
opening with neck elevation during the capture of evasive prey. This
shows that during the capture of grasshoppers and adult mice, the
later and wider the jaws open (i.e. the closer to predator–prey contact;
Fig.2A,C), the later maximum elevation of the neck occurs (i.e.
closer to predator–prey contact), showing that jaw movements and
neck movements are delayed concomitantly during the capture of
evasive prey, demonstrating their integration. The capture of adult
mice is also characterized by the correlation of the jaw factor with
neck factor 1 (r0.754, P0.005; Fig.6B) as well as with elbow
factor 2 (r0.599, P0.040; Fig.6C), indicating that the later and
wider the jaws open, the higher the neck rises and the greater the
extension of the forelimb at the elbow joint.
To investigate flexibility in jaw–neck–forelimb integration, we
compared the correlation coefficients between prey types. Only the
correlation between the jaw factor and neck factor 2 is common to
the capture of two different prey types (i.e. grasshoppers and adult
mice; Fig.6A). The Pearson’s correlation coefficients are not
significantly different (z–0.080, P0.468), and the slope of the
correlation is not significantly different either (t–0.409, P0.343).
However, the intercept differs between the capture of grasshoppers
and adult mice (t–2.347, P0.013), showing that maximum neck
elevation is achieved closer to predator–prey contact during the
capture of larger prey (i.e. adult mice) so that the head is raised
over the prey item. This indicates that the jaw–neck integration
pattern characterizing evasive prey is flexible in response to prey
length.
Variability in the synchronization of jaw, neck and forelimb
movements in response to prey properties
Synchronization of neck and forelimb movements with jaw
opening is also altered in response to prey type (Fig.7). The
analysis of variance performed on the latency of neck elevation
with respect to jaw opening reveals that prey-type effects are
significant (F3,424.121, P0.012), with maximum neck elevation
occurring significantly later in the jaw-opening phase during the
capture of dead mice (Fig.2D, Fig.4C, Fig.7D, Table1) than
during the capture of newborn mice (post hoc test P0.008; Fig.2B,
Fig.4B, Fig.7B, Table1) and grasshoppers (post hoc test P0.017;
Fig.2A, Fig.4A, Fig.7A, Table1). This indicates that maximum
neck elevation is synchronized with the instant of jaw opening
during the capture of small prey, whereas it is delayed in the jaw-
opening phase during the capture of large immobile prey. Latency
The Journal of Experimental Biology 215 (21)
Elbow factor 1 (48.3%)
–2 –1 0 1 2 3
Elbow factor 2 (36.8%)
–3
–2
–1
0
1
2
3
B
Elbow
extended
Elbow
flexed
Early flexion
late extension
Late flexion
early extension
Neck factor 1 (37.7%)
–3 –2 –1 0
1 2 3
Neck factor 2 (34.1%)
–3
–2
–1
0
1
2
3
A
Late maximum
neck elevation
Early maximum
neck elevation
Neck rises above
rest position
Neck remains close
to rest position
Fig.5. Multivariate spaces representing variation in the kinematics associated with neck elevation (A) and elbow configuration (B) during prey-capture
behavior in V. ornatus and V. niloticus feeding on different prey types. For each factor, the percentage of variance explained is indicated, as are the
kinematic variables loading on each factor (see Table2 for the complete composition of the multivariate factors). Prey types are represented by
colored symbols: grasshoppers, green circles; newborn mice, yellow diamonds; adult mice, red triangles; and dead adult mice, blue squares.
Table3. Summary of the prey-type effects on jaw and forelimb kinematics for each individual
Individual no. 1 Varanus ornatus Individual no. 2 Varanus ornatus Individual no. 3 Varanus niloticus
Jaw factor Newborn mice<grasshoppers (P0.002) Newborn mice<grasshoppers (P0.004) Grasshoppers>mice (P0.042)
Newborn mice<dead mice (P0.007) Dead mice<grasshoppers (P<0.001)
Dead mice<mice (P0.016)
Elbow factor 2 Grasshoppers<mice (P0.008) Grasshoppers<mice (P0.026)
Newborn mice>grasshoppers (P0.002)
Newborn mice>dead mice (P0.025)
ANOVA performed on the multivariate factors (see Table 2) reveal that the prey type ⫻individual interaction term is significant on the jaw factor and on elbow
factor 2, indicating different prey-type effects in each individual. Consequently, prey-type effects were tested for each individual separately, and the
significant Bonferroni post hoc tests are reported here to identify which prey type differs from the others.
THE JOURNAL OF EXPERIMENTAL BIOLOGY
3831Flexible locomotor–feeding integration
of maximum elbow angle is also affected by prey type
(F3,424.045, P0.013). Forelimb extension at the elbow joint is
achieved later in the jaw-opening phase (i.e. closer to predator–prey
contact) during the capture of dead mice (Fig.2D, Fig.4C, Fig.7D)
than during the capture of newborn mice (post hoc test P0.009;
Fig.2B, Fig.4A, Fig.7B) and adult mice (post hoc test P0.031;
Fig.2C, Fig.4A, Fig.7C). This reveals that maximum extension
of the forelimb at the elbow joint is synchronized with the instant
of jaw opening for the capture of newborn and adult mice, whereas
it is synchronized with maximum gape for the capture of dead
adult mice. No effects of prey type are significant on the latency
of minimum elbow angle. Finally, there are no significant
individual differences in the latency of neck elevation or on the
latency of minimum and maximum elbow angle.
The effects of prey length and prey mobility on the latency of
neck and forelimb movements with respect to jaw opening were
analyzed for each prey type separately. Prey length has no effect
on the latency of neck elevation, the latency of minimum elbow
angle or the latency of maximum angle in any of the four prey types
tested in our analysis. In contrast, prey mobility, described by the
maximum velocity of the prey during the approach of the predator,
is correlated with the latency of minimum elbow angle in
grasshoppers and adult mice (r0.512, P0.021 and r0.600,
P0.039, respectively; Fig.8A). This shows that forelimb flexion
is delayed closer to maximum gape and predator–prey contact for
the capture of quick prey (see Fig.4C). This late flexion of the
forelimb may be used to counter the inertia created by the body
during the strike, reducing the speed of the head as predator–prey
contact approaches. The Pearson’s correlation coefficients associated
with each correlation are significantly similar (z–0.312, P0.378),
as are their intercepts (t–0.915, P0.184). However, the difference
between the slopes of the correlation associated with each prey
approaches significance (t–1.640, P0.056), suggesting that the
latency of elbow flexion is more sensitive to changes in prey velocity
in adult mice than in grasshoppers (Fig.8A). This shows that the
effects of prey mobility on jaw–forelimb coordination are altered
in response to the length of the prey. The maximum velocity of
grasshoppers is also correlated with latency of maximum elbow
angle (r–0.482, P0.032; Fig.8B), indicating that the capture of
small and quick prey is characterized by the earlier extension of the
forelimb at the elbow joint.
DISCUSSION
In accordance with our predictions, our data show that varanid lizards
use a specific jaw–neck coordination pattern for the capture of
different prey items that vary in length and mobility (Figs3, 7).
Strikes on grasshoppers (small evasive prey) have more in common
with the strikes on live adult mice (large evasive prey) than with
the strikes on newborn mice (motionless prey of similar size),
suggesting that the effects of prey mobility overcome those of prey
size. Indeed, in addition to the fact that strikes on grasshoppers and
live adult mice are quick strikes (Table1), strikes on all sizes of
evasive prey are similar in that they are characterized by a strong
link between jaw movements and neck elevation: if one is delayed,
then the other is delayed concomitantly (Fig.6A). The capture of
grasshoppers is significantly quicker and is initiated further from
the prey, likely to avoid eliciting an anti-predator response (Table1).
The neck rises above its rest position to reach its maximum
elevation before jaw opening (Fig.3B, Fig.7A), and lowers quickly
after jaw opening as the predator lunges forward (Fig.2A, Fig.3B).
Finally, forelimbs flex and then quickly extend during the strike,
like a spring, likely contributing to the lunge by thrusting the cranio-
cervical complex forward towards the prey (Fig.2A, Fig.3C,
Fig.7A). During the strike on live adult mice, the neck rises similar
to the strikes on grasshoppers but does not lower as much as during
the strike on small prey (immobile or evasive ones; Fig.3B). Flexion
of the forelimbs is also observed during the strikes on live adult
mice, although it is not followed by a quick extension (Fig.3C,
Fig.7C). In this case, forelimb flexion is suggested to contribute to
the immobilization of large evasive prey by pinning the prey on the
ground, limiting the potential for prey escape after the strike.
To capture small motionless prey like newborn mice, the strike
is different in that it is initiated close to the prey. The strike on
newborn mice consists of the neck rising, supported by the extension
of the forelimb at the elbow joint (Fig.3B,C, Fig.7B). During the
jaw-opening phase, the neck lowers and the forelimbs flex to drop
the head down to the ground to pick up the prey item (Fig.2B,
Fig.3B,C, Fig.7B). The strike on dead adult mice is the most singular
among the strike strategies observed here. Strikes on large immobile
prey are the slowest and are initiated close to the position of the
prey (Table1). The neck rises slightly during jaw opening, remaining
close to its rest position, with maximum elevation being achieved
late in the jaw-opening phase. This indicates that neck elevation is
Jaw factor
–2 0 2
Neck factor 2
–2
0
2A
Late maximum
neck elevation
Wide and late
maximum gape
P=0.002
P=0.02
Jaw factor
Elbow factor 2
–2
0
2C
Elbow
extended
Wide and late
maximum gape
P=0.04
Jaw factor
Neck factor 1
–2
0
2B
Neck rises above
rest position
Wide and late
maximum gape
P=0.005
–2 0 2 –2 0 2
Fig.6. Bivariate correlations between the multivariate factors representing jaw movements and those representing neck and forelimb movements,
illustrating jaw–neck–forelimb integration during prey-capture behavior in V. ornatus and V. niloticus. Jaw factor is correlated with neck factor 2 during
the capture of grasshoppers and adult mice (A), indicating the timing of neck elevation is associated with the time and amplitude of maximum gape
during the capture of evasive prey. Jaw factor is also correlated with neck factor 1 (B) and elbow factor 2 (C) during the capture of adult mice,
indicating the amplitude of maximum neck elevation and the amplitude of elbow angle are both associated with the time and amplitude of maximum
gape. The kinematic variables loading on each factor are indicated (see Table2 for the complete composition of the factors). Prey types are
represented by colored symbols: grasshoppers, green circles; and adult mice, red triangles. Only the significant correlations are presented: note, no
bivariate correlation was found to be significant for immobile prey (i.e. newborn mice, dead adult mice).
THE JOURNAL OF EXPERIMENTAL BIOLOGY
3832
always initiated before jaw opening (Fig.3B, Fig.7A–C), but that
its duration is extended for the capture of large immobile prey to
allow the positioning of the head above the prey item. Finally, the
forelimbs extend slowly during the strike on dead adult mice in
order to bring the head of the predator above and forward towards
the prey item.
Within this repertoire of strike strategies, the
jaw–neck–forelimb coordination pattern is demonstrated to be
flexible in response to prey properties. Between the two prey
properties tested here, prey mobility appears to be a defining
parameter, over and above the size of the prey for instance, in
dictating what coordination pattern will be used. On the one hand,
predator–prey distance at which the predator stops before
initiating the strike (i.e. before opening the jaws) is greater for
both types of evasive prey than for any type of immobile prey
(see Table1). This indicates that varanid lizards are able to
ascertain the difference between evasive and immobile prey
during the approach, and choose the appropriate strike strategy
accordingly: stop far away and trigger a quick strike if targeting
an evasive prey, or keep approaching the target as long as no
movement is displayed (Fig.9). This demonstrates how prey
mobility is key information for the success of prey-capture
behavior in varanid lizards. By extension, it illustrates the
importance of sensory feedback from visual cues and
chemoreception during the approach of varanid lizards in order
to assess the risk of prey escape (Cooper, 1989; Garrett et al.,
1996; Kaufman et al., 1996; Cooper and Habegger, 2001; Chiszar
et al., 2009; Gaalema, 2011).
On the other hand, our data demonstrate how flexibility of
jaw–neck–forelimb integration is an important component of the
capture of evasive prey in varanid lizards (Figs6, 8). Indeed,
consistent jaw–neck integration patterns are observed during the
capture of both types of evasive prey (Fig.6A). However, despite
the consistency of this integration pattern (i.e. statistically similar
slope of bivariate correlations across experimental treatments), prey
length affects jaw–neck integration as the neck is raised higher
during the capture of large evasive prey. Such variability in the
jaw–neck integration pattern indicates that the jaw–neck integration
pattern characterizing the capture of evasive prey is flexible in
response to prey size (here represented by the length of the prey
item). This shows that prey-capture behavior in omnivorous
predators like varanid lizards is not solely based on the flexibility
of feeding movements but, rather, involves the flexibility of the
integration pattern coupling the feeding and locomotor movements.
This suggests that the motor control responsible for the integration
of multiple structures across different anatomical systems might be
modulated, although the neurological dimension of this hypothesis
remains to be investigated.
Furthermore, our results show that jaw–forelimb integration is
flexible in response to the maximum velocity of the prey during the
approach of the predator (i.e. prior to the strike; Fig.8A). When
striking on very active prey, varanids alter the jaw–forelimb
coordination pattern so that forelimb flexion is delayed in the jaw-
opening phase (i.e. closer to maximum gape; Fig.8A). Because the
jaw–forelimb integration pattern is different during the capture of
grasshoppers and adult mice (Fig.7A,C), the flexibility in response
to prey velocity yields different behavioral outputs. During the
capture of adult mice, the late flexion of the forelimb at the elbow
joint illustrates how forelimb flexion is delayed to occur closer to
predator–prey contact (Fig.8A), supporting our hypothesis that
forelimb flexion plays a role in securing the prey after the strike.
During the capture of grasshoppers, forelimb flexion occurs before
The Journal of Experimental Biology 215 (21)
A
Maximum
neck elevation
Minimum
elbow angle
Maximum
elbow angle
Latency with respect
to jaw opening (ms)
–200 0 200 400
D
Maximum
neck elevation
Minimum
elbow angle
Maximum
elbow angle
–200 0 200 400
C
Maximum
neck elevation
Minimum
elbow angle
Maximum
elbow angle
–200 0 200 400
–200 0 200 400
B
Maximum
neck elevation
Minimum
elbow angle
Maximum
elbow angle
Fig.7. Flexibility of jaw–neck–forelimb coordination in response to prey
type during prey-capture behavior in V. ornatus and V. niloticus feeding
on different prey types. Latency (i.e. time difference) of maximum neck
elevation, maximum elbow angle and minimum elbow angle with respect
to jaw opening were calculated for each prey type: grasshoppers (A),
newborn mice (B), adult mice (C) and dead mice (D). Low latency values
indicate events occurring close to the start of jaw opening, whereas high
latency values indicate events occurring later in the jaw-opening phase
(i.e. closer to maximum gape and predator–prey contact; see Materials
and methods). Long-dash lines represent the start of jaw opening (at
latency0; see Fig.4A), short-dash line represents the instant of
maximum gape, and solid lines represent the instant of predator–prey
contact. Colored symbols represent outliers: grasshoppers, green circles;
adult mice, red triangles.
THE JOURNAL OF EXPERIMENTAL BIOLOGY
3833Flexible locomotor–feeding integration
the extension of the forelimb that thrusts the head of the predator
forward onto the prey. Consequently, the delay of the flexion
(Fig.8A) coupled with the early extension (Fig.8B) of the forelimb
at the elbow joint reveals a quicker extension that is proposed to
enhance head velocity during the strike.
Jaw–neck–forelimb integration during prey capture in varanid
lizards is flexible in response to both the mobility and the size of
evasive prey, suggesting that the motor control responsible for the
coordination of jaw, neck and forelimb movements can be
modulated. Indeed, our data demonstrate that different
jaw–neck–forelimb coordination patterns are used during the capture
of small versus large prey (Fig.6A, Fig.7, Fig.8A). First, because
prey length is constant throughout the feeding sequence, varanids
are probably able to assess the length of the prey while approaching
Maximum prey velocity (cm s
–1
)
0 100 200 300 400
Latency of minimum elbow angle
with respect to jaw opening (ms)
–200
0
200
400
0 100 200 300 400
–200
0
200
400
B
A
P=0.02
P=0.04 P=0.03
Latency of maximum elbow angle
with respect to jaw opening (ms)
Time
Time of
jaw opening
Time of
maximum gape
Instant of
predator–prey contact
Approach Pre-strike pause Jaw opening Jaw closing
Strike on the prey
Evasive prey
Stop further away from the prey
(Table 2)
Quick strikes (Table 2)
Jaw/neck coordination (Fig. 6A)
Max. neck elevation in sync. with
jaw opening (Fig. 7A,C)
Immobile prey
Keep approaching the
prey (Table 2)
Slow strikes (Table 2)
Large evasive prey
Neck rises and remains raised (Fig. 3B)
Extension/flexion of the forelimb (Fig. 7C)
Quick prey: max. flexion close to predator–prey contact (Fig. 8A) for pinning effect
Small evasive prey
Neck lowers quickly for lunge (Fig. 3B)
Flexion/extension of the forelimb (Fig. 3C) to thrust the head forward towards the prey
Quick prey: quick extension (Fig. 8A,B) to enhance thrust, thus speed, of the head
Small immobile prey
Neck rises with max. elevation in sync. with jaw opening
Neck lowers to drop the head to the ground to pick up the prey (Fig. 3B)
Flexion of the forelimb to support the lo wering of the cranio-cervical complex (Fig. 7B)
Large immobile prey
Neck rises slightly until max. neck elevation occurs close to max. gape (Fig. 7D)
Extension of the forelimb to bring the head over the prey (Fig. 3C)
The effects of prey mobility overtake
the effects of prey size during prey-
capture behavior of varanids
Fig.8. Effect of prey mobility on jaw–forelimb coordination during prey-capture behavior in V. ornatus and V. niloticus feeding on evasive prey
(grasshoppers and adult mice). (A)Maximum prey velocity is correlated with the latency of minimum elbow angle, indicating the capture of quick prey
involves the flexion of the forelimb at the elbow joint being delayed in the jaw-opening phase. (B)Maximum prey velocity is correlated with the latency
of maximum elbow angle during the capture of grasshoppers, indicating the capture of quick prey involves the extension of the forelimb at the elbow
joint occurring earlier in the jaw-opening phase. Prey types are represented by colored symbols: grasshoppers, green circles; and adult mice, red
triangles. Only the significant correlations are presented: note, no bivariate correlation between maximum prey velocity and the latency of maximum
neck elevation with respect to jaw opening was significant.
Fig.9. Synthesis of the study. In prey-capture behavior of varanid lizards, the effects of prey mobility on the jaw, neck and forelimb movements, and on
their integration, appear to supersede the effects of prey size (here quantified by prey length). The time scale (bottom), from prey approach to
predator–prey contact, highlights the time dimension of the proposed decision-making process: varanids are hypothesized to assess prey mobility first
as they stop further away from evasive prey to avoid eliciting an anti-predator response, then use specific strike strategies in response to the
secondary properties of the prey (e.g. length). Inspired by Monroy and Nishikawa (Monroy and Nishikawa, 2011).
THE JOURNAL OF EXPERIMENTAL BIOLOGY
3834
it and select a particular jaw–neck–forelimb integration pattern
before the strike (i.e. feed-forward modulation). Most importantly,
jaw–neck forelimb coordination appears to be an essential
characteristic of the capture of evasive prey (Figs6, 8, 9).
Consequently, varanids first assess the mobility of the target prey
(i.e. the escape risk) (see Gaalema, 2011), followed by an assessment
of its size (Fig.9). Given that prey mobility is a parameter that cannot
be anticipated during a single prey-capture trial, varanids may rely
on sensory-driven feedback modulation to adjust the
jaw–neck–forelimb integration pattern in response to changes in prey
velocity. Investigation of the neuronal pathways responsible for the
sensory control of locomotor–feeding integration is a promising
research direction for our understanding of feeding behavior in
vertebrates.
Previously, the functional consequences of an omnivorous diet
have mainly been documented as the flexibility in the movement
of the feeding structures (i.e. the jaws, the tongue, the hyobranchial
apparatus) (e.g. Liem, 1978; Herrel et al., 1999). Even though
flexibility in the movements of locomotor structures like the
forelimbs and the vertebral column (at least in the cervical region)
has also been reported in an omnivorous lizard (G. major)
(Montuelle et al., 2010), our data indicate that flexibility in
locomotor–feeding integration may be a key component in the ability
to feed on prey items that vary in their physical and mechanical
properties, especially mobility (Fig.9). This finding may be crucial
to understanding dietary specialization. Indeed, by feeding routinely
on the same food, selective pressures are imposed on the feeding
structures to optimize prey-capture efficiency (e.g. Herrel et al.,
1997; Ralston and Wainwright, 1997; Aguirre et al., 2003; Meyers
and Herrel, 2005; Herrel and De Vree, 2009). As changes in food
properties have been shown here to affect locomotor–feeding
integration in lizards using jaw prehension, particular food properties
are suggested to require particular locomotor–feeding integration
patterns (see Fig.9), and specialization in locomotor–feeding
integration may occur in response to diet. Varanid lizards are
specialized for feeding on ‘hard to catch’ prey (Losos and Greene,
1988). Given the strong effects of prey mobility on
jaw–neck–forelimb coordination (see Figs6, 8), flexibility of
locomotor–feeding integration in response to prey mobility is
proposed to be a key functional feature optimizing the capture of
evasive prey, and hence may contribute to the dietary specialization
of varanids. Our observations of the functional basis of jaw
prehension indeed suggest that the selective pressures stemming
from food properties may not be restricted to the feeding system
only but, rather, act at the whole-organism level, selecting for
patterns of locomotor–feeding integration flexible enough to respond
to variation in prey mobility.
ACKNOWLEDGEMENTS
We would like to thank two anonymous reviewers for their comments and
suggestions on the first version of the manuscript. We would also like to thank
Susan H. Williams at OU-HCOM for her comments during the writing of the
manuscript, and Donald B. Miles at Ohio University for his suggestions about data
analysis. We also thank ANR project Kameleon (ARA 05-MMSA-0002 ʻMasse de
Donnéesʼ), which provided the opportunity to use the synchronized camera set-up
at the Plateau Technique ʻBiologie des Organismesʼ (dpt ʻEcologie et Gestion de
la Biodiversitéʼ, MNHN) and Eric Pellé for his help with the animals.
FUNDING
This work is part of the PhD project of S.J.M. while at the Muséum National
dʼHistoire Naturelle (MNHN) in Paris, France, which was supported by the Legs
Prévost (MNHN), ANR 06-BLAN-0132-02 and Phymep Corporation. S.J.M. is now
a postdoctoral associate at Ohio University Heritage College of Osteopathic
Medicine (OU-HCOM) in Athens, OH, USA, supported by the National Science
Foundation [grant MRI DBI-0922988].
REFERENCES
Aguirre, L. F., Herrel, A., Van Damme, R. and Matthysen, E. (2003). The
implications of food hardness for diet in bats. Funct. Ecol. 17, 201-212.
Alfaro, M. E. (2003). Sweeping and striking: a kinematic study of the trunk during prey
capture in three thamnophiine snakes. J. Exp. Biol. 206, 2381-2392.
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, UK: BIOS Publishers.
Bels, V. L. and Baltus, I. (1988). The influence of food items on the feeding cycle in
Anolis equestris (Reptilia, Iguanidae). Copeia 1988, 479-481.
Bels, V. L., Chardon, M. and Kardong, K. (1994). Biomechanics of the hyolingual
system in Squamata. In Advances in Comparative and Environmental Physiology 18,
Biomechanics of Feeding in Vertebrates (ed. V. L. Bels, M. Chardon and P.
Vandewalle), pp. 197-240. Berlin, Germany: Springer-Verlag.
Böhme, W. (2003). Checklist of the living monitor lizards of the world (family
Varanidae). Zoologische Verhandelingen Leiden 341, 4-43.
Chiszar, D., Krauss, S., Shipley, B., Trout, T. and Smith, H. M. (2009). Response of
hatchling komodo dragons (Varanus komodoensis) at Denver Zoo to visual and
chemical cues arising from prey. Zoo Biol. 28, 29-34.
Cooper, W. E. (1989). Prey odor discrimination in the Varanoid lizards Heloderma
suspectum and Varanus exanthematicus. Ethology 81, 250-258.
Cooper, W. E., Jr and Habegger, J. J. (2001). Responses by juvenile savannah
monitor lizards (Varanus exanthematicus) to chemical cues from animal prey, plants
palatable to herbivores, and conspecifics. J. Herpetol. 35, 618-624.
Cundall, D. and Deufel, A. (1999). Striking patterns in Boiid snakes. Copeia 1999,
868-883.
Deban, S. M. (1997). Modulation of prey-capture behavior in the plethodontid
salamander Ensatina eschscholtzii. J. Exp. Biol. 200, 1951-1964.
Deban, S. M., OʼReilly, J. C. and Nishikawa, K. C. (2001). The evolution of the motor
control of feeding in amphibians. Am. Zool. 41, 1280-1298.
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.
Dumont, E. R. (1999). The effect of food hardness on feeding behaviour in frugivorous
bats (Phylostomidae): an experimental study. J. Zool. 248, 219-229.
Ferry-Graham, L. A. (1998). Effects of prey size and mobility on prey-capture
kinematics in leopard sharks Triakis semifasciata. J. Exp. Biol. 201, 2433-2444.
Ferry-Graham, L. A., Wainwright, P. C., Westneat, M. W. and Bellwood, D. R.
(2001). Modulation of prey capture kinematics in the cheeklined wrasse Oxycheilinus
digrammus (Teleostei: Labridae). J. Exp. Zool. 290, 88-100.
Ferry-Graham, L. A., Bolnick, D. I. and Wainwright, P. C. (2002). Using functional
morphology to examine the ecology and evolution of specialization. Integr. Comp.
Biol. 42, 265-277.
Fisher, R. A. (1921). On the ʻprobable errorʼ of a coefficient of correlation deduced
from a small sample size. Metron 1, 3-32.
Frazzetta, T. H. (1966). Studies on the morphology and function of the skull in the
Boidae (Serpentes). II. Morphology and function of the jaw apparatus in Python
sebae and Python molurus. J. Morphol. 118, 217-295.
Freeman, P. W. and Lemen, C. A. (2007). Using scissors to quantify hardness of
insects: do bats select for size or hardness? J. Zool. 271, 469-476.
Gaalema, D. E. (2011). Visual discrimination and reversal learning in rough-necked
monitor lizards (Varanus rudicollis). J. Comp. Psychol. 125, 246-249.
Garrett, C. M., Boyer, D. M., Card, W. C., Roberts, D. T., Murphy, J. B. and
Chiszar, D. (1996). Comparison of chemosensory behavior and prey trail-following in
the varanoid lizards Varanus gouldii and Heloderma suspectum. Zoo Biol. 15, 255-
265.
Griffen, B. D. and Mosblack, H. (2011). Predicting diet and consumption rate
differences between and within species using gut ecomorphology. J. Anim. Ecol. 80,
854-863.
Hampton, P. M. (2011). Comparison of cranial form and function in association with
diet in natricine snakes. J. Morphol. 272, 1435-1443.
Herrel, A. and De Vree, F. (2009). Jaw and hyolingual muscle activity patterns and
bite forces in the herbivorous lizard Uromastyx acanthinurus. Arch. Oral Biol. 54,
772-782.
Herrel, A., Cleuren, J. and Vree, F. (1996). Kinematics of feeding in the lizard Agama
stellio. J. Exp. Biol. 199, 1727-1742.
Herrel, A., Wauters, I., Aerts, P. and de Vree, F. (1997). The mechanics of ovophagy
in the beaded lizard (Heloderma horridum). J. Herpetol. 31, 383-393.
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.
Herrel, A., Vanhooydonck, B. and Van Damme, R. (2004). Omnivory in lacertid
lizards: adaptive evolution or constraint? J. Evol. Biol. 17, 974-984.
Herrel, A., Huyghe, K., Vanhooydonck, B., Backeljau, T., Breugelmans, K., Grbac,
I., Van Damme, R. and Irschick, D. J. (2008). Rapid large-scale evolutionary
divergence in morphology and performance associated with exploitation of a different
dietary resource. Proc. Natl. Acad. Sci. USA 105, 4792-4795.
Herrel, A., Deban, S. M., Schaerlaeken, V., Timmermans, J. P. and Adriaens, D.
(2009). Are morphological specializations of the hyolingual system in chameleons
and salamanders tuned to demands on performance? Physiol. Biochem. Zool. 82,
29-39.
Herrel, A., Huyghe, K., Okovic, P., Lisicic, D. and Tadic, Z. (2011). Fast and furious:
effects of body size on strike performance in an arboreal viper Trimeresurus
(Cryptelytrops) albolabris. J. Exp. Zool. 315A, 22-29.
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.
Homberger, D. G. (2003). The comparative biomechanics of a prey-predator
relationship: the adaptive morphologies of the feeding apparatus of Australian black
cockatoos and their foods as a basis for the reconstruction of the evolutionary
The Journal of Experimental Biology 215 (21)
THE JOURNAL OF EXPERIMENTAL BIOLOGY
3835Flexible locomotor–feeding integration
history of the Psittaciformes. In Vertebrate Biomechanics and Evolution (ed. V. L.
Bels, J.-P. Gasc and A. Casinos), pp. 203-228. Oxford, UK: BIOS Scientific
Publishers.
Hotton, N., III (1955). A survey of adaptive relationships of dentition to diet in the
North American Iguanidae. Am. Midl. Nat. 53, 88-114.
Janoo, A. and Gasc, J.-P. (1992). High speed motion analysis of the predatory strike
and fluorographic study of the oesophagal deglutition in Vipera ammodytes: more
than meets the eye. Amphibi.-Reptil. 13, 315-325.
Kane, E. A. and Higham, T. E. (2011). The integration of locomotion and prey capture
in divergent cottid fishes: functional disparity despite morphological similarity. J. Exp.
Biol. 214, 1092-1099.
Kardong, K. V. (1998). Rattlesnake strike behavior: kinematics. J. Exp. Biol. 201, 837-
850.
Kardong, K. V. and Bels, V. L. (1998). Rattlesnake strike behavior: kinematics. J.
Exp. Biol. 201, 837-850.
Kaufman, J. D., Burghardt, G. M. and Phillips, J. A. (1996). Sensory cues and
foraging decisions in a large carnivorous lizard, Varanus albigularis. Anim. Behav.
52, 727-736.
Korzoun, L. P., Erard, C. and Gasc, J.-P. (2001). Les particularités
morphofonctionnelles des appareils du bec et hyoïdien chez les touracos (Aves,
Musophagidae): relations avec la frugivorie. [Distinctive morphofunctional features of
the bill and hyoid apparatus of turacos (Aves, Musophagidae): their relation to
frugivory]. CRAS (Hum. Services Dev.) 324, 965-977.
Korzoun, L. P., Erard, C., Gasc, J.-P. and Dzerzhinsky, F. (2003). Les adaptations
de lʼhoazin (Opisthocomus hoazin) à la folivorie. Caractéristiques morphologiques et
particularités fonctionnelles des appareils du bec et hyoïdien. [Adaptation of the
Hoatzin (Opisthocomus hoazin) to folivory. Distinctive morphological and functional
features of its bill and hyoid apparatus]. CRAS (Hum. Services Dev.) 326, 75-94.
Kupczik, K. and Stynder, D. D. (2012). Tooth root morphology as an indicator for
dietary specialization in carnivores (Mammalia: Carnivora). Biol. J. Linn. Soc. Lond.
105, 456-471.
Liem, K. F. (1978). Modulatory multiplicity in functional repertoire of feeding
mechanism in cichlid fishes. 1. Piscivores. J. Morphol. 158, 323-360.
Losos, J. B. and Greene, H. W. (1988). Ecological and evolutionary implications of
diet in monitor lizards. Biol. J. Linn. Soc. Lond. 35, 379-407.
Luiselli, L., Akani, G. C. and Capizzi, D. (1999). Is there any interspecific competition
between dwarf crocodiles (Osteolaemus tetraspis) and Nile monitors (Varanus
niloticus ornatus) in the swamps of central Africa? A study from southeastern
Nigeria. J. Zool, Lond. 247, 127-131.
Metzger, K. A. (2009). Quantitative analysis of the effect of prey properties on feeding
kinematics in two species of lizards. J. Exp. Biol. 212, 3751-3761.
Metzger, K. A. and Herrel, A. (2005). Correlations between lizard cranial shape and
diet: a quantitative, phylogenetically informed analysis. Biol. J. Linn. Soc. Lond. 86,
433-466.
Meyers, J. J. and Herrel, A. (2005). Prey capture kinematics of ant-eating lizards. J.
Exp. Biol. 208, 113-127.
Monroy, J. A. and Nishikawa, K. (2011). Prey capture in frogs: alternative strategies,
biomechanical trade-offs, and hierarchical decision making. J. Exp. Zool. 315A, 61-71.
Montuelle, S. J., Herrel, A., Libourel, P. A., Reveret, L. and Bels, V. L. (2009a).
Locomotor–feeding coupling during prey capture in a lizard (Gerrhosaurus major):
effects of prehension mode. J. Exp. Biol. 212, 768-777.
Montuelle, S. J., Herrel, A., Schaerlaeken, V., Metzger, K. A., Mutuyeyezu, A. and
Bels, V. L. (2009b). Inertial feeding in the teiid lizard Tupinambis merianae: the
effect of prey size on the movements of hyolingual apparatus and the cranio-cervical
system. J. Exp. Biol. 212, 2501-2510.
Montuelle, S. J., Herrel, A., Libourel, P. A., Reveret, L. and Bels, V. L. (2010).
Separating the effects of prey size and speed on the kinematics of prey capture in
the omnivorous lizard Gerrhosaurus major. J. Comp. Physiol. A 196, 491-499.
Montuelle, S. J., Herrel, A., Libourel, P.-A., Daillie, S. and Bels, V. (2012). Prey
capture in lizards: differences in jaw-neck-forelimbs coordination. Biol. J. Linn. Soc.
Lond. 105, 607-622.
Nemeth, D. (1997). Modulation of attack behavior and its effect on feeding
performance in a trophic generalist fish. J. Exp. Biol. 200, 2155-2164.
OʼGrady, S. P., Morando, M., Avila, L. and Dearing, M. D. (2005). Correlating diet
and digestive tract specialization: examples from the lizard family Liolaemidae.
Zoology 108, 201-210.
Perry, J. M., Hartstone-Rose, A. and Wall, C. E. (2011). The jaw adductors of
strepsirrhines in relation to body size, diet, and ingested food size. Anat. Rec.
(Hoboken) 294, 712-728.
Ralston, K. R. and Wainwright, P. C. (1997). Functional consequences of trophic
specialization in pufferfishes. Funct. Ecol. 11, 43-52.
Reed, D. A. and Ross, C. F. (2010). The influence of food material properties on jaw
kinematics in the primate, Cebus. Arch. Oral Biol. 55, 946-962.
Reilly, S. M. and McBrayer, L. D. (2007). Prey capture and prey processing behavior
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.
Rice, A. N. and Westneat, M. W. (2005). Coordination of feeding, locomotor and
visual systems in parrotfishes (Teleostei: Labridae). J. Exp. Biol. 208, 3503-3518.
Rodriguez-Robles, J. A., Bell, C. J. and Greene, H. W. (1999). Gape size and
evolution of diet in snakes: feeding ecology of erycine boas. J. Zool. 248, 49-58.
Santana, S. E., Dumont, E. R. and Davis, J. L. (2010). Mechanisms of bite force
production and their relationship with diet in Neotropical leaf-nosed bats. Integr.
Comp. Biol. 50, E155.
Santana, S. E., Strait, S. and Dumont, E. R. (2011). The better to eat you with:
functional correlates of tooth structure in bats. Funct. Ecol. 25, 839-847.
Schaerlaeken, V., Meyers, J. J. and Herrel, A. (2007). Modulation of prey capture
kinematics and the role of lingual sensory feedback in the lizard Pogona vitticeps.
Zoology 110, 127-138.
Schaerlaeken, V., Herrel, A. and Meyers, J. J. (2008). Modulation, individual
variation and the role of lingual sensory afferents in the control of prey transport in
the lizard Pogona vitticeps. J. Exp. Biol. 211, 2071-2078.
Schaerlaeken, V., Montuelle, S. J., Aerts, P. and Herrel, A. (2011). Jaw and
hyolingual movements during prey transport in varanid lizards: effects of prey type.
Zoology 114, 165-170.
Schwenk, K. (2000). Feeding in Lepidosaurs. In Feeding: Form, Function and
Evolution in Tetrapod Vertebrates (ed. K. Schwenk), pp. 175-290. San Francisco,
CA: Academic Press.
Schwenk, K. and Rubega, M. (2005). Diversity of vertebrate systems. In Physiological
and Ecological Adaptations to Feeding in Vertebrates (ed. J. M. Starck and T.
Wang), pp. 1-41. Enfield, NH: Science Publishers.
Sherbrooke, W. C. and Schwenk, K. (2008). Horned lizards (Phrynosoma)
incapacitate dangerous ant prey with mucus. J. Exp. Zool. 309A, 447-459.
Smith, T. L., Kardong, K. V. and Bels, V. L. (1999). Prey capture behavior in the
blue-tongued skink, Tiliqua scincoides. J. Herpetol. 33, 362-369.
Urbani, J. M. and Bels, V. L. (1995). Feeding-behavior in 2 Scleroglossan lizards –
Lacerta viridis (Lacertidae) and Zonosaurus laticaudatus (Cordylidae). J. Zool. 236,
265-290.
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.
Van Cakenberghe, V., Herrel, A. and Aguirre, L. F. (2002). Evolutionary
relationships between cranial shape and diet in bats (Mammalia: Chiroptera). In
Topics in Functional and Ecological Vertebrate Morphology (ed. P. Aerts, K. DʼAout,
A. Herrel and R. Van Damme), pp. 205-236. Maastricht, The Netherlands: Shaker
Publishing.
Velicer, W. F. and Fava, J. L. (1998). Effects of variable and subject sampling on
factor pattern recovery. Psychol. Methods 3, 231-251.
Vincent, S. E., Moon, B. R., Shine, R. and Herrel, A. (2006). The functional meaning
of ʻprey sizeʼ in water snakes (Nerodia fasciata, Colubridae). Oecologia 147, 204-
211.
Vitt, L. J. and Pianka, E. R. (2005). Deep history impacts present-day ecology and
biodiversity. Proc. Natl. Acad. Sci. USA 102, 7877-7881.
Vitt, L. J., Pianka, E. R., Cooper, W. E., Jr and Schwenk, K. (2003). History and the
global ecology of squamate reptiles. Am. Nat. 162, 44-60.
Wainwright, P. C., Mehta, R. S. and Higham, T. E. (2008). Stereotypy, flexibility and
coordination: key concepts in behavioral functional morphology. J. Exp. Biol. 211,
3523-3528.
Young, B. A. (2010). How a heavy-bodied snake strikes quickly: high-power axial
musculature in the puff adder (Bitis arietans). J. Exp. Zool. 313A, 114-121.
THE JOURNAL OF EXPERIMENTAL BIOLOGY
