Prey Capture in Lizards: Differences in Jaw–Neck–Forelimb Coordination

Home , Autarchoglossa, Lacertoidea, Savannah monitor

Biological Journal of the Linnean Society, 2012, 105, 607–622. With 8 ﬁgures

Prey capture in lizards: differences in jaw–neck–forelimb coordination

STÉPHANE J. MONTUELLE1*, ANTHONY HERREL2, PAUL-ANTOINE LIBOUREL3, SANDRA DAILLIE2 and VINCENT L. BELS2

1Ohio University, Heritage College of Osteopathic Medicine, Department of Biomedical Sciences, Athens, OH, USA 2Muséum National d’Histoire Naturelle, Département Ecologie et Gestion de la Biodiversité, UMR 7179, Paris, France 3Université Lyon 1, Institut fédératif des Neurosciences, UMR 5167, Lyon, France

Received 26 August 2011; revised 25 September 2011; accepted for publication 25 September 2011bij_1809 607..622

Although prey capture is thought to be based on the coordinated movements of the jaw and locomotor apparatus (i.e. the vertebral column and the limbs), jaw–neck–forelimb coordination has never been compared among related species. The kinematics of jaw, neck, and forelimb movements were recorded in lizards that use jaw prehension: Gerrhosaurus major, Tupinambis merianae, Varanus niloticus, and Varanus ornatus. These species provide a comparative framework to discuss the influence of morphological differences and ecological convergence on the jaw–neck–forelimb coordination patterns. Jaw–neck–forelimb coordination was quantified by determining whether maximum neck elevation and maximum forelimb flexion are synchronized with either the start of jaw opening or maximum gape. Significant differences in the jaw–neck–forelimb coordination pattern among species were observed, with maximum neck elevation being synchronized with the start of jaw opening in varanids, whereas in T. merianae and G. major, it is achieved closer to maximum gape. Differences in locomotor–feeding integration are suggested to be related to dietary specializations, and as such may play a role in feeding adaptation. The jaw–neck–forelimb coordination pattern used by varanids may indeed be advantageous to prepare a quick strike triggered from further away, providing a critical advantage when feeding on evasive prey. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105, 607–622.

ADDITIONAL KEYWORDS: feeding – integration – kinematics – Teiids – varanids.

INTRODUCTION 2000b; Bels, 2003; Reilly & McBrayer 2007), salamanders (for a review see Wake & Deban 2000), frogs, Living organisms exploit food resources to obtain and toads (for a review see Nishikawa 2000). The nutrients and the energy needed to function and performance of predators using tongue prehension is survive. Among the various components of feeding primarily based on the speed and accuracy of tongue behaviour, food acquisition is important as it includes projection jointly with the adhesive capacity of the stage during which the organism establishes the tongue (Wainwright, Kraklau & Bennett, 1991; contact with the food item. In animals feeding on Lappin et al., 2006; Deban et al., 2007). In other mobile prey (e.g. carnivores, insectivores), the ability tetrapods, the jaws are the elements through to decrease predator–prey distance is thus critical. which predator–prey contact is established (e.g. cro- Various predators among tetrapod vertebrates use the codylians, snakes, and autarchoglossan lizards; for a hyolingual apparatus to decrease predator–prey dis- review see Cleuren & de Vree 2000; Cundall & tance and catch prey, such as iguanian lizards (for a Greene, 2000; Schwenk, 2000b). During jaw prehen- review see Bels, Chardon & Kardong, 1994; Schwenk, sion, prey acquisition results from the movement of the head with opened jaws towards the prey, leading *Corresponding author. E-mail: [email protected] to the subsequent contact between the jaws of the

© 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105, 607–622 607 608 S. J. MONTUELLE ET AL. predator and the prey. In snakes, for instance, the nation, optimal gape angle at contact might not be extension of the vertebral column, especially in achieved (e.g. jaws are not open wide enough when the cervical region, has been demonstrated to gener- predator–prey contact occurs), leading to an unsuc- ate the thrust necessary to cover predator–prey dis- cessful capture attempt. Previous studies of jaw pre- tance (Frazzetta, 1966; Janoo & Gasc, 1992; Kardong hension highlight the role of the cervical vertebrae in & Bels, 1998; Cundall & Deufel, 1999; Alfaro, 2003; snakes (Kardong & Bels, 1998; Cundall & Deufel, Young, 2010; Herrel et al., 2011). 1999; Alfaro, 2003; Young, 2010), but the coordination The functional analysis of feeding behaviour pro- of jaw movements with those of the locomotor elements vides meaningful insights into the evolution of the remains poorly quantiﬁed in other groups (but see form and function of anatomical structures (e.g. Bock Montuelle, Daghfous & Bels, 2008; Montuelle et al., & von Wahlert, 1965; Frazzetta, 1994; Schwenk, 2009a). Consequently, the present study aims to dem- 2000a). Indeed, the morphology of the feeding ele- onstrate the role of locomotor-feeding integration ments (i.e. the skull, the jaw, and the hyolingual during jaw prehension in lizards. apparatus) is shaped by the adaptive pressures of their Jaw prehension is a key feature of the evolution of respective function. For instance, the anatomy of the the squamate lineage. In the classical phylogene- hyolingual apparatus may evolve to enhance tongue tic hypothesis (based on morphological evidence; elongation (e.g. Schwenk, 1985; Delheusy, Toubeau & Fig. 1A), the evolution of jaw prehension is considered Bels, 1994; Sherbrooke & Schwenk, 2008; Herrel et al., to have ‘released’ the hyolingual apparatus from its 2009). Similarly, the jaw apparatus and the skull itself constraints during feeding, allowing for specialization are shaped with respect to diet to generate the towards other functions such as vomeronasal adequate bite force (e.g. Herrel, Aerts & de Vree, 1998; chemoreception (Wagner & Schwenk, 2000; Schwenk Herrel et al., 2001a, 2007; Herrel, O’Reilly & Rich- & Wagner, 2001; Vitt et al., 2003). In the recent phy- mond, 2002; Metzger & Herrel, 2005; Therrien, 2005; logenetic hypothesis (based on molecular evidence; Huber et al., 2009; Freeman & Lemen, 2010; Chris- Fig. 1B), jaw prehension is considered to be the ances- tiansen, 2011). Yet, the movements of the feeding tral prey capture mode (Lee, 2005; Vidal & Hedges, elements need to be coordinated with each other to 2005). Thus in both cases, the functional characteris- ensure the success of prey capture performance (e.g. tics of jaw prehension will probably contribute in our Herrel et al., 2001b; Schwenk, 2001; Bels, 2003; understanding of the evolution of feeding in the squa- Higham, 2007; Wainwright, Mehta & Higham, 2008). mate lineage. To date, locomotor-feeding integration The crucial aspect of feeding in an adaptive context has been demonstrated during jaw prehension in one thus concerns the movements of the feeding system as squamate lizard, Gerrhosaurus major Duméril 1851 an integrated whole, rather than of the feeding ele- (Scleroglossa, Autarchoglossa, Scincoidea; Montuelle ments independently. Consequently, changes in the et al., 2009a). Here, our objective is to compare jaw– form and function of one element may affect the other neck–forelimb integration in this species with other elements, and the adaptation of anatomical elements lizards that use jaw prehension: Tupinambis meri- is under the selective pressures that stem from the anae Duméril & Bibron 1839 (Scleroglossa, Autar- functionality of the entire system (Wagner & Schwenk, choglossa, Lacertoidea, Teiidae), Varanus niloticus 2000; Schwenk & Wagner, 2001). In the case of igua- Linnaeus 1758, and V. ornatus Daudin 1803 (Sclero- nian lizards that use tongue prehension, the integra- glossa, Autarchoglossa, Varanoidea, Varanidae). Tupi- tion of the jaws and the hyolingual apparatus is such nambis merianae, V. niloticus, and V. ornatus were that the feeding system is suggested to be an evolu- selected because they share comparable ecological tionarily stable conﬁguration (Wagner & Schwenk, and behavioural features associated with feeding: 2000; Schwenk & Wagner, 2001). However, relatively an omnivorous diet (Presch, 1973; Losos & Greene, little is known about the functional basis of jaw 1988; Cooper, 2002), and similarities in foraging mode prehension in lizards. (Cooper, 1995; Thompson, 1995), prey detection From a functional perspective, prey prehension (Cooper, 1989, 1990, 1996; Yanosky, Iriart & Mercolli, relies on the positioning of the head and jaws according 1993; Kaufman, Burghardt & Phillips, 1996; Cooper to the prey characteristics. As such, jaw prehension is & Habegger, 2001; Chiszar et al., 2009), and transport achieved by the integration of the movements of the mode (Elias, McBrayer & Reilly, 2000; McBrayer & feeding elements (i.e. the jaws) with the locomotor Reilly, 2002b; Montuelle et al., 2009b; Schaerlaeken elements, especially the anterior locomotor elements et al., 2011). Morphological similarities in skull shape such as the forelimbs and the cervical vertebrae (Mon- and body proportions have also been documented tuelle et al., 2009a). Jaw movements must indeed be (Vitt & Pianka, 2004; Stayton, 2005). Given these synchronized with locomotor movements so that the similarities in morphological, behavioural, and eco- velocity of the head and the opening angle of the jaws logical traits, functional convergence in locomotor– result in predator–prey contact. Without such coordi- feeding integration pattern is predicted.

Rhyncocephalia Rhyncocephalia

Iguania Gekkota

Gekkota Scincoidea Gerrhosaurus major (Cordyliform) Scincoidea Gerrhosaurus major (Cordyliform) Lacertoidea Tupinambis merianae (Teiidae) Lacertoidea Tupinambis merianae (Teiidae) Iguania A Varanoidea Varanoidea Varanus niloticus & Varanus ornatus Varanus niloticus & Varanus ornatus

ABSerpentes (i.e. snakes) Serpentes (i.e. snakes)

Figure 1. Phylogenetic framework of the squamate lineage. A, classical hypothesis representing the phylogenetic relationships between squamate clades based on morphological evidence (based on Estes et al., 1988; Schwenk, 2000b; Vitt et al., 2003; Reilly & McBrayer, 2007). The autarchoglossan clade is illustrated by a grey diamond. B, recent hypothesis representing phylogenetic relationships among squamate clades based on molecular evidence (based on Lee, 2005; Vidal & Hedges, 2005). The taxa investigated here are indicated in both cladograms, and note branch lengths do not represent time.

However, while T. merianae and G. major have Montuelle et al., 2009a, 2010). For the recording ses- eight cervical vertebrae (Reese, 1923), varanids have sions involving T. merianae, the trackway was 3 m nine cervical vertebrae that are each elongated (Hoff- long and 45 cm wide. For the recording sessions stetter & Gasc, 1969). Neck elongation can thus be involving varanids, the trackway was extended to expected to alter the locomotor-feeding coordination 4.20 m long and 60 cm wide to match their greater pattern when comparing varanids, T. merianae, and locomotor activity. One day before the recording ses- G. major. Consequently, our hypothesis is that jaw– sions, the animal was placed on the trackway to allow neck–forelimb coordination will vary depending on it to become familiarized with the experimental set- the anatomical specificities (e.g. number of cervical up. During the feeding trials, the animals were free to vertebrae), emphasizing the role of the neck in con- move along the trackway, performing their natural tributing to the positioning of the trophic elements exploratory behaviour. Once the animal was posi- during feeding. Alternatively, similarities in jaw– tioned at one end of the track, where a lamp provided neck–forelimb coordination between T. merianae and a basking spot, the prey item was placed at the other varanids will illustrate functional convergence mir- end of the track. We then waited for the animal to roring ecological similarity. By comparing these taxa, spontaneously initiate foraging and prey capture our goal is to investigate whether the locomotor- behaviour. feeding integration pattern is dictated by (1) the Feeding behaviour was recorded using four high- morphological specificities (e.g. number of cervical speed cameras (Prosilica GE680, Allied Vision Tech- vertebrae) or (2) similarities in feeding ecology. nologies GmbH, Stadtroda, Germany) synchronized at 200 frames per second. Two cameras were set up in MATERIAL AND METHODS dorsal view, one camera was set up in oblique frontal view, and one camera in lateral view. Thus, the ana- HUSBANDRY tomical points of interest were visible in at least three All animals were purchased from commercial animal of the four views during the whole sequence recorded. dealers and were maintained individually in large Cameras were calibrated and scaled using a DLT terraria (1.5 m long ¥ 1.5 m deep ¥ 30 cm high) with routine (Hartley & Sturm, 1995) based on the digiti- sliding glass to facilitate cleaning (once a week). Tem- zation of a black-and-white checkerboard composed of perature was set at 24–30 °C in the daytime, with a ten by ten 1 cm ¥ 1 cm squares. basking spot of 31–32 °C, and no lower than 24 °C at night. A light source was set on a 12/12-h light/dark cycle. Water was available ad libitum and the sub- DATA SET jects were fed mice and grasshoppers twice a week. Prey capture behaviour was observed in three adult individuals of T. merianae (snout–vent EXPERIMENTAL PROTOCOL length = 294 ± 77 mm), two adult individuals of The experimental set-up consisted of a wooden track- V. ornatus and one adult individual of V. niloticus way covered with a non-slip green plastic flooring (see (snout–vent length = 480 ± 11 mm) while feeding

© 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105, 607–622 610 S. J. MONTUELLE ET AL. on grasshoppers (Locusta migratoria, 46 ± 1 mm). A Varanus niloticus and V. ornatus are closely related (Böhme, 2003) and used to be considered different subspecies (e.g. Luiselli, Akani & Capizzi, 1999). Because they are morphologically similar, individuals of both species are grouped in the analysis. Twenty sequences corresponding to successful prey captures were analysed for each model species: T. merianae (five, nine, and six sequences for each individual), and the varanids (eight, seven, and five sequences for each individual). Additionally, identical recording sessions B were organized to observe prey capture in Gerrhosau- rus major: ten sequences of four adult individuals (snout–vent length = 207.5 ± 4.4 mm; three sequences per individual, and only one sequence for the fourth individual) feeding on grasshoppers (L. migratoria, length = 45.0 ± 1.3 mm). In lizards, prey mobility also affects prey capture behaviour (e.g. Montuelle et al., 2010). Consequently, the sequences included in the analysis correspond to the feeding trials during which C the prey was active (i.e. two to five jumps) while the predator was approaching (i.e. the feeding trials during which the prey sat still while the predator was approaching were removed from the analysis).

KINEMATIC ANALYSIS The following markers were painted on the body and subsequently digitized: the tip of the lower and upper jaws, the corner of the mouth, one point halfway Figure 2. Illustration of the kinematic variables quanti- between the occipital and the pectoral girdle, and the fied in this study. A, typical frame extracted from one of shoulder, elbow and wrist joints (Figs 2, 3). The posi- the four synchronized high-speed cameras. B, illustration tion of the prey (point at the insertion of the head on of the kinematics extracted to quantify jaw movements: the prothorax) and the position of the eye of the gape angle. C, illustration of the kinematics extracted to predator were also digitized to quantify movements of quantify the movements of the post-cranial elements: the animal relative to the prey during the strike. elevation of the neck (Z-coordinate) and elbow angle. Screen coordinates of the digitized markers were Scale bar = 4 cm. extracted on each of the four camera views and their position in three dimensions over time was calculated. Quantifying movements of skeletal elements based on and the elbow angle (angle between shoulder, elbow, external markers must be performed carefully and wrist) were constructed. From these profiles, because of the movements of the skin, but here we the following kinematic variables were extracted: believe that potential error is reduced because of the maximum gape angle, maximum elevation of the small amount of soft tissue between the skin and the neck, and minimum elbow angle representing actual skeletal elements of interest. Additionally, maximal flexion of the forelimb (Table 1). The corre- although we acknowledge that the hind limbs are sponding timing variables were also identified: time important for propulsion during the lunge, our study of jaw opening, time of maximum gape angle, time of focuses on the movements of the forelimbs and the maximum neck elevation, and time of minimum cervical portion of the vertebral column as the require- elbow angle (Table 1). Note that time 0 was set at the ments for sufficient resolution in reconstructing instant of predator–prey contact so that negative time movements in three dimensions based on a multiple- values represent events occurring before predator– camera set-up only allowed a limited field of view. prey contact, whereas positive time values represent Kinematic profiles of changes in gape angle (angle events occurring after contact. between upper jaw, corner of the mouth, and lower Note that maximal extension of the forelimb was jaw), neck elevation (difference in Z-coordinate of the also extracted but not retained for the analysis point on the neck with respect to its position at rest), because it consistently approached 180° across

ABC

t = -160 t = -205 t = -190

t = -105 t = -155 t = -175

t = -20* t = -55 t = -75

t = -10 t = -30* t = -25 *

t = 0 t = 0 t = 0

t = +35 t = +35 t = +35

Figure 3. Representative frame sequences of prey capture behaviour of autarchoglossan lizards: A, Gerrhosaurus major; B, Tupinambis merianae;C,Varanus ornatus. Time is indicated in milliseconds for each frame. Time t = 0 indicates predator–prey contact. Symbols represent the events of interest: *, maximum opening of the jaws; ᭡, maximum elevation of the neck. Scale bar = 4 cm. sequences, illustrating how the stylo- and zeugopodal tified by calculating the angle between the elbow elements of the forelimb systematically line up during marker, the wrist marker, and a marker painted at the strike. Movements at the shoulder and wrist the base of the fourth fore toe. Unfortunately, this joints were not included in the analysis for two dif- marker was not visible on multiple views in the ferent reasons. First, movements at the shoulder joint majority of the sequences, thus preventing us from could have been quantified by calculating the angle recalculating its position in three dimensions. between the elbow marker, the shoulder marker, and Strike performance was quantified by calculating a marker painted on the back of the animal at the the peak three-dimensional (3D) velocity of displace- level of the scapular girdle (Fig. 3). However, we rec- ment of the eye of the predator, representing the ognize that the point on the back of the animal is too speed of the skull during the strike (smoothing pro- far away from the actual point of insertion of the cedure: fourth-order Butterworth low-pass filter with humerus in the shoulder girdle, and the shoulder a cut-off frequency set at 25 Hz). Based on the 3D angle was therefore not retained for analysis. Second, positions of the prey and the predator’s eye, changes movements at the wrist joint could have been quan- in predator–prey distance were calculated and the

Table 1. Summary of the kinematic variables associated with jaw movements, neck elevation, and forelimb ﬂexion observed during prey capture in Gerrhosaurus major, Tupinambis merianae and Varanus sp. (V. niloticus and V. ornatus)

Gerrhosaurus Tupinambis Varanus Varanus major merianae niloticus ornatus (N = 4) (N = 3) (N = 1) (N = 2)

Jaw opening movements Maximum gape angle (°) 29.1 ± 3.1 31.6 ± 1.7 29.8 ± 1.4 33.8 ± 0.7 Time of jaw opening (ms) -118±6 -120±13 -206±17 -161±16 Time of maximum gape angle (ms) 21 ± 19 -22±4 -13±11 -26±4 Duration of jaw opening (ms) 139 ± 21 98 ± 10 193 ± 10 135 ± 14 Neck elevation Maximum elevation of the neck (cm) 1.95 ± 0.34 2.69 ± 0.25 2.50 ± 0.46 5.52 ± 0.29 Time of maximum neck elevation (ms) -30±18 -66±12 -135±43 -144±16 Latency of maximum neck elevation (%)* 64.5 ± 9.9 60.5 ± 11.8 38.1 ± 24.6 11.2 ± 11.5 Forelimb ﬂexion Minimum elbow angle (°) 70.7 ± 7.7 80.1 ± 4.9 85.2 ± 4.8 82.1 ± 1.5 Time of minimum elbow angle (ms) -168±56 -303±36 -121±55 -77±22 Latency of minimum elbow angle (%)* -53.3 ± 52.1 -187.4 ± 33.7 40.9 ± 32.1 53.8 ± 18.1 Strike performance Skull velocity (cm s-1) 67.3 ± 8.2 81.4 ± 8.1 91.8 ± 7.8 120.4 ± 7.3 Standardized skull velocity† 17.8 ± 2.1 17.1 ± 1.8 18.6 ± 1.3 18.3 ± 1.1 Predator–prey distance at the onset of jaw opening (cm) 3.49 ± 0.33 6.50 ± 0.36 6.70 ± 0.8 14.89 ± 1.50 Standardized predator–prey distance at the onset 0.92 ± 0.08 1.33 ± 0.06 1.11 ± 0.14 2.26 ± 0.23 of of jaw opening†

N, the number of individuals. Table entries are means ± SEM. *Standardized with respect to jaw opening (see Fig. 4). †Standardized with respect to jaw length. distance at the onset of jaw opening was extracted. STATISTICAL ANALYSIS Maximum speed of the skull and predator–prey distance at the onset of jaw opening were both standard- All extracted variables were log10-transformed prior ized relative to jaw length, using a classic ratio to analysis to fulfil assumptions of normality and method (Table 1). Jaw length was chosen for stan- homoscedasticity. First, a factor analysis with dardization, instead of the length of the skull for varimax rotation was performed on the kinematic and example, because jaw length is arguably a more rel- time variables to explore the variability of movements evant parameter when studying feeding behaviour: associated with prey capture behaviour among T. merianae (jaw length = 49 ± 4 mm), Varanus sp. species (Table 2). Factors with eigenvalues greater (jaw length = 64 ± 2 mm), Gerrhosaurus major (jaw than 1 were retained and factor scores were submit- length = 37 ± 1 mm). ted to an analysis of variance (ANOVA) coupled to To quantify jaw–neck synchronization, the latency univariate F-tests to test differences among species of neck elevation was calculated as the difference (fixed factor, associated with Bonferroni’s post-hoc between time of maximum neck elevation and time of tests). The coefficients of variation (CV) of the factor jaw opening. Subsequently, to discuss time occurrence scores were calculated for each species separately, of neck elevation during jaw opening, latency of neck and compared using Levene’s test to discuss stereo- elevation with respect to jaw opening was standard- typy of movements. The individual effect was tested ized as a percentage of opening duration (defined as within each species separately using a multivariate the difference in time between jaw opening and analysis of variance (MANOVA); note that for maximum gape; Fig. 4). Thus, low latency values G. major, the individual with only one sequence was indicate neck elevation occurs close to jaw opening removed from the analysis of variance. Next, ANOVAs (Fig. 4A), whereas high latency values indicate were performed on latency of neck elevation and neck elevation is achieved close to maximum gape latency of elbow flexion with respect to jaw opening to (Fig. 4B). Latency of elbow flexion was calculated test for inter-specific differences in the pattern of similarly. coordination of neck and forelimb movements with

NECK NECK ELEVATION ELEVATION

Rest Rest position position Time of maximum TIME Time of maximum TIME elevation of the neck elevation of the neck

GAPE GAPE ANGLE ANGLE

0° 0° (jaws are (jaws are closed) closed)

Time of Time of TIME Time of Time of TIME jaw opening maximum gape angle jaw opening maximum gape angle

0% 100% 0% 100% ABOpening duration Opening duration

Figure 4. Schematics 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 t = 0 at the instant of predator–prey contact. Then, time of maximum neck elevation (dotted arrow) is transformed as a percentage of the total duration of the jaw opening phase. Two cases are illustrated: A, maximum neck elevation occurs shortly after jaw opening, and thus the latency with respect to jaw opening is represented by a low percentage value; B, maximum neck elevation occurs later during jaw opening (i.e. closer to maximum gape angle), and thus the latency with respect to jaw opening is represented by a high percentage value. Latency of forelimb ﬂexion at the elbow joint is calculated using the same procedure.

Table 2. Results of a factor analysis performed on the jaw movements (species entered as fixed factor). kinematic variables associated with jaw movements, neck Finally, to explore how movements contribute to elevation, and forelimb flexion during prey capture in strike performance, bivariate correlations between Gerrhosaurus major, Tupinambis merianae and Varanus maximum velocity of the skull and the multivariate sp. (V. niloticus and V. ornatus) factors, the predator–prey distance at the onset of jaw opening, and the latency of neck and forelimb move- Factor 1 Factor 2 Factor 3 ments were tested for each species separately. Because of the repetitive procedure testing the bivari- Variance explained (%) 30.74 20.46 18.14 ate correlations, the significance level was adjusted Cumulated variance explained (%) (51.2) (69.3) Time of jaw opening 0.882 0.074 0.002 using a Bonferroni correction. Here, because six tests Maximum gape angle -0.003 0.054 0.887 were repeated for each species separately, the signifi- Time of maximum gape angle 0.489 0.719 0.069 cance level P-value was adjusted to 0.008. Maximum elevation of the neck -0.517 0.200 0.494 Time of maximum neck elevation 0.894 0.004 -0.166 Minimum elbow angle -0.106 -0.329 0.451 Time of minimum elbow angle -0.239 0.871 -0.051 RESULTS JAW PREHENSION IN LIZARDS Values in bold represent loadings greater than 0.70 (Velicer & Fava, 1998). First, we provide a qualitative description of the feeding behaviour used by the lizard species investigated here (Fig. 3); note that this section will focus on T. merianae and varanids primarily because

© 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105, 607–622 614 S. J. MONTUELLE ET AL. qualitative and quantitative descriptions of prey 2, T. merianae is characterized by a significantly lower capture in G. major are available elsewhere (Montu- time of elbow flexion, and maximum gape is achieved elle et al., 2009a, 2010). Prior to prey approach, at least earlier than in varanids and G. major (F2,47 = 7.198, one tongue flick was observed before the predator P = 0.002; post-hoc tests: P = 0.011 and P = 0.005, stands up and starts to walk towards the prey along respectively; Fig. 5A, C). Levene’s test indicates that the trackway. In accordance with previous observa- the coefficient of variation in T. merianae is signifi- tions on closely related species (Cooper, 1989, 1990; cantly greater than in varanids (CVTupinambis = 2.24,

Kaufman et al., 1996; Cooper & Steele, 1999), tongue CVvaranids = 1.05; P = 0.003), illustrating that time of flicks occur intensively during prey approach, indicat- elbow flexion and time of maximum gape angle are ing vomerolfactive chemoreception is used by T. meri- more stereotyped in varanids than in T. merianae anae, V. niloticus, V. ornatus, and G. major to locate (Fig. 5A, C). Finally, on factor 3, G. major use signifi- active prey such as grasshoppers. Tupinambis meri- cantly smaller gape angles than varanids (F2,47 = 4.288, anae and varanids usually stop approximately 10 cm P = 0.019; post-hoc tests: P = 0.016; Fig. 5B, C), prob- away from the prey, and G. major stops closer ably reflecting differences in body size. (Table 1). During this pause, the predator stares at the Individual effects were tested for each species sepa- prey and prepares for strike, and the jaws open slightly rately using MANOVAs performed on the multivari- while the predator remains stationary. The strike ate factor scores. No individual effect is detected for consists of a lunge on the prey. The jaws continue to G. major (Wilks’ lambda = 0.087, P = 0.067), T. meri- open during the strike until maximum gape angle is anae (Wilks’ lambda = 0.690, P = 0.431), and varanids achieved and close shortly after predator–prey contact. (Wilks’ lambda = 0.502, P = 0.089) on factors 1 and 2. As expected, all species investigated here use jaw However, significant individual differences are found prehension when capturing grasshoppers. Note that on factor 3 for G. major (F2,6 = 11.345, P = 0.009) and jaw opening can be divided into two phases: slow varanids (F2,17 = 5.903, P = 0.011). Interestingly, post- opening and fast opening; no plateau (slow opening hoc tests reveal that V. niloticus uses significantly phase II) is observed (in accordance with McBrayer & smaller gape angles than V. ornatus. Reilly, 2002a; Reilly & McBrayer, 2007). In accordance The predator–prey distance at the onset of jaw with previous observations (Elias et al., 2000; opening differs among the species investigated McBrayer & Reilly, 2002b; Reilly & McBrayer, 2007; here. Indeed, the effects of species is significant

Montuelle et al., 2009b; Schaerlaeken et al., 2011), the (F2,47 = 14.391, P < 0.001) and post-hoc tests indicate transport stage following a successful prey capture that the three species differ from each other (G. major involves a series of gape cycles, including repositioning versus T. merianae, P = 0.016; G. major versus cycles, puncture crushing, and inertial transport varanids, P < 0.001; T. merianae versus varanids, cycles. P = 0.017). Our data show that G. major opens its jaws Movements associated with prey capture differ close to the prey, whereas varanids open their jaws between T. merianae, V. niloticus, V. ornatus, and while far away from the prey, the distance to the prey G. major. A factor analysis performed on displacement at the onset of jaw opening is intermediate in T. meri- and timing variables retained three factors represent- anae (Table 1). This illustrates how varanids strike ing approximately 70% of the total variance (31, 20 and from further away whereas G. major and T. merianae 18%, respectively; Table 2). The first factor is corre- approach closer to the prey before opening the jaws. lated with the time of maximum neck elevation and the time of jaw opening, the second factor represents time of forelimb flexion at the elbow joint and time of COORDINATION OF NECK ELEVATION AND FORELIMB maximum gape angle, and the third factor represents FLEXION WITH JAW OPENING the magnitude of maximum gape angle (Table 2). During the jaw opening phase (i.e. between jaw Significant differences between species are detected on opening and maximum gape), the latency of neck each of the three multivariate factors (Fig. 5). On elevation and forelimb flexion at the elbow joint factor 1, varanids display significantly lower times of differs among species (Figs 6, 7). In the species maximum neck elevation and jaw opening than T. me- studied here, maximum neck elevation occurs after rianae and G. major (F2,47 = 12.358, P < 0.001; post-hoc jaw opening, but maximum neck elevation is achieved tests: P < 0.001; Fig. 5A). Additionally, Levene’s at different times in each species (F2,47 = 5.213, tests indicate that the coefficient of variation of P = 0.009; Fig. 6). Post-hoc tests indicate that latency the factor scores of varanids is significantly greater of neck elevation in varanids is significantly different than in T. merianae (CVvaranids = 1.66, CVTupinambis = 1.25; compared with T. merianae and G. major (P = 0.019 P = 0.018), illustrating that time of maximum neck and P = 0.043, respectively; Fig. 7). This reveals that elevation and time of jaw opening are more stereotyped maximum neck elevation is achieved shortly after jaw in T. merianae than in varanids (Fig. 5A, B). On factor opening in varanids (18% of opening duration;

Figure 5. Multivariate spaces defined by the factor analysis performed on the kinematic variables associated with jaw movements, neck elevation, and forelimb flexion during prey capture behaviour of Gerrhosaurus major, Tupinambis merianae, and Varanus niloticus and V. ornatus: A, factors 1 and 2; B, factors 1 and 3; C, factors 2 and 3. Percentage of total variance explained and the variables correlated with each multivariate factor are indicated on the factor axis (see Table 2 for the complete composition of each factor). Symbols represent taxa: squares for G. major, circles for T. merianae, and triangles for V. niloticus (open) and V. ornatus (closed). Note neck elevation and jaw opening tend to occur significantly earlier in varanids than in the other taxa (factor 1), maximum opening of the jaws and elbow flexion tend to be achieved significantly earlier in T. merianae than in the other taxa (factor 2), and maximum gape angle is significantly smaller in G. major than in varanids or T. merianae (factor 3). ᭣

(Fig. 6B), whereas forelimb ﬂexion in varanids occurs after jaw opening, in the middle of the jaw opening phase (51% of jaw opening duration; Fig. 6C; Table 1).

VARIABILITY IN STRIKE PERFORMANCE Signiﬁcant differences in skull velocity during the strike are detected between the species investigated

(F2,47 = 3.769, P = 0.030). Speciﬁcally, strikes of varanids are the quickest whereas strikes in G. major are the slowest, with T. merianae falling in-between (Table 1), representing how body size affects strike velocity. However, these differences are not signiﬁcant when skull velocity is standardized with respect to

jaw length (F2,47 = 0.312, P = 0.734). To explore variability in the speed of strike, correlations of skull velocity (standardized) with the three multivariate factors, predator–prey distance at the onset of jaw opening (standardized), latency of neck elevation, and latency of elbow flexion are tested. Within each species, variability of strike performance is associated with the fine-tuning of different kinematic param- eters associated with jaw movements, neck elevation, and forelimb flexion (Fig. 8). In T. merianae and Figs 4A, 6C, 7; Table 1), whereas it occurs later in G. major, standardized skull velocity during the the jaw opening phase in T. merianae and G. major strike is correlated with factor 1 (r = 0.686, P = 0.001; (60.5 and 64.5% of opening duration, respectively, i.e. r =-0.809, P = 0.008, respectively; Fig. 8A). This indi- close to maximum gape and predator–prey contact; cates that quick strikes involve early jaw opening and Figs 4B, 6A, B, 7; Table 1). early neck elevation in G. major. In contrast, in T. me- The latency of forelimb flexion at the elbow joint rianae, quick strikes are characterized by late jaw also differs among species (F2,47 = 15.194, P < 0.001; opening and late maximum neck elevation. There are Fig. 6). Post-hoc tests reveal that forelimb flexion no significant correlations between skull velocity and occurs earlier in T. merianae than in varanids the two other multivariate factors. In varanids, there (P < 0.001) and G. major (P = 0.033). This shows that are no correlations between skull velocity and any of forelimbs are flexed before jaw opening in T. merianae the three multivariate factors.

Latency of maximum neck elevation with respect to jaw opening is also correlated with standardized skull velocity in T. merianae and G. major (r =-0.624, P = 0.003; r =-0.874, P = 0.002, respectively; Fig. 8B). The time of maximum neck elevation thus appears to be altered similarly in these species. Quick strikes in both T. merianae and G. major are characterized by maximum neck elevation being achieved earlier in the jaw opening phase, i.e. closer to jaw opening. Conse- quently, the jaw–neck coordination pattern used by T. merianae and G. major for quick strike resembles the one used by varanids. Again, no correlations between skull velocity and latency of neck elevation were significant in varanids lizards. Moreover, there were no significant correlations between standardized skull velocity and the latency of forelimb flexion at the elbow joint in any of the three species investigated here. Finally, the predator–prey distance at the onset of jaw opening (standardized over jaw length) is correlated with standardized skull velocity in T. merianae and varanids (r = 0.633, P = 0.003; r = 0.574, P = 0.008, respectively; Fig. 8C). In these two taxa, quick strikes are characterized by the jaw being open further away from the prey, indicating that faster strikes are triggered from a longer distance from the prey.

DISCUSSION DIVERSITY OF JAW–NECK–FORELIMB COORDINATION PATTERNS During jaw prehension, lunge movements are used to position the head and jaws onto the prey. The movements of the skull must be coordinated with jaw opening movements so that gape angle and skull velocity are adjusted accordingly at the onset of predator–prey contact (Kardong & Bels, 1998; Cundall & Deufel, 1999; Cundall & Greene, 2000; Alfaro, 2003; Young, 2010). To date, coordination in the timing and coupling in magnitude of jaw movements with those of the neck and forelimb have been Figure 6. Box plots illustrating the occurrence of jaw demonstrated during jaw prehension in one terres- movements (opening and maximum gape), neck elevation, trial lizard (G. major; Montuelle et al., 2009a), but no and forelimb ﬂexion (minimum elbow angle) during prey comparative study of locomotor–feeding integration capture behaviour of: A, Gerrhosaurus major;B,Tupi- has been performed. Differences in body size between nambis merianae;C,Varanus niloticus and V. ornatus. G. major and the three other species investigated Within each box, the mean is represented by the thick line affect prey capture behaviour; for example, in and the median is represented by the regular line. Outli- G. major, maximum gape angle occurs after predator– ers are also speciﬁed. Time t = 0 indicates predator–prey prey contact, representing how jaw opening continues contact and is represented by the dashed line. Note neck after contact to accommodate the larger size of the elevation is synchronized with jaw opening in varanids, prey item relative to the small skull and jaws of this whereas neck elevation is achieved closer to maximal jaw opening and predator–prey contact in T. merianae and species in comparison with the other two. Conse- G. major. quently, the discussion will focus on the comparison between T. merianae and V. niloticus and V. ornatus. Our study indicates that neck and forelimb movements are coordinated with jaw opening movements

Figure 7. Box plots illustrating the latency of neck elevation with respect to jaw opening during prey capture behaviour of Gerrhosaurus major, Tupinambis merianae, and Varanus niloticus and V. ornatus. See Material & Methods and Figure 4 for details about the calculation of latency values. Box plot values are the mean latency of neck elevation; the error bar represents the standard error of the mean. Low latency values represent neck elevation occurring shortly after jaw opening, whereas high latency values represent neck elevation being achieved closer to maximal gape opening. in four squamate species using jaw prehension: prey, both the upper and the lower jaws participate in G. major, T. merianae, V. niloticus, and V. ornatus predator–prey contact by grasping the sides of the (Fig. 5). Our data show that the pattern of neck–jaw prey. During the strike in varanids, the lower jaw coordination differs among species, with maximum slides under the prey and scoops the prey up in the neck elevation achieved at different times during jaw jaws. As such, the jaw–neck–forelimb coordination opening (Fig. 6). During the preparatory pause pattern used by varanids focuses on the preparation between prey approach and the strike itself, the neck of the strike, whereas that used by T. merianae and of varanid lizards elevates and the forelimbs extend G. major favours predator–prey contact. while the jaws open slightly. In varanid lizards, the These differences in locomotor–feeding integration neck elevates before jaw opening so that the neck is among the species investigated here can be related to maximally elevated shortly after jaw opening starts the speed of strike. During the strike, varanids move (Figs 3, 4A, 6C, 7). During the strike, the forelimbs significantly faster than either T. merianae or flex and the neck lowers as the predator lunges on the G. major (Table 1). Therefore, the jaw–neck–forelimb prey, while the jaws open to reach maximum gape, coordination pattern used by varanids may be rel- and the forelimbs extend again afterwards (Fig. 3). In evant for preparing fast strikes. By extending the contrast, in T. merianae and G. major, forelimb forelimbs and elevating the neck prior to triggering flexion occurs before jaw opening during the prepara- the strike (Figs 6C, 7; Table 1), we propose that tory phase, and neck elevation occurs later in the jaw varanids are able to better estimate the distance opening phase, reaching its maximum closer to that needs to be covered to successfully capture the maximum gape and predator–prey contact (Figs 3, prey, as well as allowing them to evaluate prey behav- 4B, 6A, B, 7). In these species, the strike on the prey iour. This preparation may be a key factor for the consists of the extension of the forelimbs at the elbow success of a fast strike. In comparison, in T. merianae joint, resulting in elevation of the neck late in the jaw and G. major, locomotor–feeding integration occurs opening phase (Fig. 4B). Synchronizing neck eleva- throughout the strike (i.e. maximum neck elevation is tion with maximum gape, as in T. merianae and reached close to maximum gape angle; Figs 6A, B, 7; G. major, sets the head above the prey at the onset of Table 1), which may facilitate precision of predator– predator–prey contact so that when the jaw closes, prey contact and the actual bite. Locomotor–feeding the head contributes to immobilizing the prey during integration in T. merianae and G. major may thus be the bite (Fig. 3). Indeed, by setting the head above the controlled throughout the strike, suggesting the

prevalence of a motor pattern that depends on feed- back modulation based on sensory cues. In contrast, locomotor–feeding integration in varanids may be mainly based on a motor control that is modified prior to strike initiation (i.e. feed-forward modulation). However, such hypotheses remain speculative at this point, and will need to be addressed experimentally, similar to studies on feeding in snakes (e.g. Cundall, Deufel & Irish, 2007). Despite the convergence in feeding morphology and ecology between T. merianae and varanids, differences in locomotor–feeding integration are present and can be linked to the morphological specificities of the vertebral column, in accordance with our hypothesis. Indeed, neck elongation in varanids may provide the cranio-cervical system with enhanced mobility, which may be of critical importance during fast strikes. Enhanced cranio-cervical mobility is suggested to allow fine-tuning of head position during the quick lunge movements that characterize prey capture behaviour of varanid lizards. The ability to tune head positioning despite its high velocity may help varanid lizards to respond to prey movements during the strike. Our study suggests how the morphology of the cervical system affects strike performance associated with jaw prehension in lizards, emphasizing the role of the vertebral column in con- tributing to feeding function. Therefore, coordination of the vertebral column, and by extension the rest of the locomotor system, with the feeding apparatus is hypothesized to respond to the selective pressures associated with the adaptation of feeding behaviour, especially with respect to feeding ecology. Compared with Iguanian lizards, scleroglossans are thought to feed predominantly on hidden prey (Vitt & Pianka, 2005), and within scleroglossan lizards, varanids are reported to feed on ‘hard to catch’ prey items (Losos & Greene, 1988). For varanids, our data demonstrate that the capture of small and evasive prey such as grasshoppers is based on a quick strike that is carefully prepared. Moreover, our data show that varanids strike from further away, as shown by Figure 8. Scatter plots illustrating variability in skull the significantly greater predator–prey distance at velocity during the strike (standardized in respect to jaw the onset of jaw opening (Table 1). The ability to length) in Gerrhosaurus major, Tupinambis merianae, and initiate the strike from further away may reduce the Varanus niloticus and V. ornatus. A, bivariate correlation risk of triggering an anti-predator response of the between standardized skull velocity and multivariate prey (i.e. escape), thus enhancing the chances of factor 1, representing time of maximum neck elevation success in prey capture. Varanid lizards may have and time of jaw opening (see Table 2 for the complete evolved to capture evasive prey by using quick strikes loadings). B, bivariate correlation between standardized triggered from further away, which benefit from a skull velocity and latency of neck elevation with respect to jaw–neck–forelimb coordination pattern favouring the jaw opening. C, bivariate correlation between standardized skull velocity and predator–prey distance at the onset preparation of the strike. In this context, the jaw– of jaw-opening (standardized with respect to jaw length). neck–forelimb coordination pattern characterizing Symbols represent taxa: squares for G. major, circles for varanids is proposed to be linked to their specializa- T. merianae, and triangles for V. niloticus and V. ornatus. tion for feeding on evasive prey, thus reflecting that Only significant correlations are presented. locomotor–feeding integration can contribute in the

© 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105, 607–622 JAW–NECK–FORELIMB COORDINATION IN LIZARDS 619 adaptation of feeding behaviour with respect to 2008) of feeding movements contributes to responding feeding ecology. to specific physical, textural, and behavioural charac- The timing of jaw–neck coordination, and to a lesser teristics of the prey in many vertebrate organisms. In extent timing of jaw–forelimb coordination, appears particular, cordyliform lizards, including G. major, to differ between ecologically convergent predators, are able to switch between tongue prehension and jaw T. merianae and varanid lizards (Figs 6B, C, 7). On prehension depending on the prey (Urbani & Bels, the other hand, the jaw–neck–forelimb coordination 1995; Smith, Kardong & Bels, 1999; Schwenk, 2000b; pattern of T. merianae is more similar to that of Reilly & McBrayer, 2007; Montuelle et al., 2009a). G. major (Figs 6A, B, 7). Tupinambis merianae and Thus, the jaw apparatus of cordyliform lizards is G. major are both Scincomorphan lizards, and thus integrated with the hyolingual apparatus. However, are more closely related to each other than to varanid because of the use of jaw prehension, jaw movements lizards (Estes, De Queiroz & Gauthier, 1988; are also limited through the constraints imposed by Schwenk, 2000b; Fig. 1A). Consequently, our study their integration with the anterior locomotor ele- suggests that the diversity of locomotor–feeding inte- ments. Consequently, cordyliform lizards use different gration during prey capture behaviour among squa- coordination patterns and are able to alter locomotor– mate taxa, as presented here, may carry a feeding integration in response to prey type (Montu- phylogenetic signal. Of course, such a hypothesis will elle et al., 2009a). Flexibility in locomotor–feeding require a broader phylogenetic framework to be tested integration may thus be a critical advantage when explicitly. Nevertheless, in the taxa investigated here, feeding on a wide variety of food items. Interestingly, phylogeny appears to supersede the convergent eco- both jaw and neck movements are affected by vari- logical constraints associated with feeding behaviour. ability in prey size and mobility in G. major (Montu- elle et al., 2010), but flexibility in jaw–neck–forelimb coordination in response to relevant prey stimuli VARIABILITY OF JAW–NECK–FORELIMB remains to be tested. Although in its infancy, the link COORDINATION PATTERNS between feeding ecology, especially diet particulari- Our data also show that quick strikes in T. merianae ties, and variability in locomotor–feeding integration and G. major are characterized by reduced latency of appears to be a promising avenue for understanding maximum neck elevation with respect to jaw opening the evolution of feeding behaviour in the squamate (Fig. 8B), illustrating that neck elevation tends to be lineage. achieved earlier, i.e. closer to jaw opening, when strik- In conclusion, our results demonstrate the coordi- ing more quickly. This indicates that T. merianae and nation of movements of the forelimbs and the cervical G. major are able to alter the jaw–neck coordination region of the vertebral column with jaw-opening pattern depending on the speed of strike. In another movements during jaw prehension in four lizard lizard, Anolis carolinensis, two prey capture strate- species. Significant differences in jaw–neck–forelimb gies have been described (Montuelle, Daghfous & coordination suggest that the diversity of locomotor– Bels, 2008). Although jaw–neck–forelimb coordination feeding integration may be of critical importance in has not been tested in A. carolinensis, each strategy the variability of strike performance in organisms appears to recruit different jaw–neck–forelimb coor- that use jaw prehension during prey capture behav- dination patterns which resemble those observed here iour. These differences are proposed to be associated in autarchoglossan lizards; for example, head-up with different strike strategies which reflect particu- capture resembles the jaw–neck–forelimb coordina- larities of the feeding ecology (e.g. differences in diet) tion pattern used by T. merianae and G. major, of the species investigated. From an evolutionary whereas jump capture may resemble the one used by point of view, such coordination probably generates varanids. This suggests that jaw–neck–forelimb coor- integrative constraints that can affect the adaptation dination is also variable in A. carolinensis. Variability of both the feeding and the locomotor elements. in the jaw–neck coordination pattern suggests that Indeed, because of their integration during tongue the motor pattern responsible for locomotor–feeding prehension (e.g. Kraklau, 1991; Wainwright, Kraklau integration can be modulated. Further investigations & Bennett, 1991; Wainwright & Bennett, 1992; of locomotor–feeding integration will thus have to test Herrel, Cleuren & de Vree, 1995; Meyers & Nish- for the potential sources of such variability. The com- ikawa, 2000; Meyers & Herrel, 2005), the jaw appa- parison of variability in locomotor–feeding integration ratus and the hyolingual apparatus are thought to be may provide insight into the diversity of feeding an evolutionary stable configuration (ESC) in igua- behaviours. nian lizards (Wagner & Schwenk, 2000; Schwenk & In the context of feeding, variability of movements Wagner, 2001). Given the importance of locomotor– are relevant with respect to prey properties. Indeed, feeding integration for jaw prehension, the jaw appa- flexibility (sensu Wainwright, Mehta & Higham, ratus may also constitute an ESC with the locomotor

© 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105, 607–622 620 S. J. MONTUELLE ET AL. elements in other lizards, although this will need a Lacertid lizards and the relationship of prey odor discrimi- wider taxonomic sample to be demonstrated. nation to foraging mode in lizard families. Copeia 1990: 237–242. Cooper WE Jr. 1995. Foraging mode, prey chemical discrimi- ACKNOWLEDGEMENTS nation, and phylogeny in lizards. Animal Behaviour 50: 973–985. This work is part of the PhD project of S.J.M. while at Cooper WE Jr. 1996. Preliminary reconstructions of nasal the Muséum National d’Histoire Naturelle (MNHN) chemosensory evolution in Squamata. Amphibia-Reptilia in Paris, France, which was supported by the Legs 17: 395–415. Prévost (MNHN), ANR 06-BLAN-0132-02 and Cooper WE Jr. 2002. Convergent evolution of plant chemical Phymep. S.J.M. is now a postdoctoral associate at discrimination by omnivorous and herbivorous scleroglossan Ohio University Heritage College of Osteopathic lizards. Journal of Zoology, London 257: 53–66. Medicine (OU-HCOM) in Athens, OH, USA, sup- Cooper WE Jr, Habegger JJ. 2001. Responses by juvenlie ported by NSF grant MRI DBI-0922988. We thank savannah monitor lizards (Varanus exanthematicus)to Susan H. Williams at OU-HCOM for comments on the chemical cues from animal prey, plants palatable to herbi- manuscript and the reviewers for their constructive vores, and conspeciﬁcs. Journal of Herpetology 35: 618–624. comments on the ﬁrst version of the manuscript. We Cooper WE Jr, Steele LJ. 1999. Mediated discriminations also thank ANR project Kameleon (ARA 05-MMSA- among prey chemicals and control stimuli in Cordyliform 0002 ‘Masse de Données’) which provided the oppor- lizards: presence in a Gerrhosaurid and absence in two tunity to use the synchronized camera set-up at the Cordylids. 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