Stéphane J. Montuelle

Locomotor-feeding coupling during prey capture in a lizard (Gerrhosaurus major): effects of prehension mode

SUMMARY In tetrapods, feeding behaviour in general, and prey capture in particular, involves two anatomical systems: the feeding system and the locomotor system. Although the kinematics associated with the movements of each system have been investigated in detail independently, the actual integration between the two systems has received less attention. Recently, the independence of the movements of the jaw and locomotor systems was reported during tongue-based prey capture in an iguanian lizard (Anolis carolinensis), suggesting a decoupling between the two systems. Jaw prehension, on the other hand, can be expected to be dependent on the movements of the locomotor system to a greater degree. To test for the presence of functional coupling and integration between the jaw and locomotor systems, we used the cordyliform lizard Gerrhosaurus major as a model species because it uses both tongue and jaw prehension. Based on a 3-D kinematic analysis of the movements of the jaws, the head, the neck and the forelimbs during the approach and capture of prey, we demonstrate significant correlations between the movements of the trophic and the locomotor systems. However, this integration differs between prehension modes in the degree and the nature of the coupling. In contrast to our expectations and previous data for A. carolinensis, our data indicate a coupling between feeding and locomotor systems during tongue prehension. We suggest that the functional integration between the two systems while using the tongue may be a consequence of the relatively slow nature of tongue prehension in this species.

Hindlimb interarticular coordinations in Microcebus murinus in maximal leaping.

SUMMARY The purpose of this study was to investigate the pattern of coordinations of the hindlimb joints in the worlds smallest living primate (Microcebus murinus). The sequencing and timing of joint rotations have been analyzed in five adult males performing maximal leaping from a take-off immobile platform to their own wooden nest. Angular kinematics of hip, knee, angle and metatarso-phalangeal (MT) joints were deduced from high-speed X-ray films in the sagittal plane of the animals. The body mass center (BMC) of the lemurs was assimilated to their iliac crest. The maximal airborne performance of the lemurs was 0.33±0.04 m, which represented 2.55±0.36 times their snout–vent length. Take-off instant occurred 72±7 ms after the start of the push-off, with a BMC velocity of 3.23±0.48 m s−1, oriented 55±14 deg. with the horizontal plane. The kinematic analysis of the joints and musculo-tendon architecture of the M. murinus plantar flexors pointed out mechanical power amplifier mechanisms (i.e. stretch-shortening cycle of hindlimb muscles and proximo-to-distal sequence).

Conquering the world in leaps and bounds: hopping locomotion in toads is actually bounding

Summary While most frogs maximize jump distance as an escape behaviour, toads have traded jump distance for endurance with a strategy of hopping repeatedly. This strategy has enabled toads to expand across the continents as one of the most diverse groups of anurans. Multiple studies have revealed physiological endurance adaptations for sustained hopping in toads, however, the kinematics of their sequential hopping behaviour, per se, has not been studied. We compared kinematics and forces of single hops and multiple hopping sequences and quantified field performance of hopping behaviours in free ranging toads of three species and discovered a novel aspect of locomotion adaptation that adds another facet to their exceptional terrestrial locomotor abilities. We found that bouts of repeated hopping are actually a series of bounding strides where toads rotate on their hands and then land on their extended their feet and jump again without stopping. In addition, free-ranging toads appear to use bounding locomotion more frequently than single hops. Bounding in toads has the advantage of maintaining velocity and producing longer jump distances. In comparison to single hops, cyclic bounding steps reduce energy expenditure and appear to provide limb loading dynamics better suited for potential cycling of elastic energy from stride to stride than would be possible with repeated single hops. This is the first case of the common use of a bounding gait outside of mammals. Bounding adds a key terrestrial locomotor trait to the toads phenotype that may help explain their history of global expansion and the challenges to modern faunas as introduced toads rapidly invade new ecosystems today.

Functional evolution of jumping in frogs: Interspecific differences in take-off and landing

Ancestral frogs underwent anatomical shifts including elongation of the hindlimbs and pelvis and reduction of the tail and vertebral column that heralded the transition to jumping as a primary mode of locomotion. Jumping has been hypothesized to have evolved in a step‐wise fashion with basal frogs taking‐off with synchronous hindlimb extension and crash‐landing on their bodies, and then their limbs move forward. Subsequently, frogs began to recycle the forelimbs forward earlier in the jump to control landing. Frogs with forelimb landing radiated into many forms, locomotor modes, habitats, and niches with controlled landing thought to improve escape behavior. While the biology of take‐off behavior has seen considerable study, interspecific comparisons of take‐off and landing behavior are limited. In order to understand the evolution of jumping and controlled landing in frogs, data are needed on the movements of the limbs and body across an array of taxa. Here, we present the first description and comparison of kinematics of the hindlimbs, forelimbs and body during take‐off and landing in relation to ground reaction forces in four frog species spanning the frog phylogeny. The goal of this study is to understand what interspecific differences reveal about the evolution of take‐off and controlled landing in frogs. We provide the first comparative description of the entire process of jumping in frogs. Statistical comparisons identify both homologous behaviors and significant differences among species that are used to map patterns of trait evolution and generate hypotheses regarding the functional evolution of take‐off and landing in frogs. J. Morphol. 277:379–393, 2016.

Effect of Locomotor Approach on Feeding Kinematics in the Green Anole (Anolis carolinensis)

Squamates are well-known models for studying to examine locomotor and feeding behaviors in tetrapods, but studies that integrate both behavioral activities remain scarce. Anolis lizards are a classical lineage to study the evolutionary relationships between locomotor behavior and complex structural features of the habitat. Here, we analyzed prey-capture behavior in one representative arboreal predator, Anolis carolinensis, to demonstrate the functional links between locomotor strategies and the kinematics of feeding. A. carolinensis uses two strategies to catch living insects on perches: Head-Up Capture and Jump Capture. In both cases, lizards use lingual prehension to capture the prey and the kinematic patterns of the trophic apparatus are not significantly influenced by the selected strategies. Therefore, to capture one prey type, movements of the trophic structures are highly fixed and A. carolinensis modulates the locomotor pattern to exploit the environment. Predation behavior in A. carolinensis integrates two different behavioral patterns: locomotor plasticity of prey-approach and biomechanical stereotypy of tongue prehension to successfully capture the prey.

Morphology and Histology of the Tongue and Oral Chamber of Eublepharis macularius (Squamata: Gekkonidae), with Special Reference to the Foretongue and its Role in Fluid Uptake and Transport

Detailed descriptions of tongue morphology of members of Squamata that refer to functional implications other than food processing are rare. Herein we focus on the morphology of the dorsal epithelium and internal structure of the tongue of the Leopard Gecko, Eublepharis macularius, emphasizing the foretongue and its relation to fluid uptake. We employ both scanning electron microscopy and serial histology to examine the morphology of the entire tongue, its component regions, and its situation in the oral chamber. We recognize five distinct morphological regions of the dorsal tongue surface, each of which is distinctive both morphologically and histologically. The foretongue bears papillae quite different in structure and spacing from those of all other tongue regions, and these non-glandular structures are involved in gathering and transporting fluid from the environment. Fluid unloaded from the foretongue in the region of the vomeronasal sinus is channeled through the network of cuboidal papillae and directed towards a pair of compartments lateral to the tongue in which fluid pools during a drinking bout. This allows the dorsal surface of the mid- and hind-tongue, which are involved in food processing and manipulation, to be largely segregated from the pathway of fluid flow. We relate our findings to descriptions of the tongue of other taxa, and propose functional hypotheses for the observed morphology. This study provides new anatomical information upon which future studies of the functional morphology of the buccal apparatus in the Gekkota can be based.

Flexibility in locomotor–feeding integration during prey capture in varanid lizards: effects of prey size and velocity

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.

Mandibular corpus bone strains during mastication in goats (Capra hircus): A comparison of ingestive and rumination chewing

OBJECTIVE To compare the mechanical loading environment of the jaw in goats during ingestive and rumination chewing. DESIGN Rosette strain gauges were attached to the external surface of the mandibular corpus in five goats to record bone strains during the mastication of hay and rumination. RESULTS Strain magnitudes and maximum physiological strain rates during the mastication of hay are significantly higher than during rumination chewing on the working and balancing sides. Principal strain ratios and orientations are similar between the two chewing behaviours. Loading and chewing cycle duration are all longer during rumination chewing, whereas chew duty factor and variances in load and chewing cycle durations are higher during ingestive chewing. For most of the variables, differences in strain magnitudes or durations are similar at all three gauge sites, suggesting that rumination and ingestive chewing do not differentially influence bone at the three gauge sites. CONCLUSIONS Despite lower strain magnitudes, the repetitive nature of rumination chewing makes it an important component of the mechanical loading environment of the selenodont artiodactyl jaw. However, similarities in principal strain orientations and ratios indicate that rumination chewing need not be considered as a unique loading behaviour influencing the biomechanics of the selenodont artiodactyl jaw. Differences in loading and chewing cycle durations during rumination and ingestion demonstrate flexibility in adult chewing frequencies. Finally, although the low within-sequence variability in chewing cycle durations supports the hypothesis that mammalian mastication is energetically efficient, chewing during rumination may not be more efficient than during ingestion.

Separating the effects of prey size and speed on the kinematics of prey capture in the omnivorous lizard Gerrhosaurus major

Feeding behavior is known to be modulated as prey properties change. During prey capture, external prey properties, including size and mobility, are likely some of the most important components in predator–prey interactions. Whereas prey size has been demonstrated to elicit modulation of jaw movements during capture, how prey speed affects the approach and capture of prey remains unknown. We quantified the kinematics associated with movements of both the feeding and locomotor systems during prey capture in a lizard, Gerrhosaurus major, while facing prey differing in size and mobility (newborn mice, grasshoppers, and mealworms). Our data show that the feeding and locomotor systems were recruited differently in response to changes in the size or speed of the prey. The timing of jaw movements and of the positioning of the head are affected by changes in prey size—and speed, to a lesser extent. Changes in prey speed resulted in concomitant changes in the speed of strike and an early and greater elevation of the neck. External prey properties, and prey mobility in particular, are relevant in predator–prey interactions and elicit specific responses in different functional systems.

In Vivo Measurement of Mesokinesis in Gekko gecko: The Role of Cranial Kinesis during Gape Display, Feeding and Biting

Cranial kinesis refers to movements of skeletal sub-units relative to one another at mobile sutures within the skull. The presence and functional significance of cranial kinesis has been investigated in various vertebrates, with much of our understanding coming from comparative studies and manipulation of ligamentous specimens. Drawing on these studies, cranial kinesis in lizards has been modeled as a four-bar linkage system involving streptostyly (rotation of the quadrate), hypokinesis (dorsoventral flexion and extension of the palato-maxillary sub-unit), mesokinesis (dorsoventral flexion and extension of the snout at the fronto-parietal suture) and metakinesis (sliding movements between parietal and supraocciptal bones). In vivo studies, although limited, suggest that cranial kinesis serves an important role during routine behaviors such as feeding. Here, we use X-ray Reconstruction Of Moving Morphology to further quantify mesokinesis in vivo in Gekko gecko during three routine behaviors: gape display, biting and post-ingestion feeding. During gape display, the snout rotates dorsally above rest position, with mesokinesis accounting for a 10% increase in maximum gape over that achieved solely by the depression of the lower jaw. During defensive biting, the snout rotates ventrally below rest position to participate in gape closure. Finally, ventroflexion of the snout also occurs during post-ingestion feeding, accounting for 42% of gape closure during intra-oral transport, 86% during puncture-crushing, and 61% during pharyngeal packing. Mesokinesis thus appears to facilitate prey puncturing by allowing the snout to rotate ventrally so that the upper teeth pierce the prey item, thus limiting the need for large movements of the lower jaw. This is suggested to maintain a firm grip on the prey and reduce the possibility of prey escape. More generally, this study demonstrates that mesokinesis is a key component of defensive biting and gape display behaviors, as well as post-ingestion feeding, all of which are linked to organismal fitness.