Morphology and fibre-type distribution in the tongue of the Pogona vitticeps lizard (Iguania, Agamidae).

Agamid lizards use tongue prehension for capturing all types of prey. The purpose of this study was to investigate the functional relationship between tongue structure, both surface and musculature, and function during prey capture in Pogona vitticeps. The lack of a detailed description of the distribution of fibre-types in the tongue muscles in some iguanian lizards has hindered the understanding of the functional morphology of the lizard tongue. Three methodological approaches were used to fill this gap. First, morphological analyses were performed (i) on the tongue surface through scanning electron microscopy, and (ii) on the lingual muscle by histological coloration and histochemistry to identify fibre-typing. Secondly, kinematics of prey capture was quantified by using high-speed video recordings to determine the movement capabilities of the tongue. Finally, electromyography (EMG) was used to identify the motor pattern tongue muscles during prey capture. Morphological and functional data were combined to discuss the functional morphology of the tongue in agamid lizards, in relation to their diet. During tongue protraction, M. genioglossus contracts 420 ± 96 ms before tongue-prey contact. Subsequently, Mm. verticalis and hyoglossus contract throughout tongue protraction and retraction. Significant differences are found between the timing of activity of the protractor muscles between omnivorous agamids (Pogona sp., this study) and insectivorous species (Agama sp.), despite similar tongue and jaw kinematics. The data confirm that specialisation toward a diet which includes more vegetal materials is associated with significant changes in tongue morphology and function. Histoenzymology demonstrates that protractor and retractor muscles differ in fibre composition. The proportion of fast glycolytic fibres is significantly higher in the M. hyoglossus (retractor muscle) than in the M. genioglossus (protractor muscle), and this difference is proposed to be associated with differences in the velocity of tongue protrusion and retraction (5 ± 5 and 40 ± 13 cm s(-1) , respectively), similar to Chamaeleonidae. This study provides a way to compare fibre-types and composition in all iguanian and scleroglossan lizards that use tongue prehension to catch prey.

Movement in a gravitational field: The question of limb interarticular coordination in terrestrial vertebrates.

In this paper, we demonstrated that interarticular coordination of terrestrial tetrapods emerges from an environment highly constrained by friction and the gravitational field. We briefly review recent works on the jumping behavior in squamates, lemurs and amphibians. We then explore previously published work as well as some unpublished experimental data on human jumping. Finally, we end by inferring locomotion in some of the first limbed vertebrates using a simulation procedure. All these data show that despite changes in shape, structure, and motor controls of taxa, the same spatio-temporal sequence of joint displacements always occurs when the movement is executed in a terrestrial environment. Comparison with aquatic locomotion argues for the hypothesis that this pattern emerged in early terrestrial tetrapods as a response to the gravitational constraint and the terrestrial frictional environment.

Food transport in Reptilia: a comparative viewpoint.

Reptilia exploit a large diversity of food resources from plant materials to living mobile prey. They are among the first tetrapods that needed to drink to maintain their water homeostasis. Here were compare the feeding and drinking mechanisms in Reptilia through an empirical approach based on the available data to open perspectives in our understanding of the evolution of the various mechanisms determined in these Tetrapoda for exploiting solid and liquid food resources. This article is part of the theme issue 'Food processing and nutritional assimilation in animals'.

The function of oscillatory tongue-flicks in snakes: insights from kinematics of tongue-flicking in the banded water snake (Nerodia fasciata).

Tongue-flicking is an important sensory behavior unique to squamate reptiles in which chemical stimuli gathered by the tongue are delivered the vomeronasal organ situated in the roof of the mouth. Because tongue-flick numbers can easily be quantified, this behavior has been widely used as a measure of vomeronasal sampling in snakes using related variables such as tongue-flick rate or tongue-flick/attack score. Surprisingly, the behavior itself and especially the function of the oscillatory tongue-flicks remains poorly understood. To describe the overall kinematics of tongue-flicking in the colubrid snake Nerodia fasciata and to test predictions on the function of oscillatory tongue-flicks, we filmed the tongue-flicks of 8 adult Nerodia fasciata using 4 synchronized high-speed cameras. Three-dimensional kinematic and performance variables were extracted from the videos in order to quantify tongue movements. Based on the kinematic analysis, we demonstrate the existence of 2 functional and behavioral tongue-flick categories. Tongue-flicks with oscillations meet all the criteria for being adapted to the collection of odorants; simple downward extensions appear better suited for the rapid pick up of nonvolatile chemical stimuli from the substrate or a food item. External stimuli such as tactile and/or vomeronasal stimulation can induce a shift between these categories.

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

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.

Studies of the Behavioral Sequences: The Neuroethological Morphology Concept Crossing Ethology and Functional Morphology.

Postures and movements have been one of the major modes of human expression for understanding and depicting organisms in their environment. In ethology, behavioral sequence analysis is a relevant method to describe animal behavior and to answer Tinbergen's four questions testing the causes of development, mechanism, adaptation, and evolution of behaviors. In functional morphology (and in biomechanics), the analysis of behavioral sequences establishes the motor pattern and opens the discussion on the links between "form" and "function". We propose here the concept of neuroethological morphology in order to build a holistic framework for understanding animal behavior. This concept integrates ethology with functional morphology, and physics. Over the past hundred years, parallel developments in both disciplines have been rooted in the study of the sequential organization of animal behavior. This concept allows for testing genetic, epigenetic, and evo-devo predictions of phenotypic traits between structures, performances, behavior, and fitness in response to environmental constraints. Based on a review of the literature, we illustrate this concept with two behavioral cases: (i) capture behavior in squamates, and (ii) the ritualistic throat display in lizards.

Variation in the sacroiliac joint in Felidae.

Felidae species show a great diversity in their diet, foraging and hunting strategies, from small to large prey. Whether they belong to solitary or group hunters, the behavior of cats to subdue resisting small or large prey presents crucial differences. It is assumed that pack hunting reduces the per capita risk of each individual. We hypothesize that the sacroiliac articulation plays a key role in stabilizing the predator while subduing and killing prey. Using CT-scan from 59 felid coxal bones, we calculated the angle between both iliac articular surfaces. Correlation of this inter-iliac angle with body size was calculated and ecological stressors were evaluated on inter-iliac angle. Body size significantly influences inter-iliac angle with small cats having a wider angle than big cats. Arboreal species have a significantly larger angle compared to cursorial felids with the smallest value, and to scansorial and terrestrial species with intermediate angles. Felids hunting large prey have a smaller angle than felids hunting small and mixed prey. Within the Panthera lineage, pack hunters (lions) have a larger angle than all other species using solitary hunting strategy. According to the inter-iliac angle, two main groups of felids are determined: (i) predators with an angle of around 40° include small cats (i.e., Felis silvestris, Leopardus wiedii, Leptailurus serval, Lynx Canadensis, L. rufus; median = 43.45°), the only pack-hunting species (i.e., Panthera leo; median = 37.90°), and arboreal cats (i.e., L. wiedii, Neofelis nebulosa; median = 49.05°), (ii) predators with an angle of around 30° include solitary-hunting big cats (i.e., Acinonyx jubatus, P. onca, P. pardus, P. tigris, P. uncia; median = 31.80°). We suggest different pressures of selection to interpret these results. The tightening of the iliac wings around the sacrum probably enhances big cats' ability for high speed and large prey control. In contrast, pack hunting in lions reduced the selective pressure for large prey.

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.

Hindlimb interarticular coordinations in Microcebus murinus in maximal leaping.

The purpose of this study was to investigate the pattern of coordinations of the hindlimb joints in the world's 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).

Assisted walking in Malagasy dwarf chamaeleons.

Chamaeleons are well known for their unique suite of morphological adaptations. Whereas most chamaeleons are arboreal and have long tails, which are used during arboreal acrobatic manoeuvres, Malagasy dwarf chamaeleons (Brookesia) are small terrestrial lizards with relatively short tails. Like other chamaeleons, Brookesia have grasping feet and use these to hold on to narrow substrates. However, in contrast to other chamaeleons, Brookesia place the tail on the substrate when walking on broad substrates, thus improving stability. Using three-dimensional synchrotron X-ray phase-contrast imaging, we demonstrate a set of unique specializations in the tail associated with the use of the tail during locomotion. Additionally, our imaging demonstrates specializations of the inner ear that may allow these animals to detect small accelerations typical of their slow, terrestrial mode of locomotion. These data suggest that the evolution of a terrestrial lifestyle in Brookesia has gone hand-in-hand with the evolution of a unique mode of locomotion and a suite of morphological adaptations allowing for stable locomotion on a wide array of substrates.

Iliac auricular surface morphofunctional study in felidae.

Felids show remarkable phenotypic similarities and are conservative in behavioral and ecological traits. In contrast, they display a large range in body mass from around 1kg to more than 300kg. Body size and locomotory specializations correlate to skull, limb and vertebral skeleton morphology. With an increase in body mass, felids prey selection switches from small to large, from using a rapid skull or spine lethal bite for small prey, to sustained suffocating bite for large prey. Dietary specialization correlates to skull and front limbs morphology but no correlation was found on the spine or on the hind limb. The morphology of the sacroiliac junction in relation to ecological factors remained to be described. We are presenting a study of the overall shape of the iliac auricular surface with qualitative and quantitative analyses of its morphology. Our results demonstrate that body mass, prey selection, and bite type, crucially influence the auricular surface, where no significant effect of locomotor specialization was found. The outline of the surface is significantly more elevated dorso-caudally and the joint surface shows an irregular W-shape topography in big cats whereas the surface in small cats is smoother with a C-shape topography and less of an elevated ridge. Biomechanically, we suggest that a complex auricular surface increases joint stiffness and provides more support in heavier cats, an advantage for subduing big prey successfully during a sustained bite.

Biomechanical study of grasping according to the volume of the object: human versus non-human primates.

The evolution of the precision grips, in which an object is held between the distal surfaces of thumb and fingers and the power grip, in which an object is grasped with the palm, is poorly understood in spite of hypothesis stipulating an evolution from power toward precision grips. In human, numerous studies have shown that the external factors such as the size or the form of an object influenced grasp patterns whereas in non-human primates, those parameters are poorly known. The objective of the present study was to investigate the variation in the use of different grips according to the volume of the object for six primate species representative of the phylogeny: human, chimpanzee, orangutan, macaque, baboon and capuchin. For those species, the grasping patterns were examined during grasping of spherical objects of two different volumes. Frame-by-frame analysis of digit contact strategies indicated: (1) an effect of the species on the category of grasping whatever the volume of the object, (2) a high degree of species variability and (3) no individual difference whatever the species. These results are discussed in relation to its potential contribution to understand the evolution of grasping.

Locomotion patterns in two South American gymnophthalmid lizards: Vanzosaura rubricauda and Procellosaurinus tetradactylus.

We quantified gait and stride characteristics (velocity, frequency, stride length, stance and swing duration, and duty factor) in the bursts of locomotion of two small, intermittently moving, closely related South American gymnophthalmid lizards: Vanzosaura rubricauda and Procellosaurinus tetradactylus. They occur in different environments: V. rubricauda is widely distributed in open areas with various habitats and substrates, while P. tetradactylus is endemic to dunes in the semi-arid Brazilian Caatinga. Both use trot or walking trot characterised by a lateral sequence. For various substrates in a gradient of roughness (perspex, cardboard, sand, gravel), both species have low relative velocities in comparison with those reported for larger continuously moving lizards. To generate velocity, these animals increase stride frequency but decrease relative stride length. For these parameters, P. tetradactylus showed lower values than V. rubricauda. In their relative range of velocities, no significant differences in stride length and frequency were recorded for gravel. However, the slopes of a correlation between velocity and its components were lower in P. tetradactylus on cardboard, whereas on sand this was only observed for velocity and stride length. The data showed that the difference in rhythmic parameters between both species increased with the smoothness of the substrates. Moreover, P. tetradactylus shows a highly specialised locomotor strategy involving lower stride length and frequency for generating lower velocities than in V. rubricauda. This suggests the evolution of a central motor pattern generator to control slower limb movements and to produce fewer and longer pauses in intermittent locomotion.

Assessment of the mass, length, center of mass, and principal moment of inertia of body segments in adult males of the brown anole (Anolis sagrei) and green, or carolina, anole (Anolis carolinensis).

This study provides a morphometric data set of body segments that are biomechanically relevant for locomotion in two ecomorphs of adult male anoles, namely, the trunk-ground Anolis sagrei and the trunk-crown Anolis carolinensis. For each species, 10 segments were characterized, and for each segment, length, mass, location of the center of mass, and radius of gyration were measured or calculated, respectively. The radii of gyration were computed from the moments of inertia by using the double swing pendulum method. The trunk-ground A. sagrei has relatively longer and stockier hindlimbs and forelimbs with smaller body than A. carolinensis. These differences between the two ecomorphs demonstrated a clear relationship between morphology and performance, particularly in the context of predator avoidance behavior, such as running or jumping in A. sagrei and crypsis in A. carolinensis. Our results provide new perspectives on the mechanism of adaptive radiation as the limbs of the two species appear to scale via linear factors and, therefore, may also provide explanations for the mechanism of evolutionary changes of structures within an ecological context.

Chemical basis of prey recognition in thamnophiine snakes: the unexpected new roles of parvalbumins.

Detecting and locating prey are key to predatory success within trophic chains. Predators use various signals through specialized visual, olfactory, auditory or tactile sensory systems to pinpoint their prey. Snakes chemically sense their prey through a highly developed auxiliary olfactory sense organ, the vomeronasal organ (VNO). In natricine snakes that are able to feed on land and water, the VNO plays a critical role in predatory behavior by detecting cues, known as vomodors, which are produced by their potential prey. However, the chemical nature of these cues remains unclear. Recently, we demonstrated that specific proteins-parvalbumins-present in the cutaneous mucus of the common frog (Rana temporaria) may be natural chemoattractive proteins for these snakes. Here, we show that parvalbumins and parvalbumin-like proteins, which are mainly intracellular, are physiologically present in the epidermal mucous cells and mucus of several frog and fish genera from both fresh and salt water. These proteins are located in many tissues and function as Ca(2+) buffers. In addition, we clarified the intrinsic role of parvalbumins present in the cutaneous mucus of amphibians and fishes. We demonstrate that these Ca(2+)-binding proteins participate in innate bacterial defense mechanisms by means of calcium chelation. We show that these parvalbumins are chemoattractive for three different thamnophiine snakes, suggesting that these chemicals play a key role in their prey-recognition mechanism. Therefore, we suggest that recognition of parvalbumin-like proteins or other calcium-binding proteins by the VNO could be a generalized prey-recognition process in snakes. Detecting innate prey defense mechanism compounds may have driven the evolution of this predator-prey interaction.

Tropical hornbills (Aceros cassidix, Aceros undulatus, and Buceros hydrocorax) use ballistic transport to feed with their large beaks.

The most common and plesiomorphic mechanism of food transport in tetrapods is lingual-based. Neognathous birds use this mechanism for exploiting a large diversity of food resources, whereas paleognathous birds use cranioinertial mechanism with or without tongue involvement. Food transport in three hornbills' species (Aceros cassidix, A. undulatus, and Buceros hydrocorax) is defined by a ballistic transport mechanism. Only one transport cycle is used for moving the food from the tip of the beak to the pharynx. The tongue never makes contact with the food nor is it used to expand the buccal cavity. In hornbills, filmed through high-speed video, time to food release occurred between 0.11 and 0.16 sec before time to maximum gape. The ballistic curves show similar patterns. Maximum gape angle is significantly different between the three species. Each species show a different kinematic and motor pattern of head movements associated with ballistic transport. In A. undulatus, head rotation follows a continuous pattern similar to that reported earlier in toucans. A. cassidix rotates head downward at the time of maximum gape to permit food to reach the pharynx without touching the mandible. B. hydrocorax elevates the head along the transport cycle to avoid contact with the food to the cavity of the upper beak. Selection of large food items in the diet may explain the evolutionary trend of using ballistic transport in the feeding behavior of hornbills, which play a key role in tropical forest ecology by dispersing seeds.

Submaximal leaping in the grey mouse lemur.

In arboreal animals such as the grey mouse lemur (Microcebus murinus Miller, 1777), leaping is the most frequent strategy for predator avoidance. The aim of this study was to characterise the locomotor adaptation in response to the structural constraint of the habitat (i.e., position of the landing substrate). Thus, we characterised the push-off phase by inducing the lemurs to leap up to a range of heights from horizontal to their own individual highest performance. Using uniplanar high-frequency cineradiographs collected in a sagittal plane, the relative contributions of the centre of mass (CoM) velocity vector magnitude and orientation to leaping performance were evaluated. The kinematics of the push-off phase showed that for low landing heights, leaping performance was essentially due to hip and knee extensions. Higher leaps seemed to be related to an increase in ankle contribution. At all leaping heights, the proximal-to-distal sequence of the hind limb joints controlled the orientation and magnitude of the M. murinus CoM velocity vector while pushing off. Finally, the analysis of the velocity vector at the onset of take-off suggested that the optimal solution for predator avoidance was to leap for horizontal distance and not for vertical distance.

Ballistic food transport in toucans.

The basic mechanism of food transport in tetrapods is lingual-based. Neognathous birds use this mechanism for exploiting a large diversity of food resources, whereas paleognathous birds use cranioinertial mechanism with or without tongue involvement. Food transport in two neognathous species of toucans (Ramphastos toco and R. vitellinus) is defined as ballistic transport mechanism. Only one transport cycle is used for moving the food from the tip of the beak to the pharynx. The food is projected between jaws with similar initial velocity in both species. At the time of release, the angle between trajectory of food position and horizontal is higher in R. vitellinus with a shorter beak than in R. toco. The tongue never makes contact with the food nor is it used to expand the buccal cavity. Tongue movement is associated with throat expansion, permitting the food to reach the entrance of the esophagus at the end of the ballistic trajectory. Selection of large food items in the diet may explain the evolutionary trend of using ballistic transport in the feeding behavior of toucans, which plays a key role in ecology of tropical forest.

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

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.