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.

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.

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.

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.

Inertial feeding in the teiid lizard Tupinambis merianae: the effect of prey size on the movements of hyolingual apparatus and the cranio-cervical system.

In most terrestrial tetrapods, the transport of prey through the oral cavity is accomplished by movements of the hyolingual apparatus. Morphological specializations of the tongue in some lizard taxa are thought to be associated with the evolution of vomerolfaction as the main prey detection mode. Moreover, specializations of the tongue are hypothesized to compromise the efficiency of the tongue during transport; thus, driving the evolution of inertial transport. Here we use a large teiid lizard, Tupinambis merianae, as a model system to test the mechanical link between prey size and the use of inertial feeding. We hypothesize that an increase in prey size will lead to the increased recruitment of the cranio-cervical system for prey transport and a reduced involvement of the tongue and the hyolingual apparatus. Discriminant analyses of the kinematics of the cranio-cervical, jaw and hyolingual systems show that the transport of large prey is indeed associated with a greater utilization of the cranio-cervical system (i.e. neck and head positioning). The tongue retains a kinematic pattern characteristic of lingual transport in other lizards but only when processing small prey. Our data provide evidence for an integration of the hyolingual and cranio-cervical systems; thus, providing partial support for an evolutionary scenario whereby the specialization of the tongue for chemoreception has resulted in the evolution of inertial transport strategies.

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.

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.

Steady locomotion in dogs: temporal and associated spatial coordination patterns and the effect of speed.

Only a few studies on quadrupedal locomotion have investigated symmetrical and asymmetrical gaits in the same framework because the mechanisms underlying these two types of gait seem to be different and it took a long time to identify a common set of parameters for their simultaneous study. Moreover, despite the clear importance of the spatial dimension in animal locomotion, the relationship between temporal and spatial limb coordination has never been quantified before. We used anteroposterior sequence (APS) analysis to analyse 486 sequences from five malinois (Belgian shepherd) dogs moving at a large range of speeds (from 0.4 to 10.0 m s(-1)) to compare symmetrical and asymmetrical gaits through kinematic and limb coordination parameters. Considerable continuity was observed in cycle characteristics, from walk to rotary gallop, but at very high speeds an increase in swing duration reflected the use of sagittal flexibility of the vertebral axis to increase speed. This change occurred after the contribution of the increase in stride length had become the main element driving the increase in speed - i.e. when the dogs had adopted asymmetrical gaits. As the left and right limbs of a pair are linked to the same rigid structure, spatial coordination within pairs of limbs reflected the temporal coordination within pairs of limbs whatever the speed. By contrast, the relationship between the temporal and spatial coordination between pairs of limb was found to depend on speed and trunk length. For trot and rotary gallop, this relationship was thought also to depend on the additional action of trunk flexion and leg angle at footfall.

The mechanism of dewlap extension in Anolis carolinensis (Reptilia: Iguanidae) with histological analysis of the hyoid apparatus.

Anolis carolinensis has two aggressive displays involving movements of the hyoid apparatus: erection of the throat and extension of the dewlap. Erection of the throat is an enlargement of the gular region and dewlap extension consists of a vertical erection of the gular flap. Cinefluoroscopy and high speed cinematography show that the dewlap is extended in three phases: 1) protraction of the entire hyoid apparatus; 2) forward pivoting movement of the ceratobranchials II; and 3) retraction of the ceratobranchials II and the entire hyoid apparatus. The cartilaginous elements of the hyoid apparatus are variably mineralized. The entoglossal process and the hypohyals are the most calcified elements. The mineralized portion of the hyoid body, to which the other elements articulate, presents a complex pattern. The calcification of entoglossal process and the hypohyals stop just where they are fused with the hyoid body. The hyoid body presents four mineralized masses, two central corresponding to the base of the ceratobranchials II and two lateral being the head of the ossified ceratobranchials I. The lateral masses articulate on the central masses by a synovial joint. Morphologically, the ceratobranchials II form the hyoid body and become separated at the mid length of the synovial articulation of the ceratobranchials I and the hyoid body. The calcified matrix of the ceratobranchials II gradually changes from a large calcified mass (within the hyoid body) to a semicircle, opened ventrally, which permits their bending during dewlap extension. The highly mineralized posterior tip of the entoglossal process and the hyoid body serve as a pivot to pivoting forward movement of the ceratobranchials II producing at the change of the pattern of mineralization. Forward movement of the ceratobranchials II is produced by electrical stimulation of the M. branchio hyoideus. The opposition of the throat skin to the movement of the ceratobranchials II produces the bending of those longest elements. Electrical stimulation of the hyoid muscles confirms the key role of M. branchiohyoideus during dewlap extension. Simultaneous contractions of all the hyoid and extrinsic tongue (retractor and protractor) muscles with the M. branchiohyoideus during dewlap extension may be a possible motor pattern for dewlap extension in Anolis lizards.