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.

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.

Inner architecture of vertebral centra in terrestrial and aquatic mammals: a two-dimensional comparative study.

Inner vertebral architecture is poorly known, except in human and laboratory animals. In order to document this topic at a broad comparative level, a 2D-histomorphometric study of vertebral centra was conducted in a sample of 98 therian mammal species, spanning most of the size range and representing the main locomotor adaptations known in therian taxa. Eleven variables relative to the development and geometry of trabecular networks were extracted from CT scan mid-sagittal sections. Phylogeny-informed statistical tests were used to reveal the respective influences of phylogeny, size, and locomotion adaptations on mammalian vertebral structure. The use of random taxon reshuffling and squared change parsimony reveals that 9 of the 11 characteristics (the two exceptions are total sectional area and structural polarization) contain a phylogenetic signal. Linear discriminant analyses suggest that the sampled taxa can be arranged into three categories with respect to locomotion mode: a) terrestrial + flying + digging + amphibious forms, b) coastal oscillatory aquatic taxa, and c) pelagic oscillatory aquatic forms represented by oceanic cetaceans. Pairwise comparison tests and linear regressions show that, when specific size increases, the length of trabecular network (Tt.Tb.Le), as well as trabecular proliferation in total sections (Pr.Tb.Tt), increase with positive allometry. This process occurs in all locomotion categories but is particularly pronounced in pelagic oscillators. Conversely, mean trabecular width has a lesser increase with size in pelagic oscillators. Trabecular orientation is not influenced by size. All tests were corrected for multiple testing. By using six structural variables or indices, locomotion mode can be predicted with a 97.4% success rate for terrestrial forms, 66.7% for coastal oscillatory, and 81.3% for pelagic oscillatory. The possible functional meaning of these results and their potential use for paleobiological inference of locomotion in extinct taxa are discussed.

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.

Spatio-temporal analysis of locomotion in BALB/cByJ and C57BL/6J mice in different environmental conditions.

We analysed spatial and temporal characteristics of mouse locomotion and investigated whether mouse gait differed between strains and environments. To this end, we used two inbred strains of mice (BALB/cByJ and C57BL/6J) known for their contrasting inherent level of anxiety, in three different visual surroundings. The animal position was determined relative to each environment. Gait cycle, defined as the sequence of limb movements, was analysed relative to time. We also recorded spatial parameters of gait such as stride length, track width and footfall characteristics. These measures allowed us to obtain an accurate description of locomotion and to assess subtle modifications of the gait. We found that mice adjusted their position in space, posture and gait in order to either stabilize their body on the ground in a potentially unsafe environment, or to optimize propulsion and maneuverability in a safer location. In addition, the two strains of mice used different strategies, suggesting that the inherent level of emotionality may affect the organization of locomotion in mice. We further concluded that higher structures of the central nervous system are involved in the online control of locomotion.