Estimation of the forces exerted on the limb long bones of a white rhinoceros (Ceratotherium simum) using musculoskeletal modelling and simulation.

Heavy animals incur large forces on their limb bones, due to the transmission of body weight and ground reaction forces, and the contractions of the various muscles of the limbs. This is particularly true for rhinoceroses, the heaviest extant animals capable of galloping. Several studies have examined their musculoskeletal system and the forces their bones incur, but no detailed quantification has ever been attempted. Such quantification could help understand better the link between form and function in giant land animals. Here we constructed three-dimensional musculoskeletal models of the forelimb and hindlimb of Ceratotherium simum, the heaviest extant rhino species, and used static optimisation (inverse) simulations to estimate the forces applied on the bones when standing at rest, including magnitudes and directions. Overall, unsurprisingly, the most active muscles were antigravity muscles, which generate moments opposing body weight (thereby incurring the ground reaction force), and thus keep the joints extended, avoiding joint collapse via flexion. Some muscles have an antigravity action around several joints, and thus were found to be highly active, likely specialised in body weight support (ulnaris lateralis; digital flexors). The humerus was subjected to the greatest amount of forces in terms of total magnitude; forces on the humerus furthermore came from a great variety of directions. The radius was mainly subject to high-magnitude compressive joint reaction forces, but to little muscular tension, whereas the opposite pattern was observed for the ulna. The femur had a pattern similar to that of the humerus, and the tibia's pattern was intermediate, being subject to great compression in its caudal side but to great tension in its cranial side (i.e. bending). The fibula was subject to by far the lowest force magnitude. Overall, the forces estimated were consistent with the documented morphofunctional adaptations of C. simum's long bones, which have larger insertion areas for several muscles and a greater robusticity overall than those of lighter rhinos, likely reflecting the intense forces we estimated here. Our estimates of muscle and bone (joint) loading regimes for this giant tetrapod improve the understanding of the links between form and function in supportive tissues and could be extended to other aspects of bone morphology, such as microanatomy.

Effect of mass and habitat on the shape of limb long bones: A morpho-functional investigation on Bovidae (Mammalia: Cetartiodactyla).

Limb long bones are essential to an animal's locomotion, and are thus expected to be heavily influenced by factors such as mass or habitat. Because they are often the only organs preserved in the fossil record, understanding their adaptive trends is key to reconstructing the paleobiology of fossil taxa. In this regard, the Bovidae has always been a prized group of study. This family is extremely diverse in terms of both mass and habitat, and it is expected that their bones will possess adaptations to both factors. Here, we present the first 3D geometric morphometric study focusing on bovid limb long bones. We used anatomical landmarks as well as curve and surface sliding semi-landmarks to accurately describe the stylopod and zeugopod bones. We included 50 species from ten of the twelve currently recognized tribes of bovids, ranging from 4.6 to 725 kg, and living in open plains, forests, mountains, or anywhere in-between. Shape data were correlated with the mean mass of the species and its habitat, even when taking into account the phylogenetic history of our sample. Bones pertaining to heavy species are more robust, adapted for a better repartition of stronger forces. Articulations are especially affected, being proportionally much larger in heavier species. Muscle insertion areas are unevenly affected. Insertion areas of muscles implied in body support and propulsion show a strong increase in their robustness when compared to insertion areas of muscles acting on the limb mostly when it is off the ground. Habitat influences the shape of the humerus, the radius-ulna, and the femur, but not of the tibia, whether the phylogeny is taken into account or not. Specific habitats tend to be associated with particular features on the bones. Articulations are proportionally wider in open-habitat species, and the insertion areas of muscles involved in limb extension and propulsion are wider, reflecting the fact that open habitat species are more cursorial and rely on fast running to avoid predators. Forest and mountain species generally present similar adaptations for increased manoeuvrability, such as a round femoral head, and generally have more gracile bones.

Limb myology and muscle architecture of the Indian rhinoceros Rhinoceros unicornis and the white rhinoceros Ceratotherium simum (Mammalia: Rhinocerotidae).

Land mammals support and move their body using their musculoskeletal system. Their musculature usually presents varying adaptations with body mass or mode of locomotion. Rhinocerotidae is an interesting clade in this regard, as they are heavy animals potentially reaching three tons but are still capable of adopting a galloping gait. However, their musculature has been poorly studied. Here we report the dissection of both forelimb and hindlimb of one neonate and one adult each for two species of rhinoceroses, the Indian rhinoceros (Rhinoceros unicornis) and the white rhinoceros (Ceratotherium simum). We show that their muscular organisation is similar to that of their relatives, equids and tapirs, and that few evolutionary convergences with other heavy mammals (e.g. elephants and hippopotamuses) are present. Nevertheless, they show clear adaptations to their large body mass, such as more distal insertions for the protractor and adductor muscles of the limbs, giving them longer lever arms. The quantitative architecture of rhino muscles is again reminiscent of that of horses and tapirs, although contrary to horses, the forelimb is much stronger than the hindlimb, which is likely due to its great role in body mass support. Muscles involved mainly in counteracting gravity (e.g. serratus ventralis thoracis, infraspinatus, gastrocnemius, flexores digitorum) are usually highly pennate with short fascicles facilitating strong joint extension. Muscles involved in propulsion (e.g. gluteal muscles, gluteobiceps, quadriceps femoris) seem to represent a compromise between a high maximal isometric force and long fascicles, allowing a reasonably fast and wide working range. Neonates present higher normalized maximal isometric force than the adults for almost every muscle, except sometimes for the extensor and propulsor muscles, which presumably acquire their great force-generating capacity during the growth of the animal. Our study clarifies the way the muscles of animals of cursorial ancestry can adapt to support a greater body mass and calls for further investigations in other clades of large body mass.