Limb myology and muscle architecture of the Indian rhinocerosRhinoceros unicornisand the white rhinocerosCeratotherium simum(Mammalia: Rhinocerotidae)

Abstract

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.

Sesamoid bones also show functional adaptation in their microanatomy—The example of the patella in Perissodactyla

“…The maximal cortical thickness is observed anteriorly at about mid‐length, at the insertion of the intermediate patellar ligament (Figures 6, 9a), which is very strong in ungulates (Abumandour et al, 2020; Barone, 2010; Budras et al, 2003). Ligament and muscle insertions on the patella are rather similar between horses and rhinos and thus supposedly across all perissodactyls (Barone, 2010; Etienne et al, 2021). The intermediate patellar ligament is surrounded by the lateral and medial patellar ligaments, which also insert on the anterior side (Figure 9a), but no clear specific thickening associated with the insertion of these two ligaments is observed in the sampled taxa.…”

Adaptation to graviportality in Rhinocerotoidea? An investigation through the long bone shape variation in their hindlimb

“…These areas constitute the insertion sites of powerful flexor muscles, respectively the m. tibialis cranialis, a foot flexor, and the mm. biceps femoris, popliteus, semitendinosus and sartorius, all being flexors of the leg (Etienne et al, 2021). Reinforcement of insertions for flexors and extensors are congruent with the higher forces needed to move a heavier body.…”

“…S1) follow classic veterinary terminology and anatomical works on Perissodactyla or only on rhinoceroses (Guérin, 1980;Federative Committee on Anatomical Terminology, 1998;Antoine, 2002;Prothero, 2005;Barone, 2010a;Heissig, 2012;Bai et al, 2017). Locations of muscle insertions follows Etienne, Houssaye, & Hutchinson, 2021.…”

“…Such changes are notably observed in Rhinocerotina for the insertion of the m. vastus lateralis (between the greater trochanter convexity and the third trochanter) and on both medial and lateral supracondylar tuberosities, where insert the m. gastrocnemius and digit flexors. These powerful muscles are respectively the main extensors of the zeugopodium and autopodium (Etienne et al, 2021). Differences in bone shape associated with muscle attachments as organisms increase in mass or brachypody are coherent with more powerful muscles ensuring the propulsion and support of a higher absolute weight or of a body with a lower centre of gravity.…”

The evolutionary biomechanics of locomotor function in giant land animals

“…2 ), rhinoceroses have much more compact, robust proximal limb bones (femur and humerus). Bakker (1971) , Christiansen and Paul (2001) and Paul and Christiansen (2000) added that it is the ‘flexed’ limb posture of rhinos that confers their speed, as compared with the ‘columnar’ posture of elephants (following the morphological logic of Osborn, 1900 ; for a new morphometric perspective, see Mallet et al, 2019 , 2020 ; also Etienne et al, 2021 ). There is little question that the limb posture of rhinos and elephants at top (or any) speed is different, but there is much left to be understood about the locomotion of rhinos.…”