The scaling of postcranial muscles in cats (Felidae) II: hindlimb and lumbosacral muscles

In quadrupeds the musculature of the hindlimbs is expected to be responsible for generating most of the propulsive locomotory forces, as well as contributing to body support by generating vertical forces. In supporting the body, postural changes from crouched to upright limbs are often associated with an increase of body mass in terrestrial tetrapods. However, felids do not change their crouched limb posture despite undergoing a 300‐fold size increase between the smallest and largest extant species. Here, we test how changes in the muscle architecture (masses and lengths of components of the muscle‐tendon units) of the hindlimbs and lumbosacral region are related to body mass, to assess whether there are muscular compensations for the maintenance of a crouched limb posture at larger body sizes. We use regression and principal component analyses to detect allometries in muscle architecture, with and without phylogenetic correction. Of the muscle lengths that scale allometrically, all scale with negative allometry (i.e. relative shortening with increasing body mass), whereas all tendon lengths scale isometrically. Only two muscles' belly masses and two tendons' masses scale with positive allometry (i.e. relatively more massive with increasing body mass). Of the muscles that scale allometrically for physiological cross‐sectional area, all scale positively (i.e. relatively greater area with increasing body mass). These muscles are mostly linked to control of hip and thigh movements. When the architecture data are phylogenetically corrected, there are few significant results, and only the strongest signals remain. None of the vertebral muscles scaled significantly differently from isometry. Principal component analysis and manova s showed that neither body size nor locomotor mode separate the felid species in morphospace. Our results support the inference that, despite some positively allometric trends in muscle areas related to thigh movement, larger cats have relatively weaker hindlimb and lumbosacral muscles in general. This decrease in power may be reflected in relative decreases in running speeds and is consistent with prevailing evidence that behavioural changes may be the primary mode of compensation for a consistently crouched limb posture in larger cats.     

Effective Mechanical Advantage Allometry of Felid Elbow and Knee Extensors

Larger terrestrial mammals have generally been found to use more extended limb postures, a mechanism which maintains muscular requirements at larger sizes by improving the effective mechanical advantage (EMA) of limb musculature. Felids, however, have been documented to maintain joint angles across body sizes. If felid morphology scales isometrically, it would mean larger felids have relatively weaker muscles, compromising locomotor activities. Here, we examine the allometric relationships between the EMA of the elbow and knee extensors and body mass, finding that the EMA of the triceps brachii and quadriceps muscles scale with positive allometry. When species-specific joint angles were used rather than felid-average joint angles, EMA scales to body mass with more positive allometry. When the scaling of the muscle and ground reaction force (GRF) lever arms were investigated individually the allometric signal was lost; however, the muscle lever arms generally have allometric slope coefficients that are consistent with positive allometry, while the GRF lever arms demonstrate negative allometric slope coefficients. This suggests there are subtle alterations to limb morphology allowing different felid species to achieve an increased EMA via distinctive mechanisms. The quadriceps EMA was found to scale with sufficient positive allometry to compensate for increases in size without alteration in muscular anatomy; however, this is not the case for the triceps brachii EMA. Anat Rec, 2018. © 2018 Wiley Periodicals, Inc. Anat Rec, 302:775–784, 2019. © 2018 Wiley Periodicals, Inc.     

Body composition and the evolution of the Macropodidae (Potorous, Dendrolagus, and Macropus)

Summary The segmental distribution of body weight and the proportions of skin, muscle, and bone are compared for three genera of the Macropodidae (Potorous, Dendrolagus, and Macropus) and one genus of the Petauridae (Pseudocheirus). Potorous and Macropus possess high proportions of muscle mass to total body weight, high concentrations of musculature in the lumbar extensors, thigh, and tail, and disproportionate ratios of forelimb: hindlimb bone and forelimb: hindlimb muscle which correspond to disproportions of intermembral length. These species converge with high-speed terrestrial runners in some traits and remain distinctive in others. Macropus, larger, more muscular, and faster than Potorous, appears to store and return energy to the hopping cycle more efficiently. Dendrolagus has less than three-fourths the musculature of the other macropod genera, low proportions of the back extensor muscles compared to the other macropods, and relatively more equal ratios of forelimb: hindlimb bone and forelimb: hindlimb muscle. This species converges with slow-moving arboreal climbers such as Pseudocheirus. These data on body mass and tissue proportions translate directly into center of gravity, strength-to-weight ratio, and muscular (kinetic) chains, key elements of macropod evolution. The geometric similarity of muscle between smaller potoroids and larger macropodids, an assumption critical to allometric comparison, is not confirmed.     

Bite Force Estimation and the Fiber Architecture of Felid Masticatory Muscles

Increasingly, analyses of craniodental dietary adaptations take into account mechanical properties of foods. However, masticatory muscle fiber architecture has been described for relatively few lineages, even though an understanding of the scaling of this anatomy can yield important information about adaptations for stretch and strength in the masticatory system. Data on the mandibular adductors of 28 specimens from nine species of felids representing nearly the entire body size range of the family allow us to evaluate the influence of body size and diet on the masticatory apparatus within this lineage. Masticatory muscle masses scale isometrically, tending toward positive allometry, with body mass and jaw length. This allometry becomes significant when the independent variable is a geometric mean of cranial variables. For all three body size proxies, the physiological cross‐sectional area and predicted bite forces scale with significant positive allometry. Average fiber lengths (FL) tend toward negative allometry though with wide confidence intervals resulting from substantial scatter. We believe that these FL residuals are affected by dietary signals within the sample; though the mechanical properties of felid diets are relatively similar across species, the most durophagous species in our sample (the jaguar) appears to have relatively higher force production capabilities. The more notable dietary trend in our sample is the relationship between FL and relative prey size: felid species that predominantly consume relatively small prey have short masticatory muscle fibers, and species that regularly consume relatively large prey have relatively long fibers. This suggests an adaptive signal related to gape. Anat Rec, 2012. © 2012 Wiley Periodicals, Inc.     

Anatomical,architectural, and biochemical diversity of the murine forelimb muscles

We characterized the architecture, fiber type, titin isoform distribution, and collagen content of 27 portions of 22 muscles in the murine forelimb. The mouse forelimb was different from the human arm in that it had the extensor digitorum lateralis muscle and no brachioradialis muscle. Architecturally, the mouse forelimb differed from humans with regard to load bearing, having a much larger contribution from extensors than flexors. In mice, the extensor : flexor PCSA ratio is 2.7, whereas in humans it is only 1.4. When the architectural difference index was calculated, similarities became especially apparent between flexors and extensors of the distal forelimb, as well as pronators. Discriminant analysis revealed that biochemical measures of collagen, titin, and myosin heavy chain were all strong between‐species discriminators. In terms of composition, when compared with similar muscles in humans, mice had, on average, faster muscles with higher collagen content and larger titin isoforms. This report establishes the anatomical and biochemical properties of mouse forelimb muscles. Given the prevalence of this species in biological studies, these data will be invaluable for studying the biological basis of mouse muscle structure and function.     

Dimensions of forelimb muscles in orangutans and chimpanzees

Eight forelimbs of three orangutans and four chimpanzees were dissected and the muscle mass, fascicle length and physiological cross-sectional area (PCSA) of all forelimb muscles were systematically recorded to explore possible interspecies variation in muscle dimensions. Muscle mass and PCSA were divided by the total mass and total PCSA of the entire forelimb muscles for normalization. The results indicate that the mass and PCSA ratios of the monoarticular elbow flexors ( M. brachialis and M. brachioradialis ) are significantly larger in orangutans. In contrast, the mass ratios of the biarticular muscles in the upper arm (the short head of M. biceps brachii and the long head of M. triceps brachii ) are significantly larger in chimpanzees. For the rotator cuff muscles, the force-generating capacity of M. subscapularis is significantly larger in orangutans, whereas the opposite rotator cuff muscle, M. infraspinatus , is larger in chimpanzees. These differences in forelimb muscle dimensions of the two species may reflect functional specialization for their different positional and locomotor behaviors.     

Scaling and Accommodation of Jaw Adductor Muscles in Canidae

The masticatory apparatus amongst closely related carnivoran species raises intriguing questions about the interplay between allometry, function, and phylogeny in defining interspecific variations of cranial morphology. Here we describe the gross structure of the jaw adductor muscles of several species of canid, and then examine how the muscles are scaled across the range of body sizes, phylogenies, and trophic groups. We also consider how the muscles are accommodated on the skull, and how this is influenced by differences of endocranial size. Data were collected for a suite of morphological metrics, including body mass, endocranial volume, and muscle masses and we used geometric morphometric shape analysis to reveal associated form changes. We find that all jaw adductor muscles scale isometrically against body mass, regardless of phylogeny or trophic group, but that endocranial volume scales with negative allometry against body mass. These findings suggest that head shape is partly influenced by the need to house isometrically scaling muscles on a neurocranium scaling with negative allometry. Principal component analysis suggests that skull shape changes, such as the relatively wide zygomatic arches and large sagittal crests seen in species with higher body masses, allow the skull to accommodate a relative enlargement of the jaw adductors compared with the endocranium. Anat Rec, 299:951–966, 2016. © 2016 The Authors The Anatomical Record: Advances in Integrative Anatomy and Evolutionary Biology Published by Wiley Periodicals, Inc.     

Functional specialization and ontogenetic scaling of limb anatomy in Alligator mississippiensis

Crocodylians exhibit a fascinating diversity of terrestrial gaits and limb motions that remain poorly described and are of great importance to understanding their natural history and evolution. Their musculoskeletal anatomy is pivotal to this diversity and yet only qualitative studies of muscle‐tendon unit anatomy exist. The relative masses and internal architecture (fascicle lengths and physiological cross‐sectional areas) of muscles of the pectoral and pelvic limbs of American alligators (Alligator mississippiensis Daudin 1801) were recorded for an ontogenetic series of wild specimens (n = 15, body masses from 0.5 to 60 kg). The data were analysed by reduced major axis regression to determine scaling relationships with body mass. Physiological cross‐sectional areas and therefore muscle force‐generating capacity were found to be greater in the extensor (anti‐gravity) muscles of the pelvic limb than in the pectoral limb, reflecting how crocodylians differ from mammals in having greater loading of the hindlimbs than the forelimbs. Muscle masses and architecture were generally found to scale isometrically with body mass, suggesting an ontogenetic decrease in terrestrial athleticism. This concurs with the findings of previous studies showing ontogenetic decreases in limb bone length and the general scaling principle of a decline of strength : weight ratios with increasing size in animals. Exceptions to isometric scaling found included positive allometry in fascicle length for extensor musculature of both limbs, suggesting an ontogenetic increase in working range interpreted as increasing postural variability – in particular the major hip extensors – the interpretation of which is complicated by previous described ontogenetic increase of moment arms for these muscles.     

First Evidence of Pathology in the Forelimb of the Late Miocene Saber‐Toothed Felid Promegantereon ogygia (Machairodontinae,Smilodontini)

We examined the first evidence of pathology in the forelimb of the primitive saber‐toothed felid Promegantereon ogygia, observed in a radius from the late Miocene (Vallesian, MN 10) site of La Roma 2 (Teruel, Spain). This fossil is the first evidence of a member of the Machairodontinae in this locality, and the first fossil of this species found in the Miocene basin of Teruel. The radius shows an exostosis shaped as a rough and wide bony crest probably caused by the lesion and posterior ossification of part of the tendon of the muscle abductor pollicis longus, an important extensor and abductor of the thumb. The lesion was probably due to a tearing or to high levels of exertion experienced by this muscle over a relatively long time, a general type of lesion also observed in other vertebrate fossils. With saber‐toothed felids using their thumbs to immobilize prey during the hunt, the studied lesion probably affected in a significant manner the predatory abilities of the animal, causing at least a decrease in its hunting success rate. Anat Rec, 297:1090–1095, 2014. © 2014 Wiley Periodicals, Inc.     

Scaling and mechanics of the felid calcaneus: geometric similarity without differential allometric scaling

Six mechanically significant skeletal variables were measured on the calcanei from 60 Felidae specimens (22 species) to determine whether these variables were scaled to body mass, and to assess whether differential scaling exists. The power equation (y = a · x(b) ) was used to analyse the scaling of the six variables to body mass; we compared traditional regression methods (standardised major axis) to phylogenetically independent contrasts. In agreement with previous studies that compared these methodologies, we found no significant differences between methods in the allometric coefficients (b) obtained. Overall, the scaling pattern of the felid calcaneus conformed to the predictions of the geometric similarity hypothesis, but not entirely to those of the elastic similarity hypothesis. We found that the moment arm of the ankle extensors scaled to body mass with an exponent not significantly different from 0.40. This indicated that the tuber calcanei scaled to body mass faster than calcaneus total length. This explained why the effective mechanical advantage of the ankle extensors increased with body mass, despite the fact that limb posture does not change in felid species. Furthermore, this finding was consistent with the hypothesis of the isometric scaling of ground reaction forces. No evidence for differential scaling was found in any of the variables studied. We propose that this reflected the similar locomotor pattern of all felid species. Thus, our results suggested that the differences in allometric coefficients for 'large' and 'small' mammals were in fact caused by different types of locomotion among the species included in each category.     

Comparative and Quantitative Myology of the Forearm and Hand of Prosimian Primates

Associations between the relative development of muscles of the forearm and hand of prosimian primates and locomotor behavior, body size, and grasping specializations have been made on the basis of qualitative observations. These associations are here tested through comparative and quantitative analyses of muscle mass data for a broad sample of prosimian species (i.e., strepsirrhines and tarsiers). The musculature of the forearm and hand of 17 fresh‐frozen specimens representing six families and 12 species was dissected and weighed. Muscle weights were scaled relative to body mass of individual specimens using regression and compared by limb compartment and functional group. Forearm and digital flexor muscle masses are highly correlated with body mass (r = 0.97 and r = 0.96, respectively) and scale isometrically. As a general trend within the prosimian sample, the relative mass of the flexor compartment increases with body size. Interspecific comparisons of functional groups of muscles did not identify any association between larger muscle mass and locomotor adaptations or grasping specializations of the hand. However, compared to other prosimians, the adductor pollicis muscle of Nycticebus is more developed (52% of the intrinsic hand musculature sampled) and the flexor digitorum profundus muscle has two well‐separated heads with more individualized tendons, with the pollex and digit IV receiving tendinous contributions from both muscle heads. These differences that characterize the forearm and hand of Nycticebus correlate with the extreme thumb divergence and pincer‐like grips of lorises. Anat Rec, 2013. © 2013 Wiley Periodicals, Inc.     

The Head and Neck Muscles of the Serval and Tiger: Homologies,Evolution, and Proposal of a Mammalian and a Veterinary Muscle Ontology

Here we describe the head and neck muscles of members of the two extant felid subfamilies (Leptailurus serval: Felinae; Panthera tigris: Pantherinae) and compare these muscles with those of other felids, other carnivorans (e.g., domestic dogs), other eutherian mammals (e.g., rats, tree‐shrews and modern humans), and noneutherian mammals including monotremes. Another major goal of the article is to discuss and help clarify nomenclatural discrepancies found in the Nomina Anatomica Veterinaria and in veterinary atlases and textbooks that use cats and dogs as models to understand the anatomy of domestic mammals and to stress differences with modern humans. We propose a unifying nomenclature that is expanded to all the head and neck muscles and to all mammalian taxa in order to help build veterinary and mammalian muscle ontologies. Our observations and comparisons and the specific use of this nomenclature point out that felids such as tigers and servals and other carnivorans such as dogs have more facial muscle structures related to the mobility of both the auricular and orbital regions than numerous other mammals, including modern humans, which might be the result of an ancient adaptation related to the remarkable predatory capacities of carnivorans. Interestingly, the skeletal differences, mainly concerning the hyoid apparatus, pharynx, and larynx, that are likely associated with the different types of vocalizations seen in the Felinae (mainly purring) and Pantherinae (mainly roaring) are not accompanied by clear differences in the musculature connected to these structures in the feline L. serval and the pantherine P. tigris. Anat Rec, 2012. © 2012 Wiley Periodicals, Inc.     

Distribution Pattern of Muscle Fiber Types in the Perivertebral Musculature of Two Different Sized Species of Mice

Many physiological parameters scale with body size. Regarding limb muscles, it has been shown that the demands for relatively faster muscles, less postural work, and greater heat production in small mammals are met by lower proportions of Type I and conversely higher proportions of Type II fibers. To investigate possible adaptations of the perivertebral musculature, we investigated the proportion, spatial distribution, and cross‐sectional area (csa) of the different muscle fiber types in the laboratory and harvest mouse. Serial cross sections from the posterior thoracic to the lumbo‐sacral region were prepared and Type I, IIA, and IIB fibers identified using enzymehistochemistry. The general distribution of Type I and IIB fibers, as well as the more or less equal distribution of IIA fibers, resembles the pattern found in other mammals. However, the overall proportion of Type I fibers was very low in the laboratory mouse and particularly low in the harvest mouse. Muscular adaptations to a small body size were met primarily by increased Type IIA fiber proportions. Thereby, not all muscles or muscle regions similarly reflected the expected scaling effects. However, our results clearly show that body size is a critical factor when fiber‐type proportions are compared among different sized mammals. Anat Rec, 293:446–463, 2010. © 2010 Wiley‐Liss, Inc.     

The locomotor system of the ocean sunfish Mola mola (L.): role of gelatinous exoskeleton,horizontal septum,muscles and tendons

Adult ocean sunfish are the heaviest living teleosts. They have no axial musculature or caudal fin. Propulsion is by unpaired dorsal and anal fins; a pseudocaudal fin (‘clavus’) acts as a rudder. Despite common perception, young sunfish are active predators that swim quickly, beating their vertical fins in unison to generate lift‐based propulsion and attain cruising speeds similar to salmon and marlin. Here we show that the thick subcutaneous layer (or ‘capsule’), already known to provide positive buoyancy, is also crucial to locomotion. It provides two compartments, one for dorsal fin musculature and one for anal fin muscles, separated by a thick, fibrous, elastic horizontal septum that is bound to the capsule itself, the roof of the skull and the dorsal surface of the short vertebral column. The compartments are braced sagittally by bony haemal and neural spines. Both fins are powered by white muscles distributed laterally and red muscles located medially. The anal fin muscles are mostly aligned dorso‐ventrally and have origins on the septum and haemal spines. Dorsal fin muscles vary in orientation; many have origins on the capsule above the skull and run near‐horizontally and some bipennate muscles have origins on both capsule and septum. Such bipennate muscle arrangements have not been described previously in fishes. Fin muscles have hinged tendons that pass through capsular channels and radial cartilages to insertions on fin rays. The capsule is gelatinous (89.8% water) with a collagen and elastin meshwork. Greasy in texture, calculations indicate capsular buoyancy is partly provided by lipid. Capsule, septum and tendons provide elastic structures likely to enhance muscle action and support fast cruising.     

Descriptive and functional morphology of the neck and forelimb of the striped hyena (Hyaena hyaena, L. 1758)

The musculature of the neck and the forelimb of Hyaena hyaena is described and the biomechanical implications of some morphological aspects of muscles and skeleton are discussed. The extensors of the head and neck, the protractors and retractors of the forelimb and the extensors of the shoulder, elbow and carpal joints are relatively stronger developed than those in Canidae and Felidae. Moreover these muscles have larger moments about the joints. This is considered as an adaptation to lifting and carrying large and heavy prey or carrion.     

Fitting unanchored puzzle pieces in the skeleton: appropriate 3D scapular positions for the quadrupedal support in tetrapods

Deducing the scapular positions of extinct tetrapod skeletons remains difficult, because the scapulae and rib cage are connected with each other not directly by skeletal joint, but by thoracic muscles. In extant non‐testudine quadrupedal tetrapods, the top positions of the scapulae/suprascapulae occur at the anterior portion of the rib cage, above the vertebral column and near the median plane. The adequacy of this position was tested using three‐dimensional mechanical models of Felis, Rattus and Chamaeleo that assumed stances on a forelimb on a single side and the hindlimbs. The net moment about the acetabulum generated by the gravity force and the contractive forces of the anti‐gravity thoracic muscles, and the resistance of the rib to vertical compression between the downward gravity and upward lifting force from the anti‐gravity thoracic muscle depend on the scapular position. The scapular position common among quadrupeds corresponds to the place at which the roll and yaw moments of the uplifted portion of the body are negligible, where the pitch moment is large enough to lift the body, and above the ribs having high strength against vertical compression. These relationships between scapular position and rib cage morphology should allow reliable reconstruction of limb postures of extinct taxa.     

Complete forelimb myology of the basal theropod dinosaur Tawa hallae based on a novel robust muscle reconstruction method

The forelimbs of nonavian theropod dinosaurs have been the subject of considerable study and speculation due to their varied morphology and role in the evolution of flight. Although many studies on the functional morphology of a limb require an understanding of its musculature, comparatively little is known about the forelimb myology of theropods and other bipedal dinosaurs. Previous phylogenetically based myological reconstructions have been limited to the shoulder, restricting their utility in analyses of whole‐limb function. The antebrachial and manual musculature in particular have remained largely unstudied due to uncertain muscular homologies in archosaurs. Through analysis of the musculature of extant taxa in a robust statistical framework, this study presents new hypotheses of homology for the distal limb musculature of archosaurs and provides the first complete reconstruction of dinosaurian forelimb musculature, including the antebrachial and intrinsic manual muscles. Data on the forelimb myology of a broad sample of extant birds, crocodylians, lizards, and turtles were analyzed using maximum likelihood ancestral state reconstruction and examined together with the osteology of the early theropod Tawa hallae from the Late Triassic of New Mexico to formulate a complete plesiomorphic myology for the theropod forelimb. Comparisons with previous reconstructions show that the shoulder musculature of basal theropods is more similar to that of basal ornithischians and sauropodomorphs than to that of dromaeosaurids. Greater development of the supracoracoideus and deltoideus musculature in theropods over other bipedal dinosaurs correlates with stronger movements of the forelimb at the shoulder and an emphasis on apprehension of relatively large prey. This emphasis is further supported by the morphology of the antebrachium and the intrinsic manual musculature, which exhibit a high degree of excursion and a robust morphology well‐suited for powerful digital flexion. The forelimb myology of Tawa established here helps infer the ancestral conformation of the forelimb musculature and the osteological correlates of major muscle groups in early theropods. These data are critical for investigations addressing questions relating to the evolution of specialized forelimb function across Theropoda.