Three‐dimensional skeletal kinematics of the shoulder girdle and forelimb in walking Alligator

Crocodylians occupy a key phylogenetic position for investigations of archosaur locomotor evolution. Compared to the well‐studied hindlimb, relatively little is known about the skeletal movements and mechanics of the forelimb. In this study, we employed manual markerless XROMM (X‐ray Reconstruction Of Moving Morphology) to measure detailed 3‐D kinematics of the shoulder girdle and forelimb bones of American alligators (Alligator mississippiensis) walking on a treadmill. Digital models of the interclavicle, scapulocoracoid, humerus, radius and ulna were created using a 3‐D laser scanner. Models were articulated and aligned to simultaneously recorded frames of fluoroscopic and standard light video to reconstruct and measure joint motion. Joint coordinate systems were established for the coracosternal, glenohumeral and elbow joints. Our analysis revealed that the limb joints only account for about half of fore/aft limb excursion; the remaining excursion results from shoulder girdle movements and lateral bending of the vertebral column. Considerable motion of each scapulocoracoid relative to the vertebral column is consistent with coracosternal mobility. The hemisellar design of the glenohumeral joint permits some additional translation, or sliding in the fore‐aft plane, but this movement does not have much of an effect on the distal excursion of the bone.     

Morphological Analysis of the Flippers in the Franciscana Dolphin,Pontoporia blainvillei,Applying X‐Ray Technique

Pectoral flippers of cetaceans function to provide stability and maneuverability during locomotion. Directional asymmetry (DA) is a common feature among odontocete cetaceans, as well as sexual dimorphism (SD). For the first time DA, allometry, physical maturity, and SD of the flipper skeleton—by X‐ray technique—of Pontoporia blainvillei were analyzed. The number of carpals, metacarpals, phalanges, and morphometric characters from the humerus, radius, ulna, and digit two were studied in franciscana dolphins from Buenos Aires, Argentina. The number of visible epiphyses and their degree of fusion at the proximal and distal ends of the humerus, radius, and ulna were also analyzed. The flipper skeleton was symmetrical, showing a negative allometric trend, with similar growth patterns in both sexes with the exception of the width of the radius (P ≤ 0.01). SD was found on the number of phalanges of digit two (P ≤ 0.01), ulna and digit two lengths. Females showed a higher relative ulna length and shorter relative digit two length, and the opposite occurred in males (P ≤ 0.01). Epiphyseal fusion pattern proved to be a tool to determine dolphin's age; franciscana dolphins with a mature flipper were, at least, four years old. This study indicates that the flippers of franciscana dolphins are symmetrical; both sexes show a negative allometric trend; SD is observed in radius, ulna, and digit two; and flipper skeleton allows determine the age class of the dolphins. Anat Rec, 297:1181–1188, 2014. © 2014 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.     

Linear and Geometric Morphometric Analysis of Long Bone Scaling Patterns in Jurassic Neosauropod Dinosaurs: Their Functional and Paleobiological Implications

Neosauropod dinosaurs were gigantic, herbivorous dinosaurs. Given that the limb skeleton is essentially a plastic, mobile framework that supports and moves the body, analysis of long bone scaling can reveal limb adaptations that supported neosauropod gigantism. Previously, analyses of linear dimensions have revealed a relatively isometric scaling pattern for the humerus and femur of neosauropods. Here, a combined scaling analysis of humerus and femur linear dimensions, cortical area, and shape across six neosauropod taxa is used to test the hypothesis that neosauropod long bones scaled isometrically and to investigate the paleobiological implications of these trends. A combination of linear regression and geometric morphometrics analyses of neosauropod humeri and femora were performed using traditional and thin‐plate splines approaches. The neosauropod sample was very homogeneous, and linear analyses revealed that nearly all humerus and femur dimensions, including cortical area, scale with isometry against maximum length. Thin‐plate splines analyses showed that little to no significant shape change occurs with increasing length or cortical area for the humerus or femur. Even with the exclusion of the long‐limbed Brachiosaurus, the overall trends were consistently isometric. These results suggest that the mechanical advantage of limb‐moving muscles and the relative range of limb movement decreased with increasing size. The isometric signal for neosauropod long bone dimensions and shape suggests these dinosaurs may have reached the upper limit of vertebrate long bone mechanics. Perhaps, like stilt‐walkers, the absolutely long limbs of the largest neosauropods allowed for efficient locomotion at gigantic size with few ontogenetic changes. Anat Rec, 290:1089–1111, 2007. © 2007 Wiley‐Liss, Inc.     

Scaling of axial muscle architecture in juvenile Alligator mississippiensis reveals an enhanced performance capacity of accessory breathing mechanisms

Quantitative functional anatomy of amniote thoracic and abdominal regions is crucial to understanding constraints on and adaptations for facilitating simultaneous breathing and locomotion. Crocodilians have diverse locomotor modes and variable breathing mechanics facilitated by basal and derived (accessory) muscles. However, the inherent flexibility of these systems is not well studied, and the functional specialisation of the crocodilian trunk is yet to be investigated. Increases in body size and trunk stiffness would be expected to cause a disproportionate increase in muscle force demands and therefore constrain the basal costal aspiration mechanism, necessitating changes in respiratory mechanics. Here, we describe the anatomy of the trunk muscles, their properties that determine muscle performance (mass, length and physiological cross-sectional area [PCSA]) and investigate their scaling in juvenile Alligator mississippiensis spanning an order of magnitude in body mass (359 g–5.5 kg). Comparatively, the expiratory muscles (transversus abdominis, rectus abdominis, iliocostalis), which compress the trunk, have greater relative PCSA being specialised for greater force-generating capacity, while the inspiratory muscles (diaphragmaticus, truncocaudalis ischiotruncus, ischiopubis), which create negative internal pressure, have greater relative fascicle lengths, being adapted for greater working range and contraction velocity. Fascicle lengths of the accessory diaphragmaticus scaled with positive allometry in the alligators examined, enhancing contractile capacity, in line with this muscle's ability to modulate both tidal volume and breathing frequency in response to energetic demand during terrestrial locomotion. The iliocostalis, an accessory expiratory muscle, also demonstrated positive allometry in fascicle lengths and mass. All accessory muscles of the infrapubic abdominal wall demonstrated positive allometry in PCSA, which would enhance their force-generating capacity. Conversely, the basal tetrapod expiratory pump (transversus abdominis) scaled isometrically, which may indicate a decreased reliance on this muscle with ontogeny. Collectively, these findings would support existing anecdotal evidence that crocodilians shift their breathing mechanics as they increase in size. Furthermore, the functional specialisation of the diaphragmaticus and compliance of the body wall in the lumbar region against which it works may contribute to low-cost breathing in crocodilians.     

Ontogenetic allometry of ossified fetal limb bones.

The skeletal components of fetal limbs change in both size and shape throughout gestation. Relative growth of different bones, as well as differences between homologous bones of the upper and lower limbs, are not well known for all stages of fetal development. This study used human fetal skeletal material (N = 57) ranging in age from 19 to 40 weeks gestation, and in body mass from 290g to 4650g. Measurements of maximal length and minimal width were taken from the six major long bones: femur, tibia, fibula, humerus, radius, and ulna. These data were log transformed, and growth rates determined from least squares regression of bone length or bone width on body mass and on crown-to-rump length. The results indicated that growth rates are equivalent among bones within a limb, whereas homologous bones in the upper and lower limb grew at different rates. In general, the upper limb bones display negative allometry and the lower limb bones display isometric growth in relation to body mass and crown-to-rump length. Further, there was no difference between growth rates of length and width relative to body mass. The negative slopes of upper-to-lower limb bones in relation to mass confirm the conclusion that lower limb bones grow faster than the upper limb bones from 19 weeks gestation to birth. These results, together with results from similar studies of other periods of fetal development, provide a unified picture of the prenatal growth in human skeletal limbs.     

Limb bone allometry during postnatal ontogeny in non-avian dinosaurs

Although the interspecific scaling of tetrapods is well understood, remarkably little work has been done on the ontogenetic scaling within tetrapod species, whether fossil or recent. Here the ontogenetic allometry of the femur, humerus, and tibia was determined for 23 species of non‐avian dinosaur by regressing log‐transformed length against log‐transformed circumference for each bone using reduced major axis bivariate regression. The femora of large theropod species became more robust during ontogeny, whereas growth in the femora of sauropodomorphs and most ornithischians was not significantly different from isometry. Hadrosaur hindlimb elements became significantly more gracile during ontogeny. Scaling constants were higher in all theropods than in any non‐theropod taxa. Such clear taxonomically correlated divisions were not evident in the ontogenetic allometry of the tibia and hindlimb bones did not scale uniformly within larger taxonomic groups. For taxa in which the ontogenetic allometry of the humerus was studied, only Riojasaurus incertus exhibited a significant departure from isometry. Using independent contrasts, the regression of femoral allometry against the log of adult body mass was found to have a significant negative correlation but such a relationship could not be established for other limb elements or growth parameters, mainly due to the small sample size. The intraspecific scaling patterns observed in dinosaurs and other amniotes do not support earlier hypotheses that intraspecific scaling differs between endothermic and ectothermic taxa.     

Forelimb to Hindlimb Shape Covariance in Extant Hominoids and Fossil Hominins

Researchers often attempt to use limb proportions to ascertain the locomotor repertoires of fossil hominins. This can be problematic as there are few skeletons in the fossil record that preserve both a full forelimb and hindlimb; therefore, estimates of full limb lengths are typically associated with substantial error. In this study, two‐block partial least squares analyses were used to examine covariation between forelimb and hindlimb elements in extant hominoids and fossil hominins. This has the benefit of including both forelimb and hindlimb in a type of functional analysis without necessitating an accurate length estimate. There is a high degree of covariation between forelimb and hindlimb segments in the mixed species sample, particularly in the proximal ulna, distal humerus, and proximal/distal femur and that shape covariation is significantly correlated with intermembral indices in the extant taxa. Overall, the fossil hominins most closely resembled modern humans with the exception of analyses utilizing the distal femur where some occupied a unique morphological position; thus, some fossil hominins likely possessed locomotor capabilities similar to modern humans, whereas others likely represent a unique morphological compromise between terrestrial bipedality and other positional behaviors not present among extant hominoids. Anat Rec, 2013. © 2012 Wiley Periodicals, Inc.     

Human mandibular prenatal growth: bivariate and multivariate growth allometry comparing different mandibular dimensions

Summary Mandibular growth was studied in 36 human fetuses (both sexes) ranging from 13 to 37 weeks of gestation by bivariate and multivariate analyses (bivariate allometry and principal components analysis, PCA). Several mandibular dimensions were measured and correlated with fetal weight. Considering the different mandibular dimensions in sequence of increasing component weights, PCA agreed with bivariate analysis. No mandibular dimension was considered to increase in isometric relationship. PCA showed the following distances with negative allometry: caput mandibulæ-gnathion (both sides), gonion-processus coronoideus (both sides), caput mandibulæ-processus coronoideus (both sides) and gonion-gnathion (right side). On the other hand, the following dimensions grew with positive allometry: goniongnathion (left side) and symphyseal height (both sides). PCA and bivariate analysis showed higher growth rates for the gonion-processus coronoideus distance and symphyseal height on the right side than on the left. All other mandibular dimensions presented more elevated growth rates on the left than on the right side. During the second and third trimesters of prenatal life the mandibular growth was allometrical; the mandibular body grew with more intensity than the ramus in both length and height. The greatest growth rate was found for the height at the symphysis. The angulus mandibulæ presented a negative and slight correlation with the other linear dimensions of the mandible during prenatal life.Abbreviations CM-Gn Caput mandibulæ-gnathion - Go-PC Gonion-processus coronoideus - Go-Gn Gonion-gnathion - CM-PC Caput mandibulæ-processus coronoideus - SH Symphyseal height - AM Angulus mandibulae     

3D geometric morphometric analysis of the proximal epiphysis of the hominoid humerus

In this study we perform a three‐dimensional geometric morphometric (3D GM) analysis of the proximal epiphysis of the humerus in extant great apes, including humans, in order to accurately describe the functional anatomical differences between these taxa. In addition, a fossil hominin specimen of Australopithecus afarensis was included in a multivariate GM analysis in order to test the potential of this methodological approach for making locomotor inferences from fossil remains. The results obtained show significant differences in proximal humeral morphology among the taxa studied, which had thus far largely remained unnoticed. Based on morphofunctional considerations, these anatomical differences can be correlated to differences in the locomotor repertoires of the taxa, thus confirming that the proximal humerus is suitable for constructing paleobiological inferences about locomotion. Modern humans display markedly divergent features, which set them apart from both the extant great apes and the fossil hominin A. afarensis. The morphology of the proximal epiphysis of the humerus of the latter more closely resembles that of the orangutans, thus suggesting that despite hindlimb adaptations to bipedalism, the forelimb of this taxon was still functionally involved in arboreal behaviors, such as climbing or suspension.     

Calcified cartilage shape in archosaur long bones reflects overlying joint shape in stress‐bearing elements: Implications for nonavian dinosaur locomotion

In nonavian dinosaur long bones, the once‐living chondroepiphysis (joint surface) overlay a now‐fossilized calcified cartilage zone. Although the shape of this zone is used to infer nonavian dinosaur locomotion, it remains unclear how much it reflects chondroepiphysis shape. We tested the hypothesis that calcified cartilage shape reflects the overlying chondroepiphysis in extant archosaurs. Long bones with intact epiphyses from American alligators (Alligator mississippiensis), helmeted guinea fowl (Numida meleagris), and juvenile ostriches (Struthio camelus) were measured and digitized for geometric morphometric (GM) analyses before and after chondroepiphysis removal. Removal of the chondroepiphysis resulted in significant element truncation in all examined taxa, but the amount of truncation decreased with increasing size. GM analyses revealed that Alligator show significant differences between chondroepiphysis shape and the calcified cartilage zone in the humerus, but display nonsignificant differences in femora of large individuals. In Numida, GM analysis shows significant shape differences in juvenile humeri, but humeri of adults and the femora of all guinea fowl show no significant shape difference. The juvenile Struthio sample showed significant differences in both long bones, which diminish with increasing size, a pattern confirmed with magnetic resonance imaging scans in an adult. Our data suggest that differences in extant archosaur long bone shape are greater in elements not utilized in locomotion and related stress‐inducing activities. Based on our data, we propose tentative ranges of error for nonavian dinosaur long bone dimensional measurements. We also predict that calcified cartilage shape in adult, stress‐bearing nonavian dinosaur long bones grossly reflects chondroepiphysis shape. Anat Rec, 2010. © 2010 Wiley‐Liss, Inc.     

Osteohistology and Life History of the Basal Pygostylian,Confuciusornis sanctus

More than a thousand specimens of Confuciusornis sanctus have been recovered from the Early Cretaceous Jehol Group of Northeastern China. Here, we investigate the bone microstructure of 33 long bones sampled from 14 C. sanctus specimens in an attempt to assess the life history patterns of this basal pygostylian bird. Analysis of the histology of various skeletal elements (femur, humerus, tibia, radius, and ulna) revealed differences in the histology of their bone walls. Based on the osteohistology, we coded the examined specimens into five histology age classes. We found that histological age was not strictly correlated with body size. The variability in the histology of multiple bones from single skeletons suggests differences in the growth rate of the skeleton in response to allometry, functional demands, and pathology. We show that although fibrolamellar bone is widespread across birds, the extent and duration of this rapid phase of bone deposition is highly variable. Comparisons among Mesozoic birds confirm that early ontogenetic growth was rapid, but that later post-hatching growth was strongly influenced by the ontogenetic age of the individual, body size, and local environment, as well as taxonomy. Our findings indicate that C. sanctus experienced rapid growth from early ontogeny until almost fully grown, and thereafter transitioned to slow, episodic growth (for at least 3–4 years) to reach skeletal maturity. Anat Rec, 303:949–962, 2020. © 2019 American Association for Anatomy     

Anatomy,histology and elemental profile of long bones and ribs of the Asian elephant (<Emphasis Type="Italic">Elephas maximus</Emphasis>)

This study evaluated the morphology and elemental composition of Asian elephant (Elephas maximus) bones (humerus, radius, ulna, femur, tibia, fibula and rib). Computerized tomography was used to image the intraosseous structure, compact bones were processed using histological techniques, and elemental profiling of compact bone was conducted using X-ray fluorescence. There was no clear evidence of an open marrow cavity in any of the bones; rather, dense trabecular bone was found in the bone interior. Compact bone contained double osteons in the radius, tibia and fibula. The osteon structure was comparatively large and similar in all bones, although the lacuna area was greater (P < 0.05) in the femur and ulna. Another finding was that nutrient foramina were clearly present in the humerus, ulna, femur, tibia and rib. Twenty elements were identified in elephant compact bone. Of these, ten differed significantly across the seven bones: Ca, Ti, V, Mn, Fe, Zr, Ag, Cd, Sn and Sb. Of particular interest was the finding of a significantly larger proportion of Fe in the humerus, radius, fibula and ribs, all bones without an open medullary cavity, which is traditionally associated with bone marrow for blood cell production. In conclusion, elephant bones present special characteristics, some of which may be important to hematopoiesis and bone strength for supporting a heavy body weight.     

Ontogeny of the Early Triassic Cynodont Thrinaxodon liorhinus (Therapsida): Cranial Morphology

The cranial morphology of 68 Thrinaxodon liorhinus specimens, ranging in size from 30 to 96 mm in basal skull length, is investigated using both qualitative and quantitative analyses. From this comprehensive survey, we determined that nine cranial features, including five in the temporal region, separated the sample into four ontogenetic stages. A bivariate analysis of 60 specimens indicated that the skull generally increased in size isometrically, with the exception of four regions. The orbit had negative allometry, a result consistent with other ontogenetic studies of tetrapods, whereas the length of the snout, palate, and temporal region showed positive allometry. The last trend had strong positive allometry indicating that during ontogeny the length of the sagittal crest increased at a much faster rate than the rest of the skull. The large number of changes in the temporal region of the skull of Thrinaxodon may indicate a greater development of the posterior fibres of the temporalis musculature from an early ontogenetic stage. For example, the posterior sagittal crest developed much earlier in ontogeny than the anterior crest that formed in adults, and bone was deposited dorsally creating a unified posterior sagittal crest rather than having a suture that spanned the entire depth of the skull roof. In combination with the isometric height of the zygomatic arch and the almost complete absence of the zygomatic arch angulation, these ontogenetic changes suggest that there was greater development of the temporalis relative to the masseter muscles, indicating a strong posterodorsal movement of the mandible in Thrinaxodon. Anat Rec, 298:1440–1464, 2015. © 2015 Wiley Periodicals, Inc.     

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.     

Morphological integration in the forelimb of musteloid carnivorans

The forelimb forms a functional unit that allows a variety of behaviours and needs to be mobile, yet at the same time stable. Both mobility and stability are controlled, amongst others, at the level of the elbow joint. This joint is composed of the humero‐ulnar articulation, mainly involved during parasagittal movements; and the radio‐ulnar articulation, mainly allowing rotation. In contrast, the humero‐radial articulation allows both movements of flexion–extension and rotation. Here, we study the morphological integration between each bone of the forelimb at the level of the entire arm, as well as at the elbow joint, in musteloid carnivorans. To do so, we quantitatively test shape co‐variation using surface 3D geometric morphometric data. Our results show that morphological integration is stronger for bones that form functional units. Different results are obtained depending on the level of investigation: for the entire arm, results show a greater degree of shape co‐variation between long bones of the lower arm than between the humerus and either bone of the lower arm. Thus, at this level the functional unit of the lower arm is comprised of the radius and ulna, permitting rotational movements of the lower arm. At the level of the elbow, results display a stronger shape co‐variation between bones allowing flexion and stability (humerus and ulna) than between bones allowing mobility (ulna and radius and humerus and radius). Thus, the critical functional unit appears to be the articulation between the humerus and ulna providing the stability of the joint.     

Hand development and sequence of ossification in the forelimb of the European shrew Crocidura russula (Soricidae) and comparisons across therian mammals

Hand development in the European shrew Crocidura russula is described, based on the examination of a cleared and double-stained ontogenetic series and histological sections of a c. 20-day-old embryo and a neonate. In the embryo all carpal elements are still mesenchymal condensations, and there are three more elements than in the adult stage: the 'lunatum', which fuses with the scaphoid around birth; a centrale, which either fuses with another carpal element or just disappears later in ontogeny; and the anlage of an element that later fuses with the radius. Carpal arrangement in the neonate and the adult is the same. In order to compare the relative timing of the onset of ossification in forelimb bones in C. russula with that of other therians, we built up two matrices of events based on two sets of data and used the event-pair method. In the first analysis, ossification of forelimb elements in general was examined, including that of the humerus, radius, ulna, the first carpal and metacarpal to ossify, and the phalanges of the third digit. The second analysis included each carpal, humerus, radius, ulna, the first metacarpal and the first phalanx to ossify. Some characters (= event-pairs) provide synapomorphies for some clades examined. There have been some shifts in the timing of ossification apparently not caused by ecological and/or environmental influences. In two species (Oryctolagus and Myotis), there is a tendency to start the ossification of the carpals relatively earlier than in all other species examined, the sauropsid outgroups included.