Growth of the pectoral girdle of the Leopard frog, Rana pipiens (Anura: Ranidae)

This article describes the growth of the anuran pectoral girdle of Rana pipiens and compares skeletal development of the shoulder to that of long bones. The pectoral girdle chondrifies as two halves, each adjacent to a developing humerus. In each, the scapula and coracoid form as single foci of condensed chondrocytes that fuse, creating a cartilaginous glenoid bridge articulating with the humerus. Based on histological sections, both the dermal clavicle and cleithrum begin to ossify at approximately the same time as the periosteum forms around the endochondral bones. The dermal and endochondral bones of the girdle form immobile joints with neighboring girdle elements; however, the cellular organization and growth pattern of the scapula and coracoid closely resemble those of a long bone. Similar to a long bone epiphysis, distal margins of both endochondral elements have zones of hyaline, stratified, and hypertrophic cartilages. As a result, fused elements of the girdle can grow without altering the glenoid articulation with the humerus. Comparisons of anuran long bone and pectoral girdle growth suggest that different bones can have similar histology and development regardless of adult morphology.     

MSCT-3D技术在动物与人骨骼形态比较研究中的应用

目的应用MSCT-3D显示技术比较正常贵州香猪、Marshall比格犬、恒河猴与人上肢带骨及躯干骨的形态学差异。方法采用MSCT分别对贵州香猪、比格犬和恒河猴进行CT全身扫描并进行图像重建,观察其上肢带骨、躯干骨形态结构与人的异同。结果比格犬、恒河猴、贵州香猪脊椎骨和肋的基本组成与人相同,脊椎骨由椎体和附件组成,肋骨包括真肋、假肋和浮肋。而脊柱曲度、各段椎骨数目、胸骨结构、肋的数目、胸肋连接、上肢带骨的组成与人不同,恒河猴的脊柱曲度和上肢带骨连接与人相同,有颈、胸、腰、骶四个生理性弯曲并由锁骨和肩胛骨共同连接自由上肢骨,比格犬和贵州香猪只有颈、胸腰、骶三个生理性弯曲,仅由肩胛骨连接自由上肢骨。结论恒河猴躯干骨和上肢带骨与人有良好的相似性,而比格犬和贵州香猪与人差别较大。MSCT-3D技术为实验动物形态学比较研究提供了一种相对无创、快速、可以在体研究并动态连续观察的科学有效方法。     

Musculoskeletal Model of the Upper Limb Based on the Visible Human Male Dataset

A mathematical model of Ihe human upper limb was developed based on high-resolution medical images of the muscles and bones obtained from the Visible Human Male ( HM) project. Three-dimensional surfaces of the muscles and bones were reconstructed from Computed Tomography (CT) images and Color Cryosection images obtained from the VHM cadaver. Thirteen degrees of freedom were used to describe the orientations of seven bones in the model: clavicle, scapula, humerus, radius, ulna, carpal bones, and hand. All of the major articulations from the shoulder girdle down to the wrist were included in the model. The model was actuated by 42 muscle bundles, which represented the actions of 26 muscle groups in the upper limb. The paths of the muscles were modeled using a new approach called the Obstacle-set Method (33) The calculated paths of the muscles were verified by comparing the muscle moment arms computed in the model with the results of anatomical studies reported in the literature, In-vivo measurements of maximum isometric muscle torques developed at the shoulder, elbow, and wrist were also used to estimate the architectural properties of each musculotendon actuator in the model. The entire musculoskeletal model can be reconstructed using the data given in this paper, along with information presented in a companion paper which defines the kinematic structure of the model (26)     

Musculoskeletal model of the upper limb based on the visible human male dataset

A mathematical model of the human upper limb was developed based on high-resolution medical images of the muscles and bones obtained from the Visible Human Male (VHM) project. Three-dimensional surfaces of the muscles and bones were reconstructed from Computed Tomography (CT) images and Color Cryosection images obtained from the VHM cadaver. Thirteen degrees of freedom were used to describe the orientations of seven bones in the model: clavicle, scapula, humerus, radius, ulna, carpal bones, and hand. All of the major articulations from the shoulder girdle down to the wrist were included in the model. The model was actuated by 42 muscle bundles, which represented the actions of 26 muscle groups in the upper limb. The paths of the muscles were modeled using a new approach called the Obstacle-set Method [33]. The calculated paths of the muscles were verified by comparing the muscle moment arms computed in the model with the results of anatomical studies reported in the literature. In-vivo measurements of maximum isometric muscle torques developed at the shoulder, elbow, and wrist were also used to estimate the architectural properties of each musculotendon actuator in the model. The entire musculoskeletal model can be reconstructed using the data given in this paper, along with information presented in a companion paper which defines the kinematic structure of the model [26].     

The role of the forelimb in prey capture in the Late Triassic reptile Megalancosaurus (Diapsida,Drepanosauromorpha)

The pectoral girdle and forelimb of the Late Triassic drepanosauromorph reptile Megalancosaurus are redescribed and their function reinterpreted. The whole skeleton of this diapsid is highly specialised for arboreal life, and also the peculiarities of the shoulder girdle and forelimb were interpreted as adaptations for a limb-based locomotion using gap-bridging to move from one support to another, as in chameleons. Re-examination of the pectoral girdle and forelimb revealed the presence of clavicles fused into a furcula-like structure, a saddle-shaped glenoid and a tight connection between the radius and ulna that strengthened the forearm but hindered pronation and supination movements at that joint. The new information plus a reconstruction of the pectoral and forelimb musculature suggests that the forelimb was also specialised for grasping and raking in addition to climbing and thus prey capture may have been an important function for the forelimb. The new functional interpretation fits well with the overall body architecture of Megalancosaurus’ skeleton, suggesting that this reptile was an ambush predator that may have assumed a stable tripodal position, secured by the hooked tail and hind limbs, freeing its forelimbs to catch prey by sudden extension of the arm and firm grasping with the pincer-like digits.     

Functional analysis of the shoulder girdle of cats during locomotion

The movements of the shoulder girdle of eight adult cats during overground stepping were studied, using standard slow motion cinematographic techniques. The patterns of activity of shoulder muscles were examined, using simultaneous intramuscular electromyography. Walking, trotting and galloping steps were analyzed from digitized single motion picture frame images. Angular movements of the shoulder girdle consist of biphasic flexion and extension of the shoulder joint and a monophasic flexion-extension alternation of the scapula on the thorax during each step cycle. In addition, the center of the scapula moves craniad during the swing phase and caudad during the stance phase with respect to a fixed reference point on the animal. Similar vertical movements of the center of the scapula also occur in each step cycle. Results of EMG studies of the 17 muscles capable of acting on the shoulder girdle indicate that three overall patterns of activity are found: (1) a pattern typical of extensor muscles, active during all the extension epochs; (2) a pattern typical of flexor muscles, active during the flexion epoch; and (3) a biphasic pattern of activity, active twice in each step. There data are used, along with a re-examination of previous models of the mechanics of the shoulder girdle of carnivores to examine the function and mechanics of shoulder motion. It is concluded that the rotary and translatory movements of the shoulder girdle during stepping combine to enhance step length.     

On the osteology and myology of catfish pectoral girdle, with a reflection on catfish (Teleostei: Siluriformes) plesiomorphies

The configuration of the pectoral girdle bones and muscles of numerous catfishes was studied in detail and compared with that of other siluriforms, as well as of other teleosts, described in the literature. The pectoral girdle of catfishes is composed of only three bones, which probably correspond to the posttemporo-supracleithrum (posttemporal + supracleithrum), scapulo-coracoid (scapula + coracoid), and cleithrum of other teleosts. These latter two bones constitute the place of origin of the pectoral girdle muscles. Two of these muscles are related to the movements of the pectoral fin. These two muscles correspond, very likely, to the abductor superficialis and to the adductor superficialis of other teleostean fishes. In relation to the pectoral spine (thickened first pectoral fin ray), it is usually moved by three well-developed muscles, which are probably homologous with the arrector ventralis, arrector dorsalis, and abductor profundus of nonsiluriform teleosts. The morphological diversity and the plesiomorphic configuration of these muscles, as well as of the other catfish pectoral girdle structures, are discussed.     

Scapular position in primates

Scapular position affects shoulder mobility, which plays an important role in the upper limb adaptations in primates. However, currently available data on scapular position are unsatisfactory because of the failure to simultaneously consider the relative dimensions of all the three skeletal elements of the shoulder girdle, i.e. the clavicle, the scapula and the thorax. In the present study, the clavicular length and the scapular spine length were measured on preserved cadavers, and the dorsoventral thoracic diameter was measured on scaled radiographs of a wide range of primates, permitting a quantitative comparison of scapular position among primates. It was found that arboreal monkeys have a more dorsally situated scapula than terrestrial ones, but the same difference was not found between terrestrial and arboreal prosimians. Hominoids were found to have the most dorsally situated scapula. Contrary to the slow climbing theory of hominoid evolution, which tries to explain most postcranial specializations of hominoids as adaptations for slow climbing, the scapulae of slow-climbing lorines and Alouatta are much less dorsal than those of the hominoids.     

A regression-based 3-D shoulder rhythm

In biomechanical modeling of the shoulder, it is important to know the orientation of each bone in the shoulder girdle when estimating the loads on each musculoskeletal element. However, because of the soft tissue overlying the bones, it is difficult to accurately derive the orientation of the clavicle and scapula using surface markers during dynamic movement. The purpose of this study is to develop two regression models which predict the orientation of the clavicle and the scapula. The first regression model uses humerus orientation and individual factors such as age, gender, and anthropometry data as the predictors. The second regression model includes only the humerus orientation as the predictor. Thirty-eight participants performed 118 static postures covering the volume of the right hand reach. The orientation of the thorax, clavicle, scapula and humerus were measured with a motion tracking system. Regression analysis was performed on the Euler angles decomposed from the orientation of each bone from 26 randomly selected participants. The regression models were then validated with the remaining 12 participants. The results indicate that for the first model, the r² of the predicted orientation of the clavicle and the scapula ranged between 0.31 and 0.65, and the RMSE obtained from the validation dataset ranged from 6.92° to 10.39°. For the second model, the r² ranged between 0.19 and 0.57, and the RMSE obtained from the validation dataset ranged from 6.62° and 11.13°. The derived regression-based shoulder rhythm could be useful in future biomechanical modeling of the shoulder.     

金丝猴肩带和前肢的性二型

本文研究了两种金丝猴(Rhinopitheous bieti和R.brelichi)肩带及上肢的62项线性变量及指数的性二型,其中64.5%达到了显著性差异水平。结果表明,两性在运动行为上存在一些差异。在所分析的变量中,性别间的差异主要由于成熟时间的不同所引起(雄性比雌性具更长的生长时期),其次是生长速率的不同(雄性比雌性具有更明显的正异速生长率)。对一些指数及不同部位的性二型分析表明,在上肢利用和尺、桡骨的前旋及后旋活动方面,两性也具一些不同。     

Three-dimensional kinematic analysis of the pectoral girdle during upside-down locomotion of two-toed sloths (Choloepus didactylus, Linné 1758)

Background

Theria (marsupials and placental mammals) are characterized by a highly mobile pectoral girdle in which the scapula has been shown to be an important propulsive element during locomotion. Shoulder function and kinematics are highly conservative during locomotion within quadrupedal therian mammals. In order to gain insight into the functional morphology and evolution of the pectoral girdle of the two-toed sloth we here analyze the anatomy and the three-dimensional (3D) pattern of shoulder kinematics during quadrupedal suspensory ('upside-down') locomotion.

Methods

We use scientific rotoscoping, a new, non-invasive, markerless approach for x-ray reconstruction of moving morphology (XROMM), to quantify in vivo the 3D movements of all constituent skeletal elements of the shoulder girdle. Additionally we use histologic staining to analyze the configuration of the sterno-clavicular articulation (SCA).

Results

Despite the inverse orientation of the body towards gravity, sloths display a 3D kinematic pattern and an orientation of the scapula relative to the thorax similar to pronograde claviculate mammalian species that differs from that of aclaviculate as well as brachiating mammals. Reduction of the relative length of the scapula alters its displacing effect on limb excursions. The configuration of the SCA maximizes mobility at this joint and demonstrates a tensile loading regime between thorax and limbs.

Conclusions

The morphological characteristics of the scapula and the SCA allow maximal mobility of the forelimb to facilitate effective locomotion within a discontinuous habitat. These evolutionary changes associated with the adoption of the suspensory posture emphasized humeral influence on forelimb motion, but allowed the retention of the plesiomorphic 3D kinematic pattern.     

The kinematics of the scapulae and spine during a lifting task

Simultaneous motion of the scapula and humerus is widely accepted as a feature of normal upper limb movement, however this has usually been investigated under conditions in which purposeful, functional tasks were not considered. The aim of this study was to investigate the synchrony and coordination of the constituent 3D movements of the shoulder girdle and trunk, during a functional activity. 45 healthy women, aged between 20 and 80 years, performed a simple lifting task, moving a loaded box from a shelf at waist level to one at shoulder level and then reversed the movement, during which the linear and angular motions of the scapulae, upper and lower thoracic spine and upper limbs were monitored and analysed using cross-correlation techniques. Results indicated a close and consistent set of coordinated movement patterns, which suggest biomechanical invariance in the responses of the structures adjacent to the upper limb during such a lifting task. These scapulohumeral relationships were, however, more constant and phase-locked when there was a specific purpose to the movement than during periods in which the arm was lowered without load. There were no age-related differences in any movement responses.     

Neural Crest Does Not Contribute to the Neck and Shoulder in the Axolotl (Ambystoma mexicanum)

Background

A major step during the evolution of tetrapods was their transition from water to land. This process involved the reduction or complete loss of the dermal bones that made up connections to the skull and a concomitant enlargement of the endochondral shoulder girdle. In the mouse the latter is derived from three separate embryonic sources: lateral plate mesoderm, somites, and neural crest. The neural crest was suggested to sustain the muscle attachments. How this complex composition of the endochondral shoulder girdle arose during evolution and whether it is shared by all tetrapods is unknown. Salamanders that lack dermal bone within their shoulder girdle were of special interest for a possible contribution of the neural crest to the endochondral elements and muscle attachment sites, and we therefore studied them in this context.

Results

We grafted neural crest from GFP+ fluorescent transgenic axolotl (Ambystoma mexicanum) donor embryos into white (d/d) axolotl hosts and followed the presence of neural crest cells within the cartilage of the shoulder girdle and the connective tissue of muscle attachment sites of the neck-shoulder region. Strikingly, neural crest cells did not contribute to any part of the endochondral shoulder girdle or to the connective tissue at muscle attachment sites in axolotl.

Conclusions

Our results in axolotl suggest that neural crest does not serve a general function in vertebrate shoulder muscle attachment sites as predicted by the “muscle scaffold theory,” and that it is not necessary to maintain connectivity of the endochondral shoulder girdle to the skull. Our data support the possibility that the contribution of the neural crest to the endochondral shoulder girdle, which is observed in the mouse, arose de novo in mammals as a developmental basis for their skeletal synapomorphies. This further supports the hypothesis of an increased neural crest diversification during vertebrate evolution.     

OSSIFICATION HETEROCHRONY IN THE THERIAN POSTCRANIAL SKELETON AND THE MARSUPIAL–PLACENTAL DICHOTOMY

Postcranial ossification sequences in 24 therian mammals and three outgroup taxa were obtained using clear staining and computed tomography to test the hypothesis that the marsupial forelimb is developmentally accelerated, and to assess patterns of therian postcranial ossification. Sequence rank variation of individual bones, phylogenetic analysis, and algorithm-based heterochrony optimization using event pairs were employed. Phylogenetic analysis only recovers Marsupialia, Australidelphia, and Eulipotyphla. Little heterochrony is found within marsupials and placentals. However, heterochrony was observed between marsupials and placentals, relating to late ossification in hind limb long bones and early ossification of the anterior axial skeleton. Also, ossification rank position of marsupial forelimb and shoulder girdle elements is more conservative than that of placentals; in placentals the hind limb area is more conservative. The differing ossification patterns in marsupials can be explained with a combination of muscular strain and energy allocation constraints, both resulting from the requirement of active movement of the altricial marsupial neonates toward the teat. Peramelemorphs, which are comparatively passive at birth and include species with relatively derived forelimbs, differ little from other marsupials in ossification sequence. This suggests that ossification heterochrony in marsupials is not directly related to diversity constraints on the marsupial forelimb and shoulder girdle.     

Evolution of the turtle bauplan: the topological relationship of the scapula relative to the ribcage

The turtle shell and the relationship of the shoulder girdle inside or ‘deep’ to the ribcage have puzzled neontologists and developmental biologists for more than a century. Recent developmental and fossil data indicate that the shoulder girdle indeed lies inside the shell, but anterior to the ribcage. Developmental biologists compare this orientation to that found in the model organisms mice and chickens, whose scapula lies laterally on top of the ribcage. We analyse the topological relationship of the shoulder girdle relative to the ribcage within a broader phylogenetic context and determine that the condition found in turtles is also found in amphibians, monotreme mammals and lepidosaurs. A vertical scapula anterior to the thoracic ribcage is therefore inferred to be the basal amniote condition and indicates that the condition found in therian mammals and archosaurs (which includes both developmental model organisms: chickens and mice) is derived and not appropriate for studying the developmental origin of the turtle shell. Instead, among amniotes, either monotreme mammals or lepidosaurs should be used.     

Ossification heterochrony in the therian postcranial skeleton and the marsupial-placental dichotomy.

Postcranial ossification sequences in 24 therian mammals and three outgroup taxa were obtained using clear staining and computed tomography to test the hypothesis that the marsupial forelimb is developmentally accelerated, and to assess patterns of therian postcranial ossification. Sequence rank variation of individual bones, phylogenetic analysis, and algorithm-based heterochrony optimization using event pairs were employed. Phylogenetic analysis only recovers Marsupialia, Australidelphia, and Eulipotyphla. Little heterochrony is found within marsupials and placentals. However, heterochrony was observed between marsupials and placentals, relating to late ossification in hind limb long bones and early ossification of the anterior axial skeleton. Also, ossification rank position of marsupial forelimb and shoulder girdle elements is more conservative than that of placentals; in placentals the hind limb area is more conservative. The differing ossification patterns in marsupials can be explained with a combination of muscular strain and energy allocation constraints, both resulting from the requirement of active movement of the altricial marsupial neonates toward the teat. Peramelemorphs, which are comparatively passive at birth and include species with relatively derived forelimbs, differ little from other marsupials in ossification sequence. This suggests that ossification heterochrony in marsupials is not directly related to diversity constraints on the marsupial forelimb and shoulder girdle.     

The Upper Devonian tetrapodomorph Gogonasus andrewsae from Western Australia: Reconstruction of the shoulder girdle and opercular series using X-ray Micro-Computed Tomography

The tetrapodomorph fish, Gogonasus andrewsae is a three dimensionally well-preserved sarcopterygian from the Gogo Formation (Frasnian, early Upper Devonian, ∼380 million years ago) in Western Australia. High-resolution X-ray Micro-Computed Tomography and 3D printouts were used to obtain a digital reconstruction of its shoulder girdle and opercular series. Our new findings show the opercular series in a close fit against the upper bones of the shoulder girdle only if the anocleithrum, supracleithrum and post-temporal are aligned more horizontally than in previous reconstructions. The lowermost subopercular bone also differs, in partly covering the clavicle of the shoulder girdle. The ascending process of the clavicle, and the ventral process of the anocleithrum, do not fit closely inside the cleithrum, and perhaps functioned for ligamentous attachment. A rugose area on the anocleithral process is in a similar relative position to the attachment of a muscle ligament on the shoulder girdle of various living actinopterygians. Our manipulation of 3D printouts permits testing of the morphological fit of extremely fragile acid-etched bones, and indicates a new way to investigate the constructional morphology of one or more mechanical units of the vertebrate skeleton. It is suggested that Micro-CT imaging, reconstruction, visualisation and 3D printing techniques will provide a rigorous new test leading to modification of previous reconstructions of extinct vertebrates that were based on graphical methods and 2D imaging.     

Crouched posture and high fulcrum, a principle in the locomotion of small mammals: The example of the rock hyrax (Procavia capensis) (Mammalia: Hyracoidea)

The cineradiographic study of the locomotion of the rock hyrax (Procavia capensis) and the functional interpretation of its locomotory system, reveals that the main action of proximal segments is combined with flexed position and low movements of limb joints. This observation can be applied to the locomotion of other small mammals. In the forelimb, scapular rotation and translation account for more than 60% of step length. Effective shoulder joint movements are mostly restricted to less than 20°, and elbow movements range mainly between 20°-50°. The detachment of the shoulder girdle of therian mammals from the axial skeleton, and development of a supraspinous fossa, are correlated with movements at a high scapular fulcrum. Movements at such a high fulcrum are in interdependency with a crouched posture. Only flexed limbs can act as shock absorbers and prevent vertical changes in the center of gravity. Basic differences in forelimb movements exist between larger primates (humeral retraction) and smaller mammals (scapula retraction). In the hyrax, propulsion is due mainly to hip joint movements in symmetrical gaits, but sagittal lumbar spine movements play the dominant role at in-phase gaits. Joint and muscular anatomy, especially of the shoulder region, are discussed in view of the kinematic data.     

A nearly complete skeleton of an early juvenile diplodocid (Dinosauria: Sauropoda) from the Lower Morrison Formation (Late Jurassic) of north central Wyoming and its implications for early ontogeny and pneumaticity in sauropods

A nearly complete skeleton of a juvenile sauropod from the Lower Morrison Formation (Late Jurassic, Kimmeridgian) of the Howe Ranch in Bighorn County, Wyoming is described. The specimen consists of articulated mid-cervical to mid-caudal vertebrae and most appendicular bones, but cranial and mandibular elements are missing. The shoulder height is approximately 67 cm, and the total body length is estimated to be less than 200 cm. Besides the body size, the following morphological features indicate that this specimen is an early juvenile; (1) unfused centra and neural arches in presacral, sacral and first to ninth caudal vertebrae, (2) unfused coracoid and scapula, (3) open coracoid foramen, and (4) relatively smooth articular surfaces on the limb, wrist, and ankle bones. A large scapula, short neck and tail and elongate forelimb bones relative to overall body size demonstrate relative growth. A thin-section of the mid-shaft of a femur shows a lack of annual growth lines, indicating an early juvenile individual possibly younger than a few years old. Pneumatic structures in the vertebral column of the specimen SMA 0009 show that pneumatisation of the postcranial skeleton had already started in this individual, giving new insights in the early ontogenetic development of vertebral pneumaticity in sauropods.

The specimen exhibits a number of diplodocid features (e.g., very elongate slender scapular blade with a gradually dorsoventrally expanded distal end, a total of nine dorsal vertebrae, presence of the posterior centroparapophyseal lamina in the posterior dorsal vertebrae). Although a few diplodocid taxa, Diplodocus, cf. Apatosaurus, and cf. Barosaurus, are known from several fossil sites near the Howe Ranch, identification of this specimen, even at a generic level, is difficult due to a large degree of ontogenetic variation.