Forelimb Kinematics of Rats Using XROMM,with Implications for Small Eutherians and Their Fossil Relatives

The earliest eutherian mammals were small-bodied locomotor generalists with a forelimb morphology that strongly resembles that of extant rats. Understanding the kinematics of the humerus, radius, and ulna of extant rats can inform and constrain hypotheses concerning typical posture and mobility in early eutherian forelimbs. The locomotion of Rattus norvegicus has been extensively studied, but the three-dimensional kinematics of the bones themselves remains under-explored. Here, for the first time, we use markerless XROMM (Scientific Rotoscoping) to explore the three-dimensional long bone movements in Rattus norvegicus during a normal, symmetrical gait (walking). Our data show a basic kinematic profile that agrees with previous studies on rats and other small therians: rats maintain a crouched forelimb posture throughout the step cycle, and the ulna is confined to flexion/extension in a parasagittal plane. However, our three-dimensional data illuminate long-axis rotation (LAR) movements for both the humerus and the radius for the first time. Medial LAR of the humerus throughout stance maintains an adducted elbow with a caudally-facing olecranon process, which in turn maintains a cranially-directed manus orientation (pronation). The radius also shows significant LAR correlated with manus pronation and supination. Moreover, we report that elbow flexion and manus orientation are correlated in R. norvegicus: as the elbow angle becomes more acute, manus supination increases. Our data also suggest that manus pronation and orientation in R. norvegicus rely on a divided system of labor between the ulna and radius. Given that the radius follows the flexion and extension trajectory of the ulna, it must rotate at the elbow (on the capitulum) so that during the stance phase its distal end lies medial to ulna, ensuring that the manus remains pronated while the forelimb is supporting the body. We suggest that forelimb posture and kinematics in Juramaia, Eomaia, and other basal eutherians were grossly similar to those of rats, and that humerus and radius LAR may have always played a significant role in forelimb and manus posture in small eutherian mammals.     

The osteology and musculature of the pectoral limb of small captorhinids

The osteology of the pectoral limb of small captorhinids is described and figured in detail. A cartilaginous sternum was present. The glenoid was not a simple sliding or rocking joint, as was previously supposed, but considerable rotation was also an integral part of the humeral movement. The structure of the elbow joint is such that when the lower arm was extended, its distal end swung forward and extended the anterior reach of the hand. When the lower arm was flexed, the posterior reach of the hand was extended. Articulated specimens allow a recontruction of the manus. There was no well developed wrist joint, but rather the manus, as a whole, was a flexible structure. A pisiform was present. Sesamoid bones were developed in the tendons of the palmaris communis profundus muscle. Study of forelimb musculature of living reptiles based on dissections and the literature indicates that its evolution has been very conservative. The forelimb musculature of small captorhinids probably was very similar to that of all living reptiles except turtles.     

Density of muscle spindle profiles in the intrinsic forelimb muscles of the dog

The concept of parallel muscle combinations, in which spindle density is significantly higher in small muscles compared to their larger counterparts in large-small muscle combinations acting across a joint, is supported by the results of this study regardless of the joint. Analysis of the canine data as well as previously published guinea pig forelimb and human pelvic limb data revealed no significant difference in spindle density between antigravity and non-antigravity muscles. Furthermore, a gradual increase in spindle density from proximal to distal on the limb was not found, although spindle density was significantly higher in the intrinsic manus or pes muscles compared to more proximal limb muscles in all three species. The significant differences in spindle densities in parallel muscle combinations and in manus/pes versus proximal muscles are discussed relative to their possible role in the control of locomotion.     

Interspecific variation in the tetradactyl manus of modern tapirs (Perissodactyla: Tapirus) exposed using geometric morphometrics

The distal forelimb (autopodium) of quadrupedal mammals is a key morphological unit involved in locomotion, body support, and interaction with the substrate. The manus of the tapir (Perissodactyla: Tapirus ) is unique within modern perissodactyls, as it retains the plesiomorphic tetradactyl (four‐toed) condition also exhibited by basal equids and rhinoceroses. Tapirs are known to exhibit anatomical mesaxonic symmetry in the manus, although interspecific differences and biomechanical mesaxony have yet to be rigorously tested. Here, we investigate variation in the manus morphology of four modern tapir species (Tapirus indicus , Tapirus bairdii , Tapirus pinchaque , and Tapirus terrestris ) using a geometric morphometric approach. Autopodial bones were laser scanned to capture surface shape and morphology was quantified using 3D‐landmark analysis. Landmarks were aligned using Generalised Procrustes Analysis, with discriminant function and partial least square analyses performed on aligned coordinate data to identify features that significantly separate tapir species. Overall, our results support the previously held hypothesis that T. indicus is morphologically separate from neotropical tapirs; however, previous conclusions regarding function from morphological differences are shown to require reassessment. We find evidence indicating that T. bairdii exhibits reduced reliance on the lateral fifth digit compared to other tapirs. Morphometric assessment of the metacarpophalangeal joint and the morphology of the distal facets of the lunate lend evidence toward high loading on the lateral digits of both the large T. indicus (large body mass) and the small, long limbed T. pinchaque (ground impact). Our results support other recent studies on T. pinchaque , suggesting subtle but important adaptations to a compliant but inclined habitat. In conclusion, we demonstrate further evidence that the modern tapir forelimb is a variable locomotor unit with a range of interspecific features tailored to habitual and biomechanical needs of each species.     

An Investigation of the Locomotor Function of Therian Forearm Pronation Provides Renewed Support for an Arboreal,Chameleon-like Evolutionary Stage

Although investigations of forelimb characteristics are central to therian evolutionary studies, the functional origins of forearm pronation are neglected. However, recent research based on bipedal manipulations strongly suggests that proximal radioulnar joint mobility is highly conserved in tetrapods. This new information calls for a replication of previously published physical simulations of forearm bone movements, to investigate whether active therian pronation/supination evolved from the plesiomorphic mechanism via which locomotor-induced torsion is passively alleviated during forelimb retraction. Preliminary results using representative extant and extinct tetrapod forelimb elements are supportive, and also offer insight into why another overlooked forearm trait, osteological full pronation (mechanically aligned elbow and wrist/finger joints), evolved only in therians and chameleons. During forelimb retraction in tetrapods with unfused radii/ulnae, the radius unexpectedly remains fixed in place as a functional complex with the firmly planted manus/carpus, which the ulnar complex (ulna/humerus) displaces relative to. Therefore, the highly conserved functional morphology of the tetrapod forearm indicates that enhanced therian manual dexterity, which emphasizes isolated radial movements bipedally, was preceded by the locomotor evolution of ulnar supination relative to the radius quadrupedally. This counterintuitive information indicates that the traditional hypothesis, that therian pronation/supination evolved arboreally to amplify radial mobility, requires modification. The authors propose that proximal long-axis rotations of the therian ulnar complex co-evolved with osteological full pronation during a period of arboreal, chameleon-like locomotion, to continue allowing torsion at a reinforced proximal radioulnar joint. These adaptations were later or simultaneously co-opted for object manipulation using active radioulnar pronation/supination.     

The anatomy of the forelimb in the anteater (Tamandua) and its functional implications

The forelimbs of anteaters play a major role in obtainment of food, defense, and locomotion. The greatly enlarged claws on the manus are used for ripping open insect nests and insect-infested wood; the claws also serve as the animals' only defensive weapons, since they lack teeth. Specialization of the claws for these functions has also had a substantial effect on the ways in which the forelimb is used for posture and locomotion. Modifications of the forelimb in the anteater Tamandua include the following. Attachments of the medial head of triceps are rearranged so as to greatly increase capability for powerful flexion of the claws. Ability to flex the elbow and to retract the humerus is also augmented; these movements would assist digital flexion in applying traction with the claws to material being torn away during food procurement. This traction can be supplemented by a variety of powerful side-to-side and/or twisting movements of the hand, brought about primarily by axial rotation of the upper arm and forearm. The digital joints are reinforced to resist the deviational and torsional loading to which the digits would be subjected during such movements. The morphological modifications of the forelimb in Tamandua are discussed in terms of how they affect the mechanical capabilities of the limb, what functions the limb is best designed to perform, how they may relate to what little is known about the specialized behavior of this animal, and what behavioral predictions may be made based on mechanical design.     

Morphological constraints in the digging apparatus of pocket gophers (Mammalia: Geomyidae)

The digging apparatus of pocket gophers offers a unique opportunity to examine morphological constraints within a historical context because relationships among extant taxa are well resolved and the features enhancing digging performance are relatively well understood. Structural and functional considerations suggest that the muscles associated with tooth- and claw-digging in pocket gophers are subjected to contrasting levels of morphological constraints. To assess this hypothesis, we analysed the bones and muscles of the jaws and forelimbs in four genera comprising five species of pocket gophers. Morphometric analyses were performed on 12 osteological measurements selected to reflect overall skull size, variation in rostral shape and procumbency, differences in overall length of the forelimbs and processes relating to the function of lever systems used in claw-digging. In addition, dissections were made of the jaw, hyoid, neck and all of the forelimb muscles excluding the intrinsic muscles of the manus. Results of our morphometric analyses corroborate the recent suggestion that pocket gophers encompass a wide range of morphological variation extending from claw-diggers to tooth-diggers. Myologically, however, we found structural variation only in the forelimb muscles, some of which may be advantageous for digging. No changes in jaw, neck and hyoid muscles, other than differences in muscle mass or those concordant with differences in rostral shape, were noted. These results support our hypothesis that constrasting levels of morphological constraint exist between the jaw and forelimb muscles of pocket gophers. We present a discussion of the structural and functional constraints on jaws and forelimbs in gophers as well as an analysis of historical constraints acting on this group, and perhaps on mammals in general.     

A new oviraptorid (Dinosauria: Theropoda) from the Upper Cretaceous of Bayan Mandahu,Inner Mongolia

Abstract: A new oviraptorid is described on the basis of a partial forelimb collected from the Upper Cretaceous redbeds of Bayan Mandahu, Inner Mongolia. Machairasaurus leptonychus, gen. et sp. nov. is diagnosed by slender, weakly curved manual unguals, reduced flexor tubercles, penultimate phalanges that are subequal in length to the preceding phalanges, and short, robust manual digits. Machairasaurus is found to be a member of the Ingeniinae, along with Ingenia yanshini, Heyuannia huangi, Conchoraptor gracilis, and Nemegtomaia barsboldi. Machairasaurus exhibits unusual proportions of the manus, suggesting that the manus was not primarily used to grasp prey. Instead, Machairasaurus and other oviraptorids are likely to have fed largely on plant material. The recognition of a previously unknown oviraptorid at Bayan Mandahu provides further evidence that the Bayan Mandahu dinosaur assemblage is distinct from that found at the Djadokhta Formation exposures at Bayn Dzak, Tugriken Shireh, and Ukhaa Tolgod. Given that these localities are separated by just a few hundred kilometres and represent similar palaeoenvironments, marked differences in the fauna suggest that the Bayan Mandahu Formation of Inner Mongolia is not coeval with the known Djadokhta localities in Mongolia.     

Derived appendicular morphology in Early Cretaceous aquatic turtles evidenced by the track record

A well‐preserved isolated manus impression evidences the presence of derived aquatic adaptations in the forelimb morphology of Berriasian turtles. Size and the abundant co‐occurring turtle fauna indicate that the track was left by a large‐sized, bottom‐walking basal pancryptodiran. The footprint shows an interesting mosaic of primitive and derived features. The basic turtle pattern is reflected by a short and broad autopodium but thin phalanges, claw reduction and extensive webbing enclosing the digits and lateral and medial margins of the distal metapodium are clearly specialized features related to the aquatic environment. Some characters including the proportional elongation of the first digit, which reached as far distally as the other digits and was probably highly mobile at the metacarpal‐phalangeal joint, indicate an even higher degree of specialization. The specimen gives evidence on a hitherto unknown range of appendicular modification in Early Cretaceous turtles, and redundantly proves the aquatic habitat and locomotion of large‐sized turtles from the Berriasian of northwestern Germany.     

The functional anatomy of the forelimb of some African viverridae (Carnivora)

The functional morphology of the forelimbs of the following African Viverridae was studied, Atilax paludinosus, Bdeogale crassicauda, Civettictis civetta, Genetta genetta, G. tigrina, Helogale parvula, Herpestes ichneumon, H. sanguineus, Ichneumia albicauda, Mungos mungo, Nandinia binotata. Their locomotory behaviour has been previously studied and described and is related to morphological differences. The osteology of all the species and the myology of three species is described. The species have been assigned to primary locomotor categories on the basis of their locomotion. These are 1, climbing, arboreal walking; 2, arboreal and terrestrial walking and jumping; 3, general terrestrial walking and scrambling; and 4, trotting. In the climbing arboreal walking category the most distinctive morphological adaptations are powerful flexors and extensors as well as a flexible plantigrade manus with retractile claws. In the arboreal and terrestrial walking category the shoulder, elbow and carpal joints are flexible and the manus has retractile claws, though the flexor and extensor musculature is insufficiently developed for controlled climbing. The trotting category is characterised by a high humero-radial index and a rigid antibrachium. The foot is digitigrade with the claws short and stout. Species in the general walking and scrambling category show many differences in the morphology of their feet, even though the proximal parts of the forelimb appear similar. Due to the restricted nature of the adaptations, these species have been assigned to secondary locomotor categories. Morphological characters typical of the locomotor categories are summarized in the discussion.     

Bird-Like Anatomy,Posture, and Behavior Revealed by an Early Jurassic Theropod Dinosaur Resting Trace

Background

Fossil tracks made by non-avian theropod dinosaurs commonly reflect the habitual bipedal stance retained in living birds. Only rarely-captured behaviors, such as crouching, might create impressions made by the hands. Such tracks provide valuable information concerning the often poorly understood functional morphology of the early theropod forelimb.

Methodology/Principal Findings

Here we describe a well-preserved theropod trackway in a Lower Jurassic (∼198 million-year-old) lacustrine beach sandstone in the Whitmore Point Member of the Moenave Formation in southwestern Utah. The trackway consists of prints of typical morphology, intermittent tail drags and, unusually, traces made by the animal resting on the substrate in a posture very similar to modern birds. The resting trace includes symmetrical pes impressions and well-defined impressions made by both hands, the tail, and the ischial callosity.

Conclusions/Significance

The manus impressions corroborate that early theropods, like later birds, held their palms facing medially, in contrast to manus prints previously attributed to theropods that have forward-pointing digits. Both the symmetrical resting posture and the medially-facing palms therefore evolved by the Early Jurassic, much earlier in the theropod lineage than previously recognized, and may characterize all theropods.     

The myology of the manus of microtine rodents

A study of the muscles of the manus of 13 genera and subgenera of microtine rodents revealed considerable variation which could be organized into 23 primitive-derived evolutionary hypotheses (transmutation series). The results, when compared with those for other mammals, produced functional/ecological hypotheses which were tested by comparing their predictions with the literature. The microtine manus is morphologically distinguished by nine characters and is adapted for a terrestrial/semi-fossorial niche. In particular, Dicrostonyx and Lemmus (distinguished by eight characters) possess the most highly fossorial manus, while the manus of Arborimus (distinguished by eight characters) contains a combination of primitive characters and derived characters which give the Tree vole the most highly developed 'clasping' ability among the microtines studied. The study has revealed characters which have potential systematic value but it is probable that parallelism has occurred in the microtine manus. When the manual characters are combined with characters from other functional complexes, their systematic value can be more clearly determined.     

A new model of forelimb ecomorphology for predicting the ancient habitats of fossil turtles

Various morphological proxies have been used to infer habitat preferences among fossil turtles and their early ancestors, but most are tightly linked to phylogeny, thereby minimizing their predictive power. One particularly widely used model incorporates linear measurements of the forelimb (humerus + ulna + manus), but in addition to the issue of phylogenetic correlation, it does not estimate the likelihood of habitat assignment. Here, we introduce a new model that uses intramanual measurements (digit III metacarpal + non‐ungual phalanges + ungual) to statistically estimate habitat likelihood and that has greater predictive strength than prior estimators. Application of the model supports the hypothesis that stem‐turtles were primarily terrestrial in nature and recovers the nanhsiungchelyid Basilemys (a fossil crown‐group turtle) as having lived primarily on land, despite some prior claims to the contrary.     

Functional osteology of the avian wrist and the evolution of flapping flight

The avian wrist is extraordinarily adapted for flight. Its intricate osteology is constructed to perform four very different, but extremely important, flight-related functions. (1) Throughout the downstroke, the cuneiform transmits force from the carpometacarpus to the ulna and prevents the manus from hyperpronating. (2) While gliding or maneuvering, the scapholunar interlocks with the carpometacarpus and prevents the manus from supinating. By employing both carpal bones simultaneously birds can lock the manus into place during flight. (3) Throughout the downstroke-upstroke transition, the articular ridge on the distal extremity of the ulna, in conjuction with the cuneiform, guides the manus from the plane of the wing toward the body. (4) During take-off or landing, the upstroke of some heavy birds exhibits a pronounced flick of the manus. The backward component of this flick is produced by reversing the wrist mechanism that enables the manus to rotate toward the body during the early upstroke. The upward component of the flick is generated by mechanical interplay between the ventral ramus of the cuneiform, the ventral ridge of the carpometacarpus, and the ulnocarpo-metacarpal ligament. Without the highly specialized osteology of the wrist it is doubtful that birds would be able to carry out successfully the wing motions associated with flapping flight. Yet in Archaeopteryx, the wrist displays a very different morphology that lacks all the key features found in the modern avian wrist. Therefore, Archaeopteryx was probably incapable of executing the kinematics of modern avian powered flight.     

Limb movements and locomotor function in the California sea lion (Zalophus californianus)

The peculiar amphibious mode of life of California sea lions suggests that their locomotor systems may contain adaptations both to life on land and in the water. Previous studies of their locomotor behaviour have been either superficial or based on inferences which were derived from limb structure. Limb movements associated with locomotor behaviour in California sea lions are described on the basis of frame-by-frame analysis of slow motion cinematography of typical aquatic and terrestrial locomotor sequences. Results are compared to reports of terrestrial and aquatic locomotor behaviour in fissiped carnivores, whose locomotor behaviour is presumed to reflect the framework from which the locomotor behaviour of sea lions was derived. The major distinction between sea lions and fissipeds in terms of aquatic locomotor behaviour involves the use of the forelimb in sea lions. Propulsive thrust is generated by medial rotation, adduction and retraction of the forelimbs in sea lions, in contrast to nearly pure limb retraction in fissipeds. The major features which distinguish terrestrial locomotor behaviour in sea lions from that of fissipeds are use of the manus as a transverse rather than sagittal propulsive lever and extensive use of posterior axial and head and neck movements rather than hindlimb movements. The biomechanical implications of these movements are used to elucidate their potentially adaptive features.     

Postcranial morphology of the extinct caviine rodent Microcavia criolloensis (late Pleistocene,South America)

A comparative study of the appendicular skeletal morphology, with a particular emphasis on the autopodial elements (manus and pes), of the extinct caviine rodent Microcavia criolloensis (Late Pleistocene, Uruguay), together with that of living species of Microcavia and some allied caviines is performed. Burrow‐digging and above‐ground behaviour by M. criolloensis could have evolved in the Late Pleistocene, as with its relative M. australis in the Recent. This is suggested based on the morphology of preserved articulated skeletons along with fossil burrow‐like structures. The most remarkable features are: in its forelimb, where the humerus has a structure that would have allowed it to perform similar activities to M. australis, based on humeral width across the epicondiles relative to total humerus length index and a good resistance as indicated by high values relating the diameter of the diaphysis to its total length. Qualitative comparison shows that M. criolloensis had a stout, wide manus with relatively short digits including short, wide phalanges, despite its large size. In its hind limb there is a stout hind‐foot with relatively short and wide metatarsals and phalanges, as compared with those of the recent species, that could arguably be considered a useful tool for shovelling out displaced soil. The generalized morphology suggests above‐ground behaviour together with digging ability. The environmental adaptations of M. criolloensis are also briefly discussed, which seem to differ from those of its extant relatives. © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society, 2008, 154 , 795–806.     

An unusual pattern of limb morphology in the Tithonian marine turtle Neusticemys neuquina from the Vaca Muerta Formation,Neuquén Basin,Argentina

de la Fuente M.S. & Fernández, M.S. 2010: An unusual pattern of limb morphology in the Tithonian marine turtle Neusticemys neuquina from the Vaca Muerta Formation, Neuquén Basin, Argentina. Lethaia, Vol. 44, pp. 15–25. Here, we report an unusual pattern in the manus and pes morphology of the Tithonian marine turtle Neusticemys neuquina. We analyse the forelimbs of two previously known specimens and describe the hind limbs of two previously undescribed specimens. Neusticemys neuquina is characterized by a relative elongation of both the forelimb and hind limb, compared with stem Chelonoidea, as well as an elongation of the pedal digit V, achieved through the elongation of the bones, as well as a moderate hyperphalangy. The elongation of pedal digit V is the most striking feature of N. neuquina, a feature unknown in other turtles. □Limb morphology, Neusticemys neuquina, Tithonian turtle.     

Claw retraction and protraction in the carnivora: Skeletal microvariation in the phalanges of the Felidae

All carnivorans retract and protract their claws. In felids and some viverrids the claws of digits II through V of both the manus and pes have a larger arc of rotation than those of other carnivorans; the claws retract to the lateral side of the middle phalanx rather than onto its dorsal surface as in most other carnivorans. This condition should be termed hyper-retraction. Morphological features of the middle and distal (ungual) phalanges that have been purported to be necessary for hyper-retraction in felids vary considerably among digits within the manus and pes. These features include the lateral projection of the distal head and the asymmetry of the shaft of the middle phalanx, and the oblique orientation of the articular surface on the distal phalanx. None of these features is necessary in every instance for hyperretraction, and some of the variation in these features is associated instead with protraction. Differences among digits in the orientation of the articular surface on the distal phalanx are associated with differences in the degree to which the claws must move laterally to rotate from the protracted to the retracted position. Differences in the orientation of the distal head on the middle phalanx are associated with the spreading of the claws during protraction. The manual claws are hook-shaped, whereas the pedal claws are more blade-like; this morphological difference is associated with differences in function between the manus and pes. In the manus the medial claws have a larger radius of curvature and a smaller angle of arc as compared to the more lateral claws; in the pes, the claws on digits III and IV have larger radii of curvature and smaller angles of arc. Digit I of the manus lacks the hyper-retraction mechanism; nonetheless, this digit shares many of the attributes that are associated with this mechanism. © 1996 Wiley-Liss, Inc.     

Pterosaur tracks and the terrestrial ability of pterosaurs

Unusual tracks of a quadrupedal animal with a three-digit (occasionally four-digit) manus print and four-digit pes print were first interpreted as those of pterosaurs in the 1950s. In the 1980s these tracks were reinterpreted as crocodilian, but new material shows that the original identification was correct. Two features: evidence for elongate penultimate phalanges in digits two to four of the pes, and manus trackways up to three times the width of pes trackways, can only be attributed to pterosaurs. Recent improvements in understanding of pterosaur anatomy and functional morphology explain remaining difficulties regarding the interpretation of ich-nites such as the orientation of the manus digits and the absence of some expected ichnological features. Pteraichnus and Pteraichnus-like tracks show that, when grounded, some, perhaps all, pterosaurs were plantigrade, quadrupedal, and had a semi-erect stance and gait. This is consistent with some functional interpretations of pterosaur anatomy and resolves a long-running debate regarding the terrestrial ability of this group.     

A New Specimen of Carroll’s Mystery Hupehsuchian from the Lower Triassic of China

A new specimen of an enigmatic hupehsuchian genus is reported. The genus was first recognized by Robert L. Carroll and Zhi-ming Dong in 1991, who refrained from naming it because of the poor quality of the only specimen known at the time. After more than two decades, we finally report a second specimen of this genus, which remained unprepared until recently. The new specimen preserves most of the skeleton except the skull, allowing us to erect a new genus and species, Eretmorhipis carrolldongi. The new species shares many characters with Parahupehsuchus longus, including the strange axial skeleton that forms a bony body tube. However, the body tube is short in the new species, being limited to the pectoral region. The vertebral count and limb morphology considerably differ between the new species and P. longus. The forelimb of E. carrolldongi is markedly larger than its hind limb as in Hupehsuchus nanchangensis but unlike in P. longus. The new species is unique among hupehsuchians in a list of features. It has manual and pedal digits that spread radially, forming manus and pes that are almost as wide as long. The third-layer elements of the dermal armor are unusually large, spanning four vertebral segments, yet there are substantial gaps among them. With the addition of the unique paddle, it is now clear that Hupehsuchia had diverse forelimb morphologies spanning from paddles to flippers, unlike ichthyopterygians that were taxonomically more diverse yet only had flippers.