Evidence at hand: Diversity, functional implications, and locomotor prediction in intrinsic hand proportions of diprotodontian marsupials

Knowledge about the diversity, locomotor adaptations, and evolution of the marsupial forelimb is limited, resulting in an underrepresentation of marsupials in comparative anatomical literature on mammalian forelimb anatomy. This study investigated hand proportions in the diverse marsupial order Diprotodontia. Fifty-two measurements of 95 specimens representing 47 species, as well as 6 non-diprotodontian specimens, were explored using principal components analysis (PCA). Bootstrapping was used to assess the reliability of the loadings. Phylogenetically independent contrasts and phylogenetic ANOVA were used to test for correlation with size and functional adaptation of forelimbs for locomotor habit, scored as arboreal vs. terrestrial. Analysis of first principal component (PC1) scores revealed significant differences between arboreal and terrestrial species, and was related to relative slenderness of their phalangeal elements. Both locomotor groups displayed allometry along PC1 scores, but with different intercepts such that PC1 discriminated between the two locomotor habits almost completely. PC2 separated some higher-level clades and burrowing species. Analysis of locomotor predictors commonly applied by palaeontologists indicates that ratios between proximal and intermediate phalanges were unsuitable as predictors of arboreality/terrestriality, but the phalangeal index was more effective. From PCA results, a phalangeal slenderness ratio was developed which proved to be a useful discriminator, suggesting that a single unallocated phalanx can be used for an impression of locomotor mode in fossils. Most Diprotodontia are laterally paraxonic or ectaxonic, with the exception of digging species whose hands are medially paraxonic. Our results complement those of studies on placental mammals, suggesting that the demands of arboreality, terrestriality, or frequent digging on intrinsic hand proportions are met with similar anatomical adaptations in marsupials.     

Tail loss, body condition and swimming performances in tiger snakes, Notechis ater occidentalis

In limbless tetrapods such as snakes, propulsive forces are generated by lateral undulations of the body and of the tail. In a large population of tiger snakes from Western Australia, tail loss was extremely common (58% of the individuals) and often very severe (more than two-thirds of the tail was missing in 14% of the cases, and in some instances, the tail was totally lost). Tail loss was not however correlated with body size, mass or body condition of wild individuals, and hence did not influence their abilities to acquire resources. These large venomous snakes exhibit marked aquatic habits. Locomotor tests in controlled conditions revealed that tail loss had a significant negative influence on burst swimming performances. However, no effect was found on routine swimming speed and total distance travelled over 5 min. These results suggest that a long and slender tail, although important for maximal speed, is not necessarily relevant for the locomotor abilities required for successful hunting. Tail-damaged individuals outnumbered intact snakes, suggesting that tail loss did not severely compromise survival. Overall, in this species, a slight deterioration of maximal speed due to severe tail loss probably has a low (undetectable) ecological impact, at least for adults.     

Forelimb anatomy and the discrimination of the predatory behavior of carnivorous mammals: The thylacine as a case study

Carnivorous mammals use their forelimbs in different ways to capture their prey. Most terrestrial carnivores have some cursorial (running) adaptations, but ambush predators retain considerable flexibility in their forelimb movement, important for grappling with their prey. In contrast, predators that rely on pursuit to run down their prey have sacrificed some of this flexibility for locomotor efficiency, in the greater restriction of the forelimb motion to the parasagittal plane. In this article, we measured aspects of the forelimb anatomy (44 linear measurements) in 36 species of carnivorous mammals of known predatory behavior, and used multivariate analyses to investigate how well the forelimb anatomy reflects the predatory mode (ambush, pursuit, or pounce‐pursuit). A prime intention of this study was to establish morphological correlates of behavior that could then be applied to fossil mammals: for this purpose, five individuals of the recently extinct thylacine (Thylacinus cynocephalus) were also included as unknowns. We show that the three different types of predators can be distinguished by their morphology, both in analyses where all the forelimb bones are included together, and in the separate analyses of each bone individually. Of particular interest is the ability to distinguish between the two types of more cursorial predators, pursuit and pounce‐pursuit, which have previously been considered as primarily size‐based categories. Despite a prior consideration of the thylacine as a “pounce‐pursuit” or an “ambush” type of predator, the thylacines did not consistently cluster with any type of predatory carnivores in our analyses. Rather, the thylacines appeared to be more generalized in their morphology than any of the extant carnivores. The absence of a large diversity of large carnivorous mammals in Australia, past and present, may explain the thylacine's generalized morphology. J. Morphol. 275:1321–1338, 2014. © 2014 Wiley Periodicals, Inc.     

Functional-adaptive analysis of the hindlimb anatomy of extant marsupials and the paleobiology of the Paleocene marsupials Mayulestes ferox and Pucadelphys andinus

This article analyzes the adaptations of the hindlimb of two Early Paleocene marsupials, Mayulestes ferox and Pucadelphys andinus. This analysis is based on detailed comparisons with various extant marsupials, both South American and Australian. In the case of the South American opossums, original myological data were collected and osteological-myological associations were related to their locomotor behavior. The use of Australian genera helped to improve the appraisal of the locomotory habits of the fossil taxa. Several features are indicative of the ability of Mayulestes to climb or walk on uneven surfaces (e.g., very mobile hip joint, astragalocalcaneal joint pattern), and some other features emphasize a relative agility (e.g., strongly everted iliac blades, morphology of the distal epiphysis of the femur, medially stabilized cruroastragalar joint). Pucadelphys exhibits a hindlimb relatively similar morphologically to that of Mayulestes, but with features indicating slightly increased agility and a terrestrial component that is more emphasized than in Mayulestes. The Tiupampa fossils were therefore more agile than most living didelphids and resembled the condition observed in living dasyurids more. These conclusions complement a previous study performed on the forelimb of these fossils.     

Energetic and locomotor costs of tail loss in the Chinese skink, Eumeces chinensis

Caudal autotomy is a defense mechanism used by numerous lizards to evade predators, but this entails costs. We collected 294 adult Chinese skinks (Eumeces chinensis) from a population in Lishui (eastern China) to evaluate energetic and locomotor costs of tail loss. Of the 294 skinks, 214 (c. 73%) had previously experienced caudal autotomy. Neither the proportion of individuals with regenerated tails nor the frequency distribution of locations of the tail break differed between sexes. We successively removed four tail segments from each of the 20 experimental skinks (adult males) initially having intact tails. Lipid content in each removed tail segment was measured, and locomotor performance (sprint speed, the maximal length traveled without stopping and the number of stops in the racetrack) was measured for each skink before and after each tail-removing treatment. Another independent sample of 20 adult males with intact tails was measured for locomotor performance to serve as controls for successive measurements taken for the experimental lizards. Caudal lipids were disproportionately stored along the length of the tail, with most lipids being aggregated in its proximal portion. Tail loss significantly affected sprint speed, but not the maximal length of, or the number of stops during the sprint. However, the adverse influence of tail loss on sprint speed was not significant until more than 51% of the tail (in length) was lost. Our data show that partial tail loss due to predatory encounters or other factors may not severely affect energy stores or locomotor performance in E. chinensis. As tail breaks occurred more frequently in the proximal portion of the tail in skinks collected from the field, we conclude that caudal autotomy occurring in nature often incurs substantial energetic and locomotor costs in E. chinensis.     

Partial tail loss has no severe effects on energy stores and locomotor performance in a lacertid lizard, <Emphasis Type="Italic">Takydromus septentrionalis</Emphasis>

Many species of lizards use caudal autotomy as a defense strategy to avoid predation, but tail loss entails costs. These topics were studied experimentally in the northern grass lizard, Takydromus septentrionalis. We measured lipids in the three-tail segments removed from each of the 20 experimental lizards (adult females) initially having intact tails to evaluate the effect of tail loss on energy stores; we obtained data on locomotor performance (sprint speed, the maximal length traveled without stopping and the number of stops in the racetrack) for these lizards before and after the tail-removing treatments to evaluate the effect of tail loss on locomotor performance. An independent sample of 20 adult females that retained intact tails was measured for locomotor performance to serve as controls for successive measurements taken for the experimental lizards. The lipids stored in the removed tail was positively correlated with tailbase width when holding the tail length constant, indicating that thicker tails contained more lipids than did thinner tails of the same overall length. Most of the lipids stored in the tail were concentrated in the proximal portion of the tail. Locomotor performance was almost unaffected by tail loss until at least more than 71% of the tail (in length) was lost. Our data show that partial tail loss due to predatory encounters or other factors may not severely affect energy stores and locomotor performance in T. septentrionalis.     

Body proportions,microhabitat selection,and adaptive radiation of Liolaemus lizards in central Chile

Summary A biometric analysis of body proportions with presumably functional meaning for microhabitat selection was made on 12 species of Liolaemus lizards in central Chile. Characters studied were forelimb length, hindlimb length, tail length (all standardized by the corresponding snout-vent length), and the ratio forelimb/hindlimb length. It is shown that irrespective of terrestrial, saxicolous, or arboreal habits, Liolaemus species are remarkably similar in body proportions. The only exceptions are: L. lemniscatus, an open ground-dweller which exhibits significantly shorter limbs; and L. chiliensis and L. schroederi, both shrub-climbers which exhibit significantly longer tail. It is concluded that the adaptive radiation of Liolaemus lizards in central Chile has been accomplished mainly by diversification of activity time, food size, and microhabitat type. Morphological divergence in body proportions seems to have played an unimportant role.     

Postcranial morphology and the locomotor habits of living and extinct carnivorans

Members of the order Carnivora display a broad range of locomotor habits, including cursorial, scansorial, arboreal, semiaquatic, aquatic, and semifossorial species from multiple families. Ecomorphological analyses from osteological measurements have been used successfully in prior studies of carnivorans and rodents to accurately infer the locomotor habits of extinct species. This study uses 20 postcranial measurements that have been shown to be effective indicators of locomotor habits in rodents and incorporates an extensive sample of over 300 individuals from more than 100 living carnivoran species. We performed statistical analyses, including analysis of variance (ANOVA) and stepwise discriminant function analysis, using a set of 16 functional indices (ratios). Our ANOVA results reveal consistent differences in postcranial skeletal morphology among locomotor groups. Cursorial species display distal elongation of the limbs, gracile limb elements, and relatively narrow humeral and femoral epicondyles. Aquatic and semiaquatic species display relatively robust, shortened femora and elongate metatarsals. Semifossorial species display relatively short, robust limbs with enlarged muscular attachment sites and elongate claws. Both semiaquatic and semifossorial species have relatively elongate olecranon process of the ulna and enlarged humeral and femoral epicondyles. Terrestrial, scansorial, and arboreal species are characterized by having primarily intermediate features, but arboreal species do show relatively elongate manual digits. Morphological indices effectively discriminate locomotor groups, with cursorial and arboreal species more accurately classified than terrestrial, scansorial, or semiaquatic species. Both within and between families, species with similar locomotor habits converge toward similar postcranial morphology despite their independent evolutionary histories. The discriminant analysis worked particularly well to correctly classify members of the Canidae, but not as well for members of the Mustelidae or Ursidae. Results are used to infer the locomotor habits of extinct carnivorans, including members of several extinct families, and also 12 species from the Pleistocene of Rancho La Brea. J. Morphol., 2013. © 2012 Wiley Periodicals, Inc.     

Locomotor behavior and muscular anatomy of sympatric Malaysian leaf-monkeys (Presbytis obscura and Presbytis melalophos).

Sympatric Malaysian leaf-monkeys, Presbytis obscura and Presbytis melalophos show quantitative differences in their use of different locomotor patterns during daily activities. P. obscura primarily moves quadrupedally along large boughs; P. melalophos relies more on leaping between smaller supports. P. melalophos also uses forelimb suspension more than does P. obscura. Comparison of the muscular anatomy of the shoulder, arm, trunk, hip and thigh show numerous statistically significant differences between the two species in relative mass of individual muscles and in details of muscular origin and insertion. In almost all instances these differences accord with the types of differences in muscular anatomy predictable from either biomechanical analyses of locomotor behavior or comparative anatomical studies of other mammalian species.     

长掌义县龙(兽脚类:恐龙)及其在手盗龙类进化和热河动物群生态学研究中的意义(英文)

重新研究了产于辽西义县组下部的带羽毛小型兽脚类恐龙长掌义县龙(Yixianosaurus longimanus) 的不完整骨架。系统发育分析得出义县龙属于手盗龙类基干类群,与阿尔瓦雷斯龙( Alvarezsaurus) 、镰刀龙类、除阿尔瓦雷斯龙之外的其他阿尔瓦雷斯龙类以及由窃蛋龙类和副鸟龙类等进步手盗龙类组成的一个类群形成多分支状态。义县龙既有原始特征,如臂指数低,第三指强壮; 也有进步特征,如乌喙骨近长方形,表明在手盗龙类当中,前肢演化呈现出比以前认为的更加复杂的镶嵌现象。强壮的前肢骨骼以及厚重、弯曲而尖利的手爪表明义县龙是捕食者,尽管这一认识尚待该属种更完整化石的发现来证实。义县龙在手盗龙类系统发育中的基部位置暗示,在虚骨龙类演化的这一节点上,前肢形态的变异范围更大。在许多方面,义县龙强壮的前肢和过度增大的弯曲爪子与长臂猎龙(Tanycolagreus) 和虚骨龙(Coelurus) 的相似,可能代表了这些属种与基干镰刀龙类和窃蛋龙类之间的过渡形态。义县龙保存了大的片状体羽,表明这些皮肤衍生物在虚骨龙类中的起源可能比以前报道的要早。最后,强壮而伸长的前肢暗示了其生态功能与根据同一区域的其他小型兽脚类推测的不同,支持了热河生物群的小型非鸟兽脚类中存在小生境划分的观点。     

Biomechanical analysis of vertical climbing in the spider monkey and the Japanese macaque

Climbing is one of the most important components of primate locomotor modes. We previously reported that the kinesiological characteristics of vertical climbing by the spider monkey and Japanese macaque are clearly different, based on their kinetics and kinematics. In this study, a more detailed analysis using inverse dynamics was conducted to estimate the biomechanical characteristics of vertical climbing in the spider monkey and Japanese macaque. One of the main findings was the difference in forelimb use by the two species. The results of a joint moment analysis and estimates of muscular force indicate that the spider monkey uses its forelimbs to keep the body close to the substrate, rather than to generate propulsion. The forelimb of the Japanese macaque, on the other hand, likely contributes more to propulsion. This supports the idea that "forelimb-hindlimb differentiation" is promoted in the spider monkey. The estimated muscular force also suggests that the spider monkey type of climbing could develop the hindlimb extensor muscles, which are important in bipedal posture and walking. As a result, we conclude that the spider monkey type of climbing could be functionally preadaptive for human bipedalism. This type of climbing would develop the hip and knee extensor muscles, and result in more extended lower limb joints, a more erect trunk posture, and more functionally differentiated fore- and hindlimbs, all of which are important characteristics of human bipedalism.     

LOCOMOTOR MODULES AND THE EVOLUTION OF AVIAN FLIGHT

The evolution of avian flight can be interpreted by analyzing the sequence of modifications of the primitive tetrapod locomotor system through time. Herein, we introduce the term “locomotor module” to identify anatomical subregions of the musculoskeletal system that are highly integrated and act as functional units during locomotion. The first tetrapods, which employed lateral undulations of the entire body and appendages, had one large locomotor module. Basal dinosaurs and theropods were bipedal and possessed a smaller locomotor module consisting of the hind limb and tail. Bird flight evolved as the superimposition of a second (aerial) locomotor capability onto the ancestral (terrestrial) theropod body plan. Although the origin of the wing module was the primary innovation, alterations in the terrestrial system were also significant. We propose that the primitive theropod locomotor module was functionally and anatomically subdivided into separate pelvic and caudal locomotor modules. This decoupling freed the tail to attain a new and intimate affiliation with the forelimb during flight, a configuration unique to birds. Thus, the evolution of flight can be viewed as the origin and novel association of locomotor modules. Differential elaboration of these modules in various lineages has produced the diverse locomotor abilities of modern birds.     

Functional anatomy and biomechanics of the postcranial skeleton of Simocyon batalleri (Viret, 1929) (Carnivora, Ailuridae) from the Late Miocene of Spain

We describe the postcranial anatomy of the Miocene puma-sized ailurid Simocyon batalleri , discussing some aspects of its biomechanics and inferring a probable life style. The postcranial anatomy of S. batalleri was previously unknown due the fragmentary nature of its fossil record, and most of the available fossils corresponded to cranial and dental material. With the discovery of a rich sample from the Late Miocene natural trap of Batallones-1, to the south of Madrid (Spain), including the remains of at least two individuals of S. batalleri , it is possible to study for the first time the anatomy of the cervical and lumbar vertebrae, complete forelimb and partial hind limb. The morphology of the forelimb, the lumbar region and the unexpected presence of a false-thumb are strongly suggestive of arboreal capabilities. Such locomotor abilities are consistent with a palaeobiological model of a generalized carnivore that foraged mainly on the ground but could readily climb to trees for safety if faced with the threat of larger competing carnivores.  © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society , 2008, 152 , 593–621.     

Functional anatomy of the olecranon process in hominoids and plio-pleistocene hominins

This study examines the functional morphology of the olecranon process in hominoids and fossil hominins. The length of the bony lever of the triceps brachii muscle (TBM) is measured as the distance between the trochlear articular center and the most distant insertion site of the TBM, and olecranon orientation is measured as the angle that this bony lever makes with the long axis of the ulna. Results show that Homo, Pan, Gorilla, most monkeys, and the Australopithecus fossils studied have similar relative olecranon lengths. Suspensory hominoids and Ateles have shorter olecranons, suggesting, in some instances, selection for greater speed in extension. The orientation that the lever arm of the TBM makes with the long axis of the ulna varies with preferred locomotor mode. Terrestrial primates have olecranons that are more posteriorly oriented as body size increases, fitting general models of terrestrial mammalian posture. Arboreal quadrupeds have more proximally oriented lever arms than any terrestrial quadrupeds, which suggests use of the TBM with the elbow in a more flexed position. Olecranon orientation is not consistent in suspensory hominoids, although they are all characterized by orientations that are either similar or more posterior than those observed in quadrupeds. Homo and the fossils have olecranons that are clearly more proximally oriented than expected for a quadruped of their size. This suggests that Homo and Australopithecus used their TBM in a flexed position, a position most consistent with manipulatory activities.     

Nice snake, shame about the legs

Snakes are one of the most extraordinary groups of terrestrial vertebrates, with numerous specializations distinguishing them from other squamates (lizards and their allies). Their musculoskeletal system allows creeping, burrowing, swimming and even gliding, and their predatory habits are aided by chemo- and thermoreceptors, an extraordinary degree of cranial kinesis and, sometimes, powerful venoms. Recent discoveries of indisputable early fossil snakes with posterior legs are generating intense debate about the evolutionary origin of these reptiles. New cladistic analyses dispute the precise significance and phylogenetic placement of these fossils. These conflicting hypotheses imply radically different scenarios of snake origins and relationships with wide biological implications.     

Body mass and locomotor habits of the smallest darter,Anhinga minuta (Aves,Anhingidae)

During the Neogene of South America, Anhingidae was represented by several species, mainly with greater sizes than the extant members. In the present contribution, body mass and locomotor habits of Anhinga minuta, the smallest known darter, were inferred. Body mass was estimated using two methods, one with measures of a tibiotarsus (the holotype) and the other, with measurements of a humerus; locomotor habits were inferred through muscular reconstructions and wing parameters (wing span, wing area and wing loading). Estimates of wing span and wing area were based on the length of humerus, assuming a condition of isometry with respect to Anhinga anhinga; wing loading was obtained through a relation formula between wing area and body mass. The results obtained indicate a body mass of about 729 g, a wing span of 0.958 m, a wing area of 0.117 m² and a corresponding wing loading of 61 N/m². These values and also the proximal insertion of the musculus pectoralis are consistent with those of a soaring bird but with more frequent flapping than extant anhingids. Furthermore, the inferred musculature for tibiotarsus indicates abilities for swimming, climbing and moving through the vegetation as in extant representatives.     

Ontogeny of limb force distribution in squirrel monkeys (Saimiri boliviensis): insights into the mechanical bases of primate hind limb dominance

The distribution of peak vertical forces between the forelimbs and the hind limbs is one of the key traits distinguishing primate quadrupedal locomotion from that of other mammals. Whereas most mammals generate greater peak vertical forelimb forces, primates generate greater peak vertical hind limb forces. At the ultimate level, hind limb dominance in limb force distribution is typically interpreted as an adaptation to facilitate fine-branch arboreality. However, the proximate biomechanical bases for primate limb force distribution remain controversial. Three models have been previously proposed. The Center of Mass (COM) Position model attributes primates’ unique mode of limb loading to differences in the position of the whole-body COM relative to the hands and feet. The Active Weight Shift model asserts that primates actively redistribute body weight to their hind limbs by pitching the trunk up via the activation of hind limb retractor muscles. Finally, the Limb Compliance model argues that primates selectively mitigate forelimb forces by maintaining a compliant forelimb and a flat shoulder trajectory. Here, a detailed dataset of ontogenetic changes in morphology and locomotor mechanics in Bolivian squirrel monkeys (Saimiri boliviensis) was employed as a model system to evaluate each of these proposed models in turn. Over the first 10 months of life, squirrel monkeys transitioned from forelimb dominant infants to hind limb dominant juveniles, a change that was precipitated by decreases in peak vertical forelimb forces and increases in peak vertical hind limb forces. Results provided some support for all three of the models, although the COM Position and Active Weight Shift models were most strongly supported by the data. Overall, this study suggests that primates may use a variety of biomechanical strategies to achieve hind limb dominance in limb force distribution.     

A three‐dimensional morphometric analysis of upper forelimb morphology in the enigmatic tapir (Perissodactyla: Tapirus) hints at subtle variations in locomotor ecology

Forelimb morphology is an indicator for terrestrial locomotor ecology. The limb morphology of the enigmatic tapir (Perissodactyla: Tapirus) has often been compared to that of basal perissodactyls, despite the lack of quantitative studies comparing forelimb variation in modern tapirs. Here, we present a quantitative assessment of tapir upper forelimb osteology using three‐dimensional geometric morphometrics to test whether the four modern tapir species are monomorphic in their forelimb skeleton. The shape of the upper forelimb bones across four species (T. indicus; T. bairdii; T. terrestris; T. pinchaque) was investigated. Bones were laser scanned to capture surface morphology and 3D landmark analysis was used to quantify shape. Discriminant function analyses were performed to reveal features which could be used for interspecific discrimination. Overall our results show that the appendicular skeleton contains notable interspecific differences. We demonstrate that upper forelimb bones can be used to discriminate between species (>91% accuracy), with the scapula proving the most diagnostic bone (100% accuracy). Features that most successfully discriminate between the four species include the placement of the cranial angle of the scapula, depth of the humeral condyle, and the caudal deflection of the olecranon. Previous studies comparing the limbs of T. indicus and T. terrestris are corroborated by our quantitative findings. Moreover, the mountain tapir T. pinchaque consistently exhibited the greatest divergence in morphology from the other three species. Despite previous studies describing tapirs as functionally mediportal in their locomotor style, we find osteological evidence suggesting a spectrum of locomotor adaptations in the tapirs. We conclude that modern tapir forelimbs are neither monomorphic nor are tapirs as conserved in their locomotor habits as previously described. J. Morphol. 277:1469–1485, 2016. © 2016 Wiley Periodicals, Inc.