Human beings have been credited with unparalleled capabilities for digital prehension grasping. However, grasping behaviour is widespread among tetrapods. The propensity to grasp, and the anatomical characteristics that underlie it, appear in all of the major groups of tetrapods with the possible exception of terrestrial turtles. Although some features are synapomorphic to the tetrapod clade, such as well-defined digits and digital musculature, other features, such as opposable digits and tendon configurations, appear to have evolved independently in many lineages. Here we examine the incidence, functional morphology, and evolution of grasping across four major tetrapod clades. Our review suggests that the ability to grasp with the manus and pes is considerably more widespread, and ecologically and evolutionarily important, than previously thought. The morphological bases and ecological factors that govern grasping abilities may differ among tetrapods, yet the selective forces shaping them are likely similar. We suggest that further investigation into grasping form and function within and among these clades may expose a greater role for grasping ability in the evolutionary success of many tetrapod lineages.
Frogs are characterized by a unique morphology associated with their saltatory lifestyle. Although variation in the form and function of the pelvic girdle and associated appendicular system related to specialized locomotor modes such as swimming or burrowing has been documented, the forelimbs have typically been viewed as relatively unspecialized. Yet, previous authors have noted versatility in forelimb function among arboreal frogs associated with feeding. Here we study the morphology and function of the forelimb and hand during locomotion in two species of arboreal frogs ( Litoria caerulea and Phyllomedusa bicolor ). Our data show a complex arrangement of the distal forelimb and hand musculature with some notable differences between species. Analyses of high-speed video and video fluoroscopy recordings show that forelimbs are used in alternating fashion in a diagonal sequence footfall pattern and that the position of the hand is adjusted when walking on substrates of different diameters. Electromyographic recordings show that the flexors of the hand are active during substrate contact, suggesting the use of gripping to generate a stabilizing torque. Measurements of grasping forces in vivo and during stimulation experiments show that both species, are capable of executing a so-called power grip but also indicates marked differences between species, in the magnitude of forces generated. Stimulation experiments showed an increased control of digit flexion in the more specialized of the two species, allowing it to execute a precision grip paralleled only by that seen in primates.
In lizards, distinct patterns of the tendinous structures associated with the forearm flexors have been described. In most lizards, the m. flexor digitorum longus ends in a tendinous plate with an embedded sesamoid, from which tendons run to the terminal phalanx of each digit. This structure is known as the flexor plate. In many polychrotid lizards, however, the flexor digitorum longus muscle is continuous with individual tendons running to each digit, and no complete flexor plate is present. In most geckos, the flexor plate is reduced to a tendinous plate without sesamoid. To evaluate the consequences of these differences in morphology on locomotion and grasping, we compared the use of the fore-arm and hand in lizards exhibiting three different tendon patterns (Pogona vitticeps, an agamid with a well-developed flexor plate; Gekko gecko, a gekkonid with a flexor plate, but without an embedded sesamoid; Anolis equestris, a polychrotid without flexor plate, but showing independent tendons running to each digit) while moving on different substrates. We found that the presence of a flexor plate with sesamoid bone prevents digital flexion and creates a rather stiff palmar surface in P. vitticeps. This configuration makes it impossible for P. vitticeps to grasp narrow branches and results in a strongly impaired locomotor performance on narrow substrates. Both G. gecko and A. equestris can flex the palms of their hands and their fingers more extensively, and do so when moving on narrow substrates. We suggest that the reduction of the flexor plate in both G. gecko and A. equestris allows these animals to move effectively on narrow substrates. Anat Rec, 292:842-853, 2009. V V C 2009 Wiley-Liss, Inc.Key words: flexor plate; forearm muscles; grasping hand; lizards; palmar sesamoid; tendons All limbed tetrapods have flexor tendons in the palmar surface of the manus that connect the muscles of the forearm with the digits. These tendons emerge from the superficial (m. flexor carpi ulnaris; m. flexor carpi radialis), and deeper (m. flexor digitorum longus) muscles of the forearm. Each layer (superficial and deep) of these skeletal muscles exerts its actions on the bones of the hand by means of an independent set of tendons (Davis, 1964). In lizards, however, only the m. flexor digitorum longus sends flexor tendons to the digits. This muscle flexes the digits via five strong tendons that generally
Intercalary elements are additional skeletal structures of digits of many anuran amphibians. Twelve terminal clades in the neobatrachian lineage of frogs have intercalary elements revealing it is a homoplastic character with five to seven gains and two to four losses along a consensus phylogeny of the Neobatrachia. We analyzed anatomical variation of intercalary elements, related structures (distal phalanges, tendons, and muscles), and articulations of digits of 45 anuran species, representing eight suprageneric terminal taxa. The intercalary elements are integrated in a complex system that is probably related to different types of movements, which are produced by a similar set of muscles and tendons with limited variation among the studied taxa. Species in the clades Hyloides and Ranoides show distinctive patterns of morphostructural features in their intercalary elements that are usually wedge-shaped and composed of hyaline cartilage in Ranoides, and biconcave and composed of embryonic cartilage in Hyloides. Features derived from the typical hyloid condition may only be interpreted in some Hylidae (Pseudis and Lysapsus) and Centrolenidae. In Ranoides, the described features of the intercalary elements are found in all taxa examined with the exception of Leptopelis, which have an intercalary element similar to the other Ranoides but formed by connective tissue. Several features are shared by all taxa having intercalary elements: (1) the intercalary elements differ from the phalanges by lacking terminal epiphyses, (2) they are present in hands and feet, and (3) they appear in all digits. This finding suggests that the genetic basis for presence of intercalary elements may be homologous in all these taxa and may have evolved only once early in neobatrachian history. Anat Rec,
We compared the muscular anatomy of the distal front limb in terrestrial and aquatic chelonians to test whether observed differences between the two groups are associated with their divergent lifestyles and locomotor modes. Given the different use of the forelimb in the two environments (body support and propulsion on land vs. mainly propulsion in water) we expected that: (1) aquatic and terrestrial turtles would show differences in their muscular anatomy, with aquatic species having more individualized muscle bundles to allow for the complex forearm movements observed during swimming, and (2) that terrestrial turtles would have more robust muscles to support their body weight against gravity. To address these questions, we examined the forelimb myology and associated tissues in six aquatic or semi-aquatic turtles ( Phyrnops hilarii , Podocnemis unifilis, Trachemys scripta , Sacalia bealei , Cuora amboinensis and Mauremys caspica ) and six terrestrial or semi-terrestrial turtles ( Geochelone chilensis , Testudo graeca , Cuora galbinifrons , Glyptemys insculpta , Terrapene carolina and Rhinoclemmys pulcherrima ). This paper describes the general structure of the forelimb musculature in all species, and quantifies muscle masses in those species with more than five specimens available ( Ph. hilarii , Po. unifilis and Ge. chilensis ). The general structure of the forelimb muscles in the strictly terrestrial species Ge. chilensis and Tes. graeca was found to be notably different from the pattern of the aquatic and semi-aquatic species examined, showing a distinct fusion of the different muscular bodies. Ter. carolina also show a distinctly terrestrial pattern, but a less extensive tendon development. R. pulcherrima and Gl. insculpta were found to be morphologically intermediate; in the geoemydids the strictly terrestrial bauplan never appears. Quantitative differences in the robustness or mass of the distal forelimb muscles were also observed for the species investigated, supporting our prediction that the extensor muscles are more robust in terrestrial turtles. However, in contrast to our expectations, not only the extensor muscles of the distal forelimb (which are crucial in providing both body support and propulsion), but all muscles acting around the wrist were found to be heavier in terrestrial turtles.
Although Pleurodiran turtles represent an important component of extant turtle radiation, our knowledge of the development and homology of limb bones in turtles rests mostly upon observations made on derived members of the Cryptodiran clade. Herein, we describe limb development in three pleurodirans: Podocnemis unifilis Troschel, 1848, Podocnemis sextuberculata Cornalia, 1849 and Phrynops hilarii (Dumeril and Bibron, 1835), in an effort to contribute to filling this anatomical gap. For earlier stages of limb development, we described the Y-shaped condensation that gave rise to the zeugopodial cartilages, and differentiation of the primary axis/digital arch that reveals the invariant pattern common to tetrapods. There are up to four central cartilaginous foci in the carpus, and the proximal tarsale is formed by the fusion of the fibulare, intermedium, and centrale 4. Digital development is similar for the five digits. Changes in toe V occur predominantly in the distal tarsale 5. Ontogenetic reduction of phalanges is observed in toe V of Podocnemis. Based on these results, we suggest that the hooked element present in the chelonian tarsus, and traditionally recognized as a modified fifth metatarsale, is actually the fifth distal tarsale. Additionally, our data on limb development of pleurodiran turtles supply more taxonomically comprehensive information to interpret limb configuration within the chelonian clade.
We present the ontogeny of the integrated musculoskeletal complex that comprises the pelvic girdle and hind limbs of anurans. Our histological data show that the pelvic girdle originates from a single mesenchymatic condensation. The tissue differentiation sequence is cartilage, muscle and tendon. The intrusion of the ischiadic nerve into the limb bud is produced very early in ontogeny. The pre‐cartilage appears in the pre‐motile stage. Therefore, the nerve produces a movement analogous to the ‘embryonic motility’ that would induce the emergence of the pre‐cartilage. The acetabulum is the first of all cavitation processes to form, the second one being the knee. The acetabulum appears before the muscles are mature, although it has been stressed that the muscle contraction maintains joint progenitors committed to their fate. Our data indicate an explosive differentiation of all 11 muscular masses together. We provide three new characters that support the monophyly of Hyloides, Acosmanura and Neobatrachia.
SUMMARYFrogs are characterized by a unique morphology associated with their saltatory lifestyle. Yet, arboreal species show morphological specializations relative to other ecological specialists allowing them to hold on to narrow substrates. However, almost nothing is known about the effects of substrate characteristics on locomotion in frogs. Here, we quantified the 3D kinematics of forelimb movement for frogs moving across branches of different diameters (1 and 40mm) and two different inclines (horizontal and 45deg uphill). Our results show that grip types differ while moving across substrates of different diameters and inclines. The kinematics of the wrist, elbow and shoulder as well as the body position relative to the substrate also showed significant effects of individual, diameter and incline. Kinematic differences involved duration, velocity of movement and angular excursions. Differences were most pronounced for the proximal joints of the forelimb and effects for substrate diameter were greater than for incline. Interestingly, the effects of diameter and incline on both grip type and kinematics are similar to what has been observed for lizards and primates, suggesting that the mechanics of narrow substrate locomotion drive the kinematics of movement independent of morphology and phylogeny.
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