Adriana S. Manzano

Getting a grip on tetrapod grasping: form, function, and evolution

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.

Morphology and function of the forelimb in arboreal frogs: specializations for grasping ability?

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.

The Tendinous Patterns in the Palmar Surface of the Lizard Manus: Functional Consequences for Grasping Ability

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.

The distal forelimb musculature in aquatic and terrestrial turtles: phylogeny or environmental constraints?

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.

Intercalary Elements, Treefrogs, and the Early Differentiation of a Complex System in the Neobatrachia

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, 2007.

The effect of substrate diameter and incline on locomotion in an arboreal frog

SUMMARY Frogs 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 40 mm) and two different inclines (horizontal and 45 deg 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.

Anuran Locomotion: Ontogeny and Morphological Variation of a Distinctive Set of Muscles

Adult morphological variation of muscles originating on the iliac shaft (M. iliacus externus, M. internus, and tensor fasciae latae) and vertebrae (M. longissimus dorsi, M. coccygeosacralis, and M. coccygeoiliacus) that are involved in postmetamorphic anuran locomotion was recorded in 41 neobatrachians and coded in 13 more based on the literature, for a total of 54 anuran species. In addition, we explored the spatial and temporal sequences in the ontogeny of these set of muscles from larval series of 19 neobatrachians whose adults differ in locomotion and lifestyle. Our findings suggest that: (1) jumping, swimming, and/or walking are capabilities that could have been achieved from novelties of limbs and protractor muscles of the femur rather than from changes in the axial musculoskeletal system; (2) the initial ontogenetic phase of the locomotion comprises the capability to escape, when the tail is still present; (3) the secondary phase of locomotion comprises changes in the axial skeleton and muscles integrated to the pelvis and might develop simultaneously with the new feeding mechanism of the recently metamorphosed frog.

The Tropical Tortoise Chelonoidis denticulata (Testudines: Testudinidae) from the Late Pleistocene of Argentina and Its Paleoclimatological Implications

Fil: Manzano, Adriana Silvina. Consejo Nacional de Investigaciones Cientificas y Tecnicas; Argentina. Universidad Autonoma de Entre Rios; Argentina

Does the Morphology of the Forelimb Flexor Muscles Differ Between Lizards Using Different Habitats?: HABITAT USE AND FORELIMB FLEXOR MUSCLES IN LIZARDS

Lizards are an interesting group to study how habitat use impacts the morphology of the forelimb because they occupy a great diversity of ecological niches. In this study, we specifically investigated whether habitat use impacts the morphology of the forelimb flexor muscles in lizards. To do so, we performed dissections and quantified the physiological cross sectional area (PCSA), the fiber length, and the mass of four flexor muscles in 21 different species of lizards. Our results show that only the PCSA of the m. flexor carpi radialis is different among lizards with different ecologies (arboreal versus non‐arboreal). This difference disappeared, however, when taking phylogeny into account. Arboreal species have a higher m. flexor carpi radialis cross sectional area likely allowing them to flex the wrist more forcefully which may allow them climb and hold on to branches better. In contrast, other muscles are not different between arboreal and non‐arboreal species. Further studies focusing on additional anatomical features of the lizard forelimb as well as studies documenting how lizards use the arboreal niche are needed to fully understand how an arboreal life style may constrain limb morphology in lizards. Anat Rec, 301:424–433, 2018.

Muscle Development in the Abdominal Region of Larval Hylidae (Amphibia: Anura)

Larval muscle development in the abdominal region of five species of hylid frogs (Scinax nasicum, S. fuscovarium, Hyla andina, Phyllomedusa boliviana, Gastrotheca gracilis) was studied using differential staining techniques. These five species represent three major hylid subfamilies. The development of the main abdominal muscles, the rectus abdominis, the two lateral muscles (obliquus externus and transversus), and the lateral pectoralis abdominalis is described. The number of myotomes of the rectus abdominis varies between five and six, and the abdominal muscles associated with the rectus abdominis (obliquus externus, pectoralis abdominalis, and rectus cervicis) vary interspecifically in time of appearance and configuration. The presence of gaps in the configuration of the rectus abdominis has been related to the lotic habits of the larvae. However, our observations indicate the presence of such gaps in larvae that inhabit lentic environments as well. These results suggest that the presence of these gaps is unrelated to larval habitat. There are relatively small differences in muscle morphology among these closely related species, which apparently cannot be explained by morphological adaptations related to their ecology. In the species studied, the number of elements that form the abdominal musculature in larvae is equal to that observed in adults. Likewise, the general morphology of the muscles is ontogenetically conserved. This suggests that both the axial skeleton and musculature are more ontogenetically conserved in relation to the substantial changes that are observed in the skull and head muscles of developing anurans. J. Morphol. 241:275–282, 1999.