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

Abstract

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.

MUSCULAR ANATOMY OF THE PECTORAL AND FORELIMB OF Caiman crocodilus crocodilus (LINNAEUS, 1758) (CROCODYLIA: ALLIGATORIDAE)

“…Howell (30) , Meers, (24) and Romão et al (23) described one short and another long muscle in crocodilians, but some authors defended that the reptile present a single muscle. Diogo et al (21) described a single extensor carpi radialis (brevis), but with three heads (superficialis, profundus and supinator) as in testudines, lepdosauria and amphibians, (25,26,31) except for some variations. Meers (24) reported that crocodilians present two discrete heads for the extensor carpi radialis brevis muscle (pars radialis and pars ulnaris), both described in C. latirostris, (23) and C. crocodilus crocodilus; however, with a slight variation in the insertion points.…”

Myology of the forelimb of Majungasaurus crenatissimus (Theropoda, Abelisauridae) and the morphological consequences of extreme limb reduction

“…If this muscle has not been lost, the only other location for its insertion is on the distal radius, as it is in some turtles (Abdala et al. ) and teiid lizards with reduced forelimbs (Abdala et al. ).…”

Ontogenetic Scaling of the Humerus in Sea Turtles and Its Implications for Locomotion

“…In water, the limbs are no longer used for body support and are mainly utilized for propulsion (Fish, 2000;Abdala et al, 2008). Both juvenile and adult sea turtles perform simultaneous beating of their flippers in water, similar to the aquatic locomotor pattern of penguins (Alexander, 2003;Davenport et al, 1984;Wyneken, 1997).…”

“…During terrestrial locomotion, the limbs must provide support against gravity, in addition to providing the propulsive forces for forward locomotion (Miller et al, 2008;Zani et al, 2005). In aquatic environments, however, the limbs are mainly utilized for propulsion, not for body support (Fish, 2000;Abdala et al, 2008). Therefore, ontogenetic scaling of the limbs of animals should be considered in relation to locomotion under the prevailing physical conditions.…”