Pelvic girdle mobility of cryptodire and pleurodire turtles during walking and swimming

Abstract

Movements of the pelvic girdle facilitate terrestrial locomotor performance in a wide range of vertebrates by increasing hind limb excursion and stride length. The extent to which pelvic movements contribute to limb excursion in turtles is unclear because the bony shell surrounding the body presents a major obstacle to their visualization. In the Cryptodira, which are one of the two major lineages of turtles, pelvic anatomy indicates the potential for rotation inside the shell. However, in the Pleurodira, the other major suborder, the pelvis shows a derived fusion to the shell, preventing pelvic motion. In addition, most turtles use their hind limbs for propulsion during swimming as well as walking, and the different locomotor demands between water and land could lead to differences in the contributions of pelvic rotation to limb excursion in each habitat. To test these possibilities, we used X-ray reconstruction of moving morphology (XROMM) to compare pelvic mobility and femoral motion during walking and swimming between representative species of cryptodire (Pseudemys concinna) and pleurodire (Emydura subglobosa) turtles. We found that the pelvis yawed substantially in cryptodires during walking and, to a lesser extent, during swimming. These movements contributed to greater femoral protraction during both walking and swimming in cryptodires when compared with pleurodires. Although factors related to the origin of pelvic-shell fusion in pleurodires are debated, its implications for their locomotor function may contribute to the restriction of this group to primarily aquatic habits.

“On the Fence” versus “All in”: Insights from Turtles for the Evolution of Aquatic Locomotor Specializations and Habitat Transitions in Tetrapod Vertebrates

“…Though it might have been expected that the femur would rotate about its long axis to contribute to this rotation of the foot during swimming strokes, our strain measurements indicate that, instead, axial rotation must be concentrated in the distal limb, because femoral twisting is drastically reduced in water (Young and Blob 2015a). Our subsequent studies have, in fact, confirmed this inference through X-ray based analyses of femoral kinematics (Mayerl et al 2016). Such reduction of twisting in the proximal limb bones of rowing swimmers could have facilitated the evolution of hydrodynamically advantageous limb bone flattening (Young and Blob 2015a).…”

“…Measurements of forelimb loading during swimming could provide useful perspective for understanding how loading influences the skeletal design of swimming tetrapods (Young and Blob 2015b). In addition, our XROMM data comparing pelvic mobility between cryptodiran and pleurodiran turtles (Mayerl et al 2016) sets the stage for direct comparisons of aquatic stability and maneuverability between these lineages (Mayerl et al 2015).…”

“…We are currently pursuing such studies through comparisons of aquatic and terrestrial locomotion between cryptodiran and pleurodiran turtles (Mayerl et al 2016). These clades represent the primary phylogenetic division among extant turtle lineages (Barley et al 2010), and their species differ in their most common locomotor habitat.…”

“…To begin assessing how structural differences between cryptodires and pleurodires might relate to their differing degrees of specialization for aquatic locomotion, we used marker-based X-ray Reconstruction of Moving Morphology (XROMM: Brainerd et al 2010) to compare pelvic mobility and femoral motion during walking and swimming between representative species of cryptodire (Pseudemys concinna) and pleurodire (Emydura subglobossa) turtles that both regularly inhabit aquatic environments (Mayerl et al 2016). The pelvis, femur, and shell of each individual were implanted with radio-opaque beads, and animals were filmed during swimming and walking using biplanar X-ray video.…”

“…4). These differences in pelvic movement also contributed to cryptodires having greater femoral protraction in both walking and swimming when compared to pleurodires (Mayerl et al 2016). In light of these results, we are now pursuing comparisons of hydrodynamic stability and maneuverability between these taxa, to evaluate if the functional consequences of this structural feature might enhance an aspect of pleurodire locomotor performance that facilitated their specialization for aquatic habitats (Mayerl et al 2015).…”