Hindlimb muscle function in turtles: is novel skeletal design correlated with novel muscle function?

Abstract

Variations in musculoskeletal lever systems have formed an important foundation for predictions about the diversity of muscle function and organismal performance. Changes in the structure of lever systems may be coupled with changes in muscle use and give rise to novel muscle functions. The two extant turtle lineages, cryptodires and pleurodires, exhibit differences in hindlimb structure. Cryptodires possess the ancestral musculoskeletal morphology, with most hip muscles originating on the pelvic girdle, which is not fused to the shell. In contrast, pleurodires exhibit a derived morphology, in which fusion of the pelvic girdle to the shell has resulted in shifts in the origin of most hip muscles onto the interior of the shell. To test how variation in muscle arrangement might influence muscle function during different locomotor behaviors, we combined measurements of muscle leverage in five major hindlimb muscles with data on muscle use and hindlimb kinematics during swimming and walking in representative semiaquatic cryptodire () and pleurodire () species. We found substantial differences in muscle leverage between the two species. Additionally, we found that there were extensive differences in muscle use in both species, especially while walking, with some pleurodire muscles exhibiting novel functions associated with their derived musculoskeletal lever system. However, the two species shared similar overall kinematic profiles within each environment. Our results suggest that changes in limb lever systems may relate to changes in limb muscle motor patterns and kinematics, but that other factors must also contribute to differences in muscle activity and limb kinematics between these taxa.

The impact of keels and tails on turtle swimming performance and their potential as models for biomimetic design

“…Comparative studies of keel function in animals have produced varied results: while some have found that keels improve stability and hydrodynamic performance [4, 22,23,34], others have failed to find that keels decrease body oscillations [52]. Such differences in the results across studies might arise from other features of body shape that were not controlled for in our comparisons, such as subtle differences in keel shape between our structures and those found in nature, as well as possible differences in the lateral margins of the turtle carapace that are associated with keels, or the kinematic patterns that freshwater turtles use relative to fishes [53][54][55]. In addition, whereas our study focused on how intrinsic perturbations arising from limb movements during linear swimming impacted performance, it is possible that keels may, instead, have a greater effect on stability when animals are recovering from extrinsic perturbations.…”

Central pattern generators in the turtle spinal cord: selection among the forms of motor behaviors

“…EMG motor patterns for terrestrial forward locomotion (walking) share some features with EMG motor patterns for the three forms of scratch and the two forms of swimming, including rhythmic alternation between hip-flexor and hip-extensor activities (Earhart and Stein 2000b;Mayerl et al 2017). The timing of the monoarticular knee extensor during walking is particularly interesting in that it fires in two distinct bursts during the step cycle, once during hip flexion and a second time during hip extension.…”

“…Turtle hindlimb musculature has been well described (Mayerl et al 2017;Walker 1973). Muscles that have received special attention in studies (Bakker and Crowe 1982;Robertson et al 1985;Stein and Daniels-McQueen 2003) are 1) the hip flexor, also called hip protractor, VP-HP, puboischiofemoralis internus, pars anteroventralis; 2) the hip extensor, also called hip retractor, HR-KF, flexor cruris, pars flexor tibialis internus; 3) the monoarticular knee extensor, FT-KE, triceps femoris, pars femorotibialis; 4) the biarticular knee extensor and hip adductor, AM-KE, triceps femoris, pars ambiens; 5) the biarticular knee extensor, hip abductor, and hip flexor, IT-KE, triceps femoris, pars iliotibialis; and 6) the knee flexor, ILFIB, iliofibularis.…”

“…Future studies of turtle hindlimb locomotor behaviors. Redeared turtles are semiaquatic and produce a wide variety of locomotor behaviors (Blob et al 2008;Earhart and Stein 2000b;Mayerl et al 2017;Rivera and Blob 2010;Rivera et al 2006;Walker 1979;Welch and Currie 2014;Zug 1971). They locomote gracefully in water during forward swims, turning swims, and backward swims.…”

Forelimb muscle activation patterns in American alligators: Insights into the evolution of limb posture and powered flight in archosaurs

“…In addition to soft tissue anatomy, muscle activation patterns can only be measured in living animals through electromyography (EMG), which provides insights into the timing, intensity, and frequency of myoelectric signals across a range of speed and locomotor modes employed by an animal (Blob et al., 2008; Cappellini et al., 2006; Foster & Higham, 2014; Gatesy, 1994, 1997; Gorvet et al., 2020; Loeb & Gans, 1986; Mayerl et al., 2017; Rivera & Blob, 2010; von Tscharner, 2000; Wakeling et al., 2002). With regard to shifts in posture, a comparison of hindlimb muscle activation in American alligators showed increases in the activation of knee and ankle extensors when assuming a more upright limb posture (Reilly & Blob, 2003).…”