Mechanics of limb bone loading during terrestrial locomotion in river cooter turtles (Pseudemys concinna)

Studies of limb bone loading during terrestrial locomotion have focused primarily on birds and mammals. However, data from a broader functional and phylogenetic range of species are critical for understanding the evolution of limb bone function and design. Turtles are an interesting lineage in this context. Although their slow walking speeds and robust limb bones might lead to low locomotor forces and limb bone stresses similar to other non-avian reptiles, their highly sprawled posture could produce high bending loads, leading to high limb bone stresses similar to those of avian and mammalian species, as well as high torsion. To test between these possibilities, we evaluated stresses experienced by the femur of river cooter turtles (Pseudemys concinna) during terrestrial walking by synchronizing measurements of three-dimensional joint kinematics and ground reaction forces (GRFs) during isolated hindlimb footfalls. Further, we evaluated femoral safety factors for this species by comparing our locomotor stress calculations with the results of mechanical property tests. The net GRF magnitude at peak tensile bone stress averaged 0.35 BW (body weight) and was directed nearly vertically for the middle 40–65% of the contact interval, essentially orthogonal to the femur. Peak bending stresses experienced by the femur were low (tensile: 24.9±9.0 MPa; compressive: –31.1±9.1 MPa) and comparable to those in other reptiles, yet peak shear stresses were higher than those in other reptiles, averaging 13.7±4.2 MPa. Such high torsion is present despite cooters lacking a large tail, a feature that has been hypothesized to contribute to torsion in other reptiles in which the tail is dragged along the ground. Comparison of femoral stresses to measurements of limb bone mechanical properties in cooters indicates safety factors to yield of 13.9 in bending and 6.3 in torsion, considerably higher than values typical for birds and mammals, and closer to the elevated values calculated for other reptile species. Thus, not only do turtle limb bones seem considerably `over-designed\u27 for resisting the loads that they encounter, but comparisons of bone loading across tetrapod lineages are consistent with the hypothesis that low limb bone loads, elevated torsion and high safety factors may be primitive features of limb bone design

In vivo locomotor strain in the hind limb bones of Alligator mississipiensis and Iguana iguana: implications for the evolution of limb bone safety factor and non-sprawling limb posture.

Limb postures of terrestrial tetrapods span a continuum from sprawling to fully upright; however, most experimental investigations of locomotor mechanics have focused on mammals and ground-dwelling birds that employ parasagittal limb kinematics, leaving much of the diversity of tetrapod locomotor mechanics unexplored. This study reports measurements of in vivo locomotor strain from the limb bones of lizard (Iguana iguana) and crocodilian (Alligator mississippiensis) species, animals from previously unsampled phylogenetic lineages with non-parasagittal limb posture and kinematics. Principal strain orientations and shear strain magnitudes indicate that the limb bones of these species experience considerable torsion during locomotion. This contrasts with patterns commonly observed in mammals, but matches predictions from kinematic observations of axial rotation in lizard and crocodilian limbs. Comparisons of locomotor load magnitudes with the mechanical properties of limb bones in Alligator and Iguana indicate that limb bone safety factors in bending for these species range from 5.5 to 10.8, as much as twice as high as safety factors previously calculated for mammals and birds. Limb bone safety factors in shear (3.9-5.4) for Alligator and Iguana are also moderately higher than safety factors to yield in bending for birds and mammals. Finally, correlations between limb posture and strain magnitudes in Alligator show that at some recording locations limb bone strains can increase during upright locomotion, in contrast to expectations based on size-correlated changes in posture among mammals that limb bone strains should decrease with the use of an upright posture. These data suggest that, in some lineages, strain magnitudes may not have been maintained at constant levels through the evolution of a non-sprawling posture unless the postural change was accompanied by a shift to parasagittal kinematics or by an evolutionary decrease in body size

Mechanics of limb bone loading during terrestrial locomotion in the green iguana (Iguana iguana) and American alligator (Alligator mississippiensis)

In vivo measurements of strain in the femur and tibia of Iguana iguana (Linnaeus) and Alligator mississippiensis (Daudin) have indicated three ways in which limb bone loading in these species differs from patterns observed in most birds and mammals: (i) the limb bones of I. iguana and A. mississippiensis experience substantial torsion, (ii) the limb bones of I. iguana and A. mississippiensis have higher safety factors than those of birds or mammals, and (iii) load magnitudes in the limb bones of A. mississippiensis do not decrease uniformly with the use of a more upright posture. To verify these patterns, and to evaluate the ground and muscle forces that produce them, we collected three-dimensional kinematic and ground reaction force data from subadult I. iguana and A. mississippiensis using a force platform and high-speed video. The results of these force/kinematic studies generally confirm the loading regimes inferred from in vivo strain measurements. The ground reaction force applies a torsional moment to the femur and tibia in both species; for the femur, this moment augments the moment applied by the caudofemoralis muscle, suggesting large torsional stresses. In most cases, safety factors in bending calculated from force/video data are lower than those determined from strain data, but are as high or higher than the safety factors of bird and mammal limb bones in bending. Finally, correlations between limb posture and calculated stress magnitudes in the femur of I. iguana confirm patterns observed during direct bone strain recordings from A. mississippiensis: in more upright steps, tensile stresses on the anterior cortex decrease, but peak compressive stresses on the dorsal cortex increase. Equilibrium analyses indicate that bone stress increases as posture becomes more upright in saurians because the ankle and knee extensor muscles exert greater forces during upright locomotion. If this pattern of increased bone stress with the use of a more upright posture is typical of taxa using non-parasagittal kinematics, then similar increases in load magnitudes were probably experienced by lineages that underwent evolutionary shifts to a non-sprawling posture. High limb bone safety factors and small body size in these lineages could have helped to accommodate such increases in limb bone stress

In vivo strains in the femur of river cooter turtles (Pseudemys concinna) during terrestrial locomotion: tests of force-platform models of loading mechanics

Previous analyses of ground reaction force (GRF) and kinematic data from river cooter turtles (Pseudemys concinna) during terrestrial walking led to three primary conclusions about the mechanics of limb bone loading in this lineage: (1) the femur was loaded in a combination of axial compression, bending and torsion, similar to previously studied non-avian reptiles, (2) femoral shear stresses were high despite the possession of a reduced tail in turtles that does not drag on the ground and (3) stress-based calculations of femoral safety factors indicated high values in bending and torsion, similar to other reptiles and suggesting that substantial `overbuilding\u27 of limb bones could be an ancestral feature of tetrapods. Because force-platform analyses produce indirect estimates of bone loading, we sought to validate these conclusions by surgically implanting strain gauges on turtle femora to directly measure in vivo strains during terrestrial walking. Strain analyses verified axial compression and bending as well as high torsion in turtle femora, with peak axial strains comparable to those of other non-avian reptiles at similar walking speeds but higher peak shear strains approaching 2000 μϵ. Planar strain analyses showed patterns of neutral axis (NA) of femoral bending orientations and shifting generally consistent with our previous force-platform analyses of bone stresses, tending to place the anterior and dorsal aspects of the femur in tension and verifying an unexpected pattern from our force studies that differs from patterns in other non-avian reptiles. Calculated femoral safety factors were 3.8 in torsion and ranged from 4.4 to 6.9 in bending. Although these safety factors in bending were lower than values derived from our stress-based calculations, they are similar to strain-based safety factors calculated for other non-avian reptiles in terrestrial locomotion and are still high compared with safety factors calculated for limb bones of birds and mammals. These findings are consistent with conclusions drawn from our previous models of limb bone stresses in turtles and suggest that not only are turtle limb bones `overbuilt\u27 in terms of resisting the loads that they experience during locomotion but also, across tetrapod lineages, elevated torsion and high limb bone safety factors may be primitive features of limb bone design

Hindlimb function in the alligator: integrating movements, motor patterns, ground reaction forces and bone strain of terrestrial locomotion

Alligator hindlimbs show high torsional loads during terrestrial locomotion, in sharp contrast to the bending or axial compressive loads that predominate in animals that use parasagittal limb movements. The present study integrates new data on hindlimb muscle function with previously obtained data on hindlimb kinematics, motor patterns, ground reaction forces and bone strain in order to (1) assess mechanisms underlying limb bone torsion during non-parasagittal locomotion in alligators and (2) improve understanding of hindlimb dynamics during terrestrial locomotion. Three dynamic stance phase periods were recognized: limb-loading, support-and-propulsion, and limb-unloading phases. Shear stresses due to torsion were maximized during the limb-loading phase, during which the ground reaction force (GRF) and caudofemoralis (CFL) muscles generated opposing moments about the femur. Hindlimb retraction during the subsequent stance-and-propulsion phase involves substantial medial rotation of the femur, powered largely by coordinated action of the GRF and CFL. Several muscles that actively shorten to flex and extend limb joints during stance phase in sprawling and erect quadrupeds act in isometric or even eccentric contraction in alligators, stabilizing the knee and ankle during the support-and-propulsion phase. Motor patterns in alligators reveal the presence of local and temporal segregation of muscle functions during locomotion with muscles that lie side by side dedicated to performing different functions and only one of 16 muscles showing clear bursts of activity during both stance and swing phases. Data from alligators add to other recent discoveries that homologous muscles across quadrupeds often do not move joints the same way as is commonly assumed. Although alligators are commonly considered models for early semi-erect tetrapod locomotion, many aspects of hindlimb kinematics, muscle activity patterns, and femoral loading patterns in alligators appear to be derived in alligators rather than reflecting an ancestral semi-erect condition

Functional Relationship between Skull Form and Feeding Mechanics in Sphenodon, and Implications for Diapsid Skull Development

The vertebrate skull evolved to protect the brain and sense organs, but with the appearance of jaws and associated forces there was a remarkable structural diversification. This suggests that the evolution of skull form may be linked to these forces, but an important area of debate is whether bone in the skull is minimised with respect to these forces, or whether skulls are mechanically “over-designed” and constrained by phylogeny and development. Mechanical analysis of diapsid reptile skulls could shed light on this longstanding debate. Compared to those of mammals, the skulls of many extant and extinct diapsids comprise an open framework of fenestrae (window-like openings) separated by bony struts (e.g., lizards, tuatara, dinosaurs and crocodiles), a cranial form thought to be strongly linked to feeding forces. We investigated this link by utilising the powerful engineering approach of multibody dynamics analysis to predict the physiological forces acting on the skull of the diapsid reptile Sphenodon. We then ran a series of structural finite element analyses to assess the correlation between bone strain and skull form. With comprehensive loading we found that the distribution of peak von Mises strains was particularly uniform throughout the skull, although specific regions were dominated by tensile strains while others were dominated by compressive strains. Our analyses suggest that the frame-like skulls of diapsid reptiles are probably optimally formed (mechanically ideal: sufficient strength with the minimal amount of bone) with respect to functional forces; they are efficient in terms of having minimal bone volume, minimal weight, and also minimal energy demands in maintenance

Intra- and inter-specific morphological diversity of amphidromous gobies influences waterfall-climbing performance

The morphology of an individual can affect functional performance and, ultimately, survival and fitness. To study these links, a first step is to evaluate the relationship between morphology and performance. Sicydiine fishes are an interesting model for such studies, because successful completion of their life cycle depends on a functionally demanding task: climbing waterfalls when they return to freshwater from the ocean. Previous studies identified two different climbing modes among sicydiines: 'inching' and 'powerburst'. Relationships between morphology and climbing performance have been found for inching and powerburst species present on different islands from distant oceans (Pacific and Caribbean), but species from the same island have not been compared. In this study, we challenged two different sicydiine species from Reunion Island to an artificial climbing ramp: the inching climber Sicyopterus lagocephalus and the powerburst climber Cotylopus acutipinnis. For each species, we evaluated differences in morphology between successful and unsuccessful climbers. We predicted that species with similar climbing styles (S. lagocephalus and S. stimpsoni) would show differences between successful and unsuccessful climbers that more closely resembled each other than differences between successful and unsuccessful climbers across species from the same island (S. lagocephalus and C. acutipinnis). This prediction was only partially met. S. lagocephalus individuals with a streamlined body showed better climbing performance, as observed for S. stimpsoni. However, the size of the pelvic sucker, which fish use to attach to the substrate while resting, appeared less important for S. lagocephalus than for S. stimpsoni and C. acutipinnis. Instead, the size of the mouth, which inching species use to attach to the substrate while moving up, seemed important for S. lagocephalus but not for other species. Thus, differences in the morphology-performance relationship among sicydiines may relate not only to differences in climbing mode, but also to species-specific specializations within each climbing mode