Members of several terrestrial vertebrate lineages have returned to nearly exclusive use of aquatic habitats. These transitions were often accompanied by changes in skeletal morphology, such as flattening of limb bone shafts. Such morphological changes might be correlated with the exposure of limb bones to altered loading. Though the environmental forces acting on the skeleton differ substantially between water and land, no empirical data exist to quantify the impact of such differences on the skeleton, either in terms of load magnitude or regime. To test how locomotor loads change between water and land, we compared in vivo strains from femora of turtles (Trachemys scripta) during swimming and terrestrial walking. As expected, strain magnitudes were much lower (by 67.9%) during swimming than during walking. However, the loading regime of the femur also changed between environments: torsional strains are high during walking, but torsion is largely eliminated during swimming. Changes in loading regime between environments may have enabled evolutionary shifts to hydrodynamically advantageous flattened limb bones in highly aquatic species. Although circular cross sections are optimal for resisting torsional loads, the removal of torsion would reduce the advantage of tubular shapes, facilitating the evolution of flattened limbs.
During evolutionary reinvasions of water by terrestrial vertebrates, ancestrally tubular limb bones often flatten to form flippers. Differences in skeletal loading between land and water might have facilitated such changes. In turtles, femoral shear strains are significantly lower during swimming than during walking, potentially allowing a release from loads favoring tubular shafts. However, flipper-like morphology in specialized tetrapod swimmers is most accentuated in the forelimbs. To test whether the forelimbs of turtles also experience reduced torsional loading in water, we compared strains on the humerus of river cooters () between swimming and terrestrial walking. We found that humeral shear strains are also lower during swimming than during terrestrial walking; however, this appears to relate to a reduction in overall strain magnitude, rather than a specific reduction in twisting. These results indicate that shear strains show similar reductions between swimming and walking for forelimb and hindlimb, but these reductions are produced through different mechanisms.
Synopsis Though ultimately descended from terrestrial amniotes, turtles have deep roots as an aquatic lineage and are quite diverse in the extent of their aquatic specializations. Many taxa can be viewed as ''on the fence'' between aquatic and terrestrial realms, whereas others have independently hyperspecialized and moved ''all in'' to aquatic habitats. Such differences in specialization are reflected strongly in the locomotor system. We have conducted several studies to evaluate the performance consequences of such variation in design, as well as the mechanisms through which specialization for aquatic locomotion is facilitated in turtles. One path to aquatic hyperspecialization has involved the evolutionary transformation of the forelimbs from rowing, tubular limbs with distal paddles into flapping, flattened flippers, as in sea turtles. Prior to the advent of any hydrodynamic advantages, the evolution of such flippers may have been enabled by a reduction in twisting loads on proximal limb bones that accompanied swimming in rowing ancestors, facilitating a shift from tubular to flattened limbs. Moreover, the control of flapping movements appears related primarily to shifts in the activity of a single forelimb muscle, the deltoid. Despite some performance advantages, flapping may entail a locomotor cost in terms of decreased locomotor stability. However, other morphological specializations among rowing species may enhance swimming stability. For example, among highly aquatic pleurodiran turtles, fusion of the pelvis to the shell appears to dramatically reduce motions of the pelvis compared to freshwater cryptodiran species. This could contribute to advantageous increases in aquatic stability among predominantly aquatic pleurodires. Thus, even within the potential constraints of a body plan in which the body is encased by a shell, turtles exhibit diverse locomotor capacities that have enabled diversification into a wide range of aquatic habitats.
Habitats vary in temperature both spatially and temporally. Variation in thermal habitat introduces challenges to organisms and may reduce fitness unless organisms can physiologically adjust to such changes. Theory predicts that thermal variability should influence the capacity for acclimation such that increased variation should favor a reduction in the thermal sensitivity of physiological traits. In this study, we investigated acclimation to constant and variable conditions in populations of the salamander Desmognathus brimleyorum from the Ouachita Mountains of Arkansas, USA. We exposed salamanders to constant and variable temperature regimes for 8 weeks in the laboratory. We then tested salamanders for acclimation of thermal tolerance, and the thermal sensitivities of swimming performance and standard metabolic rate. Our results indicate limited capacity for thermal acclimation to constant and variable conditions in D. brimleyorum. Instead, variation in physiological traits is dominated by differences among populations. Population differences do not appear to be correlated with observed variation in the thermal conditions of the streams, but are likely a consequence of structural and ecological differences. Due to the mixed support for theoretical predictions for acclimation to alternative environments, further consideration should be given to revising and expanding current theoretical models.
Specialization for a new habitat often entails a cost to performance in the ancestral habitat. Although aquatic lifestyles are ancestral among extant cryptodiran turtles, multiple lineages, including tortoises (Testudinidae) and emydid box turtles (genus Terrapene), independently specialized for terrestrial habitats. To what extent is swimming function retained in such lineages despite terrestrial specialization? Because tortoises diverged from other turtles over 50 Ma, but box turtles did so only 5 Ma, we hypothesized that swimming kinematics for box turtles would more closely resemble those of aquatic relatives than those of tortoises. To test this prediction, we compared high-speed video of swimming Russian tortoises (Testudo horsfieldii), box turtles (Terrapene carolina) and two semi-aquatic emydid species: sliders (Trachemys scripta) and painted turtles (Chrysemys picta). We identified different kinematic patterns between limbs. In the forelimb, box turtle strokes most resemble those of tortoises; for the hindlimb, box turtles are more similar to semi-aquatic species. Such patterns indicate functional convergence of the forelimb of terrestrial species, whereas the box turtle hindlimb exhibits greater retention of ancestral swimming motions.
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