Terrestrial feeding in aquatic turtles: environment-dependent feeding behavior modulation and the evolution of terrestrial feeding in Emydidae

Evolutionary transitions between aquatic and terrestrial environments are common in vertebrate evolution. These transitions require major changes in most physiological functions, including feeding. Emydid turtles are ancestrally aquatic, with most species naturally feeding only in water, but some terrestrial species can modulate their feeding behavior appropriately for both media. In addition, many aquatic species can be induced to feed terrestrially. A comparison of feeding in both aquatic and terrestrial environments presents an excellent opportunity to investigate the evolution of terrestrial feeding from aquatic feeding, as well as a system within which to develop methods for studying major evolutionary transitions between environments. Individuals from eight species of emydid turtles (six aquatic, two terrestrial) were filmed while feeding underwater and on land. Bite kinematics were analyzed to determine whether aquatic turtles modulated their feeding behavior in a consistent and appropriate manner between environments. Aquatic turtles showed consistent changes between environments, taking longer bites and using more extensive motions of the jaw and hyoid when feeding on land. However, these motions differ from those shown by species that naturally feed in both environments and mostly do not seem to be appropriate for terrestrial feeding. For example, more extensive motions of the hyoid are only effective during underwater suction feeding. Emydids evolving to feed on land probably would have needed to evolve or learn to overcome many, but not all, aspects of the intrinsic emydid response to terrestrial feeding. Studies that investigate major evolutionary transitions must determine what responses to the new environment are shown by naïve individuals in order to fully understand the evolutionary patterns and processes associated with these transitions.

Evolution of the Morphology of Bottom Walking Turtles

Ecomorphology and functional morphology are two distinct disciplines within biology that are often conflated and erroneously used interchangeably. By investigating the morphological distinctiveness of bottom-walking turtles relative to aquatic swimmers and terrestrial walkers, we can disentangle the effects of ecology and performance. Shell morphology, tail length, digit length, webbing length, and integumental differences were examined using dry and wet preserved specimens. Bottom-walkers were hypothesized to be distinct in all measurements. Instead, bottom-walkers were typically distinct from terrestrial taxa but not aquatic taxa, although for integumentary structures, only bottom-walkers were found to have significantly more integumentary structures than terrestrial turtles. This demonstrates that, despite sometimes highly differential locomotor modes, ecology, defined as habitat type, can show a stronger morphological signal than function.

Finite Element Modeling of Shell Shape in the Freshwater Turtle Pseudemys concinna Reveals a Trade-Off between Mechanical Strength and Hydrodynamic Efficiency

Aquatic species can experience different selective pressures on morphology in different flow regimes. Species inhabiting lotic regimes often adapt to these conditions by evolving low-drag (i.e., streamlined) morphologies that reduce the likelihood of dislodgment or displacement. However, hydrodynamic factors are not the only selective pressures influencing organismal morphology and shapes well suited to flow conditions may compromise performance in other roles. We investigated the possibility of morphological trade-offs in the turtle Pseudemys concinna. Individuals living in lotic environments have flatter, more streamlined shells than those living in lentic environments; however, this flatter shape may also make the shells less capable of resisting predator-induced loads. We tested the idea that ‘‘lotic’’ shell shapes are weaker than ‘‘lentic’’ shell shapes, concomitantly examining effects of sex. Geometric morphometric data were used to transform an existing finite element shell model into a series of models corresponding to the shapes of individual turtles. Models were assigned identical material properties and loaded under identical conditions, and the stresses produced by a series of eight loads were extracted to describe the strength of the shells. ‘‘Lotic’’ shell shapes produced significantly higher stresses than ‘‘lentic’’ shell shapes, indicating that the former is weaker than the latter. Females had significantly stronger shell shapes than males, although these differences were less consistent than differences between flow regimes. We conclude that, despite the potential for many-to-one mapping of shell shape onto strength, P. concinna experiences a trade-off in shell shape between hydrodynamic and mechanical performance. This trade-off may be evident in many other turtle species or any other aquatic species that also depend on a shell for defense. However, evolution of body size may provide an avenue of escape from this trade-off in some cases, as changes in size can drastically affect mechanical performance while having little effect on hydrodynamic performance.

Biomechanics on the Half Shell: Functional Performance Influences Patterns of Morphological Variation in the Emydid Turtle carapace

This study uses the carapace of emydid turtles to address hypothesized differences between terrestrial and aquatic species. Geometric morphometrics are used to quantify shell shape, and performance is estimated for two shell functions: shell strength and hydrodynamics. Aquatic turtle shells differ in shape from terrestrial turtle shells and are characterized by lower frontal areas and presumably lower drag. Terrestrial turtle shells are stronger than those of aquatic turtles; many-to-one mapping of morphology to function does not entirely mitigate a functional trade-off between mechanical strength and hydrodynamic performance. Furthermore, areas of morphospace characterized by exceptionally poor performance in either of the functions are not occupied by any emydid species. Though aquatic and terrestrial species show no significant differences in the rate of morphological evolution, aquatic species show a higher lineage density, indicative of a greater amount of convergence in their evolutionary history. The techniques employed in this study, including the modeling of theoretical shapes to assess performance in unoccupied areas of morphospace, suggest a framework for future studies of morphological variation.

Morphological and Mechanical Changes in Juvenile Red-Eared Slider Turtle (Trachemys Scripta Elegans) Shells During Ontogeny

Turtles experience numerous modifications in the morphological, physiological, and mechanical characteristics of their shells through ontogeny. Although a general picture is available of the nature of these modifications, few quantitative studies have been conducted on changes in turtle shell shape through ontogeny, and none on changes in strength or rigidity. This study investigates the morphological and mechanical changes that juvenile Trachemys scripta elegans undergo as they increase in size. Morphology and shell rigidity were quantified in a sample of 36 alcohol-preserved juvenile Trachemys scripta elegans. Morphometric information was used to create finite element models of all specimens. These models were used to assess the mechanical behavior of the shells under various loading conditions. Overall, we find that turtles experience complementary changes in size, shape, deformability, and relative strength as they grow. As turtles age their shells become larger, more elongate, relatively flatter, and more rigid. These changes are associated with decreases in relative (size independent) strength, even though the shells of larger turtles are stronger in an absolute sense. Decreased deformability is primarily due to changes in the size of the animals. Residual variation in deformability cannot be explained by changes in shell shape. This variation is more likely due to changes in the degree of connectedness of the skeletal elements in the turtle's shells, along with changes in the thickness and degree of mineralization of shell bone. We suggest that the mechanical implications of shell size, shape, and deformability may have a large impact on survivorship and development in members of this species as they mature. J. Morphol. 275:391-397, 2014. 2013 Wiley Periodicals, Inc. Copyright 2013 Wiley Periodicals, Inc.