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.     

The influence of multiple functional demands on morphological diversification: A test on turtle shells

Organismal parts are often involved in the performance of more than one function. The role of trade‐offs in influencing phenotypic evolution of such parts is well‐studied; less well‐understood is their role in influencing phenotypic diversity. Increases in the number of functions a part is involved in may inhibit subsequent diversification, as the number of trade‐offs increases. Alternately, such an increase might promote phenotypic diversification, by increasing adaptive landscape complexity and promoting specialization for different roles. We compare these predictions by testing whether aquatic turtle shells, which resist loads, act as hydrodynamic elements, facilitate self‐righting, and exchange heat with the environment, differ in phenotypic diversity from those of terrestrial species, which perform all the same functions except for hydrodynamics. We used 53 3D landmarks digitized on 2722 specimens of 274 hard‐shelled turtle species to quantify shell shape variation, and a set of phylogenetic hypotheses to examine evolutionary patterns. Terrestrial turtles consistently had higher phenotypic diversity than aquatic species. Differences are not due to differences in the rates of evolution between the two groups, but rather differences in evolutionary mode. Thus this study supports the traditional view of the role of multiple functions in determining phenotypic diversity.     

Climatic niche evolution in turtles is characterized by phylogenetic conservatism for both aquatic and terrestrial species

Understanding how the climatic niche of species evolved has been a topic of high interest in current theoretical and applied macroecological studies. However, little is known regarding how species traits might influence climatic niche evolution. Here, we evaluated patterns of climatic niche evolution in turtles (tortoises and freshwater turtles) and whether species habitat (terrestrial or aquatic) influences these patterns. We used phylogenetic, climatic and distribution data for 261 species to estimate their climatic niches. Then, we compared whether niche overlap between sister species was higher than between random species pairs and evaluated whether niche optima and rates varied between aquatic and terrestrial species. Sister species had higher values of niche overlap than random species pairs, suggesting phylogenetic climatic niche conservatism in turtles. The climatic niche evolution of the group followed an Ornstein–Uhlenbeck model with different optimum values for aquatic and terrestrial species, but we did not find consistent evidence of differences in their rates of climatic niche evolution. We conclude that phylogenetic climatic niche conservatism occurs among turtle species. Furthermore, terrestrial and aquatic species occupy different climatic niches but these seem to have evolved at similar evolutionary rates, reinforcing the importance of habitat in understanding species climatic niches and their evolution.     

Palaeoecology of triassic stem turtles sheds new light on turtle origins

Competing hypotheses of early turtle evolution contrast sharply in implying very different ecological settings-aquatic versus terrestrial-for the origin of turtles. We investigate the palaeoecology of extinct turtles by first demonstrating that the forelimbs of extant turtles faithfully reflect habitat preferences, with short-handed turtles being terrestrial and long-handed turtles being aquatic. We apply this metric to the two successive outgroups to all living turtles with forelimbs preserved, Proganochelys quenstedti and Palaeochersis talampayensis, to discover that these earliest turtle outgroups were decidedly terrestrial. We then plot the observed distribution of aquatic versus terrestrial habits among living turtles onto their hypothesized phylogenies. Both lines of evidence indicate that although the common ancestor of all living turtles was aquatic, the earliest turtles clearly lived in a terrestrial environment. Additional anatomical and sedimentological evidence favours these conclusions. The freshwater aquatic habitat preference so characteristic of living turtles cannot, consequently, be taken as positive evidence for an aquatic origin of turtles, but must rather be considered a convergence relative to other aquatic amniotes, including the marine sauropterygians to which turtles have sometimes been allied.     

The effects of temperature and inter-individual variation on the locomotor performance of juvenile turtles

The effects of temperature on aquatic and terrestrial locomotor performance, including measures of burst speed, endurance, and righting response, the inter-individual correlation between measures of locomotor performance, and the temporal repeatability of performance were assessed in juvenile western painted turtles, Chrysemys picta bellii. Locomotor performance increased as temperature increased, with Q ₁₀ values ranging from 1.33 to 1.98 for burst speed and 2.28 to 2.76 for endurance measures. Righting response performance also increased with temperature. Aquatic and terrestrial measures of locomotor performance were highly correlated; however, righting response was not correlated with any other measure of performance. Measures of terrestrial locomotor performance were highly repeatable over the entire 30-week study period, whereas aquatic locomotor performance was only repeatable through week 12. The righting response was repeatable over a 6-week study period. Both the interindividual variation and temperature effects on locomotor performance likely influences the survival of turtles, especially juveniles, by affecting the length of time turtles are exposed to potential predators and their ability to escape.     

Shell bone histology indicates terrestrial palaeoecology of basal turtles

The palaeoecology of basal turtles from the Late Triassic was classically viewed as being semi-aquatic, similar to the lifestyle of modern snapping turtles. Lately, this view was questioned based on limb bone proportions, and a terrestrial palaeoecology was suggested for the turtle stem. Here, we present independent shell bone microstructural evidence for a terrestrial habitat of the oldest and basal most well-known turtles, i.e. the Upper Triassic Proterochersis robusta and Proganochelys quenstedti. Comparison of their shell bone histology with that of extant turtles preferring either aquatic habitats or terrestrial habitats clearly reveals congruence with terrestrial turtle taxa. Similarities in the shell bones of these turtles are a diploe structure with well-developed external and internal cortices, weak vascularization of the compact bone layers and a dense nature of the interior cancellous bone with overall short trabeculae. On the other hand, 'aquatic' turtles tend to reduce cortical bone layers, while increasing overall vascularization of the bone tissue. In contrast to the study of limb bone proportions, the present study is independent from the uncommon preservation of appendicular skeletal elements in fossil turtles, enabling the palaeoecological study of a much broader range of incompletely known turtle taxa in the fossil record.     

Aquatic feeding in a terrestrial turtle: a functional-morphological study of the feeding apparatus in the Indochinese box turtle Cuora galbinifrons (Testudines, Geoemydidae)

The Indochinese box turtle Cuora galbinifrons is regarded as a purely terrestrial species, but our results demonstrate that it can feed both on land and in water. The inverse relationship between the relative development of the hyoid apparatus and the tongue found in the most investigated chelonians is not valid in the Indochinese box turtle. Our morphological analysis of the feeding apparatus reveals that the palate shape and the design of the tongue are consistent with terrestrial feeders, but the construction of the hyoid complex is more characteristic of aquatic feeders. Previous studies have demonstrated that tongue enlargement negatively impacts the capacity of the turtles to suction feed. The present study focuses on the aquatic intraoral prey transport kinematic patterns. Our analysis is based on high-speed films with 250 fr/s and high-speed cineradiography with 50 fr/s. The aquatic intraoral food transport mechanisms differ depending on prey size: small items are transported predominantly by “inertial suction”, whereas larger items are moved by the tongue—normally a clear terrestrial strategy. As the genus Cuora is ancestrally aquatic, the use of lingual food transport in the aquatic environment is presumably an aberrant modus typical only for the most terrestrial among the Asian box turtles.     

Comparative limb bone scaling in turtles: Phylogenetic transitions with changes in functional demands?

Several terrestrial vertebrate clades include lineages that have evolved nearly exclusive use of aquatic habitats. In many cases, such transitions are associated with the evolution of flattened limbs that are used to swim via dorsoventral flapping. Such changes in shape may have been facilitated by changes in limb bone loading in novel aquatic environments. Studies on limb bone loading in turtles found that torsion is high relative to bending loads on land, but reduced compared to bending during aquatic rowing. Release from torsion among rowers could have facilitated the evolution of hydrodynamically advantageous flattened limbs among aquatic species. Because rowing is regarded as an intermediate locomotor stage between walking and flapping, rowing species might show limb bone flattening intermediate between the tubular shapes of walkers and the flattened shapes of flappers. We collected measurements of humeri and femora from specimens representing four functionally divergent turtle clades: sea turtles (marine flappers), softshells (specialized freshwater rowers), emydids (generalist semiaquatic rowers), and tortoises (terrestrial walkers). Patterns of limb bone scaling with size were compared across lineages using phylogenetic comparative methods. Although rowing taxa did not show the intermediate scaling patterns we predicted, our data provide other functional insights. For example, flattening of sea turtle humeri was associated with positive allometry (relative to body mass) for the limb bone diameter perpendicular to the flexion-extension plane of the elbow. Moreover, softshell limb bones exhibit positive allometry of femoral diameters relative to body mass, potentially helping them maintain their typical benthic position in water by providing additional weight to compensate for shell reduction. Tortoise limb bones showed positive allometry of diameters, as well as long humeri, relative to body mass, potentially reflecting specializations for resisting loads associated with digging. Overall, scaling patterns of many turtle lineages appear to correlate with distinctive behaviors or locomotor habits.     

Analysis of prey capture and food transport kinematics in two Asian box turtles,Cuora amboinensis and Cuora flavomarginata (Chelonia,Geoemydidae), with emphasis on terrestrial feeding patterns

This study examines the kinematics and morphology of the feeding apparatus of two geoemydid chelonians, the Malayan (Amboina) box turtle (Cuora amboinensis) and the yellow-margined box turtle (Cuora flavomarginata). Both species are able to feed on land as well as in water. Feeding patterns were analysed by high-speed cinematography. The main focus of the present study is on the terrestrial feeding strategies in both Asian box turtles, because feeding on land has probably evolved de novo within the ancestrally aquatic genus Cuora. During terrestrial feeding (analysed for both species), the initial food prehension is always done by the jaws, whereas intraoral food transport and pharyngeal packing actions are tongue-based. The food uptake modes in Cuoras differ considerably from those described for purely terrestrial turtles. Lingual food prehension is typical of all tortoises (Testudinidae), but is absent in C. amboinensis and C. flavomarginata. A previous study on Terrapene carolina shows that this emydid turtle protrudes the tongue during ingestion on land, but that the first contact with the food item occurs by the jaws. Both Asian box turtles investigated here have highly movable, fleshy tongues; nonetheless, the hyolingual complex remains permanently retracted during initial prey capture. In aquatic feeding (analysed for C. amboinensis only), the prey is captured by a fast forward strike of the head (ram feeding). As opposed to ingestion on land, in the underwater grasp the hyoid protracts prior to jaw opening. The head morphology of the investigated species differs. In contrast to the Malayan box turtle, C. flavomarginata exhibits a more complexly structured dorsal lingual epithelium, a considerable palatal vault, weaker jaw adductor muscles and a simplified trochlear complex. The differences in the hyolingual morphology reflect the kinematic patterns of the terrestrial feeding transport.     

Survival and Causes of Mortality of Head-Started Western Pond Turtles on Pierce National Wildlife Refuge,Washington

ABSTRACT The western pond turtle (Actinemys marmorata) is a species of conservation concern over much of its range and is listed as endangered in Washington State. From 2000 to 2004, we used radiotelemetry to document survival and mortality factors of head-started western pond turtles (n = 68) released into Pierce National Wildlife Refuge in southwestern Washington. Survival estimates for first year and older turtles ranged from 86% to 97% and overlapping confidence intervals indicated no detectible differences among age classes or among years. Subadult turtles released at ≥90-mm carapace length apparently avoided capture by most aquatic predators, indicating that terrestrial predators should be the focus of research and management where predation on larger age-classes is a concern. High annual survival combined with the documented nesting by ≥7-year-old female head-started turtles in Washington suggest that recruitment of adults is being achieved; however, head-starting is only practical as an interim solution and strategies for effective removal of aquatic predators must be developed and implemented where natural recruitment is inadequate to maintain populations.     

Functional performance of turtle humerus shape across an ecological adaptive landscape

The concept of the adaptive landscape has been invaluable to evolutionary biologists for visualizing the dynamics of selection and adaptation, and is increasingly being used to study morpho‐functional data. Here, we construct adaptive landscapes to explore functional trade‐offs associated with variation in humerus morphology among turtles adapted to three different locomotor environments: marine, semiaquatic, and terrestrial. Humerus shape from 40 species of cryptodire turtles was quantified using a pseudolandmark approach. Hypothetical shapes were extracted in a grid across morphospace and four functional traits (strength, stride length, mechanical advantage, and hydrodynamics) measured on those shapes. Quantitative trait modeling was used to construct adaptive landscapes that optimize the functional traits for each of the three locomotor ecologies. Our data show that turtles living in different environments have statistically different humeral shapes. The optimum adaptive landscape for each ecology is defined by a different combination of performance trade‐offs, with turtle species clustering around their respective adaptive peak. Further, species adhere to pareto fronts between marine–semiaquatic and semiaquatic–terrestrial optima, but not between marine–terrestrial. Our study demonstrates the utility of adaptive landscapes in informing the link between form, function, and ecological adaptation, and establishes a framework for reconstructing turtle ecological evolution using isolated humeri from the fossil record.     

Morphogenetic and constructional differences of the carapace of aquatic and terrestrial turtles and their evolutionary significance

The postembryonic development of the turtle carapace was studied in the aquatic Еmys orbicularis and the terrestrial Тestudo graeca. Differences in the structure of the bony shell in aquatic and terrestrial turtles were shown to be associated with varying degrees of development of epidermal derivatives, namely, the thickness of the scutes and the depth of horny furrows. Sinking of the horny furrows into the dermis causes local changes in the structure of the collagen matrix, which might precondition the acceleration of the ossification. Aquatic turtles possess a relatively thin horny cover, whose derivatives are either weakly developed or altogether absent and thus make no noticeable impact on the growth dynamics of bony plates. Carapace plates of these turtles outgrow more or less evenly around the periphery, which results in uniform costals, relatively narrow and partly reduced neurals, and broad peripherals extending beyond the marginal scutes. In terrestrial turtles (Testudinidae), horny structures are much more developed and exert a considerable impact on the growth of bony elements. As a result, bony plates outgrow unevenly in the dermis, expanding fast in the zones under the horny furrows and slowly outside these zones. This determines the basic features of the testudinid carapace: alternately cuneate shape of costals, an alternation of broad octagonal and narrow tetragonal neurals, and the limitation of the growth of peripherals by pleuro-marginal furrows. The evolutionary significance of morphogenetic and constructional differences in the turtle carapace, and the association of these differences with the turtle habitats are discussed.     

Is sexual body shape dimorphism consistent in aquatic and terrestrial chelonians?

Comparisons between aquatic and terrestrial species provide an opportunity to examine how sex-specific adaptations interact with the environment to influence body shape. In terrestrial female tortoises, selection for fecundity favors the development of a large internal abdominal cavity to accommodate the clutch; in conspecific males, sexual selection favors mobility with large openings in the shell. To examine to what extent such trends apply in aquatic chelonians we compared the body shape of males and females of two aquatic turtles (Chelodina colliei and Mauremys leprosa). In both species, females were larger than males. When controlled for body size, females exhibited a greater relative internal volume and a higher body condition index than males; both traits potentially correlate positively with fecundity. Males were more streamlined (hydrodynamic), and exhibited larger openings in the shell providing more space to move their longer limbs; such traits probably improve mobility and copulation ability (the males chase and grab the female for copulation). Overall, although the specific constraints imposed by terrestrial and aquatic locomotion shape the morphology of chelonians differently (aquatic turtles were flatter, hence more hydrodynamic than terrestrial tortoises), the direction for sexual shape dimorphism remained unaffected. Our main conclusion is that the direction of sexual shape dimorphism is probably more consistent than sexual size dimorphism in the animal kingdom.     

Great Lakes coastal wetland habitat use by seven turtle species: influences of wetland type, vegetation, and abiotic conditions

Great Lakes coastal wetlands are important habitats for turtles but few studies have looked at factors driving community structure in these systems. We evaluated the effects of wetland type, vegetation, and abiotic conditions on turtle communities for 56 wetlands in Lakes Huron, Michigan, and Superior with data collected during the summers of 2000–2008. Overall, 1,366 turtles representing seven species were captured using fyke nets. For the majority of species, catches were highest in drowned river mouth wetlands In addition, turtles tended to be more abundant in water lilies, submersed aquatic vegetation, and cattails compared to bulrush. We also found positive correlations between catches of four of the species as well as total turtle catch and turtle species richness with a human disturbance gradient. These correlations suggest that turtles may be able to utilize coastal wetland areas that are inhospitable to fish because of hypoxic conditions. Our results show the importance Great Lakes coastal wetlands to turtles, and stress the need for managers to take into account turtle populations when preparing conservation and restoration strategies.     

Genetic effects of landscape,habitat preference and demography on three co‐occurring turtle species

Expanding the scope of landscape genetics beyond the level of single species can help to reveal how species traits influence responses to environmental change. Multispecies studies are particularly valuable in highly threatened taxa, such as turtles, in which the impacts of anthropogenic change are strongly influenced by interspecific differences in life history strategies, habitat preferences and mobility. We sampled approximately 1500 individuals of three co‐occurring turtle species across a gradient of habitat change (including varying loss of wetlands and agricultural conversion of upland habitats) in the Midwestern USA. We used genetic clustering and multiple regression methods to identify associations between genetic structure and permanent landscape features, past landscape composition and landscape change in each species. Two aquatic generalists (the painted turtle, Chrysemys picta, and the snapping turtle Chelydra serpentina) both exhibited population genetic structure consistent with isolation by distance, modulated by aquatic landscape features. Genetic divergence for the more terrestrial Blanding's turtle (Emydoidea blandingii), on the other hand, was not strongly associated with geographic distance or aquatic features, and Bayesian clustering analysis indicated that many Emydoidea populations were genetically isolated. Despite long generation times, all three species exhibited associations between genetic structure and postsettlement habitat change, indicating that long generation times may not be sufficient to delay genetic drift resulting from recent habitat fragmentation. The concordances in genetic structure observed between aquatic species, as well as isolation in the endangered, long‐lived Emydoidea, reinforce the need to consider both landscape composition and demographic factors in assessing differential responses to habitat change in co‐occurring species.     

Energy and water flux during terrestrial estivation and overland movement in a freshwater turtle

The doubly labeled water (DLW) method for studying energy and water balance in field-active animals is not feasible for freshwater animals during aquatic activities, but several species of nominally aquatic reptiles leave wetlands for several critical and extended behaviors, where they face challenges to their energy and water balance. Using DLW, we studied energy and water relations during terrestrial estivation and movements in the eastern long-necked turtle (Chelodina longicollis), a species that inhabits temporary wetlands in southeastern Australia. Water efflux rates of 14.3-19.3 mL (kg d)(-1 ) during estivation were nearly offset by influx, indicating that turtles did not maintain water balance while terrestrial, though dehydration was slow. Estivation energy expenditure declined over time to 20.0-24.6 kJ (kg d)(-1) but did not indicate substantial physiological specializations. Energy reserves are predicted to limit survival in estivation to an estimated 49-261 d (depending on body fat), which is in close agreement with observed bouts of natural estivation in this population. The energy cost and water flux rates associated with overland movement behavior ranged from 46 to 99 kJ (kg d)(-1 ) and from 21.6 to 40.6 mL (kg d)(-1), respectively, for turtles moving 23-34 m d(-1). When a wetland dries, a turtle that forgoes movement to other wetlands can save sufficient energy to fuel up to 134 d in estivation. The increasing time in estivation with travel distance gained in this energy "trade-off" fits our previous observations that more turtles estivate when longer distances must be traveled to the nearest permanent lake, whereas emigration is nearly universal when only short distances must be traversed. The DLW method shows promise for addressing questions regarding the behavioral ecology and physiology of freshwater turtles in terrestrial situations, though validation studies are needed.     

Non‐marine turtle plays important functional roles in Indonesian ecosystems

The Southeast Asian box turtle (Cuora amboinensis) is numerically the most important turtle exported from Indonesia. Listed as Vulnerable by the IUCN, this turtle is heavily harvested and exported for food and traditional medicine in China and for the pet trade primarily in the United States, Europe, and Japan. Despite its significance in global markets, relatively little is known about the species’ ecology or importance to ecosystems. We conducted our research in a national park in Sulawesi, Indonesia, and our objectives were to quantify trophic breadth, capacity for seed dispersal between aquatic and terrestrial ecosystems, and whether ingestion of seeds by C. amboinensis enhances germination. We obtained diet samples from 200 individual turtles and found that the species is omnivorous, exhibiting an ontogenetic shift from more carnivorous to more omnivorous. Both subadults and adults scavenged on other vertebrates. In a seed passage experiment, turtles passed seeds for 2?9 days after ingestion. Radio‐tracked turtles moved, on average, about 35 m per day, indicating that seeds from ingested fruits, given seed passage durations, could be dispersed 70?313 m from the parent tree and potentially between wetland and upland ecosystems. In a seed germination experiment, we found that ingestion of seeds by turtles enhanced germination, as compared with control seeds, for four of six plant species tested. Of these, two are common in the national park, making up a significant proportion of plant biomass in lowland swamp forest and around ephemeral pools in savanna, and are highly valued outside of the park for their lumber for construction of houses, furniture, and boats. Protection of C. amboinensis populations may be important for maintaining trophic linkages that benefit biodiversity, communities, and local economies.