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.     

Oropharyngeal morphology in the basal tortoise Manouria emys emys with comments on form and function of the testudinid tongue

In tetrapods, the ability to ingest food on land is based on certain morphological features of the oropharynx in general and the feeding apparatus in particular. Recent paleoecological studies imply that terrestrial feeding has evolved secondarily in turtles, so they had to meet the morphological oropharyngeal requirements independently to other amniotes. This study is designed to improve our limited knowledge about the oropharyngeal morphology of tortoises by analyzing in detail the oropharynx in Manouria emys emys. Special emphasis is placed on the form and function of the tongue. Even if Manouria is considered a basal member of the only terrestrial turtle clade and was hypothesized to have retained some features reflecting an aquatic ancestry, Manouria shows oropharyngeal characteristics found in more derived testudinids. Accordingly, the oropharyngeal cavity in Manouria is richly structured and the glands are large and complexly organized. The tongue is large and fleshy and bears numerous slender papillae lacking lingual muscles. The hyolingual skeleton is mainly cartilaginous, and the enlarged anterior elements support the tongue and provide insertion sides for the well‐developed lingual muscles, which show striking differences to other reptiles. We conclude that the oropharyngeal design in Manouria differs clearly from semiaquatic and aquatic turtles, as well as from other reptilian sauropsids. J. Morphol., 2011. © 2011 Wiley‐Liss, Inc.     

Triassic turtle tracks and the origin of turtles

Turtle (Testudines) tracks, Chelonipus torquatus, reported from the early Middle Triassic (Anisian) of Germany, and Chelonipus isp. from the late Early Triassic (Spathian) of Wyoming and Utah, are the oldest fossil evidence of turtles, but have been omitted in recent discussions of turtle origins. These tracks provide significant clues as to how early the turtle Bauplan originated. Turtle trackways are quite distinctive: the manus and pes form tracks nearly parallel to the midline and indicate an unusually wide gait in which the trackway width is nearly equal to the stride length. These tracks do not fit what would be expected to be made by Triassic Pappochelys or Odontochelys, a supposed prototurtle and an early turtle, respectively. In contrast, these tracks are consistent with what would be expected from the Triassic turtles Proganochelys and Palaeochersis. The features inferred to be present in Triassic turtle tracks support the notion that Odontochelys is a derived aquatic branch of the turtle stem lineage rather than the ancestral state of all turtles. Chelonipus also resembles the Permian track Pachypes dolomiticus, generally assigned to a pareiasaur trackmaker. These revelations highlight the need to consider all available evidence regarding turtle origins, rather than just the body fossils.     

First fossil gravid turtle provides insight into the evolution of reproductive traits in turtles

Here we report on the first discovery of shelled eggs inside the body cavity of a fossil turtle and on an isolated egg clutch, both referable to the Cretaceous turtle Adocus. These discoveries provide a unique opportunity to gain insight into the reproductive traits of an extinct turtle and to understand the evolution of such traits among living turtles. The gravid adult and egg clutch indicate that Adocus laid large clutches of rigid-shelled spherical eggs and established their nests near rivers, traits that are shared by its closest living relatives, the soft-shelled turtles. Adocus eggshell, however, was probably more rigid than that of living turtles, based on its great thickness and structure, features that may represent unique adaptations to intense predation or to arid nest environments. In light of the reproductive traits observed in Adocus, the distribution of reproductive traits among turtles reveals that large clutches of rigid-shelled eggs are primitive for hidden-necked turtles (cryptodirans) and that spherical eggs may have evolved independently within this group.     

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.     

Thermal plasticity of diving behavior, aquatic respiration, and locomotor performance in the Mary River turtle Elusor macrurus

Locomotion is a common measure of performance used in studies of thermal acclimation because of its correlation with predator escape and prey capture. However, for sedentary animals such as freshwater turtles, we propose that diving behavior may be a more ecologically relevant measure of performance. Increasing dive duration in hatchling turtles reduces predator exposure and therefore functions as an ecological benefit. Diving behavior is thermally dependent, and in some species of freshwater turtles, it is also reliant on aquatic respiration. This study examined the influence of thermal acclimation on diving behavior, aquatic respiration, and locomotor performance in the endangered, bimodally respiring Mary River turtle Elusor macrurus. Diving behavior was found to partially acclimate at 17 degrees C, with turtles acclimated to a cold temperature (17 degrees C) having a significantly longer dive duration than hatchlings acclimated to a warm temperature (28 degrees C). This increase in dive duration at 17 degrees C was not a result of physiological alterations in metabolic rate but was due instead to an increase in aquatic oxygen consumption. Increasing aquatic oxygen consumption permitted cold-acclimated hatchlings to remain submerged for significantly longer periods, with one turtle undertaking a dive of over 2.5 d. When burst-swimming speed was used as the measure of performance, thermal acclimation was not detected. Overall, E. macrurus demonstrated a partial ability to acclimate to changes in environmental temperature.     

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.     

Risk analysis reveals global hotspots for marine debris ingestion by sea turtles

Plastic marine debris pollution is rapidly becoming one of the critical environmental concerns facing wildlife in the 21st century. Here we present a risk analysis for plastic ingestion by sea turtles on a global scale. We combined global marine plastic distributions based on ocean drifter data with sea turtle habitat maps to predict exposure levels to plastic pollution. Empirical data from necropsies of deceased animals were then utilised to assess the consequence of exposure to plastics. We modelled the risk (probability of debris ingestion) by incorporating exposure to debris and consequence of exposure, and included life history stage, species of sea turtle and date of stranding observation as possible additional explanatory factors. Life history stage is the best predictor of debris ingestion, but the best‐fit model also incorporates encounter rates within a limited distance from stranding location, marine debris predictions specific to the date of the stranding study and turtle species. There is no difference in ingestion rates between stranded turtles vs. those caught as bycatch from fishing activity, suggesting that stranded animals are not a biased representation of debris ingestion rates in the background population. Oceanic life‐stage sea turtles are at the highest risk of debris ingestion, and olive ridley turtles are the most at‐risk species. The regions of highest risk to global sea turtle populations are off of the east coasts of the USA, Australia and South Africa; the east Indian Ocean, and Southeast Asia. Model results can be used to predict the number of sea turtles globally at risk of debris ingestion. Based on currently available data, initial calculations indicate that up to 52% of sea turtles may have ingested debris.     

Phylogeny and paraphyly among tetrapod blood flukes (Digenea: Schistosomatidae and Spirorchiidae)

The blood flukes of turtles (Digenea: Spirorchiidae) and the blood flukes of crocodilians, birds and mammals (Digenea: Schistosomatidae) have long been considered as closely related, but distinct evolutionary lineages. Recent morphological and molecular studies have considered these families as sister taxa within the Schistosomatoidea. Representatives of both families have similar furcocercous cercariae and similar two-host life cycles, but have different definitive hosts, distinct reproductive patterns and different morphologies. Sequences including approximately 1800 bases of the small subunit ribosomal DNA and 1200 bases of the large subunit ribosomal DNA were generated from representatives of eight spirorchiid genera. These sequences were aligned with pre-existing sequences of Schistosomatidae and other representatives of the Diplostomida and analysed for phylogenetic signal using maximum parsimony and Bayesian inference. These analyses revealed that the Spirorchiidae is paraphyletic and that the turtle blood flukes are basal to the highly derived schistosomatids. Three genera of spirorchiids from marine turtles form a sister group to the Schistosomatidae and five genera of spirorchiids from freshwater turtles occupy basal positions in the phylogeny of tetrapod blood flukes. Marine turtles are considered to be derived from freshwater turtles and the results of the current study indicate that the spirorchiid parasites of marine turtles are similarly derived from a freshwater ancestor. The close relationship of the marine spirorchiids to schistosomatids and the basal position of the marine transmitted Austrobilharzia and Ornithobilharzia in the schistosomatid clade suggests that schistosomatids arose after a marine turtle blood fluke ancestor successfully colonised birds.     

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.     

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.     

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.     

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.     

Pareiasaur phylogeny and the origin of turtles

The evolutionary relationship of all the valid species (and thus genera) of pareiasaurs are assessed through a phylogcnctic analysis of these taxa together with turtles, Owenetta, Barasaurus, Sclerosaurus, procolophonids, lanthanosuchids, nyctiphruretids, and nycterolctcrids. 128 os-teological characters were used, and almost all relevant taxa were examined. The results confirm that among these taxa, pareiasaurs and turtles form a robust clade, to the exclusion of all other taxa including procolophonids. However, pareiasaurs might not be the mono-phyletic sister group of turtles, as previously suggested. Rather, there is some evidence that pareiasaurs are paraphyletic with respect to (i.e. ‘ancestral to’) turtles. Among pareiasaurs, the early, large, heavily ossified forms such as Brady.saurus are most distantly related to turtles. These forms are characterized by rather smooth skulls, and dermal armour restricted to the dorsal midline. More closely related to turtles are forms such as Scutosaurus, Pareiasuchus, and Elginia. These taxa form a distinct clade of pareiasaurs, characterized by a very ‘mammallike’ pelvis, elaborate cranial ornamentation and a loose covering of osteoderms over the entire dorsum. The late, dwarf pareiasaurs Nanoparia, Anthodon, and Pumiliopareia are the nearest relatives of turtles. These forms exhibit otherwise uniquely turtle features such as a rigid covering of dermal armour over the entire dorsal region, expanded flattened ribs, cylindrical scapula blade, great reduction of humeral torsion (to 25^o), greatly developed trochanter major, offset femoral head, and reduced cnemial crest of the tibia. Thus, many features thought to be restricted to turtles (and thus to have evolved simultaneously with the turtle shell) actually arose earlier, at various points along the pareiasaurian stem lineage. The identification of the nature and sequence of anatomical changes leading to the origin of turtles, and the possibility that turtles are derived from dwarf pareiasaurs, should have important implications for speculations on the evolutionary biology of turtle origins.     

Sex determination,longevity, and the birth and death of reptilian species

Vertebrate sex‐determining mechanisms (SDMs) are triggered by the genotype (GSD), by temperature (TSD), or occasionally, by both. The causes and consequences of SDM diversity remain enigmatic. Theory predicts SDM effects on species diversification, and life‐span effects on SDM evolutionary turnover. Yet, evidence is conflicting in clades with labile SDMs, such as reptiles. Here, we investigate whether SDM is associated with diversification in turtles and lizards, and whether alterative factors, such as lifespan's effect on transition rates, could explain the relative prevalence of SDMs in turtles and lizards (including and excluding snakes). We assembled a comprehensive dataset of SDM states for squamates and turtles and leveraged large phylogenies for these two groups. We found no evidence that SDMs affect turtle, squamate, or lizard diversification. However, SDM transition rates differ between groups. In lizards TSD‐to‐GSD surpass GSD‐to‐TSD transitions, explaining the predominance of GSD lizards in nature. SDM transitions are fewer in turtles and the rates are similar to each other (TSD‐to‐GSD equals GSD‐to‐TSD), which, coupled with TSD ancestry, could explain TSD's predominance in turtles. These contrasting patterns can be explained by differences in life history. Namely, our data support the notion that in general, shorter lizard lifespan renders TSD detrimental favoring GSD evolution in squamates, whereas turtle longevity permits TSD retention. Thus, based on the macro‐evolutionary evidence we uncovered, we hypothesize that turtles and lizards followed different evolutionary trajectories with respect to SDM, likely mediated by differences in lifespan. Combined, our findings revealed a complex evolutionary interplay between SDMs and life histories that warrants further research that should make use of expanded datasets on unexamined taxa to enable more conclusive analyses.     

Genomic variation of the fibropapilloma-associated marine turtle herpesvirus across seven geographic areas and three host species

Fibropapillomatosis (FP) of marine turtles is an emerging neoplastic disease associated with infection by a novel turtle herpesvirus, fibropapilloma-associated turtle herpesvirus (FPTHV). This report presents 23 kb of the genome of an FPTHV infecting a Hawaiian green turtle (Chelonia mydas). By sequence homology, the open reading frames in this contig correspond to herpes simplex virus genes UL23 through UL36. The order, orientation, and homology of these putative genes indicate that FPTHV is a member of the Alphaherpesvirinae. The UL27-, UL30-, and UL34-homologous open reading frames from FPTHVs infecting nine FP-affected marine turtles from seven geographic areas and three turtle species (C. mydas, Caretta caretta, and Lepidochelys olivacea) were compared. A high degree of nucleotide sequence conservation was found among these virus variants. However, geographic variations were also found: the FPTHVs examined here form four groups, corresponding to the Atlantic Ocean, West pacific, mid-Pacific, and east Pacific. Our results indicate that FPTHV was established in marine turtle populations prior to the emergence of FP as it is currently known.     

Impalement of marine turtles (Reptitia,Chelonia: Cheloniidae and Dermochelyidae) by billfishes (Osteichthyes,Perciformes: Istiophoridae and Xiphiidae)

Synopsis Billfishes have long been known to impale a great variety of objects, but there are only two brief, obscure records of marine turtles being speared. Details are presented on these two, as well as on two other confirmed records; data from two additional unconfirmed records are also presented. In total, three species of marine turtles are known to have been impaled by three species of billfishes; a fourth species of fish and a fourth species turtle are listed in an unconfirmed case. Records come from the eastern and western Pacific as well as the eastern Atlantic. Of the four confirmed cases, the turtles survived in two, and apparently died as an effect of the spearing in the other two. In three confirmed cases only the impaled rostrum was encountered, and in one confirmed case the entire fish was found, with its rostrum piercing the turtle. There is no obvious advantage — or clear disadvantage — involved in impaling turtles. It is argued that these attacks are accidental, and the result of attempts made by the billfish to capture prey that are near the turtle. These spearings indicate that the chelonians serve as shelters for prey animals on the high seas, and thus, are further evidence of the pelagic existence of marine turtles. The impalings are evidence of a singular ecological role of the turtles — as live fish aggregation devices.