Pleurodiran Turtles Research Articles

An unexpected finding: identification of the first complete shell of the Franco-Belgian middle Eocene littoral pleurodiran turtle Eocenochelus eremberti in Spain

ABSTRACT Pleurodiran turtles are relatively abundant in the Eocene record of Europe, being mostly represented by Podocnemididae. Two genera have been identified. The most abundant and diverse is the well-known freshwater Neochelys. The other is Eocenochelus. The record of this poorly-known genus is very scarce. It is the only representative of the Upper Cretaceous to extant Erymnochelyini (i.e., a new tribe proposed here for the ‘Erymnochelys group of turtles’) interpreted as a littoral form, and the only one known outside Africa. The finding of the only complete shell of Eocenochelus hitherto identified is presented here. It comes from the Castejón de Sobrarbe-41 site, in the middle Eocene (Lutetian) of the Sobrarbe Formation of the Ainsa Basin (Huesca, Spain). The sedimentary environment of the site is compatible with its attribution to a littoral form. It is attributed to the type species of the genus, Eocenochelus eremberti, so far exclusively known by two partial shells from the middle Eocene of the Franco-Belgian Basin. Therefore, the paleobiogeographic distribution of this species is markedly increased, from the southern area of the North Sea to the Bay of Biscay. This finding provides new anatomical data on the species Eocenochelus eremberti and on its poorly known genus. urn:lsid:zoobank.org:act:5FF64A63-3187-4752-A62E-016308877022

A new member of Taphrosphyini (Pleurodira, Bothremydidae) from the Maastrichtian of Niger

A new pleurodiran turtle, corresponding to a bothremydid Taphrosphyini, is described in this paper. This form, Ilatardia cetiotesta gen. et sp. nov., is represented by a large skull, with a length of about 20 cm. It is one of the few Mesozoic representatives of Taphrosphyini known by the skull. This new Maastrichtian taxon comes from the Mount Ilatarda area of the Tahoua Region, in south-western Niger. The detailed comparison of this form with the other Cretaceous and Paleogene representatives of this clade is carried out.

Ontogeny, morphology and performance: changes in swimming stability and turning performance in the freshwater pleurodire turtle, Emydura subglobosa

Ontogeny, morphology and performance: changes in swimming stability and turning performance in the freshwater pleurodire turtle, Emydura subglobosa

Character definition and tempus optimum in comparative chondrocranial research

AbstractHere, we define a research program using primordial skull characters for broad scale phylogenetic comparisons, particularly for amniotes. There are many chondrocranium descriptions in the literature, encompassing many clades of vertebrates. The definition of a comparable “tempus optimum” for fully formed chondrocrania, as developed herein, will enable discrete character definition in the sense of phylogenetic systematics. The “tempus optimum” is a time period in which the nose region shows full chondrification and the basicranium has not yet changed in its anatomy by ossification processes. For studies on heterochrony, changes in the developmental timing through evolution, the available data in the literature are insufficient. Anatomical standardizations, traceable methodological approaches and clear definitions of comparable developmental stages are needed. Moreover, for profound homology assertions of chondrocranial structures, ontogeny needs to be traced from early mesenchymal condensation, through several stages of cartilage development, up to postnatal stages, in which ossifications are already present. A holistic observation, including hard and soft tissue anatomy, is of paramount importance to generate hypotheses of homology with much explanatory power and to derive conclusions on functional morphology. For that, traditional histological methodology is needed. We exemplify the suggested approach in two case studies on the disputed laterosphenoid in turtles and crocodiles and on the homology of pila antotica in a pleurodire turtle, and, using here defined criteria, we formulate hypotheses on their homology.

Identification of the Lower Cretaceous pleurodiran turtle Taquetochelys decorata as the only African araripemydid species

Araripemydidae is a clade of freshwater pleurodiran turtles originally described in South America, where it is represented by the Brasilian Aptian–Albian Araripemys barretoi. Two potential members of this lineage were defined in an Aptian level of Africa, in Gadoufaoua (Niger): Taquetochelys decorata, described from several isolated plates, and Lagaremys tenerensis, known from an almost complete skeleton. The review of the Araripemydidae record, and the analysis of the intraspecific variability present in that and in other clades of Pleurodira, allow me to refute their attribution to two different forms. ‘L. tenerensis’ is here recognized as a junior synonym of T. decorata. Therefore, the priority of T. decorata is demonstrated, as well as its attribution to Araripemydidae. The almost complete skeletal anatomy of the two currently recognized members of this Aptian–Albian clade (i.e. the African T. decorata and the South American A. barretoi) is well known, which is uncommon for the Cretaceous pleurodiran turtles.

Identification of the French Upper Cretaceous bothremydid turtle Foxemys mechinorum in the Spanish record

Bothremydidae is the most abundant and diverse group of turtles in the upper Cretaceous fossil sites of southwestern Europe. Several species a priori recognized as exclusive of the Portuguese, Spanish and French records were defined. The most abundant and best-preserved Spanish collection of pleurodiran turtles from the last Stages of the Upper Cretaceous comes from the fossil site of Lo Hueco (Cuenca Province, Central Spain). The bothremydid Iberoccitanemys convenarum, defined by a single specimen from the Maastrichtian of Haute-Garonne (Southern France), was subsequently recognized as a very abundant form in this Spanish site, corresponding to the only bothremydid so far identified as being part of the diversity of Bothremydidae of both countries. The presence of a second member of Bothremydidae was recognized in Lo Hueco, representing the only evidence of the synchronic and sympatric coexistence of two members of this lineage in a European site. However, very scarce information about this second form from Lo Hueco was available. Thus, its attribution to a new taxon or to a member of Foxemydina previously identified in the Spanish record, or in that of other European regions, could not be evaluated until now. New material from Lo Hueco, not attributable to I. convenarum but to this second larger form, allows its generic and specific identification. Close paleobiogeographical relationships considering the fauna of pleurodiran turtles from Spain and France are recognized thanks to the findings performed in Lo Hueco: not only I. convenarum is known in both countries, but also the French Foxemys mechinorum is identified in Central Spain.

Biomechanical factors influencing successful self-righting in the pleurodire turtle Emydura subglobosa.

Self-righting performance is a key ability for most terrestrial animals, and has been used as a metric of fitness, exhaustion and thermal limits in a variety of taxa. However, there is little understanding of the underlying mechanisms that drive variation in self-righting performance. To evaluate the mechanical factors that contribute to success versus failure when animals attempt to self-right, we compared force production and kinematic behavior in the rigid-bodied, pleurodire turtle Emydura subglobosa between successful and unsuccessful self-righting efforts. We found that the moment exerted during efforts to roll the body and the velocity of that roll are the primary drivers behind self-righting success. Specifically, turtles that self-righted successfully produced both larger moments and faster rolls than turtles that failed. In contrast, the angle at which the head was directed to lever the body and the extent of yaw that was incorporated in addition to roll had little impact on the likelihood of success. These results show that specific performance metrics can predict the ability of animals to self-right, providing a framework for biomimetic applications as well as future comparisons to test for differences in self-righting performance across animals from different environments, sexes, populations and species.

Identification of the African–European <i>Erymnochelys</i> group (Pleurodira, Podocnemididae) in the Belgian fossil record: first finding of <i>Eocenochelus eremberti</i> outside its type locality

Abstract. An almost complete plastron, as well as several peripherals and a costal plate of a turtle from the middle Eocene of Saint-Gilles, is presented here. Although this turtle specimen was donated to the Institut royal des Sciences naturelles de Belgique (Brussels, Belgium) more than a century ago, it remained undescribed. Its study allows us to recognize the second pleurodiran in the Belgian fossil record, where, until now, the Eocene Neochelys was the only one known. The Belgian material of Neochelys is known in lower Eocene (early Ypresian) levels, but the new pleurodiran specimen comes from the middle Eocene (early Lutetian). It is the first partial articulate shell of a pleurodiran turtle recognized in Belgium, and the only member of this clade recognized in this country at specific level. The new specimen is a representative of the so-called Erymnochelys group, this lineage being known in Africa from the Upper Cretaceous to the present but in Europe only during the Eocene. It represents the first specimen of Eocenochelus eremberti identified outside its type locality, the French region of Saint-Germain-en-Laye (Yvelines, Île-de-France), where only one specimen was found. The plastron of the Belgian individual corresponds to the most complete for this species. Its analysis allows us not only to broaden the range of paleobiogeographical distribution of Eocenochelus eremberti but also to improve the knowledge about the anatomy and variability of this taxon.

New information and establishment of a new genus for the Egyptian Paleogene turtle ‘Stereogenys’ libyca (Podocnemididae, Erymnochelyinae)

The poorly known pleurodiran turtle ‘Stereogenys’ libyca (Podocnemididae, Erymnochelyinae) is studied in this paper. It was defined in lower Oligocene levels of the Fayum Depression (Egypt), its presence in the upper Eocene levels of the same area being confirmed here. Its holotype corresponds to an almost complete and well preserved shell, that was until recently considered to be lost. No photograph of material attributable to this species had hitherto been published. Thus, the current knowledge about it was exclusively based on the limited information published more than a century ago. The recently rediscovered holotype, and also more than fifteen additional historical but unpublished specimens recognized here as attributable to this species, are studied in this paper. This species is attributed to a new genus, Andrewsemys, and the new combination Andrewsemys libyca is proposed.http://www.zoobank.org/urn:lsid:zoobank.org:pub:6D87831A-4510-4A3E-A624-C40FD644F448

A bothremydid from the middle Cenomanian of Portugal identified as one of the oldest pleurodiran turtles in Laurasia

The relatively complete and well preserved shell of a turtle, from the middle Cenomanian of Nazaré (Portugal), is studied here. It is recognized as a member of the crown group Pleurodira and, more specifically, of Bothremydidae. Pleurodira are one of the two lineages of modern turtles, their origin being in Gondwana. Pleurodira are very abundant in the uppermost Cretaceous record of Europe. However, this new finding is one of the few occurrences in the lower Upper Cretaceous of Laurasia. A single member of Bothremydidae had so far been identified in Portugal: the late Campanian-early Maastrichtian Rosasia soutoi. It was the only Cretaceous turtle identified in that country both at specific and at generic levels, being exclusive of Portugal. The taxon from Nazaré is identified as Algorachelus peregrinus, this form is also present in the contemporaneous beds in Spain, and is the oldest member of Bothremydidae in Laurasia. Algorachelus peregrinus is confirmed here to be a coastal form, which facilitated its spread. The two oldest known bothremydids from Laurasia, the European A. peregrinus and the North American Paiutemys tibert, are compared for the first time. They are recognized as closely related taxa. This study provides new data allowing a more precisely characterization of the oldest so far known dispersal event of Pleurodira in Laurasia, which was performed by an African lineage of Bothremydidae that reached the east coast of the Atlantic Ocean at least in the middle Cenomanian, and the west region of that Ocean at least in the late Cenomanian.

Side-necked Versus Hidden-necked: A Comparison of Shell Morphology Between Pleurodiran and Cryptodiran Turtles

Abstract: This study explores the potential morphological differences between pleurodiran and cryptodiran turtle shells. Pleurodires (Suborder Pleurodira), as suggested by their name, retract their heads into the shell by bending the neck to the side; this is different from cryptodires (Suborder Cryptodira), which withdraw their necks along a sagittal plane. Pleurodires also have evolved a unique pelvic morphology typified by two columnar pelvic elements sutured to both the carapace and plastron; in contrast, the pelvic girdle in cryptodires is loosely connected to the shell. These differences might put very different selective pressures on shell shape in these animals: The different head retraction strategies in the two groups could lead pleurodires to evolve wider and flatter anterior apertures while the differences in pelvic structure might permit the evolution of flatter carapaces (particularly in the posterior carapace) and narrower bridges as compared to cryptodires. We used 3D landmark data to char...

"On the Fence" versus "All in": Insights from Turtles for the Evolution of Aquatic Locomotor Specializations and Habitat Transitions in Tetrapod Vertebrates.

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.

An early bothremydid (Testudines, Pleurodira) from the Late Cretaceous (Cenomanian) of Utah, North America.

BackgroundBothremydidae is a clade of extinct pleurodiran turtles known from the Cretaceous to Paleogene of Africa, Europe, India, Madagascar, and North and South America. The group is most diverse during the Late Cretaceous to Paleogene of Africa. Little is known, however, about the early evolution of the group.MethodsWe here figure and describe a fossil turtle from early Late Cretaceous deposits exposed at MacFarlane Mine in Cedar Canyon, southwestern Utah, USA. The sediments associated with the new turtle are utilized to infer its stratigraphic provenience and the depositional settings in which it was deposited. The fossil is compared to previously described fossil pleurodires, integrated into a modified phylogenetic analysis of pelomedusoid turtles, and the biogeography of bothremydid turtles is reassessed. In light of the novel phylogenetic hypotheses, six previously established taxon names are converted to phylogenetically defined clade names to aid communication.ResultsThe new fossil turtle can be inferred with confidence to have originated from a brackish water facies within the late Cenomanian Culver Coal Zone of the Naturita Formation. The fossil can be distinguished from all other previously described pleurodires and is therefore designated as a new taxon, Paiutemys tibert gen. et. sp. nov. Phylogenetic analysis places the new taxon as sister to the European Polysternon provinciale, Foxemys trabanti and Foxemys mechinorum at the base of Bothremydinae. Biogeographic analysis suggests that bothremydids originated as continental turtles in Gondwana, but that bothremydines adapted to near-shore marine conditions and therefore should be seen as having a circum-Atlantic distribution.

A new side-neck turtle (Pelomedusoides: Bothremydidae) from the EarlyPaleocene (Danian) Maria Farinha Formation, Paraíba Basin, Brazil.

Limestone and marl from Maria Farinha Formation (Paraíba Basin, NE Brazil) accumulated in a shallow continental shelf environment during the expansion of the Atlantic Ocean in early Paleocene (Danian). It contains a rich paleontological record, which comprises many marine invertebrates, several species of bony and cartilaginous fishes, a crocodyliform and turtle remains. Here, we describe a new genus and species of pleurodire turtle from Maria Farinha Formation, based on a nearly complete plastron, an incomplete left pelvic girdle, and four dermal plates of the carapace. We tested the phylogenetic position of Inaechelys pernambucensis gen. et sp. nov. by including it in a comprehensive cladistic analysis of pleurodires. The new species is included within Botrhemydidae, with affinities to Bothremydini, positioned as sister group of Rosasia soutoi. Inaechelys pernambucensis gen. et sp. nov. differs from R. soutoi for the almost straight anterior lobe cranial edge of its plastron, as well as for its pentagonal shaped entoplastron and its abdominal shield midline, which is considerably smaller than the respective femoral shield midline. Inaechelys pernambucensis is the first turtle species formally described from Brazilian Paleocene strata. Within Bothremydidae, it is also the first conclusively fully marine species described for this country. This new record contributes to the understanding of the ecology and paleobiogeographical distribution of Bothremydidae family.

Atolchelys lepida, a new side-necked turtle from the Early Cretaceous of Brazil and the age of crown Pleurodira.

We report a new pleurodiran turtle from the Barremian Morro do Chaves Formation, Sergipe-Alagoas Basin, Brazil. We tested the phylogenetic position of Atolchelys lepida gen. et sp. nov. by including it in a comprehensive cladistic analysis of pleurodires. The new species is a basal member of Bothremydidae and simultaneously the oldest unambiguous crown Pleurodira. The biogeographic and chronostratigraphic significance of the finding has implications for the calibration of molecular clocks studies by pushing back the minimum age of crown Pleurodira by more than 12 Ma (ca 125 Ma). The reanalysis of Pelomedusoides relationships provides evidence that the early evolution and relationships among the main lineages of side-necked turtles can be explained, at least partially, by a sequence of vicariance events.

Comparative analysis of pleurodiran and cryptodiran turtle embryos depicts the molecular ground pattern of the turtle carapacial ridge.

The turtle shell is a wonderful example of a genuine morphological novelty, since it has no counterpart in any other extant vertebrate lineages. The evolutionary origin of the shell is a question that has fascinated evolutionary biologists for over two centuries and it still remains a mystery. One of the turtle innovations associated with the shell is the carapacial ridge (CR), a bulge that appears at both sides of the dorsal lateral trunk of the turtle embryo and that probably controls the formation of the carapace, the dorsal moiety of the shell. Although from the beginning of this century modern genetic techniques have been applied to resolve the evolutionary developmental origin of the CR, the use of different models with, in principle, dissimilar results has hampered the establishment of a common mechanism for the origin of the shell. Although modern turtles are divided into two major groups, Cryptodira (or hidden-necked turtles) and Pleurodira (or side-necked turtles), molecular developmental studies have been carried out mostly using cryptodiran models. In this study, we revisit the past data obtained from cryptodiran turtles in order to reconcile the different results. We also analyze the histological anatomy and the expression pattern of main CR factors in a pleurodiran turtle, the red-bellied short-necked turtle Emydura subglobosa. We suggest that the turtle shell probably originated concomitantly with the co-option of the canonical Wnt signaling pathway into the CR in the last common ancestor of the turtle.

The hooked element in the pes of turtles (Testudines): a global approach to exploring primary and secondary homology.

The hooked element in the pes of turtles was historically identified by most palaeontologists and embryologists as a modified fifth metatarsal, and often used as evidence to unite turtles with other reptiles with a hooked element. Some recent embryological studies, however, revealed that this element might represent an enlarged fifth distal tarsal. We herein provide extensive new myological and developmental observations on the hooked element of turtles, and re-evaluate its primary and secondary homology using all available lines of evidence. Digital count and timing of development are uninformative. However, extensive myological, embryological and topological data are consistent with the hypothesis that the hooked element of turtles represents a fusion of the fifth distal tarsal with the fifth metatarsal, but that the fifth distal tarsal dominates the hooked element in pleurodiran turtles, whereas the fifth metatarsal dominates the hooked element of cryptodiran turtles. The term 'ansulate bone' is proposed to refer to hooked elements that result from the fusion of these two bones. The available phylogenetic and fossil data are currently insufficient to clarify the secondary homology of hooked elements within Reptilia.

Embryonic remnants of intercentra and cervical ribs in turtles

SummaryA broad sample of extant turtles possesses a series of paired bones in the neck that are situated between the cervical vertebrae. These paired bones were originally proposed to be cervical rib remnants, but have more recently been interpreted as vestiges of intercentra. Here, we document, for the first time, the neck development of a pleurodire turtle, Emydura subglobosa, and identify blastematous structures, which partially recapitulate the ribs and intercentra of the plesiomorphic tetrapod condition. We identify blastematous “bridges” between intercentra and the corresponding ribs, which we homologize with the vestiges visible in extant turtles and with the remnant parapophyseal articulation processes of the intercentra of some stem taxa. Only the unpaired, median part of the intercentrum of the atlas is retained in adult turtles, but intercentra are recapitulated along the entire vertebral column during development; they are embedded in the cervical myosepta and serve as attachment sites for neck musculature. We also identify two rib rudiments in the occipital region, which may indicate that at least two vertebrae are integrated into the cranium of turtles in particular, and of amniotes in general.

Anatomy of the fully formed chondrocranium of Podocnemis unifilis (Pleurodira: Podocnemididae)

AbstractThis study describes the anatomy of the chondrocranium of Podocnemis unifilis (Pleurodira, Podocnemididae), based on recently hatched specimens, and cleared and double‐stained specimens. The orbitotemporal region is dramatically different from those observed for other species of turtles in that the: (1) planum supraseptale is greatly reduced and present only as tiny projections on the posterodorsal margin of the interorbital septum, (2) pila metoptica is free from all neighbouring structures and bifurcates distally, (3) pila antotica is greatly reduced, (4) foramina for optic nerve, ophthalmic artery and oculomotor nerves are open dorsally by virtue of this species lacking the taenia marginalis and taenia medialis, and (5) tectum synoticum is present and invested dorsally by the supraoccipital, despite the fact that this bone forms by replacement of the supraoccipital. The unique morphology of the pila metoptica is explained either as de novo formation of processes on the terminus of this cartilage or by retention of portions of the taenia medialis (anteriorly) and pila antotica or pila accessoria (posteriorly). Variation in the orbitotemporal region presented here is discussed for two other pleurodiran turtles (Phrynops hilarii and Emydura subglobosa) and briefly compared with the anatomy observed in Cryptodira.

A ZZ/ZW microchromosome system in the spiny softshell turtle, Apalone spinifera, reveals an intriguing sex chromosome conservation in Trionychidae

Reptiles display a wide diversity of sex-determining mechanisms ranging from temperature-dependent sex determination (TSD) to genotypic sex determination (GSD) with either male (XY) or female (ZW) heterogamety. Despite this astounding variability, the origin, structure, and evolution of sex chromosomes remain poorly understood. In turtles, TSD is purportedly ancestral while GSD arose multiple times independently. Here we test whether independent (XY or ZW) or morphologically divergent heterogametic sex chromosome systems evolved in tryonichids (Cryptodira) using the GSD spiny softshell turtle, Apalone spinifera, a species with previously unidentified sex chromosomes. A female-specific signal from comparative genomic hybridization (CGH) was detected in a Giemsa/4',6-diamidino-2-phenylindole faint portion of a microchromosome, indicating the presence of a ZZ/ZW system in A. spinifera. In situ hybridization of a fluorescently labeled 18S rRNA probe identified a large nucleolar organizer region block in the female-specific region of the W (co-localizing with the female-specific CGH signal) and a smaller block on the Z. The heteromorphic ZZ/ZW micro-sex chromosome system detected here is identical to that found in another tryonichid, the Chinese softshell turtle Pelodiscus sinensis, from which A. spinifera diverged ∼95 million years ago. These results reveal a striking sex chromosome conservation in tryonichids, compared to the divergent sex chromosome morphology observed among younger XX/XY systems in pleurodiran turtles. Our findings highlight the need to understand the drivers behind sex chromosome lability and conservation in different lineages and contribute to our knowledge of sex chromosome evolution in reptiles and vertebrates.