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The Endocranial Anatomy of the Stem Turtle Naomichelys Speciosa from the Early Cretaceous of North America

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The Endocranial Anatomy of the Stem Turtle Naomichelys Speciosa from the Early Cretaceous of North America The endocranial anatomy of the stem turtle Naomichelys speciosa from the Early Cretaceous of North America ARIANA PAULINA-CARABAJAL, JULIANA STERLI, and INGMAR WERNEBURG Paulina-Carabajal, A., Sterli, J., and Werneburg, I. 2019. The endocranial anatomy of the stem turtle Naomichelys spe- ciosa from the Early Cretaceous of North America. Acta Palaeontologica Polonica 64 (4): 711–716. Fossil turtles are one of the least studied clades in regard to endocranial anatomy. Recently, the use of non-invasive technologies, such as radiographic computed tomography (CT), increased the knowledge of the neuroanatomy of several extinct and extant taxa. Here, we provide the description of the nasal cavity, cranial endocast, and inner ear of the stem turtle Naomichelys speciosa based on digital 3D reconstructions. This terrestrial form is characterized by a nasal cavity with anteroposteriorly elongated vestibulum and a large cavum nasi proprium, traits typically related to terrestrial habits. The large olfactory region of the cavum nasi proprium suggests that olfaction was probably the most important sense for this species. Our description of N. speciosa adds novel information to the knowledge of endocranial anatomy in early turtle evolution and provides an important foundation for future analyses and comparisons. Key words: Reptilia, Helochelydridae, cranial endocast, paleoneurology, Mesozoic, North America. Ariana Paulina-Carabajal [[email protected]], INIBIOMA, Universidad Nacional del Comahue, CONICET, Quintral 1250, San Carlos de Bariloche (8400), Argentina. Juliana Sterli [[email protected]], CONICET-Museo Paleontológico Egidio Feruglio, Av. Fontana 140, 9100 Trelew, Argentina. Ingmar Werneburg [[email protected]], Senckenberg Centre for Human Evolution and Palaeoenvi- ronment (HEP) an der Eberhard Karls Universität, Sigwartstraße 10, 72076 Tübingen, Germany; Fachbereich Geow- issenschaften, Eberhard-Karls-Universität, Hölderlinstraße 12, 72074 Tübingen, Germany. Received 5 February 2019, accepted 9 May 2019, available online 16 September 2019. Copyright © 2019 A. Paulina-Carabajal et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License (for details please see http://creativecommons.org/licenses/by/4.0/), which permits unre- stricted use, distribution, and reproduction in any medium, provided the original author and source are credited. for comparative purposes, Lautenschlager et al. (2018) pre- Introduction sented an endocranial reconstruction of N. speciosa in lateral view. Here, we provide new anatomical information about this Members of Helochelydridae are large-bodied stem tur- species with a detailed description of its endocranial anatomy tles with terrestrial habits, characterized by their noticeable based on a digital 3D model, which includes a partially pre- dermatocranial bone ornamentation, formed by tubercles served endocast, a right inner ear, and the nasal cavity. (Fig. 1A1, A2). Helochelydrids are present in North America The endocranial morphology in turtles is still under- and in Europe since the Tithonian and up to the Maastrichtian explored (see Paulina-Carabajal et al. 2017 for a detailed (Joyce et al. 2011). In particular, Naomichelys speciosa Hay, history). Some neuroanatomical studies have been con- 1908 is the only known helochelydrid species present in North ducted on extant turtles, but they are isolated attempts and America and it has been recognized in different localities the taxon sampling is not yet inclusive (e.g., Bojanus 1819; ranging from the Aptian to the Campanian (Joyce et al. 2011; Ogushi 1913; Edinger 1929, 1934; Zangerl 1960; Gaffney Joyce 2017). Hay (1908) originally named N. speciosa based and Zangerl 1968; Wyneken 2001; Deantoni et al. 2012). on an isolated entoplastron. Recently, Joyce et al. (2014) pro- The situation is similar when extinct taxa are considered, vided a detailed description of a complete specimen (FMNH although this has been changing in recent years with the PR273) assigned to N. speciosa and provided some endocra- use of CT-scans (e.g., Georgi 2008; Paulina-Carabajal et al. nial descriptions based on CT-scans. However, different re- 2013a, b; Ferreira et al. 2018). The use of this non-invasive searchers partially studied this specimen before. Hirayama et technique for the study of the neuroanatomy in fossil rep- al. (2000) illustrated the carapace of FMNH PR273. Barrett et tilian taxa dates back to the late 1990’s (e.g., dinosaur brain al. (2002) described a limb with osteoderms, and Scheyer and studies by Rogers 1998; Knoll et al. 1999), but only recently Anquetin (2008) presented its shell bone histology. Recently, it has been used to explore the endocranial cavities (particu- Acta Palaeontol. Pol. 64 (4): 711–716, 2019 https://doi.org/10.4202/app.00606.2019 712 ACTA PALAEONTOLOGICA POLONICA 64 (4), 2019 A A A cartilaginous 1 2 3 rider cavum nasi fossa orbitalis proprium apertura narium canalis incisura cavernosus vestibulum externa internal nasi columella auris carotid ductus nasopharyngeus B fossa B B 1 orbitalis 2 3 vestibulum cartilaginous cavum nasi nasi rider proprium apertura nasal duct narium cranial externa impression of nerve XII inner ear median septum cavum acustico-jugulare condylus 50 mm mandibularis foramen structure 4 C1 C2 C3 internal view cavum skull roof acustico-jugulare cranial vestibulum nerve V nasi condylus occipitalis internal ductus carotid nasopharyngeus foramen posterior canalis carotici interni Fig. 1. Digitally rendered skull and endocranial anatomy of helochelydrid turtle Naomichelys speciosa Hay, 1908 (FMNH PR273) from the Early Cretaceous (Aptian/Albian) Trinity Group, Texas; in lateral (A), dorsal (B), and ventral (C) views. Surface reconstruction of the skull (A1–C1), cranial endocast including brain, inner ear, canalis cavernosus, and nasal cavity in situ with the bone rendered semi-transparent to allow observation of internal structures (A2–C2), isolated endocasts (A3–C3). larly those occupied by brain and inner ear) of extinct turtles pher (Phoe nix v|tome|x). In total, 675 slices were obtained (Paulina-Carabajal et al. 2013a, 2017; Lautenschlager et al. using a voltage of 150 kV and a current of 170 mA. The 2018; Evers and Benson 2019; Evers et al. 2019). voxel size is x = 1068 pixels and y = 1382 pixels. Our main goal was to describe in detail the endocranial Since the anteroventral region of the snout is ossified, a anatomy of N. speciosa, which was only preliminarily studied complete turtle cranial endocast includes the space occupied so far (Paulina-Carabajal et al. 2013b; Lautenschlager et al. by the encephalic structures proper, plus most of the cast 2018: fig. 2). Special emphasis is devoted to the nasal cavity of the nasal duct and the nasal cavity anteriorly (Paulina- due to its particularly large development in terrestrial turtles. Carabajal et al. 2019). Although the skull of N. speciosa is more or less com- Institutional abbreviation.—FMNH, Field Museum of Natu- plete and preserved in 3D (Joyce et al. 2014; Fig. 1), it has ral History, Chicago, USA. some missing regions that had been reconstructed with plas- ter, which is clearly distinguishable from the bone in the μCT scan. These regions include parts of the skull roof and, Material and methods therefore, the osseous correlates of the olfactory bulbs. Also the cerebral hemispheres are not observed in the cranial en- Specimen FMNH PR273 of Naomichelys speciosa was docast, such as the forebrain and the nasal canal connecting found in the Early Cretaceous (Aptian/Albian) Trinity Group the olfactory bulbs posteriorly and the nasal cavity anteri- in Texas, USA. The μCT scan of the skull of Naomichelys orly (Fig. 1A3). speciosa (FMNH PR273) was made at the Department of Anatomical nomenclature follows Gaffney (1979) for Prehistory and Archeological Sciences of the University of skull, and non-preserved soft tissue anatomy observed in Tübingen (Tü bin gen, Germany) using a medical tomogra- the cranial endocast follows Witmer et al. (2008). PAULINA-CARABAJAL ET AL.—ENDOCRANIAL ANATOMY OF LATE CRETACEOUS TERRESTRIAL TURTLE 713 canalis inner Descriptions and comparisons stapedio- cartilaginous rider ear temporalis Endocast of the nasal cavity.—The three portions of the medulla A1 oblongata cavum nasi vertebrate nasal cavity (blue in Figs. 1, 2) (see Parsons proprium 1959, 1970) are recognized in the endocast of Naomichelys speciosa: the vestibulum nasi, the cavum nasi proprium, and the ductus nasopharyngeus (Figs. 1A3, 2A1). Worth mentioning is the clear separation of the vestibulum nasi from the cavum nasi proprium and the relatively large canalis cavernosus development of the former (Figs. 1A2, A3, B2, B3, 2A1). 4 ductus vestibulum A well-developed vestibulum nasi is associated with an internal nasopharyngeus nasi elongate nose, as in Chelus fimbriata, trionychids, and carotid canalis Carettochelys insculpta (Parsons 1970). The vestibulum semicircularis nasi is also large in the extinct terrestrial meiolaniids crus anterius communis A (Paulina-Carabajal et al. 2017), and in the extant terres- canalis cavum nasi 2 semicircularis nasal duct proprium trial Gopherus berlandieri (Paulina-Carabajal et al. 2017), posterius vestibulum Macrochelys temminckii (Lautenschlager et al. 2018: fig. 3) nasi and Malacochersus tornieri (Maunter et al. 2017). Since the external nasal gland in extant reptiles arises from the cranial nerve V posterior portion of the vestibulum nasi (Parsons 1970), the anterior
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