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Year: 2019

With plates and spikes - the heavily armoured Eusaurosphargis aff. dalsassoi

Scheyer, Torsten M ; Klein, Nicole ; Sichelschmidt, Olivier ; Neenan, James M ; Albers, Paul

Abstract: Besides the wealth of nothosaur and pachypleurosaur fossils from the Vossenveld Formation, there are fi ndings of bones that show very peculiar shapes, not easily attributable to the aforementioned groups. Among these are vertebrae with very long transverse processes, curved dorsal ribs with broadened portions known as uncinate processes, and peculiar shaped dermal armour (generally referred to as osteoderms), usually in the form of small bony cones. For a long time, the identity of these bones remained obscure, but lately, there is increasing evidence that all those materials belong to a single enigmatic diapsid, Eusaurosphargis, known from several European fossil localities.

Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-181071 Journal Article Published Version

Originally published at: Scheyer, Torsten M; Klein, Nicole; Sichelschmidt, Olivier; Neenan, James M; Albers, Paul (2019). With plates and spikes - the heavily armoured Eusaurosphargis aff. dalsassoi. Staringia, 16(5/6):216-222. A B

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FIGURE 1. | Specimens of Eusaurosphargis dalsassoi from the Middle Triassic of the Alpine region. A-E, selected bones (not to scale) of the holotype specimen BES SC 390 from Besano, Italy. A, caudal (tail) vertebra with conical osteoderm sitting on the neural spine. B, isolated osteoderm from the lateral side of the trunk. C, two anterior thoracic ribs with wide uncinate processes. D, thoracic vertebra with elongated transverse processes in dorsal (top) view. E, dentary of the left lower jaw carrying characteristic teeth with distinctive curved crowns. F, specimen PIMUZ A/III 4380 from the Ducan area, Switzerland (Image from Scheyer et al., 2017). G, life reconstruction of Eusaurosphargis, mainly based on PIMUZ A/ III 4380. Note that the article of Scheyer et al. (2017) and its online supplement were published by Scientifi c Reports under Creative Commons Attribution 4.0 International License and can be accessed freely via https://doi.org/10.1038/ s41598-017-04514-x.

20 1 6 G RONDBOOR & H AMER With plates and spikes - the heavily armoured Eusaurosphargis a ff . dalsassoi U vindt een samenvatting aan het eind van dit artikel.

TORSTEN M. SCHEYER1, Besides the wealth of nothosaur and pachypleurosaur fossils from the Vossen- NICOLE KLEIN2, veld Formation, there are fi ndings of bones that show very peculiar shapes, not OLIVER SICHELSCHMIDT3, easily attributable to the aforementioned groups. Among these are vertebrae JAMES M. NEENAN4, with very long transverse processes, curved dorsal ribs with broadened PAUL ALBERS5 portions known as uncinate processes, and peculiar shaped dermal armour (generally referred to as osteoderms), usually in the form of small bony cones. 1UNIVERSITÄT ZÜRICH, PALÄONTOLO- For a long time, the identity of these bones remained obscure, but lately, GISCHES INSTITUT UND MUSEUM, there is increasing evidence that all those materials belong to a single enig- KARL SCHMID-STRASSE 4, 8006 matic diapsid, Eusaurosphargis, known from several European fossil localities. ZURICH, SWITZERLAND Previous works 2ABTEILUNG PALÄONTOLOGIE, In a previous overview work on the fauna recovered in the sediments exposed INSTITUT FÜR GEOWISSENSCHAFTEN, in Winterswijk, the peculiarly shaped bones mentioned above were thought to UNIVERSITÄT BONN, GERMANY possibly belong to ‘Saurosphargis’ (e.g., Oosterink et al., 2003). This was accom- 3WORKGROUP MUSCHELKALK panied by a note that this taxon, ‘Saurosphargis’, might be synonymous with the WINTERSWIJK, DUTCH GEOLOGICAL placodont Paraplacodus broilii Peyer, 1931, which is well known from the Middle SOCIETY, Triassic World Heritage Site Monte San Giorgio, Ticino, Switzerland (Peyer, WINTERSWIJK, THE NETHERLANDS 1931; Kuhn-Schnyder, 1942; Rieppel, 2000). Unfortunately, the holotype of Saurosphargis volzi Huene, 1936, a partial postcranial skeleton preserving mostly 4OXFORD UNIVERSITY MUSEUM OF part of the trunk, was lost during WWII and thus cannot be studied anymore. NATURAL HISTORY, PARKS ROAD, Furthermore, due to the lack of diagnostic features of that partial skeleton, some OXFORD OX1 3PW, UK authors consider the genus and species as a ‘nomen dubium’ (e.g., Nosotti & 5NATURALIS BIODIVERSITY CENTER, Rieppel, 2003; Scheyer et al., 2017). Concerning Oosterink et al.’s (2003) LEIDEN, THE NETHERLANDS statement above, it is noteworthy that both Paraplacodus and ‘Saurosphargis’ share similarities in vertebral and rib anatomy, but they also differ in an important aspect. For example, both taxa have trunk ribs carrying uncinate processes (Huene, 1936; Rieppel, 2000), but whereas dermal armour is completely lacking in all known specimens of Paraplacodus, the holotype of ‘Saurosphargis’ had osteoderms associated with the uncinate processes of its ribs.

With the description of a new 'Saurosphargis'-like taxon from the early Middle Triassic of southern China, Sinosaurosphargis yunguiensis (Li et al., 2011), the species 'Saurosphargis volzi' was recently resurrected and the family Saurosphargidae was erected (Li et al., 2011). In that study, yet undescribed material proposedly referable to 'Saurosphargis' from the Lower Muschelkalk of Winterswijk was mentioned as “(Paul Albers, pers. comm.)”. Since then, the additional sauro- sphargid taxa Largocephalosaurus polycarpon (Cheng et al., 2012) and L. qianensis (Li et al., 2014) have been described from the Middle Triassic of Yunnan and Guizhou Provinces in southern China, which are very similar in anatomy to the European 'Saurosphargis'.

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FIGURE 2. | Main matrix block NMNHL RGM 449487 with bone accumulation including a basal pistosauroid skeleton, a skull fragment of Anarosaurus heterodontus, as well as scattered postcranial bones identifi able as belonging to Eusaurosphargis (see also Sander et al., 2014: Fig. 3). A, photograph of the matrix block. B, sketch of the bones with the bones of Eusaurosphargis highlighted in grey. C, kidney-shaped coracoid with the notch of the (open) coracoid ‘foramen’ on the right side. D, left ischium with strongly concave anteromedial margin. The bone is partially overlapped by a rod-like bone (possibly a caudal transverse process). E, thoracic vertebra with elongated transverse processes in dorsal view (anterior is towards the top). F, caudal (tail) vertebra with conical osteoderm sitting on the neural spine. G, two thoracic vertebrae, the upper one in dorsal view, the lower in angled view, topped by a conical osteoderm. H, two thoracic vertebrae with elongated transverse processes in ventral (bottom) view. I, long bones (femur and humerus), with a thoracic vertebra with osteoderm lying in between. Abbreviations: f, foramen; fe, femur; hu, humerus; o, osteoderm.

In 2014, a study by a Dutch-German blished, focussing on associated skeletal remains being preserved close together research team lead by Martin Sander on one slab (NMNHL RGM 449487). Sander et al. (2014) identifi ed three taxa: from the University of Bonn was pu- articulated remains were found pertaining to the pistosauroid cf. Cymatosaurus,

02 1 8 G RONDBOOR & H AMER an isolated fragmentary skull belonging to the pachypleurosaur Anarosaurus slabs belong that largely contain further heterodontus, and the remaining scattered postcranial bones belonging to the bones of Eusaurosphargis and which are enigmatic diapsid aff. Eusaurosphargis. The latter taxon was identifi ed based on housed in Naturalis. In addition, nume- the vertebrae carrying elongated transverse processes and the presence of conical rous remains of isolated vertebrae with osteoderms. The authors provided a solid anatomical description and comparison, elongated transverse processes with or which supports their taxonomic interpretation of the fossils. Sander et al. (2014) without associated osteoderms, ribs thus also refuted a previous assessment of the very same fossils by Diedrich and with uncinate processes, as well as iso- Gradinaru (2013) to taxa known mostly from the Alpine Triassic. In the same lated osteoderms are known that are year, two types of isolated broadened dorsal rib morphologies from Winterswijk housed in the collections of Naturalis with more or less strongly developed uncinate processes were identifi ed and and TWE or private collections. compared to other European fossil material (Klein & Sichelschmidt, 2014). The authors concluded that the majority of the ribs were referable to Eusauro- There are several groups of animals sphargis as well. The question arises of course what this enigmatic Eusaurosphargis that show elongated transverse pro- really is and whether part of specimen NMNHL RGM 449487, as well as the cesses of their dorsal vertebrae. Among other remains from Winterswijk displaying this peculiar vertebral and rib extant reptiles, the mid- and posterior morphology, can be confi dently referred to this taxon. trunk vertebrae can become quite elongated in crocodylians. In the Current taxonomic identifi cation fossil record, however, the armoured So far, Eusaurosphargis was mainly described from Alpine Triassic localities (Fig. 1). placodonts (i.e., Cyamodus spp.) with- The genus and species Eusaurosphargis dalsassoi, a small to medium-sized animal in Sauropterygia might be viewed as that might have reached 1.5 to 2 m in body length, was fi rst described based on an extreme form, with most of their scattered remains of a sub-adult specimen (BES SC 390) found in the Middle trunk below the wide carapace being Triassic of Besano, Italy (Nosotti & Rieppel, 2003). Although much of the supported by the transverse processes anatomy of the species became thus known, other aspects remained obscure due rather than ribs; the latter can be to incomplete and scattered preservation of the bones. A complete and well- rudiments restricted to the lateral preserved skeleton (except the skull) from a small individual (PIMUZ A/III 4380) body wall (Scheyer, 2010). In Eusau- from the Middle Triassic sediments (Prosanto Formation) of the Ducan area, rosphargis, the transverse processes are Switzerland, was found to increase the overall understanding of the species’ also strongly elongated, but the ribs anatomy further and allowed, for the fi rst time, a life reconstruction and better are not reduced as in Cyamodus interpretation of its palaeoecology (Scheyer et al., 2017). Based on the extreme but rather robust, carrying isolated scarcity of Eusaurosphargis in Alpine Triassic localities in Switzerland and Italy osteoderms atop their uncinate pro- that yielded hundreds of other, similar-sized marine reptiles (i.e., pachypleuro- cesses. In this regard, Eusaurosphargis saurs, nothosaurs), as well as osteological features including stout limbs with resembles more closely the condition widened terminal phalanges, the authors argued for a terrestrial lifestyle. seen in the Chinese saurosphargids Sinosaurosphargis and Largocephalosaurus The study of Scheyer et al. (2017) also relied to a large degree on facilitating (Cheng et al., 2012; Li et al., 2014). One micro-computed tomography scanning of the fossil and subsequent three- might speculate that the elongation of dimensional reconstruction and modelling on powerful computer workstations. the transverse processes could be linked Due to the excellent and almost completely undisturbed preservation of PIMUZ to the development of body armour A/III 4380, the association of the different aspects of the complex dermal as this would increase rigidity in the armour and the underlying endoskeletal bones could be studied in detail. dorsal part of the trunk and likely As such, conical or spiked osteoderms were found associated with vertebrae, serve as muscle attachment sites in the ribs, and the girdles, whereas fl at or keeled osteoderms were found associated aforementioned groups, but to our with the forelimbs and the lateral edges of the gastralia. Previous systematic knowledge the elongation of transverse works found Eusaurosphargis either as sister taxon to the large and enigmatic processes and its functional implica- marine reptile Helveticosaurus from the Besano Formation at Monte San Giorgio, tions has so far received little attention. Switzerland (Nosotti & Rieppel 2003; Li et al., 2011), or to Hanosaurus from the Early to Middle Triassic Jialingjiang Formation of China (Neenan et al., 2013; Eusaurosphargis further shares with the Cheng et al., 2016). The latest phylogenetic analysis, following the discovery non-cyamodontoid placodont Placodus and description of PIMUZ A/III 4380, recovered Helveticosaurus and Eusauro- the presence of a single row of osteo- sphargis, not in a monophyletic clade but as successive sister taxa to Sauropterygia derms over the neural spines (Drever- (Scheyer et al., 2017). Accordingly, though it has a similar name, these analyses mann, 1933; Jiang et al., 2008). In do not fi nd Eusaurosphargis forming a natural group (i.e., a monophyletic clade) Placodus, however, the triangular- with other Saurosphargidae known mainly from the Middle Triassic of China. shaped osteoderms fi t within the space between two adjacent transverse Eusaurosphargis from Winterswijk processes, whereas in Eusaurosphargis Based on the above, several specimens from Winterswijk can be assigned to the osteoderms sit directly on top of Eusaurosphargis. Until the Winterswijk material is further studied in detail, the fl at and low neural spines of the however, it is best to assign the materials to Eusaurosphargis aff. dalsassoi. precaudal vertebrae. These materials include disarticulated long bones, vertebrae, ribs, and osteoderms that are associated with the basal pistosauroid on slab NMNHL RGM 449487 Finally, it is noteworthy that some of (Sander et al., 2014). The collection number NMNHL RGM 449487 refers to a the Eusaurosphargis materials recovered main matrix block (Fig. 2) of a bone accumulation to which several smaller from Winterswijk, as exemplifi ed by the

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FIGURE 3. | Additional material assignable to Eusaurosphargis from Winterswijk stored at Naturalis. A, associated postcranial bones. B, thoracic rib with wide uncinate process. C, isolated thoracic vertebra with elongated transverse processes in ventral view. D, cervical vertebra (middle) with conical osteoderm and attached neck rib in left lateral view. Next to the vertebra, isolated neck ribs are visible. E, isolated conical osteoderm, possibly from the shoulder region, showing broad sculptured base. bones on slab NMNHL RGM 449487, (see Sander et al., 2014), indicating that this specimen is more than 30 % larger are distinctly larger than the material than the holotype specimen BES SC 390. Other material from Winterswijk from Italy and Switzerland and thus (Fig. 3) is comparable in size to the Ducan specimen from Switzerland. likely represent different ontogenetic stages of this animal. For the holotype In conclusion, although no complete skeleton has been recovered in Winters- of E. dalsassoi, originally described as wijk so far, and even partially associated materials are rare, there are several a subadult, the width of the larger trunk specimens known that can be assigned to the diapsid Eusaurosphargis aff. dalsassoi vertebrae measured over the transverse (Nosotti & Rieppel, 2003) based on their peculiar morphology. processes would be 31-33 mm (see Nosotti & Rieppel, 2003); that of a Abbreviations mid-trunk vertebra in the juvenile BES, Palaeontological Collection of the Museo Civico di Storia Naturale di specimen from Ducan area ca. 23 mm. Milano, Italy; NMNHL, National Museum of Natural History (NCB Naturalis), In contrast, the larger, well-preserved Leiden, The Netherlands; PIMUZ, University of Zurich, Palaeontological trunk vertebrae known from NMNHL Institute and Museum, Zurich, Switzerland; TWE, Museum TwentseWelle, RGM 449487 measure about 45 mm Enschede, The Netherlands.

02 2 0 G RONDBOOR & H AMER Acknowledgements taxon en zijn verwantschappen aan We thank all curators of the aforementioned collections for access to specimens. andere taxa, in het bijzonder aan de Furthermore, we would like to thank Sibelco Europe MineralsPlus Winterswijk placodont Paraplacodus broilii, waar het and the members of the Muschelkalk Workgroup, Winterswijk, for their various nauw verwant aan wordt geacht. Sinds- supports. Martin Sander is acknowledged for long-term support and discussions, dien is er echter een veel completer fos- Olaf Dülfer and Natascha Makschinski for skilful preparation, and Georg siel ontdekt op de Monte San Georgio Oleschinski (all IGM Bonn) for outstanding photographs of the Winterswijk met opvallende overeenkomsten met specimens. Finally, we thank Martijn Guliker for reviewing the draft, Stephan Saurosphargis. Dit complete maar ver- Spiekman for discussions, and the editors for their efforts in putting this updated spoelde fossiel is toegewezen aan het format on the Winterswijk locality in honour of Henk Oosterink together. nieuwe taxon Eusaurosphargis dalsassoi. Recentelijk is een nieuw fossiel van Abstract deze soort in de Prosanto Formatie in Saurosphargis voltzi was described based on a fragmentary specimen, which was lost de Ducan regio in Zwitserland ontdekt. during WWII. Because of this, the nature of this taxon and its exact relationships, Het postcraniale skelet is compleet en particularly to the placodont Paraplacodus broilii to which it was considered to be gearticuleerd, wat ons een goed beeld closely related, are unclear. However, since then, a much more complete fossil van het uiterlijk van dit dier geeft. Ver- has emerged from Monte San Georgio that exhibits striking similarities with dere kennis omtrent deze soort komt uit Saurosphargis. This complete but disarticulated fossil was assigned to the new vergelijkingen met fossielen uit China, taxon Eusaurosphargis dalsassoi. Recently, a fossil assigned to this species from the zoals Sinosaurosphargis en Largocephalo- Prosanto Formation has been found in the Ducan region of Switzerland. The post- saurus. Deze Chinese fossielen helpen cranial skeleton is completely intact, allowing us a good insight into the appea- ons te begrijpen hoe de karakteristieke rance of the animal. Further knowledge about this species comes from compari- bepantsering van deze dieren, met de son with fossils from China, such as Sinosaurosphargis and Largocephalosaurus. zijdelings uitgegroeide wervels, been- These Chinese fossils help us understand how the characteristic armour of these platen en stekels, functioneel in elkaar animals, with the transversely elongated vertebral processes, bone plates, and zit. In de Vossenveld Formatie van spines, is functionally put together. In the Vossenveld Formation of Winters- Winterswijk worden fossielen gevonden wijk, fossils are found that we can best describe as Eusaurosphargis aff. dalsassoi. die we het beste kunnen beschrijven Further research may change this, in particular, because many of the fossils from als Eusaurosphargis aff. dalsassoi. Verder Winterswijk are much larger than the specimens known from E. dalsassoi. onderzoek zal daar mogelijk verande- ring in brengen, met name omdat Samenvatting nogal wat fossielen uit Winterswijk Saurosphargis voltzi is beschreven op basis van een fragmentarisch exemplaar dat veel groter zijn dan de exemplaren die verloren is gegaan tijdens WOII. Hierdoor is er veel onduidelijkheid over dit van E. dalsassoi bekend zijn.

REFERENCES origin of placodont marine reptiles and the of a basal Pistosauroidea (Sauropterygia) evolution of crushing dentition in Placodontia. from the Lower Muschelkalk of Winters- - Jiang, D.Y., Motani, R., Hao, Nature Communications 4, 1621 [doi: wijk, The Netherlands. Paläontologische W.C., Rieppel, O., Sun, Y.L., 10.1038/ncomms2633]. Zeitschrift 88(1), pp. 55-71. Schmitz, L., Sun, Z.Y., 2008. First record of Placodontoidea (Reptilia, - Nosotti, S. and Rieppel, O., 2003. - Scheyer, T.M., 2010. New interpre- Sauropterygia, Placodontia) from the Eusaurosphargis dalsassoi n. gen. n. sp., tation of the postcranial skeleton and overall Eastern Tethys. Journal of Vertebrate a new, unusual diapsid reptile from the body shape of the placodont Cyamodus Paleontology 28(3), pp. 904-908. Middle Triassic of Besano (Lombardy, N hildegardis Peyer, 1931 (Reptilia, Italy). Memorie della Società Italiana di Sauropterygia). Palaeontologia Electronica - Klein, N. & Sichelschmidt, O.J., Scienze Naturali e del Museo Civico di 13(2), 15A:15p [http://palaeo-electroni- 2014. Remarkable dorsal ribs with distinct Storia Naturale di Milano 31(3), pp. 3-33. ca.org/2010_2/232/index.html]. uncinate processes from the early Anisian of the Germanic Basin (Winterswijk, - Oosterink, H.W., Berkelder, W., - Scheyer, T.M., Neenan, J.M., The Netherlands). Neues Jahrbuch für de Jong, C., Lankamp, J., Winkel- Bodogan, T., Furrer, H., Obrist, Geologie und Paläontologie, Abhand- horst, H., 2003. Sauriërs uit de onder- C., Plamondon, M., 2017. A new, lungen 271(3), pp. 307-314. muschelkalk van Winterswijk. Tilburg: exceptionally preserved juvenile specimen Nederlandse Geologische Vereniging of Eusaurosphargis dalsassoi (Diapsida) - Li, C., Jiang, D.Y., Cheng, L., [Staringia 11, Grondboor & Hamer 57, 1a]. and implications for Mesozoic marine diapsid Wu, X.C., Rieppel, O., 2014. phylogeny. Scientifi c Reports 7:4406 A new species of Largocephalosaurus - Rieppel, O., 2000. Paraplacodus and [doi: 10.1038/s41598-017-04514-x]. (Diapsida: Saurosphargidae), with im- the phylogeny of the Placodontia (Reptilia: plications for the morphological diversity Sauropterygia). Zoological Journal of the The full list of references can be found at: and phylogeny of the group. Geological Linnean Society 130, pp. 635-659. http://www.geologienederland.nl > Magazine 151(1), pp. 100-120. Grondboor & Hamer > Staringia 16. - Sander, P.M., Klein, N., Albers, De volledige literatuurlijst is te vinden op: - Neenan, J.M., Klein, N., P.C.H., Bickelmann, C., Winkel- http://www.geologienederland.nl > Scheyer, T.M., 2013. European horst, H., 2014. Postcranial morphology Grondboor & Hamer > Staringia 16

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