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Identification of the French Upper Cretaceous bothremydid turtle Foxemys mechinorum in the Spanish record
Geobios 51 (2018) 211–217
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Original article
Identification of the French Upper Cretaceous bothremydid turtle Foxemys mechinorum in the Spanish record§ Ada´n Pe´rez-Garcı´a *, Francisco Ortega Grupo de Biologı´a Evolutiva, Facultad de Ciencias, UNED, Paseo Senda del Rey, 9, 28040 Madrid, Spain
A R T I C L E I N F O
A B S T R A C T
Article history: Received 11 January 2018 Accepted 17 April 2018 Available online 20 April 2018
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.
C 2018 Elsevier Masson SAS. All rights reserved.
Keywords: Pleurodira Bothremydidae Lo Hueco fossil site Campanian-Maastrichtian Phylogeny Paleobiogeography
1. Introduction Bothremydidae is the best-represented group of turtles in the coastal and freshwater ecosystems of the Upper Cretaceous of southwestern Europe (Lapparent de Broin, 2001; Gaffney et al., 2006; Pe´rez-Garcı´a, 2017b). The knowledge about the diversity and distribution of this lineage of Pleurodira in this region has improved markedly over the last twenty years (Tong et al., 1998; Lapparent de Broin and Murelaga, 1996, 1999; Laurent et al., 2002; Pe´rez-Garcı´a et al., 2012; Pe´rez-Garcı´a, 2016, 2017a). Bothremydidae is a group of Gondwanian origin, which reached Europe through several diachronic dispersion events (Pe´rez-Garcı´a, 2017b). The oldest evidence of this lineage in this continent corresponds to the record of the Bothremydina (Bothremydini) Algorachelus peregrinus Pe´rez-Garcı´a, 2017a, recognized in both the uppermost middle-lowermost upper Cenomanian of Algora (Guadalajara Province, Central Spain) and the middle Cenomanian
§
Corresponding editor: Gilles Escarguel. * Corresponding author. E-mail address: [email protected] (A. Pe´rez-Garcı´a).
https://doi.org/10.1016/j.geobios.2018.04.002 C 2018 Elsevier Masson SAS. All rights reserved. 0016-6995/
of Nazare´ (Central Portugal) (Pe´rez-Garcı´a, 2017a; Pe´rez-Garcı´a et al., 2017). The Campanian-Maastrichtian record of southwestern Europe includes a member of Taphosphyini (i.e., Taphrosphys ambiguus (Gaudry, 1890), represented by a single specimen from the Maastrichtian of the French locality of Mont-Aime´; Broin, 1977; Martin and Delfino, 2010; Pe´ rezGarcı´ a, 2016), as well as several representatives of Bothremydini. Rosasia soutoi Carrington da Costa, 1940 (Bothremydina) is recognized as an exclusive form of the Campanian-Maastrichtian record of Portugal (Carrington da Costa, 1940; Antunes and Broin, 1988; Pe´rez-Garcı´a, 2017b). Several members of the sister group of Bothremydina (i.e., Foxemydina) have been identified. The first bothremydid defined in the European record, Polysternon provinciale (Matheron, 1869), is an exclusive form of the French record, its presence having been only confirmed in Campanian levels of the south of this country (Matheron, 1869; Portis, 1882; Nopcsa, 1931; Broin, 1977; Gaffney et al., 2006). Two other forms so far identified as exclusive of the French record are recognized: Elochelys perfecta Nopcsa, 1931, from the Campanian of the Fuveau Basin, and Foxemys mechinorum Tong, Gaffney et Buffetaut, 1998, recognized in the upper Campanian-lower
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Maastrichtian of several sites of the south of France (Nopcsa, 1931; Tong et al., 1998; Pe´rez-Garcı´a et al., 2012). Polysternon atlanticum Lapparent de Broin et Murelaga, 1996, is exclusive of the Spanish record, being only identified in its type locality, the upper Campanian ˜o (Burgos Province) (Lapparent de Broin and Murelaga, site of Lan 1996, 1999; Pereda Suberbiola et al., 2015; Pe´rez-Garcı´a, 2017b). The only bothremydid from the Campanian-Maastrichtian record of southwestern Europe recognized in more than one country is Iberoccitanemys convenarum (Laurent, Tong et Claude, 2002). This form was defined by a single shell from the upper Maastrichtian of the French region of Haute-Garonne, subsequently recognized as a wellrepresented taxon in the upper Campanian-lower Maastrichtian site of Lo Hueco (Cuenca Province, Spain), and more recently having been ˜a (Segovia identified in the Spanish upper Campanian site of Armun Province) (Laurent et al., 2002; Pe´rez-Garcı´a et al., 2010, 2012, 2016). The tetrapod fauna from Lo Hueco has been identified as closely related to that of the synchronous record of France. In addition to the identification of several shared lineages, some genera, corresponding to different clades, have been identified in both regions. They correspond to the eusuchian crocodyliform Lohuecosuchus (L. megadontos being present in Lo Hueco), the ornithopod dinosaur Rhabdodon (with Rhabdodon sp. in Lo Hueco) and the sauropod dinosaur Ampelosaurus (Ampelosaurus sp. having been identified in this site) (Ortega et al., 2015). Therefore, the only species whose presence has been confirmed in both Lo Hueco and the French record is the bothremydid Iberoccitanemys convenarum. Lo Hueco is the Spanish site of the last Stages of the Upper Cretaceous that has yielded the most abundant record of Bothremydidae, and one of the few localities where articulated shells have been found (Pe´rez-Garcı´a, 2017b). In addition to the remains of Iberoccitanemys convenarum, a plastron of a second member of the Bothremydidae has been reported there (Pe´rezGarcı´a et al., 2013). Thus, Lo Hueco is the only European site where the synchronous and sympatric coexistence of two members of Bothremydidae is currently recognized. The scarce information so far available on this second form was exclusively based on an almost complete plastron which was attributed, in a preliminary way, to an indeterminate member of Foxemydina (Pe´rez-Garcı´a et al., 2013). New remains referable to this second form, also from Lo Hueco, are presented here. The study of these specimens allows us to identify this second form from Lo Hueco, at both generic and specific levels, expanding the knowledge about the diversity of Bothremydidae in the Spanish Upper Cretaceous record and that about the paleobiogeographical distribution of Foxemys mechinorum, so far considered endemic to France. Institutional abbreviations: HUE, Lo Hueco collection, Museo de Paleontologı´a de Castilla-La Mancha, Cuenca, Spain; MD, Muse´e des Dinosaures, Espe´raza, France.
2. Systematic palaeontology Testudines Batsch, 1788 Pleurodira Cope, 1864 Pelomedusoides Cope, 1868 Podocnemidoidea Cope, 1868 Bothremydidae Baur, 1891 Bothremydodda Gaffney, Tong et Meylan, 2006 Bothremydini Gaffney, Tong et Meylan, 2006 Foxemydina Gaffney, Tong et Meylan, 2006 Genus Foxemys Tong, Gaffney et Buffetaut, 1998 Foxemys mechinorum Tong, Gaffney et Buffetaut, 1998 Figs. 1, 2 Material: Two unpublished specimens, corresponding to an almost complete and disarticulated carapace, preserving the
articulate left ilium, HUE-8532 (Figs. 1, 2(A–H)), and an isolated nuchal plate, HUE-10218 (Fig. 2(I, J)), as well as an almost complete plastron, HUE-1220 (Fig. 2(K, L)), previously attributed to Foxemydina indet. by Pe´rez-Garcı´a et al. (2013). Locality and horizon: Lo Hueco fossil site (Fuentes, Cuenca Province, Castilla-La Mancha, Central Spain); Margas, Arcillas y Yesos de Villalba de la Sierra Formation (Ortega et al., 2015); upper Campanian-lower Maastrichtian. Description: The only plates not preserved in the carapace HUE-8532 are the sixth and seventh left peripherals and the sixth right peripheral (Fig. 1). Most plates of this specimen are disarticulated, except those corresponding to the following four areas: the nuchal and the first right peripheral; the first and second left peripherals; the first neural and the first left costal; and a fragment composed of the last two neurals, the fifth to eighth left costals, the seventh and eighth right costals, the suprapygal, the pygal, the eighth to eleventh left peripherals, and the eleventh right peripheral. The length of the complete carapace is identified as close to 52 cm. The outer surface of the plates shows an ornamental pattern consisting of dichotomic and discontinuous sulci, which are anastomosed, generating small and low polygons (Fig. 2(H)). This specimen lacks well-developed parallel striations, but some poorly developed striations are present in the medial region (Fig. 2(G)). The carapace is oval, markedly longer than wide. The maximum width is located about half its length. It lacks a nuchal embayment, and the anterior carapace margin is substraight (Fig. 1). The length of the nuchal plate is slightly greater than its width (Fig. 1). Seven neurals are present. The first is rectangular, longer than wide. The second to sixth neurals are hexagonal, with their anterolateral margins being shorter than the posterolateral. All these plates, except the sixth, are longer than wide. The seventh neural is pentagonal. The sagittal contact between the two posterior pairs of costals is observed. The first costal is approximately two times longer than the second. A pentagonal suprapygal plate is present. The anterior and posterior peripherals are noticeably longer than wide. The contact between the first pair of peripherals and the first pair of costals is short, the width of the anterior margin of this pair of peripherals being more than twice as long as the length of that contact. The peripherals of the bridge area are high. The axillary processes contact the posterior half of the third peripherals. They extend more than one third of the lateral width of the first pair of costals, being slightly wider posteromedially than anterolaterally. These processes are well separated from the second pair of costals. The inguinal processes contact the anterior half of the eighth peripherals, as well as the posterior region of the lateral area of the fifth costals (Fig. 1(B)). The pelvis is sutured to the shell. The ilium is columnar, much higher than wide (Fig. 2(A–D)). The iliac scar is located on the last two pairs of costals, reaching the suprapygal plate (Fig. 1(B)). This carapace lacks a cervical scute (Fig. 1). The vertebral scutes are narrower than the pleurals. The lateral margins of the first vertebral are markedly divergent towards the anterior region. The anterolateral margins of this scute are located on the lateral region of the first pair of peripherals. This scute is almost as wide as the second vertebral. An anomaly is identified in this specimen: the lateral region of the fifth vertebral is located on the eighth costal on the left side, but on the seventh costal on the right. The first pair of marginals meet on midline. These scutes are longer than wide, and overlap more than half of the nuchal lateral margins. The isolated nuchal plate HUE-10218 (Fig. 2(I, J)) is similar to that of the specimen HUE-8532. It has a very similar size, its length being 8.6 cm, and that of HUE-8532 being 8.7 cm. It is also longer than wide. It lacks an anterior notch. The first pair of marginals overlaps more than half of the lateral margins of this plate.
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Fig. 1. HUE-8532, carapace and left ilium of the bothremydid Foxemys mechinorum from the upper Campanian-lower Maastrichtian Lo Hueco fossil site (Fuentes, Cuenca Province, Central Spain). A, A’. Dorsal view. B. Ventral view. C. Reconstruction of the complete and articulate carapace, in dorsal view. Scale bar: 10 cm.
HUE-1220 is an almost complete plastron that only lacks the right mesoplastron (Fig. 2(K, L)). Its length is 39.5 cm. For a detailed description of this specimen, see Pe´rez-Garcı´a et al. (2013). 3. Discussion 3.1. Comparison of the second taxon of Bothremydidae from Lo Hueco with the European Cretaceous representatives Iberoccitanemys convenarum is very abundant in the Spanish fossil site of Lo Hueco (Pe´rez-Garcı´a et al., 2010, 2012, 2013; Ortega et al., 2015). The new carapace studied in this paper, HUE-8532, differs from that of I. convenarum in several characters, including those recognized as exclusive for this taxon (sensu Pe´rez-Garcı´a et al., 2012): it lacks a rectangular carapace with a slightly notched anterior margin; its maximum width is not located in the posterior
half of the carapace, but about half its length; it has not only six neural plates but seven and, therefore, the sagittal contact between the posterior costals does not affect the last three pairs of costals but only the seventh and eighth; the first pair of marginals is not square, but longer than wide. In addition, the length of the carapace studied here, estimated as close to 52 cm, is much greater than that known for the adult specimens of I. convenarum, being about 35 cm. The length of the isolated nuchal plate studied here (HUE-10218) is also considerably greater than that of I. convenarum. However, it is similar to that of the carapace analyzed here, the morphology of this plate and the arrangement of the scutes being compatible with the same taxon. The plastron HUE-1220, with a length close to 40 cm, is also much larger than that of Iberoccitanemys convenarum, but comparable with the carapace and the nuchal plate studied in this paper. In addition, other characters, such as the absence of
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Fig. 2. Three specimens of Foxemys mechinorum from the upper Campanian-lower Maastrichtian Lo Hueco fossil site (Fuentes, Cuenca Province, Central Spain). A–H. Details of the specimen HUE-8532. A–D: posterior area of the carapace, showing the ventral view of the sacral vertebrae (A), and the medial (B), anterolateral (C) and lateral (D) views of the left ilium; E, F: first neural and articulated dorsal vertebra in ventral (E) and left lateral (F) views; G, H: details of the outer surface of the carapace in the region corresponding to the second neural and adjacent plates (G), and in that corresponding to the first and second left peripherals (H). I, I’, J. Nuchal plate HUE-10218, in dorsal (I, I’) and ventral (J) views. K, K’, L. Plastron HUE-1220, in ventral (K) and dorsal (L) views. Scale bars: 3 cm (A, B, G), 2 cm (C–F, H–J), 10 cm (K, L).
straight edges of the entoplastron, the posterior end of this plate reaching the bridge level, and the presence of medial contact between the humeral scutes, allow us to confirm that it cannot be attributed to I. convenarum (Pe´rez-Garcı´a et al., 2013). The size of the shell of the specimens from Lo Hueco not attributable to Iberoccitanemys convenarum is comparable with that of the French Campanian-Maastrichtian forms Foxemys mechinorum and
Polysternon provinciale, being noticeably larger than that of the three other members of Bothremydini known from the last Stages of the Cretaceous in southwestern Europe: the French Elochelys perfecta, the Portuguese Rosasia soutoi, and the Spanish Polysternon atlanticum. In addition, the personal observation (A.P.G.) of representatives of all these species allows the identification of numerous characters through which the
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attribution of these specimens from Lo Hueco to these taxa can be excluded. The carapace of Elochelys perfecta differs from that studied here in several characters, including its protruding and convex anterior region; very wide anterior margin of the nuchal plate; absence of suprapygal; nearly parallel lateral margins of the first vertebral scute; first vertebral considerably narrower than the second; and first marginal scute much wider than long. The plastron of Elochelys perfecta is also characterized by several characters that differ from those present in HUE-1220, including: posterior end of the entoplastron anterior to the bridge level; mesoplastra wider than long; large intergular scute reaching the pectorals and, therefore, separating the humerals; pectoral-abdominal sulcus placed well anterior to the mesoplastra (Pe´rez-Garcı´a et al., 2012). The elements of the carapace studied here cannot be assigned to Rosasia soutoi because they do not share several characters recognized for this taxon: rounded carapace; well-developed nuchal embayment; wider than long nuchal plate; longer contact between the first pair of peripherals and the first pair of costals, the anterior margin of the first peripherals being less than twice that length. Numerous differences are also recognized when the plastron from Lo Hueco and that of Rosasia soutoi are compared: the posterior margin of the entoplastron of the Portuguese form is anterior to the bridge level; the lateral borders of the posterior plastral lobe are straight; the pectorals do not overlap the entoplastron and are located far behind the epiplastra; and the pectorals overlap the mesoplastra (Carrington da Costa, 1940, 1958; Antunes and Broin, 1988). Although the Spanish Polysternon atlanticum is a relatively poorly known taxon, only known by some isolated plates, characters such as the much smaller size and the presence of a narrow first vertebral, allow the identification of differences between this form and that from Lo Hueco (Lapparent de Broin and Murelaga, 1999). The member of Taphrosphyini defined in the European record, the Maastrichtian Taphrosphys ambiguus, represented by a single partial plastron from France, clearly differs from the plastron from Lo Hueco (HUE-1220) in characters such as, among others: its markedly trapezoidal anterior lobe; the wider than long mesoplastra; its wide and long intergular, showing a long contact with the pectoral scutes; the overlap of the pectorals on the mesoplastra; and its ornamental pattern, composed of strong granulated polygons (Broin, 1977). The two pre-Campanian members of Bothremydini defined in the European record also show clear differences with the taxon studied here. Thus, the Iberian Cenomanian Algorachelus peregrinus differs from this form in characters such as: noticeably smaller carapace size, not exceeding 25 cm; wider than long nuchal plate; first marginals much wider than long; overlap of the first pair of marginals on no more than half of the nuchal lateral margins; absence of overlap of the pectorals on the epiplastra; pectoral-abdominal sulci crossing the mesoplastra (Pe´rezGarcı´a, 2017a). Scarce information about the shell of the Hungarian Santonian Foxemys trabanti is currently available (Rabi et al., 2012, 2013). This taxon has a well-developed nuchal embayment, a character not shared with the taxon from Lo Hueco studied here. In addition to its size, this Bothremydidae from Lo Hueco shares with the French Upper Cretaceous forms Foxemys mechinorum and Polysternon provinciale all previously discussed characters. The information available in the plastron HUE-1220 makes it possible to exclude its attribution to P. provinciale. So, it shares with F. mechinorum, but not with P. provinciale, several characters (Tong et al., 1998; Lapparent de Broin, 2001; Gaffney et al., 2006): anterior plastral lobe more than twice as wide as long; sub-straight lateral borders of the anterior half of the posterior lobe; wide anal notch; and posterior tip of the ischiatic scar located well anterior relative to the anal notch. Some characters considered in the original diagnosis of Foxemys mechinorum as different from those present in
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Polysternon atlanticum, such as the putative presence of a longer intergular scute and, therefore, of a shorter medial contact between the humerals (Tong et al., 1998), were subsequently recognized as subject to intraspecific variation (Pe´rez-Garcı´a et al., 2013). The presence of a relatively long epiplastral symphysis observed in the plastron HUE-1220 is part of the intraspecific variation recognized by the first-hand study of the French material of F. mechinorum. In the same way, the absence of contact between the gular scutes and the entoplastron is also present in some of those specimens (e.g., MD t 09). Although HUE-1220 was previously attributed to an indeterminate member of Foxemydina, the better understanding of the representatives of this lineage and the detailed study of the specimen allow us to recognize that it shares a unique character combination with the French form F. mechinorum. The new material from Lo Hueco presented here confirms the presence of this French form in this Spanish site. An exclusive combination for the carapace of F. mechinorum is also recognized in the carapace from Lo Hueco. Thus, characters such as the long oval carapace morphology; the absence of nuchal emargination, the anterior carapace margin being substraight; and the absence of the thin parallel striations that are well developed on the dorsal carapace of P. provinciale, allow to exclude its attribution to this species. Thus, the presence of F. mechinorum in Lo Hueco is confirmed. Iberoccitanemys convenarum and Foxemys mechinorum correspond to the only tetrapod species whose presence has been confirmed in both the Spanish site of Lo Hueco and the French record. 3.2. Phylogenetic discussion The plastron from Lo Hueco was previously included in a data matrix which pursues the study of the phylogenetic relationships among the representatives of Bothremydidae (data matrix used in Pe´rez-Garcı´a et al., 2013, based on the matrix of Pe´rez-Garcı´a et al., 2012, which corresponded to a modified version of that proposed by Gaffney et al., 2006). It was recognized as a branch of a polytomy in which the members of Foxemydina were located (Pe´rez-Garcı´a et al., 2013). The finding of a carapace preserving the ilium allows coding many more characters for this second form of Bothremydidae from Lo Hueco (more than twice than those previously known; see Appendices A and B). For Foxemys mechinorum, the character 154 (Carapace, nuchal embayment), erroneously coded as 1 (present), is recoded as 0 (absent), which is compatible with the diagnosis of this taxon (Tong et al., 1998; Gaffney et al., 2006), and has been confirmed based on the personal observation of both the holotype and other published and unpublished specimens. The character combination encoded based on the material of this taxon from Lo Hueco is only comparable with that of the French material of F. mechinorum. A simplified version of the indicated data matrix was used, in which only the taxa represented by both shell and skull have been considered (Appendix B). A heuristic tree search was employed, using TNT 1.0 (Goloboff et al., 2008), with 1000 replications of Wagner trees (using random addition sequences) followed by tree bisection recognition (TBR) as a swapping algorithm, saving 100 trees per replication. As a result, this taxon from Lo Hueco is unambiguously grouped with the specimens of Foxemys mechinorum from France (Fig. 3).
4. Conclusions New material of bothremydid turtles from the Spanish upper Campanian–lower Maastrichtian fossil site of Lo Hueco (Fuentes, Cuenca Province, Central Spain) is studied in this paper. In addition, an almost complete plastron from this locality, previously attributed to an indeterminate member of Foxemydina, is also
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Fig. 3. Single most parsimonious tree obtained here, with a length of 249 steps (CI = 0.815; RI = 0.762), showing the phylogenetic position of the bothremydid from the upper Campanian-lower Maastrichtian Lo Hueco fossil site (Fuentes, Cuenca Province, Central Spain) studied in this paper as grouped with the French material of Foxemys mechinorum. Bootstrap frequencies (top; only values 50% shown) and Bremer support values (bottom) are indicated.
analyzed. The remains of Bothremydidae from Lo Hueco are very abundant. The most complete shells from the last Stages of the Cretaceous in Spain, including the only almost complete ones, come from this site. The study of some of these specimens allowed recognizing the presence of Iberoccitanemys convenarum in Spain, a taxon previously known by a single specimen from southern France. It was the only species of Bothremydidae which had been identified as being part of the diversity of turtles from the Upper Cretaceous records of both France and Spain. Previous studies allowed recognizing the presence of a second taxon of Bothremydidae in Lo Hueco, also attributable to Foxemydina. That finding corresponded to the only available evidence on the synchronic and sympatric coexistence of two members of Bothremydidae in a single fossil site of Europe. However, the limited information on this second taxon from Lo Hueco, whose size was considerably larger than that of Iberoccitanemys convenarum, did not allow its identification at a specific or generic level. The new material of Bothremydidae analyzed here, and its direct comparison with the other European taxa, allows the attribution of the larger form from Lo Hueco to Foxemys mechinorum, a taxon so far considered as exclusive of the French record. In fact, no species of Bothremydidae was recognized as being part of the paleobiodiversity of both France and Spain before the finding of the specimens from Lo Hueco. The study of the turtles from this site allows to refute the hypothesis on the endemism of all Spanish and French Campanian and Maastrichtian pleurodiran turtle species. In this way, the south of France and the center of Spain are recognized as being part of the distribution area of both Iberoccitanemys convenarum and Foxemys mechinorum.
Acknowledgements This research has been funded by the Ministerio de Economı´a, Industria y Competitividad (FPDI-2013-18986, IJCI-2016-30427
and CGL2015-68363-P). The preparation of the new specimens has been performed in the ‘‘Taller de Empleo Restauracio´n del Patrimonio Paleontolo´gico de los Yacimientos de Cuenca’’, funded by the Junta de Comunidades de Castilla-La Mancha. The authors thank H. Tong (Institute of Vertebrate Paleontology and Paleoanthropology, China), C. Corral (MCNA, Spain), J. Le Loeuff (Muse´e des Dinosaures d’Espe´raza, France), T. Tortosa (Muse´um d’Histoire Naturelle d’Aix-en-Provence, France), F. de Lapparent de Broin, R. ¨ si Allain and N.-E. Jalil (Pale´ontologie, MNHN Paris, France), A. O and M. Rabi (Magyar Terme´szettudoma´nyi Mu´zeum, Hungary), and A. Mechin and P. Mechin (Vitrolles, France) for access to several of the bothremydid specimens used for the comparisons performed here. The members of the Grupo de Biologı´a Evolutiva (UNED), especially F. Marcos, M. Martı´n and I. Narva´ez, are thanked for the collaboration in the excavation, preparation and study of the Lo Hueco specimens of Foxemys mechinorum. Thanks to the editor G. Escarguel and to J. Claude, R. Vullo and an anonymous reviewer for comments and suggestions.
Appendix A. Supplementary information New characters coded for the taxon from Lo Hueco studied in this paper, relative to those considered by Pe´rez-Garcı´a et al. (2013): Pelvis sutured to the shell (Character 133, State 1) Ilium columnar, expanded mediolaterally (Character 134, State 1) Pelvis narrow, ilia close to midline (Character 135, State 1) Cervical scute absent (Character 138, State 1) Nuchal width equals to its length (Character 139, State 2) Pygal notch absent, margin smooth (Character 140, State 2)
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Neural series completeness to costals 7 (Character 141, State 2) Iliac scar on costals 7 and 8 and suprapygal (Character 142, State 2) Costal 1 two times longer than costal 2 (Character 143, State 1) Rectangular first neural (Character 144, State 0) Neural series pattern regular, most hexagonal, coffin-shaped (Character 145, State 2) Seven neurals (Character 146, State 2) Narrow peripheral 1/costal 1 contact, the anterior margin 2 times this contact (Character 147, State 2) Contact of the axillary process with the costal 1 present, but separated from the costal 2 suture (Character 148, State 1) Axillary process extent on the main body of the peripheral 3 (Character 149, State 2) Inguinal buttress extends medially to the center of the costal 5 (Character 150, State 1) Absence of supramarginal scutes (Character 151, State 2) Vertebral scutes narrower than the pleurals (Character 152, State 1) Absence of nuchal embayment (Character 154, State 0) First thoracic rib smaller and closer to the 2nd rib (Character 155, State 1) Small costovertebral tunnel (Character 156, State 2) Shell texture composed by weak granulated polygons (Character 175, State 1) Axillary scar slightly wider posteromedially than anterolaterally (Character 176, State 1) Vertebral 1 anterolaterally covering peripheral 1 only or the suture between peripheral 1 and 2 (Character 177, State 0) Vertebral 1 as wide as vertebral 2 (Character 178, State 1) Posterior end of the entoplastron reaching the carapace-plastron bridge level (Character 179, State 1) Ischiac scar triangular in shape with the posterior tip very anterior to the anal notch (Character 180, State 2)
Appendix B. Supplementary data Supplementary information (NEXUS file for the data matrix used in this paper, including 180 characters and 15 taxa) associated with this article can be found, in the online version, at: https://doi. org/10.1016/j.geobios.2018.04.002. References Antunes, M.T., Broin, F. de, 1988. Le Cre´tace´ terminal de Beira Litoral, Portugal : remarques stratigraphiques et e´cologiques ; e´tude comple´mentaire de Rosasia soutoi (Chelonii Bothremydidae). Cieˆncias da Terra 9, 153–200. Broin, F. de, 1977. Contribution a` l’e´tude des Che´loniens. Che´loniens continentaux du Cre´tace´ et du Tertiaire de France. Me´moires du Muse´um National d’Histoire Naturelle C 38, i–ix, 1–366. Carrington da Costa, J., 1940. Un novo quelo´nio fo´ssil. Comunicac¸o˜es dos Servic¸os Geolo´gicos de Portugal 21, 105–125. Carrington da Costa, J., 1958. Novos metatipos para o ge´nero Rosasia (Testudinata Pelomedusidae). Comunicac¸o˜es dos Servic¸os Geolo´gicos de Portugal 62, 5–30. Gaffney, E.S., Tong, H., Meylan, P.A., 2006. Evolution of the side-necked turtles: the families Bothremydidae Euraxemydidae, and Araripemydidae. Bulletin of the American Museum of Natural History 300, 1–700. Goloboff, P., Farris, J.S., Nixon, K.C., 2008. TNT, a free program for phylogenetic analysis. Cladistics 24, 1–13.
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Lapparent de Broin, F. de, 2001. The European turtle fauna from the Triassic to the Present. Dumerilia 4, 155–216. Lapparent de Broin, F de., Murelaga, X., 1996. Une nouvelle faune de che´loniens dans le Cre´tace´ supe´rieur europe´en. Comptes Rendus de l’Acade´mie des Sciences de Paris 323, 729–735. Lapparent de Broin, F de., Murelaga, X., 1999. Turtles from the Upper Cretaceous of ˜ o (Iberian Peninsula). Estudios del Museo de Ciencias Naturales de A´lava 14, Lan 135–211. Laurent, Y., Tong, H., Claude, J., 2002. New side-necked turtle (Pleurodira: Bothremydidae) from the Upper Maastrichtian of the Petites-Pyre´ne´es (HauteGaronne France). Cretaceous Research 23, 465–471. Martin, J.E., Delfino, M., 2010. Recent advances in the comprehension of the biogeography of Cretaceous European eusuchians. Palaeogeography Palaeoclimatology Palaeoecology 293, 406–418. Matheron, P., 1869. Notice sur les reptiles fossiles des de´poˆts fluvio-lacustres cre´tace´s du bassin a` lignite de Fuveau. Me´moires de l’Acade´mie Impe´riale des Sciences Belles-Lettres et Arts de Marseille 1, 1–39. Nopcsa, F., 1931. Sur des nouveaux restes de Tortues du Danien du Midi de la France. Bulletin de la Socie´te´ Ge´ologique de France 1, 223–236. Ortega, F., Bardet, N., Barroso-Barcenilla, F., Callapez, P.M., Cambra-Moo, O., Daviero-Go´mez, V., Dı´ez-Dı´az, V., Elvira, A., Escaso, F., Garcı´a-Oliva, M., Go´mez, B., Houssaye, A., Knoll, F., Marcos-Ferna´ndez, F., Martı´n, M., Narva´ez, I., Pe´rezGarcı´a, A., Serrano, H., Torices, A., Vidal, D., Sanz, J.L., 2015. The biota of the Upper Cretaceous site of ‘‘Lo Hueco’’ (Cuenca, Spain). Journal of Iberian Geology 41, 83–99. Pereda Suberbiola, X., Corral, J.C., Astibia, H., Badiola, A., Bardet, N., Berreteaga, A., Buffetaut, E., Buscalioni, A.D., Cappetta, H., Cavin, L., Dı´ez Dı´az, V., Gheerbrant, E., Murelaga, X., Ortega, F., Pe´rez-Garcı´a, A., Poyato-Ariza, F., Rage, J.-C., Sanz, J.L., Torices, A., 2015. Late Cretaceous continental and marine vertebrate assem˜ o quarry (Basque-Cantabrian Region, Iberian Peninsula): an blages from the Lan update. Journal of Iberian Geology 41, 101–124. Pe´rez-Garcı´a, A., 2016. A new turtle confirms the presence of Bothremydidae (Pleurodira) in the Cenozoic of Europe and expands the biostratigraphic range of Foxemydina. The Science of Nature 103, 1–14. Pe´rez-Garcı´a, A., 2017a. A new turtle taxon (Podocnemidoidea, Bothremydidae) reveals the oldest known dispersal event of the crown Pleurodira from Gondwana to Laurasia. Journal of Systematic Palaeontology 15, 709–731. Pe´rez-Garcı´a, A., 2017b. The Iberian fossil record of turtles: an update. Journal of Iberian Geology 43, 155–191. Pe´rez Garcı´a, A., Ortega, F., Murelaga, X., 2010. Ampliacio´n de la distribucio´n geogra´fica y temporal de Elochelys convenarum (Chelonii Bothremydidae) en el Creta´cico Superior de la Penı´nsula Ibe´rica. Ameghiniana 47, 307–315. Pe´rez-Garcı´a, A., Ortega, F., Murelaga, X., 2012. A new genus of Bothremydidae (Chelonii Pleurodira) in the Cretaceous of Southwestern Europe. Geobios 45, 219–229. Pe´rez-Garcı´a, A., Ortega, F., Murelaga, X., 2013. Two synchronic and sympatric Bothremydidae taxa (Chelonii, Panpleurodira) in the Upper Cretaceous site of ‘‘Lo Hueco’’ (Cuenca, Spain). In: Brinkman, D., Holroyd, P., Gardner, J. (Eds.), Morphology and Evolution of Turtles: Papers in Honor of Eugene S. Gaffney, Vol. 3, Pleurodires. Springer, Dordrecht, The Netherlands, pp. 251–259. Pe´rez-Garcı´a, A., Antunes, M.T., Barroso-Barcenilla, F., Callapez, P.M., Segura, M., Soares, A.F., Torices, A., 2017. A bothremydid from the middle Cenomanian of Portugal identified as one of the oldest pleurodiran turtles in Laurasia. Cretaceous Research 78, 61–70. Pe´rez-Garcı´a, A., Ortega, F., Bolet, A., Escaso, F., Houssaye, A., Martı´nez-Salanova, J., Miguel Chaves, C. de., Mocho, P., Narva´ez, I., Segura, M., Torices, A., Vidal, D., ˜a Sanz, J.L., 2016. A review of the upper Campanian vertebrate site of Armun (Segovia Province, Spain). Cretaceous Research 57, 591–623. Portis, A., 1882. Les Che´loniens de la Molasse vaudoise conserve´s dans le Muse´e Ge´ologique de Lausanne. Appendice, Sur un nouveau genre de Che´loniens fossiles de la Craie supe´rieure de Fuveau. Me´moires de la Socie´te´ Pale´ontologique Suisse 9, 65–76. Rabi, M., Tong, H., Botfalvai, G., 2012. A new species of the side-necked turtle Foxemys (Pelomedusoides: Bothremydidae) from the Late Cretaceous of Hungary and the historical biogeography of the Bothremydini. Geological Magazine 149, 662–674. Rabi, M., Vremir, M., Tong, H., 2013. Preliminary overview of Late Cretaceous turtle diversity in Eastern Central Europe (Austria, Hungary, and Romania). In: Brinkman, D., Holroyd, P., Gardner, J. (Eds.), Morphology and Evolution of Turtles: Papers in Honor of Eugene S. Gaffney, Vol. 3, Pleurodires. Springer, Dordrecht, The Netherlands, pp. 251–259. Tong, H., Gaffney, E.S., Buffetaut, E., 1998. Foxemys, a new side-necked turtle (Bothremydidae: Pelomedusoides) from the Late Cretaceous of France. American Museum Novitates 3251, 1–19.
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Original article
Identification of the French Upper Cretaceous bothremydid turtle Foxemys mechinorum in the Spanish record§ Ada´n Pe´rez-Garcı´a *, Francisco Ortega Grupo de Biologı´a Evolutiva, Facultad de Ciencias, UNED, Paseo Senda del Rey, 9, 28040 Madrid, Spain
A R T I C L E I N F O
A B S T R A C T
Article history: Received 11 January 2018 Accepted 17 April 2018 Available online 20 April 2018
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.
C 2018 Elsevier Masson SAS. All rights reserved.
Keywords: Pleurodira Bothremydidae Lo Hueco fossil site Campanian-Maastrichtian Phylogeny Paleobiogeography
1. Introduction Bothremydidae is the best-represented group of turtles in the coastal and freshwater ecosystems of the Upper Cretaceous of southwestern Europe (Lapparent de Broin, 2001; Gaffney et al., 2006; Pe´rez-Garcı´a, 2017b). The knowledge about the diversity and distribution of this lineage of Pleurodira in this region has improved markedly over the last twenty years (Tong et al., 1998; Lapparent de Broin and Murelaga, 1996, 1999; Laurent et al., 2002; Pe´rez-Garcı´a et al., 2012; Pe´rez-Garcı´a, 2016, 2017a). Bothremydidae is a group of Gondwanian origin, which reached Europe through several diachronic dispersion events (Pe´rez-Garcı´a, 2017b). The oldest evidence of this lineage in this continent corresponds to the record of the Bothremydina (Bothremydini) Algorachelus peregrinus Pe´rez-Garcı´a, 2017a, recognized in both the uppermost middle-lowermost upper Cenomanian of Algora (Guadalajara Province, Central Spain) and the middle Cenomanian
§
Corresponding editor: Gilles Escarguel. * Corresponding author. E-mail address: [email protected] (A. Pe´rez-Garcı´a).
https://doi.org/10.1016/j.geobios.2018.04.002 C 2018 Elsevier Masson SAS. All rights reserved. 0016-6995/
of Nazare´ (Central Portugal) (Pe´rez-Garcı´a, 2017a; Pe´rez-Garcı´a et al., 2017). The Campanian-Maastrichtian record of southwestern Europe includes a member of Taphosphyini (i.e., Taphrosphys ambiguus (Gaudry, 1890), represented by a single specimen from the Maastrichtian of the French locality of Mont-Aime´; Broin, 1977; Martin and Delfino, 2010; Pe´ rezGarcı´ a, 2016), as well as several representatives of Bothremydini. Rosasia soutoi Carrington da Costa, 1940 (Bothremydina) is recognized as an exclusive form of the Campanian-Maastrichtian record of Portugal (Carrington da Costa, 1940; Antunes and Broin, 1988; Pe´rez-Garcı´a, 2017b). Several members of the sister group of Bothremydina (i.e., Foxemydina) have been identified. The first bothremydid defined in the European record, Polysternon provinciale (Matheron, 1869), is an exclusive form of the French record, its presence having been only confirmed in Campanian levels of the south of this country (Matheron, 1869; Portis, 1882; Nopcsa, 1931; Broin, 1977; Gaffney et al., 2006). Two other forms so far identified as exclusive of the French record are recognized: Elochelys perfecta Nopcsa, 1931, from the Campanian of the Fuveau Basin, and Foxemys mechinorum Tong, Gaffney et Buffetaut, 1998, recognized in the upper Campanian-lower
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Maastrichtian of several sites of the south of France (Nopcsa, 1931; Tong et al., 1998; Pe´rez-Garcı´a et al., 2012). Polysternon atlanticum Lapparent de Broin et Murelaga, 1996, is exclusive of the Spanish record, being only identified in its type locality, the upper Campanian ˜o (Burgos Province) (Lapparent de Broin and Murelaga, site of Lan 1996, 1999; Pereda Suberbiola et al., 2015; Pe´rez-Garcı´a, 2017b). The only bothremydid from the Campanian-Maastrichtian record of southwestern Europe recognized in more than one country is Iberoccitanemys convenarum (Laurent, Tong et Claude, 2002). This form was defined by a single shell from the upper Maastrichtian of the French region of Haute-Garonne, subsequently recognized as a wellrepresented taxon in the upper Campanian-lower Maastrichtian site of Lo Hueco (Cuenca Province, Spain), and more recently having been ˜a (Segovia identified in the Spanish upper Campanian site of Armun Province) (Laurent et al., 2002; Pe´rez-Garcı´a et al., 2010, 2012, 2016). The tetrapod fauna from Lo Hueco has been identified as closely related to that of the synchronous record of France. In addition to the identification of several shared lineages, some genera, corresponding to different clades, have been identified in both regions. They correspond to the eusuchian crocodyliform Lohuecosuchus (L. megadontos being present in Lo Hueco), the ornithopod dinosaur Rhabdodon (with Rhabdodon sp. in Lo Hueco) and the sauropod dinosaur Ampelosaurus (Ampelosaurus sp. having been identified in this site) (Ortega et al., 2015). Therefore, the only species whose presence has been confirmed in both Lo Hueco and the French record is the bothremydid Iberoccitanemys convenarum. Lo Hueco is the Spanish site of the last Stages of the Upper Cretaceous that has yielded the most abundant record of Bothremydidae, and one of the few localities where articulated shells have been found (Pe´rez-Garcı´a, 2017b). In addition to the remains of Iberoccitanemys convenarum, a plastron of a second member of the Bothremydidae has been reported there (Pe´rezGarcı´a et al., 2013). Thus, Lo Hueco is the only European site where the synchronous and sympatric coexistence of two members of Bothremydidae is currently recognized. The scarce information so far available on this second form was exclusively based on an almost complete plastron which was attributed, in a preliminary way, to an indeterminate member of Foxemydina (Pe´rez-Garcı´a et al., 2013). New remains referable to this second form, also from Lo Hueco, are presented here. The study of these specimens allows us to identify this second form from Lo Hueco, at both generic and specific levels, expanding the knowledge about the diversity of Bothremydidae in the Spanish Upper Cretaceous record and that about the paleobiogeographical distribution of Foxemys mechinorum, so far considered endemic to France. Institutional abbreviations: HUE, Lo Hueco collection, Museo de Paleontologı´a de Castilla-La Mancha, Cuenca, Spain; MD, Muse´e des Dinosaures, Espe´raza, France.
2. Systematic palaeontology Testudines Batsch, 1788 Pleurodira Cope, 1864 Pelomedusoides Cope, 1868 Podocnemidoidea Cope, 1868 Bothremydidae Baur, 1891 Bothremydodda Gaffney, Tong et Meylan, 2006 Bothremydini Gaffney, Tong et Meylan, 2006 Foxemydina Gaffney, Tong et Meylan, 2006 Genus Foxemys Tong, Gaffney et Buffetaut, 1998 Foxemys mechinorum Tong, Gaffney et Buffetaut, 1998 Figs. 1, 2 Material: Two unpublished specimens, corresponding to an almost complete and disarticulated carapace, preserving the
articulate left ilium, HUE-8532 (Figs. 1, 2(A–H)), and an isolated nuchal plate, HUE-10218 (Fig. 2(I, J)), as well as an almost complete plastron, HUE-1220 (Fig. 2(K, L)), previously attributed to Foxemydina indet. by Pe´rez-Garcı´a et al. (2013). Locality and horizon: Lo Hueco fossil site (Fuentes, Cuenca Province, Castilla-La Mancha, Central Spain); Margas, Arcillas y Yesos de Villalba de la Sierra Formation (Ortega et al., 2015); upper Campanian-lower Maastrichtian. Description: The only plates not preserved in the carapace HUE-8532 are the sixth and seventh left peripherals and the sixth right peripheral (Fig. 1). Most plates of this specimen are disarticulated, except those corresponding to the following four areas: the nuchal and the first right peripheral; the first and second left peripherals; the first neural and the first left costal; and a fragment composed of the last two neurals, the fifth to eighth left costals, the seventh and eighth right costals, the suprapygal, the pygal, the eighth to eleventh left peripherals, and the eleventh right peripheral. The length of the complete carapace is identified as close to 52 cm. The outer surface of the plates shows an ornamental pattern consisting of dichotomic and discontinuous sulci, which are anastomosed, generating small and low polygons (Fig. 2(H)). This specimen lacks well-developed parallel striations, but some poorly developed striations are present in the medial region (Fig. 2(G)). The carapace is oval, markedly longer than wide. The maximum width is located about half its length. It lacks a nuchal embayment, and the anterior carapace margin is substraight (Fig. 1). The length of the nuchal plate is slightly greater than its width (Fig. 1). Seven neurals are present. The first is rectangular, longer than wide. The second to sixth neurals are hexagonal, with their anterolateral margins being shorter than the posterolateral. All these plates, except the sixth, are longer than wide. The seventh neural is pentagonal. The sagittal contact between the two posterior pairs of costals is observed. The first costal is approximately two times longer than the second. A pentagonal suprapygal plate is present. The anterior and posterior peripherals are noticeably longer than wide. The contact between the first pair of peripherals and the first pair of costals is short, the width of the anterior margin of this pair of peripherals being more than twice as long as the length of that contact. The peripherals of the bridge area are high. The axillary processes contact the posterior half of the third peripherals. They extend more than one third of the lateral width of the first pair of costals, being slightly wider posteromedially than anterolaterally. These processes are well separated from the second pair of costals. The inguinal processes contact the anterior half of the eighth peripherals, as well as the posterior region of the lateral area of the fifth costals (Fig. 1(B)). The pelvis is sutured to the shell. The ilium is columnar, much higher than wide (Fig. 2(A–D)). The iliac scar is located on the last two pairs of costals, reaching the suprapygal plate (Fig. 1(B)). This carapace lacks a cervical scute (Fig. 1). The vertebral scutes are narrower than the pleurals. The lateral margins of the first vertebral are markedly divergent towards the anterior region. The anterolateral margins of this scute are located on the lateral region of the first pair of peripherals. This scute is almost as wide as the second vertebral. An anomaly is identified in this specimen: the lateral region of the fifth vertebral is located on the eighth costal on the left side, but on the seventh costal on the right. The first pair of marginals meet on midline. These scutes are longer than wide, and overlap more than half of the nuchal lateral margins. The isolated nuchal plate HUE-10218 (Fig. 2(I, J)) is similar to that of the specimen HUE-8532. It has a very similar size, its length being 8.6 cm, and that of HUE-8532 being 8.7 cm. It is also longer than wide. It lacks an anterior notch. The first pair of marginals overlaps more than half of the lateral margins of this plate.
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Fig. 1. HUE-8532, carapace and left ilium of the bothremydid Foxemys mechinorum from the upper Campanian-lower Maastrichtian Lo Hueco fossil site (Fuentes, Cuenca Province, Central Spain). A, A’. Dorsal view. B. Ventral view. C. Reconstruction of the complete and articulate carapace, in dorsal view. Scale bar: 10 cm.
HUE-1220 is an almost complete plastron that only lacks the right mesoplastron (Fig. 2(K, L)). Its length is 39.5 cm. For a detailed description of this specimen, see Pe´rez-Garcı´a et al. (2013). 3. Discussion 3.1. Comparison of the second taxon of Bothremydidae from Lo Hueco with the European Cretaceous representatives Iberoccitanemys convenarum is very abundant in the Spanish fossil site of Lo Hueco (Pe´rez-Garcı´a et al., 2010, 2012, 2013; Ortega et al., 2015). The new carapace studied in this paper, HUE-8532, differs from that of I. convenarum in several characters, including those recognized as exclusive for this taxon (sensu Pe´rez-Garcı´a et al., 2012): it lacks a rectangular carapace with a slightly notched anterior margin; its maximum width is not located in the posterior
half of the carapace, but about half its length; it has not only six neural plates but seven and, therefore, the sagittal contact between the posterior costals does not affect the last three pairs of costals but only the seventh and eighth; the first pair of marginals is not square, but longer than wide. In addition, the length of the carapace studied here, estimated as close to 52 cm, is much greater than that known for the adult specimens of I. convenarum, being about 35 cm. The length of the isolated nuchal plate studied here (HUE-10218) is also considerably greater than that of I. convenarum. However, it is similar to that of the carapace analyzed here, the morphology of this plate and the arrangement of the scutes being compatible with the same taxon. The plastron HUE-1220, with a length close to 40 cm, is also much larger than that of Iberoccitanemys convenarum, but comparable with the carapace and the nuchal plate studied in this paper. In addition, other characters, such as the absence of
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Fig. 2. Three specimens of Foxemys mechinorum from the upper Campanian-lower Maastrichtian Lo Hueco fossil site (Fuentes, Cuenca Province, Central Spain). A–H. Details of the specimen HUE-8532. A–D: posterior area of the carapace, showing the ventral view of the sacral vertebrae (A), and the medial (B), anterolateral (C) and lateral (D) views of the left ilium; E, F: first neural and articulated dorsal vertebra in ventral (E) and left lateral (F) views; G, H: details of the outer surface of the carapace in the region corresponding to the second neural and adjacent plates (G), and in that corresponding to the first and second left peripherals (H). I, I’, J. Nuchal plate HUE-10218, in dorsal (I, I’) and ventral (J) views. K, K’, L. Plastron HUE-1220, in ventral (K) and dorsal (L) views. Scale bars: 3 cm (A, B, G), 2 cm (C–F, H–J), 10 cm (K, L).
straight edges of the entoplastron, the posterior end of this plate reaching the bridge level, and the presence of medial contact between the humeral scutes, allow us to confirm that it cannot be attributed to I. convenarum (Pe´rez-Garcı´a et al., 2013). The size of the shell of the specimens from Lo Hueco not attributable to Iberoccitanemys convenarum is comparable with that of the French Campanian-Maastrichtian forms Foxemys mechinorum and
Polysternon provinciale, being noticeably larger than that of the three other members of Bothremydini known from the last Stages of the Cretaceous in southwestern Europe: the French Elochelys perfecta, the Portuguese Rosasia soutoi, and the Spanish Polysternon atlanticum. In addition, the personal observation (A.P.G.) of representatives of all these species allows the identification of numerous characters through which the
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attribution of these specimens from Lo Hueco to these taxa can be excluded. The carapace of Elochelys perfecta differs from that studied here in several characters, including its protruding and convex anterior region; very wide anterior margin of the nuchal plate; absence of suprapygal; nearly parallel lateral margins of the first vertebral scute; first vertebral considerably narrower than the second; and first marginal scute much wider than long. The plastron of Elochelys perfecta is also characterized by several characters that differ from those present in HUE-1220, including: posterior end of the entoplastron anterior to the bridge level; mesoplastra wider than long; large intergular scute reaching the pectorals and, therefore, separating the humerals; pectoral-abdominal sulcus placed well anterior to the mesoplastra (Pe´rez-Garcı´a et al., 2012). The elements of the carapace studied here cannot be assigned to Rosasia soutoi because they do not share several characters recognized for this taxon: rounded carapace; well-developed nuchal embayment; wider than long nuchal plate; longer contact between the first pair of peripherals and the first pair of costals, the anterior margin of the first peripherals being less than twice that length. Numerous differences are also recognized when the plastron from Lo Hueco and that of Rosasia soutoi are compared: the posterior margin of the entoplastron of the Portuguese form is anterior to the bridge level; the lateral borders of the posterior plastral lobe are straight; the pectorals do not overlap the entoplastron and are located far behind the epiplastra; and the pectorals overlap the mesoplastra (Carrington da Costa, 1940, 1958; Antunes and Broin, 1988). Although the Spanish Polysternon atlanticum is a relatively poorly known taxon, only known by some isolated plates, characters such as the much smaller size and the presence of a narrow first vertebral, allow the identification of differences between this form and that from Lo Hueco (Lapparent de Broin and Murelaga, 1999). The member of Taphrosphyini defined in the European record, the Maastrichtian Taphrosphys ambiguus, represented by a single partial plastron from France, clearly differs from the plastron from Lo Hueco (HUE-1220) in characters such as, among others: its markedly trapezoidal anterior lobe; the wider than long mesoplastra; its wide and long intergular, showing a long contact with the pectoral scutes; the overlap of the pectorals on the mesoplastra; and its ornamental pattern, composed of strong granulated polygons (Broin, 1977). The two pre-Campanian members of Bothremydini defined in the European record also show clear differences with the taxon studied here. Thus, the Iberian Cenomanian Algorachelus peregrinus differs from this form in characters such as: noticeably smaller carapace size, not exceeding 25 cm; wider than long nuchal plate; first marginals much wider than long; overlap of the first pair of marginals on no more than half of the nuchal lateral margins; absence of overlap of the pectorals on the epiplastra; pectoral-abdominal sulci crossing the mesoplastra (Pe´rezGarcı´a, 2017a). Scarce information about the shell of the Hungarian Santonian Foxemys trabanti is currently available (Rabi et al., 2012, 2013). This taxon has a well-developed nuchal embayment, a character not shared with the taxon from Lo Hueco studied here. In addition to its size, this Bothremydidae from Lo Hueco shares with the French Upper Cretaceous forms Foxemys mechinorum and Polysternon provinciale all previously discussed characters. The information available in the plastron HUE-1220 makes it possible to exclude its attribution to P. provinciale. So, it shares with F. mechinorum, but not with P. provinciale, several characters (Tong et al., 1998; Lapparent de Broin, 2001; Gaffney et al., 2006): anterior plastral lobe more than twice as wide as long; sub-straight lateral borders of the anterior half of the posterior lobe; wide anal notch; and posterior tip of the ischiatic scar located well anterior relative to the anal notch. Some characters considered in the original diagnosis of Foxemys mechinorum as different from those present in
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Polysternon atlanticum, such as the putative presence of a longer intergular scute and, therefore, of a shorter medial contact between the humerals (Tong et al., 1998), were subsequently recognized as subject to intraspecific variation (Pe´rez-Garcı´a et al., 2013). The presence of a relatively long epiplastral symphysis observed in the plastron HUE-1220 is part of the intraspecific variation recognized by the first-hand study of the French material of F. mechinorum. In the same way, the absence of contact between the gular scutes and the entoplastron is also present in some of those specimens (e.g., MD t 09). Although HUE-1220 was previously attributed to an indeterminate member of Foxemydina, the better understanding of the representatives of this lineage and the detailed study of the specimen allow us to recognize that it shares a unique character combination with the French form F. mechinorum. The new material from Lo Hueco presented here confirms the presence of this French form in this Spanish site. An exclusive combination for the carapace of F. mechinorum is also recognized in the carapace from Lo Hueco. Thus, characters such as the long oval carapace morphology; the absence of nuchal emargination, the anterior carapace margin being substraight; and the absence of the thin parallel striations that are well developed on the dorsal carapace of P. provinciale, allow to exclude its attribution to this species. Thus, the presence of F. mechinorum in Lo Hueco is confirmed. Iberoccitanemys convenarum and Foxemys mechinorum correspond to the only tetrapod species whose presence has been confirmed in both the Spanish site of Lo Hueco and the French record. 3.2. Phylogenetic discussion The plastron from Lo Hueco was previously included in a data matrix which pursues the study of the phylogenetic relationships among the representatives of Bothremydidae (data matrix used in Pe´rez-Garcı´a et al., 2013, based on the matrix of Pe´rez-Garcı´a et al., 2012, which corresponded to a modified version of that proposed by Gaffney et al., 2006). It was recognized as a branch of a polytomy in which the members of Foxemydina were located (Pe´rez-Garcı´a et al., 2013). The finding of a carapace preserving the ilium allows coding many more characters for this second form of Bothremydidae from Lo Hueco (more than twice than those previously known; see Appendices A and B). For Foxemys mechinorum, the character 154 (Carapace, nuchal embayment), erroneously coded as 1 (present), is recoded as 0 (absent), which is compatible with the diagnosis of this taxon (Tong et al., 1998; Gaffney et al., 2006), and has been confirmed based on the personal observation of both the holotype and other published and unpublished specimens. The character combination encoded based on the material of this taxon from Lo Hueco is only comparable with that of the French material of F. mechinorum. A simplified version of the indicated data matrix was used, in which only the taxa represented by both shell and skull have been considered (Appendix B). A heuristic tree search was employed, using TNT 1.0 (Goloboff et al., 2008), with 1000 replications of Wagner trees (using random addition sequences) followed by tree bisection recognition (TBR) as a swapping algorithm, saving 100 trees per replication. As a result, this taxon from Lo Hueco is unambiguously grouped with the specimens of Foxemys mechinorum from France (Fig. 3).
4. Conclusions New material of bothremydid turtles from the Spanish upper Campanian–lower Maastrichtian fossil site of Lo Hueco (Fuentes, Cuenca Province, Central Spain) is studied in this paper. In addition, an almost complete plastron from this locality, previously attributed to an indeterminate member of Foxemydina, is also
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Fig. 3. Single most parsimonious tree obtained here, with a length of 249 steps (CI = 0.815; RI = 0.762), showing the phylogenetic position of the bothremydid from the upper Campanian-lower Maastrichtian Lo Hueco fossil site (Fuentes, Cuenca Province, Central Spain) studied in this paper as grouped with the French material of Foxemys mechinorum. Bootstrap frequencies (top; only values 50% shown) and Bremer support values (bottom) are indicated.
analyzed. The remains of Bothremydidae from Lo Hueco are very abundant. The most complete shells from the last Stages of the Cretaceous in Spain, including the only almost complete ones, come from this site. The study of some of these specimens allowed recognizing the presence of Iberoccitanemys convenarum in Spain, a taxon previously known by a single specimen from southern France. It was the only species of Bothremydidae which had been identified as being part of the diversity of turtles from the Upper Cretaceous records of both France and Spain. Previous studies allowed recognizing the presence of a second taxon of Bothremydidae in Lo Hueco, also attributable to Foxemydina. That finding corresponded to the only available evidence on the synchronic and sympatric coexistence of two members of Bothremydidae in a single fossil site of Europe. However, the limited information on this second taxon from Lo Hueco, whose size was considerably larger than that of Iberoccitanemys convenarum, did not allow its identification at a specific or generic level. The new material of Bothremydidae analyzed here, and its direct comparison with the other European taxa, allows the attribution of the larger form from Lo Hueco to Foxemys mechinorum, a taxon so far considered as exclusive of the French record. In fact, no species of Bothremydidae was recognized as being part of the paleobiodiversity of both France and Spain before the finding of the specimens from Lo Hueco. The study of the turtles from this site allows to refute the hypothesis on the endemism of all Spanish and French Campanian and Maastrichtian pleurodiran turtle species. In this way, the south of France and the center of Spain are recognized as being part of the distribution area of both Iberoccitanemys convenarum and Foxemys mechinorum.
Acknowledgements This research has been funded by the Ministerio de Economı´a, Industria y Competitividad (FPDI-2013-18986, IJCI-2016-30427
and CGL2015-68363-P). The preparation of the new specimens has been performed in the ‘‘Taller de Empleo Restauracio´n del Patrimonio Paleontolo´gico de los Yacimientos de Cuenca’’, funded by the Junta de Comunidades de Castilla-La Mancha. The authors thank H. Tong (Institute of Vertebrate Paleontology and Paleoanthropology, China), C. Corral (MCNA, Spain), J. Le Loeuff (Muse´e des Dinosaures d’Espe´raza, France), T. Tortosa (Muse´um d’Histoire Naturelle d’Aix-en-Provence, France), F. de Lapparent de Broin, R. ¨ si Allain and N.-E. Jalil (Pale´ontologie, MNHN Paris, France), A. O and M. Rabi (Magyar Terme´szettudoma´nyi Mu´zeum, Hungary), and A. Mechin and P. Mechin (Vitrolles, France) for access to several of the bothremydid specimens used for the comparisons performed here. The members of the Grupo de Biologı´a Evolutiva (UNED), especially F. Marcos, M. Martı´n and I. Narva´ez, are thanked for the collaboration in the excavation, preparation and study of the Lo Hueco specimens of Foxemys mechinorum. Thanks to the editor G. Escarguel and to J. Claude, R. Vullo and an anonymous reviewer for comments and suggestions.
Appendix A. Supplementary information New characters coded for the taxon from Lo Hueco studied in this paper, relative to those considered by Pe´rez-Garcı´a et al. (2013): Pelvis sutured to the shell (Character 133, State 1) Ilium columnar, expanded mediolaterally (Character 134, State 1) Pelvis narrow, ilia close to midline (Character 135, State 1) Cervical scute absent (Character 138, State 1) Nuchal width equals to its length (Character 139, State 2) Pygal notch absent, margin smooth (Character 140, State 2)
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Neural series completeness to costals 7 (Character 141, State 2) Iliac scar on costals 7 and 8 and suprapygal (Character 142, State 2) Costal 1 two times longer than costal 2 (Character 143, State 1) Rectangular first neural (Character 144, State 0) Neural series pattern regular, most hexagonal, coffin-shaped (Character 145, State 2) Seven neurals (Character 146, State 2) Narrow peripheral 1/costal 1 contact, the anterior margin 2 times this contact (Character 147, State 2) Contact of the axillary process with the costal 1 present, but separated from the costal 2 suture (Character 148, State 1) Axillary process extent on the main body of the peripheral 3 (Character 149, State 2) Inguinal buttress extends medially to the center of the costal 5 (Character 150, State 1) Absence of supramarginal scutes (Character 151, State 2) Vertebral scutes narrower than the pleurals (Character 152, State 1) Absence of nuchal embayment (Character 154, State 0) First thoracic rib smaller and closer to the 2nd rib (Character 155, State 1) Small costovertebral tunnel (Character 156, State 2) Shell texture composed by weak granulated polygons (Character 175, State 1) Axillary scar slightly wider posteromedially than anterolaterally (Character 176, State 1) Vertebral 1 anterolaterally covering peripheral 1 only or the suture between peripheral 1 and 2 (Character 177, State 0) Vertebral 1 as wide as vertebral 2 (Character 178, State 1) Posterior end of the entoplastron reaching the carapace-plastron bridge level (Character 179, State 1) Ischiac scar triangular in shape with the posterior tip very anterior to the anal notch (Character 180, State 2)
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