[Palaeontology, Vol. 54, Part 6, 2011, pp. 1393–1414]

A NEW LATE JURASSIC TURTLE FROM SPAIN: PHYLOGENETIC IMPLICATIONS, TAPHONOMY AND PALAEOECOLOGY by BEN J. SLATER1, MATI´AS REOLID2, REMMERT SCHOUTEN3 and MICHAEL J. BENTON3 1School of Geography, Earth and Environmental Sciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK; e-mail: [email protected] 2Departmento de Geologı´a, Universidad de Jae´n, Campus Las Lagunillas sn, 23071 Jae´n, Spain; e-mail: [email protected] 3School of Earth Sciences, University of Bristol, Wills Memorial Building, Queen’s Road, Bristol BS8 1RJ, UK; e-mails: [email protected], [email protected]

Typescript received 26 October 2010; accepted in revised form 27 May 2011

Abstract: The Jurassic was an important period in the evo- of the new taxon is hard to resolve, and it might be either a lution of Testudinata and encompasses the origin of many paracryptodire or a basal testudine, but it is distinct from clades, and this is especially true of Jurassic turtles from Wes- Plesiochelys. A complex taphonomic history is shown by a tern Europe. A new genus and species of Late Jurassic turtle, range of overlying grazing traces and bioerosion on the cara- Hispaniachelys prebetica gen. et sp. nov. from the upper Ox- pace. The carapace was subsequently overturned and buried fordian of the Prebetic (Southern Spain), is described on the ventrally up, terminating grazing activity, and was then bored basis of postcranial material. The specimen is the only known by sponges before final burial. Scanning electron microscopy tetrapod from the Mesozoic of the Prebetic and the oldest reveals phosphatic microspheroids associated with bacterial turtle from southern Europe. A mosaic of characters indicates decay in the vascular cavities of the cancellous bone, suggest- this is a new genus: it displays basal features including dorsal ing the carapace may have acted as a closed microenviron- epiplastral processes ⁄ reduced cleithra, no medial contact of ment in which decay-derived authigenic minerals formed. the extragulars and a long first thoracic rib, alongside derived characters including an absence of mesoplastra and the verte- Key words: Testudinata, Testudines, taphonomy, marine bral 3 ⁄ 4 sulcus crossing neural 5. The phylogenetic position turtles, Oxfordian, Spain.

T he stratigraphic range of turtles (i.e. Testudinata sensu The earliest known turtle is Odontochelys semitestacea Joyce et al., 2004) extends from the Triassic to the present from the Late Triassic of Guizhou, China, which is day, with extant species occupying an array of niches, 220 myr old (Li et al. 2008), some 10 myr older than Pro- from terrestrial and aquatic to fully marine (Ernst and ganochelys quenstedti from Germany, previously regarded Barbour 1989). The evolution and development of the as the basal sister group to all other turtles (Gaffney and highly derived body plan of turtles has been a focus of Meylan 1988; Gaffney 1990; Joyce 2007). Modern turtles much attention (deBraga and Rieppel 1997; Lee 1997; are divided into two clades, Pleurodira and Cryptodira, Rieppel and Reisz 1999; Cebra-Thomas et al. 2005; Joyce based on the manner in which they withdraw their head et al. 2009; Rieppel 2009), which reflects the extreme and neck into the shell: pleurodires retract the head by modification of the basic tetrapod body plan in turtles, making a horizontal ‘S’ bend in the neck, whereas cryp- and their long-lasting success. New information has come todires make a vertical bend. These neck-folding modes from significant discoveries of early fossil stem turtles (Li are hard to determine in early fossil turtles, and the et al. 2008; Joyce et al. 2009) and study of the growth, assignment of some Jurassic taxa has been debated. For embryology and ontogeny of modern turtles (Burke 1989; example, Kayentachelys aprix from the Early Jurassic Hirayama 1998; Joyce and Gauthier 2004; Scheyer et al. (190 Ma) was previously thought to be the earliest cryp- 2008; Snover and Rhodin 2008; Rieppel 2009). Neverthe- todire (Gaffney et al. 1987), but more recent studies less, much is still not understood about early turtle evolu- (Joyce 2007) have suggested it is a more basal turtle and tion and divergence, particularly their relationship to that Pancryptodira, the clade including modern cryptod- other groups of amniotes (Laurin and Reisz 1995; Burke ires and their stem taxa, did not diverge until the Middle et al. 1996; Lee 1997; Zardoya and Meyer 2001). Jurassic (Danilov and Parham 2006, 2008; Sterli 2008).

ª The Palaeontological Association doi: 10.1111/j.1475-4983.2011.01100.x 1393 1394 PALAEONTOLOGY, VOLUME 54

Complete turtle specimens are rare in the Jurassic cates that the turtle occurs in the Bimammatum Biozone (Joyce 2000), being confined usually to fragmentary (Olo´riz et al. 1999). The sediments were deposited in a remains of either the skull or shell in isolation. Much pre- mid-shelf environment on a carbonate epicontinental vious work on turtles has therefore focused on identifying shelf system. The marl-limestone rhythmites represent phylogenetic relationships through cranial (e.g. Gaffney fluctuations in carbonate productivity and delivery of si- 1975a, 1984) or shell characters (Joyce 2003). The skull liciclastic material derived from the proximal Iberian pal- displays wide disparity between species and contains aeomargin, which is defined by the extent of Iberian many diagnostic characters (Gaffney 1979), but it is often Massif tabular sediments immediately to the north (Olo´- not preserved, or only in isolation from carapace and riz et al. 2003, 2006; Reolid et al. 2010). The RGCH sec- plastron elements. Joyce (2007) provided a comprehensive tion has been heavily studied for its rich invertebrate character matrix of both cranial and postcranial charac- fauna (Olo´riz et al. 2002, 2003, 2006; Reolid 2003, 2008; ters, helpful here in that our specimen consists primarily Reolid et al. 2008), but vertebrates have not so far been of dermal elements of the shell, with some isolated verte- reported. brae. Late Jurassic turtles are distributed widely across Eur- ope, with specimens from Britain, Germany, France and METHODS Switzerland (Lapparent de Broin 2001). The majority of these have been assigned to the families Plesiochelyidae, The specimen was prepared by Remmert Schouten (RS) Eurysternidae and Thalassemydidae, but the distinctive- using both mechanical and chemical means. Pneumatic ness of these families has been questioned in recent air pens were used to remove the extensive limestone phylogenetic analyses (Joyce 2007). Late Jurassic turtles matrix, and the remaining material was dissolved in from the Iberian microcontinent include those from the 5 per cent acetic acid, buffered with calcium phosphate Lourinha˜ Formation (Kimmedigian–Tithonian) of wes- to protect the bone surface. In addition, a solution of tern Portugal (Antunes et al. 1988) and trackways from Paraloidª followed by a paraffin wax coating was the Late Jurassic Vega, Teren˜es, and Lastres formations painted onto the exposed areas of the bone prior to (Kimmeridgian) of Asturias, Spain (Avanzini et al. each acid treatment to further protect the bone from 2005). Turtles are poorly represented in the Oxfordian acid attack. Thin sections of the carapace were studied (Bardet 1995), with only an incomplete Plesiochelys and photographed under a plain light microscope to specimen from the Oxfordian of Germany (Kuhn assess the bone histology. 1949). Many fossil turtles are known from the Oxford For scanning electron microscopy (SEM), fragments of Clay of England, but this is largely Callovian in age carapace and indeterminate fossil bones were mounted (Martill and Hudson 1991). Outside Europe the Oxfor- and coated with gold and carbon. Secondary electron dian turtle Caribemys oxfordiensis has been found in images were made to study internal ultrastructure and Cuba (De la Fuente and Iturralde-Vinent 2001). Con- crystal morphology, and back-scattered electron (BSE) sidering their paucity in the Oxfordian, the discovery of imaging and energy-dispersive X-ray (EDX) analyses to a new turtle of this age from Spain is significant. obtain textural and chemical data. These analyses were The aim of this paper is to describe the new specimen performed using the FEI Quanta 400 at the Centro And- in detail, to identify it and determine its relationships, to aluz de Medio Ambiente (CEAMA, Granada). present information on its bone histology and taphonomy and to discuss its palaeoecology. SYSTEMATIC PALAEONTOLOGY

GEOGRAPHICAL AND GEOLOGICAL Order TESTUDINATA Klein, 1760 (sensu Joyce et al. 2004) SETTING Infraorder TESTUDINES Batsch, 1788

The specimen was found by Matı´as Reolid (MR) in bed Hispaniachelys prebetica gen. et sp. nov. 62 (upper Oxfordian) of the Riogazas-Chorro (RGCH) Text-figure 2 section of the Lorente Formation of the External Prebetic, the northernmost part of the Betic Cordillera in southeast Derivation of name. Genus after the Latin for Spain and Greek Spain (Text-fig. 1). Bed 62 is within a 22-m sequence of for turtle, species after the Prebetic of Andalucı´a (Spain), where well-stratified limestone and marl rhythmites dominated the specimen was found. by limestones, which make up the Middle Oxfordian to Lower Kimmeridgian age Lorente Formation (Olo´riz Holotype. RGCHSP-62-52 (Text-fig. 2), housed in the Museo de ´ et al. 2002, 2003). The ammonite biostratigraphy indi- Paleontologıa of the Universidad de Granada, Spain. SLATER ET AL.:NEWJURASSICTURTLEFROMSPAIN 1395

TEXT-FIG. 1. Geological map of the Prebetic outcrops (Betic Cordillera) in the Sierra de Cazorla area (A) with location of the Riogazas-Chorro (RGCH) section (co-ordinates 3;0¢25¢¢– 35;52¢55¢¢ sheet 928 (Cazorla) of the National Topographic Map; Scale 1:50 000), and stratigraphic section (B) with the ammonite biostratigraphy for the Bimammatum Biozone within the Lorente Formation (based on Olo´riz et al. 1999); note black arrow indicates the level with the fossil turtle remains.

Type stratum and locality. Bed 62 of the Lorente Formation; of preservation states. Consequently, specimen RGCHSP- Bimammatum Ammonite Biozone, Oxfordian, Late Jurassic; Sierra 62-52 is compared primarily to species and genera in de Cazorla: Riogazas-Chorro-Sponges section, Prebetic, Betic which the morphology of the carapace and plastron is Cordillera, western Andalucı´a, east of Jae´n, southeast Spain. well established. Throughout the comparison and descrip- tion, the following species are considered, with key refer- Diagnosis. Moderately large turtle with a thick fully ossi- ences: Eileanchelys waldmani (Anquetin et al., 2008); fied carapace; eight hexagonal neurals; eight costals; trape- Condorchelys antiqua (Sterli, 2008); Plesiochelys soloduren- zoidal nuchal; a dorsal epiplastral process (cleithra); sis (Ru¨timeyer, 1873; Bra¨m 1965); Tropidemys langi (Ru¨ti- diamond shaped entoplastron that does not separate the meyer, 1873; Bra¨m 1965); Thalassemys hugii (Ru¨timeyer, anterior portions of the epiplastra; single cervical scute 1873; Bra¨m 1965); ‘Craspedochelys’ picteti (Ru¨timeyer, covering half of the nuchal; vertebral 3–4 sulcus crossing 1873; Bra¨m 1965); Idiochelys fitzingeri (Meyer, 1839; Ru¨ti- neural 5; anteroposteriorly narrow pectoral scutes; a par- meyer 1873); Kayentachelys aprix (Gaffney et al., 1987; tially sinusoidal pectoral ⁄ humeral sulcus; anal scute con- Joyce et al. 2006); Platychelys oberndorferi (Wagner, 1853; fined to xiphiplastron. Bra¨m 1965); Proganochelys quenstedti (Baur, 1887; Gaffney 1990); Proterochersis robusta (Fraas, 1913); Palaeochersis Comparison. As noted by Joyce (2000), a large number of talampayensis (Rougier et al., 1995); Xinjiangchelys lati- turtle specimens from the Jurassic of Europe have been marginalis (Peng and Brinkman, 1993); Mongolochelys described on the basis of postcranial material in a range 1396 PALAEONTOLOGY, VOLUME 54

AB

50 mm

TEXT-FIG. 2. Hispaniachelys prebetica n. gen. et n. sp., RGCHSP-62-52, Oxfordian, Riogazas-Chorro section, Betic Cordillera, SE Spain. A, Dorsal and B, ventral views of the specimen. efremori (Khosatzky, 1997) and Glyptops plicatulus (Cope, taxon Kayentachelys aprix also shows features present in 1877). H. prebetica, including dorsal epiplastral processes ⁄ cleithra Hispaniachelys prebetica gen. et sp. nov. is a moderately (Joyce et al. 2006) and a single, wide but narrow cervical. large turtle with a thick carapace, similar in its oval out- H. prebetica differs from K. aprix and other taxa such as line and thickness to the specimen described as Plesioche- Glyptops plicatulus because it lacks mesoplastra. lys solodurensis by Bra¨m (1965). H. prebetica differs from P. solodurensis and all other Plesiochelys in its possession of a dorsal epiplastral process. The presence of this basal Comparative description character means the new turtle can therefore be excluded from the ‘Plesiochelyidae’. It has previously been demon- General preservation. The specimen comprises solely postcranial strated that the dorsal epiplastral process may be a rem- elements, including the majority of the carapace and plastron nant of the cleithrum (Joyce et al. 2006). H. prebetica (Text-fig. 2), some disarticulated cervical and thoracic vertebrae, shares many characters with Eileanchelys waldmani from and some of the internal bones of the shell such as the dorsal vertebrae, and the scapula. Elements of the skeleton that pro- the Bathonian (Anquetin et al. 2008), such as a dorsal trude from the carapace such as the skull, tail and limbs are epiplastral process (reduced cleithra), a trapezoidal missing, as is commonly the case in fossil turtles (Meyer 1991). nuchal, an osseous connection of the plastron to the cara- The posterior elements of the carapace are also disarticulated or pace, an entoplastron that does not divide the epiplastra missing, including much of the pygal region. The carapace itself anteriorly and an anal scute that does not extend to the is preserved in three dimensions and therefore displays its origi- hypoplastron. H. prebetica differs from E. waldmani, how- nal curvature with no signs of flattening. The right-lateral ever, in lacking mesoplastra. Additionally, the sulcus peripherals are disarticulated from the carapace, although some between vertebrals III and IV crosses neural 6 in E. wald- are preserved in isolation. The plastron collapsed into the cara- mani and another stem turtle, Condorchelys antiqua (Sterli pace, as the specimen was preserved with the ventral surface fac- 2008), rather than neural 5, as in H. prebetica. The basal ing upwards, and consequently, the plastron is broken up but SLATER ET AL.:NEWJURASSICTURTLEFROMSPAIN 1397 still relatively well preserved. A number of isolated fragments of nuchal is subrectangular, with a partially convex anterior mar- the carapace are also preserved. gin, shallow trapezoidal posterior margin and linear lateral edges, similar to that seen in the Plesiochelyidae and Eurysterni- dae (Joyce 2003). The posterior margin is serrated and interlocks Carapace with the first costals and first neural. The nuchal is domed and does not become depressed at the anterior end, in contrast to The carapace (Text-figs 2, 3A) is 430 mm long in the midline, Xinjiangchelys latimarginalis and Solnhofia parsonsi. The carapa- 340 mm wide at right angles through peripheral V, and 175 mm cial morphology of Eileanchelys waldmani is domed (Anquetin deep at the dorsoventral axis, the highest point. The carapace is et al. 2008), though all reported specimens are variably frag- significantly domed at the anterior end, but becomes progres- mented and compressed. A trapezoidal nuchal is also present in sively flattened in the posterior half. The preserved elements of Eileanchelys waldmani (Anquetin et al. 2008). The first thoracic the carapace include the nuchal, 12 of the 16 costals, three of vertebra is preserved on the underside of the nuchal. which are partially preserved, neurals 1, 3, 4, 5, 6, 7 and 8, and part of the first suprapygal. Sixteen of the 22 peripherals are pre- Neurals. The specimen possesses eight neural plates, the first of served. The carapacial plates have a relatively even and continu- which is partially preserved but can be seen to be subrectangular, ous thickness of c. 9 mm. The outline of the carapace is oval, as with two small ‘V’-shaped notches on the anterior margin that in Plesiochelys solodurensis (Ru¨timeyer 1873; Bra¨m 1965). Cara- interdigitate with the posterior margin of the nuchal. The second pace elements lack sculpture and keels or other external orna- neural is not preserved, and only its length can be inferred ment, as is the case in most other turtles (Joyce 2007). The through the border with the costal. Neurals III–VII are of a dis- smooth carapace separates the specimen from Platychelys obern- tinctive hexagonal shape with short anterior sides, similar to dorferi (Wagner 1853; Bra¨m 1965), which exhibits angular sculp- those of Solnhofia parsonsi (Joyce 2000) and Plesiochelys solodur- turing of the carapace. ensis (Bra¨m 1965), with a relatively narrow anterolateral edge that enlarges increasingly in more posterior neurals (Text-fig. 3A). Nuchal. The nuchal bone is poorly preserved as its dorsal sur- Neurals II–VII also decrease in length towards the posterior. In face is heavily weathered and pitted, and the right anterolateral contrast to P. solodurensis, in which the longest neurals occur in margin is damaged by bioerosion, but the outline is clear. The the centre (Oertel 1924; Bra¨m 1965), neural IV in this specimen

CE GUL MA I EG A MA I B per I nu MA II per II MA II co1 ne1 VE I MAIII epi MA III ent per III PL I MA IV MA IV ne2 co2 VE II bu HUM per IV co3 ne3 MA V MAV per V PL II hyo PECT MA VI IM per VI co4 ne4 MA VI VE III per VII MAVII ne5 ABD co5 PL III MA VIII MA VII hyp per VIII MA VIII ne6 co6 MA IX VE IV FEM

perIX ne7 100 mm MA IX co7 PL IV MA X ne8 xiph MA X per X co8 AN spy MA XI VE V MA XI

per XI MA XII MA XII

TEXT-FIG. 3. Hispaniachelys prebetica n. gen. et n. sp., RGCHSP-62-52, Oxfordian, Riogazas-Chorro section, Betic Cordillera, SE Spain. A, restored carapace in dorsal view, dashed lines detailing arrangement of scutes, and solid lines the sulci between the underlying bones. B, restored plastron in ventral view, dashed lines detailing arrangement of scutes. Abbreviations: ABD, abdominal scute; AN, anal scute; bu, axillary buttress; CE, cervical scute; co, costal bones; EG, extragular scute; ent, entoplastron; epi, epiplastron; FEM, femoral scute; GUL, gular scute; HUM, humeral scute; hyo, hyoplastron; hyp, hypoplastron; IG, intragular scute; IM, inframarginal scute; MA, marginal scute; ne, neural bones; nu, nuchal bone; PECT, pectoral scute; per, peripheral bones; PL, pleural scute; spy, suprapygal bone; VE, vertebral scute; xiph, xiphiplastron. 1398 PALAEONTOLOGY, VOLUME 54 is shorter than neurals III and V. Neural VIII is the smallest in vessel in life. The internal morphology of the bridge peripherals total area, being wider than it is long and asymmetrical in form. is often not described in turtle fossils, as it is generally not visi- The shape of the eighth neural is variable in some species of tur- ble. All preserved peripherals are longer than they are wide. tles, and this may therefore be a developmental feature (Peng and Brinkman 1993). In Plesiochelys and ‘Craspedochelys’ picteti (Ru¨ti- Costals. The presence of eight costal bones can be inferred, meyer 1873; Bra¨m 1965; considered a junior synonym of Plesi- though the eighth is only partially preserved. The anterior costals ochelys by Gaffney 1975b), the position of the vertebral IV ⁄ V are deeply arched, whereas posterior costals are flattened, giving sulcus is variable (Bra¨m 1965). The dorsal row of neurals has no the carapace a lower region towards the rear. Costal I is similar gaps, which prevents medial contact of the costals, as in most to that of Plesiochelys solodurensis, although the sutures to the basal eucryptodires (Joyce 2007). The neurals differ from those of nuchal and peripherals I and II are less linear with more protru- Tropidemys langi (Ru¨timeyer, 1873; Bra¨m 1965) because they lack sions. Costal II has a shorter contact with the neural than the the distinct ridge that runs the length of the neurals. The neurals peripherals, matching its laterally flared shape (Text-fig. 3A). of Eileanchelys waldmani are badly preserved in comparison to Costals III–VII are perpendicular to the longitudinal axis and Hispaniachelys prebetica, and it is not possible to discern whether possess relatively parallel borders. Costal VIII is narrower, giving it possessed 8 or 9 neurals (Anquetin et al. 2008). it a wedge-shaped appearance, and it has a rounded lateral mar- gin with peripheral X rather than the triangular peripheral-costal Peripherals. There are 11 pairs of peripherals, an unequivocal contacts of the other costals. There are no carapacial fontanelles, synapomorphy of Testudines and some basal clades (Joyce as in Plesiochelys, but differing from other Late Jurassic turtles 2007). The anteriormost peripherals are well preserved, with such as Eurysternum wagleri (Zittel 1877), Idiochelys fitzingeri obvious sulci portraying the arrangement of overlapping mar- (Meyer 1839; Ru¨timeyer 1873), Solnhofia parsonsi (Joyce 2000) ginal scutes, each of which overlaps two peripherals. The periph- and Thalassemys hugii (Bra¨m 1965) which all have carapacial erals are all sutured to the costals (Text-figs 2, 3A). The first fontanelles. Where visible in ventral view, the costals have pro- peripheral is elongate and contacts a large portion of the first nounced rib heads (Text-fig. 5), which shallow rapidly towards costal. This is the condition (Peng and Brinkman 1993) in Plesi- the centre of the costal. ochelys, Solnhofia parsonsi and Kayentachelys aprix, whereas more derived taxa such as Xinjiangchelys latimarginalis have a short- ened first peripheral. The second peripheral is shorter than the Carapacial scutes first and contacts both the first and second costals. The second peripheral also has a serrated protrusion at its dorso-posterior Sulci are well developed across the entire carapace in RGCHSP- edge that intersects between the first and second costals, forming 62-52, although bioerosion has removed or obscured their con- a ‘V’-shaped triangular division between the peripheral margins figuration in some places, such as the right side (Plate 1F). of the two costals. Peripheral III is proportionally longer than in P. solodurensis, with a serrated contact to peripheral IV, and Cervical scute. RGCHSP-62-52 shows only one cervical scute, a contacting only costal II. Peripheral IV does not contact the character that excludes the specimen from the Plesiochelyidae third costal as in P. solodurensis, only bordering costal II, which (Bra¨m 1965; Lapparent de Broin et al. 1996; Joyce 2003, 2007), is also the case in Kayentachelys aprix. Peripheral V is only all of which possess three cervical scutes. The cervical scute is sutured to costal III. Peripheral VI contacts both costals III and close to rectangular in shape, differing from the trapezoidal cer- IV. Peripheral VII is shorter and is fused to both costals IV and vical scute of Solnhofia parsonsi (Joyce 2000), and from that of V. Peripheral VIII has a long contact with costal V and a rela- Idiochelys fitzingeri (Meyer 1839; Ru¨timeyer 1873), which is tively short contact with costal VI. The suture between peripher- wider than the entire nuchal. als VIII and IX is partly sinuous. Peripheral X is different in that it intersects deeply between costals VII and VIII, giving it a con- Vertebral scutes. The vertebral scutes are hexagonal in form, as cave lateral margin with costal VIII. The margin of peripheral X revealed by the prominent sulci (Text-fig. 3A), similar in shape is also elongate, meaning that the suture between peripherals X but narrower than those of P. solodurensis, being more akin to and XI is curved. Peripheral XI contacts costal VIII and the first the hexagonal vertebrals of Eurysternum wagleri (Zittel 1877), suprapygal, and the posterior suture to peripheral XI is deeply Palaeomedusa testa (Meyer 1860; Joyce 2003) and Idiochelys fit- serrated. Peripheral XI would contact the second suprapygal and zingeri (Meyer 1839; Ru¨timeyer 1873). Tropidemys langi (Ru¨ti- the pygal in life, but these are not preserved. Several disarticulat- meyer 1873; Bra¨m 1965) also possesses narrow vertebral scutes, ed peripherals (Text-fig. 4) are bridge peripherals from the but these are somewhat more rectangular. Consequently, the right-hand side and show a triangular pit with a rugose surface four pleural scutes on either side are wide. Nonetheless, the ver- on their internal side (Text-fig. 4D, G), which presumably tebral scutes are wider than long, the primitive condition (Peng accommodated the osseous connection between carapace and and Brinkman 1993). The anterior and posterior margins of the plastron. Similar pits were also described in Xinjiangchelys chowi vertebral and pleural scutes run parallel to those of the costal (Matzke et al. 2005), though these were interpreted as sockets bones. The vertebral III–IV sulcus is on neural V, differing from for pegs that protrude from the plastron into the peripherals, both Eileanchelys waldmani and Condorchelys antiqua where it is which is a more derived feature (Tong et al. 2002). A small tun- on neural VI. Anterolaterally, the margins of the first vertebral nel structure extends from the pits on the internal surface of the scute contact the cervical scute and the first and second margi- bridge peripherals (Text-fig. 4E–H), which likely housed a blood nals (Text-fig. 3A). SLATER ET AL.:NEWJURASSICTURTLEFROMSPAIN 1399

AB C D rugose surface

matrix

bridge peripheral fragment bridge peripheral fragment per II? 10 mm per II?

EF G H

vs vs vs vs

matrix

per VI per VI per IV per IV rugose surface rugose surface

I J M

per II? bridge peripheral fragment 10 mm K L

per VI

per IV 20 mm

TEXT-FIG. 4. Hispaniachelys prebetica n. gen. et n. sp., RGCHSP-62-52, Oxfordian, Riogazas-Chorro section, Betic Cordillera, SE Spain. Internal and external surfaces of isolated peripherals, with corresponding interpretive diagrams, and damaged scapula. A, C, I, fragment of bridge peripheral in internal (A, C) and external (I) views. B, D, J, fragment of bridge peripheral in internal (B, D) and external (J) views. E, G, K, fragment of bridge peripheral IV in internal (E, G) and external (K) views. F, H, L, bridge peripheral VI in internal (F, H) and external (L) views. Dashed lines indicate sulci. M, dorsal view of damaged right scapula shown by black arrow; white arrow indicates part of the fourth dorsal vertebra. Abbreviations: per, peripheral; vs, vascular structure.

Pleural scutes. The pleural scutes (Text-fig. 3A) are proportion- langi (Ru¨timeyer 1873; Bra¨m 1965). All pleurals have a margin ally wider than in Plesiochelys solodurensis, more akin to the with two vertebrals and three marginal scutes, aside from the extension over a large area of the costals as seen in Tropidemys first pleural which contacts marginals II–V (as well as a small 1400 PALAEONTOLOGY, VOLUME 54

TEXT-FIG. 5. Hispaniachelys prebetica AB n. gen. et n. sp., RGCHSP-62-52, rh co VII Oxfordian, Riogazas-Chorro section, Betic Cordillera, SE Spain. A, underside of a fragment of right costal VII showing part of the rib process. B, part of epiplastron. C, unknown fragment. D, fragment of left posterior part of carapace, including parts of peripherals VIII, IX and X. E, fragment of unknown rh? epi costal. Abbreviations: co, costal; co?, 10 mm possible fragment of costal; epi, C DE co? per VIII epiplastron; per, peripherals; rh, rib- head; rh?, possible rib-head. co?

fracture

per IX

per X

supramarginal scute) and has no border with the first bridge is longer than the anterior or posterior plastral lobes marginal. (Text-fig. 3B), as in Plesiochelys. The absence of mesoplastra is a synapomorphy of the Eucryptodira (Gaffney and Meylan 1988). Marginal scutes. There are 12 pairs of marginal scutes (Text- Musk ducts in the plastron, known from Siamochelys peninsular- fig. 3A) that do not encroach onto the surface of the costals, as is, are unknown in H. prebetica. A central plastral fontanelle is in Plesiochelys and Tropidemys langi. A small supernumerary sub- present, although its apparent size is enhanced by damage. The marginal scute is visible on the left side between marginals III central plastral fontanelle is exhibited by specimens described as and IV and the first pleural. This could be an anomaly particular P. ‘etalloni’ (Oertel 1924; Bra¨m 1965), but not by P. solodurensis, to this specimen, as it cannot be checked on the right side. Zan- which exhibits a fully ossified plastron. Plastral fontanelles may gerl (1957) reported that such abnormalities are common in be a juvenile feature (Joyce 2007), although the features and extant turtles, and a similar submarginal is reported from Sol- proportions of this specimen suggest it is an adult. nhofia parsonsi (Joyce 2007). Epiplastron. The anterior portions of the epiplastra meet each other at the midline, and the entoplastron and hyoplastron pos- Plastron teriorly (Text-figs 3B, 6A, B). The epiplastra also have shallow notches at their anterior edges centred upon the sulci of the The individual elements of the plastron are well preserved, but gular scutes (Text-fig. 3B), but these are not anterior plastral they have collapsed after fossilization. The original form (Text- tuberosities that give the anterior plastral rim a sculptured mar- figs 2B, 3B) can be discerned, however, as the margins of each gin in the basal Proganochelys quenstedti and Proterochersis element of the plastron and the buttresses are visible. The plas- robusta. A dorsal epiplastral process (Text-fig. 6B) extends from tron is highly ossified, as in Plesiochelys (Bra¨m 1965; Joyce the middle of the epiplastron and is concave on the anterior 2000), lacking any bridge fontanelles. The anterior plastral lobe surface. A dorsal epiplastral process is a primitive feature seen in differs from that of P. solodurensis in being more elongate. The a larger form than that described here in Proganochelys quen-

EXPLANATION OF PLATE 1 Plain light microscope images of bone histology of Hispaniachelys prebetica n. gen et n. sp., RGCHSP-62-52. A, Thin section of costal carapacial bone (outer surface at top). B, Cancellous bone. C, layers of external cortical bone. D, External cortical bone. E, Borings on the dorsal surface of the carapace. F, Entobia bioerosion on the right-lateral costals. G, Grazing activity of regular echinoids (Gnatichnus) on dorsal surface of costals. PLATE 1

A B

500 μm

C

100 μm

D

1000 μm

500 μm

E F 50 mm

10 mm

G

10 mm

SLATER et al., bone histology of Hispaniachelys prebetica 1402 PALAEONTOLOGY, VOLUME 54

TEXT-FIG. 6. Hispaniachelys prebetica A ent B C 10 mm n. gen. et n. sp., RGCHSP-62-52, 10 mm Oxfordian, Riogazas-Chorro section, epi epi Betic Cordillera, SE Spain. A, ventral view of anterior portion of hyoplastron, abu dp epiplastron and entoplastron. B, left- lateral view of epiplastron. C, ventral D hyo 50 mm view of axillary buttress region. D, hyoplastron, dorsal surface, showing hyo muscle attachment scar; E, ventral view hyo of specimen; F, dorsal view of parts of E peripherals IX, X and XI. G, right-lateral view of inguinal buttress region and inguinal notch, including peripherals VII and VIII. H, view of displaced peripheral ibu VII. I, dorsal view of xiphiplastron. 100 mm Abbreviations: abu, axillary buttress; dp, F per IX G 10 mm dorsal process; ent, entoplastron; epi, epiplastron; hyo, hyoplastron; hyp, hypoplastron; ibu, inguinal buttress; per, peripherals; xiph, xiphiplastron.

50 mm per X I

per XI

H hyp

10 mm

xiph 10 mm

stedti (Baur 1887; Gaffney 1990), Proterochersis robusta (Fraas (Text-figs 3B, 6A). The anterior extension of the entoplastron 1913) and Palaeochersis talampayensis Rougier et al. 1995, and in forms an arrow shape between the epiplastra similar to that a reduced form equivalent to that seen in our specimen in Eile- described in Eileanchelys waldmani (Anquetin et al. 2008). anchelys waldmani (Anquetin et al. 2008), Kayentachelys aprix (Gaffney et al. 1987; Joyce et al. 2006), Xinjiangchelys latimargi- Hyoplastron. The anterior elements can be identified as the hy- nalis (Peng and Brinkman 1993), Meiolania platyceps (Owen oplastron in a slightly displaced position because of the position 1886; Gaffnet 1996), Mongolochelys efremovi (Khosatzky 1997) of the pectoral ⁄ humeral sulcus, which runs anterior to the axil- and Glyptops plicatulus (Cope, 1877). Joyce et al. (2006) demon- lary notch (femur hole) and the attachment of the buttress to strate that the dorsal epiplastral processes actually represent the the peripherals. The midline edge of the hyoplastron is lined by cleithra, as was suspected in earlier work (Jaekel 1915), but then a short row of processes that interdigitate with the opposite ele- reinterpreted as dorsal outgrowths emanating from the epiplastra ment. The axillary buttresses of the hyoplastron (Text-fig. 6C) (Gaffney 1990). are strongly developed and contact the internal surface of peripherals II and III and extend anteriorly and dorsally to con- Entoplastron. One lateral half of the entoplastron is preserved, tact the visceral surface of the first and second costals (Text- and its overall shape can be discerned from this and the oppos- figs 3B, 6C). This differs from Plesiochelys solodurensis and the ing gap in the hyoplastron. The entoplastron is smaller than the specimen described as P. ‘etalloni’ by Bra¨m (1965), in which the epiplastron and forms a small diamond shape with slightly axillary buttress only reaches peripheral III. The anterior exten- curved anterior margins, being sutured to both epiplastra at the sion of the buttresses to peripheral II is seen in Xinjiangchelys anterior margin and to the hyoplastra at the posterior margins latimarginalis (Peng and Brinkman 1993) and Solnhofia parsonsi SLATER ET AL.:NEWJURASSICTURTLEFROMSPAIN 1403

(Joyce 2000). The hyoplastron is sutured to peripherals II, III, The femorals are positioned further back than those of Sol- IV and V. The internal surface of isolated bridge peripherals can nhofia parsonsi and P. solodurensis, but in other respects are be seen in Text-figure 4, displaying holes that accommodated identical. The posterior midline femoral sulcus is partly sinusoi- the connection from the margins of the hyoplastron. dal and terminates at the anterior margin of the xiphiplastra. The anal scutes only overlay the xiphiplastra and do not Hypoplastron. The abdominal ⁄ femoral sulcus runs into the extend onto the hypoplastron, as in Eileanchelys waldmani inguinal notch. The inguinal buttresses attaching the hypoplas- (Anquetin et al. 2008) and Plesiochelys solodurensis. tron to the carapace run from the very anterior of peripheral V, along peripherals VI, VII and VIII (Text-figs 3B, 6G, F). The inguinal buttress also contacts costal VI; Kayentachelys Postcranial skeleton aprix and Plesiochelys classically possess large buttresses (Gaff- ney et al. 1987; Gaffney and Meylan 1988), which provide the Vertebrae. There is an isolated partly damaged cervical centrum shell with support by joining the plastron to the peripherals (Text-fig. 7A–E, K–O), and a partly preserved cervical (Text- (Joyce 2007). fig. 7V–A1). The isolated cervical centrum, possibly the fifth, shows a strongly developed ventral keel and a single transverse Xiphiplastron. The xiphiplastra (Text-figs 2, 3B, 6H) are similar process. It is short and wide, with stout pre- and postzygapoph- in outline to those of the specimen described as ‘Plesiochelys yses. The centrum is amphicoelous and ventrally keeled, as in hannoverana’ by Oertel (1924), with the suture to the hypopla- Proganochelys, Xinjiangchelys and Plesiochelys, and has a single stra sloping anterolaterally, rather than horizontally as in P. solo- short transverse process over the middle of the centrum. Cervical durensis. The suture to the hypoplastra is heavily serrated, ribs are not preserved. The neural canal is large and circular, possessing a rounded interdigitation at the midline and a sub- while the neural arch is relatively short and extends almost the triangular interdigitation at the anterolateral edge. length of the centrum but can only be observed in lateral view as matrix obscures anterior and posterior views. The diapophysis Plastral scutes. There is a single row of inframarginal scutes and parapophysis are separate, a primitive cryptodiran feature (Text-fig. 3B) laterally narrower than those of Plesiochelys solo- (Gaffney and Meylan 1988; Peng and Brinkman 1993). The first durensis. The full sequence of inframarginal scutes is unclear thoracic vertebra (Text-figs 7F–J, P–T; 8E, F) is partially pre- because some of the hypoplastron is obscured (Text-fig. 2). The served, the first thoracic rib being very long. The second thoracic first inframarginal overlaps peripherals III and IV and the hyopl- vertebra (Text-fig. 8A–D) has large parapophyses, and a dorso- astron, contacting marginals III and IV, the pectoral scute and ventrally elongate neural arch. Where visible, the sequential dor- the second inframarginal at the posterior margin. Inframarginal sal vertebrae are similar in appearance and bordered by strongly II contacts the pectoral scute and marginal V and is approxi- developed rib heads. The centrum of the second thoracic is mately square. Inframarginal III is an elongate version of the partly covered by matrix, which obscures some of the surface preceding one, contacting the pectoral, marginals V and VI and detail. The third and fourth dorsal vertebrae are also partly visi- the abdominal scute at the anterior margin. Inframarginal IV is ble in dorsal view where the carapace is damaged. an elongate rectangle that is laterally thin, covering peripherals V, VI and VIII, but it is uncertain whether there is another in- Ribs. The first thoracic rib (Text-fig. 8) extends almost the framarginal between this and the abdominal scute, as the area is length of the first costal, being very elongate. The second tho- partially obscured. racic rib almost reaches the axillary buttress. The gular scutes (Text-fig. 3B) cover the anterior portion of the epiplastra and together form a ‘V’ shape that meets posteri- Scapula. There is a partially preserved right scapula (Text- orly at the margin between the epiplastra and entoplastron. The fig. 4M), which shows a damaged portion of a somewhat flat- extragulars lay either side of the gulars with their posterior mar- tened acromial process. gins perpendicular to the midline plastral sulcus. There is no medial contact of the extragulars, as in Kayentachelys aprix. Both Manus. Some isolated fragments of bone are preserved which the gulars and extragulars are confined to the epiplastra, with no are possibly part of a phalange and a carpal, but they are too extension onto the entoplastron. damaged to be conclusive. The humeral scutes collectively cover the entoplastron, the posterior part of the epiplastron and the anterior plastral lobe of the hyoplastron (Text-fig. 3B). The humerals are elongate ante- PHYLOGENETIC ANALYSIS roposteriorly in comparison to those of Plesiochelys. The pectorals are short and broad. The pectoral ⁄ abdominal sulcus is linear and runs parallel to the hyoplastron ⁄ hypoplas- At one time, the Spanish specimen might have been tron suture (Text-fig. 3B). assigned to the family ‘Plesiochelyidae’, together with The abdominal scutes are similar to those of Solnhofia parsonsi many other apparently aquatic Late Jurassic forms, and so and P. solodurensis, but the abdominal ⁄ femoral sulcus bisects the placed unequivocally within Eucryptodira, as one of sev- plastral midline further behind (Text-fig. 3B). The abdominals eral basal outgroups to Cryptodira. However, ‘Plesioch- appear to extend onto peripherals VI and VII, but there may elyidae’ turns out to be an ill-defined ragbag of species in have been an additional inframarginal scute. 1404 PALAEONTOLOGY, VOLUME 54

A B C D

lateral

ke E FGke H

posterior

ke I JKL

anterior tp tp cot

M NOP

dorsal tp

con con

QR S T

ventral

10 mm

con con

VWX U

matrix covered na YZ A1

prz tp nsu tp nsu cot cot SLATER ET AL.:NEWJURASSICTURTLEFROMSPAIN 1405

TEXT-FIG. 8. Hispaniachelys prebetica A B ne I poz n. gen. et n. sp., RGCHSP-62-52, Oxfordian, Riogazas-Chorro section, Betic Cordillera, SE Spain. First and second thoracic vertebrae. A–D, second dorsal vertebra, in posterior (A–B) and lateral (C–D) views. E–F, ventral view of rh dorsal II and part of dorsal I. Abbreviations: cen-f, centrum fragment; 10 mm nc con, part of condyle anterior end of centrum; cos I, first costal; cv VIII, part cen-f of eighth cervical vertebra; dor I, II, first C D and second dorsal vertebrae; na, neural arch; nc, neural canal; ne I, first neural; na ns, neural spine; nu, nuchal; pa, parapophysis; poz, postzygapophysis; rh, rib-head. ns

pa con 10 mm

cen-f nu dor I E F

cos

rh dor II poz ns 20 mm

need of revision, it has proved hard to retrieve in phylo- waldmani, Heckerochelys romani and Condorchelys antiqua, genetic analyses, and it is regarded as paraphyletic by as well as the three additional characters they added. We Joyce (2007). Further, the classic assumption that cryp- excluded the three ‘rogue’ taxa identified by Joyce (2007) todires and pleurodires are distinct clades among turtles and Anquetin et al. (2008), namely Portlandemys mcdow- that both originated in the Early Jurassic has not been elli, Sandownia harrisi and Mongolemys elegans. We coded confirmed by more recent phylogenetic analyses (e.g. Hispaniachelys according to those 139 characters (Table 1) Joyce 2007; Anquetin et al. 2008), and many Jurassic taxa and ran a cladistic analysis, in PAUP (Swofford 2002) have proved hard to resolve in the cladogram. using a heuristic search and a tree-bisection algorithm In view of these difficulties, we performed a cladistic with 5,000 replicates. analysis to determine the phylogenetic position of the The phylogenetic analysis (Text-fig. 9) gave mixed Spanish taxon. We used the cladistic data matrix from results, confirming the difficulty of achieving strong reso- Joyce (2007, pp. 80–95), with the addition of the three lution in parts of the tree, as reported earlier by Joyce taxa noted by Anquetin et al. (2008), namely Eileanchelys (2007) and Anquetin et al. (2008). The Adams and 50 per

TEXT-FIG. 7. Hispaniachelys prebetica n. gen. et n. sp., RGCHSP-62-52, Oxfordian, Riogazas-Chorro section, Betic Cordillera, SE Spain. Isolated cervical and dorsal centra. A–E, K–O, isolated cervical centrum, in lateral (A, K), posterior (B, L), anterior (C, M), dorsal (D, N) and ventral (E, O) views. F–J, P–T, isolated first thoracic centrum, in lateral (F, P), posterior (G, Q), anterior (H, R), dorsal (I, S) and ventral (J, T) views. U, first thoracic centrum in position on the ventral portion of the neural arch. V–A1, possibly fifth cervical vertebra in anterior view (V, Y), lateral view (W, Z) and posterior view (X, A1). Abbreviations: con, condyle posterior of centrum; cot, cotyle anterior of centrum; ke, ventral keel; na, neural arch; nsu, neurocentral suture; prz, prezygapophyses; tp, transverse process. 1406 PALAEONTOLOGY, VOLUME 54

TABLE 1. Character codings for Hispaniachelys prebetica gen et sp. nov.

????? ????? ????? ????? ????? ????? ????? ????? ????? ????? ????? ????001001 00000 21110 [01]0111 00012 10000 00010 00000 ????? ????? ??1??0???1 ????0 ????? ????? ???0

Codings according to the data matrix (136 characters) of Joyce (2007), as modified by Anquetin et al. (2008) by the addition of three further characters (139 characters). cent majority rule consensus trees (Text-fig. 9A, B) differ- in succession. It is a member of Testudinata (Joyce’s node entiated the major clades in Joyce’s (2007, p. 62) ‘pre- 1) based on the carapace, plastron and other classic turtle ferred’ tree, but with less resolution. Pleurodira, apomorphies, but cannot be assessed at the Palaeochersis Paracryptodira, Eucryptodira and Cryptodira are distin- node (node 2) because diagnostic apomorphies are all guished, but not always with the exact composition noted cranial. It is an unequivocal member of the Proterocher- by Joyce (2007). For example, in the Adams and majority sis + Testudines clade (node 3) based on derived states of rule consensus trees (Text-fig. 9A, B), the Pleurodira characters 71 (reduction in number of supramarginals), encompasses Platychelys, Caribemys and Notoemys, 72 (five or more vertebrals) and 80 (absence of postero- whereas these are close outgroups of Pleurodira in Joyce’s lateral entoplastral process), and of the Kayentache- (2007) preferred solution, although his consensus tree lys + Testudines clade (node 4) based on derived states of shows similar issues. The bootstrapped strict consensus characters 65 (11 pairs of peripherals), 71 (supramarginals tree (Text-fig. 9C), however, identified the components of absent), 94 (anterior plastral tuberosities absent) and 120 Pleurodira correctly. On the other hand, Paracryptodira is (cleithra reduced and with no osseous contact with cara- retrieved in the Adams consensus tree (Text-fig. 9A), but pace). Hispaniachelys is not a member of the Mongoloche- not in the 50 per cent majority or strict trees (Text- lys-Meiolania clade (node 5), but does belong to the fig. 9B, C) in which the two paracryptodire subclades, the Mongolochelys + Testudines clade (node 6), based on the Pleurosternidae and Baenidae, are separated as parts of an derived state of character 78 (medial contact of epipla- unresolved polytomy. The major clades Eucryptodira and stra), to the Kallokibotion + Testudines clade (node 7), Cryptodira are identified in the first two consensus trees based on derived states of characters 84 (axillary but- (Text-fig. 9A, B), but they are lost when only bootstraps tresses contact peripherals and first costal) and 86 (axil- over 50 per cent are retained (Text-fig. 9C). lary buttresses contact peripherals and costal V), and to In the light of the incomplete resolution of several Testudines (node 8), based on derived states of characters major clades, as noted earlier by Joyce (2007) and Anque- 62 (articulation of nuchal with eighth cervical vertebra tin et al. (2008), it is hard to be entirely confident about absent) and 79 (reduced posterior entoplastral process). the placement of a new taxon. According to the three Each of these nodes is associated with other apomorphies, consensus trees, Hispaniachelys prebetica appears at first but those could not be coded on our material, and there to occupy very different phylogenetic positions: in the are no contradictory codings in Hispaniachelys. Adams consensus tree (Text-fig. 9A), it is part of a basal Within Testudines, the situation is less clear, largely tritomy among Testudines, neither definitively a pleuro- because the codable characters themselves have equivocal dire ⁄ paracryptodire, nor a eucryptodire; in the 50 per evolutionary histories, according to Joyce’s (2007) phylo- cent majority rule consensus tree (Text-fig. 9B), it is a genetic analysis, and we lack evidence in the material of paracryptodire, associated with the baenid clade; and in Hispaniachelys to assess the unequivocally distributed the strict consensus tree (Text-fig. 9C), it is one of a large cranial and postcranial characters. For example, characters number of unresolved testudines that are not assigned to 73 (narrow vertebrals) and 74 (vertebral II–III sulcus shifts any major subclade. One observation is that, although the from neural VI to V) provide some evidence for assign- new Spanish turtle might well have been named as a spe- ment to Pleurodira or Pancryptodira, but cannot indicate cies of Plesiochelys, this genus falls definitively at the base a particular clade assignment. Character 85 (mesoplastra of Eucryptodira according to the first two consensus trees absent) is an apomorphy of Pancryptodira (but also Cryp- (Text-fig. 9A, B), and thus, it is distant phylogenetically todira and Chelidae), and 113 (first dorsal rib intermedi- from Hispaniachelys. ate in length) is an apomorphy of several pleurodire and In terms of character evolution, Hispaniachelys could cryptodire clades. Hispaniachelys does not appear to be a be coded for 46 of the 139 characters (33 per cent cod- member of the Platychelys clade (node 9) because it lacks ing), and of these coded characters, only 15 (11 per cent) derived states of characters 87, 91 and 100, even though it are in a derived state. These are sufficient to determine equivocally shows characters 76 and 85. Most apomor- that Hispaniachelys is a testudine. Comparison with phies of Pleurodira (node 12) are cranial, and Hispani- Joyce’s (2007, fig. 18) preferred phylogeny confirms that achelys lacks the derived state of character 68, but shows Hispaniachelys belongs within all the most inclusive clades 73, 74, 76 (?) and 120, but these can also apply to other Hypothetical ancestor Hypothetical ancestor Hypothetical ancestor Proganochelys quenstedti Proganochelys quenstedti Proganochelys quenstedti Proterochersis robusta Proterochersis robusta Proterochersis robusta Palaeochersis talampayensis Palaeochersis talampayensis Palaeochersis talampayensis Australochelys africanus Australochelys africanus 100 Australochelys africanus Kayentachelys aprix Kayentachelys aprix Kayentachelys aprix Eileanchelys waldmani Condorchelys antiqua 100 Condorchelys antiqua Eileanchelys waldmani 82 Eileanchelys waldmani Heckerochelys romani 98 Condorchelys antiqua Heckerochelys romani 73 Heckerochelys romani Meiolania platyceps 100 Meiolania platyceps 73 Meiolania platyceps Mongolochelys efremovi Mongolochelys efremovi Mongolochelys efremovi Kallokibotion bajazidi Kallokibotion bajazidi Kallokibotion bajazidi 100 Hispaniachelys prebetica Dorsetochelys delairi Dorsetochelys delairi Plesiochelys solodurensis Dorsetochelys delairi 100 Pleurosternon bullockii 92 Platychelys oberndorferi 100 100 Glyptops plicatulus Hispaniachelys prebetica Solnhofia parsonsi Elseya dentata 73 Dinochelys whitei Chelodina oblonga Hispaniachelys prebetica Thalassemys moseri PARACRYPTODIRA 73 Santanachelys gaffneyi Phrynops geoffroanus 93 65 Neurankylus eximius PLEURODIRA Trinitichelys hiatti Hangjiangchelys latimarginalis Caribemys oxfordiensis 83 Hangaiemys hoburensis Notoemys laticentralis TESTUDINES 100 Plesiobaena antiqua Boremys pulchra Judithemys sukhanovi Pelomedusa subrufa 100 Dracochelys bicuspis Erymnochelys madagascariensis 100 Baena arenosa Podocnemis expansa Chisternon undatum Sinemys lens 69 Ordosemys leios Pleurosternon bullockii Thalassemys moseri TESTUDINES 67 Plesiochelys solodurensis Platysternon megacephalum Glyptops plicatulus Emarginachelys cretacea Dinochelys whitei EUCRYPTODIRA 52 Solnhofia parsonsi Santanachelys gaffneyi Baptemys wyomingensis PARACRYPTODIRA Neurankylus eximius Dermatemys mawii Trinitichelys hiatti 61 Hangjiangchelys latimarginalis Mesodermochelys undulatus Hoplochelys crassa Plesiobaena antiqua 100 Pleurosternon bullockii Boremys pulchra 80 Toxochelys latiremis 59 93 Dermochelys coriacea 54 Glyptops plicatulus Baena arenosa 87 Dinochelys whitei Chisternon undatum 100 Caretta caretta Chelonia mydas 72 Protochelydra zangerli Thalassemys moseri 85 Macroclemys temminckii Plesiochelys solodurensis Hangaiemys hoburensis 93 61 Judithemys sukhanovi Chelydra serpentina Solnhofia parsonsi Gopherus polyphemus EUCRYPTODIRA Santanachelys gaffneyi CRYPTODIRA 90 Dracochelys bicuspis 62 Hangjiangchelys latimarginalis 100 Sinemys lens 53 Geoclemys hamiltonii Ordosemys leios Chrysemys picta Hangaiemys hoburensis TESTUDINES SLATER Mesodermochelys undulatus Platysternon megacephalum 95 Staurotypus triporcatus 56 99 Sternotherus odoratus Toxochelys latiremis 91 93 Protochelydra zangerli Dermochelys coriacea 100 Macroclemys temminckii Kinosternon flavescens Chelydra serpentina Mesodermochelys undulatus Caretta caretta 71 Chelonia mydas Gopherus polyphemus Toxochelys latiremis Judithemys sukhanovi 93 Geoclemys hamiltonii 73 Dermochelys coriacea CRYPTODIRA 89 Caretta caretta Dracochelys bicuspis 93 57 Chrysemys picta Elseya dentata Chelonia mydas Sinemys lens 93 100 Neurankylus eximius AL. ET Ordosemys leios 100 Chelodina oblonga 53 Phrynops geoffroanus 67 Trinitichelys hiatti Platysternon megacephalum 100 Plesiobaena antiqua Protochelydra zangerli 93 Notoemys laticentralis 67 Macroclemys temminckii 93 Platychelys oberndorferi 62 Boremys pulchra 93 Caribemys oxfordiensis 67 Baena arenosa Chelydra serpentina 93 Chisternon undatum Emarginachelys cretacea 100 Pelomedusa subrufa 93 Erymnochelys madagascariensis 54 Adocus beatus :NEWJURASSICTURTLEFROMSPAIN Gopherus polyphemus 89 Zangerlia neimongolensis Geoclemys hamiltonii Podocnemis expansa Emarginachelys cretacea 59 Basilemys variolosa Chrysemys picta 55 Peltochelys durlstonensis Baptemys wyomingensis Baptemys wyomingensis 50 Dermatemys mawii 74 Dermatemys mawii Anosteira ornata 97 Carettochelys insculpta Hoplochelys crassa 56 Hoplochelys crassa Staurotypus triporcatus 100 Apalone spinifera Staurotypus triporcatus 55 100 Sternotherus odoratus 100 Sternotherus odoratus Lissemys punctata Kinosternon flavescens Platychelys oberndorferi Kinosternon flavescens TRIONYCHOIDEA Caribemys oxfordiensis 100 Adocus beatus TRIONYCHOIDEA Adocus beatus 84 Notoemys laticentralis Zangerlia neimongolensis 100 Zangerlia neimongolensis 100 Basilemys variolosa 87 Elseya dentata Basilemys variolosa 74 Chelodina oblonga Peltochelys durlstonensis Peltochelys durlstonensis 51 100 Anosteira ornata Phrynops geoffroanus Anosteira ornata 100 Pelomedusa subrufa Carettochelys insculpta Carettochelys insculpta 95 100 Apalone spinifera Erymnochelys madagascariensis A Apalone spinifera B C Podocnemis expansa Lissemys punctata Lissemys punctata

TEXT-FIG. 9. Cladograms showing possible phylogenetic positions of Hispaniachelys prebetica, using the character matrix from Joyce (2007) and Anquetin et al. (2008), with the new specimen RGCHSP-62-52 inserted (character codings in Table 1), and the three ‘rogue taxa’ identified by those authors, namely Portlandemys mcdowelli, Sandownia harrisi and Mongolemys elegans, omitted. The cladistic analysis was performed in PAUP (Swofford 2002), using a heuristic search (5000 replicates, tree-bisection-reconnection, all character unordered; 481 trees retained; tree length = 365; consistency index = 0.47; retention index = 0.81; rescaled consistency index = 0.38). The three tree solutions are an Adams consensus tree (A), a 50 per cent majority rule consensus tree (B), and a strict consensus tree with bootstrap values (1000 replicates, only values over 50 per cent shown; C). 1407 1408 PALAEONTOLOGY, VOLUME 54 nodes, as noted. Assignment to certain key clades cannot which surround the porous cancellous region (Plate 1B). be assessed because relevant characters cannot be coded: The porous cancellous bone can also be seen under the Paracryptodira (node 15), Eucryptodira (node 18) and the SEM (Plate 2F). The external cortical region comprises Santanachelys clade (node 20). Hispaniachelys could densely compacted regular layers (Plate 1C). The collagen belong to the Solnhofia clade (node 19), based on posses- fibril bundles and thin vascular structures of the external sion of the derived state of characters 84 and 86, but it cortical layer are well preserved and can be made out in lacks 75, and the Xinjiangchelys clade (node 21) based on thin section and under the SEM (Plate 2A, B, E). the possession of the derived state of characters 73 and Towards the periphery of the external cortex, the colla- 113, but it lacks 99, but not to the Hangaiemys clade gen fibril bundles become more densely packed and (node 22) because it lacks the derived states of characters increasingly interwoven. Growth layers can be seen as 83 and 92, or to the Cryptodira (node 25) because the distinct parallel lines particularly in the outer half of the cleithra are reduced, but not absent (character 120(2)). external cortex and are wavy and less distinct in the More material of the vertebrae, limbs and especially of internal half (Plate 1A). The number of growth lines can- the skull of Hispaniachelys would assist in placing this not be determined because of weathering and pitting of taxon phylogenetically. However, as noted by previous the outer surface, regrettable because these have been authors (Joyce 2007; Anquetin et al. 2008), much more used in modern turtles to determine individual age work has yet to be carried out on all Jurassic turtles, and (Wilson and Tracy 2003). Vascular structures are con- further unequivocal apomorphies have yet to be discov- fined exclusively to the inner half of the cortical layers ered, before the phylogeny becomes clearer. and their abundance obscures any layering, although they are less abundant than in the porous cancellous region. Large primary vascular canals are scattered throughout TAPHONOMY AND PALAEOECOLOGY the inner half of the cortical layers. The internal cortical layer is like a reversed external layer in appearance, the Preservation and bone histology only significant difference being the absence of oxidation or weathering on the outer surface. In the cancellous The specimen is largely intact, with most of the elements region, vascular cavities average 0.1 to 0.2 mm in diame- of the carapace in original position. When found, the ter and constitute c. 75 per cent of the total area in cross specimen was overturned. The degree of fragmentation is section. The vascular spaces become increasingly flattened low and appears largely to affect the distal parts of some and elongated with increasing proximity to the cortical bones, which are fractured and not rounded. Other com- bone. ponents display some fragmentation and disarticulation An SEM EDX spectrum analysis (not illustrated) but are not significantly displaced (e.g. carapace plates). showed that the remains are preserved as calcium phos- The plastron has collapsed into the cavity of the carapace. phate (francolite). Aligned francolite crystal bundles are The external surface of the carapace displays traces of visible within the bone (Plate 2E), perhaps pseud- grazing composed of radial grooves, isolated circular bor- omorphs of the original collagen fibrils of the bone, ings (<5 mm) and small interlaced boring fields resem- revealing a linear structure to the cortical region. Fur- bling Entobia, which are created by endolithic sponges ther, filaments (<5 lm in diameter; Plate 2A, B) and (Farinati and Zavala 2002). The plastron and other bones globular structures (10–50 lm in diameter; Plate 2C, D) do not have trace marks on their surface. composed of authigenic francolite are also present in the Thin sections of the bone (Plate 1A–D) show details cancellous region. Some surfaces of the bones are densely from a fragment of the carapace. The cortical bone layers covered by microspheres (<1 lm; Plate 2B, C; Schmitz (Plate 1D) are separated into an inner and outer layer, and Ernst 1994).

EXPLANATION OF PLATE 2 Scanning electron microscope images of bone histology of Hispaniachelys prebetica n. gen et n. sp., RGCHSP-62-52. A, Filamentous structures on the walls of the cancellous bone (white arrow). B, Filaments (white arrow) coating the inner surface of the bone, composed of francolite. C, Both globular structures (around 10 lm, white arrow) and microspheres (<1 lm) from the internal surface of the carapacial bone. D, Large globular structures made up of small francolite crystals. E, Francolite crystals that have pseudomorphed the original positions of the collagen fibrils of the bone. F, Porous ⁄ vascular structure of the cancellous region of the bone. PLATE 2

A B

10.0 μm 20.0 μm

C D

20.0 μm 50.0μm

E F

20.0 μm 1.0 mm

SLATER et al., bone histology of Hispaniachelys prebetica 1410 PALAEONTOLOGY, VOLUME 54

A B C

D E F

TEXT-FIG. 10. Cartoon sequence showing possible stages in death and burial of the carcass of Hispaniachelys prebetica, RGCHSP- 62-52. A, following death, the carcass likely floated in the surface waters, but only for a relatively short time, as suggested by the completeness of the specimen. B, the carcass came to rest on the sea floor in calm current conditions. C, grazers colonized the carapace microenvironment, forming Pascichnia traces. D, after some time, the carapace was overturned, possibly by a large scavenger as the palaeocurrents were insufficient to move the carapace; this would have terminated any grazing activity on the carapace. E, the plastron collapsed into the body cavity, probably under sediment loading, while the carapace retained its integrity because of underlying sediment support. F, the exposed portion of the carapace protruding from the sediment was colonized by sponges as it provided an island of hard substrate among the poorly consolidated soft sediments; Entobia traces were left by sponges before final burial and diagenesis.

Taphonomic interpretation There are some fractures in the distal portions of the carapace, which suggests the action of larger scavengers or The specimen was probably overturned before burial, as that sediment compaction under loading caused the frac- shown by its original orientation when collected and the tures. These fractures are unlikely to have resulted from plastron fragments filling the carapacial bowl. This pre- reworking, as sedimentological data (Olo´riz et al. 2003; sumably explains the absence of borings and traces on the Reolid 2008) indicate low-energy conditions: the micro- plastron, which would have been buried and so sheltered facies is a fine-grained wackestone with peloids, and there from borers and grazers. The collapse of the plastron per- are no sedimentary structures indicating turbulence. Asso- haps resulted from early burial beneath loose sediment, ciated macroinvertebrates are intact and unfragmented, causing it to cave in to the internal cavities. This unusual including ammonoid, bivalve and brachiopod shells, burial position is also recorded in the Solothurn turtle which are articulated. The distal portions of the bones limestone (Late Jurassic, Kimmeridgian) of the Jura also lack signs of abrasion. The sedimentary setting was a Mountains, Switzerland (Meyer 1991; Billon-Bruyat 2005). softground at mid-shelf and a depth of c. 60–80 m (Olo´- The carapace is relatively intact, and the fragments are riz et al. 2006). The action of scavengers is cited as a not widely dispersed, although distal elements including further possible reason for carapace-down burial of turtles the limbs and head are missing, perhaps from scavenging in both modern and fossil death assemblages, in studies of more accessible parts. A convex-down position of a of turtle taphonomy by Corsini et al. (2006) and Corsini turtle carapace prevents or slows down disarticulation, and Chamberlain (2009). as shown in burial experiments using hawksbill turtles The carapace went through a series of colonization (Meyer 1991); in these studies, a carapace buried convex- events after death (Text-fig. 10). Bioerosion indicates ini- up was completely disarticulated within 10 days, whereas tial colonization of the exposed carapace primarily by a carapace buried convex-down was still almost intact grazers, Gnatichnus (A. Santos and E. Mayoral, pers. after 15 days. Previous taphonomic studies showed that comm. 2009), before the overturning of the carapace the skull, neck, tail and limbs of turtles become disarticu- (Corsini and Chamberlai 2009). Meyer (1991) noted that lated early, but also that the carapace usually becomes the costal plates of modern hawksbill turtle skeletons are disarticulated before the plastron (Bertini et al. 2006). often covered in grazing traces formed by sea urchins as SLATER ET AL.:NEWJURASSICTURTLEFROMSPAIN 1411 they remove algae and other organic material encrusting its abundant circular primary vascular canals in the inner the carapace, seen also in carapaces from Solothurn. In cortical layers, a feature characteristic of extant aquatic our specimen, borings along the right-lateral edge of the turtles (Scheyer and Sander 2007). The overall structure costals on the right side of the carapace where the margi- of the bone is more vascularized than that typical of ter- nals are disarticulated are interpreted as clionaid sponge restrial species (Scheyer and Sander 2007). encrustation marks, possibly Entobia based on the inter- Hispaniochelys prebetica exhibits a rather domed anterior laced morphology of the bored chambers. Other types of portion of the shell, which might be interpreted to suggest sponges (mainly Hexactinellida) are found in this section the individual was female. This suggestion follows Oertel as isolated clumps and as sponge-microbialite buildups (1924) and Bra¨m (1965), who argued that female P. solo- (Reolid 2010), so it is possible that the carapace acted as durensis had an arched or domed anterior portion of the a suitable firm ground for them, amidst the surrounding carapace. This gender assignment is presumably based on loosely consolidated sediment. The rest of the carapace is the need for females to house larger shoulder muscles and covered by a network of interlaced Gnatichnus borings girdles to excavate nests on the shore. Specimens of Plesi- produced by the grazing activity of regular echinoids ochelys described by Bra¨m (1965) are distorted to various while the carapace was resting in the sediment with the degrees, so the reality of this supposedly gender-specific colonization of clionaid sponges and disarticulated section character is dubious (Gaffney 1975b), and nothing can be exposed at the surface (Plate 1E, F, G). The possibility of said about the gender of our specimen. colonization by some trace-makers during postmortem The thick, heavily ossified carapace of H. prebetica transport and floating, however, should not be dis- would have been useful in a coastal marine habitat where counted. No epibionts were found encrusting the speci- manoeuvrability and protection are more important men, even though barnacles and algae are common than weight reduction and energy conservation. Ocean encrusters in recent turtles. Indeed, many barnacle species wandering turtles today reduce drag by having a shallow are found exclusively attached to turtle shells today, streamlined shell. However, they also typically have a dor- although these would be removed when the turtle died soventrally deep-set anterior carapace, as in highly aquatic and the dermal scutes to which they were attached rotted freshwater turtles (Depecker et al. 2006), but more mas- away (Pfaller et al. 2006, 2008). sive and typically dorsoventrally longer. This creates an The filaments, globular structures and microspheres anterior dome that is intermediately arched between that observed under the SEM (Plate 2C) are related to micro- of highly aquatic freshwater turtles and the extremely bial (fungal or bacterial) activity associated with decay of arched carapaces of terrestrial species. the organic matter. Similar microspheroids were recorded by Elorza et al. (1999) in Upper Cretaceous turtle bone Acknowledgements. We thank Simon Braddy (University of Bris- fragments from the Lan˜o Quarry in the Basque-Cantabri- tol) for providing advice and literature on trace fossils, and per- an region of northern Iberia. Schmitz and Ernst (1994) sonal comments by Ana Santos and Eduardo Mayoral proposed that such microspheroids, which also occur in (Universidad de Huelva) about grazing traces on the turtle cara- the Eocene Messel Oilshale Pit in Germany, are by-prod- pace. We are also enormously grateful to Walter Joyce, Juliana Sterli and Jean-Paul Billon-Bruyat for their advice on turtle tax- ucts of bacterial action, perhaps associated with the decay onomy and morphology, informally and formally through the of organic tissues in the cancellous layer of the bone. review process. This study is part of a research project by BJS, These microspheroids and crystal bundles suggest that the carried out in partial fulfilment of the MSc in Palaeobiology at carapace may have acted as an enclosed microenviron- the University of Bristol. ment favourable to the development of decay-induced au- thigenic mineralization, and therefore facilitating its own Editor. Marcello Ruta preservation (Briggs 2003).

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