New Highlights About the Enigmatic Marine

[Palaeontology, Vol. 56, Part 3, 2013, pp. 647–661]

NEW HIGHLIGHTS ABOUT THE ENIGMATIC MARINE SNAKE PALAEOPHIS MAGHREBIANUS (PALAEOPHIIDAE; PALAEOPHIINAE) FROM THE YPRESIAN (LOWER EOCENE) PHOSPHATES OF MOROCCO by ALEXANDRA HOUSSAYE1,2*, JEAN-CLAUDE RAGE1, NATHALIE BARDET1, PEGGY VINCENT3, MBAREK AMAGHZAZ4 and SAID MESLOUH5 1De´partement Histoire de la Terre, UMR 7207 du CNRS, Museúm National d’Histoire Naturelle, 57 rue Cuvier CP 38, 75005 Paris, France; e-mails: [email protected], [email protected], [email protected] 2Steinmann Institut fu¨r Geologie, Palaöntologie und Mineralogie, Universita¨t Bonn, Nussallee 8, 53115 Bonn, Germany; e-mail: [email protected] 3Staatliches Museum fu¨r Naturkunde Rosenstein 1, D-70191 Stuttgart, Germany; e-mail: [email protected] 4Office Che´rifien des Phosphates, Centre Minier de Khouribga, Khouribga, Morocco; e-mail: [email protected] 5Ministe`re de l’Energie, des Mines, de l’Eau et de l’Environnement, Rabat, Morocco; e-mail: [email protected] *Corresponding author.

Typescript received 23 March 2012; accepted in revised form 4 September 2012

Abstract: Palaeophis maghrebianus belongs to the Palaeo- analysis of some vertebrae illustrating diverse positions along phiinae (Palaeophiidae). This snake subfamily is relatively the vertebral column reveals the presence of osteosclerosis, poorly known, and it is mainly represented by disarticulated especially in the anterior and mid-precloacal regions. The vertebrae and ribs and by a few vertebral segments. Its intracol- occurrence of this osseous specialization implies a role in umnar variability remains also poorly understood. The discovery buoyancy and body trim control in this taxon, which is consid- of new isolated vertebrae and vertebral segments of Palaeophis ered a shallow marine dweller based on its anatomical features maghrebianus in the Ypresian (Lower Eocene) Phosphates of and geological data. Palaeophis maghrebianus also displays a Morocco enables us to provide a more detailed diagnosis of dense vascular network suggesting a growth speed, and thus a this species and to describe its intracolumnar variability. metabolic rate, much higher than in the biggest extant snakes. Moreover, the new material reveals that this species could reach gigantic size being, with Palaeophis colossaeus, one of the Key words: snakes, Palaeophiidae, palaeobiology, palaeoe- two longer palaeophiids. The microanatomical and histological cology, gigantism, histology.

Palaeophiinae Lydekker, 1888 (Squamata, Ophidia) 2003). Moreover, the morphological variations along the lived from the Maastrichtian to the Late Eocene (Rage vertebral column remain rather unknown, so that infer- et al. 2003). This subfamily, which includes the two gen- ring the original position of vertebrae along the vertebral era Palaeophis Owen, 1841 (Maastrichtian–Eocene) and column is still extremely difficult. Palaeophiinae includes Pterosphenus Lucas, 1899 (Eocene) is, with the subfamily a wide range of species sizes. The biggest species so far is Archaeophiinae Janensch, 1906, part of the family Palaeo- considered to be Palaeophis colossaeus Rage, 1983a, esti- phiidae Lydekker, 1888. Palaeophiidae is one of the mated to be about 9 m long (Rage 1983b), whereas the only five extinct families (with Anomalophiidae Auffen- smallest species P. casei Holman, 1982 was apparently berg, 1959; Nigerophiidae Rage, 1975; Pachyophiidae about 1–1.3 m long (Parmley & Reed 2003). This subfam- Nopcsa, 1923; and Russellophiidae Rage, 1978) among ily includes various species illustrating three ecological Ophidia that adapted to various freshwater and marine grades. The ‘primitive’ Palaeophis grade (sensu Rage et al. environments. 2003) comprises species with vertebrae only slightly modi- Palaeophiine snakes are in fact relatively poorly known; fied for an aquatic life, whereas the ‘advanced’ Palaeophis the material available consists only of disarticulated verte- grade (sensu Rage et al. 2003) includes species with vertebrae and ribs and of a few vertebral segments (Rage et al. brae clearly modified for an aquatic life (see Rage et al.

ª The Palaeontological Association doi: 10.1111/pala.12008 647 648 PALAEONTOLOGY, VOLUME 56

2003 for more details). The third grade is comprised only GEOLOGICAL SETTING of Pterosphenus, whose vertebrae are highly modified for an aquatic life. The Phosphates of Morocco, exploited as an economical The species P. maghrebianus Arambourg, 1952 is one of resource since the 1920s (Office Cherifien des Phosphates the better documented species, but it has not been revised 1989), are part of the ‘Mediterranean Tethyan phospho- since its original description by Arambourg (1952). It is genic Province’, a large belt of sedimentary deposits only known from the Ypresian Phosphates of Morocco. It located around palaeolatitude 20S that currently crops is the only squamate discovered in the Ypresian of out widely from the Middle East up to the Pernambuco Moroccan Phosphates so far (Bardet et al. 2010). This Province of Brazil, via North and West Africa (Lucas and large snake is considered aquatic based on its vertebral Pre´voˆt-Lucas 1996). In Morocco, these phosphates crop morphology (Bardet et al. 2010). However, it belongs to out into two main exploited, large areas known as the the ‘primitive’ Palaeophis grade (cf. Rage et al. 2003). Oulad Abdoun and the Ganntour basins (Fig. 1A). Strati- The discovery of new isolated vertebrae and three artic- graphically, the phosphatic strata of Morocco range in age ulated vertebral segments, which correspond to the lon- from the Late Cretaceous (Maastrichtian) to the Middle gest vertebral segments known for a palaeophiine, enabled Eocene (basal Lutetian), spanning the longest time interval us to obtain new anatomical data about this species. of all Tethyan phosphates (Lucas & Pre´voˆt-Lucas 1996). Moreover, the microanatomical and histological features The Lower Eocene phosphatic series in the Oulad of some vertebrae were investigated to obtain new infor- Abdoun basin is the most developed compared to the Ma- mation about the biology of this taxon and to discuss its astrichtian (Bed IIII) and Danian–Thanetian (Bed II) beds. palaeoecology. The Ypresian levels include several levels and horizons,

FIG. 1. Geographical and stratigraphical occurrences of Palaeophis maghrebianus Arambourg, 1952 in Morocco. A, location of the main phosphatic basins. B, details of the Oulad Abdoun basin. C, synthetic stratigraphical column of the phosphatic series in the Daoui zone, NE part of the Oulad Abdoun basin, where most specimens of P. maghrebianus have been found in the Intercalary beds II ⁄ I to bed 0 (Ypresian). (A–B) Modified from Bardet et al. (2010) and (C) from Sole et al. (2009). HOUSSAYE ET AL.:NEWHIGHLIGHTSABOUTPALAEOPHIS MAGHREBIANUS 649 which are, from bottom to top, Bed I, 0¢ and 0, and troughs MATERIALS AND METHODS B and A (Fig. 1C). All of these more or less soft phosphatic levels are separated by hard calcareous phosphatic beds Materials. The material consists of 163 isolated vertebrae, called Intercalary beds. The Lower Eocene phosphatic series including the ones originally described by Arambourg in the Ganntour basin is less expansive than the Maastrich- (MNHN APH 1–2, MNHN APH 4–5 (being figured) tian series, contrary to what occurs in the Oulad Abdoun and MNHN APH3, 6–16) as well as newly collected basin. This series begins with a plastic clay level that corre- vertebrae (OCP DEK ⁄ GE 500-535, OCP DEK ⁄ GE 537- sponds to a reference level in the Ganntour basin, followed 646), and includes three articulated portions of the verte- by 11-m thick unnamed bed, then troughs B to F. bral column (sometimes with ribs): OCP DEK ⁄ GE 95, One of the main characteristics of these Phosphates is OCP DEK ⁄ GE 418 and OCP DEK ⁄ GE 536. their extreme richness in fossil vertebrate remains of latest Cretaceous–Palaeogene age, known since the pioneer Methods. To complete the anatomical observations, vari- works of Arambourg (1952). Since 1997, an active ous measurements (Rage 2001; Houssaye et al. 2011) were French–Moroccan scientific collaboration (Acknowledge- taken for the vertebrae when the degree of preservation ments) has permitted new palaeontological field cam- was sufficient: WPr, width across the articular facets of paigns, which has resulted in an abundant collection from the prezygapophyses; WPa, maximal width across the both Maastrichtian and Palaeogene deposits of new verte- articular facets of the paradiapophyses; WPt, width across brate remains (including articulated skeletons) belonging the articular facets of the postzygapophyses; WIC, width to selachians (Noubhani and Cappetta 1997), bony fishes of interzygapophyseal constriction; CL, centrum length; (Cavin et al. 2000), marine and continental sauropsids CTW, cotyle width. (see Bardet et al. 2010 for bibliographical details), as well Five vertebrae (OCP DEK-GE 642–646) illustrating var- as continental mammals (Gheerbrant et al. 2003). These ious positions along the vertebral column (cf. Table 1) new discoveries significantly improve our knowledge of were used for histological sections. They were sectioned these vertebrate assemblages, which were either previously using standard techniques (Houssaye et al. 2008) along unknown or represented only by fragmentary or isolated their mid-sagittal and neutral transverse (sensu Buffreńil remains (Arambourg 1952). et al. 2008) planes. The sections were examined micro- The specimens, on which the original description of scopically at low- and medium-power magnifications Palaeophis maghrebianus is based, have been reported by (25–100·) in natural and polarized transmitted light. Arambourg (1952, pp. 291–294, pl. 41, figs 8–12) as com- They were drawn to scale with a camera lucida, and two ing from the Ypresian levels of both the Oulad Abdoun measurements were taken following Houssaye et al. and Ganntour basins. However, this last mention from the (2008): (1) the global compactness in transverse section Ganntour appears unclear. Although Arambourg (1952, p. (Cts), calculated as the total sectional area minus the area 294) stated ‘Au Maroc, les restes de P. maghrebianus ap- occupied by cavities and the neural canal multiplied by partiennent au niveau ypre´sien des Ouled Abdoun et des 100 and divided by the total area minus the area occupied Ganntour’ (‘In Morocco, remains of P. maghrebianus by the neural canal, and (2) the global compactness of belong to the Ypresian level of the Oulad Abdoun and the centrum in longitudinal section (Cls), calculated as Ganntour’; translation A), he does not mention vertebrae the total area of the centrum minus the area occupied by from the Ganntour in his description. From the Oulad cavities multiplied by 100 and divided by the total area of Abdoun basin, two localities were mentioned by Aram- the centrum. bourg: Djemaıä (locus typicus), east of Khouribga and Bou Jniba, north-east of El Borouj (Arambourg 1952; Fig. 1B). In fact, part of the material he described was dis- TABLE 1. Compactness indices obtained for the five vertebrae. covered in other additional localities from the Ouled Ab- doun (e.g. Oued Zem and Oued Oussen), but they are not Collection number Supposed position Cls Cts specified for each vertebra. The vertebra coming from Bou OCP DEK ⁄ GE 646 Anterior 82 89 Jniba and figured by Arambourg (1952, pl. 41, fig. 12) is OCP DEK ⁄ GE 643 Anterior 91 83* considered lost. The specimens are said to come from Bed OCP DEK ⁄ GE 645 Middle (anterior) 85 92 0, but no precise details on location are given. No details OCP DEK ⁄ GE 644 Middle 92 90 were provided for the Ypresian levels of the Ganntour OCP DEK ⁄ GE 642 Posterior 82 79 basin. The new specimens all come from the Grand Daoui Vertebrae histologically analysed, with their supposed position area, near the city of Oued Zem, north-eastern part of the along the vertebral column. Cls, global compactness of the cen- Oulad Abdoun basin (Fig. 1B). Most come from the Bed I trum in longitudinal section; Cts, global vertebral compactness and some from the Intercalary Bed II ⁄ I, that is, from the in transverse section. *Minimal value as part of the – presum- lower part of the Ypresian. ably – very compact neural spine is missing. 650 PALAEONTOLOGY, VOLUME 56

Institutional abbreviations. MNHN, Museúm National d’Histoire single large median foramen between the two zygantral Naturelle (Paris, France); OCP, Office Che´rifien des Phosphates fossae; it differs from P. virginianus by the presence of an (Khouribga, Morocco). additional hypapophysis in anterior vertebrae and by the less depressed neural arch; from P. zhylan by its clearly narrower, less markedly depressed cotyles and condyles; SYSTEMATIC PALAEONTOLOGY from P. vastaniensis in vertebrae being less depressed; from P. africanus in the absence of very sharp interzygapo- Family PALAEOPHIIDAE Lydekker, 1888 physeal ridges (sensu Rage and Neraudeau 2004, text-fig. 2 Subfamily PALAEOPHIINAE Lydekker, 1888 inside) and of a neural spine encroaching upon the zy- Genus PALAEOPHIS Owen, 1841 gosphene; from P. casei in that its neural spine is not restricted to the posterior one-third of the vertebra, in its Palaeophis maghrebianus Arambourg, 1952 longer hypapophysis on posterior precloacal vertebrae and Figures 2–9 in its pterapophyses well shaped on all the precloacal vertebrae. In P. maghrebianus, the zygosphene is narrower Original diagnosis. Large Palaeophis with short and low than the cotyle but larger than the neural canal; none of vertebrae that lack a median ridge and lateral grooves on the vertebrae shows subcentral grooves or paracotylar the ventral surface, with reduced and obtuse hypapophy- notches (sensu LaDuke 1991, fig. 1 inside), and zygantral ses, with low and wide zygosphenes, zygantra laterally foramina are always present in each zygantral fossa. exceeding the edges of the articular condyle, pterapophyses projecting only slightly above the level of the zygosph- Holotype. Trunk vertebra MNHN APH 5 (Arambourg 1952). enes (translated from Arambourg 1952). Referred specimens. MNHN APH 1–4, APH 6–16 (Arambourg Revised diagnosis. Snake referred to the Palaeophiidae on 1952); OCP DEK/GE 500-535, OCP DEK ⁄ GE 537–646 (new the basis of the following assemblage of characters: pte- collected isolated vertebrae); OCP DEK ⁄ GE 95, OCP DEK ⁄ GE rapophyses present, axis of the cotyle–condyle system hor- 418 and OCP DEK ⁄ GE 536 (new collected articulated vertebral izontal, position of the paradiapophyses relatively low and segments). hypapophyses not restricted to cervical vertebrae. Assigned to the Palaeophiinae on account of the presence of at least Type locality and horizon. Oulad Abdoun basin, Morocco, Ypre- one hypapophysis on all precloacal, the presence of a sec- sian (Eocene). ond small hypapophysis under the cotyle in anterior ver- Referred specimens localities and horizons. MNHN APH 1–4, tebrae, the presence of pterapophyses through the entire APH 6–16, Oulad Abdoun basin, Morocco, Ypresian. OCP precloacal series and the marked projection of the paradi- DEK ⁄ GE 95, 418, 500–646, Grand Daoui, Oulad Abdoun basin. apophyses below the ventral border of the centrum.

Comparison. This palaeophiine snake differs from Ptero- DESCRIPTION sphenus and is, therefore, referred to Palaeophis, in the neural spine rising behind (and not on) the roof of the zy- Morphology gosphene, in the zygosphene being not clearly convex dorsally, in the cotyle being truncated dorsally and in the Isolated vertebrae (MNHN APH 1–16 and OCP DEK ⁄ GE 500– prezygapophyses lying clearly above the ﬂoor of the neural 535, OCP DEK ⁄ GE 537–646). Only precloacal vertebrae are canal. It differs from Palaeophis species of the ‘advanced’ known (as shown by the absence of lymphapophyses, pleurap- group (sensu Rage et al. 2003: P. casei Holman, 1982; ophyses and haemapophyses). Based on the morphological fea- P. ferganicus Averianov, 1997; P. littoralis Cope, 1868; tures of these vertebrae and on our knowledge of the P. toliapicus Owen, 1841; P. typhaeus Owen, 1850; P. gran- intracolumnar variability within snakes, three main vertebral dis Marsh, 1869; P. tamdy Averianov, 1997; P. nessovi regions could be determined for the precloacal portion of the Averianov, 1997; and P. udovichenkoi Averianov, 1997) in vertebral column, and their anteroposterior polarity assumed: (1) retaining at least some vertebrae with a rather marked lat- anteriormost region: vertebrae display two well-deﬁned hypapophyses (one located anteriorly and the other posteriorly) and a eral projection of the zygapophyses. Within the ‘primitive’ round cotyle (Fig. 2A–B); (2) mid-region: the anterior hypap- group of Palaeophis species, P. maghrebianus differs from ophysis is reduced to a small bulge, and the cotyle is slightly P. colossaeus in the absence of parazygosphenial foramina, ovoid (Fig. 2I–J); (3) posterior region: only the posterior hyp- in the stronger lateral compression of its vertebrae, in a apohysis is present, and the cotyle is ovoid (Fig. 2K–L). Transi- zygosphene not larger than the cotyle, in the relatively fee- tion between these regions is naturally progressive and not ble inclination of the prezygapophyses, as well as in the marked by any drastic change at a peculiar position. Despite constant presence of zygantral foramina and never of a these differences, it can also be noted that the width of the verte- HOUSSAYE ET AL.:NEWHIGHLIGHTSABOUTPALAEOPHIS MAGHREBIANUS 651

ABCD

E F G H

IJKL

MN OP

FIG. 2. Palaeophis maghrebianus. Ypresian. Grand Daoui area, Oulad Abdoun basin, Morocco. A–C, anterior precloacal vertebra OCP DEK ⁄ GE 646. D, anterior precloacal vertebra OCP DEK ⁄ GE 503. E, mid-precloacal vertebra OCP DEK ⁄ GE 592. F–G, mid-precloacal vertebra OCP DEK ⁄ GE 534. H, mid-precloacal vertebra OCP DEK ⁄ GE 532. I–J, mid-precloacal vertebra OCP DEK ⁄ GE 544. K, posterior precloacal vertebra OCP DEK ⁄ GE 554. L–M, posterior precloacal vertebra OCP DEK ⁄ GE 517. N–O, posterior precloacal vertebra OCP DEK ⁄ GE 642. P, posterior precloacal vertebra OCP DEK ⁄ GE 525. In A, E, F, J, K, M – anterior; B, H, I, L – ventral; C–P – dorsal; D, O – left lateral; G – right lateral; and N – posterior views. Scale bars represent 5 mm. NTP, neutral transverse plane; MSP, mid-sagital plane. brae proportionally to their length, as a result of the lateral pro- In anterior view, the prezygapophyses and paradiapophyses do jection of the zygapophyses, increases posteriorly (Fig. 2C, P). not strongly project laterally. The degree of lateral projection Despite these intracolumnar variations, all vertebrae display vari- does vary and is, however, more important in posterior vertebrae. ous common morphological features. All centra are procoelous. The maximum width is observed just under the prezygapophyseal 652 PALAEONTOLOGY, VOLUME 56 facets, which are ventrally prolonged by an anterolateral ridge directed, and the posterior hypapophysis, which is not strongly forming a lateral salient; the ridge extends from the anterolateral posteriorly located, is posteroventrally directed (Fig. 2D, O). tip of the prezygapophyses (just beneath the articular facet) to The anterior hypapophysis is relatively small, whereas the pos- the dorsal border of the paradiapophysis (Fig. 2A, F, K). There terior one can be comparatively deep, almost reaching the are no prezygapophyseal processes. Thanks to the presence of few height of the centrum. It is not slender but rather thick at its vertebrae with well preserved paradiapophyses (that are generally base (Fig. 2B, I). Both hypapophyses appear as parts of the cen- broken), it can be stated that the paradiapophyses always project trum, any trace of suture being absent. Paradiapophyses pro- beyond the ventral border of the cotyle, even in the posterior- trude anterior to the cotyle (Fig. 2G). They bent at their middle most vertebrae (Fig. 2A, F, M). Despite this ventral projection, so that, from dorsally subvertical, they become ventrally paracotylar notches are absent in all vertebrae. Prezygapophyseal inclined, at about 45 degrees to the horizontal (Fig. 2G). The facets are only slightly inclined on the horizontal (maximum articular surface is rather large and not subdivided into para- inclination at about 25 degrees; Fig. 2A, F), especially in the mid- and diapophyseal areas. No neural spine is entirely preserved, region, where they are subhorizontal (Fig. 2J). They are located which suggests that they were thin and lightly built. Their bro- clearly above the ventral base of the neural canal. The zygosphene ken bases seem to suggest that they were relatively high and that is very thick. It is dorsally generally convex or flat (Fig. 2A, F, J, they rose subvertically. M). However, it must be specified that some zygosphenes, slightly In ventral view, the centrum appears rather cylindrical; its lat- concave in anterior view, have been observed without any appar- eral borders are poorly delimited, clear subcentral ridges being ent link with the position of the vertebra along the vertebral col- absent (Fig. 2B). However, in vertebrae from the anterior region umn (Fig. 2F, K). The neural canal is subtriangular in shape (and perhaps also in anterior vertebrae from the mid-region), (with a kind of trilobate aspect because of the two ‘ridges’ run- faint ridges run from the paradiapophyses to the condyle, as ning on the lateral walls) and rather small, being much smaller usual subcentral ridges, but in the posterior half of the centrum, than the cotyle (Fig. 2A, F, J). The zygosphene is narrower than they occupy a rather high position, the centrum being markedly the cotyle but larger than the neural canal (Fig. 2E, F). The cotyle protruding ventral to them. In such vertebrae, the centrum is subcircular in the anteriormost region and more ovoid posteri- appears constricted at mid-length (Fig. 2H, I). A slight keel con- orly; its dorsal part is only very slightly truncated at the base of nects the two hypapophyses in the anterior vertebrae (Fig. 2B). the neural canal (Fig. 2E). There is no precondylar constriction, but the condyle is clearly In dorsal view, as a result of the weak lateral projection of the distinct from the centrum. It should be noted that none of the zygapophyses, the interzygapophyseal constriction is shallow; its vertebrae shows subcentral grooves. maximum depth is located at about the mid-length of the verte- In posterior view, the height of the pterapophyses varies bra (Fig. 2C, P). The lateral projection of the zygapophyses is between specimens, being either smaller or higher than the con- weaker in the anteriormost vertebrae; thus, they appear more dyle. The zygantrum projects beyond the lateral borders of the elongated (Fig. 2C, P). However, their width at the interzygapo- condyle. physeal constriction is, proportionally to the centrum length, Various foramina (with no fixed numbers and positions) are similar to that of more posterior vertebrae, which indicates that observable independently of the original position of the vertebrae this effect is only due to the degree of projection of the zygap- along the vertebral column: lateral, subcentral, paracotylar, ophyses. The prezygapophyseal facets are elongated, especially in zygantral. However, parazygosphenal foramina are never observed. the anteriormost vertebrae, and anterolaterally directed (Fig. 2C, P). The posterior border of the neural arch is indented by a rela- OCP DEK ⁄ GE 418. This specimen corresponds to 24 articulated tively shallow, V-shaped median notch. The anterior border of precloacal vertebrae (mean CL = 2.33 cm) exposed in ventral the zygosphene is slightly concave but does not form a notch view (Fig. 3). Two rib fragments are preserved, among which (Fig. 2C, P). The neural spine extends from behind the posterior one in connection to a vertebra. As only one hypapophysis is border of the zygosphene to the posterior edge of the neural observable under the condyle of each vertebra, the vertebrae are arch (Fig. 2C, P). Pterapophyses do not project laterally as considered posterior precloacal ones. much as the zygapophyses (Fig. 2N, P) but more than the Vertebrae are very similar to the holotype (MNHN APH 5; paradiapophyses. Rage 1984, fig. 20Av). The vertebrae appear relatively wide In lateral view, the axis of the cotyle–condyle system is hori- (mean WIC ⁄ CL = 0.66; WPr ⁄ CL = 1.61; WPa ⁄ CL = 1.43), zontal. Where present, the anterior hypapophysis erects just at which indicates, as stated by Rage (1984), that lateral compres- the ventral base of the cotyle (Fig. 2D). It is ventroanteriorly sion is limited. The width across the prezygapophyses is smaller

FIG. 3. Palaeophis maghrebianus. Ypresian. Grand Daoui area, Oulad Abdoun basin, Morocco. OCP DEK ⁄ GE 418. Whole specimen. Scale bar represents 5 mm. HOUSSAYE ET AL.:NEWHIGHLIGHTSABOUTPALAEOPHIS MAGHREBIANUS 653

FIG. 4. Palaeophis maghrebianus. Ypresian. Grand Daoui area, Oulad Abdoun basin, Morocco. OCP DEK ⁄ GE 418. A, ventral view of a vertebra. B, right lateral view of a vertebra. Hy, hypapophysis; NS, neural spine; Pa, paradiapophysis; Pt, pterapophysis. Scale bar represents 5 mm. than that across the postzygapophyses. Prezygapophyses project that of the centrum. It appears from the lateral observation of much beyond the paradiapophyses (mean WPa ⁄ WPr = 0.89) two vertebrae for which the neural spine could be excavated that and anteriorly beyond the anterior border of the cotyle. The the latter is higher than the centrum (Fig. 4B). The neural spine condyle is large and depressed (Fig. 4A). The cotyle–condyle sys- does not rise from the zygosphenal roof. It is relatively short an- tem appears horizontally oriented. No precondylar constriction teroposteriorly and horizontal at the top. It rises subvertically, is observable. The subcentral ridges are not well deﬁned. The but its posterior border is concave (Fig. 4B). Prezygapophyses hypapophysis is located posteriorly, oriented posteroventrally are inclined at about 25 degrees on the horizontal. Paradiapo- and ends as a relatively thin lamina, although it is massive at its physeal facets are well inclined, at about 40 degrees on the hori- base. Two subcentral foramina appear to be always present zontal, their dorsal part bending posteriorly (Fig. 4B). (Fig. 4A). The removing of sediment at some peculiar places enabled us OCP DEK ⁄ GE 95. This specimen consists of three portions of to locally observe the lateral view of some vertebrae. The ventral articulated vertebrae with some associated ribs preserved on the border of the paradiapophyses is more ventrally located than same slab (Fig. 5). The portion A encloses one isolated and three

FIG. 5. Palaeophis maghrebianus. Ypresian. Grand Daoui area, Oulad Abdoun basin, Morocco. OCP DEK ⁄ GE 95. Whole specimen with the sections A–C discussed separately in the text delimited. Scale bar represents 5 mm.

B A

C 654 PALAEONTOLOGY, VOLUME 56

A B

FIG. 6. Palaeophis maghrebianus. Ypresian. Grand Daoui area, Oulad Abdoun basin, Morocco. OCP DEK ⁄ GE 95 Section A. A, whole section A in lateral view; arrows point to the hypapophyses. B, one vertebra in anterior view. Scale bars represent 5 mm. articulated vertebrae preserved in lateral view and some rib frag- series. Unfortunately, it cannot be stated which portion is more ments (Fig. 5A). The observation of two hypapophyses on every anterior. vertebra of this portion, one located anteriorly and the other posteriorly, as well as the rounded shape of the cotyle of the first OCP DEK ⁄ GE 536. This specimen corresponds to 44 articulated articulated vertebra, show that these vertebrae correspond to vertebrae preserved in lateral view and some associated ribs. In anterior precloacal vertebrae. It can be observed on the second this specimen, the vertebrae are much bigger than all the ones articulated vertebra that the neural spine is high (much higher described above. The length of the centrum (CL) varies between than the centrum), relatively thin and posteriorly inclined. It 2.7 and 3.3 cm. There is only one hypapophysis in each vertebra rises posteriorly to the roof of the zygosphene (Fig. 6A). The (Fig. 7). The neural spine is high, subrectangular in shape, rela- neural canal is subtriangular. The roof of the zygosphene is very tively short anteroposteriorly and posteriorly inclined. We can thick and rather flat in anterior view (Fig. 6B). It is slightly concave in dorsal view. The zygapophyses appear less inclined than in OCP DEK ⁄ GE 418 (Fig. 6A). The second portion (B) corresponds to 33 articulated vertebrae (Fig. 5B). Twenty are preserved in dorsal view with associated ribs. Most neural spines are broken, but some that are only partly broken suggest high neural spines slightly inclined posteriorly and with a subrectangular shape. The neural arch forms posteriorly a deep median notch. The preservation of one sub- complete rib in lateral view shows that it was slightly curved proximally and becoming slender distally; unfortunately, it is not possible to state whether a tuberculiform process is present. The shallow furrow extending proximodistally in its middle indicates that the rib displayed a medullary cavity and thus that it was not osteosclerotic. The thirteen other vertebrae of portion B, which are preserved in lateral view, show features similar to those from the portion A. Portion C consists of four vertebrae (Fig. 5C); one preserved in anterior view and the others in lateral view. They also display two hypapophyses each (Fig. 5C). The pterapophyses are clearly higher than the centrum. The neural spines are well preserved, and it can clearly be observed that they are high and subrectangular in shape. They are only slightly posteriorly inclined. This FIG. 7. Palaeophis maghrebianus. Ypresian. Grand Daoui area, shows that some variation affects the degree of inclination of Oulad Abdoun basin, Morocco. OCP DEK ⁄ GE 536. Two the neural spines within the anteriormost part of the precloacal vertebrae in lateral view. Scale bar represents 5 mm. HOUSSAYE ET AL.:NEWHIGHLIGHTSABOUTPALAEOPHIS MAGHREBIANUS 655 clearly see that the paradiapophyses project more ventrally than about 76 per cent. They also clearly show a variation along the the ventral border of the centrum. The prezygapophyses are vertebral column as OCP DEK ⁄ GE 642 clearly shows a lower inclined at about 25–30 degrees to the horizontal (Fig. 7). compactness (cf. Table 1). Important secondary deposits of lamellar bone are observable in the intertrabecular spaces of the endosteo-enchondral terri- Microanatomical and histological features tory. As a consequence, the intertrabecular spaces are much reduced (sometimes even completely filled), which explains the All vertebrae analysed (cf. Table 1) display relatively similar mi- bone’s high compactness. A dense network of radially oriented croanatomical and histological features, despite some relative simple vascular canals, presenting some anastomoses, is observed variability (see below). In longitudinal sections, primary perio- in P. maghrebianus vertebral cortex (Fig. 10A). steal bone is highly vascularized (Fig. 8A). One big cavity occu- pies the core of the centrum, whereas the cortex appears relatively thick as a result of remodelling inhibition (as com- DISCUSSION pared to what is observed in extant snakes; Houssaye et al. 2010). Intertrabecular spaces in the endosteo-enchondral territory are rather small. In OCP DEK ⁄ GE 642, cavities are much Taxonomic and evolutive aspects more numerous and smaller (Fig. 8B). In transverse sections, remodelling is mainly restricted to the The pterapophyses, the horizontal axis of the cotyle–con- centrum and notably to its core (Fig. 9A). Only OCP DEK ⁄ GE dyle system, the relatively low position of the paradiap- 642 (the posteriormost vertebra from this sample) displays some ophyses and the fact that hypapophyses are not restricted remodelling in the neural arch (Fig. 9B) and both OCP DEK ⁄ GE to cervicals make an assemblage of characters typical of 642 and OCP DEK ⁄ GE 644 (the two posteriormost vertebrae Palaeophiidae (Rage 1984). The presence of at least one from this sample) in the neural spine. A thick layer of compact hypapophysis on all precloacal vertebrae (whereas in Ar- and highly vascularized primary periosteal bone surrounds the chaeophiinae posterior precloacal vertebrae only bear a periphery of the vertebrae (Fig. 9A). Remodelling appears lim- prominent haemal keel) and of a second small one under ited, and compactness is relatively high. Bone compactness indices show that vertebral compactness is the cotyle in anterior vertebrae, the presence of pterapoph- high in this taxon. Cls varies between 82 and 92 per cent, yses along the entire precloacal series and the marked pro- whereas its mean value in modern snakes is about 71 per cent jection of the paradiapophyses below the ventral border of (Houssaye et al. 2010), and Cts varies between more than 79 the centrum (contrary to what is observed in Archaeophii- and 92 per cent, whereas its mean value in modern snakes is nae) indicate that this taxon belongs to the Palaeophiinae

FIG. 8. Palaeophis maghrebianus. Ypresian. Grand Daoui area, Oulad Abdoun basin, Morocco. Longitudinal sections in natural light (NL). A, OCP DEK ⁄ GE 646. Scale bar represents 2 mm. B, OCP DEK ⁄ GE 642. Scale bar represents 4 mm. 656 PALAEONTOLOGY, VOLUME 56

(Rage 1984). This is in agreement with the thick zygosphene, the relatively reduced size of the neural canal, the rather large size of the cotyle and condyle, the horizontal- ity of the cotyle–condyle axis (which is, in Ophidians, only found in palaeophiids and nigerophiids; JCR, pers. obs.), the peculiar morphology of the prezygapophyses, which form an anterolateral ridge (a more or less similar morphology occurs in the Nigerophiidae, Russellophiidae and Anomalophiidae) and the fact that the zygapophyseal articular facets are rather narrow and anteriorly directed. The neural spine rising behind (and not on) the roof of the zygosphene, the zygosphene only slightly dorsally concave, the horizontally truncated (though slightly) dorsal part of the cotyle and the prezygapophyses laying clearly above the floor of the neural canal (and not at the same level) show that this taxon belongs to Palaeophis and not to Pterosphenus, which also displays a stronger lateral compression, paradiapophyses located lower on the centrum and higher pterapophyses (Rage and Wouters 1979; Rage 1983b, 1984; Rage et al. 2003). Rage (1984) and Rage et al. (2003) defined two ecological grades within the Palaeophis species. These groups have no systematic value. They distinguish between species of the ‘primitive’ group (see below) that do retain at least some vertebrae with a rather marked lateral projection of the zygapophyses and which thus appear relatively wide and therefore only slightly modified for an aquatic life, whereas species from the ‘advanced’ group (P. casei, P. ferganicus, P. littoralis, P. toliapicus, P. typhaeus, P. grandis, P. tamdy, P. nessovi and P. udovichenkoi) never have such AB vertebrae. Such vertebrae are known in P. maghrebianus. The new material shows that such vertebrae are from the FIG. 9. Palaeophis maghrebianus. Ypresian. Grand Daoui area, posterior part of the precloacal region (contrary to what is Oulad Abdoun basin, Morocco. Half transverse sections in NL. observed in living marine snakes in which posterior verte- A, OCP DEK ⁄ GE 646. Scale bar represents 2 mm; B, OCP DEK ⁄ GE 642. Scale bar represents 5.2 mm. brae are usually the most modified, that is, laterally flattened). However, anterior vertebrae of this taxon are

FIG. 10. Comparison between the degrees of vascularization in the vertebral cortex between A, Palaeophis maghrebianus. Ypresian. Grand Daoui area, Oulad Abdoun basin, Morocco. OCP DEK ⁄ GE 646. B, Eunectes murinus MNHN AC 1893 197. Scale bars represent 500 lm. HOUSSAYE ET AL.:NEWHIGHLIGHTSABOUTPALAEOPHIS MAGHREBIANUS 657 rather similar to vertebrae from the ‘advanced’ ecological quite distinct species whose neural spine is restricted to grade. This causes difficulty in distinguishing between the the posterior one-third of the vertebra, whose hypapophy- different species of Palaeophis. Although rather limited, sis is very short on posterior precloacal vertebrae and the intracolumnar variability must be taken into consider- whose pterapophyses are hardly visible on anterior preclo- ation. The species P. typhaeus and P. toliapicus that belong acal vertebrae and seemingly absent on the others (Hol- to the ‘advanced’ grade are well known from various man 1982); it, thus, clearly differs from P. maghrebianus deposits (Auge´ et al. 1997; Rage 1983b). It seems highly and from other species. probable that the intracolumnar variability for these spe- Palaeophis maghrebianus, therefore, appears as a dis- cies is known. It has already been described that, in these tinct species, although further studies may demonstrate species, the posterior hypapophysis is reduced to a haemal synonymy with P. virginianus and ⁄ or P. vastaniensis when keel in the posterior region, whereas the anterior hypap- additional material belonging to these species becomes ophysis is present, even just as a small bump, in all the known. Palaeophis maghrebianus becomes the most well- precloacal vertebrae (Rage 1983b). In contrast to species of known species from the Palaeophis genus. the primitive group, P. typhaeus and P. toliapicus do not In our opinion, vertebrae do not permit phylogenetic have massive vertebrae retaining markedly laterally pro- analysis at a low taxonomic level, although some vertebral jecting prezygapophyses in any part of the precloacal features appear to be significant for higher taxonomic lev- region. Species from the ‘primitive’ grade (sensu Rage els. However, Snetkov (2011) made such an attempt et al. 2003) are P. maghrebianus Arambourg, 1952 (Ypre- within the acrochordid–nigerophiid–palaeophiid assem- sian of Morocco); P. colossaeus Rage, 1983a (Lutetian of blage. In the resulting cladogram, Palaeophis maghrebi- Mali); P. virginianus Lynn, 1934 (Ypresian or Lutetian of anus is in a large polytomy along with other Palaeophis the USA); P. zhylan Nessov, 1984 (Palaeocene or Ypresian species, Nigerophis Rage, 1975 and the enigmatic Tuscaho- of Kazakhstan); P. vastaniensis Bajpai & Head, 2007 (Ypre- maophis Holman and Case, 1992. Although we consider it sian of India); and P. africanus Andrews, 1924 (Lutetian of interesting to have tried a phylogenetic analysis based Nigeria), although P. africanus shows tendencies towards only on vertebral characters (as other characters are not the morphology of the ‘advanced’ grade. available for all palaeophiine taxa), we have reservations Palaeophis maghrebianus differs from P. colossaeus in about the significance of these results. Moreover, although the absence of parazygosphenial foramina, in the stronger he excluded some species that are clearly based on a too lateral compression of its vertebrae, in a zygosphene not scarce material or whose validity is questioned, several larger than the cotyle, in the relatively feeble inclination of features that vary continuously are treated as discrete the prezygapophyses, as well as in the constant presence of characters, and ⁄ or character states are too vague (e.g. syn- zygantral foramina and absence of a single large median apophyses in a high position versus in a low position, foramen between the two zygantral fossae (Rage 1983a). extent of lateral flattening of the middle trunk vertebrae: Palaeophis maghrebianus differs from P. virginianus in the slightly flattened or strongly flattened). At least one char- presence of an additional hypapophysis in anterior verte- acter (shape of the dorsal surface of zygosphene) clearly brae (Parmley and Case 1988) and a less depressed neural varies within a single species as illustrated in our material. arch. Palaeophis zhylan is poorly described and based on In addition, a character state that cannot exist (‘condyle very few vertebrae, which impedes a proper comparison. much lower than cotyle’) was assigned to Palaeophis zhy- However, the rare vertebrae of this species differ from lan, P. virginianus and P. casei. Therefore, beyond the dis- those of P. maghrebianus by their wider, markedly cussion about the relevance of a phylogenetic analysis at a depressed cotyles and condyles. The diagnosis of P. va- low taxonomic level based only on vertebral characters, staniensis, known from only five vertebrae does not we consider that the vertebral morphology of these taxa, include enough characters to distinguish it from our mate- and notably the intracolumnar variability, is not well rial. The most diagnostic character is considered to be the known enough for such an analysis, and thus, the rela- strong inclination of the paradiapophyseal facets that tionship of P. maghrebianus within Palaeophiinae remains approaches the horizontal (Bajpai and Head 2007), but unknown. However, the new material we present here is this character is also observed in our material. Aside from sufficient to provide a more detailed diagnosis of this features in the diagnosis, the vertebrae of P. vastaniensis previously poorly known taxon and to illustrate some appear to be more depressed than those of P. maghrebi- degree of its intracolumnar variability. This is of particular anus. Palaeophis africanus is known by only three verte- interest because, as stated by Rage et al. (2003) ‘It should brae, only one being useful for comparisons. This vertebra be noted that the variation within the vertebral column is differs from those of P. maghrebianus by its very sharp in- poorly known in the Palaeophiinae. A thorough revision terzygapophyseal ridges and by the neural spine that of the subfamily would probably show that features on encroaches upon the zygosphene, thus heralding the mor- which several species are based are only intracolumnar phology in Pterosphenus. Palaeophis casei is a peculiar, variation’. 658 PALAEONTOLOGY, VOLUME 56

As far as evolution of snakes is concerned, Bajpai and periosteal bone resorption is rather limited so that the Head (2007) raised a question that deserves special atten- vertebrae appear compacted in the periosteal territory as tion. They state that the paravertebral lymphatic system, compared to those of extant snakes. In the endosteo-en- which is characteristic of crown snakes, would have been chondral territory, important secondary bone deposits, already present in Palaeophis vastaniensis. The presence of which occur during remodelling, confer to this bone terri- this lymphatic apparatus results in two parasagittal tory a very compact structure in most of the vertebrae marked depressions on the ventral face of the vertebral (more relative in OCP DEK ⁄ GE 642). These vertebrae centrum in the posterior precloacal region. These depres- appear thus peculiarly compact, as a result of a combined sions, usually termed ‘subcentral grooves’ (Szyndlar 1984; inhibition of primary bone remodelling and of additional Holman 2000), were named ‘subcentral paramedian lym- deposits of secondary bone during remodelling. They are phatic fossae’ by LaDuke (1991). Anteriorly, each fossa thus osteosclerotic. Compactness decreases in posterior opens as a marked notch (paracotylar notch; LaDuke vertebrae, as shown by the lower compactness indices of 1991) between the parapophysis and ventrolateral part of OCP DEK ⁄ GE 642 relative to those of the other verte- the cotylar rim. The notch may be partly bounded ven- brae. Osteosclerosis in the anterior and mid-precloacal tromedially by a ventrolateral cotylar process that origi- regions would have been useful in aquatic taxa for buoy- nates from the cotylar rim (LaDuke 1991, ﬁg. 1A inside). ancy (to achieve neutral buoyancy at the depth at which In snakes whose vertebrae from the posterior precloacal they want to swim) and body trim control (cf. Houssaye region bear a hypapophysis, the ventral fossae may be 2009, 2012). We could tentatively suggest that this part of restricted to the anterior part of the centrum (LaDuke the body might have been where the one or two lungs 1991). Where present, these vertebral structures are easily (see below) extended. In marine snakes, the uniquely observable on isolated vertebrae. developed lung extends over much of the body. It cannot In Palaeophis maghrebianus, none of the vertebrae dis- be known whether this fossil taxon retained one or two play marked fossae that may be regarded as subcentral developed lungs. A high vertebral compactness has also paramedian lymphatic fossae. Posteriorly, the centrum is been observed in the living marine snake Hydrophis sp. convex ventrally. Because palaeophiids have hypapophyses and the freshwater snake Enhydris bocourti (AH, pers. throughout the entire precloacal region, depressions obs.). These data are thus consistent with an aquatic might have been restricted to the anterior part of the cen- mode of life for this taxon. trum. Nonetheless, in P. maghrebianus, in the anterior Palaeophis was a near-shore and estuarine dweller that part of the centrum, only the grooves that separate the lived in shallow marine, brackish and even probably parapophyses from the cotylar rim are present; such short freshwater environments. According to Gheerbrant et al. and shallow grooves are not evidence of the presence of a (2003), the Grand Daoui area, from which all the new lymphatic system. In addition, all vertebrae lack paracoty- specimens of P. maghrebianus come, was located close to lar notches and ventrolateral cotylar processes. the shoreline and river outlets. Interestingly, they hypoth- We checked these features in two other species repre- esized the presence of a mangrove. The presence of man- sented by a number of vertebrae: Palaeophis colossaeus from groves was already reported in Eocene environments that the Lutetian of Mali and P. typhaeus from the Ypresian of housed the ‘advanced’ palaeophiid Pterosphenus (Westgate France. The two species lack any trace of a paraventral lym- and Gee 1990; Gingerich 1992; Westgate 2001). However, phatic apparatus. Therefore, the available evidence, that is, whereas Pterosphenus was found also in an open marine tens of vertebrae belonging to species of the primitive environment (Westgate 2001), Palaeophis species, even (P. colossaeus, P. maghrebianus) and advanced (P. typha- those of the ‘advanced’ group, were likely not pelagic ani- eus) groups suggests that this lymphatic system was mals (Hoch 1975). Shallow aquatic environments includ- likely absent in, at least, these three palaeophiid species. ing mangroves were especially favourable to Palaeophiidae Using a larger sample, a re-examination of this problem in (Rage et al. 2003; Parmley and DeVore 2005). P. vastaniensis would be interesting for future research.

Palaeobiology Palaeoenvironment This new material displays some vertebrae much larger Within palaeophiids, P. maghrebianus appears to be than the previously known for this taxon. With vertebrae relatively poorly adapted to an aquatic life (vertebrae only reaching 3.3 cm in length (in OCP DEK ⁄ GE 536; as weakly compressed laterally, pterapophyses not tall, para- compared to a maximal length of 1.9 cm in a 5.9-m long diapophyses not located very low). The absence of pachy- specimen of Python reticulatus (JCR, pers. obs.)), P. mag- ostosis in this taxon is clear. However, although calcified hrebianus was probably much longer than the biggest cartilage resorption does not appear inhibited, primary extant snakes. It becomes, with P. colossaeus, one of the HOUSSAYE ET AL.:NEWHIGHLIGHTSABOUTPALAEOPHIS MAGHREBIANUS 659 two longer palaeophiids, assuming that the number of Acknowledgements. This work has benefited from the scientific vertebrae was similar in these two species (which cannot program of collaboration between the Office Che´rifien des Phos- yet be determined based on the available fossil material). phates (OCP, Casablanca, Morocco), the Ministe`re de l’Energie, As a result of a reduced vertebral lateral compression in des Mines, de l’Eau et de l’Environnement (MEMEE, Rabat, Mor- ´ P. colossaeus, vertebral width is much more important in occo), the Museum National d’Histoire Naturelle (MNHN, Paris), and the Universities Cadi Ayyad (Marrakech, Morocco) and this taxon than in P. maghrebianus. So, if P. maghrebianus Chouaıˆb Doukkali (El Jadida, Morocco). The first authors thank could reach lengths similar to those of the largest P. co- all the OCP staff in Khouribga for their logistic support and the lossaeus, its diameter would be generally much lower. MEMEE for administrative facilities. Thanks also to R. Allain and Whereas a wide range of sizes is observed among isolated C. Sagne (Museúm National d’Histoire Naturelle, Paris, France) vertebrae of P. maghrebianus, this is not the case in P. co- for access to the material of Arambourg, to M. Lemoine lossaeus for which only few smaller vertebrae are known (MNHN, Paris, France) for the thin sections, to G. Oleschinski (likely a sample bias). (Bonn Universita¨t, Bonn, Deutschland) for various photographs A dense vascular network is observed in P. maghrebi- and to J. Mitchell (Bonn Universita¨t, Bonn, Deutschland) for anus (see above). Vascularization is generally absent or improving the english. We are also grateful to M. Lee (University consists of a few simple vascular canals radially oriented of Adelaide, Australia) and D. Parmley (Georgia College and State in extant squamates (Fig. 10B). Vascularization is University, Georgia, USA) for useful comments that improved the manuscript and to M. Ruta (University of Bristol, England) and observed in only the biggest species of extant squamates. S. Thomas for editorial work. A. H. and P. V. acknowledge finan- The degree of vascularization in P. maghrebianus is much cial support from the A. v. Humboldt Foundation and N.B. from higher than in Eunectes murinus (green anaconda; the French-Morrocan International Research Program (PICS) Fig. 10B) or Python reticulatus (reticulated python), which MARPIC n 4892. are some of the biggest extant snakes (up to 7 and 9 m respectively). This important vascular network indicates Editor. Marcello Ruta that this taxon was growing much faster and thus had a much higher metabolic rate than the largest extant snakes (cf. Montes et al. 2007). REFERENCES

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