Amphisbaenians from the European Eocene: a biogeographical review
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In this paper, part of the amphisbaenian fossil record from the european Eocene is revised. There is no evidence for the existence of amphisbaenian lizards in Europe or on other continents during the Late Cretaceous. Crown amphisbaenians were present in Europe in the early Paleocene and throughout the Paleogene, with the notable exception of the middle Eocene. In particular, they were not found at Messel. European fossil taxa previously assigned to the amphisbaenians are briefly reviewed, and a description of some representative specimens from the Eocene fossil record is presented: dentary and vertebrae from Mutigny (early Eocene, France) are referred to the North American genus Anniealexandria; fossils from the late Eocene of the Phosphorites du Quercy (France) are attributed to Blanidae, and they are the earliest secure occurrence of Blanidae in the fossil record; and dentaries and maxillae from Grisolles (middle-late Eocene, Paris Basin, France) are referred to a new species, Louisamphisbaena ferox. Global distribution of fossil amphisbaenians in the Eocene reveals at least one episode of dispersal between North America and Europe during the early Eocene. Finally, some explanations are suggested for the absence of crown amphisbaenians at Messel and in the European middle Eocene.
KeywordsAmphisbaenians Blanidae Eocene Europe
Amphisbaenians are small, fossorial reptiles that inhabit tropical or subtropical regions of the world. Setting aside the efficiently burrowing small snakes of the family Uropeltidae and the Scolecophidia, the Amphisbaenia are the only true burrowers among reptilia. Among the six families of Amphisbaenia, all taxa are limbless except the Bipedidae, which have no hind limbs but do have well-developed front legs
Most morphological studies show that amphisbaenians share numerous derived characters (Estes et al. 1988; Pianka and Vitt 2003). Its members also share some derived morphological characters with several distinct clades (gekkotans, scincomorphans, anguimorphans, dibamids, snakes), making the position and origin of this clade within squamata uncertain. Beyond the monophyly of Amphisbaenia, morphological characters give little indication of the relationships among its members. The confusion clearly results from their burrowing habits (Kearney and Stuart 2004), with the parallel reduction or loss of limbs in many clades of squamates and the derived nature of the amphisbaenian skull, modified for burrowing. The most obvious amphisbaenian characteristics represent synapomorphies associated with limb loss and burrowing patterns, and, according to Wiens et al. (2006), limb loss and fossoriality occurred at least 25 times during squamate evolution. Mott and Vieites (2009) state that the morphological characters, especially cranial morphology, used to diagnose amphisbaenian taxa may be subject to independent evolution (homoplasy) on different continents (Kearney 2003, fig. 3). Hence, there is substantial disagreement between morphological and molecular data about the taxonomy of amphisbaenians.
According to morphological data, five extant families are recognised (Kearney 2003). Three of these families contain only a single genus: the Rhineuridae, with a single relict species now restricted to Florida (Rhineura floridana); the Bipedidae, (genus Bipes), with three species restricted to Mexico; and the Blanidae (genus Blanus), with four species found in the Mediterranean region. Blanus was previously placed in the Amphisbaenidae, but morphological and molecular studies (Kearney 2003; Kearney and Stuart 2004; Vidal and Hedges 2009) have supported the independant origin of Blanus, as previously thought by Gans (1978). Hence, Blanus is placed in its own family (Blanidae).
The family Trogonophidae includes four genera with six species that now occur in North Africa and the Arabian Peninsula including the island of Socotra. This family is the only one to have acrodont dentition.
The Amphisbaenidae are the largest and most diverse family, and includes 15 recognised genera and ∼175 species. They are found on both sides of the Atlantic, with species occurring in Africa and South and Central America (Gans 1978, 2005; Mott and Vieites 2009,) but there are no shared genera between the two continents. Morphological and molecular studies have also confirmed that Old and New World Amphisbaenidae are monophyletic (Vidal and Hedges 2009), so that Macey et al. (2004) (see also Gans 1990) has suggested that this family dates back at least to the opening of the Atlantic Ocean 80 Mya.
The majority of described fossil amphisbaenians are known from North America (Western United States; Gilmore 1928; Estes 1983; among others). However, the fossil record outside North America is often ignored or underestimated, and this may cause some difficulty in interpreting the relationships among amphisbaenians, along with their historical biogeography (Hembree 2006; Kearney and Stuart 2004).
The oldest fossil records of European amphisbaenians (several fossil vertebrae) may be of late Cretaceous age (Late Campanian–Maastrichtian). Trunk vertebrae from Laño (Spain, late Campanian) have been tentatively attributed to an indeterminate amphisbaenian (Astibia et al. 1990; Rage 1999). Gheerbrant et al. (1997) suggested, without comment, that an incomplete vertebra (Petites Pyrénées, Maastrichtian) may belong to an amphisbaenian. Blain et al. (2010) described five trunk vertebrae from Blasi 2 (Spain, Huesca; Maastrichtian). These fossils are morphologically very similar to the putative amphisbaenian vertebrae described by Rage (1999) at Laño. However, Blain et al. (2010) attributed these vertebrae—and probably those from Laño—to an indeterminate anguid. Rage (1999) has already questioned the relationship of the material from Laño (see discussion in Rage 1999), and he did not exclude the possibility that the vertebrae belong to an anguid. To sum up, it appears from the foregoing that the presence of amphisbaenid lizards in the European Late Cretaceous is far from established, if not dubious.
Numerous amphisbaenian fossils have been collected throughout the Cenozoic in Europe (see, for earlier reviews, Augé 2005; Delfino 1997; Rage 2006; Rage and Augé 1993). Some European specimens consist of cranial and mandibular elements (maxilla, premaxilla, dentary) that could possess taxonomically significant characters, and the primary goal of this study is to provide a detailed account of the amphisbaenian fossil record in Europe, during the Eocene period.
Amphisbaenians are present in Europe in the early Paleogene: middle Paleocene from Hainin, Belgium, MP1–5 (Folie 2006; Van Dyck 1983), late Paleocene of Cernay, France, MP6 (Augé 2005) and possibly Walbeck, Germany, MP1–5 (see Augé 2005, Pseudeumeces wahlbeckensis ? Estes, 1983). The material from Hainin and Cernay is currently being studied by A. Folie in Brussels.
Many amphisbaenians have been named from the Paleocene of North America, and nearly all these fossils are thought to be related to extant Rhineura (Rhineuridae) (Berman 1973; Gans 1978; Estes 1983, Sullivan 1985, Sullivan and Holman 1996; Smith 2006, Stocker and Kirk 2011). The fossil record of rhineurids extends back to the early Paleocene, based on the genus Plesiorhineura from the Torrejonian of New Mexico (Sullivan 1985) and is exclusively North American. Smith (2009) named and described the genus Anniealexandria (Wyoming, early Eocene), a ‘higher’ amphisbaenian, distinct from the basal Rhineuridae. Of particular interest is the species Oligodontosaurus wyomingenis (upper Paleocene, Wyoming). It is known only from a mandible and was referred to Lacertilia incertae sedis by Gilmore (1942). Estes (1965, 1975) placed it in its own family (Oligodontosauridae) and referred it to the Amphisbaenia. Kearney (2003) tentatively included Oligodontosaurus among the rhineurids, but noted that it is lacking diagnostic rhineurid features. Furthermore, Oligodontosaurus differs from all other rhineurids in having a strong posterolabial process of the dentary. Estes (1983) suggested that Oligodontosaurus was a member of the Amphisbaenidae. He stated the mandible of Oligodontosaurus resembles that group, and more precisely, “its mandible closely resembles, for example, that of Cadea”. At that time, Cadea was regarded as a member of the Amphisbaenidae. Now, Cadea constitutes a separate family (Cadeidae) and, according to Vidal and Hedges (2009), Cadeidae and Blanidae are sister-taxa.
Fossil evidence indicates that amphisbaenians were present in Africa by the late Paleocene (Augé and Rage 2006). The fossiliferous locality is situated in the Ouarzazate basin, Morocco (Gheerbrant et al. 1993). Adrar Mgorn 1 (upper Paleocene) is the richest locality and has yielded amphisbaenian fossils that represent two distinct taxa. Other amphisbaenian have been recovered in the Neogene from Africa: two fossil skulls (Miocene of Kenia) were recognised as Amphisbaenidae by Charig and Gans (1990). Bailon (2000) described lizard material from the late Pliocene of Morocco (Ahl al Oughlam, Casablanca). He named a new species, Trogonophis darelbeidae, and included it in the Trogonophidae. Bailon (2000) compared the fossil specimens directly with the extant species Trogonophis wiegmanni, and found that they are very close in all comparable features. In addition, several dentaries from the Moroccan Miocene (Rage 1976) and Pliocene (Bailon 2000) have been attributed to the genus Blanus.
The fossil record from Asia is disputed (Kearney 2003). The first purported amphisbaenian from Asia (Crythiosaurus mongoliensis, Oligocene from Mongolia), described by Gilmore (1943), has been subsequently recognised as a probable snake (Estes 1983; Hoffstetter 1962). A late Cretaceous fossil from Mongolia (Sineoamphisbaena hexatabularis) was identified as a primitive amphisbaenian (Wu et al. 1993, 1996). However, according to Kearney (2003), Sineoamphisbaena is not related to the amphisbaenian. Borsuk-Bialynicka (1991) reported an indeterminate amphisbaenian from the Maastrichtian of Mongolia. The species Hodzhakulia magna (Albian of Uzbekhistan) was regarded as a possible amphisbaenian (Nessov 1985; Nessov and Gao 1993). However, its dentary offers limited phylogenetic information and it does not show any unambiguous amphisbaenid character according to Kearney (2003). K. Smith (personal communication) suggests that an incomplete dentary figured in Böhme (2007, Squamata indet., early Oligocene from Mongolia) is related to amphisbaenid lizards. Some interesting resemblances to the dentary of extant amphisbaenids are present (e.g. intramandibulary septum fused to dentary wall). However, this dentary seems more delicately built than those of extant amphisbaenians. Some dentaries from the Paleocene of Hainin, Belgium, referred to Amphisbaenians (Folie 2006), bears a close resemblance to the Mongolian specimen, particularly in the general shape and tooth morphology.
Material from the Phosphorites du Quercy was obtained during two phases. The old collections were gathered during the mining exploitation period of the phosphorites and they have no detailed provenance data, and hence their age is uncertain and probably mixed, with most of these fossils probably ranging from late Eocene to Oligocene in age. From 1965 onwards, new excavations were undertaken by research teams. This palaeontological exploration has resulted in the discovery of many small fossils, which all fit into a detailed biochronologic framework (Rage 2006).
The time scale used here (mammalian standard levels, MP) is that defined in Schmidt-Kittler (1987) and BiochroM’97 (1997), see also Hooker et al. (2004) and Franzen (2005). The institutions referred to are: IRScNB, Institut Royal des Sciences Naturelles de Belgique, Brussels, Belgium; MNHN, the Muséum National d’Histoire Naturelle, Paris, France; USTL, Université des Sciences et Techniques du Languedoc, Montpellier, France.
Paleogene species previously assigned to the Amphisbaenia
Omoiotyphlops priscus De Rochebrune, 1884
De Rochebrune (1884) named and briefly described this species, based on several associated trunk vertebrae from the Phosphorites du Quercy (no detailed provenance data, probably Eocene or Oligocene) and considered it to be a snake. It is worth noting that the illustration was labelled “Typhlops edwardsi” (see Rage 1978). Hoffstetter (1942) was the first to assess critically the status of Omoiotyphlops priscus and showed that it represents a member of the Amphisbaenia. Amphisbaenian vertebrae are not diagnostic to genus or species, according to Estes (1983), and, thus Omoiotyphlops priscus is a nomen dubium.
Remarks: Rocek (1984) described amphisbaenian remains from the Miocene of Dolnice (MN4, Czech Republic) and referred them to the genus Omoiotyphlops as gracilis. Venczel and Stiuca (2008) attributed amphisbaenian fossils from the Miocene of Romania to the species Blanus gracilis. According to Venczel and Stiuca (2008), the material from Dolnice appears to be related to the genus Blanus, and Venczel and Stiuca regarded Omoiotyphlops as a junior synonym of Blanus
Campinosaurus woutersi Augé, 1992
Holotype: partial left dentary, R119, IRScNB, Brussels.
Occurrence: earliest Eocene, Ypresian, MP7; Dormaal, Belgium.
This dentary was originally identified as a primitive anguimorphan lizard (Dorsetisauridae, see Hoffstetter 1967). However, some features of this fossil do not exist in anguimorphan, and, subsequently, I have suggested that Campinosaurus could pertain to an amphisbaenian (Augé 2005). Some problems remain, and it is difficult to be sure whether this attribution is correct. Further study of the specimen from Dormaal must precede further speculation on the affinities of Campinosaurus.
Schleich (1988) named and described the species Palaeoblanus tobieni from the early Miocene of Germany. Fossil dentaries from Ehrenstein and Gaimersheim (late Oligocene, MP30, Germany) are attributed to Palaeoblanus sp. (Schleich 1988). However, the features that defined this species seem rather plesiomorphic within Amphisbaenia.
Hecht and Hoffstetter (1962) suggested that amphisbaenian remains from Dormaal (Belgium, MP7) may be referred to the genus Blanus. Milner et al. (1982) questionably referred a maxilla, some dentaries and vertebrae from the upper Eocene of England to the genus Blanus, without further comment.
MU 17467, Fig. 2. This right dentary is lacking only the posterior tip, otherwise it is complete and retains the complete tooth count. The dentary is short, relatively deep and robust, and it measures 4.2 mm from the anterior tip to the coronoid process. The tooth row is complete and comprises nine teeth. The ventral border of the dentary is slightly concave.
In medial view (Fig. 2a), the anterior part of the Meckelian canal is restricted in a narrow furrow and it extends almost up to the symphysis. It is exposed ventromedially for most of its length with a wide posterior opening after the level of the 7th tooth. The intramandibular septum is subvertical and well-developed: it extends far back to exceed the level of the last tooth. Its ventral border is not free but fuses with the dental wall. The posterior margin of the intramandibular septum is deeply incised. Immediately at the base of the septum is a distinct, narrow and elongated incision that certainly receives the splenial (or the anterior tip of the angular).
In front of and above the Meckelian canal, the subdental shelf (sensu Rage and Augé 2010) is deep and its dorsal margin nearly horizontal. Posterodorsally, the subdental shelf narrows and curves posterodorsally, ending posterior to the last tooth. Immediately behind this tooth, the dentary bears a strong coronoid process that projects posterodorsally, well above the level of the tooth row. Medially, this process shows a distinct facet that extends on the intramandibular septum and that received the anteromedial process of the coronoid bone. At the base of the teeth, the sulcus dentalis is well defined.
The posteroventral process is broken off but its large base indicates that the process was certainly quite strong.
The nine teeth are pleurodont, having two-thirds of their height projecting above the lateral parapet of the jaw. All teeth are high and unicuspid with a moderately pointed apex. The first teeth are peg-like and inclined forwards. The posterior ones (from the fifth tooth position) are markedly expanded, with broad bases, and the last two teeth are reduced. Small basal foramina that open medially are clearly visible at the bases of some teeth. The base of the second tooth is deeply incised by an important replacement pit that opens anteromedially.
The lateral surface of the dentary is smooth, moderately convex and has a row of four alveolar foramina, situated in the anterior half of the bone. The posterior area shows a shallow and broad depression (that maybe represents the insertion of one of the mandibular adductors).
MNHN, MU 7912., Fig. 3. The vertebrae are well preserved. MU 7912 are procoelous, dorsoventrally moderately depressed and measures 2 mm from the cotyle to the posterior end of the condyle. In dorsal view, the vertebrae are constricted between the pre-and postzygapophyses. The prezygapophyseal facets are inclined towards the neural arch and form an angle of about 30° with the horizontal plane. The prezygapophyses are broader than the postzygapophyses, so the vertebrae are wider at the front than at the back.
The anterior edge of the neural arch is nearly straight, while the posterior one is widely concave, without median denticulation. The vertebrae show a thin but distinct sagittal ridge on the dorsal surface of its neural arch. This ridge does not reach the posterior border of the vertebrae. Between the postzygapophyses, the neural arch bears a flat, triangular tuberosity and the neural spine is absent.
Laterally, the synapophyseal facet is large and globular, and extends the entire height of the centrum.
In ventral view, the centrum is rather elongated, entirely flat, without any keel and laterally delimited by slightly concave and subparallel margins. No foramina are perceptible on the ventral surface of the centrum.
In anterior view, the neural arch is arched and devoid of a zygosphene. The cotyle is strongly dorso-ventrally depressed, being approximately two times wider than high. The neural canal opens widely and is subtriangular.
In posterior view, the neural arch is hardly vaulted and it lacks a zygantrum. The condyle is depressed.
These vertebrae are associated with the dentary described above on the basis of amphisbaenian morphology, comparable size and same provenance.
Within squamates, trunk vertebrae with a flat ventral surface of the centrum and subparallel margins are common in amphisbaenians, some anguids (genus Anguis) and Helodermatidae. Helodermatid and anguid lizards always bear a well-developed neural spine. Some extant amphisbaenids show a slight sagittal ridge on the neural arch that may extend up to the posterior margin of the vertebra (Rage 1999). However, this feature hardly deserves to be called a neural spine. In addition, Sineoamphisbaena, which bears a well-developed neural spine, is no longer considered as an amphisbaenian (Kearney 2003). Torres and Montero (1998) reviewed amphisbaenian fossil vertebrae from the Pleistocene of Argentina. This material was originally assigned to an iguanid lizard (Rusconi 1937), and named Leiosaurus marellii Rusconi 1937. It was subsequently recognised as an amphisbaenid by Donadio (1982). These vertebrae bear distinct but low neural spines. Thus, I subscribe to the statement of Blain et al. (2010): “The presence of a well-developed neural spine on trunk vertebrae is not known in any fossil amphisbaenian”. In short, all the characters of the vertebrae from Mutigny accord with the description of an amphisbaenian (see Fig. 4).
Amphisbaenians differ from other lizards by their short dentary (and maxilla) and a low number of large teeth, two prominent features of the dentary from Mutigny. According to Gans (1974), as the work needed to form a length of tunnel varies with the tunnel’s diameter, it is advantageous for a burrowing predator to elongate and to reduce its body diameter, including the head. Thus, the jaw would shorten, reducing the maximum gape. In addition, an increase in the relative height of the coronoid process increases the mechanical advantage of the temporal muscles.
The dentary from Mutigny shares many derived characters with ‘higher’ amphisbaenians (Bipedidae, Blanidae, Trogonophidae and Amphisbaenidae; see Smith 2009): strong coronoid process that projects posterodorsally well above the level of the tooth row, intramandibular septum well-developed, and development of a facet for the splenial (or the angular) on the ventral margin of the intramandibular septum. The specimen described here is diagnosed as an amphisbaenian differing from the Trogonophidae in having pleurodont teeth and from the Rhineuridae and Oligodontosaurus (Oligodontosauridae Estes, 1975) in having an open Meckelian canal. The presence of a strong coronoid process and intramandibular septum points to both the Amphisbaenidae and Blanidae. In addition, this dentary shares many similarities with the dentary of Bipes (Bipedidae) but, generally, the presence of the family Bipedidae in European Paleogene or Neogene localities is excluded for geographical and stratigraphical reasons (Delfino 1997).
The morphology of the dentary from Mutigny conforms to all corresponding features seen in the type dentary of Anniealexandria gansi Smith 2009. This species from the earliest Eocene of Western North America (Wyoming) is diagnosed as: “Amphisbaenian differing from all living taxa in having nine dentary teeth…”. Thus, the amphisbaenian fossils from Mutigny are referred to the genus Anniealexandria. However, additional material is needed to discuss the possibility of referring those fossils to the type species A. gansi.
Blanidae genus and species indeterminate
Localities and age: Escamps (Phosphorites du Quercy, France, late Eocene, Priabonian, MP19); St Néboule (Phosphorites du Quercy, France, late Eocene, Priabonian, MP18); Malpérié (Phosphorites du Quercy, France, late Eocene, Priabonian, MP17).
The most completely preserved dentary (Fig. 5, right dentary, USTL, ECB 1704, Escamps B, Phosphorites du Quercy, Priabonian, MP19) bears eight pleurodont teeth or tooth positions. Its posterior and anterior ends are broken (in particular, the coronoid process). The mandibular symphysis is moderately broad.
Medially, the subdental table (sensu Rage and Augé 2010) is subhorizontal and a slight sulcus dentalis runs along the tooth row. The subdental shelf is rather prominent and, beneath the foremost six tooth positions, it is of a relatively constant depth, with a gently convex ventral margin. Posterior to the sixth tooth position, the subdental shelf narrows and turns dorsally; it appears to extend to the level of the last tooth, but the posterior part could have been broken. Beneath the subdental shelf, the Meckelian canal extends almost up to the anterior end of the symphysis. It is exposed ventromedially for most of its length. A well-preserved feature of ECB 1704 is the intramandibular septum; its ventral margin is fused with the medial wall of the dentary. The posterior edge of the septum shows a wide, subtriangular notch. A narrow and elongated incision runs along the base of the septum; it appears to correspond to the impression of the splenial (or the angular) on the dentary.
The eight teeth are evenly and closely spaced and inclined forwards. The bases of the teeth are enlarged and nearly cylindrical, the shaft tapers steadily to a blunt point but the apex of most of the teeth is badly worn. The sixth tooth is distinctly larger than the others and the posterior two teeth are much smaller than the preceding ones.
Four mental foramina are present on the lateral wall of the dentary, the first one being situated below the level of the following foramina.
Posterior part of a left dentary (Fig. 6, MNHN, SNB 1034, St Néboule, Phosphorites du Quercy, late Eocene, Priabonian, MP18). This specimen permits additional observations: the strong coronoid process is well preserved and it projects posterodorsally, above the level of the tooth row. The intramandibular septum is made up of two divergent surfaces separated by an important step. The posterior three teeth are mostly complete; their morphology is identical to those of ECB 1704. Their crown is very weakly concave towards the rear, so that the apex is slightly recurved.
(Figure 7, USTL, MAL 609, Malpérié, Phosphorites du Quercy, late Eocene, Priabonian, MP17). The lateral margins of this fossil are broken, thus it is difficult to estimate the total premaxillary tooth count. Five teeth are rather poorly preserved but a sixth tooth seems to be present on the right lateral margin of the specimen, which gives a tooth count of seven. The median tooth is the strongest of the tooth row. The supradental shelf forms a shallow ridge above the tooth row. On the midline, a weak and rounded incisive process projects ventrally. The nasal process is almost entirely broken. However, it is clear that there is not a sharp angle between its basis and the lateral margins of the premaxilla. A pair of large premaxillary foramina open just behind the nasal process.
At the front, the premaxillary process is dorsally and medially deflected (the inturning of the anterior end of the maxilla is pronounced). Just behind the premaxillary process, there is a large concavity on the lateral wall of the dentary. The facial process (or nasal process; see Oelrich 1956) is roughly triangular. The anterior margin of this process rises steeply posterior to the premaxillary process and shows an important medial deflection. A short frontal process (terminology of Kritzinger 1946) is present at the top of the facial process. Posteriorly, the facial process drops gradually towards the posterior end of the maxilla, and at the level of the last tooth, it begins to descend sharply. The lateral surface of the facial process is smooth, but near its base there is a row of three large labial foramina. In addition a small, fourth labial foramen is present at the base of the frontal process.
Medially, near the anterior base of the facial process is the anterior inferior alveolar foramen of the maxilla. An important concavity, set on the medial wall of the palatal process, is situated above the level of the second tooth. The palatal shelf extends medially as a subhorizontal surface. The palatal shelf is divided into two areas by an oblique step that runs up onto the medial wall of the facial process. The posterior part of the palatal shelf narrows beneath the level of the last tooth, and a prominent step marks the boundary between the posterior, narrowed part and the anterior part of the process. This step marks the limit of the overlap of the palatal process by the ectopterygoid. A wide notch is present on the posterior margin of the palatal shelf, thus this margin is V-shaped.
(Escamps C, USTL, ECC 2509). Those vertebrae are similar to the dorsal vertebrae from Mutigny described above. In particular, they lack a distinct neural spine dorsally. It is perhaps worthwhile to note that a few vertebrae from Escamps show an incipient notch on the posterodorsal margin of the neural arch.
Discussion: The premaxilla, with its enlarged median tooth, belongs to an amphisbaenian (Gans 1978; Estes et al. 1988). In addition, large anterior premaxillary foramina appear to be an amphisbaenian synapomorphy, according to Smith (2009). The short tooth row, low tooth count and tooth morphology are sufficient to assign the dentary and maxilla to Amphisbaenia (the first two features are certainly not independent). The strong inturning of the anterior end of the maxilla is also an amphisbaenian synapomorphy (Smith 2009). The dentary shows the synapomorphies of higher amphisbaenians, according to Smith 2009 (see above, discussion on the dentary from Mutigny).
Hence, these fossils could be assigned to higher amphisbaenians, except Trogonophidae (Blanus, Amphisbaenidae, Bipes).
Most of the trunk vertebrae associated with the material from the late Eocene have a smooth posterior margin (character 136 in Kearney 2003). This condition is common in Blanidae and Bipedidae. In many, but not all, extant Amphisbaenidae, the posterior margins of the neural archs are distinctly denticulate (derived state). To be fair, it must be acknowledged that a few amphisbaenian vertebrae from the late Eocene of the Phosphorites du Quercy show a small indentation on their posterior margin, but this feature is not comparable with the notch seen in amphisbaenid vertebrae.
The dentary from Escamps differs from Amphisbaenidae in having a deep forward Meckelian groove. In contrast with Amphisbaenidae, this condition is encountered in Blanidae.
The maxilla from Escamps is very similar to that of the extant genus Blanus (Blanidae): the premaxillary process projects dorsally; the posterior part of the facial process drops gradually; the posterior end of the maxilla tapers regularly; and the posterior margin of the palatal shelf is forked. At the top of the facial process, the frontal process is short and rounded. The posterior part of the palatal shelf narrows beneath the level of the last tooth. This maxilla differs from Amphisbaenidae in all these characters, based on figures of the maxilla of Amphisbaena alba in Montero and Gans 1999. Moreover, the maxilla from Escamps differs significantly from the maxillae of Diplometodon (Trogonophidae; Maisano et al. 2006, fig. 8) and Rhineura (Rhineuridae; Kearney et al. 2005, fig. 9) which have a prominent frontal process. Finally, ECC 2508 cannot be confused with the maxilla of any Bipedidae that are characterised by a very narrow facial process (Zangerl 1944, fig. 9).
Hence, the amphisbaenian fossils from the late Eocene of the Phosphorites du Quercy described above are referred to the family Blanidae. Although this material is very similar to the extant genus Blanus, the number of teeth of the maxilla (five) appears to distinguish those fossils from extant Blanidae (three or four teeth on the maxilla, according to Kearney 2003). Taxonomic separation of these fossils from Blanus needs additional material and further studies, but could be realistic in view of the number of teeth of the maxilla. These fossils are the earliest secure records of definite Blanidae in the fossil record.
Schleich (1985, 1988) named and described two amphisbaenian species, Blanus antiquus and Palaeoblanus tobieni, from the Miocene of Germany. Blanus antiquus shows a number of interesting resemblance to the fossils from the late Eocene of the Phosphorites du Quercy: in particular, B. antiquus has seven premaxillary teeth and five maxillary teeth. However, further study of the German fossils must precede further speculation on their affinities, although many characters indicate affiliation within Blanidae.
This dentary bears triangular, labio-lingually compressed teeth that distinguish it from all the dentaries registered above. The intramandibular septum is also unusual: it is made up of dorsal and ventral facets separated by a step. The ventral facet of the specimen SNB 1035 is less inclined and shallower than the subvertical dorsal facet.
Genus Louisamphisbaena nov.
Type species:Louisamphisbaena ferox sp. nov.
Diagnosis: as for the type and only known species.
Etymology: In honour to the late Pierre Louis, a distinguished palaeontologist and a friend.
Louisamphisbaena ferox sp. nov.
Occurrence: Grisolles, Paris Basin, France, latest middle Eocene, Bartonian, MP16.
Etymology: from Latin ferox, as the species has canine-like teeth.
Diagnosis: Amphisbaenian differing from all fossil and extant taxa in having a prominent, recurved, second tooth on the maxilla. Its apex is sharply pointed and this tooth is canine-like. The inturning of the anterior end of the maxilla is limited. Dentary relatively elongated with widely spaced teeth. Differs from Rhineuridae in retaining an open Meckelian canal and from Trogonophidae in having a pleurodont dentition.
The holotype (Fig. 10, MNHN, GRI 17494) is a right maxilla bearing its complete tooth row with five pleurodont teeth. The maxilla is broken above the level of the superior alveolar foramen and nearly all of the facial process is lacking. Medially most of the supradental shelf is broken. However, an important concavity (dimple, according to Smith 2009) is preserved just beneath the premaxillary process. A slight sulcus dentalis is present along the tooth bases. The palatal shelf (dorsal part of the supradental shelf) extends medially as a large sub-horizontal shelf and forward it contacted the premaxilla. The premaxillary process projects dorsally but less than the premaxillary process of the maxilla described at Escamps C (ECC 2508, however, its anterior end may have been broken). The inturning of the anterior end of the maxilla is limited. The palatal shelf is divided into an anterior and posterior areas by a deep, transverse step situated at the level of the third tooth position. The posterior part of the palatal shelf narrows at the level of the last tooth. The posterior end of the palatal shelf shows a small notch. A maxillary foramina opens through the posterior part of the palatal shelf, where that shelf narrows.
Labially, the facial process is entirely lacking, the labial foramina are not preserved except the ventral half of one of them, above the level of the penultimate tooth. Posterior to the premaxillary process and above the second tooth, there is a large concavity, but its dorsal margin is broken. The most posterior part of the facial process is probably preserved, and it appears to drop gradually towards the posterior end of the maxilla.
The dentition is complete and highly distinctive. The five maxillary teeth are unicuspid, their shaft bends anteriorly, their base is broad, elliptical and labiolingually compressed and their crown is posteriorly recurved. The teeth vary in size and inclination along the tooth row, the second tooth being by far the largest. Its apex is sharply pointed and recurved, and incipient posterior and anterior cutting edges seem to be present.
The left dentary (Fig. 11, MNHN, GRI 17495) has six nearly complete teeth and the base of one other, so the tooth row is probably complete. The posteriormost part of the dentary is missing because of breakage. The dentary is rather elongated and shallow, by amphisbaenian standards. The Meckelian canal is exposed ventromedially and it opens widely towards the symphysis. The subdental table is horizontal and a sulcus dentalis runs along the tooth row. Medial to the subdental table, the subdental shelf is of a relatively constant depth even at the back with a gently convex medial surface, and it curves upwards towards the symphysis which is a strong articulation surface. The intramandibular septum is badly damaged, as is the posterior part of the dentary.
The lateral surface of the dentary is smooth. There are five large oval alveolar foramina. The ventral margin is slightly concave with a low ‘heel’ beneath the symphysis.
The tooth row has seven, widely spaced tooth positions. Although no teeth are fully preserved in this specimen, it shows a tooth morphology similar to that of the maxilla. However, no dentary teeth are as developed as the second maxillary tooth. The slender, widely spaced teeth are a typical feature of this dentary.
Discussion: These specimens show typical amphisbaenian features such as a low tooth count, short tooth row, tooth morphology (teeth robust, unicuspid with a rather pointed apex), and anterior part of the maxilla curved inwards (Smith 2009). These fossils may be confidently excluded from the families Rhineuridae and Trogonophidae: closure of the Meckelian canal occurs in Rhineuridae and Trogonophidae have an acrodont dentition. The wide opening of the Meckelian canal of the dentary in the symphysis is consistent with the Blanidae, as are the premaxillary process of the maxilla that projects dorsally, the narrowed posterior part of the palatal shelf and the posterior part of the facial process that drops gradually towards the posterior end of the maxilla. Thus, the attribution of these specimens to the Blanidae is partially supported in this study but is uncertain on account of their incomplete preservation.
The dentition is distinctive in GRI 17494 and differs from all other amphisbaenian species by the presence of a large, canine-like second tooth on the maxilla, and the widely spaced teeth of the dentary. The relative elongation of the dentary and the slight degree of inturning of the anterior end of the maxilla are also very unusual among amphisbaenians. These features are certainly autapomorphic within amphisbaenians, and they are used to diagnose the new species Louisamphisbaena ferox.
These characters are associated with the carnivorous habits of many predatory lizards (e.g. Varanidae), but L. ferox could be one of the few amphisbaenians that exhibits these features, at least in their embryonic form. The biting of prey may require a wide gape. Clearly, amphisbaenians are active predators of fossorial prey, but increasing the gape of the jaws conflicts with other demands, notably their adaptation to a burrowing existence that constrains their body diameter (Gans 1974).
As far as I am aware, Gans (1968, 1990) was the first author to address the biogeography of Amphisbaenia. He suggested a western Mediterranean origin of amphisbaenians during the Jurassic and proposed that amphisbaenians may have separated from other squamates very early. Central to this argument was the necessity for faunal exchange between Africa and South America before these continents separated. The close similarities of the African and the American amphisbaenids suggested what would now be called a vicariance event initiated by the opening of the Atlantic. Subsequently, several studies, integrating phylogenetic and biogeographic data, followed Gans and indicated that the family Amphibaenidae could have originated before the Late Triassic breakup of Pangea (Kearney 2003; Macey et al. 2004). Thus, the diversification of Amphisbaenidae correlates with a major large-scale geological and geographical event forming barriers, leading to vicariant speciation in well-defined areas of endemism (here, Africa and South America, respectively).
The widespread acceptance of vicariance may be explained by development of historical geography (Nelson and Platnick 1981), and, to a great extent, vicariance has become the default explanation for any observation of allopatry (e.g. Erwin 1979, 1981; Nelson 1974; Savage 1982). Dispersal explanation have been usually rejected by cladistic biogeographers as ad hoc explanations.
A first shortcoming in vicariance biogeography is the issue of how ancestral species became widespread enough to be affected by vicariant events. It seems reasonable to assume that, at some point in the past, the members of the biota expanded their geographical ranges, so that they could be affected by subsequent vicariance events. However, early advocates of vicariance biogeography minimised such a dispersal. Now, beliefs have changed, and Lieberman (2000) and Brooks and McLennan (2002) have pointed out that large-scale biotic diversification would comprise a combination of episodes of dispersal as well as episodes of vicariance. For example, Hembree (2006) suggests that the biogeography of the Amphisbaenia is not simply the result of vicariance due to the breakup of Pangea and the opening of oceanic realms but is also the result of range expansion throughout the Mesozoic and Cenozoic. During periods of emergence, continental organisms would be able to move between formerly separated regions.
Molecular time estimates of divergences among amphisbaenians have indicated young divergences among families, mostly in the Cenozoic, less than 65 Mya, from the Paleocene to Eocene (Vidal and Hedges 2005, 2009; Vidal et al. 2008; Wiens et al. 2006). All studies confirmed the basal position of Rhineuridae within amphisbaenians. Vidal and Hedges (2009) estimated the basal split between Rhineuridae and the remaining Amphisbaenia at 109 Mya (154–76). Wiens et al. (2006) also give an early origin for amphisbaenians, during the Late Jurassic–Early Cretaceous. However, Wiens et al. (2006) use a fossil from the Early Cretaceous (Hodzhakulia magna) to calibrate the Amphisbaenia–Lacertidae split, and Kearney (2003) has expressed serious doubts about the supposed amphisbaenian affinities of Hodzhakulia. Hipsley et al. (2009) place the split between amphisbaenians and lacertids during the Late Cretaceous.
Obviously, these data conflict with the vicariant biogeographic scenario mentioned above.
Time slicing (Fig. 13)
Incorporation of temporal information (fossil record) may be used to identify the absolute timing of the diversification of the lineages and their biogeographic history (Hunn and Upchurch 2001). Time slicing corresponds to the analysis of biotic distributional data according to a sequence of individual stratigraphic intervals (time slices; Morrone 2009; Upchurch et al. 2002).
In order to apply time slicing, the cladogram is temporally partitioned by deleting all taxa that did not exist at a particular time slice. The area cladogram is applied to “time-slices”: amphisbaenian phylogeny is “adapted” so that only taxa present within the relevant time-slice (here, the Eocene) are retained: Rhineuridae (North America); Blanidae (Europe); Anniealexandria (North America; Europe). Rhineuridae have a basal position within amphisbaenians and Blanidae are more derived (see above). Anniealexandria appears to represent an early record of ‘higher’ amphisbaenians (this genus is more derived than Rhineuridae), according to Smith (2009). However, this genus presents some primitive characters for amphisbaenians that suggests it does not belong to the crown group of ‘higher’ amphisbaenians (Smith 2009). Thus, Anniealexandria is tentatively considered to have a basal position within higher amphisbaenians, and this is a preliminary analysis that needs phylogenetic corroboration.
The presence of Blanidae in Europe may result from a second dispersal event or from a sympatric speciation. Vidal et al. (2008) recognised that transatlantic dispersal played an important role in explaining the distribution of modern amphisbaenids. These authors also suggest that the most probable hypothesis to explain the presence of Cadea on Cuba is by a second, Eocene, transatlantic dispersal from Africa (or Europe) to Cuba.
It is clear that there is a high degree of congruence between the phylogenetic tree (clade rank) and the order of occurrence of fossils in the stratigraphic record (age rank). Stratigraphic consistency index (SCI) = 1 (it varies between 0 and 1; Huelsenbeck and Rannala 2000). In addition, there is a good agreement between molecular dates for the origin of Blanidae (40 Mya; Hedges and Vidal 2009) and the first occurrence of blanid lizards in the fossil record: late Eocene, MP19, 35 Mya.
A second analysis, including the stem taxa Cryptolacerta hassiaca Müller et al. 2011, has been performed (Fig. 13b). A vicariance event may have resulted from the fragmentation of the area occupied by stem amphisbaenians. Throughout most of the Mesozoic, North America and Eurasia were one landmass, sometimes called Laurasia. Separation between Europe and North America took place during the Late Cretaceous, and the final phase in the breakup occured during the early Cenozoic: the North Atlantic Ocean opened as rifts propagated on either side of Greenland (Scotese 2004). However, in this case, the occurence of Cryptolacerta in the stratigraphic record does not match the phylogenetic tree (or clade rank): Rhineuridae and “higher amphisbaenians” diverged at least in the early Paleocene, well before the occurrence of Cryptolacerta (see discussion in Müller et al. 2011).
The geographical distribution of Eocene amphisbaenians supports the hypothesis that dispersal had exerted a powerful influence on their current distribution. The fossils described here are also taxonomically significant, containing the first secure evidence for the presence of Blanidae in the fossil record.
An intriguing question is the absence of ‘crown’ amphisbaenians at Messel (potential stem taxa like Cryptolacerta Müller et al. 2011 are not discussed). What factor(s) may explain this absence? First, we might address the issue as to whether this lack of amphisbaenians reflects a true absence rather than a taphonomic or environmental bias.
The burrowing lifestyle of the amphisbaenians might explain their absence. Extant amphisbaenians prefer dry substrata to dig their burrows, and they could have avoided the immediate vicinity of the Messel lake. In addition, it is widely held that amphisbaenians display low water-dispersal capabilities. However, some extant amphisbaenians do not avoid aquatic environments. For example, Señaris (1999) observed that, when disturbed, Amphisbaena gracilis tried to escape immediately towards water, and Maschio et al. (2009) provide data on the utilization of aquatic environments in Brazilian Amazonia by two amphisbaenid species, Amphisbaena amazonica and A. alba.
Messel is not the only locality without amphisbaenians in the European middle Eocene. No amphisbaenians have been found in the European earliest middle Eocene in at least eight localities: Messel, Geiseltal, St. Maximin, Lissieu, Cuzal, Laprade, Aumelas, La Défense. This “dark » period for amphisbaenians in Europe is sandwiched between older and younger amphisbaenian assemblages (with different taxa). At St. Maximin and Lissieu (France, middle Eocene, MP13 and MP14, respectively), fossils are recovered from fissure fillings, taphonomy is entirely different, and, thus far, amphisbaenians have not been found (the herpetofauna from Lissieu is as diverse as is that from Messel; Rage and Augé 2010). Thus, the lack of amphisbaenian remains certainly reflects a sharp decline or even a true absence during the middle Eocene in Europe rather than a taphonomic bias at Messel. Further arguments support the decline (or absence) of amphisbaenians in the European middle Eocene: The change between the rich amphisbaenian fauna of Dormaal (early Eocene, MP7) and their absence in the middle Eocene of Messel (MP11) is gradual and the depauperate amphisbaenian fauna of Prémontré (MP10) prefigure their absence at Messel (Augé 2005, see fig. 205). Other lizard taxa disappeared from Europe across the early Eocene–middle Eocene boundary: Tinosaurus (Agamidae) and Saniwa (Varanoidea). In the same vein, Hartenberger (1987) reported a significant episode of mammalian reorganisation near the Ypresian–Lutetian boundary (see also Leduc 1996).
Thus, the decline of amphisbaenians in the European middle Eocene may be connected to climatic and palaeoenvironmental changes (Zachos et al. 2001): loss of amphisbaenids in Europe is contemporaneous with a climatic deterioration (end of the early Eocene climatic optimum, EECO). The cooler conditions may have had a strong impact on the broad pattern of terrestrial vertebrate evolution and promoted the disappearance of early Eocene amphisbaenians like Anniealexandria. For example, Woodburne et al. (2009) reported an important faunal diversity loss during the climate deterioration subsequent to the early Eocene climatic optimum in North America (from 50 to 46 Mya).
Some authors have cautioned against assigning to the climate a direct (or exclusive) role in faunal changes, and, according to Schopf (1984), climate is only half the story in the evolution of organisms through time. Over the scale of the whole Cenozoic, Alroy et al. (2000) state that biotic factors such as diversity dynamic within lineages, competition or resource availability seem to be more important than the effects of climate change on mammalian evolution. Gaston (2003) discussed the general difficulty of imputing a direct effect of climatic factor on the distribution of extant species. In particular, the amphisbaenians were not eradicated at the Eocene–Eocene boundary (Augé and Smith 2009) during the major climatic deterioration that took place across this transition. Why would they have been decimated by the relatively mild cooling after the EECO?
Biotic factors play an important role in limiting the geographic ranges of many species. Interactions with other species ultimately restrict their distribution by preventing expansion of their boundaries. In particular, interaction between biogeography and competition may be important: Huey et al. (1974) commented that sympatry of fossorial lizard species is unusual, and Wiens et al. (2006) suggested that when a limb-reduced, burrowing squamate lineage is present in a region it preempts the presence or the evolution of other lineages that have the same trait. In the same vein, the disappearance of a lineage has often been ascribed to competitive replacement: e.g. extinction of Old World iguanid lizards has been attributed to pressure from diversifying agamid or lacertid lizards (Augé 2007; Avery and Tanner 1971; Camp 1923: 334; Milner et al. 2000). Hence, it is worth noting that the first limb-reduced european anguid lizards (Ophisauriscus quadrupes Kuhn 1940; see Sullivan et al. 1999) appeared at Messel. According to Wiens et al. (2006), this clade first evolved in Europe and subsequently spread to Asia. However, this assumption also has its own shortcomings: for example, Gans (1974) observes that, in South America, several species may be sympatric in the central parts of the amphisbaenian range, more specialised species occuring in the deeper layers of the soil.
This paper discusses the fossil record of amphisbaenian from the European Eocene. Biogeographers and phylogenetists increasingly rely on the historical record to evaluate their interpretation and to reconstruct the spatial pattern and the timing of the diversification of lineages. Therefore, the application of total evidence phylogenetic analysis to amphisbaenians could provide new opportunities.
It is a particular pleasure to thank the Senckenberg Institute for its invitation to participate in the 22nd International Senckenberg Conference, and in particular T. Lehmann, S.F.K Schaal and S. Weber. For helpful advice and assistance, I would like to thank J.-C. Rage, K. Smith, J. Müller and S. Bailon. It is a pleasure to acknowledge the assistance provided by the MNHN and in particular by P. Janvier. I am indebted to C. Lemzaouda and P. Loubry from the MNHN for the photographs.
- Alroy J, Koch PL, Zachos JC (2000) Global climate change and North American mammalian evolution. In: Erwin DH, Wing SL (eds) Deep time. Paleobiology Suppl 26(4):259–288Google Scholar
- Astibia H, Buffetaut E, Buscalioni AD, Cappetta H, Corral C, Garcia-Garmilla F, Jaeger JJ, Jimenez-Fuentes E, Le Loeuff J, Mazin JM, Orue-Etxebarria X, Pereda-Suberbiola J, Powell JE, Rage JC, Rodriguez-Lazaro J, Sanz JL, Tong H (1990) The fossil vertebrates from Lano (Basque Country, Spain); new evidence on the composition and affinities of the Late Cretaceous continental faunas of Europe. Terra Nova 2:460–466CrossRefGoogle Scholar
- Augé M (1992) Campinosaurus woutersi n.g. n.sp., Anguimorphe nouveau (Lacertilia) de l’Eocène inférieur de Dormaal, Belgique. Une relique éocène des Dorsetisauridae du Crétacé basal? CR Acad Sci, Paris 315(II):885–889Google Scholar
- Augé M (2003) Lacertilian faunal change across the Paleocene-Eocene boundary in Europe. In Wing SL, Gingerich PD, Schmitz B, Thomas E (eds), Causes and Consequences of globally warm climates in the Early Paleogene. Boulder, Colorado, Geol Soc Am Spec Paper 369:441–453Google Scholar
- Augé M (2005) Evolution des lézards du Paléogène en Europe. Mém Mus Natl Hist Nat Paris 192Google Scholar
- Augé M (2007) Past and present distribution of iguanid lizards. Arqu Museu Nac Rio de Janeiro 65(4):403–416Google Scholar
- Avery DF, Tanner W (1971) Evolution of the Iguanine lizards (Sauria, Iguanidae) as determined by osteological and myological characters. Brigh Young Univ Sci Bull 12:1–79Google Scholar
- Bailon S (2000) Amphibiens et reptiles du Pliocène terminal d’Ahl al Oughlam (Casablanca, Maroc). Geodiversitas 22(4):539–558Google Scholar
- Berman DS (1972) Hyporhina tertia, new species (Reptilia: Amphisbaenia), from the early Oligocene (Chadronian) white river formation of Wyoming. Ann Carn Mus 44:1–10Google Scholar
- BiochroM’97 (1997) Actes du Congrès BiochroM’97. In: Aguilar JP, Legendre S, Michaux J (eds) Mem Trav EPHE, Inst Montpellier 21Google Scholar
- Blain HA, Bailon S, Agusti J (2007) Anurans and squamate reptiles from the latest early Pleistocene of Almenara-Casablanca-3 (Castellón, East of Spain). Systematic, climatic and environmental considerations. Geodiversitas 29(2):269–295Google Scholar
- Böhme M (2007) Herpetofauna (Anura, Squamata) and paleoclimatic implications: preliminary results. In: Daxner-Höck G (ed) Oligocene vertebrates from the Valley of lakes (Central Mongolia): morphology, phylogenetic and stratigraphic implications. Ann Naturhist Mus Wien 108A:43–52Google Scholar
- Böhme M (2008) Ectothermic vertebrates (Teleostei, Allocaudata, Urodela, Anura, Testudines, Choristodera, Crocodylia, Squamata) from the Upper Oligocene of Oberleichtersbach (Northern Bavaria, Germany). Cour Forsch-Inst Senckenberg 260:161–183Google Scholar
- Brooks DR, McLennan DA (2002) The nature of diversity. University of Chicago Press, ChicagoGoogle Scholar
- Camp CL (1923) A classification of the lizards. Bull Am Mus Nat Hist 48:289–481Google Scholar
- Charig AJ, Gans C (1990) Two new amphisbaenians from the Lower Miocene of Kenia. Bull Br Mus Nat Hist (Geol) 46(1):19–36Google Scholar
- De Rochebrune A (1884) Faune ophiologique des Phosphorites du Quercy. Mém Soc Sci Nat Saône et Loire 5:149–164Google Scholar
- Delfino M (1997) Blanus from the early pleistocene of Southern Italy, another small tessera from a big mosaic. In: Böhme W, Bischoff W, Ziegler T (eds) Herpetologia Bonnensis II. Societas Europea Herpetologica, Bonn, pp 89–97Google Scholar
- Donadio OE (1982) Restos de anfisbenidos fósiles de Argentina (Squamata, Amphisbaenidae) del Pli- oceno y Pleistoceno de la provincia de Buenos Aires. Circ Inf Asoc Paleont Arg 10:10Google Scholar
- Erwin TL (1979) Thoughts on the evolutionary history of ground beetles: Hypotheses generated from comparative faunal analyses of lowland forest sites in temperate and tropical regions. In: Erwin TL, Ball GE, Whitehead DR (eds) Carabid beetles: Their evolution, natural history, and classification. Junk, The Hague, pp 539–592Google Scholar
- Erwin TL (1981) Taxon pulses, vicariance, and dispersal: An evolutionary synthesis illustrated by carabid beetles. In: Nelson G, Rosen DE (eds) Vicariance biogeography: A critique. Columbia University Press, New York, pp 371–391Google Scholar
- Estes R (1975) Lower vertebrates from the Fort Union formation, late Paleocene, Big Horn Basin, Wyoming. Herpetologica 31:365–385Google Scholar
- Estes R (1983) Sauria terrestria, Amphisbaenia. In: Kuhn O, Wellnhofer P (eds) Handbuch der Paläoherpetologie, Teil 10A, Gustav Fischer, pp 1–249Google Scholar
- Estes R, de Queiroz K, Gauthier J (1988) Phylogenetic relationships within Squamata. In: Estes R, Pregill G (eds) Phylogenetic relationships of the lizard Families. Stanford University Press, Stanford, pp 119–281Google Scholar
- Folie A (2006) Evolution des amphibiens et squamates de la transition Crétacé-Paléogène en Europe: les faunes du Maastrichtien du Bassin de Hateg (Roumanie) et du Paléocène du Bassin de Mons (Belgique). Dissertation, Université libre de BruxellesGoogle Scholar
- Gans C (1974) Biomechanics, an approach to vertebrate biology. Lippincott, PhiladelphiaGoogle Scholar
- Gans C (1990) Patterns in amphisbaenian biogeography: A preliminary analysis. In: Peters G, Hutterer R (eds) Vertebrates in the tropics. Museum Alexander Koenig, Bonn, pp 133–143Google Scholar
- Gaston K (2003) The structure and dynamics of geographic ranges. Oxford University Press, OxfordGoogle Scholar
- Gheerbrant E, Cappetta H, Feist M, Jaeger JJ, Sudre J, Vianey-Liaud M (1993) La succession des faunes de vertébrés d’âge paléocène supérieur et Eocène inférieur dans le Bassin d’Ouarzazate. Portée biostratigraphique et paléogéographique. Newslett Strati 28:33–55Google Scholar
- Gilmore CW (1928) Fossil lizards of North America. Mem Natl Acad Sci 22(3):1–201Google Scholar
- Gilmore CW (1942) Paleocene faunas of the polecat bench formation, Park County, Wyoming. part. II Lizards. Am Philos Soc Proc 85:159–167Google Scholar
- Gilmore CW (1943) Fossil lizards of Mongolia. Bull Am Mus Nat Hist 81:361–384Google Scholar
- Hartenberger JL (1987) Modalités des extinctions et apparitions chez les mammifères du Paléogène d’Europe. Mém Soc Géol Fr NS 150:133–143Google Scholar
- Hecht MK, Hoffstetter R (1962) Note préliminaire sur les Amphibiens et les Squamates du Landenien supérieur et du Tongrien de Belgique. Bull Inst R Soc Nat Belg 39:1–30Google Scholar
- Hedges SB, Vidal N (2009) Lizards, snakes and amphisbaenians (squamata). In: Hedges SB, Kumar S (eds) The timetree of life. Oxford University Press, Oxford, pp 383–389Google Scholar
- Hoffstetter R (1942) Sur la présence d’Amphisbaenidae dans les gisements tertiaires français. CR Sci Soc Geol Fr 3:24–25Google Scholar
- Hoffstetter R (1962) Revue des récentes acquisitions concernant l’histoire et la systématique des squamates. Problèmes actuels de Paléontologie (evolution des vertébrés). Coll Inter CNRS Paris 104:243–279Google Scholar
- Hoffstetter R (1967) Coup d’oeil sur les Sauriens (Lacertiliens) des couches de Purbeck (Jurassique supérieur d’Angleterre, Résumé d’un mémoire). Coll Inter CNRS 163:349–371Google Scholar
- Huelsenbeck JP, Rannala B (2000) Using stratigraphic information in phylogenetics. In: Wiens JJ (ed) Phylogenetic analysis of morphological data. Smithsonian Institution Press, Washington DC, pp 165–191Google Scholar
- Hunn CA, Upchurch P (2001) The importance of time/space in diagnosing the causality of phylogenetic events: towards a chronobiogeographical paradigm. Syst Biol 50:391–407Google Scholar
- Kritzinger CC (1946) The cranial anatomy and kinesis of the South African amphisbaenid Monopeltis capensis Smith. South Afr J Sci 42:175–204Google Scholar
- Kuhn O (1940) Die Placosauriden und Anguiden aus dem Mittleren Eozän des Geiseltales. Nov Act Acad Leopoldina-Carolinska 53(8):461–486Google Scholar
- Leduc P (1996) Caractéristiques évolutives des faunes d’Europe occidentale et d’Amérique du Nord au Paléogène. Dissertation, l’Université Paris VIGoogle Scholar
- Lieberman BS (2000) Paleobiogeography, using fossils to study global change, plate tectonics, and evolution. Topics in Geobiology, 16. Kluwer, NetherlandsGoogle Scholar
- Maschio GF, Prudente A, Mott T (2009) Water dispersal of Amphisbaena alba and Amphisbaena amazonica (Squamata: Amphisbaenia: Amphisbaenidae) in Brazilian Amazonia. Zoologia (2009)Google Scholar
- Milner AC, Milner AR, Estes R (1982) Amphibians and squamates from the Upper Eocene of Hordle Cliff, Hampshire, a preliminary report. Tert Res 4(1):149–154Google Scholar
- Milner AC, Milner AR, Evans SE (2000) Amphibians, reptiles and birds: a biogeographical review. In: Culver SJ, Rawson PF (eds) Biotic response to global change. Cambridge University Press, CambridgeGoogle Scholar
- Montero R, Gans C (1999) The head skeleton of Amphisbaena alba Linnaeus. Ann Carn Mus 68:15–80Google Scholar
- Morrone JJ (2009) Evolutionary biogeography, an integrative approach with case studies. Columbia University Press, New YorkGoogle Scholar
- Nelson G, Platnick NI (1981) Systematics and biogeography: Cladistics and vicariance. Columbia University Press, New YorkGoogle Scholar
- Nessov LA (1985) Rare bony fishes, terrestrial lizards and mammals from the lagoonal zone of the Littoral lowlands of the Cretaceous of the Kyzylkumy. Yearbook All-Union Palaeont Soc, Leningrad 28:199–219Google Scholar
- Nessov LA, Gao K (1993) Cretaceous lizards from the Kizylkum Desert, Uzbekhistan. J Vertebr Paleontol 13:51AGoogle Scholar
- Oelrich T (1956) The anatomy of the head of Ctenosaura pectinata (Iguanidae). Misc Publ Mus Zool, Uni Michigan 94:1–122Google Scholar
- Pianka ER, Vitt LJ (2003) Lizards, windows to the evolution of diversity. University of California Press, BerkeleyGoogle Scholar
- Rage JC (1976) Les squamates du Miocène de Béni Mellal, Maroc. Géol medit 3:57–70Google Scholar
- Rage JC (1978) Squamates. In: Geze B, Rage JC, Vergnaud-Grazzini C, de Broin F, Buffetaut E, Mourer-Chauviré C, Crochet JY, Sigé B, Sudre J, Rémy JA, Lange-Badré B, de Bonis L, Hartenberger JL, Vianey-Liaud M (eds) La Poche à Phosphate de Ste-Néboule (Lot) et sa faune de vertébrés du Ludien supérieur. Palaeovertebrata 8:167–326Google Scholar
- Rage JC (1999) Squamates (Reptilia) from the Upper Cretaceous of Laño (Basque Country, Spain). Estud Museo Cienc Natur Alava, 14 num espec 1:121–133Google Scholar
- Rage JC (2006) The lower vertebrates from the Eocene and Oligocene of the Phosphorites du Quercy (France): an overview. Strata série 1(13):161–173Google Scholar
- Rage JC, Augé M (1993) Squamates from the Cainozoic of the western part of Europe. A review. Rev Paléobiol 7:199–216Google Scholar
- Rocek Z (1984) Lizards (Reptilia: Sauria) from the lower Miocene locality Dolnice (Bohemia, Czechoslovakia). Rozp Ceskoslo Akad Rada matem prirod ved 94(1):1–69Google Scholar
- Rose KD (2011) Importance of Messel for interpreting Eocene Holarctic mammalian faunas. In: Lehmann T, Schaal SFK (eds) The world at the time of Messel: puzzles in the palaeobiology, palaeoenvironment, and the history of the early primates (22nd Int Senckenberg conf, conference volume). Senckenberg Gesellschaft für Naturforschung, Frankfurt am Main, pp 143–146Google Scholar
- Rusconi C (1937) La presencia de lagartijas en el piso Ensenadense. Bolet Paleont 9:6–7Google Scholar
- Schleich HH (1985) Neue Reptilienfunde aus dem Tertiär Deutschlands. 3. Erstnachweis von Doppelschleichen (Blanus antiquus sp. nov.) aus dem Mittelmiozän Süddeutschlands. Münch Geowiss Abh (A) 4:67–149Google Scholar
- Schleich HH (1988) Neue Reptilienfunde aus dem Tertiär Deutschlands 8. Palaeoblanus tobieni n. gen., n. sp.- neue Doppelschleichen aus dem Tertiär Deutschlands. Paläontol Z 62(1/2):95–105Google Scholar
- Schmidt-Kittler N (ed) (1987) European reference levels and correlation tables. Münch Geowiss Abh (A) 10:15–31Google Scholar
- Schopf TJ (1984) Climate is only half the story in the evolution of organisms through time. In: Brenchley P (ed) Fossils and climate. Wiley, New YorkGoogle Scholar
- Scotese CR (2004) Cenozoic and Mesozoic paleogeography: changing terrestrial biogeographic pathways. In: Lomolino MV, Heaney LR (eds) Frontiers of biogeography. Sinauer, SunderlandGoogle Scholar
- Señaris JC (1999) Aportes al conocimiento taxonômico y ecológico de Amphisbaena gracilis Strauch 1881 (Squamata: Amphisbaenidae) em Venezuela. Fundación La Salle Ciências Naturales 152:115–120Google Scholar
- Smith KT (2006) A diverse new assemblage of late eocene squamates (Reptilia) from the Chadron formation of North Dakota, U.S.A. Palaeont Electro 9(2):1–44Google Scholar
- Stocker MR, Kirk EC (2011) The Herpetofauna from the late Uintan of West Texas. In: Lehmann T, Schaal SFK (eds) The world at the time of Messel: Puzzles in the palaeobiology, palaeoenvironment, and the history of the early primates (22nd Int Senckenberg conf, conference volume). Senckenberg Gesellschaft für Naturforschung, Frankfurt am Main, pp 159–160Google Scholar
- Sullivan RM (1985) A new middle Paleocene (Torrejonian) rhineurid amphisbaenian, Plesiorhineura tsentasi new genus, new species, from the San Juan Basin, New Mexico. J Paleontol 59:1481–1485Google Scholar
- Sullivan RM, Holman JA (1996) Squamata. In: Prothero D, Emry R (eds) The terrestrial eocene-oligocene transition in North America. Cambridge University Press, Cambridge, pp 354–372Google Scholar
- Sullivan RM, Keller T, Habersetzer J (1999) Middle Eocene (Geiseltalian) anguid lizards from Geiseltal and Messel, Germany. I. Ophisauriscus quadrupes Kuhn 1940. Cour Forsch–Inst Senckenberg 216:97–129Google Scholar
- Van Dyck MC (1983) Etude de la faune herpétologique du “Montien” continental de Hainin (Hainaut, Belgique) et d’autres gisements paléogènes du Nord-Ouest de l’Europe. Thèse, Université Catholique de Louvain (Belgique), Faculté des Sciences, p 199Google Scholar
- Vanzolini PE (1951) Evolution, adaptation and distribution of the amphisbaenid lizards (Sauria: Amphisbaenidae). Thesis, Harvard UniversityGoogle Scholar
- Venczel M, Stiuca E (2008) Late middle Miocene amphibians and squamate reptiles from Taut, Romania. Geodiversitas 30(4):731–763Google Scholar
- Wiens JJ, Brandley MC, Reeder TW (2006) Why does a trait evolve multiple times within a clade? Repeated evolution of snakelike body form in squamate reptiles. Evolution 60(1):123–141Google Scholar
- Wu XC, Brinkman DB, Russell AP (1996) Sineoamphisbaena hexatabularis, an amphisbaenian (Diapsida: Squamata) from the Upper Cretaceous redbeds at Bayan Mandahu (Inner Mongolia, People’s Republic of China), and comments on the phylogenetic relationships of the Amphisbaenia. Can J Earth Sci 33:541–577CrossRefGoogle Scholar