Isolated teeth of Anhangueria  (Pterosauria: Pterodactyloidea) from the Lower Cretaceous of Lightning Ridge, New South Wales, Australia

Taxonomic identification

Elongate, conical teeth similar in morphology to those described above have been previously reported from Lightning Ridge, and include plesiosaurs (Kear, 2006b), ichthyosaurs (Kear, Boles & Smith, 2003), theropods (Bell et al., 2015) and crocodylians (Molnar, 1980). Other contemporaneous vertebrates that have been reported elsewhere from Australia that also bear similar teeth include pterosaurs (Molnar & Thulborn, 2007), teleost fish (Lees & Bartholomai, 1987; Berrell et al., 2014) and ichthyosaurs (Kear, Boles & Smith, 2003). The dental morphology of these groups is reviewed in brief below and compared with LRF 759 and 3142 to establish the basis for their assignment to Pterosauria.

Exclusion from Teleostei

The ichthyodectiform actinopterygians Cooyoo australis (Lees & Bartholomai, 1987) and Cladocyclus geddes (Berrell et al., 2014), both from the Albian of central Queensland have simple, conical and elongate teeth averaging only a few millimetres in height, with the dentary teeth of Cladocyclus also displaying a slight distal recurvature. The teeth are unornamented and do not bear any carinae on either the mesial or distal surfaces of the crown, unlike the condition in LRF 3142. The teeth of saurodontids have short, labiolingually-compressed triangular crowns and serrated carinae and have previously been mistaken for those of pterosaurs, particularly istiodactylids (e.g., Mkhitaryan & Averianov, 2011; Vullo, Buffetaut & Everhart, 2012). The Lightning Ridge teeth contrast strongly with those of saurodontids in their tall, elongate and slightly distally recurved crowns.

Exclusion from Plesiosauria

Plesiosaurs were ubiquitous in marine and marginal marine environments in Australia during the Lower Cretaceous (Kear, 2005a; Kear, 2005c; Kear, 2006b; Kear, 2006a). LRF 759 and LRF 3142 differ from previously described Australian plesiosaur teeth in the overall morphology of the tooth crown, development of carinae and enamel ornamentation. Plesiosaur teeth are typically elongate, lingually curved cones with a circular to ovoid basal cross-section. The mesial and distal surfaces of the crown lack carinae and have an apicobasally fluted enamel texture restricted to the lingual side of the crown, with flutes often bifurcating towards the base (Kear, 2005a, fig. 3f and 4b, Kear, 2005c; Kear, 2006b, figs. 2a–2g), although isolated teeth of Opallionectes lack any form of surface ornamentation (Kear, 2006a, text-fig. 2a).

Exclusion from Ichthyosauria

Only one valid species of ichthyosaur from Australia is presently recognised: Platypterygius longmani from the Albian Toolebuc Formation of central Queensland (Wade, 1990). P. longmani is known from an exceptionally preserved and articulated skull, complete with dentition. The teeth of P. longmani, and ichthyosaurs in general, differ from LRF 759 and LRF 3142 in the more robust and distally unrecurved crown with little or no labiolingual compression, a subcircular basal cross section and the presence of a fluted enamel texture that extends from near the tip of the crown down towards the base (Kear, 2005b, fig. 16).

Exclusion from Theropoda

The majority of unambiguous theropod remains from Australia have been referred to the recently diagnosed clade Megaraptora (Benson, Carrano & Brusatte, 2010). The dentition of megaraptorans is known in Australia from in situ and isolated teeth of the early Late Cretaceous Queensland theropod Australovenator wintonensis (Hocknull et al., 2009; White et al., 2015), as well as isolated teeth from the Aptian–Albian of the south coast of Victoria (Benson et al., 2012) and undescribed teeth from the Albian of Lightning Ridge (Smith, 1999; TB, ES & PB, pers. obs., 2016). These teeth are of the ziphodont type (sensu Hendrickx, Mateus & Araújo, 2015), that is strongly labiolingually-compressed, distally recurved and bearing denticulate distal carinae. Megaraptoran dentition is further characterised by pronounced labial and lingual depressions on the roots that extend onto the basal portion of the crown, such that the cross-section of the base of the crown has a ‘figure-eight’ shape (Novas, Ezcurra & Lecuona, 2008; Porfiri et al., 2014; White et al., 2015; Coria & Currie, 2016).

Teeth described as ‘conidont’ (sensu Hendrickx, Mateus & Araújo, 2015), similar to LRF 759 and LRF 3142, are present within theropods, most notably in spinosaurids. Spinosaurids are purportedly represented in Australia by a cervical vertebra from the Aptian–Albian Eumerella Formation (Barrett et al., 2011) but teeth are as yet unknown. The basal cross-section of baryonychine teeth is subcircular (e.g., Baryonyx; Charig & Milner, 1997) and differs from the oval basal cross-section typical of spinosaurine teeth (Richter, Mudroch & Buckley, 2012); however, in Spinosaurus, the shapes of the dentary alveoli transition from circular at the anterior end to more mesiodistally elongate and ovoid posteriorly (Stromer, 1915). Spinosaurid crowns often display a slight lingual curvature of the crown (Kellner & Mader, 1997; Richter, Mudroch & Buckley, 2012). Mesial and distal carinae in baryonychine teeth are ornamented by very fine serrations (e.g., Baryonyx, Suchomimus; Charig & Milner, 1997; Sereno et al., 1998) whereas the carinae of spinosaurines lack serrations entirely (e.g., Spinosaurus, Irritator; Stromer, 1915; Sues et al., 2002). The enamel of the crown in spinosaurid teeth appears granular and finely wrinkled with apicobasal fluting (see Hendrickx, Mateus & Araújo, 2015, fig. 4H, 6C–6D) that is usually more deeply impressed in baryonychines compared to spinosaurines (Stromer, 1915; Charig & Milner, 1997). However, baryonychine teeth have been reported with smooth enamel that is devoid of apicobasal flutes (Hone, Xu & Wang, 2010).

LRF 759 and LRF 3142 are distinct from megaraptorid teeth, and from ziphodont theropod teeth in general, in the oval basal cross-section of the crown, the slight degree of labiolingual compression of the crown, the apicobasal elongation of the crown, the lack of denticulated carinae and the absence of lingual or labial depressions at the base of the crown. LRF 759 and LRF 3142 are similar to spinosaurid teeth in their conical, elongate and slightly distally recurved crowns, and in the case of LRF 3142, the slight lingual curvature of the crown. However, they differ from the teeth of spinosaurines and baryonychines in lacking distinct fluting on either the labial or lingual surfaces. LRF 3142 has only very weak enamel ornamentation, but it is not certain if this is representative of the original enamel surface or a taphonomic artefact. The fine, discontinuous and irregularly-spaced longitudinal grooves of LRF 759 are unlike the enamel ornamentation of any known spinosaurid. In summary, the combination of features presented above for LRF 759 and LRF 3142 are inconsistent with spinosaurid dentition, and theropod dentition more broadly.

Exclusion from Crocodyliformes

Cretaceous crocodyliforms in Australia are rare and known only from an almost complete and articulated specimen of the neosuchian Isisfordia duncani from the upper Albian of central Queensland (Salisbury et al., 2006) and isolated skeletal material, including teeth, from Lightning Ridge (Etheridge, 1917; Molnar, 1980; Molnar & Willis, 2000). The teeth of Isisfordia are labiolingually compressed and distally unrecurved with distinct flutes extending along the crown (Salisbury et al., 2006, fig. 4F), whereas those from Lightning Ridge are conical and distally unrecurved with weak carinae (Molnar, 1980; Molnar & Willis, 2000).

The morphology of crocodyliform teeth, particularly those from the Mesozoic, displays considerable variation in terms of the degree of apicobasal elongation, mesiodistal curvature, acuteness of the apex, labiolingual compression, basal cross-sectional shape, presence and mode of development of carinae and denticles, and the presence and form of enamel ornamentation (Prasad & De Broin, 2002). In addition, many crocodyliform taxa display variation in tooth morphology along the premaxillary-maxillary and dentary tooth rows, while others retain a homodont dentition with variation, if any, only in the relative size of the tooth crowns. A homodont dentition of simple conical teeth appears in protosuchids, tethysuchians, paralligatorids, atoposaurids, and teleosaurs (e.g., Michard et al., 1990; Pol & Norell, 2004; Jouve, 2005; Young et al., 2014b; Tennant, Mannion & Upchurch, 2016). Thalattosuchian and some goniopholid teeth display a slight distal recurvature of the crown (e.g., Eutretauranosuchus, Machimosuchus; Smith et al., 2010; Young et al., 2014b). The remaining crocodyliform groups are heterodont to some degree. This may take the form of simple anterior-posterior morphological differentiation (e.g., Wannchampsus; Adams, 2014). More complex heterodonty occurs in notosuchians such as Notosuchus and Araripesuchus and the neosuchian Theriosuchus, in which at least three distinct tooth morphologies are present (Lecuona & Pol, 2008; Sereno & Larsson, 2009; Young et al., 2016).

Carinae are widely present on the dentition of crocodyliforms, with only a few exceptions (e.g., Eutretauranosuchus, Smith et al., 2010). Serrated carinae characterises the notosuchians, peirosaurids, Theriosuchus, paralligatorids, basal tethysuchians and thalattosuchians (e.g., Gasparini, Chiappe & Fernandez, 1991; De Lapparent De Broin, 2002; Schwarz & Salisbury, 2005; Sereno & Larsson, 2009; Andrade et al., 2010; Adams, 2014). Enamel ornamentation in crocodyliforms is typically in the form of flutes, and is present most notably in notosuchians, paralligatorids, goniopholids, Theriosuchus, basal eusuchians, tethysuchians and teleosaurids (e.g., Salisbury et al., 1999; Jouve, 2005; Schwarz & Salisbury, 2005; Delfino et al., 2008; Sereno & Larsson, 2009; Adams, 2014; Young et al., 2014b). In addition to or in place of flutes, fine anastomosing enamel textures are present in some tethysuchians, goniopholids and teleosaurs (e.g., De Lapparent De Broin, 2002; Andrade et al., 2011; Young et al., 2014a).

Some characteristics of crocodyliform teeth as reviewed above can be observed in LRF 759 and LRF 3142, such as the presence of unserrated carinae and slight labiolingual compression and distal recurvature of the crown. However, the confluence of the above characters is rarely present in any one crocodyliform taxon, and the comparatively smooth surface of LRF 3142 is unlike that seen in any of the aforementioned crocodyliform groups. Therefore, the possibility of crocodyliform affinities for LRF 759 and LRF 3142 is excluded here in favour of a group of terrestrial vertebrates whose teeth more closely match their distinct characteristics (see below).

Inclusion within Pterosauria

Australian pterosaur teeth are known only from in situ dentary and maxillary teeth of Mythunga camara (Molnar & Thulborn, 2007, fig. 2) and an isolated tooth associated with the rostral portion of an ornithocheiroid mandible (Fletcher & Salisbury, 2010, figs. 3I–3J), both from the Lower Cretaceous of central Queensland. All teeth have elongated conical crowns with heights averaging approximately 20 mm and an oval basal cross-section. The teeth of Mythunga camara are slightly distally recurved and bear an enamel ornamentation of irregularly-spaced longitudinal grooves on the basal two thirds of the crown. The single tooth described by Fletcher & Salisbury (2010) is devoid of any enamel ornamentation.

Pterosaur teeth are infrequently preserved with cranial material and readily dislodge from the alveoli post mortem. Isolated teeth are more common, but comprise a relatively small proportion of the terrestrial vertebrate fossil record during the Mesozoic. The overwhelming majority of pre-Cretaceous pterosaurs had toothed jaws, but during the Cretaceous a number of pterosaur lineages independently lost dentition either partially or completely. Among these clades are the nyctosaurids, pteranodontids, chaoyangopterids, tapejarids and azhdarchids, and as such they cannot be considered as candidates for the Lightning Ridge teeth.

Ctenochasmatidae is the only clade of archaeopterodactyloids to have survived into the Cretaceous. The dentition of ctenochasmatids consists of a large number of recurved, elongated, needle-like teeth in both the upper and lower jaws (e.g., Huanhepterus, Gegepterus, Moganopterus; Dong, 1982; Wang et al., 2007; Lü et al., 2012). This dental morphology is taken to an extreme by Pterodaustro in which approximately 1,000 bristle-like teeth lined the jaws (Chiappe & Chinsamy, 1996). Among ornithocheiroids, istiodactylids have ‘lancet-shaped’, or triangular, labiolingually-compressed crowns (Witton, 2012). Carinae may either be present mesially and/or distally (e.g., Nurhachius, Istiodactylus sinensis; Wang et al., 2005; Andres & Ji, 2006) or absent entirely (e.g., Hongshanopterus, Wang et al., 2008). Dsungaripterids are the only azhdarchoid pterosaurs that are not edentulous. Dsungaripterid dentition consists of apicobasally-short crowns with obtusely-pointed apices, restricted to the posterior part of the upper and lower jaws (Young, 1964; Unwin, 2003).

The teeth of anhanguerians (Rodrigues & Kellner, 2013) are typically slightly labiolingually-compressed with an elliptical basal cross section. The posterior dentition in some taxa is characterised by low, labiolingually triangular crowns (e.g., Cearadactylus atrox, Guidraco venator; Wang et al., 2012; Vila Nova et al., 2014). The crowns are slender and elongate, though not to the extent seen in ctenochasmatids. A slight distal recurvature of the crown is common to most anhanguerians (e.g., Anhanguera araripensis, A. piscator, Siroccopteryx, Ludodactylus; Wellnhofer, 1985; Mader & Kellner, 1999; Kellner & Tomida, 2000; Frey, Martill & Buchy, 2003) although in some taxa the crowns are recurved only apically or not at all (e.g., Cearadactylus atrox; Vila Nova et al., 2014). A slight lingual curvature is also present in some anhanguerian teeth (e.g., Wellnhofer & Buffetaut, 1999; Averianov, 2007) but can become very strong as in the posterior dentition of A. araripensis in which the apices can point directly lingually (Wellnhofer, 1985, fig. 7). Both mesial and distal carinae are present in some taxa (e.g., A. santanae; Wellnhofer, 1985) but are absent in others (e.g., A. robustus, Siroccopteryx; Wellnhofer, 1987; Wellnhofer & Buffetaut, 1999). The enamel on the crowns is typically ornamented by longitudinal grooves (e.g., A. robustus, A. piscator, Mythunga, Guidraco; Wellnhofer, 1987; Kellner & Tomida, 2000; Molnar & Thulborn, 2007; Wang et al., 2012). The teeth of A. araripensis appear to lack any longitudinal grooves (Wellnhofer, 1985); however, only the posterior dentition of this taxon is currently known and it is possible that its anterior teeth were similar to those of its congenerics.

LRF 759 and LRF 3142 bear little resemblance to the needle-like dentition of ctenochasmatids, the ‘lancet-like’ dentition of istiodactylids, or the blunt triangular dentition of dsungaripterids. However, a comparison of anhanguerian dentition to the Lightning Ridge teeth demonstrates a compelling similarity. The teeth of the probable anhanguerian Mythunga camara are similar in size and shape to the Lightning Ridge teeth, and in the case of LRF 759 have a similar enamel ornamentation of discontinuous longitudinal grooves (Molnar & Thulborn, 2007). The longitudinal grooves on the crown of LRF 759 are not as deeply impressed as in some species of Anhanguera (e.g., A. robustus, A. piscator; Wellnhofer, 1987; Kellner & Tomida, 2000) and are more similar to those described from other anhanguerians (e.g., Guidraco; Wang et al., 2012). The small degree of lingual curvature of the crowns is also observed in the anterior dentition of some species of Anhanguera (e.g., A. araripensis, A. santanae; Wellnhofer, 1985).

Isolated anhanguerian-like teeth described as Morphotype III from Morocco (Wellnhofer & Buffetaut, 1999, fig. 8), Morphotype 3 from Spain (Sánchez-Hernández, Benton & Naish, 2007, fig. 5) and ZIN PH no. 41/43 of Averianov (2007, figs. 1d–1f) share with LRF 3142 elongate and slightly labiolingually-compressed crowns with an oval basal cross-section, very slight distal recurvature, and unserrated carinae on both mesial and distal edges. Pterosaur teeth recovered from the middle Cretaceous Alcântara Formation and the Lower Cretaceous Recôncavo Basin, both in Brazil (Elias, Bertini & Medeiros, 2007; Rodrigues & Kellner, 2010), are morphologically similar in comparison to LRF 3142 with the exception of the absence of carinae. The distribution and phylogenetic significance of carinae in pterosaur dentition has yet to be examined in detail (Rodrigues & Kellner, 2010). It is uncertain whether the absence of characteristic pterosaurian surface ornamentation in LRF 3142 is genuine or a result of taphonomic processes. However, isolated pterosaur teeth without observable longitudinal grooves have been documented (e.g., Rodrigues & Kellner, 2010, fig. 3). Previously reported isolated anhanguerian-like teeth appear to be much longer than either LRF 759 or LRF 3142 (e.g., Wellnhofer & Buffetaut, 1999; Averianov, 2007). The morphology of both teeth appears to indicate that they were positioned towards the anterior end of their respective tooth rows, where the crowns are longer and more elongate in comparison to the more posterior crowns. However, the apical ends of both teeth are eroded, and the gentle degree of curvature of the mesial and distal margins in lateral perspective indicates that the apices would have been much longer prior to their taphonomic loss. Furthermore, the teeth are of a similar length to those preserved in the jaws of Mythunga camara (Molnar & Thulborn, 2007, figs. 2, 4).

Despite recent revisions of taxa and specimens that have historically been referred to Ornithocheirus and closely-related taxa (Unwin, 2001; Rodrigues & Kellner, 2008; Rodrigues & Kellner, 2013), many ‘ornithocheirids’ are still known from only partial and fragmentary remains and which lack diagnostic cranial material, including teeth. The continuing uncertainly surrounding the affinities of these remains hinders a comprehensive assessment of anhanguerian phylogeny, and in lieu of such assessments the isolated teeth cannot presently be referred to a clade less inclusive than Anhangueria.

Significance for Australian pterosaur diversity

This account represents the first description of pterosaur material from New South Wales, and permits the recognition of a new occurrence of this group of otherwise rare and poorly-known reptiles in Australia. Two pteranodontoid pterosaur taxa are currently recognised in Australia: Mythunga camara (QM F18896); and Aussiedraco molnari (QM F10613), both from the Lower Cretaceous of central Queensland. The jaw fragment WAM 68.5.11 (Kear, Deacon & Siverson, 2010) and partial mandible QM F44423 (Fletcher & Salisbury, 2010) possibly represent distinct ornithocheiroid taxa—the former based on its temporal separation from the aforementioned Queensland taxa and the latter from the distinct morphology of the mandibular symphysis (Kellner, Rodrigues & Costa, 2011). In addition, the azhdarchid ulna (WAM 60.57) from the Late Maastrichtian of Western Australia (Bennett & Long, 1991), and the ctenochasmatoid humeral fragment (QM F42739) (Fletcher & Salisbury, 2010) most likely represent distinct Australian pterosaur taxa. The remainder of the partial pterosaur material from Queensland and Western Australia may pertain to one or more of the aforementioned Early Cretaceous pterosaur taxa, or may represent new taxa that cannot be confidently identified. Thus it would seem reasonable to assume that at least six pterosaur taxa were present in Australia during the Cretaceous.

Although dentition may be diagnostic for particular pterosaur clades (see above), in the absence of articulated or associated skeletal material they typically are insufficient for identification of the tooth-bearer to a specific or generic level. In Australia, this problem is exacerbated by the scarcity of pterosaur remains to which the teeth described here can be compared. It is currently not possible to determine with certainty whether the Lightning Ridge teeth belong to one of the named or unnamed but potential Australian pterosaur taxa, or whether they constituted the dentition of a taxon that is yet to be discovered. Furthermore, given the subtle observed morphological differences between the two teeth (e.g., degree of recurvature, presence of carinae, enamel ornamentation, etc.) it is also uncertain whether the two teeth are derived from a single taxon or separate taxa. Further finds are needed in order to evaluate whether these differences are indicative of the presence of more than one pterosaur taxon, or whether taphonomic or other processes have affected the appearance of the tooth crowns.

The identification of anhanguerian teeth from the Griman Creek Formation is consistent with the reports of anhanguerid-like and ‘ornithocheirid’ skeletal material from the Early Cretaceous of Queensland (Molnar & Thulborn, 1980; Molnar & Thulborn, 2007; Fletcher & Salisbury, 2010) and the cosmopolitan distribution of ornithocheiroids at this time (Upchurch et al., 2015). The similarities in morphology are further supported by the similarities in palaeoenvironments. The Queensland pterosaur material from the Toolebuc and Mackunda formations of the Eromanga Basin were deposited in shallow waters near the central part of the Eromanga Sea during the early to middle Albian (Fletcher & Salisbury, 2010). Similar conditions prevailed during the middle Albian in the vicinity of present day Lightning Ridge. The occurrence of anhanguerid-like pterosaurs in near-shore and shallow water environments in Australia appears to correlate with the presumed diet of fish and other aquatic organisms that has been inferred for some anhanguerids (Kellner & Tomida, 2000), and which is evident from the slender, elongate and apically acute tooth crowns.