Significance of association of Pteranodon and Cretoxyrhina

Ecological interactions between pterosaurs and other species are rarely represented in fossil specimens, despite vast increases in pterosaur specimen numbers in recent years (Witton, 2018). Data on diet from stomach contents is sparse, limited to a handful of taxa known to have eaten fish (e.g., Eudimorphodon—Wild, 1978, Pteranodon, Rhamphorhynchus—Wellnhofer, 1991). Coprolites are also scarce, with only one record for pterosaurs known to date (Hone et al., 2015). A number of animals are recorded as pterosaur consumers, including fish (e.g., Frey & Tischlinger, 2012), dinosaurs (e.g., Hone et al., 2012), Crocodyliformes (Vremir et al., 2013) and possibly plesiosaurs (Cicimurri & Everhart, 2001), although also see (Witton, 2018), but they remain very rare despite the good fossil records of these ‘consumer’ taxa. Thus, this additional potential record of a pterosaur-carnivore association is significant.

The taphonomic history and association of LACM 50926 is unknown so it is difficult to draw firm conclusions about the action that left the shark tooth in situ. However, we rule out abiotic association of the pterosaur and shark tooth for several reasons: (1) embedded Cretoxyrhina teeth and feeding traces are known from numerous Smoky Hill vertebrate fossils, and are widely interpreted as related to feeding behaviour (Shimada, 1997; Everhart, 2004; Everhart, 2005); (2) although isolated Cretoxyrhina teeth are common fossils in the Smoky Hill Chalk Member (Everhart, 2005), its teeth have not been reported in association with any Pteranodon fossils in the past, despite the large sample size of this pterosaur and the fact that other fish remains (e.g., vertebrae) are not uncommonly associated with their remains (Bennett, 2001; Hargrave, 2007); (3) the spatial relationship between the tooth and the vertebra is complex and intimate, and unlike that expected to have occurred by chance association in a low energy deposit such as the Niobrara Chalk. We thus prefer an interpretation of the tooth becoming associated with the vertebra though the biting action of a small Cretoxyrhina.

We were unable to find additional indications of bite traces on LACM 50926. There is a small and almost perfectly circular puncture on the neural arch of cervical four, behind the left prezygapophysis but this is most likely a preparation trace or damage derived from a previous museum mount. The damaged and missing neural spines of the cervical series may be linked to the shark bite, but other pterosaur fossils show that these elements are prone to damage and/or poor preservation, so other causes cannot be excluded.

Cretoxyrhina was a large (up to 7 m in length) and powerful carnivore, perhaps one of the top predators of the Smoky Hill Chalk fauna (Everhart, 2005). Shimada (1997) compared its likely ecological feeding guild to larger modern species of lamnid and carcharhinid sharks, and there is fossil evidence that it consumed a variety of large vertebrates including mosasaurs, plesiosaurs and large teleost fish (Shimada, 1997; Everhart, 2004; Everhart, 2005). LACM 50926 is the first palaeoecological link between this shark genus and a pterosaur however, this rarity perhaps reflecting the relatively delicate nature of pterosaur skeletons against the evident bite force of Cretoxyrhina. Extremely hollow bones such as those characterising most of the Pteranodon skeleton are especially prone to failure against buckling forces (Currey, 2002) and likely broke easily under strong bites from large predators.

Both Bennett (2001) and Hargrave (2007) have noted that Pteranodon may have been consumed destructively by large aquatic carnivores. Predator targeting of their relatively muscular torsos might explain why wing skeletons (which had considerably less soft-tissue, see Bennett, 2003) are the most common form of associated pterosaur fossil in the Smoky Hill Chalk Member. Articulated wings are also common in the Late Jurassic Solnhofen fauna where this may reflect decay and the loss of wings from floating pterosaur corpses (Beardmore, Lawlor & Hone, 2017), although this is not mutually exclusive with the effects of predation and scavenging. Witton (2018) noted that, to date, only the larger, more robust elements—limb bones and neck vertebrae—of larger pterosaur species are known to preserve embedded teeth and speculated that small pterosaurs and more gracile pterosaur bones were probably too easily destroyed to record evidence of carnivore bites. It may be that pterosaurs were not rare dietary components of Cretoxyrhina or other animals, but that their anatomy precludes common fossilisation of evidence for these acts.

Figure 4: Restored scene of Cretoxyrhina attacking Pteranodon. Life reconstruction of a c. 2.5 m long breaching Cretoxyrhina mantelli biting the neck of a 5 m wingspan Pteranodon longiceps, a scene inspired by LACM 50926. The predatory behaviour of this scene is speculative with respect to the data offered by the specimen, but reflects the fact that Cretoxyrhina is generally considered a predatory species, the vast weight advantage of the shark against the pterosaur (see text), and the juvenile impulse of the artist to draw an explosive predatory scene. Image credit: Mark Witton.

There is limited potential for knowing whether the LACM 50926 association reflects predatory or scavenging behaviour from Cretoxyrhina. Pteranodon is widely considered to have been a pelagic pterosaur species which foraged for small aquatic prey by means of dip-feeding, fishing from an alighted position on the water surface or diving after food (Wellnhofer, 1991; Bennett, 2001; Witton, 2013; Witton, 2018). Adaptations to aquatic launch (identified by Habib & Cunningham, 2010) are apparent in Pteranodon and suggest that it may have routinely entered (and thus needed to launch from) bodies of water. Thus, there are good reasons to think living Pteranodon could have been within reach of predatory sharks, and the likely pterodactyloid floating posture places their head and neck close to the waters’ surface (Hone & Henderson, 2014). Various modern seabirds are predated by pelagic predators, including sharks (Wetherbee, Cortés & Bizzarro, 2004; Johnson et al., 2006), and we cannot exclude this possibility for the LACM Pteranodon. Witton (2018) noted that even moderately-sized sharks, akin to the 2.5 m long Cretoxyrhina indicated by the LACM tooth, would vastly outweigh the largest Pteranodon (35–50 kg—see Paul, 2002; Witton, 2008; Henderson, 2010 for Pteranodon mass estimates), and we have little doubt that such predators could subdue these pterosaurs if they caught them (Fig. 4). Conversely, Pteranodon likely had a relatively low body density and their carcasses may have floated for sustained periods (Hone & Henderson, 2014). This would make them obvious targets for scavenging marine animals. Ultimately, LACM 50926 preserves no evidence to falsify any of these hypotheses.

Evidence of the anacoracid shark Squalicorax consuming Pteranodon is known in the Niobrara (e.g., KU 972 - KU, Kansas University, USA; YPM 2597, YPM 42810—SC Bennett, pers. comm., 2016), and recent finds of Mooreville Chalk Formation Pteranodon also have bite marks attributed to Squalicorax kaupi (RMM 3274 and ALMNH 8630) Ehret & Harrell Jr (2018). This body of evidence, augmented with the Cretoxyrhina-Pteranodon association described here, and the recovery of fish remains within the gular region of Pteranodon specimens (Brown, 1943; Bennett, 2001; Bennett, 2018) makes the trophic interactions of Pteranodon well understood compared to most other pterosaurs (Witton, 2018). However, such finds are still relatively rare occurrences—these seven associations are less than 1% of the >1,100 specimens of Pteranodon on record. In contrast, at least ten palaeoecologically significant fossil associations are known for the Late Jurassic Solnhofen pterosaur Rhamphorhynchus muensteri (including five associations with the carnivorous fish Aspidorhynchus acutirostris (e.g., Frey & Tischlinger, 2012) and four examples of consumed items (Witton, 2018). There are perhaps 150 specimens of Rhamphorhynchus in public collections, suggesting that recording of palaeoecological events is several times higher than in Pteranodon (>6%) despite a considerably smaller sample size. The taphonomic factors contributing to this difference may be worthy of further study.