Abstract The largest reported ichthyosaurs lived during the Late Triassic (~235–200 million years ago), and isolated, fragmentary bones could be easily mistaken for those of dinosaurs because of their size. We report the discovery of an isolated bone from the lower jaw of a giant ichthyosaur from the latest Triassic of Lilstock, Somerset, UK. It documents that giant ichthyosaurs persisted well into the Rhaetian Stage, and close to the time of the Late Triassic extinction event. This specimen has prompted the reinterpretation of several large, roughly cylindrical bones from the latest Triassic (Rhaetian Stage) Westbury Mudstone Formation from Aust Cliff, Gloucestershire, UK. We argue here that the Aust bones, previously identified as those of dinosaurs or large terrestrial archosaurs, are jaw fragments from giant ichthyosaurs. The Lilstock and Aust specimens might represent the largest ichthyosaurs currently known.

Citation: Lomax DR, De la Salle P, Massare JA, Gallois R (2018) A giant Late Triassic ichthyosaur from the UK and a reinterpretation of the Aust Cliff ‘dinosaurian’ bones. PLoS ONE 13(4): e0194742. https://doi.org/10.1371/journal.pone.0194742 Editor: William Oki Wong, Indiana University Bloomington, UNITED STATES Received: November 21, 2017; Accepted: March 8, 2018; Published: April 9, 2018 This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication. Data Availability: All relevant data are within the paper. Additional data have been uploaded to figshare and are accessible using the following DOI: 10.6084/m9.figshare.5975440. Funding: The authors received no funding for this work. Competing interests: Author affiliations of Gallois Geological Consultancy and the Etches Collection do not alter our adherence to PLOS ONE policies on sharing data and materials.

Introduction Ichthyosaurs were major components of Mesozoic marine ecosystems from the Early Triassic (Olenekian) until their extinction in the early Late Cretaceous (Cenomanian). Their wide geographic range in the Early Triassic suggests a very early Triassic radiation for the clade [1]. They reached their maximum disparity in feeding type, locomotory styles, and especially body size (1 m to >20 m) in the Late Triassic [1–3]. A major reduction in the morphospace occupied by ichthyosaurs occurred from the Late Triassic into the Early Jurassic [3,4]. A reduction in taxonomic diversity also occurred within that interval, with only the parvipelvian ichthyosaurs surviving into the Early Jurassic [4,5; but see 6]. Thus the latest Triassic-earliest Jurassic was a critical interval in the evolution of ichthyosaurs. The largest ichthyosaurs of the Late Triassic were the shastasaurids (Family Shastasauridae), which ranged in size from about 6 m to more than 20 m [5,7]. Shastasauridae, as defined by Ji et al [5], includes six genera of large, long-bodied forms (precaudal centra count >55): Shastasaurus, Besanosaurus, Guanlingsaurus, Guizhouichthyosaurus, Shonisaurus, and ‘Callawayia’ wolonggangensis. Himalayasaurus was tentatively referred to the Shastasauridae [8,9], but the genus has not been included in recent phylogenies [e.g., 5,10,11], so its affinities are unresolved. Shastasaurids appeared in the Ladinian (Middle Triassic) and persisted to at least the Rhaetian (Late Triassic), with their highest taxonomic diversity occurring in the Carnian (early Late Triassic) [5, 12]. The shastasaurids might even have survived into the early Jurassic [6], although this has been questioned [13]. The last of the shastasaurid taxa that can be assigned to genera are Shonisaurus sikanniensis, and, probably Himalayasaurus tibetensis, both of which occurred in the Norian (middle to late Late Triassic). The former species is the largest ichthyosaur previously known, with an estimated total length of 21 m [7]. No specimen that can be assigned to a genus is known from the Rhaetian (latest Triassic), but shastasaurids have been reported from France [12]. In addition, large ichthyosaur bones from the Rhaetian of the UK [14] could possibly be shastasaurids, based on their size. This work reports the discovery of a large, isolated jaw fragment of a giant ichthyosaur from the UK, which estimates suggest was even larger than S. sikanniensis. Some ichthyosaurs were as large or larger than contemporaneous Late Triassic dinosaurs. Isolated bone fragments of giant ichthyosaurs could easily be mistaken for those of dinosaurs because of their size. For that reason, this discovery has prompted a reinterpretation of the ‘dinosaur bone shafts’ [15,16] from the historic Aust Cliff site in southwestern UK.

Material Institutional abbreviations BRSMG, Bristol Museum and Art Gallery, UK; BRSUG, University of Bristol, UK; TMP, The Royal Tyrrell Museum of Palaeontology, Alberta, Canada; NSMLV, Nevada State Museum, Las Vegas, USA. Material examined in this study The new specimen reported herein, BRSMG Cg2488, is a portion of an ichthyosaurian surangular from the Westbury Mudstone Formation of Lilstock, Somerset, UK. BRSMG Cb3869, BRSMG Cb3870 and BRSMG Cb4063, identified herein as ichthyosaurian, are from the Westbury Mudstone Formation of Aust Cliff, Gloucestershire, UK, as is BRSUG 7007, an isolated vertebra (20 cm diameter) of a very large ichthyosaur. TMP 1994.378.02, the holotype of Shonisaurus sikanniensis, is from the Upper Triassic (Norian) Pardonet Formation of northeastern British Columbia, Canada. Measurements were taken with digital callipers and a tape measure, and recorded to the nearest 1 mm.

The Cuers ichthyosaur A very large ‘fused mandible’ of an ichthyosaur has been reported from the Late Triassic (Rhaetian) of France [12]. The fusion of a mandible is a unique condition among ichthyosaurs of any age. Even the very large shastasaurids, Shonisaurus sikanniensis ([7]; DRL, JAM pers. obs.) and S. popularis [22] have sutures in the mandible. A second unique feature of the Cuers specimen is what was identified as a narrow dental groove on the medial surface of the ‘mandible’ [12]. We argue that the Cuers specimen is not a jaw in which all of the bones are fused, but it is a single bone, another very large surangular. The overall shape is similar to the Lilstock specimen [12: fig 2]. The posterior end is markedly curved and dorsoventrally tall. No coronoid process can be confidently identified in the Cuers specimen, due to poor preservation, but the posterior end is high and it decreases fairly abruptly anteriorly, similar to the Lilstock specimen. The position of the groove on the medial surface and its extent along the bone in the Cuers specimen is also very similar to the groove for the Meckelian canal in the Lilstock specimen. The purported presence of a dental groove on the medial side of the mandible is not found in any other ichthyosaur, as noted by Fischer et al. [12], whereas the groove for the Meckelian canal has been reported on the medial surface in many ichthyosaurs (e.g. [24,28,29]). In the Cuers specimen, the aligned foramina on the lateral surface were identified as part of the fossa dentalis [12], but they are similar to the foramina on the lateral surface of the Lilstock specimen and could be part of the fossa surangularis. Thus, the bone morphology of the Cuers specimen is consistent with that of a surangular and does not require calling on an unusual morphology for the specimen. Fischer et al. [12] also provided a redescription of Ichthyosaurus carinatus [30], also from the French Rhaetian, which included another large mandible fragment, identified as a portion of dentary. They concluded that the morphology was similar to that of the Cuers specimen in having a continuous dental groove on the medial surface, but noted that the groove appeared much deeper in this specimen. The cross-section is also similar to the Lilstock specimen, especially with respect to a prominent ridge (wall), ventral to the groove [12: supp. S5 fig]. Although this specimen is not as complete as the Cuers ichthyosaur, we suspect that this is probably also a portion of a surangular, and the medial groove is the groove for the Meckelian canal, not the dental groove. Fischer et al. [12] argued that the Cuers specimen and the remains of ‘Ichthyosaurus carinatus’ should be regarded as Aff. Shastasauridae, although they could not be identified more precisely. The geological age and giant size of the Lilstock specimen also suggests possible shastasaurid affinities. Overall, the shape of the Lilstock and Cuers surangulars are more similar to S. sikanniensis than to S. popularis, especially in the posterior portion.

Implications for the Aust Cliff ‘Bone Shafts’ Five large ‘limb bone shafts’ were collected from the Upper Triassic ‘Rhaetic Bone Bed’, at or close to the base of the Westbury Mudstone Formation at Aust Cliff, Gloucestershire (Fig 1), although two of the specimens were presumed destroyed in the 1940 bombing of Bristol [14,15,16]. A detailed account of their history has been provided elsewhere [15]. The first described specimen, which is now missing, was originally referred to the Labyrinthodontia [15,31]. This bone, along with two other specimens, was later identified as dinosaurian [15,32]. Recent work has suggested that one or more of the three surviving Aust bones are from stegosaurian dinosaurs [15], sauropod dinosaurs [15,33] (although this has been challenged [34]), indeterminate dinosaurs [14,15,16,35], archosaurian (pseudosuchian) reptiles [16] or indeterminate reptiles [36,37]. The surviving Aust bones have been illustrated elsewhere [15]. Large bones belonging to the sauropodomorph dinosaur Camelotia borealis are known from the Westbury Mudstone Formation of Somerset [15,38,39], thus the previous identifications of the Aust bones were consistent with those finds. In each interpretation, other than perhaps the very first description [31], the Aust bones were thought to be from a large terrestrial reptile, although one study noted that the bone microstructure was unusual [16]. This study identifies the Aust bones as ichthyosaurian because of similarities to the Lilstock specimen. The ‘unusual foramen’ on one of the Aust specimens (BRSMG Cb3869) identified as the nutrient foramen by Galton [15] is similar in morphology and extent to the fossa surangularis of the Lilstock specimen (e.g. see Fig 8). However, similar grooves and series of foramina are also found in the premaxilla (fossa praemaxillaris) and the dentary (fossa dentalis) of several ichthyosaurs (e.g. [23,26, 40]). Galton [15] pointed out that a foramen is rarely preserved in the femoral shaft of sauropodomorphs. It is difficult to determine whether this specimen (BRSMG Cb3869) is a portion of surangular, dentary or premaxilla, although the cross-sectional shape of the specimen would suggest it is unlikely to be the latter. Unfortunately, the medial surface is crushed, damaged and partly eroded and thus a groove cannot be identified. The cylindrical shape of BRSMG Cb3869 [15: fig 4F and 4G] is comparable to the third or fourth anterior segment of the Lilstock surangular (Fig 5). Another Aust specimen (BRSMG Cb3870), considered the same species as the aforementioned specimen based on bone microstructure [16], lacks any identifiable foramina, but it has suffered significant surface erosion. It and the remaining Aust specimen (BRSMG Cb4063) could be portions of a surangular, another bone from the jaw, or possibly a ceratobranchial (hyoid). The latter is very long and robust in S. sikanniensis (120 cm long, with a max diameter of 11 cm [7]). Very large ichthyosaurian vertebrae (e.g., BRSUG 7007, 20 cm diameter) from Aust Cliff have been previously reported [14], so the presence of giant ichthyosaurs at this location has already been confirmed. By comparison, the size of BRSUG 7007 is within the range of centrum size of S. popularis and S. sikanniensis, although some of those reached diameters of 25 cm or more [7: Appendix 1; 22: tables 1–4; 41]. PPT PowerPoint slide

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larger image TIFF original image Download: Fig 8. Comparison of a portion of the Lilstock specimen to an Aust specimen. A. Anterior-most preserved portion of the Lilstock ichthyosaur surangular (BRSMG Cg2488), showing an elongated foramen on the lateral surface, part of the fossa surangularis. B. BRSMG Cb3869, the largest Aust specimen, displaying a similar foramen, interpreted here as most likely part of the fossa surangularis. Scales equal 5 cm. https://doi.org/10.1371/journal.pone.0194742.g008 The posterior segments of the Lilstock specimen preserve a good view of the bone microstructure on the cross-sections (Fig 6A). An irregular vacuity is slightly offset from the centre. The rest of the interior bone is filled with thin trabeculae surrounding large, frequently elongated, vacuities. This texture grades outward into somewhat denser spongy bone with smaller, irregular vacuities (Fig 6B). Another gradual transition leads to the outer cortical bone, which has even smaller vacuities (Haversian canals) that are frequently aligned roughly parallel to the outer bone surface and might define growth lines (Fig 6C). The outer cortical bone layer is relatively thin, 0.8–1.3 cm on the lateral side, for a cross-section width of at least 8.5 cm (measured on the second segment from the posterior end), although the boundary with the spongy bone is not well defined. The more or less concentric pattern of the changes in microstructure suggest that there has not been fusion of two or more bones. The microstructure of the Aust bones is similar to that of the Lilstock ichthyosaur in the large region of spongy bone that grades into a relatively thin, outer layer of cortical bone [16]. Both have longitudinally oriented vascular canals, although the canals are more numerous in the Lilstock ichthyosaur. Both the Lilstock specimen and the Aust bones have abundant vacuities in their bones, resulting in a less dense bone that is more typical of aquatic tetrapods than terrestrial ones [42,43]. The details of the microstructure are beyond the scope of the paper. In any case, it is likely that different taxa of ichthyosaurs will differ in their bone microstructure, as is the case for mosasaurs, marine squamates of the Cretaceous [42]. The unusual microstructure of the Aust bones was interpreted as an indication that the animal was still growing, possibly a mechanism to attain a large size [16]. A similar mechanism was suggested for mosasaurs [43]. Mosasaurs retained characteristics of juvenile bone, indicating paedomorphosis, a mechanism that could have allowed mosasaurs to continue juvenile growth rates after sexual maturity and reach much larger sizes than terrestrial squamates [43]. Such mechanisms could also explain the giant size of ichthyosaurs.

Size estimation Determining the size of an extinct animal, especially if it is known from isolated or poorly preserved remains, is a challenge. Large shastasaurid ichthyosaurs can provide a rough estimate for the total length of the Lilstock ichthyosaur by using a simple scaling factor. Such estimates, however, are not entirely realistic because of differences among taxa in bone morphology and overall body proportions, as well as effects of individual variation and allometric growth [44]. Nonetheless, simple scaling is commonly used to estimate size, especially when comparative material is scarce (e.g., [45,46]). The largest shastasaurid, Shonisaurus sikanniensis has an estimated length of up to 21 m, based on length estimates of the specimen in situ [7]. The only specimen of the species (TMP 1994.378.02) preserves portions of the surangular, which has a maximum height at the posterior end of 19 cm ([7]; DRL, JAM pers. obs.). The maximum height of the posterior end of the surangular in the Lilstock specimen is at least 24 cm, ~25% larger than that. Simple scaling would suggest that the Lilstock ichthyosaur has an estimated total length of up to 26 m, approaching the size of a blue whale. A smaller shastasaurid, Besanosaurus leptorhynchus has an estimated total length of 5.4 m [47]. Measurements of a drawing of the skull [47: fig 9] gives an estimate for the height of the surangular exposure as 4.5–4.7 cm at the coronoid process. The height of the Lilstock surangular at the coronoid process is 19 cm, suggesting that the Lilstock ichthyosaur is about four times larger than Besanosaurus, with a total length estimate of about 22 m. It is difficult to provide an estimate for the skull length of the Lilstock specimen because the skull length of S. sikanniensis is itself an estimate, and relative skull length varies among shastasaurid taxa [22,47]. Furthermore, there are clear differences in snout length in shastasaurids, some with long snouts (e.g. Shonisaurus popularis [22], Besanosaurus [47]), and others with short snouts (Guanlingsaurus liangae [10,48]). The same method has its limitations, but a comparison can be made to the Aust specimen (BRSMG Cb3869) that might be a portion of surangular. The maximum cross-sectional dimension of the Aust fragment is 13.8 cm ([15]; DRL, PDLS pers. obs.), which is similar in cross-sectional shape to a portion of the Lilstock surangular anterior to the coronoid, where the bone is roughly cylindrical. That region of the Lilstock specimen has a dorsoventral height of 10.6–9.2 cm, suggesting that the Aust ichthyosaur was a much larger animal, perhaps more than 30% larger. If the Aust specimen is a portion of the dentary or premaxilla, then the ichthyosaur was probably even larger. Of course, considering that the Lilstock and Aust bones represent only portions of the lower jaw, these estimates are very speculative. Nevertheless, it is reasonable to suggest that the Lilstock ichthyosaur was on the order of 20–25 m long. Previously, the largest ichthyosaur from the UK was estimated as about 15 m, based on isolated elements of an unnamed ichthyosaur from the Early Jurassic [49]. Even accounting for the limitations in the size estimates, the Lilstock and Aust ichthyosaurs were much larger.

Conclusion The discovery of a large ichthyosaur surangular from the Upper Triassic of England has documented that giant ichthyosaurs persisted well into the Rhaetian Stage. The Upper Triassic also records the appearance of the more advanced parvipelvian ichthyosaurs [50–52]. The Lilstock specimen confirms that giant shastasaurid-like ichthyosaurs overlapped temporally (before and possibly after the Late Triassic extinction) with the early parvipelvian ichthyosaurs [12]. A large, shastasaurid-like radius from Penarth has been reported from the lowest Jurassic [6] (Fig 3), indicating that the shastasaurids might have survived the Late Triassic extinction. However, the specimen was found loose on the beach and the stratigraphy of the specimen is not well constrained. It is possible that the specimen is actually from the Westbury Mudstone Formation [13], which would be more consistent with the occurrences of the Lilstock and Aust specimens. The Lilstock surangular has also clarified the affinities of the historically important Aust Cliff ‘dinosaurian bone shafts’. They are portions of giant ichthyosaurs and are not an example of an early experiment in gigantism in archosaurian reptiles as previously suggested [16]. Size estimates suggest that the Lilstock and Aust ichthyosaurs are the largest ichthyosaurs presently known.

Acknowledgments We thank D. Hutchinson and I. Gladstone (BRSMG), C. Hildebrandt (BRSUG), and B. Strilisky, T. Courtenay and D. Henderson (TMP) for access to and assistance with specimens in collections at their institutions. We are grateful to S. Underwood and V. Lucas (NSMLV) for providing images of the surangular of S. popularis, and to N. Hanigan for providing images of specimens from Berlin Ichthyosaur State Park, Nevada. Thanks also to S. Dey (ThinkSee3D) for creating the photogrammetry model in the supplementary data. Our work benefitted from discussions with W. Wahl, M. Maisch, B. Moon, and A. Sheldon. Finally, we thank V. Fischer, J. Martin, and an anonymous reviewer for their helpful suggestions, but any errors are our own.