Palaeodietary Implications

Ankylosauria. The inferred ankylosaur ecomorph is characterized by a small, proportionally wide skull, with a relatively deep mandible and short tooth row. The snout is ventrally deflected, but not as strongly as in hadrosaurids. First-hand examination of ankylosaur specimens reveals that the depth of the mandible is exaggerated by the dorsal bowing of the tooth row (Figure 2A). Ankylosaurs are not strongly distinguished from either ceratopsids or hadrosaurids based on the distance between the jaw joint and coronoid process apex. This is somewhat surprising because both ceratopsids and hadrosaurids possess elevated coronoid processes and depressed jaw joints that are otherwise not developed to the same degree in ankylosaurs [84]–[86]. It may be that the ankylosaur coronoid apex is more rostrally displaced than in ceratopsids and hadrosaurids, resulting in subequal measurements of this variable. Further work illuminating the differences in jaw mechanics between these taxa is in progress. Because jaw adductor muscle mass–and by extension, bite force–generally scales positively with skull size (e.g., [87]–[91]), it is likely that ankylosaurs possessed a weaker bite than the larger ceratopsids and hadrosaurids. Likewise, the rostral placement of the tooth row relative to the coronoid process in ankylosaurs means that they did not possess as powerful a bite as the other two taxa, in which the tooth row extends caudal to the coronoid process, resulting in increased leverage of the distal tooth row [84]–[86]. Other evidence cited in favour of a relatively weak bite in ankylosaurs is the presence of small, phyliform teeth with peg-like roots [92]–[94], and simple jaw musculature [95]. Nonetheless, the ankylosaur skull exhibits other features thought to correlate with either high bite forces or repetitive masticatory movements–both adaptations for comminuting resistant plant matter. For example, the proportionally great transverse breadth of the skull may have accommodated larger jaw adductor muscles. This explanation was offered by Herrel et al. [96] to account for the fact that finches with relatively wide skulls also possess the highest bite forces. Henderson [44] likewise used beam theory to show that wider skulls are able to resist high torsional stresses incurred by elevated bite forces. Furthermore, the curved tooth row of ankylosaurs is reminiscent of that of grazing macropodoids, the function of which Sanson [97] surmised was to concentrate bite forces in response to a tough diet. The secondary increase in the depth of the mandible likewise would have served to withstand repeated bending forces associated with mastication, preventing bone fatigue [98], [99]. Finally, Vickaryous et al. [100] cited the presence of an ossified secondary palate in ankylosaurs as evidence that their skulls were adapted to resisting strain resulting from complex jaw movements used in the comminution of tough plants. Besides reconstructed feeding envelopes [5], several other morphological characters attest to the low-browsing habit of ankylosaurs. First is the broad, ventrally-deflected snout, which is otherwise observed most frequently among grazing bovids [99]. The relatively great breadth of the snout undoubtedly enables these mammals to feed more efficiently on fibrous, low-growing grasses [25]–[32]. However, the purpose of the ventral deflection of the snout in these bovids is not yet fully understood. It may serve to bring the cropping mechanism (incisors) closer to the ground, similar to what has been proposed for marine grazing dugongs [101], but this is speculation. It may also reflect the fact that grazers tend to have faces more strongly flexed on the basicranium than browsers [27], [28], [31], but the reason for this correlation is likewise unknown. Second is the relatively great transverse breadth of the paroccipital processes, which is also common among grazing bovids. Spencer [99] suggested that this may reflect the fact that grazers tend to use sharp head movements for cropping forage, effected by the nuchal musculature, whereas browsers rely more on their lips and tongue. Perhaps ankylosaurs also relied on head movements to sever plant food, but no corresponding study on head mobility in these animals has been conducted to date. Challenging this hypothesis is the observation of Maryańska [102] that ankylosaurs possessed a well-developed hyoid apparatus and entoglossal process, which would have supported a long and mobile tongue. Ankylosaurs may have used such a tongue in the cropping of vegetation. Therefore, while it is likely that they consumed soft, pulpy plant tissues (e.g., fruits [93], [103]), ankylosaurs probably subsisted on tough leaves that required more thorough mastication as well [104]. This interpretation is corroborated by circumstantial evidence in the form of a cololite associated with a Lower Cretaceous ankylosaurid from Australia [105]. The fossil comprises angiosperm fruits or endocarps, small seeds, possible fern sporangia, and abundant vascular tissue (probably leaves). The plant material exhibits signs of having been comminuted by the jaws [105]; however, the finding of gastroliths associated with a specimen of Panoplosaurus mirus (ROM 1215 [106]) suggests that additional food processing occurred in the gizzard. If so, then it is likely that the ankylosaur skull ecomorph does not accurately reflect the associated palaeodiet. Nonetheless, there is some doubt about whether the gastroliths truly pertain to the specimen in question, as neither the field notes nor the original description [92] mention the existence of gizzard stones (K. Seymour, pers. comm., 2011). Ankylosaur families differ in their mandibular morphologies such that nodosaurids possess a relatively greater offset between the jaw joint and coronoid apex than ankylosaurids. This suggests that the mechanical advantage of the nodosaurid mandible was elevated relative to that of ankylosaurids (due to the increased length of the applied force moment arm), resulting in a more powerful bite. Supporting this interpretation, Carpenter [106] and Vickaryous [107] reported on the existence of dorsoventrally deep (fused) vomers with a distally dilated process among nodosaurids, which may have served to further dissipate stress associated with either elevated bite forces or repetitive masticatory movements. Therefore, it seems likely that nodosaurids subsisted on harder or tougher plants than ankylosaurids, necessitating a more powerful bite and cranial structures associated with stress distribution. Perhaps surprisingly, the contention of Carpenter [38]–[41] that ankylosaurids and nodosaurids differ appreciably in relative beak width is not well-supported here. In the time-averaged ankylosaur analysis above, the separation of the two families along PC 1 is due in part to the relatively wider beak of ankylosaurids, but this variable loads comparatively weakly on the axis, and its signal is otherwise contradicted by loadings on other PCs. It is possible that relative beak width did not prove to be a stronger discriminator of ankylosaurids and nodosaurids because: (1) it was overwhelmed by other, stronger loading variables; (2) it was not captured by the first PCs considered here; or (3) it was not captured at all due to the confounding effects of missing data. Additional research into the specific question of ankylosaur beak width variation is in progress.

Ceratopsidae. The inferred ceratopsid ecomorph is characterized by a particularly large and narrow skull, distally-elongate tooth row, and rostrally projecting snout. Although the relative transverse width of the paroccipital processes is most developed in ankylosaurs, the separation of ceratopsids from hadrosaurids along DF 2 of the time-averaged analysis suggests that the former taxon is characterized by slightly wider paroccipital processes as well. Two features in particular attest to the especially powerful bite of ceratopsids. The first is overall skull size, which is the largest of any of the forms from the DPF. The second is the distal extension of the tooth row beyond the apex of the coronoid process. Ostrom [35], [85] demonstrated that this morphology equates to a shift in the behaviour of the jaw mechanism, from a class 3 to a class 1 lever, because the relative lengths of the applied and resistance force moment arms are switched. Therefore, the ceratopsid jaw mechanism appears to have been more efficient than that of ankylosaurs. The elevation of the coronoid process and concomitant depression of the jaw joint would have further served to enhance the leverage of the ceratopsid mandible [35], [85]. The transversely wide paroccipital processes of ceratopsids–although not as developed as in ankylosaurs–may correlate with low browsing. On the other hand, it may reflect the development of the nuchal musculature in support of the large parietosquamosal frill. Paradoxically, although ceratopsids appear to have been restricted to feeding below one metre from the ground [5], the cropping mechanism is not ventrally deflected as in mammalian grazers [99]. This might be attributable to the great mobility of the head, which could have pivoted easily about the spherical occipital condyle to bring the beak near to the ground [108]. Bearing these points in mind, ceratopsids can be characterized as low-level browsers that probably sustained themselves on mechanically resistant vegetation requiring high bite forces. Mechanical resistance comprises various physical properties such as strength, toughness, and ‘hardness’ (a general term that encompasses the properties of plasticity and stiffness). The bladed dentition of ceratopsids [34], [35], [85], [109]–[111] almost certainly was not suitable for processing particularly strong or hard plant types, which require a durophagous dentition [82]. Therefore, it is likely that ceratopsids specialized on tough plant parts that resisted crack propagation, such as low-growing, woody browse. The ‘weedy’ angiosperms of the Late Cretaceous, which grew most commonly in coastal plain settings [112] alongside ceratopsids [113], may have provided an abundant and renewable food resource for these animals [114]–[116]. The interpretation of ceratopsids as woody browse specialists might help to explain the narrowness of their beaks, which would have restricted them to selective foraging, but more work in this area is required. NPMANOVA indicates that centrosaurines and chasmosaurines probably differ in their skull proportions, but low sample size generally impedes the interpretation of the results. For example, whereas the two subfamilies differ primarily according to cranial depth and distal tooth row extension in the time-averaged comparison (where the probabilities are not quite significant), their differences are better attributed to the transverse width of the occipital region in the MAZ-1 comparison (where the probabilities are significant). It is possible that morphological disparity between centrosaurines and chasmosaurines may truly manifest itself differently within MAZ-1, but it is also likely that the smaller samples in this assemblage zone do not adequately capture the true ecological signal therein, and, in fact, artificially inflate statistical significance by reducing taxonomic overlap in morphospace [117]. There is some evidence, however, that ceratopsid subfamilies differ at least partly according to cranial depth in MAZ-1, as in the time-averaged analysis. This might be taken as tentative support for the finding of Henderson [44] that centrosaurines possess taller crania than chasmosaurines, making them more resistant to bending and torsional stresses. These differences were said to have facilitated niche partitioning between the two subfamilies, as centrosaurines presumably would have been capable of subsisting on a more resistant plant diet than sympatric chasmosaurines. Nonetheless, although Henderson [44] was careful to account for the confounding effects of taphonomic distortion, he considered only a single specimen per species, and therefore did not account for intraspecific variation. This omission is likely to have introduced some systematic bias into the results because numerous studies have shown that individual ceratopsid species actually vary quite widely, even when ontogenetic effects are accounted for [34], [109], [118]–[126]. For example, long-faced Centrosaurus apertus have been described (e.g., Ce. “longirostris” [127]), as well as short-faced Chasmosaurus belli (e.g., Ch. “brevirostris” [34]). It is therefore necessary that statistical approaches be taken to account for the significance of this variation.