Phylogenetic relationships of A. mcintoshi
In order to resolve the phylogenetic position of Abydosaurus among sauropods, we conducted a cladistic analysis based on the data matrix of Wilson (2002) with modified taxonomic and character scope and with suggested scoring changes (Wilson and Upchurch 2009; see Online Resource 4). Ingroup terminal taxa were restricted to neosauropods, and several genera were bundled into higher-level terminal taxa. The reduced taxonomic scope of the analysis necessitated removal of characters whose scorings do not vary within Neosauropoda, either because they distinguish among basal clades or because they vary between genera subsumed within higher-level terminal taxa. We augmented the data matrix by including autapomorphies of neosauropod genera listed by Wilson (2002: appendix C) that are shared with Abydosaurus. The resultant matrix included 151 characters scored in ten ingroup taxa and two outgroup taxa (Omeisaurus, Shunosaurus) that were chosen based on their completeness and unanimous acceptance of their phylogenetic position outside Neosauropoda.
The low number of terminal taxa allowed for use of “branch-and-bound” treebuilding methods, which guarantee discovery of the shortest tree but not all trees (Swofford 2001). Five most parsimonious trees were discovered (235 steps) that differed in the positions of Jobaria and Haplocanthosaurus within Neosauropoda. Apart from this uncertainty, tree topology is consistent with that of Wilson (2002). Neosauropoda is monophyletic and consists of Diplodocoidea and Macronaria. Diplodocoidea includes the sister taxa Flagellicaudata and Rebbachisauridae, whereas Macronaria includes Camarasaurus, Brachiosaurus (i.e., B. altithorax + B. brancai), and Euhelopus as successive outgroups to Titanosauria (Malawisaurus + Lithostrotia). Abydosaurus could be scored for almost 50% of the characters, which resolved it within Macronaria as the sister taxon to Brachiosaurus (decay index = 3). Abydosaurus is positioned within Titanosauriformes based on the presence of spongy (camellate) presacral vertebrae and resolved as sister taxon to Brachiosaurus by the presence of an anterior process on the lacrimal, narrow separation of the supratemporal fossae on the skull roof, dentary with a divided posteroventral process, and transverse processes of anterior caudal vertebrae with a prominent ventral bulge.
Evolution of tooth shape in sauropods
Sauropod tooth shape has long been characterized as either ‘broad crowned’ or ‘narrow crowned’ (Janensch 1929), and the ever-improving sauropod fossil record indicates that whereas both morphs coexisted in Late Jurassic ecosystems, only narrow-crowned forms survived into the latest Cretaceous (Barrett and Upchurch 2005; Wilson 2005). The transition between these two endpoints occurred during the Early Cretaceous, which is an undersampled interval in sauropod history—particularly in North America (Wedel et al. 2000), where they are thought to have gone extinct after the Albian and re-entered from South America or Asia during the Maastrichtian (Lucas and Hunt 1989). A. mcintoshi was part of this general trend of reduction of tooth crown breadth during the Cretaceous.
To examine broad-scale changes in tooth morphology in sauropodomorph dinosaurs, we measured a simple index of tooth crown shape called the Slenderness Index (SI), which is the ratio of crown length to crown breadth (Upchurch 1998). This metric has been used previously to bin sauropods into broad-crowned (SI ≤ 4.0) and narrow-crowned (SI ≥ 4.0) morphs and to identify a gradual replacement of the former by the latter during the Cretaceous (Barrett and Upchurch 2005:128). In Fig. 5, we plot the distribution of SI in all known sauropod teeth and a representative sample of basal sauropodomorph teeth to examine changes in sauropod tooth morphospace during the Mesozoic (see Online Resource 5, 6).
The basal sauropodomorph outgroups to sauropods, generally referred to as ‘prosauropods’, were the earliest saurischian herbivores (Martínez and Alcober 2009). During their 40 million year history, they occupied a fairly narrow band of tooth crown breadth (SI = 1.56–2.43) that can be regarded as the primitive condition for sauropods. For nearly 20 million years, prosauropods coexisted with basal sauropods, with which they overlapped in tooth shape space. Notably, however, basal sauropods attained broader tooth crown proportions than did prosauropods early in their history and achieved their broadest crown proportions by the end of the Middle Jurassic (SI = 1.16). Although prosauropods and basal sauropods overlap in tooth shape space, it is not known whether they competed for similar resources; very few horizons (e.g., lower and upper Elliot Formation) preserve both basal sauropodomorphs and basal sauropods (Yates and Kitching 2003; Knoll 2004, 2005; Yates et al. 2004).
There is very little temporal overlap between basal sauropods and neosauropods (macronarians and diplodocoids). In fact, the original partition of sauropods into ‘eosauropods’ (i.e., basal sauropods) and neosauropods took advantage of their stratigraphic distribution on either side of the Middle–Late Jurassic boundary (Bonaparte 1986). Although this pattern still holds generally, at least one Cretaceous genus potentially falls outside the neosauropod radiation (Jobaria; Sereno et al. 1999). More recent analyses have suggested Jobaria is a basal macronarian (e.g., Upchurch et al. 2004; Remes et al. 2009) of potentially older stratigraphic age (Rauhut and López-Arbarello 2009). If either of these hypotheses is correct, then basal sauropods are restricted to infra-Cretaceous sediments (cross-hatching in Fig. 5). The first reduction in relative crown breadth beyond the primitive ‘prosauropod’ range appeared in the Late Jurassic, with the appearance of diplodocoids such as Diplodocus and Apatosaurus. Diplodocoids are separated from contemporaneous neosauropods by a notable SI gap, which may have been bridged by the currently unsampled phylogenetic intermediates present during the early Late Jurassic or Middle Jurassic. The widest range of crown proportions was achieved during the Late Jurassic, after which neosauropods (diplodocoids plus macronarians) underwent a dramatic shift towards narrower crown proportions.
The neosauropod subgroups Macronaria and Diplodocoidea coexisted for nearly 50 million years but did not overlap in tooth shape space. During the Late Jurassic and Early Cretaceous, macronarians occupied a wide range of tooth crown shapes but never attained the narrow proportions of diplodocoids. After the extinction of diplodocoids at the beginning of the Late Cretaceous, macronarians radiated into the narrow tooth crown shape space previously occupied by diplodocoids. This, combined with the extinction of broad-crowned sauropods ca. 125 million years ago, led to a sauropod fauna consisting exclusively of narrow-crowned taxa, as previously mentioned (Barrett and Upchurch 2005; Wilson 2005). By the latest Cretaceous, all sauropod teeth are narrower than the narrowest ‘prosauropod’ or basal sauropod teeth, and titanosaurs are the only remaining sauropod lineage (Fig. 5).
A. mcintoshi has an intermediate crown breadth that is narrower than that of ‘prosauropods’ and basal sauropods but not nearly as narrow as that of diplodocoids or titanosaurs. Abydosaurus lies within a cluster of Early Cretaceous tooth forms that have narrower crown breadths than their antecedents, marking a shift in crown breadth that appears to be independent of changes to narrow crown breadths in titanosaurs in the Cretaceous and in diplodocoids in the Late Jurassic. This shift did not result in major changes in sauropod absolute and relative diversity and absolute abundance, which remain relatively stable throughout the Cretaceous (Butler et al. 2009: fig. 1) apart from a minor decline in the mid-Cretaceous that coincides with a drop in the number of dinosaur-bearing formations (Upchurch and Barrett 2005: fig. 3.6; Barrett et al. 2009).
Sauropod–plant coevolution?
Although numerous authors have suggested a connection between the origin and radiation of angiosperms and changes in herbivorous dinosaur faunas (e.g., Bakker 1978), recent analyses have unanimously concluded that there is no demonstrable coevolutionary relationship between major events in dinosaur and plant evolution (Sereno 1997; Weishampel and Jianu 2000; Barrett and Willis 2001; Barrett and Rayfield 2006; Butler et al. 2009). To examine potential links between the shift in Cretaceous sauropod dentitions detailed above (Fig. 5) with changes in contemporaneous floras, below we explore the functional implications of narrow-crowned dentitions.
Reduction in tooth crown breadth is correlated with increased packing of teeth into the jaws. In diplodocoids, for example, narrow crowns are associated with as many as seven replacement teeth per tooth position and tooth replacement rates of every 30 days (Nigersaurus; Sereno et al. 2007) or every 35 days (Diplodocus; D’Emic et al. 2009). These rates are higher than those of the broad-crowned sauropod Camarasaurus, which replaces its teeth every 62 days (J. Whitlock, unpublished data). Narrow-crowned sauropods replace their teeth faster than contemporaneous ornithischian dinosaurs with dental batteries, the fastest of which replaces every 50 days (Edmontosaurus; Erickson 1996). In addition to differences in tooth replacement rates, tooth formation times are nearly twice as fast for the narrow-crowned sauropod Diplodocus compared to the broad-crowned Camarasaurus (ca. 185 days vs. ca. 315 days; J. Whitlock, unpublished data). Narrow-crowned macronarians such as titanosaurs have not been histologically sampled to measure replacement rates, but these can be estimated by comparing relative sizes of functional and replacement teeth. In rapidly replacing dentitions, a functional tooth and its replacement teeth are close to one another in size, whereas in slowly replacing dentitions they are more disparate in size. Like diplodocoids, narrow-crowned macronarians have tooth families composed of teeth that are close to one another in size, implying they too replaced rapidly (D’Emic et al. 2009). We hypothesize that the high replacement rates associated with narrow-crowned sauropod dentitions suggest that they were subjected to high rates of wear, which may have been caused by one or more of several factors, including: (1) mechanics of biting or chewing; (2) diet; or (3) feeding ecology.
Mechanics of biting or chewing
Despite similarities in the shapes of crania of narrow-crowned sauropod taxa, some of which have elongate skulls with an anteriorly restricted dentition (see below), there is no evidence that the mechanics of these skulls would increase wear on teeth. In fact, the magnitude of loads generated by adductor musculature placed on terminally positioned dentition in an elongate skull is expected to be lower than those generated by a shorter-jawed form with a proportionately longer dentigerous region. In addition, differences in the direction of bite force (e.g., shift from orthal to propalinal stroke) would not be expected to dramatically increase wear rates in the absence of other differences. This suggests that the observed changes in crown breadth may be related to something other than jaw mechanics, such as a shift in diet and/or feeding ecology.
Diet
The transition from a broad range of crown breadths to predominantly, and later exclusively, narrow dentitions took place in the Cretaceous (Fig. 5), during which time a major shift in global floral composition occurred. In the Early Cretaceous, several major plant groups contributed subequally to global abundances, but from the Albian until the end-Cretaceous angiosperms and conifers comprised nearly 80% of vascular plant occurrences (Butler et al. 2009: Fig. 2). This change to a conifer–angiosperm predominated flora suggests that sauropods would, on average, encounter these plants more often than others. Despite this general correlation between changes in sauropod tooth shape and conifer–angiosperm abundances, these plants are not especially abrasive and would not have produced comparatively high rates of wear. Living conifers and angiosperms have been shown to have lower silica content overall than other plant groups, even if certain subgroups such as grasses were silica accumulators (Hodson et al. 2005). Although there are records of modern grasses in the Cretaceous, they were not ecologically predominant (Prasad et al. 2005). Apart from grasses, there are several non-angiosperm, non-conifer plants with Mesozoic representatives (e.g., the pteridophyte Equisetum, the fern Osmundia) that have been demonstrated to be both nutritious and digestible (Hummel et al. 2008) and highly abrasive (Hodson et al. 2005).
These silica accumulating plants are all potential wear-inducing foodstuffs for sauropod dinosaurs, but there is no direct evidence that sauropods ate them. In fact, no bona fide coprolites or enterolites have been directly associated with sauropod skeletons, and no plant remains have been found in situ on sauropod dentitions. The sauropod stomach contents reported by Stokes (1964) were not found in place within an articulated skeleton and were later determined to be part of a laterally extensive, twig laden, lacustrine deposit (J. H. Madsen and W. D. Tidwell, personal communication, 2002). They provide a less convincing case of direct association than do other recent discoveries from non-sauropod dinosaurs (e.g., Molnar and Clifford 2000; Varricchio 2001; Tweet et al. 2008). A case for indirect association of coprolites with sauropods was made by Matley (1939), who described abundant, well-preserved coprolites from the Late Cretaceous Lameta Formation of India. There, sauropods are abundant and the only large-bodied herbivores known from the landmass. The Indian coprolites contain grass phytoliths as well soft tissues of other angiosperms, gymnosperms, and pteridophytes, indicating a diet of mixed composition and abrasiveness (Mohabey and Samant 2003; Prasad et al. 2005).
Feeding ecology
Although narrow-crowned sauropods do not form a monophyletic group, there are cranial features shared between certain members of the two main lineages. Reduction of tooth breadth in both derived diplodocoids (e.g., Diplodocus, Nigersaurus) and derived titanosaurs (e.g., Rapetosaurus, Nemegtosaurus) resulted in dentitions that were positioned anteriorly in the jaws (Curry Rogers and Forster 2001). Anteriorly restricted dentition, along with an elongate skull shape, squared jaws, elevated tooth replacement rates, microwear data, and vertical head orientation were interpreted as adaptations to a low-browsing feeding strategy in Nigersaurus (Sereno et al. 2007), a feeding strategy suggested to be general for diplodocoids (Upchurch and Barrett 2000). Comparable data is not yet available for head orientation in titanosaurs, but the presence of an elongate skull with anteriorly restricted, rapidly replacing narrow crowns may suggest that at least some of them were also low browsers.
In sum, the shift to rapidly replacing, high-wear dentitions in Cretaceous sauropods does not appear to be related to any major change in global floral diversity, despite its coincidence with increased abundance of conifers and angiosperms. Instead, this pattern may be explained by a shift in diet to highly abrasive vegetation or to a shift in feeding ecology to low browsing, possibilities to be explored by future work.
Sauropod skulls: spartan design
Sauropods are notable among dinosaurian herbivores for their relatively simple and static skull design. Even the bizarre Nigersaurus represents an extreme version of a diplodocoid rather than a substantially neomorphic form (Sereno et al. 2007). The absence in sauropods of complex masticatory adaptations (e.g., beaks, cheeks, kinesis, and heterodonty) and cranial display structures (e.g., crests, frills, and ornamentation)—all of which are present within ornithischian herbivores—is somewhat surprising given the success of sauropod dinosaurs. However, the proportions of sauropod skeletons may offer insight into this counterintuitive pattern.
The sauropod body plan was acquired quite early in their evolutionary history and remained relatively unchanged during the Mesozoic. All sauropods have a small head, long neck, long tail, and deep bodies supported by four columnar legs. Even the relatively large head of B. brancai only accounts for approximately 1/200th of total body volume (0.4%; Gunga et al. 2008). This proportion was probably similar for Abydosaurus but even smaller for sauropods such as Diplodocus. In contrast, the heads of ornithischian herbivores are an order of magnitude larger relative to body volume. The head of Edmontosaurus accounts for approximately 1/30th body volume (3.2%; Bates et al. 2009). Although the body mass of B. brancai (38,000 kg; Gunga et al. 2008) is nearly 50 times that of Edmontosaurus (813.25 kg; Bates et al. 2009), the observed difference in body proportions does not appear to be mass-dependent. The prosauropod Plateosaurus, which has a body mass (630–912 kg) comparable to Edmontosaurus, has a head volume that is approximately 1/125 body volume (0.8–0.9%; Gunga et al. 2007).
We conclude that whereas complex intraoral processing and cranial display structures may have been effective for relatively large-headed, short-necked ornithischians, they may not have been advantageous for sauropods. Instead, sauropods evolved small skulls and elongate necks early in their evolutionary history. They adopted a strategy of maximizing intake by specialized cropping with little to no processing and maximizing feeding envelope by changes in the length, mobility, support, and neutral pose of the neck.