Herbivorous Dinosaur Jaw Disparity and Its Relationship to Extrinsic Evolutionary Drivers

Paleobiology, 43(1), 2017, pp. 15–33 DOI: 10.1017/pab.2016.31

Herbivorous dinosaur jaw disparity and its relationship to extrinsic evolutionary drivers

Jamie A. MacLaren, Philip S. L. Anderson, Paul M. Barrett, and Emily J. Rayﬁeld

Abstract.—Morphological responses of nonmammalian herbivores to external ecological drivers have not been quantified over extended timescales. Herbivorous nonavian dinosaurs are an ideal group to test for such responses, because they dominated terrestrial ecosystems for more than 155 Myr and included the largest herbivores that ever existed. The radiation of dinosaurs was punctuated by several ecologically important events, including extinctions at the Triassic/Jurassic (Tr/J) and Jurassic/Cretaceous (J/K) boundaries, the decline of cycadophytes, and the origin of angiosperms, all of which may have had profound consequences for herbivore communities. Here we present the firstanalysisofmorphologicaland biomechanical disparity for sauropodomorph and ornithischian dinosaurs in order to investigate patterns of jaw shape and function through time. We find that morphological and biomechanical mandibular disparity are decoupled: mandibular shape disparity follows taxonomic diversity, with a steady increase through the Mesozoic. By contrast, biomechanical disparity builds to a peak in the Late Jurassic that corresponds to increased functional variation among sauropods. The reduction in biomechanical disparity following this peak coincides with the J/K extinction, the associated loss of sauropod and stegosaur diversity, and the decline of cycadophytes. We find no specific correspondence between biomechanical disparity and the proliferation of angiosperms. Continual ecological and functional replacement of pre-existing taxa accounts for disparity patterns through much of the Cretaceous, with the exception of several unique groups, such as psittacosaurids that are never replaced in their biomechanical or morphological profiles.

Jamie A. MacLaren. Department of Biology, Universiteit Antwerpen, Campus Drie Eiken, Universiteitsplein, Wilrijk, Antwerp, 2610, Belgium Philip S. L. Anderson. Department of Animal Biology, University of Illinois at Urbana–Champaign, 515 Morrill Hall, 505 S. Goodwin Ave., Urbana, Illinois 61801, U.S.A. Paul M. Barrett. Department of Earth Sciences, Natural History Museum, London, Cromwell Road, London, SW7 5BD, U.K. Emily J. Rayﬁeld. * School of Earth Sciences, University of Bristol, 24 Tyndall Avenue, Bristol, BS8 1TQ, U.K.

Accepted: 19 July 2016 Published online: 15 December 2016 Data available from the Dryad Digital Repository: http://dx.doi.org/10.5061/dryad.c78k5

Introduction A number of studies have investigated the ecological and evolutionary responses of Sauropodomorph and ornithischian dino- dinosaurs to the Tr/J mass extinction in terms saurs were the foremost herbivorous terrestrial of diversity analyses, but only a handful of vertebrates of the Mesozoic Era in terms of studies have quantiﬁed morphological dispar- species richness, abundance, and functional ity (Brusatte et al. 2008a,b) or the evolution of diversity (Weishampel and Norman 1989; Sereno other traits across this interval (Irmis 2011; 1999; Weishampel et al. 2004; Barrett 2014). Sookias et al. 2012). These studies found that Both groups survived two extinction events— dinosaur morphospace occupation was not the end-Triassic mass extinction (Tr/J) and a greatly affected by the Tr/J extinction (Brusatte smaller extinction at the Jurassic/Cretaceous et al. 2008a,b): dinosaurian disparity remained boundary (J/K)—and persisted through several essentially unchanged across the Tr/J episodes of ﬂoral turnover, including the boundary, whereas crurotarsans became almost decline of cycadophytes and the proliferation completely extinct (Brusatte et al. 2008a). With of angiosperms (Sereno 1997; Barrett and Willis respect to dinosaurs the J/K extinction has been 2001; Lloyd et al. 2008; Butler et al. 2009b). studied in terms of diversity analyses (e.g., However, relatively few studies have attempted Upchurch and Barrett 2005; Barrett et al. 2009; to quantify the responses of nonavian dinosaurs Butler et al. 2010, 2011; Upchurch et al. 2011), to these extrinsic environmental drivers. and the potential ecological consequences of

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this event have been discussed qualitatively in been conducted on various extinct vertebrate terms of changes to dinosaur browsing regimes groups, including dinosaurs (Brusatte et al. and community composition (Bakker 1978; 2008a,b, 2012; Young and Larvan 2010; Butler Barrett and Willis 2001; Barrett and Upchurch et al. 2011; Foth and Rauhut 2013; Button et al. 2005). Possible associations between paleobota- 2014). By contrast, a new method for assessing nical turnovers and dinosaur evolution have the diversity of biomechanical profiles, been proposed (e.g., Bakker 1978; Weishampel multivariate biomechanical disparity (Anderson and Norman 1989; Tiffney 1992; Mustoe 2009; Anderson et al. 2011, 2013; Stubbs et al. 2007), with the suggestion that changes in the 2013), has not been widely applied. Biomecha- prevalent mode of dinosaur herbivory (e.g., nical disparity offers a novel means to quantify high-browsing vs. low browsing; extensive oral variation in biomechanically relevant traits and processing vs. lack of oral processing) were to infer their potential ecological significance: reciprocally related to changes in the taxonomic for example, biomechanical traits might and ecological composition of contemporary include mechanical advantage (the ratio of plant communities. In particular, it has been muscle moment arms indicating the efficiency suggested that a decline in sauropodomorph of force transfer during biting), polar moment and stegosaur abundance and diversity might of inertia (a proxy for flexural stiffness), and be associated with a decline in cycadophyte mandibular articulation offset (dictating diversity during the Early Cretaceous and that simultaneous occlusion of the entire tooth the ecological radiation of angiosperms during row, or scissor-like occlusion) (Anderson the same period may have been fostered 2009; Anderson et al. 2011, 2013; Stubbs et al. by a coincident taxonomic radiation of low- 2013). Other studies have explored disparity browsing ornithischian dinosaurs with complex of individual biomechanical traits such as jaw mechanisms (e.g., Bakker 1978; Weishampel mechanical advantage (Sakamoto 2010; and Norman 1989; Tiffney 1992; Mustoe Brusatte et al. 2012), average maximum stress, 2007). Hypotheses regarding dinosaur–plant or a metric of skull strength (Foth and Rauhut coevolution have been more recently tested 2013). Continuous measurements can be quantitatively and qualitatively using spatio- projected into multivariate “biomechanical temporal comparisons between the dinosaur morphospace.” Previous work in this area has and paleobotanical records (Barrett and used two-dimensional (2D) views of mandib- Willis 2001; Butler et al. 2009a,b, 2010). These ular elements to investigate the appearance diversity-based spatiotemporal studies found and diversity of biomechanical profiles during no definitive evidence for the coradiation of any the radiation of Paleozoic fishes (Anderson Mesozoic plant and dinosaur group, although 2009; Anderson et al. 2011), the water-to-land some temporal correlations were suggestive of transition in tetrapods (Anderson et al. 2013), possible interactions. Physiological limits on the Mesozoic diversification of crocodylomorphs some of these coevolutionary hypotheses have (Stubbs et al. 2013), and niche partitioning in also been proposed on the basis of the possible sauropod dinosaurs (Button et al. 2014). nutritional value of potential food plants (e.g., Despite previous work, the functional Hummel et al. 2008; Gee 2011). responses to these potential evolutionary Disparity analyses quantify morphological drivers, and hence how the organism inter- diversity within a group of organisms, rather acted with its environment and potential than merely documenting taxonomic richness drivers of selection, have not been quantified. (Wills et al. 1994; Ciampaglio et al. 2009). Without this information we lack a complete Unlike species-richness estimates, disparity picture of how dinosaur communities and analyses can be robust to sampling biases and clades interacted with and exploited Mesozoic document the variation in morphology and environments over time. In addressing potential function within taxonomic groups these questions, assessing the morphological (Wills et al. 1994). Assessments of morpholo- variation evident from the fossil record may gical disparity using either anatomical not be sufficient, as we do not know whether measurements or cladistic characters have morphology and morphological diversity are

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reliable predictors of function and functional which are unrelated to feeding, such as housing diversity. Therefore, in order to assess the the brain and sensory organs (Hylander et al. relationship between jaw shape, function, and 1991; Hylander and Johnson 1997). extrinsic evolutionary drivers, we provide the Morphology.—The archosaur mandible is a first quantitative assessment of the morpho- primarily planar structure, although its logical and biomechanical disparity of an morphology does differ between groups, with individual functional unit (the lower jaw) in varying degrees of inturning and bowing, herbivorous nonavian dinosaurs through time. particularly with respect to its symphyseal This approach complements previous attempts region (Romer 1956). However, to include as to examine these questions though spatiotem- many taxa as possible, in order to account for poral comparisons of species-richness patterns the greatest amount of biomechanical and and provides the only rigorous biomechani- mandibular and dental shape variation, we cally and functionally based analysis of these selected a standard lateral view of the issues attempted to date. We hypothesize that mandible as the basis for this study. The 2D ornithischians and sauropodomorphs will landmarks were applied to homologous and show distinct morphologies and biomechani- analogous points on lateral images of dinosaur cal profiles (i.e., in both the shape and jaws using tpsDig II software (Rohlf 2004; mechanical capabilities of the jaw). We also Zelditch et al. 2012). Six fixed landmarks hypothesize that the shift in plant community were described, identifying biologically and structure after the J/K boundary will trigger operationally homologous points on both a corresponding shift in dinosaurian jaw sauropodomorph and ornithischian jaws (see biomechanical profiles, due to the differing Supplementary Fig.1). The overall morphology physiognomies, digestibility, and mechanical of each jaw was described by a series of sliding properties of the varied potential food plant semilandmarks (sLM). Six sLM curves, each clades that were ecologically important at bracketed by two of the fixed landmarks, were different times throughout the Mesozoic used to define the shape of the jaw. In total, 88 (Bakker 1978; Weishampel 1984; Niklas 1992; landmarks (both fixed and sliding) were Hummel et al. 2008; Gee 2011). We use a described. sLMs were slid using the Chord-d2 geometric morphometric landmark analysis to technique to minimize Procrustes distances compare dinosaur mandibular shape variabil- rather than bending energy (Rohlf 2008); this ity to variation in mandibular biomechanical was performed in tpsRelw. Described curves profiles. We then compare these data with the were appended to landmarks in tpsUtil (Rohlf timing of several extrinsic events (tetrapod 2004); appended landmarks were then extinctions, changes in floral communities) that superimposed using generalized least-squares have been proposed to influence dinosaur (Procrustes) methods in tpsRelw (Rohlf 2008). evolutionary history, in order to determine Procrustes superimposition aligned jaws, whether coincident patterns are present. eliminating scale, location, and rotational differences between specimens (Rohlf 2004). Consensus models, partial warps, and relative Materials and Methods warps were then calculated using tpsRelw Data for 2D landmark and biomechanical trait software. Relative warp scores were subjected analyses were compiled from 167 sauropodo- to principal components analysis (PCA) to morph and ornithischian dinosaur taxa (see produce shape-based morphospace plots. Supplementary Information,Appendix6).Herbi- Biomechanics.—Eighteen continuous biome- vorous nonavian theropods were excluded from chanical characters or traits were quantified, this data set, as complete mandibular material for many of which have important functional these animals is rare. A mandibular biomechani- consequences in extant organisms (Table 1). cal profile represents a good proxy for character- Full details of the biomechanical characters izing the feeding system, as the mandible is are described in the Supplementary Material. primarily adapted for feeding, whereas the Biomechanical trait measurements were cranium has multiple functional roles, some of standardized using a z-transformation

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TABLE 1. Continuous biomechanical characters used in this study.

Code Functional trait Description C1 Anterior mechanical advantage Ratio of maximum out-lever (on functional tooth row) and jaw muscle in-lever moment arms C2 Posterior mechanical advantage Ratio of minimum out-lever (on functional tooth row) and jaw muscle in-lever moment arms C3 Opening mechanical advantage Ratio of maximum out-lever and opening in-lever moment arms C4 Maximum aspect ratio Proxy for maximum ﬂexural stiffness in the jaw C5 Average aspect ratio Proxy for average ﬂexural stiffness across the entire jaw C6 Relative adductor fossa length Length of adductor muscle attachment; proxy for jaw muscle size C7 Relative dental row length Length of functional tooth row relative to total jaw length C8 Relative articular offset Proxy for deviation of biting action from scissor-like mastication. C9 Relative mandibular fenestra Area of mandibular fenestrae relative to total lateral jaw area C10 Relative dental curvature Curvature of functional tooth row; proxy for shearing vs. compressive mastication C11 Cheek tooth height:breadth Proxy for maximum tooth size for teeth occluding with maxillary teeth C12 Premaxilliary occluding tooth height: Proxy for maximum tooth size for teeth occluding with premaxillary teeth breadth C13 Tooth packing Proxy for tooth separation and how closely teeth are packed C14 Predentary tooth procumbancy Proxy for anterior-most tooth procumbancy C15 Tooth height:jaw depth Height of tooth present above deepest section of functional jaw taken C16 Relative symphyseal length Proxy for robustness of anterior jaw C17 Mandibular symphysis orientation Proxy for symphyseal resistance to bending during biting C18 Predentary offset Proxy for predentary curvature in ornithischians

technique, giving all characters a mean of 0 Disparity.—Disparity through time was and a variance of 1 (Anderson et al. 2011). A calculated across sixteen 10 Myr time bins. The standardized matrix of biomechanical character lengths of the time bins either side of the Tr/J scores was then subjected to principal boundary were adjusted to accommodate the coordinates analysis (PCoA), using the Gower date of the boundary as in Butler et al. (2012). model to correct for missing data to produce Use of 10 Myr time bins enables comparisons biomechanical morphospace plots. PCoA and across both the Tr/J and J/K boundaries, creation of morphospace plots was performed standardizes bin length, and provides greater in Past, Version 3 (Hammer et al. 2001). sample sizes per bin than those available for Signiﬁcant differences in morphospace occu- strict stage-level comparisons. Sauropodomorph pation were tested using nonparametric multi- disparity was also analyzed for vertical feeding variate analysis of variance (NPMANOVA) in envelopes in 3 m intervals. Species assignment Past, Version 3 (Hammer et al. 2001). All princi- to each maximum feeding envelope is listed in pal axes accounting for more than 1% of varia- the Supplementary Material. To account for tion were used in the NPMANOVA, resulting in variation in the published literature, maximum 12 axes for shape-based and 15 axes for sauropodomorph feeding envelopes were biomechanical morphospace. Principal axes taken from published works, including were used to display two types of morphospace reconstructions from new material (e.g., comparisons: overall shape-based and bio- Upchurch and Barrett 2000; Apesteguía 2004; mechanical morphospace between sauropodo- Sander et al. 2006; Peyer and Allain 2010; morphs and ornithischians. We also created a Whitlock 2011; Stevens 2013). Disparity series of morphospace plots representing eight analyses were carried out using the Morpho- 20Myrtimeslices.Thesetimesliceswerecon- logical Disparity Analysis (MDA) package for structed by combining taxa from two adjacent Matlab (Navarro 2003). For all disparity tests, 10 Myr time bins used for the disparity analyses two variance-based disparity metrics were (see following section). Combining time bins tested: the sum of variance and mean pairwise allowed for good sample size and enabled com- distance. Both these metrics are robust to sample parisons across major ecological transitions, for size variation (Ciampaglio et al. 2009). The sum example, mass extinction events. of variance metric is plotted in the main text.

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FIGURE 1. Patterns of morphospace occupation for herbivorous nonavian ornithischian and sauropodomorph dinosaurs. PC1 and PC2 account for 50.4% of variation. Ornithischian and sauropodomorph taxa occupy signiﬁcantly different regions of shape-based morphospace (p < 0.05). Filled circles, Sauropodomorpha; open circles, Ornithischia. Silhouettes represent jaw proﬁles found in that region of morphospace.

Mean pairwise distance results can be viewed ornithischian jaws occupy significantly different in the Supplementary Material. Data were regions of morphological morphospace (p < 0.01; bootstrapped (1000 replicates), and 95% Fig. 1; Table 2). There is minimal overlap confidence intervals were calculated and between sauropodomorphs and ornithischians graphically presented. Significant differences along PC1, with only seven ornithischian jaw and likelihood ratios between each time bin morphologies occupying similar regions to were calculated using pairwise t-tests and sauropodomorphs. Overlapping ornithischian marginal-likelihood assessment on sum of taxa represent basal members of their variance measures (Finarelli and Flynn 2007). respective groups (basal ornithischians: A likelihood ratio >8 is considered a likely result Agilisaurus and Pisanosaurus; thyreophorans (Finarelli and Flynn 2007). Results of t-tests were Emausaurus and Gigantspinosaurus;andthe subsequently corrected for multiple com- basal ceratopsian Yinlong), with the exception parisons, using Bonferroni corrections where of Stegosaurus (two species). Regions of overlap appropriate (Holm 1979). Results for mean are occupied by a wide range of both basal pairwise distance can be found in the Supple- and derived sauropodomorphs; these mentary Material. include: Plateosaurus gracilis, Lamplughsaura, mamenchisaurids, brachiosaurids, and two Results South American titanosaurids (Antarctosaurus and Bonitasaura). Sauropodomorphs occupy Shape Morphospace Occupation.—Our results morphospace exclusively in the − PC1 region: demonstrate that sauropodomorph and this region is characterized by dorsoventrally

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TABLE 2. Results of significance testing (NPMANOVA) ornithischian taxa occupying morphospace on morphospace occupation (PC1 and PC2) and bio- that is shared with sauropodomorphs mechanical occupation (PCo1 and PCo2; PCo1 and PCo3) between Ornithischia and Sauropodomorpha (at p < 0.05). (Figs. 2, 3). Overlapping ornithischian taxa include basal ornithischians (Pisanosaurus, Shape–based heterodontosaurids) and basal members of morphospace Sauropodomorpha Ornithischia Thyreophora (Emausaurus, stegosaurs), Sauropodomorpha — <0.001 Ornithischia <0.001 — Marginocephalia (Yinlong), and Ornithopoda Biomechanical Sauropodomorpha Ornithischia (Changchunsaurus, Dysalotosaurus). Sauro- morphospace podomorphs occupy regions of +PCo1. Sauropodomorpha — <0.001 Ornithischia <0.001 — Noneusauropod sauropodomorphs (e.g., Coloradisaurus, Pantydraco) predominate in +PCo1/−PCo2. This region is characterized by jaws with a high mechanical advantage and narrow jaws and the lack of a prominent a large adductor muscle attachment area. coronoid process. Noneusauropod sauropod- Diplodocids, nonneosauropods, and nontita- omorphs (e.g., Plateosaurus, Melanorosaurus), for nosaurian macronarians (e.g., Mamenchisaurus, the most part, account for sauropodomorph Camarasaurus) stretch sauropodomorph occupation of morphospace in +PC2: this occupation into +PCo2. Jaws in this region region is typified by very narrow anterior jaws. also display high mechanical advantages, Macronarian and diplodocoid taxa (including coupled with high aspect ratios. Many Diplodocus and Tapuiasaurus)primarilyoccupy iguanodontian, ceratopsid, and psittacosaurid −PC2 regions of morphospace (Fig. 1). The center jaw profiles occupy similar regions of of the morphospace (0.0 PC1; 0.0 PC2) is +PCo2 biomechanical morphospace (Fig. 2). occupied by nonhadrosaurid iguanodontians Occupation is spread deeper into −PCo1 by (Parksosaurus, Theiophytalia,andDryosaurus). leptoceratopsids (e.g., Montanoceratops). This Jaws in this region exhibit a greater gap region of functional space is characterized by between landmarks 1 and 2 than in sauropod- deep jaws with short adductor muscle omorph morphospace (due to the presence of the attachment and a high posterior mechanical predentary in iguanodontians). Disparate advantage. Expansion into −PCo2 is accounted groups of nonthyreophoran ornithischians for by deep-jawed ankylosaurs (Euoplocephalus, expand morphospace occupation into +PC1 Silvisaurus), with low tooth:jaw depth ratios and +PC2 (hadrosaurids) and −PC2 regions and high relative dental length (Fig. 2). Similar (leptoceratopsids and psittacosaurids). +PC1 patterns are observed in PCo3, with more and +PC2 regions typically contain jaws with basal sauropodomorphs occupying −PCo3, prominent coronoid processes and downwardly with a large cluster of iguanodontians and deflected predentaries; −PC2 regions contain ceratopsids occupying regions of central robust, dorsoventrally broad jaws. Non- morphospace (0.0 PCo1; 0.0 PCo3). Functional ceratopsid marginocephalian jaw morpho- loadings, interpretations for the first four logies, such as those of psittacosaurids and principal axes, and individual species leptoceratopsids, contribute strongly to the placement in morphospace can be found in expansion of ornithischian shape morphospace, the Supplementary Material. predominantly into +PC1/−PC2. Taxa are Morphospace Occupation through Time.— absent in a region of morphospace around Breakdown of shape and biomechanical +0.05 PC1/−0.075 PC2. morphospace into 20 Myr time bins highlights Biomechanical Morphospace Occupation.—Our patterns of morphospace occupation by each results demonstrate that sauropodomorph and clade through time (Figs. 4–6). Initial ornithischian taxa also occupy significantly occupation during the Late Triassic–Middle different regions of biomechanical morpho- Jurassic is dominated by sauropodomorphs, space (p < 0.01; Figs. 2, 3; Table 2). There is with low numbers of contemporaneous basal greater overlap in biomechanical morphospace ornithischians (e.g., heterodontosaurids and occupation than shape morphospace, with 16–20 thyreophorans). In the bin representing the

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FIGURE 2. Patterns of biomechanical morphospace occupation for herbivorous nonavian ornithischian and sauropodomorph dinosaurs. PCo1 and PCo2 account for 25.2% of variation. Ornithischian and sauropodomorph taxa occupy signiﬁcantly different regions of biomechanical morphospace (p < 0.05). Filled circles, Sauropodomorpha; open circles, Ornithischia. Silhouettes represent jaw biomechanical proﬁles found in that region of biomechanical morphospace.

20 Myr prior to the J/K boundary (165–145 Ma), expansion in disparity by marginocephalians thyreophorans, ornithopods, marginocepha- and, later, ornithopods (Figs. 4–6, 145–65 Ma). lians, and heterodontosaurids all occupy By the Early Cretaceous, the surviving Jurassic similar regions of shape morphospace, yet at herbivorous dinosaur clades (sauropodo- this time, the same clades occupy disparate morphs, marginocephalians, ornithopods, and regions of biomechanical morphospace with thyreophorans) are statistically distinct in both little overlap (Figs. 5, 6; 165–145 Ma, Table 3). shape and biomechanical morphospace Sauropodomorphs at this time show signi- (Table 2). Sauropodomorphs display substan- ﬁcantly different biomechanical occupation tially reduced variation, whereas ankylosaurs, to stegosaurs and ornithopods, but not ceratopsians, and ornithopods expand into heterodontosaurids or the basal ceratopsian hitherto unoccupied regions of biomechanical Yinlong (NPMANOVA, p < 0.01; Table 3). The morphospace. Marginocephalians (e.g., sauropodomorphs are biomechanically diverse Psittacosaurus) share areas of biomechanical prior to the J/K boundary, occupying the region morphospace with iguanodontians but occupy of morphospace that correlates to high tooth very different regions of shape space (Fig. 4, height:base, high mechanical advantages, and 145–105 Ma). large mandibular fenestrae. After the J/K In the latest Cretaceous, the four clades boundary, morphospace and biomechanical present occupy distinct regions of shape mor- morphospace plots show a drop in sauropo- phospace (p < 0.01; Table 2), with the exception domorph morphological and biomechanical of one marginocephalian taxon (Stegoceras) that variation as sample size diminishes and plots between nonhadrosaurid ornithopods

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FIGURE 3. Patterns of biomechanical morphospace occupation for herbivorous nonavian ornithischian and sauropodomorph dinosaurs. PCo1 and PCo3 account for 23.9% of variation. Ornithischian and sauropodomorph taxa occupy signiﬁcantly different regions of biomechanical morphospace (p < 0.05). Filled circles, Sauropodomorpha; empty circles, Ornithischia. Silhouettes represent jaw biomechanical proﬁles found in that region of biomechanical morphospace.

and ankylosaurians (Fig. 4, 85–65 Ma). Bio- (Figs. 5, 6). Full details of the biomechanical mechanically, Stegoceras is nested among character loadings are described in the ornithopods and is closer to sauropods than Supplementary Appendix 5. many contemporaneous ceratopsians. Corre- Disparity.—Morphological (shape) and sponding biomechanical morphospace plots biomechanical disparity measures are show a very different trend. Margin- decoupled through the Mesozoic (Fig. 7). ocephalians overlap with both ornithopods Morphological disparity primarily tracks and thyreophorans. Thyreophorans and sample diversity (Fig. 7A): it does not ornithopods do not overlap, and saur- fluctuate greatly through the first 80 Myr of opodomorphs overlap minimally with orni- dinosaur evolution, begins to increase from the thopods (Figs. 5, 6, 85–65 Ma). Whereas Middle Jurassic onward, and reaches a peak in variation in marginocephalian jaw shape the Late Cretaceous (Fig. 7A). There are no and biomechanics increases throughout the significant differences in disparity between Cretaceous, ornithopod shape and biomechanical time bins (p > 0.05). By contrast, biomechanical variation remains constant throughout the Late disparity undulates through the Mesozoic Cretaceous. Leptoceratopsids (e.g., Udanocera- (Fig. 7B), a decoupling from sample diversity tops, Montanoceratops) extend biomechanical and morphological diversity. Several small morphospace occupation into the region of peaks and troughs (for example the peak in the morphospace characterized by deep mandibles Late Jurassic) correspond to increased sample with short adductor muscle attachment size (Fig. 7B, diamond data points): however, and high posterior mechanical advantages time periods with greatest sample sizes do not

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TABLE 3. NPMANOVA signiﬁcance testing between clade occupations of biomechanical morphospace through time. Bold p-values represent signiﬁcant differences (at p < 0.05). SA, Sauropodomorpha; BO, Basal Ornithischia; TH, Thyreophora; OR, Ornithopoda; MA, Marginocephalia.

Time bin NPMANOVA p-values Clades SA BO

225–202 Ma SA — 0.114 BO 0.114 — Clades SA BO

202–185 Ma SA — 0.009 BO 0.009 — Clades SA BO TH

185–165 Ma SA — 0.142 1 BO 0.142 — 1 TH 1 1 — Clades SA BO TH OR MA

165–145 Ma SA — 0.505 0.009 0.015 1 BO 0.505 — 0.520 0.124 1 TH 0.009 0.520 — 0.158 1 OR 0.015 0.124 0.158 — 1 Clades SA OR MA

145–125 Ma SA — 0.084 0.003 OR 0.084 — 0.016 MA 0.003 0.016 — Clades SA TH OR MA

125–105 Ma SA — 0.186 <0.001 <0.001 TH 0.186 — 0.003 0.007 OR <0.001 0.003 — <0.001 MA <0.001 0.007 <0.001 — Clades SA TH OR MA

105–85 Ma SA — 0.164 0.002 0.043 TH 0.164 — 0.005 0.037 OR 0.002 0.005 — <0.001 MA 0.043 0.037 <0.001 — Clades SA TH OR MA

85–65 Ma SA — <0.001 <0.001 <0.001 TH <0.001 — <0.001 <0.001 OR <0.001 <0.001 — <0.001 MA <0.001 <0.001 <0.001 —

correspond to peaks in biomechanical disparity of 8. There are a few instances where disparity (during the latest Cretaceous, for example). The diverges markedly from sample size, peak in the latest Jurassic also corresponds with suggesting that a trend, albeit nonsigniﬁcant, the presence of high-browsing sauropodo- might be observed. For example, morphological morphs (>9 m), which display a higher degree disparity rises in the Early Cretaceous, of biomechanical disparity than some lower- immediately after the J/K extinction, and in browsing forms (p > 0.05; see Supplementary the early Late Cretaceous, while sample size Fig. 10). There are no signiﬁcant differences drops. Likewise, biomechanical disparity drops in disparity between successive time bins in the Middle Jurassic while sample size rises for either biomechanical or morphological slightly. Conversely, in the latest Cretaceous, disparity curves (at p = 0.05) and no marginal- sample size rises sharply while biomechanical likelihood values exceed the threshold value disparity drops very slightly.

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FIGURE 4. Patterns of morphospace occupation for herbivorous nonavian dinosaurs through the Mesozoic (20 Myr time bins), based on PC1 and PC2 (accounting for 50.4% of variation). Sauropodomorpha occupy isolated regions of morphospace for the majority of the Mesozoic, with overlap between North American sauropods and thyreophorans between 185 and 145 Ma.

Discussion Carnian (225 Ma) to the Tr/J boundary, across which there is a further nonsignificant decrease Impact of Extinction on Herbivorous Dinosaur (Fig. 7B). The placement of taxa in biomechanical Disparity.—Our results from both morpho- morphospace suggests that both ornithischian logical and biomechanical disparity curves and sauropodomorph taxa share similar support conclusions from previous studies biomechanical profiles immediately before and examining dinosaur disparity around after the Tr/J boundary (Figs. 5, 6). By contrast, extinction events (Brusatte et al. 2008a, 2012). the transition across the J/K boundary shows a Morphological disparity across the Tr/J decoupled relationship between biomechanical boundary increases slightly, likely triggered and morphological disparity (Fig. 7). Morpho- by the addition of heterodontosaurid jaw profiles logical disparity after the J/K boundary increases to the morphospace (Fig. 7B). Biomechanical sharply: this pattern can be attributed to the disparity decreases from an initial peak in the presence of novel jaw morphologies such

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FIGURE 5. Patterns of biomechanical morphospace occupation for herbivorous nonavian dinosaurs through the Mesozoic (20 Myr time bins), based on PCo1 and PCo2 (accounting for 25.2% of variation). Sauropodomorphs predominantly overlap only with heterodontosaurids (202–145 Ma). Aptian–Maastrichtian marginocephalians and ornithopods occupy similar regions of morphospace (125–65 Ma).

as those of psittacosaurids and early disparity shows a decrease across the J/K hadrosauroids in combination with those of boundary (Fig. 7B). The majority of the new sauropod clades (Fig. 4, 145–125 Ma). biomechanical proﬁles exhibited prior to the It should be noted that this disparity increase J/K boundary do not persist into the earliest is nonsigniﬁcant, likely due to the low taxon Cretaceous (Figs. 5, 6, 145–125 Ma), which is count (n = 5). The lack of many dinosaur-bearing consistent with the fundamental faunal turnover formations between the Berriasian and Albian that takes place and the proliferation of may partially account for the low species marginocephalian and ornithopod taxa (e.g., richness observed in this interval, although it Bakker 1978; Weishampel and Norman 1989; could also be attributed to the J/K extinction Barrett and Willis 2001). Finally, our results event (Barrett et al. 2009; Upchurch et al. 2011). concur with disparity patterns observed in the Nevertheless, shape variation at this time does latest Cretaceous leading to the Cretaceous/ not track sample diversity. Biomechanical Paleogene (K/Pg) mass extinction (Brusatte et al.

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FIGURE 6. Patterns of biomechanical morphospace occupation for herbivorous nonavian dinosaurs through the Mesozoic (20 Myr time bins), based on PCo1 and PCo3 (accounting for 23.9% of variation). Sauropodomorphs overlap very little with contemporaneous taxa before the latest Cretaceous (85–65 Ma). Albian–Maastrichtian marginocephalians and thyreophorans occupy similar regions of biomechanical morphospace (105–65 Ma).

2012): both morphological and biomechanical Limited overlap between these clades suggests curves show a decrease in disparity from the little competition between ornithischians and Campanian to the Maastrichtian, despite a sauropodomorphs in feeding function, notable increase in sample size. particularly during the latter part of the Patterns of Morphospace Occupation.—Discrete Mesozoic (see also Barrett and Upchurch 2005). morphospace occupation suggests that, when However, where overlap does occur, it tends to considered as a single data set, the jaws of be between the basal members of various sauropodomorphs and ornithischians are ornithischian clades (e.g., heterodontosaurids, differentinbothshapeandinjawbio- basal thyreophorans, and basal ceratopsians) mechanics (Figs. 1–3). Individual occupation of and sauropodomorphs. This suggests that early morphospace by each taxon is graphically ornithischians adopted similar morphological represented in Supplementary Figures 2–6. and mechanical attributes to their feeding

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FIGURE 7. Comparison of shape-based and biomechanical disparity curves across 10 Myr time bins based on sum of variance metric. (A) shape-based disparity; (B) biomechanical disparity. Morphological and biomechanical disparity curves are decoupled, with morphological disparity increasing through the Mesozoic and biomechanical disparity peaking in the latest Jurassic. Shaded region spans the 95% conﬁdence intervals based on 1000 bootstrap replicates. Disparity (dots) is plotted alongside jaw specimen sample size curve (diamonds). Flower represents earliest fossil angiosperms (Sun et al. 2002; Du and Wang 2015).

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apparatus as macronarian sauropodomorphs Jurassic sauropods such as Camarasaurus show (Supplementary Fig. 2, a–c). Later groups of some morphological overlap in mandibular ornithischians radiated into distinct areas of shape with stegosaurs. By contrast, these same morphospace (Figs. 4–6). Breakdown of mor- clades show minimal overlap in biomechanical phological and biomechanical morphospace morphospace: only Gigantspinosaurus into 20 Myr time bins shows that earlier (Stegosauria) and Manidens (Heterodontosau- sauropodomorphs are, in general, replaced in ridae) share occupation of Late Jurassic their biomechanical profiles by later sauropo- sauropodomorph biomechanical morphospace domorphs through the Jurassic and Cretaceous (Supplementary Figs. 3,b–c, 4,b–c). This suggests (Figs. 4–6). Sauropodomorph morphospace that mandibles with similar gross morphology occupation shows a degree of migration were biomechanically and functionally through time, with basal sauropodomorphs differentiated by this time. In general, sauropo- occupying different regions of morphospace to domorphs and heterodontosaurids occupy Jurassic and Cretaceous neosauropods (Figs. 4–6, similar regions of both shape-based and filled circles). Some later sauropods show biomechanical morphospace and do not extend convergence in biomechanical profile with their occupation of morphospace beyond regions other, earlier forms. For example, the macro already occupied by the end of the Early Jurassic narian Camarasaurus occupies very similar (Figs. 4–6). From the Middle Jurassic onward, regions of morphospace to the earlier diverg- there is slight expansion of morphospace ing eusauropod Datousaurus (Supplementary along PC1 by diplodocoid sauropodomorphs Fig. 2a–c), despite the former existing around and Jurassic ornithopods (e.g., Camptosaurus), 10 Myr earlier: this pattern supports the results of which is also reflected in the morphological another recent quantitative craniodental study disparity curve (Fig. 4, 165–145 Ma; Fig. 7A). (Button et al. 2014). Similarly, the titanosaurid Morphological disparity shows an increase from Antarctosaurus occupies biomechanical morpho- the latest Jurassic through the Cretaceous with space almost identical to the basal macronarian the evolution of new groups of ornithischian Abrosaurus (Supplementary Fig. 2a–c). Perhaps dinosaurs, particularly marginocephalians. surprisingly, we find minimal convergent Early Cretaceous marginocephalians (psit- occupation in biomechanical morphospace tacosaurids, Archaeoceratops, and Liaoceratops) between titanosaurids (e.g., Antarctosaurus)and occupy novel regions of morphological and diplodocids (e.g., Diplodocus) (Supplementary biomechanical morphospace: these taxa share Fig. 2a–c: see also Button et al. 2014). This regions of biomechanical morphospace with patternisincontrasttoshape-basedmorpho- hadrosauroids until the disappearance of basal space (this study), in which these groups occupy marginocephalians prior to the last 20 Myr of similar regions of morphospace (Fig. 1 and the Mesozoic (Figs. 4–6, 85–65 Ma). Regions of Supplementary Fig. 2). Both shape-based and biomechanical morphospace formerly occu- biomechanical morphospace patterns show pied by psittacosaurids were then occupied extensive overlap between phylogenetically exclusively by derived hadrosaurids and separate groups of sauropodomorphs. Within ankylosaurs (Figs. 5, 6, 85–65 Ma). However, the sauropods, brachiosaurids are found to be the morphological profile of psittacosaurids biomechanically intermediate between basal was never replaced. The latest Cretaceous sees macronarian sauropods with short snouts and an expansion of biomechanical and shape- closely packed tooth rows (such as Camarasaurus) based morphospace by two distinct groups of and titanosaurids with longer snouts and marginocephalians: ceratopsids (e.g., Tricera- pencil-like teeth (such as Antarctosaurus), and tops) and leptoceratopsids (e.g., Udanoceratops). diplodocids are outliers in this biomechanical The biomechanical profiles of ceratopsids morphospace. This pattern supports quantitative show no overlap with those of hadrosaurids. work on sauropodomorph cranial morphology This supports the conclusions of Mallon and related to feeding, with similar placement of the Anderson (2013) who, in their study of herbi- same taxa in cranial (Button et al. 2014) and vores from the Dinosaur Park Formation mandibular morphospace (this study). Late (Campanian), found that contemporaneous

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hadrosaurids, ankylosaurs, and ceratopsids gymnosperms, and pteridophytes; rise of occupied different feeding niches based upon angiosperms to ecological dominance) (e.g., differing cranial and mandibular mechanics Weishampel and Norman 1989; Tiffney 1992; and morphologies. This study also supports Mustoe 2007). Our results provide quantitative previous conclusions on niche partitioning evidence that the mandibles of sauropodo- between hadrosaurs and ceratopsids (Mallon morphs and ornithischians evolved different and Anderson 2013). However, this study also morphologies and biomechanical profiles, found that the majority of derived ceratopsids potentially enabling them to feed on different plot in similar regions of biomechanical mor- plants in different ways. Moreover, their phospace to contemporaneous ankylosaurs, in minimal overlap in biomechanical morpho- contrast to the conclusions of Mallon and space suggests that there was limited Anderson (2013). In addition, Asian ankylo- competition between ornithischians and sauro- saurs show biomechanical morphospace occu- podomorphs when feeding (see also Barrett pation more similar to leptoceratopsids than to and Upchurch 2005). Our data demonstrate ceratopsids or North American ankylosaurs. that there was no significant increase in the It should be noted, however, that neither biomechanical disparity of the feeding apparatus leptoceratopsids nor Asian ankylosaurs were of either major herbivorous dinosaur clade included in Mallon and Anderson (2013), that was coincident with the proliferation of which focused solely on the Dinosaur Park angiosperms (Fig. 7). Nevertheless, although Formation fauna. Leptoceratopsids expand this novel food source appears to have had into regions of shape-based and biomechanical no discernible impact on the mandibular morphospace that had no previous occupants: biomechanical morphospace occupation of their extreme mandibular morphologies herbivorous dinosaurs, patterns of morphological account for the peak in morphological disparity do show a marked increase coincident disparity in the latest Cretaceous (Fig. 7A). with the later Cretaceous proliferation of Contemporaneous taxa include ceratopsids angiosperms. This coincident increase is not and ankylosaurs that have similar biomecha- interpreted as indication of direct causality, nical profiles to each other (see above). This but reflects the appearance of the highly biomechanical similarity would cause disparity disparate ankylosaurid and leptoceratopsian to be low: however, the inclusion of the highly jaw morphotypes. disparate leptoceratopsids (in addition to Potential links to cycadophyte decline hadrosaurids and the rhabdodontid Zalmoxes) through the Late Jurassic–Early Cretaceous are leads to an increase in biomechanical disparity less clear. The Early Cretaceous decline in levels from the early Late Cretaceous. Margin- cycadophytes occurred at a time of major ocephalian, ornithopod, and thyreophoran bio- faunal change affecting dinosaur clades, but mechanical morphospace occupation in the previous analyses of dinosaur and plant dis- latest Cretaceous suggests that these groups, tribution have shown that few of the observed while varying from each other in mandibular changes in dinosaur faunas could be linked shape, also share a variety of functional and directly with cycadophyte decline (Butler et al. biomechanical traits relating to feeding. Late 2009b). Although reduced biomechanical Cretaceous hadrosaurids and ankylosaurids mandibular disparity across the J/K boundary filled the biomechanical roles vacated by Early does coincide with the onset of this event, Cretaceous nonhadrosaurid iguanodontians direct evidence of dinosaur herbivory on and nodosaurids, respectively. Individual cycads is sparse (Hummel et al. 2008; Butler occupation of morphospace by each taxon can et al. 2009b; Gee 2011), and other causes relat- be viewed in Supplementary Figures 2–6. ing to the poorly understood J/K extinction Dinosaur–Plant Coevolution.—Changes in may also be involved (Butler et al. 2011; dinosaur communities and feeding regimes Upchurch et al. 2011). In addition, morpholo- during the Late Jurassic–Early Cretaceous gical disparity after this extinction event shows interval have been linked to several major a notable increase, with different clades of floristic changes (decline of cycadophytes, dinosaurs diversifying into new, unexplored

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regions of mandibular morphospace (e.g., diversity in the Cretaceous. The addition of psittacosaurids, early titanosaurs). Results titanosaurid taxa to the analysis may increase from this study do not support a coevolu- both the disparity and overall morphospace tionary relationship between herbivorous occupation of sauropodomorphs, although the dinosaur mandibular disparity and angios- titanosaur jaws sampled in this study already perm proliferation and show a similarly account for a broad range of morphologies negative relationship to the decline of cycado- (Supplementary Fig. a–c, taxon 37–44). phytes. Rather, patterns of mandibular shape Supplementary analyses of biomechanical and mechanical diversity seem to be most and shape-based disparity within sauropodo- greatly affected by the extinction and emer- morphs in relation to maximum feeding height gence of different dinosaurian clades. show higher levels of disparity in high-browsing Sampling Issues.—When disparity tracks sauropods (>9 m; e.g., Brachiosaurus, Mamenchi- sample diversity closely, as it does in this saurus) when compared with mid-browsing taxa study for shape-based disparity, sampling bias (6–9 m; e.g., Camarasaurus), and almost equal cannot be ruled out. Morphological disparity indisparitytoverylow-browsingsauropo- in this study partly tracks jaw sample size, domorphs (0–3m; e.g., Pantydraco, Riojasaurus) suggesting a potential bias in the data set for (see Supplementary Fig. 10). This pattern con- some features of the disparity curve (e.g., high trasts with sample diversity, with the lowest sample and disparity in latest Cretaceous; sample size found in the high-browsing feeding Fig. 7A). The use of the sum of variance envelope (n = 6) (Supplementary Fig. 10). disparity measure and bootstrapping the data Unfortunately, low sample sizes within each has accounted for sample size as best as is feeding level prevent any significant differences possible for the data set (Foote 1992, 1994; or definitive conclusions to be made. However, Ciampaglio et al. 2009) (Fig. 7A). Peaks of high this pattern remains intriguing and the addi- shape disparity in the earliest Cretaceous and tion of more mandibular remains from high- early Late Cretaceous do not correlate with and mid-browsing taxa to our sample (as and peaks in sample size. Biomechanical variation when they are discovered) would complement displays a different trend, demonstrating a this study. This is an avenue of study that decoupling of morphological and biomechanical requires more investigation in the future to diversity through time. A peak in biomechanical enable deeper insights into niche partitioning disparity in the Late Jurassic is coincident with between sauropod groups based on maximum an increase in jaw sample size, but also browse height. corresponds to the evolution of high-browsing Relatively few Early Cretaceous sauro- (>9 m) sauropods (e.g., Upchurch and Barrett podomorph, thyreophoran, or marginocephalian 2000). In addition, many of the sauropod taxa in taxa possess well-preserved mandibular mate- this time slice are recovered from the Morrison rial (see list of taxa in Supplementary Material). FormationofthewesternUnitedStates(n = 6out The dip in biomechanical disparity after the of a total of 14 sauropods). The exclusion of the J/K recovered by our analyses may, therefore, Morrison taxa removes the Late Jurassic peak in be an artefact due to either geological biases or biomechanical disparity (Supplementary Fig. 8i). uneven collection effort, underrepresenting the A similar jackknifing of the taxa from the true diversity of jaw biomechanical profiles at Dashanpu Formation (including the “Upper this time. Due to the lack of complete mand- and Lower Shaximiao” formations) yielded a ibles from rebbachisaurids, dicraeosaurids, trough in disparity in the Middle Jurassic but and other clades, it is possible that the latest retained a strong peak in the latest Jurassic Jurassic and earliest Cretaceous disparity (Supplementary Fig. 8ii). These results suggest levels reported herein are currently under- that the data may be sensitive to the inclusion or sampling the total diversity of mandible exclusion of particularly rich fossil-bearing sites. morphology and potential function. Such In addition, the lack of available jaw material exclusions cannot be corrected for by our ana- fromNorthandSouthAmericantitanosaurs lyses and represent a limitation of the fossil seriously underrepresents sauropodomorph material currently available.

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Conclusions filled by Late Cretaceous leptoceratopsids (e.g., Udanoceratops), a group that is also present in For the first time, we have quantified the North America. Late Cretaceous hadrosaurids morphological and biomechanical variation of and ankylosaurids filled the biomechanical roles ornithischian and sauropodomorph jaws vacated by Early Cretaceous nonhadrosaurid throughout the Mesozoic and examined how iguanodontians and nodosaurids respectively. diversity related to external extrinsic drivers Our results imply that, after the establishment of such as extinction events and the rise of peak overall biomechanical variation in the angiosperms. We find that herbivorous dino- latest Jurassic, only marginocephalians demon- saur clades have jaws that occupy different strated widespread variation in biomechanical regions of morphospace throughout the profiles over time, triggered by the isolated Mesozoic. Furthermore, sauropodomorphs and adaptive radiations of psittacosaurids and ornithischians have jaws that also function in leptoceratopsians. The remainder of Cretaceous broadly different ways, yet there is some herbivorous dinosaurs underwent progressive potentially convergent overlap in biomechanical niche replacement, with successive replacement function between different ornithischian clades by related taxa with comparable biomechanical in the Cretaceous. Basal members of each clade profiles. tend to be more similar in form and function to each other, while derived taxa are more functionally and morphologically divergent. Herbi- Acknowledgments vorous dinosaur jaws maintained a numerically The authors would like to thank D. Button steady diversity of biomechanical traits, with a and T. Stubbs (both University of Bristol) for peak observed in the Late Jurassic triggered by fi taxonomic and methodological discussion and the diversi cation of high-browsing sauropods. S. Chapman (NHM) for specimen provision. This is consistent with a rapid evolutionary Funding support was received from the Bob radiation in biomechanical diversity among Savage Fund of University of Bristol and from herbivorous dinosaurs followed by a plateau. a BBSRC grant BB/I011668/1 awarded to The Tr/J extinction had no overall effect on E.J.R. Helpful reviews of this contribution were biomechanical variation among herbivorous received from J. Whitlock and an anonymous dinosaurs, despite fundamental changes in fl referee. P.S.L.A., E.J.R., and P.M.B. conceived oral and faunal composition across the bound- and developed the project idea. J.A.M. col- ary. This consistency suggests that Early Jurassic fi lected the data and performed the analyses. dinosaurs lled the functional feeding niches J.A.M., along with P.S.L.A., E.J.R., and P.M.B. vacated by the extinction of Late Triassic taxa. interpreted the data. All authors contributed to Similar successive replacement patterns are also writing the manuscript. J.A.M. designed and seen in Devonian gnathostomes and Devo- prepared the figures. nian to mid-Pennsylvanian tetrapodomorphs (Anderson et al. 2011, 2013). Biomechanical disparity across the J/K boundary suggests that Literature Cited large-scale faunal turnover at this time did affect Anderson, P. S. L. 2009. Biomechanics, functional patterns, and mandibular disparity, which did not recover to disparity in Late Devonian arthrodires. Paleobiology 35: pre-J/K disparity levels through the Cretaceous 321–342. (Fig. 7). A diverse fauna of high-browsing Anderson, P. S. L., M. Friedman, M. D. Brazeau, and E. J. Rayfield. 2011. Initial radiation of jaws demonstrated stability despite sauropods did not persist into the Early Cretac- faunal and environmental change. Nature 476:206–209. eous, and the sauropodomorph contribution to Anderson, P. S. L., M. Friedman, and M. Ruta. 2013. Late to the overall disparity wanes through the Cretaceous, table: diversification of tetrapod mandibular biomechanics lagged behind the evolution of terrestriality. Integrative and despite a later increase in their Late Cretaceous Comparative Biology 53:197–208. species richness. The highly specialized Apesteguía, S. 2004. Bonitasaura salgadoi gen. et sp. nov.: a beaked psittacosaurids were not replaced in their sauropod from the Late Cretaceous of Patagonia. Nat- fi urwissenschaften 91:493–497. biomechanical pro le. However, their role as a Bakker, R. T. 1978. Dinosaur feeding behaviour and the origin of biomechanically disparate group in Asia is later flowering plants. Nature 274:661–663.

Downloaded from http://pubs.geoscienceworld.org/paleobiol/article-pdf/43/1/15/2924671/S0094837316000312a_hi.pdf by guest on 02 October 2021 32 JAMIE A. MACLAREN ET AL.

Barrett, P. M. 2014. Paleobiology of herbivorous dinosaurs. Annual Biology of the sauropod dinosaurs: understanding the life of Review of Earth and Planetary Sciences 42:207–230. giants. Indiana University Press, Indianapolis. Barrett, P. M., and K. J. Willis. 2001. Did dinosaurs invent flowers? Hammer, Ø., D. A. T. Harper, and P. D. Ryan. 2001. Paleontological Dinosaur–angiosperm coevolution revisited. Biological Reviews statistics software package for education and data analysis. 76:411–447. Palaeontologia Electronica 4:9. Barrett, P. M., and P. M. Upchurch. 2005. Sauropodomorph diver- Holm, S. 1979. A simple sequentially rejective multiple test proce- sity through time. Pp. 125–128 in K. A. Curry Rogers, and dure. Scandinavian Journal of Statistics 6:65–70. J. A. Wilson, eds. The sauropods: evolution and paleobiology. Hummel, J., C. T. Gee, K.-H. Südekum, P. M. Sander, G. Nogge, and University of California Press, Berkeley. M. Clauss. 2008. In vitro digestibility of fern and gymnosperm Barrett, P. M., A. J. McGowan, and V. Page. 2009. Dinosaur diver- foliage: implications for sauropod feeding ecology and diet sity and the rock record. Proceedings of the Royal Society B selection. Proceedings of the Royal Society B 275:1015–1021. 276:2667–2674. Hylander, W. L., and K. R. Johnson. 1997. In vivo bone strain patterns Brusatte, S. L., M. J. Benton, M. Ruta, and G. T. Lloyd. 2008a. in the zygomatic arch of macaques and the significance of these The first 50 Myr of dinosaur evolution: macroevolutionary patterns for functional interpretations of craniofacial form. Amer- pattern and morphological disparity. Biology Letters 4: ican Journal of Physical Anthropology 102:203–232. 733–736. Hylander, W. L., P. G. Picq, and K. R. Johnson. 1991. Masticatory- ——. 2008b. Superiority, competition, and opportunism in the stress hypotheses and the supraorbital region of primates. evolutionary radiation of dinosaurs. Science 321:1485–1488. American Journal of Physical Anthropology 86:1–36. Brusatte, S. L., R. J. Butler, A. Prieto-Márquez, and M. A. Norell. Irmis, R. B. 2011. Evaluating hypotheses for the early diversification 2012. Dinosaur morphological diversity and the end-Cretaceous of dinosaurs. Earth and Environmental Science Transactions of extinction. Nature Communications 3:804. the Royal Society of Edinburgh 101:397–426. Butler, R. J., P. M. Barrett, P. Kenrick, and M. G. Penn. 2009a. Lloyd,G.T.,K.E.Davis,D.Pisani,J.E.Tarver,M.Ruta,M.Sakamoto, Diversity patterns amongst herbivorous dinosaurs and plants D. W. E. Hone, R. Jennings, and M. J. Benton. 2008. Dinosaurs and during the Cretaceous: implications for hypotheses of dinosaur/ the Cretaceous terrestrial revolution. Proceedings of the Royal angiosperm co-evolution. Journal of Evolutionary Biology 22: Society B 275:2483–2490. 446–459. Mallon, J. C., and J. S. Anderson. 2013. Skull ecomorphology of ——. 2009b. Testing co-evolutionary hypotheses over geological megaherbivorous dinosaurs from the dinosaur park formation timescales: interactions between Mesozoic non-avian dinosaurs (upper Campanian) of Alberta, Canada. PloS ONE 8:e67182. and cycads. Biological Reviews 84:73–89. Mustoe, G. 2007. Coevolution of cycads and dinosaurs. Cycad Butler, R. J., P. M. Barrett, M. G. Penn, and P. Kenrick. 2010. Testing Newsletter 30:6–9. coevolutionary hypotheses over geological timescales: interac- Navarro, N. 2003. MDA: a MATLAB-based program for morphospace- tions between Cretaceous dinosaurs and plants. Biological disparity analysis. Computers and Geosciences 29:655–664. Journal of the Linnean Society 100:1–15. Niklas, K. J. 1992. Plant biomechanics. University of Chicago Press, Butler, R. J., R. B. J. Benson, M. T. Carrano, P. D. Mannion, and Chicago. P. Upchurch. 2011. Sea level, dinosaur diversity and sampling Peyer, K., and R. Allain. 2010. A reconstruction of Tazoudasaurus biases: investigating the “common cause” hypothesis in the naimi (Dinosauria, Sauropoda) from the late Early Jurassic of terrestrial realm. Proceedings of the Royal Society B 278: Morocco. Historical Biology 22:134–141. 1165–1170. Rohlf, F. J. 2004. tpsDig. Department of Ecology and Evolution, Butler, R. J., S. L. Brusatte, B. Andres, and R. B. J. Benson. 2012. How State University of New York, Stony Brook, N.Y. do geological sampling biases affect studies of morphological ——. 2008. tpsRelW. Department of Ecology and Evolution, State evolution in deep time? A case study of pterosaur (Reptilia: University of New York, Stony Brook, N.Y. Archosauria) disparity. Evolution 66:147–162. Romer, A. S. 1956. Osteology of the reptiles. University of Chicago Button, D. J., E. J. Rayfield, and P. M. Barrett. 2014. Cranial Press, Chicago. biomechanics underpins high sauropod diversity in resource- Sakamoto, M. 2010. Jaw biomechanics and the evolution of biting poor environments. Proceedings of the Royal Society B 281: performance in theropod dinosaurs. Proceedings of the Royal 20142114. Society of London B 277:3327–3333. Ciampaglio, C. N., M. Kemp, and D. W. McShea. 2009. Detecting Sander, P. M., O. Mateus, T. Laven, and N. Knótschke. 2006. Bone changes in morphospace occupation patterns in the fossil histology indicates insular dwarfism in a new Late Jurassic record: characterization and analysis of measures of disparity. sauropod dinosaur. Nature 441:739–741. Paleobiology 27:695–715. Sereno, P. C. 1997. The origin and evolution of dinosaurs. Annual Du, Z.-Y., and Q.-F. Wang. 2015. Phylogenetic tree of vascular Review of Earth and Planetary Sciences 25:435–489. plants reveals the origins of aquatic angiosperms. Journal of ——. 1999. The evolution of dinosaurs. Science 284:2137–2147. Systematics and Evolution 54:342–348. Sookias, R. B., R. J. Butler, and R. B. J. Benson. 2012. Rise of Finarelli, J. A., and J. J. Flynn. 2007. The evolution of encephaliza- dinosaurs reveals major body-size transitions are driven by tion in caniform carnivorans. Evolution 61:1758–1772. passive processes of trait evolution. Proceedings of the Royal Foote, M. 1992. Rarefaction analysis of morphological and Society B 279:2180–2187. taxonomic diversity. Paleobiology 18:1–16. Stevens, K. A. 2013. The articulation of sauropod necks: ——. 1994. Morphological disparity in Ordovician–Devonian methodology and mythology. PloS ONE 8:e78572. Crinoids and the Early Saturation of Morphological Space. Stubbs, T. L., S. E. Pierce, E. J. Rayfield, and P. S. L. Anderson. 2013. Paleobiology 20:320–344. Morphological and biomechanical disparity of crocodile-line Foth, C., and O. W. M. Rauhut. 2013. The good, the bad, and the archosaurs following the end-Triassic extinction. Proceedings of ugly: the influence of skull reconstructions and intraspecific the Royal Society B 280:20131940. variability in studies of cranial morphometrics in theropods and Sun, G., Q. Ji, D. L. Dilcher, S. Zheng, K. C. Nixon, and X. Wang. basal saurischians. PLoS One 8:e72007. 2002. Archaefructaceae, a new basal angiosperm family. Science Gee, C. T. 2011. Dietary options for the sauropod dinosaurs 296:899–904. from an integrated botanical and paleobotanical perspective. Tiffney, B. H. 1992. The role of vertebrate herbivory in the evolution Pp. 34–56 in N. Klein, K. Remes, C. T. Gee, and P. M. Sander, eds. of land plants. Palaeobotanist 41:87–97.

Downloaded from http://pubs.geoscienceworld.org/paleobiol/article-pdf/43/1/15/2924671/S0094837316000312a_hi.pdf by guest on 02 October 2021 HERBIVOROUS DINOSAUR JAW DISPARITY 33

Upchurch, P. M., and P. M. Barrett. 2000. The evolution of Weishampel, D. B., and D. B. Norman. 1989. Vertebrate herbivory sauropod feeding mechanisms. Pp. 79–122. in H.-D. Sues, in the Mesozoic; jaws, plants, and evolutionary metrics. Geolo- ed. Evolution of herbivory in terrestrial vertebrates: gical Society of America Special Paper 238:87–101. perspectives from the fossil record. Cambridge University Press, Weishampel, D. B., P. Dodson, and H. Osmolska. 2004. The Cambridge. Dinosauria. University of California Press, Berkeley. ——. 2005. Phylogenetic and taxic perspectives on sauropod Whitlock, J. A. 2011. Inferences of diplodocoid (Sauropoda: diversity. Pp. 104–124 in K. A. Curry Rogers, and J. A. Wilson, Dinosauria) feeding behavior from snout shape and microwear eds. The sauropods: evolution and paleobiology. University of analyses. PLoS ONE 6:e18304. California Press, Berkeley. Wills, M. A., D. E. G. Briggs, and R. A. Fortey. 1994. Disparity as an Upchurch, P. M., P. D. Mannion, R. B. J. Benson, R. J. Butler, and evolutionary index: a comparison of Cambrian and Recent M. T. Carrano. 2011. Geological and anthropogenic controls on arthropods. Paleobiology 20:93–130. the sampling of the terrestrial fossil record: a case study from the Young, M. T., and M. D. Larvan. 2010. Macroevolutionary trends in Dinosauria. Geological Society of London Special Publications the skull of sauropodomorph dinosaurs—the largest terrestrial 358:209–240. animals to have ever lived. In A. M. T. Elewa, ed. Morphometrics Weishampel, D. B. 1984. Interactions between Mesozoic for nonmorphometricians: lecture notes in Earth sciences plants and vertebrates: fructiﬁcations and seed predation. Neues 124:259–269. Springer, Berlin. Jahrbuch für Geologie und Paläontologie, Abhandlungen Zelditch, M. L., D. L. Swiderski, and H. D. Sheets. 2012. Geometric 167:224–250. morphometrics for biologists: a primer. Academic, New York.

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