Quantitative Analysis of Dental Microwear in Hadrosaurid Dinosaurs, and the Implications for Hypotheses of Jaw Mechanics and Feeding
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Quantitative analysis of dental microwear in hadrosaurid dinosaurs, and the implications for hypotheses of jaw mechanics and feeding Vincent S. Williamsa, Paul M. Barrettb, and Mark A. Purnella,1 aDepartment of Geology, University of Leicester, Leicester LE1 7RH, United Kingdom; and bDepartment of Palaeontology, Natural History Museum, Cromwell Road, London SW7 5BD, United Kingdom Edited by Peter R. Crane, University of Chicago, Chicago, IL, and approved May 5, 2009 (received for review December 11, 2008) Understanding the feeding mechanisms and diet of nonavian functional analogue, and no fossil evidence exists to show the dinosaurs is fundamental to understanding the paleobiology of size and shape of the interarticular fibrocartilages and the these taxa and their role in Mesozoic terrestrial ecosystems. Var- limitations these would have placed on jaw motions. Here, we ious methods, including biomechanical analysis and 3D computer present the results of quantitative tooth microwear analysis of a modeling, have been used to generate detailed functional hypoth- hadrosaurian dinosaur, and we demonstrate how these provide eses, but in the absence of either direct observations of dinosaur a robust test of functional hypotheses. feeding behavior, or close living functional analogues, testing Previous research into hadrosaurid feeding mechanisms these hypotheses is problematic. Microscopic scratches that form reached contradictory conclusions. The extensive early work of on teeth in vivo during feeding are known to record the relative Ostrom (7) suggested propalinal translation of the mandibles (an motion of the tooth rows to each other during feeding and to anteroposterior movement of the lower jaw during the power capture evidence of tooth–food interactions. Analysis of this dental stroke). This was later questioned (8), and tooth wear was used microwear provides a powerful tool for testing hypotheses of jaw to infer side-to-side (transverse) movements of the mandibles mechanics, diet, and trophic niche; yet, quantitative analysis of relative to the maxilla. Norman and Weishampel (6, 9–11) microwear in dinosaurs has not been attempted. Here, we show conducted kinematic and detailed functional anatomical analy- that analysis of tooth microwear orientation provides direct evi- ses of all available hypotheses of hadrosaurid jaw mechanics and dence for the relative motions of jaws during feeding in hadro- postulated a novel jaw mechanism, termed pleurokinesis. In this saurid ornithopods, the dominant terrestrial herbivores of the Late Cretaceous. Statistical testing demonstrates that Edmontosaurus model, isognathic vertical adduction of the lower jaws generated teeth preserve 4 distinct sets of scratches in different orientations. a transverse power stroke. This was brought about by lateral In terms of jaw mechanics, these data indicate an isognathic, rotation of the maxillae and suspensorium relative to the skull near-vertical posterodorsal power stroke during feeding; near- roof and driven by contact between the dentary and maxillary vertical jaw opening; and propalinal movements in near anterior teeth during occlusion. Lateral rotation of the maxillae was and near posterior directions. Our analysis supports the presence accommodated by a pleurokinetic hinge (between the maxilla/ of a pleurokinetic hinge, and the straightness and parallelism of jugal/quadrate and the akinetic skull) and was associated with scratches indicate a tightly controlled occlusion. The dominance of slight propalinal movements caused by abduction and retraction scratched microwear fabrics suggests that Edmontosaurus was a of the quadrate (streptostylism). However, recent work involving grazer rather than a browser. 3D modeling of feeding kinematics in Edmontosaurus has sug- gested that pleurokinesis would generate extensive secondary Cretaceous ͉ Ornithopoda ͉ tooth ͉ trophic ecology ͉ Vertebrata (intracranial) movements beyond the pleurokinetic hinge (12). Testing of these functional models has been difficult because of econstructing the feeding mechanisms and details of trophic the absence of direct evidence for the mastication process in Recology of extinct animals based on functional morphology is hadrosaurids. fraught with difficulty (1). In vertebrates, tooth form provides only Quantitative analysis of tooth microwear offers a hitherto a general guide to diet: the same tooth form can serve more than unexplored route to testing feeding mechanisms in nonavian one function, and that function can vary with specific feeding dinosaurs. Microwear refers to the microscopic polished, behavior. Further complications arise because functional optimi- scratched, or pitted textures produced in vivo by the actions of zation of tooth form can be constrained by the need to process abrasives in food and by the compressive and shearing forces that fallback foods during times of resource scarcity (2), and animals act on teeth during feeding (13, 14). Quantitative analysis of with an apparently specialized feeding apparatus can have gener- tooth microwear is an extremely powerful tool and has been alist diets (3). These problems are especially acute in groups like applied extensively to fossil primates and hominins to evaluate herbivorous, nonavian dinosaurs, where most species have gener- the role of dietary changes in human evolution (15, 16). Applied alized homodont dentitions and lack close living analogues. to extinct nonprimate mammals, quantitative tooth microwear Among herbivorous dinosaurs, feeding of hadrosaurids has analysis has also provided direct evidence of tooth use, diet, and attracted particular attention. They were the dominant herbiv- feeding (13, 17, 18) and has revealed how feeding in ungulates orous vertebrates in many Late Cretaceous ecosystems, in terms has tracked past environmental change (19). of both species richness and abundance, and they achieved a near-global distribution (4, 5). This success is frequently attrib- uted to the complex jaw mechanisms possessed by these taxa, Author contributions: V.S.W. and M.A.P. designed research; V.S.W. and M.A.P. performed which would have given them a level of masticatory prowess research; V.S.W. and M.A.P. analyzed data; and V.S.W., P.M.B., and M.A.P. wrote the paper. equal to that of many extant mammals (6). Current models of The authors declare no conflict of interest. feeding mechanisms in hadrosaurid dinosaurs are based on This article is a PNAS Direct Submission. analyses of functional morphology and rely on interpretations of 1To whom correspondence should be addressed. E-mail: [email protected]. musculature rather than direct evidence. No extant species has This article contains supporting information online at www.pnas.org/cgi/content/full/ a sufficiently similar skull morphology to act as a convincing 0812631106/DCSupplemental. 11194–11199 ͉ PNAS ͉ July 7, 2009 ͉ vol. 106 ͉ no. 27 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0812631106 B 2323 2222 2121 2020 1919 1818 1717 1616 1515 1414 1313 1212 1111 1010 9 8 7 6 5 4 3 2 1 10 mm mean orientations, 4 classes C0° 10 teeth 1 4 A 2 3 180° 20.13° D 11 5 mm 10 63.17° 1 9 64.56° E 115.62°100 µm Right Anteriorr LingualL PosteriorLabial Left 3 5 l Labial 8 2 6 4 F mean orientations, 4 classes 0° tooth 2, 11 sites 1 4 2 3 180° 7 24.14° 1 58.23° 1 left left right right 62.63° ° dentary maxilla dentary maxilla 115.84 Fig. 1. Microwear in Edmontosaurus.(A) Orientation of functional surfaces (wear facets) on teeth, in approximate life orientation; diagrams below show these same 4 functional surfaces oriented with tips upward and viewed perpendicular to the occlusal plane. (B) Right maxilla, specimen NHM R3638, anterior to left. Vector plots indicate mean scratch orientation and relative length for each of the 4 classes in 10 teeth, line weight proportional to number of scratches. (C) Mean orientations for each class of scratches in each of the 10 teeth; for each class, the mean of the mean orientations with 99% confidence interval is shown. Dashed lines lie outside the confidence interval. (D) Second tooth from posterior (box in B). Vector plots indicate mean scratch orientation and relative length for each of the 4 classes in 11 sites, line weight proportional to number of scratches. Gray boxes show sites sampled for transect data (Fig. S1): 1 toward tip, 6 toward base; site 7 more basal than field of view shown. (E) One of the sampled areas (black box in D); diagonal lower right shows feature markup from Microware 4.0.2. (F) Mean orientations for each class of scratches in each of the 11 sites; for each class, the mean of the mean orientations with 99% confidence interval is also shown. Dashed lines lie outside the confidence interval. Microwear analysis is starting to be applied widely to dino- Here, we test the null hypotheses that microwear does not saurs (20–23), and recent research on living and fossil fish differ between sample sites within the occlusal surface of a tooth suggests that quantitative microwear analysis has broad appli- and that microwear does not differ between teeth along a tooth cability beyond mammals (24, 25), but to date there has been no row within an individual. We show that hadrosaurid dinosaur quantitative analysis of tooth microwear in dinosaurs. However, teeth have well-developed microwear signatures that allow us to there are significant differences between dinosaur and mammal conduct robust statistical testing of these hypotheses, and we feeding mechanisms that make microwear analysis and inter- demonstrate that quantitative microwear