Osteoderms of the titanosaur sauropod dinosaur <i>Alamosaurus sanjuanensis</i> Gilmore, 1922

<div><p>SUPPLEMENTAL DATA—Supplemental materials are available for this article for free at www.tandfonline.com/UJVP; CT data are available as Morphobank project P2093 at http://www.morphobank.org.</p></div

Evolution of high tooth replacement rates in theropod dinosaurs

© 2019 D’Emic et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Tooth replacement rate is an important contributor to feeding ecology for polyphyodont animals. Dinosaurs exhibit a wide range of tooth replacement rates, mirroring their diverse craniofacial specializations, but little is known about broad-scale allometric or evolutionary patterns within the group. In the current broad but sparse dinosaurian sample, only three non-avian theropod tooth replacement rates have been estimated. We estimated tooth formation and replacement rates in three additional non-avian theropod dinosaurs, the derived latest Cretaceous abelisaurid Majungasaurus and the more generalized Late Jurassic Allosaurus and Ceratosaurus. We created the largest dental histological and CT dataset for any theropod dinosaur, sectioning and scanning over a dozen toothed elements of Majungasaurus and several additional elements from the other two genera. Using this large sample, we created models of tooth formation time that allow for theropod replacement rates to be estimated non-destructively. In contrast to previous results for theropods, we found high tooth replacement rates in all three genera, with Allosaurus and Ceratosaurus rates of ~100 days and 56 days for Majungasaurus. The latter rate is on par with those of derived herbivorous dinosaurs including some neosauropods, hadrosaurids, and ceratopsians. This elevated rate may be a response to high rates of tooth wear in Majungasaurus. Within Dinosauria, there is no relationship between body mass and tooth replacement rate and no trends in replacement rate over time. Rather, tooth replacement rate is clade-specific, with elevated rates in abelisaurids and diplodocoids and lower rates in coelurosaurs

Summary of enamel thickness (mm) in <i>Diplodocus</i> (YPM 4677) and <i>Camarasaurus</i> (UMNH 5527) at different tooth developmental stages (i–v).

<p>Summary of enamel thickness (mm) in <i>Diplodocus</i> (YPM 4677) and <i>Camarasaurus</i> (UMNH 5527) at different tooth developmental stages (i–v).</p

Evolution of High Tooth Replacement Rates in Sauropod Dinosaurs

<div><p>Background</p><p>Tooth replacement rate can be calculated in extinct animals by counting incremental lines of deposition in tooth dentin. Calculating this rate in several taxa allows for the study of the evolution of tooth replacement rate. Sauropod dinosaurs, the largest terrestrial animals that ever evolved, exhibited a diversity of tooth sizes and shapes, but little is known about their tooth replacement rates.</p><p>Methodology/Principal Findings</p><p>We present tooth replacement rate, formation time, crown volume, total dentition volume, and enamel thickness for two coexisting but distantly related and morphologically disparate sauropod dinosaurs <i>Camarasaurus</i> and <i>Diplodocus</i>. Individual tooth formation time was determined by counting daily incremental lines in dentin. Tooth replacement rate is calculated as the difference between the number of days recorded in successive replacement teeth. Each tooth family in <i>Camarasaurus</i> has a maximum of three replacement teeth, whereas each <i>Diplodocus</i> tooth family has up to five. Tooth formation times are about 1.7 times longer in <i>Camarasaurus</i> than in <i>Diplodocus</i> (315 vs. 185 days). Average tooth replacement rate in <i>Camarasaurus</i> is about one tooth every 62 days versus about one tooth every 35 days in <i>Diplodocus</i>. Despite slower tooth replacement rates in <i>Camarasaurus</i>, the volumetric rate of <i>Camarasaurus</i> tooth replacement is 10 times faster than in <i>Diplodocus</i> because of its substantially greater tooth volumes. A novel method to estimate replacement rate was developed and applied to several other sauropodomorphs that we were not able to thin section.</p><p>Conclusions/Significance</p><p>Differences in tooth replacement rate among sauropodomorphs likely reflect disparate feeding strategies and/or food choices, which would have facilitated the coexistence of these gigantic herbivores in one ecosystem. Early neosauropods are characterized by high tooth replacement rates (despite their large tooth size), and derived titanosaurs and diplodocoids independently evolved the highest known tooth replacement rates among archosaurs.</p></div

Cladogram of sauropodomorphs showing the optimization of key features related to elevated tooth replacement rates.

<p>The light gray field indicates taxa that have at least three replacement teeth at each tooth position; dark gray field encapsulates taxa that have narrow tooth crowns. Silhouettes along the top of the cladogram show the number and size of replacement teeth in one tooth position. These include (from left to right): <i>Patagosaurus</i> (MPEF-PV 1670), <i>Mamenchisaurus</i> <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0069235#pone.0069235-Ouyang1" target="_blank">[47]</a>, <i>Diplodocus</i> (this study), <i>Nigersaurus</i> [Sereno, Wilson, Witmer, Whitlock, Maga, Ide and Rowe, unpublished data], <i>Camarasaurus</i> (this study), and the Río Negro titanosaur (MPCA-79) <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0069235#pone.0069235-Coria1" target="_blank">[48]</a>. Number of replacement teeth is unknown in Brachiosauridae, but the taxon is optimized to have had at least three. Cladogram based on <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0069235#pone.0069235-Wilson2" target="_blank">[30]</a> with the addition of <i>Tazoudasaurus</i> <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0069235#pone.0069235-Allain1" target="_blank">[49]</a> and <i>Bonitasaura</i> <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0069235#pone.0069235-Gallina1" target="_blank">[50]</a>. [planned for column width].</p

Tooth formation time (days) and replacement rate (1 tooth/X days) in <i>Diplodocus</i> (YPM 4677) and <i>Camarasaurus</i> (UMNH 5527).

<p>Tooth formation time (days) and replacement rate (1 tooth/X days) in <i>Diplodocus</i> (YPM 4677) and <i>Camarasaurus</i> (UMNH 5527).</p

Tooth replacement rates (days) for archosaurs.

<p>Tooth replacement rates (days) for archosaurs.</p

Estimated tooth formation times (ages) and replacement rates in several sauropodomorphs.

<p>Estimated tooth formation times (ages) and replacement rates in several sauropodomorphs.</p

Tooth replacement in the sauropod dinosaurs <i>Camarasaurus</i> and <i>Diplodocus</i>.

<p>Reconstructed skulls (<b>A</b>, <b>D</b>) and premaxillary teeth (<b>B</b>, <b>C</b>) of <i>Camarasaurus</i> (<b>A</b>, <b>B</b>) and <i>Diplodocus</i> (<b>C</b>, <b>D</b>). <b>B</b> and <b>C</b> include CT-generated sagittal and transverse sections of premaxillary alveoli and photographs of thin sections of <i>Camarasaurus</i> (UMNH 5527) and <i>Diplodocus</i> (YMP 4677). Premaxillae show replacement teeth in each of the four alveoli adjacent to the symphysis labelled by their position along the tooth row (1–4) and their position in the replacement sequence at each tooth position (i–v). Sagittal sections in <b>B</b> and <b>C</b> were taken at premaxillary tooth position 4 in <i>Camarasaurus</i> and premaxillary tooth position 1 in <i>Diplodocus</i>. The symphysis faces the bottom of the page in transverse sections. Photographs of thin sections of <i>Diplodocus</i> and <i>Camarasaurus</i> teeth show enamel (<b>en</b>), the pulp cavity (<b>pc</b>), daily-deposited incremental lines of von Ebner (arrowheads mark every other line) in the dentin (<b>den</b>), and the crown-root junction (<b>crj</b>). The 20 mm scale bar is for the premaxilla and tooth images in (<b>B</b>); 10 mm scale bar is for premaxilla and tooth images in (<b>C</b>). Skull reconstructions are from <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0069235#pone.0069235-Wilson1" target="_blank">[19]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0069235#pone.0069235-Whitlock2" target="_blank">[46]</a>[planned for page width].</p