High-resolution CT-scan data reveals the tooth replacement pattern of the Late Jurassic tyrannosauroid Guanlong wucaii (Dinosauria, Theropoda)
Received date: 2024-04-15
Online published: 2024-07-15
The Tyrannosauridae, which is characterized by specialized pachydont dentition and putative bone-cracking predatory strategies, is one of the most extensively studied theropod lineages. Although tooth replacement patterns, crucial for understanding feeding behaviors, have been thoroughly studied in this group, studies on non-tyrannosaurid tyrannosauroids are relatively scarce. This study utilizes high-resolution CT data to investigate the tooth replacement pattern in two specimens of Guanlong wucaii , a Late Jurassic tyrannosauroid, and provides insights into the evolution of tooth replacement across Tyrannosauroidea. Second-generation replacement teeth, a rarity observed mainly in giant predatory theropods (e.g. some tyrannosaurids), were detected in the dentary dentition of the juvenile Guanlong . Zahnreihen reconstructions display a consistent cephalad alternating tooth replacement pattern in the maxilla and the dentary of both of the examined individuals, with Z-spacing values exceeding 2.0. As Guanlong grows, the Z-spacing value in the maxillary dentition increases, resembling the ontogenetic changes documented in the Tyrannosauridae. Additionally, like Tarbosaurus , Guanlong also displays a discontinuity between the tooth replacement waves at the premaxilla-maxilla boundary. This study thus demonstrates that some tyrannosaurid-like tooth replacement patterns were acquired before the origin of the Tyrannosauridae.
Key words： Late Jurassic; Tyrannosauroidea; tooth replacement; 3D reconstruction
KE Yi-Hui , PEI Rui , XU Xing . High-resolution CT-scan data reveals the tooth replacement pattern of the Late Jurassic tyrannosauroid Guanlong wucaii (Dinosauria, Theropoda)[J]. Vertebrata Palasiatica, 2024 , 62(3) : 225 -244 . DOI: 10.19615/j.cnki.2096-9899.240715
| [1] | Abler W L, 1992. The serrated teeth of tyrannosaurid dinosaurs, and biting structures in other animals. Paleobiology, 18: 161-183 |
| [2] | Averianov A O, Krasnolutskii S A, Ivantsov S V, 2010. A new basal coelurosaur (Dinosauria: Theropoda) from the Middle Jurassic of Siberia. Proc Zool Inst Russ Acad Sci, 314: 42-57 |
| [3] | Bolt J R, DeMar R E, 1986. Computer simulation of tooth replacement with growth in lower tetrapods. J Vert Paleont, 6: 233-250 |
| [4] | Brink K S, LeBlanc A R, 2023. How the study of crocodylian teeth influences our understanding of dental development, replacement, and evolution in dinosaurs. In: AraújoR, FernandezV, JohnstonP S eds. Rudling Reptiles:Crocodylian Biology and Archosaur Paleobiology. Bloomington: Indiana University Press. 240-257 |
| [5] | Brochu C A, 2003. Osteology of Tyrannosaurus rex : insights from a nearly complete skeleton and high-resolution computed tomographic analysis of the skull. J Vert Paleont, 22: 1-138 |
| [6] | Brusatte S L, Carr T D, 2016. The phylogeny and evolutionary history of tyrannosauroid dinosaurs. Sci Rep, 6: 20252 |
| [7] | Brusatte S L, Norell M A, Carr T D et al., 2010. Tyrannosaur paleobiology: new research on ancient exemplar organisms. Science, 329: 1481-1485 |
| [8] | Buckley L G, Larson D W, Reichel M et al., 2010. Quantifying tooth variation within a single population of Albertosaurus sarcophagus (Theropoda: Tyrannosauridae) and implications for identifying isolated teeth of tyrannosaurids. Can J Earth Sci, 47: 1227-1251 |
| [9] | Carr T D, 2016. Toward understanding phylogenetic and ontogenetic tooth loss in Archosauria:documenting patterns of tooth replacement in Tyrannosaurus rex . Paper presented at the 76th Annual Meeting of the Society of Vertebrate Paleontology. Utah: Grand America Hotel. 110 |
| [10] | Carr T D, 2020. A high-resolution growth series of Tyrannosaurus rex obtained from multiple lines of evidence. PeerJ, 8: e9192 |
| [11] | Currie P J, 2003. Cranial anatomy of tyrannosaurid dinosaurs from the Late Cretaceous of Alberta, Canada. Acta Palaeontol Pol, 48: 191-226 |
| [12] | Currie P J, Rigby J K, Sloan R E, 1990. Theropod teeth from the Judith River Formation of southern Alberta, Canada. In: CarpenterK, CurrieP J eds. Dinosaur Systematics:Approaches and Perspectives. Cambridge: Cambridge University Press. 107-125 |
| [13] | Dalman S G, Loewen M A, Pyron R A et al., 2023. A giant tyrannosaur from the Campanian-Maastrichtian of southern North America and the evolution of tyrannosaurid gigantism. Sci Rep, 13: 22124 |
| [14] | DeMar R, 1972. Evolutionary implications of Zahnreihen. Evolution, 26: 435-450 |
| [15] | DeMar R, 1973. The functional implications of the geometrical organization of dentitions. J Vert Paleont, 47: 452-461 |
| [16] | DeMar R, Bolt J R, 1981. Dentitional organization and function in a Triassic reptile. J Vert Paleont, 55: 967-984 |
| [17] | DePalma II R A, Burnham D A, Martin L D et al., 2013. Physical evidence of predatory behavior in Tyrannosaurus rex . Proc Natl Acad Sci, 110: 12560-12564 |
| [18] | Dumont M, Tafforeau P, Bertin T et al., 2016. Synchrotron imaging of dentition provides insights into the biology of Hesperornis and Ichthyornis , the “last” toothed birds. BMC Evol Biol, 16: 178 |
| [19] | D’Emic M D, O’Connor P M, Pascucci T R et al., 2019. Evolution of high tooth replacement rates in theropod dinosaurs. PLoS One, 14: e0226897 |
| [20] | Edmund A G, 1960. Tooth replacement phenomena in the lower vertebrates. R Ont Mus, 52: 1-190 |
| [21] | Edmund A G, 1962. Sequence and rate of tooth replacement in the Crocodilia. R Ont Mus, 56: 1-42 |
| [22] | Edmund A G, 1969. Dentition. In: Gans C, Bellairs A A, Parson T S eds.eds. Biology of the Reptilia. London and New York: Academic Press. 117-200 |
| [23] | Erickson G M, 1995. Split carinae on tyrannosaurid teeth and implications of their development. J Vert Paleont, 15: 268-274 |
| [24] | Erickson G M, 1996. Incremental lines of von Ebner in dinosaurs and the assessment of tooth replacement rates using growth line counts. Proc Natl Acad Sci, 93: 14623-14627 |
| [25] | Erickson G M, Olson K H, 1996. Bite marks attributable to Tyrannosaurus rex : preliminary description and implications. J Vert Paleont, 16: 175-178 |
| [26] | Erickson G M, Kirk S D V, Su J et al., 1996. Bite-force estimation for Tyrannosaurus rex from tooth-marked bones. Nature, 382: 706-708 |
| [27] | Farlow J O, Brinkman D L, 1994. Wear surfaces on the teeth of tyrannosaurs. The Paleontological Society Special Publications. Cambridge: Cambridge University Press. 165-176 |
| [28] | Fastnacht M, 2008. Tooth replacement pattern of Coloborhynchus robustus (Pterosauria) from the Lower Cretaceous of Brazil. J Morphol, 269: 332-348 |
| [29] | Fong R K, LeBlanc A R, Berman D S et al., 2016. Dental histology of Coelophysis bauri and the evolution of tooth attachment tissues in early dinosaurs. J Morphol, 277: 916-924 |
| [30] | Funston G F, Powers M J, Whitebone S A et al., 2021. Baby tyrannosaurid bones and teeth from the Late Cretaceous of western North America. Can J Earth Sci, 58: 756-777 |
| [31] | Gignac P M, Erickson G M, 2017. The biomechanics behind extreme osteophagy in Tyrannosaurus rex . Sci Rep, 7: 2012 |
| [32] | Hanai T, Tsuihiji T, 2018. Description of tooth ontogeny and replacement patterns in a juvenile Tarbosaurus bataar (Dinosauria: Theropoda) using CT-scan data. Anat Rec, 302: 1210-1225 |
| [33] | He Y, Makovicky P J, Xu X et al., 2018. High-resolution computed tomographic analysis of tooth replacement pattern of the basal neoceratopsian Liaoceratops yanzigouensis informs ceratopsian dental evolution. Sci Rep, 8: 5870 |
| [34] | Hendrickx C, Mateus O, Araújo R, 2015. A proposed terminology of theropod teeth (Dinosauria, Saurischia). J Vert Paleont, 35: e982797 |
| [35] | Holtz Jr T R, 2021. Theropod guild structure and the tyrannosaurid niche assimilation hypothesis: implications for predatory dinosaur macroecology and ontogeny in later Late Cretaceous Asiamerical. Can J Earth Sci, 58: 778-795 |
| [36] | Hone D W, Watabe M, 2010. New information on scavenging and selective feeding behaviour of tyrannosaurids. Acta Palaeontol Pol, 55: 627-634 |
| [37] | Horner J R, Padian K, 2004. Age and growth dynamics of Tyrannosaurus rex . Proc R Soc B, 271: 1875-1880 |
| [38] | Hu J, Forster C A, Xu X et al., 2022. Computed tomographic analysis of the dental system of three Jurassic ceratopsians and implications for the evolution of tooth replacement pattern and diet in early-diverging ceratopsians. Elife, 11: e76676 |
| [39] | Hurum J R H, Currie P J, 2000. The crushing bite of tyrannosaurids. J Vert Paleont, 20: 619-621 |
| [40] | Hurum J R H, Sabath K, 2003. Giant theropod dinosaurs from Asia and North America: skulls of Tarbosaurus bataar and Tyrannosaurus rex compared. Acta Palaeontol Pol, 48: 161-190 |
| [41] | Kellner A W, Azevedo S A, Machado E B et al., 2011. A new dinosaur (Theropoda, Spinosauridae) from the Cretaceous (Cenomanian) Alcantara Formation, Cajual Island, Brazil. An Acad Bras Cienc, 83: 99-108 |
| [42] | Kundrát M, Nudds J, Kear B P et al., 2019. The first specimen of Archaeopteryx from the Upper Jurassic M?rnsheim Formation of Germany. Hist Biol, 31: 3-63 |
| [43] | Lambe L M, 1917. The Cretaceous theropodus dinosaur Gorgosaurus . Mem Geol Surv Canada, 100: 1-84 |
| [44] | Lautenschlager S, Witmer L M, Altangerel P et al., 2014. Cranial anatomy of Erlikosaurus andrewsi (Dinosauria, Therizinosauria): new insights based on digital reconstruction. J Vert Paleont, 34: 1263-1291 |
| [45] | Lawson R, Wake D B, Beck N T, 1971. Tooth replacement in the red‐backed salamander, Plethodon cinereus. J Morphol, 134: 259-269 |
| [46] | LeBlanc A R, Brink K S, Cullen T M et al., 2017. Evolutionary implications of tooth attachment versus tooth implantation: a case study using dinosaur, crocodilian, and mammal teeth. J Vert Paleont, 37: e1354006 |
| [47] | Lu J, 2023. Vayu 1.0, a new set of tools for visualizing surface meshes. Vert PalAsiat, 61: 71-80 |
| [48] | Maho T, Reisz R R, 2024. Exceptionally rapid tooth development and ontogenetic changes in the feeding apparatus of the Komodo dragon. PLoS One, 19: e0295002 |
| [49] | Maho T, Maho S, Scott D et al., 2022. Permian hypercarnivore suggests dental complexity among early amniotes. Nat Commun, 13: 4882 |
| [50] | Marshall C R, Latorre D V, Wilson C J et al., 2021. Absolute abundance and preservation rate of Tyrannosaurus rex . Science, 372: 284-287 |
| [51] | Meers M B, 2002. Maximum bite force and prey size of Tyrannosaurus rex and their relationships to the inference of feeding behavior. Hist Biol, 16: 1-12 |
| [52] | Osborn H F, 1905. Article XIV.- Tyrannosaurus and other Cretaceous carnivorous dinosaurs. Bull Am Mus Nat Hist, 21: 259-265 |
| [53] | Osborn H F, Brown B, 1906. Tyrannosaurus, Upper Cretaceous carnivorous dinosaur: second communication. Bull Am Mus Nat Hist, 22: 281-296 |
| [54] | Osborn J W, 1972. On the biological improbability of Zahnreihen as embryological units. Evolution, 26: 601-607 |
| [55] | Osborn J W, 1974. On the control of tooth replacement in reptiles and its relationship to growth. J Theor Biol, 46: 509-527 |
| [56] | Osborn J W, 1977. The interpretation of patterns in dentitions. Zool J Linn Soc, 9: 217-229 |
| [57] | Owocki K, Kremer B, Cotte M et al., 2020. Diet preferences and climate inferred from oxygen and carbon isotopes of tooth enamel of Tarbosaurus bataar (Nemegt Formation, Upper Cretaceous, Mongolia). Palaeogeogr Palaeoclimatol Palaeoecol, 537: 109190 |
| [58] | Paul G S, Persons W S, Van Raalte J, 2022. The tyrant lizard king, queen and emperor: multiple lines of morphological and stratigraphic evidence support subtle evolution and probable speciation within the North American genus Tyrannosaurus . Evol Biol, 49: 156-179 |
| [59] | Peterson J E, Tseng Z J, Brink S, 2021. Bite force estimates in juvenile Tyrannosaurus rex based on simulated puncture marks. PeerJ, 9: e11450 |
| [60] | Powers M J, Fabbri M, Doschak M R et al., 2021. A new hypothesis of eudromaeosaurian evolution: CT scans assist in testing and constructing morphological characters. J Vert Paleont, 41: e2010087 |
| [61] | Rauhut O W, Milner A C, Moore-Fay S, 2010. Cranial osteology and phylogenetic position of the theropod dinosaur Proceratosaurus bradleyi (Woodward, 1910) from the Middle Jurassic of England. Zool J Linn Soc, 158: 155-195 |
| [62] | Rayfield E J, 2004. Cranial mechanics and feeding in Tyrannosaurus rex . Proc R Soc B, 271: 1451-1459 |
| [63] | Reichel M, 2010. The heterodonty of Albertosaurus sarcophagus and Tyrannosaurus rex : biomechanical implications inferred through 3-D models. Can J Earth Sci, 49: 1253-1261 |
| [64] | Reichel M, 2012. The variation of angles between anterior and posterior carinae of tyrannosaurid teeth. Can J Earth Sci, 49: 477-491 |
| [65] | Rowe A J, Snively E, 2022. Biomechanics of juvenile tyrannosaurid mandibles and their implications for bite force: evolutionary biology. Anat Rec, 305: 373-392 |
| [66] | Sassoon J, Foffa D, Marek R, 2015. Dental ontogeny and replacement in Pliosauridae. R Soc Open Sci, 2: 150384 |
| [67] | Sattler F, Schwarz D, 2021. Tooth replacement in a specimen of Tyrannosaurus rex (Dinosauria, Theropoda) from the Hell Creek Formation (Maastrichtian), Montana. Hist Biol, 33: 949-972 |
| [68] | Scherer C R, Voiculescu-Holvad C, 2024. Reanalysis of a dataset refutes claims of anagenesis within Tyrannosaurus -line tyrannosaurines (Theropoda, Tyrannosauridae). Cretaceous Res, 155: 105780 |
| [69] | Schwarz D, Kosch J C, Fritsch G et al., 2015. Dentition and tooth replacement of Dicraeosaurus hansemanni (Dinosauria, Sauropoda, Diplodocoidea) from the Tendaguru Formation of Tanzania. J Vert Paleont, 35: e1008134 |
| [70] | Smith J B, 2005. Heterodonty in Tyrannosaurus rex : implications for the taxonomic and systematic utility of theropod dentitions. J Vert Paleont, 25: 865-887 |
| [71] | Therrien F, Zelenitsky D K, Voris J T et al., 2021. Mandibular force profiles and tooth morphology in growth series of Albertosaurus sarcophagus and Gorgosaurus libratus (Tyrannosauridae: Albertosaurinae) provide evidence for an ontogenetic dietary shift in tyrannosaurids. Can J Earth Sci, 58: 812-828 |
| [72] | Therrien F, Zelenitsky D K, Tanaka K et al., 2023. Exceptionally preserved stomach contents of a young tyrannosaurid reveal an ontogenetic dietary shift in an iconic extinct predator. Sci Adv, 9: eadi0505 |
| [73] | Tsuihiji T, Watabe M, Tsogtbaatar K et al., 2011. Cranial osteology of a juvenile specimen of Tarbosaurus bataar (Theropoda, Tyrannosauridae) from the Nemegt Formation (Upper Cretaceous) of Bugin Tsav, Mongolia. J Vert Paleont, 31: 497-517 |
| [74] | Wang Y F, Wei C F, Que J M et al., 2019. Development and applications of paleontological computed tomography. Vert PalAsiat, 57: 84-92 |
| [75] | Westergaard B, Ferguson M W J, 1986. Development of the dentition in Alligator mississippiensis : early embryonic development in the lower jaw. J Zool, 210: 575-597 |
| [76] | Westergaard B, Ferguson M W J, 1987. Development of the dentition in Alligator mississippiensis : later development in the lower jaws of embryos, hatchlings and young juveniles. J Zool, 212: 191-222 |
| [77] | Westergaard B, Ferguson M W J, 1990. Development of the dentition in Alligator mississippiensis : upper jaw dental and craniofacial development in embryos, hatchlings, and young juveniles, with a comparison to lower jaw development. Am J Anat, 187: 393-421 |
| [78] | Winkler D E, Iijima M, Blob R W et al., 2022. Controlled feeding experiments with juvenile alligators reveal microscopic dental wear texture patterns associated with hard-object feeding. Front Ecol Evol, 10: 957725 |
| [79] | Woodward H N, Tremaine K, Williams S A et al., 2020. Growing up Tyrannosaurus rex : osteohistology refutes the pygmy “ Nanotyrannus ” and supports ontogenetic niche partitioning in juvenile Tyrannosaurus . Sci Adv, 6: eaax6250 |
| [80] | Wu Y H, Chiappe L M, Bottjer D J et al., 2021. Dental replacement in Mesozoic birds: evidence from newly discovered Brazilian enantiornithines. Sci Rep, 11: 19349 |
| [81] | Xu X, Clark J M, Forster C A et al., 2006. A basal tyrannosauroid dinosaur from the Late Jurassic of China. Nature, 439: 715-718 |
| [82] | Xu X, Wang K, Zhang K et al., 2012. A gigantic feathered dinosaur from the Lower Cretaceous of China. Nature, 484: 92-95 |
| [83] | Xu X, Clark J M, Eberth D A et al., 2022. The Shishugou Fauna of the Middle‐Late Jurassic transition period in the Junggar Basin of western China. Acta Geol Sin, 96: 1115-1135 |
/
| 〈 |
|
〉 |