Hostname: page-component-f554764f5-68cz6 Total loading time: 0 Render date: 2025-04-22T01:49:40.955Z Has data issue: false hasContentIssue false
  • English
  • Français

Endocranial morphology of three early-diverging ceratopsians and implications for the behavior and the evolution of the endocast in ceratopsians

Published online by Cambridge University Press:  30 October 2024

Jinfeng Hu Open the ORCID record for Jinfeng Hu [Opens in a new window] ,
Xing Xu ,
Qi Zhao ,
Yiming He ,
Catherine A. Forster  and
Fenglu Han
Jinfeng Hu
Affiliation:
School of Earth Sciences, China University of Geosciences, Wuhan, Hubei, China
Xing Xu
Affiliation:
Key Laboratory of Vertebrate Evolution and Human Origins, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing, China Center for Vertebrate Evolutionary Biology, Yunnan University, Kunming, China
Qi Zhao
Affiliation:
Key Laboratory of Vertebrate Evolution and Human Origins, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing, China
Yiming He
Affiliation:
Nanjiang Museum of Paleontology, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing, China
Catherine A. Forster
Affiliation:
Department of Biological Sciences, George Washington University, Washington, D.C., U.S.A.
Fenglu Han*
Affiliation:
School of Earth Sciences, China University of Geosciences, Wuhan, Hubei, China
*
Corresponding author: Fenglu Han; Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Ceratopsian dinosaurs underwent great changes, including a shift of locomotion mode, enlarged horns and frills, and increased body size. These changes occur alongside the evolution of endocranial morphology and physiology such as the size and shape of the flocculus, hearing range, olfactory ratio, and the reptile encephalization quotient (REQ). However, the evolution of endocranial structures in early ceratopsians is still unclear because of a lack of information on the earliest ceratopsians. Here, we reconstructed the endocasts of three early-diverging ceratopsians including the Late Jurassic Yinlong, and the Early Cretaceous Liaoceratops and Psittacosaurus. These ceratopsians display obvious flocculi, large and separate olfactory bulbs, long and high anterior semicircular canals, and relatively long cochlear ducts. In the evolution of the earliest ceratopsians to early neoceratopsians, changes include the increasing size of the flocculus (which is reduced or absent in late-diverging ceratopsids), the attenuation of the semicircular canals, and the heightening of the anterior semicircular canal (which is shortened in late-diverging ceratopsids). The endocranial structures suggest early-diverging ceratopsians had a higher olfactory acuity and were adapted to hearing higher frequencies than late-diverging ceratopsians. Furthermore, the REQ suggests that Yinlong and Psittacosaurus were more highly encephalized than late-diverging ceratopsians and most extant reptiles. The angle of the lateral semicircular canal suggests that heads in ceratopsians display a transition from a forward posture to a more downward posture. Our new findings are significant for understanding the physiological changes during ceratopsian evolution and also have implications for the evolution of physiology in extant tetrapods.

Type
Article
Information
Paleobiology , Volume 50 , Issue 3 , August 2024 , pp. 490 - 502
Check for updates
Copyright
Copyright © The Author(s), 2024. Published by Cambridge University Press on behalf of Paleontological Society

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Literature Cited

Balanoff, A. M., Bever, G. S., Colbert, M. W., Clarke, J. A., Field, D. J., Gignac, P. M., Ksepka, D. T., et al. 2016. Best practices for digitally constructing endocranial casts: examples from birds and their dinosaurian relatives. Journal of Anatomy 229:173–190.CrossRefGoogle ScholarPubMed
Brochu, C. A. 2000. A digitally-rendered endocast for Tyrannosaurus rex. Journal of Vertebrate Paleontology 20:1–6.CrossRefGoogle Scholar
Brown, B. 1914. Anchiceratops, a new genus of horned dinosaurs from the Edmonton Cretaceous of Alberta; with discussion of the origin of the ceratopsian crest and the brain casts of Anchiceratops and Trachodon. Bulletin of the American Museum of Natural History 33:348–539.Google Scholar
Brown, D. B., and Schlaikjer, D. E. M.. 1940. The structure and relationships of Protoceratops. Annals of the New York Academy of Sciences 40(3 Series II):133–265.CrossRefGoogle Scholar
Brown, E. E., Butler, R. J., Ezcurra, M. D., Bhullar, B.-A. S., and Lautenschlager, S.. 2020. Endocranial anatomy and life habits of the Early Triassic archosauriform Proterosuchus fergusi. Palaeontology 63:255–282.CrossRefGoogle Scholar
Bullar, C. M., Zhao, Q., Benton, M. J., and Ryan, M. J.. 2019. Ontogenetic braincase development in Psittacosaurus lujiatunensis (Dinosauria: Ceratopsia) using micro-computed tomography. PeerJ 7:e7217.CrossRefGoogle ScholarPubMed
Button, D. J., and Zanno, L. E.. 2023. Neuroanatomy of the late Cretaceous Thescelosaurus neglectus (Neornithischia: Thescelosauridae) reveals novel ecological specialisations within Dinosauria. Scientific Reports 13:19224.CrossRefGoogle ScholarPubMed
Campione, N. E., and Evans, D. C.. 2012. A universal scaling relationship between body mass and proximal limb bone dimensions in quadrupedal terrestrial tetrapods. BMC Biology 10:60.CrossRefGoogle ScholarPubMed
Campione, N. E., Evans, D. C., Brown, C. M., and Carrano, M. T.. 2014. Body mass estimation in non-avian bipeds using a theoretical conversion to quadruped stylopodial proportions. Methods in Ecology and Evolution 5:913–923.CrossRefGoogle Scholar
Coutier, F., Hautier, L., Cornette, R., Amson, E., and Billet, G.. 2017. Orientation of the lateral semicircular canal in Xenarthra and its links with head posture and phylogeny. Journal of Morphology 278:704–717.CrossRefGoogle ScholarPubMed
Evans, D. C., Ridgely, R., and Witmer, L. M.. 2009. Endocranial anatomy of lambeosaurine hadrosaurids (Dinosauria: Ornithischia): a sensorineural perspective on cranial crest function. Anatomical Record 292:1315–1337.CrossRefGoogle ScholarPubMed
Forster, C. A. 1996. New information on the skull of Triceratops. Journal of Vertebrate Paleontology 16:246–258.CrossRefGoogle Scholar
Galton, P. 1989. Crania and endocranial casts from ornithopod dinosaurs of the families Dryosauridae and Hypsilophodentidae (Reptilia: Ornithischia). Geologica et Palaeontologica 23:217–239.Google Scholar
Giffin, E. B. 1989. Pachycephalosaur paleoneurology (Archosauria: Ornithischia). Journal of Vertebrate Paleontology 9:67–77.CrossRefGoogle Scholar
Gleich, O., Dooling, R. J., and Manley, G. A.. 2005. Audiogram, body mass, and basilar papilla length: correlations in birds and predictions for extinct archosaurs. Naturwissenschaften 92:595–598.CrossRefGoogle ScholarPubMed
Han, F. L., Forster, C. A., Clark, J. M., and Xu, X.. 2016. Cranial anatomy of Yinlong downsi (Ornithischia: Ceratopsia) from the Upper Jurassic Shishugou Formation of Xinjiang, China. Journal of Vertebrate Paleontology 36:e1029579.CrossRefGoogle Scholar
Han, F. L., Forster, C. A., Xu, X., and Clark, J. M.. 2018. Postcranial anatomy of Yinlong downsi (Dinosauria: Ceratopsia) from the Upper Jurassic Shishugou Formation of China and the phylogeny of basal ornithischians. Journal of Systematic Palaeontology 16:1159–1187.CrossRefGoogle Scholar
Hanson, M., Hoffman, E. A., Norell, M. A., and Bhullar, B.-A. S.. 2021. The early origin of a birdlike inner ear and the evolution of dinosaurian movement and vocalization. Science 372:601–609.CrossRefGoogle ScholarPubMed
Heffner, R. S., and Heffner, H. E.. 1983. Hearing in large mammals: horses (Equus caballus) and cattle (Bos taurus). Behavioral Neuroscience 97:299–309.CrossRefGoogle Scholar
Heffner, R. S., and Heffner, H. E.. 1992. Hearing in large mammals: sound-localization acuity in cattle (Bos taurus) and goats (Capra hircus). Journal of Comparative Psychology 106:107–113.CrossRefGoogle ScholarPubMed
Hopson, J. A. 1975. The evolution of cranial display structures in hadrosaurian dinosaurs. Paleobiology 1:21–43.CrossRefGoogle Scholar
Hopson, J. A. 1979. Paleoneurology. Academic Press, New York.Google Scholar
Horner, J. R. 2000. Dinosaur reproduction and parenting. Annual Review of Earth and Planetary Sciences 28:19–45.CrossRefGoogle Scholar
Horner, J. R., and Makela, R.. 1979. Nest of juveniles provides evidence of family structure among dinosaurs. Nature 282:296–298.CrossRefGoogle Scholar
Hu, J., Forster, C. A., Xu, X., Zhao, Q., He, Y., and Han, F.. 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.CrossRefGoogle ScholarPubMed
Hurlburt, G. R. 1996. Relative brain size in recent and fossil amniotes: determination and interpretation. Doctoral thesis. University of Toronto, Toronto.Google Scholar
Jerison, H. J. 1973. Evolution of the brain and intelligence. Academic Press, New York.Google Scholar
Knapp, A., Knell, R. J., and Hone, D. W. E.. 2021. Three-dimensional geometric morphometric analysis of the skull of Protoceratops andrewsi supports a socio-sexual signalling role for the ceratopsian frill. Proceedings of the Royal Society B 288:20202938.CrossRefGoogle ScholarPubMed
Knoll, F., Lautenschlager, S., Kawabe, S., Martínez, G., Espílez, E., Mampel, L., and Alcalá, L.. 2021. Palaeoneurology of the Early Cretaceous iguanodont Proa valdearinnoensis and its bearing on the parallel developments of cognitive abilities in theropod and ornithopod dinosaurs. Journal of Comparative Neurology 529:3922–3945.CrossRefGoogle ScholarPubMed
Lautenschlager, S., and Hübner, T.. 2013. Ontogenetic trajectories in the ornithischian endocranium. Journal of Evolutionary Biology 26:2044–2050.CrossRefGoogle ScholarPubMed
Manley, G. A. 1972. A review of some current concepts of the functional evolution of the ear in terrestrial vertebrates. Evolution 26:608–621.CrossRefGoogle ScholarPubMed
Müller, R. T., Ferreira, J. D., Pretto, F. A., Bronzati, M., and Kerber, L.. 2021. The endocranial anatomy of Buriolestes schultzi (Dinosauria: Saurischia) and the early evolution of brain tissues in sauropodomorph dinosaurs. Journal of Anatomy 238:809–827.CrossRefGoogle ScholarPubMed
Napoli, J. G., Hunt, T., Erickson, G. M., and Norell, M. A.. 2019. Psittacosaurus amitabha, a new species of ceratopsian dinosaur from the Ondai Sayr Locality, Central Mongolia. American Museum Novitates 2019(3932):1–36.CrossRefGoogle Scholar
Norell, M. A., Clark, J. M., Chiappe, L. M., and Dashzeveg, D.. 1995. A nesting dinosaur. Nature 378:774–776.CrossRefGoogle Scholar
Norell, M. A., Balanoff, A. M., Barta, D. E., and Erickson, G. M.. 2018. A second specimen of Citipati osmolskae associated with a nest of eggs from Ukhaa Tolgod, Omnogov Aimag, Mongolia. American Museum Novitates 2018(3899):1–44.CrossRefGoogle Scholar
Paulina-Carabajal, A., and Currie, P. J.. 2017. The braincase of the theropod dinosaur Murusraptor: osteology, neuroanatomy and comments on the paleobiological Implications of certain endocranial features. Ameghiniana 54:617–640.CrossRefGoogle Scholar
Pérez-Barbería, F. J., and Gordon, I. J.. 2005. Gregariousness increases brain size in ungulates. Oecologia 145:41–52.CrossRefGoogle ScholarPubMed
Rogers, S. W. 1999. Allosaurus, crocodiles, and birds: evolutionary clues from spiral computed tomography of an endocast. Anatomical Record 257:162–173.3.0.CO;2-W>CrossRefGoogle ScholarPubMed
Sakagami, R., and Kawabe, S.. 2020. Endocranial anatomy of the ceratopsid dinosaur Triceratops and interpretations of sensory and motor function. PeerJ 8:e9888.CrossRefGoogle ScholarPubMed
Sakagami, R., Kawabe, S., Hattori, S., Wenjie, Z., and Xinsheng, J.. 2023. Endocranial anatomy of the ceratopsian dinosaur Psittacosaurus lujiatunensis and its bearing on sensory and locmotor abilities. Memoir of the Fukui Prefectural Dinosaur Museum 22:1–12.Google Scholar
Schellhorn, R. 2018. A potential link between lateral semicircular canal orientation, head posture, and dietary habits in extant rhinos (Perissodactyla, Rhinocerotidae). Journal of Morphology 279:50–61.CrossRefGoogle ScholarPubMed
Shultz, S., and Dunbar, R. I. M.. 2006. Both social and ecological factors predict ungulate brain size. Proceedings of the Royal Society B 273:207–215.CrossRefGoogle ScholarPubMed
Taylor, M. P., Wedel, M. J., and Naish, D.. 2009. Head and neck posture in sauropod dinosaurs inferred from extant animals. Acta Palaeontologica Polonica 54:213–220.CrossRefGoogle Scholar
Thomas, D. A. 2015. The cranial anatomy of Tenontosaurus tilletti Ostrom, 1970 (Dinosauria, Ornithopoda). Palaeontologia Electronica 18:1–99.Google Scholar
Tykoski, R. S., and Fiorillo, A. R.. 2012. Beauty or brains? The braincase of Pachyrhinosaurus perotorum and its utility for species-level distinction in the centrosaurine ceratopsid Pachyrhinosaurus. Transactions of the Royal Society of Edinburgh (Earth and Environmental Science) 103(3–4):487–499.CrossRefGoogle Scholar
Walsh, S. A., Barrett, P. M., Milner, A. C., Manley, G., and Witmer, L. M.. 2009. Inner ear anatomy is a proxy for deducing auditory capability and behaviour in reptiles and birds. Proceedings of the Royal Society B 276:1355–1360.CrossRefGoogle ScholarPubMed
Walsh, S. A., Iwaniuk, A. N., Knoll, M. A., Bourdon, E., Barrett, P. M., Milner, A. C., Nudds, R. L., Abel, R. L., and Sterpaio, P. D.. 2013. Avian cerebellar floccular fossa size is not a proxy for flying ability in birds. PLoS ONE 8:e67176.CrossRefGoogle Scholar
Watanabe, A., Gignac, P. M., Balanoff, A. M., Green, T. L., Kley, N. J., and Norell, M. A.. 2019. Are endocasts good proxies for brain size and shape in archosaurs throughout ontogeny? Journal of Anatomy 234:291–305.CrossRefGoogle ScholarPubMed
Weishampel, D. B. 1997. Dinosaurian cacophony. BioScience 47:150–159.CrossRefGoogle Scholar
Willemet, R. 2013. Reconsidering the evolution of brain, cognition, and behavior in birds and mammals. Frontiers in Psychology 4:396.CrossRefGoogle ScholarPubMed
Witmer, L. M., and Ridgely, R. C.. 2008. Structure of the brain cavity and inner ear of the centrosaurine ceratopsid dinosaur Pachyrhinosaurus based on CT scanning and 3D visualization. Pp. 117–144 in Currie, P. J., , J. W. L., and Tanke, D. H., eds. A new horned dinosaur from an Upper Cretaceous bone bed in Alberta. National Research Council of Canada, Ottawa.Google Scholar
Witmer, L. M., Chatterjee, S., Franzosa, J., and Rowe, T.. 2003. Neuroanatomy of flying reptiles and implications for flight, posture and behaviour. Nature 425:950–953.CrossRefGoogle ScholarPubMed
Witmer, L. M., Ridgely, R. C., Dufeau, D. L., and Semones, M. C.. 2008. Using CT to peer into the past: 3D visualization of the brain and ear regions of birds, crocodiles, and nonavian dinosaurs. Pp. 67–87 in Endo, H. and Frey, R., eds. Anatomical imaging: towards a new morphology. Springer Japan, Tokyo.CrossRefGoogle Scholar
Xu, X., Forster, C. A., Clark, J. M., and Mo, J.. 2006. A basal ceratopsian with transitional features from the Late Jurassic of northwestern China. Proceedings of the Royal Society B 273:2135–2140.CrossRefGoogle ScholarPubMed
Yang, Y., Gong, E., Zhao, C., Wu, W., Godefroit, P., and Hu, D.. 2023. Endocranial morphology of Liaoceratops yanzigouensis (Dinosauria: Ceratopsia) from Early Cretaceous Jehol Biota of Liaoning in China. Historical Biology 36:650–656.CrossRefGoogle Scholar
Zelenitsky, D. K., Therrien, F., and Kobayashi, Y.. 2009. Olfactory acuity in theropods: palaeobiological and evolutionary implications. Proceedings of the Royal Society B 276:667–673.CrossRefGoogle ScholarPubMed
Zhang, Q. n., King, J. L., Li, D. q., Hou, Y. m., and You, H. l.. 2020. Endocranial morphology of Auroraceratops sp. (Dinosauria: Ceratopsia) from the Early Cretaceous of Gansu Province, China. Historical Biology 32:1355–1360.CrossRefGoogle Scholar
Zhao, Q., Benton, M. J., Sullivan, C., Martin Sander, P., and Xu, X.. 2013a. Histology and postural change during the growth of the ceratopsian dinosaur Psittacosaurus lujiatunensis. Nature Communications 4:2079.CrossRefGoogle ScholarPubMed
Zhao, Q., Michael, J. B., Xing, X., and Sander, P. M.. 2013b. Juvenile-only clusters and behaviour of the Early Cretaceous dinosaur Psittacosaurus. Acta Palaeontologica Polonica 59:827–833.Google Scholar
Zhou, C. f., Gao, K. q., Fox, R. C., and Du, X. k.. 2007. Endocranial morphology of psittacosaurs (Dinosauria: Ceratopsia) based on CT scans of new fossils from the Lower Cretaceous, China. Palaeoworld 16:285–293.CrossRefGoogle Scholar