Ontogenetic changes in the craniomandibular skeleton of the abelisaurid dinosaur Majungasaurus crenatissimus from the Late Cretaceous of Madagascar

• Autorzy: Ratsimbaholison N.O. , Felice R.N. , O’Connor P.M.
• Języki publikacji: EN

Abstrakty

EN

Abelisaurid theropods were one of the most diverse groups of predatory dinosaurs in Gondwana during the Cretaceous. The group is characterized by a tall, wide skull and robust cervical region. This morphology is thought to have facilitated specialized feeding behaviors such as prolonged contact with prey. The Late Cretaceous abelisaurid Majungasaurus crenatissimus typifies this abelisaurid cranial morphotype. Recent fossil discoveries of this species include a partial growth series that allows for the first time an investigation of ontogenetic variation in cranial morphology in a representative abelisaurid. Herein we examine growth trajectories in the shape of individual cranial bones and articulated skulls of Majungasaurus using geometric morphometrics. Several major changes in skull shape were observed through ontogeny, including an increase in the height of the jugal, postorbital, and quadratojugal, an increase in the extent of the contacts between bones, and a decrease in the circumference of the orbit. The skull transitions from relatively short in the smallest individual to tall and robust in large adults, as is seen in other theropods. Such morphological change during ontogeny would likely have resulted in different biomechanical properties and feeding behaviors between small and large individuals. These findings provide a post-hatching developmental framework for understanding the evolution of the distinctive tall skull morphology seen in abelisaurids and other large-sized theropod dinosaurs.

Słowa kluczowe

EN

ontogenetic change; craniomandibular skeleton; abelisaurid dinosaur; Majungasaurus crenatissimus; Dinosauria; Abelisauridae; geometric morphometrics; ontogenesis; skull; Cretaceous; Gondwana; Late Cretaceous; Madagascar

• Wydawca: -
• Czasopismo: Acta Palaeontologica Polonica
• Rocznik: 2016
• Tom: 61
• Numer: 2
• Opis fizyczny: p.281-292,fig.,ref.

Twórcy

autor

Ratsimbaholison N.O.

• Department of Paleontology and Biological Anthropology, University of Antananarivo, BP 906, Antananarivo 101, Madagascar
• Ohio Center for Ecology and Evolutionary Studies, 228 Irvine Hall, Athens, Ohio 45701, USA

autor

Felice R.N.

• Ohio Center for Ecology and Evolutionary Studies, 228 Irvine Hall, Athens, Ohio 45701, USA
• Department of Biological Sciences, Ohio University, 228 Irvine Hall, Athens, Ohio 45701, USA
• Department of Genetics, Evolution and Environment, University College London, London, U.K.

autor

O’Connor P.M.

• Ohio Center for Ecology and Evolutionary Studies, 228 Irvine Hall, Athens, Ohio 45701, USA
• Department of Biomedical Sciences, Ohio University Heritage College of Osteopathic Medicine, 228 Irvine Hall, Athens, Ohio 45701, USA

Bibliografia

• Accarie, H., Beaudoin, B., Dejax, J., Fries, G., Micard, J.-G., and Taquet, P. 1995. Découverte d’un dinosaure théropode nouveau (Genusaurus sisteronis n. g., n. sp.) dans l’Albien marin de Sisteron (Alpes de Haute-Provence, France) et extension au Crétacé inférieur de la lignée cératosaurienne. Comptes Rendus de l’Académie Sciences, Paris, Série IIa 320: 327–334.
• Adams, D.C. and Otárola-Castillo, E. 2013. geomorph: an R package for the collection and analysis of geometric morphometric shape data. Methods in Ecology and Evolution 4: 393–399.
• Adams, D., Rohlf, F., and Slice, D.E. 2004. Geometric morphometrics: ten years of progress following the “revolution”. Italian Journal of Zoology 71: 5–16.
• Adams, D.C., Rohlf, F.J., and Slice, D.E. 2013. A field comes of age: geometric morphometrics in the 21st century. Hystrix, Italian Journal of Mammalogy 24: 7–14.
• Baltanás, A. and Danielopol, D.L. 2011. Geometric Morphometrics and its use in ostracod research: a short guide. Joannea Geologie und Paläontologie 11: 235–272.
• Bever, G.S. and Norell, M. 2009. The perinate skull of Byronosaurus (Troodontidae) with observations on the cranial ontogeny of paravian theropods. American Museum Novitates 3657: 1–51.
• Bhullar, B.A., Marugan-Lobon, J., Racino, F., Bever, G.S., Rowe, T.B., Norell, M.A., and Abzhanov, A. 2012. Birds have paedomophic dinosaur skulls. Nature 487: 223–226.
• Bonaparte, J.F. and Novas, F.E. 1985. Abelisaurus comahuensis new carnosauria from Late Cretaceous of Patagonia. Ameghiniana 21: 259–265.
• Bonaparte, J.F., Novas, F.E., and Coria, R. 1990. Carnotaurus sastrei Bonaparte, the horned, lightly built carnosaur from the middle Cretaceous of Patagonia. Natural History Museum of Los Angeles County, Contributions in Science 416: 1–41.
• Bonnan, M.F. 2007. Linear and geometric morphometric analysis of long bone scaling patterns in Jurassic neosauropod dinosaurs: their functional and paleobiological implications. Anatomical Record 290: 1089–1111.
• Bookstein, F.L. 1991. Morphometric Tools for Landmark Data. 456 pp. Cambridge University Press, Cambridge.
• Breuker, C.J., Patterson, J.S., and Klingenberg, C.P. 2006. A single basis for developmental buffering of Drosophila wing shape. PLoS ONE 1: e7.
• Brusatte, S.L., Sakamoto, M, Montanari, S., and Smith, W.E.H. 2012. The evolution of cranial form and function in theropod dinosaurs: insights from geometric morphometrics. Journal of Evolutionary Biology 25: 365–377.
• Burch, S.H. and Carrano, M.T. 2012. An articulated pectoral girdle and forelimb of the abelisaurid theropod Majungasaurus crenatissimus from the Late Cretaceous of Madagascar. Journal of Vertebrate Paleontology 32: 1–16.
• Canale, J.I., Novas, F.E., Salgado, L., and Coria, R.A. 2015. Cranial ontogenetic variation in Mapusaurus roseae (Dinosauria: Theropoda) and the probable role of heterochrony in carcharodontosaurid evolution. Paläontologische Zeitschrift 89: 983–993.
• Canale, J.I., Scanferla, C.A., Agnolin, F.L, and Novas, F.E. 2008. New carnivorous dinosaur from the Late Cretaceous of NW Patagonia and the evolution of abelisaurid theropods. Naturwissenschaften 96: 409–414.
• Calvo, J.O., Rogers-Rubilar, D., and Moreno, K. 2004. A new Abelisauridae (Dinosauria: Theropoda) from northwest Patagonia. Ameghiniana 41: 555–563.
• Campione, N.E. and Evans, D.C. 2011. Cranial growth and variation in edmontosaurs (Dinosauria: Hadrosauridae): implications for latest Cretaceous megaherbivore diversity in North America. PLoS ONE 6 (9): e25186.
• Carpenter, K. 1990. Variation in Tyrannosaurus rex. In: K. Carpenter and P.J. Currie (eds.), Dinosaur Systematics: Perspectives and Approaches, 141–145. Cambridge University Press, Cambridge.
• Carr, T.D. 1999. Craniofacial ontogeny in Tyrannosauridae (Dinosauria, Coelurosauria). Journal of Vertebrate Paleontology 19: 497–520.
• Carr, T.D. and Williamson, T.E. 2004. Diversity of late Maastrichtian Tyrannosauridae (Dinosauria: Theropoda) from western North America. Zoological Journal of the Linnean Society 142: 479–523.
• Carrano, M.T. and Sampson, S.D. 2008. The phylogeny of Ceratosauria (Dinosauria: Theropoda). Journal of Systematic Palaeontology 6: 183–236.
• Carrano, M.T., Loewen, M.A., and Sertich, J.J.W. 2011. New materials of Masiakasaurus knopfleri Sampson, Carrano, and Forster, 2001, and implications for the morphology of the Noasauridae (Theropoda: Cereatosauria). Smithsonian Contribution to Paleobiology 95: 1–53.
• Chapman, R.E. 1990. Shape analysis in the study of dinosaur morphology. In: K. Carpenter and P.J. Currie (eds.), Dinosaur Systematics: Approaches and Perspectives, 21–42. Cambridge University Press, Cambridge.
• Coria, R.A. and Salgado, L. 1998. A basal Abelisauria Novas, 1992 (Theropoda–Ceratosauria) from the Cretaceous of Patagonia, Argentina. Gaia 15: 89–102.
• Coria, R.A., Chiappe, L.M., and Dingus, L. 2002. A new close relative of Carnotaurus sastrei Bonaparte 198 (Theropoda: Abelisauridae) from the Late Cretaceous of Patagonia. Journal of Vertebrate Paleontology 22: 460–465.
• De Meulemeester, T., Michez, D., Aytekin, A.M., and Danforth, B.N. 2012. Taxonomic affinity of halictid bee fossils (Hymenoptera: Anthophila) based on geometric morphometrics analyses of wing shape. Journal of Systematic Palaeontology 10: 755–764.
• Depéret, C. 1896a. Note sur les Dinosauriens Sauropodes et Théropodes du Crétacé supérieur de Madagascar. Bulletin de la Société Géologique de France 21: 176–194.
• Depéret, C. 1896b. Sur l’existence de Dinosauriens, Sauropodes et Théropodes dans le Crétacé supérieur de Madagascar. Comptes Rendus de l’Académie des Sciences (Paris), Série II 122: 483–85.
• Erickson, G.M., Gignac, P.M., Steppan, S.J., Lappin, A.K., Vliet, K.A., Brueggen, J.D., Inouye, B.D., Kledzik, D., and Webb, G.J.W. 2012. Insights into the ecology and evolutionary success of crocodilians revealed through bite-force and tooth-pressure experimentation. PLoS ONE 7: e31781.
• Erickson, G.M., Lappin, A.K., and Vliet, K.A. 2003. The ontogeny of biteforce performance in American alligator (Alligator mississippiensis). Zoological Society of London 260: 317–327.
• Farke, A.A. and Sertich, J.J.W. 2013. An Abelisauroid theropod dinosaur from the Turonian of Madagascar. PLoS ONE 8: e62047.
• Foth, C. 2013. Ontogenetic, Macroevolutionary, and Morphofunctional Patterns in Archosaur Skulls: A Morphometric Approach. 369 pp. Unpublished Ph.D. Dissertation. Ludwig Maximilians University, Munich.
• Foth, C. and Rauhut, O.W.M. 2013a. Macroevolutionary and morphofunctional patterns in theropod skulls: a morphometric approach. Acta Palaentologica Polonica 58: 1–16.
• Foth, C. and Rauhut, O.W.M. 2013b. The good, the bad, and the ugly: the influence of skull reconstructions and intraspecific variability in studies of cranial morphometrics in theropods and basal saurischians. PLoS ONE 8: e72007.
• Foth, C., Bona, P., and Desojo, J.B. 2013. Intraspecific variation in the skull morphology of the black caiman Melanosuchus niger (Alligatoridae, Caimaninae). Acta Zoologica 96: 1–13.
• Foth, C., Hedrick, B.P., and Ezcurra, M.D. 2016. Cranial ontogenetic variation in early saurischians and the role of heterochrony in the diversification of predatory dinosaurs. PeerJ 4: e1589.
• Gilmore, C.W. 1920. Osteology of the carnivorous Dinosauria in the United States National Museum, with special reference to the genera Antrodemus (Allosaurus) and Ceratosaurus. Bulletin of the United States National Museum 110: 1–159.
• Hedrick, B.P. and Dodson, P. 2013. Lujiatun psittacosaurids: understanding individual and taphonomic variation using 3D geometric morphometrics. PLoS ONE 8: e69265.
• Henderson, D.M. 2002. The eyes have it: The sizes, shapes, and orientations of theropod orbits as indicators of skull strength and bite force. Journal of Vertebrate Paleontology 22: 766–778.
• Hendrickx, C. and Mateus, O. 2014. Torvosaurus gurneyi n. sp., the largest terrestrial predatory from Europe, and a proposed terminology of the maxilla anatomy in nonavian theropods. PLoS ONE 9: e88905.
• Herring, S.W. and Herring, S.E. 1974. The superficial masseter and gape in mammals. American Naturalist 108: 561–576.
• Hieronymus, T.L. 2009. Osteological Correlates of Cephalic Skin Structures in Amniota: Documenting the Evolution of Display and Feeding Structures with Fossil Data. 254 pp. Unpublished Ph.D. Dissertation, Ohio University, Athens.
• Holliday, C.M. 2009. New insights into dinosaur jaw muscle anatomy. Anatomical Record 292: 1246–1265.
• Huene, F. von and Matley, C.A. 1933. The Cretaceous Saurischia and Ornithischia of the Central Provinces of India. Memoirs of the Geological Society of India: Palaeontologica Indica 21: 1–72.
• Kassam, D.D., Adams, D.C., Ambali, A., and Yamaoka, K. 2003. Body shape variation in relation to resource partitioning within cichlid trophic guilds coexisting along the rocky shore of Lake Malawi. Animal Biology 53: 59–70.
• Krause, D.W., Sampson, S.D., Carrano, M.T., and O’Connor, P.M. 2007. Overview of the history of the discovery, taxonomy, phylogeny, and biogeography of Majungasaurus crenatissimus (Theropoda: Abelisauridae) from the Late Cretaceous of Madagascar. Journal of Vertebrate Paleontology, Memoir 8: 1–20.
• Lamanna, M.C., Martínez, R.D., and Smith, J.B. 2002. A definitive abelisaurid theropod dinosaur from the Early Cretaceous of Patagonia. Journal of Vertebrate Paleontology 22: 58–69.
• Lautenschlager, S. 2015. Estimating cranial musculoskeletal constraints in theropod dinosaurs. Royal Society Open Science 2: 150495.
• Madsen, J.H. and Welles, S.P. 2000. Ceratosaurus (Dinosauria, Theropoda). A revised osteology. Miscellaneous Publications of the Utah Geological Survey 00-2: 1–80.
• Maoirino, L., Farke, A.A, Kotsakis, T., and Piras, P. 2013. Is Torosaurus Triceratops? Geometric morphometric evidence of Late Maastrichtian Ceratopsid dinosaurs. PLoS ONE 8: e81608.
• Martin-Serra, A., Figuerido, B., and Palmqvist, P. 2014. A three-dimensional analysis of morphological evolution and locomotor performance of the carnivoran forelimb. PLoS ONE 9: 1–20.
• Mazzetta, G.V., Farina, R.A., and Vizcaino, S.F. 1998. On the palaeobiology of the South American horned theropod Carnotaurus sastrei Bonaparte. Gaia 15: 185–192.
• Meloro, C.C. and Jones, M.E.H. 2012. Tooth and cranial disparity in the fossil relatives of Sphenodon (Rhynchocephalia) dispute the persistent “living fossil” label. Journal of Evolutionary Biology 25: 2194–2209.
• Méndez, A. 2014. The cervical vertebrate of the Late Creteaceous abelisaurid dinosaur Carnotaurus sastrei. Acta Palaeontologica Polonica 59: 569–579.
• Novas, F.E., Agnolin, F.L., and Bandyopadhyay S. 2004. Cretaceous theropods from India; a review of specimens described by Huene and Matley (1933). Revista del Museo Argentino de Ciencias Naturales 6: 67–103.
• Novas, F.E., Agnolin, F.L., Ezcurra, M.D., Porfiri, J., and Canale, J.I. 2013. Evolution of the carnivorous dinosaurs during the Cretaceous: The evidence from Patagonia. Cretaceous Research 45: 174–215.
• O’Connor, P.M. 2007. The postcranial axial skeleton of Majungasaurus crenatissimus (Theropoda: Abelisauridae) from the Late Cretaceous of Madagascar. Journal of Vertebrate Paleontology, Memoir 8: 127–162.
• O’Connor, P.M., Rogers, R.R., Groenke, J.R., Burch, S.H., and Turner, A.H. 2011. A multi-taxon theropod dinosaur accumulation from the Late Cretaceous of Madagascar: near-instantaneous entombment of small-bodied avialans. Journal of Vertebrate Paleontology 31 (Supplement 3): 168.
• Openshaw, G.H. and Keogh, J.S. 2014. Head shape evolution in monitor lizards (Varanus): interactions between extreme size disparity, phylogeny and ecology. Journal of Evolutionary Biology 27: 363–373.
• Pierce, S.E., Angielczyk, K.D., and Rayfield, E.J. 2008. Patterns of morphospace occupation and mechanical performance in extant crocodilian skulls: a combined geometric morphometric and finite element modeling approach. Journal of Morphology 269: 840–864.
• Piras, P., Salvi, D., Ferrara, G., Maiorino, L., Delfino, M., Pedde, L., and Kotsakis, T. 2011. The role of post-natal ontogeny in the evolution of phenotypic diversity in Podarcis lizards. Journal of Evolutionary Biology 24: 2705–2720.
• Pol, D. and Rauhut, O.W.M. 2012. A Middle Jurassic abelisaurid from Patagonia and the early diversification of theropod dinosaurs. Proceedings of the Royal Society B 279: 3170–3175.
• Rauhut, O.W.M. and Fechner, R. 2005. Early development of the facial region in a non-avian theropod dinosaur. Proceedings of the Royal Society B 272: 1179–1183.
• Rohlf, J.F. 2013. tpsDig, Digitize Landmarks and Outlines, version 2.17. Department of Ecology and Evolution, State University of New York, Stony Brook. Available at http://life.bio.sunysb.edu/morph (accessed 7/1/2013).
• Rohlf, J.F. and Marcus, L.F. 1993. A revolution in morphometrics. Trends in Ecology and Evolution 8: 129–132.
• Russell, D. 1996. Isolated dinosaur bones from the middle Cretaceous of the Tafilalt, Morocco. Bulletin Muséum National d’Histoire Naturelle, Paris, séries 4C 18: 349–402.
• Sakamoto, M. 2010. Jaw biomechanics and the evolution of biting performance in theropod dinosaurs. Proceedings of the Royal Society B 277: 3327–3333.
• Sampson, S.D. and Krause, D.W. (eds.) 2007. Majungasaurus crenatissimus (Theropoda: Abelisauridae) from the Late Cretaceous of Madagascar. Society of Vertebrate Paleontology Memoir 8 (Supplement to Journal of Vertebrate Paleontology 27 [2]): 1–184.
• Sampson, S.D. and Witmer, L.M. 2007. Craniofacial anatomy of Majungasaurus crenatissimus (Theropoda: Abelisauridae) from the Late Cretaceous of Madagascar. In: S.D. Sampson and D.W. Krause (eds.), Majungasaurus crenatissimus (Theropoda: Abelisauridae) from the Late Cretaceous of Madagascar. Society of Vertebrate Paleontology Memoir 8 (Supplement to Journal of Vertebrate Paleontology 27 [2]): 32–102.
• Sampson, S.D., Witmer, L.M., Forster, C.A., Krause, D.W., O’Connor, P.M., Dodson, P., and Ravoavy, F. 1998. Predatory dinosaur remains from Madagascar: Implications for the Cretaceous biogeography of Gondwana. Science 280: 1048–1051.
• Schott, R.K., Evans, D.C., Goodwin, M.B., Horner, J.R., Brown, C.M., and Longrich, N.R. 2011. Cranial ontogeny in Stegoceras validum (Dinosauria: Pachycephalosauria): a quantitative model of pachycephalosaur dome growth and variation. PLoS ONE 6: e21092.
• Sereno, P.C. and Brusatte, S.L. 2008. Basal abelisaurid and carcharodontosaurid theropods from the Lower Cretaceous Elrhaz Formation of Niger. Acta Palaeontologica Polonica 53: 15–46.
• Sereno, P.C., Wilson, J.A., and Conrad, J.L. 2004. New dinosaurs link southern landmasses in the Mid-Cretaceous. Proceedings of the Royal Society B 271: 1325–1330.
• Stayton, C.T. and Ruta, M. 2006. Geometric morphometrics of the skull roof of stereospondyls (Amphibia: Temnospondyli). Palaeontology 49: 307–337.
• Tsuihiji, T., Watabe, M., Tsogtbaatar, K., Tsubamoto, T., Barsbold, R., Suzuki, S., Lee, A.H., Ridgely, R.C., Kawahara, Y., and Witmer, L.M. 2011. Cranial osteology of a juvenile specimens of Tarbosaurus bataar (Theropoda, Tyrannosauridae) from the Nemegt Formatipn (Upper Cretaceous) of Bugin Tsav, Mongolia. Journal of Vertebrate Paleontology 31: 497–517.
• Webster, M. and Zelditch, M.L. 2011. Evolutionary lability of integration in Cambrian ptychoparioid trilobites. Journal of Evolutionary Biology 38: 144–162.
• Wiley, D.F., Amenta, N., Alcantara, D.A., Ghosh, D., Kil, Y.J., Delson, E., Harcourt-Smith, W., Rohlf, F.J., John, K.S., and Hamann, B. 2005. Evolutionary morphing. Proceedings of IEEE Visualization 2005: 431–438.
• Wilson, J.A., Sereno, P.C., and Srivastava, S., Bhatt, D.K., Khosla, A., and Sahni, A. 2003. A new Abelisaurid (Dinosauria, Theropoda) from the Lameta Formation (Cretaceous, Maastrichtian) of India. Contributions from the Museum of Paleontology, University of Michigan 31: 1–42.
• Xu, X., Clark, J.M., Mo, J., Choiniere, J., Forster, C.A., Erickson, G.M., Hone, D.W.E., Sullivan, C., Eberth, D.A., Nesbitt, S., Zhoa, Q., Hernandez, R., Jia, C.-K., Han, F.-L., and Guo, Y. 2009. A Jurassic ceratosaur from China helps clarify avian digital homologies. Nature 459: 940–944.
• Young, M.T. and Larvan, M.D. 2010. Macroevolutionary trends in the skull of sauropodomorph dinosaurs—the largest terrestrial animals to have ever lived. In: A.M.T. Elewa (ed.), Morphometrics for Nonmorphometricians. Lecture Notes in Earth Sciences 124: 259–269.
• Young, M.T., Brusatte, S.L., Ruta, M., and De Andrade, M.B. 2010. The evolution of Metriorhynchoidea (Mesoeucrocodylia, Thalattosuchia): an integrated approach using geometric morphometrics, analysis of disparity, and biomechanics. Zoological Journal of the Linnean Society 158: 801–859.
• Zanno, L.E. and Makovicky P.J. 2011. Herbivorous ecomorphology and specialization patterns in theropod dinosaur evolution. Proceedings of the National Academy of Sciences 108: 232–237.
• Zelditch, M.L., Swiderski, D.L, Sheets, H.D., and Fink, W.L. 2004. Geometric Morphometrics for Biologists: A Primer. 443 pp. Elsevier Academic Press, San Diego.

Identyfikatory

DOI

10.4202/app.00132.2014