The evolution of jaw mechanism and dental function in heterodont crocodyliforms ATTILA ŐSI1 1Hungarian Academy of Sciences – Eötvös Loránd University, Lendület Dinosaur Research Group, Pázmány Péter sétány 1/c, Budapest, 1117, Hungary; e-mail: [email protected] ABSTRACT Heterodont dentition sometimes including multicuspid crowns appeared in numerous fossil forms through all main lineages of the Crocodyliformes. Teeth in these complex dentitions frequently bear wear facets that are exclusive indicators of tooth–tooth occlusion. Besides dental features, specializations of the jaw apparatus, jaw adductors and mandibular movement can be recognized, all reflecting a high variability of jaw mechanism and of intraoral food processing. Comparative study of these features revealed four main types of jaw mechanism some of which evolved independently in several lineages of Crocodyliformes. Isognathous orthal jaw closure (precise jaw joint, rough wear facets) is characteristic for heterodont protosuchians and all forms possessing crushing posterior teeth. Proal movement (protractive powerstroke) occured independently in Malawisuchus and Chimaerasuchus is supported by the antagonistic, vertically oriented carinae. Developed external adductors are the main indicators of palinal movement (retractive powerstroke) that evolved at least two times in various South American taxa. The fourth type (in Iharkutosuchus) is characterized by lateromedial mandibular rotation supported by extensive horizontal wear facets. This evolutionary scenario resembles that of the masticatory system of mammals and suggests that the ecological roles of some mammalian groups in North America and Asia were occupied in Western Gondwana by highly specialized crocodyliforms. INTRODUCTION Generally, the feeding apparatus and feeding mechanism of crocodyliforms is regarded as conservative because it does not show radical changes during the evolution of the group. Among the few hundred valid species from protosuchians to the 23 extant taxa, tooth and jaw morphology, jaw articulation and adductor muscle architecture did not change significantly in most species. Their dentition is formed usually of widely-spaced, conical, monocusped teeth (although with highly variable in tooth count), dominantly with unserrated mesiodistal carinae mesiodistally. Jaw articulation is precise with quadrate condyles separated by a marked intercondylar groove and the condyles nicely fit into the glenoid cavity of the articular. This is a key feature (along with the wide pterygoid flanges preventing lateromedial movement) to ensure precise orthal movement during opening and closure of the jaws. Of the jaw adductor musculature, the main muscle groups are the pterygoid muscles (MPT) and the external adductors (parts of the MAME). Their state of development and importance in the jaw closure, however, alternate depending on skull architecture and the mode of prey capture. For example, in longirostrine forms (thalattosuchians, dyrosaurs, gavial) being dominantly aquatic piscivorous predators, the bundles of the external adductors responsible for rapid jaw closure (like the temporalis muscles in mammals, Smith 1993) are highly developed and play an extremely important role in food capture. These muscles have short bundles and are responsible for a relatively fast jaw closure (Iordansky 1964, Mueller-Töwe 2006). In small bodied, brevirostrine forms (e.g. Bernissartia, Allognathosuchus, Brachychampsa, Iharkutosuchus) often possessing bulbous crushing teeth the pterygoid muscles responsible for relatively slow but effective jaw closure (like the masseter and pterygoid muscles in mammals, Smith 1993) are the dominant adductors (Ősi and Weishampel 2009, Figure 1). In the last decades, however, new discoveries, especially in former Gondwanan landmasses, provided evidence for diverse and abundant assemblages of highly specialized crocodyliforms (Figure 2) that possess heterodont, sometimes mammal-like dentition (Figure 3) (e.g. Clark et al. 1989, Carvalho 1994, Buckley et al. 2000, Pol 2003, Nobre and Carvalho 2006, Marinho and Carvalho 2009, O’Connor et al. 2010, Iori and Carvalho 2011). These forms are usually characterized by complex jaw mechanism complemented by dental occlusion that refers to efficient oral food processing (Ősi 2010). The appearence of these fundamental craniodental features among Cretaceous Gondwanan notosuchians suggests that these small bodied forms „probably filled niches and inhabited ecomorphospace that were otherwise occupied by mammals on northern continents” (O’ Connor et al. 2010:748). Nevertheless, crocodyliforms with mammal-like craniodental features were not restricted to the notosuchian clade and to the Cretaceous Gondwana but they also occured in the Early Jurassic of North America and in the Cretaceous of Europe and eastern Asia, where they were represented by both the protosuchian and modern, eusuchian clades (Young 1973, Li 1985, Clark and Fastovsky 1986, Sues et al. 1994, Wu et al. 1995, Pol et al. 2004, Ősi et al. 2007). In addition to these forms with multicusped teeth, the bulbous, crushing teeth in several lineages of the neosuchian crocodyliforms (e.g. Weitzel 1935, Buffetaut and Ford 1979, Buscalioni and Sanz 1990, Brinkmann 1992, Norell et al. 1994, Brochu 1999, Lucas and Estep 2000, Ősi 2010, Ősi and Barrett 2011) represent a further adaptation among the specialized feeding strategies of the group that, again, clearly emphasizes that feeding adaptations within the Crocodyliformes were much more diverse than previously thought. The aim of this work is to collect, review and compare all these specialized heterodont crocodyliforms in a functional perspective completed with the descripton and detailed illustration of the cranial material and craniodental features. Reconstruction of the main cranial adductors and analyses of dental wear patterns are fulfilled to understand the process of dental occlusion and movements of the lower jaw during food processing in each taxon. Putting the taxa in a phylogenetic context, the evolution of craniodental characters and jaw mechanisms is discussed. Results of these investigations offer new insights into the evolution of crocodyliform trophic adaptations and in the case of Gondwanan notosuchians they help to reconstruct possible scenarios of competition, dietary overlap and partitioning between small bodied, heterodont crocodyliforms and mammals. Institutional Abbreviations— ACAP Association Culturelle, Archéologique et Paléontologique de l’Ouest Biterrois, Cruzy, Hérault, France; BSM, Bayerische Staatssammlung für Paläontologie und Geologie, Münich, Germany; FMNH, The Field Museum, Chicago, USA; HLMD, Hessisches Landmuseum; Darmstadt, Germany; IPFUB, Institut für Paläontologie der Freien Universität, Berlin, Berlin, Germany; IRSNB, Institut Royal des Sciences Naturelles de Belgique, Bruxelles, Belgium; IVPP, Institute of Vertebrate Paleontology and Paleoanthropology, Beijing, People’s Republic of China; MACN, Museo Argentino de Ciencias Naturales, Buenos Aires, Argentina; MAL, Malawi Department of Antiqities, Malawi; MCSNT, Museo Civico di Storia Naturale di Trieste, Italy; MN, Museu Nacional, Rio de Janeiro, Brasil; MNHN, Musée National d'Histoire Naturelle, Paris, France; MPMA, Museu de Paleontologia de Monte de Alto, Monte Alto, Brasil; MTM, Hungarian Natural History Museum, Budapest, Hungary; MZSP-PV, Museu de Zoologia, Universidade de São Paulo, Brazil; NHM, Natural History Museum, London, England; UA, University of Antananarivo, Antananarivo, Madagascar; UCMP, Museum of Paleontology, University of California, Berkeley, USA; UFRJ, Universidad Federal do Rio de Janeiro, Brazil. Anatomical abbreviations used in the figures: a anterior icgr intercuspidate groove acav accessory cavities of the antorbital if incisive foramen fossa imf caudal intermandibular foramen acc accessory cusp j jugal adt anterior dentary tooth l lateral aexa attachment area of external la labial adductors lacr lacrimal agr apical groove lac labial cusp aMAMP attachment surface for lal last alveolus MAMP larc labial row of cusps aMPTV attachment surface for lawf labial wear facet MPTV lca lower caniniform tooth alv alveolus lco lateral cotyle amx1 first maxillary alveolus ler longitudinal enamel ridges an angular li lingual aof antorbital fenestra lic lingual cusp ap apical lirc lingual row of cusps ar articular liwf lingual wear facet awf apical wear facet ls laterosphenoid ba basal ltf lateral temporal fenestra bc broken crown m medial bit bicusped teeth MAMEM Musculus adductor bo basioccipital mandibulae externus c carina medialis ca caniniform tooth MAMEP Musculus adductor car cervical armour mandibulae externus ced distal carina of the central cusp profundus ch choana MAMES Musculus adductor ci cingulum mandibulae externus co coronoid superficialis coa conical apex MAMP Musculus adductor cr crest mandibulae posterior crc central row of cusps mc main cusp d dentale mcq medial condyle of the quadrate de dentine me mesial d1–10 first to tenth dentary teeth MI Musculus intramandibularis di distal mot molariform teeth do dorsal mpf maxilla–palatine foramen ec ectopterygoid MPSS Musculus pseudotemporalis edi enamel–dentine interface superficialis emf external mandibular fenestra MPTD Musculus pterygoideus ena external nares dorsalis en enamel MPTV Musculus pterygoideus fm foramen magnum ventralis fo foramen mri median ridge fr frontal mut multicusped tooth gl glenoid surface mx maxilla gr groove mx1–10 first to sixth maxillary teeth mxsh maxillary