[Papers in Palaeontology, 2020, pp. 1–27] TOOTH REPLACEMENT IN MANIDENS CONDORENSIS: BASELINE STUDY TO ADDRESS THE REPLACEMENT PATTERN IN DENTITIONS OF EARLY ORNITHISCHIANS by MARCOS G. BECERRA1 ,DIEGOPOL1 , JOHN A. WHITLOCK2,3 and LAURA B. PORRO4 1Consejo Nacional de Investigaciones Cientıficas y Tecnicas (CONICET), Museo Paleontologico Egidio Feruglio, Fontana 140, Trelew, Chubut U9100GYO, Argentina; [email protected], [email protected] 2Biology Department, Mount Aloysius College, Admiral Peary Highway 7373, Cresson, PA 16630, USA; [email protected] 3Section of Vertebrate Paleontology, Carnegie Museum of Natural History, 4400 Forbes Avenue, Pittsburgh, PA 15213, USA 4Centre for Integrative Anatomy, Department of Cell & Developmental Biology, University College London, Gower Street, London, WC1E 6BT, UK; [email protected] Typescript received 4 March 2020; accepted in revised form 2 July 2020 Abstract: Dental replacement in Heterodontosauridae has Newly erupted teeth imbricate in a mesial cavity–distal been debated over the last five decades primarily on indirect crown base relationship during eruption, so that imbrication evidence, such as the development of wear facets and the of the midposterior dentition remains unaltered during tooth position of erupted teeth. Direct observation of unerupted replacement. The presence/absence of a small caniniform teeth provides unambiguous data for understanding tooth tooth in the D3 position of several specimens suggests possi- replacement but this has been done only for Heterodon- ble intraspecific dimorphism in Manidens. On longitudinal tosaurus and Fruitadens. This study addresses dental replace- sections of isolated crowns the histological features such as ment in Manidens condorensis based on the positioning of Howship’s lacunae and odontoclast spaces are similar in size functional and replacement teeth using microcomputed to extant reptiles. The differential wear decreasing posteriorly tomography data, differential wear along the dentition and and hypothetical Z-spacing below 2.3 in Manidens are simi- the differences in labiolingual/apicobasal level of functional lar to basal ornithischians. Tooth replacement in Heterodon- teeth. Dental replacement in Manidens condorensis was con- tosauridae (and other early ornithischians) provides key tinuous in an anterior-to-posterior wave pattern, with asyn- information for understanding the dynamics of jaw function chronous tooth eruption and the addition of new teeth and craniomandibular specialization to herbivory. posteriorly to the toothrow during ontogeny. Manidens shows the first evidence of dental replacement for the large Key words: Ornithischia, Heterodontosauridae, tooth dentary caniniform in Heterodontosauridae, which possibly replacement, 3D reconstruction, intraspecific dimorphism, had replacement timing distinct from the cheek dentition. dentition. T HE development of precise occlusion and tooth wear is a non-cerapodan ornithischians, non-hadrosaurid dry- recurrent trend that has improved chewing efficiency in omorphs and early ceratopsians (Norman & Weishampel different herbivorous lineages (Janis & Fortelius 1988; 1985; Weishampel & Norman 1989; Sander 1997; Norman MacFadden 2000; Kaiser et al. 2013; Madden 2014; Erick- 2004; Tanoue et al. 2009; Strickson et al. 2016). The condi- son et al. 2016). The consequences of extensive tooth wear tion of high replacement rates alongside tightly packed can be overcome by the appearance of high-crowned (hyp- dental batteries that form a continuous grinding surface is sodont) dentitions or high rates of tooth replacement a derived stage of polyphyodonty that appeared indepen- (D’Emic et al. 2013; Erickson et al. 2016). High replace- dently in ceratopsids, hadrosaurids, and some neosauro- ment rates have been inferred for many dinosaur clades, pods (Dodson et al. 2004; Horner et al. 2004; Sereno & including polyphyodont dentitions (i.e. dentitions with Wilson 2005; Bell et al. 2009). Within Heterodontosauridae continuous tooth replacement) with spaced teeth as in (and convergently shared with Therizinosauria; Button © The Palaeontological Association doi: 10.1002/spp2.1337 1 2 PAPERS IN PALAEONTOLOGY et al. 2017), more derived species had polyphyodont high- midposterior toothrow that allows close-packing, thick- crowned and tightly packed dentitions with low replace- ened enamel in the cutting edges of denticles (although ment rates, mixing two different evolutionary stages that only dentary teeth bear crenulated edges), and the devel- represent a novel adaptive path to increased herbivory in opment of apical and basal wear facets that indicate a the Ornithischia (Norman et al. 2011; Sereno 2012). The novel and complex pattern of tooth–tooth occlusion, above-mentioned cases indicate that different clades of her- making this taxon unique in terms of its adaptations to bivorous dinosaurs developed different adaptations to her- herbivory (Becerra et al. 2014, 2018). Here we describe bivory. However, there is still a lack of understanding of tooth replacement inferred for this taxon based on dental evolution in dinosaurs due to the small number of microcomputed tomography (lCT) of its dentition and studies of species representing early adaptive stages to her- interpret its significance for the early evolution of bivory (Stirton 1947; Erickson et al. 2016; Strickson et al. heterodontosaurids and ornithischians. 2016; Button et al. 2017). Furthermore, studies on tooth replacement in early ornithischians are rare despite their Institutional abbreviations. BP, Bernard Price Institute for importance for understanding the evolution of herbivory Palaeontological Research, Johannesburg, South Africa; in this diverse and successful clade (Sciscio et al. 2017; IVPP, Institute of Vertebrate Paleontology and Paleoan- Chen et al. 2018). thropology, Beijing, China; MPEF, Museo Paleontologico The middle–late Toarcian to Aalenian–Bajocian Egidio Feruglio, Trelew, Chubut, Argentina; NHMUK, Canad~ on Asfalto Formation (Cuneo et al. 2013) has The Natural History Museum London, UK; NM, Nazio- yielded one of the most important continental vertebrate nale Museum, Bloemfontein, South Africa; SAM, Iziko faunas from the early Jurassic of the southern hemi- South African Museum, Cape Town, South Africa; YPM, sphere (Bonaparte 1979; Rauhut et al. 2001; Escapa et al. Peabody Museum of Natural History, Yale University, 2008; Pol & Rauhut 2012). The record of ornithischians New Haven, USA. from this unit is so far limited to the heterodontosaurid Manidens condorensis (Pol et al. 2011); a second heterodontosaurid species lacking diagnostic features MATERIAL AND METHOD (Becerra et al. 2016); and an isolated ungual referred to Cerapoda (Rauhut & Lopez-Arbarello 2008). Manidens is Material the most complete early Jurassic ornithischian from South America and one of the most complete heterodon- All the fossil material used in this study is housed in tosaurids. The holotype material MPEF-PV 3211 of the the vertebrate palaeontology collection of the MPEF in small-sized heterodontosaurid Manidens condorensis, Trelew (Chubut), Argentina. All specimens included in which includes cranial and postcranial remains, preserves this study were found in the Queso Rallado locality a posteriorly incomplete right maxillary dentition and a except for MPEF-PV 3808, which was found in the nearly complete dentary dentition in both dentaries (Pol Frenguelli fossil site. Both localities belong to the lower et al. 2011). Regardless of its preservation, the maxillary levels of the Canad~ on Asfalto Formation (Pol et al. and dentary dentitions in known specimens range 2011; Cuneo et al. 2013; Becerra et al. 2014, 2018, between 10 and 13 tooth positions, a low count that is Becerra & Pol 2020). characteristic for Heterodontosauridae (Pol et al. 2011; Becerra et al. 2014, 2018). The morphology of the maxil- Specimen MPEF-PV 3211. The preserved elements on this lary dentition was characterized based on MPEF-PV 3211 specimen consist of at least 80% of the cranial bones, and 3809 by Becerra et al. (2018) as symmetric diamond- scattered vertebrae representing all axial regions (cervical, shaped teeth with a low number of denticles, enlarged dorsal and caudal vertebrae, and the complete sacral labial and lingual crests in the crown bases (cingular region), the left scapula and coracoid, an almost complete mesial and distal entolophs and ectolophs), with both pelvic girdle, and rib fragments (Pol et al. 2011; Becerra entolophs in a V- to Z-shaped disposition and bearing et al. 2014). The specimen corresponds to the holotype denticles/serrations. The morphology of the dentary den- material of Manidens condorensis, as defined by Pol et al. tition as detailed by Pol et al. (2011) and Becerra et al. (2011). (2014), is based on MPEF-PV 3211 and isolated teeth, and consists of an enlarged caniniform in the first tooth Specimen MPEF-PV 3808. This new specimen consists of position and symmetrical diamond-shaped (‘hand- partially exposed fossil remains at the face and back of a shaped’) postcaniniform teeth. Although these dentitions lacustrine tuffaceous shale rock fragment, corresponding to show a strongly contrasting morphology, they share a a right dentary, at least five dorsal vertebrae, most of a sca- height–width proportion heterodonty along the toothrow, pula, and other unidentified elements inside the rock (see the presence of a mesial cavity in teeth from the below). The poor preservation of the fossil prevents its BECERRA ET AL.: DENTAL REPLACEMENT IN MANIDENS