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Remains from Basturs Poble Bonebed (Late Early Maastrichtian, Tremp Syncline, Spain)

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Remains from Basturs Poble Bonebed (Late Early Maastrichtian, Tremp Syncline, Spain) RESEARCH ARTICLE Ontogeny and taxonomy of the hadrosaur (Dinosauria, Ornithopoda) remains from Basturs Poble bonebed (late early Maastrichtian, Tremp Syncline, Spain) 1,2 1,3 4 1,4 VõÂctor FondevillaID *, Fabio Marco Dalla Vecchia , Rodrigo Gaete , Àngel Galobart , Blanca Moncunill-Sole 1,5, Meike KoÈ hler1,6 a1111111111 1 Institut Català de Paleontologia Miquel Crusafont, Sabadell, Catalonia, Spain, 2 Departament de Geologia, Universitat Aut noma de Barcelona, Bellaterra, Catalonia, Spain, 3 Museo Friulano di Storia Naturale, Udine, a1111111111 ò Italy, 4 Museu de la Conca Dellà, Isona (Lleida), Catalonia, Spain, 5 Departament de Biologia Animal i a1111111111 Vegetal, Universitat Autònoma de Barcelona, Bellaterra, Catalonia, Spain, 6 Institucio Catalana de Recerca i a1111111111 Estudis AvancËats ICREA, Barcelona, Catalonia, Spain a1111111111 * [email protected], [email protected] Abstract OPEN ACCESS Citation: Fondevilla V, Dalla Vecchia FM, Gaete R, The lower Maastrichtian site of Basturs Poble (southern Pyrenees, Spain) is the first hadro- Galobart À, Moncunill-Sole B, KoÈhler M (2018) saur bonebed reported from Europe. It is an accumulation of disarticulated lambeosaurine Ontogeny and taxonomy of the hadrosaur skeletal elements, possibly belonging to Pararhabdodon isonensis. The sample shows high (Dinosauria, Ornithopoda) remains from Basturs intraspecific morphological variability among many skeletal elements, suggesting the need Poble bonebed (late early Maastrichtian, Tremp Syncline, Spain). PLoS ONE 13(10): e0206287. for caution in choosing characters for phylogenetic analyses. Juvenile to adult individuals are https://doi.org/10.1371/journal.pone.0206287 represented in the sample, while hatchling remains are absent. Bone histology reveals that Editor: Phil R. Bell, University of New England, juveniles are over-represented and that the youngest individuals represented by tibia speci- AUSTRALIA mens were two years old. Adult individuals, with tibiae 550±600 mm long, were 14±15 years Received: November 13, 2017 old when they died. However, individual variation in tibia length at skeletal maturity occurs within the sample, so individual maturity cannot be assumed on the basis of bone size alone. Accepted: October 9, 2018 The Basturs Poble bonebed occurs within the upper part of the C31r magnetochron. Thus, Published: October 31, 2018 lambeosaurine hadrosaurids were already present and abundant in the Ibero-Armorica Island Copyright: © 2018 Fondevilla et al. This is an open at the end of the early Maastrichtian and P. isonensis spans the upper part of the lower Maas- access article distributed under the terms of the trichtian to the upper part of the upper Maastrichtian (upper part of C31r-lower part of C29r). Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Introduction Funding: This paper is a contribution to the During the latest Cretaceous (the Campanian and Maastrichtian Ages, 83.6±66 Ma), hadro- projects CGL2011-30069-C02-01 (PI: ÀG), saurid hadrosauroids were the dominant herbivorous dinosaurs of the Asian and North Ameri- CGL2016-77230-P (PI: ÀG) and CGL-2015-63777 can landmasses [1]. Europe at that time was an archipelago of comparatively small islands that (PI: MK) funded by the Spanish Ministerio de EconomõÂa y Competitividad (www.mineco.gob.es, was populated by both hadrosaurids and the more primitive non-hadrosaurid hadrosauroids and the projects 20014/100927 (PI: ÀG) and 2014- (the latter including Telmatosaurus transsylvanicus from Romania and Tethyshadros insularis SGR-1207 (PI: MK) funded by the Generalitat de from Italy; [2]). European hadrosauroid remains are reported from the uppermost Cretaceous PLOS ONE | https://doi.org/10.1371/journal.pone.0206287 October 31, 2018 1 / 33 The Basturs Poble hadrosaur bonebed: Ontogeny and taxonomy Catalunya (www.gencat.cat). V. Fondevilla of Ukraine, Bulgaria, Romania, Italy, Slovenia, Germany, Belgium and the Netherlands, but acknowledges support from the Ministerio de most of the hadrosauroid sites are in the French and Spanish Pyrenees [2,3]. To date, four EconomõÂa y Competitividad (FPI grant, BES-2012- hadrosauroid taxa (all belonging to the Lambeosaurinae) have been named from the Pyrenees: 052366). The funders had no role in study design, data collection and analysis, decision to publish, or Pararhabdodon isonensis Casanovas-Cladellas, SantafeÂ-Llopis and Isidro-Llorens [4]; Areny- preparation of the manuscript. saurus ardevoli Pereda-Suberbiola, Canudo, Cruzado-Caballero, Barco, LoÂpez-MartõÂnez, Oms and Ruiz-Omeñaca [5]; Blasisaurus canudoi Cruzado-Caballero, Pereda-Suberbiola and Ruiz- Competing interests: The authors have declared that no competing interests exist. Omeñaca [6]; and Canardia garonnensis Prieto-MaÂrquez, Dalla Vecchia, Gaete and Galobart [3]. However, most of the hadrosauroid material from the Pyrenees cannot be referred to spe- cies and genus level, because of fragmentary or missing-diagnostic features [2,3,7±10]. Basturs Poble (henceforth referred to as BP) is the richest of the hadrosauroid-bearing local- ities from the southern Pyrenees [7]. It is the largest hadrosauroid sample from a single locality and horizon in a palaeoinsular context, because the present-day Pyrenean region was part of an island (the Ibero-Armorican Island) within the European Archipelago during latest Creta- ceous times [11]. In the absence of evidence supporting the presence of distinct species, the BP hadrosauroid sample initially was referred to a single hadrosauroid species at different ontogenetic stages [12,13]. Prieto-MaÂrquez et al. [14] provisionally referred this species to the Lambeosaurinae on the basis of features of the jugal and maxilla, and suggested that it could be Koutalisaurus kohlerorum. However, this taxon later was demonstrated to be invalid, because its holotype and unique specimen (an incomplete dentary) lacks autapomorphies or an autapomorphic combination of characters [3]. Blanco et al. [15] identified two differently-sized dentary morphotypes in the BP sample by multivariate analysis. A monotaxic sample was ruled out on the basis of the different allometric trajectories of the small and larger dentary morphotypes, and the small "morphotype 3" was referred to a distinct, basal and possibly dwarf hadrosauroid taxon. This paper deals with the osteology, histology and taxonomy of the hadrosauroid specimens from the BP bonebed. Our aim is to establish: 1) whether the presence of more than one taxon can be detected through morphological and histological study; 2) the size distribution and the frequency of ontogenetic stages within the assemblage; 3) the systematic affinity of that taxon/ those taxa at the clade level (non-hadrosaurid hadrosauroid, hadrosaurid, saurolophine or lambeosaurine) or at the species level. The relative abundance of fossil remains allowed us to undertake a histological study of the BP hadrosauroids in order to identify the ontogenetic stage (juvenile, subadult, or adult) of dif- ferently-sized individuals and hopefully to establish the presence of one or more species in the sample. In order to achieve this, we constructed a growth curve using the most-represented skeletal elements. Institutional abbreviationsÐIPS, Institut de Paleontologia Miquel Crusafont, currently ICP, Institut Català de Paleontologia `Miquel Crusafont', Sabadell, Spain; MCD, Museu de la Conca Dellà, Isona, Spain; MPZ, Museo PaleontoloÂgico de la Universidad de Zaragoza, Zara- goza, Spain; TMP, Royal Tyrrell Museum of Paleontology, Drumheller, Canada; ROM, Royal Ontario Museum, Toronto, Canada. Material and methods Field work at the BP locality was undertaken in 2001±2007 and 2009±2011 by the MCD and the IPS-ICP. All necessary excavation permits were obtained for the described study, which complied with all relevant regulations. They were granted by the Catalan Government (Depar- tament de Cultura, Generalitat de Catalunya). Permit numbers are: 494 K0121 N355, 437 K121 N355, 437 K121 N355 3793, 470 K121 N355/-2011-1-6910. The fossil specimens and PLOS ONE | https://doi.org/10.1371/journal.pone.0206287 October 31, 2018 2 / 33 The Basturs Poble hadrosaur bonebed: Ontogeny and taxonomy thin sections involved in this study are deposited and accessible to other researchers at the MCD (Isona, Spain) and the ICP (Bellaterra, Cerdanyola del Vallès, Spain), respectively. Per- mission was granted to the authors for accessing the collections at the MCD, ICP and the TMP (Drumheller, Canada) in order to examine the materials housed at these institutions. The portion of the prepared BP sample that can be referred to hadrosauroids with confi- dence is composed of 270 skeletal elements, which mostly are incomplete or fragmentary. Thirty-six specimens are from the skull and lower jaw (17 are cranial elements and 19 are den- taries); three are isolated teeth; 131 or 132 are axial elements (21 belonging to cervical vertebrae, five to dorsal vertebrae, 11 to the sacrum [including three partial sacra], 48 to caudal vertebrae, 15 to unidentified vertebrae, 14 to dorsal ribs, seven or eight to chevrons, and ten to segments of ossified tendons); eight are girdle elements (six from the shoulder and two from the pelvic gir- dle); and 92 are limb bones (10 humeri, five ulnae, three radii, five metacarpals, one manual phalanx, 23
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