Question: When did the Pararhabdodon live?

Pararhabdodon


Pararhabdodon (meaning "near fluted tooth" in reference to Rhabdodon) is a genus of tsintaosaurin hadrosaurid dinosaur, from the Maastrichtian-age Upper Cretaceous Tremp Formation of Spain. The first remains were discovered from the Sant Romà d’Abella fossil locality and assigned to the genus Rhabdodon, and later named as the distinct species Pararhabdodon isonensis in 1993. Known material includes assorted postcranial remains, mostly vertebrae, as well as maxillae from the skull. Specimens from other sites, including remains from France, a maxilla previously considered the distinct taxon Koutalisaurus kohlerorum, an additional maxilla from another locality, the material assigned to the genera Blasisaurus and Arenysaurus, and the extensive Basturs Poble bonebed have been considered at different times to belong to the species, but all of these assignments have more recently been questioned.
Initially, the material was thought to belong to a rhabdodontid dinosaur, or some other similar type of primitive iguanodontian. Later discoveries of additional material revealed its true nature as a hadrosaur. Its placement within the group remained controversial - in 1999 it was proposed it belonged to the subfamily Lambeosaurinae, making it the first known from the continent of Europe. Later studies questioned this, instead classifying it as a more primitive hadrosauroid. In 2009 evidence was put forward that it was indeed a lambeosaurine, and more specifically a close relative of Tsintaosaurus, a genus from China. This position has been consistently found since, and the group containing them was later named Tsintaosaurini.
History and material
Sant Romà d’Abella material

Excavation of specimens that would later be used to erect Pararhabdodon began in Spring 1985, at the Sant Romà d’Abella (SRA) locality (in the Pyrenees near Isona, Lleida, Spain) of Tremp Formation.[1][2] In 1987, Casanovas-Cladellas et al. described remains of an ornithopod from Catalonia, including a cervical vertebra, some partial dorsals, a humerus, and a fragmentary scapula, as Rhabdodon sp.[3] New remains from this site, excavated in 1990,[2] brought about a reconsideration of the material, and Casanovas-Cladellas and colleagues named it as the new genus and species Pararhabdodon isonense in 1993. At the time, it was still considered to be a rhabdodont-like basal iguanodont, hence the name; isonense was in reference to Isona.[4]
Additional material from the type locality was collected in 1994 - including two maxillae, two dorsal vertebrae, a complete sacrum, two fragmentary ribs, and a partial ischium - and the species name was corrected to isonensis in 1997 by Laurent et al..[5] New material, most importantly cranial and mandibular elements (those from the skull) led to Casanovas-Cladellas' team re-classifying it as a hadrosaurid as opposed to a basal iguanodont.[6] In 1999 it was more specifically identified as a lambeosaurine hadrosaur, in a paper again by Casanovas-Cladellas et al.. This made it the first member of the subfamily from the continent, and the second valid hadrosaur, preceeded by Telmatosaurus and the dubious Orthomerus.[2][7]
In total, known material from the type locality includes: a left and a right maxilla; five cervical, five dorsal, and one caudal vertebra; a sacrum; fragmentary rib bones; one end of the right ischium; a fragment of the left scapula, an ulna and a humerus.[1][2][8] All of this material was excavated from a 4 metres (13ft) by 2.5 metres (8.2ft) surface, and it is thought to have belonged to a single individual.[2] The holotype is a nearly complete caudally located cervical vertebra (a cervical vertebra located near the base of the neck), specimen number IPS SRA-1.[1][3] Another cervical, a humerus, and an ulna were designated the paratype specimens.[2]
Referred material from other localities

In their 1997 paper, Laurent and colleagues referred additional remains (jaw material, vertebrae, and limb bones of multiple individuals of different ages) from the Le Bexen site of the uppermost Cretaceous of Aude, southern France, to the genus.[5][1] Prieto-Márquez and colleagues commented on this referral in a 2006 paper, though noting they had not examined the material themselves. They concluded all of the specimens, excepting one fragmentary humerus, were too poorly preserved to allow proper comparison with the Spanish Pararhabdodon material, and so disagreed with the referral. Of the humerus, they found it was distinguishable from P. isonensis, and so also not referable to the species.[1] A group composed of some of the same authors as the 2006 study, including Prieto-Márquez, investigated the material first hand for a 2013 re-evaluation of all European lambeosaurine material, and supported their previous conclusions.[8] Laurent had, in a 2003 dissertation, referred more French lambeosaurine material to Pararhabdodon; in this case, material held at the Musée des Dinosaures d’Espéraza. The referral was made as the genus was, at that point, the only lambeosaurine named from the continent.[8][9] Prieto-Márquez et al. (2013) used this material to establish their new taxon, Canardia garonnensis.[8]
In 2013, a maxilla, specimen designation MCD 4919, was referred to P. isonensis. It possessed synapomorphies of the tsintaosaurin tribe to which Pararhabdodon was by that point assigned to, and was referable to Pararhabdodon in particular due to rostrocaudally broad rostrocaudal region of the maxilla, a trait unique to P. isonensis relative to Tsintaosaurus, the other named tsintaosaurin taxon. The specimen was discovered at the Serrat del Rostiar 1 locality, part of the "lower red unit" of the Tremp formation just like the type locality, SRA, but in a lower section of the strata, making it older. This extended the range of species further within the upper Maastrichtian. The Serrat del Rostiar 1 locality is near the village of Basturns.[8] In 2019, the new genus and species Adynomosaurus arcanus was described, and in the paper describing the referral of MCD 4919 to P. isonensis was questioned. The specimen was found to have a differing ectopterygoid shelf to the maxilla of the SRA Pararhabdodon, which would conflict with their identity as belonging to the same species. As the specimen was still recognized as having tsintaosaurin characteristics, the authors still considered it to likely belong to a close relative of P. isonensis.[10]
The same study also evaluated Blasisaurus canudoi, from the Blasi 1 locality of the underlying Arén Formation, and Arenysaurus ardevoli, from the Blasi 3 locality of the earlier "gray unit" of the Tremp Formation. Previously claimed diagnostic traits of the two taxa were shown to be found in other hadrosaurs. This left the former with two unique characteristics - both in the jugal - and a unique combination of other characteristics, and the latter with only one unique characteristic - in the frontal. As overlapping fossils were not known for the relevant areas, it couldn't be ruled out that they were indeed synonymous, representatives of a single species. The same re-evaluation could not rule out that this single species or either of the separated species were synonyms of Pararhabdodon isonensis, as no taxonomically informative areas of the skeleton are known from both Pararhabdodon and the other two taxa. The authors refrained from considering any of them representatives of one species pending data from more material.[8]
Relationship with "Koutalisaurus"
Near the village Abella de la Conca, in the 1990s, palaeontologist Marc Boada discovered a new site in the Tremp Formation, bearing dinosaur fossils. From this site, later named Les Llaus (LL), a right dentary, specimen designation IPS SRA 27, was excavated.[1] In 1997, Casanovas-Cladellas and colleagues stated this dentary was discovered from SRA, the site where the original Pararhabdodon remains were found.[1][6] The following year, they described the specimen and referred it to P. isonensis, and again stated it was from the same stratigraphic level.[2] In 2006, the stratigraphy of the region was re-evaluated, and the dentary's location was corrected to the LL locality, 750 metres (2,460ft) away from and 9 metres (30ft) below the SRA locality.[1]

The same 2006 study, by Albert Prieto-Márquez and colleagues, noted that no dentary had been found at the SRA locality to compare to the LL specimen, and so they restricted P. isonensis to material known from its original locality. Additionally, they named a genus and species for IPS SRA 27, Koutalisaurus kohlerorum. The generic name is derived from the Greek word koutali, meaning spoon, in reference to the shape the jaw of the animal would've had, and the specific name honours Terry and Mary Kohler, for their support of vertebrate paleontology. One autapomorphy (unique trait) was used to diagnose the taxon as a new species: a very elongated edentulous section on the dentary, which was medially (inwardly) extended. No teeth were preserved, but there are 35 tooth positions. Several other European hadrosaur dentaries were compared based on published data, and the specimen was found to be unique compared to all of them. Though the specimen proved too fragmentary to be used for phylogenetic analysis, it was determined to be a hadrosaurid of some kind, more derived than Pararhabdodon, considered the sister taxon to Hadrosauridae. The authors noted the possibility future discoveries could lead to synonymization of their taxon with P. isonensis[1]

Evidence for this synonymy would later come in a 2009 study, from Prieto-Márquez alongside Jonathan R. Wagner. Material from Pararhabdodon, the holotype of Koutalisaurus, and material of the Chinese species Tsintaosaurus spinorhinus were examined and compared, and the edentulous slope previously thought unique to Koutalisaurus was found to be nearly identical in T. spinorhinus. It was noted various approaches could be taken to this matter. As the species K. koelerororum shared a unique trait with Tsintaosaurus and could not be distinguished from it, the former could be considered a junior synonym of the latter. However, it was noted that the likelihood of a large archosaur species with a large enough range to include both specimens is completely unprecedented, so they refrained from this referral. K. kohlerorum could instead be considered a nomen dubium, a taxon of uncertain distinctiveness due to lacking any autapomorphies. But they disliked this course of action too, as unless a second taxon with the same morphology was found in the area, they posited the specimen likely did represent a unique component of the local fauna. Thus, they decided to keep it distinct, relative to Tsintaosaurus. No material had, as yet, been discovered from the SRA locality permitting comparison with Pararhabdodon. However, traits uniting P. isonensis with T. spinorhinus were found. As both taxa from the Tremp Formation uniquely shared traits with the Asian genus, the authors decided to treat the two as one species, as maintaining them as provisionally separate would in their eyes be misleading to non-specialists, who would likely not distinguish the two taxa were kept separate to be conservative and not due to strong evidence for two hadrosaurs in the area.[11]
Prieto-Márquez returned again to the dentary in 2013, in a study alongside colleagues providing a review and investigation of hadrosaurs from all over Europe. Further preparation of the specimen in the time since his last study regarding it revealed the uniqueness of the dentary had been exaggerated significantly by reconstruction of the specimen when it was first prepared in the 1990s. The Tsintaosaurus specimens showing the similar condition were found to have been distorted from a similar process. Correcting for the innaccuracies, the Los Llaus dentary is indistinguishable from that of multiple lambeosaurines, and shares no particular connection to Tsintaosaurus. With this, their reasoning for assignment of the specimen to Pararhabdodon was voided, and the specimen is now considered a completely indeterminate lambeosaurine dentary.[8]
Basturs Poble bonebed

Marc Boada discovered, in the late 1990s, a new fossil-bearing locality 300 metres (980ft) from the village of Basturs. As the village already lent its name to a locality where dinosaur eggs had been found, it was named the Basturs Poble (BP) locality, "poble" derived from the word for village. The locality belongs to the Conques Formation of the Tremp Group, dated to the late-Early Maastrictian.[12] Over ten years, from 2001 through 2011, field work was done at this site, and a massive bonebed - consisting of some one thousand skeletal elements - was discovered.[12][13] The discovery was first reported in the literature in an abstract at the "55th Symposium for Vertebrate Palaeontology and Comparative Anatomy and the 16th meeting of the Symposium for Palaeontological Preparation and Conservation" conference in 2007. The authors, then, approached the bonebed under the hypothesis of a single species being present at the site. It was reported that all ontogenetic stages were present.[14] Later, a poster presentation and abstract at another conference suggested the specimens may have belonged to Koutalisaurus kohlororum, but they cautioned an adult dentary from the bonebed would need to be discovered to test the hypothesis.[15] This was later rejected, as Koutalisaurus was found to be an invalid nomen dubium.[8] In 2018, the material was instead noted as possibly referrable to Pararhabdodon isonensis.[12]
The stratigraphic layer where the bonebed was found is 1.5 metres (4.9ft) in thickness. Around 95% of all remains from the site belong to dinosaurs; nearly all identified specimens from this sample belong to hadrosaurs. Of prepared material, 270 skeletal elements can confidently be identified as belonging to hadrosauroids.[12][13] The number of hadrosaur specimens from the site in total could number over 500, and possibly as much as 900.[13][16] In addition to the large numbers of fossils of the animals themselves, the BP locality is one of many sites from the Tremp Syncline where hadrosaurs tracks have been found. At least one track is preserved at the site, in a sandstone block from a stratigraphic level similar to that of the bonebed.[13][17] It is the richest hadrosaur bonebed ever found in Europe, and the largest ever found in one palaeoinsular locale; as such, it is the most important hadrosauroid site of the eastern Tremp Syncline.[12][13]

The primary subject of research regarding the bonebed has been the taxonomic identity of the hadrosaurs there - namely, whether only one taxon or multiple taxa are present.[12] The question has been complicated by a rarity of cranial elements in the sample, since they are the most taxonomically informative areas of the skeleton in hadrosaurs.[12] Initially, it was assumed that only a single species was present in the sample.[14] In 2015, a study by Alejandro Blanco and colleagues performed multiple types of morphometric analysis to investigate hadrosaur diversity in from the Pyrenees using dentaries. The number of alveolar positions in the dentary was the primary metric for distinctiveness, as more basal taxa possess less, though it was noted this can also increase with age as an individual grows. Three morphotypes (groupings of specimens with a distinct anatomy from the other groupings) were found in the sample, of which two (numbers two and three) were present in the BP bonebed. Growth trajectory analysis of the different morphotypes supported their separation. Sexual dimorphism being the reason for different anatomy was considered unlikely due to different results in regression analysis. Morphotype three was interpreted as belonging to dwarf, potentially relictual hadrosauroids; and morphotype two was considered to represent larger, lambeosaurine animals. It was stressed each morphotype was not necessarily just one species, but merely representative of a distinct lineage of hadrosaurs.[16] In 2018, a more extensive study of the material was conducted by Víctor Fondevilla and colleagues, and the question of how many taxa were present of the sample was investigated using specimens from multiple parts of the body, as opposed to just the dentaries. Overall, a large amount of variation was noted in the specimens, but as it was gradual, rather than a case of two obvious morphotypes, the authors attributed it to individual variation. Regarding the dentaries, they too were not found to obviously sort into multiple morphotypes due to a high amount of variation between all of them. One particular dentary was noted to be rather distinct from the rest, but taphonomic damage or improper restoration during preparation of the fossil were considered possible explanations as opposed to taxonomic distinctiveness. The authors favored identification of the hadrosaurs present in the bonebed as a singular taxon of lambeosaurine.[12]

An intertwined subject to the taxonomy which has been noted and studied has been the size and ontogeny (growth and development) of the individuals represented. Individuals of multiple sizes are represented in the sample, but overall they represent smaller animals than the hadrosaurs known from Asian and North American species. Despite this, a small number of individuals falling into the adult size ranges of other hadrosaurs are indicated by isolated elements, such as femurs.[12][13] Multiple hypotheses have been put forward to explain this: firstly, juvenile individuals may have been the dominant life stage living in the area where the bonebed was preserved, due to ecological differences over lifespan; secondly, it's possible they represent dwarfed animals dominating the environment relative to rare a larger species; lastly, it's possible the large individuals were comparative giants of a single dwarfed species, near the extreme end of individual variation in the species.[13] The 2015 analysis of hadrosaur dentaries from the Pyrenees found two morphotypes to be present in the bonebed, so they favored the second hypothesis.[16] The more in-depth 2018 study used histological analysis in order to assess the age of different individuals, using tibiae. Of the several tibiae tested, four (between 390–450 millimetres (15–18in) long)  were identified as juveniles between the ages of one and three based on comparisons to tissue patterns in other ornithopods, and three more were found to likely be juveniles based on similarities to the former four. The eighth (550 millimetres (22in) long) and ninth (720 millimetres (28in) long) were found to belong to an early adult and subadult individual respectively. A 720 millimetres (28in) femur was found to share subadult growth features with the subadult tibia. Three tibiae (550 millimetres (22in), 600 millimetres (24in), and around 900 millimetres (35in) respectively) were found to belong to adult individuals. Growth trajectory was found to be consistent between the tibiae, supporting the idea that the site represents a large variety of age stages of a single species.[12]
Fondevilla et al. (2018) compared to the material from Basturs Poble to recognized species of lambeosaurine from geographically and temporally similar locations in the Pyrenees. The jugals from the sample were found to be distinct from those known from  Blasisaurus and Arenysaurus (possible synonyms of Pararhabdodon), and the frontals were also distinguishable from the latter. Identity as specimens as either of those taxa was therefore ruled out. Overlapping taxonomically informative material with Pararhabdodon was not found from the bonebed, excepting a maxilla too fragmentary for use in referral. However, both the type locality of SRA and the locality of the referred maxilla MCD 4919 are close to the area the bonebed was found. As such, it was considered most likely the Basturs Poble hadrosaurs are members of the species P. isonensis, but the poor state of preservation of the only comparable material in the bonebed prevented a secure referral.[12] Later, a 2019 study by Prieto-Márquez et al. described a new genus and species of Spanish lambeosaurine, Adynomosaurus arcanus. They compared the material of their species to that of the bonebed, and though similarities were found, their tooth crowns and ilia had different shapes, and the scapulae from the site lacked the distinct shallow nature that characterizes A. arcanus. Accordingly, they considered it unlikely the bonebed belonged to their species. Additionally, they commented on the lack of tsintaosaurin synapomorphies in the bonebed material and so kept a referral as indeterminate lambeosaurines rather than considering it to represent Pararhabdodon.[10]
Description
Pararhabdodon most likely was a bipedal-quadrupedal herbivore, in the neighborhood of 6m (19.7ft) long, fully grown. The dorsal and sacral neural spines were elongate, so the animal would have had a tall back, like other hadrosaurids.  Because the material is sparse, more specific conclusions cannot be reached.[1]
Classification

Pararhabdodon has been classified in a number of different positions within Iguanodontia since its remains were first discovered in the mid-1980s.[1][11] When the first speciemens were originally discovered and described by Casanovas-Cladellas and colleagues, they were not thought to belong a new taxon at all, but merely to belong to the genus Rhabdodon, and of an uncertain species.[3] Not long after, they would be recognized of those of a unique species, and in 1993 they were given their modern name. At this point it was still thought to be a rhabdodontid or some other type of primitive iguanodont closely related to them. This was based on the characteristics of its vertebrae, as the cranial remains had not yet been found.[4] In 1994 these cranial remains would be found - two maxilla - and these would be used by the original authors to establish it as a species of hadrosaur.[6]

Casanovas-Cladellas et al. revised their position for a final time in 1999, when they published a paper arguing for a position as a primitive member of the hadrosaur subfamily Lambeosaurinae - this made it the first such species known from the continent of Europe. Characters of the skeleton supporting this viewpoint were the truncated and rounded anatomy of the articulation of the maxilla to the jugal, the truncated nature of the back of the maxilla itself, the ventral deflection of the front of the dentary (thought the only known dentary was later referred to a new species, Koutalisaurus, and later declared that of indeterminate lambeosaurine[8]), its tall neural spines, and deltopectoral crest of the humerus being distally projected.[2]
The proposal that P. isonensis was the first known European lambeosaurine was soon challenged, however. In 2001, Jason Head, in a study re-evaluating the status of another species, Eolambia caroljonesa, as a primitive lambeosaur. Both were determined to instead be more primitive hadrosauroids more basal than the split between Lambeosaurinae and "Hadrosaurinae" (later renamed to Saurolophinae[18]). In regards to Pararhabdodon, this was based on rebuttal of arguments put forward in the 1999 study; the present anatomy maxilla-jugal articulation was not considered a synapomorphy in Lambeosaurinae, merely the presence of this in the jugal itself, unknown in the species, and the angular deltopectoral crest is a trait present even in primitive iguanodontians. Additionally, its tooth count was lower than those of known lambeosaurs.[19] In the 2006 re-evaluation of the genus by Albert Prieto-Márquez and colleagues, it was included in a phylogenetic analysis for the first time. This found it to be a non-hadrosaurid hadrosauroid, a similar position as had been argued by Head. The cladogram of Prieto-Márquez et al. (2006) is seen below on the left:[1]



































Iguanodon bernissartensis
Iguanodon atherfieldensis











Probactrosaurus gobiensis











Ouranosaurus nigeriensis











Protohadros byrdi















Bactrosaurus johnsoni
Gilmoreosaurus mongoliensis















Telmatosaurus transsylvanicus
Tanius sinensis











Pararhabdodon isonensisHadrosauridae











Hadrosaurinae
Lambeosaurinae

















Equijubus normani











Probactrosaurus gobiensis






















Protohadros byrdi
Eolambia caroljonesa











Tanius sinensis











Bactrosaurus johnsoni











Telmatosaurus transsylvanicus











Tethyshadros insularis











Lophorhothon atopusHadrosauridae











Hadrosaurus foulkii






















Edmontosaurus annectens
Brachylophosaurus canadensisLambeosaurinae











Aralosaurini











Jaxartosaurus aralensis










Tsintaosaurini











Tsintaosaurus spinorhinus
Pararhabdodon isonensis











Parasaurolophini
Lambeosaurini


Prieto-Márquez would return to the issue in 2009 along with Jonathan R. Wagner. They once again turned to the articulation between the maxilla and the jugal, finding this to link Pararhabdodon to the Asian lambeosaurine, Tsintaosaurus spinorhinus. In the 2006 phylogenetic analysis, P. isonenis had been scored as having an ancestral hadrosauroid condition for this trait, which had a strong effect on its position. Upon instead coding it for a modified version of the more advanced hadrosaurid condition, the connection between the two species to the exclusion of other lambeosaurines was supported. Multiple synapomorphies were found uniting to the two taxa, as well as identifying Pararhabdodon as a member of the subfamily as opposed to outside of Hadrosauridae.[11] This relationship was again supported in Prieto-Márquez et al. (2013), where the  group containing the two genera was coined as the taxonomic tribe Tsintaosaurini; a diagnosis for the tribe was provided. Their cladogram is reproduced above, on the right.[8]
See also
Timeline of hadrosaur research