The First Definite Lambeosaurine Bone From the Liscomb Bonebed of the Upper Cretaceous Prince Creek Formation, Alaska, United States

The Prince Creek Formation of Alaska, a rock unit that represents lower coastal plain and delta deposits, is one of the most important formations in the world for understanding vertebrate ecology in the Arctic during the Cretaceous. Here we report on an isolated cranial material, supraoccipital, of a lambeosaurine hadrosaurid from the Liscomb Bonebed of the Prince Creek Formation. The lambeosaurine supraoccipital has well-developed squamosal bosses and a short sutural surface with the exoccipital-opisthotic complex, and is similar to lambeosaurine supraoccipitals from the Dinosaur Park Formation in having anteriorly positioned squamosal bosses. Affinities with Canadian lambeosaurines elucidate more extensive faunal exchange between the Arctic and lower paleolatitudes which was previously suggested by the presence of Edmontosaurus, Pachyrhinosaurus, tyrannosaurids, and troodontids in both regions. The presence of one lambeosaurine and nine hadrosaurine supraoccipitals in the Liscomb Bonebed suggests hadrosaurine dominated faunal structure as in the Careless Creek Quarry of the USA that was also deposited under a near-shore environment. It differs from the lambeosaurine dominant structures of localities in Russia and China interpreted as inland environments. This may suggest that lambeosaurines had less preference for near-shore environments than hadrosaurines in both Arctic and lower paleolatitudes.

The ascending process is well-developed, taller and wider anteriorly than posteriorly, and divides the bone along the midline (Fig. 1a,d). It extends posterior to the posterior margin of the articulation surface with the exoccipital-opisthotic complex (Fig. 1a, 52 are nearly parallel or divergent, and those of non-hadrosaurid hadrosauroids (Bactrosaurus johnsoni 56 , Batyrosaurus rozhdestvenskyi 57 , Eolambia caroljonesa 58 , Eotrachodon orientalis 59 ) are strongly divergent posteroventrally. The dorsal surface of the ascending process is rounded (Fig. 1d) unlike the bi-lobed ascending process of Hypacrosaurus stebingeri (USNM 11893 54,55 ). The dorsal surface is rugose and lacks the nuchal crest. On either side of the ascending process, a deep post-temporal groove 53 runs anteroposteriorly (Fig. 1a,d) unlike in supraoccipitals of non-hadrosaurid hadrosauroids which have no distinct post-temporal groove [56][57][58][59] . The grooves are strongly divergent anteriorly as in the indeterminate lambeosaurine (CMN 0170 52,53 ; Fig. 2n Fig. 2b-e) which run nearly parallel to or only slightly divergent from each other. Lateral to the groove, an anterolaterally oriented squamosal boss is present (Fig. 1a,d) 58 ), in which the boss is also formed in part of the exoccipital-opisthotic complex.

Discussion
The new hadrosaurid supraoccipital DMNH 2014-12-266 largely differs from those of the Liscomb Edmontosaurus sp. in the presence of the well-developed squamosal bosses (Fig. 2a-e) and the short exoccipital articulation surface (Fig. 2f-j; Table 2). The length of the exoccipital articulation surface is equivalent with a phylogenetic character that differentiates hadrosaurines from lambeosaurines and non-hadrosaurid hadrosauroids (degree of the caudal extension of the supraoccipital-exoccipital shelf 35,61,62 ). The well-developed squamosal bosses are widely seen in lambeosaurines as well as in a few non-hadrosaurid hadrosauroids, but has never been reported in hadrosaurines ( Fig. 3; Table 2). The appearance of squamosal bosses is an ontogenetic change in the non-hadrosaurid hadrosauroid Bactrosaurus johnsoni 56 ; however, the presence of well-developed squamosal www.nature.com/scientificreports www.nature.com/scientificreports/ bosses in both juvenile (AMNH FARB 5461, skull length approximately 30% of the holotype MOR 549; Fig. 3g) and adult (MOR 455) individuals of Hypacrosaurus stebingeri suggests that the well-developed squamosal boss of DMNH 2014-12-266 is unlikely to be a result of ontogenetic variation but more likely is a taxonomic difference.
Isolated lambeosaurine supraoccipitals from the Oldman and Dinosaur Park formations can be divided into two morphotypes by the position of the squamosal bosses. While the squamosal bosses of the first morphotype (UALVP 48, UALVP 53092, and UALVP 53106 from the Oldman Formation and CMN 170 from the Dinosaur Park Formation; Fig. 2k,l,m,n) are posteriorly positioned, those of the other morphotype (UALVP 55300 and UALVP 54569 from the Dinosaur Park Formation; Fig. 2o,p) are anteriorly positioned, which are also seen in the Liscomb lambeosaurine (Fig. 2a). Although the Liscomb lambeosaurine shares this character with UALVP 55300 and UALVP 54569, it differs from UALVP 55300 in having posteriorly extended ascending process (Fig. 2a,f,o,u,p,v). Additionally, the Liscomb lambeosaurine differs from all other lambeosaurine supraoccipitals from the Oldman and the Dinosaur Park formations in having a rugose surface of the ascending . Dorsal (a-e,k-p) and ventral (f-j,q-v) views. Abbreviations: asp, ascending process; ap, anterior process; eo, articulation surface for the exoccipital-opisthotic complex; eog, exoccipital groove; nc, nuchal crestp, articulation surface for the parietal, ptg, post-temporal groove; sqb, squamosal boss. Scale = 2 cm. ( More than half as wide as the posteroventral margin of the supraoccipital Continued www.nature.com/scientificreports www.nature.com/scientificreports/ process, the laterally completed squamosal bosses, and the ventrally bowed posteroventral margin (Figs 1 and 2). Furthermore, the Liscomb lambeosaurine also differs from penecontemporaneous lambeosaurine Hypacrosaurus altispinus (AMNH FARB 5248) from the Horseshoe Canyon Formation, which has weakly developed ascending process and squamosal bosses that are partly formed by the exoccipital-opisthotic complex 60    www.nature.com/scientificreports www.nature.com/scientificreports/ supraoccipital characters with the Canadian specimens indicate that the Liscomb lambeosaurine is distinct from the Canadian specimens but shows affinities with the supraoccipitals from the Dinosaur Park Formation.
Previous studies suggested presence of lambeosaurine in the Arctic 29,64,65 with no definitive descriptions of fossil materials. Russell 65 , cited by Rich and others 66 , noted occurrence of lambeosaurine from the Bylot Island of Canada, but details of the record are unknown. Russell 64 and Gangloff 29 mentioned possible lambeosaurine records from the North Slope of the Alaska, but the identification in the former was based on a personal communication (by John R. Horner) and the latter did not provide a specimen number or the basis for the identification. The Liscomb lambeosaurine is the first definitive occurrence of this group from the Arctic and confirms that lambeosaurines inhabited the ancient Arctic terrestrial environment. This greatly expands the paleogeographic distribution of lambeosaurines much further north than previously known from taxa such as Hypacrosaurus altispinus from southern Alberta, Canada (Fig. 4). At the same time, the morphological affinities with the Canadian lambeosaurines elucidate more extensive faunal exchange between the Arctic and lower paleolatitudes within North America than previously suggested, which is also supported by the presence of Edmontosaurus, Pachyrhinosaurus, tyrannosaurids, and troodontids in both regions 4,12,13,15,25,35 .
The co-occurrence of hadrosaurine and lambeosaurine supraoccipitals from the Liscomb Bonebed suggests that the validity of Ugrunaaluk kuukpikensis should be treated with caution because hadrosaur bones from the bonebed may consist of these hadrosaurid sub-families as well as different ontogenetic stages 35 and, more importantly, indicates that hadrosaurine and lambeosaurine dinosaurs co-existed in the Cretaceous Arctic region. The presence of one lambeosaurine supraoccipital and eight previously reported hadrosaurine supraoccipitals 15 , as well as additional unpublished hadrosaurine specimens in the Perot Museum of Nature and Science collections, suggests numerical dominance of hadrosaurines over lambeosaurines in the ancient Liscomb region. While the hadrosaurine dominance may indicate their better adaptation to Arctic environment than lambeosaurines, hadrosaurine dominance is known from lower latitudes marine deposits 67 and regions closer to paleoshorelines of North America 68 and eastern Asia 34,[40][41][42][43][44]69 , indicative of near-shore environment preferences by hadrosaurines. Consequently, the hadrosaurine dominant faunal structure of the Liscomb Bonebed, deposited in lower coastal environment, may indicate that Arctic hadrosaurids performed environment preferences similar to those in the lower latitudes (Figs 5 and 6). www.nature.com/scientificreports www.nature.com/scientificreports/

Material and Method
DMNH 2014-12-266, collected from the Liscomb Bonebed and stored in the collection of the Perot Museum of Nature and Science, Dallas, USA, was examined and described herein. Its symmetrical shape and the endocranial wall suggest that the bone is a sagittal endocranial element such as basioccipital, basisphenoid, and supraoccipital. Absences of structures present in basioccipital and basisphenoid (occipital condyle, sphenoccipital tubera, foramina for cranial nerves, basipterygoid process) leaves supraoccipital the only possible candidate. Although multiple large tetrapods are known from the Prince Creek Formation, complete exclusion of supraoccipital from the foramen magnum, suggested by the rugose sutural surface for the exoccipital-opisthotic complex, indicate that the supraoccipital does not belong to basal ornithopod 70 , dromaeosaurids 71 , pachycephalosaurines 72 , troodintids 73 , or tyranosaurids 74 . Additionally, the absence of the rostrodorsal process suggest that it does not belong to ceratopsids 75 . On the other hand, DMNH 2014-12-266 resembles the supraoccipitals of hadrosaurids in complete exclusion from foramen magnum 26 and lambeosaurines and non-hadrosaurid hadrosauroids in presence of well-developed squamosal bosses [52][53][54]56,57,59 . Therefore, DMNH 2014-12-266 is identified as a supraoccipital of hadrosauroid.