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

The First Definite Lambeosaurine Bone From the Liscomb Bonebed of the Upper Cretaceous Prince... www.nature.com/scientificreports opeN The First Definite Lambeosaurine Bone From the Liscomb Bonebed of the Upper Cretaceous Prince Creek Received: 30 September 2018 Formation, Alaska, United States Accepted: 1 March 2019 Published: xx xx xxxx 1 2 3 2 Ryuji t akasaki , Anthony R. Fiorillo , Yoshitsugu Kobayashi , Ronald S. t ykoski & Paul J. McCarthy 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. Vertebrate animals in the Arctic have experienced physiological, behavioral, and morphological adaptations to 1–3 survive in an extreme environment . Rocks from the North Slope of Alaska are important for the understanding 4,5 of the ecology of fossil vertebrates in the Arctic during the Cretaceous Period . There are abundant fossiliferous exposures of the lower part of the Prince Creek Formation on the North Slope, which range from Campanian to early Maastrichtian in age . e Th Prince Creek Formation is a non-marine succession deposited on a high-latitude, low-gradient alluvial/coastal plain. An integrated reconstruction of pedogenic processes and biota suggests that this ancient Arctic coastal plain was influenced by seasonally fluctuating water table levels and floods, and in distal areas, marine waters. The formation has yielded a diverse dinosaur assemblage that includes ceratopsids, 4,5,8–16 dromaeosaurids, hadrosaurids, basal ornithopods, pachycephalosaurids, troodintids, and tyrannosaurids . e Th Liscomb Bonebed is one of the most prolic fi dinosaur bearing localities within this rock unit. Radiometric dating based on tephra near the bonebed indicates that the Liscomb Bonebed is early Maastrichtian with esti- 17 18 19 mated ages of 71–68 Ma , 69.1 ± 0.3 Ma , and younger than 69.2 ± 0.5 Ma . These dates are concordant with 20,21 palynomorph analyses which suggest early Maastrichtian age . The rocks were deposited at an estimated pale- olatitude of 74.5° ± 7.5° . The Liscomb Bonebed is from the distal area of coastal plain and is represented by lower delta plain facies . Further, the stratigraphic interval containing the Liscomb Bonebed represents a series of 19,23 episodic floods and specifically these episodic flood events created deposition by fine-grained viscous hyper - concentrated flows that transported the remains of scores of juvenile dinosaurs onto floodplains adjacent to dis- tributary channels. The Liscomb Bonebed is characterized by high specimen density (up to 160–220 elements/m ) Department of Natural History and Planetary Sciences, Hokkaido University, Kita 10, Nishi 8, Kita-ku, Sapporo, 2 3 Hokkaido, 060-0810, Japan. Perot Museum of Nature and Science, Dallas, Texas, 75201, United States. Hokkaido University Museum, Kita 10, Nishi 8, Kita-ku, Sapporo, Hokkaido, 060-0810, Japan. University of Alaska, Department of Geosciences, Fairbanks, Alaska, 99775, United States. Correspondence and requests for materials should be addressed to A.R.f . (email: tony.fiorillo@perotmuseum.org ) Scientific Repo R ts | (2019) 9:5384 | https://doi.org/10.1038/s41598-019-41325-8 1 www.nature.com/scientificreports www.nature.com/scientificreports/ Figure 1. Lambeosaurine supraoccipital (DMNH 2014-12-266) from the Liscomb Bonebed. (a) Dorsal view. (b) Ventral view. (c) Left lateral view. (d) Posterior view. (e) Anterior view. (f) Right lateral view. Abbreviations: asp, ascending process; eo, articulation surface for the exoccipital-opisthotic complex; eog, exoccipital groove; ptg, post-temporal groove; sqb, squamosal boss. Scale = 2 cm. 15,24 and has yielded over six thousand bones . It is a monodominant multitaxic bonebed consisting of three thero- 7,10,25 pod taxa (dromaeosaurid, troodontid, and tyrannosaurid) and hadrosaurid skeletal elements which com- prises 98.5% of dinosaur skeletal elements . The Hadrosauridae is a derived clade of Hadrosauroidea and comprise two stem-sister lineages, Lambeosaurinae and Hadrosaurinae . The Liscomb hadrosaurid materials were initially identified as Lambeosaurinae , although osteological features to support the identification were not provided. Comparisons based on isolated cranial elements later demonstrated that the Liscomb hadrosaurs showed close similarity to the hadrosaurine Edmontosaurus saskatchewanensis , which is now considered a junior synonym of Edmontosaurus annectens . Since then, a general consensus formed that the Liscomb hadrosaur bones represent specimens of 5,23,29–34 Edmontosaurus . Recently, it was proposed that the Liscomb hadrosaur bones represent a new distinct hadrosaurine taxon, Ugrunaaluk kuukpikensis . However, subsequent workers argued that the proposed new taxon was invalid in part because it was diagnosed on immature growth stage features preserved in the known specimens . Despite of the taxonomic controversy, these studies have agreed upon the presence of a hadrosaurine hadrosaurid in the Liscomb Bonebed. Here we report the first definitive lambeosaurine hadrosaurid fossil from the Liscomb Bonebed (DMNH 2014–12–266), represented by an isolated cranial material, a supraoccipital. The supraoccipital demonstrates that the Liscomb Bonebed contains both lambeosaurine and hadrosaurine materials. While co-occurrences of hadro- 36–38 saurine and lambeosaurine are widely known in the northern hemisphere (e.g., Careless Creek Quarry and 39 40,41 42,43 Jack’s Birthday Site of Montana, United States; Blagoveschensk locality and Kundur localities of southern Amur region, Russia; and Wulaga locality of northern Heilongjiang Province, China), the Liscomb Bonebed is the first to demonstrate the co-occurrence in the Arctic. Therefore, the new discovery oer ff s an important oppor - tunity to infer possible determinant factors of hadrosaurid taxonomic structure in the Arctic, in comparison with lower latitude regions. Results Systematic paleontology. Dinosauria Owen, 1842 Ornithischia Seeley, 1887 Cerapoda Sereno, 1986 Ornithopoda Marsh, 1881 Iguanodontia Dollo, 1888 Hadrosauridae Cope, 1870 Lambeosaurinae Parks, 1923 Description. The new supraoccipital (DMNH 2014-12-266; Fig.  1) is nearly complete but missing both anterior processes and anterodorsal end of the ascending process. Its maximum width along the posteroven- tral margin is 44.8 mm, which is slightly larger than those of Edmontosaurus sp. specimens from the Liscomb 52,53 Bonebed, nearly equivalent with that of the indeterminate lambeosaurine CMN 0170 , and smaller than that of Prosaurolophus maximus MOR 447-8-8-7-14 (Table 1). The width is also much less than the posteriorly exposed supraoccipital surfaces of adult articulated skulls of Edmontosaurus regalis (100.3 mm, CMN 2278), Gryposaurus notabilis (102.4 mm, CMN 2288), Hypacrosaurus stebingeri (87.1 mm, MOR 553 s; 98.0 mm, MOR 455), and Lambeosaurus lambei (79.5 mm, ROM 1218). Its small size may indicates that the supraoccipital (DMNH 2014- 12-266) belonged to an immature individual. Scientific Repo R ts | (2019) 9:5384 | https://doi.org/10.1038/s41598-019-41325-8 2 www.nature.com/scientificreports www.nature.com/scientificreports/ Length, ventral Width, posteroventral Maximum L/W ratio H/W ID Formation Subfamily Taxa surface (mm) margin (mm) height (mm) (%) ratio (%) DMNH 2014-12-266 Prince Creek Formation Lambeosaurinae unknown 12.0 44.8 24.9 26.8% 55.6% USNM 11893 Two Medicine Formation Lambeosaurinae Hypacrosaurus stebingeri 17.9 52.8 35.3 33.9% 67.0% UALVP 48 Oldman Formation Lambeosaurinae unknown 13.4 38.1 22.2 35.2% 58.3% UALVP 53092 Oldman Formation Lambeosaurinae unknown 25.8 66.3 37.9 38.9% 57.1% UALVP 53106 Oldman Formation Lambeosaurinae unknown 17.5 48.4 — 36.0% — CMN 0170 Dinosaur Park Formation Lambeosaurinae unknown 19.4 46.8 24.1 41.4% 51.5% UALVP 54569 Dinosaur Park Formation Lambeosaurinae unknown 28.4 — 29.1 — — UALVP 55300 Dinosaur Park Formation Lambeosaurinae unknown 17.1 43.2 26.2 39.7% 60.7% DMNH EPV 127701 Lance Formation Hadrosaurinae Edmontosaurus annectens 66.0 48.5 33.6 135.9% 69.2% MOR 447-8-8-7-14 Two Medicine Formation Hadrosaurinae Prosaurolophus maximus 43.0 85.7 34.7 50.1% 40.5% DMNH 22807 Prince Creek Formation Hadrosaurinae Edmontosaurus sp. 24.4 30.2 15.3 80.9% 50.5% UAMES 4291 Prince Creek Formation Hadrosaurinae Edmontosaurus sp. 24.4 31.5 15.8 77.4% 50.1% UAMES 12727 Prince Creek Formation Hadrosaurinae Edmontosaurus sp. 36.6 37.8 12.7 97.0% 33.6% UAMES 21544 Prince Creek Formation Hadrosaurinae Edmontosaurus sp. 20.5 29.2 15.4 70.3% 52.7% Table 1. Selected measurements and ratios of hadrosaurid supraoccipitals. 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,b), unlike the anteriorly positioned ascending process of Edmontosaurus sp. (DMNH 22807, UAMES 4291, UAMES 12727, UAMES 21544; Fig. 2). The ascending process is convergent 54,55 posteroventrally (Fig. 1a,d) as in Hypacrosaurus stebingeri (USNM 11893 ), while those of Edmontosaurus sp. (DMNH 22807, UAMES 21544, UAMES 4291, UAMES 12727; Fig. 2b–e) and Prosaurolophus maximus are nearly parallel or divergent, and those of non-hadrosaurid hadrosauroids (Bactrosaurus johnsoni , Batyrosaurus 57 58 59 rozhdestvenskyi , Eolambia caroljonesa , Eotrachodon orientalis ) are strongly divergent posteroventrally. The dorsal surface of the ascending process is rounded (Fig. 1d) unlike the bi-lobed ascending process of 54,55 Hypacrosaurus stebingeri (USNM 11893 ). The dorsal surface is rugose and lacks the nuchal crest. On either side of the ascending process, a deep post-temporal groove runs anteroposteriorly (Fig. 1a,d) unlike in supraoc- 56–59 cipitals of non-hadrosaurid hadrosauroids which have no distinct post-temporal groove . The grooves are 52,53 strongly divergent anteriorly as in the indeterminate lambeosaurine (CMN 0170 ; Fig. 2n), differing from those of Prosaurolophus maximus (MOR 447-8-8-7-14 ) and Edmontosaurus sp. (DMNH 22807, UAMES 4291, UAMES 12727, UAMES 21544; 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). The squamosal bosses are well-developed unlike in Prosaurolophus maximus (MOR 447-8-8-7-14 ) and Edmontosaurus sp. (DMNH 22807, UAMES 4291, UAMES 12727, UAMES 21544; Fig. 2b–e). The squamosal bosses of DMNH 2014-12-266 are formed solely by the supraoccipital without participation of the exoccipital-opisthotic complex. This morphol- ogy of the squamosal boss differs from those of Hypacrosaurus altispinus (AMNH FARB 5248 ), Hypacrosaurus 54,55 52,53 stebingeri (USNM 11893 ), the indeterminate lambeosaurine (CMN 0170 ; Fig. 2n), and non-hadrosaurid 56 57 58 hadrosauroids (Bactrosaurus johnsoni , Batyrosaurus rozhdestvenskyi , Eolambia caroljonesa ), in which the boss is also formed in part of the exoccipital-opisthotic complex. The anteroposterior length of the ventral sutural surface is short (Fig.  1b), being 26.8% of the mediolateral width along the posteroventral margin. e Th ratio is much smaller than those of the Liscomb Edmontosaurus sp. (DMNH 22807, UAMES 4292, UAMES 21544, UAMES 12727), Edmontosaurus annectens (DMNH EPV 127701), and Prosaurolophus maximus (MOR 447-8-8-7-14 ), but resembles lambeosaurines (Table 1). The sutural surface with the exoccipital-opisthotic complex is bowed ventrally toward the midline (Fig. 1d) as in the largest supraoc- cipital of Edmontosaurus sp. from the Liscomb Bonebed (UAMES 12727), but unlike in the smaller three. The exoccipital groove, located laterodorsal to the ventral sutural surface with the exoccipital-opisthotic complex, faces lateroventrally (Fig. 1b,c,f ). e ex Th occipital groove is mediolaterally narrower than those of Prosaurolophus maximus (MOR 447-8-8-7-14 ) and Edmontosaurus sp. (DMNH 22807, UAMES 4291, UAMES 12727, UAMES 52,53 21544; Fig. 2g–j), but resembles the indeterminate lambeosaurine (CMN 0170 ; Fig. 2t). The anterior surface of the supraoccipital is smooth and slightly concave to form a part of the endocranial wall (Fig. 1e). However, detailed morphology of the endocranial wall is uncertain because of the missing anterior processes. The height of the supraoccipital is 55.6% of its posteroventral width (Fig. 1d,e; Table 1). 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 hadrosau- 35,61,62 roids (degree of the caudal extension of the supraoccipital-exoccipital shelf ). e Th 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 ; however, the presence of well-developed squamosal Scientific Repo R ts | (2019) 9:5384 | https://doi.org/10.1038/s41598-019-41325-8 3 www.nature.com/scientificreports www.nature.com/scientificreports/ Figure 2. Hadrosaurid supraoccipitals. DMNH 2014-12-266 (a,f). Edmontosaurus sp: cast of UAMES 21544 (b,g); cast of UAMES 4291 (c,h); DMNH 22807 (d,i); cast of UAMES 12727 (e,j). Indeterminate lambeosaurines: UALVP 48 (k,q); UALVP 53092 (l,r); UALVP 53106 (m,s); CMN 0170 (n,t); UALVP 55300 (o,u); UALVP 54569 (p,v). 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. 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. DMNH 2014-12-266 shows a posteroventrally convergent ascending process (Fig. 2a), which is seen only in lambeosaurines (Hypacrosaurus stebingeri USNMH 11893; indeterminate lambeosaurines UALVP 48, UALVP 55300, UALVP 54569; Fig. 2k,o,p), but die ff rent from a posteroventrally divergent ascending process in 57–59,63 non-hadrosaurid hadrosauroids and a parallel or posteroventrally divergent ascending process in hadrosau- rines (e.g., Edmontosaurus annectens, DMNH EPV 127701; Prosaurolophus maximus ) (Table 2). Additionally, the gently curved posterodorsal border of the ascending process (Fig. 1c,f ) suggests anterior inclination of the 26,35 posterior surface of the supraoccipital in articulation, which is a synapomorphic character of hadrosaurids . Therefore, the combination of the four characters mentioned above (the short exoccipital articular surface, well-developed squamosal bosses, posteroventrally convergent ascending process, and anteriorly inclined poster- odorsal surface of the ascending process) is unique to Lambeosaurinae (Table 2), suggesting DMNH 2014-12-266 is a supraoccipital of a lambeosaurine hadrosaur. 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 mor - photype (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 ascend - ing 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 Scientific Repo R ts | (2019) 9:5384 | https://doi.org/10.1038/s41598-019-41325-8 4 www.nature.com/scientificreports www.nature.com/scientificreports/ Length of the Posterior exposure exoccipital Post-temporal of the ascending Taxon ID Group Squamosal boss articulation surface Ascending process grooves process Less than half of the width of the DMNH 2014-12- Converge Present, converge — Lambeosaurinae Present posteroventral ? 266 posteroventrally posteroventrally margin of the supraoccipital Much less than half of the width of Amurosaurus AEHM 1/232 Lambeosaurinae Present ? ? ? the posteroventral riabinini margin of the supraoccipital Much less than half of the width of Aralosaurus PIN 2229 Lambeosaurinae Present ? ? ? the posteroventral tuberiferus margin of the supraoccipital Much less than half of the width of Charonosaurus CUST JV 1251-57 Lambeosaurinae Present ? ? ? the posteroventral jiayinensis margin of the supraoccipital Much less than half of the width of Corythosaurus ROM 776 Lambeosaurinae Present ? ? ? the posteroventral casuarius margin of the supraoccipital Much less than AMNH 5248 half of the width of Hypacrosaurus CMN 2247 Lambeosaurinae Present ? ? ? the posteroventral altispinus CMN 8675 margin of the ROM 702 supraoccipital Less than half of Much less than the width of the Present, nearly half of the width of Hypacrosaurus AMNH 5461 Converge Lambeosaurinae Present posteroventral pararell to each the posteroventral stebingeri USNMH 11893 posteroventrally margin of the other margin of the supraoccipital supraoccipital Jaxartosaurus PIN 5009/1 Lambeosaurinae Present ? ? ? ? aralensis Much less than half of the width of Lambeosaurus CMN 1218 Lambeosaurinae Present ? ? ? the posteroventral lambei CMN 2759 margin of the supraoccipital Much less than half of the width of Olorotitan AEHM 2/845 Lambeosaurinae Present ? ? ? the posteroventral arharensi margin of the supraoccipital Much less than half of the width of Velafrons CPC-59 Lambeosaurinae Present ? ? ? the posteroventral coahuilensis margin of the supraoccipital More than half as wide as the Acristavus UMNHVP 16607 Hadrosaurinae Absent ? ? ? posteroventral gaglarsoni margin of the supraoccipital Half or more than More than half DMNH EPV. 127701 the width of the Present, nearly as wide as the Edmontosaurus ROM 53494 Diverge Hadrosaurinae Absent posteroventral pararell to each posteroventral annectens ROM 59786 posteroventrally margin of the other margin of the ROM 64623 supraoccipital supraoccipital More than half as wide as the Edmontosaurus CMN 2289 Hadrosaurinae ? ? ? ? posteroventral regalis margin of the supraoccipital More than half as wide as the Gryposaurus AMNH FARB 5350 Hadrosaurinae ? ? ? ? posteroventral notabilis margin of the supraoccipital More than half as wide as the Maiasaura ROM 44770 Hadrosaurinae ? ? ? ? posteroventral peeblesorum ROM 66182 margin of the supraoccipital Continued Scientific Repo R ts | (2019) 9:5384 | https://doi.org/10.1038/s41598-019-41325-8 5 www.nature.com/scientificreports www.nature.com/scientificreports/ Length of the Posterior exposure exoccipital Post-temporal of the ascending Taxon ID Group Squamosal boss articulation surface Ascending process grooves process Half or more than the width of the Present, nearly Prosaurolophus MOR 447-8-8-7-14 Hadrosaurinae Absent posteroventral Nearly parallel pararell to each ? maximus other margin of the supraoccipital Bactrosaurus Non-hadrosaurid Diverge SBDE 95E5/29 Present ? Absent ? johnsoni hadrosauroid posteroventrally Batyrosaurus Non-hadrosaurid Diverge Absent ? AEHM 4/1 Absent ? rozhdestvenskyi hadrosauroid posteroventrally Less than half of the width of the Eolambia CEUM 14525 Non-hadrosaurid Diverge Absent posteroventral Absent ? caroljonesa CEUM 355626 hadrosauroid posteroventrally margin of the supraoccipital Eotrachodon Non-hadrosaurid Diverge MSC 7949 Absent ? Absent ? orientalis hadrosauroid posteroventrally Levnesovia Non-hadrosaurid USNM 538191 Present ? ? ? ? transoxiana hadrosauroid Table 2. List of hadrosauroid supraoccipital features. Figure 3. Supraoccipitals of Liscomb hadrosaurid DMNH 2014-12-266 (a,d), an indeterminate lambeosaurine CMN 0170 (b,e), and Edmontosaurus annectens DMNH EPV 127701 (c,f) in dorsal (a–c) and posterior (e–f) views. Posterior views of articulated skulls of Hypacrosaurus stebingeri (g) and Edmontosaurus annectens (h). Abbreviations: asp, ascending process; eo, articulation surface for the exoccipital-opisthotic complex; ptg, post- temporal groove; sqb, squamosal boss; Ex, Exoccipital-opisthotic complex, Sq, Squamosal. Scale = 2 cm (a–f), 5 cm (g,h). Dashed line represents the boundary of supraoccipital in (g,h). 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 . Comparisons of Scientific Repo R ts | (2019) 9:5384 | https://doi.org/10.1038/s41598-019-41325-8 6 www.nature.com/scientificreports www.nature.com/scientificreports/ Figure 4. Paleogeographical records records of lambeosaurines during the Late Cretaceous. The red star represents the Liscomb lambeosaurine reported herein. Map is redrawn from Deep Time Maps . The paleocoordinates are obtained from the Paleobiology Database (www.paleobiodb.org). 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. 29,64,65 Previous studies suggested presence of lambeosaurine in the Arctic with no definitive descriptions of 65 66 fossil materials. Russell , cited by Rich and others , noted occurrence of lambeosaurine from the Bylot Island 64 29 of Canada, but details of the record are unknown. Russell and Gangloff mentioned possible lambeosaurine records from the North Slope of the Alaska, but the identification in the former was based on a personal commu- nication (by John R. Horner) and the latter did not provide a specimen number or the basis for the identification. e Th Liscomb lambeosaurine is the first definitive occurrence of this group from the Arctic and confirms that lam - beosaurines inhabited the ancient Arctic terrestrial environment. This greatly expands the paleogeographic distri- bution 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 lam- beosaurines 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, 4,12,13,15,25,35 tyrannosaurids, and troodontids in both regions . 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 and, more impor- tantly, 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 , 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, had- rosaurine dominance is known from lower latitudes marine deposits and regions closer to paleoshorelines of 68 34,40–44,69 North America and eastern Asia , 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). Scientific Repo R ts | (2019) 9:5384 | https://doi.org/10.1038/s41598-019-41325-8 7 www.nature.com/scientificreports www.nature.com/scientificreports/ Figure 5. Schematic drawing of differential habitat preference between hadrosaurines and lambeosaurines. Figure 6. Life reconstruction of lambeosaurine-hadrosaurine co-occurrence based on the Liscomb Bonebed hadrosaurids. Artwork by Masato Hattori. 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 supraoccip- ital. 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 70 71 72 that the supraoccipital does not belong to basal ornithopod , dromaeosaurids , pachycephalosaurines , trood- 73 74 intids , or tyranosaurids . Additionally, the absence of the rostrodorsal process suggest that it does not belong to ceratopsids . On the other hand, DMNH 2014-12-266 resembles the supraoccipitals of hadrosaurids in com- plete exclusion from foramen magnum and lambeosaurines and non-hadrosaurid hadrosauroids in presence 52–54,56,57,59 of well-developed squamosal bosses . Therefore, DMNH 2014-12-266 is identified as a supraoccipital of hadrosauroid. Comparisons with isolated supraoccipitals of hadrosaurines from the Liscomb Bonebed (DMNH 22807 and casts of UAMES 4291, UAMES 12727, UAMES 21544, housed at the Canadian Museum of Nature), 52 54,55 Prosaurolophus maximus MOR 447-8-8-7-14 , Hypacrosaurus stebingeri USNM 11893 , an indeterminate 52,53 56 lambeosaurine CMN 0170 , and non-hadrosaurid hadrosauroids (Bactrosaurus johnsoni , Batyrosaurus 57 58 59 rozhdestvenskyi , Eolambia caroljonesa , Eotrachodon orientalis ) were made for taxonomic identification. Scientific Repo R ts | (2019) 9:5384 | https://doi.org/10.1038/s41598-019-41325-8 8 www.nature.com/scientificreports www.nature.com/scientificreports/ To further investigate similarities and differences with the late Cretaceous lambeosaurines in Canada, DMNH 2014-12-266 is compared with isolated lambeosaurine supraoccipitals from the Campanian Oldman Formation (UALVP 48, UALVP 53092, UALVP 53106) and the Campanian Dinosaur Park Formation (CMN 0170, UALVP 55300, UALVP 54569). Because Xing and others argued that Ugrunaaluk kuukpikensis is a nomen dubium, we conservatively regard the hadrosaurine specimens from the Liscomb Bonebed as Edmontosaurus sp. as they were 5,7,23,29–33,76 in prior works . References 1. Prestrud, P. Adaptation by the Arctic Fox (Alopex lagopus) to the Polar Winter. Arctic 44, 132–138, https://doi.org/10.14430/ arctic1529 (1991). 2. Scholander, P. F., Hock, R., Walters, V. & Irving, L. 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A new basal hadrosauroid dinosaur from the Late Cretaceous of Uzbekistan and the early radiation of duck-billed dinosaurs. Proc Biol Sci 276, 2549–2555, https://doi.org/10.1098/rspb.2009.0229 (2009). Acknowledgements We thank Kevin Seymour, Margaret Currie, and Clive Coy for their kind help during collection visits for comparisons. We are also grateful to Greg Funston, Kristen MacKenzie, and Jessica Johnson for their kind help on photography. The first author is thankful to Masaya Iijima, Junki Yoshida, and Yoshihiro Tanaka for their comments on earlier versions of the manuscript. The fieldworks were financially supported by the National Office of Polar Programs (OPP 0424594 and OPP 0425636) and National Geographic Society (W221-12). The collection visits are supported by Grant-in-Aid for JSPS Research Fellow Grant Number 17J06410. Author Contributions A.R.F. and P.J.M. conducted the field work and collected the material. R.S.T. prepped the specimen. R.T., Y.K. and A.R.F. wrote the main manuscript text. R.T. prepared the figures. Y.K. and A.R.F. supervised the project. All authors reviewed the manuscript. Additional Information Competing Interests: The authors declare no competing interests. Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Cre- ative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. 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The First Definite Lambeosaurine Bone From the Liscomb Bonebed of the Upper Cretaceous Prince Creek Formation, Alaska, United States

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www.nature.com/scientificreports opeN The First Definite Lambeosaurine Bone From the Liscomb Bonebed of the Upper Cretaceous Prince Creek Received: 30 September 2018 Formation, Alaska, United States Accepted: 1 March 2019 Published: xx xx xxxx 1 2 3 2 Ryuji t akasaki , Anthony R. Fiorillo , Yoshitsugu Kobayashi , Ronald S. t ykoski & Paul J. McCarthy 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. Vertebrate animals in the Arctic have experienced physiological, behavioral, and morphological adaptations to 1–3 survive in an extreme environment . Rocks from the North Slope of Alaska are important for the understanding 4,5 of the ecology of fossil vertebrates in the Arctic during the Cretaceous Period . There are abundant fossiliferous exposures of the lower part of the Prince Creek Formation on the North Slope, which range from Campanian to early Maastrichtian in age . e Th Prince Creek Formation is a non-marine succession deposited on a high-latitude, low-gradient alluvial/coastal plain. An integrated reconstruction of pedogenic processes and biota suggests that this ancient Arctic coastal plain was influenced by seasonally fluctuating water table levels and floods, and in distal areas, marine waters. The formation has yielded a diverse dinosaur assemblage that includes ceratopsids, 4,5,8–16 dromaeosaurids, hadrosaurids, basal ornithopods, pachycephalosaurids, troodintids, and tyrannosaurids . e Th Liscomb Bonebed is one of the most prolic fi dinosaur bearing localities within this rock unit. Radiometric dating based on tephra near the bonebed indicates that the Liscomb Bonebed is early Maastrichtian with esti- 17 18 19 mated ages of 71–68 Ma , 69.1 ± 0.3 Ma , and younger than 69.2 ± 0.5 Ma . These dates are concordant with 20,21 palynomorph analyses which suggest early Maastrichtian age . The rocks were deposited at an estimated pale- olatitude of 74.5° ± 7.5° . The Liscomb Bonebed is from the distal area of coastal plain and is represented by lower delta plain facies . Further, the stratigraphic interval containing the Liscomb Bonebed represents a series of 19,23 episodic floods and specifically these episodic flood events created deposition by fine-grained viscous hyper - concentrated flows that transported the remains of scores of juvenile dinosaurs onto floodplains adjacent to dis- tributary channels. The Liscomb Bonebed is characterized by high specimen density (up to 160–220 elements/m ) Department of Natural History and Planetary Sciences, Hokkaido University, Kita 10, Nishi 8, Kita-ku, Sapporo, 2 3 Hokkaido, 060-0810, Japan. Perot Museum of Nature and Science, Dallas, Texas, 75201, United States. Hokkaido University Museum, Kita 10, Nishi 8, Kita-ku, Sapporo, Hokkaido, 060-0810, Japan. University of Alaska, Department of Geosciences, Fairbanks, Alaska, 99775, United States. Correspondence and requests for materials should be addressed to A.R.f . (email: tony.fiorillo@perotmuseum.org ) Scientific Repo R ts | (2019) 9:5384 | https://doi.org/10.1038/s41598-019-41325-8 1 www.nature.com/scientificreports www.nature.com/scientificreports/ Figure 1. Lambeosaurine supraoccipital (DMNH 2014-12-266) from the Liscomb Bonebed. (a) Dorsal view. (b) Ventral view. (c) Left lateral view. (d) Posterior view. (e) Anterior view. (f) Right lateral view. Abbreviations: asp, ascending process; eo, articulation surface for the exoccipital-opisthotic complex; eog, exoccipital groove; ptg, post-temporal groove; sqb, squamosal boss. Scale = 2 cm. 15,24 and has yielded over six thousand bones . It is a monodominant multitaxic bonebed consisting of three thero- 7,10,25 pod taxa (dromaeosaurid, troodontid, and tyrannosaurid) and hadrosaurid skeletal elements which com- prises 98.5% of dinosaur skeletal elements . The Hadrosauridae is a derived clade of Hadrosauroidea and comprise two stem-sister lineages, Lambeosaurinae and Hadrosaurinae . The Liscomb hadrosaurid materials were initially identified as Lambeosaurinae , although osteological features to support the identification were not provided. Comparisons based on isolated cranial elements later demonstrated that the Liscomb hadrosaurs showed close similarity to the hadrosaurine Edmontosaurus saskatchewanensis , which is now considered a junior synonym of Edmontosaurus annectens . Since then, a general consensus formed that the Liscomb hadrosaur bones represent specimens of 5,23,29–34 Edmontosaurus . Recently, it was proposed that the Liscomb hadrosaur bones represent a new distinct hadrosaurine taxon, Ugrunaaluk kuukpikensis . However, subsequent workers argued that the proposed new taxon was invalid in part because it was diagnosed on immature growth stage features preserved in the known specimens . Despite of the taxonomic controversy, these studies have agreed upon the presence of a hadrosaurine hadrosaurid in the Liscomb Bonebed. Here we report the first definitive lambeosaurine hadrosaurid fossil from the Liscomb Bonebed (DMNH 2014–12–266), represented by an isolated cranial material, a supraoccipital. The supraoccipital demonstrates that the Liscomb Bonebed contains both lambeosaurine and hadrosaurine materials. While co-occurrences of hadro- 36–38 saurine and lambeosaurine are widely known in the northern hemisphere (e.g., Careless Creek Quarry and 39 40,41 42,43 Jack’s Birthday Site of Montana, United States; Blagoveschensk locality and Kundur localities of southern Amur region, Russia; and Wulaga locality of northern Heilongjiang Province, China), the Liscomb Bonebed is the first to demonstrate the co-occurrence in the Arctic. Therefore, the new discovery oer ff s an important oppor - tunity to infer possible determinant factors of hadrosaurid taxonomic structure in the Arctic, in comparison with lower latitude regions. Results Systematic paleontology. Dinosauria Owen, 1842 Ornithischia Seeley, 1887 Cerapoda Sereno, 1986 Ornithopoda Marsh, 1881 Iguanodontia Dollo, 1888 Hadrosauridae Cope, 1870 Lambeosaurinae Parks, 1923 Description. The new supraoccipital (DMNH 2014-12-266; Fig.  1) is nearly complete but missing both anterior processes and anterodorsal end of the ascending process. Its maximum width along the posteroven- tral margin is 44.8 mm, which is slightly larger than those of Edmontosaurus sp. specimens from the Liscomb 52,53 Bonebed, nearly equivalent with that of the indeterminate lambeosaurine CMN 0170 , and smaller than that of Prosaurolophus maximus MOR 447-8-8-7-14 (Table 1). The width is also much less than the posteriorly exposed supraoccipital surfaces of adult articulated skulls of Edmontosaurus regalis (100.3 mm, CMN 2278), Gryposaurus notabilis (102.4 mm, CMN 2288), Hypacrosaurus stebingeri (87.1 mm, MOR 553 s; 98.0 mm, MOR 455), and Lambeosaurus lambei (79.5 mm, ROM 1218). Its small size may indicates that the supraoccipital (DMNH 2014- 12-266) belonged to an immature individual. Scientific Repo R ts | (2019) 9:5384 | https://doi.org/10.1038/s41598-019-41325-8 2 www.nature.com/scientificreports www.nature.com/scientificreports/ Length, ventral Width, posteroventral Maximum L/W ratio H/W ID Formation Subfamily Taxa surface (mm) margin (mm) height (mm) (%) ratio (%) DMNH 2014-12-266 Prince Creek Formation Lambeosaurinae unknown 12.0 44.8 24.9 26.8% 55.6% USNM 11893 Two Medicine Formation Lambeosaurinae Hypacrosaurus stebingeri 17.9 52.8 35.3 33.9% 67.0% UALVP 48 Oldman Formation Lambeosaurinae unknown 13.4 38.1 22.2 35.2% 58.3% UALVP 53092 Oldman Formation Lambeosaurinae unknown 25.8 66.3 37.9 38.9% 57.1% UALVP 53106 Oldman Formation Lambeosaurinae unknown 17.5 48.4 — 36.0% — CMN 0170 Dinosaur Park Formation Lambeosaurinae unknown 19.4 46.8 24.1 41.4% 51.5% UALVP 54569 Dinosaur Park Formation Lambeosaurinae unknown 28.4 — 29.1 — — UALVP 55300 Dinosaur Park Formation Lambeosaurinae unknown 17.1 43.2 26.2 39.7% 60.7% DMNH EPV 127701 Lance Formation Hadrosaurinae Edmontosaurus annectens 66.0 48.5 33.6 135.9% 69.2% MOR 447-8-8-7-14 Two Medicine Formation Hadrosaurinae Prosaurolophus maximus 43.0 85.7 34.7 50.1% 40.5% DMNH 22807 Prince Creek Formation Hadrosaurinae Edmontosaurus sp. 24.4 30.2 15.3 80.9% 50.5% UAMES 4291 Prince Creek Formation Hadrosaurinae Edmontosaurus sp. 24.4 31.5 15.8 77.4% 50.1% UAMES 12727 Prince Creek Formation Hadrosaurinae Edmontosaurus sp. 36.6 37.8 12.7 97.0% 33.6% UAMES 21544 Prince Creek Formation Hadrosaurinae Edmontosaurus sp. 20.5 29.2 15.4 70.3% 52.7% Table 1. Selected measurements and ratios of hadrosaurid supraoccipitals. 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,b), unlike the anteriorly positioned ascending process of Edmontosaurus sp. (DMNH 22807, UAMES 4291, UAMES 12727, UAMES 21544; Fig. 2). The ascending process is convergent 54,55 posteroventrally (Fig. 1a,d) as in Hypacrosaurus stebingeri (USNM 11893 ), while those of Edmontosaurus sp. (DMNH 22807, UAMES 21544, UAMES 4291, UAMES 12727; Fig. 2b–e) and Prosaurolophus maximus are nearly parallel or divergent, and those of non-hadrosaurid hadrosauroids (Bactrosaurus johnsoni , Batyrosaurus 57 58 59 rozhdestvenskyi , Eolambia caroljonesa , Eotrachodon orientalis ) are strongly divergent posteroventrally. The dorsal surface of the ascending process is rounded (Fig. 1d) unlike the bi-lobed ascending process of 54,55 Hypacrosaurus stebingeri (USNM 11893 ). The dorsal surface is rugose and lacks the nuchal crest. On either side of the ascending process, a deep post-temporal groove runs anteroposteriorly (Fig. 1a,d) unlike in supraoc- 56–59 cipitals of non-hadrosaurid hadrosauroids which have no distinct post-temporal groove . The grooves are 52,53 strongly divergent anteriorly as in the indeterminate lambeosaurine (CMN 0170 ; Fig. 2n), differing from those of Prosaurolophus maximus (MOR 447-8-8-7-14 ) and Edmontosaurus sp. (DMNH 22807, UAMES 4291, UAMES 12727, UAMES 21544; 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). The squamosal bosses are well-developed unlike in Prosaurolophus maximus (MOR 447-8-8-7-14 ) and Edmontosaurus sp. (DMNH 22807, UAMES 4291, UAMES 12727, UAMES 21544; Fig. 2b–e). The squamosal bosses of DMNH 2014-12-266 are formed solely by the supraoccipital without participation of the exoccipital-opisthotic complex. This morphol- ogy of the squamosal boss differs from those of Hypacrosaurus altispinus (AMNH FARB 5248 ), Hypacrosaurus 54,55 52,53 stebingeri (USNM 11893 ), the indeterminate lambeosaurine (CMN 0170 ; Fig. 2n), and non-hadrosaurid 56 57 58 hadrosauroids (Bactrosaurus johnsoni , Batyrosaurus rozhdestvenskyi , Eolambia caroljonesa ), in which the boss is also formed in part of the exoccipital-opisthotic complex. The anteroposterior length of the ventral sutural surface is short (Fig.  1b), being 26.8% of the mediolateral width along the posteroventral margin. e Th ratio is much smaller than those of the Liscomb Edmontosaurus sp. (DMNH 22807, UAMES 4292, UAMES 21544, UAMES 12727), Edmontosaurus annectens (DMNH EPV 127701), and Prosaurolophus maximus (MOR 447-8-8-7-14 ), but resembles lambeosaurines (Table 1). The sutural surface with the exoccipital-opisthotic complex is bowed ventrally toward the midline (Fig. 1d) as in the largest supraoc- cipital of Edmontosaurus sp. from the Liscomb Bonebed (UAMES 12727), but unlike in the smaller three. The exoccipital groove, located laterodorsal to the ventral sutural surface with the exoccipital-opisthotic complex, faces lateroventrally (Fig. 1b,c,f ). e ex Th occipital groove is mediolaterally narrower than those of Prosaurolophus maximus (MOR 447-8-8-7-14 ) and Edmontosaurus sp. (DMNH 22807, UAMES 4291, UAMES 12727, UAMES 52,53 21544; Fig. 2g–j), but resembles the indeterminate lambeosaurine (CMN 0170 ; Fig. 2t). The anterior surface of the supraoccipital is smooth and slightly concave to form a part of the endocranial wall (Fig. 1e). However, detailed morphology of the endocranial wall is uncertain because of the missing anterior processes. The height of the supraoccipital is 55.6% of its posteroventral width (Fig. 1d,e; Table 1). 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 hadrosau- 35,61,62 roids (degree of the caudal extension of the supraoccipital-exoccipital shelf ). e Th 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 ; however, the presence of well-developed squamosal Scientific Repo R ts | (2019) 9:5384 | https://doi.org/10.1038/s41598-019-41325-8 3 www.nature.com/scientificreports www.nature.com/scientificreports/ Figure 2. Hadrosaurid supraoccipitals. DMNH 2014-12-266 (a,f). Edmontosaurus sp: cast of UAMES 21544 (b,g); cast of UAMES 4291 (c,h); DMNH 22807 (d,i); cast of UAMES 12727 (e,j). Indeterminate lambeosaurines: UALVP 48 (k,q); UALVP 53092 (l,r); UALVP 53106 (m,s); CMN 0170 (n,t); UALVP 55300 (o,u); UALVP 54569 (p,v). 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. 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. DMNH 2014-12-266 shows a posteroventrally convergent ascending process (Fig. 2a), which is seen only in lambeosaurines (Hypacrosaurus stebingeri USNMH 11893; indeterminate lambeosaurines UALVP 48, UALVP 55300, UALVP 54569; Fig. 2k,o,p), but die ff rent from a posteroventrally divergent ascending process in 57–59,63 non-hadrosaurid hadrosauroids and a parallel or posteroventrally divergent ascending process in hadrosau- rines (e.g., Edmontosaurus annectens, DMNH EPV 127701; Prosaurolophus maximus ) (Table 2). Additionally, the gently curved posterodorsal border of the ascending process (Fig. 1c,f ) suggests anterior inclination of the 26,35 posterior surface of the supraoccipital in articulation, which is a synapomorphic character of hadrosaurids . Therefore, the combination of the four characters mentioned above (the short exoccipital articular surface, well-developed squamosal bosses, posteroventrally convergent ascending process, and anteriorly inclined poster- odorsal surface of the ascending process) is unique to Lambeosaurinae (Table 2), suggesting DMNH 2014-12-266 is a supraoccipital of a lambeosaurine hadrosaur. 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 mor - photype (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 ascend - ing 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 Scientific Repo R ts | (2019) 9:5384 | https://doi.org/10.1038/s41598-019-41325-8 4 www.nature.com/scientificreports www.nature.com/scientificreports/ Length of the Posterior exposure exoccipital Post-temporal of the ascending Taxon ID Group Squamosal boss articulation surface Ascending process grooves process Less than half of the width of the DMNH 2014-12- Converge Present, converge — Lambeosaurinae Present posteroventral ? 266 posteroventrally posteroventrally margin of the supraoccipital Much less than half of the width of Amurosaurus AEHM 1/232 Lambeosaurinae Present ? ? ? the posteroventral riabinini margin of the supraoccipital Much less than half of the width of Aralosaurus PIN 2229 Lambeosaurinae Present ? ? ? the posteroventral tuberiferus margin of the supraoccipital Much less than half of the width of Charonosaurus CUST JV 1251-57 Lambeosaurinae Present ? ? ? the posteroventral jiayinensis margin of the supraoccipital Much less than half of the width of Corythosaurus ROM 776 Lambeosaurinae Present ? ? ? the posteroventral casuarius margin of the supraoccipital Much less than AMNH 5248 half of the width of Hypacrosaurus CMN 2247 Lambeosaurinae Present ? ? ? the posteroventral altispinus CMN 8675 margin of the ROM 702 supraoccipital Less than half of Much less than the width of the Present, nearly half of the width of Hypacrosaurus AMNH 5461 Converge Lambeosaurinae Present posteroventral pararell to each the posteroventral stebingeri USNMH 11893 posteroventrally margin of the other margin of the supraoccipital supraoccipital Jaxartosaurus PIN 5009/1 Lambeosaurinae Present ? ? ? ? aralensis Much less than half of the width of Lambeosaurus CMN 1218 Lambeosaurinae Present ? ? ? the posteroventral lambei CMN 2759 margin of the supraoccipital Much less than half of the width of Olorotitan AEHM 2/845 Lambeosaurinae Present ? ? ? the posteroventral arharensi margin of the supraoccipital Much less than half of the width of Velafrons CPC-59 Lambeosaurinae Present ? ? ? the posteroventral coahuilensis margin of the supraoccipital More than half as wide as the Acristavus UMNHVP 16607 Hadrosaurinae Absent ? ? ? posteroventral gaglarsoni margin of the supraoccipital Half or more than More than half DMNH EPV. 127701 the width of the Present, nearly as wide as the Edmontosaurus ROM 53494 Diverge Hadrosaurinae Absent posteroventral pararell to each posteroventral annectens ROM 59786 posteroventrally margin of the other margin of the ROM 64623 supraoccipital supraoccipital More than half as wide as the Edmontosaurus CMN 2289 Hadrosaurinae ? ? ? ? posteroventral regalis margin of the supraoccipital More than half as wide as the Gryposaurus AMNH FARB 5350 Hadrosaurinae ? ? ? ? posteroventral notabilis margin of the supraoccipital More than half as wide as the Maiasaura ROM 44770 Hadrosaurinae ? ? ? ? posteroventral peeblesorum ROM 66182 margin of the supraoccipital Continued Scientific Repo R ts | (2019) 9:5384 | https://doi.org/10.1038/s41598-019-41325-8 5 www.nature.com/scientificreports www.nature.com/scientificreports/ Length of the Posterior exposure exoccipital Post-temporal of the ascending Taxon ID Group Squamosal boss articulation surface Ascending process grooves process Half or more than the width of the Present, nearly Prosaurolophus MOR 447-8-8-7-14 Hadrosaurinae Absent posteroventral Nearly parallel pararell to each ? maximus other margin of the supraoccipital Bactrosaurus Non-hadrosaurid Diverge SBDE 95E5/29 Present ? Absent ? johnsoni hadrosauroid posteroventrally Batyrosaurus Non-hadrosaurid Diverge Absent ? AEHM 4/1 Absent ? rozhdestvenskyi hadrosauroid posteroventrally Less than half of the width of the Eolambia CEUM 14525 Non-hadrosaurid Diverge Absent posteroventral Absent ? caroljonesa CEUM 355626 hadrosauroid posteroventrally margin of the supraoccipital Eotrachodon Non-hadrosaurid Diverge MSC 7949 Absent ? Absent ? orientalis hadrosauroid posteroventrally Levnesovia Non-hadrosaurid USNM 538191 Present ? ? ? ? transoxiana hadrosauroid Table 2. List of hadrosauroid supraoccipital features. Figure 3. Supraoccipitals of Liscomb hadrosaurid DMNH 2014-12-266 (a,d), an indeterminate lambeosaurine CMN 0170 (b,e), and Edmontosaurus annectens DMNH EPV 127701 (c,f) in dorsal (a–c) and posterior (e–f) views. Posterior views of articulated skulls of Hypacrosaurus stebingeri (g) and Edmontosaurus annectens (h). Abbreviations: asp, ascending process; eo, articulation surface for the exoccipital-opisthotic complex; ptg, post- temporal groove; sqb, squamosal boss; Ex, Exoccipital-opisthotic complex, Sq, Squamosal. Scale = 2 cm (a–f), 5 cm (g,h). Dashed line represents the boundary of supraoccipital in (g,h). 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 . Comparisons of Scientific Repo R ts | (2019) 9:5384 | https://doi.org/10.1038/s41598-019-41325-8 6 www.nature.com/scientificreports www.nature.com/scientificreports/ Figure 4. Paleogeographical records records of lambeosaurines during the Late Cretaceous. The red star represents the Liscomb lambeosaurine reported herein. Map is redrawn from Deep Time Maps . The paleocoordinates are obtained from the Paleobiology Database (www.paleobiodb.org). 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. 29,64,65 Previous studies suggested presence of lambeosaurine in the Arctic with no definitive descriptions of 65 66 fossil materials. Russell , cited by Rich and others , noted occurrence of lambeosaurine from the Bylot Island 64 29 of Canada, but details of the record are unknown. Russell and Gangloff mentioned possible lambeosaurine records from the North Slope of the Alaska, but the identification in the former was based on a personal commu- nication (by John R. Horner) and the latter did not provide a specimen number or the basis for the identification. e Th Liscomb lambeosaurine is the first definitive occurrence of this group from the Arctic and confirms that lam - beosaurines inhabited the ancient Arctic terrestrial environment. This greatly expands the paleogeographic distri- bution 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 lam- beosaurines 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, 4,12,13,15,25,35 tyrannosaurids, and troodontids in both regions . 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 and, more impor- tantly, 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 , 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, had- rosaurine dominance is known from lower latitudes marine deposits and regions closer to paleoshorelines of 68 34,40–44,69 North America and eastern Asia , 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). Scientific Repo R ts | (2019) 9:5384 | https://doi.org/10.1038/s41598-019-41325-8 7 www.nature.com/scientificreports www.nature.com/scientificreports/ Figure 5. Schematic drawing of differential habitat preference between hadrosaurines and lambeosaurines. Figure 6. Life reconstruction of lambeosaurine-hadrosaurine co-occurrence based on the Liscomb Bonebed hadrosaurids. Artwork by Masato Hattori. 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 supraoccip- ital. 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 70 71 72 that the supraoccipital does not belong to basal ornithopod , dromaeosaurids , pachycephalosaurines , trood- 73 74 intids , or tyranosaurids . Additionally, the absence of the rostrodorsal process suggest that it does not belong to ceratopsids . On the other hand, DMNH 2014-12-266 resembles the supraoccipitals of hadrosaurids in com- plete exclusion from foramen magnum and lambeosaurines and non-hadrosaurid hadrosauroids in presence 52–54,56,57,59 of well-developed squamosal bosses . Therefore, DMNH 2014-12-266 is identified as a supraoccipital of hadrosauroid. Comparisons with isolated supraoccipitals of hadrosaurines from the Liscomb Bonebed (DMNH 22807 and casts of UAMES 4291, UAMES 12727, UAMES 21544, housed at the Canadian Museum of Nature), 52 54,55 Prosaurolophus maximus MOR 447-8-8-7-14 , Hypacrosaurus stebingeri USNM 11893 , an indeterminate 52,53 56 lambeosaurine CMN 0170 , and non-hadrosaurid hadrosauroids (Bactrosaurus johnsoni , Batyrosaurus 57 58 59 rozhdestvenskyi , Eolambia caroljonesa , Eotrachodon orientalis ) were made for taxonomic identification. Scientific Repo R ts | (2019) 9:5384 | https://doi.org/10.1038/s41598-019-41325-8 8 www.nature.com/scientificreports www.nature.com/scientificreports/ To further investigate similarities and differences with the late Cretaceous lambeosaurines in Canada, DMNH 2014-12-266 is compared with isolated lambeosaurine supraoccipitals from the Campanian Oldman Formation (UALVP 48, UALVP 53092, UALVP 53106) and the Campanian Dinosaur Park Formation (CMN 0170, UALVP 55300, UALVP 54569). Because Xing and others argued that Ugrunaaluk kuukpikensis is a nomen dubium, we conservatively regard the hadrosaurine specimens from the Liscomb Bonebed as Edmontosaurus sp. as they were 5,7,23,29–33,76 in prior works . References 1. Prestrud, P. Adaptation by the Arctic Fox (Alopex lagopus) to the Polar Winter. Arctic 44, 132–138, https://doi.org/10.14430/ arctic1529 (1991). 2. Scholander, P. F., Hock, R., Walters, V. & Irving, L. 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A new basal hadrosauroid dinosaur from the Late Cretaceous of Uzbekistan and the early radiation of duck-billed dinosaurs. Proc Biol Sci 276, 2549–2555, https://doi.org/10.1098/rspb.2009.0229 (2009). Acknowledgements We thank Kevin Seymour, Margaret Currie, and Clive Coy for their kind help during collection visits for comparisons. We are also grateful to Greg Funston, Kristen MacKenzie, and Jessica Johnson for their kind help on photography. The first author is thankful to Masaya Iijima, Junki Yoshida, and Yoshihiro Tanaka for their comments on earlier versions of the manuscript. The fieldworks were financially supported by the National Office of Polar Programs (OPP 0424594 and OPP 0425636) and National Geographic Society (W221-12). The collection visits are supported by Grant-in-Aid for JSPS Research Fellow Grant Number 17J06410. Author Contributions A.R.F. and P.J.M. conducted the field work and collected the material. R.S.T. prepped the specimen. R.T., Y.K. and A.R.F. wrote the main manuscript text. R.T. prepared the figures. Y.K. and A.R.F. supervised the project. All authors reviewed the manuscript. Additional Information Competing Interests: The authors declare no competing interests. Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Cre- ative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not per- mitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. © The Author(s) 2019 Scientific Repo R ts | (2019) 9:5384 | https://doi.org/10.1038/s41598-019-41325-8 11

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