NEW INFORMATION ON THE CRANIUM OF BRACHYLOPHOSAURUS CANADENSIS (DINOSAURIA, HADROSAURIDAE), WITH A REVISION OF ITS PHYLOGENETIC POSITION

Journal of Vertebrate Paleontology 25(1):144 156, March 2005 2005 by the Society of Vertebrate Paleontology NEW INFORMATION ON THE CRANIUM OF BRACHYLOPHOSAURUS CANADENSIS (DINOSAURIA, HADROSAURIDAE), WITH A REVISION OF ITS PHYLOGENETIC POSITION ALBERT PRIETO-MARQUEZ 1 1 Museum of the Rockies, Montana State University, Bozeman, Montana 59717, redshore@hotmail.com ABSTRACT The cranium of the hadrosaurid dinosaur Brachylophosaurus canadensis is redescribed on the basis of abundant and complete material from the Lower Campanian Judith River Formation of Malta, northeastern Montana. The diagnosis of this taxon is emended, and the species Brachylophosaurus goodwini is now considered to be a junior synonym of Brachylophosaurus canadensis. Autapomorphies of Brachylophosaurus are: nasal greatly developed into paddle-like solid crest extending caudodorsally, overhanging dorsal region of skull; nasal possessing anteroposteriorly oriented groove terminating in elongated foramen located medial to prefrontal; prefrontal projecting posteriorly and resting dorsomedially over anterior process of postorbital and, more posteriorly, extending ventromedially under nasal; only anterior sharp tip of lacrimal contacting maxilla; jugal with ventrally projecting semicircular flange; extremely elongated, rod-like anterodorsal process of maxilla projecting medial to narial cavity along most of anteroposterior length of external naris; anteroposteriorly short exoccipital-supraoccipital roof posterior and dorsal to foramen magnum. Most autapomorphies of the junior synonym species Brachylophosaurus goodwini originated from misplacement of a nasal fragment and individual variation of the jugal. The new osteological information supports Brachylophosaurus canadensis as the sister taxon to Maiasaura peeblesorum, and suggests that the two taxa form a robust and basal clade within the Hadrosaurinae. Two new characters are discussed as phylogenetically informative for hadrosaurids: the mediolateral and anteroposterior predentary proportions and the length of the prequadratic process of the squamosal. INTRODUCTION The Late Cretaceous hadrosaurids were among the most derived and specialized herbivorous dinosaurs. Abundant remains of these animals, including complete and partial skeletons, eggs, nests, babies, and even integumentary traces, have been collected for more than one hundred and fifty years in the Americas (Lull and Wright, 1942; Dodson, 1971; Bonaparte et al., 1984), Europe (Weishampel et al., 1993; Casanovas et al., 1999), Asia (Maryañska and Osmolska, 1982; Buffetaut and Tong-Buffetaut, 1993), and the Antarctica (Case, 2000). Brachylophosaurus canadensis was originally erected and briefly described by Sternberg in 1953 on the basis of a complete skull and partial postcranial skeleton found in the Oldman (Judith River) Formation of southern Alberta. Later, Horner (1988) named a second species, B. goodwini, on the basis of a partial skull and skeleton collected from the Judith River Formation of central Montana, and emended Sternberg s diagnosis of B. canadensis. In the mid-1990s, new skeletal remains of the hadrosaurid dinosaur B. canadensis were excavated from Campanian (Upper Cretaceous) strata in the lower Judith River Formation of eastern Montana (Harmon, 1997). These remains include an isolated, nearly complete articulated skeleton as well as a bone bed containing hundreds of disarticulated elements representing individuals from different ontogenetic stages. All the specimens were found in medium-grained, tan sandstones that accumulated in shallow meandering channels under low-flow conditions (LaRock, 2000). This preservational environment left the bones in a pristine state of preservation, and even preserved soft-tissue impressions (Negro and Prieto-Marquez, 2001; Murphy et al., 2002). The completeness of the new material allowed a revision of the taxonomy, phylogeny, and cranial osteology of B. canadensis. In particular, B. canadensis is rediagnosed and the cranium is redescribed, extracting information on intraspecific variation and reassessing its phylogenetic position using a recent character list for the Hadrosauridae (Horner et al., in press). The results add further support to the hypothesis that B. canadensis is a relatively primitive hadrosaurine and the sister taxon of Maiasaura peeblesorum (Weishampel and Horner, 1990; Horner, 1992). In addition, a few new characters that are phylogenetically informative for hadrosaurids are discussed and integrated into this phylogenetic hypothesis. Finally, B. goodwini is considered a junior synonym of B. canadensis. Institutional Abbreviations AMNH, American Museum of Natural History (New York City, New York, USA); FMNH, Field Museum of Natural History (now housed at the Museum of the Rockies, Bozeman, Montana, USA); MOR, Museum of the Rockies (Bozeman, Montana, USA); OTM, Old Trail Museum (Choteau, Montana, USA); UCMP, University of California, Museum of Paleontology (Berkeley, California, USA). Anatomical Abbreviations an, angular; ap, alar process of basisphenoid; ax, axis; bo, basioccipital; bs, basisphenoid; bspr, basipterygoid process; c.n., cranial nerve(s); d, dentary; f, frontal; hy, hyoid; j, jugal; l, lacrimal; ls, laterosphenoid; mx, maxilla; ns, nasal; op, opisthotic; op-ex, opisthotic-exoccipital; os, orbitosphenoid; pa, parietal; pd, predentary; pf, prefrontal; pmx, premaxilla; po, postorbital; pr, prootic; prs, presphenoid; ps, parasphenoid; ptg, pterygoid; q, quadrate; qj, quadratojugal; sa, surangular; spl, splenial; sq, squamosal. SYSTEMATIC PALEONTOLOGY DINOSAURIA Owen, 1842 ORNITHISCHIA Seeley, 1888 ORNITHOPODA Marsh, 1881 HADROSAURIDAE Cope, 1869 BRACHYLOPHOSAURUS Sternberg, 1953 BRACHYLOPHOSAURUS CANADENSIS (Sternberg, 1953) Brachylophosaurus goodwini Horner, 1988 Referred Specimens MOR 794, a complete adult articulated skeleton lacking only the distal part of the tail; MOR 1071, more than 800 subadult and adult specimens from a monospecific bone bed, including disarticulated or partially articulated and/or associated coracoids, scapulae, sternals, ilia, pubes, ischia, cervical, dorsal, sacral and posterior vertebrae, ribs, humeri, radii, ulnae, carpals, metacarpals, phalanges, femora, tibiae, fibulae, tarsals, 144

PRIETO-MARQUEZ CRANIUM OF BRACHYLOPHOSAURUS 145 metatarsals, pedal phalanges, premaxillae, maxillae, a partial nasal, prefrontals, postorbitals, jugals, quadratojugals, quadrates, dentaries, predentary, splenials, surangular, angulars, articulars, pterygoids, ectopterygoids, palatines, frontals, and two articulated skull roofs with preserved braincases, plus a disarticulated partial subadult skull; FMNH 862, a partial skull roof with associated jugals, dentaries, pterygoid, nasals, right surangular, angulars, and left quadrate; UCMP 130139, a partial nasal from the holotype of B. goodwini. Locality The quarry of MOR 794 (MOR locality JR-168) and the bone bed of MOR 1071 (MOR locality JR-224) correspond to two stratigraphically equivalent sites located in Phillips County, 27 km north of Malta, northeastern Montana, and 87 km from the Canadian border (LaRock, 2000). FMNH 862 was found in 1922 by the Elmer S. Riggs expedition, in the Red Deer River area, north of Medicine Hat, Alberta, Canada. The nasal UCMP 130139 is material found by Mark Goodwin in 1981 in the Judith River Formation, UCMP locality no. V83125, Canadian Creek, Hill County, Montana. Horizon MOR 794 and MOR 1071 correspond to the lower Judith River Formation. FMNH 862 was unearthed from strata of the Two Medicine Formation. Both formations are Campanian in age. Emended Diagnosis for the Genus and Species Brachylophosaurus canadensis is rediagnosed on the basis of the following autapomorphies: nasals greatly developed into paddle-like solid crest extending caudodorsally, overhanging dorsal region of skull; nasals possessing anteroposteriorly oriented groove terminating in elongated foramen, located medial to prefrontal; prefrontal projected posteriorly, resting dorsomedially over anterior process of postorbital and, more posteriorly, extending ventromedially, underlying nasal; only anterior sharp tip of lacrimal contacting maxilla; jugal with ventrally projected semicircular flange deeper overall than that of M. peeblesorum but more lightly built than in remaining hadrosaurines; extremely elongated, rod-like anterodorsal process of maxilla projecting medial to narial cavity along most of anteroposterior length of external naris; anteroposteriorly short exoccipital-supraoccipital roof posterior and dorsal to foramen magnum. CRANIAL OSTEOLOGY Mandibular Complex Predentary Brachylophosaurus canadensis has a subrectangular skull, with a relatively deep premaxilla that makes contact ventrally with a wide predentary. As in M. peeblesorum (Horner, 1983:fig. 4A), the predentary of B. canadensis is twice as wide mediolaterally as anteroposteriorly (Fig. 1A, B), whereas in other taxa, such as Prosaurolophus blackfeetensis and Hypacrosaurus stebingeri, the lateral process is as long as the transversal bar. A large keel-shaped symphyseal process divides the posterodorsal region of the predentary into two symmetrical halves (Fig. 1A). Along the anterodorsal triturating surface, there are six small conical nodes at each side of the symphyseal process (Fig. 1A, arrow). A central pair of smaller nodes is located on the parasagittal plane of the bone (Fig. 1A). The anterodorsal edge with its series of processes is dorsally elevated relative to a transverse row of nutrient foramina symmetrically arranged across the parasagittal plane. The anterior face of the anterodorsal border of the predentary is slightly convex dorsoventrally and forms the dorsal half of the anterior side of the bone. The ventral region of the anterior surface of the bone shows a bifurcated, posteroventrally projecting process at the center (Fig. 1B), that underlies the dentary symphysis. This process is also bilobate in M. peeblesorum and the genus Gryposaurus, but in other hadrosaurids such as H. stebingeri this process is a single triangular unit. Posterior to the bilobate process are a pair of deep oval FIGURE 1. Dorsal (A) and ventral (B) views of Brachylophosaurus canadensis predentary (MOR 1071 7-28 98 299). C, Medial view of B. canadensis right dentary. excavations. The lateral branches show a strongly depressed lateral portion adjacent to a convex medial surface. Ventromedially, they possess flat surfaces bounded by a ridge that forms the medial border of these branches. Dentary The diastema accounts for one third of the length of the dentary (Fig. 1C) and its ventral deflection is well developed. The dental battery shows a maximum of 33 tooth positions and between 2 and 5 teeth arranged vertically on each tooth position, depending on its location along the tooth row. The crown has a single keel, faces medially forming an angle of 35 with the long axis of the root, and is longitudinally bisected by a median carina. In occlusal view, as many as three teeth are exposed. The occlusal surface runs obliquely and, as in M. peeblesorum (OTM F138), Kritosaurus notabilis (AMNH 5465) and Edmontosaurus cf. E. annectens (MOR 003) the occlusal surface is concave. In P. blackfeetensis and H. stebingeri the occlusal surface is flat, and the section of each tooth position is obliquely directed, not mediolaterally straight as in B. canadensis.

146 JOURNAL OF VERTEBRATE PALEONTOLOGY, VOL. 25, NO. 1, 2005 Surangular The surangular (Fig. 2A) has a long anterolateral process that ascends dorsally from the anterior region of the bone. Most of the medial border of the surangular is divided by a low, longitudinal ridge that separates the dorsal splenial groove from the articular one. The splenial groove is much wider than the articular groove. From the quadrate joint, the surangular elongates posteriorly into an obliquely compressed and posteriorly projected process that tapers caudally into a sharp edge. Articular The articular (Fig. 2B) is relatively small and saddle shaped. The medial side bears two surfaces separated by a diagonal and posteroventrally directed low ridge. The remaining posterodorsal surface of the medial side of the articular is slightly concave and faces nearly dorsally. The dorsolateral border of the articular thickens along the anterior half of the element into a narrow concavity that receives a small medioventral process of the quadrate. Splenial The splenial (Fig. 2C) is dorsally convex in lateral profile. The medial side is dorsoventrally convex, whereas the lateral side is concave. Anteriorly, the bone is deeper and bifurcates to form a deeper ventral expansion and a shallow expansion dorsally. The triangular groove for the splenial process of the dentary is limited ventrally by a sharp edge in P. blackfeeten- FIGURE 2. Brachylophosaurus canadensis mandibular elements. A, Dorsal view of a left surangular (MOR 1071). B, mediodorsal view of a right articular (MOR 1071 8-13 98 554A). C, lateral view of a right splenial (MOR 1071 8-6 98 483). D, lateral view of a right angular (MOR 1071).

sis that is not seen in B. canadensis. Posteroventrally, the splenial is mediolaterally compressed. In P. blackfeetensis, the splenial is deeper, especially along the central and the posterior regions. The splenial of B. canadensis is more elongated and slender than that in P. blackfeetensis. Angular The angular is rod-like and, posteriorly, it is mediolaterally compressed (Fig. 2D). The angular is relatively smooth laterally, whereas the medial side shows an array of longitudinal grooves and ridges, especially along the posterior segment, which is mediolaterally compressed. Anteriorly, the angular becomes gradually thicker and nearly cylindrical. The angular of B. canadensis is more slender compared with that of P. blackfeetensis, which is mediolaterally thicker, less variable in thickness, and less irregular in morphology. Hyoid Apparatus A pair of hyoid bones lies parallel to the posterior region of the dentary, angular, surangular, and retroarticular process, forming a V-shaped structure along the ventromedial posterior half of the mandible (Fig. 3A). Each hyoid consists of a compressed, rod-like shaft curved posterodorsally. Anteriorly the shaft gradually becomes more mediolaterally compressed and dorsoventrally expanded, showing a triangular outline (Fig. 3B). Each hyoid in B. canadensis is relatively longer and shows a more expanded rostral end than in M. peeblesorum. Facial Complex PRIETO-MARQUEZ CRANIUM OF BRACHYLOPHOSAURUS 147 Premaxilla In B. canadensis, the anterior border of the premaxilla is ventrally deflected, triangular, and rounded (Fig. 4A). FIGURE 4. A, lateral view of the left premaxilla of a subadult Brachylophosaurus canadensis (MOR 1071 7-7 98 84). B, medial view of B. canadensis left quadratojugal (MOR 1071 7-15 98 218A). C, lateral view of a B. canadensis right maxilla (MOR 1071 7-6 98 79). D, lateral view of B. canadensis right jugal (MOR 1071 7-16 98 248G). FIGURE 3. A, detail of the ventral view of the cranium of Brachylophosaurus canadensis, showing the articulated hyoid apparatus (MOR 794). B, lateral view of a right hyoid of B. canadensis (MOR 1071 7-16 98 248K). This condition is also found in M. peeblesorum (OTM F138) and differs from the reflected anterior rim of P. blackfeetensis (MOR 454 7-8 2-9) and Gryposaurus sp (MOR 553S-7 18 91 107). The anterior portion of the premaxilla is pocket-like dorsally and expanded laterally. Posteriorly, the element diverges into the long posterodorsal and the short posteroventral processes. The anterior edge of the narial cavity is mostly formed by the space enclosed by these processes. The posteroventral process is mediolaterally thin, and its laterodorsal surface is strongly concave longitudinally, containing the circumnarial depression. Anterior to the deflection of the premaxilla, the posteroventral process bulges to form a ventral convexity. The anterior edge of the premaxilla is denticulate. Two large foramina are located anteromedially. One foramen is located near the anterior border of the anterior depression. Dorsomedial to this foramen is another, located near of the base of the posterodorsal process. This foramen exits ventrally and perforates the premaxilla. It corresponds to the ventral premaxillary foramen of P. blackfeetensis (Horner, 1992). Maxilla The anteroventral and anterodorsal processes are separated by a crescentic notch (Fig. 4C). The anteroventral process is relatively short and tapers anteroventrally in a very pronounced slope. The anterodorsal process is very long and extends along the anteroposterior length of the narial cavity (Fig.

148 JOURNAL OF VERTEBRATE PALEONTOLOGY, VOL. 25, NO. 1, 2005 1A). The jugalar process has a rather symmetrical triangular outline. The ectopterygoid shelf has a slight posteroventral slope, in contrast to the more horizontal shelf present in other taxa such as Edmontosaurus sp. (AMNH 5879) and Kritosaurus notabilis (AMNH 5472). Anterior and mediodorsal to the short posteromedial pterygoid process, the ridge that receives the ventral groove of the palatine is very narrow. Between 40 and 43 vertical tooth families are present, with 2 teeth on the occlusal plane and at least 3 teeth per family. A single median carina bisects the crown longitudinally without reaching its apical end. Small papillae are present along the edges of the crown. Jugal The lateral outline of the rostral process is triangular and symmetrical, and it tapers anteriorly into a sharp and pointed end that arches anteroventrally (Fig. 4D). The maxillalacrimal joint prevents the jugal from contact with the nasal. The palatine joint on the medial side of the anterior process of the jugal is ellipsoidal and oblique. Heaton (1971) noted that the lacrimal flange of the maxilla participates in the articulation with the anterolateral process of the palatine. In B. canadensis it is unlikely because of the distance separating the posterior edge of the lacrimal flange and the jugal-palatine articulation. At the middle of its length, the dorsal edge of the jugal shows a long and slender postorbital process. Posteroventrally, the jugal expands into an oval boss. The quadratojugal process is dorsoventrally expanded and flared. Quadratojugal The quadratojugal (Fig. 4B) is dorsoventrally deeper and mediolaterally thicker near its posterior border. The element is anteriorly projected into a triangular edge. Two depressions are present on the medial side of the element, flush with the posterior edge. One is located posterodorsally and is relatively narrow. The other depression is deeper and located posteroventrally. Lacrimal The lacrimal (Fig. 5A, B) resembles that of M. peeblesorum (Horner, 1983) in its wedge-shaped, triangular lateral outline bordered by a horizontal ventral border. On its medial side the lacrimal shows a triangular posterodorsal process that indents into the prefrontal. The posterior border of the lacrimal bears a dorsally projected process that borders the posteroventral edge of the prefrontal and inserts into a deep cleft on the posterior side of this element. Whereas in B. canadensis that process arches dorsomedially, in P. blackfeetensis it projects straight dorsally. Another dorsally projecting but shorter posteromedial process forms the medial wall of the lacrimal foramen. The dorsal surface of this process receives the posteroventral process of the prefrontal. The medial lacrimal canal begins anteriorly as a wide depression and exits through the dorsal third of the posterior border of the bone. Prefrontal Anterodorsal to the frontal articulation, the mediodorsal border of the prefrontal is medioventrally tilted and joins the lateral border of the nasal. The lateral edge of the prefrontal extends farther posteriorly over the orbit and overlies the frontal extending parallel to the nasals. Along that posterior segment the prefrontal tapers as seen in dorsal view and extends medioventrally underneath the nasal crest (arrow on Fig. 5D). The dorsal side of the prefrontal contains a deep groove, parallel to the lateral border of the nasal, and ending anteriorly in a large foramen, posterior to the supraorbital one. The supraorbital foramen is located on the anterodorsal surface of the prefrontal, in front of the anterodorsal corner of the orbit. In that area some specimens exhibit more than one foramen. The medial side of the anteroventral lamina of the prefrontal is separated from the ventral surface of the anterodorsal roof of the orbit by a sharp ridge; a triangular groove receives the posterodorsal process of the lacrimal (Fig. 5B). The anterior edge of the prefrontal overlaps a small portion of the posterodorsal end of the posteroventral process of the premaxilla. The anterodorsal rim of the orbit is crenulated and dorsally elevated relative to the dorsal surface of the skull. FIGURE 5. Left lacrimal and prefrontal of a subadult Brachylophosaurus canadensis (MOR1071 8-5 99 447G) in (A) lateral and (B) medial views. C, left postorbital of a subadult B. canadensis (MOR 1071 7-13 99 87-G) in ventromedial view. D, ventral view of FMNH 862, a partial B. canadensis skull roof, showing the prefrontal underlying the nasal crest; the arrow points to the posterior edge of the prefrontal. E, right squamosal of a subadult B. canadensis (MOR 1071 7-13 99 87-H) in anterolateral view. F, fragment of right nasal of B. canadensis (UCMP 130139) in laterodorsal view. Postorbital The anterior, triangular, and rostrally directed process of the postorbital has an indented border as in the prefrontal (Fig. 5C). Most of that anteromedial border joins the frontal through a thick, crenulated suture. That border further projects caudomedially, forming a process that meets the anterodorsal and lateral crenulated border of the parietal, located dorsal and adjacent to the laterosphenoid. The jugal process projects anteroventrally and is slightly offset lateroventrally from the parasagittal plane to meet the jugal. Near the anterodorsal rim of the orbit the supraorbital foramen penetrates the postorbital dorsoventrally. Squamosal The squamosal (Fig. 5E) is excluded from contacting its counterpart by the parasagittal crest of the parietal. The parietal process projects medially from the posterior corner of the element. This process curves posteriorly and then anteriorly, joining the supraoccipital ventrally. The postorbital process is dorsoventrally compressed and thins mediolaterally while extending anteriorly. Its dorsal surface bears a deep groove that receives the squamosal process of the postorbital. The spike-like pre-quadratic process is relatively short in B. canadensis, whereas it is longer and more robust in other taxa, such as P. blackfeetensis, E. cf. E. annectens (MOR 003), and H. stebingeri. The postquadratic process projects lateroventrally and posteriorly from the posterolateral corner of the squamosal. Medially and adjacent to the posterior concavity on the postquadratic process for the exoccipital is a shallow depression.

PRIETO-MARQUEZ CRANIUM OF BRACHYLOPHOSAURUS 149 Nasal The nasal (Figs. 5C, F, 6A-C) extends from the anterodorsal area of the external naris to the posterodorsal region of the skull. Posterodorsally, the nasal forms a paddle-like crest that covers either entirely or partially (depending on the specimen) the supratemporal fenestra (see intraspecific variation for further details). The parasagittal plane of the skull is formed by the articulation of the nasals. The nasal forms a sheet over the rostrum of B. canadensis that is convex laterally throughout the laterodorsal middle region and the anterodorsal portion of the skull. Anteriorly, the nasal consists of a central subtriangular body from which three processes emerge. Two of these project anteroventrally and articulate with the two processes of the premaxilla to collectively enclose the external naris. The third extends posterodorsally over the skull forming the flat crest and contacts the prefrontal and the frontal. The nasal crest overhangs the parietal posterior to the articulation with the frontal. The hook-like anterodorsal process of the nasal is very long and arches anteroventrally to form nearly the entire dorsal rim of the external naris. The anterodorsal process of the nasal overlaps laterally the posterodorsal process of the premaxilla, except for its anteriormost region, over which the nasal tapers anteroventrally into a hooked end. The anteroventral process is very short and reduced to a triangular wedge that forms the posteroventral border of the external naris. Its ventral portion is medially recessed to join the posteroventral process of the premaxilla. The central body of the nasal articulates with the prefrontal posteroventrally. Along this articulation, the lateral convex wall of the nasal changes in orientation and forms the crest. At the anterior portion of the crest the nasal forms a sharp lateral edge over the prefrontal and postorbital. The nasal overlaps dorsally with the mediodorsal border of the prefrontal and fits into an excavation on the ventral side of the roof of the nasal. Medially, the central body of the nasal overlaps a portion of the anterodorsal region of the concave medial face of the lacrimal. The nasal also abuts the dorsal border of the lacrimal flange of the maxilla. The articulation with the frontal occurs ventrally, where the nasals overlie the posterodorsal surface of the skull. In a subadult individual (MOR 1071 8-5 99 447), the nasofrontal joint extends anteroposteriorly over two-thirds the length of the frontals. Mediolaterally, this articulation is also limited to the two medial thirds of the frontal. The posterior end of the nasofrontal articulation is M-shaped in outline across both frontals and is bounded by a sharp rim of bone. Posterior to the frontal joint, in all specimens, the nasal crest is supported ventrally by the expanded posteromedial portion of the prefrontal. The crest is solid and tonguelike, and contains the parasagittal plane of the skull. The joint between the two nasals forms a low ridge along the crest. A foramen is located medial to the prefrontal (Fig. 6B, C). On the ventral surface of the nasal, an anteroposteriorly directed narrow groove emerges anteriorly from the foramen (arrows on Fig. 6C). On the dorsal surface another groove of similar proportions departs posteriorly from the foramen. Anteromedial to the nasal foramina, the ventral surface of the nasal contains a shallow bulge around the nasal joint. Quadrate The anteromedial pterygoid process is very expanded, trapezoidal, and curves slightly medially (Fig. 7A, B). Its medial surface is strongly concave where the posterodorsal and posteroventral quadrate processes of the pterygoid articulate. A small buttress hangs a short distance posteroventrally and laterally from the posterior border of the quadrate head to meet the anterior side of the posteroventral process of the squamosal. Palatal Complex Pterygoid Anteriorly, a vaulted, folded palatine ramus projects anterodorsally (Fig. 7A, B). A shorter process projects ventrally to contact the posterior end of the maxilla and the ectopterygoid laterally. The dorsal quadrate wing is a triangular lamina that projects caudodorsally and laterally. The ventral quadrate ramus is caudoventrally and laterally projected. On the medial side, a strongly buttressed process projects caudomedially from the center of the element. The palatine ramus links with this buttress, which is also linked to the ventral quadrate and ectopterygoid processes by two thin flanges. Longitudinally the palatine ramus is about one third longer than the dorsal quadrate wing. As in M. peeblesorum (Trexler, 1995), the lateral border of the palatine ramus possesses a dorsal expansion in the form of a small flange near its anterodorsal sharp end. Palatine The ventral elongated maxillary segment splits rostrally into the anterolateral and anterodorsomedial processes (Fig. 7C). At its anterior extreme, a sharp ridge divides the ventral side of the palatine into a deep, lateral cleft and a shallow, medial, and rugose surface. A mediolaterally compressed pyramidal, rugose, and sharp elevation of the dorsomedial ridge of the maxilla fits into a corresponding concavity on the ventral groove of the palatine. The anterolateral jugal process of the palatine is compressed and dorsoventrally expanded distally. The anterodorsomedial process of the palatine is a fan-shaped flange of bone that contacts the palatine ramus of the pterygoid. Horner (1992) indicates that in P. blackfeetensis the palatine meets the lacrimal, but this joint is not observed in B. canadensis. Ectopterygoid The ectopterygoid (Fig. 7D) is an L-shaped sheet of bone, elongated anteroposteriorly and compressed dorsoventrally. In B. canadensis, the ectopterygoid is proportionately longer than that in M. peeblesorum but shorter than that in E. annectens. In B. canadensis the rostral long segment thins more gradually than does that in M. peeblesorum. The ectopterygoid is gradually expanded mediolaterally near its posterior border. The posterodorsal corner of the ectopterygoid is dorsoventrally thickened and shows a posteromedially facing process (the triangular, ventrally projecting process of Trexler, 1995). In M. peeblesorum, this triangular process is more elongated, and its posterodorsal edge is not blended into the medial side of the bone. In contrast, in B. canadensis the process has only a ventral apex and an anteroventral sharp edge, being less defined and less triangular. Neurocranial Complex Frontal The nasofrontal joint (Fig. 8A, white arrow) consists of a wide M-shaped area that extends along two thirds of the dorsal surface of the frontal. The frontals contribute to the roof of the posterior half of the skull, including the medial side of the orbital cavity and the olfactory and cerebral cavities. The interfrontal articulation is posterodorsally elevated at the parietal contact. Anteriorly the frontal is dorsoventrally thinner. As in M. peeblesorum, but unlike that of P. blackfeetensis and other hadrosaurines, the frontal forms a small portion of the dorsal rim of the orbit, between the prefrontal and the postorbital (Sternberg, 1953). Anterior to its contribution to the orbit, the dorsal surface of the frontal is ventrally recessed and slightly curved ventrally, showing a deep fossa that is penetrated by the posteromedial triangular process of the prefrontal. Ventrally, a notch bounded by an anterolateral hook-like projection of the frontal receives the posteromedial end of the posteromedial ridge of the prefrontal. Ventrally, the anteromedial half of the cerebral cavity is bounded by the interfrontal articulation, whereas its posterior half is limited by the parietal joint. A short ridge separates the presphenoid from the orbitosphenoid articulation and anteriorly separates the olfactory from the orbital depression. A low ridge separates the orbital from the olfactory depression. Parietal The parasagittal crest is relatively high and extends along the anteroposterior length of the element (Fig. 8A). The crest is taller and thicker at the squamosal articulation. The anterolateral postorbital process is curved. The central anterior process shows a crenulated border and forms a triangular wedge

150 JOURNAL OF VERTEBRATE PALEONTOLOGY, VOL. 25, NO. 1, 2005 FIGURE 6. A, Brachylophosaurus canadensis skull, MOR 794, in left lateral view. B, ventral view of the skull roof MOR 1071 7-7 98 86; the rectangle indicates the area shown in C. C, ventral view of the nasal of MOR 1071 7-7 98 86, showing the location of the groove and foramina (arrows).

PRIETO-MARQUEZ CRANIUM OF BRACHYLOPHOSAURUS 151 FIGURE 7. Brachylophosaurus canadensis right quadrate and pterygoid (MOR 1071) in (A) lateral and (B) posteromedial views. C, B. canadensis right palatine (MOR 1071 7-16 98 248S) in lateral view. D, left B. canadensis ectopterygoid (MOR 1071 8-13 98 559E) in medioventral view. that fits between the posteromedial corners of both frontals and separates the interfrontal suture. On the ventral surface a smooth convexity lies between the cerebral cavity and its posterior canal, where the parietal is wider. The prootic contacts the ventral lateral border of the supraoccipital, posterior to the laterosphenoid, but does not join the parietal. Presphenoid The presphenoid (Fig. 8B, C) consists of a convex wall of bone that is briefly projected anteroventrally. The bone abuts rostrodorsally the ventral surface of the olfactory depression of the frontal. Unlike in P. blackfeetensis (Horner, 1992), the presphenoid does not join the parasphenoid. Orbitosphenoid The orbitosphenoid (Fig. 8B, C) is slightly rounded anteriorly and extends posteriorly encasing the olfactory foramen. The posterior half of the orbitosphenoid wedges posteroventrally under the anteroventral border of the laterosphenoid. The dorsal trochlear foramen is located in the laterosphenoid, posterior to the rounded termination of the orbitosphenoid. Ventrally, the second foramen is more elongated and is contained in the orbitosphenoid. The ventral surface of the orbitosphenoid forms the dorsal roof of the optic foramen. The posterior wedge-like extension of the orbitosphenoid contributes to the anterodorsal inner face of the oculomotor foramen. Laterosphenoid In the laterosphenoid (Fig. 8B, C), the orbitosphenoid process is relatively small and forms a tongue-like expansion anteromedial to the ventral ridge of the postorbital process. The prootic and the postorbital processes form a concave and posterolaterally facing surface, located adjacent and posterior to the caudal limit of the orbital cavity anterior to the crista prootica. The postorbital process is relatively short when compared to other specimens, such as the lambeosaurines AMNH 5248 and 5433. The prootic process is compressed mediolaterally, deep dorsoventrally, and projects posteriorly. The basisphenoid process is subrectangular and forms the anterior boundary of the trigeminal foramen, comprising the trigeminal groove and extending ventrally. The posterior border of the basisphenoid process joins the prootic. This joint forms the anteroventral limit of the trigeminal foramen. Prootic The prootic (Fig. 8C) does not contact the parietal due to the intervening supraoccipital. A large subtriangular process attaches to the opisthotic-exoccipital complex on its medial side. The prootic contributes to the trigeminal foramen dorsally, forms most of its ventral rim, and also its posterior boundary by means of a sharp edge. The anteroventral laterosphenoid process is subrectangular, mediolaterally expanded, and strongly concave laterally. The anterodorsal laterosphenoid process curves dorsomedially and meets the intervening supraoccipital mediodorsally. The facial foramen penetrates ventrally the central body of the prootic. The posterior central border of the prootic contributes to the anterior half of the fenestra ovalis. A small, triangular process protrudes posteriorly from the inner portion of its lateral wall. Opisthotic-Exoccipital The paroccipital process (Fig. 8B, C) is anteroventrally and laterally directed, as in other hadrosaurines, but unlike the lambeosaurines AMNH 5248 and 5433, where the process is posteroventrally and laterally directed. Anterior to the proximal end of the paroccipital process is the joint for the prootic posterodorsal process. The wing-like supraoccipital process is compressed dorsoventrally. At its anterior end, a ridge connects this process with the medial surface of the basioccipital process. Posteriorly, a smooth, triangular depression surrounds the dorsal portion of the foramen magnum. The basioccipital process is subrectangular, compressed, and expanded anteroposteriorly. Anteriorly, the basioccipital process forms the posterior half of the fenestra ovalis. Supraoccipital The supraoccipital fuses with the exoccipitals to form a dorsoventrally thin roof posterodorsal to the foramen magnum. The element forms a greatly excavated and crescentic area on the dorsal surface of this roof. In MOR 1071 7-13 99 87-I, a disarticulated braincase from a subadult individual, the supraoccipital is subrectangular and wedges anteriorly between the parietal above and the prootic below. Basioccipital The basioccipital (Fig. 8C) is anteroposteriorly longer than mediolaterally wide. The basisphenoid-basioccipital joint is oblique and directed anteroventrally. Anterolaterally, the basioccipital fuses with the prootic along a small portion of its ventrolateral border, between the basisphenoid-prootic and the opisthotic-prootic joints. Posteriorly, the basioccipital articulates with the opisthotic ventral to the line of foramina for cranial nerves IX, X, XI, and XII. Posteroventrally, the basioccipital joins the exoccipitals to contribute ventrally to the occipital condyles. Basisphenoid In the basisphenoid (Fig. 8B, C) the posteroventral constriction is relatively narrow mediolaterally. It bounds ventrally the large ellipsoidal foramen that houses the internal carotid artery through the carotid canal, a pathway of the facial nerve. In B. canadensis and M. peeblesorum, the alar processes are relatively large and well developed. The triangular surface located between the pterygoid processes is flattened, in contrast to the depressed one present in other taxa such as Saurolophus osborni. Parasphenoid The parasphenoid (Fig. 8B) is fused to the basisphenoid and probably consist only of the cultriform process. As in M. peeblesorum (Trexler, 1995), the anterior tip of the cultriform process is U-shaped and concave dorsally. Likewise, it

152 JOURNAL OF VERTEBRATE PALEONTOLOGY, VOL. 25, NO. 1, 2005 FIGURE 8. A, dorsal view of the frontal of a subadult Brachylophosaurus canadensis skull (MOR 1071 8-5 99 447). The black arrows point to the frontal depressions; the white arrow is placed on the surface of the nasofrontal joint and points to its posterior boundary. B, anterior and C, lateral views of the braincase of B. canadensis (MOR 1071 7-7 98 86).

is slightly arched longitudinally and posteriorly expanded dorsally. Intraspecific Morphological Variation PRIETO-MARQUEZ CRANIUM OF BRACHYLOPHOSAURUS 153 Specimens MOR 794, MOR 1071, and FMNH 862 show individual and ontogenetic morphological variation. Subadult specimens are approximately 50 60% of the size of the largest specimens (considered adult size). MOR 794 is an articulated skull measuring 830 mm in maximum length and 390 mm in maximum dorsoventral length. MOR 794, FMNH 862, and the two articulated skull roofs, MOR 1071 7-7 98 86 and MOR 1071 7-16 98 248, present the same size. Although only MOR 794 preserves the rostral half of the cranium, all four specimens measure approximately 250 mm in mediolateral width across the posterodorsal edge of the orbits. The following observations are based on the partial articulated subadult skull MOR 1071 8-5 99 447. The preorbital region of the subadult skull is shorter anteroposteriorly. The subadult skull shows relatively larger openings and proportionately larger foramina in the braincase. The subadult orbital cavity and the elements surrounding it are proportionately large. In subadults, the postorbital and prefrontal are near the size of those of the adult specimens. The brain cavity and the mediolateral breath of the laterosphenoids is narrow, but neurocranial foramina are proportionately large. The prefrontal is not extended caudally and medially in subadults, a difference probably associated with a lesser development of the nasal crest. Individual variation led to the recognition of a relatively robust morphotype and a slender one. Each morphotype has the same size range (as noted above) and there is a proportion of 50% for each morphotype of the total sample of articulated crania. The presence of intraspecific robust and slender morphotypes has been recognized in other dinosaur taxa, such as theropods (Carpenter, 1990; Raath, 1990) and ceratopsians (Lehman, 1990). The robust morphotype is exemplified by MOR 794 (complete skeleton), MOR 1071 7-16 98 248-Q (jugal), and FMNH 862 (partial skull roof). In this morphotype, the nasal crest extends to the dorsal border of the squamosal, covering the supratemporal fenestra and slightly widening posteriorly (Fig. 9B). In extending farther caudally and medially underlying the nasal, the prefontal forms a sharp lateral border along the dorsolateral edge of the skull that ends caudal to the orbit. Other morphologies found only in MOR 794 and FMNH 862 are: a relatively more massive and deeper dentary; a deeper jugal with distinctive deeper anterior processes, wider boss, and less dorsoventrally narrowed segment between the anterior and postorbital and quadratojugal processes; and a relatively greater ornamentation of the postorbital. The slender morphotype is exemplified by the two skull roofs, MOR 1071 7-16 98 248 and MOR 1071 7-7 98 86, and cranial material from the bone bed associated with these specimens. In this morphotype, the nasal crest does not reach the squamosal and is mediolaterally narrower. The crest covers little more than half the width of the supratemporal fenestra, and posteriorly it narrows mediolaterally (Fig. 9A). The prefrontal does not extend posterior to the orbit. PHYLOGENETIC ANALYSIS A phylogenetic analysis is intended to reassess the position of B. canadensis within hadrosaurids but is not intended to revise the clade as a whole. I used 43 characters from a recent character list for the Hadrosauridae (Horner et al., in press) and 4 new characters not previously included in any hadrosaurid phylogentic analysis (see discussion below and Appendix 1). Because my analysis focused on the relationships within the Hadrosaurinae, only one of the ten selected taxa was chosen to represent the Lambeosaurinae (H. stebingeri, because their remains were FIGURE 9. A, dorsal view of MOR 1071 7-7 98 86, one of the two articulated Brachylophosaurus canadensis skull roofs collected from the Malta bonebed. B, B. canadensis skull, MOR 794, in dorsal view. available to the author for examination). Iguanodon bernissartensis was chosen as outgroup taxon to the Hadrosauridae sensu Head (1998). Only hadrosaurines with complete skeletal representation were included, and only those personally examined at the Museum of the Rockies, including P. blackfeetensis, M. peeblesorum, species of Edmontosaurus, and Gryposaurus sp. The character list and data matrix are given in Appendices 1 and 2. The 47 characters were equally weighted and analyzed with ACCTRAN transformation. Two most-parsimonious trees of 79 steps resulted from both exhaustive and branch-and-bound searches in PAUP (Swofford, 2000), with a consistency index of 0.76 and a retention index of 0.72 (Fig. 10). The strict-consensus, 50% majority-rule, and bootstrap trees show the same topology as the two trees provided by the branch-and-bound search, except that Telmatosaurus transsylvanicus is the most basal taxon after I. bernissartensis in one cladogram, and Protohadros byrdi is the most basal taxon in the other (Fig. 10). These results add further support to the hypothesis that B. canadensis is the sister taxon to Maiasaura and that the two taxa form a basal clade within the Hadrosaurinae (Weishampel and Horner, 1990; Horner, 1992). The B. canadensis-m. peeblesorum clade is one of the most robust in the hadrosaurid phylogeny and is supported by the following synapomorphies: predentary with anterior mediolateral breath twice anteroposterior length of lateral processes; premaxilla with ventrally deflected anterior corner; symmetrical, pointed, and triangular anterior process of jugal; short squamosal prequadratic process only slightly longer than anteroposterior width of quadrate cotylus; large development of alar process of basisphenoid; and presence of plantar keel on pedal unguals. The next most inclusive clade that includes B. canadensis (a dichotomy composed of the B. canadensis-m. peeblesorum, and the G. sp-p. blackfeetensis-s. osborni clades) is based on the presence of a solid nasal or nasofrontal crest over the snout or braincase and the inclusion of the nasal bone in this crest. In the present analysis, the genus Gryposaurus is not included in the Brachylophosaurus-Maiasaura clade, in contrast to previous

154 JOURNAL OF VERTEBRATE PALEONTOLOGY, VOL. 25, NO. 1, 2005 FIGURE 10. Strict consensus cladogram showing the evolutionary position of Brachylophosaurus canadensis within the Hadrosaurinae; numbers represent only unambiguous synapomorphies, and numbers in parentheses represent character states, corresponding to those listed in Appendix 1. studies (the Kritosaurini of Brett-Surman, 1989; Weishampel and Horner, 1990). Instead, it is considered here the sister taxon to the Prosaurolophus-Saurolophus clade. This new position is potentially unstable because it is based on a single character: the presence of a narrow reflected rim along the whole border of the premaxilla, as observed in RTPM 80 22 1. DISCUSSION AND CONCLUSION In 1988, Horner emended Sternberg s diagnosis of the genus Brachylophosaurus. He characterized the taxon as having a solid, low, sheet-like nasal crest that is directed posteriorly, a nasal depression that does not extend to the crest, a lightly constructed jugal with a ventrally projecting boss, and a cranioposteriorly short supraoccipital-exoccipital roof posterior to the foramen magnum (Horner, 1988, emended diagnosis). This diagnosis has been extended here to accommodate additional autapomorphies, such as the presence of a foramen on the nasal, medial to the prefrontal, and the presence of a prefrontal that extends posteromedially, underlying the nasal crest. In the same paper the species B. goodwini was described, named, and diagnosed on the basis of fragmentary cranial elements from the Judith River Formation of Montana. The diagnosis of B. goodwini consisted of a deep and rounded dorsal depression or pit at or near the junction of the frontal and postorbital, dorsally concave upper process of the nasal, contact of the posterolateral surface of the nasal with the orbital rim, and quadratojugal process of the jugal parallel with postorbital process (Horner, 1988). The depression on the dorsal surface of the frontal near the postorbital joint has also been found other specimens, such as for example MOR 1071 7-13 99 87-I (Fig. 8A, black arrows) and MOR 1071 6-30 98 4. These depressions are elongated rather than rounded, but individual and/or ontogenetic variation might well account for that difference. This trait has not been considered here an autapomorphy of B. canadensis because it is also present in other hadrosaurids, such as in a lambeosaurine braincase (AMNH 5248). The nasal characters result from the reconstruction of UCMP 130139 (Fig. 5F), a nasal fragment in a very poor condition of preservation. UCMP 130139 was interpreted as having a concave relief, in contrast to the arched relief of the holotype and the other specimens of B. canadensis. However, the UCMP nasal was incorrectly oriented, as evidenced by comparisons with the well-preserved specimens MOR 794 and MOR 1071. What was described as the dorsal edge of UCMP 130139 is actually the ventral border. Therefore, UCMP 130139 corresponds to the rostral preorbital facial sheet of the nasal, drawing the convex dorsal outline seen in all B. canadensis skulls. The parallelism between the quadratojugal and postorbital processes of the jugal is a case of individual variation. MOR 794 shows jugals with postorbital processes only slightly divergent. The bone-bed specimens show variation in the divergence between the postorbital and quadratojugal processes, coupled with a remarkable variation in the size and shape of the quadratojugal process. Therefore, B. goodwini is considered invalid and a junior synonym of B. canadensis. Two of the new characters that are proposed in the present study are the length of the pre-quadratic process of the squamosal and the relative proportions of the anteroposterior and mediolateral dimensions of the predentary. I hypothesize that the basal condition of the hadrosaurid squamosal, exemplified by M. peeblesorum and B. canadensis, is characterized by a prequadratic process that is only slightly longer than the width of the quadrate cotylus. In the remaining hadrosaurids, the prequadratic process is much longer than the quadrate cotylus, as in P. blackfeetensis and E. annectens. The ratio of the mediolateral breath of the predentary to the length of the lateral bars sets M. peeblesorum and B. canadensis apart from the remaining hadrosaurids. The predentary of these two hadrosaurids is twice as broad mediolaterally as it is long anteroposteriorly, a condition here considered derived, at least among the examined taxa. Primitively, the predentary is as wide as it is long, as in I. bernissartensis and P. byrdi. The predentary becomes wider than longer in hadrosaurines such as P. blackfeetensis and the genus Gryposaurus, and also in lambeosaurines, such as H. stebingeri. This trend is further expressed in M. peeblesorum and B. canadensis. AKNOWLEDGMENTS I am grateful to my mentor at Montana State University, John R. Horner, for opening for me the door to dinosaur research. I am very grateful to Mr. Terry and Mrs. Mary Kohler for funding this project. Thanks also go to graduate students Jill Holiday and Jeff LaRock, and to Professors James G. Schmitt, David J. Varricchio, David B. Weishampel, Carlos Bonet, and especially Gregory Erickson and Anne Thistle, whose reviews greatly improved this manuscript. Thanks go to Catherine A. Forster, David B. Weishampel, and John R. Horner for allowing me the use of their character list for the Hadrosauridae. LITERATURE CITED Bonaparte, J. F., M. R. Franchi, J. E. Powell, and E. G. Sepulveda. 1984. La formacion Los Alamitos (Campanio-Maastrichtiano) del sudeste de Rio Negro, con descripcion de Kritosaurus australis n. sp. (Hadrosauridae). Significado paleogeografico de los vertebrados. Asociacion Geologica Argentina, Revista 34:284 299. Brett-Surman, M. K. 1989. A revision of the Hadrosauridae (Reptilia: Ornithischia) and their evolution during the Campanian and Maastrichtian. Unpublished Ph.D. dissertation, George Washington University, Washington D.C., 272 pp. Buffetaut, E., and H. Tong-Buffetaut. 1993. Tsintaosaurus spinorhinus Young and Tanius sinensis Wiman: a preliminary comparative study of two hadrosaurs (Dinosauria) from the Upper Cretaceous of China. Comptes Rendus de l Academie de Sciences II 317: 1255 1261. Carpenter, K. 1990. Variation in Tyrannosaurus rex; pp. 141 145 in K. Carpenter and P. J. Currie (eds.), Dinosaur Systematics: Approaches and Perspectives. Cambridge University Press, New York.