peerj_json_files/PeerJ_Json_133.json

{
    "v1_col_introduction": "introduction  : Ontogenetic changes in the vertebrate skull have numerous functional, ecological, and behavioral consequences (e.g., Erickson et al., 2003; Herrel and Gibb, 2006; Herrel and O\u2019Reilly, 2006; Cole, 2010). Variation in the timing and degree of development of these changes relative to the ancestral condition (heterochrony; e.g., Gould, 1977; Alberch et al., 1979; Klingenberg, 1998; Smith, 2001) is responsible, in part, for the diversity seen even among closely related species. The ontogeny of the skull in ornithischian dinosaurs has received particular attention, due to their elaborate horns, crests, casques and domes in a number of species, variously interpreted to function in visual display, sound production, and intraspecific combat (see Hone et al., 2012 for a recent summary). These cranial modifications demonstrate considerable variation in their morphology as well as heterochrony in their appearance and modification. For instance, the dome-headed pachycephalosaurs show early development of peripheral spikes and knobs and late development of an enlarged central dome (Horner and Goodwin, 2009; Schott et al., 2011; Schott and Evans, 2012), whereas the horned dinosaurs (ceratopsians) have early and continuous development of horns and frills with a final burst of extreme modification to the horns and marginal bones of the frill late in ontogeny (Dodson, 1976; Sampson et al., 1997; Horner and Goodwin, 2006; Currie et al., 2008). These developmental patterns have been leveraged to better inform speculation on cranial function in each of these groups. Among the hadrosaurids, or duck-billed dinosaurs, lambeosaurines are remarkable for their heavily modified nasal passages within a bony crest. Various functional hypotheses have been proposed for this anatomical complex, including air storage during underwater feeding, enhanced olfaction, housing for a salt gland, vocal resonance chambers, and visual display for mate attraction and/or species recognition (reviewed in Weishampel, 1981a). Currently, vocalization and visual display together are the most broadly accepted hypotheses (Evans, 2006), based in part on ontogenetic patterns for the crests. These structures are not well-manifested externally until the skull reaches approximately 50 percent of maximum adult size, and then apparently grew continuously and with strong positive allometry relative to the rest of the skull (Dodson, 1976; Evans, 2010). These patterns of cranial ontogeny are best documented in Lambeosaurini, the clade of \u201chelmet-crested\u201d lambeosaurines that includes taxa such as Corythosaurus, Lambeosaurus, and Hypacrosaurus (Dodson, 1975; Horner and Currie, 1994; Evans et al., 2005, 2009, 2009; Evans, 2010; Bailleul et al., 2012). Data from a number of wellpreserved specimens representing individuals of various sizes and ontogenetic stages allow detailed comparisons of growth and anatomy in closely related species. Importantly, results show that some diagnostic anatomical features arise early in development (e.g., the lack of a premaxilla-nasal fontanelle in Hypacrosaurus altispinus), whereas others (e.g., the distinct hatchet-shaped crest of Lambeosaurus lambei) arise later (Evans, 2010). In any case, the final adult profile is not completed until late in ontogeny, when the animals reach nearly full adult skull size. Although these data have been critical in defining models of lambeosaurine ontogeny, the narrow taxonomic sampling limits application of these models across the clade. In gross view, the cranial crests of lambeosaurins are fairly uniform, dominated by a hemicircular profile sometimes augmented with a caudally projecting spike. This contrasts with the condition in Parasaurolophini, the other major clade of lambeosaurines that includes Parasaurolophus and Charonosaurus. Parasaurolophins are notable for their greatly elongated, tubular crests that project caudally from the skull. The differences between adult parasaurolophins and lambeosaurins almost certainly reflect different ontogenetic trajectories, but the ontogeny of the skull in general and the crest in particular is poorly known in parasaurolophins. Sullivan and Bennett (2000) referred an incomplete and disarticulated skull from New Mexico to Parasaurolophus, but this specimen (approximately one-third the size of an adult) did not include any portion of the skull roof except for a possible postorbital. Evans et al. 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62\nPeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013)\nR ev ie w in g M an\nus cr ip t\n(2007) referred a braincase from Alberta to Parasaurolophus, from an individual approximately half of adult size. Although the crest itself was not preserved, the frontal platform that supported the crest was well-developed (in contrast with the poorly developed platform of lambeosaurins at all ontogenetic stages), implying that the tubular crest was already at least partially developed in that individual. This limited evidence suggests fundamental differences between the cranial development of parasaurolophins and lambeosaurins. Heterochrony in hadrosaurid dinosaurs has received limited attention to date, perhaps in part due to the absence of multiple comprehensive growth series for this clade. One of the first treatments (Weishampel and Horner, 1996) focused primarily on the interplay between body size and age, positing a reduction in skeletal maturity at hatching. Along with the retention of small teeth into adulthood (Weishampel et al., 1993), this would suggest paedomorphosis (prolonged retention of juvenile characters through development relative to the ancestral condition [Alberch et al., 1979]) as a factor in development of these structures. Peramorphosis\u2014acceleration and/or exaggeration of growth in certain features relative to the ancestral condition (Alberch et al., 1979) \u2014was implicated in the development of cranial ornamentation and the oral margins in many hadrosaurids (Long and McNamara, 1997). Additional work on the postcranial skeleton showed heterochrony in some aspects of its ontogeny, such as peramorphosis of the supraacetabular process in the ilium of Hypacrosaurus relative to other hadrosaurids (Guenther, 2009, within the conceptual framework of sequence heterochrony). Overall, heterochrony in the evolution of lambeosaurine cranial ornamentation has received little detailed evaluation. During the 2009 joint field season for The Webb Schools and the Raymond M. Alf Museum of Paleontology (RAM, Claremont, California, USA), high school student Kevin Terris discovered the articulated skeleton and skull of a small hadrosaurid dinosaur (total body length ~2.5 m). The specimen originated in the late Campanian (~75.5 million years old) Kaiparowits Formation, exposed within Grand Staircase-Escalante National Monument in southern Utah (Fig. 1; Roberts et al., 2005; Roberts, 2007). This fossil (RAM 14000) is here referred to Parasaurolophus, representing the ontogenetically youngest and most complete specimen ever recovered for the genus. The nearly complete skull, articulated postcranial skeleton, and associated soft-tissue in RAM 14000 (Figs. 2\u20134) provide important new data on anatomy and ontogeny in Parasaurolophus and hadrosaurids in general. Here, we present a comprehensive description of RAM 14000, placing it within the broader context of ontogeny and heterochrony in lambeosaurines and other dinosaurs. Critically, the specimen provides the best record to date of an early ontogenetic stage in a parasaurolophin, clearly elucidating previously suspected differences between the ontogeny in this clade and in lambeosaurins. Furthermore, the specimen provides a starting point for a broader discussion of heterochrony and \u201codd\u201d cranial structures in dinosaurs.",
    "v2_Abstract": "The tube-crested hadrosaurid dinosaur Parasaurolophus is remarkable for its unusual cranial ornamentation, but little is known about its growth and development, particularly relative to well-documented ontogenetic series for corythosaurin hadrosaurs (such as Corythosaurus, Lambeosaurus, and Hypacrosaurus). The skull and skeleton of a juvenile Parasaurolophus from the late Campanian-aged (~75.5 Ma) Kaiparowits Formation of southern Utah, USA, represents the smallest and most complete specimen yet described for this taxon. The individual was approximately 2.5 meters in body length (~25% maximum adult body length) at death, with a skull measuring 246 mm long and a femur 329 mm long. A histological section of the tibia shows well-vascularized, woven and parallel-fibered primary cortical bone typical of juvenile ornithopods. The histological section revealed no lines of arrested growth or annuli, suggesting the animal may have still been in its first year at the time of death. Impressions of the upper rhamphotheca are preserved in association with the skull, showing that the soft tissue component for the beak extended for some distance beyond the limits of the oral margin of the premaxilla. In marked contrast with the lengthy tube-like crest in adult Parasaurolophus, the crest of the juvenile specimen is low and hemicircular in profile, with an open premaxilla-nasal fontanelle. Unlike juvenile corythosaurins, the nasal passages occupy nearly the entirety of the crest in juvenile Parasaurolophus. Furthermore, Parasaurolophus initiated development of the crest at less than 25% maximum skull size, contrasting with 50% of maximum skull size in hadrosaurs such as Corythosaurus. This early development may correspond with the larger and more derived form of the crest in Parasaurolophus, as well as the close relationship between the crest and the respiratory system. In general, ornithischian dinosaurs formed bony cranial ornamentation at a relatively younger age and smaller size than seen in extant birds. This may reflect, at least in part, that ornithischians probably reached sexual maturity prior to somatic maturity, whereas birds become reproductively mature after reaching adult size.",
    "v2_col_introduction": "introduction  : Ontogenetic changes in the vertebrate skull have numerous functional, ecological, and behavioral consequences (e.g., Erickson et al., 2003; Herrel and Gibb, 2006; Herrel and O\u2019Reilly, 2006; Cole, 2010). The ontogeny of the skull in ornithischian dinosaurs has received particularly attention, due to elaborate horns, crests, casques and domes in a number of species, variously interpreted to function in visual display, sound production, and intraspecific combat (see Hone et al., 2012 for a recent summary). These cranial modifications demonstrate considerable variation in their morphology as well as in the developmental timing of their appearance and modification (i.e., heterochrony). For instance, the dome-headed pachycephalosaurs show early development of peripheral spikes and knobs and late development of an enlarged central dome (Horner and Goodwin, 2009; Schott et al., 2011; Schott and Evans, 2012), whereas the horned dinosaurs (ceratopsians) have early and continuous development of horns and frills with a final burst of extreme modification to the horns and marginal bones of the frill late in ontogeny (Dodson, 1976; Sampson et al., 1997; Horner and Goodwin, 2006; Currie et al., 2008). These developmental patterns have been leveraged to better inform speculation on cranial function in each of these groups. Among the hadrosaurids, or duck-billed dinosaurs, lambeosaurines are remarkable for their heavily modified nasal passages within a bony crest. Various functional hypotheses have been proposed for this anatomical complex, including air storage during underwater feeding, enhanced olfaction, housing for a salt gland, resonance chambers during vocalization, and visual display for mate attraction and/or species recognition (reviewed in Weishampel, 1981a). Currently, vocalization and visual display together are the most broadly-accepted hypotheses (Evans, 2006), based in part on ontogenetic patterns for the crests. These structures are not well-manifested externally until the skull reaches approximately 50 percent of maximum adult size, and then apparently grew continuously and with strong positive allometry relative to the rest of the skull (Dodson, 1976; Evans, 2010). These patterns of cranial ontogeny are best documented in corythosaurins, the clade of \u201chelmet-crested\u201d lambeosaurines that includes taxa such as Corythosaurus, Lambeosaurus, and Hypacrosaurus (Dodson, 1975; Horner and Currie, 1994; Evans et al., 2005, 2009, 2009; Evans, 2010; Bailleul et al., 2012). Data from a number of well-preserved specimens representing individuals of various sizes and ontogenetic stages have allowed detailed comparisons of growth and anatomy in closely related species. Importantly, results show that some diagnostic anatomical features arise early in development (e.g., the lack of a premaxilla-nasal fontanelle in Hypacrosaurus altispinus), whereas others (e.g., the distinct hatchet-shaped crest of Lambeosaurus lambei) arise later (Evans, 2010). In any case, the final adult profile is not manifested until late in ontogeny, when the animals reach nearly full adult skull size. Although these data have been critical in defining models of lambeosaurine ontogeny, the narrow taxonomic sampling limits application of these models across the clade. In gross view, the cranial crests of corythosaurins are fairly uniform, dominated by a hemicircular profile sometimes augmented with a caudally-projecting spike. This contrasts with the condition in Parasaurolophini, the other major clade of lambeosaurines that includes Parasaurolophus and Charonosaurus. Parasaurolophins are notable for their greatly elongated, tubular crests that project caudally from the skull. The differences between adult parasaurolophins and corythosaurins almost certainly were reflected in differing ontogenetic trajectories, but the ontogeny of the skull in general and the crest in particular is poorly known in 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55\nPeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013)\nR ev ie w in g M an\nus cr ip t\nparasaurolophins. Sullivan and Bennett (2000) referred an incomplete and disarticulated skull from New Mexico to Parasaurolophus, but this specimen (approximately one-third the size of an adult) did not include any portion of the skull roof except for a possible postorbital. Evans et al. (2007) referred a braincase from Alberta to Parasaurolophus, from an individual approximately half of adult size. Although the crest itself was not preserved, the frontal platform that supported the crest was well-developed (in contrast with the poorly-developed platform of corythosaurins at all ontogenetic stages), implying that the tubular crest was already at least partially developed. This limited evidence suggests fundamental differences between the cranial development of parasaurolophins and corythosaurins. During the 2009 joint field season for The Webb Schools and the Raymond M. Alf Museum of Paleontology (RAM, Claremont, California, USA), high school student Kevin Terris discovered the articulated skeleton and skull of a small hadrosaurid dinosaur (total body length ~2.5 m). The specimen originated in the late Campanian (~75.5 million years old) Kaiparowits Formation, exposed within Grand Staircase-Escalante National Monument in southern Utah (Fig. 1; Roberts et al., 2005; Roberts, 2007). This fossil (RAM 14000) is here referred to Parasaurolophus, representing the ontogenetically youngest and most complete specimen ever recovered for the genus. The nearly complete skull, articulated postcranial skeleton, and associated soft-tissue in RAM 14000 (Figs. 2\u20134) provide important new data on anatomy and ontogeny in Parasaurolophus and hadrosaurids in general. Here, we present a comprehensive description of RAM 14000, placing it within the broader context of ontogeny and heterochrony in lambeosaurines and other dinosaurs. Critically, the specimen provides the best record to date of an early ontogenetic stage in a parasaurolophin, clearly elucidating previously suspected differences between the ontogeny in this clade and in corythosaurins. Furthermore, the specimen provides a starting point for a broader discussion of heterochrony and \u201codd\u201d cranial structures in dinosaurs.",
    "v1_text": "results systematic paleontology : Dinosauria Owen, 1842 Ornithischia Seeley, 1888 Hadrosauridae Cope, 1869 Lambeosaurinae Parks, 1923 Parasaurolophus Parks, 1922 Parasaurolophus sp. acknowledgements : We acknowledge Kevin Terris for his discovery of RAM 14000, and thank Michael Stokes for his skillful excavation and preparation of the specimen. Don Lofgren and numerous students, faculty, and volunteers from the Alf Museum and The Webb Schools provided field assistance. We also thank Johnson Lightfoote and staff at Pomona Valley Hospital Medical Center for CT scanning RAM 14000. We thank the UCMP for access to histological sectioning equipment and Kevin Padian for imaging equipment. Kirstin Brink, Nic Campione, David Evans, Terry Gates, Mark Loewen, Scott Sampson, Jack Horner, and many others offered insightful discussion about lambeosaurine ontogeny. Larry Witmer provided comparative models of lambeosaurine crania, and Scott Hartman and Ville Sinkonnen provided reconstructions of RAM 14000. Casey Holliday and Henry Tsai compiled the 3D PDF files illustrating the nasal passages and endocranial cavity, and Joseph Peterson compiled the files for the postcrania. William Abersek and Benjamin Kwon assisted with laser scanning of RAM 14000. We thank Ashley Fragomeni and Peter Kloess for curatorial assistance. RAM 14000 was collected under United States Department of the Interior Bureau of Land Management Paleontological Resources Use Permit (surface collection permit UT06-001S and excavation permit UT10-006E-Gs), with permitting assistance from Scott Foss and Alan Titus. Brandon Strilisky (RTMP) provided access to specimens in his care. Comments from John Hutchinson, David Weishampel, and two anonymous reviewers greatly improved the manuscript. 1630 1631 1632 1633 1634 1635 1636 1637 1638 1639 1640 1641 1642 1643 1644 1645 1646 1647 1648 1649 1650 1651 1652 1653 1654 1655 1656 1657 1658 1659 1660 1661 1662 1663 1664 1665 1666 1667 1668 1669 1670 1671 1672 1673 1674 1675 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t methods : discussion : RAM 14000 is Parasaurolophus Although the visually striking and taxonomically diagnostic crests of lambeosaurine hadrosaurids do not reach their ultimate morphology until adulthood, many genus- and specieslevel autapomorphies appear earlier in ontogeny (Evans et al., 2005, 2007; Evans, 2010; Brink et al., 2011). Based on a combination of anatomical features in RAM 14000, as well as stratigraphic and geographic evidence, we identify the specimen as a juvenile Parasaurolophus. However, we do not assign it to a particular species. Although both hadrosaurids and basal neornithischians (\u201chypsilophodontids\u201d) occur in the Kaiparowits Formation (Gates et al., 2013), RAM 14000 is clearly identifiable as a hadrosaurid. 1190 1191 1192 1193 1194 1195 1196 1197 1198 1199 1200 1201 1202 1203 1204 1205 1206 1207 1208 1209 1210 1211 1212 1213 1214 1215 1216 1217 1218 1219 1220 1221 1222 1223 1224 1225 1226 1227 1228 1229 1230 1231 1232 1233 1234 1235 1236 1237 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t It possesses numerous synapomorphies not found in \u201chypsilophodontids,\u201d including three or more replacement teeth in each tooth family as well as absence of a surangular foramen or free palpebral (Horner et al., 2004). Furthermore, a series of synapomorphies clearly place RAM 14000 within Lambeosaurinae. These include a domed frontal in subadults, development of an enlarged crest formed from the premaxillae and nasals as well as a nasal vestibule completely enclosed by the premaxillae, a triangular rostrolateral corner of the premaxilla, and many others (Horner et al., 2004; Prieto-M\u00e1rquez, 2010). Based on CT scan data, we reconstruct RAM 14000 as lacking an S-loop in the proximal portion of the nasal passages (Fig. 9), an ontogeny-independent synapomorphy that occurs in most post-embryonic lambeosaurins (Evans and Reisz, 2007; Evans et al., 2009). Additionally, there is no solid, fin-like caudal extension of the crest, found in all juvenile and adult lambeosaurins for which CT scan data are available (Evans et al., 2009). Relative to Velafrons coahuilensis, RAM 14000 lacks the unique \u201ckinked\u201d squamosal morphology of that taxon (Gates et al., 2007). In all juvenile and adult lambeosaurins for which the feature is known, the caudolateral process of the premaxilla is moderately to extremely angled at its contact with the maxilla, rather than straight as in RAM 14000 (Fig. 7A; a feature otherwise found in Parasaurolophus). Finally, RAM 14000 shows accelerated development of some features relative to known lambeosaurins (outlined below; Fig. 28). There are thus no firm characters to identify RAM 14000 as a lambeosaurin. Previous authors have identified a suite of characteristics that unite parasaurolophins (Charonosaurus and Parasaurolophus), which can also be potentially evaluated in RAM 14000 (characters that are not preserved in the specimen are not considered here). These include: 1) a massive frontal platform extending caudally at least to the level of the supratemporal fenestrae; 2) thickening of the dorsal surface of the postorbital in adults to form a promontorium; and 3) an expanded distal head of the fibula (Godefroit et al., 2004; Evans and Reisz, 2007; Evans et al., 2007; Prieto-M\u00e1rquez, 2010). Characters 1 and 2 are intimately linked with the development of the massive crest (at least in Parasaurolophus, where crest morphology is known, and presumably also in Charonosaurus). RAM 14000 lacks these features, but their absence is not surprising in light of the crest\u2019s incipient development in this specimen. The distal end of the fibula is slightly expanded in RAM 14000, but not to the degree seen in P. cyrtocristatus or C. jiayinensis (Ostrom, 1963; Godefroit et al., 2001). However, this feature also occurs to a lesser degree in Corythosaurus intermedius and Hypacrosaurus stebingeri (Prieto-M\u00e1rquez, 2010), and thus cannot be considered taxonomically significant in RAM 14000. Other important characters, such as the number of cervical vertebrae, relative length of metacarpal V, and the participation of the parietal in the occiput, cannot be determined in RAM 14000. Based on a referred juvenile braincase (CMN 8502), Evans and colleagues (2007) identified several features of the skull roof that they hypothesized to be relatively consistent through ontogeny in Parasaurolophus, at least for the sample known at that time. These included: 1) frontal with a thick and steeply angled nasal articular surface; 2) frontals comparatively short; 3) frontals with a poorly developed median cleft at rostral-most extent; 4) rostral processes of frontal meet at broad and obtuse angle in dorsal view; and 5) olfactary depression offset ventrally from roof of cerebral fossa. Characters 1, 2, 4, and 5 are demonstrably absent in RAM 14000, and character 3 cannot be evaluated. Arguably, all of the characters (particularly character 1) are related to the development of the enlarged bony crest supported by the frontals. We thus attribute their absence in RAM 14000, an extremely young individual in which the crest is only incipient, to ontogenetic effects. Prieto-M\u00e1rquez (2010) also identified several unambiguous synapomorphies from his dataset that unite Parasaurolophus species. Unfortunately, these are either not preserved in RAM 1238 1239 1240 1241 1242 1243 1244 1245 1246 1247 1248 1249 1250 1251 1252 1253 1254 1255 1256 1257 1258 1259 1260 1261 1262 1263 1264 1265 1266 1267 1268 1269 1270 1271 1272 1273 1274 1275 1276 1277 1278 1279 1280 1281 1282 1283 1284 1285 1286 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t 14000 (number of teeth per alveolus at mid-dentary; morphology of deltoid ridge of scapula; proportions of ulna) or are widely distributed across lambeosaurines (proportions of humerus). Parasaurolophus is also reconstructed as having an extreme lateroventral extension of the supraacetabular process of the ilium (Fig. 19C), lacking in RAM 14000 (Figs. 18B and 19D). However, this character is ontogenetically dependent (Guenther, 2009), and even variable among Parasaurolophus species (much more prominent in P. cyrtocristatus specimen FMNH P 27393 than in P. walkeri specimen ROM 768). Thus, its absence in RAM 14000 is not unexpected, nor is it of taxonomic consequence. Although RAM 14000 does not preserve major, previously recognized autapomorphies for Parasaurolophus, several cranial features strongly support referral to this taxon. Most significantly, the caudal edge of the caudolateral process of the premaxilla is interpreted as nearly straight along its entire length (Fig. 7A), a feature also found in all species of Parasaurolophus. In every other lambeosaurine of all ontogenetic stages for which the character can be determined, the edge is moderately to strongly kinked. The feature may be associated at least in part with the development of the S-loop in the nasal passages, another feature lacking in RAM 14000 and presumed absent in Parasaurolophus, based on CT-scan data (Sullivan and Williamson, 1999). Additionally, the nasal passages fill nearly the entire crest in RAM 14000 (Figs. 9A and 11C), as in Parasaurolophus but unlike the condition in lambeosaurins (adults and juveniles alike). Morphology of the jugal is also informative in RAM 14000, with a relatively long and slender quadrate process that, in concert with the postorbital process, bounds a narrow infratemporal fenestra (width:length ratio=0.3; Fig. 7). This morphology is also consistently seen in adult Parasaurolophus (P. tubicen, NMMNH P-25100, PMU.R1250; P. walkeri, ROM 768; P. species, UMNH VP 16666, UCMP 143270; Fig. 28). A narrow infratemporal fenestra also occurs variably in subadults and adults of other lambeosaurines (e.g., Hypacrosaurus altispinus, CMN 8501; Kazaklambia convincens, PIN 2230; Velafrons coahuilensis, CPC-59), but never in combination with a narrow quadrate process of the jugal. Furthermore, the quadrate process is distinctly constricted (Fig. 7), so that the ventral border is slightly concave along its entire length. This feature occurs in other Parasaurolophus specimens (P. tubicen, PMU.R1250; P. walkeri, ROM 768; UMNH VP 16666). Some other lambeosaurines have a similar concave border (e.g., Lambeosaurus lambei, CMN 2869), but never in combination with other features. We also note that the quadrate process on the jugal of Kazaklambia convincens expands caudally, contrasting with the comparatively uniform width seen in RAM 14000 and other juvenile lambeosaurines. The impression of the jugal on the right side shows a narrow, triangular extension of the maxillary process between the maxilla and lacrimal (Fig. 13B), also found only in Parasaurolophus (e.g., ROM 768; Fig. 14D). Thus, although individual features of the jugal in RAM 14000 are found in various lambeosaurines, the combination of features is exclusive to Parasaurolophus. Within the Kaiparowits Formation of Utah, three hadrosaurid taxa are known: the hadrosaurines Gryposaurus monumentensis and Gryposaurus sp., as well as the lambeosaurine Parasaurolophus sp. (Gates et al., 2013; Weishampel and Jensen, 1979; Gates and Sampson, 2007). The known Kaiparowits Formation adult material is most similar to Parasaurolophus cyrtocristatus, but some differences in skull morphology suggest that the specimens may represent a distinct but closely related species or a different ontogenetic stage relative to the P. cyrtocristatus holotype specimen (Gates et al., 2013). This issue is currently under study (T. A. Gates and D. C. Evans, personal communication to AAF, 2012). Of eight adult lambeosaurine skulls from the Kaiparowits Formation (BYU 2467; UMNH VP 16394, 16666, 16689, two unnumbered; RAM unnumbered; UCMP 143270), all are referable to Parasaurolophus (Gates et al., 2013). Continued collecting may certainly uncover evidence of other taxa, but to date Parasaurolophus is the only known lambeosaurine from the Kaiparowits Formation. This 1287 1288 1289 1290 1291 1292 1293 1294 1295 1296 1297 1298 1299 1300 1301 1302 1303 1304 1305 1306 1307 1308 1309 1310 1311 1312 1313 1314 1315 1316 1317 1318 1319 1320 1321 1322 1323 1324 1325 1326 1327 1328 1329 1330 1331 1332 1333 1334 1335 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t circumstantial evidence is also consistent with the referral of RAM 14000 to the genus. The described species of Parasaurolophus are distinguished by autapomorphies of the crest (Sullivan and Williamson, 1999) that had not yet developed in RAM 14000. Thus, we cannot assign RAM 14000 to a particular species based upon morphology. In summary, the bulk of the evidence\u2014morphological and geological\u2014is most parsimonious with the referral of RAM 14000 to Parasaurolophus. Specific autapomorphies for the genus that are lacking in the specimen\u2014such as the unique crest and frontal morphology\u2014 are hypothesized to have developed later in ontogeny. Furthermore, the skull of RAM 14000 shows unique morphology relative to known juvenile lambeosaurins. in (a), the jaws are shown without the rhamphotheca, in the approximate position where the : upper and lower bony beak surfaces would first make contact. In (B), the jaws are shown with the upper rhamphotheca (orange), in the approximate position where the upper and lower beak surfaces would first make contact. Note that this is at a wider gape than in (A). Abbreviations: a, distance from the center of the glenoid to the center of the coronoid process; d, distance from the glenoid to the top of the coronoid process; e, distance from the center of the coronoid process to the bite point; \u03b8, the angle between the line of the jaw and the applied force on the coronoid process (measured from the center of the supratemporal fenestra); and \u03b4 , the angle of the diagonal between the top of the coronoid and the glenoid, relative to the line of the jaw. x is the change in gape angle produced by the rhamphotheca. The equation to calculate bite force is given in the text. PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t The black and red scale indicates percentage of maximum reported skull length in increments of 10 percent. The yellow sunburst indicates the approximate skull size at which ornamentation initially appears. Note that Parasaurolophus develops its crest at a very small skull size relative to Corythosaurus, and both hadrosaurids initiate the development of cranial ornamentation at a smaller relative skull size than in Casuarius. Skulls for Parasaurolophus sp. are based on RAM 14000, a hypothetical subadult (Fig. 11B), and the holotype for Parasaurolophus cyrtocristatus (FMNH P 27393, with missing elements patterned after ROM 768). The growth series for Corythosaurus is a composite, with the two smallest skulls (at left) patterned after Hypacrosaurus stebingeri. Because the two taxa are so closely related, and because they show broadly similar patterns of cranial growth where individuals of overlapping size are known (Evans, 2010; Brink et al., 2011), we consider this a reasonable assumption. The smallest skull (at left) is based on RTMP 89.79.52, 87.79.206, 87.79.241, conclusions : RAM 14000 represents the smallest and most complete Parasaurolophus specimen described to date and illustrates a unique juvenile morphology of this taxon relative to other lambeosaurine dinosaurs. Based on histology of the tibia, RAM 14000 exhibits no lines of arrested growth and thus was likely less than a year old at the time of death. Notably, Parasaurolophus initiated crest development at a much smaller body size (and presumably younger age) than did lambeosaurin lambeosaurines. At least in part, this is probably because of the extreme morphology of the crest in Parasaurolophus, which required a longer period of development. The timing of the onset of ornamentation development varies dramatically across amniotes, a topic that deserves considerably more attention. This timing is probably influenced by life history traits such as the timing of reproductive maturity, functional demands upon the skull, and phylogenetic history. As a group, lambeosaurine hadrosaurids initiated crest growth well before reaching adult size (between 25\u201350 percent maximum skull length), a condition shared with most other ornithischian dinosaurs with cranial ornamentation. This may result from the intimate association of the ornamentation with essential functional complexes such as the nasal passages (in the case of hadrosaurids) or musculature (in the case of ceratopsians). If cranial ornamentation played at least some role in sexual selection and/or species recognition, early reproductive maturity may also be related to the precocious development of such ornamentation. Understanding these attributes in dinosaurs requires the documentation of more juvenile specimens with associated skeletochronological data, as well as documentation of patterns in extant species. a) : The elliptically polarized light is under full retarder plate, and the sample is a cross-section \u03bb through the proximal portion of the diaphysis. Moving periosteally through the cortex, the bone tissue comprising the laminae becomes progressively more organized. In the inner cortex (A, B), osteocytes are densely packed in the interstices between vascular canals, and their lacunae are oriented randomly with respect to the long axis of the bone and to each other. In this region, the laminae are mainly comprised of woven bone, with lamellar bone surrounding each vascular canal. In the mid-cortex (C, D), woven bone comprises a smaller portion of the laminae, and parallel-fibered bone lies between the woven and lamellar components. In the outer cortex (E, F), at most only a thin band of woven bone lies in the cores of the laminae, and much of the interstices are comprised of parallel-fibered bone. The periosteum lies to the upper right of each image. Arrows in (B), (D), and (F) indicate the orientation of the slow axis of the plate. All scale bars equal 250 \u00b5m.\u03bb PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Figure 26 Bone microstructure of juvenile Parasaurolophus tibia in regular transmitted light (RAM data for rom 768 and fmnh p 27393 are from weishampel (1981a). : PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Frequency (Hz) Taxon Specime n Tube length (m) Mode 1 Mode 2 Mode 3 Mode 4 Mode 5 P. walkeri ROM 768 3.46 48 96 144 192 240 P. cyrtocrist atus FMNH P 27393 2.21 75 150 225 300 375 P. sp. RAM 14000 0.195 872 1,744 2,616 3,488 4,360 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Figure 1 Outcrops of Kaiparowits Formation (orange) within the state of Utah, USA. The arrow indicates the approximate site of RAM V200921, the locality where RAM 14000 was discovered. PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Figure 2 Skeleton of Parasaurolophus sp., RAM 14000, in right lateral view. (A) interpretive drawing; (B) photograph. Bones are bounded by solid lines and colored orange; matrix is gray. Abbreviations: f, femur; fib, fibula; il, ilium; isc, ischium; MT III, metatarsal III; MT IV, metatarsal IV; ppr, postpubic rod; prp, prepubic process; sc, scapula; sr, sacral rib; tib, tibia. Scale bar equals 10 cm. PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Figure 3 Skeleton of Parasaurolophus sp., RAM 14000, in left lateral view. (A) interpretive drawing; (B) photograph. Bones are bounded by solid lines and colored orange; blue indicates areas of fragmented and powdered bone due to weathering, and green indicates bone impressions. The pink area indicates the location of skin impressions shown in Fig. 21. In (A), the left half of the skull is indicated. A detailed outline of the medial surface of the right half of the skull shown in (B) is contained in Fig. 13B. Abbreviations: f, femur; fib, fibula; h, humerus; il, ilium; isc, ischium; MT III, metatarsal III; prp, prepubic process; sc, scapula; si, skin impression; tib, tibia. Scale bar equals 10 cm. PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Figure 4 Reconstructed skeleton of juvenile Parasaurolophus sp., in left lateral view, based on RAM 14000. Missing elements are patterned after other lambeosaurines (particularly a juvenile Lambeosaurus sp., AMNH 5340). Scale bar equals 10 cm. Reconstruction courtesy of and copyright Scott Hartman. PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Figure 5 ct scanning : In order to better visualize internal cranial anatomy, the skull of RAM 14000 was CT scanned on a Toshiba Aquilion 64 scanner at Pomona Valley Hospital Medical Center, Claremont, California, USA. For the large skull blocks, the specimen was initially scanned at 120 kV and 350 mA, slice thickness of 0.5 mm and reconstruction diameter of 300 mm. This resulted in an in-plane resolution of 0.586 mm by 0.586 mm per pixel. After additional preparation, the specimen was rescanned. The left side of the skull was scanned at 120 kV and 400 mA, slice thickness of 0.5 mm, and reconstruction diameter of 229.687 mm, using a standard bone reconstruction algorithm, resulting in an in-plane resolution of 0.45 mm by 0.45 mm per pixel. The isolated portion of the braincase and maxilla were also scanned at identical parameters except for a reconstruction diameter of 140.625 mm, resulting in an in-plane resolution of 0.274 mm by 0.274 mm. The resulting data were then segmented and measured in 3D Slicer 4.2 (available at www.slicer.org; Gering et al., 1999; Pieper et al., 2004, 2006). Because of internal fracturing of the specimen and areas of poor contrast between bone and matrix, a combination of automatic thresholding and manual segmentation were used in order to visualize endocranial features. All CT scan and segmentation data are reposited at Figshare (Table 1, Supplemental Article S1), and downsampled versions of the mesh are contained in Supplemental Figures S1 and S2. 10 cm. : PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Figure 10 Left half of skull of Parasaurolophus sp., RAM 14000, in medial view. (A) interpretive drawing; (B) photograph. Abbreviations: cb, first ceratobranchial; cmc, common medial chamber; csc, caudal semicircular canal; d, dentary; dd, dentition from dentary (displaced); en, endocranial cavity; exo, exoccipital-opisthotic; m, maxilla; ncp, nasal cavity proper; nf, nutrient foramina; pd, predentary; pm, premaxilla; pt, pterygoid; pti, pterygoid impression; q, quadrate; sa, surangular; st, stapes; t, tooth; v, vomer. Scale bar equals 10 cm. PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Figure 11 Ontogenetic changes in the nasal passages and crest of Parasaurolophus. All images illustrate the condition immediately lateral to the sagittal plane, and rostral is to the left in all images. (A), adult individual, modified after Ostrom (1963). The lateral diverticulum has been altered based on data from RAM 14000, indicating a more proximal origin for the chamber. (B), hypothetical subadult Parasaurolophus. (C), juvenile, based on RAM 14000. Note that the intermediate-sized individual is largely speculative, although the enlarged size of the crest is consistent with a referred braincase, CMN 8502 (Evans et al., 2007). In (B) and (C), the dotted lines separating the lateral diverticulum and the main airway indicate that the diverticulum is obscuring the view of the main airway, and the two chambers run parallel to each other. Dashed lines indicate the positions of the left orbit and infratemporal fenestra. Abbreviations: ld, lateral diverticulum; ma, main airway; vma, ventral portion of main airway. description : RAM 14000 is preserved in nearly perfect articulation, with the neck, hip, lower leg and metatarsals strongly flexed (opisthotonic posture, probably resulting from the fresh carcass\u2019s immersion in water; Reisdorf and Wuttke, 2012; Figs. 2 and 3, Supplemental Fig. S3). The right humerus and pedal digits are gently extended. The specimen was lying on its left side; although more bones are represented on this side, they are much more badly weathered than on the right. Tree roots, freeze-thaw cycles, and recent rodent activity fragmented and displaced many of the elements on the left side. In contrast, the right side is less complete in terms of element representation, but the quality of bone preservation is generally better than on the left side. institutional abbreviations : AMNH, American Museum of Natural History, New York, New York, USA; BYU, Brigham Young University, Provo, Utah, USA; CMN, Canadian Museum of Nature, Ottawa, Ontario, Canada; CPC, Colecci\u00f3n Paleontol\u00f3gica de Coahuila, Museo del Desierto, Saltillo, Coahuila, M\u00e9xico; NMMNH, New Mexico Museum of Natural History, Albuquerque, New Mexico, USA; OUVC, Ohio University Veterinary Collection, Athens, Ohio, USA; PIN, Paleontological Institute, Russian Academy of Sciences, Moscow, Russia; PMU, Museum of Evolution, Uppsala University, Uppsala, Sweden; RAM, Raymond M. Alf Museum of Paleontology, Claremont, California, USA; ROM, Royal Ontario Museum, Toronto, Ontario, Canada; SMP, State Museum of Pennsylvania, Harrisburg, Pennsylvania, USA; TMP, Royal Tyrrell Museum of Paleontology, Drumheller, Alberta, Canada; UCMP, University of California Museum of Paleontology, 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Berkeley, California, USA; UMNH, Natural History Museum of Utah, Salt Lake City, Utah, USA. fieldwork and preparation : All fieldwork was conducted under United States Department of the Interior Bureau of Land Management Paleontological Resources Use Permit (surface collection permit UT06-001S and excavation permit UT10-006E-Gs). For specific locality information, see the \u201cSystematic Paleontology\u201d section below. After discovery in 2009, the specimen was stabilized with polyvinyl acetate (Vinac\u2122 PVA-15, McGean Rohco, Inc., Cleveland, Ohio, USA) dissolved in acetone. Because of weathering, portions of the pedal phalanges and the right half of the skull were collected in 2009, separately from the rest of the skeleton. Surface dry screening uncovered additional bone fragments. During the 2010 field season, the specimen was encased in a plaster and burlap field jacket and airlifted from Grand Staircase-Escalante National Monument by helicopter. Subsequently, the fossil was mechanically prepared using pneumatic engravers of varying sizes (PaleoTools, Brigham City, Utah, USA; Chicago Pneumatic, Independence, Ohio, USA). A minimal amount of matrix was left in place, in order to support and preserve the relative positions of the bones as well as soft tissue impressions. Full field and lab documentation are on file at RAM. photogrammetry : Because the humerus was preserved as a natural mold, we produced a digital cast of the element using photogrammetry. 12 color photos at 4000\u00d73000 pixel resolution were acquired with a Nikon CoolPix L22 digital camera (Nikon Inc., Melville, New York, USA), and were resized to 2000\u00d71500 pixels. Data were processed using BundlerTools (available at server.topoi.hu-berlin.de/groups/bundlertools/), which in turn uses Bundler 0.4, CMVS, and PMVS2. The resulting raw point cloud was processed further in MeshLab 1.3.0 (available at www.meshlab.org), in which a surface mesh was produced using a Poisson surface reconstruction 112 113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130 131 132 133 134 135 136 137 138 139 140 141 142 143 144 145 146 147 148 149 150 151 152 153 154 155 156 157 158 159 160 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t algorithm (Octree Depth=10, Solver Divide=9, 1 sample per node, Surface Offsetting=1). Because the original mesh represented a natural mold, normals were inverted to produce a digital cast. The mesh was scaled by comparison with measurements of the original specimen, and data were exported in STL file format. A downsampled version of the mesh is contained in Supplemental Figure S4. A similar procedure was used with a series of photos of the right side of the skeleton, to produce additional 3D renderings. Photographs at 2848\u00d74288 pixel resolution were acquired with a Nikon D90 SLR digital camera (Nikon, Inc., Melville, New York, USA) fitted with a Tamron 179D lens (Tamron Co., Ltd., Saitama, Japan), and were resized to 2000\u00d71500 pixels. Ten separate reconstructions were generated, for the ventral, central, and caudal portions of the rib cage (utilizing 15, 24, and 24 photos, respectively), femur (16 photos), tibia and fibula (29 photos), pes (27 photos), pelvic region (21 photos), skull (17 photos), tail (24 photos), and dorsal view of the skeletal block (18 photos). The point clouds were aligned and meshed in MeshLab (Poisson surface reconstruction algorithm, Octree Depth=12, Solver Divide=12, 5 samples per node, Surface Offsetting=1). The original point clouds and surface mesh are reposited at Figshare. A downsampled version of the mesh is contained in Supplemental Figure S3. The point clouds for the hind limb were combined and meshed to produce a separate rendering of this part of the body; a downsampled version of this mesh is contained in Supplemental Figure S5. All surface meshes are reposited at Figshare (Table 1, Supplemental Article S1). laser scanning : A disarticulated squamosal and pedal phalanges were laser scanned to produce full-color digital models. The original point clouds were captured using a NextEngine 3D color laser scanner (NextEngine, Inc., Santa Monica, California). For each element, a series of individual scans (varying depending upon the complexity of the element) were acquired at a resolution of 6,200 points/cm2. The individual scans were stitched together in ScanStudio HD Pro 1.3.2 (NextEngine, Inc., Santa Monica, California) and fused into a single watertight mesh. All surface meshes, along with full technical details, are reposited at Figshare (Table 1, Supplemental Article S1). histological sampling : Two samples from the right tibia were extracted for histological analysis. This bone was chosen because of its excellent preservation and easy accessibility on the specimen. Additionally, studies in other ornithischian dinosaurs (the basal iguanodontian Tenontosaurus tilletti and the hadrosaurine hadrosaurid Maiasaura peeblesorum) suggest that the tibia undergoes less remodeling at midshaft than do other skeletal elements, a characteristic critical for estimating the age of the animal at death using lines of arrested growth (Horner et al., 2000; Werning, 2012). Thus, the tibia is an ideal element for histological study. The position of natural cracks in the bone precluded sampling exactly at the tibial middiaphysis. However, we were able to sample at two points slightly proximal to this point. The more proximal sample \u201cA\u201d was taken 120 mm from the proximal end of the bone (~39 percent of the total tibial length, 307 mm), and sample \u201cB\u201d was taken 135 mm (~44 percent total length) from the proximal end of the bone (Fig. 17D). Prior to sampling, we photographed and molded the surface of this region to document original morphology. Afterward, the sampled region was refilled with plaster to approximate the original anatomy. We removed both samples using a Dremel Moto-Tool Model 395 rotary tool (Dremel, Inc., Racine, Wisconsin, USA) and small chisel. Because the tibia is partially embedded in matrix, only the caudolateral quadrant of the shaft, rather than a full cross-section, was extracted. We estimate the maximum craniocaudal diameter of the tibia at these points to be 40 mm. Both 161 162 163 164 165 166 167 168 169 170 171 172 173 174 175 176 177 178 179 180 181 182 183 184 185 186 187 188 189 190 191 192 193 194 195 196 197 198 199 200 201 202 203 204 205 206 207 208 209 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t samples include both compact and cancellous bone; the cortex of sample A is ~12 mm thick, and sample B is ~15\u201316 mm thick. The longitudinal sections made from sample A span 12 mm (proximo-distally) along the diaphysis. Given the maximum diameter relative to the thickness of the sections, and that the medullary cavity is open (i.e., not completely filled by cancellous bone) at both points, we think our samples likely capture most if not all of the preserved histology in this quadrant of the bone. Histological samples were prepared by SW at UCMP. Before embedding, the periosteal surfaces were cleaned with acetone to remove any traces of polyvinyl acetate. Both samples were then embedded in Silmar-41 clear polyester casting resin (Interplastic Corporation, Saint Paul, Minnesota, USA) catalyzed with methyl ethyl ketone peroxide (Norac, Inc., Helena, Arkansas, USA) at 1 percent by mass and allowed them to cure for 48 hours at room temperature. Thick transverse (cross-sectional) sections (1\u20131.5mm) were cut using a diamond-tipped wafering blade on a low-speed Isomet lapidary saw (Buehler, Inc., Lake Bluff, Illinois), mounted to glass slides, and ground to optical clarity using the materials and methods described in Werning (2012). Two slides in transverse section were made from sample A and three from sample B. Additionally, two slides in longitudinal section were made from some of the remaining embedded portion of sample A. All histological slides are reposited at RAM. Histological Imaging All slides were examined under regular transmitted light, elliptically polarized light (i.e., using a full wave retarder or red tint plate, \u03bb = 530 nm) and crossed plane polarizing filters. The filters were used to enhance birefringence. Overlapping digital images photographs (50% overlap by eye in X and Y directions) were taken using a D300 DSLR camera (Nikon Inc., Melville, New York, USA) mounted to an Optiphot2-Pol light transmission microscope (Nikon Inc.). To image the entire slide or radial \u201ctransects\u201d, digital images were photomontaged using Autopano Giga 2.0 64Bit (Kolor, Challes-les-Eaux, France), using the program settings described in Werning (2012). High-resolution histological images are digitally reposited online for scholarly use at MorphoBank (http://morphobank.org/permalink/?P836, project p836; see Table 2 for a list of accession numbers). Digital images larger than 25,000 pixels in either dimension were digitally reduced (preserving original dimension ratios) to allow processing on MorphoBank. These edits were made after scale bars had been added. linear measurements : Linear measurements under 300 mm were measured to the nearest 0.l mm with digital calipers, and non-linear measurements as well as those over 300 mm were measured to the nearest mm with a cloth measuring tape. Landmarks for most cranial measurements were patterned after those in Dodson (1975) and Evans (2010), and are diagrammed along with postcranial measurements in Fig. 5. Relevant measurements are contained in Tables 3\u201310. skeletal completeness : In order to assess relative skeletal representation for the three most complete specimens of Parasaurolophus (FMNH P 27393, RAM 14000, and ROM 768), we tallied the preserved elements for each. The skull and mandible were considered a single unit, as were the sacrum and sacral ribs. Partial elements were counted as present in the specimen, and we only counted bilateral elements once (e.g., even if both humeri were present, this element was counted only once). Tallies are contained in Supplemental Table S1. nomenclatural conventions : In this paper, the following conventions are utilized. These are defined here so as to avoid 210 211 212 213 214 215 216 217 218 219 220 221 222 223 224 225 226 227 228 229 230 231 232 233 234 235 236 237 238 239 240 241 242 243 244 245 246 247 248 249 250 251 252 253 254 255 256 257 258 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t confusion in the event of future systematic or phylogenetic revisions. Following the recent formal definition by Prieto-M\u00e1rquez and colleagues (2013), the clade Lambeosaurini (lambeosaurins) includes all taxa closer to Lambeosaurus lambei than to Parasaurolophus walkeri, Tsintaosaurus spinorhinus, or Aralosaurus tuberiferus. This clade is approximately equivalent to the informally used but never formally defined \u201cCorythosaurini\u201d (Godefroit et al., 2004; Evans and Reisz, 2007). Unless otherwise specified, comparisons here involve the North American genera Corythosaurus, Lambeosaurus, Hypacrosaurus, and Velafrons, as well as the Asian taxon Nipponosaurus. The clade Parasaurolophini (parasaurolophins) includes all taxa closer to Parasaurolophus walkeri than to Lambeosaurus lambei, Tsintaosaurus spinorhinus, or Aralosaurus tuberiferus (Godefroit et al., 2004; Evans and Reisz, 2007; Prieto-M\u00e1rquez et al., 2013). This includes two genera, Parasaurolophus and Charonosaurus. Unless otherwise specified, usage of the name Parasaurolophus alone refers to all three named species, P. walkeri, P. cyrtocristatus, and P. tubicen. referred material : RAM 14000, a partial skull and articulated skeleton (Figs. 2 and 3). locality and horizon : RAM V200921, Grand Staircase-Escalante National Monument, Garfield County, Utah, USA (Fig. 1); upper part of middle unit (sensu Roberts, 2007) of the Kaiparowits Formation; Late Cretaceous (late Campanian; Roberts et al., 2005). The site is stratigraphically between two locally prominent bentonites, tentatively correlated with bentonites KBC-109 and KBC-144 of Roberts et al. (2005), both exposed less than 10 km away from RAM V200921 and dated to 75.51 +-0.15 Ma (Roberts et al., 2013). The specimen was preserved within a cross-bedded tabular sandstone, tentatively interpreted as a channel deposit following previous literature (Roberts, 2007). Detailed locality data are on file at the RAM and are available to qualified investigators upon request. skull and mandible : The skull of RAM 14000 was split in two (parasagittally) by erosion; in order to preserve 259 260 261 262 263 264 265 266 267 268 269 270 271 272 273 274 275 276 277 278 279 280 281 282 283 284 285 286 287 288 289 290 291 292 293 294 295 296 297 298 299 300 301 302 303 304 305 306 307 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t visibility of internal structures, the two halves have not been reassembled. The skull and mandible are in articulation, with only slight displacement of the quadrate and mandible relative to each other. The left side is more complete, preserving nearly all elements (with the exception of a portion of the premaxilla). The dorsal and rostral portions of the right side are missing, with the exception of some elements (such as the maxilla, parts of the dentary, and braincase) that were separated from the main block by erosion. A digital reconstruction, based on RAM 14000 with missing sections modeled after juvenile lambeosaurins, is presented in Fig. 6. Measurements are included in Tables 3\u20135 In lateral view (Fig. 7), the skull has a profile typical of a juvenile hadrosaur\u2013squared caudally and triangular rostrally. The orbit is proportionately large and slightly longer than tall. The infratemporal fenestra is inclined caudally and quite narrow, with a slight constriction at its midpoint. Because the midline of the skull is missing, the exact shape of the supratemporal fenestra is unknown. However, the preserved portion is roughly trapezoidal. Individual bones and skull regions are described below. Premaxilla. The premaxilla is the most prominent cranial bone in lateral view, extending from the upper \u201cbeak\u201d to the dorsum of the skull. The bone is roughly divisible into three portions: a lower portion including the oral margin and external (bony) naris as well as caudodorsal and caudolateral processes that form the remainder of the premaxilla and much of the crest. The rostroventral-most segment of the premaxilla forms the dorsal oral margin. In lateral view (Fig. 7), most of the edge of the beak is straight and only slightly inclined (relative to the maxillary tooth row), contrasting with the more inclined surface seen in most other lambeosaurine specimens (Evans, 2010), including Parasaurolophus walkeri (ROM 768). Furthermore, the caudal corner of the beak is sharply hooked to form a tab-like process below a broadly concave postoral margin. Although this process occurs to varying degrees in many lambeosaurines of all ontogenetic stages (Evans, 2010), the condition in RAM 14000 is unusually prominent and most similar to that in Parasaurolophus walkeri (Parks, 1922; Sullivan and Williamson, 1999), particularly in the combination of the tab-like process and rounded postoral margin. The only major difference is that the concavity in the postoral margin is sharper in ROM 768 (Parasaurolophus walkeri) than in RAM 14000. Measuring from the midline, the mediolateral width of the oral margin is estimated at 26 mm, and the estimated entire width of the free oral margin (perpendicular to the midline) is thus 52 mm. The oral margin is fairly uniform in outline, with no major denticulations. The lower portion of the premaxilla encloses the external (bony) naris. The dorsal margin of the bone is eroded away, but its impression is preserved along the narial margin. The bony naris is roughly lenticular, rounded at its distal (rostroventral) end and pointed at its proximal (caudodorsal) end. The depression in the lateral surface of the premaxilla that houses the naris is delimited from the rest of the skull by a gentle ridge that is most prominent caudodorsally. The caudolateral process of the premaxilla forms the ventral margin of the external (bony) naris and extends caudolaterally. Dorsally, the process contacts the caudodorsal process of the premaxilla. Although much of this suture is extremely fragmented, it appears quite straight along its preserved portions (Fig. 7A). This contrasts with the more sinuous suture seen in juvenile and adult Hypacrosaurus, Corythosaurus, and Lambeosaurus (Evans, 2010; Brink et al., 2011), but more closely matches the fairly straight suture (where it can be discerned) in specimens of Parasaurolophus (Sullivan and Williamson, 1999). Similarly, the sutures with the maxilla, lacrimal, and prefrontal, where they can be discerned, are straight, much closer to the condition in Parasaurolophus than in lambeosaurins. This may reflect the internal absence of an \u201cS-loop\u201d in the narial passages, a feature that occurs in lambeosaurins (e.g., Weishampel, 1981b; Evans et al., 2009). The ventral portions of the process are comparatively narrow, but the process expands 308 309 310 311 312 313 314 315 316 317 318 319 320 321 322 323 324 325 326 327 328 329 330 331 332 333 334 335 336 337 338 339 340 341 342 343 344 345 346 347 348 349 350 351 352 353 354 355 356 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t dorsally, where it forms part of the crest. The caudolateral process forms the ventral border of the premaxilla-nasal fontanelle and presumably contacts the nasal at the caudal extent of the fontanelle. The caudodorsal process of the premaxilla, which forms much of the rostral profile of the skull, is poorly preserved. Its contact with the nasal cannot be interpreted with confidence due to extensive cracking, so no further comment will be offered here. Nasal. Much of the nasal is poorly preserved in gross external view, with the exception of its suture with the frontal and a portion along the caudal margin of the crest (Fig. 7A). The nasal forms the rostrodorsal margin of the premaxilla-nasal fontanelle, as well as the caudal edge of the crest. The dorsal margin of the nasal is strongly rounded and almost horizontal, unlike the peaked margin seen in juvenile lambeosaurins ROM 758 and 759 (Lambeosaurus sp. and Corythosaurus sp., respectively). The nasal\u2019s suture with the prefrontal is not readily visible, and the contact with the frontal is described with that element. The internasal suture in the crest is flat along the suture\u2019s medial surface. Crest (premaxilla and nasal). The crest is roughly dome-shaped, with a broad and rounded profile. It is semi-circular in lateral view, with its midpoint rostral to the orbit (Fig. 7). Unlike adult lambeosaurines, including Parasaurolophus, the crest does not overhang the frontal. Based on the position of the premaxilla-nasal fontanelle, and its relationships in lambeosaurins, the nasal is inferred to be the bone that bounds the dorsal and caudal margins of the crest (Fig. 7A). The presence of a premaxilla-nasal fontanelle contrasts with its absence in adult Parasaurolophus and Hypacrosaurus altispinus of all ontogenetic stages, but is similar to juvenile Corythosaurus, Lambeosaurus, and Hypacrosaurus stebingeri, and probably also Kazaklambia convincens (Bell and Brink, in press; Horner and Currie, 1994; Evans et al., 2005; Brink et al., 2011). Unlike juvenile lambeosaurins or Kazaklambia convincens, the fontanelle is exceptionally dorsally placed relative to the rest of the crest in RAM 14000. In dorsal and rostral view (Fig. 8A\u2013D), the margins of the crest are strongly rounded. The caudal margin is only gently tapered. This contrasts with the condition in both juvenile and adult lambeosaurins (Corythosaurus, Lambeosaurus, and Hypacrosaurus), in which a thin flange of bone projects from the caudal edge of the crest (Weishampel, 1981b; Evans et al., 2009). In these animals, the flange of bone is not occupied by the nasal passages. In RAM 14000, the nasal passages fill nearly the entirety of the crest, similar to the condition in adult Parasaurolophus (Weishampel, 1981b; Sullivan and Williamson, 1999). Furthermore, the crest in RAM 14000 is quite broad, whereas the crest is also fairly narrow along its length in juvenile and adult lambeosaurins. Nasal cavity. The nasal passages are preserved only on the left side and were studied by gross examination of broken surfaces as well as using CT scans (Fig. 9, Supplemental Fig. S1). Terminology for anatomical structures follows that of Evans et al. (2009) and Weishampel (1981b). The airway closest to the external naris is termed \u201cproximal,\u201d and the airway furthest from the naris and closest to the internal choanae is termed \u201cdistal.\u201d Portions of the nasal passages and their surrounding bones, particularly the interval immediately caudal to the external naris, are heavily fractured. Furthermore, it appears that some areas were not completely ossified at the time of death, and we hypothesize that some aspects of the chambers may have become more prominently separated later in ontogeny. Thus, we must emphasize that aspects of our digital reconstructions may be subject to alternative interpretation. Points of particular concern are noted as such at the appropriate points in the description. The external naris is ovoid and strongly elongated (Fig. 7). Part of the main airway distal to this point is fragmented and poorly preserved, but has been reconstructed based on the CT scan data as well as physical examination of the specimen itself. The reconstruction shows the airway to be straight in lateral view (Fig. 7A\u2013C), with no evidence for an S-loop as seen in 357 358 359 360 361 362 363 364 365 366 367 368 369 370 371 372 373 374 375 376 377 378 379 380 381 382 383 384 385 386 387 388 389 390 391 392 393 394 395 396 397 398 399 400 401 402 403 404 405 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t lambeosaurins of all known post-embryonic stages (Horner and Currie, 1994; Evans et al., 2009). It is possible that the S-loop simply wasn\u2019t preserved, but based on the contours of the betterpreserved distal airway, we do not consider this particularly likely. The main airway progresses in the segment known as the dorsal ascending tract, homologous to the nasal vestibule of other sauropsids (Weishampel, 1981b), and continues to the apex of the crest (Fig. 9D,E), measuring 170 mm from the proximal end of the airway to the summit of the dorsal ascending tract. At a sharp U-bend, the airway enters the section known as the ventral ascending tract (Fig. 9D,E), which drops ventrally to enter the main body of the skull. The ventral ascending tract (homologous to the nasopharyngeal duct of other sauropsids; Weishampel, 1981b) is only 33 mm long and much shorter than the dorsal equivalent. In lambeosaurins, this communication between the main airway and the rest of the skull is reconstructed to occur at the midline via a common median chamber (Evans et al., 2009). By contrast, the airway of RAM 14000 enters the skull separately on both right and left sides, as is more usual for tetrapods. The common median chamber is clearly separated from the ventral aspects of the skull by a thin lamina of bone (preserved as an impression visible in medial view as well as a small piece of bone visible in CT scan; Figs. 9D,E,M and10). The common median chamber of the nasal airway is directly visible on the broken medial surface of the left half of the skull (Figs. 9D,E and 10). In profile, this chamber is oval and rostrocaudally elongated (25.5 mm long by 15 mm tall). It is positioned just above the level of the dorsal margin of the skull roof, at the very lower edge of the crest. Relative to the orbit, the common median chamber is dorsal and slightly rostral. This chamber, along with the lateral diverticulum, is probably homologous to the nasal cavity proper of other sauropsids (Weishampel, 1981b). The lateral diverticulum is prominent, shaped approximately like a shepherd\u2019s crook and coiled clockwise in left lateral view (Fig. 9A\u2013C). An incompletely ossified lamina separates the diverticulum from the main airway (Fig. 9I\u2013K); proximally, this coincides with a lamina of bone that may represent the premaxilla-nasal suture. Ventrally, the lateral diverticulum appears to communicate with the main nasal airway within the skull (Fig. 9M). In lambeosaurins, the lateral diverticulum does not communicate directly with the main airway in the skull, but is separated by a bony lamina. We hypothesize that a similar condition occurred in RAM 14000, but that the lamina was not completely ossified at the ontogenetic stage represented here. Density differences in the sediment are faintly visible in CT scan along this line. These are not definitively bone, and the morphology is suggestive of a soft tissue pattern that may have been preserved through early infilling of the skull by sediment (Daniel, 2012). As interpreted here, the lateral diverticulum diverges from the main airway approximately halfway between the external naris and the common median chamber (Fig. 9C). This is a much more proximal origination than in Corythosaurus (subadult CMN 34825 and juvenile ROM 759) and Lambeosaurus (juvenile ROM 758), but matches the condition seen in Hypacrosaurus (adult ROM 702). Thus, the lateral diverticulum is quite extensive in RAM 14000. Unlike Hypacrosaurus, however, the lateral diverticulum is not positioned ventrally to the main airway at any point; the two passages are genuinely parallel (as reconstructed for adult Parasaurolophus; Weishampel, 1981b). The apex of the lateral diverticulum opens to the premaxilla-nasal fontanelle. Thus, the lateral diverticulum is bordered primarily by the premaxillae, with a small contribution from the nasals. Compared to reconstructions for Parasaurolophus cyrtocristatus and P. walkeri (Weishampel, 1981b), RAM 14000 displays several important departures from the adult condition (Fig. 11). Corresponding to the small crest, the nasal passages are much shorter in overall length. Unlike adult specimens, the ventral ascending tract of the nasal passages of RAM 14000 is quite short relative to the dorsal ascending tract. Furthermore, the lateral diverticulum of RAM 14000 is virtually the same length as the dorsal ascending tract. In adult P. cyrtocristatus 406 407 408 409 410 411 412 413 414 415 416 417 418 419 420 421 422 423 424 425 426 427 428 429 430 431 432 433 434 435 436 437 438 439 440 441 442 443 444 445 446 447 448 449 450 451 452 453 454 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t and P. walkeri, the lateral diverticulum only extends slightly past the midpoint of the crest (Fig. 11A), and is reconstructed as a blind-ended chamber (Ostrom, 1963; Weishampel, 1981b). This reconstruction should be tested against CT scan data. The hooked morphology of the lateral diverticulum in RAM 14000 is reminiscent of the condition reconstructed for P. tubicen (Sullivan and Williamson, 1999). The olfactory region of RAM 14000, as in juvenile lambeosaurins (ROM 758, 759), is a subdivision of the nasal cavity located rostral to the olfactory bulbs and caudal to the entrance of the main airway to the respiratory region contained within the bulk of the skull (\u201cantorbital region\u201d; Fig. 9C,H). In lateral view, the olfactory region is strongly dorsally arched and approximately level with the rostral half of the orbit (Fig. 9B,C), as seen in other lambeosaurins for which data are available. In dorsal view (Fig. 9F\u2013H), the olfactory region is less strongly tapered caudad than in lambeosaurins (ROM 758, 759; CMN 34825). Maxilla. Like other hadrosaurids, the maxilla is triangular in lateral view (Figs. 7 and 12D), apparently with a straight suture with the premaxilla (unlike some lambeosaurins; e.g., Hypacrosaurus altispinus, ROM 702). Fracturing and weathering obscure many additional details. The prominent ectopterygoid ridge extends from the base of the maxilla\u2019s dorsal process to the caudal edge of the maxilla (Fig. 12D). A marked ventral curvature in the ridge from rostral to caudal corresponds with the shape of the ectopterygoid. Along the flattened medial surface of the maxilla, a series of alveolar foramina, one between each alveolus, forms a dorsally arched sequence (Fig. 10). A subtle ridge, increasing in prominence caudally, occurs immediately dorsal to the foramina and continues at least for the rostral third of the maxilla; the caudal extent is obscured by fracturing. This morphology can only be evaluated on the left maxilla; the medial surface of the right maxilla is too poorly preserved. CT scans indicate approximately 20 tooth positions in the maxillary tooth row, with two (rostrally) to three (at mid-point of tooth row) teeth in each file. The greatest internal height of the tooth file is 20 mm at the middle of the bone, and the smallest height is 8 mm at the rostral margin. As exposed on the left maxilla, there were usually two functional teeth on the wear surface at a time. The wear surfaces on each functional tooth range from 4 to 7 mm tall and 3 to 5 mm wide, and the maximum height of the wear surface as exposed at alveolus 5 is 15 mm. Adult Parasaurolophus have 40 or more tooth positions in the maxilla (NMMNH P-25100, PMU.R1250; Sullivan and Williamson, 1999), twice the number in RAM 14000. This low tooth count is typical of juvenile hadrosaurids (Suzuki et al., 2004). Jugal. Although the left jugal is more complete, crushing obscures the sutures along the rostral margin (Fig. 7). The right side preserves the impressions of these sutures (Fig. 13B,D), and the following description is thus a composite of both sides. The jugal forms part of the rostral margin and the entire caudal margin of both the orbit and infratemporal fenestra. The rostral process, along its contact with the maxilla and lacrimal, is triangular and sharply pointed (Fig. 13B). The ventral edge of this rostral process is longer than the dorsal edge, unlike most lambeosaurins of various ontogenetic stages (in which the ventral edge is equal to or shorter in length to the dorsal edge) but similar to the condition in Parasaurolophus walkeri (ROM 768; Fig. 14D) as well as a larger juvenile Parasaurolophus sp. (SMP VP-1090). A distinct, slightly constricted extension occurs at the rostral end of this rostral process, visible as an impression on the right side, which creates a hooked ventral margin on the process. The ventral and dorsal margins of this rostral process are more acutely angled than seen in adult P. walkeri (Figs. 14C,D). These shape differences may due, at least in part, to the relatively larger orbit in juveniles. The postorbital process is inclined parallel to the quadratojugal process and tapers along the infratemporal fenestra towards an articulation with the descending process of the postorbital. The quadrate process is tapered and caudodorsally inclined at a 40\u00ba angle. Its 455 456 457 458 459 460 461 462 463 464 465 466 467 468 469 470 471 472 473 474 475 476 477 478 479 480 481 482 483 484 485 486 487 488 489 490 491 492 493 494 495 496 497 498 499 500 501 502 503 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t caudodorsal edge is exceptionally pointed compared to other lambeosaurines, and is not expanded relative to the rest of the process as in Kazaklambia convincens. The jugal is dorsoventrally constricted ventral to the orbit (19 mm tall) and on the quadrate process ventral to the infratemporal fenestra (22 mm tall). Similar constrictions are also seen in Corythosaurus, Lambeosaurus, and other Parasaurolophus (Evans, 2010). The angle between the postorbital and quadrate processes is quite tight, similar to the condition in Hypacrosaurus, Parasaurolophus, and Kazaklambia convincens (Bell and Brink, in press; Rozhdestvensky, 1968). As preserved, the jugal forms only the ventral third and quarter of the rostral and caudal margins of the infratemporal fenestra, respectively (Figs. 7 and 13). Quadrate. The quadrate is complete on both sides, but the right quadrate is slightly displaced ventrally and both quadrates are slightly displaced laterally. The quadrate forms the caudal margins of the infratemporal fenestra and the skull (Figs. 7 and 13). The dorsal condyle of the quadrate articulates with the squamosal cotyle, as is typical of hadrosaurids. Dorsal to its contact with the jugal, the quadrate is slightly concave caudally and is inclined caudodorsally at 30\u00b0 relative to vertical. The ventral third of the quadrate is straight. The surface for articulation with the caudal process of the jugal is rostrally bifurcated, resulting in an S-shaped sutural surface (Fig. 7); the dorsal half of the quadrate tapers along the infratemporal fenestra towards this articulation. The dorsal condyle of the quadrate is triangular (with a rounded and medially directed apex) in dorsal view, whereas it is rounded in lateral view. The ventral end is rounded in lateral view and trapezoidal with a saddle-shaped articular surface in ventral view. The ventral condyle of the quadrate is 21.4 mm wide and 18.2 mm long on its lateral edge and 8.7 mm long on its medial edge, respectively. In caudal view, the quadrate is straight but slightly bowed medially (Fig. 8F,G). The quadrate articulates with the pterygoid wing rostromedially along a Vshaped suture, extending from the quadratojugal to the dorsal margin of the infratemporal fenestra (Fig. 10). The pterygoid flange of the quadrate is only partially preserved, forming a plate-like and slightly concave (in medial view) region of bone (Fig. 10). At its ventral third, the caudal edge of the quadrate is flattened; dorsally, the element\u2019s caudal edge tapers to a rounded ridge. The quadrate in RAM 14000 is more gracile than seen in adult Parasaurolophus (Figs. 14G,H). Quadratojugal. The quadratojugal is not visible on the left side, but CT scans indicate that the rest of the element is displaced rostromedially relative to the jugal. The quadratojugal is a thin, sinuous and rostrally inclined element that rostrodorsally tapers to a point and buttresses the quadrate caudoventrally. Squamosal. The squamosal is thin and arched dorsally, with a concave quadrate cotyle on its ventrolateral surface (Fig. 12A). The prequadratic process is sharply pointed rostrodorsally. The postquadratic process has a straight rostral border and a convex caudal border that abuts the paroccipital process (Fig. 7). The squamosal forms the caudolateral margin of the supratemporal fenestra and the dorsal margin of the infratemporal fenestra. Measuring from its edge on the base of the paroccipital process to the dorsal margin of the squamosal, the element is 67 mm tall. The caudomedial corner of the squamosal hooks upward in lateral view, and the dorsal surface of the squamosal is entirely convex. The medial extents of the squamosals are not preserved, so we cannot determine if they contacted each other as in most lambeosaurins, Kazaklambia convincens and adult Parasaurolophus, or were separated by the parietals as in Velafrons (Bell and Brink, in press; Gates et al., 2007; Brink et al., 2011). . Lacrimal. The lacrimal forms the mid-rostral margin of the orbit. Sutures with the prefrontal are difficult to interpret, as are those with the premaxilla. Impressions on the right side (Fig. 13B) show that the lacrimal articulates ventrally with the jugal along a caudoventrally inclined, slightly ventrally convex suture. Postorbital. The postorbital is T-shaped in lateral view (Figs. 7, 14A), bounding part of 504 505 506 507 508 509 510 511 512 513 514 515 516 517 518 519 520 521 522 523 524 525 526 527 528 529 530 531 532 533 534 535 536 537 538 539 540 541 542 543 544 545 546 547 548 549 550 551 552 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t the dorsal margin of the orbit and nearly the entire caudal margin as well. The postorbital articulates with the prefrontal rostromedially along a straight suture and the frontal medially along a more sinuous suture (Fig. 8D). The jugal process is slightly curved rostrally and forms most of the rostrodorsal margin of the infratemporal fenestra, tapering alongside the caudal towards articulation with the ascending process of the jugal. The caudal process of the postorbital measures 13 mm wide at its narrowest point, but broadens caudally. The caudal-most portion of the caudal process thins and splits into dorsal and ventral prongs (Fig. 7A), as in Parasaurolophus and lambeosaurins except for Hypacrosaurus altispinus (Evans, 2010); the ventral prong is more extensive. This process overlaps the dorsal surface of the squamosal, and forms a small part of the rostrolateral margin of the supratemporal fenestra. In lateral view, the dorsal edge of the postorbital is slightly concave, unlike the convex margin in P. walkeri (ROM 768). The maximum length of the jugal and caudal processes are roughly equal, similar to lambeosaurins of various sizes, but unlike adult Parasaurolophus (where the jugal process is longer; NMMNH P-25100, ROM 768) or Charonosaurus (where the caudal process is longer). Similarly, the rostral process of the postorbital is much shorter in adult Parasaurolophus (e.g., ROM 768, Fig. 14B) than in RAM 14000. Consequently, the proportion of the skull roof in RAM 14000 formed by the postorbital is much greater than that formed by the squamosal in lateral view (Fig. 7A), unlike adult Parasaurolophus. Unlike Kazaklambia convincens or Charonosaurus jiayinensis (Bell and Brink, in press), the postorbital lacks a dome on its rostral process in RAM 14000. Frontal. The left frontal is nearly completely preserved with visible sutures, except for its extreme caudomedial portion (Fig. 8C,D). In dorsal view, the frontal articulates with the prefrontal rostrolaterally along a linear suture that trends laterally along its caudal extent. The suture with the postorbital is comparatively linear also, with a slight medial trend from rostral to caudal. The contact with the parietal is obscured, but a small portion of the frontal\u2019s contribution to the supratemporal fenestra is visible. The paired nasals form a triangular prong that laps onto the rostral end of the dorsal surface of the frontals (Fig. 8D). This morphology is unique relative to the rounded or squared contact in lambeosaurins and adult Parasaurolophus, where the sutures can be determined (Evans et al., 2007; Brink et al., 2011). It also differs from Kazaklambia convincens, where a prong of the paired frontals inserts between the nasals on the midline (Bell and Brink, in press). Adult and subadult Parasaurolophus have a nasofrontal suture that is expanded caudodorsally and sharply angled relative to the rest of the skull roof (Evans et al., 2007); there is no evidence in CT scan or direct visual observation of such a feature in RAM 14000. Thus, the condition here is comparable to the non-angled and unexpanded state in lambeosaurin juveniles and adults, as well as the condition in K. convincens. Similarly, the individual frontal in RAM 14000 is approximately as long at the midline (measuring from the caudal extent of the nasal suture to the rostral extent of the parietal suture) as it is wide (34.2 mm vs. 31.7 mm, a ratio of 1.08; doubling to approximate the width across both frontals produces a ratio of 0.54). The median frontal dome is thus fairly elongate (Fig. 7). This too contrasts with the condition in adult and subadult Parasaurolophus (where the frontal is wider than long) and is more similar to the state in lambeosaurins of various growth stages (Evans et al., 2007). Similar to other lambeosaurines, the frontal does not reach the orbital rim. Prefrontal. Only the sutures on the caudal edge of the left prefrontal are clearly visible (Figs. 7 and 8C,D). Here, the bone forms a triangular point interposed between the medial margin of the postorbital and the lateral margin of the frontal, as in other lambeosaurines. The bone forms the rostrodorsal margin of the orbit and contacts the lacrimal ventrally. Based on the extent of the premaxilla, it is unlikely that the prefrontal formed any significant portion of the crest in RAM 14000 (unlike adult lambeosaurines but similar to many subadult specimens; Evans et al., 2005). 553 554 555 556 557 558 559 560 561 562 563 564 565 566 567 568 569 570 571 572 573 574 575 576 577 578 579 580 581 582 583 584 585 586 587 588 589 590 591 592 593 594 595 596 597 598 599 600 601 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Ectopterygoid. The ectopterygoid sits atop the caudodorsal margin of the caudal process of the maxilla, extending medial to the coronoid as viewed on CT scans. The element is bestpreserved on the right side (Fig. 12D), showing that the ectopterygoid is a thin and broad element with a prominent ventral bend at its caudal third. The mediolateral width of the ectopterygoid and its relationship to structures such as the pterygoid cannot be visualized because of weathering. Pterygoid. The pterygoid is visible only on the left side (Fig. 10), with just its caudal quadrate wing preserved. The wing is thin (<1 mm) and gently concave medially, paralleling the corresponding medial surface of the quadrate ramus. As viewed in CT scan, the nearly complete pterygoid on the right side is typical of the condition expected for hadrosaurids (Ostrom, 1961; Heaton, 1972). Palatine. The palatine is not sufficiently preserved or exposed to comment upon its morphology. Vomer. The caudodorsal portion of the vomer is exposed on the left half of the skull (Fig. 10). The preserved dorsal edge is acutely angled, and the rostral edge of the element tapers rostrolaterally towards its (inferred) insertion between the premaxillae. The apex of the vomer is located just rostral to the rostral end of the orbit, at approximately the same height (dorso-ventral level). The vomer is not sufficiently preserved for detailed comparison with the element in other hadrosaurids. Braincase. Most of the braincase was partially disarticulated from the rest of the skull by weathering, and the right side was prepared out to show relevant details (Fig. 15). Additional features are seen as impressions on the right skull block (Fig. 13B,D). This section describes only visible features. Additional internal details were reconstructed from CT scans and are described in the section on the endocast. With the exception of the sutures between the exoccipital and basioccipital on the occipital condyle, sutures within the braincase are not visible due to crushing, weathering, and fusion. The parasphenoid, represented by an impression, is 28 mm long, gently arched along its length, and tapered to a point at its rostral end (Fig. 13B,D). It terminates just caudal to the midpoint of the orbit. A shallow sulcus occupies the lateral surface of the bone. Faint impressions tentatively identified as presphenoid occur dorsal to the parasphenoid, but no notable details are visible. The form is generally similar to that seen in P. tubicen (NMMNH P-25100, PMU.R1250). A foramen interpreted as that for cranial nerve XII (hypoglossal nerve) is small (1.9 by 2.2 mm) and located roughly midway between the caudal extent of the occipital condyle and a ridge of bone that slants caudodorsally along the braincase (Fig. 15). Additional foramina may have occurred also, as in Hypacrosaurus altispinus (Evans, 2010), but cannot be confirmed in the specimen\u2019s current state of preparation and preservation. A portion of the trigeminal foramen is exposed at the front of the right side of the isolated braincase (Fig. 15), and the remainder of the impression is seen on the right skull block (Fig. 13C,D). This impression is triangular, measuring 11 mm long and 9 mm tall. Two distinct grooves (ridges on the natural mold) extend from the foramen; one trends directly rostrally from the rostral edge of the foramen (probably representing the path for CN V1), and the other trends rostroventrally from the ventral edge (representing the path for CN V2,3). The left caudal semicircular canal is exposed through a fortuitous break (Fig. 10). The maximum diameter of its lumen is 1.8 mm. The occipital condyle is roughly cardoid in caudal view, composed of the basioccipital at the ventral and ventrolateral edges and the exoccipitals at the dorsolateral edges (Fig. 15). All three elements are bulbous on their caudal edges. The rounded basal tuberosity has its maximum lateral extent slightly lateral to the extreme edge of the occipital condyle. In lateral view, the exoccipitals rise to bound the exposed portion of the foramen magnum, sweeping dorsally. The exoccipital and opisthotic are fused both in gross examination and CT scans. The 602 603 604 605 606 607 608 609 610 611 612 613 614 615 616 617 618 619 620 621 622 623 624 625 626 627 628 629 630 631 632 633 634 635 636 637 638 639 640 641 642 643 644 645 646 647 648 649 650 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t most prominent and best-preserved aspect of these elements is the paroccipital process, which curves rostrally and tapers dorsoventrally along the caudal margin of the paroccipital process and upper squamosal (Figs. 7 and 8F,G). The caudal surface of the bones is remarkably flat, with only a slight concavity at its distal extent (Fig. 8F,G). The fenestra vestibuli (fenestra ovalis) measures approximately 5 mm tall by 2.6 mm long. The auditory recess is deepest and narrowest by the fenestra vestibuli, becoming broader and shallower dorsocaudally (Fig. 15). Dentary. The ramus of the left dentary has an average height of 27 mm. The edentulous process is roughly 25 percent of the dentary\u2019s length, and the rostral border of the process is rostroventrally inclined (Fig. 7). The ventral border of the dentary is relatively straight, with comparatively little declination at its rostral portion. This is comparable to the morphology in Parasaurolophus walkeri (Fig. 14F, ROM 768; Evans, 2010), but different from the more inclined morphology in P. tubicen (NMMNH P-25100), a dentary from the Fruitland Formation tentatively identified as juvenile Parasaurolophus sp. (SMP VP-1090; Sullivan and Bennett, 2000), and other lambeosaurines. The condition in P. cyrtocristatus is unknown. The lateral surface of the body of the dentary is strongly convex (Fig. 7). The coronoid process is perpendicular to the ventral margin of the dentary, and, based on CT scans and the incomplete dentary on the right half of the skull (Fig. 13B,D), reaches the ventral margin of the orbit when in articulation, roughly 72 mm above the ventral margin of the dentary. The rostral margin of the coronoid process is more prominently extended than the caudal process. Rostrally, the dentary tapers to articulate with the caudal margin of the predentary. Caudally, the dentary articulates with the surangular along a sinuous suture (Fig. 7). The number of dentary teeth cannot be determined. Predentary. Only the left side of the predentary is preserved (Figs. 7, 8A,B, and 14E), but the element can be mirrored to reconstruct the overall shape. In dorsal view, the element would have been roughly horseshoe-shaped, with a moderately convex rostral margin. As exposed at the midline, the cross-section of the rostral portion is approximately triangular (Fig. 10). The dorsal triturating surface is approximately 14 mm long and only slightly rostrally inclined. This inclination becomes more extreme towards the lateral and caudal wings of the predentary, so that the triturating surface is nearly vertical and laterally facing (14 mm tall) at its caudal end. Thus, the surface only changes its orientation and not its width. The ventral surface of the predentary is gently convex. The caudal edge of the lateral wing of the predentary is forked; the ventral process of this fork is slightly longer and more sharply pointed (Fig. 7). This is in contrast to the unforked lateral wing in the holotype of P. walkeri, ROM 768 (Fig. 14F), but similar to the condition in other lambeosaurines. The morphology is not known in other species of Parasaurolophus. The median process of the predentary is not definitively preserved in RAM 14000. Surangular. The surangular (Figs. 7, 13A,C, and 14E) buttresses the caudal margin of the coronoid process, with a smoothly continuous lateral surface at this point. A ridge at the base of the contribution to the coronoid process continues onto the lateral edge of the articular surface for the quadrate. This coronoid process is also relatively broader than in ROM 768 or NMMNH P25100. The surangular\u2019s ventral margin is slightly convex, with a strong curvature caudally on the articular process. The surangular receives the ventral condyle of the quadrate and articulates with the angular caudomedially. The retroarticular process of the surangular is thinner and more horizontal than in P. walkeri (ROM 768, Fig. 14F). Angular. The angular is a flattened bone that curves caudodorsally and articulates medially with the surangular. On both sides, the element has been displaced downward so that its ventral margins are visible beyond that of the surangular (Figs. 7 and 13A,C). It is inferred to receive the distal end of the quadrate. In ventral view, the element is long and narrow. Hyoid. A bone interpreted as the caudal end of the first ceratobranchial is positioned immediately ventral to the surangular (Figs. 7 and 13A,C); the right first ceratobranchial is 651 652 653 654 655 656 657 658 659 660 661 662 663 664 665 666 667 668 669 670 671 672 673 674 675 676 677 678 679 680 681 682 683 684 685 686 687 688 689 690 691 692 693 694 695 696 697 698 699 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t slightly better preserved than the left. The element is partially exposed, and described from gross examination as well as CT scan reconstructions (Fig. 12B,C). Although the ceratobranchials of hadrosaurids (including Hypacrosaurus sternbergii, adults of Saurolophus osborni, Lambeosaurus lambei, and Corythosaurus casuarius, as well as juveniles of Hypacrosaurus altispinus and H. stebingeri) previously have been described as generally uniform (Ostrom, 1961; Gates et al., 2007; Brink et al., 2011), the morphology of these elements in RAM 14000 has some unique aspects. These differences may be taxonomic or perhaps ontogenetic. However, the hyoids of embryonic H. stebingeri (RTMP 89.79.52) are quite similar to those of Corythosaurus in major details, so we posit that taxonomic differences are most influential here. The articulated preserved portion of each ceratobranchial in RAM 14000 is gently arched ventrally, with a slight dorsoventral curvature. The caudal portion is dorsoventrally flattened (rather than cylindrical, as described for other hadrosaurids; Ostrom, 1961). Rostrally, the bone twists so that it is mediolaterally compressed at the rostral-most preserved portion. This caudal portion is approximately 43 mm long, as preserved. The rostral end of the right first ceratobranchial is within a disarticulated block of matrix; impressions of surrounding elements permit confident placement of the bone. The part that connects with the rest of the ceratobranchial is missing, but the preserved portion in this separate block (including a partial impression) is 37 mm long. The impression is 8 mm tall at narrowest, 14 mm tall at its rostral end, and only 3.5 mm thick mediolaterally. Such extremely expanded rostral ends are typical of known hadrosaurid ceratobranchials (Ostrom, 1961). Including both portions, the total ceratobranchial length was at least 80 mm. The rostral end of the left first ceratobranchial was displaced by erosion (Fig. 10), and is similar in overall morphology to the element on the right. Endocast. A partial cranial endocast for RAM 14000 was reconstructed from CT scan data (Fig. 16, Supplemental Figs. S1 and S2), the first ever for Parasaurolophus of any ontogenetic stage. The endocast was reconstructed in two sections, one on the portion of the braincase articulated with the left half of the skull (Supplemental Fig. S1) and the remainder on the disarticulated portion of the braincase (Supplemental Fig. S2). Their relative position was then approximated based on cranial landmarks and comparison with other hadrosaurids. Because of weathering, many of the smaller neurovascular canals and foramina could not be discerned with confidence. The overall shape of the endocast is broadly similar to that previously described for juvenile and adult lambeosaurines (Evans, 2006; Evans et al., 2009). In dorsal view, the cerebrum is strongly expanded laterally (Fig. 16B), with an estimated width across the midline of 36 mm, dorsoventral height (perpendicular to the aforementioned width) of 28 mm, and an estimated cerebral length of 39 mm. In lateral view (Fig. 16A), the cerebrum is very strongly arched, much more so than in larger juvenile (Lambeosaurus sp., ROM 758; Corythosaurus sp., ROM 759), subadult (Corythosaurus sp., CMN 34825), or adult (Hypacrosaurus altispinus, ROM 702) lambeosaurins. This may in part be due to the young ontogenetic status of RAM 14000, in that the frontals (and hence cerebra) are more strongly arched in young individuals (e.g., Hypacrosaurus stebingeri, MOR 548). An opposite trend in cerebral morphology may occur in Alligator mississippiensis, in that the cerebral region of the endocast is less strongly arched in hatchlings than in adults (e.g., the hatchling OUVC 10606 versus the adult OUVC 9761; AAF, personal observation). The olfactory bulb endocast is a maximum of 14 mm across. As reconstructed, the olfactory bulbs are approximately half the thickness of the cerebrum in lateral view, and are depressed considerably below the cranial roof (frontal, in this case), particularly at their origin (Fig. 16A,B). Angulation between the cerebrum and postcerebral region (equivalent to \u201ccephalic flexure\u201d as measured in endocasts of the ornithopod Dysalotosaurus lettowvorbecki by 700 701 702 703 704 705 706 707 708 709 710 711 712 713 714 715 716 717 718 719 720 721 722 723 724 725 726 727 728 729 730 731 732 733 734 735 736 737 738 739 740 741 742 743 744 745 746 747 748 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Lautenschlager and H\u00fcbner, 2013) cannot be determined with confidence, so any taxonomic or ontogenetic comparisons of this region cannot be conducted. The postcerebral region (a term used here because the cerebellum itself is not well distinguished in hadrosaurid endocasts; Evans, 2006) is much narrower and deeper than the cerebrum (Fig. 16A,B). The ventral margin is broadly rounded in lateral view, contrasting with the straighter margin seen in lambeosaurins (Evans et al., 2009:fig. 7). The dorsal margin of this region, equivalent to the dural peak of Lautenschlager and H\u00fcbner (2013:fig. 2) is much more sharply angled (approximately 90\u00b0) than in larger lambeosaurins (e.g., around 120\u00b0 in subadult Corythosaurus sp., CMN 34825). The angulation (but not the prominence) of the dural peak is mostly unchanged through known ontogenetic stages of the small ornithopod Dysalotosaurus lettowvorbecki (Lautenschlager and H\u00fcbner, 2013), so we hypothesize that phylogenetic differences between lambeosaurins and parasaurolophins explain these differences among hadrosaurids. The endosseous labyrinth is best-preserved on the right side, although not all aspects of the labyrinth could be traced continuously on the CT scan data (Fig. 16C\u2013F and Supplemental Fig. S2). The rostral semicircular canal is only slightly taller than the caudal semicircular canal (when the lateral canal is oriented horizontally; Fig. 16D), a less marked size disparity than seen in ontogenetically older lambeosaurins (Evans et al., 2009: fig. 8). We estimate the maximum breadth of the rostral canal at 11 mm (from ampulla to crus communis), and that for the caudal canal at 10.5 mm (from ampulla to crus communis). Between its bounding ampullae, the lateral semicircular canal spans approximately 9 mm (Fig. 16C). The rostral canal has the tightest arch whereas the caudal canal is broadest, and the lateral semicircular canal is the smallest. The lateral ampulla is the largest of the three. From the foramen vestibuli, cochlea is estimated to be approximately 7.6 mm long. Note that the ventral margins of the cochlea are poorly visible on the CT scans (Fig. 16), and thus this measurement should be considered only an approximation. The endolymphatic duct is not clearly visible. Overall, the morphology of the endosseous labyrinth is broadly similar to that described for other hadrosaurids (e.g., Ostrom, 1961; Evans et al., 2009). Stapes. The left stapes of RAM 14000 is immediately caudal to the quadrate and pterygoid and rostral to the paroccipital-opisthotic process (Fig. 10), consistent with the position in adult Corythosaurus casuarius AMNH 5338 (Colbert and Ostrom, 1958). The proximal end of the stapes is presumed missing, probably due to post-depositional separation of the braincase. The remaining structure suggests that the stapes was a cylindrical, rod-like element. The bone is slightly bent mediolaterally, probably from taphonomic deformation. The maximum preserved length is 12.5 mm, whereas the maximum width is between 0.6 and 0.8 mm (with the widest portion proximally; i.e., towards the braincase), suggesting a slight tapering of the bone laterally (away from the braincase). The distal end of the stapes is positioned 8 mm dorsal to the ventral tip of the paroccipital-opisthotic process. postcranial axial skeleton : Vertebrae. The vertebral column is poorly preserved, with many details obscured by fragmentation of the bones and matrix. Thus, the following description is necessarily incomplete. We are unable to evaluate neurocentral fusion in any vertebrae, although we do note that the sacral ribs are not fused to the sacral vertebrae. Measurements are presented in Table 6. The complete count of cervical vertebrae cannot be determined, because the most caudally placed cervicals are missing (Fig. 13). Individual components of the atlas are unfused and partially exposed (Figs. 13 and 15). The atlas intercentrum, as exposed, is triangular in crosssection, with a sharp ventral keel (Fig. 15). Its caudal, dorsal, and cranial edges are not exposed, so the nature of their articulations is not known. The odontoid (atlas centrum) is partially exposed and globulose, showing a convex cranial margin and a concave caudal margin (Fig. 15). The fragmentary neural arch for the atlas shows no remarkably morphology. An impression of the 749 750 751 752 753 754 755 756 757 758 759 760 761 762 763 764 765 766 767 768 769 770 771 772 773 774 775 776 777 778 779 780 781 782 783 784 785 786 787 788 789 790 791 792 793 794 795 796 797 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t neural spine of the axis (C2; Fig. 13B,D) shows the element to be tall (~26 mm) and elongate (17 mm long at its base). The morphologies of both the atlas and axis broadly agree with those previously described for Gryposaurus incurvimanus (Parks, 1920), although the preservation in RAM 14000 is not sufficient to compare any details, nor has adequate comparative material been illustrated or described for other lambeosaurines. In the cervicals for which a centrum is preserved (?C4-?C7), the centrum is strongly opisthocoelous and sharply pinched in mediolateral cross-section, with a strong ridge on the lateral surface of the centrum (Fig. 13A,C). The dorsal edge of the lamina connecting the zygapophyses is strongly arched, and the diapophyses in the middle of the cervical vertebral series project laterally with a ventral inclination from medial to lateral. The tips of the diapophyses are at approximately the upper half of the centrum. The vertebrae themselves are partly eroded, so little more can be said about their morphology. In both proportions and overall shape, the preserved cervical vertebrae appear similar to comparable elements in the adult P. walkeri ROM 767 (Parks, 1922). The dorsal vertebrae are poorly preserved (Figs. 2, 3, and 13). There were at least 17 dorsal vertebrae (determined by counting the centra, exposed transverse processes, and ribs), but the exact count is unknown. Impressions of the neural spines for three cranial dorsals show the spines to be strongly caudally inclined, mediolaterally compressed, and craniocaudally narrow (Figs. 13B,D and 17A), contrasting with the more robust (craniocaudally elongated) spines in adult lamebosaurines (e.g., P. walkeri, ROM 767; Corythosaurus casuarius, AMNH 5338). The associated transverse spines for these vertebrae are triangular in lateral view and rounded along their lateral extrema (Fig. 13A,C). Centra are visible (but poorly preserved) only for the caudal dorsals; here, the centra are slightly taller than long. The sacrum is neither well exposed nor well-preserved. The fragmentary neural spines are erect and straight (Fig. 3), similar to the condition in adult Parasaurolophus spp. (e.g., FMNH P 27393, ROM 767; AAF personal observation). The caudal vertebrae are best exposed on the left side (Fig. 3) but are poorly preserved. As articulated, the series of caudal centra is gently arched, with an overall ventral concavity along its margin. In contrast with the neural spines of the sacral vertebrae, the preserved neural spines of the cranial caudal vertebrae are distinctly curved. The proximal portion (nearest the neural arch) projects caudally at approximately 45\u00ba and then curves dorsally at its distal two-thirds. Thus, the cranial margin of the neural spine is concave and the caudal margin convex. The neural spines at the cranial end of the tail are quite tall relative to the centra, as is typical for hadrosaurids. Moving distally along the tail, the neural spines lose their curvature by approximately caudal 8. This contrasts with adult P. cyrtocristatus, in which the neural spines maintain their curvature at least through the middle section of the tail (Ostrom, 1963), but is similar to adult P. walkeri (ROM 767). The transverse processes are most pronounced in the cranial caudal vertebrae, becoming successively less prominent distally. By caudal 13 or 14, the transverse processes are gone. A total of 19 centra are visible, and they exhibit the typical hexagonal shape of hadrosaurids. Assuming a typical caudal vertebral count and proportion of the tail for lambeosaurines (see data in Lull and Wright, 1942), just under half of the physical length of the tail is preserved in RAM 14000, and perhaps another 30 to 40 additional vertebrae are missing. Ribs. Cervical ribs are visible on the fourth through seventh cervical vertebrae (Fig. 13A,C). The fourth cervical rib is tripartite, with a rounded capitulum and a tab-like tuberculum of approximately the same size. The shaft of the rib is short and triangular in cross-section, with a distinct flange on its lateral surface. This flange terminates in a discrete knob on the lateral surface of the proximal end of the rib, equidistant between the capitulum and tuberculum. Both the ridge and the knob become less pronounced on the successive two cervical ribs (with C5 and 798 799 800 801 802 803 804 805 806 807 808 809 810 811 812 813 814 815 816 817 818 819 820 821 822 823 824 825 826 827 828 829 830 831 832 833 834 835 836 837 838 839 840 841 842 843 844 845 846 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t C6) and are entirely absent by C7. Similarly, the tuberculum becomes successively less pronounced relative to the capitulum on the ribs associated with C5 and C6. All of the preserved cervical ribs are short, no longer than the centra of their associated vertebrae. In general, the cervical ribs of RAM 14000 are less expanded distally than seen in adult P. walkeri, ROM 768 (Parks, 1922: plate VII, fig. 1). In this specimen, the distal ends are expanded so as to be somewhat paddle-shaped. Thirteen dorsal ribs are preserved with RAM 14000 (Figs. 2 and 13); some of the more caudally placed ribs may be missing or unexposed, which may explain the discrepency from the count of 17 dorsal ribs in adult P. walkeri (Parks, 1922). The first three ribs drastically increase in size successively, and the third rib is the longest by far. The fourth through seventh ribs are approximately the same length, with a drastic, successive decrease in size for the eighth through eleventh dorsal ribs. The twelfth and thirteenth dorsal ribs are approximately the same size. By contrast, the successive elongation of dorsal ribs in adult P. walkeri (ROM 767) continues through the fifth rib, and the successive shortening of dorsal ribs commences at position nine. This may reflect ontogenetic or potentially species-level differences. The preserved portions of the first two ribs in RAM 14000 show that their shafts are quite straight in lateral and cranial view. The third through tenth ribs are straight in lateral view but have a gentle medial concavity. The eleventh through thirteenth ribs are once again straight in lateral and cranial view. As a consequence of the flexion of the dorsal vertebrae, the first through eighth ribs converge upon each other distally. The ninth and tenth ribs are less convergent along their shafts, but appear to be mostly in natural position. The eleventh through thirteenth ribs are slightly disarticulated on the right (up) side, suggesting disturbance from scavengers or water currents prior to burial. The ribs on the left side are too fragmented to evaluate their anatomy. The first and second sacral ribs are visible on the right side (Fig. 2), with the first better exposed. The following description focuses on the first sacral rib. As with the caudal dorsal ribs, this sacral rib is slightly out of articulation. Its proximal end is strongly flared; the capitulum and tuberculum are connected by a thin web of bone. The distal termination of the rib flares slightly relative to the shaft, at approximately 17 mm wide. Both dorsal and ventral borders of the rib are concave, with the dorsal border more strongly so. Measurements for the ribs are presented in Table 7. Haemal arches. The haemal arches are fragmented. Only one cranial arch (perhaps with Ca6?) is sufficiently preserved for description (Fig. 3). This element is exposed along its lateral surface only, and the shaft of the bone is straight. appendicular skeleton : Pectoral girdle. The blades of both scapulae are preserved (Figs. 2 and 3), with the left more complete. Measurements are presented in Table 8. The scapular neck has a distinct constriction cranially, typical of lambeosaurines. However, the caudal expansion of the blade is less pronounced than in adult Parasaurolophus (FMNH P 27393, ROM 768). Overall, the scapula is more robust than seen in Corythosaurus, Lambeosaurus, or Nipponosaurus (Suzuki et al., 2004). The preserved ventral border of the left scapula is entirely intact in RAM 14000, whereas the dorsal border is less complete. Only the ventral border is intact on the right side; here, it is slightly sinuous, with a distinct constriction at the cranial third of the element. No sternal elements are preserved. Pelvic girdle. The pubes are somewhat fragmented, but the general shape of the prepubic process (pubic blade) is intact (Figs. 2 and 3). The cranial end is dorsoventrally expanded (as is typical of lambeosaurines), with the ventral margin slightly more extended cranially than the dorsal margin. The blade narrows caudally. A short segment of the postpubic rod is exposed (Fig. 2), showing that this was a thin process with morphology typical of lambeosaurines. 847 848 849 850 851 852 853 854 855 856 857 858 859 860 861 862 863 864 865 866 867 868 869 870 871 872 873 874 875 876 877 878 879 881 882 883 884 885 886 887 888 889 890 891 892 893 894 895 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t The right ischium is represented by bone proximally and by impressions distally (Fig. 3). The dorsal acetabular process is longer and broader than the ventral, as seen in other hadrosaurids. The impression of the shaft is comparatively straight, showing that the shaft expands dorsoventrally towards its distal end. Unlike adult-sized Parasaurolophus cyrtocristatus (FMNH P 27393), the distal extremity of the ischium is not prominently hooked cranially. At most, there was only a slight expansion. A similar expansion of the distal hook during ontogeny occurs in Hypacrosaurus stebingeri (Horner and Currie, 1994), but in this taxon the hook develops at a comparatively smaller body size than that of RAM 14000. The ilium is well-preserved, particularly on the right side (Figs. 2, 18B, and 19D), but only the lateral surface is exposed. The caudal end is tapered, rather than tab-like and rounded as seen in P. cyrtocristatus (Fig. 19C) or P. walkeri. Little ontogenetic change in the shape of the caudal end is evident in Hypacrosaurus stebingeri (Horner and Currie, 1994), so this may be due to taxonomic differences or individual variation. The lateral surface of the postacetabular process is slightly concave and strongly sloped laterally, so that the ventral edge is more laterally placed than the dorsal edge. The ventral edge of the postacetabular process is slightly concave, but the dorsal margin of the blade is nearly straight, up to the preacetabular blade. This contrasts with the prominent concavity seen dorsal to the supraacetabular process in other Parasaurolophus (FMNH P 27393, Fig. 19C; ROM 768); development of the concavity seems to be an ontogenetic feature, more strongly pronounced in adults than juveniles (Guenther, 2009: fig. 9). The preacetabular blade is longer and more slender than the postacetabular blade, narrowing towards the cranial-most tip. The ventral edge of the preacetabular blade is broadly sinuous. Compared to adult Parasaurolophus, the preacetabular process is relatively shorter (Fig. 19C,D). The supraacetabular process protrudes laterally and is proportionately smaller than seen in adult Parasaurolophus (Fig. 19C,D). This too is a general ontogenetic trend across hadrosaurids (Guenther, 2009). The pubic peduncle has a gentle cranial slant and is more robust and better defined than the smoothly curved ischiadic peduncle. In between the peduncles the concavity of the acetabulum is shallow and hemielliptical in profile. Measurements for the pelvic girdle are presented in Table 8. Forelimb. The forelimbs are entirely missing, with the exception of an impression of the medial surface of the right humerus (maximum length=175 mm; Figs. 18A and 19B; Supplemental Fig. S4). The deltopectoral crest extends for more than half the length of the humerus (101 mm), with a slight inward curvature at the crest\u2019s midpoint. Compared to adult Parasaurolophus (e.g., P. cyrtocristatus, FMNH P 27393, Fig. 19A; P. walkeri, ROM 768), the overall form of the humerus in RAM 14000 is less sigmoidal and more slender (Fig. 19B), with a less prominent (but just as long) deltopectoral crest. This contrasts with Hypacrosaurus stebingeri, in which the humerus was reported to be \u201crelatively stout\u201d in juveniles versus larger specimens (Horner and Currie, 1994), and with negative allometry reported for the circumference of the midshaft of the humerus regressed upon the length of the humerus in Maiasaura peeblesorum (Dilkes, 2001; Kilbourne and Makovicky, 2010; note that the results are identical but presented differently in the two studies). Thus, RAM 14000 may suggest that Parasaurolophus departs from the expected allometric pattern for hadrosaurids. However, the specimen\u2019s slender appearance could be misleading if it only preserves a portion of the bone\u2019s profile. More specimens are needed to evaluate this hypothesis. The lateral distal condyle is more prominent than the medial condyle, but this is at least in part preservational. Measurements are presented in Table 9. Hind limb. The right femur is mostly exposed, although its caudomedial surface and parts of the distal condyles are partially obscured by rock (Figs. 2, 18C, and 19F; Supplemental Fig. S5). The head and greater trochanter are separated by a broad, v-shaped sulcus. The greater trochanter is prominent, with a flattened lateral surface and a broadly and convexly arched dorsal 896 897 898 899 900 901 902 903 904 905 906 907 908 909 910 911 912 913 914 915 916 917 918 919 920 921 922 923 924 925 926 927 928 929 930 931 932 933 934 935 936 937 938 939 940 941 942 943 944 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t (proximal) margin in lateral view (Fig. 18C). The cranial trochanter extends for approximately one-fourth the length of the femur; this structure is a low and narrow process situated at the craniolateral surface of the greater trochanter. The shaft of the femur is straight, with the fourth trochanter centered at mid-shaft. The trochanter is clearly defined but relatively less prominent in terms of length and height than in adult lambeosaurines (e.g., P. cyrtocristatus, FMNH P 27393, Fig. 19E; P. walkeri, ROM 768). The medial and lateral distal condyles are not well-separated on their cranial surfaces, although a shallow depression occurs at the midline just dorsal to the condyles. The tibia is a robust bone, approximately equal in length to the femur (Figs. 2 and 18D; Supplemental Fig. S5). The cnemial crest is prominent, extending for at least a third of the tibial shaft. The crest is hooked laterally, wrapping around the cranial surface of the fibula at its proximal end. The proximal third of the crest is most robust and situated farthest from the main portion of the tibia, with the rest of the crest tapering gently towards the main shaft of the tibia. The distal end of the tibia is flattened caudally with a craniocaudal expansion relative to the midshaft in lateral view. A distinct ridge occurs on the caudo-lateral aspect of the distal quarter of the tibia. The proximal half of the shaft is gently concave in lateral view. The fibula (Figs. 2, 18D, and 19H; Supplemental Fig. S5), as is typical for hadrosaurids, is a slender bone that tapers distally. It is strongly mediolaterally compressed, particularly at the proximal half. The proximal articular end has a fairly linear profile in comparison to larger hadrosaurids, and the caudal edge of the shaft is also quite straight. The cranial edge is gently and broadly curved, particularly at the distal half. The distal end of the fibula is gently expanded and slightly hooked cranially, articulating tightly with the calcaneum. Overall, the element is less robust and has a less prominent distal curvature than seen in larger Parasaurolophus (e.g., FMNH P 27393, Fig. 19G). The calcaneum is articulated with the fibula, but only the lateral surface is exposed (Figs. 2 and 18D). It is slightly concave and has a kidney-shaped outline, with the convex end pointing distally. A small but bulbous lump of bone interposed between the distal articular surfaces of the calcaneum and astragalus may represent tarsal IV. The astragalus is insufficiently exposed to comment upon its morphology. The right pes is poorly exposed, and only digits III and IV are represented (Figs. 2, 3, and 20). Digit IV conforms to the standard hadrosaurid phalangeal count of five phalanges. The first phalanx (IV-1) is longest, and following three (IV-2, IV-3, and IV-4) are considerably shorter proximo-distally. The terminal phalanx (IV-5) is expanded into a triangular ungual. Digit III has a similar pattern (Fig. 20), with the most proximal phalanx (III-1) being longest, the next two (III-2 and III-3; Fig. 20A,B,D,E) quite abbreviated proximo-distally, and a terminal ungual (III-4). Each phalanx after the most proximal one is broader than long. The unguals in RAM 14000 are fairly narrow (Fig. 20C,F), lacking the broader expansion of adults. Measurements for the hind limb elements are presented in Table 9. ossified tendons : Ossified tendons or their impressions are visible at only two portions of the skeleton. The first set occurs lateral and ventral to the neural spine of the ?fourth dorsal vertebra (Fig. 17A). Two tendons are preserved here, both of which roughly parallel the long axis of the vertebral column. They are approximately 0.8 mm in maximum diameter, and the longest preserved segment is 21 mm long (including an impression of the tendon in the measurement. Both tendons occur on the lateral surface of the caudal quarter of the neural spine and just dorsal to the transverse process, and trend very slightly ventrally. The longest preserved one extends at least to the cranial quarter of the next spinous process. Based on the position and orientation of these tendons, we hypothesize that they represent portions of M. iliocostalis or potentially M. 945 946 947 948 949 950 951 952 953 954 955 956 957 958 959 960 961 962 963 964 965 966 967 968 969 970 971 972 973 974 975 976 977 978 979 980 981 982 983 984 985 986 987 988 989 990 991 992 993 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t longissimus dorsi (Organ, 2006). A second set of ossified tendons, represented only by impressions, occurs ventral to the margins of the impressions of the neural spines of vertebrae and dorsal to the fragments of the transverse processes on the left side (Fig. 17B). The tendons themselves were destroyed by weathering prior to discovery. The exact position of the tendons in the vertebral column cannot be determined, but the tendons lie just dorsal to the cranial end of the ilium and thus at the very caudal end of the dorsal vertebrae or cranial end of the sacral vertebrae. At least seven parallel tendons occur here, with a maximum diameter of each impression 2.0\u20132.5 mm and the longest impression with a preserved length of at least 55 mm (and probably longer). The tendons were lateral to the neural spines, moving dorsally towards the caudal direction (i.e., caudodorsally inclined). Based on the position and orientation of these impressions, we hypothesize that they represent tendons of M. tendinoarticularis within M. transversospinalis (Organ, 2006). integument : Soft (non-bone) tissue impressions are preserved around the left foot and rostral end of the skull. Despite careful mechanical preparation with an aim to identify other areas of soft tissue preservation, no additional, unambiguous impressions were identified. Upper rhamphotheca. A series of parallel, dorsoventrally oriented grooves rostral and ventral to the oral margin of the premaxilla (Fig. 8A,B,E) are interpreted as impressions of the internal surface of the upper rhamphotheca, in light of similarly interpreted anatomy in other hadrosaurids (Morris, 1970). From the inferred midline, a total of eight grooves are preserved (Fig. 8E); they may have extended farther laterally. Each groove is 2.5\u20133.5 mm wide. In rostral view, the ventral edge of the series dips ventrally from medial to lateral. This suggests a broad, inverted \u201cV\u201d profile for the complete series when including both left and right sides of the skull (Fig. 6C). The greatest mediolateral width of the series is 38 mm. The greatest preserved dorsoventral depth of the preserved flutes is 16 mm, but their proximal and lateral portions were inadvertently prepared away. Thus, the distance between the oral margin of the premaxilla and the distal extremity of the rhamphotheca averaged around 25 mm. These impressions indicate that the soft-tissue profile of the oral margin extended significantly beyond the bone (Fig. 7A). This is consistent with previous reports of an internally fluted beak that extended well beyond the premaxilla in Edmontosaurus annectens (Versluys, 1923; Morris, 1970). The margins of the premaxilla and impressions are closely parallel in E. annectens, indicating that bone shape is a fairly accurate proxy for soft tissue shape. We hypothesize a similar pattern for Parasaurolophus based on RAM 14000. A specimen of Corythosaurus casuarius (CMN 8676) originally preserved a portion of the impressions of the rhamphotheca (Sternberg, 1935). Initially interpreted as the lower rhamphotheca (Ostrom, 1961), we agree with later interpretations of the structure as the upper rhamphotheca (Morris, 1970). Only a fragment of this impression is now available. Based on the original photographs (Sternberg, 1935), the internal surface of the upper rhamphotheca was grooved as in RAM 14000. However, we cannot determine with confidence the shape of the margin of the rhamphotheca in CMN 8676 for comparison. Although such features are not evident in RAM 14000, projections from the oral margin of the premaxilla in many hadrosaurids may correlate with the grooves on the rhamphotheca. Additional work is needed to verify this. Skin impressions. Two small (<5 cm maximum dimension) patches of skin impressions are associated with the region caudal to the right metatarsal III and phalanx III-1 (Figs. 3 and 21). This impression is gently folded upon itself, and covered by non-imbricating, roughly circular tubercles that average ~2 mm in maximum diameter (Fig. 3; pebble-type basement scales of Bell, 2012). The impression was exposed to weathering prior to discovery, and thus surface detail is muted. The overall appearance, including the folding, is reminiscent of the equivalent region in 994 995 996 997 998 999 1000 1001 1002 1003 1004 1005 1006 1007 1008 1009 1010 1011 1012 1013 1014 1015 1016 1017 1018 1019 1020 1021 1022 1023 1024 1025 1026 1027 1028 1029 1030 1031 1032 1033 1034 1035 1036 1037 1038 1039 1040 1041 1042 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Corythosaurus casuarius (AMNH 5240; Brown, 1916). The only major difference in RAM 14000 concerns the smaller tubercles relative to AMNH 5240, which are undoubtedly related to the animal\u2019s small body size. bone histology : We describe the histology of the tibia based on two samples from the caudolateral quadrant of the proximal shaft, close to the mid-diaphysis (see Fig. 18D for positions). We follow the terminology of Francillon-Vieillot et al. (1990), with additional terminology related to the orientation and arrangement of osteocytes following Werning (2012). Section B (Figs. 22 and 23) lies closer to the mid-diaphysis. The section is ~15\u201316 mm thick (= radially \u201cdeep\u201d) including the cortical and cancellous bone. The cancellous region comprises the inner 3\u20137 mm of the sample. A good deal of fracturing is visible throughout the section. In the cancellous region, the cracks are infilled by crystals and/or a dark, amorphous matrix, but in the cortex, many of the cracks lack infilling. It is possible that these cortical cracks formed during extraction from the ground or extraction of the sample for histological preparation. Crystals and the black matrix also infill the interstices between trabecular and the canals of the cortex. The bone is strongly birefringent, but shows a negative optical sign when viewed under elliptically polarized light (e.g., Fig. 25). This suggests that the collagen has been secondarily replaced by apatite crystals (Lee and O\u2019Connor, 2013). The internalmost portion of the cancellous region (Figs. 22A and 23A) shows thick trabeculae that delineate large (up to 1 mm) amorphous intertrabecular chambers. The cores of the largest trabeculae are comprised of woven or parallel-fibered primary bone and the edges are lined with several lamellae (true lamellar bone) or pseudolamellae (loose layers of parallelfibered bone). The lamellae do not appear to cut across the cores; rather, they appear to have been deposited appositionally to them. The osteocyte density is much higher in the trabecular cores than in the lamellar/pseudolamellar bone lining the trabecular margins; in fact, they appear as densely packed as they are in the primary woven bone that forms the internalmost cortex. These osteocytes are aligned along the long axis of each trabecula and change orientation as trabecular orientation changes. This strongly suggests that at least some of these trabeculae formed de novo rather than by resorption of primary cortical tissues; if this is correct, these are remnants of embryonic or perinatal bone tissue and the intertrabecular chambers. The appearance of the trabeculae in this region is extremely similar to that described for embryonic ornithopods, including those of Maiasaura (Horner et al., 2000, 2001), Hypacrosaurus (Horner and Currie, 1994; Horner et al., 2001), Dryosaurus (Horner et al., 2009) and Tenontosaurus (Horner et al., 2009; Werning, 2012). Given the tibial diameter of ~40 mm in RAM 14000, and that this region comprises no more than 3.5 mm of the preserved section (i.e., there is 11.5\u201312.5 mm of cortical bone external to it), the neonatal tibial diameter could not have exceeded 15\u201317 mm (47\u201353 mm circumference). This is very close in size to the embryonic femora of Hypacrosaurus (32.5\u201340 mm circumference; Horner and Currie, 1994). Other, incipient cancellous bone is visible just external to the preserved embryonic tissues (Fig. 23B). Contrary to the cancellous bone described above, this tissue is not as porous and clearly formed by the resorption of primary cortical tissues. In this region, the cores of the incipient trabeculae comprise primary woven bone, but the orientations of primary osteons and osteocytes do not correspond with trabecular orientation. Erosion rooms ranging in size from .1\u20132 mm cut across primary bone tissue, and many are unlined. Where lamellar bone lines the resorption rooms, it cuts across the primary tissues forming the cores of the incipient trabeculae. The cortex near the mid-diaphysis is comprised mainly of well-vascularized, woven primary bone tissue. In the inner cortex (Fig. 23C), the bone is exclusively woven and the canals are a mixture of primary osteons and simple primary canals. The canals of this region are mainly 1043 1044 1045 1046 1047 1048 1049 1050 1051 1052 1053 1054 1055 1056 1057 1058 1059 1060 1061 1062 1063 1064 1065 1066 1067 1068 1069 1070 1071 1072 1073 1074 1075 1076 1077 1078 1079 1080 1081 1082 1083 1084 1085 1086 1087 1088 1089 1090 1091 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t longitudinal, but short radial, circumferential, and oblique canals are also common. The canals in this region are not as organized as the mid- or outer cortex and generally anastomose with several (two to four) other canals. Osteocyte density in this region is extremely high, and osteocytes show no preferred orientation relative to the long axis of the bone nor a preferred arrangement relative to each other. Osteocytes encircle some primary osteons, but equally often, they are oriented oblique to the canals in the tissue that surround them. In the regions closest to the canals, the bone is less cellular compared to the cores of the laminae/interstices between them. In the mid- and outer cortex (Fig. 23D), the bone is similar in its components but shows more organization in its vascular canals and in its osteocytes. Vascular canals are again a mix of primary osteons and simple primary canals, which are generally wider in diameter compared to those of the inner cortex. As noted by Starck and Chinsamy (2002), this reflects the ontogeny of the canals themselves; the inner canals are older and have had more time to deposit bone since the initial bone scaffolding was deposited. Canals in this region show strong circumferential signal; in the mid-cortex, circumferential canals dominate, and in the outer cortex, the longitudinal canals are arranged circumferentially in rows. Osteocyte density is lower in the outer cortex compared to the inner cortex. Additionally, the disorganization is confined to a slightly narrower region at the center of each lamina. In the outermost cortex, the canals are often encircled by a thin band of fairly acellular bone (Fig. 23D). In some cases, it appears that a region of parallel-fibered bone, less dense in osteocytes, separates the acellular lining bone from the \u201ccore\u201d of woven bone at the center of each lamina. Despite histological indications that bone deposition rate was slightly lower in the outer cortex compared to the inner cortex, no annuli or lines of arrested growth (LAGs) are visible in this section. Section A (Figs. 24\u201326) is taken from a more proximal portion of the diaphysis. The section is ~11\u201312 mm thick (deep), including the cortical and cancellous bone. The cancellous region comprises only the inner ~2.5 mm of the sample. The section sampled in longitudinal section runs proximally along the shaft for 12 mm from the site of the cross-sectional sample. In cross-section (Fig. 24), section A resembles section B in its vascular patterning. It differs in the degree of organization of the primary cortical tissues (Figs. 24C and 25), in the secondary remodeling of the inner cortex (Fig. 24D), and in its thicker and more closely spaced trabeculae. As in Section B, the trabeculae show no secondary osteons in their cores. The edges of all trabeculae are lined with distinct lamellae, often five or more in number. Some of these trabeculae clearly formed by resorption and secondary deposition; the lamellae on one side of a trabecula often cut through the lamellae on the other side. Although a few larger erosion rooms are present, most are between .1 and .5 mm in diameter. The inner cortex was clearly experiencing active secondary remodeling at the time of the animal\u2019s death. Distinct resorption rooms of varying age (based on number of lamellae) are visible throughout the innermost cortex; these may be up to .15 mm wide. Several generations of secondary osteons are also visible (Fig. 24D). Although some primary tissue is clearly visible between secondary osteons, they cut across each other in places. The primary cortical tissues increase in organization moving periosteally through the section (Fig. 25). As in section B, the inner cortex of Section A (Fig. 25A,B) shows highly disorganized bone tissue. The interstices between vascular canals (nearly all are randomly arranged longitudinal primary osteons) form laminae mainly comprised of woven bone that shows a high density of randomly oriented osteocytes. Parallel-fibered bone or, more often, lamellar bone encircles the canals themselves. This is also cellular, but not to the extent of that in the interstices. The boundary between the woven bone and lamellar bone is distinct. This bone is clearly \u201cfibro-lamellar tissue\u201d as defined by Francillon-Vieillot et al. (1990). In the mid-cortex (Fig. 25C,D), the bone is more laminar, because the primary osteons anastomose circumferentially with adjacent canals. Here, the woven \u201ccores\u201d of the interstitial 1092 1093 1094 1095 1096 1097 1098 1099 1100 1101 1102 1103 1104 1105 1106 1107 1108 1109 1110 1111 1112 1113 1114 1115 1116 1117 1118 1119 1120 1121 1122 1123 1124 1125 1126 1127 1128 1129 1130 1131 1132 1133 1134 1135 1136 1137 1138 1139 1140 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t bone have fewer osteocytes, but the ones that are present are equally disorganized. The bone encircling the primary osteons is exclusively lamellar and less cellular than in the inner cortex. Very thin bands of parallel-fibered bone lie between the woven component and the lamellar component surrounding the canals. Thus, the woven component grades into the lamellar component and the boundary between interstitial and circumvascular bone tissue is not as abrupt. In the outer cortex (Fig. 25E,F), woven bone is restricted to the center of the interstitial \u201ccores\u201d and much more parallel-fibered bone separates the woven component from the lamellar component. In this region, far fewer osteocytes occur in either the interstices or the lamellar bone of the primary osteons. The same pattern is also evident in longitudinal section (Fig. 26). Stein and Prondvai (2013) describe a similar condition in the long bones of the sauropods Alamosaurus, Apatosaurus, and Camarasaurus. In these taxa, woven bone is restricted to a thin splint at the center of bony laminae, and highly organized parallel-fibered and lamellar bone fills the space between the woven splint and the vascular canals. This reflects the process of bone deposition; a scaffold of woven bone is deposited rapidly around vascular canals so that the diameter of the bone can be rapidly expanded. Subsequently, more organized tissues are deposited onto this scaffold (Stein and Prondvai, 2013). body size and completeness : Aside from RAM 14000, the most complete and smallest associated juvenile lambeosaurine skeleton is AMNH 5340, referable to Lambeosaurus sp. (Evans, 2010). This individual had a total length of 4.31 m (Lull and Wright, 1942), and comparable-sized postcranial elements are 1.74 to 1.89 times the length of those in RAM 14000 (Table 10; ischium length is excluded as an outlier). Scaling from AMNH 5340, we estimate total body length in RAM 14000 conservatively at 2.28 to 2.48 m, considerably smaller than the 9.45 m total body length estimated for the holotype of Parasaurolophus walkeri, ROM 768 (Lull and Wright, 1942). Associated cranial bones from the Kirtland Formation of New Mexico, SMP VP-1090, were tentatively identified as a juvenile Parasaurolophus sp. (Sullivan and Bennett, 2000). The quadrate in this specimen is 185 mm long, 67 percent larger than the quadrate in RAM 14000 (111 mm long). A braincase assigned to juvenile Parasaurolophus sp. from the Dinosaur Provincial Park region of Alberta, CMN 8502, has a frontal width of 38 mm, 20 percent larger than the equivalent dimension in RAM 14000 (31.7 mm). By contrast, the skull length (horizontal from rostrum to paroccipital process) in the P. walkeri holotype (ROM 768) is 745 mm versus 246 mm in RAM 14000, or 303 percent larger. Thus, RAM 14000 represents the smallest confidently identifiable specimen of Parasaurolophus known to date. In terms of skeletal representation, RAM 14000 is the most complete single individual of Parasaurolophus described to date (Supplemental Table S1). Approximately 46 percent of skeletal elements are preserved here, contrasting with 43 percent in the holotype of P. walkeri (ROM 768) and 35 percent in the holotype of P. cyrtocristatus (FMNH P 27393). crest acoustics : Following the methods of Weishampel (1981a), we estimated the resonant frequencies of the main passageway of the nasal cavity for RAM 14000. Because the lateral diverticulum is poorly separated from the rest of the nasal passages and is not close-ended in RAM 14000, we did not calculate its corresponding resonant frequency. Necessary parameters to calculate f (frequency, in Hz) included n (resonance mode, set between 1 and 5), v (velocity of sound at sea level, 340 m/s), and L (length of tube, set at 0.195 m for RAM 14000 as measured from CT scan data). These parameters were entered into the following equation: f = n(v/2L) Results are summarized in Table 11. The estimated resonant nasal frequencies of RAM 1141 1142 1143 1144 1145 1146 1147 1148 1149 1150 1151 1152 1153 1154 1155 1156 1157 1158 1159 1160 1161 1162 1163 1164 1165 1166 1167 1168 1169 1170 1171 1172 1173 1174 1175 1176 1177 1178 1179 1180 1181 1182 1183 1184 1185 1186 1187 1188 1189 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t 14000 are approximately 11 to 18 times higher than those for P. cyrtocristatus and P. walkeri, respectively, as expected given the difference in cavity lengths. mandibular mechanics : Most discussions of hadrosaurid jaw mechanics have focused, directly or indirectly, on the dental occlusal surfaces and movements associated with that complex (e.g., Ostrom, 1961; Weishampel, 1983; Erickson et al., 2012), but no detailed consideration has been given to the potential mechanical consequences of the premaxillary \u201cbeak\u201d. Adding a keratinous rhamphotheca increases the minimum gape at which contact between upper and lower jaws is made with a food item, with corresponding effects upon bite force. As in previous studies (e.g., Ostrom, 1964; Bell et al., 2009), the ornithischian lower jaw can most simply be approximated as a third class lever, with the applied muscle force located between the fulcrum (glenoid) and the resistance (usually the dentition, but in this case the predentary). Here, the force lever arm is the distance between the coronoid process and glenoid, whereas the resistance lever arm is the distance from bite point to glenoid (following Ostrom, 1964). In order to calculate usable force at a given point on the mandible, five parameters are needed (see Ostrom, 1964, for a full explanation): e, distance from the center of the coronoid process to the bite point; a, distance from the center of the glenoid to the center of the coronoid process; d, distance from the glenoid to the top of the coronoid process; \u03b8, the angle between the line of the jaw and the applied force on the coronoid process (measured from the center of the supratemporal fenestra); and \u03b4, the angle of the diagonal between the top of the coronoid and the glenoid, relative to the line of the jaw (Fig. 27). All of the parameters are then entered into the equation: S (e + a) = F sin (\u03b8 + \u03b4) d where S is the percentage of usable force at a given point relative to the input force F. All variables are the same in all conditions, except for \u03b8. When accounting for increased gape due to the rhamphotheca, \u03b8 is accordingly reduced (Fig. 27B). Thus, at a gape of 10\u00b0, \u03b8-10\u00b0 would be used as the appropriate value. Here, we make the simplification that F is constant across the relatively small differences in gape considered here. Based on measurements from the original specimen, the rhamphotheca in RAM 14000 decreased the angle of gape at which upper and lower beaks contacted by approximately 7\u00b0. Thus, \u03b8=44\u00b0 without a rhamphotheca and \u03b8=37\u00b0 when the rhamphotheca is included. For other parameters, e=150 mm (measured to rostral-most extent of predentary), a=48 mm, d=80 mm, and \u03b4=42\u00b0. Because absolute values are not a concern, F was set at 100%. Using the above numbers and equation, the percentage of usable force at the predentary is 40.3% without the rhamphotheca and 39.6% with the rhamphotheca. Thus, the rhamphotheca introduced a 0.7% decrease in bite force relative to the condition without. age of ram 14000 : The tibial bone microstructure of RAM 14000 preserves no lines of arrested growth (LAGs) or annuli, suggesting that this animal did not stop, pause, or dramatically slow its growth at any time between hatching and death. As noted in Nesbitt et al. (2013), the absence of LAGs does not necessarily imply that an animal died within its first year of growth, although that is one possibility. LAGs are not visible when they are deposited but later obscured by secondary remodeling, in animals that grow to full size in less than a year but live for several years afterward, or in animals that grow to full size over several years without pausing or stopping (Horner et al., 1999; Nesbitt et al., 2013). Secondary remodeling of primary tissues that once preserved LAGs can be eliminated for RAM 14000. Near the mid-diaphysis (section B; Fig. 22), bone tissue strongly resembles that of embryonic and perinatal ornithopods (e.g., Horner and Currie, 1994; Horner et al., 2000, 2001, 2009; Werning, 2012). This region extends to a radius consistent with the size of other perinatal lambeosaurines (Horner and Currie, 1994; Horner et al., 2000). This possible embryonic/perinatal tissue is not remodeled by secondary osteons, nor is any of the tissue external to it. Because of this, we are confident that the section represents an unobscured record of growth from a time near birth to death and that no LAGs are missing. We also find it unlikely that RAM 14000 lacks LAGs because Parasaurolophus finished growth in less than a year. All four of the other hadrosaurids that have been examined histologically [Telmatosaurus (Benton et al., 2010), Maiasaura (Horner et al., 2000, 2001), Hypacrosaurus (Horner and Currie, 1994; Horner et al., 1999; Cooper et al., 2008), and Edmontosaurus (Reid, 1985)] exhibit several LAGs in the cortices of adult limb bones. Because LAGs are deposited annually in vertebrates (Castanet, 1985, 1986\u20131987; Castanet and Naulleau, 1985; Francillon-Vieillot et al., 1990), this suggests that hadrosaurids required more than one year to reach full size. The presence of several cortical LAGs in related taxa also suggests that large hadrosaurids did not grow over several years without stopping, though in the absence of samples from subadult or adult specimens, this possibility cannot be excluded for Parasaurolophus. The histology of RAM 14000 excludes some broader age categories. The section studied here preserves some possible embryonic or perinatal tissues, but it has clearly deposited a significant amount of tissue external to these. Most of this tissue is mature enough to show primary osteons, indicating that some time has passed since deposition of the initial woven \u201cscaffolding\u201d (Stein and Prondvai, 2013). Additionally, more organized bone microstructure and a larger parallel-fibered component of the bony laminae suggests slower bone depositional rates in the outer cortex relative to the inner cortex of RAM 14000 (Stein and Prondvai, 2013). Embryos, perinates, and very young juvenile hadrosaurids exhibit only woven bone (Horner and Currie, 1994; Horner et al., 2000), so RAM 14000 does not likely belong to these age categories. Despite relative slowing of growth between the inner and outer regions of the cortex, RAM 14000 was still growing actively at the time of death. It does not exhibit the LAGs or 1336 1337 1338 1339 1340 1341 1342 1343 1344 1345 1346 1347 1348 1349 1350 1351 1352 1353 1354 1355 1356 1357 1358 1359 1360 1361 1362 1363 1364 1365 1366 1367 1368 1369 1370 1371 1372 1373 1374 1375 1376 1377 1378 1379 1380 1381 1382 1383 1384 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t secondary remodeling of the mid-diaphyseal cortex of subadult or adult hadrosaurids (Horner et al., 1999, 2000, 2001), and certainly not the external fundamental system observed in senescent, large-bodied archosaurs (e.g., Woodward et al., 2011). Therefore, we feel it is also unlikely that RAM 14000 is a subadult or senescent individual. Given that RAM 14000 is not likely a perinate or a subadult, we hypothesize it to be a large juvenile. The only published histological section sampled from the long bones of a juvenile lambeosaurine is from the femur of MOR 548, a Hypacrosaurus stebingeri nestling. This material was described briefly by Horner and Currie (1994) and is currently being redescribed by Horner and his students as part of a larger study of Hypacrosaurus growth and ontogeny (John R. Horner, personal communication to SW, 2013). The femur of MOR 548 is approximately 23 cm long (~2.5 cm diameter; John R. Horner, personal communication to SW, 2013); smaller than RAM 14000 (325 mm). As reported in Horner and Currie (1994), much of the cortex comprises woven bone organized around primary vascular canals. The published image shows a looser compacta relative to RAM 14000, but images of the full cross-section show a great deal of similarity in terms of the organization and patterning of primary osteons and compactness of the bone in the outer cortex (John R. Horner, personal communication to SW, 2013). No LAGs were reported for MOR 548 (Horner and Currie, 1994). The bone microstructure of an ontogenetic series of the saurolophine Maiasaura has also been described (Horner et al., 2000). RAM 14000 is intermediate in size between the Maiasaura juveniles YPM-PU-22472 and MOR-005JV in size (18 cm and 50 cm femur length, respectively; Horner et al., 2000) and compares well histologically to Maiasaura juveniles in most respects. Horner and colleagues note primary osteons with distinct/organized lamellae surrounding the vessels. These primary canals are most commonly longitudinal canals arranged in parallel circumferential rows, but also in laminar and even plexiform patterns. LAGs are rare in juveniles, despite being \u201canimals of considerable size\u201d (Horner et al., 2000: p. 119), although a LAG occurs in some elements of MOR-005JV (ibid.). RAM 14000 differs from Maiasaura juveniles in that it does not exhibit secondary osteons at the mid-diaphysis, though they occur in the more proximal section. Given that RAM 14000 was clearly still growing at the time of its death, and that the skeletal morphology and bone microstructure are similar to juveniles of other hadrosaurids, we hypothesize that RAM 14000 was a large juvenile. Cooper et al. (2008) estimated growth curves for Hypacrosaurus based on LAG circumferences throughout the ontogeny of MOR 549, an adult. Using their models, we reconstruct an age of ~1 year for juveniles the size of MOR 548, though again, no LAGs were reported by Horner and Currie (1994). A single LAG was reported in some elements of MOR-005JV (Horner et al., 2000), a juvenile Maiasaura that showed similar histology to RAM 14000. Because no LAGs occur in the similarly sized RAM 14000, we tentatively suggest that the animal was under a year of age at the time of death. However, we note that the number of hadrosaurids with good ontogenetic sampling is still very low (only Maiasaura and Hypacrosaurus), and so our estimate will need revision if future studies show that hadrosaurids sustained uninterrupted high growth rates for longer than the first year of growth. If our estimates of age and size for RAM 14000 are correct, Parasaurolophus must have experienced extremely rapid growth rates. Our results suggest that RAM 14000 reached 25\u201332% of adult size (based on total body length length and skull length, respectively) in less than a year. Growth curves based on estimates of circumference and mass (as derived from circumference), have been modeled for Hypacrosaurus (Cooper et al., 2008) and Maiasaura (Erickson et al., 2001) Because we lack histological samples from any adult Parasaurolophus specimens, we cannot construct growth curves directly comparable to those estimated for Hypacrosaurus and Maiasaura. However, our estimates of growth (25\u201332% of adult size in less than a year) are reasonable based on the ontogeny of femoral length reconstructed for both Maiasaura and 1385 1386 1387 1388 1389 1390 1391 1392 1393 1394 1395 1396 1397 1398 1399 1400 1401 1402 1403 1404 1405 1406 1407 1408 1409 1410 1411 1412 1413 1414 1415 1416 1417 1418 1419 1420 1421 1422 1423 1424 1425 1426 1427 1428 1429 1430 1431 1432 1433 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Hypacrosaurus. MOR-005JV, a juvenile Maiasaura, was estimated to be one year old at time of death by Erickson and colleagues (2001). That individual had a femoral length half that of MOR-005A (50 cm vs. 100 cm; Horner et al., 2000), an adult specimen estimated to be six years old at time of death (Erickson et al., 2001). MOR 548, a juvenile Hypacrosaurus approximately 1 year old (see above) had a femur of 23 cm, whereas the adult MOR 549 had a femur 102 cm long (Horner et al., 1999). In light of similarly rapid first-year growth in these other hadrosaurids, our assessment for Parasaurolophus is reasonable. Ontogeny in Parasaurolophus Accepting the identification of RAM 14000 as a juvenile Parasaurolophus, several notable ontogenetic changes can be inferred for the skull and postcrania in this taxon. Some of these are consistent with previous reports on other lambeosaurines, but others are exclusive to Parasaurolophus. Because the following discussion includes at least three different species (P. walkeri, P. cyrtocristatus, and P. tubicen), we caution that some ontogenetic changes may be more phylogenetically restricted than indicated here. Nonetheless, broad similarities across Parasaurolophus species imply that many changes are universal to the taxon. The crest of RAM 14000 differs from that of all known adult Parasaurolophus in several important ways. First, the crest in RAM 14000 is restricted to a low eminence rather than an elongated, curved tube that overhangs the braincase (Fig. 11A,C). Second, the crest in RAM 14000 is bordered caudally and at its apex by the nasal. Although the exact sutural relations of adult Parasaurolophus are controversial (e.g., differing reconstructions in Weishampel and Jensen, 1979:fig. 2, versus Sullivan and Williamson, 1999:fig. 5), it seems likely that the nasal formed only a small portion of the ventral margin of the crest in adult individuals (Sullivan and Williamson, 1999). Thus, the already minimal contribution of the nasal was further minimized through ontogeny. Third, the premaxilla-nasal fontanelle is open, whereas it is completely closed in all other, ontogenetically older specimens. These differences between the crests of juvenile and adult Parasaurolophus are intimately tied to ontogenetic changes in the braincase. The frontal of Parasaurolophus thickened and achieved a nearly vertical contact with the nasal only in later ontogenetic stages. At the latest, this occurred by the time the individual reached half of adult skull size (Evans et al., 2007). Finally, a broad nasal-frontal suture also only occurred at half maximum skull size. In all of these details, where known, RAM 14000 is more similar to juveniles of most lambeosaurin species than to subadult or adult Parasaurolophus. Based on reconstructions of the nasal passages in Parasaurolophus (Fig. 11), RAM 14000 indicates that several important transformations occurred as the crest elongated. The lateral diverticulum exhibits perhaps the most notable changes. In the smallest juvenile condition (Fig. 11C), the diverticulum completely obscures the main airway in lateral view. In adults (P. walkeri, P. tubicen, and P. cyrtocristatus; Fig. 11A), the main airway greatly exceeded the extent of the lateral diverticulum, as well as bounding the diverticulum dorsally and ventrally. Additionally, the lateral diverticulum is reconstructed as a single blind chamber in adult P. cyrtocristatus, whereas it is clearly looped in young juveniles (however, a looped lateral diverticulum has been reconstructed for P. tubicen; Sullivan and Williamson, 1999). Additional information (particularly for adult Parasaurolophus from the Kaiparowits Formation) may revise this reconstructed sequence. In any case, juvenile Parasaurolophus differ markedly in most aspects of their nasal passages from all known adult Parasaurolophus as well as from lambeosaurins of all ontogenetic stages. The only major feature that appears to be constant is the lack of an S-loop; Parasaurolophus lacks this feature throughout ontogeny, whereas lambeosaurins retain the feature throughout ontogeny (Evans et al., 2009). 1434 1435 1436 1437 1438 1439 1440 1441 1442 1443 1444 1445 1446 1447 1448 1449 1450 1451 1452 1453 1454 1455 1456 1457 1458 1459 1460 1461 1462 1463 1464 1465 1466 1467 1468 1469 1470 1471 1472 1473 1474 1475 1476 1477 1478 1479 1480 1481 1482 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t The extent of the contributions of the nasal and premaxillae to the crest in Parasaurolophus has been a long-standing problem (summarized in Sullivan and Williamson, 1999). Based on the new information from RAM 14000 and comparison with lambeosaurins, we offer some new observations. In lambeosaurins, the relationships of different sections of the nasal passages (e.g., lateral diverticulum) and the surrounding bones (premaxillae and nasals) are relatively invariant through ontogeny. For instance, the nasal bounds the caudal edge of the lateral diverticulum in juvenile (ROM 759) and subadult (CMN 34825) Corythosaurus (Evans et al., 2009). A similar relationship exists between the nasal and the lateral diverticulum in RAM 14000. Unlike lambeosaurins, adult Parasaurolophus have a much more extensive lateral diverticulum (occupying up to half the length of the crest; e.g., Fig. 11A). However, the most recent interpretation of the crest sutures require that the lateral diverticulum, particularly at its caudal end, be enclosed nearly exclusively by the premaxillae (Sullivan and Williamson, 1999). In contrast, Weishampel (1981b) proposed that the nasals in P. walkeri (ROM 768) reached to the mid-length of the crest (see fig. 2H in that paper). This is roughly coincidental with the extent of the lateral diverticula in P. walkeri. We thus summarize two alternative hypotheses: 1) the relationships between the bony elements and the nasal passages were highly plastic through ontogeny in Parasaurolophus, due in part to its massive crest, and the crest predominantly is composed of the premaxillae; or 2) the nasal forms a major portion of the crest. We speculate that the latter hypothesis is most likely, based on the lateral diverticulum. Unfortunately, sutures are ambiguous in many skulls of adult Parasaurolophus due to crushing or fusion, and thus a rigorous test of the hypothesis will require description of better material and other ontogenetic stages. The morphology of RAM 14000 also implies that several features of the skull were relatively invariant in Parasaurolophus throughout ontogeny. The narrow infratemporal fenestra, constrained by a tightly angled jugal, occurs at all ontogenetic stages. The shape of the oral margin of the premaxilla is also relatively unchanged through ontogeny. Finally, the absence of an S-loop also appears to be invariant throughout ontogeny. Ontogenetic changes in the postcrania of hadrosaurids are well-documented (Horner and Currie, 1994; Dilkes, 2001; Suzuki et al., 2004; Guenther, 2009; Kilbourne and Makovicky, 2010). The patterns in RAM 14000 and Parasaurolophus, both for limb proportions and overall morphology, generally are consistent with observations from other taxa, particularly the lambeosaurine Hypacrosaurus stebingeri. Notably, the distal expansion of the ischium is minimal in RAM 14000 (unlike adult individuals of P. cyrtocristatus). Similar ontogenetic patterns in the ischium occur in H. stebingeri (Horner and Currie, 1994), suggesting that this change is generalized across lambeosaurines with the feature. The most dramatic changes are seen in the ilium, particularly in the reduced size of the supraacetabular process relative to that in adult Parasaurolophus (Fig. 19C,D). Again, this pattern is probably generalized across hadrosaurids (Guenther, 2009). The humerus:femur ratio is approximately the same in RAM 14000 and adult Parasaurolophus ROM 768 and FMNH P 27393 (0.53, 0.50, and 0.51, respectively), but the femur:fibula ratio differs more strongly (1.14 and 1.24 in RAM 14000 and FMNH P 27393, respectively; no complete tibias are known for adult Parasaurolophus). Thus, the portion of the leg below the knee joint is slightly longer in the younger animal. This may differ from the condition in Alligator mississippiensis, which shows isometry over the ontogeny of the fibula relative to the femur (Livingston et al., 2009). Both Alligator and Parasaurolophus seem to maintain a consistent humerus:femur ratio over ontogeny. Interestingly, this differs from strong negative allometry seem in the latter ratio for Massospondylus, although the sample in this case is much larger (Reisz et al., 2005). A broader sample of associated limb elements is needed to assess ontogenetic changes in limb proportions in hadrosaurids relative to other archosaurs. 1483 1484 1485 1486 1487 1488 1489 1490 1491 1492 1493 1494 1495 1496 1497 1498 1499 1500 1501 1502 1503 1504 1505 1506 1507 1508 1509 1510 1511 1512 1513 1514 1515 1516 1517 1518 1519 1520 1521 1522 1523 1524 1525 1526 1527 1528 1529 1530 1531 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t cranial functional morphology : The rhamphotheca on the upper jaw resulted in a minor reduction in bite force at the tip of the beak, relative to the condition without a rhamphotheca. Although this arguably enforced a slight limitation on the type of food items that could be cropped and ingested, a rhamphotheca would also have had some potential benefits. In particular, the expanded keratinous structure would have increased the area available for cropping, and thus the potential volume of food taken in per bite. Additionally, the rhamphotheca may have allowed the hadrosaur to more efficiently crop plants at ground level, by moving the bite point closer to the ground without having to bend the neck. The effect of a rhamphotheca upon mastication is a topic worthy of additional exploration. As expected by its smaller size and shorter airway, the crest of RAM 14000 produced a higher resonant frequency than did the crests of adults (assuming that the structure was indeed used in sound production). If such vocalizations played a role in the social behavior of Parasaurolophus, perhaps in distinguishing different age categories, (Weishampel, 1981a; Evans et al., 2009), the vastly different frequencies of adult and juvenile animals would have been easily distinguishable (Table 11). heterochrony in hadrosaurids and other ornithischians : Heterochrony\u2014variation in developmental timing of the appearance of anatomical features relative to the ancestral condition (e.g., Gould, 1977; Alberch et al., 1979; Klingenberg, 1998; Smith, 2001)\u2014presumably played an important part in the evolution of lambeosaurine crests. A robust assessment of crest heterochrony requires knowledge of the extent of crest development at given sizes and absolute ages for several taxa, in addition to their stratigraphic ranges and phylogenetic relationships. Estimates of absolute age for fossil taxa are only obtainable from skeletochronological assessments of bone histology. Unfortunately, despite much higher taxonomic diversity within Ankylopollexia and especially within Hadrosauridae, the vast majority of ornithopods sampled for histological study fall outside Ankylopollexia (Werning 2012). Prior to this study, only four hadrosaurids had been sampled: Telmatosaurus (Benton et al., 2010), Maiasaura (Horner et al., 2000, 2001), Hypacrosaurus (Horner and Currie, 1994; Horner et al., 1999; Cooper et al., 2008), and Edmontosaurus (\u201cAnatosaurus\u201d; Reid, 1985). Of these, the only lambeosaurine is Hypacrosaurus, a lambeosaurin. Additionally, only the histology of Maiasaura has been studied throughout ontogeny (Horner et al., 2000, 2001), and growth curves have been estimated only for Maiasaura (Erickson et al., 2001) and Hypacrosaurus (Cooper et al., 2008). Thus, the skeletochronological data necessary to link skull size, body size, and crest development with age are virtually nonexistent for lambeosaurines. This is especially unfortunate given that the phylogeny (e.g., Evans and Reisz, 2007; Gates et al., 2007; Prieto-M\u00e1rquez, 2010) and stratigraphic context (e.g., Ryan and Evans, 2005; Mallon et al., 2012) of hadrosaurids is increasingly well resolved. Embryonic and post-hatchling material (Horner and Currie, 1994) necessarily imply extremely young age (~a few months at most) for such specimens. To date, only the holotype specimen of Hypacrosaurus stebingeri, MOR 549, has been aged (Horner et al., 1999; Cooper et al., 2008), with an estimate of approximately 13 years old. This specimen is the only described adult specimen for H. stebingeri, and unsurprisingly has the largest crest of any specimen. Nonetheless, the structure is still relatively modest in size relative to the largest crests seen in specimens of Corythosaurus casuarius or Hypacrosaurus altispinus. This may reflect taxonomic differences, individual variation, sexual dimorphism, or another factor, but these hypotheses cannot be tested without a larger sample. Extrapolating from the growth curve presented for H. stebingeri, and assuming that sexual maturity occurred at or near the growth curve inflection (Erickson et al., 2007; Lee and Werning, 1532 1533 1534 1535 1536 1537 1538 1539 1540 1541 1542 1543 1544 1545 1546 1547 1548 1549 1550 1551 1552 1553 1554 1555 1556 1557 1558 1559 1560 1561 1562 1563 1564 1565 1566 1567 1568 1569 1570 1571 1572 1573 1574 1575 1576 1577 1578 1579 1580 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t 2008), sexual maturity occurred in this species at two to three years of age (Cooper et al., 2008). The reconstructed mean femoral length at this point was 450 mm. This is slightly smaller than the femoral lengths associated with juvenile skeletons referred to H. stebingeri (590 mm and 522 mm for AMNH 5340 and 5461, respectively; Lull and Wright, 1942; Evans, 2010). In both cases, the crest is only barely developed, suggesting that crest development in H. stebingeri did not occur until after the onset of sexual maturity but well before the animal reached full adult size. Additional histological work is needed to test this hypothesis. Assuming that RAM 14000 was still in its exponential growth phase (pre-inflection), a reasonable assumption given its bone microstructure, it had not yet reached sexual maturity despite already initiating crest development. Using skull length as a rough proxy for ontogenetic age, it is clear that Parasaurolophus initiated externally visible crest development at a much earlier point than did lambeosaurins (~30% maximum skull size versus ~50% maximum skull size exclusive of the crest; Fig. 28). Juvenile lambeosaurins nearly twice the size of RAM 14000 have far more subdued crests relative to the rest of the skull; a similar pattern is seen for the potentially basal lambeosaurine Kazaklambia convincens. This could result from different life history parameters (e.g., differences in overall growth rate or the onset of sexual maturity), but we suggest it is more likely related to the larger and more \u201cextreme\u201d nature of the crest in Parasaurolophus versus lambeosaurins. In other words, the crest had to begin growth at an earlier stage in order to achieve its full extent. Within a standard terminological framework for heterochrony, the earlier and more extreme final development of the crest in Parasaurolophus relative to lambeosaurins is a classic example of peramorphosis (sensu Alberch et al., 1979). Assuming that Kazaklambia convincens is a basal lambeosaurine (Bell and Brink, in press), lambeosaurins such as Corythosaurus retained the ancestral condition of crest development occurring relatively late in ontogeny (~50% maximum skull size). Parasaurolophus, relative to the ancestral condition, thus shows the peramorphic phenomena of predisplacement (related to early onset of growth of the crest) as well as probable hypermorphosis (continued, extreme growth of the crest). Despite the differences in crest development between lambeosaurins and Parasaurolophus, lambeosaurine hadrosaurids fit an overall pattern of relatively early development of bony cranial ornamentation in ornithischian dinosaurs. This contrasts with birds that initiate crest growth only as the animal reaches nearly full adult size, such as the cassowary (Fig. 28; Dodson, 1975). Two potential factors may contribute to these differences. First, among neornithines, sexual maturity occurs well after somatic maturity (roughly equivalent to full adult body size. This condition contrasts with that of non-avian dinosaurs which apparently achieved sexual maturity well before somatic maturity (Erickson et al., 2007; Lee and Werning, 2008). Thus, if cranial crests in ornithischians had some species-specific display function\u2014whether for species recognition, sexual selection, or any related use\u2014it is intuitive that the structures appeared before the animal reached full adult body size, and conversely for neornithines. A second important factor considers the integration of cranial ornamentation into the overall skull in ornithischians versus avians. In birds such as cassowaries and hornbills, the massive casques are simple \u201cadd-ons\u201d to the overall skull, formed strictly of a bony core without major involvement of respiratory or muscular systems (Rothschild, 1900; AAF, personal observation). By contrast, the crests of hadrosaurids are intimately integrated with the respiratory system, by virtue of the airway passing through the crest (Fig. 11). Thus, the crest had to form early in development, simply so that the animals could continue to breathe. Similar constraints may have affected the frills of ceratopsians, at least part of which supported jaw musculature (Rieppel, 1981). However, this does not necessarily explain the early development of horns in ceratopsids (Horner and Goodwin, 2006), or nodes and spikes in pachycephalosaurs (Horner and Goodwin, 2009; Schott et al., 2011), structures that seem to be decoupled from more \u201cutilitarian\u201d 1581 1582 1583 1584 1585 1586 1587 1588 1589 1590 1591 1592 1593 1594 1595 1596 1597 1598 1599 1600 1601 1602 1603 1604 1605 1606 1607 1608 1609 1610 1611 1612 1613 1614 1615 1616 1617 1618 1619 1620 1621 1622 1623 1624 1625 1626 1627 1628 1629 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t aspects of the skull. Here, timing of sexual maturity may have played a role. We thus hypothesize that development of different structures was subject to different constraints depending upon their function and location. 2010) are diagrammed in figure 5. dashes indicate missing measurements. : PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Element Measurement and Description Value (mm) Left Right Skull 1 Length from tip of rostrum to paroccipital process, parallel to maxillary tooth row 246.0 \u2014 2 Length from tip of rostrum to quadrate, parallel to maxillary tooth row 211.2 \u2014 3 Preorbital length, parallel to maxillary tooth row 125.2 \u2014 4 Height at caudal end, perpendicular to maxillary tooth row 142.0 \u2014 5 Height from maxillary tooth row to top of crest 120.1 \u2014 6 Length from caudal end of crest to paroccipital process 112.8 \u2014 7 Maximum width across postorbitals from midline 46.1 \u2014 8 Height of caudal plane, perpendicular to tooth row 81.6 \u2014 External naris 38 Maximum length 55.1 \u2014 39 Maximum width 21.9 \u2014 Orbit 40 Maximum length 62.4 58.9 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t 41 Maximum height 53.5 48.0 Laterotemporal fenestra 42 Maximum length 63.7 \u2014 43 Maximum width 18.8 20.1 Dorsotemporal fenestra 44 Maximum length on lateral edge 42.6 \u2014 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Table 4(on next page) Measurements of individual cranial bones of Parasaurolophus sp., RAM 14000. The standards for these measurements (modified from those in Dodson, 1975; Evans, 2010) are diagrammed in Figure 5. Dashes indicate missing measurements. PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Element Measurement and Description Value (mm) Left Right Crest 9 Length from rostrum to crest midpoint, parallel to tooth row 118.7 \u2014 10 Angle between crest and snout 120\u00ba \u2014 11 Length parallel to tooth row, level with skull roof 61.8 \u2014 12 Length of crest at half-height 46.9 \u2014 13 Crest height above orbit, from postorbital/prefr ontal suture 61.8 \u2014 14 Height of crest above skull roof 25.1 \u2014 15 Maximum width of crest from midline 46.1 \u2014 16 Maximum width of premaxillary-nas al fontanelle 9.4 \u2014 Maxilla 17 Length along tooth row 117.7 *110.1 18 Height from tooth row to jugal-maxilla suture *44.4 31.8 Premaxilla 19 Straight-line length of oral margin, from midline 42.9 \u2014 20 Depression of oral margin below maxillary tooth row 32.6 \u2014 Jugal 21 Maximum length *113.1 107.7 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t 22 Maximum width of rostral process \u2014 35.6 23 Minimum width below orbit 19.2 19.2 24 Maximum width of blade 30.9 31.8 25 Minimum width of quadrate process 22.2 21.7 Postorbital 26 Maximum length 83.7 \u2014 27 Maximum height 53.4 \u2014 28 Minimum width of caudal process 13.3 \u2014 Quadrate 29 Maximum length 109.9 112.3 30 Craniocaudal length of lateral edge of distal condyle 18.2 17.6 31 Mediolateral width of distal condyle (not shown) 21.4 \u2014 Frontal 32 Length at midline 34.2 \u2014 33 Maximum width from midline 31.7 \u2014 Paroccipital process 34 Maximum width 18.3 \u2014 35 Maximum length 32.4 \u2014 36 Maximum separation from quadrate 15.9 11.0 37 Minimum separation from quadrate 11.1 9.9 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Table 5(on next page) Measurements of the lower jaw of Parasaurolophus sp., RAM 14000. The standards for these measurements (modified from those in Dodson, 1975) are diagrammed in Figure 5. Dashes indicate missing measurements. PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Element Measurement and Description Value (mm) Left Right Mandible 45 Maximum length 223.5 \u2014 Dentary 46 Maximum length along ventral edge 134.2 142.1 47 Length of edentulous process to caudal edge of predentary 15.3 \u2014 48 Maximum height from ventral edge to alveoli 30.7 33.1 49 Maximum height at coronoid process \u2014 72 50 Maximum width of coronoid process \u2014 27.9 Predentary 51 Length parallel to midline 49.8 \u2014 Surangular 50 Maximum length 54.8 46.2 51 Length of retroarticular process 42.6 38.5 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Table 6(on next page) Measurements of the vertebrae of Parasaurolophus sp., RAM 14000. The standards for these measurements are diagrammed in Figure 5. *indicates approximate measurement. PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Element Measurement and Description Value (mm) Cervical vertebra ?5 101 Maximum length of centrum 20.0 Cervical vertebra ?6 101 Maximum length of centrum 20.0 Dorsal vertebra ?14 101 Maximum length of centrum 28.8 Dorsal vertebra ?15 101 Maximum length of centrum 27.3 Dorsal vertebra ?16 101 Maximum length of centrum 26.7 Dorsal vertebra ?17 101 Maximum length of centrum 30.8 Dorsal vertebra ?18 101 Maximum length of centrum 35.8 Caudal vertebra ?2 103 Maximum craniocaudal length of neural spine 16.5 Caudal vertebra ?3 101 Maximum length of centrum 21.0 103 Maximum craniocaudal length of neural spine 16.1 Caudal vertebra ?4 101 Maximum length of centrum 20.3 103 Maximum craniocaudal length of neural spine 15.9 Caudal vertebra ?5 101 Maximum length of centrum 18.5 103 Maximum craniocaudal length of neural spine 14.9 Caudal vertebra ?6 101 Maximum length of centrum 16.7 102 Maximum proximodistal length of neural spine *107.9 103 Maximum craniocaudal length of neural spine 13.6 Caudal vertebra ?7 101 Maximum length of centrum 19.4 103 Maximum craniocaudal length 15.0 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t of neural spine Caudal vertebra ?8 101 Maximum length of centrum 16.5 103 Maximum craniocaudal length of neural spine 11.5 Caudal vertebra ?9 101 Maximum length of centrum 67.3 103 Maximum craniocaudal length of neural spine 13.6 Caudal vertebra ?10 103 Maximum craniocaudal length of neural spine 10.3 Caudal vertebra ?12 101 Maximum length of centrum 19.3 103 Maximum craniocaudal length of neural spine 8.6 Caudal vertebra ?13 101 Maximum length of centrum 19.5 102 Maximum proximodistal length of neural spine 30.9 Caudal vertebra ?14 101 Maximum length of centrum 18.3 102 Maximum proximodistal length of neural spine 29.2 Caudal vertebra ?15 101 Maximum length of centrum 19.1 102 Maximum proximodistal length of neural spine 29.2 Caudal vertebra ?16 101 Maximum length of centrum 20.5 103 Maximum craniocaudal length of neural spine 9.8 Caudal vertebra ?17 101 Maximum length of centrum 20.3 103 Maximum craniocaudal length of neural spine 9.4 Caudal vertebra ?18 101 Maximum length of centrum 21.3 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Caudal vertebra ?19 102 Maximum proximodistal length of neural spine 49.1 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Table 7(on next page) Measurements of the ribs of Parasaurolophus sp., RAM 14000. The standards for these measurements are diagrammed in Figure 5. PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Element Measurement and Description Value (mm) Cervical rib ?4 104 Maximum width between capitulum and tuberculum 19.6 105 Maximum length from capitulum to distal end of shaft 27.1 Cervical rib ?5 104 Maximum width between capitulum and tuberculum 19.7 105 Maximum length from capitulum to distal end of shaft 29.3 Cervical rib ?6 104 Maximum width between capitulum and tuberculum 17.9 105 Maximum length from capitulum to distal end of shaft 30.8 Dorsal rib 1 (left) 106 Maximum length from capitulum to distal end of shaft 235.0 Dorsal rib 2 (left) 106 Maximum length from capitulum to distal end of shaft 285.0 Dorsal rib 3 (left) 106 Maximum length from capitulum to distal end of shaft 325.0 Sacral rib 1 104 Maximum width between capitulum and tuberculum 39.4 Sacral rib 1 105 Maximum length from capitulum to distal end of shaft 54.3 Torso length (left) Distance between scapular glenoid and pelvic acetabulum 620.0 Rib cage Maximum depth 339.0 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Table 8(on next page) Measurements of the pectoral and pelvic elements of Parasaurolophus sp., RAM 14000. The standards for these measurements are diagrammed in Figure 5. *indicates approximate measurement. PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Element Measurement and Description Value (mm) Scapula (left) 52 Maximum length *267.6 53 Maximum width of blade 55.0 54 Minimum width of blade 36.3 Ilium 55 Greatest length 300.8 56 Length of preacetabular process 120.7 57 Minimum height of preacetabular process 21.5 58 Maximum height of preacetabular process 36.8 59 Maximum height of ilium 60.9 60 Length of postacetabular process, ventral 89.9 61 Length of postacetabular process, dorsal 104.7 62 Minimum height of postacetabular process 30.8 63 Mediolateral width of supraacetabular process 28.4 64 Length of ischiadic peduncle 28.7 65 Length of pubic peduncle 31.6 66 Width of acetabulum 52.1 Ischium (left) 67 Maximum length 243.1 68 Maximum width of distal end 30.0 Pubis 69 Length of prepubic blade 147.3 70 Maximum depth of prepubic blade 83.0 71 Minimum depth of prepubic blade 46.2 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Table 9(on next page) Measurements of the limb bones of Parasaurolophus sp., RAM 14000. The standards for these measurements are diagrammed in Figure 5. PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Element Measurement and Description Value (mm) Humerus 72 Maximum length 174.6 73 Length of deltopectoral crest (1) 101.1 74 Length of deltopectoral crest (2) 96.6 75 Maximum width at deltopectoral crest 38.1 76 Maximum width at proximal end 50.5 77 Minimum diameter of diaphysis 24.5 78 Maximum width at distal end 35.2 Femur 79 Maximum length 328.9 80 Craniocaudal width of proximal end on lateral surface 66.8 81 Craniocaudal length of cranial trochanter 25.8 82 Proximodistal length of 4th trochanter 73.3 83 Craniocaudal height of 4th trochanter 15.6 84 Craniocaudal length at midshaft excluding 4th trochanter 40.9 85 Distance between distal ends of 4th trochanter and femur 127.2 Tibia 86 Maximum length 306.9 87 Maximum craniocaudal width at proximal end 80.6 88 Maximum projection of cnemial crest 22.1 89 Maximum proximodistal length of cnemial crest 113.0 90 Maximum craniocaudal width at distal end 47.5 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Fibula 91 Maximum length 288.3 92 Maximum craniocaudal diameter at proximal end 43.2 93 Minimum craniocaudal diameter of diaphysis 15.7 94 Maximum craniocaudal diameter at distal end 25.2 Calcaneum 95 Maximum craniocaudal length 25.4 96 Minimum proximodistal length 14.6 Metatarsal IV 97 Maximum length on dorsal midline (not shown) 100.1 Phalanx IV-1 98 Maximum length on dorsal midline 25.9 Phalanx IV-2 98 Maximum length on dorsal midline 8.8 Phalanx IV-3 98 Maximum length on dorsal midline 7.3 Phalanx IV-4 98 Maximum length on dorsal midline 2.3 Phalanx IV-5 99 Maximum length on dorsal midline 31.3 Phalanx IV-5 100 Maximum mediolateral width (estimated) 25.6 Phalanx III-2 98 Maximum length on dorsal midline 7.3 Phalanx III-3 98 Maximum length on dorsal midline 5.1 Phalanx III-4 99 Maximum length on dorsal midline 29.0 PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Table 10(on next page) Measurements of Parasaurolophus sp., RAM 14000, compared with those for selected other lambeosaurines. Measurements of Parasaurolophus sp., RAM 14000, compared with those for selected other lambeosaurines. Measurements for FMNH P 27393 are from Ostrom (1963), and measurements for other lambeosaurines (excepting RAM 14000) are from Lull and Wright (1942), Evans (2010) , and Sullivan and Williamson (1999). The crest length for AMNH 5340 is estimated from photographs; the crest length for FMNH P 27393 is approximate. All cranial measurements follow those of Dodson (1975) and Evans (2010); crest length is from the top of the orbit to the maximum extent of the crest. AMNH 5340 is included as the most complete and best-known associated skeleton of a juvenile lambeosaurine. Complete measurements, as well as a description of the landmarks used for each measurement, are contained in Figure 5 and Tables 2\u20138. *indicates an incomplete or estimated element length. The number in parentheses in each entry indicates the size relative to RAM 14000. PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Taxon Parasaurolophus sp. P. cyrtocristatus P. walkeri Lambeosaurus sp. Specimen RAM 14000 FMNH P27393 ROM 768 AMNH 5340 Humerus length (mm) 175 565 (0.31) 520 (0.34) 305 (0.57) Ilium length (mm) 301 975 (0.31) 1015 (0.30) 570 (0.53) Prepubis length (mm) 147 430 (0.34) 516 (0.28) 260* (0.57) Ischium length (mm) 243* 1040 (0.23) \u2013 630* (0.39) Femur length (mm) 329 1105 (0.30) 1032 (0.32) 590 (0.56) Tibia length (mm) 307 \u2013 \u2013 550 (0.56) Fibula length (mm) 288 890 (0.32) \u2013 530* (0.54) MT IV length (mm) 100 335 (0.30) \u2013 \u2013 Fibula / femur 0.88 0.80 \u2013 0.90 Skull length (mm) 246 \u2013 745 (0.33) 380 (0.65) Quadrate length (mm) 111 \u2013 272 (0.41) 165 (0.67) Orbit length (mm) 60 \u2013 105 (0.57) 77 (0.78) Orbit height (mm) 50 \u2013 170 (0.29) 82 (0.61) Dentary length (mm) 138 \u2013 455 (0.30) \u2013 Crest length (mm) 62 404* (0.15) 970 (0.06) 90* (0.69) PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Table 11(on next page) Estimated resonant frequencies of the crest in Parasaurolophus skulls. standards for skeletal measurements. : Those for the skull and lower jaw augment standards published elsewhere (Dodson, 1975; Evans, 2010). Numbers associated with each measurement correspond to those in Tables 3\u2013 9 (a) and (b) skull in left lateral view; (c) right half of caudal section of skull in dorsal view; : (D) mandible in left lateral view; (E) scapula; (F) ilium; (G) ischium; (H) pubis; (I) humerus; (J) femur; (K) tibia; (L) fibula; (M) calcaneum; (N) pedal phalanx; (O) pedal ungual; (P) caudal vertebra (also used for other vertebrae); (Q) cervical rib (also used for sacral rib); (R) dorsal rib. (A\u2013M) and (P\u2013R) are in right lateral view; (N) and (O) are in dorsal view. Drawings are not to scale. PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Figure 6 Reconstruction of the skull of Parasaurolophus sp., RAM 14000. (A) lateral view; (B) dorsal view; (C) rostral view. Missing elements (including sutural relationships that are not visible in RAM 14000) are patterned after other lambeosaurines, and the rhamphotheca is shown in place. Reconstruction copyright Ville Sinkkonen. PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Figure 7 Left half of the skull of Parasaurolophus sp., RAM 14000, in lateral view. (A) interpretive drawing; (B) photograph. Abbreviations: an, angular; cb, first ceratobranchial; d, dentary; en, external naris; exo, exoccipital-opisthotic; f, frontal; itf, infratemporal fenestra; j, jugal; m, maxilla; n, nasal; o, orbit; pd, predentary; pm, premaxilla; pnf, premaxilla-nasal fontanelle; po, postorbital; prf, prefrontal; q, quadrate; ri, extent of impressions of upper rhamphotheca; sa, surangular; sq, squamosal. Scale bar equals 10 cm. PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Figure 8 Left half of the skull of Parasaurolophus sp., RAM 14000. (A) and (B), rostral view; (C) and (D), dorsal view; (F) and (G) caudal view. (E) detail of the impression of the upper rhamphotheca in rostral view. (A), (C), (E), and (F) are photographs, and (B), (D), and (G) are interpretive line drawings. Abbreviations: cb, first ceratobranchial; d, dentary; en, external naris; exo, exoccipital-opisthotic; f, frontal; j, jugal; n, nasal; o, orbit; p, parietal; pd, predentary; pm, premaxilla; po, postorbital; prf, prefrontal; pt, pterygoid; q, quadrate; ri, impression of rhamphotheca; sa, surangular; sq, squamosal; stf, supratemporal fenestra. Scale bar equals 10 cm for (A\u2013D) and (F\u2013G), and 1 cm for (E). In (A) and (B), scale bar is approximately in the plane of the crest; in (C) and (D), the scale bar is approximately in the plane of the frontal bone; in (F) and (G), the scale bar is in the plane of the quadrate. PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Figure 9 Skull of Parasaurolophus sp., RAM 14000, with digital reconstruction showing endocranial features. (A)\u2013(C), left lateral view; (D)\u2013(E), medial view; (F)\u2013(H), dorsal view; (I)\u2013(K), rostral view; (L)\u2013 (M), coronal section schematics. (A), (F), and (I) show the endocranial cavity (blue) and nasal passages (green) relative to the cranium, and (B), (D), (G), and (J) show the features without the skull bones. (C), (E), (H), and (K) show a schematic of the various parts of the nasal passages. The positions of the planes of section for (L) and (M) are indicated on (C) as X\u2013X\u2019 and Y\u2013Y\u2019, respectively. Dashed lines in (C), (E), (H), and (K) indicate areas of communication between different parts of the nasal passages. In (E), note that the dorsal ascending tract (dat) is not continuous with the naris; this is due to a missing section of the airway. Abbreviations: cmc, common median chamber (homologous to nasal cavity proper); dat, dorsal ascending tract (homologous to nasal vestibule); ec, endocranial cavity; en, external naris; ld, lateral diverticulum (homologous to nasal cavity proper); ma, main airway (homologous to nasal vestibule); or, olfactory region; vat, ventral ascending tract (homologous to nasopharyngeal duct); vma, ventral portion of main airway. Scale bar equals scale bars equal 10 cm. : PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Figure 12 Disarticulated skull elements of Parasaurolophus sp., RAM 14000. (A) partial right squamosal in lateral view; (B) right maxilla in lateral view; (C\u2013E) right first ceratobranchial in lateral (C, E) and dorsal (D) views. (C) and (D) are reconstructed from CT scan data. (C) includes the caudal portion of the element, and (E) includes the rostral portion, with the relative position of the two parts approximating their original relationship. Abbreviations: ep, ectopterygoid; qc, quadrate cotyle. Scale bar equals 1 cm. PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Figure 13 Skull and neck of Parasaurolophus sp., RAM 14000. (A) and (C) are in right lateral view; (B) and (D) are a medial view of the same block. (A), (B), interpretive drawings; (C), (D), photographs. Abbreviations: bo, basioccipital; cb, first ceratobranchial; cc, centrum of cervical vertebra; cr, cervical rib; cv, cervical vertebra; d, dentary; dr, dorsal rib; ex, exoccipital; j, jugal; la, lacrimal m, maxilla; nat, neural arch of atlas; nax, neural spine of axis; nc, neural canal; ns, neural spine; pd, predentary; po, postorbital; prs, presphenoid; ps, parasphenoid; q, quadrate; sa, surangular; sq, squamosal; tp, transverse process; V, foramen for CN V; V2,3, sulcus for CN V2 and V3. Bone is shown in white, impressions of bone are shown in green, and rock without bone impressions is shown in gray. Scale bar equals 10 cm. PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Figure 14 Ontogenetic changes in selected cranial elements of Parasaurolophus. Juvenile elements (A, C, E, G) are from RAM 14000; adult elements (B, D, F, H) are from the holotype of P. walkeri (ROM 768). All elements are in left lateral view. (A) and (B) postorbital; (C) and (D) jugal; (E) and (F) lower jaw; (G) and (H) quadrate. The jugal in (C) is a composite of the bone preserved on the left side and the impressions of the sutural regions on the right side. Parasaurolophus walkeri elements are redrawn and modified after Evans et al. (2007). PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Figure 15 Partial braincase of Parasaurolophus sp., RAM 14000, in right lateral view. (A) interpretive drawing; (B) photograph. Abbreviations: atc, atlas centrum (odontoid); ati, atlas intercentrum; axc, axis centrum; bo, basioccipital; ex, exoccipital; fv, foramen vestibuli; nat, neural arch of atlas; XII?, foramen tentatively identified as that for CN XII; V, foramen for CN V; V2,3, sulcus for CN V2 and V3. Bone is shown in white, broken bone surface is shown in light gray, and matrix is shown in dark gray. Unlabeled bones are not confidently identified, but may represent vertebral fragments. Scale bar equals 1 cm. PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Figure 16 Cranial endocast of Parasaurolophus sp., RAM 14000, reconstructed from CT scans. (A) left lateral view of entire endocast; (B) dorsal view of entire endocast. The rostral and caudal portions were disarticulated, and thus their relative positions (joined by the black lines) should be considered tentative. The caudal portion was mirrored to match the rostral portion. (C\u2013F), endosseous labyrinth of right inner ear. (C) dorsal view; (D) lateral view; (E) caudal view; (F) rostral view. The endocast of the brain is colored blue and the endocast of the bony labyrinth is colored orange. Abbreviations: c, cochlear duct; cer, cerebrum; crc, crus communis; csc, caudal semicircular canal; fm, endocast of foramen magnum; fv, fenestra vestibulae (approximate location); lab, endosseous labyrinth; lsc, lateral semicircular canal; ob, olfactory bulbs; pcer, postcerebral region; rsc, rostral semicircular canal; rsca, ampulla of rostral semicircular canal; ve, vestibule. Scale bar at left is for (A) and (B) and equals 1 cm. Scale bar at right is for (C\u2013F) and equals 5 mm. Because of differences in perspective between images, the scale bar is only approximate. PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Figure 17 Ossified tendons of Parasaurolophus sp., RAM 14000. (A) ossified tendons associated with cranial dorsal vertebra (?D4), with medial surface of tendons visible (cranial end is to left of image); (B) impressions of ossified tendons associated with either caudally placed dorsal vertebrae or cranially placed sacral vertebrae (cranial end is to right of image). Abbreviations: ins, impression of neural spine; iot, impression of ossified tendon; ns, neural spine; ot, ossified tendon. Scale bars equal 1 cm. PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Figure 18 Major limb bones from the right side of Parasaurolophus sp., RAM 14000, in lateral view. (A) humerus; (B) ilium; (C) femur; (D) tibia and fibula. The image in (A) is a digital surface model generated from photogrammetric reconstruction of the natural mold. The head appears unusually flat because some bone still fills that area. Abbreviations: cal, calcaneum; cnc, cnemial crest of tibia; ctr, cranial trochanter; di, diaphysis of humerus; dpc, deltopectoral crest; ftr, fourth trochanter; gtr, greater trochanter; h, head; histA, location of histology sample A; histB, location of histology sample B; ip, ischiadic peduncle; lc, lateral condyle of humerus; mc, medial condyle of humerus; poap, postacetabular process; pp, pubic peduncle; prap, preacetabular process; sap, supraacetabular process. Scale bars equal 10 cm; upper scale bar is for (A); lower scale bar is for (B\u2013D). PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Figure 19 Comparisons of selected postcranial elements in adult (A, C, E, G) and juvenile (B, D, F, H) Parasaurolophus. (A) and (B) right humerus; (C) and (D) right ilium; (E) and (F) right femur; (G) and (H) right fibula. Juvenile elements are from RAM 14000; adult elements represent FMNH P 27393, Parasaurolophus cyrtocristatus, and are traced from Ostrom (1963). (A) is reversed from the original. Scale bars equal 10 cm. PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Figure 20 Phalanges of right pedal digit III of Parasaurolophus sp., RAM 14000. (A) and (D) phalanx III-2; (B) and (E) phalanx III-3; (C) and (F) phalanx III-4 (ungual); (A\u2013C) dorsal view; (D\u2013F) lateral view. The distal ends of the bones are to the right of the image. PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t The proximal end of the digit is to the lower right end of the image, and the distal end is towards the top middle edge of the image. The arrow indicates one individual tubercle. Abbreviations: MT III, caudal surface of metatarsal III. Scale bar equals 1 cm. PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Figure 22 Bone microstructure of juvenile Parasaurolophus tibia in regular transmitted light (RAM PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Figure 27 Schematic of the hadrosaur jaw system, showing the effects of a rhamphotheca on bite mechanics. 14000, histological sample b, near mid-diaphysis; see fig. 18d for position of sample). : (A) entire sample in cross-section (transverse plane), with inset box showing the position of position of sample). (A) inner cancellous region; (B) outer cancellous region; (C) inner/mid-cortex; (D) outer cortex close to the periosteum. In (A), the cores of trabeculae are comprised of unremodeled primary woven bone tissue and the edges lined by pseudolamellae of parallel-fibered bone and true lamellar bone. In (B), incipient cancellous bone, forming by expansion of canals. Most spaces are unlined. In (C), woven bone forms much of the laminae and parallel-fibered bone lines the primary osteons rather than lamellar bone. In (D), longitudinal simple primary canals and primary osteons begin to anastomose laterally. Osteocyte density is noticeably higher in (B), (C), and (D) compared to (A), though they are randomly oriented through the entire section. The periosteum lies to the top of each image. All scale bars equal 500 \u00b5m. PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Figure 24 Bone microstructure of juvenile Parasaurolophus tibia in regular transmitted light (RAM position of sample). (A) entire sample in cross-section (transverse plane); (B) radial \u201ctransect\u201d across A; (C) and (D), enlargements of B showing primary osteons and osteocytic arrangement. Proximal in the diaphysis, the cortex is better organized (C) compared to the mid-diaphysis (Fig. 22) and there is much more secondary remodeling in the inner cortex (D). The periosteum lies to the top of each image. Scale bar equals 5 mm for A, 2 mm for B, and 250 \u00b5m for C and D. PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t (A) entire sample in longitudinal section; (B) enlargement of (A) showing primary osteons and osteocytic arrangement in the cortex; (C) osteocytes. The amount of woven bone in the laminae between primary osteons varies through the cortex. In (B), osteocytes in regions of woven bone are randomly oriented and densely packed (e.g., to right of image). Closer to canals, osteocytes are fewer in number and much more organized (center of image). In (C), the more disorganized woven bone is visible on the left side of the image and the more organized parallel-fibered bone is to the right. The periosteum lies to the left in all images. b; (b) radial \u201ctransect\u201d across a, with inset box showing positions of enlargements c and d; : (C) and (D) enlargements of B showing primary osteons and osteocytic arrangement. The primary cortex is virtually unremodeled and shows no lines of arrested growth. Most longitudinal primary osteons anastomose circumferentially with two to five other canals, especially in the mid-cortex. The woven component of the bone is less prominent in the outer cortex (C) compared to the midcortex and inner cortex (D). The periosteum lies to the top of each image. Scale bar equals 5 mm for (A), 2 mm for (B), and 250 \u00b5m for (C) and (D). PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t Figure 23 Bone microstructure of juvenile Parasaurolophus tibia in regular transmitted light (RAM 87 and 87.79.333, and represents an embryonic individual (redrawn from horner and : Currie, 1994). The next smallest skull is patterned after MOR 548 (also redrawn from Horner and Currie, 1994). The remaining skulls, from left, are patterned after ROM 759, CMN 34825, ROM 5856, and ROM 871, redrawn from Evans (2010). Skulls of Casuarius are redrawn from Dodson (1975) and based on (from left) YPM 6208, YPM 1736 (snout region reconstructed), and AMNH 3870. Maximum skull lengths for Parasaurolophus, Corythosaurus, and Casuarius are 745 mm (ROM 768), 750 mm (ROM 792) and 200 mm, respectively (Dodson, 1975; evans, 2010). scale bars equal 10 cm. : PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:1:0:NEW 27 Sep 2013) R ev ie w in g M an us cr ip t",
    "v2_text": "results systematic paleontology : Dinosauria (Owen, 1842) Ornithischia (Seeley, 1888) Hadrosauridae (Cope, 1869) Lambeosaurinae (Parks, 1923) Parasaurolophus (Parks, 1922) Parasaurolophus sp. acknowledgements : We acknowledge Kevin Terris for his discovery of RAM 14000, and thank Michael Stokes for his skillful excavation and preparation of the specimen. Don Lofgren and numerous students, faculty, and volunteers from the Alf Museum and The Webb Schools provided field assistance. We also thank Johnson Lightfoote and staff at Pomona Valley Hospital Medical Center for CT scanning RAM 14000. We thank the UCMP for access to histological sectioning equipment and Kevin Padian for imaging equipment. Kirstin Brink, Nic Campione, David Evans, Terry Gates, Mark Loewen, Scott Sampson, Jack Horner, and many others offered insightful discussion about lambeosaurine ontogeny. Larry Witmer provided comparative models of lambeosaurine crania, and Scott Hartman and Ville Sinkonnen provided reconstructions of RAM 14000. Casey Holliday and Henry Tsai compiled the 3D PDF files illustrating the nasal passages and endocranial cavity. We thank Ashley Fragomeni and Peter Kloess for curatorial assistance. RAM 14000 was collected under United States Department of the Interior Bureau of Land Management Paleontological Resources Use Permit (surface collection permit UT06-001S and excavation permit UT10-006E-Gs), with permitting assistance from Scott Foss and Alan Titus. Brandon Strilisky (RTMP) provided access to specimens in his care. 1506 1507 1508 1509 1510 1511 1512 1513 1514 1515 1516 1517 1518 1519 1520 1521 1522 1523 1524 1525 1526 1527 1528 1529 1530 1531 1532 1533 1534 1535 1536 1537 1538 1539 1540 1541 1542 1543 1544 1545 1546 1547 1548 1549 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t discussion : RAM 14000 is Parasaurolophus Although the visually-striking and taxonomically-diagnostic crests of lambeosaurine hadrosaurids do not reach their ultimate morphology until adulthood, many genus- and species-level autapomorphies appear earlier in ontogeny (Evans et al., 2005, 2007; Evans, 2010; Brink et al., 2011). Based on a combination of anatomical features in RAM 14000, as well as circumstantial stratigraphic and geographic evidence, we identify the specimen as a juvenile Parasaurolophus sp. Although both hadrosaurids and basal neornithischians (\u201chypsilophodontids\u201d) occur in the Kaiparowits Formation (Gates et al., in press), RAM 14000 is clearly identifiable as a hadrosaurid. It possesses numerous synapomorphies not found in \u201chypsilophodontids,\u201d including three or more replacement teeth in each tooth family as well as absence of a surangular foramen or free palpebral (Horner et al., 2004). Furthermore, a series of synapomorphies clearly place RAM 14000 well within Lambeosaurinae, including a domed frontal in subadults, development of an enlarged crest formed from the premaxillae and nasals as well as a nasal vestibule completely enclosed by premaxillae, a triangular rostrolateral corner of the premaxilla, and many others (Horner et al., 2004; Prieto-M\u00e1rquez, 2010). Based on CT scan data, we reconstruct RAM 14000 as lacking an S-loop in the proximal portion of the nasal passages (Fig. 9), an ontogeny-independent synapomorphy that occurs in most post-embryonic corythosaurins (Evans and Reisz, 2007; Evans et al., 2009). Additionally, there is no solid, fin-like caudal extension of the crest, found in all juvenile and adult corythosaurins for which CT scan data are available (Evans et al., 2009). Relative to Velafrons coahuilensis, RAM 14000 lacks the unique \u201ckinked\u201d squamosal morphology of that taxon (Gates et al., 2007). In all juvenile and adult corythosaurins for which the feature is known, the 1111 1112 1113 1114 1115 1116 1117 1118 1119 1120 1121 1122 1123 1124 1125 1126 1127 1128 1129 1130 1131 1132 1133 1134 1135 1136 1137 1138 1139 1140 1141 1142 1143 1144 1145 1146 1147 1148 1149 1150 1151 1152 1153 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t caudolateral process of the premaxilla is moderately to extremely angled at its contact with the maxilla, rather than straight as in RAM 14000 (Fig. 7A; a feature otherwise found in Parasaurolophus). Finally, RAM 14000 shows accelerated development of some features relative to known corythosaurins (outlined below; Fig. 27). There are thus no firm characters to identify RAM 14000 as a corythosaurin. Previous authors have identified a suite of characteristics that unite parasaurolophins (Charonosaurus and Parasaurolophus), which can also be potentially evaluated in RAM 14000 (characters that are not preserved in the specimen are not considered here). These include: 1) a massive frontal platform extending caudally at least to the level of the supratemporal fenestrae; 2) thickening of the dorsal surface of the postorbital in adults to form a promontorium; and 3) an expanded distal head of the fibula (Godefroit et al., 2004; Evans and Reisz, 2007; Evans et al., 2007; Prieto-M\u00e1rquez, 2010). Characters 1 and 2 are intimately linked with the development of the massive crest (at least in Parasaurolophus, where crest morphology is known, and presumably also in Charonosaurus). RAM 14000 lacks these features, but their absence is not surprising in light of the crest\u2019s incipient development. The distal end of the fibula is slightly expanded in RAM 14000, but not to the degree seen in P. cyrtocristatus or C. jiayinensis (Ostrom, 1963; Godefroit et al., 2001). However, this feature also occurs to a lesser degree in Corythosaurus intermedius and Hypacrosaurus stebingeri (Prieto-M\u00e1rquez, 2010), and thus cannot be considered taxonomically significant in RAM 14000. Other important characters, such as the number of cervical vertebrae, relative length of metacarpal V, and the participation of the parietal in the occiput, cannot be determined in RAM 14000. Based on a referred juvenile braincase (CMN 8502), Evans and colleagues (2007) identified several features of the skull roof that they hypothesized to be relatively consistent through ontogeny in Parasaurolophus, at least for the sample accessible at that time. These included: 1) frontal with a thick and steeply-angled nasal articular surface; 2) frontals comparatively short; 3) frontals with a poorly-developed median cleft at rostral-most extent; 4) rostral processes of frontal meet at broad and obtuse angle in dorsal view; and 5) olfactary depression offset ventrally from roof of cerebral fossa. Characters 1, 2, 4, and 5 are demonstrably absent in RAM 14000, and character 3 cannot be evaluated. Arguably, all of the characters (particularly character 1) are related to the development of the enlarged bony crest supported by the frontals. We thus attribute their absence in RAM 14000, an extremely young individual in which the crest is only incipient, to ontogenetic effects. Prieto-M\u00e1rquez (2010) also identified several unambiguous synapomorphies from his dataset that unite Parasaurolophus species. Unfortunately, these are either not preserved in RAM 14000 (number of teeth per alveolus at mid-dentary; morphology of deltoid ridge of scapula; proportions of ulna) or are widely distributed across lambeosaurines (proportions of humerus). Parasaurolophus is also reconstructed as having an extreme lateroventral extension of the supraacetabular process of the ilium (Fig. 18C), lacking in RAM 14000 (Figs. 17B and 18D). However, this character is ontogenetically-dependent (Guenther, 2009), and even variable among Parasaurolophus species (much more prominent in P. cyrtocristatus specimen FMNH P 27393 than in P. walkeri specimen ROM 768). Thus, its absence in RAM 14000 is not unexpected, nor is it of taxonomic consequence. Although RAM 14000 does not preserve major, previously-recognized autapomorphies for Parasaurolophus, several cranial features strongly support referral to this taxon. Most 1154 1155 1156 1157 1158 1159 1160 1161 1162 1163 1164 1165 1166 1167 1168 1169 1170 1171 1172 1173 1174 1175 1176 1177 1178 1179 1180 1181 1182 1183 1184 1185 1186 1187 1188 1189 1190 1191 1192 1193 1194 1195 1196 1197 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t significantly, the caudal edge of the caudolateral process of the premaxilla is interpreted as nearly straight along its entire length (Fig. 7A), a feature also found in all species of Parasaurolophus. In every other lambeosaurine of all ontogenetic stages for which the character can be determined, the edge is moderately to strongly kinked. The feature may be associated at least in part with the development of the S-loop in the nasal passages, another feature lacking in RAM 14000 and presumed absent in Parasaurolophus, based on CT-scan data (Sullivan and Williamson, 1999). Additionally, the nasal passages fill nearly the entire crest in RAM 14000 (Figs. 9A and 11C), as in Parasaurolophus but unlike the condition in corythosaurins (adults and juveniles alike). Morphology of the jugal is also informative in RAM 14000, with a relatively long and slender quadrate process that, in concert with the postorbital process, bounds a narrow infratemporal fenestra (width:length ratio=0.3; Fig. 7). This morphology is also consistently seen in adult Parasaurolophus (P. tubicen, NMMNH P-25100, PMU.R1250; P. walkeri, ROM 768; P. species, UMNH VP 16666, UCMP 143270; Fig. 27). A narrow infratemporal fenestra also occurs variably in sub-adults and adults of other lambeosaurines (e.g., Hypacrosaurus altispinus, CMN 8501; \u201cProcheneosaurus convincens\u201d, PIN 2230; Velafrons coahuilensis, CPC-59), but never in combination with a narrow quadrate process. Furthermore, the quadrate process of the jugal is distinctly constricted (Fig. 7), so that the ventral border is slightly concave along its entire length. This feature occurs in other Parasaurolophus specimens (P. tubicen, PMU.R1250; P. walkeri, ROM 768; UMNH VP 16666). Some other lambeosaurines have a similar concave border (e.g., Lambeosaurus lambei, CMN 2869), but never in combination with other features. We also note that the quadrate process on the jugal of \u201cProcheneosaurus convincens\u201d expands caudally, contrasting with the comparatively uniform width seen in RAM 14000 and other juvenile lambeosaurines. The impression of the jugal on the right side shows a narrow, triangular extension of the maxillary process between the maxilla and lacrimal (Fig. 13B), also found only in Parasaurolophus (e.g., ROM 768). Thus, although individual features of the jugal in RAM 14000 are found in various lambeosaurines, the combination of features is exclusive to Parasaurolophus. Within the Kaiparowits Formation of Utah, three hadrosaurid taxa are known: the hadrosaurines Gryposaurus monumentensis and Gryposaurus sp., as well as the lambeosaurine Parasaurolophus sp. (Gates et al., in press; Weishampel and Jensen, 1979; Gates and Sampson, 2007). The known Kaiparowits Formation adult material is most similar to Parasaurolophus cyrtocristatus, but some differences in skull morphology suggest that the specimens may represent a distinct but closely related species or a different ontogenetic stage relative to the P. cyrtocristatus holotype specimen (Gates et al., in press). This issue is currently under study (T. A. Gates and D. C. Evans, personal communication to AAF, 2012). Of eight adult lambeosaurine skulls from the Kaiparowits Formation (BYU 2467; UMNH VP 16394, 16666, 16689, two unnumbered; RAM unnumbered; UCMP 143270), all are referable to Parasaurolophus (Gates et al., in press). Continued collecting may certainly uncover evidence of other taxa, but to date Parasaurolophus is the only known lambeosaurine from the Kaiparowits Formation. This circumstantial evidence is also consistent with the referral of RAM 14000 to the genus. The recognized species of Parasaurolophus are distinguished by autapomorphies of the crest (Sullivan and Williamson, 1999) that had not yet developed in RAM 14000. Thus, we cannot assign RAM 14000 to a particular species based upon morphology. In summary, the bulk of the evidence\u2014morphological and geological\u2014is most 1198 1199 1200 1201 1202 1203 1204 1205 1206 1207 1208 1209 1210 1211 1212 1213 1214 1215 1216 1217 1218 1219 1220 1221 1222 1223 1224 1225 1226 1227 1228 1229 1230 1231 1232 1233 1234 1235 1236 1237 1238 1239 1240 1241 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t parsimonious with the referral of RAM 14000 to Parasaurolophus. Specific autapomorphies for the genus that are lacking in the specimen\u2014such as the unique crest and frontal morphology\u2014 are hypothesized to have developed later in ontogeny. Furthermore, the skull of RAM 14000 shows unique morphology relative to known juvenile corythosaurins. in a, the jaws are shown without the rhamphotheca, in the approximate position where the upper and : lower bony beak surfaces would first make contact. In B, the jaws are shown with the upper rhamphotheca (orange), in the approximate position where the upper and lower beak surfaces would first make contact. Note that this is at a wider gape than in A. Abbreviations: a, distance from the center of the glenoid to the center of the coronoid process; d, distance from the glenoid to the top of the coronoid process; e, distance from the center of the coronoid process to the bite point; \u03b8, the angle between the line of the jaw and the applied force on the coronoid process (measured from the center of the dorsotemporal fenestra ); and \u03b4, the angle of the diagonal between the top of the coronoid and the glenoid, relative to the line of the jaw. x is the reduction in gape angle produced by the rhamphotheca. The equation to calculate bite force is given in the text. PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t The black and red scale indicates percentage of maximum reported skull length in increments of 10 percent. The yellow sunburst indicates the approximate skull size at which ornamentation initially appears. Note that Parasaurolophus develops its crest at a very small skull size relative to Corythosaurus, and both hadrosaurs initiate the development of cranial ornamentation at a smaller relative skull size than in Casuarius. Skulls for Parasaurolophus sp. are based on RAM 14000, a hypothetical subadult (Fig. 11B), and the holotype for Parasaurolophus cyrtocristatus (FMNH P 27393, with missing elements patterned after ROM 768). The growth series for Corythosaurus is a composite, with the two smallest skulls (at left) patterned after Hypacrosaurus stebingeri. Because the two taxa are so closely related, and because they show broadly similar patterns of cranial growth where individuals of overlapping size are known (Evans, 2010; Brink et al., 2011) , we consider this a reasonable assumption. The smallest skull (at left) is based on RTMP 89.79.52, 87.79.206, 87.79.241, a and b are in rostral view; c and d are in dorsal view; f and g are in caudal view. e shows a detail : of the impression of the upper rhamphotheca in rostral view. A, C, E, and F are photographs, and B, D, and G are interpretive line drawings. Abbreviations: cb, first ceratobranchial; d, dentary; dtf, dorsotemporal fenestra; en, external naris; exo, exoccipital-opisthotic; f, frontal; j, jugal; n, nasal; o, orbit; p, parietal; pd, predentary; pm, premaxilla; po, postorbital; prf, prefrontal; pt, pterygoid; q, quadrate; ri, impression of rhamphotheca; sa, surangular; sq, squamosal. Scale bar equals 10 cm for A\u2013D and F\u2013G, and 1 cm for E. In A and B, scale bar is approximately in the plane of the crest; in C and D, the scale bar is approximately in the plane of the frontal bone; in F and G, the scale bar is in the plane of the quadrate. PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t A\u2013C, left lateral view; D\u2013E, medial view; F\u2013H, dorsal view; I\u2013K, rostral view; L\u2013M, coronal schematics. A, F, and I show the endocranial cavity (blue) and nasal passages (green) relative to the cranium, and B, D, G, and J show the features without the skull bones. C, E, H, and K show a schematic of the various parts of the nasal passages. The sections for L and M are indicated on C as X\u2013X\u2019 and Y\u2013Y\u2019, respectively. Dashed lines indicate areas of communication between different parts of the nasal passages. In E, note that the dorsal ascending tract (dat) is not continuous with the naris; this is due to a missing section of the airway. Abbreviations: cmc, common median chamber; dat, dorsal ascending tract; ec, endocranial cavity; en, external naris; ld, lateral diverticulum; ma, main airway; or, olfactory region; vat, ventral ascending tract; vma, ventral portion of main airway. Scale bar equals 10 cm. PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Figure 10 Left half of skull of Parasaurolophus sp., RAM 14000, in medial view. A, interpretive drawing; B, photograph. Abbreviations: cmc, common medial chamber; csc, caudal semicircular canal; d, dentary; dd, dentition from dentary (displaced); en, endocranial cavity; exo, exoccipital-opisthotic; m, maxilla; ncp, nasal cavity proper; nf, nutrient foramina; pd, predentary; pm, premaxilla; pt, pterygoid; pti, pterygoid impression; q, quadrate; sa, surangular; st, stapes; t, tooth; v, vomer. Scale bar equals 10 cm. PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Figure 11 Ontogenetic changes in the nasal passages and crest of Parasaurolophus. drawings; C, D, photographs. Abbreviations: bo, basioccipital; cb, first ceratobranchial; cc, centrum of cervical vertebra; cr, cervical rib; cv, cervical vertebra; d, dentary; dr, dorsal rib; ex, exoccipital; j, jugal; la, lacrimal m, maxilla; nat, neural arch of atlas; nax, neural spine of axis; nc, neural canal; ns, neural spine; pd, predentary; po, postorbital; prs, presphenoid; ps, parasphenoid; q, quadrate; sa, surangular; sq, squamosal; tp, transverse process; V, foramen for CN V; V2,3, sulcus for CN V2 and methods : Fieldwork and Preparation\u2014All fieldwork was conducted under United States Department of the Interior Bureau of Land Management Paleontological Resources Use Permit (surface collection permit UT06-001S and excavation permit UT10-006E-Gs). For specific 56 57 58 59 60 61 62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t locality information, see the \u201cSystematic Paleontology\u201d section below. After discovery in 2009, the specimen was stabilized with polyvinal acetate (Vinac\u2122 PVA-15, McGean Rohco, Inc., Cleveland, Ohio) dissolved in acetone. Because of weathering, portions of the pedal phalanges and the right half of the skull were collected in 2009, separately from the rest of the skeleton. Surface dry screening uncovered additional bone fragments. During the 2010 field season, the specimen was encased in a plaster and burlap field jacket and airlifted from Grand Staircase-Escalante National Monument by helicopter. Subsequently, the fossil was mechanically prepared using pneumatic engravers of varying sizes (PaleoTools, Brigham City, Utah; Chicago Pneumatic, Independence, Ohio). A minimal amount of matrix was left in place, in order to support and preserve the relative positions of the bones as well as soft tissue impressions. Full field and lab documentation are on file at RAM. CT Scanning\u2014In order to better visualize internal cranial anatomy, the skull of RAM 14000 was CT scanned on a Toshiba Aquilion 64 scanner at Pomona Valley Hospital Medical Center, Claremont, California. For the large skull blocks, the specimen was initially scanned at 120 kV and 350 mA, slice thickness of 0.5 mm and reconstruction diameter of 300 mm. This resulted in an in-plane resolution of 0.586 mm by 0.586 mm per pixel. After additional preparation, the specimen was rescanned. The left side of the skull was scanned at 120 kV and 400 mA, slice thickness of 0.5 mm, and reconstruction diameter of 229.687 mm, using a standard bone reconstruction algorithm, resulting in an in-plane resolution of 0.45 mm by 0.45 mm per pixel. The isolated portion of the braincase and maxilla were also scanned at identical parameters except for a reconstruction diameter of 140.625 mm, resulting in an in-plane resolution of 0.274 mm by 0.274 mm. The resulting data were then segmented and measured in 3D Slicer 4.2 (available at www.slicer.org; Gering et al., 1999; Pieper et al., 2004, 2006). Because of internal fracturing of the specimen and areas of poor contrast between bone and matrix, a combination of automatic thresholding and manual segmentation were used in order to visualize endocranial features. All CT scan and segmentation data are reposited at Figshare (Table 1, Supplemental Article S1). Photogrammetry\u2014Because the humerus was preserved as a natural mold, we produced a digital cast of the element using photogrammetry. 12 color photos at 4000x3000 pixel resolution were acquired with a Nikon CoolPix L22 digital camera (Nikon Inc., Melville, New York), and were resized to 2000x1500 pixels. Data were processed using BundlerTools (available at server.topoi.hu-berlin.de/groups/bundlertools/), which in turn uses Bundler 0.4, CMVS, and PMVS2. The resulting raw point cloud was processed further in MeshLab 1.3.0 (available at www.meshlab.org), in which a surface mesh was produced using a Poisson surface reconstruction algorithm (Octree Depth=10, Solver Divide=9, 1 sample per node, Surface Offsetting=1). Because the original mesh represented a natural mold, normals were inverted to produce a digital cast. The mesh was scaled by comparison with measurements of the original specimen, and data were exported in STL file format. The surface mesh is reposited at Figshare (Table 1, Supplemental Article S1). Histological Sampling\u2014Two samples from the right tibia were extracted for histological analysis. This bone was chosen because of its excellent preservation and easy accessibility on the specimen. Additionally, studies in other ornithischian dinosaurs (the basal iguanodontian Tenontosaurus tilletti and the hadrosaurine hadrosaurid Maiasaura peeblesorum) suggest that the tibia undergoes less remodeling at midshaft than do other skeletal elements, a characteristic 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130 131 132 133 134 135 136 137 138 139 140 141 142 143 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t critical for estimating the age of the animal at death using lines of arrested growth (Horner et al., 2000; Werning, 2012). Thus, the tibia is an ideal element for histological study. The position of natural cracks in the bone precluded sampling exactly at the tibial mid-diaphysis. However, we were able to sample at two points slightly proximal to this point. The more proximal sample \u201cA\u201d was taken 120 mm from the proximal end of the bone (~39% of the total tibial length, 307 mm), and sample \u201cB\u201d was taken 135 mm (~44% total length) from the proximal end of the bone (Figure 15D). Prior to sampling, we photographed and molded the surface of this region to document original morphology. Afterward, the sampled region was refilled with plaster to approximate the original anatomy. We removed both samples using a Dremel Moto-Tool Model 395 rotary tool (Dremel, Inc., Racine, Wisconsin) and small chisel. Because the tibia is partially embedded in matrix, only the caudolateral quadrant of the shaft, rather than a full cross-section, was extracted. We estimate the maximum craniocaudal diameter of the tibia at these points to be 40 mm. Both samples include both compact and cancellous bone; sample A is ~12 mm thick (thickness=radial \u201cdepth\u201d), and sample B is ~15\u201316 mm thick. The longitudinal sections made from sample A span 12 mm (proximo-distally) along the diaphysis. Given the maximum diameter relative to the thickness of the sections, and that the medullary cavity is open (i.e., not completely filled by cancellous bone) at both points, we think our samples likely capture most if not all of the preserved histology in this quadrant of the bone. Histological samples were prepared by SW at UCMP. Before embedding, the periosteal surfaces were cleaned with acetone to remove any traces of polyvinyl acetate. Both samples were then embedded in Silmar-41 clear polyester casting resin (Interplastic Corporation, Saint Paul, Minnesota) catalyzed with methyl ethyl ketone peroxide (Norac, Inc., Helena, Arkansas) at 1% by mass and allowed them to cure for 48 hours at room temperature. Thick transverse (cross-sectional) sections (1\u20131.5mm) were cut using a diamond-tipped wafering blade on a low-speed Isomet lapidary saw (Buehler, Inc., Lake Bluff, Illinois), mounted to glass slides, and ground to optical clarity using the materials and methods described in Werning (2012). Two slides in transverse section were made from sample A and three from sample B. Additionally, two slides in longitudinal section were made from some of the remaining embedded portion of sample A. All histological slides are reposited at RAM. Histological Imaging\u2014All slides were examined under regular transmitted light, elliptically polarized light (i.e., using a full wave retarder or red tint plate, \u03bb = 530 nm) and crossed plane polarizing filters. The filters were used to enhance birefringence. Overlapping digital images photographs (50% overlap by eye in X and Y directions) were taken using a D300 DSLR camera (Nikon Inc., Melville, New York) mounted to an Optiphot2-Pol light transmission microscope (Nikon Inc.). To image the entire slide or radial \u201ctransects\u201d, digital images were photomontaged using Autopano Giga 2.0 64Bit (Kolor, Challes-les-Eaux, France), using the program settings described in Werning (2012). High-resolution histological images are digitally reposited online for scholarly use at MorphoBank (http://morphobank.org/permalink/?P836, project p836; see Table 2 for a list of accession numbers). Digital images larger than 25,000 pixels in either dimension were digitally reduced (scaled but preserving original dimension ratios) to allow processing on MorphoBank. These edits were made after scale bars had been added. Linear Measurements\u2014Linear measurements under 300 mm were measured to the 144 145 146 147 148 149 150 151 152 153 154 155 156 157 158 159 160 161 162 163 164 165 166 167 168 169 170 171 172 173 174 175 176 177 178 179 180 181 182 183 184 185 186 187 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t nearest 0.l mm with digital calipers, and non-linear measurements as well as those over 300 mm were measured to the nearest mm with a cloth measuring tape. Landmarks for most cranial measurements were patterned after those in Dodson (1975) and Evans (2010), and are diagrammed along with postcranial measurements in Fig. 5. Relevant measurements are contained in Tables 3\u201310. Skeletal Completeness\u2014In order to assess relative skeletal representation for the three most complete specimens of Parasaurolophus (FMNH P 27393, RAM 14000, and ROM 768), we tallied the preserved elements for each. The skull and mandible were considered a single unit, as was the sacrum and sacral ribs. Partial elements were counted as present in the specimen, and we only counted bilateral elements once (e.g., even if both humeri were present, this element was counted once). Tallies are contained in Supplemental Table S1. Nomenclatural Conventions\u2014In this paper, the following conventions are utilized. These are defined here so as to avoid confusion in the event of future systematic or phylogenetic revisions. The clade Corythosaurini (corythosaurins) includes all taxa closer to Corythosaurus casuarius than to Parasaurolophus walkeri (Godefroit et al., 2004; Evans and Reisz, 2007). Unless otherwise specified, comparisons here involve the North American genera Corythosaurus, Lambeosaurus, Hypacrosaurus, and Velafrons, as well as the Asian taxon Nipponosaurus. The clade Parasaurolophini (parasaurolophins) includes all taxa closer to Parasaurolophus walkeri than to Corythosaurus casuarius (Godefroit et al., 2004; Evans and Reisz, 2007). This includes two genera, Parasaurolophus and Charonosaurus. Unless otherwise specified, usage of the name Parasaurolophus alone refers to all three named species, P. walkeri, P. cyrtocristatus, and P. tubicen. Although the enigmatic Kazakh lambeosaurine \u201cProcheneosaurus convincens\u201d has been subjectively synonymized with the coeval Jaxartosaurus aralensis (Horner et al., 2004), we maintain the former name here pending a more thorough evaluation of the former taxon. 2 meters in body length (~25% maximum adult body length) at death, with a skull measuring 246 : mm long and a femur 329 mm long. A histological section of the tibia shows well-vascularized, woven and parallel-fibered primary cortical bone typical of juvenile ornithopods. The histological section revealed no lines of arrested growth or annuli, suggesting the animal may have still been in its first year at the time of death. Impressions of the upper rhamphotheca are preserved in association with the skull, showing that the soft tissue component for the beak extended for some distance beyond the limits of the oral margin of the premaxilla. In marked contrast with the lengthy tube-like crest in adult Parasaurolophus, the crest of the juvenile specimen is low and hemicircular in profile, with an open premaxilla-nasal fontanelle. Unlike juvenile corythosaurins, the nasal passages occupy nearly the entirety of the crest in juvenile Parasaurolophus. Furthermore, Parasaurolophus initiated development of the crest at less than 25% maximum skull size, contrasting with 50% of maximum skull size in hadrosaurs such as Corythosaurus. This early development may correspond with the larger and more derived form of the crest in Parasaurolophus, as well as the close relationship between the crest and the respiratory system. In general, ornithischian dinosaurs formed bony cranial ornamentation at a relatively younger age and smaller size than seen in extant birds. This may reflect, at least in part, that ornithischians probably reached sexual maturity prior to somatic maturity, whereas birds become reproductively mature after reaching adult size. PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Andrew A. Farke1,*, Derek J. Chok2, Annisa Herrero2, Brandon Scolieri2, and Sarah Werning3 1Raymond M. Alf Museum of Paleontology, 1175 West Baseline Road, Claremont, CA 91711, USA 2The Webb Schools, 1175 West Baseline Road, Claremont, CA 91711, USA 3Department of Integrative Biology, Museum of Paleontology, and Museum of Vertebrate Zoology, University of California, Berkeley, CA 94720, USA *Author for correspondence. Address: Raymond M. Alf Museum of Paleontology, 1175 West Baseline Road, Claremont, CA 91711, USA. Office telephone: 909-482-5244. Email: afarke@webb.org. 1 2 3 4 5 6 7 8 9 10 11 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t conclusions : RAM 14000 represents the smallest and most complete Parasaurolophus specimen described to date, illustrating the unique juvenile morphology of this taxon relative to other lambeosaurine dinosaurs. Based on histology of the tibia, RAM 14000 exhibits no lines of arrested growth, and thus was likely under a year old. Notably, Parasaurolophus initiated crest development at a much smaller body size (and presumably younger age) than did corythosaurin lambeosaurines. At least in part, this is probably because of the extreme morphology of the crest in Parasaurolophus, which required a longer period of development. The timing of the onset of ornamentation development varies dramatically across amniotes, a topic which deserves considerably more attention. It is probably influenced by life history traits such as the timing of reproductive maturity, functional demands upon the skull, and phylogenetic history. As a group, lambeosaurine hadrosaurids initiated crest growth well before reaching adult size (between 25\u201350 percent maximum skull length), a feature common to most other ornithischian dinosaurs with cranial ornamentation. This may result from the intimate association of the ornamentation with essential functional complexes such as the nasal passages (in the case of hadrosaurs) or musculature (in the case of ceratopsians). If cranial ornamentation played at least some role in sexual selection and/or species recognition, early reproductive maturity may also be related to the precocious development of such ornamentation. Understanding these attributes in dinosaurs requires the documentation of more juvenile specimens with associated skeletochronological data, as well as documentation of patterns in extant species. a) adult individual, modified after ostrom (1963). the lateral diverticulum has been altered based on : data from RAM 14000, indicating a more proximal origin for the chamber. B) Hypothetical subadult Parasaurolophus. C) Juvenile, based on RAM 14000. Note that the intermediate-sized individual is largely speculative, although the enlarged size of the crest is consistent with a referred braincase, CMN data for rom 768 and fmnh p 27393 are from weishampel (1981a). : PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Frequency (Hz) Taxon Specime n Tube length (m) Mode 1 Mode 2 Mode 3 Mode 4 Mode 5 P. walkeri ROM 768 3.46 48 96 144 192 240 P. cyrtocrist atus FMNH P 27393 2.21 75 150 225 300 375 P. sp. RAM 14000 0.195 872 1,744 2,616 3,488 4,360 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t a, interpretive drawing; b, photograph. bones are bounded by solid lines and colored orange; matrix : is gray. Scale bar equals 10 cm. Abbreviations: f, femur; fib, fibula; il, ilium; isc, ischium; MT III, metatarsal III; MTIV, metatarsal IV; ppr, postpubic rod; prp, prepubic process; sc, scapula; sr, sacral rib; tib, tibia. PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Figure 3 Skeleton of Parasaurolophus sp., RAM 14000, in left lateral view. indicates areas of fragmented and powdered bone due to weathering, and green indicates bone impressions. The pink area indicates the location of skin impressions shown in Fig. 20. In A, the left half of the skull is indicated. A detailed outline of the medial surface of the right half of the skull shown in B is contained in Fig. 13. Abbreviations: f, femur; fib, fibula; h, humerus; il, ilium; isc, ischium; MTIII, metatarsal III; prp, prepubic process; sc, scapula; tib, tibia. Scale bar equals 10 cm. PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t AMNH 5340). Scale bar equals 10 cm. Reconstruction copyright Scott Hartman. PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Figure 5 lambeosaurines, and the rhamphotheca is shown in place. Reconstruction copyright Ville Sinkkonen. PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Figure 7 Left half of the skull of Parasaurolophus sp., RAM 14000, in lateral view. A, interpretive drawing; B, photograph. Abbreviations: an, angular; cb, first ceratobranchial; d, dentary; en, external naris; exo, exoccipital-opisthotic; f, frontal; j, jugal; ltf, laterotemporal fenestra; m, maxilla; n, nasal; o, orbit; pd, predentary; pm, premaxilla; pnf, premaxilla-nasal fontanelle; po, postorbital; prf, prefrontal; q, quadrate; ri, extent of impressions of upper rhamphotheca; sa, surangular; sq, squamosal. Scale bar equals 10 cm. PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Figure 8 Left half of the skull of Parasaurolophus sp., RAM 14000. views, as reconstructed from CT scan data; D, right maxilla in lateral view. Abbreviations: ep, ectopterygoid; qc, quadrate cotylus. Scale bar equals 1 cm. PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Figure 13 Skull and neck of Parasaurolophus sp., RAM 14000. portions were disarticulated, and thus their relative positions (joined by the black lines) should be considered tentative. The caudal portion was mirrored to match the rostral portion. C\u2013F, endosseous labyrinth of right inner ear. C, dorsal view; D, lateral view; E, caudal view; F, rostral view. Abbreviations: c, cochlear duct; cer, cerebrum; csc, caudal semicircular canal; crc, crus communis; fm, endocast of foramen magnum; fv, fenestra vestibulae (approximate location); lab, endosseous labyrinth; lsc, lateral semicircular canal; ob, olfactory bulbs; pcer, postcerebral region; rsc, rostral semicircular canal; rsca, ampulla of rostral semicircular canal; ve, vestibule. Scale bar at left is for A and B and equals 1 cm. Scale bar at right is for C\u2013F and equals 5 mm. Because of perspective, scale bar is only approximate. PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Figure 16 Ossified tendons of Parasaurolophus sp., RAM 14000. visible (cranial end to left of image); B, impressions of ossified tendons associated with caudally-placed dorsal vertebrae or cranially-placed sacral vertebrae (cranial end to right of image). Abbreviations: ins, impression of neural spine; iot, impression of ossified tendon; ns, neural spine; ot, ossified tendon. Scale bar equals 1 cm. PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Figure 17 Major limb bones from right side of Parasaurolophus sp., RAM 14000, in lateral view. generated from photogrammetric reconstruction of the natural mold. The head appears unusually flat because some bone still fills that area. Abbreviations: cal, calcaneum; cnc, cnemial crest of tibia; ctr, cranial trochanter; di, diaphysis of humerus; dpc, deltopectoral crest; ftr, fourth trochanter; gtr, greater trochanter; h, head; histA, location of histology sample A; histB, location of histology sample B; ip, ischiadic peduncle; lc, lateral condyle of humerus; mc, medial condyle of humerus; poap, postacetabular process; pp, pubic peduncle; prap, preacetabular process; sap, supraacetabular process. Scale bar equals 10 cm; upper scale bar is for A; lower scale bar is for B\u2013D. PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Figure 18 Comparisons of selected postcranial elements in adult (A, C, E, G) and juvenile (B, D, F, H) Parasaurolophus. RAM 14000; adult elements represent FMNH P 27393, Parasaurolophus cyrtocristatus, and are traced from Ostrom (1963). A is reversed from the original. Scale bars equal 10 cm. PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Figure 19 Phalanges of right pedal digit III of Parasaurolophus sp., RAM 14000. view. Scale bar equals 1 cm. PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Figure 20 Skin impressions of Parasaurolophus sp., RAM 14000, from plantar surface of right pedal digit of B showing primary osteons and osteocytic arrangement. The primary cortex is virtually unremodeled and shows no lines of arrested growth. Most longitudinal primary osteons anastomose circumferentially with two to five other canals, especially in the mid-cortex. The woven component of the bone is less prominent in the outer cortex (C) compared to the inner cortex (D). The periosteum lies to the top of each image. The scale bar for A equals 5 mm; B equals 2 mm; C, D equals 250 \u00b5m. PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Figure 22 Bone microstructure of juvenile Parasaurolophus tibia in regular transmitted light (RAM 14000, histological sample B, cross-section near mid-diaphysis). the periosteum. In A, the cores of trabeculae are comprised of unremodeled primary woven bone tissue and the edges lined by pseudolamellae of parallel-fibered bone and true lamellar bone. In B, incipient cancellous bone is clearly forming by expansion of canals. In C, woven bone forms much of the laminae and parallel-fibered bone lines the primary osteons rather than lamellar bone. In D, longitudinal simple primary canals and primary osteons begin to anastomose laterally. Osteocyte density is noticeably higher in B, C, and D compared to A, though they are randomly oriented through the entire section. The periosteum lies to the top of each image. All scale bars equal 500 \u00b5m. PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Figure 23 Bone microstructure of juvenile Parasaurolophus tibia in regular transmitted light (RAM 14000, histological sample A, cross-section through proximal portion of diaphysis). of B showing primary osteons and osteocytic arrangement. Proximal in the diaphysis, the cortex is better organized (C) compared to the mid-diaphysis (FigA) and there is much more secondary remodeling in the inner cortex (D). The periosteum lies to the top of each image. Scale bar for A equals 5 mm; B equals 2 mm; C, D equals 250 \u00b5m. PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t The elliptically polarized light is under full \u03bb retarder plate, and the sample is a cross-section through the proximal portion of the diaphysis. Moving periosteally through the cortex, the bone tissue comprising the laminae becomes progressively more organized. In the inner cortex (A, B), osteocytes are densely packed in the interstices between vascular canals, and their lacunae are oriented randomly with respect to the long axis of the bone and to each other. In this region, the laminae are mainly comprised of woven bone, with lamellar bone surrounding each vascular canal. In the mid-cortex (C, D), woven bone comprises a smaller portion of the laminae, and parallel-fibered bone lies between the woven and lamellar components. In the outer cortex (E, F), at most only a thin band of woven bone lies in the cores of the laminae, and much of the interstices are comprised of parallel-fibered bone. The periosteum lies to the upper right of each image. All scale bars equal 250 \u00b5m. Arrows in B, D, and F indicate the orientation of the slow axis of the \u03bb plate. PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Figure 25 Bone microstructure of juvenile Parasaurolophus tibia in regular transmitted light (RAM 14000, sample A; proximal portion of diaphysis). arrangement in the cortex; C, osteocytes. The amount of woven bone in the laminae between primary osteons varies through the cortex. In B, osteocytes in regions of woven bone are randomly oriented and densely packed (e.g., to right of image). Closer to canals, osteocytes are fewer in number and much more organized (center of image). In C, the more disorganized woven bone is visible on the left side of the image and the more organized parallel-fibered bone is to the right. The periosteum lies to the left in all images. Scale bar A equals 2 mm, B equals 250 \u00b5m, and C equals 100 \u00b5m. PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Figure 26 Schematic of the hadrosaur jaw system, showing the effects of a rhamphotheca on bite mechanics. description : RAM 14000 is preserved in nearly perfect articulation, with the neck, hip, lower leg and metatarsals strongly flexed (opisthotonic posture, probably resulting from the fresh carcass\u2019s immersion in water; Reisdorf and Wuttke, 2012; Figs. 2 and 3). The right humerus and pedal digits are gently extended. The specimen was lying on its left side; although more bones are represented on this side, they are much more badly weathered than on the right. Tree roots, freeze-thaw cycles, and recent rodent activity fragmented and displaced many of the elements on the left side. By contrast, the right side is less complete in terms of element representation, but the quality of bone preservation is generally better than on the left side. institutional abbreviations : AMNH, American Museum of Natural History, New York, New York, USA; BYU, Brigham Young University, Provo, Utah, USA; CMN, Canadian Museum of Nature, Ottawa, Ontario, Canada; CPC, Colecci\u00f3n Paleontol\u00f3gica de Coahuila, Museo del Desierto, Saltillo, Coahuila, M\u00e9xico; NMMNH, New Mexico Museum of Natural History, Albuquerque, New Mexico, USA; PIN, Paleontological Institute, Russian Academy of Sciences, Moscow, Russia; PMU, Museum of Evolution, Uppsala University, Uppsala, Sweden; RAM, Raymond M. Alf Museum of Paleontology, Claremont, California, USA; ROM, Royal Ontario Museum, Toronto, Ontario, Canada; SMP, State Museum of Pennsylvania, Harrisburg, Pennsylvania, USA; TMP, Royal Tyrrell Museum of Paleontology, Drumheller, Alberta, Canada; UCMP, University of California Museum of Paleontology, Berkeley, California, USA; UMNH, Natural History Museum of Utah, Salt Lake City, Utah, USA. referred material : RAM 14000, a partial skull and articulated skeleton (Figs. 2 and 3). locality and horizon : RAM V200921, Grand Staircase-Escalante National Monument, Garfield County, Utah, USA (Fig. 1); upper part of middle unit (sensu Roberts, 2007) of the Kaiparowits Formation; Late Cretaceous (late Campanian; Roberts et al., 2005). The site is stratigraphically between two locally prominent bentonites, tentatively correlated with bentonites KBC-109 and KBC-144 of Roberts et al. (2005), both exposed less than 10 km away from RAM V200921 and dated to 188 189 190 191 192 193 194 195 196 197 198 199 200 201 202 203 204 205 206 207 208 209 210 211 212 213 214 215 216 217 218 219 220 221 222 223 224 225 226 227 228 229 230 231 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t 75.51 +-0.15 Ma (Roberts et al., in press). The specimen was preserved within a cross-bedded tabular sandstone, tentatively interpreted as a channel deposit following previous literature (Roberts, 2007). Detailed locality data are on file at the RAM and are available to qualified investigators upon request. skull and mandible : The skull of RAM 14000 was split in two by erosion; in order to preserve visibility of internal structures, the two halves have not been reassembled. The skull and mandible are in articulation, with only slight displacement of the quadrate and mandible relative to each other. The left side is more complete, preserving nearly all elements (with the exception of a portion of the premaxilla). The dorsal and rostral portions of the right side are missing, with the exception of some elements (such as the maxilla, parts of the dentary, and braincase) that were separated from the main block by erosion. A digital reconstruction, based on RAM 14000 with missing sections modeled after juvenile corythosaurins, is presented in Fig. 6. Measurements are included in Tables 3\u20135 In lateral view (Fig. 7), the skull has a profile typical of a juvenile hadrosaur \u2013 squared caudally and triangular rostrally. The orbit is proportionately large and slightly longer than tall. The laterotemporal fenestra is inclined caudally and quite narrow, with a slight constriction at its midpoint. Because the midline of the skull is missing, the exact shape of the dorsotemporal fenestra is unknown. However, the preserved portion is roughly trapezoidal. Individual bones and skull regions are described below. Premaxilla. The premaxilla is the most prominent cranial bone in lateral view, extending from the upper \u201cbeak\u201d to the dorsum of the skull. The bone is roughly divisible into three portions: a lower portion including the oral margin and naris as well as caudodorsal and caudolateral processes that form the remainder of the premaxilla and much of the crest. The rostroventral-most segment of the premaxilla forms the dorsal oral margin. In lateral view (Fig. 7), most of the edge of the beak is straight and only slightly inclined (relative to the maxillary tooth row), contrasting with the more inclined surface seen in most other lambeosaurine specimens (Evans, 2010), including Parasaurolophus walkeri (ROM 768). Furthermore, the caudal corner of the beak is sharply hooked to form a tab-like process below a broadly concave postoral margin. Although this process occurs to varying degrees in many lambeosaurines of all ontogenetic stages (Evans, 2010), the condition in RAM 14000 is unusually prominent and most similar to that in Parasaurolophus walkeri (Parks, 1922; Sullivan and Williamson, 1999), particularly in the combination of the tab-like process and rounded 232 233 234 235 236 237 238 239 240 241 242 243 244 245 246 247 248 249 250 251 252 253 254 255 256 257 258 259 260 261 262 263 264 265 266 267 268 269 270 271 272 273 274 275 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t postoral margin. The only major difference is that the concavity in the postoral margin is sharper in ROM 768 (Parasaurolophus walkeri) than in RAM 14000. Measuring from the midline, the mediolateral width of the oral margin is estimated at 26 mm, and the estimated entire width of the free oral margin (perpendicular to the midline) is thus 52 mm. The oral margin is fairly uniform in outline, with no major denticulations in evidence. The lower portion of the premaxilla encloses the naris. The dorsal margin of the bone is eroded away, but its impression is preserved along the narial margin. The naris is roughly lenticular, rounded at its distal (rostroventral) end and pointed at its proximal (caudodorsal) end. The depression in the lateral surface of the premaxilla that houses the naris is delimited from the rest of the skull by a gentle ridge that is most prominent caudodorsally. The caudolateral process of the premaxilla forms the ventral margin of the naris and extends caudolaterally. Dorsally, the process contacts the caudodorsal process of the premaxilla. Although much of this suture is extremely fragmented, it appears to be quite straight along its preserved portions (Fig. 7A). This contrasts with the more sinuous suture seen in juvenile and adult Hypacrosaurus, Corythosaurus, and Lambeosaurus (Evans, 2010; Brink et al., 2011), but more closely matches the fairly straight suture (where it can be discerned) in specimens of Parasaurolophus (Sullivan and Williamson, 1999). Similarly, the sutures with the maxilla, lacrimal, and prefrontal, where they can be discerned, are straight, much closer to the condition in Parasaurolophus than in lambeosaurins. This may reflect the internal absence of an \u201cS-loop\u201d in the narial passages. The ventral portions of the process are comparatively narrow, but the process expands dorsally, where it forms part of the crest. The caudolateral process forms the ventral border of the premaxilla-nasal fontanelle, and presumably contacts the nasal at the caudal extent of the fontanelle. The caudodorsal process of the premaxilla, which forms much of the rostral profile of the skull, is poorly preserved. Its contact with the nasal cannot be interpreted with confidence due to extensive cracking, so no further comment will be offered here. Nasal. Much of the nasal is poorly preserved in gross external view, with the exception of its suture with the frontal and a portion along the caudal margin of the crest (Fig. 7A). The nasal forms the rostrodorsal margin of the premaxilla-nasal fontanelle, as well as the caudal edge of the crest. The dorsal margin of the nasal is strongly rounded and almost horizontal, unlike the peaked margin seen in juvenile corythosaurins ROM 758 and 759 (Lambeosaurus sp. And Corythosaurus sp., respectively). The nasal\u2019s suture with the prefrontal is not readily visible, and the contact with the frontal is described with that element. The internasal suture in the crest is flat. Crest (premaxilla and nasal). The crest is roughly dome-shaped, with a broad and rounded profile. It is semi-circular in lateral view, with its midpoint rostral to the orbit (Fig. 7). Unlike adult lambeosaurines, including Parasaurolophus, the crest does not overhang the frontal. Based on the position of the premaxilla-nasal fontanelle, and its relationships in corythosaurins, the nasal is inferred to be the bone that bounds the dorsal and caudal margins of the crest (Fig. 7A). The presence of a premaxilla-nasal fontanelle contrasts with its absence in adult Parasaurolophus and Hypacrosaurus altispinus of all ontogenetic stages, but is similar to juvenile Corythosaurus, Lambeosaurus, Hypacrosaurus stebingeri, and \u201cProcheneosaurus convincens\u201d (Rozhdestvensky, 1968; Horner and Currie, 1994; Evans et al., 2005; Brink et al., 2011). Unlike juvenile corythosaurins or \u201cP. convincens\u201d, the fontanelle is exceptionally 276 277 278 279 280 281 282 283 284 285 286 287 288 289 290 291 292 293 294 295 296 297 298 299 300 301 302 303 304 305 306 307 308 309 310 311 312 313 314 315 316 317 318 319 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t dorsally-placed relative to the rest of the crest in RAM 14000. In dorsal and rostral view (Fig. 8A\u2013D), the margins of the crest are strongly rounded. The caudal margin is only gently tapered. This contrasts with the condition in both juvenile and adult corythosaurins (Corythosaurus, Lambeosaurus, and Hypacrosaurus), in which a thin flange of bone projects from the caudal edge of the crest (Weishampel, 1981b; Evans et al., 2009). In these animals, the flange of bone is not occupied by the nasal passages. In RAM 14000, the nasal passages fill nearly the entirety of the crest, similar to the condition in adult Parasaurolophus (Weishampel, 1981b; Sullivan and Williamson, 1999). Furthermore, the crest in RAM 14000 is quite broad, whereas the crest is also fairly narrow along its length in juvenile and adult corythosaurins. Nasal cavity. The nasal passages are preserved only on the left side and were studied by gross examination of broken surfaces as well as using CT scans (Fig. 9, Supplemental Fig. S1). Terminology for anatomical structures follows that of Evans et al. (2009) and Weishampel (1981b). The airway closest to the external naris is termed \u201cproximal,\u201d and the airway furthest from the naris and closest to the internal choanae is termed \u201cdistal.\u201d Portions of the nasal passages and their surrounding bones, particularly the interval immediately caudal to the external naris, are heavily fractured. Furthermore, it appears that some areas were not completely ossified at the time of death, and we hypothesize that some aspects of the chambers may have become more prominently separated later in ontogeny. Thus, we must emphasize that aspects of our digital reconstructions may be subject to alternative interpretation. Points of particular concern are noted as such at the appropriate points in the description. The external naris is ovoid and strongly elongated (Fig. 7). Part of the main airway distal to this point is fragmented and poorly preserved, but has been reconstructed based on the CT scan data as well as physical examination of the specimen itself. The reconstruction shows the airway to be straight in lateral view (Fig. 7A\u2013C), with no evidence for an S-loop as seen in corythosaurins of all known post-embryonic stages (Horner and Currie, 1994; Evans et al., 2009). It is possible that the S-loop simply wasn't preserved, but based on the contours of the better-preserved distal airway, we do not consider this particularly likely. The main airway progresses in the segment known as the dorsal ascending tract (Weishampel, 1981b) and continues to the apex of the crest (Fig. 9D,E), measuring 170 mm from the proximal end of the airway to the summit of the dorsal ascending tract. At a sharp U-bend, the airway enters the section known as the ventral ascending tract (Fig. 9D,E), which drops ventrally to enter the main body of the skull. The ventral ascending tract is much shorter than the dorsal equivalent, only 33 mm long. In corythosaurins, this communication between the main airway and the rest of the skull is reconstructed to occur at the midline via a common median chamber (Evans et al., 2009). By contrast, the airway of RAM 14000 enters the skull separately on both right and left sides, as is more usual for tetrapods. The common median chamber is clearly separated from the ventral aspects of the skull by a thin lamina of bone (preserved as an impression visible in medial view as well as a small piece of bone visible in CT scan; Figs. 9D,E,M and10). The common median chamber of the nasal airway is directly visible on the broken medial surface of the left half of the skull (Figs. 9D,E and 10). In profile, this chamber is oval and rostrocaudally elongated (25.5 mm long by 15 mm tall). It is positioned just above the level of the dorsal margin of the skull roof, at the very lower edge of the crest. Relative to the orbit, the 320 321 322 323 324 325 326 327 328 329 330 331 332 333 334 335 336 337 338 339 340 341 342 343 344 345 346 347 348 349 350 351 352 353 354 355 356 357 358 359 360 361 362 363 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t common median chamber is dorsal and slightly rostral. The lateral diverticulum is prominent, shaped approximately like a shepherd's crook and coiled clockwise in left lateral view (Fig. 9A\u2013C). An incompletely ossified lamina separates the diverticulum from the main airway (Fig. 9I\u2013K); proximally, this coincides with a lamina of bone that may represent the premaxilla-nasal suture. Ventrally, the lateral diverticulum appears to communicate with the main nasal airway within the skull (Fig. 9M). In corythosaurins, the lateral diverticulum does not communicate directly with the main airway in the skull, but is separated by a bony lamina. We hypothesize that a similar condition occurred in RAM 14000, but that the lamina was not completely ossified at the ontogenetic stage represented here. Density differences in the sediment are faintly visible in CT scan along this line. These are not definitively bone, and the morphology is suggestive of a soft tissue pattern that may have been preserved through early infilling of the skull by sediment (Daniel, 2012). As interpreted here, the lateral diverticulum diverges from the main airway approximately halfway between the external naris and the common median chamber (Fig. 9C). This is a much more proximal origination than in Corythosaurus (subadult CMN 34825 and juvenile ROM 759) and Lambeosaurus (juvenile ROM 758), but matches the condition seen in Hypacrosaurus (adult ROM 702). Thus, the lateral diverticulum is quite extensive in RAM 14000. Unlike Hypacrosaurus, however, the lateral diverticulum is not positioned ventrally to the main airway at any point; the two passages are genuinely parallel (as reconstructed for adult Parasaurolophus; Weishampel, 1981b). The apex of the lateral diverticulum opens to the premaxilla-nasal fontanelle. Thus, the lateral diverticulum is bordered primarily by the premaxillae, with a small contribution from the nasals. Compared to reconstructions for Parasaurolophus cyrtocristatus and P. walkeri (Weishampel, 1981b), RAM 14000 displays several important departures from the adult condition (Fig. 11). Corresponding to the small crest, the nasal passages are much shorter in overall length. Unlike adult specimens, the ventral ascending tract of the nasal passages of RAM 14000 is quite shortened relative to the dorsal ascending tract. Furthermore, the lateral diverticulum of RAM 14000 is virtually the same length as the dorsal ascending tract. In adult P. cyrtocristatus and P. walkeri, the lateral diverticulum only extends slightly past the midpoint of the crest (Fig. 11A), and is reconstructed as a blind-ended chamber (Ostrom, 1963; Weishampel, 1981b). This reconstruction may need to be revised with CT scan data. The hooked morphology of the lateral diverticulum in RAM 14000 is reminiscent of the condition reconstructed for P. tubicen (Sullivan and Williamson, 1999). The olfactory region of RAM 14000, as in juvenile corythosaurins (ROM 758, 759), is a subdivision of the nasal cavity located rostral to the olfactory bulbs and caudal to the entrance of the main airway to the respiratory region contained within the bulk of the skull (\u201cantorbital region\u201d; Fig. 9C,H). In lateral view, the olfactory region is strongly dorsally arched and approximately level with the rostral half of the orbit (Fig. 9B,C), as seen in other corythosaurins for which data are available. In dorsal view (Fig. 9F\u2013H), the olfactory region is less strongly tapered caudad than in corythosaurins (ROM 758, 759; CMN 34825). Maxilla. Like other hadrosaurids, the maxilla is triangular in lateral view (Figs. 7 and 12D), apparently with a straight suture with the premaxilla (unlike some corythosaurins; e.g., Hypacrosaurus altispinus, ROM 702). Fracturing and weathering obscure many additional details. The prominent ectopterygoid ridge extends from the base of the maxilla\u2019s dorsal process 364 365 366 367 368 369 370 371 372 373 374 375 376 377 378 379 380 381 382 383 384 385 386 387 388 389 390 391 392 393 394 395 396 397 398 399 400 401 402 403 404 405 406 407 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t to the caudal edge of the maxilla (Fig. 12D). A marked ventral curvature in the ridge from rostral to caudal corresponds with the shape of the ectopterygoid. Along the flattened medial surface of the maxilla, a series of alveolar foramina, one between each alveolus, forms a dorsally-arched sequence (Fig. 10). A subtle ridge, increasing in prominence caudally, occurs immediately dorsal to the foramina and continues at least for the rostral third of the maxilla; the caudal extent is obscured by fracturing. This morphology can only be evaluated on the left maxilla; the medial surface of the right maxilla is too poorly preserved. CT scans indicate approximately 20 tooth positions in the maxillary tooth row, with two teeth in each file. The greatest internal height of the tooth file is 20 mm at the middle of the bone, and the smallest height is 8 mm at the rostral margin. As exposed on the left maxilla, there were usually two functional teeth on the wear surface at a time. The wear surfaces on each functional tooth range from 4 to 7 mm tall and 3 to 5 mm wide, and the maximum height of the wear surface as exposed at alveolus 5 is 15 mm. Adult Parasaurolophus have 40 or more tooth positions in the maxilla (NMMNH P-25100, PMU.R1250; Sullivan and Williamson, 1999), twice the number in RAM 14000. This low tooth count is typical of juvenile hadrosaurids (Suzuki et al., 2004). Jugal. Although the left jugal is more complete, crushing obscures the sutures along the rostral margin (Fig. 7). The right side preserves the impressions of these sutures (Fig. 13B,D), and the following description is thus a composite of both sides. The jugal forms part of the rostral margin and the entire caudal margin of both the orbit and infratemporal fenestra. The rostral process, along its contact with the maxilla and lacrimal, is triangular and sharply pointed (Fig. 13B). The ventral edge of this rostral process is longer than the dorsal edge, unlike most corythosaurins of various ontogenetic stages (in which the ventral edge is equal to or shorter in length to the dorsal edge) but similar to the condition in Parasaurolophus walkeri (ROM 768) as well as a larger juvenile Parasaurolophus sp. (SMP VP-1090). A distinct, slightly constricted extension occurs at the rostral end of this rostral process, visible as an impression on the right side, which creates a hooked ventral margin on the process. The postorbital process is inclined parallel to the quadratojugal process and tapers along the infratemporal fenestra towards an articulation with the descending process of the postorbital. The quadrate process is tapered and caudodorsally inclined at a 40\u00ba angle. Its caudodorsal edge is exceptionally pointed compared to other lambeosaurines, and is not expanded relative to the rest of the process as in \u201cProcheneosaurus convincens\u201d. The jugal is dorsoventrally constricted ventral to the orbit (19 mm tall) and on the quadrate process ventral to the infratemporal fenestra (22 mm tall). Similar constrictions are also seen in Corythosaurus, Lambeosaurus, and other Parasaurolophus (Evans, 2010). The angle between the postorbital and quadrate processes is quite tight, similar to the condition in Hypacrosaurus, Parasaurolophus, and \u201cP. convincens\u201d (Rozhdestvensky, 1968). As preserved, the jugal forms only the ventral third and quarter of the rostral and caudal margins of the laterotemporal fenestra, respectively (Figs. 7 and 13). Quadrate. The quadrate is complete on both sides, but the right quadrate is slightly displaced ventrally and both quadrates are slightly displaced laterally. The quadrate forms the caudal margins of the infratemporal fenestra and the skull (Figs. 7 and 13). The dorsal condyle of the quadrate articulates with the squamosal cotylus, as is typical of hadrosaurids. Dorsal to its contact with the jugal, the quadrate is slightly concave caudally and is inclined caudodorsally at 408 409 410 411 412 413 414 415 416 417 418 419 420 421 422 423 424 425 426 427 428 429 430 431 432 433 434 435 436 437 438 439 440 441 442 443 444 445 446 447 448 449 450 451 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t 30\u00b0 relative to vertical. The ventral third of the quadrate is straight. The surface for articulation with the caudal process of the jugal is rostrally bifurcated, resulting in an S-shaped sutural surface (Fig. 7); the dorsal half of the quadrate tapers along the infratemporal fenestra towards this articulation. The dorsal condyle of the quadrate is triangular (with a rounded and medially directed apex) in dorsal view, whereas it is rounded in lateral view. The ventral end is rounded in lateral view and trapezoidal with a saddle-shaped articular surface in ventral view. The ventral condyle of the quadrate is 21.4 mm wide and 18.2 mm long on its lateral edge and 8.7 mm long on its medial edge, respectively. In caudal view, the quadrate is straight but slightly bowed medially (Fig. 8F,G). The quadrate articulates with the pterygoid wing rostromedially along a V-shaped suture, extending from the quadratojugal to the dorsal margin of the infratemporal fenestra (Fig. 10). The pterygoid flange of the quadrate is only partially preserved, forming a plate-like and slightly concave (in medial view) region of bone (Fig. 10). At its ventral third, the caudal edge of the quadrate is flattened; dorsally, the element\u2019s caudal edge tapers to a rounded ridge. Quadratojugal. The quadratojugal is not visible on the left side, but CT scans indicate that the rest of the element is displaced rostromedially relative to the jugal. The quadratojugal is a thin, sinuous and rostrally inclined element that rostrodorsally tapers to a point while buttressing the quadrate caudoventrally. Squamosal. The squamosal is thin and arched dorsally, with a concave quadrate cotylus on its ventrolateral surface (Fig. 12A). The prequadratic process is sharply pointed rostrodorsally. The postquadratic process has a straight rostral border and a convex caudal border that abuts the paroccipital process (Fig. 7). The squamosal forms the caudolateral margin of the supratemporal fenestra and the dorsal margin of the infratemporal fenestra. Measuring from its edge on the base of the paroccipital process to the dorsal margin of the squamosal, the element is 67 mm tall. The caudomedial corner of the squamosal hooks upward in lateral view, and the dorsal surface of the squamosal is entirely convex. The medial extent of the squamosals is not preserved, so we cannot determine if they contacted each other as in most corythosaurins and adult Parasaurolophus, or were separated by the parietals as in Velafrons (Gates et al., 2007; Brink et al., 2011). Lacrimal. The lacrimal forms the mid-rostral margin of the orbit. Sutures with the prefrontal are difficult to interpret, as are those with the premaxilla. Impressions on the right side (Fig. 13B) show that the lacrimal articulates ventrally with the jugal along a caudoventrally inclined, slightly ventrally convex suture. Postorbital. The postorbital is T-shaped in lateral view (Fig. 7), bounding part of the dorsal margin of the orbit and nearly the entire caudal margin as well. The postorbital articulates with the prefrontal rostromedially along a straight suture and the frontal medially along a more sinuous suture (Fig. 8D). The jugal process is slightly curved rostrally and forms most of the rostrodorsal margin of the infratemporal fenestra, tapering alongside the caudal towards articulation with the ascending process of the jugal. The caudal process of the postorbital measures 13 mm wide at its narrowest point, but broadens caudally. The caudal-most portion of the caudal process thins and splits into dorsal and ventral prongs (Fig. 7A), as in Parasaurolophus and corythosaurins except for Hypacrosaurus altispinus (Evans, 2010); the ventral prong is more extensive. This process overlaps the dorsal surface of the squamosal, and forms a small part of the rostrolateral margin of the supratemporal fenestra. In lateral view, the dorsal edge of the postorbital is slightly concave, unlike the convex margin in P. walkeri (ROM 452 453 454 455 456 457 458 459 460 461 462 463 464 465 466 467 468 469 470 471 472 473 474 475 476 477 478 479 480 481 482 483 484 485 486 487 488 489 490 491 492 493 494 495 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t 768). The maximum length of the jugal and caudal processes are roughly equal, similar to corythosaurins of various sizes, but unlike adult Parasaurolophus (where the jugal process is longer; NMMNH P-25100, ROM 768) or Charonosaurus (where the caudal process is longer). Consequently, the proportion of the skull roof in RAM 14000 formed by the postorbital is much greater than that formed by the squamosal in lateral view (Fig. 7A), unlike adult Parasaurolophus. Frontal. The left frontal is nearly completely preserved with visible sutures, except for its extreme caudomedial portion (Fig. 8C,D). In dorsal view, the frontal articulates with the prefrontal rostrolaterally along a straight suture that trends laterally along its caudal extent. The suture with the postorbital is comparatively straight, with a slight medial trend from rostral to caudal. The contact with the parietal is obscured, but a small portion of the frontal\u2019s contribution to the dorsotemporal fenestra is visible. The paired nasals form a triangular prong that laps onto the rostral end of the dorsal surface of the frontals (Fig. 8D). This morphology is unique relative to corythosaurins and Parasaurolophus, where the sutures can be determined (Evans et al., 2007; Brink et al., 2011). Adult and sub-adult Parasaurolophus have a nasofrontal suture that is expanded caudodorsally and sharply angled relative to the rest of the skull roof (Evans et al., 2007); there is no evidence in CT scan or direct visual observation of such a feature in RAM 14000. Thus, the condition here is comparable to the state in corythosaurin juveniles and adults. Similarly, the individual frontal in RAM 14000 is approximately as long at the midline (measuring from the caudal extent of the nasal suture to the rostral extent of the parietal suture) as it is wide (34.2 mm vs. 31.7 mm, a ratio of 1.08; doubling to approximate both frontals produces a ratio of 0.54). The median frontal dome is thus fairly elongate (Fig. 7). This too contrasts with the condition in adult and sub-adult Parasaurolophus (where the frontal is wider than long) and is more similar to the state in corythosaurins of various growth stages (Evans et al., 2007). Similar to other lambeosaurines, the frontal does not reach the orbital rim. Prefrontal. Only the sutures on the caudal edge of the left prefrontal are clearly visible (Figs. 7 and 8C,D). Here, the bone forms a triangular point interposed between the medial margin of the postorbital and the lateral margin of the frontal, as in other lambeosaurines. The bone forms the rostrodorsal margin of the orbit, and contacts the lacrimal ventrally. Based on the extent of the premaxilla, it is unlikely that the prefrontal formed any significant portion of the crest in RAM 14000 (unlike adult lambeosaurines but similar to many subadult specimens; Evans et al., 2005). Ectopterygoid. The ectopterygoid sits atop the caudodorsal margin of the caudal process of the maxilla, extending medial to the coronoid as viewed on CT scans. The element is best-preserved on the right side (Fig. 12D), showing that the ectopterygoid is a thin and broad element with a prominent ventral bend at its caudal third. The medio-lateral width of the ectopterygoid and its relationship to structures such as the pterygoid cannot be visualized because of weathering. Pterygoid. The pterygoid is visible only on the left side (Fig. 10), with just its caudal quadrate wing preserved. The wing is thin (<1 mm) and gently concave medially, paralleling the corresponding medial surface of the quadrate ramus. As viewed in CT scan, the nearly complete pterygoid on the right side is typical of the condition expected for hadrosaurids (Ostrom, 1961; Heaton, 1972). Palatine. The palatine is not sufficiently preserved or exposed to comment upon its 496 497 498 499 500 501 502 503 504 505 506 507 508 509 510 511 512 513 514 515 516 517 518 519 520 521 522 523 524 525 526 527 528 529 530 531 532 533 534 535 536 537 538 539 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t morphology. Vomer. The caudodorsal portion of the vomer is exposed on the left half of the skull (Fig. 10). The preserved dorsal edge is acutely angled, and the rostral edge of the element tapers rostrolaterally towards its (inferred) insertion between the premaxillae. The apex of the vomer is located just rostral to the rostral end of the orbit, at approximately the same height (dorso-ventral level). The vomer is not sufficiently preserved for detailed comparison with other hadrosaurids. Braincase. Most of the braincase was partially disarticulated from the rest of the skull by weathering, and the right side was prepared out to show relevant details (Fig. 14). Additional features are seen as impressions on the right skull block (Fig. 13B,D). This section describes only visible features. Additional internal details were reconstructed from CT scans, and are described in the section on the endocast. With the exception of the sutures between the exoccipital and basioccipital on the occipital condyle, sutures within the braincase are not visible due to crushing and weathering. The parasphenoid, represented by an impression, is 28 mm long, gently arched along its length, and tapered to a point at its rostral end (Fig. 13B,D). It terminates just caudal to the midpoint of the orbit. A shallow sulcus occupies the lateral surface of the bone. Faint impressions tentatively identified as presphenoid occur dorsal to the parasphenoid, but no notable details are visible. The form is generally similar to that seen in P. tubicen (NMMNH P-25100, PMU.R1250). A foramen interpreted as that for cranial nerve XII (hypoglossal nerve) is small (1.9 by 2.2 mm) and located roughly midway between the caudal extent of the occipital condyle and a ridge of bone that slants caudodorsally along the braincase (Fig. 14). Additional foramina may have occurred also, as in Hypacrosaurus altispinus (Evans, 2010), but cannot be confirmed in the specimen\u2019s current state of preparation and preservation. A portion of the trigeminal foramen is exposed at the front of the right side of the isolated braincase (Fig. 14), and the remainder of the impression is seen on the right skull block (Fig. 13C,D). This impression is triangular, measuring 11 mm long and 9 mm tall. Two distinct grooves (ridges on the natural mold) extend from the foramen; one trends directly rostrally from the rostral edge of the foramen (probably representing the path for CN V1), and the other trends rostroventrally from the ventral edge (representing the path for CN V2,3). The left caudal semicircular canal is exposed through a fortuitous break (Fig. 10). The maximum diameter of its lumen is 1.8 mm. The occipital condyle is roughly cardoid in caudal view, composed of the basioccipital at the ventral and ventrolateral edges and the exoccipitals at the dorsolateral edges (Fig. 14). All three elements are bulbous on their caudal edges. The rounded basal tuberosity has its maximum lateral extent slightly lateral to the extreme edge of the occipital condyle. In lateral view, the exoccipitals rise to bound the exposed portion of the foramen magnum, sweeping dorsally. The exoccipital and opisthotic are fused both in gross examination and CT scans. The most prominent and best-preserved aspect of these elements is the paroccipital process, which curves rostrally and tapers dorsoventrally along the caudal margin of the paroccipital process and upper squamosal (Figs. 7 and 8F,G). The caudal surface of the bones is remarkably flat, with only a slight concavity at its distal extent (Fig. 8F,G). The fenestra vestibuli (fenestra ovalis) measures approximately 5 mm tall by 2.6 mm long. The auditory recess is deepest and narrowest by the fenestra vestibuli, becoming broader and shallower dorsocaudally (Fig. 14). 540 541 542 543 544 545 546 547 548 549 550 551 552 553 554 555 556 557 558 559 560 561 562 563 564 565 566 567 568 569 570 571 572 573 574 575 576 577 578 579 580 581 582 583 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Dentary. The ramus of the left dentary has an average height of 27 mm. The edentulous process is roughly 25 percent of the dentary\u2019s length, and the rostral border of the process is rostroventrally-inclined (Fig. 7). The ventral border of the dentary is relatively straight, with comparatively little declination at its rostral portion. This is comparable to the morphology in Parasaurolophus walkeri (ROM 768; Evans, 2010), but different from the more inclined morphology in P. tubicen (NMMNH P-25100), a dentary from the Fruitland Formation tentatively identified as juvenile Parasaurolophus sp. (SMP VP-1090; Sullivan and Bennett, 2000), and other lambeosaurines. The condition in P. cyrtocristatus is unknown. The lateral surface of the body of the dentary is strongly convex (Fig. 7). The coronoid process is perpendicular to the ventral margin of the dentary, and, based on CT scans and the incomplete dentary on the right half of the skull (Fig. 13B,D), reaches the ventral margin of the orbit when in articulation, roughly 72 mm above the ventral margin of the dentary. The rostral margin of the coronoid process is more prominently extended than the caudal process. Rostrally, the dentary tapers to articulate with the caudal margin of the predentary. Caudally, the dentary articulates with the surangular along a sinuous suture (Fig. 7). The number of dentary teeth cannot be determined. Predentary. Only the left side of the predentary is preserved (Figs. 7 and 8A,B), but the element can be mirrored to reconstruct the overall shape. In dorsal view, the element would have been roughly horseshoe-shaped, with a moderately convex rostral margin. As exposed at the midline, the cross-section of the rostral portion is approximately triangular (Fig. 10). The dorsal triturating surface is approximately 14 mm long and only slightly rostrally inclined. This inclination becomes more extreme towards the lateral and caudal wings of the predentary, so that the triturating surface is nearly vertical and laterally facing (14 mm tall) at its caudal end. Thus, the surface only changes its orientation and not its width. The ventral surface of the predentary is gently convex. The caudal edge of the lateral wing of the predentary is forked; the ventral process of this fork is slightly longer and more sharply pointed (Fig. 7). This is in contrast to the unforked lateral wing in the holotype of P. walkeri, ROM 768, but similar to other lambeosaurines. The morphology is not known in other species of Parasaurolophus. The median process of the predentary is not definitively preserved in RAM 14000. Surangular. The surangular (Figs. 7 and 13A,C) buttresses the caudal margin of the coronoid process, with a smoothly continuous lateral surface at this point. A ridge at the base of the contribution to the coronoid process continues onto the lateral edge of the articular surface for the quadrate. This coronoid process is also relatively broader than in ROM 768 or NMMNH P-25100. The surangular\u2019s ventral margin is slightly convex, with a strong curvature caudally on the articular process. The surangular receives the ventral condyle of the quadrate and articulates with the angular caudomedially. The retroarticular process of the surangular is thinner and more horizontal than in P. walkeri (ROM 768). Angular. The angular is a flattened bone that curves caudodorsally and articulates medially with the surangular. On both sides, the element has been displaced downward so that its ventral margins are visible beyond that of the surangular (Figs. 7 and 13A,C). It is inferred to receive the distal end of the quadrate. In ventral view, the element is long and narrow. Hyoid. A bone interpreted as the first ceratobranchial are positioned immediately ventral to the surangular (Figs. 7 and 13A,C); the right first ceratobranchial is slightly better preserved. The element is partially exposed, and described from gross examination as well as CT scan 584 585 586 587 588 589 590 591 592 593 594 595 596 597 598 599 600 601 602 603 604 605 606 607 608 609 610 611 612 613 614 615 616 617 618 619 620 621 622 623 624 625 626 627 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t reconstructions (Fig. 12B,C). Although the ceratobranchials of hadrosaurids (including Hypacrosaurus sternbergii, adults of Saurolophus osborni, Lambeosaurus lambei, and Corythosaurus casuarius, as well as juveniles of Hypacrosaurus altispinus and H. stebingeri) previously have been described as generally uniform (Ostrom, 1961; Gates et al., 2007; Brink et al., 2011), the morphology of these elements in RAM 14000 has some unique aspects. These differences may be taxonomic or perhaps ontogenetic. However, the hyoids of embryonic H. stebingeri (RTMP 89.79.52) are quite similar to those of Corythosaurus in major details, so we posit that taxonomic differences are most influential here. The preserved portion of each ceratobranchial in RAM 14000 is gently arched ventrally, with a slight mediolateral curvature. The caudal portion is dorsoventrally flattened (rather than cylindrical, as described for other hadrosaurids; Ostrom, 1961). Rostrally, the bone twists so that it is mediolaterally compressed at the rostral-most preserved portion. Extremely expanded rostral ends, characterizing other known hadrosaurid ceratobranchials, are not evident; they may be eroded away in RAM 14000. The ceratobranchial approximately 43 mm long, as preserved. Endocast. A partial cranial endocast for RAM 14000 was reconstructed from CT scan data (Fig. 15, Supplemental Figs. S1 and S2), the first ever for Parasaurolophus of any ontogenetic stage. The endocast was reconstructed in two sections, one on the portion of the braincase articulated with the left half of the skull (Supplemental Fig. S1), and the remainder on the disarticulated portion of the braincase (Supplemental Fig. S2). Their relative position was then approximated based on cranial landmarks and comparison with other hadrosaurids. Because of weathering, many of the smaller neurovascular canals and foramina could not be discerned with confidence. The overall shape of the endocast is broadly similar to that previously described for juvenile and adult lambeosaurines (Evans, 2006; Evans et al., 2009). In dorsal view, the cerebrum is strongly expanded laterally (Fig. 15B), with an estimated width across the midline of 36 mm, dorsoventral height (perpendicular to the aforementioned width) of 28 mm, and an estimated cerebral length of 39 mm. In lateral view (Fig. 15A), the cerebrum is very strongly arched, much more so than in larger juvenile (Lambeosaurus sp., ROM 758; Corythosaurus sp., ROM 759), subadult (Corythosaurus sp., CMN 34825), or adult (Hypacrosaurus altispinus, ROM 702) corythosaurins. This may in part be due to the young ontogenetic status of RAM 14000, in that the frontals (and hence cerebra) are more strongly arched in young individuals (e.g., Hypacrosaurus stebingeri, MOR 548). The olfactory bulb endocast is a maximum of 14 mm across. As reconstructed, the olfactory bulbs are approximately half the thickness of the cerebrum in lateral view, and are depressed considerably below the cranial roof (frontal, in this case), particularly at their origin (Fig. 15A,B). Angulation between the cerebrum and postcerebral region cannot be determined with confidence. The postcerebral region (a term used here because the cerebellum itself is not well represented in hadrosaurid endocasts; Evans, 2006) is much narrower and deeper than the cerebrum (Fig. 15A,B). The ventral margin is broadly rounded in lateral view, contrasting with the straighter margin seen in corythosaurins (Evans et al., 2009:fig. 7). The dorsal margin of this region is much more sharply angled (approximately 90\u00b0) than in larger corythosaurins (e.g., around 120\u00b0 in subadult Corythosaurus sp., CMN 34825). Whether this results from ontogenetic, phylogenetic, or individual differences can only be tested with a larger sample. The endosseous labyrinth is best-preserved on the right side, although not all aspects of 628 629 630 631 632 633 634 635 636 637 638 639 640 641 642 643 644 645 646 647 648 649 650 651 652 653 654 655 656 657 658 659 660 661 662 663 664 665 666 667 668 669 670 671 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t the labyrinth could be traced continuously on the CT scan data (Fig. 15C\u2013F and Supplemental Fig. S2). The rostral semicircular canal is only slightly taller than the caudal semicircular canal (when the lateral canal is oriented horizontally; Fig. 15D), a less marked size disparity than seen in ontogenetically older corythosaurins (Evans et al., 2009: fig. 8). We estimate the maximum breadth of the rostral canal at 11 mm (from ampulla to crus communis), and that for the caudal canal at 10.5 mm (from ampulla to crus communis). Between its bounding ampullae, the lateral semicircular canal spans approximately 9 mm (Fig. 15C). The rostral canal has the tightest arch whereas the caudal canal is broadest, and the lateral semicircular canal is the smallest. The lateral ampulla is the largest of the three. From the foramen vestibuli, cochlea is estimated to be approximately 7.6 mm long. Note that the ventral margins of the cochlea are poorly visible on the CT scans (Fig. 15), and thus this measurement should be considered only an approximation. The endolymphatic duct is not clearly visible. Overall, the morphology of the endosseous labyrinth is broadly similar to that described for other hadrosaurids (e.g., Ostrom, 1961; Evans et al., 2009). Stapes. The left stapes of RAM 14000 is immediately caudal to the quadrate and pterygoid and rostral to the paroccipital-opisthotic process (Fig. 10), consistent with the position in adult Corythosaurus casuarius AMNH 5338 (Colbert and Ostrom, 1958). The proximal end of the stapes is presumed missing, probably due to post-depositional separation of the braincase. The remaining structure suggests that the stapes was a cylindrical, rod-like element. The bone is slightly bent mediolaterally, probably from taphonomic deformation. The maximum preserved length is 12.5 mm, whereas the maximum width is between 0.6 and 0.8 mm (with the widest portion proximally; i.e., towards the braincase), suggesting a slight tapering of the bone laterally (away from the braincase). The distal end of the stapes is positioned 8 mm dorsal to the ventral tip of the paroccipital-opisthotic process. postcranial axial skeleton : Vertebrae. The vertebral column is poorly preserved, with many details obscured by fragmentation of the bones and matrix. Thus, the following description is necessarily incomplete. We are unable to evaluate neurocentral fusion in any vertebrae, although we do note that the sacral ribs are not fused to the sacral vertebrae. Measurements are presented in Table 6. The complete count of cervical vertebrae cannot be determined, because the most caudally-placed cervicals are missing (Fig. 13). Individual components of the atlas are unfused and partially exposed (Figs. 13 and 14). The atlas intercentrum, as exposed, is triangular in cross-section, with a sharp ventral keel (Fig. 14). Its caudal, dorsal, and cranial edges are not exposed, so the nature of their articulations is not known. The odontoid (atlas centrum) is partially exposed and globulose, showing a convex cranial margin and a concave caudal margin (Fig. 14). The fragmentary neural arch for the atlas shows no remarkably morphology. An impression of the neural spine of the axis (C2; Fig. 13B,D) shows the element to be tall (~26 mm) and elongate (exact length uncertain). In the cervicals for which a centrum is preserved (?C4-?C7), the centrum is strongly opisthocoelous and sharply pinched in medio-lateral cross-section, with a strong ridge on the lateral surface of the centrum (Fig. 13A,C). The dorsal edge of the lamina connecting the zygapophyses is strongly arched, and the diapophyses in the middle of the cervical vertebral series project laterally with a ventral inclination from medial to lateral. The tips of the 672 673 674 675 676 677 678 679 680 681 682 683 684 685 686 687 688 689 690 691 692 693 694 695 696 697 698 699 700 701 702 703 704 705 706 707 708 709 710 711 712 713 714 715 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t diapophyses are at approximately the upper half of the centrum. The vertebrae themselves are partly eroded, so little more can be said about their morphology. The dorsal vertebrae are poorly preserved (Figs. 2, 3, and 13). There were at least 17 dorsal vertebrae (determined by counting the centra, exposed transverse processes, and ribs), but the exact count is unknown. Impressions of the neural spines for three cranial dorsals show the spines to be strongly caudally inclined, mediolaterally compressed, and craniocaudally narrow (Figs. 13B,D and 16A). The associated transverse spines for these vertebrae are triangular in lateral view and rounded along their lateral extrema (Fig. 13A,C). Centra are visible (but poorly preserved) only for the caudal dorsals; here, the centra are slightly taller than long. The sacrum is neither well exposed nor well-preserved. The fragmentary neural spines are erect and straight (Fig. 3). The caudal vertebrae are best exposed on the left side (Fig. 3), but poorly-preserved. As articulated, the series of caudal centra is gently arched, with an overall ventral concavity along its margin. In contrast with the neural spines of the sacral vertebrae, the preserved neural spines of the cranial caudal vertebrae are distinctly curved. The proximal portion (nearest the neural arch) projects caudally at approximately 45\u00ba, and then curves dorsally at its distal two-thirds. Thus, the cranial margin of the neural spine is concave and the caudal margin convex. The neural spines at the cranial end of the tail are quite tall relative to the centra, as is typical for hadrosaurs. Moving distally along the tail, the neural spines lose their curvature by approximately caudal 8. This contrasts with P. cyrtocristatus, in which the neural spines maintain their curvature at least through the middle section of the tail (Ostrom, 1963). The transverse processes are most pronounced in the cranial caudal vertebrae, becoming successively less prominent distally. By caudal 13 or 14, the transverse processes are gone. A total of 19 centra are visible, and they exhibit the typical hexagonal shape of hadrosaurids. Assuming a typical caudal vertebral count and proportion of the tail for lambeosaurines (see data in Lull and Wright, 1942), just under half of the physical length of the tail is preserved in RAM 14000, and perhaps another 30 to 40 additional vertebrae are missing. Ribs. Cervical ribs are visible on the fourth through seventh cervical vertebrae (Fig. 13A,C). The fourth cervical rib is tripartite, with a rounded capitulum and a tab-like tuberculum of approximately the same size. The shaft of the rib is short and triangular in cross-section, with a distinct flange on its lateral surface. This flange terminates in a discrete knob on the lateral surface of the proximal end of the rib, equidistant between the capitulum and tuberculum. Both the ridge and the knob become less pronounced on the successive two cervical ribs (with C5 and C6) and are entirely absent by C7. Similarly, the tuberculum becomes successively less pronounced relative to the capitulum on the ribs associated with C5 and C6. All of the preserved cervical ribs are short, no longer than the centra of their associated vertebrae. In general, the cervical ribs are less expanded distally than seen in adult P. walkeri, ROM 768 (Parks, 1922: plate VII, fig. 1). In this specimen, the ends are expanded so as to be somewhat paddle-shaped. Thirteen dorsal ribs are preserved with RAM 14000 (Figs. 2 and 13); unless one more was disarticulated from the specimen prior to burial, this is the complete count. The first three ribs drastically increase in size successively, and the third rib is the longest by far. The fourth through seventh ribs are approximately the same length, with a drastic, successive decrease in size for the eighth through eleventh dorsal ribs. The twelfth and thirteenth dorsal ribs are approximately the same size. The preserved portions of the first two ribs show that their shafts 716 717 718 719 720 721 722 723 724 725 726 727 728 729 730 731 732 733 734 735 736 737 738 739 740 741 742 743 744 745 746 747 748 749 750 751 752 753 754 755 756 757 758 759 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t are quite straight in lateral and cranial view. The third through tenth ribs are straight in lateral view but have a gentle medial concavity. The eleventh through thirteenth ribs are once again straight in lateral and cranial view. As a consequence of the flexion of the dorsal vertebrae, the first through eighth ribs converge upon each other distally. The ninth and tenth ribs are less convergent along their shafts, but appear to be mostly in natural position. The eleventh through thirteenth ribs are slightly disarticulated on the right (up) side, suggesting disturbance from scavengers or water currents prior to burial. The ribs on the left side are too fragmented to evaluate their anatomy. The first and second sacral ribs are visible on the right side (Fig. 2), with the first better exposed. The following description focuses on the first sacral rib. As with the caudal dorsal ribs, this sacral rib is slightly out of articulation. Its proximal end is strongly flared; the capitulum and tuberculum are connected by a thin web of bone. The distal termination of the rib flares slightly relative to the shaft, at approximately 17 mm wide. Both dorsal and ventral borders of the rib are concave, with the dorsal border more strongly so. Measurements for the ribs are presented in Table 7. Haemal arches. The haemal arches are fragmented. Only one cranial arch (perhaps with Ca6?) is sufficiently preserved for description (Fig. 3). This element is exposed along its lateral surface only, and the shaft of the bone is straight. appendicular skeleton : Pectoral girdle. The blades of both scapulae are preserved (Figs. 2 and 3), with the left more complete. Measurements are presented in Table 8. The scapular neck has a distinct constriction cranially, typical of lambeosaurines. However, the caudal expansion of the blade is less pronounced than in adult Parasaurolophus (FMNH P 27393, ROM 768). Overall, the scapula is more robust than seen in Corythosaurus, Lambeosaurus, or Nipponosaurus (Suzuki et al., 2004). The preserved ventral border of the left scapula is entirely intact in RAM 14000, whereas the dorsal border is less complete. Only the ventral border is intact on the right side; here, it is slightly sinuous, with an evident constriction at the cranial third of the element. No sternal elements are preserved. Pelvic girdle. The pubes are somewhat fragmented, but the general shape of the prepubic process (pubic blade) is intact (Figs. 2 and 3). The cranial end is dorsoventrally expanded (as is typical of lambeosaurines), with the ventral margin slightly more extended than the dorsal margin. The blade narrows caudally. A short segment of the postpubic rod is exposed (Fig. 2), showing that this was a thin process with morphology typical of lambeosaurines. The right ischium is represented by bone proximally and by impressions distally (Fig. 3). The dorsal acetabular process is longer and broader than the ventral, as seen in other hadrosaurids. The impression of the shaft is comparatively straight, showing that the shaft expands dorsoventrally towards its distal end. Unlike adult-sized Parasaurolophus cyrtocristatus (FMNH P 27393), the distal extremity of the ischium is not prominently hooked cranially. At most, there was only a slight expansion. A similar expansion of the distal hook during ontogeny occurs in Hypacrosaurus stebingeri (Horner and Currie, 1994), but in this taxon the hook develops at a comparatively smaller body size than that of RAM 14000. The ilium is well-preserved, particularly on the right side (Figs. 2, 17B, and 18D), but only the lateral surface is exposed. The caudal end is tapered, rather than tab-like and rounded as 760 761 762 763 764 765 766 767 768 769 770 771 772 773 774 775 776 777 779 780 781 782 783 784 785 786 787 788 789 790 791 792 793 794 795 796 797 798 799 800 801 802 803 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t seen in P. cyrtocristatus (Fig. 18C) or P. walkeri. Little ontogenetic change in the shape of the caudal end is evident in Hypacrosaurus stebingeri (Horner and Currie, 1994), so this may be due to taxonomic differences or individual variation. The lateral surface of the postacetabular process is slightly concave and strongly sloped laterally, so that the ventral edge is more laterally placed than the dorsal edge. The ventral edge of the postacetabular process is slightly concave, but the dorsal margin of the blade is nearly straight, up to the preacetabular blade. This contrasts with the prominent concavity seen dorsal to the supraacetabular process in other Parasaurolophus (FMNH P 27393, Fig. 18C; ROM 768); and development of the concavity seems to be an ontogenetic feature, more strongly pronounced in adults than juveniles (Guenther, 2009: fig. 9). The preacetabular blade is longer and more slender than the postacetabular blade, narrowing towards the cranial-most tip. The ventral edge of the preacetabular blade is broadly sinuous. Compared to adult Parasaurolophus, the preacetabular process is relatively shorter (Fig. 18C,D). The supraacetabular process protrudes laterally and is proportionately smaller than seen in adult Parasaurolophus (Fig. 18C,D). This too is a general ontogenetic trend across hadrosaurids (Guenther, 2009). The pubic peduncle has a gentle cranial slant and is more robust and better defined than the smoothly curved ischiadic peduncle. In between the peduncles the concavity of the acetabulum is shallow and hemielliptical in profile. Measurements for the pelvic girdle are presented in Table 8. Forelimb. The forelimbs are entirely missing, with the exception of an impression of the medial surface of the right humerus (maximum length=175 mm; Figs. 17A and 18B). The deltopectoral crest extends for more than half the length of the humerus (101 mm), with a slight inward curvature at the crest\u2019s midpoint. Compared to adult Parasaurolophus (e.g., P. cyrtocristatus, FMNH P 27393, Fig. 18A; P. walkeri, ROM 768), the overall form of the humerus in RAM 14000 is less sigmoidal and more slender (Fig. 18B), with a less prominent (but just as long) deltopectoral crest. This contrasts with Hypacrosaurus stebingeri, in which the humerus was reported to be \u201crelatively stout\u201d in juveniles versus larger specimens (Horner and Currie, 1994), and with negative allometry reported for the midshaft of the humerus in Maiasaura peeblesorum (Dilkes, 2001). Thus, RAM 14000 may suggest that Parasaurolophus departs from the expected allometric pattern for hadrosaurs. However, the specimen\u2019s slender appearance could be misleading if it only preserves a portion of the bone\u2019s profile. More specimens are needed to evaluate this hypothesis. The lateral distal condyle is more prominent than the medial condyle, but this is at least in part preservational. Measurements are presented in Table 9. Hind limb. The right femur is mostly exposed, although its caudomedial surface and parts of the distal condyles are partially obscured by rock (Figs. 2, 17C, and 18F). The head and greater trochanter are separated by a broad, v-shaped sulcus. The greater trochanter is prominent, with a flattened lateral surface and a broadly and convexly arched dorsal (proximal) margin in lateral view (Fig. 17C). The cranial trochanter extends for approximately one-fourth the length of the femur; this structure is a low and narrow process situated at the cranio-lateral surface of the greater trochanter. The shaft of the femur is straight, with the fourth trochanter centered at mid-shaft. The trochanter is clearly defined but relatively less prominent in terms of length and height than in adult lambeosaurines (e.g., P. cyrtocristatus, FMNH P 27393, Fig. 18E; P. walkeri, ROM 768). The medial and lateral distal condyles are not well-separated on their cranial surfaces, although a shallow depression occurs at the midline just dorsal to the condyles. 804 805 806 807 808 809 810 811 812 813 814 815 816 817 818 819 820 821 822 823 824 825 826 827 828 829 830 831 832 833 834 835 836 837 838 839 840 841 842 843 844 845 846 847 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t The tibia is a robust bone, approximately equal in length to the femur (Figs. 2 and 17D). The cnemial crest is prominent, extending for at least a third of the tibial shaft. The crest is hooked laterally, wrapping around the cranial surface of the fibula at its proximal end. Its proximal third is most robust and situated farthest from the main portion of the tibia, with the rest of the crest tapering gently towards the main shaft of the tibia. The distal end of the tibia is flattened caudally with a craniocaudal expansion relative to the mid-shaft in lateral view. A distinct ridge occurs on the caudo-lateral aspect of the distal quarter of the tibia. The proximal half of the shaft is gently concave in lateral view. The fibula (Figs. 2, 17D, and 18H), as is typical for hadrosaurs, is a slender bone that tapers distally. It is strongly mediolaterally compressed, particularly at the proximal half. The proximal articular end has a fairly linear profile in comparison to larger hadrosaurs, and the caudal edge of the shaft is also quite straight. The cranial edge is gently and broadly curved, particularly at the distal half. The distal end of the fibula is gently expanded and slightly hooked cranially, articulating tightly with the calcaneum. Overall, the element is less robust and has a less prominent distal curvature than seen in larger Parasaurolophus (e.g., FMNH P 27393, Fig. 18G). The calcaneum is articulated with the fibula, but only the lateral surface is exposed (Figs. 2 and 17D). It is slightly concave and has a kidney-shaped outline, with the convex end pointing distally. A small but bulbous lump of bone interposed between the distal articular surfaces of the calcaneum and astragalus may represent tarsal IV. The astragalus is insufficiently exposed to comment upon its morphology. The right pes is poorly exposed, and only digits III and IV are represented (Figs. 2, 3, and 19). Digit IV conforms to the standard hadrosaurid phalangeal count of five phalanges. The first phalanx (IV-1) is longest, and following three (IV-2, IV-3, and IV-4) are considerably shorter proximo-distally. The terminal phalanx (IV-5) is expanded into a triangular ungual. Digit III has a similar pattern (Fig. 19), with the most proximal phalanx (III-1) being longest, the next two (III-2 and III-3; Fig. 19A,B,D,E) quite abbreviated proximo-distally, and a terminal ungual (III-4). Each phalanx after the most proximal one is broader than long. The unguals in RAM 14000 are fairly narrow (Fig. 19C,F), lacking the broader expansion of adults. Measurements for the hind limb elements are presented in Table 9. ossified tendons : Ossified tendons or their impressions are visible at only two portions of the skeleton. The first set occurs lateral and ventral to the neural spine of the ?fourth dorsal vertebra (Fig. 16A). Two tendons are preserved here, both of which roughly parallel the long axis of the vertebral column. They are approximately 0.8 mm in maximum diameter, and the longest preserved segment is 21 mm long (including an impression of the tendon in the measurement. Both tendons occur on the lateral surface of the caudal quarter of the neural spine and just dorsal to the transverse process, and trend very slightly ventrally. The longest preserved one extends at least to the cranial quarter of the next spinous process. Based on the position and orientation of these tendons, we hypothesize that they represent portions of M. iliocostalis or potentially M. longissimus dorsi (Organ, 2006). A second set of ossified tendons, represented only by impressions, occurs ventral to the extrema of the impressions of the neural spines of vertebrae and dorsal to the fragments of the 848 849 850 851 852 853 854 855 856 857 858 859 860 861 862 863 864 865 866 867 868 869 870 871 872 873 874 875 876 877 878 879 880 881 882 883 884 885 886 887 888 889 890 891 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t transverse processes on the left side (Fig. 16B). The tendons themselves were destroyed by weathering prior to discovery. The exact position of the tendons in the vertebral column cannot be determined, but it is just dorsal to the cranial end of the ilium and thus at the very caudal end of the dorsal vertebrae or cranial end of the sacral vertebrae. At least seven parallel tendons occur here, with a maximum diameter of each impression 2.0\u20132.5 mm and the longest impression with a preserved length of at least 55 mm (and probably longer). The tendons were lateral to the neural spines, moving dorsally towards the caudal direction (i.e., caudodorsally inclined). Based on the position and orientation of these impressions, we hypothesize that they represent tendons of M. tendinoarticularis within M. transversospinalis (Organ, 2006). integument : Soft (non-bone) tissue impressions are preserved around the left foot and rostral end of the skull. Despite careful mechanical preparation with an aim to identify other areas of soft tissue preservation, no additional, unambiguous impressions were identified. Upper rhamphotheca. A series of parallel, dorsoventrally-oriented grooves rostral and ventral to the oral margin of the premaxilla (Fig. 8A,B,E) are interpreted as impressions of the internal surface of the upper rhamphotheca, in light of similarly-interpreted anatomy in other hadrosaurids (Morris, 1970). From the inferred midline, a total of eight grooves are preserved (Fig. 8E); they may have extended farther laterally. Each groove is 2.5\u20133.5 mm wide. In rostral view, the ventral edge of the series dips ventrally from medial to lateral. This suggests a broad, inverted \u201cV\u201d profile for the complete series when including both left and right sides of the skull. The greatest mediolateral width of the series is 38 mm. The greatest preserved dorsoventral depth of the preserved flutes is 16 mm, but their proximal and lateral portions were inadvertently prepared away. Thus, the distance between the oral margin of the premaxilla and the distal extremity of the rhamphotheca averaged around 25 mm. These impressions indicate that the soft-tissue profile of the oral margin extended significantly beyond the bone (Fig. 7A). This is consistent with previous reports of an internally-fluted beak that extended well beyond the premaxilla in Edmontosaurus annectens (Versluys, 1923; Morris, 1970). The margins of the premaxilla and impressions are closely parallel in E. annectens, indicating that bone shape is a fairly accurate proxy for soft tissue shape, and a similar pattern is supported by RAM 14000. A specimen of Corythosaurus casuarius (CMN 8676) originally preserved a portion of the impressions of the rhamphotheca (Sternberg, 1935). Initially interpreted as the lower rhamphotheca (Ostrom, 1961), we agree with later interpretations of the structure as the upper rhamphotheca (Morris, 1970). Only a fragment of this impression is now available. Based on the original photographs (Sternberg, 1935), the internal surface of the upper rhamphotheca was grooved as in RAM 14000. However, we cannot determine with confidence the shape of the margin of the rhamphotheca in CMN 8676 for comparison. Although such features are not evident in RAM 14000, projections from the oral margin of the premaxilla in many hadrosaurids may correlate with the grooves on the rhamphotheca. Additional work is needed to verify this. Skin impressions. Two small (<5 cm maximum dimension) patches of skin impressions are associated with the region caudal to the right metatarsal III and phalanx III-1 (Figs. 3 and 20). This impression is gently folded upon itself, and covered by non-imbricating, roughly circular tubercles that average ~2 mm in maximum diameter (Fig. 3; pebble-type basement 892 893 894 895 896 897 898 899 900 901 902 903 904 905 906 907 908 909 910 911 912 913 914 915 916 917 918 919 920 921 922 923 924 925 926 927 928 929 930 931 932 933 934 935 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t scales of Bell, 2012). The impression was exposed to weathering prior to discovery, and thus surface detail is muted. The overall appearance, including the folding, is reminiscent of the equivalent region in Corythosaurus casuarius (AMNH 5240; Brown, 1916). The only major difference in RAM 14000 concerns the smaller tubercles relative to AMNH 5240, which are undoubtedly related to the animal\u2019s small body size. Bone Histology NOTE TO REVIEWERS: To access high-resolution MorphoBank images, go to http://www.morphobank.org. Log in (upper right of page) by entering this information: Email address: 836 Password: baby We describe the histology of the tibia based on two samples from the caudolateral quadrant of the proximal shaft, close to the mid-diaphysis. We follow the terminology of Francillon-Vieillot et al. (1990), with additional terminology related to the orientation and arrangement of osteocytes following Werning (2012). Section B (Figs. 21 and 22) lies closer to the mid-diaphysis. The section is ~15\u201316 mm thick (= radially \u201cdeep\u201d) including the cortical and cancellous bone. The cancellous region comprises the inner 3\u20137 mm of the sample. A good deal of fracturing is visible throughout the section. In the cancellous region, the cracks are infilled by crystals and/or a dark, amorphous matrix, but in the cortex, many of the cracks lack infilling. It is possible that these cortical cracks formed during extraction from the ground or extraction of the sample for histological preparation. Crystals and the black matrix also infill the interstices between trabecular and the canals of the cortex. The bone is strongly birefringent, but shows a negative optical sign when viewed under elliptically polarized light (e.g., Fig. 24). This suggests that the collagen has been secondarily replaced by apatite crystals (Lee and O\u2019Connor, in press). The internalmost portion of the cancellous region (Figs. 21A and 22A) shows thick trabeculae that delineate large (up to 1 mm) amorphous \u201cresorption\u201d rooms. The cores of the largest trabeculae are comprised of woven or parallel-fibered primary bone and the edges are lined with several lamellae (true lamellar bone) or pseudolamellae (loose layers of parallel-fibered bone). The lamellae do not appear to cut across the cores; rather, they appear to have been deposited appositionally to them. The osteocyte density is much higher in the trabecular cores than in the lamellar/pseudolamellar bone lining the trabecular margins; in fact, they appear as densely packed as they are in the primary woven bone that forms the internalmost cortex. These osteocytes are aligned along the long axis of each trabecula and change orientation as trabecular orientation changes. This strongly suggests that at least some of these trabeculae formed de novo rather than by resorption of primary cortical tissues; if this is correct, these are remnants of embryonic or perinatal bone tissue and the \u201cresorption\u201d rooms are probably better described as intertrabecular chambers (because they did not form by resorption). The appearance of the trabeculae in this region is extremely similar to that described for embryonic ornithopods, including those of Maiasaura (Horner et al., 2000, 2001), Hypacrosaurus (Horner and Currie, 1994; Horner et al., 2001), Dryosaurus (Horner et al., 2009) and Tenontosaurus (Horner et al., 2009; Werning, 2012). Given the tibial diameter of ~40 mm in RAM 14000, and that this region comprises no more than 3.5 mm of the preserved section (i.e., there is 11.5\u201312.5 mm of cortical bone external to it), the neonatal tibial diameter could not have 936 937 938 939 940 941 942 943 944 945 946 947 948 949 950 951 952 953 954 955 956 957 958 959 960 961 962 963 964 965 966 967 968 969 970 971 972 973 974 975 976 977 978 979 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t exceeded 15\u201317 mm (47\u201353 mm circumference). This is very close in size to the embryonic femora of Hypacrosaurus (32.5\u201340 mm circumference; Horner and Currie, 1994). Other, incipient cancellous bone is visible just external to the preserved embryonic tissues (Fig. 22B). Contrary to the cancellous bone described above, this tissue is not as porous and clearly formed by the resorption of primary cortical tissues. In this region, the cores of the incipient trabeculae comprise primary woven bone, but the orientation of primary osteons and osteocytes do not correspond with trabecular orientation. Resorption rooms ranging in size from . 1\u20132 mm cut across primary bone tissue, and many are unlined. Where lamellar bone lines the resorption rooms, it cuts across the primary tissues forming the cores of the incipient trabeculae. The cortex near the mid-diaphysis is comprised mainly of well-vascularized, woven primary bone tissue. In the inner cortex (Fig. 22C), the bone is exclusively woven and the canals are a mixture of primary osteons and simple primary canals. The canals of this region are mainly longitudinal, but short radial, circumferential, and oblique canals are also common. The canals in this region are not as organized as the mid- or outer cortex and generally anastomose with several (two to four) other canals. Osteocyte density in this region is extremely high and there is no preferred orientation relative to the long axis of the bone nor a preferred arrangement relative to each other. Osteocytes encircle some primary osteons, but equally often, they are oriented oblique to the canals in the tissue that surround them. In the regions closest to the canals, the bone is less cellular compared to the cores of the laminae/interstices between them. In the mid- and outer cortex (Fig. 22D), the bone is similar in its components but shows more organization in its vascular canals and in its osteocytes. Vascular canals are again a mix of primary osteons and simple primary canals, which are generally wider in diameter compared to those of the inner cortex. As noted by Starck and Chinsamy (2002), this reflects the ontogeny of the canals themselves; the inner canals are older and have had more time to deposit bone since the initial bone scaffolding was deposited. Canals in this region show strong circumferential signal; in the mid-cortex, circumferential canals dominate, and in the outer cortex, the longitudinal canals are arranged circumferentially in rows. Osteocyte density is lower in the outer cortex compared to the inner cortex. Additionally, the disorganization is confined to a slightly narrower region at the center of each lamina. In the outermost cortex, the canals are often encircled by a thin band of fairly acellular bone (Fig. 22D). In some cases, it appears that a region of parallel-fibered bone, less dense in osteocytes, separates the acellular lining bone from the \u201ccore\u201d of woven bone at the center of each lamina. Despite histological indications that bone deposition rate was slightly lower in the outer cortex compared to the inner cortex, no annuli or lines of arrested growth (LAGs) are visible in this section. Section A (Figs. 23\u201325) is taken from a more proximal portion of the diaphysis. The section is ~11\u201312 mm thick (deep), including the cortical and cancellous bone. The cancellous region comprises only the inner ~2.5 mm of the sample. The section sampled in longitudinal section runs proximally along the shaft for 12 mm from the site of the cross-sectional sample. In cross-section (Fig. 23), section A resembles section B in its vascular patterning. It differs in the degree of organization of the primary cortical tissues (Figs. 23C and 24), in the secondary remodeling of the inner cortex (Fig. 23D), and in its thicker and more closely-spaced trabeculae. As in Section B, the trabeculae show no secondary osteons in their cores. The edges of all trabeculae are lined with distinct lamellae, often five or more in number. Some of these trabeculae clearly formed by resorption and secondary deposition; the lamellae on one side of a 980 981 982 983 984 985 986 987 988 989 990 991 992 993 994 995 996 997 998 999 1000 1001 1002 1003 1004 1005 1006 1007 1008 1009 1010 1011 1012 1013 1014 1015 1016 1017 1018 1019 1020 1021 1022 1023 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t trabecula often cut through the lamellae on the other side. Although a few larger resorption rooms are present, most are between .1 and .5 mm in diameter. The inner cortex was clearly experiencing active secondary remodeling at the time of the animal\u2019s death. Distinct resorption rooms of varying age (based on number of lamellae) are visible throughout the innermost cortex; these may be up to .15 mm wide. Several generations of secondary osteons are also visible (Fig. 23D). Although some primary tissue is clearly visible between secondary osteons, they cut across each other in places. The primary cortical tissues increase in organization moving periosteally through the section (Fig. 24). As in section B, the inner cortex of Section A (Fig. 24A,B) shows highly disorganized bone tissue. The interstices between vascular canals (nearly all are randomly arranged longitudinal primary osteons) form laminae mainly comprised of woven bone that shows a high density of randomly oriented osteocytes. Parallel-fibered bone or, more often, lamellar bone encircles the canals themselves. This is also cellular, but not to the extent of that in the interstices. The boundary between the woven bone and lamellar bone is distinct. This bone clearly conforms to the description of \u201cfibro-lamellar bone\u201d described by Francillon-Vieillot et al. (1990). In the mid-cortex (Fig. 24C,D), the bone is more laminar, because the primary osteons anastomose circumferentially with adjacent canals. Here, the woven \u201ccores\u201d of the interstitial bone have fewer osteocytes, but the ones that are present are equally disorganized. The bone encircling the primary osteons is exclusively lamellar and less cellular than in the inner cortex. Very thin bands of parallel-fibered bone lie between the woven component and the lamellar component surrounding the canals. Thus, the woven component grades into the lamellar component and the boundary between interstitial and circumvascular bone tissue is not as abrupt. In the outer cortex (Fig. 24E,F), woven bone is restricted to the center of the interstitial \u201ccores\u201d and much more parallel-fibered bone separates the woven component from the lamellar component. In this region, far fewer osteocytes occur in either the interstices or the lamellar bone of the primary osteons. The same pattern is also evident in longitudinal section (Fig. 25). Stein and Prondvai (in press) describe a similar condition in the long bones of the sauropods Alamosaurus, Apatosaurus, and Camarasaurus. In these taxa, woven bone is restricted to a thin splint at the center of bony laminae, and highly-organized parallel-fibered and lamellar bone fills the space between the woven splint and the vascular canals. This reflects the process of bone deposition; a scaffold of woven bone is deposited rapidly around vascular canals so that the diameter of the bone can be rapidly expanded. Subsequently, more organized tissues are deposited onto this scaffold (Stein and Prondvai, in press). body size and completeness : The most complete and smallest associated juvenile lambeosaurine skeleton aside from RAM 14000 is AMNH 5340, referable to Lambeosaurus sp. (Evans, 2010). This individual had a total length of 4.31 m (Lull and Wright, 1942), and comparable-sized postcranial elements are 1.74 to 1.89 times the length of those in RAM 14000 (Table 10; ischium length is excluded as an outlier). Scaling from AMNH 5340, we estimate total body length in RAM 14000 conservatively at 2.28 to 2.48 m, considerably smaller than the 9.45 m total body length estimated for the holotype of Parasaurolophus walkeri, ROM 768 (Lull and Wright, 1942). Associated cranial bones from the Kirtland Formation of New Mexico, SMP VP-1090, 1024 1025 1026 1027 1028 1029 1030 1031 1032 1033 1034 1035 1036 1037 1038 1039 1040 1041 1042 1043 1044 1045 1046 1047 1048 1049 1050 1051 1052 1053 1054 1055 1056 1057 1058 1059 1060 1061 1062 1063 1064 1065 1066 1067 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t were tentatively identified as a juvenile Parasaurolophus sp. (Sullivan and Bennett, 2000). The quadrate in this specimen is 185 mm long, 67 percent larger than the quadrate in RAM 14000 (111 mm long). A braincase assigned to juvenile Parasaurolophus sp. from the Dinosaur Provincial Park region of Alberta, CMN 8502, has a frontal width of 38 mm, 20 percent larger than the equivalent dimension in RAM 14000 (31.7 mm). By contrast, the skull length (horizontal from rostrum to paroccipital process) in the P. walkeri holotype (ROM 768) is 745 mm versus 246 mm in RAM 14000, or 303 percent larger. Thus, RAM 14000 represents the smallest confidently identifiable specimen of Parasaurolophus known to date. In terms of skeletal representation, RAM 14000 is the most complete single individual of Parasaurolophus described to date (Supplemental Table S1). Approximately 46 percent of skeletal elements are preserved here, contrasting with 43 percent in the holotype of P. walkeri (ROM 768) and 35 percent in the holotype of P. cyrtocristatus (FMNH P 27393). crest acoustics : Following the methods of Weishampel (1981a), we estimated the resonant frequencies of the main passageway of the nasal cavity for RAM 14000. Because the lateral diverticulum is poorly separated from the rest of the nasal passages and is not close-ended in RAM 14000, we did not calculate its corresponding resonant frequency. Necessary parameters to calculate f (frequency, in Hz) included n (resonance mode, set between 1 and 5), v (velocity of sound at sea level, 340 m/s), and L (length of tube, set at 0.195 m for RAM 14000 as measured from CT scan data). These parameters were entered into the following equation: f = n(v/2L) Results are summarized in Table 11. The estimated resonant nasal frequencies of RAM 14000 are approximately 11 to 18 times higher than those for P. cyrtocristatus and P. walkeri, respectively, as expected given the difference in cavity lengths. mandibular mechanics : Most discussions of hadrosaurid jaw mechanics have focused, directly or indirectly, on the dental occlusal surfaces and movements associated with that complex (e.g., Ostrom, 1961; Weishampel, 1983), but no detailed consideration has been given to the potential mechanical consequences of the premaxillary \u201cbeak\u201d. Adding a keratinous rhamphotheca increases the minimum gape at which contact between upper and lower jaws is made with a food item, with corresponding effects upon bite force. As in previous studies (e.g., Ostrom, 1964; Bell et al., 2009), the ornithischian lower jaw can most simply be approximated as a third class lever, with the applied muscle force located between the fulcrum (glenoid) and the resistance (usually the dentition, but in this case the predentary). Here, the force lever arm is the distance between the coronoid process and glenoid, whereas the resistance lever arm is the distance from bite point to glenoid (following Ostrom, 1964). In order to calculate usable force at a given point on the mandible, five parameters are needed (see Ostrom, 1964, for a full explanation): e, distance from the center of the coronoid process to the bite point; a, distance from the center of the glenoid to the center of the coronoid process; d, distance from the glenoid to the top of the coronoid process; \u03b8, the angle between the line of the jaw and the applied force on the coronoid process (measured from the center of the 1068 1069 1070 1071 1072 1073 1074 1075 1076 1077 1078 1079 1080 1081 1082 1083 1084 1085 1086 1087 1088 1089 1090 1091 1092 1093 1094 1095 1096 1097 1098 1099 1100 1101 1102 1103 1104 1105 1106 1107 1108 1109 1110 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t dorsotemporal fenestra); and \u03b4, the angle of the diagonal between the top of the coronoid and the glenoid, relative to the line of the jaw (Fig. 26). All of the parameters are then entered into the equation: S (e + a) = F sin (\u03b8 + \u03b4) d where S is the percentage of usable force at a given point relative to the input force F. All variables are the same in all conditions, except for \u03b8. When accounting for increased gape due to the rhamphotheca, \u03b8 is accordingly reduced (Fig. 26B). Thus, at a gape of 10\u00b0, \u03b8-10\u00b0 would be used as the appropriate value. Here, we make the simplification that F is constant across the relatively small differences in gape considered here. Based on measurements from the original specimen, the rhamphotheca in RAM 14000 decreased the angle of gape at which upper and lower beaks contacted by approximately 7\u00b0. Thus, \u03b8=44\u00b0 without a rhamphotheca and \u03b8=37\u00b0 when the rhamphotheca is included. For other parameters, e=150 mm (measured to rostral-most extent of predentary), a=48 mm, d=80 mm, and \u03b4=42\u00b0. Because absolute values are not a concern, F was set at 100%. Using the above numbers and equation, the percentage of usable force at the predentary is 40.3% without the rhamphotheca and 39.6% with the rhamphotheca. Thus, the rhamphotheca introduced a 0.7% decrease in bite force relative to the condition without. age of ram 14000 : The tibial bone microstructure of RAM 14000 preserves no LAGs or annuli, suggesting that this animal did not stop, pause, or dramatically slow its growth at any time between hatching and death. As noted in Nesbitt et al. (2013), the absence of LAGs does not necessarily imply that an animal died within its first year of growth, although that is one possibility. LAGs are not visible when they are deposited but later obscured by secondary remodeling, in animals that grow to full size in less than a year but live for several years afterward, or in animals that grow to full size over several years without pausing or stopping (Horner et al., 1999; Nesbitt et al., 2013). Secondary remodeling of primary tissues that once preserved LAGs can be eliminated for RAM 14000. Near the mid-diaphysis (section B; Fig. 21), bone tissue strongly resembles that of embryonic and perinatal ornithopods (e.g., Horner and Currie, 1994; Horner et al., 2000, 2001, 2009; Werning, 2012). This region extends to a radius consistent with the size of other perinatal lambeosaurines (Horner and Currie, 1994; Horner et al., 2000). This possible embryonic/perinatal tissue is not remodeled by secondary osteons, nor is any of the tissue external to it. Because of this, we are confident that the section represents an unobscured record of growth from a time near birth to death, and that no LAGs are missing. We also find it unlikely that RAM 14000 lacks LAGs because Parasaurolophus finished growth in less than a year. All four of the other hadrosaurids that have been examined histologically [Telmatosaurus (Benton et al., 2010), Maiasaura (Horner et al., 2000, 2001), Hypacrosaurus (Horner and Currie, 1994; Horner et al., 1999; Cooper et al., 2008), and Edmontosaurus (Reid, 1985)] exhibit several LAGs in the cortices of adult limb bones. Because LAGs are deposited annually in vertebrates (Francillon-Vieillot et al., 1990), this suggests that hadrosaurids required more than one year to reach full size. The presence of several cortical LAGs in related taxa also suggests that large hadrosaurids did not grow over several years without stopping, though in the absence of samples from subadult or adult specimens, this possibility cannot be excluded for Parasaurolophus. The histology of RAM 14000 excludes some broader age categories. The section studied here preserves some possible embryonic or perinatal tissues, but it has clearly deposited a significant amount of tissue external to these. Most of this tissue is mature enough to show primary osteons, indicating that some time has passed since deposition of the initial woven \u201cscaffolding\u201d (Stein and Prondvai, in press). Additionally, more organized bone microstructure and a larger parallel-fibered component of the bony laminae suggests slower bone depositional rates in the outer cortex relative to the inner cortex of RAM 14000 (Stein and Prondvai, in press). Embryos, perinates, and very young juvenile hadrosaurs exhibit only woven bone (Horner and Currie, 1994; Horner et al., 2000), so RAM 14000 does not likely belong to these age categories. Despite relative slowing of growth between the inner and outer regions of the cortex, RAM 14000 was still growing actively at the time of death. It does not exhibit the LAGs or secondary remodeling of the mid-diaphyseal cortex of subadult or adult hadrosaurs (Horner et al., 1999, 2000, 2001), and certainly not the external fundamental system observed in senescent, 1242 1243 1244 1245 1246 1247 1248 1249 1250 1251 1252 1253 1254 1255 1256 1257 1258 1259 1260 1261 1262 1263 1264 1265 1266 1267 1268 1269 1270 1271 1272 1273 1274 1275 1276 1277 1278 1279 1280 1281 1282 1283 1284 1285 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t large-bodied archosaurs (e.g., Woodward et al., 2011). Therefore, we feel it is also unlikely that RAM 14000 is a sub-adult or senescent individual. Given that RAM 14000 is not likely a perinate or a subadult, we hypothesize it to be a large juvenile. The only published histological section sampled from the long bones of a juvenile lambeosaurine is from the femur of MOR 548, a Hypacrosaurus stebingeri nestling. This material was described briefly by Horner and Currie (1994) and is currently being redescribed by Horner and his students as part of a larger study of Hypacrosaurus growth and ontogeny (John R. Horner, personal communication to SW, 2013). The femur of MOR 548 is approximately 23 cm long (~2.5 cm diameter; John R. Horner, personal communication to SW, 2013); smaller than RAM 14000 (325 mm). As reported in Horner and Currie (1994), much of the cortex comprises woven bone organized around primary vascular canals. The published image shows a looser compacta relative to RAM 14000, but images of the full cross-section show a great deal of similarity in terms of the organization and patterning of primary osteons and compactness of the bone in the outer cortex (John R. Horner, personal communication to SW, 2013). No LAGs were reported for this specimen. The bone microstructure of an ontogenetic series of the saurolophine Maiasaura has also been described (Horner et al., 2000). RAM 14000 is intermediate between the Maiasaura juveniles YPM-PU-22472 and MOR-005JV in size (18 cm and 50 cm femur length, respectively; Horner et al., 2000) and compares well histologically to Maiasaura juveniles in most respects. Horner and colleagues note well-formed primary osteons with distinct/organized lamellae surrounding the vessels. These primary canals are most commonly longitudinal canals arranged in parallel circumferential rows, but also in laminar and even plexiform patterns. LAGs are rare in juveniles, despite being \u201canimals of considerable size\u201d (p. 119), although a LAG occurs in some elements of MOR-005JV (Horner et al., 2000). RAM 14000 differs from Maiasaura juveniles in that it does not exhibit secondary osteons at the mid-diaphysis, though they occur in the more proximal section. Given that RAM 14000 was clearly still growing at the time of its death, and that the skeletal morphology and bone microstructure are similar to juveniles of other hadrosaurids, we hypothesize that RAM 14000 was a large juvenile. Cooper et al. (2008) estimated growth curves for Hypacrosaurus based on LAG circumferences throughout the ontogeny of MOR 549, an adult. Using their models, we reconstruct an age of ~1 year for juveniles the size of MOR 548, though again, no LAGs were reported by Horner and Currie (1994). A single LAG was reported in some elements of MOR-005JV (Horner et al., 2000), a juvenile Maiasaura that showed similar histology to RAM 14000. Because no LAGs occur in the similarly-sized RAM 14000, we tentatively suggest that the animal was under a year of age at the time of death. However, we note that the number of hadrosaurs with good ontogenetic sampling is still very low (only Maiasaura and Hypacrosaurus), and so our estimate will need revision if future studies show that hadrosaurs sustained uninterrupted high growth rates for longer than the first year of growth. For our estimates of age and size for RAM 14000 to be correct, extremely rapid growth rates would have been required for Parasaurolophus. Our results suggest that RAM 14000 reached 25\u201332 percent of adult size (based on total body length length and skull length, respectively) in less than a year. Growth curves based on estimates of circumference and mass (as derived from circumference), have been modeled for Hypacrosaurus (Cooper et al., 2008) and Maiasaura (Erickson et al., 2001), respectively. Because we lack histological samples from 1286 1287 1288 1289 1290 1291 1292 1293 1294 1295 1296 1297 1298 1299 1300 1301 1302 1303 1304 1305 1306 1307 1308 1309 1310 1311 1312 1313 1314 1315 1316 1317 1318 1319 1320 1321 1322 1323 1324 1325 1326 1327 1328 1329 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t any adult Parasaurolophus specimens, we cannot construct growth curves directly comparable to those estimated for Hypacrosaurus and Maiasaura. However, our estimates of growth (25\u201332 percent of adult size in less than a year) are reasonable based on the ontogeny of femoral length reconstructed for both Maiasaura and Hypacrosaurus. MOR-005JV, a Maiasaura juvenile, was estimated to be one year old at time of death by Erickson and colleagues (2001). That individual had a femoral length half that of MOR-005A (50 cm vs. 100 cm; Horner et al., 2000), an adult specimen estimated to be six years old at time of death (Erickson et al., 2001). MOR 548, a juvenile Hypacrosaurus approximately 1 year old (see above) had a femur of 23 cm, whereas the adult MOR 549 had a femur 102 cm long (Horner et al., 1999). In light of similarly rapid first-year growth in these other hadrosaurids, we think our assessment for Parasaurolophus is reasonable. Ontogeny in Parasaurolophus Accepting the identification of RAM 14000 as a juvenile Parasaurolophus, several notable ontogenetic changes can be inferred for the skull and postcrania in this taxon. Some of these are consistent with previous reports on other lambeosaurines, but others are exclusive to Parasaurolophus. Because the following discussion includes at least three different species (P. walkeri, P. cyrtocristatus, and P. tubicen), we caution that some ontogenetic changes may be more phylogenetically restricted than indicated here. Nonetheless, broad similarities across Parasaurolophus species imply that many changes are universal to the taxon. The crest of RAM 14000 differs from that of all known adult Parasaurolophus in several important ways. First, the crest in RAM 14000 is restricted to a low eminence rather than an elongated, curved tube that overhangs the braincase (Fig. 11A,C). Second, the crest in RAM 14000 is bordered caudally and at its apex by the nasal. Although the exact sutural relations of adult Parasaurolophus are controversial, it seems likely that the nasal formed only a small portion of the ventral margin of the crest at its base in adult individuals (Sullivan and Williamson, 1999). Thus, the already minimal contribution of the nasal was further minimized through ontogeny. Third, the premaxilla-nasal fontanelle is open, whereas it is completely closed in all other, ontogenetically older specimens. These differences between the crests of juvenile and adult Parasaurolophus are intimately tied to inferred ontogenetic changes in the braincase. The frontal of Parasaurolophus thickened and achieved a nearly vertical contact with the nasal only in later ontogenetic stages, at latest by the time the individual reached half of adult skull size (Evans et al., 2007). Finally, a broad naso-frontal suture also only occurred at half maximum skull size. In all of these details, where known, RAM 14000 is more similar to juveniles of most corythosaurin species than to subadult or adult Parasaurolophus. Based on reconstructions of the nasal passages in Parasaurolophus (Fig. 11), RAM 14000 indicates that several important transformations occurred as the crest elongated. The lateral diverticulum exhibits perhaps the most notable changes. In the smallest juvenile condition (Fig. 11C), the diverticulum completely obscures the main airway in lateral view. In adults (P. walkeri, P. tubicen, and P. cyrtocristatus; Fig. 11A), the main airway greatly exceeded the extent of the lateral diverticulum, as well as bounding the diverticulum dorsally and ventrally. Additionally, the lateral diverticulum is reconstructed as a single blind chamber in adult P. cyrtocristatus, whereas it is clearly looped in young juveniles (however, a looped lateral 1330 1331 1332 1333 1334 1335 1336 1337 1338 1339 1340 1341 1342 1343 1344 1345 1346 1347 1348 1349 1350 1351 1352 1353 1354 1355 1356 1357 1358 1359 1360 1361 1362 1363 1364 1365 1366 1367 1368 1369 1370 1371 1372 1373 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t diverticulum has been reconstructed for P. tubicen; Sullivan and Williamson, 1999). Additional information (particularly for adult Parasaurolophus from the Kaiparowits Formation) may revise this reconstructed sequence. In any case, juvenile Parasaurolophus differ markedly in the morphology of their nasal passages from all known adult Parasaurolophus as well as from corythosaurins of all ontogenetic stages. The extent of the contributions of the nasal and premaxillae to the crest in Parasaurolophus has been a long-standing problem (summarized in Sullivan and Williamson, 1999). Based on the new information from RAM 14000 and comparison with corythosaurins, we offer some new observations. In corythosaurins, the relationships of different sections of the nasal passages (e.g., lateral diverticulum) and the surrounding bones (premaxillae and nasals) are relatively invariant through ontogeny. For instance, the nasal bounds the caudal edge of the lateral diverticulum in juvenile (ROM 759) and subadult (CMN 34825) Corythosaurus (Evans et al., 2009). A similar relationship exists between the nasal and the lateral diverticulum in RAM 14000. Unlike corythosaurins, adult Parasaurolophus have a much more extensive lateral diverticulum (occupying up to half the length of the crest; e.g., Fig. 11A). However, the most recent interpretation of the crest sutures require that the lateral diverticulum, particularly at its caudal end, be enclosed nearly exclusively by the premaxillae (Sullivan and Williamson, 1999). By contrast, Weishampel (1981b) proposed that the nasals in P. walkeri (ROM 768) reached to the mid-length of the crest (see fig. 2H in that paper). This is roughly coincidental with the extent of the lateral diverticula in P. walkeri. We thus summarize two alternative hypotheses: 1) the relationships between the bony elements and the nasal passages were highly plastic through ontogeny in Parasaurolophus, due in part to its massive crest, and the crest predominantly is composed of the premaxillae; or 2) the nasal forms a major portion of the crest. We speculate that the latter hypothesis is most likely, based on the lateral diverticulum. Unfortunately, sutures are ambiguous in many skulls of adult Parasaurolophus due to crushing or fusion, and thus a rigorous test of the hypothesis will require description of better material. RAM 14000 also implies that several features of the skull were relatively ontogenetically invariant in Parasaurolophus. The narrow infratemporal fenestra, constrained by a tightly angled jugal, occurs at all ontogenetic stages. The shape of the oral margin of the premaxilla is also relatively unchanged through ontogeny. Ontogeny of the postcrania in hadrosaurids has been well-documented elsewhere (Horner and Currie, 1994; Dilkes, 2001; Suzuki et al., 2004; Guenther, 2009). The patterns in RAM 14000 and Parasaurolophus, both for limb proportions and overall morphology, generally are consistent with observations from other taxa, particularly the lambeosaurine Hypacrosaurus stebingeri. Notably, the distal expansion of the ischium is minimal in RAM 14000 (unlike adult individuals of P. cyrtocristatus). Similar ontogenetic patterns in the ischium occur in H. stebingeri (Horner and Currie, 1994), suggesting that this change is generalized across lambeosaurines with the feature. The most dramatic changes are seen in the ilium, particularly in the reduced size of the supraacetabular process relative to that in adult Parasaurolophus (Fig. 18C,D). Again, this pattern is probably generalized across hadrosaurids (Guenther, 2009). The humerus:femur ratio is approximately the same in RAM 14000 and adult Parasaurolophus ROM 768 and FMNH P 27393 (0.53, 0.50, and 0.51, respectively), but the femur:fibula ratio differs greatly (1.14 and 1.24 in RAM 14000 and FMNH P 27393, respectively). Thus, the portion of the leg below the knee joint is slightly longer in the older animal. 1374 1375 1376 1377 1378 1379 1380 1381 1382 1383 1384 1385 1386 1387 1388 1389 1390 1391 1392 1393 1394 1395 1396 1397 1398 1399 1400 1401 1402 1403 1404 1405 1406 1407 1408 1409 1410 1411 1412 1413 1414 1415 1416 1417 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t cranial functional morphology : The rhamphotheca on the upper jaw resulted in a minor reduction in bite force at the tip of the beak, relative to the condition without a rhamphotheca. Although this arguably enforced a slight limitation on the type of food items that could be cropped and ingested, a rhamphotheca would also have had some potential benefits. In particular, the expanded keratinous structure would have increased the area available for cropping, and thus the potential volume of food taken in per bite. Additionally, the rhamphotheca may have allowed the hadrosaur to more efficiently crop plants at ground level, by moving the bite point closer to the ground without having to bend the neck. The effect of a rhamphotheca upon mastication is a topic worthy of additional exploration. As expected by its smaller size and shorter airway, the crest of RAM 14000 produced a higher resonant frequency than did the crests of adults (assuming that the structure was indeed used in sound production). If such vocalizations played a role in the social behavior of Parasaurolophus, perhaps in distinguishing different age categories, (Weishampel, 1981a; Evans et al., 2009), the vastly different frequencies of adult and juvenile animals would have been easily distinguishable (Table 11). Heterochrony in hadrosaurs and other ornithischians Heterochrony\u2014variation in developmental timing of the appearance of anatomical features\u2014clearly played an important part in the evolution of lambeosaurine crests. A robust assessment of crest heterochrony requires knowledge of the extent of crest development at given sizes and absolute ages for several taxa, in addition to their stratigraphic ranges and phylogenetic relationships. Estimates of absolute age for fossil taxa are only obtainable from skeletochronological studies of bone histology. Unfortunately, despite much higher taxonomic diversity within Ankylopollexia and especially within Hadrosauridae, the vast majority of ornithopods sampled for histological study fall outside Ankylopollexia (Werning 2012). Prior to this study, only four hadrosaurids had been sampled: Telmatosaurus (Benton et al., 2010), Maiasaura (Horner et al., 2000, 2001), Hypacrosaurus (Horner and Currie, 1994; Horner et al., 1999; Cooper et al., 2008), and Edmontosaurus (\u201cAnatosaurus\u201d; Reid, 1985). Of these, the only lambeosaurine is Hypacrosaurus, a corythosaurin. Additionally, only the histology of Maiasaura has been studied throughout ontogeny (Horner et al., 2000, 2001), and growth curves have been estimated only for Maiasaura (Erickson et al., 2001) and Hypacrosaurus (Cooper et al., 2008). Thus, the skeletochronological data necessary to link skull size, body size, and crest development with age is virtually nonexistent for lambeosaurines. This is especially unfortunate given that the phylogeny (e.g., Evans and Reisz, 2007; Gates et al., 2007; Prieto-M\u00e1rquez, 2010) and stratigraphic context (e.g., Ryan and Evans, 2005; Mallon et al., 2012) of hadrosaurids is increasingly well resolved. Embryonic and post-hatchling material (Horner and Currie, 1994) necessarily imply extremely young age (~a few months at most) for such specimens. To date, only the holotype specimen of Hypacrosaurus stebingeri, MOR 549, has been aged (Horner et al., 1999; Cooper et al., 2008), with an estimate of approximately 13 years old. This specimen is the only described adult specimen for H. stebingeri, and unsurprisingly has the largest crest of any specimen. Nonetheless, the structure is still relatively modest in size relative to the largest crests seen in 1418 1419 1420 1421 1422 1423 1424 1425 1426 1427 1428 1429 1430 1431 1432 1433 1434 1435 1436 1437 1438 1439 1440 1441 1442 1443 1444 1445 1446 1447 1448 1449 1450 1451 1452 1453 1454 1455 1456 1457 1458 1459 1460 1461 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t specimens of Corythosaurus casuarius or Hypacrosaurus altispinus. This may reflect taxonomic differences, individual variation, sexual dimorphism, or another factor, but these hypotheses cannot be tested without a larger sample. Extrapolating from the growth curve presented for H. stebingeri, and assuming that sexual maturity occurred at or near the growth curve inflection (Erickson et al., 2007; Lee and Werning, 2008), sexual maturity occurred in this species at two to three years of age (Cooper et al., 2008). The reconstructed mean femoral length at this point was 450 mm. This is slightly smaller than the femoral lengths associated with juvenile skeletons referred to H. stebingeri (590 mm and 522 mm for AMNH 5340 and 5461, respectively; Lull and Wright, 1942; Evans, 2010). In both cases, the crest is only barely developed, suggesting that crest development in H. stebingeri did not occur until after the onset of sexual maturity but well before the animal reached full adult size. Additional histological work is needed to test this hypothesis. Assuming that RAM 14000 was still in its exponential growth phase (pre-inflection), a reasonable assumption given its bone microstructure, it had not yet reached sexual maturity despite already initiating crest development. Using skull size as a rough proxy for ontogenetic age, it is clear that Parasaurolophus initiated visible crest development at a much earlier point than did corythosaurins (~30% maximum skull size versus ~50% maximum skull size; Fig. 27). Juvenile corythosaurins nearly twice the size of RAM 14000 have far more subdued crests relative to the rest of the skull; a similar pattern is seen for the potentially basal lambeosaurine \u201cProcheneosaurus convincens\u201d. This could result from different life history parameters (e.g., differences in growth rate or the onset of sexual maturity), but we suggest it is more likely related to the larger and more \u201cextreme\u201d nature of the crest in Parasaurolophus versus corythosaurins. In other words, the crest had to begin growth at an earlier stage in order to achieve its full extent. Despite the differences in crest development between corythosaurins and Parasaurolophus, lambeosaurine hadrosaurids fit an overall pattern of relatively early development of bony cranial ornamentation in ornithischian dinosaurs. This contrasts with birds that initiate crest growth only as the animal reaches nearly full adult size, such as the cassowary (Fig. 27; Dodson, 1975). Two potential factors may be behind these differences. First, among neornithines, sexual maturity occurs well after somatic maturity (roughly equivalent to full adult body size), in contrast with non-avian dinosaurs that apparently achieved sexual maturity well before somatic maturity (Erickson et al., 2007; Lee and Werning, 2008). Thus, if cranial crests in ornithischians had some species-specific display function\u2014whether for species recognition, sexual selection, or any related use\u2014it is intuitive that the structures appeared before the animal reached full adult body size, and conversely for neornithines. A second important factor considers the integration of cranial ornamentation into the overall skull in ornithischians versus avians. In birds such as cassowaries and hornbills, the massive casques are simple \u201cadd-ons\u201d to the overall skull, formed strictly of a bony core without major involvement of respiratory or muscular systems (Rothschild, 1900; AAF, personal observation). By contrast, the crests of hadrosaurids are intimately integrated with the respiratory system, by virtue of the airway passing through the crest (Fig. 11). Thus, the crest had to form early in development, simply so that the animals could continue to breathe. Similar constraints may have affected the frills of ceratopsians, at least part of which supported jaw musculature (Rieppel, 1981). However, this does not necessarily explain the early development of horns in 1462 1463 1464 1465 1466 1467 1468 1469 1470 1471 1472 1473 1474 1475 1476 1477 1478 1479 1480 1481 1482 1483 1484 1485 1486 1487 1488 1489 1490 1491 1492 1493 1494 1495 1496 1497 1498 1499 1500 1501 1502 1503 1504 1505 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t ceratopsids (Horner and Goodwin, 2006), or nodes and spikes in pachycephalosaurs (Horner and Goodwin, 2009; Schott et al., 2011), structures which seem to be decoupled from more \u201cutilitarian\u201d aspects of the skull. Here, timing of sexual maturity may have played a role. We thus hypothesize that, unsurprisingly, development of different structures was subject to different constraints depending upon their function and location. standards for skeletal measurements. : Standards for skeletal measurements. Those for the skull and lower jaw augment standards published elsewhere (Dodson, 1975; Evans, 2010). Numbers associated with each measurement correspond to those in Tables 3\u20139. A and B, skull in left lateral view; C, right half of caudal section of skull in dorsal view; D, mandible in left lateral view; E, scapula; F, ilium; G, ischium; H, pubis; I, humerus; J, femur; k, tibia; l, fibula; m, calcaneum; n, pedal phalanx; o, pedal ungual; p, caudal vertebra (also used for : other vertebrae); Q, cervical rib (also used for sacral rib); R, dorsal rib. A\u2013M and P\u2013R are in right lateral view; N and O are in dorsal view. Drawings are not to scale. PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Figure 6 Reconstruction of the skull of Parasaurolophus sp., RAM 14000. 8502 (evans et al., 2007). in b and c, the dotted lines separating the lateral diverticulum and the main : airway indicate that the diverticulum is obscuring the view of the main airway, and the two chambers run parallel to each other. Abbreviations: ld, lateral diverticulum; ma, main airway; vma, ventral portion of main airway. Scale bar equals 10 cm. PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Figure 12 Disarticulated skull elements of Parasaurolophus sp., RAM 14000. v3 bone is shown in white, impressions of bone are shown in green, and rock without bone : impressions is shown in gray. Scale bar equals 10 cm. PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Figure 14 Partial braincase of Parasaurolophus sp., RAM 14000, in right lateral view. A, interpretive drawing; B, photograph. Abbreviations: atc, atlas centrum (odontoid); ati, atlas intercentrum; axc, axis centrum; bo, basioccipital; ex, exoccipital; fv, foramen vestibuli; nat, neural arch of atlas; XII?, foramen tentatively identified as that for CN XII; V, foramen for CN V; V2,3, sulcus for CN V2 and V3. Bone is shown in white, broken bone surface is shown in light gray, and matrix is shown in dark gray. Unlabeled bones are not confidently identified, but may represent vertebral fragments. Scale bar equals 1 cm. PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Figure 15 Cranial endocast of Parasaurolophus sp., RAM 14000, reconstructed from CT scans. iii : The proximal end of the digit is to the lower right end of the image, and the distal end end is towards the top middle edge of the image. The arrow indicates one individual tubercle. Abbreviations: MT III, caudal surface of metatarsal III. Scale bar equals 1 cm. PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Figure 21 Bone microstructure of juvenile Parasaurolophus tibia in regular transmitted light (RAM 14000, histological sample B, near mid-diaphysis). 87 and 87.79.333, and represents an embryonic individual (redrawn from horner and currie, : 1994). The next smallest skull is patterned after MOR 548 (also redrawn from Horner and Currie, 1994). The remaining skulls, from left, are patterned after ROM 759, CMN 34825, ROM 5856, and ROM 871, redrawn from Evans (2010). Skulls of Casuarius are redrawn from Dodson (1975) , and based on (from left) YPM 6208, YPM 1736 (snout region reconstructed), and AMNH 3870. Maximum skull lengths for Parasaurolophus, Corythosaurus, and Casuarius are 745 mm (ROM 768), 750 mm (ROM 792) and 200 mm, respectively (Dodson, 1975; Evans, 2010) . Scale bars equal 10 cm. PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Table 1(on next page) Summary of digital data available via Figshare. Additional detailed information is contained in Supplemental Article S1. PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Element Data Type URL Braincase segmentation data http://dx.doi.org/10.6084/m9.figshare.6641 71 Braincase CT scan data http://dx.doi.org/10.6084/m9.figshare.6641 67 Braincase surface models http://dx.doi.org/10.6084/m9.figshare.6921 50 Maxilla CT scan data http://dx.doi.org/10.6084/m9.figshare.6641 68 Skull (left half) CT scan data http://dx.doi.org/10.6084/m9.figshare.6641 69 Skull (left half) segmentation data http://dx.doi.org/10.6084/m9.figshare.6910 47 Skull (left half with structures) surface models http://dx.doi.org/10.6084/m9.figshare.6921 51 Skull (left half) surface model http://dx.doi.org/10.6084/m9.figshare.6921 52 Skull and neck (right half) CT scan data http://dx.doi.org/10.6084/m9.figshare.6641 70 Skull and neck (right half) segmentation data http://dx.doi.org/10.6084/m9.figshare.6910 53 Skull and neck (right half) surface models http://dx.doi.org/10.6084/m9.figshare.6921 53 Humerus (right) surface model http://dx.doi.org/10.6084/m9.figshare.6921 55 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Table 2(on next page) MorphoBank (project 836) accession numbers for high-resolution histological images used in this study. Abbreviations: LS, longitudinal section; XS, cross (transverse) section. These images can be accessed online at: http://www.morphobank.org/permalink/?P836 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Section View Accession # Image Contents A XS M193513 Entire section A (entire slide), brightfield M193511 Radial transect through section A, brightfield M283554 Inner cortex, brightfield M283547 Inner cortex, brightfield M283550 Inner cortex, elliptically polarized light M283548 Mid-cortex, brightfield M283551 Mid-cortex, elliptically polarized light M283553 Outer cortex, brightfield M283549 Outer cortex, brightfield M283552 Outer cortex, elliptically polarized light M193514 Osteocytes M193515 Osteocytes A LS M193522 Entire section A (entire slide), brightfield M283543 Inner cortex, brightfield M283544 Mid-cortex, brightfield M283545 Outer cortex, brightfield M283546 Osteocytes B XS M151601 Entire section B (entire slide), brightfield M193512 Radial transect through section B, brightfield M283539 Inner cancellous region, brightfield M283540 Outer cancellous region, brightfield M283537 Inner cortex, brightfield M283541 Inner/mid-cortex, brightfield M283538 Outer cortex, brightfield M283542 Outer cortex, brightfield PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Table 3(on next page) Measurements of the skull of Parasaurolophus sp., RAM 14000. The standards for these measurements (modified from those in Dodson, 1975, and Evans, 2010) are diagrammed in Figure 5. Dashes indicate missing measurements. PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Element Measurement and Description Value (mm) Left Right Skull 1 Length from tip of rostrum to paroccipital process, parallel to maxillary tooth row 246.0 \u2014 2 Length from tip of rostrum to quadrate, parallel to maxillary tooth row 211.2 \u2014 3 Preorbital length, parallel to maxillary tooth row 125.2 \u2014 4 Height at caudal end, perpendicular to maxillary tooth row 142.0 \u2014 5 Height from maxillary tooth row to top of crest 120.1 \u2014 6 Length from caudal end of crest to paroccipital process 112.8 \u2014 7 Maximum width across postorbitals from midline 46.1 \u2014 8 Height of caudal plane, perpendicular to tooth row 81.6 \u2014 External naris 38 Maximum length 55.1 \u2014 39 Maximum width 21.9 \u2014 Orbit 40 Maximum length 62.4 58.9 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t 41 Maximum height 53.5 48.0 Laterotemporal fenestra 42 Maximum length 63.7 \u2014 43 Maximum width 18.8 20.1 Dorsotemporal fenestra 44 Maximum length on lateral edge 42.6 \u2014 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Table 4(on next page) Measurements of individual cranial bones of Parasaurolophus sp., RAM 14000. The standards for these measurements (modified from those in Dodson, 1975; Evans, 2010) are diagrammed in Figure 5. Dashes indicate missing measurements. PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Element Measurement and Description Value (mm) Left Right Crest 9 Length from rostrum to crest midpoint, parallel to tooth row 118.7 \u2014 10 Angle between crest and snout 120\u00ba \u2014 11 Length parallel to tooth row, level with skull roof 61.8 \u2014 12 Length of crest at half-height 46.9 \u2014 13 Crest height above orbit, from postorbital/prefr ontal suture 61.8 \u2014 14 Height of crest above skull roof 25.1 \u2014 15 Maximum width of crest from midline 46.1 \u2014 16 Maximum width of premaxillary-nas al fontanelle 9.4 \u2014 Maxilla 17 Length along tooth row 117.7 *110.1 18 Height from tooth row to jugal-maxilla suture *44.4 31.8 Premaxilla 19 Straight-line length of oral margin, from midline 42.9 \u2014 20 Depression of oral margin below maxillary tooth row 32.6 \u2014 Jugal 21 Maximum length *113.1 107.7 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t 22 Maximum width of rostral process \u2014 35.6 23 Minimum width below orbit 19.2 19.2 24 Maximum width of blade 30.9 31.8 25 Minimum width of quadrate process 22.2 21.7 Postorbital 26 Maximum length 83.7 \u2014 27 Maximum height 53.4 \u2014 28 Minimum width of caudal process 13.3 \u2014 Quadrate 29 Maximum length 109.9 112.3 30 Craniocaudal length of lateral edge of distal condyle 18.2 17.6 31 Mediolateral width of distal condyle (not shown) 21.4 \u2014 Frontal 32 Length at midline 34.2 \u2014 33 Maximum width from midline 31.7 \u2014 Paroccipital process 34 Maximum width 18.3 \u2014 35 Maximum length 32.4 \u2014 36 Maximum separation from quadrate 15.9 11.0 37 Minimum separation from quadrate 11.1 9.9 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Table 5(on next page) Measurements of the lower jaw of Parasaurolophus sp., RAM 14000. The standards for these measurements (modified from those in Dodson, 1975) are diagrammed in Figure 5. Dashes indicate missing measurements. PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Element Measurement and Description Value (mm) Left Right Mandible 45 Maximum length 223.5 \u2014 Dentary 46 Maximum length along ventral edge 134.2 142.1 47 Length of edentulous process to caudal edge of predentary 15.3 \u2014 48 Maximum height from ventral edge to alveoli 30.7 33.1 49 Maximum height at coronoid process \u2014 72 50 Maximum width of coronoid process \u2014 27.9 Predentary 51 Length parallel to midline 49.8 \u2014 Surangular 50 Maximum length 54.8 46.2 51 Length of retroarticular process 42.6 38.5 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Table 6(on next page) Measurements of the vertebrae of Parasaurolophus sp., RAM 14000. The standards for these measurements are diagrammed in Figure 5. *indicates approximate measurement. PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Element Measurement and Description Value (mm) Cervical vertebra ?5 101 Maximum length of centrum 20.0 Cervical vertebra ?6 101 Maximum length of centrum 20.0 Dorsal vertebra ?14 101 Maximum length of centrum 28.8 Dorsal vertebra ?15 101 Maximum length of centrum 27.3 Dorsal vertebra ?16 101 Maximum length of centrum 26.7 Dorsal vertebra ?17 101 Maximum length of centrum 30.8 Dorsal vertebra ?18 101 Maximum length of centrum 35.8 Caudal vertebra ?2 103 Maximum craniocaudal length of neural spine 16.5 Caudal vertebra ?3 101 Maximum length of centrum 21.0 103 Maximum craniocaudal length of neural spine 16.1 Caudal vertebra ?4 101 Maximum length of centrum 20.3 103 Maximum craniocaudal length of neural spine 15.9 Caudal vertebra ?5 101 Maximum length of centrum 18.5 103 Maximum craniocaudal length of neural spine 14.9 Caudal vertebra ?6 101 Maximum length of centrum 16.7 102 Maximum proximodistal length of neural spine *107.9 103 Maximum craniocaudal length of neural spine 13.6 Caudal vertebra ?7 101 Maximum length of centrum 19.4 103 Maximum craniocaudal length 15.0 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t of neural spine Caudal vertebra ?8 101 Maximum length of centrum 16.5 103 Maximum craniocaudal length of neural spine 11.5 Caudal vertebra ?9 101 Maximum length of centrum 67.3 103 Maximum craniocaudal length of neural spine 13.6 Caudal vertebra ?10 103 Maximum craniocaudal length of neural spine 10.3 Caudal vertebra ?12 101 Maximum length of centrum 19.3 103 Maximum craniocaudal length of neural spine 8.6 Caudal vertebra ?13 101 Maximum length of centrum 19.5 102 Maximum proximodistal length of neural spine 30.9 Caudal vertebra ?14 101 Maximum length of centrum 18.3 102 Maximum proximodistal length of neural spine 29.2 Caudal vertebra ?15 101 Maximum length of centrum 19.1 102 Maximum proximodistal length of neural spine 29.2 Caudal vertebra ?16 101 Maximum length of centrum 20.5 103 Maximum craniocaudal length of neural spine 9.8 Caudal vertebra ?17 101 Maximum length of centrum 20.3 103 Maximum craniocaudal length of neural spine 9.4 Caudal vertebra ?18 101 Maximum length of centrum 21.3 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Caudal vertebra ?19 102 Maximum proximodistal length of neural spine 49.1 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Table 7(on next page) Measurements of the ribs of Parasaurolophus sp., RAM 14000. The standards for these measurements are diagrammed in Figure 5. PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Element Measurement and Description Value (mm) Cervical rib ?4 104 Maximum width between capitulum and tuberculum 19.6 105 Maximum length from capitulum to distal end of shaft 27.1 Cervical rib ?5 104 Maximum width between capitulum and tuberculum 19.7 105 Maximum length from capitulum to distal end of shaft 29.3 Cervical rib ?6 104 Maximum width between capitulum and tuberculum 17.9 105 Maximum length from capitulum to distal end of shaft 30.8 Dorsal rib 1 (left) 106 Maximum length from capitulum to distal end of shaft 235.0 Dorsal rib 2 (left) 106 Maximum length from capitulum to distal end of shaft 285.0 Dorsal rib 3 (left) 106 Maximum length from capitulum to distal end of shaft 325.0 Sacral rib 1 104 Maximum width between capitulum and tuberculum 39.4 Sacral rib 1 105 Maximum length from capitulum to distal end of shaft 54.3 Torso length (left) Distance between scapular glenoid and pelvic acetabulum 620.0 Rib cage Maximum depth 339.0 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Table 8(on next page) Measurements of the pectoral and pelvic elements of Parasaurolophus sp., RAM 14000. The standards for these measurements are diagrammed in Figure 5. *indicates approximate measurement. PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Element Measurement and Description Value (mm) Scapula (left) 52 Maximum length *267.6 53 Maximum width of blade 55.0 54 Minimum width of blade 36.3 Ilium 55 Greatest length 300.8 56 Length of preacetabular process 120.7 57 Minimum height of preacetabular process 21.5 58 Maximum height of preacetabular process 36.8 59 Maximum height of ilium 60.9 60 Length of postacetabular process, ventral 89.9 61 Length of postacetabular process, dorsal 104.7 62 Minimum height of postacetabular process 30.8 63 Mediolateral width of supraacetabular process 28.4 64 Length of ischiadic peduncle 28.7 65 Length of pubic peduncle 31.6 66 Width of acetabulum 52.1 Ischium (left) 67 Maximum length 243.1 68 Maximum width of distal end 30.0 Pubis 69 Length of prepubic blade 147.3 70 Maximum depth of prepubic blade 83.0 71 Minimum depth of prepubic blade 46.2 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Table 9(on next page) Measurements of the limb bones of Parasaurolophus sp., RAM 14000. The standards for these measurements are diagrammed in Figure 5. PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Element Measurement and Description Value (mm) Humerus 72 Maximum length 174.6 73 Length of deltopectoral crest (1) 101.1 74 Length of deltopectoral crest (2) 96.6 75 Maximum width at deltopectoral crest 38.1 76 Maximum width at proximal end 50.5 77 Minimum diameter of diaphysis 24.5 78 Maximum width at distal end 35.2 Femur 79 Maximum length 328.9 80 Craniocaudal width of proximal end on lateral surface 66.8 81 Craniocaudal length of cranial trochanter 25.8 82 Proximodistal length of 4th trochanter 73.3 83 Craniocaudal height of 4th trochanter 15.6 84 Craniocaudal length at midshaft excluding 4th trochanter 40.9 85 Distance between distal ends of 4th trochanter and femur 127.2 Tibia 86 Maximum length 306.9 87 Maximum craniocaudal width at proximal end 80.6 88 Maximum projection of cnemial crest 22.1 89 Maximum proximodistal length of cnemial crest 113.0 90 Maximum craniocaudal width at distal end 47.5 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Fibula 91 Maximum length 288.3 92 Maximum craniocaudal diameter at proximal end 43.2 93 Minimum craniocaudal diameter of diaphysis 15.7 94 Maximum craniocaudal diameter at distal end 25.2 Calcaneum 95 Maximum craniocaudal length 25.4 96 Minimum proximodistal length 14.6 Metatarsal IV 97 Maximum length on dorsal midline (not shown) 100.1 Phalanx IV-1 98 Maximum length on dorsal midline 25.9 Phalanx IV-2 98 Maximum length on dorsal midline 8.8 Phalanx IV-3 98 Maximum length on dorsal midline 7.3 Phalanx IV-4 98 Maximum length on dorsal midline 2.3 Phalanx IV-5 99 Maximum length on dorsal midline 31.3 Phalanx IV-5 100 Maximum mediolateral width (estimated) 25.6 Phalanx III-2 98 Maximum length on dorsal midline 7.3 Phalanx III-3 98 Maximum length on dorsal midline 5.1 Phalanx III-4 99 Maximum length on dorsal midline 29.0 PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Table 10(on next page) Measurements of Parasaurolophus sp., RAM 14000, compared with those for selected other lambeosaurines. Measurements of Parasaurolophus sp., RAM 14000, compared with those for selected other lambeosaurines. Measurements for FMNH P 27393 are from Ostrom (1963), and measurements for other lambeosaurines (excepting RAM 14000) are from Lull and Wright (1942), Evans (2010) , and Sullivan and Williamson (1999). The crest length for AMNH 5340 is estimated from photographs; the crest length for FMNH P 27393 is approximate. All cranial measurements follow those of Dodson (1975) and Evans (2010); crest length is from the top of the orbit to the maximum extent of the crest. AMNH 5340 is included as the most complete and best-known associated skeleton of a juvenile lambeosaurine. Complete measurements, as well as a description of the landmarks used for each measurement, are contained in Figure 5 and Tables 2\u20138. *indicates an incomplete or estimated element length. The number in parentheses in each entry indicates the size relative to RAM 14000. PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Taxon Parasaurolophus sp. P. cyrtocristatus P. walkeri Lambeosaurus sp. Specimen RAM 14000 FMNH P27393 ROM 768 AMNH 5340 Humerus length (mm) 175 565 (0.31) 520 (0.34) 305 (0.57) Ilium length (mm) 301 975 (0.31) 1015 (0.30) 570 (0.53) Prepubis length (mm) 147 430 (0.34) 516 (0.28) 260* (0.57) Ischium length (mm) 243* 1040 (0.23) \u2013 630* (0.39) Femur length (mm) 329 1105 (0.30) 1032 (0.32) 590 (0.56) Tibia length (mm) 307 \u2013 \u2013 550 (0.56) Fibula length (mm) 288 890 (0.32) \u2013 530* (0.54) MT IV length (mm) 100 335 (0.30) \u2013 \u2013 Fibula / femur 0.88 0.80 \u2013 0.90 Skull length (mm) 246 \u2013 745 (0.33) 380 (0.65) Quadrate length (mm) 111 \u2013 272 (0.41) 165 (0.67) Orbit length (mm) 60 \u2013 105 (0.57) 77 (0.78) Orbit height (mm) 50 \u2013 170 (0.29) 82 (0.61) Dentary length (mm) 138 \u2013 455 (0.30) \u2013 Crest length (mm) 62 404* (0.15) 970 (0.06) 90* (0.69) PeerJ reviewing PDF | (v2013:02:267:0:0:NEW 26 Apr 2013) R ev ie w in g M an us cr ip t Table 11(on next page) Estimated resonant frequencies of the crest in Parasaurolophus skulls.",
    "url": "https://peerj.com/articles/183/reviews/",
    "review_1": "Stephen Johnson \u00b7 Oct 1, 2013 \u00b7 Academic Editor\nACCEPT\nThank you for your comprehensive treatment of the reviewers' and my comments. The final manuscript should be relevant to a broader audience than was originally the case.",
    "review_2": "Stephen Johnson \u00b7 Sep 20, 2013 \u00b7 Academic Editor\nMINOR REVISIONS\nThank you for a sound bibliometric study of the differences and relationships between h-indexes calculated by a variety of indexing services. There are some minor errors and issues with the use of English, which are covered comprehensively by the reviewers.\n\nThe only substantial change I would suggest is that you include a short discussion of the features of the soil science literature. The study is probably of interest to a broader audience and a consideration of the nature of this literature would go a long way to helping the reader judge its wider relevance. With this in mind, you might also consider replacing \"pedobibliometric\" with the more general \"bibliometric\" in the abstract and elsewhere.\n\nIf you have not already done so, please ensure that the data you used for the analysis are available, either as a supplementary file with PeerJ, or externally. If there is not a field-specific database of data available, there are a number of general purpose databases, including figshare.com and datadryad.com that you might use.",
    "review_3": "Jennifer Roach \u00b7 Sep 20, 2013\nBasic reporting\nThe problem clearly stated and explained. The article flows nicely and the organization is easy to follow.\nExperimental design\nNo comments\nValidity of the findings\nCheck the paragraph beginning L239 \"The Thompson Reuters Journal Citation Reports... \" The first use of Soil Research as the journal name was February 2011. In 2010 the name was still Australian Journal of Soil Research, so I'm confused. This paragraph needs another look.\nAdditional comments\nThis paper is interesting to read with value to many researchers beyond soil scientists. Acknowledging  the differences between metrics from Web of Science, Google Scholar, and Scopus while demonstrating the relationship is interesting, and I am curious to see this applied in other disciplines. \n\nAdd finesse to the conclusions by eliminating the bullet points. This section should flow like the rest of the paper. \n\nCatch the minor errors with a careful proofreading. Are the references in L220 and L255 for Table 6?\nCite this review as\nRoach J (2013) Peer Review #1 of \"Citations and the h index of soil researchers and journals in the Web of Science, Scopus, and Google Scholar (v0.1)\". PeerJ https://doi.org/10.7287/peerj.183v0.1/reviews/1",
    "review_4": "Eric Brevik \u00b7 Sep 18, 2013\nBasic reporting\nThere are some places where the English usage in the paper could be improved or where points being made need clarification. Detailed comments are:\n\nLine 7 \u2013 The proper address protocol for the United States would be \u201c\u2026Madison, WI, 53706, USA.\u201d\n\nLine 14 \u2013 rewrite \u201c\u2026journal was being used\u2026\u201d to \u201c\u2026journal was used\u2026\u201d\n\nLine 26 \u2013 rewrite \u201c\u2026seem to provided\u2026\u201d to \u201c\u2026seem to provide\u2026\u201d\n\nLine 26 \u2013 rewrite \u201c\u2026higher number of\u2026\u201d to \u201c\u2026higher numbers of\u2026\u201d\n\nLine 33 \u2013 \u201c\u2026mid-west\u2026\u201d should be \u201c\u2026Midwestern\u2026\u201d\n\nLine 51 \u2013 Vine, 2006 is not in the references list.\n\nLine 59 \u2013 rewrite \u201c\u2026citations is reliable\u2026\u201d to \u201c\u2026citations are reliable\u2026\u201d\n\nLine 63 \u2013 suggest rewriting \u201c\u2026researchers with the following areas of interest in:\u2026\u201d to read \u201c\u2026researchers who listed their areas of interest as\u2026\u201d\n\nLine 65 \u2013 rewrite \u201c\u2026Google Scholar\u2019s author\u2026\u201d to \u201c\u2026Google Scholar author\u2026\u201d\n\nLine 65 \u2013 rewrite \u201c\u2026author page.\u201d to \u201c\u2026author pages.\u201d\n\nLine 66 \u2013 rewrite \u201c\u2026researcher was\u2026\u201d to \u201c\u2026researchers were\u2026\u201d (note both words are changed)\n\nLine 69 \u2013 rewrite \u201c\u2026publication were inconsistent\u2026\u201d to \u201c\u2026publication record were inconsistent\u2026\u201d\n\nLines 76-77 \u2013 suggest rewriting \u201cTable 1 shows the statistics of h index, number of publications, number of citations, and year of the first paper from 340 soil researchers in the three databases.\u201d to read \u201cTable 1 shows the h index, number of publications, number of citations, and year of the first paper statistics for 340 soil researchers in the three databases.\n\nLines 81-82 \u2013 Patel et al. is listed as 2013 in the manuscript, but as 2012 in the references. Which is correct?\n\nLine 85 \u2013 rewrite \u201c\u2026of citation is\u2026\u201d to \u201c\u2026of citations is\u2026\u201d\n\nLine 85 \u2013 rewrite \u201c\u2026Google scholar and the median is 866\u2026\u201d to \u201c\u2026Google Scholar, with a median of 866\u2026\u201d (note there are 5 changes in this line)\n\nLine 90 \u2013 You state the periods are slightly different. I assume you mean the periods of time covered by each of the 3 databases? This should be clarified.\n\nLine 96 \u2013 suggest rewriting \u201c\u20261995 and revising the\u2026\u201d to \u201c\u20261995 a revision was made to the\u2026\u201d\n\nLine 96 \u2013 there should be a semicolon (;) after \u201cauthors\u201d\n\nLine 97 \u2013 rewrite \u201c\u202620% extra..\u201d to \u201c\u202620% higher\u2026\u201d\n\nLine 98 \u2013 rewrite \u201c\u2026finding by Falagas\u2026\u201d to \u201c\u2026findings of Falagas\u2026\u201d\n\nLine 104 \u2013 rewrite \u201c\u2026relationship of number\u2026\u201d to \u201c\u201c\u2026relationship between number\u2026\u201d\n\nLine 114 \u2013 suggest rewriting \u201c\u2026citations will not affect much of the\u2026\u201d to \u201c\u2026citations do not have a large effect on the\u2026\u201d\n\nLine 115 \u2013 rewrite \u201c\u2026citations the additional\u2026\u201d to \u201c\u2026citations additional\u2026\u201d\n\nLine 115 \u2013 rewrite \u201c\u2026 paper does not\u2026\u201d to \u201c\u2026 paper do not\u2026\u201d\n\nLine 118 \u2013 rewrite \u201c\u2026study from Franceschet\u2026\u201d to \u201c\u2026study by Franceschet\u2026\u201d\n\nLine 121 \u2013 rewrite \u201c\u2026Scholar has five\u2026\u201d to \u201c\u2026Scholar had five\u2026\u201d\n\nLine 122 \u2013 rewrite \u201c\u2026results of 340\u2026\u201d to \u201c\u2026results from 340\u2026\u201d Also, researchers is spelled wrong in this line.\n\nLine 124 \u2013 rewrite \u201c\u2026for the h index Google\u2026\u201d to \u201c\u2026the h index from Google\u2026\u201d\n\nLine 125 \u2013 rewrite \u201c\u2026is 1.1 higher\u2026\u201d to \u201c\u2026is 1.1 times higher\u2026\u201d\n\nLine 127 \u2013 rewrite \u201c\u2026from UK\u2026\u201d to \u201c\u2026from the UK\u2026\u201d\n\nLine 128 \u2013 Patel et al. is listed as 2013 in the manuscript, but as 2012 in the references. Which is correct?\n\nLine 149 \u2013 rewrite \u201c\u2026publishing since 10 years\u2026\u201d to \u201c\u2026publishing for 10 years\u2026\u201d\n\nLine 151 \u2013 suggest rewriting \u201c\u2026340 soil researchers (which\u2026\u201d to \u201c\u2026340 soil researchers in this study (which\u2026\u201d\n\nLine 155-156 \u2013 There appears to be some misidentification of tables, and what the convey, in this section. In line 155 Table 4 is called for, but the information appears to come from Table 1. Then, in line 156, Table 1 is called for, but the information appears to come from Table 4. There should also probably be a call for Table 4 after the \u201c0.7\u201d in line 155.\n\nLine 161 \u2013 rewrite \u201c\u2026ecology having the\u2026\u201d to \u201c\u2026ecology have the\u2026\u201d\n\nLine 164 \u2013 rewrite \u201c\u2026consistent that soil\u2026\u201d to \u201c\u2026consistent in that soil\u2026\u201d\n\nLine 165 \u2013 rewrite \u201c\u2026sub-discipline also varies in\u2026\u201d to \u201c\u2026sub-disciplines also vary in\u2026\u201d (note there are 2 changes)\n\nLine 166 \u2013 delete the \u2013 after the :\n\nLine 175 \u2013 rewrite \u201c\u2026low number of citations and the\u2026\u201d to \u201c\u2026low numbers of citations with the\u2026\u201d\n\nLine 176 \u2013 rewrite \u201c\u2026decreases with\u2026\u201d to \u201c\u2026decreasing with\u2026\u201d\n\nLines 182-184 \u2013 There is a discussion here of how many citations the average soil researcher receives from various types of publications. Is this the average number of citations per year? The time interval needs to be clarified within this sentence.\n\nLine 183 \u2013 rewrite \u201c\u2026journal articles, additional\u2026\u201d to \u201c\u2026journal articles, an additional\u2026\u201d\n\nLine 199 \u2013 \u201c\u2026references quoted\u2026\u201d Wouldn\u2019t it be more accurate to say \u201c\u2026references cited\u2026\u201d?\n\nLine 204 \u2013 rewrite \u201c\u2026percentage self-citation\u2026\u201d as \u201c\u2026percentage of self-citation\u2026\u201d\n\nLines 204-205 \u2013 It is stated here that established authors cite less of their own work, and that is based on the fact that a weak relationship was found between % of self-citation and scientific age. But the analysis was based on % self-citation. If a young author has 400 citations, and 40 of them are self-citations, they have a self-citation rate of 10%. However, if an established author has 8000 citations, and 400 of them are self-citations, that established author has cited themselves as many times as the young author has total citations, but has a lower self-citation % (5%, or half as much on a % basis). Therefore, I don\u2019t think it is accurate to stay in your paper \u201c\u2026established authors cite less of their own work.\u201d In the example above, the established author has cited more of their own work than the young author. What is true is that a lower % of the citations received by established authors is due to self-citation, and that statement would work in your manuscript.\n\nLine 207 \u2013 rewrite \u201c\u2026researcher matures the papers\u2026\u201d to \u201c\u2026researcher matures their papers\u2026\u201d\n\nLine 208 \u2013 suggest changing \u201c\u2026and more citations\u2026\u201d to \u201c\u2026and more external citations\u2026\u201d\n\nLine 214 \u2013 rewrite \u201c\u2026of journal\u2019s metric, h5-index\u2026\u201d to \u201c\u2026of a journal\u2019s metrics, the h5-index\u2026\u201d (note 3 corrections in this line)\n\nLine 215 \u2013 rewrite \u201c\u2026journals for soil\u2026\u201d to \u201c\u2026journals for the soil\u2026\u201d\n\nLine 219 \u2013 rewrite \u201c\u2026Scholar metric\u2026\u201d to \u201c\u2026Scholar metrics\u2026\u201d (metrics is plural on the Google Scholar page)\n\nLine 220 \u2013 The manuscript refers to Table 5, but the material referenced appears to be in Table 6.\n\nLine 221 \u2013 rewrite \u201c\u2026IF, whereas Figure\u2026\u201d to \u201c\u2026IF, and Figure\u2026\u201d\n\nLine 222 \u2013 rewrite \u201c\u2026year IF has a\u2026\u201d to \u201c\u2026year IF have a\u2026\u201d\n\nLine 225 \u2013 rewrite \u201c\u2026different in the ranking\u2026\u201d to \u201c\u2026different in their ranking\u2026\u201d\n\nLine 226 \u2013 rewrite \u201cThe 2 journals are\u2026\u201d to \u201cThe top two journals are\u2026\u201d\n\nLine 226 \u2013 rewrite \u201c\u2026maintain high number\u2026\u201d to \u201c\u2026maintain a high number\u2026\u201d\n\nLine 227 \u2013 rewrite \u201c\u2026papers they published.\u201d to \u201c\u2026papers they publish.\u201d\n\nLine 233 \u2013 rewrite \u201cAll these are journals\u2026\u201d to \u201cAll these journals\u2026\u201d\n\nLine 235 \u2013 rewrite \u201c\u2026GS and ranked 25 in\u2026\u201d to \u201c\u2026GS and 25 in\u2026\u201d\n\nLine 248 \u2013 rewrite \u201c\u2026increase much rapidly with\u2026\u201d to \u201c\u2026increase rapidly with\u2026\u201d\n\nLine 249 \u2013 rewrite \u201c\u20261000 citation). For the other 7 journals\u2026\u201d to \u201c\u20261000 citations). For the seven journals\u2026\u201d\n\nLine 250 \u2013 rewrite \u201c\u2026is half (0.6 IF increase\u2026\u201d to \u201c\u2026is half as much (0.6 IF increase\u2026\u201d\n\nLine 251 \u2013 rewrite \u201c\u2026for journals to publish\u2026\u201d to \u201c\u2026for journals that publish\u2026\u201d\n\nLine 251 \u2013 rewrite \u201cMeanwhile h5-index\u2026\u201d to \u201cMeanwhile the h5-index\u2026\u201d\n\nLine 252 \u2013 rewrite \u201c\u2026by no. citations\u2026\u201d to \u201c\u2026by no. of citations\u2026\u201d\n\nLine 253 \u2013 rewrite \u201c\u2026from WoS, h5-index\u2026\u201d to \u201c\u2026from WoS, the h5-index\u2026\u201d\n\nLine 255 \u2013 Table 5 is referenced but the material seems to be in Table 6.\n\nLine 255 \u2013 rewrite \u201c\u2026that GS h5-index\u2026\u201d to \u201c\u2026that the GS h5-index\u2026\u201d\n\nLine 258 \u2013 rewrite \u201cCitation from a highly\u2026\u201d to \u201cA citation from a highly\u2026\u201d\n\nLine 260 \u2013 rewrite \u201c\u2026self-citation as compared to impact\u2026\u201d to \u201c\u2026self-citation than the impact\u2026\u201d\n\nLines 267-268 \u2013 \u201c\u2026and is shows that only 1-9% (median 5%) of the total papers that contributed to h5-index.\u201d This is an incomplete thought. What about the 1-9% of the total papers that contributed to the h5-index?\n\nLine 268 \u2013 rewrite \u201cAnd we also\u2026\u201d to \u201cWe also\u2026\u201d\n\nLine 268 \u2013 rewrite \u201c\u2026that h5-index keeps\u2026\u201d to \u201c\u2026that the h5-index keeps\u2026\u201d\n\nLine 270 \u2013 rewrite \u201c\u2026use of GS h index\u2026\u201d to \u201c\u2026use of the GS h index\u2026\u201d\n\nLine 272 \u2013 rewrite \u201c\u2026performance when compared to impact\u2026\u201d to \u201c\u2026performance than the impact\u2026\u201d\n\nLine 275 \u2013 Should Falagas and Alexiou, 2008 be Falagas et al., 2008? There is a Falagas et al. in the references list, but no Falagas and Alexiou.\n\nLine 277 \u2013 rewrite \u201c\u2026artificially increases the\u2026\u201d to \u201c\u2026artificially increase the\u2026\u201d\n\nLine 288 \u2013 rewrite \u201c\u2026of citation and\u2026\u201d to \u201c\u2026of citations and\u2026\u201d\n\nLine 290 \u2013 rewrite \u201c\u2026relationships of the h index between these\u2026\u201d to \u201c\u2026relationships between the h indices in these\u2026\u201d\n\nLine 294 \u2013 rewrite \u201c\u2026affects for assessing scientific\u2026\u201d to \u201c\u2026affects the assessment of scientific\u2026\u201d\n\nLine 299 \u2013 rewrite \u201c\u2026Scholar include other\u2026\u201d to \u201c\u2026Scholar includes other\u2026\u201d\n\nLine 301 \u2013 rewrite \u201c\u2026anyone interested\u2026\u201d to \u201c\u2026anyone interested in\u2026\u201d\n\nLine 302 \u2013 rewrite \u201c\u2026aware whether these\u2026\u201d to \u201c\u2026aware of whether these\u2026\u201d\n\nLine 304 \u2013 rewrite \u201c\u2026relating h index\u2026\u201d to \u201c\u2026relating the h index\u2026\u201d\n\nLines 316-318 \u2013 Should this be Falagas et al., 2008 or Falagas and Alexiou, 2008?\n\nLines 351-354 \u2013 Should this be Patel et al. 2012 or 2013?\n\nLine 357 \u2013 Vine, 2006 should be entered here.\n\nTable 1 \u2013 The right side of my Table 1 has been cut off.\nExperimental design\nThe experimental design and statistical analyses are solid.\nValidity of the findings\nThe findings are supported by the statistical analysis.\nAdditional comments\nThis is an interesting study that sheds light on how we rate, or evaluate, the prestige of scientific work done by individual researchers and the journals that publish that work in the soil science discipline. Such studies are important to fully understand the reporting of scientific findings and motivations behind the choices scientists make in selecting publication outlets.\nCite this review as\nBrevik E (2013) Peer Review #2 of \"Citations and the h index of soil researchers and journals in the Web of Science, Scopus, and Google Scholar (v0.1)\". PeerJ https://doi.org/10.7287/peerj.183v0.1/reviews/2",
    "pdf_1": "https://peerj.com/articles/183v0.2/submission",
    "pdf_2": "https://peerj.com/articles/183v0.1/submission",
    "review_5": "Reviewer 3 \u00b7 Sep 13, 2013\nBasic reporting\nI think that it is a useful bibliometric study, which would be useful for all the specialists in scientific planning, and especially for soil scientists. The only addition I would suggest is a short discussion of the peculiarity of publication in soil science (generally it is a longer period between data collection and publication, relatively small community etc.). I think that a couple of sentences in the introductory part would be great.\nExperimental design\nNo comments.\nValidity of the findings\nNo comments.\nCite this review as\nAnonymous Reviewer (2013) Peer Review #3 of \"Citations and the h index of soil researchers and journals in the Web of Science, Scopus, and Google Scholar (v0.1)\". PeerJ https://doi.org/10.7287/peerj.183v0.1/reviews/3",
    "all_reviews": "Review 1: Stephen Johnson \u00b7 Oct 1, 2013 \u00b7 Academic Editor\nACCEPT\nThank you for your comprehensive treatment of the reviewers' and my comments. The final manuscript should be relevant to a broader audience than was originally the case.\nReview 2: Stephen Johnson \u00b7 Sep 20, 2013 \u00b7 Academic Editor\nMINOR REVISIONS\nThank you for a sound bibliometric study of the differences and relationships between h-indexes calculated by a variety of indexing services. There are some minor errors and issues with the use of English, which are covered comprehensively by the reviewers.\n\nThe only substantial change I would suggest is that you include a short discussion of the features of the soil science literature. The study is probably of interest to a broader audience and a consideration of the nature of this literature would go a long way to helping the reader judge its wider relevance. With this in mind, you might also consider replacing \"pedobibliometric\" with the more general \"bibliometric\" in the abstract and elsewhere.\n\nIf you have not already done so, please ensure that the data you used for the analysis are available, either as a supplementary file with PeerJ, or externally. If there is not a field-specific database of data available, there are a number of general purpose databases, including figshare.com and datadryad.com that you might use.\nReview 3: Jennifer Roach \u00b7 Sep 20, 2013\nBasic reporting\nThe problem clearly stated and explained. The article flows nicely and the organization is easy to follow.\nExperimental design\nNo comments\nValidity of the findings\nCheck the paragraph beginning L239 \"The Thompson Reuters Journal Citation Reports... \" The first use of Soil Research as the journal name was February 2011. In 2010 the name was still Australian Journal of Soil Research, so I'm confused. This paragraph needs another look.\nAdditional comments\nThis paper is interesting to read with value to many researchers beyond soil scientists. Acknowledging  the differences between metrics from Web of Science, Google Scholar, and Scopus while demonstrating the relationship is interesting, and I am curious to see this applied in other disciplines. \n\nAdd finesse to the conclusions by eliminating the bullet points. This section should flow like the rest of the paper. \n\nCatch the minor errors with a careful proofreading. Are the references in L220 and L255 for Table 6?\nCite this review as\nRoach J (2013) Peer Review #1 of \"Citations and the h index of soil researchers and journals in the Web of Science, Scopus, and Google Scholar (v0.1)\". PeerJ https://doi.org/10.7287/peerj.183v0.1/reviews/1\nReview 4: Eric Brevik \u00b7 Sep 18, 2013\nBasic reporting\nThere are some places where the English usage in the paper could be improved or where points being made need clarification. Detailed comments are:\n\nLine 7 \u2013 The proper address protocol for the United States would be \u201c\u2026Madison, WI, 53706, USA.\u201d\n\nLine 14 \u2013 rewrite \u201c\u2026journal was being used\u2026\u201d to \u201c\u2026journal was used\u2026\u201d\n\nLine 26 \u2013 rewrite \u201c\u2026seem to provided\u2026\u201d to \u201c\u2026seem to provide\u2026\u201d\n\nLine 26 \u2013 rewrite \u201c\u2026higher number of\u2026\u201d to \u201c\u2026higher numbers of\u2026\u201d\n\nLine 33 \u2013 \u201c\u2026mid-west\u2026\u201d should be \u201c\u2026Midwestern\u2026\u201d\n\nLine 51 \u2013 Vine, 2006 is not in the references list.\n\nLine 59 \u2013 rewrite \u201c\u2026citations is reliable\u2026\u201d to \u201c\u2026citations are reliable\u2026\u201d\n\nLine 63 \u2013 suggest rewriting \u201c\u2026researchers with the following areas of interest in:\u2026\u201d to read \u201c\u2026researchers who listed their areas of interest as\u2026\u201d\n\nLine 65 \u2013 rewrite \u201c\u2026Google Scholar\u2019s author\u2026\u201d to \u201c\u2026Google Scholar author\u2026\u201d\n\nLine 65 \u2013 rewrite \u201c\u2026author page.\u201d to \u201c\u2026author pages.\u201d\n\nLine 66 \u2013 rewrite \u201c\u2026researcher was\u2026\u201d to \u201c\u2026researchers were\u2026\u201d (note both words are changed)\n\nLine 69 \u2013 rewrite \u201c\u2026publication were inconsistent\u2026\u201d to \u201c\u2026publication record were inconsistent\u2026\u201d\n\nLines 76-77 \u2013 suggest rewriting \u201cTable 1 shows the statistics of h index, number of publications, number of citations, and year of the first paper from 340 soil researchers in the three databases.\u201d to read \u201cTable 1 shows the h index, number of publications, number of citations, and year of the first paper statistics for 340 soil researchers in the three databases.\n\nLines 81-82 \u2013 Patel et al. is listed as 2013 in the manuscript, but as 2012 in the references. Which is correct?\n\nLine 85 \u2013 rewrite \u201c\u2026of citation is\u2026\u201d to \u201c\u2026of citations is\u2026\u201d\n\nLine 85 \u2013 rewrite \u201c\u2026Google scholar and the median is 866\u2026\u201d to \u201c\u2026Google Scholar, with a median of 866\u2026\u201d (note there are 5 changes in this line)\n\nLine 90 \u2013 You state the periods are slightly different. I assume you mean the periods of time covered by each of the 3 databases? This should be clarified.\n\nLine 96 \u2013 suggest rewriting \u201c\u20261995 and revising the\u2026\u201d to \u201c\u20261995 a revision was made to the\u2026\u201d\n\nLine 96 \u2013 there should be a semicolon (;) after \u201cauthors\u201d\n\nLine 97 \u2013 rewrite \u201c\u202620% extra..\u201d to \u201c\u202620% higher\u2026\u201d\n\nLine 98 \u2013 rewrite \u201c\u2026finding by Falagas\u2026\u201d to \u201c\u2026findings of Falagas\u2026\u201d\n\nLine 104 \u2013 rewrite \u201c\u2026relationship of number\u2026\u201d to \u201c\u201c\u2026relationship between number\u2026\u201d\n\nLine 114 \u2013 suggest rewriting \u201c\u2026citations will not affect much of the\u2026\u201d to \u201c\u2026citations do not have a large effect on the\u2026\u201d\n\nLine 115 \u2013 rewrite \u201c\u2026citations the additional\u2026\u201d to \u201c\u2026citations additional\u2026\u201d\n\nLine 115 \u2013 rewrite \u201c\u2026 paper does not\u2026\u201d to \u201c\u2026 paper do not\u2026\u201d\n\nLine 118 \u2013 rewrite \u201c\u2026study from Franceschet\u2026\u201d to \u201c\u2026study by Franceschet\u2026\u201d\n\nLine 121 \u2013 rewrite \u201c\u2026Scholar has five\u2026\u201d to \u201c\u2026Scholar had five\u2026\u201d\n\nLine 122 \u2013 rewrite \u201c\u2026results of 340\u2026\u201d to \u201c\u2026results from 340\u2026\u201d Also, researchers is spelled wrong in this line.\n\nLine 124 \u2013 rewrite \u201c\u2026for the h index Google\u2026\u201d to \u201c\u2026the h index from Google\u2026\u201d\n\nLine 125 \u2013 rewrite \u201c\u2026is 1.1 higher\u2026\u201d to \u201c\u2026is 1.1 times higher\u2026\u201d\n\nLine 127 \u2013 rewrite \u201c\u2026from UK\u2026\u201d to \u201c\u2026from the UK\u2026\u201d\n\nLine 128 \u2013 Patel et al. is listed as 2013 in the manuscript, but as 2012 in the references. Which is correct?\n\nLine 149 \u2013 rewrite \u201c\u2026publishing since 10 years\u2026\u201d to \u201c\u2026publishing for 10 years\u2026\u201d\n\nLine 151 \u2013 suggest rewriting \u201c\u2026340 soil researchers (which\u2026\u201d to \u201c\u2026340 soil researchers in this study (which\u2026\u201d\n\nLine 155-156 \u2013 There appears to be some misidentification of tables, and what the convey, in this section. In line 155 Table 4 is called for, but the information appears to come from Table 1. Then, in line 156, Table 1 is called for, but the information appears to come from Table 4. There should also probably be a call for Table 4 after the \u201c0.7\u201d in line 155.\n\nLine 161 \u2013 rewrite \u201c\u2026ecology having the\u2026\u201d to \u201c\u2026ecology have the\u2026\u201d\n\nLine 164 \u2013 rewrite \u201c\u2026consistent that soil\u2026\u201d to \u201c\u2026consistent in that soil\u2026\u201d\n\nLine 165 \u2013 rewrite \u201c\u2026sub-discipline also varies in\u2026\u201d to \u201c\u2026sub-disciplines also vary in\u2026\u201d (note there are 2 changes)\n\nLine 166 \u2013 delete the \u2013 after the :\n\nLine 175 \u2013 rewrite \u201c\u2026low number of citations and the\u2026\u201d to \u201c\u2026low numbers of citations with the\u2026\u201d\n\nLine 176 \u2013 rewrite \u201c\u2026decreases with\u2026\u201d to \u201c\u2026decreasing with\u2026\u201d\n\nLines 182-184 \u2013 There is a discussion here of how many citations the average soil researcher receives from various types of publications. Is this the average number of citations per year? The time interval needs to be clarified within this sentence.\n\nLine 183 \u2013 rewrite \u201c\u2026journal articles, additional\u2026\u201d to \u201c\u2026journal articles, an additional\u2026\u201d\n\nLine 199 \u2013 \u201c\u2026references quoted\u2026\u201d Wouldn\u2019t it be more accurate to say \u201c\u2026references cited\u2026\u201d?\n\nLine 204 \u2013 rewrite \u201c\u2026percentage self-citation\u2026\u201d as \u201c\u2026percentage of self-citation\u2026\u201d\n\nLines 204-205 \u2013 It is stated here that established authors cite less of their own work, and that is based on the fact that a weak relationship was found between % of self-citation and scientific age. But the analysis was based on % self-citation. If a young author has 400 citations, and 40 of them are self-citations, they have a self-citation rate of 10%. However, if an established author has 8000 citations, and 400 of them are self-citations, that established author has cited themselves as many times as the young author has total citations, but has a lower self-citation % (5%, or half as much on a % basis). Therefore, I don\u2019t think it is accurate to stay in your paper \u201c\u2026established authors cite less of their own work.\u201d In the example above, the established author has cited more of their own work than the young author. What is true is that a lower % of the citations received by established authors is due to self-citation, and that statement would work in your manuscript.\n\nLine 207 \u2013 rewrite \u201c\u2026researcher matures the papers\u2026\u201d to \u201c\u2026researcher matures their papers\u2026\u201d\n\nLine 208 \u2013 suggest changing \u201c\u2026and more citations\u2026\u201d to \u201c\u2026and more external citations\u2026\u201d\n\nLine 214 \u2013 rewrite \u201c\u2026of journal\u2019s metric, h5-index\u2026\u201d to \u201c\u2026of a journal\u2019s metrics, the h5-index\u2026\u201d (note 3 corrections in this line)\n\nLine 215 \u2013 rewrite \u201c\u2026journals for soil\u2026\u201d to \u201c\u2026journals for the soil\u2026\u201d\n\nLine 219 \u2013 rewrite \u201c\u2026Scholar metric\u2026\u201d to \u201c\u2026Scholar metrics\u2026\u201d (metrics is plural on the Google Scholar page)\n\nLine 220 \u2013 The manuscript refers to Table 5, but the material referenced appears to be in Table 6.\n\nLine 221 \u2013 rewrite \u201c\u2026IF, whereas Figure\u2026\u201d to \u201c\u2026IF, and Figure\u2026\u201d\n\nLine 222 \u2013 rewrite \u201c\u2026year IF has a\u2026\u201d to \u201c\u2026year IF have a\u2026\u201d\n\nLine 225 \u2013 rewrite \u201c\u2026different in the ranking\u2026\u201d to \u201c\u2026different in their ranking\u2026\u201d\n\nLine 226 \u2013 rewrite \u201cThe 2 journals are\u2026\u201d to \u201cThe top two journals are\u2026\u201d\n\nLine 226 \u2013 rewrite \u201c\u2026maintain high number\u2026\u201d to \u201c\u2026maintain a high number\u2026\u201d\n\nLine 227 \u2013 rewrite \u201c\u2026papers they published.\u201d to \u201c\u2026papers they publish.\u201d\n\nLine 233 \u2013 rewrite \u201cAll these are journals\u2026\u201d to \u201cAll these journals\u2026\u201d\n\nLine 235 \u2013 rewrite \u201c\u2026GS and ranked 25 in\u2026\u201d to \u201c\u2026GS and 25 in\u2026\u201d\n\nLine 248 \u2013 rewrite \u201c\u2026increase much rapidly with\u2026\u201d to \u201c\u2026increase rapidly with\u2026\u201d\n\nLine 249 \u2013 rewrite \u201c\u20261000 citation). For the other 7 journals\u2026\u201d to \u201c\u20261000 citations). For the seven journals\u2026\u201d\n\nLine 250 \u2013 rewrite \u201c\u2026is half (0.6 IF increase\u2026\u201d to \u201c\u2026is half as much (0.6 IF increase\u2026\u201d\n\nLine 251 \u2013 rewrite \u201c\u2026for journals to publish\u2026\u201d to \u201c\u2026for journals that publish\u2026\u201d\n\nLine 251 \u2013 rewrite \u201cMeanwhile h5-index\u2026\u201d to \u201cMeanwhile the h5-index\u2026\u201d\n\nLine 252 \u2013 rewrite \u201c\u2026by no. citations\u2026\u201d to \u201c\u2026by no. of citations\u2026\u201d\n\nLine 253 \u2013 rewrite \u201c\u2026from WoS, h5-index\u2026\u201d to \u201c\u2026from WoS, the h5-index\u2026\u201d\n\nLine 255 \u2013 Table 5 is referenced but the material seems to be in Table 6.\n\nLine 255 \u2013 rewrite \u201c\u2026that GS h5-index\u2026\u201d to \u201c\u2026that the GS h5-index\u2026\u201d\n\nLine 258 \u2013 rewrite \u201cCitation from a highly\u2026\u201d to \u201cA citation from a highly\u2026\u201d\n\nLine 260 \u2013 rewrite \u201c\u2026self-citation as compared to impact\u2026\u201d to \u201c\u2026self-citation than the impact\u2026\u201d\n\nLines 267-268 \u2013 \u201c\u2026and is shows that only 1-9% (median 5%) of the total papers that contributed to h5-index.\u201d This is an incomplete thought. What about the 1-9% of the total papers that contributed to the h5-index?\n\nLine 268 \u2013 rewrite \u201cAnd we also\u2026\u201d to \u201cWe also\u2026\u201d\n\nLine 268 \u2013 rewrite \u201c\u2026that h5-index keeps\u2026\u201d to \u201c\u2026that the h5-index keeps\u2026\u201d\n\nLine 270 \u2013 rewrite \u201c\u2026use of GS h index\u2026\u201d to \u201c\u2026use of the GS h index\u2026\u201d\n\nLine 272 \u2013 rewrite \u201c\u2026performance when compared to impact\u2026\u201d to \u201c\u2026performance than the impact\u2026\u201d\n\nLine 275 \u2013 Should Falagas and Alexiou, 2008 be Falagas et al., 2008? There is a Falagas et al. in the references list, but no Falagas and Alexiou.\n\nLine 277 \u2013 rewrite \u201c\u2026artificially increases the\u2026\u201d to \u201c\u2026artificially increase the\u2026\u201d\n\nLine 288 \u2013 rewrite \u201c\u2026of citation and\u2026\u201d to \u201c\u2026of citations and\u2026\u201d\n\nLine 290 \u2013 rewrite \u201c\u2026relationships of the h index between these\u2026\u201d to \u201c\u2026relationships between the h indices in these\u2026\u201d\n\nLine 294 \u2013 rewrite \u201c\u2026affects for assessing scientific\u2026\u201d to \u201c\u2026affects the assessment of scientific\u2026\u201d\n\nLine 299 \u2013 rewrite \u201c\u2026Scholar include other\u2026\u201d to \u201c\u2026Scholar includes other\u2026\u201d\n\nLine 301 \u2013 rewrite \u201c\u2026anyone interested\u2026\u201d to \u201c\u2026anyone interested in\u2026\u201d\n\nLine 302 \u2013 rewrite \u201c\u2026aware whether these\u2026\u201d to \u201c\u2026aware of whether these\u2026\u201d\n\nLine 304 \u2013 rewrite \u201c\u2026relating h index\u2026\u201d to \u201c\u2026relating the h index\u2026\u201d\n\nLines 316-318 \u2013 Should this be Falagas et al., 2008 or Falagas and Alexiou, 2008?\n\nLines 351-354 \u2013 Should this be Patel et al. 2012 or 2013?\n\nLine 357 \u2013 Vine, 2006 should be entered here.\n\nTable 1 \u2013 The right side of my Table 1 has been cut off.\nExperimental design\nThe experimental design and statistical analyses are solid.\nValidity of the findings\nThe findings are supported by the statistical analysis.\nAdditional comments\nThis is an interesting study that sheds light on how we rate, or evaluate, the prestige of scientific work done by individual researchers and the journals that publish that work in the soil science discipline. Such studies are important to fully understand the reporting of scientific findings and motivations behind the choices scientists make in selecting publication outlets.\nCite this review as\nBrevik E (2013) Peer Review #2 of \"Citations and the h index of soil researchers and journals in the Web of Science, Scopus, and Google Scholar (v0.1)\". PeerJ https://doi.org/10.7287/peerj.183v0.1/reviews/2\nReview 5: Reviewer 3 \u00b7 Sep 13, 2013\nBasic reporting\nI think that it is a useful bibliometric study, which would be useful for all the specialists in scientific planning, and especially for soil scientists. The only addition I would suggest is a short discussion of the peculiarity of publication in soil science (generally it is a longer period between data collection and publication, relatively small community etc.). I think that a couple of sentences in the introductory part would be great.\nExperimental design\nNo comments.\nValidity of the findings\nNo comments.\nCite this review as\nAnonymous Reviewer (2013) Peer Review #3 of \"Citations and the h index of soil researchers and journals in the Web of Science, Scopus, and Google Scholar (v0.1)\". PeerJ https://doi.org/10.7287/peerj.183v0.1/reviews/3\nReview 6: \n",
    "LLM_extracted_review": "['Review 1: Thank you for your comprehensive treatment of the reviewers\\' and my comments. The final manuscript should be relevant to a broader audience than was originally the case.\\n\\nReview 2: Thank you for a sound bibliometric study of the differences and relationships between h-indexes calculated by a variety of indexing services. There are some minor errors and issues with the use of English, which are covered comprehensively by the reviewers. The only substantial change I would suggest is that you include a short discussion of the features of the soil science literature. The study is probably of interest to a broader audience and a consideration of the nature of this literature would go a long way to helping the reader judge its wider relevance. With this in mind, you might also consider replacing \"pedobibliometric\" with the more general \"bibliometric\" in the abstract and elsewhere. If you have not already done so, please ensure that the data you used for the analysis are available, either as a supplementary file with PeerJ, or externally.\\n\\nReview 3: The problem clearly stated and explained. The article flows nicely and the organization is easy to follow. Check the paragraph beginning L239 \"The Thompson Reuters Journal Citation Reports... \" The first use of Soil Research as the journal name was February 2011. In 2010 the name was still Australian Journal of Soil Research, so I\\'m confused. This paragraph needs another look. This paper is interesting to read with value to many researchers beyond soil scientists. Acknowledging the differences between metrics from Web of Science, Google Scholar, and Scopus while demonstrating the relationship is interesting, and I am curious to see this applied in other disciplines. Add finesse to the conclusions by eliminating the bullet points. This section should flow like the rest of the paper. Catch the minor errors with a careful proofreading.\\n\\nReview 4: There are some places where the English usage in the paper could be improved or where points being made need clarification. The experimental design and statistical analyses are solid. The findings are supported by the statistical analysis. This is an interesting study that sheds light on how we rate, or evaluate, the prestige of scientific work done by individual researchers and the journals that publish that work in the soil science discipline. Such studies are important to fully understand the reporting of scientific findings and motivations behind the choices scientists make in selecting publication outlets.\\n\\nReview 5: I think that it is a useful bibliometric study, which would be useful for all the specialists in scientific planning, and especially for soil scientists. The only addition I would suggest is a short discussion of the peculiarity of publication in soil science (generally it is a longer period between data collection and publication, relatively small community etc.).']"
}