Download pdf - Goodwin & Horner, 2004

q 2004 The Paleontological Society. All rights reserved. 0094-8373/04/3002-0007/$1.00

Paleobiology, 30(2), 2004, pp. 253–267

Cranial histology of pachycephalosaurs (Ornithischia:Marginocephalia) reveals transitory structures inconsistent withhead-butting behavior

Mark B. Goodwin and John R. Horner

Abstract.—Modern histological techniques allow paleontologists to investigate the internal micro-structure of bone tissue. We apply high resolution images of histological thin sections from an on-togenetic series (not conspecific) of pachycephalosaurid frontoparietal domes to test the hypothesisthat these Late Cretaceous dinosaurs used their heads as battering rams, analogous to the behaviorof the bighorn sheep, Ovis canadensis, or as a thermoregulatory device. Our analysis reveals thatthe internal structure of the pachycephalosaur dome is a dynamic tissue that reflects the changeableexpansion and vascularity of the dome throughout ontogeny. The radiating structures within thefrontoparietal dome, used previously to support ‘‘head-butting’’ hypotheses, are unexpectedlytransitory, diminishing in mature individuals and nearly absent in adult skulls where head-buttingbehavior is presumed to occur. The unique architecture of the pachycephalosaurid dome is divid-able into three distinct Zones. We demonstrate that the relative vascularity, associated tissue struc-tures, and orientation and density of Sharpey’s fibers within these Zones are modified duringgrowth. Evidence for an external dome covering in vivo precludes the determination of the finalshape of the pachycephalosaur skull. On the basis of these new observations, we propose that cra-nial display in support of species recognition and communication is a more parsimonious inter-pretation of the function of the pachycephalosaurid dome. Sexual display behaviors were probablysecondary.

Mark B. Goodwin. Museum of Paleontology, University of California, Berkeley, California 94720 and De-partment of Geology, University of California, Davis, California 95616. E-mail: [email protected]

John R. Horner. Museum of the Rockies, Montana State University, Bozeman, Montana 59717. E-mail:[email protected]

Accepted: 15 September 2003

Introduction

Pachycephalosaurs (Ornithischia: Margino-cephalia), popularly known as dome-headeddinosaurs, are a group of bipedal ornithischi-an dinosaurs characterized by their distinctivegreatly thickened dome above their braincase(Sues and Galton 1987). The majority of LateCretaceous species occur in the Western Inte-rior of North America and central Asia (Sues1997). The pachycephalosaurid dome is madeup of the fused paired frontals and parietalbones (Fig. 1). The degree of inflation or domethickness, shape of the dome, and incorpora-tion of the squamosal and lateral cranial ele-ments into the dome have all been used as (1)diagnostic characters of the group (Maryan-ska and Osmolska 1974; Sereno 1986; Suesand Galton 1987; Maryanska 1990; Sullivan2000, 2003; Williamson and Carr 2002); (2)support for recognizing sexual dimorphism(Chapman et al. 1981); and (3) relative age as-signment of individual specimens (Giffin

1989; Goodwin et al. 1998; Williamson andCarr 2002).

The function of the domed skull of pachy-cephalosaurid dinosaurs has puzzled paleon-tologists for decades and continues to stimu-late debate on the topic (Carpenter 1997; Hor-ner and Goodwin 1998). Previous studiesform the basis for the paleobiological inter-pretation that internal cranial features in thethickened pachycephalosaurid dome support-ed head-butting behavior.

What bones in the skull contribute to thepachycephalosaurid dome? This was a ques-tion Brown and Schlaikjer asked in their 1943study describing a new assemblage of pachy-cephalosaurid dinosaurs (known then as troo-donts) from the Western Interior of NorthAmerica. Brown and Schlaikjer (1943: p.145)confirmed the absence of fused dermal ossi-fications over the skull roof (contra Gilmore1931: p. 3) and demonstrated that the pachy-cephalosaurid dome was made up of the fused

254 MARK B. GOODWIN AND JOHN R. HORNER

FIGURE 1. The pachycephalosaurid frontoparietal (fp) dome is shown in the stippled portion of this illustration ofthe skull of Stegoceras validum (UA 2) in left lateral view (A) and dorsal view (B). The fused paired frontals and theparietal coalesce and inflate during ontogeny to form the fp dome in pachycephalosaurid dinosaurs.

frontals and parietal bones. In addition, theyrecognized the variable density in the internalcomposition of the dome and described the in-terior of the dome as having a ‘‘radiatingstructure.’’ This variability in dome densitywas also noted earlier by Lambe (1918: p. 24)who described the inner organization of thedome as possessing a ‘‘columnar structure.’’

Colbert (1955: p. 195) first suggested, ‘‘Per-haps (as a very wild surmise) the skull wasused as a sort of battering ram.’’ L. Spraguede Camp (1956: p. 17) popularized this idea ayear later in his science fiction story ‘‘A Gunfor Dinosaur,’’ writing that ‘‘the males butteach other with these heads in fighting overthe females.’’ Galton (1970: p. 23) referred topachycephalosaurids as ‘‘Dinosaurian Batter-ing Rams’’ in the title of his 1970 study andproposed that the thick pachycephalosauriddome was used in the same mode as the hornsof fighting rams in the mountain sheep, Oviscanadensis. Galton (1970: p. 31) described theinternal texture of the pachycephalosauriddome as ‘‘a radiating series of trabeculae orbony fibers, each of which is perpendicular tothe outer surface of the dome’’ (sensu Brown

and Schlaikjer 1943) and suggested that thedome was used for head-butting, acknowl-edging L. Sprague de Camp’s short story. Gal-ton (1971: p. 45) went on to claim ‘‘this ar-rangement is ideal for resisting a force appliedagainst the top of the dome’’ without furtherquantification. In a follow-up study of the pa-chycephalosaurid dome using photoelasticanalysis, Sues (1978) stressed a piece of plex-iglass in the shape of a pachycephalosauriddome. This produced a radiating pattern sim-ilar to the radiating structure in the coronal-sectioned pachycephalosaurid dome de-scribed and figured earlier by Brown andSchlaikjer (1943: p. 143). Sues (1978: p. 465)concluded, ‘‘The radiating pattern of the tra-beculae and the fact that the trabeculae areoriented in a perpendicular fashion to the dor-sal surface of the frontoparietal invite a func-tional explanation. Working with the trajec-torial theory of bone architecture, the trabec-ulae could be considered to be compressiveresistant.’’ According to Alexander (1997: p.423), ‘‘the bone of the pachycephalosaur domeseems to have had a spongy texture, so itprobably deformed enough in an impact to

255PACHYCEPHALOSAUR CRANIAL HISTOLOGY

FIGURE 2. Phylogenetic placement of Pachycephalosau-rus, Stegoceras, Stygimoloch, and MOR 453 and UCMP134979. Cladistic relationships from Sereno 1986. MOR453 is a full-domed taxon with the frontoparietal domeexpanded posteriorly. The lateral cranial sutures indi-cate that the fp dome incorporates the postorbitals andsquamosals, synapomorphies for the Pachycephalosaur-inae of Sereno (1986).

provide useful cushioning.’’ Rigby et al.(1987), Landry (1995), and Reid (1996) sug-gested that the internal ‘‘radiating structures’’of the pachycephalosaur dome indicated thedome was more suitable as a heat-exchangeorgan than for head-butting.

In our preliminary study (Horner andGoodwin 1998) and in this more comprehen-sive cranial histological analysis, we confirmthat these radiating trabeculae occur in some pa-chycephalosaurid domes. Our observation,however, does not end there. We also have de-termined that these internal features of theskull are, in fact, transitory and limited to anearly stage of ontogeny. During growth of theskull, these radiating structures within thedome are transformed and later lost as thefrontoparietal dome fully develops in adultindividuals, where head-butting behavior ispresumed to occur.

Materials and Methods

Institutional Abbreviations. CM 5 CarnegieMuseum of Natural History, Pittsburgh, Penn-sylvania; CMN 5 Canadian Museum of Na-ture, formerly GSC 5 Geological Survey ofCanada and NMC 5 National Museum ofCanada, Ottawa; MOR 5 Museum of theRockies, Montana State University, Bozeman;UCMP 5 University of California Museum ofPaleontology, Berkeley; VRD 5 Sierra College,Rocklin, California.

Seven pachycephalosaurid frontoparietaldomes (not con-specific) were sectioned withan Isomet diamond saw. The samples wereembedded in Silmar-40 polyester resin priorto cutting and mounted to glass slides withepoxy resin. Sagittal, coronal, and transversecuts were made. Our use of an ultra-thin(0.012-inch) diamond saw blade results in aminimal loss of fossil material for study. Ar-chival casts were made of the specimens be-fore cutting and are cataloged in the collec-tions of the MOR and UCMP. The thin-sectionswere ground on a Buehler Ecomet grinder andsections were studied by light microscopy un-der normal and polarized light. Histologicalsections from this study are cataloged into theslide libraries of the MOR and UCMP.

The specimens are as follows: UCMP130049, Stegoceras sp., frontoparietal dome, Ju-

dith River Formation; MOR 295, Stegocerasvalidum, unfused left and right frontals, Ju-dith River Formation; UCMP 134979, pachy-cephalosaurid indet., frontoparietal dome,Hell Creek Formation; MOR 1179, Stegocerasvalidum, frontoparietal dome, Judith River For-mation; UCMP 128383, Stygimoloch spinifer,Hell Creek Formation; MOR 453, pachyce-phalosaurid indet. (full-domed taxon), fron-toparietal dome, Two Medicine Formation;VRD 13, Pachycephalosaurus wyomingensis (sen-su Sues and Galton 1987), partial skull, HellCreek Formation.

Assessing Ontogeny

The seven pachycephalosaurid frontopari-etal domes selected for histological analysiscomprise a size gradient among phylogeneti-cally closely related taxa (Fig. 2). They were allcollected from the coeval Judith River andTwo Medicine Formations, and the slightlyyounger Hell Creek Formation, all part of theUpper Cretaceous sequence of fossil-bearingsediments, Montana. Prior to sectioning, eachspecimen was: (1) identified to genus follow-ing the classification of Sereno (1986) and Suesand Galton (1987) and (2) assigned a relativeontogenetic stage (juvenile, subadult, adult)according to their phylogenetic relationships,total length and inflation of the frontoparietal,and sutural morphology. Using these results,


TABLE 1. Prior to histological sectioning, each of the seven pachycephalosaurid frontoparietal domes was identifiedto genus. Their phylogenetic relationships, comparative dome thickness, and length of the frontoparietal (fp) wereused to support their relative age assignment from youngest (top) to oldest (bottom). Cranial histological charactersprovided additional criteria after sectioning that indicated UCMP 134979 was ‘‘older’’ than MOR 1179, despite hav-ing a significantly less inflated and smaller frontoparietal dome.

Specimen no. Taxon Age

Dome thickness fromroof of the braincase to

apex of the fp dome(mm)

Length offp dome

(mm)

UCMP 130049MOR 295UCMP 134979MOR 1179UCMP 128383MOR 453VRD 13

Stegoceras sp.Stegoceras validumPachycephalosauridae indet.Stegoceras validumStygimoloch spiniferPachycephalosauridae indet.Pachycephalosaurus

wyomingensis

CampanianCampanianMaastrichtianCampanianMaastrichtianLatest CampanianMaastrichtian

18.631.423.543.456.2

104.0138.0

youngest

.

oldest

61.065.0 est.52.580.6

135.0 est.180.0267.0

we placed the specimens in a presumed on-togenetic sequence from youngest to oldest(Table 1).

The degree of sutural fusion between cra-nial elements in the skulls of dinosaurs is of-ten used as a measure of the relative age of theindividual. Timing of fusion is variableamong the Marginocephalia (Ceratopsids 1Pachycephalosaurids). For instance, the frill (5parietal and squamosal bones) and associatedcranial elements in one of the largest and pre-sumed adult Triceratops skulls (UCMP 113697)remain unfused (Forster 1996). In juvenile andsubadult pachycephalosaurid skulls, however,the degree of sutural fusion medially betweenthe paired frontals and transversely betweenthe frontals and the parietal, combined withdome size and shape, degree of closure of thesupratemporal fenestrae, and dorsal surfacetexture of the dome, appears to constitute a re-liable suite of characters for determining rel-ative age (Goodwin et al. 1998; Williamsonand Carr 2002). This is supported in the fossilrecord by the occurrence of unfused, thick,undomed frontals (Galton and Sues 1983: Fig.1C–F,G–J) and thick but uninflated parietalswith large, open supratemporal fenestrae(Goodwin 1990: Fig. 14.11, G–I; Sullivan 2003:Fig. 1C,D) in juvenile skulls of Stegoceras. Weconcur with Williamson and Carr (2002) andSullivan (2003) that these specimens, previ-ously described as Ornatotholus (Wall and Gal-ton 1979; Galton and Sues 1983) are best re-interpreted as juvenile members of Stegoceras.Low-domed frontals, some unfused along the

midline frontal suture (Goodwin 1990: Fig.14.11, A–C), also represent juveniles of Stego-ceras. In the subadult stage of frontoparietaldome development, the frontals progressfrom thick and flat to slightly inflated anddome-forming whereas the parietal remainsuninflated (Lambe 1902: Pl. XXI Figs. 1, 2;Lambe 1918: Pl. I, II; Sullivan 2003: Fig. 2D–I).The two supratemporal fenestrae begin toclose, getting smaller, sometimes asymmetri-cally. In progressively more adult pachyce-phalosaurid specimens, the paired frontalsfuse and coalesce with the increasingly inflat-ed parietal to form a dorsally round, vaultedfrontoparietal dome as the supratemporal fe-nestrae close further or entirely (Gilmore1924: Pl. I–III; Brown and Schlaikjer 1943: Pl.38). In juvenile and some subadult pachyce-phalosaurids, particularly Stegoceras and Sty-gimoloch, the frontal-parietal suture may bevisible and remain open on the dorsal surfaceof the skull (Gilmore 1924: Pl. VII, Figs. 3, 4;Sues and Galton 1987: Pl. I, Figs. 1, 2; Good-win et al. 1998: Fig. 10). Juvenile and subadultcranial records of Pachycephalosaurus are lack-ing.

UCMP 130049, a low-domed, fused fronto-parietal, is hypothesized on the basis of its in-cipient doming and large brain case relative tofrontoparietal length, to represent a juvenileStegoceras and forms the starting point in ourgrowth series. A pair of unfused frontals,MOR 295, and an equal sized but fused artic-ulated frontoparietal dome, MOR 1179, rep-resent a second and third juvenile of Stegoceras


validum, judging from their relative size, su-tural contacts, and deeply sculptured dorsalsurfaces of their domes. Three intermediate-sized domes, UCMP 134979, UCMP 128383,and MOR 453 represent a subadult stage ofontogeny. Prior to sectioning, UCMP 134979was hypothesized to represent a juvenile Pa-chycephalosaurus on the basis of its similarity tothe regular, round shape of the frontoparietaldome in some adult Pachycephalosaurus skulls.UCMP 134979 compares very well to the Pa-chycephalosaurus ‘‘morphotype’’ of CM 3180described by Gilmore (1936: p. 110). UCMP128383, on the basis of size and cranial andpostcranial morphology, represents a sub-adult Stygimoloch spinifer. MOR 453, a new tax-on from the Two Medicine Formation (seeHorner et al. 1992), is the largest frontopari-etal dome known from Campanian Age sed-iments in North America. VRD 13, the largestspecimen in our sample set, possesses diag-nostic characters consistent with Pachycephal-osaurus wyomingensis and is considered to bean adult on the basis of its relative size, a fullydeveloped frontoparietal dome, and parietos-quamosal ornamentation. This skull providesthe endpoint for the hypothesized adult con-dition.

Results and Discussion

In this study, we recognize three distinctivehistological zones, formalized as Zones I, II,and III, directly above the roof of the braincaseand continuing outward to the dorsal surfaceof the frontoparietal dome (Fig. 3). A brief de-scription of each Zone is given here, followedby examples using the sectioned frontopari-etal domes described in the previous section.

Zone I is a blend of deformed, stretched-out,and ropey-looking primary and secondary os-teons. These features are characteristic of‘‘typical’’ bone of endochondral origin. Shar-pey’s fibers occur, mainly along the roof of thebraincase. The histological features and thick-ness of Zone I remain relatively constantthroughout ontogeny, regardless of the heightof the overlying dome.

Zones II is the vascular portion of the domeand its thickness decreases during ontogeny.When Zone II is extensive, long bony struts re-veal abundant osteocyte lacunae and bundles

of radiating Sharpey’s fibers—collagen fibersoriginating in the periosteum and extendinginto peripheral lamellar bone, anchoring someform of external covering over the dome.These fibers become buried within the bonematrix as new subperiosteal bone is formed(Martin et al. 1998). Sharpey’s fibers are a mi-cron-scale constituent of the hydroxyapatitetissue of the dome, not the macroscopic hy-droxyapatite ‘‘columns’’ or ‘‘bony fibers’’ ob-served along sutural or broken surfaces (con-tra Sullivan 2003). Alternating between thebony struts are long, tubelike, radial vascularspaces that illustrate the spongy texture orig-inally described by Brown and Schlaikjer(1943: p. 145).

Zone III consists of a relatively dense,sparsely vascularized layer of bone sand-wiched between the vascular bone of Zone IIand the exterior, periosteal surface of the fron-toparietal dome. The thickness of Zone III in-creases during ontogeny. Sharpey’s fibers arevery common at the periosteal surface of thedome but are patchy, occurring as islandswithin the deeper tissues of the skull in ZonesII and III. Specific regions of Zone III are de-void of osteocyte lacunae in some specimens.

In Figure 4, five of the seven sectioned spec-imens illustrate the relative size difference be-tween the smallest (UCMP 130049; Fig. 4A)and the largest (VRD 13; Fig. 4E) specimens.UCMP 130049 (Fig. 4A), MOR 295 (Fig. 4B),and MOR 1179 (Fig. 4C) represent juveniles ofStegoceras validum. MOR 453 (Fig. 4D) andVRD 13 (Fig. 4E) represent a new full-domedtaxon and an adult Pachycephalosaurus, or al-ternatively a subadult and adult Pachycephalo-saurus, respectively.

UCMP 130049 possesses an extensive ZoneII, with only a thin veneer of bone represent-ing Zone III visible in Figures 4A and 5B. ZoneI is composed of mature primary osteons in-termixed with a small number of secondaryosteons. Zone II is extremely vascularizedwith long radially oriented canals forming avery spongy-looking bone matrix. The bonystruts between radial canals contain abundantosteocyte lacunae and occasional bundles ofSharpey’s fibers.

MOR 295 (Fig. 4B), a right frontal, and MOR1179 (Fig. 4C), a coalesced frontoparietal


FIGURE 3. This is an illustration of the three histological zones observed in the subadult domed pachycephalosaurid(MOR 453) from the Two Medicine Formation, Montana, Gen. and sp. nov. Cranial histological Zones I, II, and III,defined in this study, are shown in right lateral (A) and transverse (B) views.


FIGURE 4. Histological thin sections of five of the seven pachycephalosaurid specimens comparing their relativesizes and their cranial vascularity. A, Frontoparietal dome of a juvenile Stegoceras validum (UCMP 130049) in sagittalsection, left lateral view. B, Right unfused frontal of a juvenile Stegoceras validum (MOR 295) in sagittal section, leftmedial view. C, Frontoparietal dome of Stegoceras validum (MOR 1179) in sagittal section, left lateral view. Thefrontal-parietal (fp) suture is visible on the roof of the braincase and denoted by the arrow in A and C. D, Fron-toparietal dome of a subadult full-domed pachycephalosaurid, Gen. et sp. nov. (MOR 453) in coronal section show-ing the right half of the skull. E, Frontoparietal dome of an adult Pachycephalosaurus wyomingensis (VRD 13) in cor-onal section from ‘‘ear to ear.’’ Abbreviations: Orientation arrows denote anterior (a) and dorsal (d) for A–C; lateral(lat) and dorsal (d) for D and E. Scale bar, 5 cm.


→

FIGURE 5. Sagittal sections through the juvenile domes of Stegoceras validum illustrate the relative proportions ofZones I–III preserved. A, Posterior region of the frontal (UCMP 130049) showing a dark basal Zone I and an ex-tensive Zone II with only a thin veneer of Zone III at the dorsal surface. The frontal-parietal suture, shown by thewhite arrow, is clearly visible and bisects the basal region of Zone 1. B, Highly magnified view of Zone III, fron-

dome, represent individuals of nearly identi-cal size, histological tissue structure, and stageof ontogeny. In both specimens, Zone II tissuewithin the frontals is exceptionally vascularwith an overlying thin veneer of bone at thedorsal surface representing Zone III (Fig. 5C).In MOR 1179, Zone II of the parietal and ZoneII of the frontal both share a common spongytexture (Fig. 4C). The frontoparietal suture isclearly visible between the frontal and parie-tal, traceable from the roof of the braincase tothe dorsal surface of the dome (Fig. 4C). Theparietal portion of the dome in MOR 1179 alsopossesses a significant development of ZoneIII (see Fig. 5D). The juvenile Stegoceras fron-toparietal dome (CMN 1108) sectioned byBrown and Schlaikjer (1943: p. 129) is approx-imately the same size (length, width, andheight above the roof of the braincase) as theStegoceras dome, MOR 1179 (Fig. 4C), and re-veals an internal tissue arrangement thatmatches our Zones I–III. The coronal sectionof Brown and Schlaikjer (1943: Pl. 43, Fig. 1)shows an expansive Zone II overlain by a rel-atively thinner but identifiable Zone IIIthrough the frontoparietal.

MOR 453 is a robust, highly inflated fron-toparietal dome. The dorsal surface is smooth,a feature common in some of the largest pa-chycephalosaurid skulls (Gilmore 1936: Fig. 2;Brown and Schlaikjer 1943: Pl. 42). We thinkthis may occur late in ontogeny when the un-derlying bone becomes less sculptured as thekeratinous covering enlarges with continuedgrowth into adulthood. The dorsal surface ofsmaller domes has a contrasting sculpturedappearance produced by numerous octagonalsulci (Brown and Schlaikjer 1943: Pl. 43, Fig. 4;Williamson and Carr 2002: Fig. 10). We hy-pothesize that the sulci are scale margins. Asthe dome covering grows, these separate oc-tagonal scales join together and form a moreuniform structure with age. The sulci becomeless distinct as the bone beneath the expanded,

thicker covering is remodeled and becomessmoother.

MOR 453 reveals a reduced Zone II and arelatively thicker Zone III (see Fig. 4D). Theshape of the vascular spaces of Zone II is forthe most part less elongated compared withthe younger specimens in Fig. 4A–C and in thejuvenile Stegoceras figured by Brown andSchlaikjer (1943: Pl. 43, Fig. 1). Although post-mortem bacterial invasion obscures most ofthe tissue structure of Zone III, much of thebone is interlaced with bundles of Sharpey’sfibers. Some regions of Zone III appear to beacellular.

VRD 13 (Fig. 4E), a nearly complete adultskull of Pachycephalosaurus and the largestspecimen in our sample, is devoid of elongat-ed vascular spaces so characteristic of Zone II(Fig. 6A–D). Here, the minimal vascularitythat does exist is restricted to two very smallpockets deep within the dome (Fig. 6B), whichwe interpret to be the remaining trace of ZoneII. Zone I contains an abundance of deformedHaversian canals (Fig. 6D), and limited Shar-pey’s fibers. In several areas of Zone III, Shar-pey’s fibers are common between small vas-cular canals in a tissue complex that can be ei-ther cellular (Fig. 6C) or acellular (Fig. 7D).This combination of Sharpey’s fibers and acel-lular bone tissue is very unusual. These local‘‘islands’’ of metaplastic bone (see Haines andMohuiddin 1968) lack canaliculi in VRD 13and mature pachycephalosaurid domes. Thesetissues can theoretically be identified fromvery small samples, such as fragments in di-nosaur coprolites (Chin et al. 2003).

Prior to thin-sectioning, UCMP 128383 (Fig.7A) and UCMP 134979 (Fig. 7B), two inter-mediate-sized domes, were originally hypoth-esized to represent a subadult Stygimoloch anda juvenile Pachycephalosaurus respectively (seeTable 1). The histological profile we obtainedprovides additional data to both substantiateand challenge our original hypotheses of on-


toparietal dome (UCMP 130049) showing the interface between Zone II below the arrow and Zone III above thearrow. Note the dense accumulation of abundant Sharpey’s fibers in the darker area near the interface in the upperregion of Zone II. C, Midsection of right frontal (MOR 295) with an extensive Zone II and a very minimal Zone III.D, Midsection of parietal (MOR 1179) reveals the enhanced development of Zone III compared with A and C. Scalebar, 10 mm for A, C, D; 1 mm for B.


FIGURE 6. Selected histological thin-sections from the coronal section of Pachycephalosaurus wyomingensis (VRD 13).A, Bone tissues of Zone III near the exterior surface of the dome reveals that most vascular-rich tissue is restrictedto an area near the periosteal surface. B, A small island of vascular tissue deep within the dome is interpreted aslast remaining remnant of Zone II. C, An area deep within Zone III shows bundles of Sharpey’s fibers in a matrixof low vascularity. D, Zone I at the base of the frontoparietal dome showing the ropey texture with distorted osteons.Scale bar, 4 cm for A; 1 cm for B–D.


FIGURE 7. Histological sections from two pachycephalosaurid frontoparietal domes, UCMP 128383 in A and UCMP134979 in B, show the variable bone tissue reflecting different degrees of maturity. A, A coronal section throughthe parietal of Stygimoloch (UCMP 128383) shows a moderately developed Zone III underlain by a highly vascular-ized Zone II, indicating that this is a relatively younger, subadult. B, A sagittal section of a low domed pachyce-phalosaur frontoparietal (UCMP 134979) shows a significant reduction in Zone II with a well-developed, overlyingZone III, indicating that this is an older, more mature individual. C, Magnified region of Zone II (UCMP 134979)shows the filled-in vascular spaces (black) and struts of bone with abundant osteocyte lacunae. D, Magnified regionof Zone III (UCMP 134979) reveals a 3-D network of vessels in an acellular bone tissue. E, Cellular region of ZoneIII (UCMP 134979) with an island patch of Sharpey’s fibers (upper right corner). Scale bar, 12 mm for A and B; 1mm for C–E.


togenetic stage assignments to these two spec-imens.

UCMP 128383, the presumed subadult Sty-gimoloch, possesses a relatively thickenedZone I above the roof of the braincase, a highlyporous Zone II, and an overlying, moderatelythickened Zone III (Fig. 7A). The vascularspaces of Zone II are generally round andshortened in their radial direction. The accom-panying bony struts contain abundant osteo-cytes and Sharpey’s fibers. The bone of ZoneIII is relatively thicker than the underlyingzones and contains abundant Sharpey’s fibers,particularly near the periosteal surface. Thehistological architecture of UCMP 128383 con-firms its status as a subadult individual, andthis assignment is also supported by the pres-ervation of associated unfused vertebral neu-ral spines and immature epiphyses on the tib-ia and femur found with the partial skull(Goodwin et al. 1998).

Prior to sectioning, UCMP 134979 (Fig. 7B)was considered a potential candidate for a ju-venile Pachycephalosaurus on the basis of theoverall size and shape of the frontoparietal.Although most of Zone I is missing because ofdamage to the specimen, a small projection atthe base of the slide reveals a portion of theuppermost layers of Zone I (see Fig. 7B), al-lowing a measurement of the thickness ofZones II and III. The porous bone that is char-acteristic of Zone II is much reduced, andnearly all of the accompanying vascular spac-es are rounded or radially shortened in shape.Zone III is extensive in this frontoparietaldome and reveals a highly modified bone tis-sue, with large areas devoid of osteocytes (Fig.7D). Masses of Sharpey’s fibers (Fig. 7E), someperpendicular to one another, exist in manyregions of Zone III, particularly where osteo-cytes occur. Through high-resolution imagingof UCMP 134979, the excellent preservation ofthe microstructure reveals the vascular net-works preserved within the clear bone tissueof Zones II (Fig. 7D) and III (Fig. 7E). Overall,the histological architecture reveals a maturetissue, characteristic of an older subadult /younger adult individual. This falsifies theearlier identification of this specimen as a ju-venile Pachycephalosaurus. UCMP 134979 mostlikely represents a new low-domed pachyce-

phalosaur species from the Hell Creek For-mation, Montana.

The three small frontoparietal domes (Fig.4A–C) referable to Stegoceras possess the larg-est proportional thickness of the highly vas-cularized Zone II with only a thin veneer ofZone III overlying the frontal region. In MOR1179 (Fig. 4C) Zone III is thickest in the middleof the posterior portion of the dome formed bythe parietal. Two of the intermediate domes,MOR 453 (Fig. 4D) and UCMP 128383 (Fig.7A), possess a more extensive Zone III and areduced Zone II compared with the presumedyounger specimens of Stegoceras. Also, the vas-cular spaces of Zone II in the intermediate-sized MOR 453 and UCMP 128383 are muchless elongated than in the three smaller spec-imens of Stegoceras. The largest specimen, re-ferred to Pachycephalosaurus wyomingensis, pos-sesses a very solid robust dome composed ofbone tissues representing Zones I and III, withalmost no remaining evidence of Zone II.

Brown and Schlaikjer (1943: p. 145) notedthat the specimen they sectioned was a juve-nile, and we concur. The ‘‘radiating trabecu-lae’’ they described within the frontoparietaldome, and subsequently noted by Galton(1970, 1971) and Sues (1978) as evidence for acompression-resistant capability valuable inhead butting, is actually an expression of thegrowth mechanism that produced the domingof the pachycephalosaurid skull during ontog-eny. Francillon-Vieillot et al. (1990: p. 512) de-scribe radiating fibro-lamellar bone tissue asbeing ‘‘functionally associated with very fastdeposition of relatively modest amounts ofnew compact bone.’’ These ‘‘radiating trabec-ulae’’ are transitory growth structures and areabsent in adult pachycephalosaurs. The con-sequent reduction of vascularization in adultsnegates the dome’s utility as a heat-exchangeorgan proposed by Rigby et al. (1987), Landry(1995), and Reid (1996).

One of the more interesting discoveries re-sulting from this study is the nature of ZoneIII in adult individuals. The bone tissue ofwell-preserved individuals reveals some re-gions that are acellular adjacent to areas thatare highly cellular, and other areas wheremasses of Sharpey’s fibers are adjacent to ar-eas where none exist. In addition, there are ar-


eas where bundles of Sharpey’s fibers are per-pendicular to one another. In some individualdomes, including the juveniles, bundles ofSharpey’s fibers are bent as though the angleof attachment may have shifted duringgrowth. The unpredictability of these highlydifferentiated regions suggests that whatevertype of epidermal layer may have been at-tached to the surface of the dome, it was ex-tremely pliable, and may have changed shapedramatically during ontogeny.

Conclusion

The focus of this study is to test the previ-ously held hypotheses proposing that the pa-chycephalosaurid frontoparietal dome wasutilized either for head butting or as a heat-exchange organ. Our results dispute both hy-potheses by demonstrating that the spongy,highly vascular bone structures (or ‘‘radiatingtrabeculae’’), described by previous researchersand presented as evidence in support of theirbehavioral and functional hypotheses, arefundamentally an ephemeral ontogeneticstage of dome growth. Three histologicalzones, Zones I, II, and III, are described andmapped ontogenetically. The degree of vas-cularity within Zone II is highly variable andthe radiating structures associated with it aretransitory with growth and increasing age ofthe individual. The dense layer of Sharpey’s fi-bers on the outer margin of Zone III indicatesthat the frontoparietal dome possessed an ex-ternal covering present during the life of thesedinosaurs. Consequently, we cannot be certainof the final shape of the pachycephalosauriddome.

North American pachycephalosaurid taxaare differentiated by the relative size andshape of their frontoparietal domes and ac-companying cranial ornamentation consistingof tubercles, nodes, and horns (Maryanska1990; Williamson and Carr 2002; Sullivan2003). Their ornamented dome may haveserved as a communication system that wasprimarily visual within species, analogous tothe crests, horns, and frills of ceratopsid di-nosaurs (Sampson and Forster 2001). In themodern African bovid sister group Alcelaphi-ni-Aepycerotini, horn morphology and orien-tation are also important in species recogni-

tion (Vrba 1984). We propose that the fronto-parietal dome and accompanying cranial or-naments may also have created a uniquespecies recognition system in pachycephalo-saurids.

Did color play an additional role in visualcommunication among pachycephalosaurids?We have evidence for an external covering,however we do not know if it generated color.A diverse assortment of extant birds, includ-ing velvet asities (Eurylaimidae), cassowaries(Casuariidae), peafowls (Numididae), andtoucans (Ramphastidae), have bright integu-mental colors around the face and head for vi-sual communication (Prum et al. 1994, 1999).Colors arise from the scattering of light by col-lagen fibers. These tissues have substantial re-flection in the near-ultraviolet spectrum visi-ble to birds but not to humans, suggestingtheir role in avian communication. Followingthese lines of evidence, it is reasonable to con-sider that the external covering over the fron-toparietal dome in pachycephalosaurs mayhave also been brightly colored, or subject tocolor change seasonally.

Sexual dimorphism in pachycephalosauridsis not easily tested. Associated skeletons arerelatively rare (Maryanska 1990). Pachyce-phalosaurid cranial characters are extremelyvariable (Williamson and Carr 2002; Sullivan2003). Chapman et al.’s (1981) morphometricanalysis of the cranium of Stegoceras recog-nized two distinct phenons as males and fe-males. We can now demonstrate that theirsample was composed primarily of juvenilesand subadults. As a consequence, their genderassignment of males to individuals with larg-er and thicker domes is not supported. Wepropose that cranial display in support of spe-cies recognition is a more parsimonious inter-pretation of the function of the pachycephal-osaurid dome. If sexual display between pa-chycephalosaurs also employed a strong vi-sual component using the frontoparietaldome, these behaviors were probably second-ary, judging from the apparent late ontoge-netic development of the frontoparietal domeand absence of sexual dimorphism expressedin the group so far.

Individual variation in the morphology ofthe skull is high (Maryanska 1990; Forster and


Sereno 1997) and we show that using externalcranial morphology alone may not provideenough data to identify each of the taxa to thegeneric level. Overall, the tissue character isremarkably variable and localized particular-ly in the more mature domes. Adult skulls re-quire further study to determine all of the dif-ferent tissue types within the dome.

Aspects of cranial morphology, paired withhistological information using modern histo-logical techniques and an improved fossil re-cord, provide a more powerful assessment ofbehavioral hypotheses, ontogeny, and taxo-nomic affinity of these enigmatic and uniquedinosaurs.

Acknowledgments

We thank the numerous participants whojoined Museum of the Rockies, Montana StateUniversity, and University of California Mu-seum of Paleontology field crews over the pastsummers for finding many specimens studiedby the authors. We thank R. Hilton for inform-ing us of and making available the loan ofVRD 13. We acknowledge R. Harmon and P.Leiggi for assistance in the lab and in the field,E. Lamm for preparation of histological slides,and C. Ancell and J. Mason for fossil prepa-ration, molding, and casting. K. Carpenter, W.Clemens, and P. Galton reviewed an earlierdraft of this manuscript and provided usefulcomments. Financial support was provided byN. Myhrvold and the Hell Creek Project, theCharlotte and Walter Kohler Charitable Trust,the Museum of the Rockies, Montana StateUniversity, the University of California Mu-seum of Paleontology, Berkeley, and the De-partment of Geology, University of California,Davis. This is University of California Muse-um of Paleontology contribution 1830.

Literature CitedAlexander, R. M. 1997. Engineering a dinosaur. Pp. 414–425 in

J. O. Farlow and M. K. Brett-Surman, eds. The complete di-nosaur. Indiana University Press, Indianapolis.

Brown, B., and S. M. Schlaikjer. 1943. A study of the Troodontdinosaurs with the description of a new genus and four newspecies. Bulletin of the American Museum of Natural History82:115–150.

Carpenter, K. 1997. Agonistic behavior in pachycephalosaurs(Ornithischia: Dinosauria): a new look at head-butting behav-ior. Contributions to Geology 32:19–25.

Chapman, R. E., P. M. Galton, J. J. Sepkoski Jr., and W. P. Wall.1981. A morphometic study of the cranium of the pachyce-

phalosaurid dinosaur Stegoceras. Journal of Paleontology 55:608–618.

Chin, K., D. A. Eberth, M. H. Schweitzer, T. A. Rando, W. J. Slo-boda, and J. R. Horner. 2003. Remarkable preservation of un-digested muscle tissue within a Late Cretaceous tyranno-saurid coprolite from Alberta, Canada. Palaios 18:287–293.

Colbert, E. H. 1955. Evolution of the vertebrates. Wiley, NewYork.

de Camp, L. S. 1956. A gun for dinosaur. Galaxy Science Fiction11:5:6–49.

Forster, C. A. 1996. New information on the skull of Triceratops .Journal of Vertebrate Paleontology 16:246–258.

Forster, C. A., and P. C. Sereno. 1997. Marginocephalians. Pp.317–329 in J. O. Farlow and M. K. Brett-Surman, eds. The com-plete dinosaur. Indiana University Press, Indianapolis.

Francillon-Vieillot, H., V. de Buffrenil, J. Castanet, J. Graudie, F.J. Meunier, J. Y. Sire, L. Zylberberg, and A. de Ricqles. 1990.Microstructure and mineralization of vertebrate skeletal tis-sues. Pp. 471–548 in J. G. Carter, ed. Skeletal biomineraliza-tion: patterns, processes and evolutionary trends, Vol. 1. VanNostrand Reinhold, New York.

Galton, P. M. 1970. Pachycephalosaurids: dinosaurian batteringrams. Discovery 6:22–32.

———. 1971. A primitive dome-headed dinosaur (Ornithischia:Pachycephalosauridae) from the lower Cretaceous of Englandand the function of the dome of pachycephalosaurids. Journalof Paleontology 45:40–47.

Galton, P. M., and H.-D. Sues. 1983. New data on pachycephal-osaurid dinosaurs (Reptilia: Ornithischia) from North Amer-ica. Canadian Journal of Earth Sciences 20:462–472.

Giffin, E. B. 1989. Notes on pachycephalosaurs (Ornithischia).Journal of Paleontology 63:525–529.

Gilmore, C. W. 1924. On Troodon validus , an orthopodous dino-saur from the Belly River Cretaceous of Alberta, Canada. Uni-versity of Alberta Bulletin 1:1–43.

———. 1931. A new species of Troodont dinosaur from theLance Formation of Wyoming. Proceedings United States Na-tional Museum 79(9):1–6.

———. 1936. Remarks on the skull cap of the genus Troodon . An-nals of the Carnegie Museum 25:109–112.

Goodwin, M. B. 1990. Morphometric landmarks of pachyce-phalosaurid cranial material from the Judith River Formationof northcentral Montana. Pp. 189–201 in K. Carpenter and P.Currie, eds. Dinosaur systematics: perspectives and ap-proaches. Cambridge University Press, London.

Goodwin, M. B., E. A. Buchholtz, and R. E. Johnson. 1998. Cra-nial anatomy and diagnosis of Stygimoloch spinifer (Ornithis-chia: Pachycephalosauria) with comments on cranial displaystructures in agonistic behavior. Journal of Vertebrate Pale-ontology 18:363–375.

Haines, R. W., and A. Mohuiddin. 1968. Metaplastic bone. Jour-nal of Anatomy 103:527–538.

Horner, J. R., D. J. Varrichio, and M. B. Goodwin. 1992. Marinetransgressions and the evolution of Cretaceous dinosaurs. Na-ture 358:59–61.

Horner, J. R., and M. B. Goodwin. 1998. Did Pachycephalosaursreally head-butt? An osteohistogenic cranial analysis. Journalof Vertebrate Paleontology 18(Suppl. to No. 3):52A.

Lambe, L. M. 1902. New genera and species from the Belly Riverseries (Mid-Cretaceous). Contributions to Canadian Palaeon-tology, Geological Survey of Canada 3:25–81.

———. 1918. The Cretaceous genus Stegoceras typifying a newfamily referred provisionally to the Stegosauria. Transactionsof the Royal Society of Canada 12:23–36.

Landry, S. O. 1995. Stegoceras not a head-butter. American Zo-ologist 35:5:60A.

Martin, R. B., D. B. Burr, and N. A. Sharkey. 1998. Skeletal tissuemechanics. Springer, New York.


Maryanska, T. 1990. Pachycephalosauria. Pp. 564–577 in D. B.Weishampel, P. Dodson, and H. Osmolska, eds. The Dinosau-ria. University of California Press, Berkeley.

Maryanska, T., and H. Osmolska. 1974. Pachycephalosauria, anew suborder of ornithischian dinosaurs. Palaeontologia Po-lonica 30:45–102.

Prum, R. O., R. L. Morrison, and G. R. Ten Eyck. 1994. Structuralcolor production by constructive reflection from ordered col-lagen arrays in a bird (Philepitta castanea: Eurylaimidae). Jour-nal of Morphology 222:61–72.

Prum, R. O., R. Torres, C. Kovach, S. Williamson, and S. M.Goodman. 1999. Coherent light scattering by nanostructuredcollagen arrays in the caruncles of the Malagasy asities (Eu-rylaimidae: Aves). Journal of Experimental Biology 202:3507–3522.

Reid, R. E. H. 1996. Bone histology of the Cleveland-Lloyd di-nosaurs and of dinosaurs in general, Part I. Introduction: in-troduction to bone tissues. In B. J. Kowallis and K. Seely, eds.Brigham Young University Geology Studies 41:25–72. Provo,Utah.

Rigby, J. K., Jr., A. Rice, and P. J. Currie. 1987. Dinosaur ther-moregulatory Cretaceous/Tertiary survival strategies. Geo-logical Society of America Abstracts with Programs 19(7):820.

Sampson, S. D., and C. Forster. 2001. Parallel evolution in had-rosaurid and ceratopsid dinosaurs. Journal of Vertebrate Pa-leontology 21(Suppl. to No. 3):96A.

Sereno, P. C. 1986. Phylogeny of the bird-hipped dinosaurs (Or-der Ornithischia). National Geographic Research 2:234–256.

Sues, H.-D. 1978. Functional morphology of the dome in pachy-cephalosaurid dinosaurs. Neues Jahrbuch fur Geologie undPalaontologie, Monatsheft 1978:459–472.

———. 1997. Pachycephalosauria. Pp. 511–513 in P. J. Currie andK. Padian, eds. Encyclopedia of dinosaurs. Academic Press,San Diego.

Sues, H.-D., and P. M. Galton. 1987. Anatomy and classificationof the North American Pachycephalosauria (Dinosauria: Or-nithischia). Palaeontographica, Abteilung A 198:1–40.

Sullivan, R. M. 2000. Prenocephale edmontonensis (Brown andSchlaikjer) new comb. and P. brevis (Lambe) new comb. (Di-nosauria: Ornithischia: Pachycephalosauria) from the UpperCretaceous of North America. New Mexico Museum of Nat-ural History and Science Bulletin 17:105–108.

———. 2003. Revision of the dinosaur Stegoceras Lambe (Orni-thischia, Pachycephalosauridae). Journal of Vertebrate Pale-ontology 23:181–207.

Vrba, E. S. 1984. Evolutionary pattern and process in the sister-group Alcelaphini-Aepycerotini (Mammalia: Bovidae). Pp.62–79 in N. Eldredge and S. M. Stanley, eds. Living fossils.Springer, New York.

Wall, W. P., and P. M. Galton. 1979. Notes on pachycephalosauriddinosaurs (Reptilia: Ornithischia) from North America, withcomments on their status as ornithopods. Canadian Journalof Earth Sciences 16:1176–1186.

Williamson, T. E., and T. D. Carr. 2002. A new genus of derivedpachycephalosaurian from western North America. Journal ofVertebrate Paleontology 22:779–801.