Norell ey al, 2001

P U B L I S H E D B Y T H E A M E R I C A N M U S E U M O F N AT U R A L H I S T O RY

CENTRAL PARK WEST AT 79TH STREET, NEW YORK, NY 10024

Number 3315, 17 pp., 10 figures January 30, 2001

An Embryonic Oviraptorid (Dinosauria: Theropoda)from the Upper Cretaceous of Mongolia

MARK A. NORELL,1 JAMES M. CLARK,2 AND LUIS M. CHIAPPE3

ABSTRACT

An embryonic oviraptorid skeleton is described within an egg from the Late CretaceousDjadokha Formation of Ukhaa Tolgod, Mongolia. The specimen comprises the ventral part ofthe skull and most of the mandible, a poorly preserved axial skeleton missing most of the tail,and portions of the forelimbs, shoulder girdles, pelvis, and hindlimbs. The skull is readilyreferable to the theropod dinosaur clade Oviraptoridae on the basis of several skull speciali-zations (edentulous, vertically oriented premaxilla, a sinusoidally shaped lower jaw, and anunusual articulation of the vomer and premaxilla), and the postcranial skeleton is consistentwith this identification. The egg is equivalent in overall shape and microstructure to thosefound beneath several oviraptorid skeletons recovered from the same formation. The skeletonis well ossified and, in comparison with ossification patterns in living Aves, the evidencesuggests that this species was closer to the precocial end of the precocial-altricial spectrum ofdevelopmental patterns.

1 Chairman, Division of Paleontology, American Museum of Natural History.2 Research Associate, Division of Paleontology, American Museum of Natural History. Ronald S. Weintraub As-

sociate Professor, Department of Biological Sciences, George Washington University, Washington D.C. 20052.3 Associate Curator and Chairman, Department of Vertebrate Paleontology, Natural History Museum of Los Angeles

County, 900 Exposition Boulevard, Los Angeles, CA 90007. Research Associate, Division of Paleontology, AmericanMuseum of Natural History.

2 NO. 3315AMERICAN MUSEUM NOVITATES

INTRODUCTION

In July of 1993, during the third year of ajoint paleontological project between theAmerican Museum of Natural History andthe Mongolian Academy of Sciences (No-vacek, et al., 1994), a field party discoveredan embryonic dinosaur. The embryo (IGM100/971) (figs. 1, 3, 4) was found at Xanadu(Norell, 1997a), a sublocality of the exceed-ingly rich Ukhaa Tolgod locality (Dashzeveget al.,1995, Norell, 1997b, Loope et al.,1998) in south-central Mongolia (fig. 2).

Norell et al. (1994) presented a prelimi-nary description of the embryo. Circum-stances surrounding its discovery were fur-ther commented on by Clark (1995) and No-rell and Clark (1997). In short, the embryowas found in an eroded nest of several eggslying in a circular pattern, as is typical ofother oviraptorid clutches (Brown andSchlaikjer, 1940; Sabath, 1991; Mikhailov etal., 1994; Clark et al., 1999). One side of theegg had completely eroded away, exposingmany of the bones, and the egg was brokeninto three pieces. The largest egg portioncontains most of the preserved skeleton (fig.3); a few tarsal elements were found in asmaller fragment (fig. 4), while a third piececontains no osseous material. Associatedwith the embryo were the remains of twosmall theropod skulls (Norell et al., 1994).Eggshell samples were sectioned and exam-ined using a variety of histological tech-niques (Norell et al., 1994; Bray et al., sub-mitted).

The specimen can be assigned to the Ovi-raptoridae based on several features. As inoviraptorids, some basal avialans,4 and dro-maeosaurids, the foot has a fully developedthird metatarsal that is not ‘‘pinched’’ prox-imally. A complete furcula is present in thepectoral girdle, and it is robust as in ovirap-torids (Barsbold, 1981, 1983; Clark et al.,1999), unlike the more slender condition inVelociraptor (Norell et al., 1997; Norell andMakovicky, 1999). The unique skull of ovi-

4 The term avialan (Avialae) is used throughout forthe group including all of the descendants of the lastcommon ancestor of Archaeopteryx lithographica andmodern Aves. Aves is used for the crown group com-posed of all of the descendants of the last common an-cestor of the extant diversity.

raptorids provides the definitive evidence forreferral of IGM 100/971 to the Oviraptori-dae. Although poorly preserved, the skullmaxillae and mandibles are edentulous, thepremaxilla is oriented almost vertically, theoutline of the lower jaw forms a severe si-nusoidal wave, and the vomer forms an un-usual articulation with the premaxilla on theroof of the mouth. All of these characters arepresent only in the Oviraptoridae (Barsbold,1981, 1983; Barsbold et al., 1990; Clark etal., submitted).

Unlike eggs containing theropod embryosfrom China (Manning et al., 1997; Currie,1996), IGM 100/971 is completely filledwith sediment that is identical to the matrixsurrounding the egg. This implies that theegg was cracked and infilled before lithifi-cation of the surrounding sediments. Pres-ence of a double layer of eggshell (fig. 5)also suggests that the egg was broken andthat some of its shell rearranged not long af-ter burial and before the surrounding matrixfixed the elements in place. Dong and Currie(1993) suggested that such breakage is a crit-ical element in the preservation of embryos,because it allows the egg contents to run outof the egg before enzymatic activity associ-ated with decomposition destroys the fragileembryonic bones. However, the apparentlyunbroken eggs from China containing a widevariety of taxa seem to contradict this, atleast for specimens at one locality (Manninget al., 1997; Currie, 1996). In the case ofIGM 100/971, the fact that the skeletal ele-ments are preserved in exquisite articulationindicates that the egg was filled in with ma-trix prior to decomposition of the connectivetissue holding these articulations together.

The implications of this specimen as com-pared to other Cretaceous eggs from CentralAsia was immediately apparent (Norell et al.,1994; Clark, 1995; Norell and Clark, 1997).The shell is identical in both ultrastructureand microstructure to many eggs found atother Mongolian and Chinese localities (No-rell et al., 1994; Bray et al., submitted). No-table are those found associated with the typespecimen of Oviraptor philoceratops at theFlaming Cliffs by American Museum CentralAsiatic Expeditions in 1923 (Andrews,1932). Soon after their discovery, these eggswere assigned to the ubiquitous Protocera-

2001 3NORELL ET AL.: OVIRAPTORID EMBRYO

Fig. 1. IGM 100/971 showing the exterior of the egg.

Fig. 2. The Ukhaa Tolgod Xanadu site looking east. The site of the IGM 100/971 find is indicatedwith an arrow.


tops andrewsi (Osborn, 1924). Oviraptorphiloceratops, as its name implies, was in-terpreted as dying in the act of predating onthe nest. However, it is fair to point out thatOsborn (1924:7) cautioned that the name heproposed for the specimen ‘‘may entirelymislead us as to its feeding habits and belieits character’’.

Through the years, the interpretation ofOviraptor philoceratops as egg eater andProtoceratops andrewsi as nest builder hasbeen challenged by a few authors. Sabath(1991) and Mikhailov (1991) suggested the-ropod affinities based on eggshell histology.Nevertheless the familiar image of Protocer-atops andrewsi standing near a nest of eggsis a common one in both the popular andscientific literature and is even captured inmuseum displays (fig. 6). The find of an ovi-raptorid embryo inside a ‘‘Protoceratops’’egg modified this interpretation (Clark, 1995;Norell and Clark, 1997). Subsequent reports(Norell et al., 1995; Dong and Currie, 1996;Clark et al., 1999) of oviraptorids sitting onnests in brooding positions have enhancedthis view and allowed reinterpretation of theOviraptor philoceratops type specimen as aprobable parent directly associated with thenest.

GENERAL DESCRIPTION

The embryo lies within the egg in a fetalposition (fig. 3), with the head tucked for-ward next to the knees, as in crocodiles(Reese, 1915). This differs from the condi-tion in modern birds where the head istucked back beneath the arm (see Elzanows-ki, 1981). Little disarticulation of the ele-ments has occurred. The head is located nearthe short axis of the egg, with its mandiblesappressed against the shell. The cervical andthoracic vertebrae generally follow the arcdefined by the egg apex, and the arms andshoulder girdle lie just below the head. Thepelvis lies on the opposite side of the eggfrom the snout, and the hind leg is flexedwith the knee lying just below the chin ofthe animal. The foot is also flexed and liesparallel to the long axis of the tibia. No cau-dal vertebral elements are preserved in thespecimen; consequently the orientation of thetail cannot be ascertained.

Unfortunately much of the skeleton hasbeen lost to weathering. The following ele-ments are preserved:

● Egg fragment 1 (fig. 3) is the largestfragment, containing most of the preservedskeletal elements.

● Egg fragment 2 (fig. 4) is a small frag-ment from the caudal pole of the egg. Thisfragment contains a few tarsal bones.

● Egg fragment 3 is a piece of shell devoidof any osseous elements.

Numerous fragments were found near theembryo, and are likely from the same nest,but cannot be associated specifically with theembryo.

DESCRIPTION

SKULL

The skull is extremely fragmentary due toerosion of the dorsal elements, with only thedorsal surface of the palate, quadrates, pre-maxillae, and braincase floor exposed (fig.7). The preserved elements are extremelywell ossified, but many sutures are poorly de-fined.

The premaxillae are paired and form abeak with sharp edges at the end of the skull(fig. 8). The surface of this beak is rugose,suggesting that a horny covering may havebeen present. The anterior or nasal process isa small ridge of bone that is oriented nearlyperpendicular to the horizontal axis of theskull. Just posterior to the base of the nasalprocess, is a small fossa. On the right pre-maxilla, the external narial opening is notpreserved. The left premaxilla preservesmuch of the narial border except dorsally.The narial opening was elliptical with a sub-vertical, slightly posterodorsally inclininglong axis. Inside the oral cavity, the premax-illae meet at the midline, forming an exten-sive and complete secondary palate with themaxilla.

The dorsal surface of the palatal rami ofthe premaxillae is poorly preserved. Poste-riorly, the paired maxillae meet the premax-illae in a transverse suture. A thin premax-illary process contacts the premaxilla alongthe midline. Posteriorly, the maxilla bordersthe large choana. The palatal surface forms


Fig. 3. Egg fragment 1—the main part of the IGM 100/971. Abbreviations are given in appendix 1.


Fig. 4. Egg fragment 2—the right pes of IGM 100/971. Abbreviations are given in appendix 1.

gentle longitudinal ridges on each side of themidline. Posteriorly, along the midline at theintermaxillary suture is the contact surfacefor the vomer, which is unpreserved. In ovi-raptorids, this articulation is a complex one,where the vomer interdigitates with the max-illa via a large median process and pairedlateral processes that are splayed diagonallyin an anterolateral orientation. On the ventralsurface of the skull it is this unusual articu-lation that contributes to the large ‘‘bumps’’on the palate that have been confused withteeth (Paul, 1988: 376), but are actually ven-tromedial processes of the maxillae that liebetween the lateral process of the vomer andits median articulation with the maxilla.

Dorsal to the palatal process of the maxillais the ascending or narial process of thisbone. Only the internal surface of the narialprocess can be observed, and the left is betterpreserved than the right. The ventral and an-terior border of the antorbital fenestra is pre-sent on the left maxilla. Just ventromedial tothe antorbital fenestra on the right side is ashallow fossa that may enclose the maxillarypneumatic sinus. Posteriorly, the maxillarycontact with the jugal is not preserved, andboth jugals are absent.

The left palatine is poorly preserved, and

only its medial ascending process is present.It is attached to a small plate of bone thatrepresents the palatine surface. Anteriorly, itis covered by a fragment of maxilla. Poste-riorly, it contacts the pterygoid and ectopter-ygoid.

Just medial to the posterior edge of thepalatine is a small vertically oriented lacrimalfragment where it forms the preorbital bar. Itlies at the posterior apex of the choana, justlateral to the vomerine process of the leftpterygoid.

The left ectopterygoid can be observed indorsal view. It is hook-shaped and forms theanterior and anteromedial boundary of thetiny subtemporal fenestra. Anterolaterally,the ectopterygoid forms a triple junction withthe palatine and the maxilla. In this region,just anterior to the dorsal apex of the jugalprocess of the ectopterygoid, lies a tiny pal-atal fenestra. The jugal process broadensslightly where it would contact the unpres-erved jugal. Posteriorly, the ectopterygoidbroadens where it overlies the pterygoid.Posteromedially, the pterygoid process of theectopterygoid overlaps the pterygoid, con-tributing to the pterygoid flange.

Both pterygoids are preserved in articula-tion with the braincase and the quadrates.


Fig. 4. Continued.

Fig. 5. Egg fragment 1 showing the double layer of eggshell caused by postmortem crushing.

The pterygoids converge anteriorly, nearlymeeting at their vomerine processes, and de-limit a narrow interpterygoid vacuity. Thepterygoid is broad anteriorly, posterior to thevomerine process, and narrows just anteriorto the basipterygoid articulation. The ptery-goid flange is small. Just anterior to the smallbasipterygoid articulation, the pterygoid el-evates dorsally and with the pterygoid pro-cess of the quadrate forms a large verticalflange. This elevated area anterior to thebraincase is perforated by a large foramenexiting anteriorly. The sutural connection

with the quadrate is not apparent. However,elements of the quadratopterygoid flangecurve ventral to the braincase, defining alarge chamber between the braincase walland the flange.

As in adult oviraptorids, the quadrates aremassive, and even at this early stage of de-velopment they appear to be fused with thepterygoids. The quadrates are extremelythick anteroposteriorly. The anterior surfaceof the quadrate, just dorsal to the articularsurface, is concave. Correspondingly, theposterior surface is convex, giving the artic-ular ramus a slightly forward pointing ori-entation.

On the floor of the braincase only the ba-sisphenoid is preserved. The basioccipitalshould have survived erosion, but may havebeen separated from the skull and may beamong the unidentified quadrangular bonefragments posterior to the skull. Anteriorly,a well preserved basisphenoid rostrum liesbetween and dorsal to the pterygoids. Theparasphenoid rostrum extends anteriorly tojust beyond the level of the posterior marginof the ectopterygoid’s pterygoid process. Atthe dorsal base of the parasphenoid, the hy-pophyseal fossa is filled with matrix. Poste-rior and ventral to the braincase floor lies apair of oval articular surfaces. These repre-sent articulations with the unpreserved basi-occipital.

Both mandibles are present and in loosearticulation (the right mandible is dislocatedmedially, and the left is flattened out expos-ing its medial surface). Like the premaxillae,


Fig. 6. Although refuted by evidence, museum displays and popular accounts often show Protocer-atops andrewsi associated with oviraptorid eggs and nests. This example from the American Museumof Natural History shows two Protoceratops in the vicinity of a nest. This mount was created in 1935to highlight the findings of the first reported dinosaur nests by the museum’s Central Asiatic Expeditions.

and in contrast to the condition seen in adultoviraptorids, the dentaries are not fused atthe symphysis. The mandibular fenestra islarge. Anteriorly the mandibular fenestra iselliptical and posteriorly it is truncated by theanterodorsal-posteroventrally directed mar-gin of the surangular. As in oviraptorids gen-erally, the articular fossa is low relative tothe extremely convex, arching dorsal marginof the mandible. The toothless dentaries formthe anterior half of the mandible. The dorsalmargin is sinusoidal in lateral view and theventral surface is flat, becoming convex atthe symphysis. Inside the mouth, a broadshelf forms an anterior floor of the oral cav-ity near the midline at the symphysis.

Posteriorly, the dentary forms the anteriorapex of the mandibular fenestra. A dorsalprocess arches posteriorly to join the suran-gular dorsal to the mandibular fenestra, al-though its dorsalmost part is not preservedon the right side and it is poorly exposed onthe left side. A poorly preserved ventral pro-cess extends posteriorly to contact the sur-angular at the posterior end of the mandib-ular fenestra. The lateral surface of the bone

is crenulated in the symphyseal area, sug-gesting the presence of a horny beak sur-rounding the mouth.

In oviraptorids, the surangular is a largebone that makes up an extensive part of thelateral surface of the mandible. The suran-gular rises to a peak on the dorsal surface ofthe mandible just posterior to the level of theposterior end of the mandibular fenestra. Themedial surface of the surangular is concave.The suture between the surangular and thearticular is indistinct. The posterolateral sur-face of the mandible displays a depressionanterior to its cranial articulation that is typ-ical of adult oviraptorids.

VERTEBRAE

The vertebrae are poorly preservedthroughout the embryo. However, represen-tatives of all vertebral regions are present.

Only a single cervical vertebra can beidentified with certainty (fig. 9), lying justposterior to the skull. It comprises a neuralarch separated from its accompanying cen-trum. Apparently, and unlike those in adult


oviraptorids, the cervical rib was not fusedto the neural arch. Well-formed anterior andposterior zygapophyses can be seen. The re-maining cervical vertebrae and cervical ribsare only preserved as amorphous lumps ofbone.

A few fragmentary dorsal vertebrae arescattered through the egg. Those that are bestpreserved lie in the pelvic region and there-fore represent posterodorsals (fig. 10). Theneural arches are separated from the centraand are unpreserved, except as featurelessfragments lying near the rib heads. The cen-tra are medially constricted giving the cen-trum an anterodorsally concave appearance.The dorsal surfaces of the centra are ex-posed, and the entrances to deep, probablypneumatic, cavities are visible.

Behind and anterior to the right ilium is astring of three centra that may be sacrals. Thevertebrae are laterally compressed and sepa-rated from their neural arches. The sacralcentra are fused to each other. Unfortunatelyother aspects of sacral anatomy are either un-preserved or cannot be exposed.

The pole of the egg that housed the pos-teriormost part of the animal is not pre-served. A few tiny vertebrae, presumablyposterior caudals, are preserved just anteriorto the snout of the animal adjacent to thetibia (fig. 10), and one may lie in the mouth.These bones are extremely spongy, but theyshow a medial constriction and, although dif-ficult to orient, seem to possess zygapopo-physeal structures.

RIBS

Well-ossified, but fragmentary thoracicribs are preserved adjacent to correspondingvertebral segments. Although no exposed in-dividual rib is preserved in its entirety, sev-eral rib fragments from the mid-thoracic areaare visible. On these the heads are well-os-sified and the capitulum and tuberculum ofeach individual rib are widely separated.Throughout the column the ribs are proxi-mally flat, taking on a more circular cross-sectional shape distally. Just anterior to thepelvis, small but well-ossified ribs are pre-sent.

FORELIMB AND PECTORAL GIRDLE

A well-developed furcula is present (fig.9). It is small, robust, and boomerang shaped.In anterior view, it is flat and, at the apex,straplike. The clavicular rami broaden andgently curve posterodorsally. There is no in-dication of an interclavicular suture, or a cor-responding furcular apophysis, between lat-eral clavicular moieties, although in adultoviraptorids a hypocleidium is present (Clarket al., 1999).

Both scapulae are preserved, althoughonly the most extreme proximal end of theleft scapula is exposed (figs. 3, 9). The bro-ken right scapula indicates that the scapularblade is straplike and ventrally concave. Thehead of the scapula, which articulates withthe coracoid, is observed in both right andleft elements. The width of the scapula in-creases dramatically at this articulation. Pos-teriorly, the scapula contributes to a large,deep glenoid fossa. The acromion is separat-ed from the coracoid tubercle by a shallowlongitudinal groove to which the furcula at-taches. Ventral to the scapulae, between thesebones and the eggshell, are several small,poorly preserved plates of bone that may rep-resent fragments of the left coracoid. Theright coracoid is disarticulated from the scap-ula and lies perpendicular to it. It is poorlypreserved ventrally and is perforated by acentrally located coracoid foramen.

The proximal three-quarters of the righthumerus is preserved, with the lateral surfaceexposed. The ventral surface of the proximalleft humerus is exposed below an unprepar-able mass of bones (figs. 3, 9). The proximalhead of the humerus is greatly expanded rel-ative to the shaft, suggesting the develop-ment of a large internal tuberosity. The headis formed of unfinished bone. On the humeralshaft, just distal to the head, a rugose areamay represent the insertion point for the del-toid muscle. The deltopectoral crest is wellformed distally. However, it is not continu-ous with the humeral head (as in adult the-ropods), being separated from it by a shallowtrough. The medial surface of the proximalend of the left humerus is visible. The sur-face is anteroventrally concave and may haveserved as the insertion area for the pectoralismuscle.


Fig. 7. The skull of IGM 100/971 in dorsal view. The anterior right lateral surface of the skull isvisible due to oblique crushing on the palate. Abbreviations are given in appendix 1.

Fig. 8. The skull and left knee of IGM 100/971. The skull is in anterior view showing the mandibularsymphysis and the suture between the premaxillae. Abbreviations are given in appendix 1.

Only the most proximal fragments of theright radius and ulna are preserved. Theseelements are so fragmentary that they displayno recognizable morphology, and apparentlytheir proximal articular surfaces were formedof unfinished bone.

THE PELVIS AND HINDLIMB

The only preserved pelvic bones are por-tions of both ilia (fig. 10). The ilia are dis-articulated, and it is impossible to tell if theywere well-ossified to the sacral vertebral el-ements. The bones themselves are extremelythin, with smooth surfaces. The fragmentaryelements suggest that the lateral surface wasdorsoventrally high in comparison withadults ascribed to the smaller new speciesfrom Ukhaa Tolgod (Clark et al., submitted).The anterior blade of what appears to be theright ilium is preserved with its lateral side

visible. This surface is smooth and gentlyconcave and is slightly raised dorsal to theacetabulum. Just ventral to the shallow an-terior notch, the pubic peduncle is small andindistinct. However, this may be a preserva-tional artifact.

On the left ilium, the ischiac peduncleforms the posterior border of the acetabulumand posteriorly it forms the posteroventralmargin of a shallow posterior notch. A smallridge extending posteriorly is probably anearly developmental manifestation of the me-dial blade (posterior blade of Welles, 1984);the ventral surface of this ridge therefore rep-resents the channel for the caudofemoralismuscle.

The left hindlimb is nearly complete. Theonly remaining element of the right hindlimbis the tarsus preserved in egg fragment 2 (fig.4). The proximal end of the femur is weath-


Fig. 7. Continued.

Fig. 8. Continued.

ered, and the femoral heads are absent. Thisis probably accentuated by incomplete ossi-fication of the bone end. Just distal to theposition of the femoral head lies a small con-cavity, posteriorly delimited by a small ridgethat makes up the fourth trochanter. The fem-oral shaft is anteroposteriorly bowed. The an-terior surface of the distal end of the femuris hidden. Buttresses for the lateral and me-dial condyle delimit a deep and well-definedpopliteal fossa on the posterior surface. Thedistal surface is unfinished, although threedistinct protuberances can be seen. Two ofthese correspond to the medial and lateralcondyles. The third, lying posteromedial tothe lateral condyle, corresponds to the ecto-condylar tuber seen in adult oviraptorids.

The left tibia and fibula are preserved onIGM 100/971 fragment 1, except for theirdistalmost portions. The tibia is straight,shaftlike, and circular in cross section. Thesubtriangular proximal surface is unfinished.A small, but recognizable cnemial crest is

visible medially. Proximally, the fibula is ex-panded and extends the entire length of thepreserved proximal part of the tibia.

A small bone fragment lying adjacent tothe proximal end of the tarsus on IGM 100/971 fragment 2 probably represents the as-tragalus (fig. 4). Not much of this element ispreserved. However, it lies adjacent to theproximal end of the tarsus and seems to havea finished articular surface. If our interpre-tation of this element is correct, the area offragmented bone lying in a more proximalposition is the ascending process of the as-tragalus, which in life lay on the anterodistalsurface of the tibia.

The proximal portion of the right tarsus ispreserved on fragment 2 (fig. 4) and the dis-tal extremity of the left tarsus is exposed onfragment 1 (fig. 10). The right tarsus is ex-posed in anterior view, while the left tarsusis exposed in dorsal view. The three primarymetatarsal bones (MT II, III, and IV) arenearly equal in size distally. They are subov-al or nearly circular in cross section, indicat-ing that the metatarsus does not display thearctometatarsalian condition. The proximalends of the metatarsal bones are unfinishedbone. MT IV is expanded proximally. MT IIIis narrow and displays an anterolateral sur-face where it contacts MT IV just distal tothe proximal end of the tarsus. The distalmetatarsus, although heavily worn, showsthat MT III is the longest metatarsal. MT IIis very fragmentary, consisting of only asmall splint of bone lying adjacent to MT III.MT IV is more complete, although its slight-ly bulbous end is composed of unfinishedbone. The distal end of MT III is also ex-panded and composed of unfinished bone.Near the distal metatarsus are several smalllumps of indistinct bones that may representpedal phalanges at an early, but unrecogniz-able stage of development.

EGGSHELL MORPHOLOGY

The morphology and histology of the egg-shell of this specimen have been briefly de-scribed by Norell et al. (1994) and in moredetail by Bray et al. (submitted). In short, theegg is elongatoolithid and is covered withlongitudinal, or linearituberculate ridges. Inall aspects of ultra and microstructure, the


Fig. 9. Detail of the basicranium, cervical vertebra, and shoulder region of IGM 100/971. Abbre-viations are given in appendix 1.

Fig. 10. Detail of the pelvis and hind limb of IGM 100/971. Abbreviations are given in appendix 1.

egg is identical to those considered by Mik-hailov et al. (1994) to be of the ornithoidbasic type and ratite morphology of the tra-ditional egg parataxonomy, in their E1group. This is the same type of egg that isfound beneath several adult oviraptorid skel-etons (Norell et al., 1994; Clark et al., 1999),including two skeletons at Ukhaa Tolgod.

An interesting weathering phenomenonhas occurred in which the sculptured surfaceof the eggshell (fig. 1) has become reversed.In unworn eggshell, the horizontal growthlines of the egg lie parallel to the surface ofthe egg, mirroring the profile of the sculp-tural ridges and valleys. In the worn eggshellthe ‘‘original ridges have weathered belowthe level of the original valleys thus givingthe appearance of ‘ridges’ in place of theoriginal ‘valleys’ and a flattened valley tex-ture to the sites of the actual ridges’’ (Brayet al., submitted).

COMPARISONS WITH ADULT OVIRAPTORID

TAXA

Because of the extremely specialized na-ture of the oviraptorid skull, referral of IGM100/971 to this taxon can be made with con-fidence. However, because the Gobi Desertboasts an extensive oviraptorid diversity, re-ferral to any specific taxon within this familyis problematic. At least four taxa are knownto occur in Upper Cretaceous rocks of thisregion, variously ascribed to the Djadokhtaand Barun Goyot Formations (Barsbold etal., 1990), and two new species are knownfrom the Djadokhta Formation at Ukhaa Tol-god (Clark et al., submitted). However, pub-lished diagnoses for oviraptorid taxa are farfrom adequate. This problem is confoundedby the fact that little is known of changes tothe oviraptorid skeleton during ontogeny.

Many of the differences among oviraptoridskull morphologies concern the presence of


Fig. 9. Continued.

Fig. 10. Continued.

a crest along the dorsal midline of the skullin some specimens. Unfortunately, smallsample sizes hinder our understanding of thiscrest as either intraspecific (e.g., sexually di-morphic) or interspecific. In any case, a lackof a crest in any small oviraptorid specimensis suspicious, suggesting that a crest mightdevelop very late in ontogeny.

Although the dorsal region of the skull isnot preserved in IGM 100/971, the premax-illa does suggest affinities with a certaingroup of oviraptorids. In noncrested formslike Ingenia yanshinii, an unnamed smalltaxon from Ukhaa Tolgod (Clark et al., sub-mitted), and Conchoraptor, the anterior mar-gin of the premaxilla is oriented posterodor-sally, giving the snout a somewhat pointedprofile. In Oviraptor (including O. mongo-liensis) and a second unnamed large taxonfrom Ukhaa Tolgod (Clark et al., submitted),the anterior border of the premaxilla is ori-ented almost vertically, perpendicular to theplane of the ground, giving the skull a box-

like appearance. IGM 100/971 displays thelatter morphology, with a nearly vertical pre-maxilla. We therefore tentatively refer it tothe new large species from Ukhaa Tolgod.

Robust furculae are characteristic of ovi-raptorids, and their presence can be docu-mented with certainty in Oviraptor, Ingeniayanshinii, and two undescribed forms fromUkhaa Tolgod (Barsbold, 1981; Clark et al.,1999; Clark et al., submitted). A furcula isknown in several other theropod taxa (Norellet al., 1997; Makovicky and Currie, 1998,Xu et al., 1999, Burnham et al., 2000). InIGM 100/971, the furcula is dorsoventrallycompressed and nearly flat in cross section.This is in contrast to the condition seen inadult oviraptorids, where the furcula is sub-circular in cross section (Clark et al., 1999),and in this aspect resembles Archaeopteryxand other basal avialans, as well as the dro-maeosaurs Bambiraptor and Sinornithosau-rus. It differs from the more gracile furculaof Velociraptor (Norell et al., 1997).

PATTERNS OF OSSIFICATION AND DEVELOP-MENTAL STRATEGIES

The discovery of IGM 100/971 providesthe opportunity to compare patterns of ossi-fication in an embryo of a nonavialan dino-saur with those of living Aves. Perhaps mostsignificant is the high degree of ossificationof the skeleton of IGM 100/971. Althoughcomparisons with Aves are complicated bythe fact that the precise embryonic stage ofIGM 100/971 is unknown and that in someinstances its incompleteness may reflect pres-ervational instead of ontogenetic factors, theobserved degree of ossification of this fossilembryo at least falls toward the higher endof the spectrum observed for Aves very closeto parturition. Ossified and well-defined endsof bones, such as the scapula, appear not tobe present in living precocial hatchlings(Starck, 1993, 1994). In fact, most livinghatchlings remain largely cartilaginous andpoorly ossified, although it is known that theamount of ossification is greater in Aves witha precocial rather than an altricial mode ofdevelopment (Starck, 1993, 1994; Starck andRicklefs, 1998). For example, Starck (1994)calculated that the osseous mass of a preco-cial hatchling of Barred Buttonquail (Turnix


suscitator) ranges between 15.5 and 25.3%of the total skeletal tissue while that of analtricial hatchling Budgerigar (Melopsittacusundulatus) represents between 7.2 and 13.3%of the skeleton.

The high degree of ossification of IGM100/971 is particularly evident in the skull,where even sutures are generally undistin-guished (e.g., quadrate and pterygoid, sur-angular and angular). As in Aves (Hogg,1980; Starck, 1993) and other nonavialan di-nosaurs (Chiappe et al., 1998), the degree ofossification of the skull of IGM 100/971 ap-pears to be greater than that observed in thepostcranial elements, where most bones, es-pecially those from the limbs, have unfin-ished ends. Other aspects of the pattern ofossification of IGM 100/971 also agree withthat observed in extant Aves. The well-os-sified furcula of IGM 100/971 suggests thatthis element ossified early in embryogenesis,as in extant Aves (Russell and Joffe, 1985;Starck, 1994). For example, in the CommonQuail (Coturnix coturnix), the Barred But-tonquail (Turnix suscitator), and the Com-mon Kestrel (Falco sparvarius), the furculaossifies prior to most of the remaining skel-eton (Starck, 1993: figs. 15B, 16B, 17B). Theabsence of sternal plates in IGM 100/971,which are large and well-ossified in adultoviraptorids (Clark et al., 1999), may indi-cate that, as in Aves, the centers of ossifi-cation of the sternum were inactive in em-bryonic stages (Hogg, 1980). Alternatively,the sterna may have been present but not pre-served. The absence of symphysial fusionbetween the dentaries is perhaps the most ob-vious difference between the pattern of os-sification of IGM 100/971 and that of livingbirds. In the latter, the rostral ossificationcenters of the dentaries are nearly fused fromthe beginning of ossification (Jollie, 1957)and these two bones form a solid coossifiedsymphysis at hatching (Hogg, 1980).

The wide spectrum of morphological,physiological, behavioral, and locomotoryfeatures of hatchlings of extant Aves is usu-ally subdivided into four developmental cat-egories [additional subdivisions are used bysome authors; see Starck and Ricklefs(1998)]: precocial (e.g., megapods, tinamids,phasianids, anatids), semiprecocial (e.g., lar-ids, stercorariids), semialtricial (e.g., raptors,

ciconids, ardeids), and altricial (e.g., psitta-cids and passeriforms). Precocial hatchlingsare feathered, capable of finding their food,locomotorily active, and nidifugous; altricialhatchlings are naked and blind, unable to in-dependently feed, incapable of locomotion,and consequently, nidicolous. ‘‘Superpreco-ciality’’ represents the precocial extreme ofthe precocial-altricial gradient (Starck andRicklefs, 1998). Superprecocial neonates(e.g., megapods) are completely independentand in some instances are able to fly the sameday they have hatched. The semiprecocialand semialtricial developmental modes areintermediate categories of the precocial-altri-cial spectrum. Several authors (Elzanowski,1981; Geist and Jones, 1996) have attemptedto correlate the degree of ossification or thehistology of dinosaur fossil embryos withspecific developmental postnatal strategies ofextant Aves. Elzanowski (1981), for exam-ple, regarded the high degree of ossificationof certain Late Cretaceous embryos, usuallyattributed to the enantiornithine Gobipteryxminuta, as indicative of superprecociality,and proposed that this was the ancestral de-velopmental mode of Aves.

In a histological study of extant Aves andnonavialan dinosaurs, Geist and Jones (1996)argued that nonavialan dinosaurs were pre-cocial rather than altricial. Embryogeneticstudies of Aves, however, have shown thatthe relative degree of ossification is a weakindicator of developmental modes (Starck,1993; Starck and Ricklefs, 1998), therebyraising objections to these specific correla-tions. Although the degree of ossification ofprecocial hatchlings is significantly greaterthan that of altricial hatchlings, the degree ofossification of superprecocial, precocial, andsemiprecocial hatchlings differs little (Starck,1993). Furthermore, the degree of ossifica-tion of altricial embryos is comparable tothat of other embryos for the first three-quar-ters of their embryogenesis (Starck, 1993),and the specific developmental stages of fos-sil embryos are hard to evaluate.

The distribution of specific developmentalstrategies among living birds strongly sup-ports precociality, and not superprecociality,as the ancestral developmental mode of Aves(Starck, 1993; Chiappe, 1995). Most speciesof basal Aves (e.g., paleognaths, galliforms,


anseriforms) exhibit varying degrees of pre-cocial behaviors (Starck and Ricklefs, 1998).Thus, the superprecocial strategy of mega-pods and a few other galliforms must be de-rived (contra Elzanowski, 1981). Hatchlingcrocodilians are also precocial (in a broadsense, because the avian categories are in-applicable for crocodilians). Thus, Geist andJones’ (1996) conclusions are not surprisinggiven our knowledge of the developmentalstrategies and phylogenetic relationships ofliving archosaurs. Optimization of this char-acter in archosaurs clearly supports the no-tion that a certain degree of precociality wasprimitive for all nonavialan dinosaurs as wellas for basal Aves; altriciality, however, mayhave evolved independently in certain line-ages of nonavialan dinosaurs (Starck andRicklefs, 1998). The high degree of ossifi-cation of the skeleton of IGM 100/971 sup-ports the idea that oviraptors were not altri-cial, although without indicating a specificdevelopmental strategy. In particular, the os-sified state of its sacrum and tail is signifi-cant, because one of the differences betweenthe patterns of ossification of altricial Avesand those of other developmental modes isthe fact that the sacrum of the former doesnot ossify until postnatal stages. Thus, it islikely that the development of oviraptorid ne-onates was closer to the precocial than to thealtricial side of the precocial-altricial spec-trum of its extant counterparts.

ACKNOWLEDGMENTS

We thank the Mongolian Academy of Sci-ences, especially D. Baatar, A. Boldsukh, andR. Barsbold, the leader of the Mongolian sideof the expedition D. Dashzeveg, and ourmany friends whom we have worked with inMongolia over the years. In New York, wethank the members of our field crews overthe years and Dr. Richard Shepard. Amy Da-vidson prepared the specimen, Marilyn Foxskillfully cast it, and Michael Ellison illus-trated this paper. Richard, Lynette, and ByronJaffe are thanked for their generous supportthrough the years. This work is supported byNSF DEB 9407999, NSF DEB9300700, theNational Geographic Society, the EpplyFoundation, IREX, the Philip McKennaFoundation, the Frick Laboratory Endow-

ment, and the Department of Vertebrate Pa-leontology at the American Museum of Nat-ural History.

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APPENDIX 1

a? possible astragulusbo-bs basioccipital/basisphenoid

ch choanacv cervical vertebra

f furculaIGM Institute of Geology, Mongolia

lf left femurlh left humerusli left ilium

lm left maxillalmt II left metatarsal IIlmt III left metatarsal III

lmt IV left metatarsal IVlpmx right premaxilla

lpt left pterygoidlptv left pterygoid vacuity

lq left quadratelsa left surangularlsp left sacral process

lt left tibianar nares

p phalangesppm palatal process of premaxillapup pubic peduncle

r ribsrd right dentary

rect right ectopterygoidrh right humerusri right ilium

rm right maxillarmt II right metatarsal IIrmt III right metatarsal IIIrmt IV right metatarsal IV

rn right narial openingrpmx right premaxilla

rpt right pterygoidrq right quadraters right scapula

rsa right surangulars? possible sacral vertebraevc vomer contact

novi 00213 Mp 18File # 01TQ

No RH this page!!


No RH this page!!


No RH this page!!

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