Page 1

AMERICANt MUSEUM

Norntates

PUBLISHED BY THE AMERICAN MUSEUM OF NATURAL HISTORY

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

Number 3265, 36 pp., 15 figures

May 4, 1999

An Oviraptorid Skeleton from the Late Cretaceous

of Ukhaa Tolgod, Mongolia, Preserved in an

Avianlike Brooding Position Over an

Oviraptorid Nest

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

ABSTRACT

The articulated postcranial skeleton of an ovi-

raptorid dinosaur (Theropoda, Coelurosauria)

from the Late Cretaceous Djadokhta Formation

of Ukhaa Tolgod, Mongolia, is preserved over-

lying a nest. The eggs are similar in size, shape,

and ornamentationto another egg from this lo-

cality in which an oviraptorid embryo is pre-

served, suggesting that the nest is of the same

species as the adult skeleton overlying it and was

parented by the adult. The lack of a skull pre-

cludes specific identification, but in several fea-

tures thespecimen ismore similar to Oviraptor

than to other oviraptorids. The ventral part of the

thorax is exceptionally well preserved and pro-

vides evidence for other avian features that were

previously unreported in oviraptorids, including

the articulation of the first three thoracic ribs

with the costal margin of the sternum and the

presence of a single, ossified ventral segment in

each rib as well as ossified uncinate processes

associated with the thoracic ribs. Remnants of

keratinous sheathsare preserved with four of the

manal claws, and the bony and keratinous claws

were as strongly curved as the manal claws of

Archaeopteryx and the pedal claws of modern

climbing birds. The skeleton is positioned over

the center of the nest, with its limbs arranged

symmetrically on either side and itsarms spread

out around the nest perimeter. This is one of four

known oviraptorid skeletons preserved on nests

of this type of egg, comprising 23.5% of the 17

oviraptorid skeletons collected from the Dja-

dokhta Formation before 1996. The lack of dis-

turbance to the nest and skeleton indicate that the

specimen is preserved in the position in which

the adult died. Its posture is the same as that

' Research Associate, Department of Vertebrate Paleontology, American Museum of Natural History; Assistant

Professor, Department of Biological Sciences, George Washington University, Washington, D.C. 20052.

2 Chairman, Department of Vertebrate Paleontology, American Museum of Natural History.

3Chapman Fellow and Research Associate, Department of Ornithology, American Museum of Natural History.

Copyright ( American Museum of Natural History 1999

ISSN 0003-0082 / Price $3.90

AMERICAN MUSEUM NOVITATES

commonly taken only by birds among tetrapods

that brood their nest, and its close proximity to

the eggs indicates that the nest was not covered,

indicating that the behavior of sitting on open

nests in this posture evolved before the most re-

cent common ancestor of modern birds.

INTRODUCTION

Among the most surprising and revealing

specimens collected from Upper Cretaceous

Djadokhta-like beds in Mongolia by the joint

American Museum of Natural History-Mon-

golian Academy of Sciences expeditions are

those of the peculiar dinosaurs of the Ovi-

raptoridae (Norell and Clark, 1997). Unlike

the skulls of most other nonavian theropods,

the unusually short, often highly pneuma-

tized skull of oviraptorids lacks teeth and

may bear a crest, resembling superficially the

skull of the living cassowary. The abundance

of oviraptorid specimens at the extraordi-

narily rich locality of Ukhaa Tolgod (Dash-

zeveg et al., 1995) is most unexpected in

light of their rarity in other deposits (Bars-

bold et al., 1990). This wealth of new ma-

terial already has answered a 75 year old

enigma, and the specimen described here

played a crucial role in this story (Norell et

al., 1994).

The bizarre and poorly preserved holotype

specimen of Oviraptor philoceratops was

discovered at Bayn Dzak (the "Flaming

Cliffs") by the American Museum's Central

Asiatic Expedition in 1923, fortuitously en-

countered while excavating the first dinosaur

nest found at this famous locality (Andrews,

1932). Because eggs similar to those in this

nest are abundant at Bayn Dzak, and because

of the preponderance of skeletal material of

Protoceratops andrewsi at this locality, the

eggs were identified as belonging to Proto-

ceratops (Osborn, 1924). The skeleton over-

lying the nest therefore presented an enigma.

To explain this association, Henry Fairfield

Osborn (Osborn, 1924) speculated that the

adult animal had been preserved while rob-

bing the nest (although there wasno evi-

dence to indicate predation), hence he en-

dowed it with a name meaning "egg seizer

fond of ceratopsians."

For many years the identity of the eggs as

those of Protoceratops was accepted with little

doubt. In recent years this identification was

questioned (Sabath, 1991; Mikhailov, 1991),

but only circumstantial evidence for reiden-

tifying the eggs was forwarded. The discov-

ery of Ukhaa Tolgod in 1993 provided the

evidence crucial to deducing a definitive an-

swer-an oviraptorid embryo within the

same type of egg as those beneath the Ovi-

raptor philoceratops holotype (Norell et al.,

1994). With this reidentification of the eggs

the association of the skeleton with eggs of

its own kind became explicable as evidence

of parental care, rather than predation.

The specimen described here, IGM 100/

979 (mistakenly labeled 100/972 in fig. 1 of

Norell et al., 1995), provides further evi-

dence that this association is indeed a result

of parental behavior. The specimen (fig. 1)

was discovered in 1993, and after its prepa-

ration a preliminary note was published (No-

rell et al., 1995). A second specimen on a

nest was collected from Ukhaa Tolgod in

1995 (see Webster, 1996), and another from

correlative beds at Bayan Mandahu in Inner

Mongolia, China, was reported by Dong and

Currie (1996). These three specimens and the

0. philoceratops holotype provide compel-

ling evidence that the close association be-

tween adults and nests in Oviraptoridae has

a biological explanation.

The specimen is remarkably intact, and in

addition to its importance in preserving this

individual's relationship to the nest it pro-

vides important new data on the thoracic

skeleton in oviraptorids. Many of these fea-

tures were revealed by preparation following

publication of the preliminary note, and thus

were not reported or illustrated there. Ovi-

raptorids are among the closest relatives of

Avialae, the group comprising Archaeopter-

yx, extant birds, and related taxa (Aves of

some other authors: see Gauthier, 1986), and

these new features help determine the precise

relationships of oviraptorids among Thero-

poda and the homology of these features.

Institutional abbreviations: AMNH-

American Museum of Natural History, New

York; IGM-Mongolian Institute of Geolo-

2

NO. 3265

1999~CLARK ET AL.: NESTING OVIRAPTORID FROM MONGOLIA3

gy, Ulaan Baatar; IVPP-Institute of Verte-

brate Paleontology and Paleoanthropology,

Beijing; MIAE-field numbers ofthe collec-

tions made by the Mongolian Academy of

Sciences-American Museum of Natural His-

tory expeditions to the Gobi Desert.

GEOLOGIC SETTING OF THE FIND

The specimen is from a thick-bedded

sandstone in the lower part of the local sec-

tion at the Ankylosaur Flats sublocality,

Ukhaa Tolgod. These sediments and the fau-

na they entomb closely resemble sediments

and assemblages at localities in the Djadokh-

ta Formation, such as Bayn Dzak and Bayan

Mandahu, but some similarities with the fau-

na of the Barun Goyot Formation have also

been noted (Dashzeveg et al., 1995; Gao and

Norell, 1996). Currently the stratigraphic re-

lationships of this locality relative to other

localities, especially the type section of the

Barun Goyot Formation, are unclear and un-

der study (L. Dingus et al., in prep.).

At Ukhaa Tolgod, the specimen was col-

lected from a unit with a lithology that has

been described elsewhere as a "structureless

sandstone" and interpreted as eolian in origin

(e.g., Eberth, 1993). In the Djadokhta For-

mation at Ukhaa Tolgod this facies initially

was interpreted as eolian in origin (Dashzev-

eg et al., 1995). Recently, Loope et al. (1998)

reinterpreted these deposits as representing

low-energy debris flows from eolian deposits

that formed thick alluvial fans. The source of

these deposits was an extensive field of sta-

bilized sand dunes that destabilized when in-

undated with water during large rainstorms.

They interpreted the ancient Ukhaa Tolgod

environment as dominated by large, stabi-

lized sand dunes separated by interdunal en-

vironments such as small, ephemeral ponds.

Loope et al. (1998) suggested that sand

flowed at relatively low energy from the

dunes into the interdunal zone following

large rainstorms. The low-energy flows cov-

ered dead, or dying, animals and may have

entombed smaller animals in burrows. Low-

energy depositional conditions may therefore

be responsible for the excellent preservation

of the Ukhaa Tolgod fossils, including IGM

100/979.

As with many of the specimens from

Ukhaa Tolgod, traces of burrowing inverte-

brates are preserved with the skeleton. They

are recognizable mainly because they are

more strongly cemented than the surrounding

matrix and are lighter in color. Five burrows

were exposed during preparation, including a

long burrow on the dorsal surface of the ster-

nal plates (fig. 2). These burrows are filled

with white particles which may be pieces of

digested bone, and two in the shoulder region

are nearly white. Four of the five are slightly

curved, but the smallest one is straight. One

is preserved above the right coracoid, one to

the left of the fourth digit of the left pes, and

another between the right ischium and right

pes, and one was removed from above a right

ventral rib just behind the right sternal plate.

Most are similar in shape, ranging from 3-4

cm in length and 4-8 mm in diameter, but

the one above the sternum is over 6 cm long

(fig. 2). Although other evidence of contem-

poraneous fossil arthropods at Ukhaa Tolgod

(Loope et al., 1998) and other Djadokhta lo-

calities (see Johnston et al., 1996) may be

from the taxon responsible for the burrows,

it is also possible that burrows associated

with IGM 100/979 were formed significantly

after deposition of the bed in which it is bur-

ied.

The age of the Djadokhta Formation at

Ukhaa Tolgod and elsewhere in Mongolia

and China currently is not constrained by ra-

diometric dates, marine invertebrates, or pa-

leomagnetic polarity patterns. Comparisons

of the vertebrates suggest a correlation with

the late Campanian to early Maastrichtian

marine invertebrate stages (Lillegraven and

McKenna, 1986; Jerzykiewicz and Russell,

1991). However, the Darabasa Formation of

Kazakhstan has a mammalian fauna similar

to that of the Djadokhta Formation and is

interbedded with Early Campanian marine

invertebrates (Averianov, 1997).

DESCRIPTION

THE SKELETON

The skeleton (fig. 1) is incompletely ex-

posed, as further preparation would compro-

mise the integrity of the specimen or endan-

ger bones by removing their support. Miss-

ing are nearly the entire vertebral column,

the skull, and the ilia and left femur. The

1999

3

AMERICAN MUSEUM NOVITATES

Fig. 1. IGM 100/979, in dorsal view. See Appendix for abbreviations.

exposed portions comprise a complete right

forelimb; a partial left forelimb including the

proximal end of the humerus, the distal ends

of the radius and ulna, and all the bones of

the manus; the nearly complete furcula; the

ventral portion of both scapulae fused with

the coracoids; the left and right sternal plates;

what appears to be the ventral part of a ver-

tebral centrum in the shoulder region; the

distal ends of the ischia and pubes; the distal

end of the right femur and the proximal half

of the tibia and fibula in articulation; the

right pes distalto the middle of the metatar-

sals (the second and third digits are not ex-

posed); the left fibula, tarsus, and pes in ar-

ticulation, and what may be a fragment of

the proximal end of the tibia; and a series of

gastralia and the distal ends of seven pairs of

ribs. Most of the bones are uncrushed except

the right radius, ulna, femur, and tibia. Rem-

nants of the keratinous claws of the manus

are preserved on the ends of the second and

third unguals on the right side and the first

and third ungual on the left side.

PECTORAL GIRDLE AND FORELIMB: The fur-

cula (fig. 3) is missing the distal half of its

left side and a small part of the distal tip of

its right side, which is otherwise preserved

in articulation with the right scapula. It is

completely fused, with no indication of a su-

ture between the two clavicles. It is a robust

bone that curves posterodorsally at its distal

end (as preserved on the right side). The bro-

ken edge of the left side of the bone reveals

4

NO. 3265

CLARK ET AL.: NESTING OVIRAPTORID FROM MONGOLIA

Imd

Imd 1I

Imd III

rmd I

rmd 11

Fig. l.-Continued.

no indications of a pneumatic space within

it, as is found in the furcula of many birds.

The distal end flattens where it articulates

with a distinct shelf on the anterior edge of

the scapula. An unusually long, dorsoven-

trally flat hypocleidium extendsposteroven-

trally from the midline of the furcula, direct-

ly toward the sternum (fig. 3). It is nearly

half as long as is each half of the furcula. It

tapers distally from a broad base, and is

about twice as long as the base is wide.

Remnants of the scapulae are poorly pre-

served. A well-developed shelf is preserved

on the anterior edge of both elements dorsal

to the glenoid fossa, andthe furcula articu-

lates with this shelf on the right side. The

shelf is nearly horizontal and dorsally con-

cave, with a well-developed semicircular rim

anteriorly.

The right coracoid is partly exposed and

the left is almost completely exposed in me-

dial view. The exposed portion is similar in

size and shape to that of other oviraptorosau-

rians (Barsbold et al., 1990), which is more

elongate ventrally than in basal theropods,

forming a quadrangular shape in medial and

lateral views. The articulation with the ster-

num is exposed only on the left side, where

the coracoid has been displaced slightly an-

terodorsally. The coracoid contacts the ster-

num along the anterior edge near the midline.

The humerus (fig. 4) has a well developed

1999

5

AMERICAN MUSEUM NOVITATES

X,.

Fig. 2. IGM 100/979, invertebrate trace on

the dorsal surface of the sternal plates. Anterior

end of skeleton toward top.

deltoid crest, extending nearly the proximal

third of the bone. Opposite the deltoid crest,

near the medial edge of the humerus, is a low

prominence, the ventral (internal) tuberosity.

Only the anterior surface of the distal end is

exposed.

The shaft of the only complete ulna, the

right, is apparently broken and healed, as in-

dicated by an expanded area two-thirds of the

way down the shaft with a rugose surface. A

deep longitudinal groove medial to the ru-

gose area may also be due to this injury, but

could also be accentuated by crushing. The

ulna is relatively straight with no evidence of

bowing, and there is no evidence of quill

knobs. The olecranon process is only weakly

developed, and the proximal end is not as

robust as in an undescribed oviraptorid skel-

eton from Ukhaa Tolgod, IGM 100/1002.

The distal end is expanded into a well-

formed, convexly rounded end. The radius is

slightly more slender than the ulna, and

shows no evidence of injury. The ends of the

radius are not well exposed, but the distal

third has a slight dorsal bend to the shaft.

The carpals are poorly exposed (fig. 4).

The large distal ("semilunate") carpal is sep-

arated slightly from the proximal ends of the

metacarpals, and could not have been fused

to them. The left element appearsto have

rotated somewhat out of position. A second,

smaller carpal is preserved laterally, opposite

the proximal end of the third metacarpal. It

is triangular in shape, with a proximal apex.

There is no evidence of proximal carpals, but

this area is not completely exposed on either

side.

The manus comprises only three digits

(figs. 5, 6), homologous with 1-111 in com-

parison with other Theropoda. The first meta-

carpal is relatively robust and is approxi-

mately one-third the length of the second and

third. The second and third parallel one an-

other, the third being more slender than the

second. The lateral edge of the first metacar-

pal is in contact with the medial surface of

the second, but as preserved on both sides

the third articulates on the ventrolateral, rath-

er than lateral, edge of the proximal end of

the second. The proximal end of the third

metacarpal is well developed rather than be-

ing reduced as in some oviraptorids (such as

Ingenia).

The digital formula of the manus is 2-3-4-

X-X. The firstdigit is about two-thirds the

length of digits II and III (including meta-

carpals), which are equal in length. The prox-

imal phalanx of the first digit is long and

robust, similar in length to, but more robust

than, metacarpals II and III. The proximal

and medial phalanges of the seconddigit are

also elongate, each being approximately two-

thirds the length of the proximalphalanx of

digit I. The proximal two phalanges of the

third digit are smaller, each being approxi-

NO. 3265

CLARK ET AL.: NESTING OVIRAPTORID FROM MONGOLIA

Fig. 3. IGM 100/979, furcula in anterodorsal view. Note the elongate, flat hypocleidium (hc).

mately one third the length of the proximal

phalanx of digit I. The penultimate phalanx

of digit III is approximately 25% longer than

the proximal phalanges.

The articulations between the proximal

phalanges and the metacarpals indicate that

little rotation was possible. The surfaces are

not well rounded, and they do not extend far

beyond the minimumarea over which the

two bones contact. The articulations between

the phalanges, however, are all strongly con-

vexo-concave and extend beyond the mini-

mum area of contact, indicating a much

greater degree of anteroposterior rotation.

The manal claws are strongly curved,

deep, and laterallycompressed with well de-

veloped flexor tubercles. The proximal end

of unguals II and III has a well-developed lip

dorsal to the articular surface. The groove for

the claw sheath on each side is situated near

the ventral edge proximally and rises to the

dorsal surface distally, being symmetrically

placed on both sides. The claw of digit I is

larger than that of digit II (89 mm in greatest

length versus 77 mm), which is larger than

that of digit III (71 mm).

Remnants of the unossified, presumably

keratinous, part of the claw are preserved on

the second and third unguals on the right side

and the first and third ungual on the left side.

They indicate that the keratinous claw ex-

tended significantly beyond the end of the

bone. In all four cases the keratin is pre-

served as a thin ribbon of fibrous tissue dor-

sal to the end of the ungual, suggesting that

this region of the claw differed from others

in some way (perhaps in density or thickness

of the keratin). (A small clump of white ma-

terial beneath the ungual of left digit III near

its tip may also be from the keratinous claw.)

The longest example is on right digit II, al-

though the distal part of the keratin is sepa-

rated by a large gap from the proximal part.

The total length of the tissue,including the

1999

7

AMERICAN MUSEUM NOVITATES

rdr

rmc 3

rmt 2

rmt 3 rmt 4

Fig. 4. IGM 100/979, right fore and hindlimbs on nest in dorsal view. Note pairing of eggs. Pho-

tographed prior to preparation of sternum. See Appendix for abbreviations.

gap, is 32 mm, and it extends 23 mm beyond

the end of the bone in a direction continuous

with the curvature of the dorsal edge of the

claw.

PELVIS AND HINDLIMB: Only the distal part

of the pubes are preserved, and their distal

ends are not exposed (fig. 1). In cross section

the lateral part of each bone is subcircular,

and a thin lamina extends medially towards

the midline. The two bones are strongly su-

tured into a midline symphysis, forming a

relatively flat anterior surface. Proximally the

medial edge of each bone becomes more pos-

teriorly oriented, creating a concavity on the

anterior surface of the symphysis, and pre-

sumably a pubic apron posteriorly. The ori-

entation of the bones is similar to the posi-

tion of these bones in articulated pelves of

oviraptorids, nearly vertical but projecting

somewhat anteroventrally. The pubic bootis

not exposed and must occupy the region in

the center of the nest.

The distal end of the ischium (fig. 7) is

expanded and the two bonesform a horizon-

tal symphysis with a deeply concave dorsal

surface. The ischia are in firm contact over

the length ofthe symphysis (116 mm), and

the suture involves a complex interdigitation

of large processes and concavities in a si-

nusoidal pattern. An ischial symphysis has

not been reported in any other oviraptorid

specimen (Barsbold et al., 1990). The bone

thins dramatically distally, in the posterior

third of the symphysis, and ventrally along

the midline. The preserved portion of the is-

chia lies distal to the region an obturator pro-

cess would be expected.

The distal end of the right femur is too

8

NO. 3265

rr

CLARK ET AL.: NESTING OVIRAPTORID FROM MONGOLIA

VA

.1.~

Fig. 4.-Continued.

1999

9

AMERICAN MUSEUM NOVITATES

p 1

kc

2 cm

Fig. 5. IGM 100/979, right manus in lateral view. Note remnant of keratinous claw on digit II and

III unguals. SeeAppendix for abbreviations.

poorly preserved to offer reliable evidence of

its original condition. It is crushed dorsoven-

trally (fig. 8).

The proximal end of the right tibia is part-

ly covered by the femur, but a strong lateral

deflection proximally indicates the presence

of a lateral cnemial crest. The shaft is

crushed and exhibits few features of interest.

Both fibulae exhibit a distinct bend ap-

proximately one-third of the way down the

shaft, some (but not all) of which may be due

to post-depositional distortion. The portion

proximal to the bend expands proximally and

is mediolaterally flattened, articulating with

the lateral cnemial crest of the tibia. Distal

to the bend, the fibula becomes extremely

slender, and it extends to the tarsus to contact

the calcaneum (fig. 9).

The poorly preserved left proximal tarsals

indicate that the calcaneum is fused to the

astragalus distally but not proximally. The

ascending process of the astragalus is a broad

sheet of bone that would have covered the

entire anterior surface of the distal end of the

tibia, but it is unclear how far along the tibia

it extended proximally. The distal tarsals are

not exposed,presumably lying beneath the

proximal tarsals.

As in other Theropoda, the proximal end

of the first metatarsal is greatly reduced.

Metatarsals II-IV are similar to each other in

size, and only the proximalmost part of meta-

tarsal III narrows between II and IV, although

much less so than in, for example, Troodon-

tidae. None of the metatarsals are fused to

one another. Metatarsal III is slightly longer

than IV, which is slightly longer than II.The

articulating surfaces on the distal ends of

these metatarsals are smooth and do not

show a ginglymoid condition. They extend

anterodorsally onto the shaft, indicating the

capacity for at least limited digitigrade pos-

10

NO. 3265

CLARK ET AL.: NESTING OVIRAPTORID FROM MONGOLIA

ture. Metatarsal I articulates on the postero-

medial edge of metatarsal II three-fourths of

the way down its shaft, and is preserved in

what appears to be its natural position on

both feet. Its distal end is twisted anteriorly,

so that the toe is not reversed as it is in many

birds. The splintlike metatarsal V is exposed

on the left side, and is approximately one-

third the length of metatarsal III. It articulates

with metatarsal IV on its posterolateral edge,

and extends proximally to the same level as

metatarsals II-IV.

The digital formula of the pes is 2-3-4-5-

0. The relative lengths of the complete digits

are III>IV>II>>I. The phalanges are short

and robust with strongly curved articulation

surfaces. The unguals are broad and robust,

with very deep grooves for the keratinous

claw. The unguals are stout and only weakly

curved ventrally except that of the first toe.

AXIAL SKELETON: The only vertebra pre-

served, located between the scapulae, is too

poorly preserved to provide significant in-

formation.

The two sternal plates (fig. 10) are very

well preserved, exposed in dorsal view, and

are generally similar to those of other ovi-

raptorids with paired elements (Barsbold,

1981). They abut along the midline, without

overlapping. The right plate is slightly longer

anteriorly than the left, but otherwise the ex-

posed portions of both sides are symmetrical

across the midline. The anterior edge of each

plate is concave anterolaterally, and the cor-

acoid articulates with only a small area near

the midline. The medial edge of each plate

is straight without indentations, although an-

teriorly it is obscured by the trace fossil cov-

ering most of this region. The lateral edge is

complex but is dominated by two lateral pro-

cesses: an anteriorly placed one with a pos-

terolateral costal margin, and a blunt, poste-

riorly placed process comparable to the lat-

eral xiphoid process (or trabecula) on the

sternum of many avians.

The anterior process has a concave ante-

rior edge and a straight posterolateral edge,

forming a triangle in dorsal view. The ante-

rior edge is smooth, while the posterolateral

edge is thick, rugose, and with several ex-

pansions. The first threeventral ribs (i.e., the

ventral segments of the thoracic ribs) are pre-

served in contact with this edge on the left

plate and very close to this edge on the right,

and they undoubtedly articulated to these ir-

regularities. The fourth ventral rib terminates

far from this surface (11.5 cm from it on the

right side), and its distal end tapers to a point

rather than being expanded like the first three

ribs, strongly suggesting it did not articulate

with the costal margin of the sternum.

On the right side, which is better exposed,

the more posterior of the two lateral pro-

cesses is square, terminating in an antero-

posteriorly broad, gently rounded edge, and

it extends further laterally than the anterior

process. Its anterior edge is short and slightly

concave anteriorly, and the posterior edge is

straight and continuous medially with the

posterior edge of the plate. The posterior

edge of the plate is somewhat irregular but

is much thinner than the costal margin, and

there is no evidence for the articulation of

ribs. Near the midline the sternal plate has a

short, broad posterior process.

Only the ventral portions of the posteri-

ormost cervical rib and the first six thoracic

ribs are preserved, but they are nearly undis-

turbed and preserved in exceptional detail.

These seven ribs are folded backward ante-

rior to the pubes on the right side, which is

the basis for this description because the left

ribs are incompletely exposed (fig. 10). The

second through fourth preserved ribs articu-

late with the sternum, and because the tho-

racic series is typically defined to begin with

the first rib that articulates with the sternum

(e.g., Romer, 1956: 227) they belong to this

series. The posteriormost cervical is thinner

than the first thoracic, but is comparable in

thickness to the second thoracic.

A separate ventral (sternal) segment is pre-

sent in the first three dorsal ribs and articu-

lates ventrally with the sternum (fig. 10). The

fourth thoracic rib has a ventral segment that

does not articulate with the sternum, and it

tapers to a point ventrally. The fifth and sixth

ribs lack ventral components, and there is no

indication of an articulation surface distally

for a cartilaginous segment. All of the ventral

rib segments are well ossified, as is evident

from cancelous bone exposed within the ven-

tral end of several segments and the presence

of haversian systems (fig. 11).

The articulation surfaces between the ven-

tral and dorsal rib segments are expanded

1999

AMERICAN MUSEUM NOVITATES

NO. 3265

I'

CLARK ET AL.: NESTING OVIRAPTORID FROM MONGOLIA

with nearly flat articulation surfaces (fig. 10).

They are separated from each other by sev-

eral millimeters of matrix, suggesting the

presence of connective tissue between them.

All of the ventral rib segments are flattened

in the same directions as the corresponding

dorsal component to the rib. They are pre-

served close to one another, as a bundle, and

the ventral end of each is expanded where it

meets the sternum. The ventral segment of

the first dorsal rib is the stoutest and shortest,

and is straight. The left ribs are preserved in

articulation with the sternum (those on the

right are displaced a few centimeters poster-

omedially), and the robust ventral segment of

the first thoracic rib is the most lateral of the

three articulating on the costal margin of the

sternal plate (as inferred in Sinraptor; Currie

and Zhao, 1993). The ventral segments of the

second and third thoracic rib are progres-

sively longer and thinner and have a distinct

medial bend near the articulation with the

dorsal segment (exposed only on the right

side). The ventral segment of the fourth tho-

racic rib is much shorter and tapers to a

point, and it is preserved far from thester-

num (see above),indicating it did not artic-

ulate with it.

The fourth, fifth, and sixth thoracic ribs are

progressively shorter than those articulated

with the sternum, but because they are in-

complete proximally their actual lengths are

not known. Nevertheless, the dramatic short-

ening in these ribs and the lack of distur-

bance to the skeleton strongly suggest that

the rib cage was anteroposteriorly short in

comparison with, for example, crocodylians.

Associated with the dorsal segments of the

first four preserved ribs are four mediolater-

ally flattened uncinate processes that expand

ventrally (fig. 12). The uncinate processes

are all incomplete dorsally but their propor-

tions suggest they were at least as long as in

Velociraptor (see Norell and Makovicky, in

press). The posterior edge is straight and the

anterior edge is concave anteriorly. They are

preserved extending posterodorsally over the

lateral surface of the rib posterior to them,

Fig. 7.

IGM 100/979, ischia in dorsal view,

anterior toward the top of the figure. Note ischial

symphysis (is) and apposition of ischia and egg.

with the expanded base abutting the rib an-

terior to them.

A few segments of gastralia are partly ex-

posed near the ventral midline beneath the

ventral ribs and sternal plates and anterior to

the left pes. They continue anteriorly beneath

the sternal plates, and are easily distin-

guished from the ventral ribs by their smaller

diameter, complex articulations, and lack of

articulation with the edge of the sternum.

Four segments exposed behind the posterior

edge of the right sternal plate converge an-

teromedially and are much larger than seg-

Fig. 6. IGM 100/979, leftmanus in lateral view. Note remnant of keratinous claw (kc) on unguals

of digits I and III and strong curvature of claw.

13

1999

AMERICAN MUSEUM NOVITATES

5 cm

Fig. 8. IGM 100979, right hindlimb in dor-

solateral view. Note close proximity of fourth dig-

it and egg. See Appendix for abbreviations.

ments exposed more posteriorly. Otherwise

they are similar to those of Dromaeosauridae

(Norell and Makovicky, 1997).

THE NEST

Fifteen eggs are partially exposed beneath

the skeleton, but a similar number are esti-

mated to remain unexposed in the matrix.

The nest appears to be intact, and with a few

exceptions breakage is consistentwith com-

pression of the sediment ratherthan preburial

disturbance because there is little displace-

ment of the fragments. All of the exposed

eggs are horizontal or subhorizontal, aligned

radially within the nest, and, as exposed be-

neath the right arm, arranged in at least two

layers. The remaining thickness of the block

beneath the lower layer suggests that no

more than two layers are present beneath the

right arm, but the bottom of the nest is not

exposed. Eight eggs are arranged in pairs

(figs. 1, 4), and allmay be paired. Where

eggs are exposed in two layers, beneath the

specimen's right forelimb, matrix is absent

between some areas of the juxtaposed eggs,

but an egg in the upper layer beneath the left

manus is suspended at leastpartly by matrix

and not by the lower layer of eggs. Further-

more, at least one pair ofeggs in the upper

layer is situated farther away from the center

of the nest than the eggs upon which they

rest (fig. 4), unlike the arrangement of at least

two other nests of this type (Dong and Cur-

rie, 1996). Most of the center of the nest is

not exposed, but there is no evidence for

eggs in the center at the same level as the

uppermost eggs exposed further out from the

center.

The eggs are elongate, parallel sided, with

NO. 3265

CLARK ET AL.: NESTING OVIRAPTORID FROM MONGOLIA

If

Ica

Fig. 9. IGM 100/979, left fibula and tarsus in posterior view, left pes in dorsal

fragments beneath unguals. See Appendix for abbreviations.

rounded ends of similar shape, a shape

termed elongatoolithid (Mikhailov et al.,

1994). Although previously we implied that

they are less rounded atone end than the

other (Norell et al., 1995), in those eggs

where both ends are exposed they are sym-

metrical. The outer surface has a series of

longitudinally oriented fine ridges that grade

into dimples or smooth areasat the poles.

None of the well-exposed eggsshow indi-

cations of hatching or predation, nor are

3cm

view. Note egg

bones visible in the few in which the interior

is exposed. Two eggshellfragments, nearthe

left ischium, suggestthe presence of a bro-

ken egg, but this area is insufficiently ex-

posed to interpret definitively. A histologic

study of the egg shell will be published else-

where (Bray et al., in press).

None of the eggs are exposed in theiren-

tirety, so all of their dimensions cannot be

measured accurately. A pair of eggsbeneath

the right manus differ in their width, one be-

1999

AMERICAN MUSEUM NOVITATES

ing only 6.5 cm wide, the other 7.2, and the

difference is likely due to the effects of

crushing. An egg beneath the left carpus is

nearly completely exposed, and as preserved

is at least 18 cm in length, but less than 19

cm.

Eggs are not preserved within the pelvic

region, much of which is missing. If the an-

imal had been in the act of laying an egg or

preparing to do so, it is expected that one or

two would be preserved here. The incom-

pleteness of the pelvis makes this assessment

uncertain, but to have been lost to erosion an

egg must have been "floating" in matrix

well above the ischiadic symphysis.

There is no evidence from the outlying

sediments as to the shape or size of the nest,

although little sediment was removed with

the block. There is no obvious structure to

the sediments, nor changes in macroscopic

details away from the eggs (however, they

have not been studied microscopically).

There is also no evidence for plant matter in

the nest, but as the sediments are highly ox-

idized and poorly consolidated with large

pore spaces it is unclear whether it could

have survived diagenesis and the percolation

of ground water (D. Loope, pers. comm.),

and plant remains are not known from the

Djadokhta Formation at Ukhaa Tolgod.

POSTURE OF THE SKELETON ONTHE NEST

The most remarkable aspect of the skele-

ton is the birdlike posture in which it is pre-

served (figs. 1, 13). The body would have

completely coveredthe nest, with the abdom-

inal region over the center, and both limbs

are placed in positions nearly symmetrical

across the midline. The positions of the tibia,

fibulae, femur, pelvis, and ribs suggest that

the body was shifted slightly to the left of

center, lying on the left side of its chest, rath-

er than being exactly symmetrical. Further-

more, the right forelimb is shifted medially,

and the proximal end of the humerus has

come to lie near the midline. This shifting of

the body and right forelimb to the left sug-

gest that the sediment deposited upon the

skeleton may have come toward the animal

from its right hand side.

The gastralia, ventral ribs, and apparently

the sternal elements rest directly on eggs. An

rf

3cm

Fig. 10. IGM 100/979, sternal plates in dor-

sal view, anterior toward top of figure. Note the

articulations of the three ventral rib segments with

the sternum, dislocated slightly posteriorly on the

right side but intact on the left. Alsonote the ap-

position of the gastralia and ventral ribs with a

partially exposed egg posterior to the right sternal

plate. See Appendix for abbreviations.

egg is exposed beneath the ribs and gastralia

immediately posterior to the right sternalel-

ement (fig. 10), and the bones rest directly

on the egg surface. The more posterior ribs

are above the highest level of eggs, suggest-

ing that the center of the nest may have been

filled.

The forelimbs extend laterally and then

posteriorly to overlie the perimeter of the

nest (fig. 1). The humeri extend laterally and

slightly posteriorly from the glenoid fossa.

The right antebrachium is extended, but the

distal ends of the left indicate that the elbow

on that side was flexed about 900. The right

carpus is strongly flexed, but the left is only

slightly flexed.The hands are strongly pro-

nated and lay on their medial surface, and

NO. 3265

CLARK ET AL.: NESTING OVIRAPTORID FROM MONGOLIA

_ It ^

i.' ...4

1K

->

-K

I,a}0'.A4

r

*

,.

.I-

1K

T

Fig. 10.-Continued.

1999

1,

.11.

AL

I..i.

t-l"..a5

W e- I

1.:

is

AMERICAN MUSEUM NOVITATES

Fig. 11. IGM 100/797, thin sections of a dor-

sal segment of a thoracic rib (top) and a ventral

segment of the left first thoracic -rib (bottom).

Note the presence in both of osteons with a cen-

tral lacuna, identified by arrows in the ventral rib

section, indicative of ossification rather than cal-

cification.

the ventral displacement of the first and third

metacarpals relative to the second is most

likely due to the vertical compression that

came to bear after deposition. The right car-

pus rests on top of, or very close to, an egg,

but the left forearm is several centimeters

above the level of the eggs.

The ischia lie directly on top of an egg,

and the pubes extend into the matrix anterior

to this egg, toward the center of the nest. The

pubes have not been completely exposed, but

the preserved portions are from the pubic

symphysis andtherefore near the ventral end

of the bone. Although the expanded "boot"

at the end of the bone is not evident, the

pubes probably do not extend much further

ventrally than their exposed portions.

Both legs are oriented parasagittally with

the knee and ankle joints strongly flexed. The

toes of digits II-IV on the left pes are flexed

in several places (at the base of phalanges II-

1, 111-2, and IV-5), while the fourth toe of

the right side is completely extended (the

second and third are not exposed). The bones

of the left pes are intermixed with pieces of

egg shell, and the fourth toe of the right pes

is less than 1 cm from an egg beneath it.

The skeleton shows little indication of dis-

turbance after deposition. All of the exposed

elements are in their natural articulations,

and the few cases in which they are slightly

separated (e.g., the ungual of left pedal digit

III) are to the limited extent consistent with

postdepositional compaction. The region

showing the greatest disturbance is the shoul-

der girdle, where the coracoids are separated

from the sternal elements and the furcula is

moved anteriorly, apparently due to a medial

movement of the right, and to a lesser extent

the left, forelimbs.

DISCUSSION

PHYLOGENETIC AFFINITIES OF THE SKELETON

The precise identification of IGM 100/979

is made difficult by the lack of a skull and

vertebrae, but several features allow identi-

fication both to Oviraptoridae and to a group

within it. Skeletons of Oviraptoridae are

common at Ukhaa Tolgod (Dashzeveg et al.,

1995), and at least two taxa are present

(Clark and Norell, in prep.). Oviraptoridae

are members of the theropod group Coelu-

rosauria, but do not belong to the largest

group of coelurosaurs, the birds (i.e., Avi-

alae).

The coelurosaurian affinities of the skele-

ton are evident from the presence of elongate

forelimbs, the absence of manus digit IV and

the presence of the semilunate carpal (Gau-

thier 1986). Among nonavialan Coelurosau-

ria, only Dromaeosauridae, Therizinosauri-

dae, Troodontidae and Oviraptorosauria (in-

cluding Oviraptoridae) are known to have a

subquadrangular coracoid (Gauthier, 1986;

Russell and Dong, 1993; Sues, 1997). Dro-

maeosaurids and Oviraptorosauria both have

two broad sternal plates that are sometimes

fused (Barsbold, 1983; Norell and Makov-

icky, 1997), but dromaeosaurids have an op-

isthopubic pelvis, a thinner fibula, metatar-

sals II-IV with ginglymoid distal ends, a re-

tractable second pedal digit with a greatly en-

NO. 3265

CLARK ET AL.: NESTING OVIRAPTORID FROM MONGOLIA

Fig. 12. IGM 100/979, dorsal segments of right thoracic ribs

right dorsolateral view, anterior to the right.

larged claw, and shallower manal claws with

asymmetric grooves for the keratinous

sheath. The manus also differs in having a

shorter third digit relative to the second, and

a more slender, slightly bowed third meta-

carpal. The deep, strongly curved manal

claws of this specimen, with a dorsal lip over

the articulating surface, are similar only to

those of oviraptorosaurians and troodontids

|

l

-

_ g

r

.dB

.

.

-|

I

11f

>.S

_ *

E

w

| - |

.l

.^aX

111|1 | |

|

!j.p X

_ llg i

|

Eppl

1111 | l

l

''YZ

* Z

|

... ' 'r .s

.e

w_ - S |

|

:g.n

1

. 'iEll

g

and associated uncinate processes in

(Currie, 1990). However, troodontids have an

extremely reduced third metatarsal, an un-

usually robust fourth metatarsal, and a re-

tractable second pedal digit (Osm6lska and

Barsbold, 1990), and are reported to lack a

furcula, the clavicles instead being slender

and paired (Russell and Dong, 1993).

Oviraptoridae and the poorly known Caen-

agnathidae (including Chirostenotes, Caen-

Fig. 13. Schematic reconstruction of the oviraptorid as it might have appeared on the nest in lateral

view, based on the postureof the skeletal remains of IGM 100/979. The preserved portion of the skeleton

is shaded darker than the reconstructed portion. The arrangement of eggs in the nest is inpart hypo-

thetical, because most of the nest is not exposed, and the degree to which the outer parts of the nest

were buried is hypothetical.

1999

19

AMERICAN MUSEUM NOVITATES

agnathasia, and Elmisaurus; Sues, 1997) and

Microvenator (Makovicky and Sues, 1998)

together comprise Oviraptorosauria (Osmol-

ska and Barsbold, 1990). Many postcranial

elements are unknown for Caenagnathidae,

and the relationships of Microvenator are un-

certain, limiting the unambiguous diagnosis

of Oviraptoridae. Nevertheless, the metatar-

sals of Caenagnathidae differ from those of

Oviraptoridae and IGM 100/979 in that

metatarsal III is much narrower dorsally, and

in Elmisaurus rarus, at least, the proximal

metatarsals are fused together with the distal

tarsals (Osmolska, 1981). Furthermore, ma-

nus digits II and III are subequal in length

and robustness in Oviraptoridae (Barsbold et

al., 1990),as they are in this specimen, but

in Caenagnathidae and most other Coeluro-

sauria (with the exception of ornithomimo-

saurs) digit III is shorter and more gracile

than digit II (Gauthier, 1986). The only

known skeleton of Microvenator celer shares

few elements in common with IGM 100/979,

but the deltopectoral crest of the humerus of

Microvenator is shorter and less pronounced

(Makovicky and Sues, 1998).

Oviraptoridae are unique among nonavi-

alan theropods in the shape of their furcula,

but this element is not known in Caenag-

nathidae or Microvenator. A furcula is pre-

sent in several nonavialan theropods (Currie

and Zhao, 1993; Norell et al., 1997; Chure

and Madsen, 1996; Makovicky and Currie,

1998), but in Oviraptoridae it is particularly

robust and often has a distinct hypocleidium

(Barsbold, 1983), as on thisspecimen.

Among theropods the most similar furcula is

that of Archaeopteryx (de Beer, 1954) and

Confuciusornis (Peters, 1996; Chiappe et al.,

submitted), although these (unlike that of

many birds) lack a hypocleidium. The hy-

pocleidium of IGM 100/979 is longer than in

any describedoviraptorid, but this delicate

process may have been lost or damaged in

other specimens.

Of the three named genera of Oviraptori-

dae-Oviraptor, Ingenia, and Conchorap-

tor-the skeleton of Ingenia is the most spe-

cialized. The manus of Ingenia is unusual in

that digit I is nearly as long as digit II, and

metacarpal I is half as long as the metacarpal

II, rather than being one third the length of

metacarpal II as in Oviraptor and most other

Coelurosauria (Barsbold, 1981; Barsbold et

al., 1990), features that are absent in IGM

100/979. The sternum of Ingenia also has a

less developed lateral trabecula than does

that of Oviraptor (Barsbold, 1983, fig. 15).

The postcranial skeleton of Conchoraptor

also lacks the specializations of Ingenia

(Barsbold et al., 1990), but the numerous

specimens of this taxon preserved in the

Mongolian Institute of Geology are all much

smaller than those of IGM 100/979, whereas

several specimens of Oviraptor are of a sim-

ilar large size, much larger than any other

oviraptorosaurian. Pending revision of this

group based upon the new material from

Ukhaa Tolgod, the present evidence therefore

suggests that IGM 100/979 is an oviraptorid

most closely related to Oviraptor.

The specimen also presents some features

differing from conditions in other Ovirapto-

ridae. The posterolateral flattening and bend-

ing of the furcula and the horizontal orien-

tation of the shelf on the anterior edge of the

scapula with which it articulates are similar

to, but more developed than, theseregions in

Oviraptor philoceratops (IGM 100/42). The

strongly sutured ischial symphysis is also

unique among oviraptorid specimens, but the

bone along the symphysis is very thin and

therefore easily damaged, and none of the

known oviraptorid skeletons with complete

ischia are as large as this one.

PHYLOGENETIC AFFINITIES OF THE EGGS

Many types of eggs are known from the

Djadokhta Formation of Mongolia (Mikhai-

lov et al., 1994), but the identification with

particular groups of vertebrates is tentative

for all except the single type for which di-

agnostic embryonic remains are known. The

single exception (IGM 100/971) is an ovi-

raptorid embryo preserved within an incom-

plete egg from UkhaaTolgod (Norell et al.,

1994). The eggs of IGM100/979 are similar

in all respects to the egg with the oviraptorid

embryo.

A parataxonomy of eggs and eggshell has

been developedby Zhao (e.g.,1975), and

Mikhailov (1991) identified histologic mor-

photypes correlated with this taxonomy. The

eggs of IGM 100/979 are of the type classi-

fied as elongatoolithid in Zhao's system as

20

NO. 3265

CLARK ET AL.: NESTING OVIRAPTORID FROM MONGOLIA

modified by Mikhailov, based upon their

large size, elongate shape with parallel or

sub-parallel sides, and sculpture pattern

("discretituberculate") of nodes and short

longitudinal ridges on the long edges and

nodes on the ends. The eggs from the nest

(AMNH 6508) beneath the holotype of Ovi-

raptor philoceratops at Bayn Dzak (Norell et

al., 1994) and those from beneath the ovirap-

torid skeleton at Bayan Mandahu (Dong and

Currie, 1996) are also of this type.

The eggs of IGM 100/979 are unusually

long, at least 18 cm in length. Elongatoolith-

id eggs are generally 15-17 cm long (Mik-

hailov et al., 1994); those from Bayan Man-

dahu are only 15 cm in length, and the eggs

from beneath the 0. philoceratops holotype

(AMNH 6508) are 14 cm long (although

crushing may have shortened them by up to

2 cm). The egg from Ukhaa Tolgod with the

oviraptorid embryo (IGM 100/971) was cited

as being only 12 cm long (Norell et al.,

1994), but it is too incomplete to estimate its

length accurately.

Because of the paucity of embryonic re-

mains in fossil eggs the precise identity of

most is unclear, and the taxonomic level at

which elongatoolithid eggs are diagnostic

may extend beyond Oviraptoridae. Further-

more, the only known embryo is incomplete,

and cannot be identified below the family

level. The skull and mandible of the embryo

possess the short, vertical rostrum, edentu-

lous margins, and tall mandible that distin-

guish oviraptorids from all other theropods.

The mandible is much shorter and taller than

that of caenagnathids, placing it within the

Oviraptoridae. Unfortunately, the lack of

dorsal roofing bones and evidence of the ma-

nus (which may be covered by the rest of the

skeleton) precludes more precise identifica-

tion.

POTENTIAL SKELETAL HOMOLOGIES

WITH AVIALAE

This specimen is significant in providing

new information concerning the ventral part

of the thorax and the keratinous claws in ovi-

raptorids, andin suggesting that oviraptorids

behaved in ways similar to their living rela-

tives, birds. The ribsand sternum provide ev-

idence for features hitherto poorly known in

Oviraptoridae and unknown or rare in other

close relatives of birds: a single ossified ven-

tral rib segment in the first four thoracic ribs,

the articulation of three ribs with the costal

margin of the sternum, and ossified uncinate

processes. The specimen also confirms fea-

tures notedpreviously in other oviraptorids

(Barsbold, 1981), such as the articulation of

the coracoid with the anterior, rather than lat-

eral, edge of the sternum and the presence of

a robust furcula.

The pattern of rib segmentation in IGM

100/979, with a single, ossified ventral seg-

ment, is remarkably similar to the pattern in

the ribs of birds and unlike that in crocodyli-

an ribs. In the thoracic rib cage of nonavian

reptiles, such as crocodylians, one or two

cartilaginous segments are present between

the ossified dorsal rib and the sternum, but

they do not ossify (Parker, 1868; Hoffstetter

and Gasc, 1969). In crocodylians, the first 9

or (inGavialis) 10 thoracic ribs have two

cartilaginous segments ventral to the dorsal

rib (i.e., three segments in all), whereas the

following two ribs lack the intermediate el-

ement. The two ventral segments calcify in

some individuals, but they are not reported

to ossify (e.g., they do not have haversion

systems). The ribs of birds, however, have

only one ventral segment, and it is well os-

sified (Bellairs and Jenkin, 1960). An appar-

ently ossified, single ventral rib segment is

present in fossils of some basal avialans (e.g.,

Iberomesornis, Confuciusornis, and Hespe-

rornis) although they are not discernible on

any known specimen of Archaeopteryx.

Ossified ventral ribs were identified ten-

tatively in the dromaeosaurid Deinonychus

on the basis of isolated elements (Ostrom,

1969: 84-86), in the dromaeosaurid Veloci-

raptor (Barsbold, 1983: 34), and in the basal

troodontid Sinornithoides on the basis of CT

scans of an articulated skeleton (Russell and

Dong, 1993). Comparing Deinonychus with

crocodylians, Ostrom tentatively inferred the

presence of two ventral segments in Deinon-

ychus, but the isolated elements he studied

do not provide evidence sufficient to reach

this conclusion, especially considering the

evidence of only a single ventral segment in

their relatives, birds and oviraptorids. An os-

sified ventral segment is definitively present

in Velociraptor (Norell and Makovicky, in

1999

21

AMERICAN MUSEUM NOVITATES

Oss. ventral ribs

Sternal rib #

'

Ossified stemum

Oss. unc. proc.

o

0

0

3-4

0-6

2

0

0

0

1

0

0

1

?

1

2

3

1

1

?

1

.

,.vS°

sd

5

t

0'P

eP

-AOOJV \\10

90

s

1

0? 1

1

1

3

?

5

5

2-9

1

1

1

1

1

1

0?

1

1

2(1)

3 rib articulations

\ fl to the sternum;

ossified ventral ribs*;

ossified uncinate

processes*

Fig. 14. Cladogram of relationships among theropod taxa with well-preserved sternal regions and

distribution of osteological characters discussed in the text, and the level at which selected features are

synapomorphous (under DELTRAN optimization). Relationships are supported by the analyses of Gau-

thier (1986), Holtz (1994), and Sues (1997), and the interpretation of Currie and Zhao (1993). Ossified

ventral ribs: rib ossification confined to dorsal segment (0) or both dorsal and ventral rib segments

ossified (1); Sternal rib number: number of rib articulations to the body of the sternum (the praester-

num); Ossified sternum: sternum unossified (0) or ossified (1); Ossified uncinate processes: ossified

uncinate processes absent (0), present and separate from ribs (1), present and fused to ribs (2). Paren-

theses indicate the occurrence in a group of a condition that is most simply interpreted as secondarily

derived, asterisk indicates characters that apply to more inclusive groups under different optimization

procedures. Sources: Parker, 1868; Marsh, 1880; Furbringer, 1888; Howes and Swinnerton, 1901; Lam-

be, 1917; Hoffstetter and Gasc, 1969; Currie and Zhao, 1993; Wellnhofer, 1993; Norell and Makovicky,

in press; Chiappe et al., submitted.

press), but is not otherwise reported in non-

avialan Coelurosauria.

The ventral segments on IGM 100/979 de-

finitively confirm the presence of these struc-

tures in nonavialan theropods, and they cor-

roborate the identification of these elements

in Deinonychus, at least one example of

which is similar in shape and has expanded

ends (Ostrom, 1969: fig. 52b). The absence

of these elements in other taxa may be an

artifact of ontogenetic sampling, preserva-

tion, or the manner in which they were col-

lected. In any case, the presence of ossified

ventral rib segments is a synapomorphy of

birds with a group including at least ovirap-

torids and dromaeosaurids among dinosaurs

(fig. 14).

The articulation of three ribs with the ster-

num inIGM 100/979 is significant in com-

parison with the typically larger number in

birds and the smaller number in more basal

theropods. In birds a variable number of ribs

articulate with the sternum, but with a single

exception it is greater thantwo. The number

of rib attachments to the avian sternum is

reported to range from 2 in some species of

Dinornithidae (moas) to 9 in, for example,

Cygnus (Furbringer, 1888: table 21). The

sternum of some moas is reported to have

facets for only two ribs, but those of other

species in this family are reported to have

three (Owen, 1879; Oliver, 1949). The rela-

tionships of moas, within Paleognathae (Lee

et al., 1997), imply that the condition of hav-

ing only two rib articulations represents an

evolutionary reversal from a larger number

of articulations, given that tinamous, neo-

gnaths, and basal avialans, where known

22

NO. 3265

0.

7

2

7

CLARK ET AL.: NESTING OVIRAPTORID FROM MONGOLIA

(e.g., Hesperornis and Ichthyornis, Marsh,

1880; Confuciusornis, Chiappe et al., sub-

mitted), have a larger number. In Archaeop-

teryx a sternum is preserved on only one

specimen (Wellnhofer, 1993), and it is too

poorly preserved to determine the number of

rib articulations.

In the few nonavialan theropods for which

this feature is known (Albertosaurus and Sin-

raptor), distinct facets for only two rib artic-

ulations are evident on the sternum (Lambe,

1917; Currie and Zhao, 1993). The sternum

is known in representatives of all of the other

major groups of dinosaurs (Sauropodomor-

pha, Thyreophora, Ornithopoda, and Margin-

ocephalia), but it is unclear how many ribs

attach (Weishampel et al., 1990). A specimen

of Velociraptor mongoliensis from Tugru-

geen Shireh (IGM 100/976) has three closely

appressed ventral ribs preserved adjacent to

the right side of the right sternal plate (Norell

et al., 1997; Norell and Makovicky, in press),

providing evidence that three ribs articulated

with the sternum in this taxon as well. The

articulation of more than two ribs with the

sternum in the oviraptorid specimen de-

scribed here and in Velociraptor therefore is

a synapomorphy of these two taxa with birds,

but the lack of information about the distri-

bution of this feature among other extinct

Coelurosauria greatly limits its implications

at this time.

In crocodylians (Parker, 1868; Hoffstetter

and Gasc, 1969), the first two thoracic ribs

articulate (via cartilaginous segments) with

the broad body of the cartilaginous sternum

(the praesternum of Parker, 1868), and the

following 6or 7 ribs articulate with a much

narrower posterior extension (the mesoster-

num of Parker, 1868). In extant birds, ribs

articulate only with the anterior part of the

lateral edge of the broad, ossifiedsternal

plate, and a structure similar to the meso-

sternum of crocodylians is absent (Parker,

1868; Furbringer, 1888). The ossified ster-

num of theropods (including birds) is there-

fore most comparable to the body (praester-

num) of the crocodylian sternum, and the

presence of two ribs in articulation with the

sternum in basal theropods and with the body

of the sternum in crocodylians in conse-

quence establishes this as the primitive con-

dition for Archosauria.

The precise phylogenetic relationships

among theropods is disputed, but all recent

studies (Currie and Zhao, 1993; Holtz, 1994;

Sues, 1997) indicate that oviraptorosaurs and

dromaeosaurids are more closely related to

extant birds than are tyrannosaurids, andtyr-

annosaurids are more closely related to a

group comprising these taxa than is Sinrap-

tor. The optimization of the number of rib

articulations to the sternum ona cladogram

of these phylogenetic relationships (fig. 14)

indicates that (1) two rib articulations with

the ossified portion of the sternum is ple-

siomorphic for Theropoda, (2) three rib ar-

ticulations with the sternum is a synapomor-

phy of dromaeosaurids, oviraptorids, and

Avialae (and perhaps some other coelurosau-

rians more closely related to them than to

tyrannosaurs and more basal dinosaurs), and

3) the higher number of sternal articulations

in many birds is an evolutionary increase.

The identification of the costal margin of

the sternum allows for a more precise un-

derstanding of the morphology of this struc-

ture in oviraptorids (see Barsbold, 1981, for

descriptions of other oviraptorid sternae).

The costal margin is in a position comparable

to that of most birds, on the anterior half of

the lateral surface, rather than posteriorly as

in crocodylians and lepidosaurs. Although

there is a great deal of variation among birds

in the morphology of the lateral edge of the

sternum there is often a lateral or posterolat-

eral process immediately posterior to the cos-

tal margin, termed the external xiphoid pro-

cess of the lateral xiphisternum by Parker

(1868) and Bellairs and Jenkin (1960) but

identified as the lateral trabecula byFurbrin-

ger (1888) and Baumel and Witmer (1993).

The posterior of the two lateral processes of

the sternum described above in IGM 100/979

is in this same position, and its similarity

with the structure in extant birds and the

presence of a similar process in some basal

avialans (e.g., Concornis; Sanz et al., 1995)

is sufficient to hypothesize that it may be ho-

mologous among these taxa. Theabsence of

such a process in alvarezsaurids (Perle et al.,

1994) suggests that this feature may have

been lost and regained in the course of avi-

alan evolution, however.

The articulation of the coracoid to the an-

terior edge of the sternum is a further feature

23

1999

AMERICAN MUSEUM NOVITATES

that oviraptorids and some other nonavialan

theropods share with birds. In crocodylians

and lepidosaurs the coracoid articulates along

the lateral surface of the sternum, whereas in

birds it articulates along the anterior edge

(Parker, 1868). The sternum is poorly known

in dinosaurs, but in Ankylosauria (Coombs,

1990) and Iguanodon (Norman, 1980) the

coracoid contacts the anterolateral edge of

the sternum (Coombs, 1990) whereas in sau-

ropods it is unclear where the coracoid artic-

ulates (McIntosh, 1990). In Sinraptor (Currie

and Zhao, 1993), Albertosaurus (Lambe,

1917), and the dromaeosaurid Velociraptor

(Norell et al., 1997; Norell and Makovicky,

in press), as well as in other oviraptorids

(Barsbold, 1981), the articulation is with the

anterior edge of the sternum.

The presence of ossified uncinate process-

es in IGM 100/979 broadens the taxonomic

distribution of this character within Thero-

poda (fig. 14). Free uncinate processes as-

sociated with the thoracic ribs are present in

Velociraptor (Paul, 1988; Norell and Makov-

icky, in press) and in some basal avialans,

being especially well developed in Hespe-

rornis regalis (Marsh, 1880), Confuciusornis

(Chiappe et al., submitted) and Chaoyangia

(Hou and Zhang, 1993). In extant birds these

elements develop independent of the rib but

usually fuse to it, except in Apteryx and pen-

guins where they remain free (Parker, 1868;

Furbringer, 1888; Bellairs and Jenkin, 1960).

The incomplete elements preserved on this

specimen are similar to those of Velociraptor

but are more expanded ventrally. Those of

Hesperornis are as broad ventrally but are

shorter. Although the evidence presented by

IGM 100/979 for identifying these as unci-

nate processes is not definitive, owing to its

incompleteness dorsally, at least one other

oviraptorid specimen from Ukhaa Tolgod,

IGM 199/1002, a nearly complete articulated

skeleton, preserves similar elements inter-

laced with the ribs, corroborating this iden-

tification.

The evolution of uncinate processes in

diapsids is somewhat ambiguous, as they are

present and ossified in birds and the basal

lepidosaur Sphenodon, present but unossified

in crocodylians, and altogether absent in ex-

tant squamates (Parker, 1868; Howes and

Swinnerton, 1901; Hoffstetter and Gasc,

1969; Bellairs and Jenkin, 1960). Uncinate

processes are not reported in nontheropodan

diapsids nor in Archaeopteryx, but it is dif-

ficult to ascertain whether the apparent ab-

sence of these elements is actuallydue to the

vagaries of preservation because it requires

exceptional preservation to differentiate

these elements from the ribs proper. In any

case, the elements in IGM 100/979 are sim-

ilar to the elongate elements in basal birds

such as Hesperornis rather than to the short,

unossified elements of crocodylians, and the

distribution of elongate, ossified uncinate

processes indicates that it is a synapomorphy

of Avialae and a more inclusive group of di-

nosaurs including oviraptorids and dromaeo-

saurids (fig. 14).

In extant birds, movements of the rib cage

and sternum are critical to the passage of air

through the specialized respiratory system

(McLelland, 1989), and it is has been sug-

gested that this respiratory system was absent

in nonavialan theropods (Ruben et al., 1997).

The presence in oviraptorids of ossified un-

cinate processes, a furcula, ossified ventral

ribs in articulation with a broad, ossified ster-

num, and an anteriorlyplaced coracoid-ster-

num articulation, on the other hand, suggests

that these animals were capable of the move-

ments required by the avian respiratory sys-

tem. Cataloging the osteological components

of the avian respiratory mechanism does not

constitute a critical test of the biomechanical

capabilities of these structures, however, and

demonstrating the capability of a behavior is

not equivalent to demonstrating that the be-

havior was present. There is at present no

strong evidence for the detailedmorphology

of the respiratory system in nonavian dino-

saurs worthy of detailed consideration. In

any case, the assertion that ossified ventral

rib segments and a broad sternum are absent

in nonavialan theropods (Ruben et al., 1997)

is false, and the inference that a respiratory

system like that of avians was absent in these

taxa is not supported by any reliable evi-

dence (theinterpretation of incompletely pre-

pared soft tissue residue in Sinosauropteryx

notwithstanding).

The remains of the keratinous claws of the

manus are thefirst reported for an ovirapto-

rid, and indicate a highly curved claw

(Chiappe, 1997). The curvature of the kera-

24

NO. 3265

CLARK ET AL.: NESTING OVIRAPTORID FROM MONGOLIA

tinous pedal claws of living birds and its re-

lationship to lifestyle was studied by several

authors, most recently Feduccia (1993), in an

attempt to interpret the lifestyle of Archae-

opteryx and other theropods. Feduccia noted

that in Archaeopteryx the curvature of the

pedal claws is similar to that of perching

birds, and the curvature of the manal claws

is similar to that of climbing birds. Using

Feduccia's method of measuring curvature,

the claw of digit II on the right side of IGM

100/979 spans a minimum of 1600, similar to

the manal claws of Archaeopteryx and the

pedal claws of climbing birds (Chiappe,

1997). Furthermore, the bony manal claws of

the dromaeosaurids Deinonychus (Ostrom,

1969) and Velociraptor (Barsbold, 1983; No-

rell and Makovicky, in press) are as strongly

curved as that of IGM 100/979. This sug-

gests either that Deinonychus and ovirapto-

rids were climbers, or that there was no cor-

relation between claw curvature and climb-

ing behavior in these taxa. Correlations be-

tween form and function are a dubious means

of inferring behavior, because form does not

always indicate behavior where this relation-

ship can be examined in extant taxa (Lauder,

1995), and we are unaware of any evidence

that tests critically the climbing abilities of

oviraptorids and dromaeosaurids. In any

case, the lack of curvature in the manal claws

of nonavialan theropods reported by Feduc-

cia (1993) is contradicted by this specimen.

IMPLICATIONS OF THE SPECIMEN

FOR OVIRAPTORID BEHAVIOR

The specimen described here presents rare

evidence of behavior in an extinct animal,

but the interpretation of behavior in fossils is

more speculative thanin living organisms.

Because behavior-self-initiated movement

of living organisms-cannot be observed di-

rectly in fossils it must be inferred, and these

inferences involve untestable assumptions

beyond those involved in observing behavior

in living organisms. However, the success of

studies of insect nests, spider webs, and writ-

ten languages demonstrates that the products

of behavior are interpretable, andin some

ways more easily interpreted than is the be-

havior producing them because they can be

observed repeatedly without being affected.

The position of IGM 100/979 strongly

evokes the posture taken by birds while sit-

ting on their nests, and the occurrence of four

specimens directly on nests among the first

thirty excavated oviraptorid skeletons indi-

cates that this association is the result of a

consistent behavior of these animals, so a

careful consideration of its implications is

necessary. We review other specimens here,

because a discussion of other specimens of

oviraptorids preserved on nests is critical to

corroborating the evidence provided by our

specimen.

(1) AMNH 6517, the holotype of Ovirap-

tor philoceratops Osborn, 1924. The speci-

men is from the Djadokhta Formation at

Bayn Dzak. The skeleton is missing the hind

limbs, but the anterior part of the skeleton is

preserved lying on its side rather than in a

posture similar to that of IGM 100/979. Os-

born (1924) noted that the skull was pre-

served four inches above the nest, but the

precise position of the skeleton over the nest

is unclear because they were separated dur-

ing preparation. The nest from beneath the

skeleton (AMNH 6508) is incomplete, com-

prising only 15 eggs when collected (two of

which were not intact). The preserved por-

tion of the nest indicates that the eggs were

arranged in pairs and in at least three tiers,

and the preserved semicircular pattern sug-

gests the nest was originally circular.

(2) IVPP specimen V9608, described by

Dong and Currie (1996). Most of the skele-

ton is absent, but preserved are several ver-

tebral fragments and portions of the right

fore and hind limbs overlying six elonga-

toolithid eggs. There is no indication among

the preserved bones that the skeleton or nest

was incomplete before erosion, but the eggs

occur in only one layer. The limbelements

indicate the skeleton was in a posture similar

to that of IGM 100/979, with the arm around

the perimeter of the nest and the pes in the

center ofthe nest.

(3) An unprepared skeleton from Ukhaa

Tolgod, field numberMAE 95-97. As ex-

posed in the field, the specimen consists of

much of a skeleton (except the skull) over-

lying a nest that may be complete. Although

incompletely exposed, the eggs have discre-

tituberculate sculpturing on the poles similar

to thatof elongatoolithid eggs. A photograph

1999

25

AMERICAN MUSEUM NOVITATES

of the specimen was published by Webster

(1996: 80).

In the most recent review of Oviraptori-

dae, Barsbold et al. (1990) listed the total

number of specimens known at that time

from all formations as 13, including the first

one ever collected, AMNH 6517. Dong and

Currie (1996: 632) reported that three spec-

imens of oviraptorids were collected from

the Djadokhta Formation at Bayan Mandahu

by the Sino-Canadian Dinosaur Project, in-

cluding IVPP V9608. The American Muse-

um of Natural History-Mongolian Academy

of Sciences expeditions in 1991 and 1992

collected three oviraptorid specimens from

the Barun Goyot Formation at Ikh Khongil

(also known as Nemegt) and Khermeen Tsav,

and in 1993 discovered the wealth of fossils

at Ukhaa Tolgod (Dashzeveg et al., 1995). A

complete census of oviraptorids from Ukhaa

Tolgod must await preparation of all of the

theropod material collected thus far, but the

two specimens overlying eggs collected in

1993 and 1995 were among the first 12 spec-

imens collected that were identifiable as ovi-

raptorid (including one embryo). Thus, the

four oviraptorid skeletons overlying nests

were among the first 30 adult specimens of

this family collected, a ratio of 13.3%. If

only the remains from the structureless sand-

stones of the Djadokhta Formation are con-

sidered, then the four specimens on nests are

among only 17 adult specimens collected be-

fore 1996, a ratioof 23.5%.

The state of preservation of IGM 100/979

indicates that it was little disturbed after the

death of the animal, and its posture is likely

that taken by the animal as it died (fig. 1).

The skeleton is remarkably complete and ex-

hibits no evidence of scavenging or other dis-

turbance after death that would have altered

the posture of the skeleton (other than the

worm burrows, which are unlikely to have

altered it significantly). This is unusual for

vertebrate fossils, which are often disarticu-

lated and show other evidence of transpor-

tation, such as hydrodynamic wear. Both the

skeleton and the nest areso little disturbed

as to leavelittle doubt that they were not

transported after death and, thus, that the po-

sition in which they are preserved reflects the

position of theskeleton when it died.

The sedimentology of the deposits from

which this specimen and the three other ovi-

raptorids directly overlying nests were col-

lected suggest sudden burial, and represent

an environment in which the animal could

plausibly have been living (rather than one

to which it was carried after death). All are

from similar facies of the Djadokhta For-

mation, a facies termed a structureless sand-

stone (Eberth, 1993). Although such sand-

stones often are continuous laterally with

crossbedded sandstones, indicative of sub-

aerial, eolian deposition, there is no evidence

of crossbedding within them. The lack of in-

ternal structure to these sandstones, which

may reach 15 m in thickness, has been in-

terpreted as the result of sudden accumula-

tions of wind-borne sand (Eberth, 1993). A

recent model suggests instead that these

structureless sandstones were deposited as

mass movements from standing dunes during

rain, rather than wind, storms (Loope et al.,

1998).

Regardless of which of these two deposi-

tional models is correct, the horizontal ori-

entation of the nest and skeleton, the lack of

disturbance to them, and their occurrence

within a single bed of structureless sandstone

indicate that they were in place before burial

and then covered by a flow. The common

occurrence of apparently undisturbed nests of

dinosaur eggs in the sandstones of the Dja-

dokhta Formation (Mikhailov et al., 1994),

and to a lesser extent that of undisturbed, ar-

ticulated skeletons (which, unlike the nest,

may be transported as a unit when the car-

cass has not decomposed), indicate that the

sandstones formed the substrate of the envi-

ronment in which the adult oviraptorids

lived.

The direct apposition of the skeleton on

the nest in IGM 100/979 provides strong ev-

idence that the nest was not completely cov-

ered. The adult skeleton is separated from the

eggs in most places by little sediment, and in

some areas (e.g., the right carpus, left pedal

digits, right fourth pedal digit, ischial sym-

physis, and sternal elements)they are in con-

tact or nearly in contact. The position of the

posterior ribs, pubes, and the medial part of

the right foot above sediments in the middle

of the nest indicate that the center of the nest

was not open.

Unfortunately, it is not possible to deter-

26

NO. 3265

CLARK ET AL.: NESTING OVIRAPTORID FROM MONGOLIA

mine precisely how much of the nest was

buried, because the sediments forming the

nest are not distinguishable from those that

later buried them with the skeleton. Further-

more, although most parts of the forelimbs

are separated from the top of the nest by sev-

eral centimeters of sediment it is unclear that

this necessarily implies these areas of the

nest were covered by this sediment, because

it could have been deposited as the animal

was being buried. During burial it is much

less likely that sediment was removed from

between the skeleton and nest to bring them

closer together, rather than added to separate

them, so the separation of the skeleton and

nest probably indicate the minimal amount

of separation (except for the relatively minor

compaction of the sediments).

The precise relationship between the skel-

eton and nest is known at present for only

one other nesting oviraptorid, IVPP V9608.

Because several skeletal elements are at or

below the level of the eggs, Dong and Currie

(1996) infer that thenest was not buried.

They also infer from the position of the feet,

in the center of the nest but at the same level

as the top of the eggs, that the center of the

nest was filled in. Although the skeleton is

incomplete, the preserved portions are in po-

sitions similar to those of IGM 100/979, in-

dicating a symmetrical posture.

The symmetrical posture exhibited by

IGM 100/979 and by IVPP V9608 is similar

to the position birds take when they sit on

nests (Skutch, 1976; Campbell and Lack,

1985). Other oviraptorid skeletons from the

structureless sandstones of Ukhaa Tolgod

that are not on nests are not in thisposition,

lying instead on their sides with the limbs

extended in various positions (e.g., IGM 199/

1002). Indeed, we are unaware of any non-

avialan dinosaur specimens other than IGM

100/979 and IVPP V9608 preserved in pre-

cisely this posture.

The similarity between the posture of

these two specimens with the posture of birds

is clear, but the important question is whether

they are homologous-is this condition "the

same"l as a result of their close evolutionary

relationship? The inference of homology be-

tween behaviors shared among living organ-

isms is no more problematic than is the in-

terpretation of morphological homologues

(Wenzel, 1992; Greene, 1994), because both

are based upon thesimplest interpretation of

similarities shared among groups of taxa

(Rieppel, 1994). Because of its ephemeral

nature, however, behavior is more difficult to

document (e.g., Drummond, 1981; Miller,

1988). Sampling is a critical issue because

the condition in all relevant taxa-including

those supposedly lacking the behavior-must

be ascertained. These problems are exacer-

bated in the fossil record, because in addition

to the more speculative documentation of be-

havior it offers, sampling is biased by un-

known factors related to the genesis of the

geologic deposits in which they are pre-

served, and the taxonomic identity of the or-

ganism is often poorly resolved or, in the

case of trace fossils, conjectural. Neverthe-

less, these considerations should not neces-

sarily exclude theuse of fossil evidence of

behavior in comparative studies if they offer

reliable evidence of particular behaviors.

Among extant oviparous reptiles parental

care of eggs after deposition is common and

taxonomically widespread only in archo-

saurs. Parents remain close to their eggs after

they are laid, in some cases in direct contact

with them, in birds (Kendeigh, 1952), croc-

odylians (Magnusson et al., 1989; Thorbjar-

narson, 1996), and some squamates (Tinkle

and Gibbons, 1977; Shine, 1988) but not in

turtles (Shine, 1988) or Sphenodon (Moffat,

1985). Because parental care is pervasive in

mammals (although only one group is ovip-

arous) and is common and widespread

among amphibians (Duellman and Trueb,

1994), it may be primitive for the Tetrapoda.

Optimizing these conditions to a clado-

gram of tetrapodrelationships (fig. 15), the

condition in Squamata is critical to determin-

ing whether parental care of eggs was lost in

Reptilia and then re-evolved in some Squa-

mata and in Archosauria or whether instead

it was lost independently in turtles, rhyncho-

cephalians, and within Squamata. If the dis-

tribution of this feature among squamates

implies that it evolved in the common an-

cestor of the entire group, then the two al-

ternatives just mentioned are equally parsi-

monious. If, however, it is simpler to infer

that parental care was not present in the com-

mon ancestor of squamatesthen parental care

is most parsimoniously considered to have

1999

27

AMERICAN MUSEUM NOVITATES

Parental

+

care

"

_

_

_

Nb

Brooding +

_

7 parents

brood eggs

parents do not

brood eggs

Fig. 15. Cladogram of relationships amongextant Reptilia illustrating character distributions and

inferences of homology discussed in the text, and the levelat which they are synapomorphous (under

DELTRAN optimization). Relationships are supported by the analysis of Eernisse and Kluge (1993).

Above: Presenceor absence of parental care of eggs after deposition. Note that this assumes the con-

dition in Squamata to be variable; it isone of two equally parsimonious optimizations if brooding is

inferred to be plesiomorphic for Squamata, the other being separate losses of brooding behavior in

Testudines, Rhynchocephalia, andsome Squamata. Below: Presence or absence of direct contact between

parent and eggs after deposition (i.e., brooding). Parentheses indicate the occurrence in a group of a

condition that is most simply interpreted as secondarily derived. Conditions refer only to oviparous taxa

(i.e., monotremes, all testudines, both species of Rhynchocephalia, most squamates, and all archosaurs).

Sources: Shine, 1988; Moffat, 1985; Collias and Collias, 1984.

been lost in the common ancestor of Reptilia

and re-evolved in the Archosauria (fig. 14).

Among Squamata, parental care of eggs is

known tooccur in Iguaninae, the scincid ge-

nus Eumeces, Anguidae, the teiid genus Tup-

inambis, Varanidae, Boidae, Colubridae, and

Elapidae (Tinkle and Gibbons, 1977; Shine,

1988). Unfortunately, because of the cryptic

behavior of most squamates it is unclear

whether the absence of reports of parental

care inthe other 98% of squamatespecies

(Shine, 1988) is due to the absence of this

behavior or to insufficient opportunities for

observation of these species. Taken at face

28

NO. 3265

A.

NX

0.

IV

'lip,

6\11".1sl..3

-<..eP 0

CLARK ET AL.: NESTING OVIRAPTORID FROM MONGOLIA

value (i.e., assuming brooding is absent in

those groups for which it has not been re-

ported), the distribution of brooding behavior

in squamates implies that it evolved separate-

ly in each of these groups. However, the ac-

tual distribution of this behavior among squa-

mates is undoubtedly broader. It is therefore

uncertain whether parental care is plesiom-

orphic for Squamata, and this is how we have

treated this group in optimizing this character

to the relationships of amniotes (fig. 14).

If parental care is a synapomorphy of ar-

chosaurs, the crocodylian condition might

mistakenly be considered to represent the

primitive condition for the group. But the

primitive condition for Archosauria compris-

es only those features of parental care com-

mon to both crocodylians and birds that are

absent in outgroups. Thus, crocodylian pa-

rental care may include specializations of

Crocodylia, just as parental care of birds in-

volves specializations of Aves identifiable by

their absence in crocodylians and other avian

outgroups.

A specialized form of parental care is the

brooding of eggs, in which the parent brings

its body into direct contact with the eggs for

prolonged periods of time. In the two archo-

saur groups, only bird parents are known to

habitually brood their eggs, typically by rest-

ing directly on top of the nest (Skutch, 1976;

Campbell and Lack, 1985;Gill, 1995). Croc-

odylian eggs are instead buried en masse ei-

ther within a convex mound or a hole (Greer,

1970; Thorbjarnarson, 1996) covered by sed-

iment that in some cases is mixed with plant

debris. Although crocodylian parents (most

commonly the female) often stay near the

nest and, in some species at least, often lie

on the side of the nest (Cott, 1961, 1971),

they are not reported to lie directly on eggs

(which are buried) or with the body centered

on the nest (Magnusson et al., 1989). There

is, thus, no evidence for brooding, or even

for a consistent position or orientation of the

adult's body relative to the nest. Crocodylian

behavior is difficult to study in the wild, and

the possibility that thisparticular behavior

occurs occasionally cannot be dismissed en-

tirely, but sufficient field studies and numer-

ous observations of captive animals indicate

that in crocodylians, unlikein birds, sitting

on the center of the nest and covering the

eggs with the body is not a consistent part of

the behavioral repertoire.

Among birds, with a few interesting ex-

ceptions (e.g., megapodes), one or both par-

ents habitually sit directly on their eggs, and,

again with only a few interesting exceptions

(e.g., emperor penguins), take a characteristic

posture over the nest (Campbell and Lack,

1985). The body is centered over the nest

with the hind legs folded beneath, the ab-

domen contacts the eggs broadly, and often

the forelimb is folded back along the sides

of the body. In extant birds this behavior usu-

ally involves a brooding patch, a highly vas-

cularized area on the abdomen over which

the feathers are shed and body heat is trans-

ferred to the eggs more efficiently than else-

where on the body. Brooding behavior is pre-

sent in tinamous and ratites (although the lat-

ter lack a brooding patch) as well as in the

putatively most basal neognath taxa (Camp-

bell and Lack, 1985), and is therefore prim-

itive for modem birds.

Although it is possible that oviraptorid

nests were buried and occasionally uncov-

ered (a behavior exhibited by the Egyptian

plover; Howell, 1979), there is no compel-

ling evidence that any oviraptorid nest was

ever completely buried. It isunlikely that ev-

idence is forthcoming for specimens without

nesting adults, given the difficulty of distin-

guishing the sediments in which the nest was

deposited from those that later came to bury

them. In any case, because open nests are

present in basal ratites and neognaths (Col-

lias and Collias, 1984, appendix 1) and the

oviraptorid nest provides evidence that in

this group the nest was open at least some of

the time during the brooding period, it cor-

roborates the hypothesis that an open nest is

the plesiomorphic condition for extant Aves.

The presence of two oviraptorid adults di-

rectly on nests suggests that adults of this

taxon habitually sat on nests, but it does not

necessarily imply that they were endothermic

and provided heat to the eggs on a regular

basis, as birds do through their brooding

patch. There isno evidence available to test

this hypothesis, and the assumption that the

behavior associated with brooding and the

act of brooding itself was correlated in ovi-

raptorids is just that-an untestable assump-

tion.

1999

29

AMERICAN MUSEUM NOVITATES

It has been suggested that the posture in

this specimen is similar to that occasionally

taken by crocodylians (Geist and Jones,

1996), but few similarities are apparent on

close comparison. Indeed, the differences be-

tween the many different postures taken by

crocodylians and that of IGM 100/979 are so

obvious-the latter lies over the center of the

nest in direct contact with eggs and with its

legs folded beneath it and its arms spread

around the perimeter of the nest-that this

suggestion is easily dismissed.

The decidedly nonrandom pattern in

which the eggs within oviraptorid nests are

arranged also provides evidence of the be-

havior involved in their deposition. The pair-

ing of eggs within nests of this type (i.e.,

elongatoolithid) strongly suggests that each

pair was laid simultaneously using both ovi-

ducts (Varicchio et al., 1997). The arrange-

ment of the pairs of eggs is also highly struc-

tured, much more so than the positions of

eggs in crocodylian nests. The pairs of eggs

are spaced around the perimeter of a circle

in two layers, with a central area devoid of

eggs. We considered the circular arrangement

of the eggs to be evidence of manipulation

by an adult after deposition (Norell et al.,

1995), but alternatively it could be the result

of highly precise positioning by the mother,

standing in the middle of the nest, during the

egg laying process (Dong and Currie, 1996).

It is unclear if there is any evidence that

could falsify either of these hypotheses.

It has beensuggested that the pairing of

eggs in oviraptorid nests is evidence either

that they were laid at intervals of one day or

more ("monoautochronic ovulation") or in a

much shorter period of time, but there is no

strong evidence against either alternative.

Deposition of the eggs onmore than one day,

as in birds, was advocatedby Varicchio et al.

(1997), who cited in support the pairing of

eggs in lizards and an abnormal duck that

laid pairs of eggs over long time intervals. It

is unclear why the pairing of eggs necessarily

precludes more rapid deposition, however,

given our lack of information about the re-

productive biology of oviraptorids. The al-

ternative scenario, in which the eggs were

laid at one time, is supported mainly by a

nest in which the pairs of eggs are arranged

in a spiral pattern, with gradual changes in

position between pairs (Dong and Currie,

1996). Although this pattern suggests conti-

nuity in the process of egg deposition, and is

plausible, it is also possible that the mother

(or mothers) simply aimed well when they

returned to the nest over time. It is again un-

clear that any evidence is available that could

refute either of these hypotheses.

The behavior of egg turning, in which

birds manipulate the eggs after they have

been laid, is common to nearly all living

birds and, as far as is known, to all that di-

rectly brood their eggs (Campbell and Lack,

1985; Deeming, 1991). It has been suggested

that the apparent partial burial of the eggs in

oviraptorid nests "preclude[s] the possibility

of egg rotation as in birds" (Varicchio et al.,

1997: 249), and indicates the absence of a

structure-chalazea, fibers that support the

embryo within the egg-correlated with this

behavior. As discussed above, it is uncertain

to what extent the eggs were buried while the

adult was alive, but in any case it is unclear

why burial of the eggs necessarily precludes

periodic unburying and rotation. The repeat-

ed burial of eggs by the Egyptian plover

(Howell, 1979) demonstrates the possibility

of this behavior, and although the large num-

ber of eggs in oviraptorid nests would require

a great deal ofactivity to rotate all ofthem,

there seems no reason to consider egg turn-

ing to have been impossible or improbable

in the absence of information about ovirap-

torid metabolism and behavior. Indeed,

which of the more unusual behaviors exhib-

ited by living animals would be deemed un-

likely if only their effects were known?

Stronger evidence against egg rotation is

the pairing of the eggs, because rotation of

the eggs would presumably disrupt this pat-

tern, assumingit to have been created when

the eggs were lain. It is of course possible

that the eggs were laid so soon before their

terminal burial that rotation had not yet taken

place, or that the pairing was due to precise

parental manipulation after egg turning, so at

best the hypotheses of paired oviducts and

egg turning are only weakly tested by the

observation of egg pairs.

There remain many obvious desiderata for

understanding these fossils. In addition to the

unanswered questions just surveyed, we do

not know the sex of the adults on the nests,

NO. 3265

30

CLARK ET AL.: NESTING OVIRAPTORID FROM MONGOLIA

their precise genealogical relationship to the

eggs (e.g., whether more than one set of par-

ents contribute to the nest), how often and

for how long adults attended the nest, what

was the gestation period of the eggs, or how

long hatchlings stayed in the nest. It is tempt-

ing to speculate, but a more fruitful approach

is to continue searching the sands of Ukhaa

Tolgod and elsewhere for specimens that will

provide evidence that might address these

questions.

ACKNOWLEDGMENTS

We thank Hans-Dieter Sues, Chris Mc-

Gowan, John Wenzel, Lowell Dingus, David

Loope, Michael Novacek, Darrel Frost, and

Anusuya Chinsamay for advice on this

work, andM. Kearney, E. Strong, and other

participants in the George Washington Uni-

versity systematics discussion group for

fruitful discussion. We thank Dong Zhi-

Ming for access to the Bayan Mandahu ovi-

raptorid, and C. Brochu and D. Weishampel

for their thoughtful reviews. The histologi-

cal preparations of the ribs were prepared

by Marco van Gemeran, Mineral Optics

Laboratory, and we thank the AMNH De-

partment of Mineral and Planetary Sciences

for the use of their microscope. The fossil

was skillfully prepared by Amy Davidson,

and the illustrations are by Michael Ellison.

Funding for this work was provided by NSF

grant DEB 9407999, the Frick Laboratory

endowment, IREX, and Richard, Lynnette,

and Byron Jaffe. Finally, we thank the other

members of the 1993 field crew of the Mon-

golian Academy of Sciences-American Mu-

seum of Natural History Expedition for their

help in collecting the fossil.

REFERENCES

Andrews, R. C.

1932. The new conquest of Central Asia.

New York: Am. Mus. Nat. Hist.

Averianov, A. 0.

1997. New late Cretaceous mammals of

southern Kazakhstan, Acta Paleontol.

Pol. 42(2): 243-256.

Barsbold, R.

1981. Toothless dinosaurs of Mongolia. Joint

Soviet-Mongolian Paleontol. Exped.

Trans. 15: 28-39 [in Russian].

1983. Carnivorous dinosaurs from the Creta-

ceous of Mongolia. Ibid. 19: 1-120 [in

Russian].

Barsbold, R., T. Maryanska, and H. Osmolska

1990. Oviraptorosauria. In D. B. Weishampel,

P. Dodson, and H. Osm6lska (eds.), The

Dinosauria: 249-258. Berkeley: Univ.

California Press.

Baumel, J. J., and L. M. Witmer

1993. Osteologia. In J. J. Baumel, A. S. King,

J. E. Breazile, H. E. Evans, and J. C.

Vanden Berge (eds.), Handbook of avi-

an anatomy: Nomina anatomica avium:

45-132. 2nd ed. Publ. Nuttall Ornithol.

Club 23.

Bellairs, A. d'A., and C. R. Jenkin

1960. The skeleton of birds. In A. J. Marshall

(ed.), Biology and comparative physi-

ology of birds1: 241-300. New York:

Academic Press.

Bray, E. S., D. K. Zelenitsky, K. F Hirsch, and

M. A. Norell

In press.

Correlation of eggshell ratite mor-

photype with dinosaurs based upon the

find of a Late Cretaceous embryonic

oviraptorid. Am. Mus. Novitates.

Campbell, B., andE. Lack (eds.)

1985. A dictionary of birds. Vermillion, SD:

Buteo Books.

Chiappe, L. M.

1995. The first 85 million years of avian evo-

lution. Nature 378: 349-355.

1997. Climbing Archaeopteryx? A response

to Yalden. Archaeopteryx 15: 109-112.

Chiappe, L. M., Q. Ji, S.-A. Ji, and M. A. Norell

In prep.

Anatomy and systematics of the

Confuciusornithidae (Aves) from the

Mesozoic of northeastern China. Am.

Mus. Novitates

Chure, D. J., and J.H. Madsen, Jr.

1996. On the presence of furculae insome

non-maniraptoran theropods. J. Vertebr.

Paleontol. 16: 573-577.

Clark, J. M., A. Perle, andM. Norell

1994. The skull of Erlicosaurus(sic) andrew-

si, a LateCretaceous "segnosaur"

(Theropoda: Therizinosauridae) from

Mongolia. Am. Mus. Novitates 3113:

39 pp.

Collias, N. E., and E. C. Collias

1984. Nest building and bird behavior.

Princeton, NJ: Princeton Univ. Press.

1999

31

AMERICAN MUSEUM NOVITATES

Coombs, W. P., Jr., and T Maryanska

1990. Ankylosauria. In D. B. Weishampel, P

Dodson, and H. Osmolska (eds.), The

Dinosauria: 456-483. Berkeley: Univ.

California Press.

Cott, H.

1961. Scientific results of an inquiry into the

ecology and economic status of the

Nile Crocodile (Crocodilus niloticus) in

Uganda and northern Rhodesia. Trans.

Zool. Soc. London 29: 211-357.

1971. Parental care in Crocodilia, with special

reference to Crocodylus niloticus. Pro-

ceedings of the First Working Meeting

of Crocodile Specialists. IUCN Publ.

N. ser. 32:166-180.

Cracraft, J.

1976. The species of moas (Aves, Dinorni-

thidae). Smithsonian Contrib. Paleo-

biol. 27: 189-205.

Currie, P. J.

1990. Elmisauridae. In D. B. Weishampel, P.

Dodson, and H. Osmolska (eds.), The

Dinosauria: 245-248. Berkeley: Univ.

California Press.

1995. New information on the anatomy and

relationships of Dromaeosaurus alber-

tensis (Dinosauria: Theropoda). J. Ver-

tebr. Paleontol. 15: 576-591.

Currie, P. J., S. J. Godfrey, and L. Nessov

1993. New caenagnathid (Dinosauria: Thero-

poda) specimens from the Upper Cre-

taceous of North America and Asia.

Can. J. Earth Sci. 30: 2255-2272.

Currie, P. J., and X.-J. Zhao

1993. A new carnosaur (Dinosauria, Thero-

poda) from the Jurassic of Xinjiang,

People's Republic of China. Can. J.

Earth Sci. 30: 2037-2081.

Dashzeveg, D., M. J. Novacek, M. A. Norell, J.

M. Clark, L. M. Chiappe, A. R. David-

son, M. C. McKenna, L. Dingus, C. C.

Swisher III, and A. Perle.

1995. Unusual preservation in a new verte-

brate assemblage from the Late Creta-

ceous of Mongolia. Nature 374: 446-

449.

Deeming, D. C.

1991. Reasons for the dichotomy in egg turn-

ing in birds and reptiles. In D. C.

Deeming andM.W.J. Ferguson (eds.),

Egg incubation: 307-324. New York:

Cambridge Univ.Press.

de Beer, G. R.

1954. Description of the British Museum

specimen of Archaeopteryx and com-

parison with the Berlin specimen. Lon-

don: Trustees of the Br. Mus.

Dong, Z.-M., and P. J. Currie

1996. On the discovery of an oviraptorid

skeleton on a nest of eggs at Bayan

Mandahu, Inner Mongolia, People's

Republic of China. Can. J. Earth Sci.

33(4): 631-636.

Drummond, H.

1981. The nature and description of behavior

patterns. In P. G. Bateson and P. H.

Klopfer (eds.), Perspectives in ethology

4: 1-33. New York: Plenum Press.

Duellman, W. E., and L. R. Trueb

1994. Biology of amphibians. Baltimore:

Johns Hopkins Univ. Press.

Eberth, D. A.

1993. Depositional environments and facies

transitions of dinosaur-bearing Upper

Cretaceous redbeds at Bayan Mandahu

(Inner Mongolia, People's Republic of

China). Can. J. Earth Sci. 30(10-11):

2196-2213.

Eernisse, D., and A. G. Kluge

1993. Taxonomic congruence versus total ev-

idence, and amniote phylogeny inferred

from fossils, molecules, and morphol-

ogy. Mol. Biol. Evol. 10: 1170-1195.

Feduccia, A.

1993. Evidence from claw geometry indicat-

li[data-testid="exclude_keyword"],div[data-testid="popular-brands"],.merNavigationBottom,.kbzInU,div[data-testid="checkout-button-container"],[text="やることリスト"],mer-navigation-bottom,.gvxzwb,.merNavigationTopMenuItem,.primary__f49ba1aa,mer-information-bubble[variant="transition"],.end-section, mer-tab-item[value="/my_list"],nav[slot="end"],[name=purchase],footer, div[data-location="item_details:comment:post_button"],[data-testid="open-buyee-link"],[data-testid="cross-border-banner"], a[href="/sell"],a[href="/todos"],div[data-testid="signin-signup-nav"], a[data-location="home:recommend:component:banner"],.dcoyNT,.ciiiJf ,div[data-testid="tabs"]{display:none !important;} #sanwago-buy{cursor: pointer;border:0;display:none;height: 33px;width:190px;background-color: rgb(255 1 17);color: #fff;border-radius: 3px;} #translation{display: none;} #translation>select { appearance: none; -webkit-appearance: none; -moz-appearance: none; border: 1px solid #f5f4f4; border-radius: 4px; height: 2.2em; padding: 0 24px 0 8px; font-family: inherit; color: #666; cursor: pointer; position: relative; background: url('data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAABgAAAAYCAMAAADXqc3KAAAASFBMVEUAAAD////Nzc3Nzc3V1dXNzc3MzMzMzMzMzMzNzc3Ozs7j4+PMzMzMzMzMzMzPz8/MzMzNzc3Ozs7Ozs7MzMzNzc3Nzc3Nzc1mbvnCAAAAGHRSTlMAAymOBrtVs9RlPgnPltxPlWwvRJzBt+CSuXutAAAAM0lEQVR4nGMYBbgALycjiGIUZEaTEBLl4WJgEOZgZcLQwybOLsbHj800bhEBFqo7cfACACvdARau8cpxAAAAAElFTkSuQmCC') no-repeat right center; } #sanwago-share{cursor: pointer;display:none;height: 33px;width:190px;color: rgb(255 1 17);border-radius: 3px;border: 1px solid rgb(255 1 17)} #sanwago-collect{cursor: pointer;display:none;height: 33px;width:190px;color: rgb(255 1 17);border-radius: 3px;border: 1px solid rgb(255 1 17)} #sanwago-style{z-index:9999;position: fixed;right: 3%;top:15%;} #sanwago-style>div{margin-top: 20px} .sanwago-userinfo{z-index:9999;position: fixed;top:2%;right: 0;text-align: center;width: 20%;height: 8%;color: #7a7a7a } .sanwago-userinfo>span{margin-left: 3%} .sanwago-userinfo img{position: relative;top:5px}

  翻译：

查看mercari原页面

收藏该商品

立即下单