A new Jehol enantiornithine bird with three-dimensional preservation and ovarian follicles

Abstract

ABSTRACTWe report a new enantiornithine bird, Linyiornis amoena gen. et sp. nov., from the Lower Cretaceous Jiufotang Formation in northeastern China. Traces of ovarian follicles indicate that the specimen represents a female individual. The nearly three-dimensional preservation of the new specimen reveals morphological details rarely visible in other Early Cretaceous enantiornithines, allowing more detailed comparison with Late Cretaceous enantiornithines. Differences in the preserved morphology of the right and left coracoids suggest that the appearance of some features is strongly affected by preservation, indicating that the distribution of these features in compressed specimens may need to be reevaluated. Like Late Cretaceous enantiornithine specimens, the holotype of Linyiornis amoena preserves a hypertrophied pit for muscle attachment on the bicipital crest but clearly did not preserve a fossa for the capital ligament, present in Late Cretaceous taxa; we discuss the functional morphology and implications of these features in Linyiornis amoena.http://zoobank.org/urn:lsid:zoobank.org:pub:EFFD4348-7376-4201-A948-CEC686E2E0DCSUPPLEMENTAL DATA?Supplemental materials are available for this article for free at www.tandfonline.com/UJVPCitation for this article: Wang, Y., M. Wang, J. K. O'Connor, X. Wang, X. Zheng, and X. Zhang. 2016. A new Jehol enantiornithine bird with three-dimensional preservation and ovarian follicles. Journal of Vertebrate Paleontology. DOI: 10.1080/02724634.2015.1054496.

Full text

Full Terms & Conditions of access and use can be found at
http://www.tandfonline.com/action/journalInformation?journalCode=ujvp20
Download by: [Jingmai K. O’Connor] Date: 15 January 2016, At: 06:41
Journal of Vertebrate Paleontology
ISSN: 0272-4634 (Print) 1937-2809 (Online) Journal homepage: http://www.tandfonline.com/loi/ujvp20
A new Jehol enantiornithine bird with three-
dimensional preservation and ovarian follicles
Yan Wang, Min Wang, Jingmai K. O'connor, Xiaoli Wang, Xiaoting Zheng &
Xiaomei Zhang
To cite this article: Yan Wang, Min Wang, Jingmai K. O'connor, Xiaoli Wang, Xiaoting Zheng &
Xiaomei Zhang (2016): A new Jehol enantiornithine bird with three-dimensional preservation
and ovarian follicles, Journal of Vertebrate Paleontology, DOI: 10.1080/02724634.2015.1054496
To link to this article: http://dx.doi.org/10.1080/02724634.2015.1054496
View supplementary material
Published online: 11 Jan 2016.
Submit your article to this journal
Article views: 113
View related articles
View Crossmark data

ARTICLE
A NEW JEHOL ENANTIORNITHINE BIRD WITH THREE-DIMENSIONAL PRESERVATION
AND OVARIAN FOLLICLES
YAN WANG,
1,2
MIN WANG,*
,3
JINGMAI K. O’CONNOR,
3
XIAOLI WANG,
1
XIAOTING ZHENG,
1,4
and XIAOMEI ZHANG
4
1
Institute of Geology and Paleontology, Linyi University, Linyi, Shandong 276000, China;
2
State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of
Sciences, Nanjing 210008, China;
3
Key Laboratory of Vertebrate Evolution and Human Origins of Chinese Academy of Sciences, Institute of Vertebrate Paleontology
and Paleoanthropology, Chinese Academy of Sciences, 142 Xizhimenwai Street, Beijing 100044, China, wangmin@ivpp.ac.cn;
4
Shandong Tianyu Museum of Nature, Pingyi, Shandong 273300, China
ABSTRACT—We report a new enantiornithine bird, Linyiornis amoena gen. et sp. nov., from the Lower Cretaceous
Jiufotang Formation in northeastern China. Traces of ovarian follicles indicate that the specimen represents a female
individual. The nearly three-dimensional preservation of the new specimen reveals morphological details rarely visible in
other Early Cretaceous enantiornithines, allowing more detailed comparison with Late Cretaceous enantiornithines.
Differences in the preserved morphology of the right and left coracoids suggest that the appearance of some features is
strongly affected by preservation, indicating that the distribution of these features in compressed specimens may need to be
reevaluated. Like Late Cretaceous enantiornithine specimens, the holotype of Linyiornis amoena preserves a hypertrophied
pit for muscle attachment on the bicipital crest but clearly did not preserve a fossa for the capital ligament, present in Late
Cretaceous taxa; we discuss the functional morphology and implications of these features in Linyiornis amoena.
http://zoobank.org/urn:lsid:zoobank.org:pub:EFFD4348-7376-4201-A948-CEC686E2E0DC
SUPPLEMENTAL DATA—Supplemental materials are available for this article for free at www.tandfonline.com/UJVP
Citation for this article: Wang, Y., M. Wang, J. K. O’Connor, X. Wang, X. Zheng, and X. Zhang. 2016. A new Jehol
enantiornithine bird with three-dimensional preservation and ovarian follicles. Journal of Vertebrate Paleontology. DOI:
10.1080/02724634.2015.1054496.
INTRODUCTION
The Early Cretaceous Jehol Biota of northeastern China
undoubtedly includes the most important Mesozoic avifauna
known to science (Z. Zhou, 2014). Over the last two decades,
approximately 50 avian species have been reported (Z. Zhou
and Zhang 2006b; Benton et al., 2008; Z. Zhou and Wang,
2010), representing nearly half the known global diversity of
Mesozoic birds. The unique geologic and taphonomic environ-
ments of these lacustrine deposits have resulted in the discovery
of thousands of nearly complete skeletons, some of which addi-
tionally included preserved feathers, stomach contents, and in
rare cases traces of internal soft tissues such as ovarian follicles
(F. Zhang et al., 2006; Xu et al., 2010; Zheng et al., 2011, 2013,
2014; S. Zhou et al., 2014). The Jehol Biota bearing deposits
consist of, in ascending order, the Huajiying, Yixian, and Jiufo-
tang formations (Pan et al., 2013), which encompass over 10
million years of early avian evolution (130.7–120.0 Ma). Repre-
sentatives of all known major Mesozoic avian clades have been
described, including the long bony-tailed Jeholornithiformes, the
earliest pygostylians Sapeornithiformes and Confuciusornithi-
formes, Enantiornithes, and Ornithuromorpha—the clade
including all living birds and their fossil relatives (Z. Zhou
and Zhang, 2006b; O’Connor, 2009; Z. Zhou and Wang,
2010). The sister group to Ornithuromorpha, Enantiornithes
overwhelms other contemporary avian groups in both taxo-
nomic diversity and geographic distribution, suggesting that
Enantiornithes represents the first major avian diversification
(O’Connor, Zhang, et al., 2013; M. Wang et al., 2015). The
first stage in the Jehol Biota, the Huajiying Formation,
records the first appearance datum of this clade, represented
by only two taxa: Protopteryx fengningensis F. Zhang and
Zhou, 2000, and Eopengornis martini Wang, O’Connor,
Zheng, M. Wang, Hu, and Zhou, 2014 (130.7 Ma; Jin et al.,
2008). In the Yixian and Jiufotang formations, diversity is
much higher and more than 20 avian taxa have been named
from these two formations alone. Although nearly complete
and fully articulated specimens from this biota and other
Early Cretaceous deposits have greatly advanced our knowl-
edge of Enantiornithes, these specimens are typically heavily
compressed during diagenesis and preserved primarily in two
dimensions, limiting comparison with fragmentary but three-
dimensionally preserved specimens from the Late Cretaceous
(O’Connor, 2009; M. Wang, 2014). The disparity between the
morphological information available from Early and Late
Cretaceous faunas prevents detailed comparison and further
discussions about morphological evolution during the 65 mil-
lion-year history of this clade.
*Corresponding author.
Color versions of one or more of the figures in this article can be found
online at www.tandfonline.com/ujvp.
Journal of Vertebrate Paleontology e1054496 (15 pages)
Óby the Society of Vertebrate Paleontology
DOI: 10.1080/02724634.2015.1054496
Downloaded by [Jingmai K. O’Connor] at 06:41 15 January 2016

Here we describe a new enantiornithine bird from the
Jiufotang Formation at Yaolugou Town, Jianchang County,
in Liaoning Province (Fig. 1). The specimen preserves more
three-dimensional morphology than other Jehol specimens,
revealing anatomical details of the pectoral girdle and hindlimb
that were previously poorly known for Early Cretaceous taxa.
Fossilized ovarian follicles have recently been reported in several
Jehol birds and are also identified in the new specimen
(O’Connor, Zheng, Wang, et al., 2013; Zheng et al., 2013).
Institutional Abbreviations—CAGS-IG, Chinese Academy of
Geological Sciences, Institute of Geology, Beijing, China; IVPP,
Institute of Vertebrate Paleontology and Paleoanthropology,
Beijing, China; LP, Institut d’Estudis Ilerdencs, Lleida, Spain;
PVL, Paleontolog
ıa de Vertebrados, Fundaci
on-Instituto Miguel
Lillo, Universidal Nacional de Tuc
uman, Tuc
uman, Argentina;
STM, Shandong Tianyu Museum of Nature, Shandong, China.
MATERIALS AND METHODS
The new specimen is prepared in the IVPP and housed in the
STM under collection number STM11-80.
Anatomical terminology primarily follows Baumel and
Witmer (1993) using English equivalents of the Latin terms given
in that book. For structures not assigned preferred names by
Baumel and Witmer (1993), this article follows Howard (1929).
A phylogenetic analysis was performed using the modified
data matrix of Wang, Zhou, O’Connor, and Zelenkov (2014).
The revised matrix consists of 262 morphological characters and
57 taxa, including 26 enantiornithines (see Supplemental Data
1). Character 91 is expanded here to include an additional state
of the dorsal fossa of the coracoid: absent (0); weakly present
(1); well developed so that the sternal half is C-shaped in distal
view (2). Phylogenetic analysis was performed using TNT soft-
ware (Version 1.1; Goloboff et al., 2008), with the following set-
tings: unconstrained heuristic search starting with Wagner trees,
1,000 replicates of random stepwise addition (branch swapping:
tree bisection–reconnection, TBR), ten trees held at each step,
all characters equally weighted, and branches with minimum
branch lengths of zero collapsed to create polytomies. Bremer
values and bootstrap values were calculated as indices of clade
support. Bootstrap analysis was conducted with 1,000 replicates
using the same settings as in the primary search. Bremer values
were calculated using the bremer scripts embedded in the TNT
software.
SYSTEMATIC PALEONTOLOGY
AVES Linnaeus, 1758
ORNITHOTHORACES Chiappe, 1995
ENANTIORNITHES Walker, 1981
LINYIORNIS, gen. nov.
Type Species—Linyiornis amoena sp. nov.
Diagnosis—As for the type and only species.
Etymology—The generic name refers to Linyi County where
the fossil is housed. The gender is feminine.
LINYIORNIS AMOENA sp. nov. (Figs. 2, 3)
Holotype—STM11-80, a nearly complete and articulated adult
individual with fossilized ovarian follicles preserved in a slab and
counterslab. Bones are primarily preserved in the slab, with the
feet and partial forelimbs in the counterslab (Table 1).
Locality and Horizon—Yaolugou Town, Jianchang County,
Liaoning Province, northeastern China (Fig. 1); Lower Creta-
ceous, Jiufotang Formation (He et al., 2004); the same locality
has yielded Nemicolopterus crypticus X. Wang, Kellner, Zhou,
and Campos, 2008, the smallest known pterosaur.
Etymology—The specific name ‘amoena’ is the Latin word for
‘lovely,’ referring to the preservation of the specimen.
Diagnosis—A pigeon-sized enantiornithine bird with the
unique combination of the following features: robust rostrum
with dorsoventral height of premaxilla corpus equal to its rostro-
caudal length; bicipital crest hypertrophied with strong cranial
projection relative to humeral shaft; muscle attachment pit mas-
sive and craniodistally located on the bicipital crest; scapular
shaft sagittally curved with blunt distal end; fossa for the capital
ligament distinctly absent from the medial surface of femoral
head.
Ontogenetic Remarks—The complete fusion of constituent
bones of each of the tibiotarsus and tarsometatarsus and fusion
of the major and minor metacarpals with the semilunate carpal
indicate that the individual had reached skeletal maturity at the
time of death.
ANATOMICAL DESCRIPTION
Skull
The skull is exposed in right dorsolateral view (Fig. 4). The
premaxillae are fused together along the midline but the frontal
processes are not. The premaxilla is dorsoventrally deep, form-
ing a robust rostrum, similar to bohaiornithids, in contrast with
the delicate morphology seen in many other Early Cretaceous
enantiornithines (O’Connor and Chiappe, 2011; M. Wang, Zhou,
O’Connor, and Zelenkov, 2014). Similar to the structure of
Gobipteryx minuta Elzanowski, 1974, reported by Chiappe et al.
(2001), the rostral portion of the premaxilla (anterior to the fron-
tal process) is elongated so that the dorsoventral height is nearly
equivalent to its rostrocaudal length, whereas it is shorter than
its height in other Early Cretaceous taxa, including bohaiorni-
thids (O’Connor and Chiappe, 2011; M. Wang, Zhou, O’Connor,
and Zelenkov, 2014). The rostral portion of the premaxilla is
even more massive in the Late Cretaceous G. minuta. The fron-
tal processes are relatively short, extending caudally only to the
cranial margin of the antorbital fenestra as in Pengornis houi Z.
Zhou, Clarke, and Zhang, 2008, and Eoenantiornis buhleri Hou,
Martin, Zhou, and Feduccia, 1999, whereas they are longer in
most other enantiornithines, including Cathayornis yandica Z.
FIGURE 1. Map of China showing the fossil locality of the holotype of
Linyiornis amoena, gen. et sp. nov., STM11-80.
Wang et al.—Three-dimensional Jehol enantiornithine bird with ovarian follicles (e1054496-2)
Downloaded by [Jingmai K. O’Connor] at 06:41 15 January 2016

Zhou, Jin, and Zhang, 1992, Longipteryx chaoyangensis F.
Zhang, Zhou, Hou, and Gu, 2001, and bohaiornithids (Z. Zhou
and Hou, 2002; Z. Zhou et al., 2005; O’Connor and Chiappe,
2011; M. Wang, Zhou, O’Connor, and Zelenkov, 2014; M. Wang
and Liu, 2015). The maxillary process is short and caudally tapers
to a blunt tip. The left maxilla is preserved rotated medially so
that two alveoli within the premaxillary process are exposed
(ventral view). The jugal process is poorly preserved, making the
count of maxillary teeth equivocal. On the right, the elongate
dorsal (nasal) process of the maxilla is preserved appressed
against the lateral surface of the right nasal. The latter is nearly
complete and contacts the left nasal medially. The nasal is broad
and bears a long premaxillary process, which extends rostrally
well beyond the mid-point of the external nares. The maxillary
process of the nasal is short and has a sharp ventral tip as in
many other enantiornithines (O’Connor and Chiappe, 2011);
together with the premaxillary process it defines the caudodorsal
margin of the external nares.
The frontals are unfused to each other and to the parietals
as in other primitive birds; they are typically petal shaped
with a tapered rostral end and expanded caudal end. The
subrectangular parietals are displaced to near the proximal
cervicals. The basicranium is preserved in interior view and
with the dorsal margin facing toward the body; the exoccipi-
tals and supraoccipitals are fully fused into a single element,
but the basioccipital remains free, as in the bohaiornithid
Shenqiornis mengi X. Wang, O’Connor, Zhao, Chiappe, Gao,
and Cheng, 2010 (O’Connor and Chiappe, 2011). The exocci-
pital is deeply excavated by a large circular fossa. The basioc-
cipital plate bears well-developed basal tubera similar to but
FIGURE 2. Photograph of the holotype of
Linyiornis amoena, gen. et sp. nov., STM11-
80. A, skeleton on the main slab; B, close-up
of the traces of fossilized ovarian follicles.
Wang et al.—Three-dimensional Jehol enantiornithine bird with ovarian follicles (e1054496-3)
Downloaded by [Jingmai K. O’Connor] at 06:41 15 January 2016

longer and thinner than those present in S. mengi. Also simi-
lar to S. mengi, the foramen magnum is hexagonal and the
supraoccipitals bear blunt paroccipital processes (O’Connor
and Chiappe, 2011). Caudal to the left frontal, an elongate
process is interpreted as the basipterygoid process, based on
its position, nearly in articulation with the basioccipital, and
its similarity to the morphology of the basipterygoid process
of Zhouornis hani Z. Zhang, Chiappe, Han, and Chinsamy,
2013.
Only the right dentary is preserved and it is exposed in ventral
view, preventing the observation of teeth if they were present.
The surangular is robust with straight dorsal and ventral margins,
whereas this bone is bowed ventrally in Longusunguis kuroch-
kini M. Wang, Zhou, O’Connor, and Zelenkov, 2014, and S.
mengi as reported by M. Wang, Zhou, O’Connor, and Zelenkov
(2014). A coronoid process as present in some taxa, e.g.,
Fortunguavis xiaotaizicus M. Wang, O’Connor, and Zhou, 2014,
L. kurochkini, and Rapaxavis pani Morschhauser, Varricchio,
Gao, Liu, Wang, Chen, and Meng, 2009, is not developed in
STM11-80 (O’Connor et al., 2011; M. Wang, Zhou, O’Connor,
and Zelenkov, 2014). Caudally, the articular articulates firmly
with the surangular; they are clearly separated by a suture. The
articular is rarely preserved in enantiornithines except an
unnamed enantiornithine (LP 4450), but the morphology of this
structure is poorly preserved in specimen LP 4450 (O’Connor
and Chiappe, 2011). The well-preserved articular in L. amoena
shows that this element is triangular in lateral view with a large
caudodorsally directed retroarticular process. The ventral sur-
face is not visible and thus whether the articular is pneumatic as
in Confuciusornis sanctus Hou, Zhou, Gu, and Zhang, 1995, and
Archaeorhynchus spathula Z. Zhou and Zhang, 2006a, cannot be
determined. Given that the articulation between the dentary and
FIGURE 3. Composite line drawing of the
holotype of Linyiornis amoena, gen. et sp.
nov., STM11-80. Abbreviations:al 1, first pha-
lanx of alular digit; ca, caudal vertebrae; co,
coracoid; cv, cervical vertebrae; fe, femur; fi,
fibula; fu, furcula; hu, humerus; il, ilium; is,
ischium; mm, major metacarpal; mm 1, 2, 3,
first, second, and third phalanx of major digit;
mi, minor metacarpal; mt I–IV, metatarsals I,
II, III, and IV; of, ovarian follicles; pd, pedal
digits; pu, pubis; py, pygostyle; ra, radius; rb,
ribs; rd, radiale; sc, scapula; sk, skull; st, ster-
num; sy, synsacrum; ti, tibiotarsus; tv, thoracic
vertebrae; ul, ulna; ur, ulnare.
Wang et al.—Three-dimensional Jehol enantiornithine bird with ovarian follicles (e1054496-4)
Downloaded by [Jingmai K. O’Connor] at 06:41 15 January 2016

surangular is not visible, an alternative interpretation is that the
bone here interpreted as the surangular is the angular, and then
the ‘articular’ may represent the medial mandibular process. The
angular is poorly preserved in known enantiornithines
(O’Connor and Chiappe, 2011) and thus this interpretation
needs to be tested by new materials. Several partially exposed
elements visible in the orbit between the frontal and the surangu-
lar may represent the left surangular, angular, or jugal.
Three premaxillary teeth are preserved in situ in the rostral
half of the premaxilla, and an additional tooth was probably
present, considering the large space between the third tooth and
the caudal end of the maxillary process and that enantiornithines
typically have four premaxillary teeth (Z. Zhou et al., 2005;
O’Connor and Chiappe, 2011). Visible in a well-preserved tooth
displaced cranial to the premaxilla, the root is more than twice
as long as the height of the crown. As in the bohaiornithids, the
crown is subconical with a weak constriction at the base and has
a slightly caudally curved occlusal tip (O’Connor, Zhang, et al.,
2013; M. Wang, Zhou, O’Connor, and Zelenkov, 2014).
Axial Skeleton
The cranial-most cervical vertebrae (estimated as three to
five) are poorly preserved and overlain by skull elements. Fur-
ther caudally, seven cervicals are well preserved in ventral view
and remain loosely articulated (Figs. 2, 3). Due to poor preser-
vation, the total number of cervical vertebrae is unclear. There
are seven well-preserved cervicals that begin to decrease in
length after the third. The ventral surface of the centrum is
keeled. A weak costal process is present on the first five cervi-
cals; this process is elongated so that it reaches the mid-point
of the centrum on the sixth vertebra. Exposed on the fifth and
sixth vertebrae, the cranial articular surface appears to be het-
erocoelous and the caudal articular surface is nearly flat, a con-
dition that has been reported in some other enantiornithines
(Z. Zhang et al., 2013; M. Wang, Zhou, O’Connor, and Zelen-
kov, 2014), including Z. hani and L. kurochkini. The seventh of
these vertebrae probably represents the cervico-thoracic transi-
tion. Although the thoracic vertebrae are in articulation, the
series is largely covered by the dorsal ribs (Fig. 2). The verte-
brae are spool shaped with deep, groove-like lateral excava-
tions and centrally located parapophyses (visible in the last
free thoracic) as in other enantiornithines (Chiappe and
Walker, 2002). We estimate the total number of thoracic verte-
brae as eight to ten. As in P. fengningensis and Parabohaiornis
martini M. Wang, Zhou, O’Connor, and Zelenkov, 2014, the
synsacrum is estimated to be composed of seven fully fused ver-
tebrae (F. Zhang and Zhou, 2000; M. Wang, Zhou, O’Connor,
and Zelenkov, 2014). The cranial articular facet of the centrum
of the synsacrum is nearly flat (Fig. 5). The transverse pro-
cesses of the cranial three sacral vertebrae are laterally
TABLE 1. Selected measurements (in millimeters) of the holotype of
Linyiornis amoena gen. et sp. nov., STM11-80.
Element Length
Scapular length 38.7
Coracoid length 25.2
Humerus length 45.2
Ulna length 45.7
Radius length 43.2
Alular metacarpal length 4.35
Carpometacarpus length 19.7
Ilium length 36.1
Ischium length 19.4
Pubis length 47.0
Femur length 39.7
Tibiotarsus length 48.3
Metatarsal II length 21.2
Metatarsal III length 23.4
Metatarsal IV length 22.0
FIGURE 4. Photograph and interpretive line
drawing of the skull of Linyiornis amoena
(STM11-80). Abbreviations:ar, articular; av,
alveolus; bo, basioccipital; bp, basipterygoid
process; bt, basal tubera; de, dentary; eo, exoc-
cipital; fm, foramen magnum; fp, frontal pro-
cess of premaxilla; fr, frontal; ma, maxilla; na,
nasal; pm, premaxilla; po, paroccipital process;
pr, parietal; so, supraoccipital; su, surangular;
to, tooth.
Wang et al.—Three-dimensional Jehol enantiornithine bird with ovarian follicles (e1054496-5)
Downloaded by [Jingmai K. O’Connor] at 06:41 15 January 2016

directed and shorter than the mediolateral width of their asso-
ciated centra. The longest and most robust transverse process
is developed on the sixth vertebra and is caudolaterally
directed. A ventral groove, reported for R. pani by O’Connor
et al. (2011), is absent. Four articulated free caudals are pres-
ent in ventral view (Fig. 5); the caudal end of the series is cov-
ered by the tibiotarsus but in close proximity to the pygostyle
suggesting that L. amoena may have had fewer free caudals
than other enantiornithines, which typically have six to seven
(F. Zhang and Zhou, 2000; Sereno et al., 2002; Chiappe, Ji, and
Ji, 2007; M. Wang, Zhou, and Xu, 2014). The transverse pro-
cesses become increasingly laterally deflected in the more cau-
dally located vertebrae. Only the proximal half of the
pygostyle is preserved and partially covered by the right tibio-
tarsus (Fig. 5). As is typical of most other enantiornithines
(Chiappe and Walker, 2002), the ventral surface of the pygos-
tyle bears a pair of ventrolateral processes that project further
proximally than the articular facet. The ventrolateral processes
extend caudally at least beyond the preserved length of the
pygostyle, creating a deeply concave ventral surface similar to
Halimornis thompsoni Chiappe, Lamb, and Ericson, 2002; in
contrast, the proximoventral processes are more cranially
restricted in L. kurochkini.
Thoracic Girdle and Sternum
The right and left strut-like coracoids are exposed in ventral
and dorsal view, respectively (Fig. 6). As in other enantiorni-
thines (Chiappe and Walker, 2002), a procoracoid process is not
developed. The proximodistally aligned articular surfaces at the
omal end are strongly projected dorsocaudally so that the scapu-
lar articular surface is far dorsal to the acrocoracoid and marks
the dorsoventrally thickest level of the coracoid. Sternal to the
articular surfaces, the coracoid rapidly constricts into the neck,
where both the dorsal and ventral surfaces are fairly flat (weakly
concave dorsally, weakly convex ventrally). A comparable
degree of dorsal projection of the proximal articular surfaces is
widespread among three dimensionally preserved Late Creta-
ceous enantiornithine specimens (Chiappe, Suzuki, et al., 2007;
Walker and Dyke, 2009; Longrich et al., 2011) but can only be
recognized with certainty in the well-preserved holotypes of Z.
hani and L. kurochkini among Early Cretaceous enantiorni-
thines (Z. Zhang et al., 2013; M. Wang, Zhou, O’Connor, and
Zelenkov, 2014), suggesting that the lack of the dorsal projection
among other two-dimensionally preserved Early Cretaceous
specimens may be a taphonomic artefact resultant from postmor-
tem compression. The glenoid facet is confluent with the acro-
coracoid process, rather than separated by a deep fossa as
reported in Z. hani by Z. Zhang et al. (2013). The sternal half of
the right coracoid, visible in dorsolateral view, is excavated by a
dorsal fossa (Fig. 6), reminiscent of the characteristic deep fossa
present in some Late Cretaceous enantiornithines (Chiappe and
Walker, 2002; Walker and Dyke, 2009). This fossa is possibly
homologous to the sternocoracoidal impression of modern birds
(impressio m. sternocoracoidei; Baumel and Witmer, 1993).
Despite the large number of specimens of Jehol Biota, only shal-
low sternocoracoidal impressions have been found in other Early
Cretaceous enantiornithines and ornithuromorphs (Z. Zhang
et al., 2013; Y. Wang et al., 2013; M. Wang, O’Connor, and
Zhou 2014; M. Wang, Zhou, O’Connor, and Zelenkov 2014).
However, the left coracoid is completely flat in ventral view, as
in most Jehol enantiornithines in which the coracoid is exposed
in ventral view—this is more consistent with the rostral margin
of the sternum, which is broad and also fairly flat. We suggest
that the slight lateral preservation of the right coracoid exagger-
ates the depth of the dorsal depression while the ventral preser-
vation of the left coracoid and sternum exaggerates the flatness.
The narrow, deeply excavated morphology present in some Late
Cretaceous enantiornithines (e.g., Neuquenornis volans Chiappe
and Calvo, 1994) was clearly not present. Cranial to the sterno-
coracoidal impression, the coracoidal shaft is perforated by a
supracoracoidal nerve foramen, which is separated from the
medial margin by a bony bar as in many other enantiornithines
(Chiappe and Walker, 2002; Z. Zhou et al., 2005; Walker and
Dyke, 2009; M. Wang, O’Connor, and Zhou, 2014). The lateral
margin is not completely visible and may have been weakly con-
vex; the medial margin is weakly concave and the sternal margin
is straight (left) to weakly concave (right).
The right and left scapulae are exposed in lateral and costal
view, respectively (Fig. 6). As in Z. hani and F. xiaotaizicus, the
FIGURE 5. Photograph of the synsacrum,
pelvis and hind limbs of Linyiornis amoena
(STM11-80). A, the main slab; B, close-up the
right femoral head, revealing that the fossa for
the capital ligament is absent. Abbreviations:
ac, acetabulum; at, antitrochanter; cv, caudal
vertebrae; fe, femur; fh, femoral head; il,
ilium; is, ischium; pu, pubis; py, pygostyle; sy,
synsacrum; ti, tibiotarsus; vp, ventrolateral
process.
Wang et al.—Three-dimensional Jehol enantiornithine bird with ovarian follicles (e1054496-6)
Downloaded by [Jingmai K. O’Connor] at 06:41 15 January 2016

scapula is weakly curved sagittally (Z. Zhang et al., 2013; M.
Wang, O’Connor, and Zhou, 2014), in contrast with the straight
condition typical of other enantiornithines (Sanz et al., 1996; Z.
Zhou, 2002; Chiappe and Walker, 2002; Walker and Dyke,
2009). However, the caudal end of the scapula is blunt, as in
most other enantiornithines (Sanz et al., 2002; Chiappe and
Walker, 2002), whereas it is weakly tapered in Z. hani and F.
xiaotaizicus. As in other enantiornithines, the acromion projects
further cranially than the articular facet for the coracoid. The
acromion is robust and expanded so that the cranial end is costo-
laterally wider than deep as in Late Cretaceous enantiornithines,
e.g., Enantiornis leali Walker, 1981, and H. thompsoni, and some
Early Cretaceous taxa, e.g., C. yandica and potentially L. kur-
ochkini and Z. hani.AsinH. thompsoni, the craniomedial area
of the acromion forms a semilunate surface for articulation with
the furcula that is angled costally (Chiappe and Walker, 2002;
Chiappe et al., 2002). In H. thompsoni, the semilunate surface
bears a distinct sharp and medially oriented tip, which is absent
in L. amoena. The cranial aspect of the acromion is not fully
exposed (obscured by the bicipital crest of the left humerus) and
thus whether the acromion is separated from the articular facet
of the coracoid by a circular pit as in E. leali or a semicircular
notch as in H. thompsoni cannot be determined (Chiappe and
Walker, 2002; Chiappe et al., 2002). Both lateral and costal sur-
faces of the scapular blade are flat, without the longitudinal
groove present in H. thompsoni, R. pani, and some other enan-
tiornithines (Chiappe and Walker, 2002; Chiappe, Suzuki, et al.,
2007; O’Connor et al., 2011).
The furcula is ‘Y’-shaped—a typical condition for enantiorni-
thines (Chiappe and Walker, 2002), with an interclavicular angle
of 50(Fig. 5). The hypocleidium is poorly preserved, mostly
obscured by the left radius and ulna, and thus its length cannot
be determined. The clavicular rami are gently curved medially
similar to P. houi, in contrast with the straight condition of most
other Jehol enantiornithines, including L. chaoyangensis, R.
pani, and P. martini. The omal ends are blunt, whereas in a few
taxa they are expanded, such as in Shanweiniao cooperorum
O’Connor, Wang, Chiappe, Gao, Meng, Cheng, and Liu, 2009.
The sternum is incomplete, preserving only the rostral margin
and the right lateral trabecula. Like many enantiornithines, the
rostral margin is parabolic (Fig. 6). The lateral trabecula is
strongly caudolaterally directed similar to that of bohaiornithids
(M. Wang, Zhou, O’Connor, and Zelenkov, 2014); unfortu-
nately, the distal end of the lateral trabecula is not preserved.
Thoracic Limb
The humerus is subequal to the ulna in length. The humeral
shaft is strongly sigmoid in cranial view, with proximal and distal
halves deflecting ventrally and dorsally, respectively (Fig. 2).
The curvature is stronger than in some other enantiornithines
(Walker et al., 2007; Z. Zhou et al., 2008), e.g., P. houi, E. leali,
and Martinavis cruzyensis Walker, Buffetaut, and Dyke, 2007.
The proximal margin is typical of enantiornithines in that it is
centrally concave, bounded by elevated dorsal and ventral
regions (Chiappe and Walker, 2002; Fig. 6). The cranial surface
of the proximal humerus shows no sign of a circular fossa,
whereas in some taxa, e.g., C. yandica, Parvavis chuxiongensis
M. Wang, Zhou, and Xu, 2014, E. leali, and M. cruzyensis, a dis-
tinct fossa is present centrally on the proximocranial surface
(Chiappe and Walker, 2002; Walker et al., 2007; M. Wang,
Zhou, and Xu, 2014). As noted for Eocathayornis walkeri Z.
Zhou, 2002, Concornis lacustris Sanz and Buscalioni, 1992, E.
leali and M. cruzyensis, the bicipital crest is robust and forms a
hypertrophied cranial projection relative to the shaft (Chiappe
and Walker, 2002; Sanz et al., 2002; Z. Zhou 2002; Walker et al.,
2007; Fig. 6b), whereas the projection is weak in S. mengi, R.
pani, and P. houi.AsinE. leali and Eoalulavis hoyasi Sanz,
Chiappe, P
erez-Moreno, Buscalioni, Moratalla, Ortega, and
Poyato-Ariza, 1996, a distinct pit-shaped fossa for muscle attach-
ment is situated on the craniodistal surface of the bicipital crest
(Chiappe and Walker, 2002; Sanz et al., 2002; Fig. 6), whereas
this fossa is typically more cranioventrally located in Late Creta-
ceous taxa (Chiappe, Suzuki, et al., 2007; Walker et al., 2007),
e.g., M. cruzyensis and Elsornis keni Chiappe, Suzuki, Dyke,
Watabe, Tsogtbaatar, and Barsbold, 2007. Although imperfect
preservation prevents observation of a small pit in some Jehol
enantiornithines, a large pit of the kind present in L. amoena
and Late Cretaceous enantiornithines is clearly absent from
most other Early Cretaceous enantiornithines (where the
FIGURE 6. Photograph of the pectoral girdles of Linyiornis amoena (STM11-80). A, pectoral girdle; B, close-up of the pectoral girdle and the proxi-
mal end of the left humerus. Abbreviations:ac, acromion; bi, bicipital crest; co, coracoid; dp, deltopectoral crest; fo, fossa on bicipital crest; fu, furcula;
hu, humerus; hy, hypocleidium; ib, impression for the facies m.brachialis; lt, lateral trabecula of sternum; ra, radius; sc, scapula; sf, supracoracoidal
nerve foramen; st, sternum; ul, ulna. Arrow in Bindicates the strongly dorsocaudally projecting articular surfaces at the omal end of the coracoid;
arrow head indicates the well developed dorsal fossa on sternal half of the coracoid.
Wang et al.—Three-dimensional Jehol enantiornithine bird with ovarian follicles (e1054496-7)
Downloaded by [Jingmai K. O’Connor] at 06:41 15 January 2016

relevant view is available). The deltopectoral crest projects dor-
sally and has no cranial deflection; it extends along the proximal
third of the humeral shaft and ends gently, whereas it terminates
abruptly in P. fengningensis and E. leali. The width of the crest is
close to the width of the proximal shaft. In contrast, the deltopec-
toral crest is poorly developed in some other Early Cretaceous
enantiornithines (F. Zhang et al., 2001; Sanz et al., 2002; Z.
Zhou et al., 2005; M. Wang, Zhou, O’Connor, and Zelenkov,
2014), including E. buhleri, L. chaoyangensis, C. lacustris, and
bohaiornithids. The dorsal and ventral condyles are cranially
located; the ventral condyle is nearly transversely oriented and
the dorsal condyle is moderately inclined dorsally. Although the
flexor process is small, the marked curvature of the shaft makes
the distal margin strongly angled dorsodistally. The distal margin
is strongly angled in E. hoyasi, M. cruzyensis, and bohaiornithids,
largely due to the presence of a distally protruding flexor process
(Sanz et al., 2002; Walker et al., 2007; M. Wang, Zhou,
O’Connor, and Zelenkov, 2014).
The ulna is bowed over the proximal two thirds but straight
distally, as in other enantiornithines and most basal birds (Sanz
et al., 2002; Z. Zhou and Zhang, 2003; S. Zhou et al., 2013). The
proximal end bears a weak olecranon process. Visible on the left
ulna, the ventral cotyla slants ventrodistally and the surface is
nearly flat. A distinct groove separating the dorsal and ventral
cotylae as reported in E. leali by Chiappe and Walker (2002) is
present but shallow. Distal to the ventral cotyla, the impression
for the musculus brachialis is weakly developed. The bicipital
tubercle is apparently absent, whereas it is present in some enan-
tiornithines, such as Z. hani and specimen CAGS-IG-O4-CM-
023 (Harris et al., 2006; Z. Zhang et al., 2013). The shaft lacks
any evidence of quill knobs for the attachment of the secondary
feathers as in other enantiornithines and primitive birds
(Chiappe et al., 1999; Chiappe and Walker, 2002; Z. Zhou and
Zhang, 2003). The radius is straight and the humeral cotyla is
weakly convex. The ulnare is triangular with a shallow metacar-
pal incision; a rectangular element displaced between the right
ulna and radius may represent the radiale, but which surface is
exposed is unclear. The alular metacarpal is not fused to the
major metacarpal, typical of Jehol enantiornithines (e.g., Z. hani
and F. xiaotaizicus); an extensor process is absent as in most
enantiornithines (Z. Zhou, 2002; Chiappe and Walker, 2002; Z.
Zhang et al., 2013). The major and minor metacarpals are fused
proximally with the semilunate carpal, but a faint suture between
the proximal ends of metacarpals II and III is visible (Fig. 7).
Distally, metacarpals II and III remain unfused, as in other enan-
tiornithines including Late Cretaceous forms in which the alular
metacarpal is fully fused to the major metacarpal (Chiappe and
Walker, 2002). Also typical of enantiornithines, the minor meta-
carpal projects farther distally than the major metacarpal
(Chiappe and Walker, 2002). Proximally, the ventral surface of
the carpometacarpus is nearly flat and a pisiform process is
absent. The minor metacarpal is weakly bowed craniocaudally
but contacts firmly with the major metacarpal so that the inter-
metacarpal space is almost absent. The manual phalanges are
incomplete and disarticulated with some preserved on each of
the two slabs (Fig. 7). Based on the manual morphology of other
well-preserved Jehol enantiornithines, the preserved phalanges
are identified as follows: the rod-shaped non-ungual phalanx and
the associated claw displaced close to the left radius in the coun-
terslab are interpreted as the second phalanx and claw of the
major digit (Fig. 7); the impression left by the proximal phalanx
of the major digit in the main slab shows that this bone is of nor-
mal shape without craniocaudal expansion as in all enantiorni-
thines; the slender non-ungual phalanx situated close to the left
minor metacarpal in the counterslab is likely the proximal pha-
lanx of the alular digit, which is also preserved in the right hand
on the main slab; two rod-shaped elements overlain by the left
major and minor metacarpals in the counterslab may be addi-
tional phalanges. If these assignments are correct, then the alular
digit would clearly terminate proximal to the distal end of the
major metacarpal, unless a large claw close to the length of the
proximal phalanx of alular digit is present, which has not been
reported so far in other enantiornithines.
Pelvic Girdle
The pelvic elements, ilia, ischia, and pubes, are not fused
with each other, and ilia are separated from the synsacrum
FIGURE 7. Forelimbs of Linyiornis amoena
(STM11-80). A, photograph of right forearm
on the counterslab; B, composite line drawing
of the right forelimb; C, photograph of the left
manus on the main slab; D, line drawing of
the left hand. Abbreviations:al 1, first phalanx
of alular digit; am, alular metacarpal; ma 1,
first phalanx of major digit; mi, minor meta-
carpal; mm, major metacarpal; mm 1, 2, 3,
first, second, and third phalanx of major digit;
mp, manual phalanx; ra, radius; rd, radiale; ul,
ulna; ur, ulnare.
Wang et al.—Three-dimensional Jehol enantiornithine bird with ovarian follicles (e1054496-8)
Downloaded by [Jingmai K. O’Connor] at 06:41 15 January 2016

(Fig. 5). The left and right ilia are exposed in lateral and ven-
tral views, respectively. As in other primitive birds, the prea-
cetabular iliac wing is longer than the postacetabular iliac
wing (Chiappe et al., 1999; Elzanowski, 2002; Z. Zhou and
Zhang, 2003). In lateral view, the preacetabular iliac wing
bears a rounded cranial margin and weakly concave ventral
margin. In ventral view, the lateral margin is concave and
separated from the cranial margin by a distinct hook that
appears to be abraded in the left ilium. A craniocaudally ori-
ented broad convex ridge extends the ventral surface from
the pubic pedicel and nearly reaches the cranial margin
(Fig. 5). The postacetabular iliac wing is triangular in lateral
view and weakly excavated so that the lateral surface is
slightly concave. The dorsal margin is convex and the ventral
margin is very weakly concave; the caudal end is bluntly
tapered. The dorsal margin bears a dorsal antitrochanter
(present in Sinornis santensis Sereno and Rao, 1992; Sereno
et al., 2002) that is continuous with a weak ridge that dorsally
closes the lateral convexity of the postacetabular iliac wing.
Like other enantiornithines, a weak antitrochanter is devel-
oped on the caudodorsal margin of the acetabulum on the
ilium (Chiappe and Walker, 2002). Different from P. martini
and L. chaoyangensis, the pubic peduncle is not mediolater-
ally compressed and hook-like (M. Wang, Zhou, O’Connor,
and Zelenkov, 2014). Instead, it is developed as a ventrally
facing round concave cotyla. The narrower ischiadic peduncle
tapers bluntly and projects caudoventrally, not reaching the
ventral level of the pubic peduncle. The right pubis is only
preserved in its proximal part, which is rod shaped as in
Qiliania graffini Ji, Atterholt, O’Connor, Lamanna, Harris,
Li, You, and Dodson, 2011, whereas it is laterally compressed
in other enantiornithines (Ji et al., 2011; M. Wang, O’Connor,
and Zhou, 2014; M. Wang, Zhou, O’Connor, and Zelenkov,
2014), e.g., L. kurochkini, P. martini,andF. xiaotaizicus.The
mold of the left pubis indicates that the pubis is about twice
as long as the ischium (Fig. 2). As in many other enantiorni-
thines, the pubis is gently curved so that the caudal margin is
concave (Sereno et al., 2002; Z. Zhou et al., 2008; O’Connor
et al., 2011), in contrast with the straight condition in Q. graf-
fini. Distally, a small pubic boot appears to be developed,
preserved on the counterslab but partially overlain by the
left tibiotarsus, preventing precise recognition of its morphol-
ogy. Only the right ischium is complete, exposed in lateral
view. The bone is nearly straight with a tapered caudal end,
unlike the dorsally deflected morphology in some other enan-
tiornithines, e.g., S. santensis, P. martini, L. kurochkini,and
specimen CAGS-IG-04-CM-007 (Sereno et al., 2002;
Lamanna et al., 2006; M. Wang, Zhou, O’Connor, and Zelen-
kov, 2014). The iliac peduncle of the ischium is condylar and
its width is less than half that of the pubic peduncle; the
proximal end of the iliac peduncle bears a lateral projection
that constitutes the ventrocaudal portion of the antitro-
chanter as in S. santensis (Sereno et al., 2002). Although the
right pubis and ischium have been slightly displaced caudally,
the ilioischiadic foramen appears to have been enclosed by
unfused contact with the distinct proximodorsal process of
the ischium, as in S. santensis, Q. graffini,andtheLateCreta-
ceous specimen PVL-4032-3 (Chiappe and Walker, 2002;
Sereno et al., 2002; Ji et al., 2011). The dorsal process is
poorly preserved but appears to be hooked cranially. The
ischium lacks a lateral projecting crest of the kind reported
in S. santensis and Q. graffini (see Sereno et al., 2002; Ji
et al., 2011). The distinct triangular shape of the ischial body
in lateral view may be an artifact of abrasion; a flange of
bone may have extended ventrally, only preserved at the dis-
tal end. This flange is very thin, whereas the preserved por-
tion of the ischium appears to be robust with a triangular
cross section that becomes thicker caudally.
Hind Limb
Both femora are complete and exposed in craniomedial view
(Figs. 2, 5). The femur is approximately 82% of the length of the
tibiotarsus and weakly bowed craniocaudally as in most basal
birds (Z. Zhou and Zhang, 2003; Mayr et al., 2007; Table 1). The
femoral head is separated from the shaft by a short neck. A fossa
for the femoral origin of ligamentum capitis femoris is clearly
not developed on the femoral head (Fig. 5B). The absence of
such a fossa is also seen in other Early Cretaceous enantiorni-
thines with the medial surface of the femoral head exposed
(Sanz et al., 2002; O’Connor et al., 2011; M. Wang, Zhou,
O’Connor, and Zelenkov, 2014), e.g., R. pani, S. cooperorum, C.
lacustris, and P. martini, whereas a distinct fossa is present in
Late Cretaceous enantiornithines, like the specimens from the
El Brete of Argentina (Chiappe and Walker, 2002; Walker and
Dyke, 2009) as well as confuciusornithiforms (Chiappe et al.,
1999). In cranial view, the trochanteric crest projects less proxi-
mally than the femoral head as in specimen CAGS-IG-04-CM-
007 (Lamanna et al., 2006), whereas the opposite condition is
present in F. xiaotaizicus and Martinavis sp. as reported in
Walker and Dyke (2009) and M. Wang, Zhou, O’Connor, and
Zelenkov (2014). The crest extends down the proximal fifth of
the craniolateral surface of the femoral shaft. Distally, a patellar
groove is absent.
The proximal tarsals are fully fused to the distal tibia, forming
a true tibiotarsus. The proximal ends of both tibiotarsi are
exposed in caudal view in the main slab, whereas the distal ends
of the right and left are exposed in, respectively, cranial and lat-
eral view in the counterslab (Fig. 5). Distally, the trochlea carti-
laginis tibialis extends onto the caudal surface but without the
projecting crests seen in basal ornithuromorphs (Clarke and Nor-
ell, 2002). The distal condyles are short proximodistally and
weakly developed anteriorly, possibly due to abrasion; the
medial condyle appears larger and the two taper medially toward
each other; similar to the situation in Q. graffini, the lateral sur-
face of the lateral condyle is weakly excavated (Ji et al., 2011).
The left fibula, preserved in medial view in the main slab, is trian-
gular and rapidly tapered distally; the proximal end is mediolat-
erally compressed and the medial surface is nearly flat but
becomes craniocaudally compressed along the distal part. The
preserved length of the fibula is less than one third that of the
tibiotarsus.
The distal tarsals are fused to the proximal ends of meta-
tarsals II—IV, but the three metatarsals are unfused along
their lengths, typical of enantiornithines (Fig. 8; Chiappe and
Walker, 2002). The medial and lateral cotylae are nearly flat
but are weakly divided by a low ridge. Metatarsals II—IV
are coplanar throughout their lengths as in other enantiorni-
thines (Sanz et al., 2002; Ji et al., 2011; O’Connor, Zhang,
et al., 2013). Metatarsal III is the longest, followed by meta-
tarsal IV, which extends just past the proximal margin of the
metatarsal III trochlea. Metatarsal II is as wide as metatarsal
III and terminates just proximal to the metatarsal III troch-
lea. The metatarsal II trochlea is slightly wider than that of
metatarsal III and is weakly ginglymoid, with the lateral mar-
gin projecting further distally than the medial one, as in
many other enantiornithines (M. Wang, O’Connor, and
Zhou, 2014; M. Wang, Zhou, O’Connor, and Zelenkov,
2014), as well as in Evgenavis nobilis O’Connor, Averianov,
and Zelenkov, 2014, and C. sanctus (O’Connor et al., 2014).
As in F. xiaotaizicus, a distinct tubercle for the attachment of
the m. tibialis cranialis is lacking (M. Wang, O’Connor, and
Zhou, 2014), whereas this structure is present in many Jehol
enantiornithines (Z. Zhou et al., 2008; M. Wang, Zhou,
O’Connor, and Zelenkov, 2014), e.g., P. houi and P. martini.
The right tarsometatarsus is slightly rotated, exposing the lat-
eral surface, revealing that the middle third of the shaft of
Wang et al.—Three-dimensional Jehol enantiornithine bird with ovarian follicles (e1054496-9)
Downloaded by [Jingmai K. O’Connor] at 06:41 15 January 2016

metatarsal II is mediolaterally compressed so that the dorso-
ventral depth of the shaft is greater than the transverse
width, forming a medial plantar crest. Well-developed dorsal
trochlear depressions are visible on metatarsals II and III.
The shaft of metatarsal IV is narrower than metatarsals II
and III and the trochlea is reduced to a single condyle, both
conditions characteristic of Enantiornithes (Chiappe and
Walker, 2002). Metatarsal I is partially exposed on the left;
the lateral surface appears deeply concave to articulate with
the medial surface of metatarsal II, and the distal half
appears deflected. All of the non-ungual pedal phalanges are
weakly spool shaped with deep pits for the collateral liga-
ments. The unguals are recurved and carry laterally projec-
ting ridges underneath the neurovascular sulcus, as in some
other enantiornithines (O’Connor et al., 2009; Wang, Zhou,
and Xu, 2014); the ungual flexor processes are poorly devel-
oped. The pedal digits of the right foot are disarticulated and
overlain by metatarsals and only the hallux is clearly visible;
the third and fourth digits are clearly preserved on the left
side. The proximal phalanx of the hallux is stout and only
longer than the non-ungual phalanges of digit IV. The hallu-
cal ungual is more recurved than those of digits III and IV
and shorter but with greater dorsoventral height. The proxi-
mal phalanx of digit III is the longest non-ungual phalanx,
and the distal two phalanges are subequal in length. The four
non-ungual phalanges of digit IV are shorter than other visi-
ble phalanges, with the proximal three subequal in length
and slightly shorter than the fourth. The digit IV ungual is
reduced and smaller than those of hallux and digit III, a con-
dition present in some enantiornithines (F. Zhang et al.,
2004; Ji et al., 2011; Wang, Zhou, and Xu, 2014), including
Vescornis hebeiensis F. Zhang, Ericson, and Zhou, 2004, P.
chuxiongensis,andQ. graffini.
Soft Tissue
Black carbonized soft tissue remains are preserved ventral to
the vertebral column (Fig. 2B). With the discovery of STM11-80,
these or similar structures have been interpreted as ovarian fol-
licles in eight Jehol birds, including Jeholornis sp. (STM2-51) and
six other enantiornithine specimens (STM29-8, STM10-45,
STM10-4, STM10-12, STM11-80, STM11-121, and STM11-212;
Zheng et al., 2013; O’Connor, Zheng, Wang, et al., 2013). As in
the Jehol birds described by Zheng et al. (2013) and O’Connor,
Zheng, Wang, et al. (2013), the soft tissue structures are pre-
served just ventral to the thoracic column, caudal to the sternum,
and cranial to the pelvis, consistent with the position of the ovary
in living birds (Zheng et al., 2013). STM11-80 is preserved in lat-
eral view, whereas all other specimens are exposed in dorsoven-
tral view; thus, it cannot be confirmed in this specimen if only a
single ovary, the left one, was present as in other fossil birds
(Zheng et al., 2013). The identification of structures such as ovar-
ian soft tissue has been challenged and alternatively interpreted
as food items (Mayr and Manegold, 2013). Compared to
unequivocal food items preserved in other sympatric Jehol birds,
these structures reveal different position and morphology but are
more comparable to ovarian follicles in living birds (O’Connor,
Zheng, and Zhou, 2013). Clearly, independent evidence, possibly
deduced from geochemical studies, is needed to clarify the mech-
anism leading to such rare preservation. The preserved impres-
sions in STM11-80 are circular with a narrow size range, as in
the structures preserved in the specimen Jeholornis sp. STM2-51
and the six other enantiornithine specimens (O’Connor, Zheng,
Wang, et al., 2013). The follicles form a cluster that is two fol-
licles deep and three follicles long; seven follicles can be clearly
identified but the exact number of follicles is obscured by their
overlap. There are fewer follicles preserved than observed in
Jeholornis STM2-51 (an estimated 20 follicles) and enantiorni-
thine STM29-8 (approximately 12) but more than observed in
the other five enantiornithine specimens (which preserved
between two to six follicles). The follicles vary slightly in size,
ranging from 5.6 to 7.1 mm in diameter (6.4 mm in average),
which is generally less than those of Jeholornis STM2-51 but
comparable with other enantiornithines (O’Connor, Zheng,
Wang, et al., 2013; Zheng et al., 2013). The minimal size dispar-
ity among the preserved follicles suggests slow vitellogenesis as
observed in other basal birds, inferred to be a product of the
lower metabolic rate in primitive birds relative to living taxa
(Zheng et al., 2013).
DISCUSSION
Phylogenetic Analysis
The new specimen STM11-80 can be identified as an enan-
tiornithine bird based on the presence of the following features:
pygostyle bearing a pair of ventrolateral processes; ‘Y’-shaped
furcula; proximal margin of the humerus having a concave cen-
tral part bound by proximally elevated adjacent dorsal and ven-
tral regions; minor metacarpal projecting further distally than
the major metacarpal; metatarsal IV reduced (Chiappe and
Walker, 2002). The new specimen can be distinguished from
other enantiornithines by the unique combination of the fol-
lowing characters. The premaxilla is robust, in contrast with
the delicate form in other Jehol enantiornithines. The scapular
shaft is weakly curved sagittally with a blunt distal end, which
among other enantiornithines has only been reported in Z.
houi and F. xiaotaizicus. The ventral half of cranial surface of
bicipital crest is nearly entirely excavated by a circular pit for
muscle attachment, a feature otherwise unknown in other Early
Cretaceous taxa. The deltopectoral crest of humerus is well
developed, in contrast with the narrow condition seen in other
Early Cretaceous enantiornithines. As bohaiornithids, the ster-
nal lateral trabeculae are strongly directed laterally, but they
are parallel to the longitudinal axis of the sternum among
many other enantiornithines. Therefore, we erect the new
taxon, Linyiornis amoena gen. et sp. nov.
FIGURE 8. Photograph of the feet of Linyiornis amoena (STM11-80)
preserved on the counter slab. Abbreviations:dg I–IV, digits I, II, III,
and IV; mt I–IV, metatarsals I–IV; pu, pubis; ti, tibiotarsus.
Wang et al.—Three-dimensional Jehol enantiornithine bird with ovarian follicles (e1054496-10)
Downloaded by [Jingmai K. O’Connor] at 06:41 15 January 2016

To determine the relationship of the new taxon relative to
other enantiornithines, we performed phylogenetic analysis
by adding STM11-80 to a large data matrix of Mesozoic
birds (M. Wang, Zhou, O’Connor, and Zelenkov, 2014; see
Materials and Methods). Phylogenetic analysis produced 135
most parsimonious trees of 1,004 steps, and an additional
round of TBR branch-swapping produced 136 most parsimo-
nious trees (Consistency Index D0.364, Retention Index D
0.677). The strict consensus tree is largely consistent with
previous studies in regards to the placement of major clades
(Z. Zhou and Zhang, 2005; O’Connor et al., 2009; M. Wang,
Zhou, O’Connor, and Zelenkov, 2014; Fig. 9). The interrela-
tionships of Enantiornithes are poorly resolved: P. houi
emerges in the basal most position as in O’Connor (2009),
falling outside a polytomy consisting of P. fengningensis, E.
walkeri, E. keni, and more derived clades; the Longipterygi-
dae is not completely resolved and forms a polytomy with
Iberomesornis romerali Sanz and Bonaparte, 1992, which
together are resolved as the outgroup to the remaining
enantiornithines. The new taxon, L. amoena, is resolved in
a derived position and forms a large polytomy with F. xiao-
taizicus and bohaiornithids; the clade recently recognized by
M. Wang, Zhou, O’Connor, and Zelenkov (2014), the
Bohaiornithidae, is not resolved here.
Implications of Preservation on the Distribution of Certain
Features
The numerous nearly complete and articulated skeletons from
the Jehol Biota and, less commonly, the preservation of soft tis-
sue make it possible to address important issues regarding the
early evolution of enantiornithines. Unfortunately, the known
enantiornithine specimens from this biota, although largely com-
plete and articulated, are crushed and preserved primarily in two
dimensions. This severely limits the amount of morphological
detail that can be discerned, in particular, the anatomical fea-
tures of articular surfaces. Similar to STM11-80, most enantiorni-
thine specimens from some other Early Cretaceous avian faunas,
like Las Hoyas from Spain (Sanz et al., 2002) and the Xiagou
Formation in Gansu Province of China, are less crushed and pre-
served in relatively greater three dimensions. However, enan-
tiornithine specimens from these faunas are far more limited in
number and are only represented by partial skeletons, and no
skull material has yet been discovered (Sanz et al., 2002; You
et al., 2005; Harris et al., 2006; Lamanna et al., 2006; Ji et al.,
2011; M. Wang et al., 2015). In contrast, specimens from the
Late Cretaceous deposits, e.g., the Lecho Formation in Argen-
tina, the Csehb
anya Formation in Hungary, and Maastrichtian
age beds in North America, are very fragmentary, often consist-
ing of isolated incomplete elements but preserved in three
dimensions (Chiappe and Walker, 2002; Walker and Dyke, 2009;
Dyke and O
sl, 2010; Longrich et al., 2011), revealing detailed
anatomical features rarely preserved in Early Cretaceous materi-
als. Consequently, this preservational disparity between known
collections, which are separated by a temporal gap of 30 million
years, prevents detailed comparison and further discussion of
morphological changes during the evolution of Enantiornithes.
Due to their fragmentary nature and thus a large amount of miss-
ing data, few Late Cretaceous specimens have been included in
recent phylogenetic analyses (Z. Zhou et al., 2008; O’Connor
et al., 2009; O’Connor, Zhang, et al., 2013; M. Wang, Zhou,
O’Connor, and Zelenkov, 2014), further preventing a clear
understanding of morphological evolution within this diverse
avian group.
Preservational differences do more than account for large
amounts of missing data and prevent comparison of anatomical
details; the highly compressed style of preservation observed in
Jehol specimens may also potentially modify certain
morphologies and consequently create artificial morphological
disparity between collections. Specimen STM11-80 is unusual
among Jehol enantiornithines in that the bones are better pre-
served in three dimensions. The interiors of the bones appear to
FIGURE 9. Strict consensus tree of 136 most parsimonious tree (Length
D1003 steps, Consistency Index D0.364, Retention Index D0.677) after
second round of TBR branch-swapping search. Bootstrap and Bremer
support values are labeled in normal and italic fonts respectively near
corresponding node.
Wang et al.—Three-dimensional Jehol enantiornithine bird with ovarian follicles (e1054496-11)
Downloaded by [Jingmai K. O’Connor] at 06:41 15 January 2016

be completely filled with silica, exposed where abrasion has
removed the bone surface in some areas (e.g., ventral surfaces of
thoracic vertebrae, neck of left coracoid, mid-shaft of left
humerus and distal end of right metatarsal II; Figs. 6, 7); this
clearly would have enhanced the rigidity of the bones, which led
to the reduced postmortem compression observed in this speci-
men compared to other Jehol specimens. The relatively three-
dimensional preservation of STM11-80 therefore allows a rare
chance to explore the effects of compression on Early Creta-
ceous specimens by comparing morphologies preserved in this
specimen with those observed in other primarily two-dimen-
sional fossils.
The right coracoid appears to be excavated by a broad ster-
nocoracoidal impression, reminiscent of but much shallower
than that of Late Cretaceous taxa, in which the sternal half of
the coracoid is so deeply excavated that the lateral and medial
margins are nearly parallel to each other (Chiappe and Calvo,
1994; Chiappe and Walker, 2002; Walker and Dyke, 2009), e.g.,
E. leali, N. volans,andG. minuta.However,theleftcoracoid
appears to be flat based on following observations: the sternal
half of the coracoid is weakly convex in ventral view, and the
sternal margin is nearly straight. In contrast, in the right cora-
coid of STM11-80 and the three-dimensionally preserved Late
Cretaceous materials, the deep sternocoracoidal impression
makes the coracoid strongly convex ventrally and the sternal
margin concave (Chiappe and Walker, 2002). The different
morphology of the two coracoids in STM11-80 indicates that
the morphology of this element is strongly affected by postmor-
tem compression: the slight lateral preservation of the right
coracoid may exaggerate the depth of the dorsal excavation,
whereas the ventral preservation of the left coracoid, overlain
by the sternum, clearly exaggerates the flatness, making a
dorsal fossa appear absent. A sternocoracoidal impression is
not considered to have a wide distribution among Early Creta-
ceous enantiornithines (O’Connor et al., 2009, 2011; Wang,
O’Connor, and Zhou, 2014). However, evidence from STM11-
80 suggests that this may be a preservational artifact of com-
pression, particularly among Jehol taxa. Clearly, in two-dimen-
sional specimens where the coracoid is exposed in dorsal view,
a shallow sternocoracoidal impression should not be confi-
dently considered absent. We suggest that at least among orni-
thothoracines, the concept of a flat coracoid may be an artifact
of preservation rather than the true morphology (contra Clarke
et al., 2006). A shallow sternocoracoidal impression was proba-
bly present in these birds (e.g., P. martini, Yixianornis grabaui
Z. Zhou and Zhang, 2001, and others). For this reason, we
coded this character as missing for these taxa to incorporate
this uncertainty.
Functional Morphology of the Muscle Attachments
The sternocoracoidal impression on the coracoid of Early Cre-
taceous enantiornithines is better developed than previously rec-
ognized, but comparable deep impressions of the kind present in
Late Cretaceous specimens (e.g., N. volans and E. leali) are
apparently lacking. The sternocoracoidal impression provides
the attachment for the m. sternocoracoideus (Baumel and
Witmer, 1993), which originates from the craniolateral process
of the sternum and the ventral surfaces of the first two sternal
ribs in living birds (Rosser, 1980) and participates in the down-
stroke (Dial et al., 1991; Jackson and Dial, 2011). The sternal
half of the coracoid in Early Cretaceous specimens is generally
wider than that of Late Cretaceous forms, although this may be
exaggerated by compression. Differences in the morphology of
the impression may suggest that the broad, shallow sternocora-
coidal impression of Early Cretaceous forms provided a larger
surface area for the attachment of the m. sternocoracoideus,
whereas Late Cretaceous forms may have compensated for the
limited surface area available on their narrow corpus by increas-
ing the depth of the impression itself. It is noted that deep sterno-
coracoidal impressions are usually associated with increased
pneumatism of the impressions in modern birds (T. Worthy,
pers. comm.), but no pneumatic foramina have been found
within this impression among enantiornithines.
The bicipital crest bears a circular fossa on the ventral half of
its cranial surface, which is considered as a synapomorphy for
Euenantiornithes (Chiappe and Walker, 2002), although this is
no longer valid given that the fossa is absent in some recently
reported taxa (e.g., P. martini; M. Wang, Zhou, O’Connor, and
Zelenkov, 2014). Although consistently suggested to reflect a
muscle insertion, the identity of the muscle has been poorly
explored in previous studies about Mesozoic birds. A similar
structure has been reported in other Mesozoic birds, including
the basal pygostylians C. sanctus and some Mesozoic ornithuro-
morphs, where this fossa is developed on the ventrodistal sur-
face of the crest (Chiappe et al., 1999; Clarke and Norell, 2002;
Clarke, 2004; You et al., 2006; O’Connor, Zhang, et al., 2013).
In living birds, a scar in the approximate position (distal end of
caudal surface of the bicipital crest) is for the attachment of the
m. scapulohumeralis posterior (Howell, 1937; Ashley, 1941;
Ballmann, 1976), which originates from the lateral surface of
the proximal scapular blade and acts to retract the humerus
(Jasinoski et al., 2006; Maxwell and Larsson, 2007). The fossa
varies its position within enantiornithines, and in certain taxa is
located at the distal end of cranial surface of the bicipital crest
(e.g., E. hoyasi and M. cruzyensis), as in some Cretaceous orni-
thuromorphs (e.g., Jianchangornis microdonta Z. Zhou, Zhang,
and Li, 2009, Longicrusavis houi O’Connor, Gao, and Chiappe,
2010, and Ichthyornis dispar Marsh, 1872, as reported by
Clarke, 2004), implying that the position of this fossa is not con-
servative or that in these rather disparate taxa more than one
impressio is represented. There is no insertion scar for the m.
scapulohumeralis posterior reported on the corresponding area
in known enantiornithines and thus we tentatively propose
based on proximity that this pit-shaped scar in enantiornithines
likely represents the attachment of the scapulohumeralis mus-
cle. The hypertrophied shape of this scar may suggest an
enlarged scapulohumeralis in L. amoena relative to most other
enantiornithines.
A distinct fossa for the insertion of the capital ligament is
present on the femoral head in Late Cretaceous enantiorni-
thines and ornithuromorphs (Forster et al., 1996; Chiappe and
Walker, 2002; Clarke and Norell, 2002; Clarke, 2004). The fossa
is located on the medial surface, which is not often exposed in
most two-dimensionally preserved Early Cretaceous specimens.
This fossa is clearly shown to be absent in L. amoena (Fig. 5B),
some Early Cretaceous enantiornithines, including C. lacustris,
and some longipterygids (R. pani and S. cooperorum) and
bohaiornithids (Z. hani and P. martini; Sanz et al., 2002;
O’Connor et al., 2009, 2011; Z. Zhang et al., 2013; M. Wang,
Zhou, O’Connor, and Zelenkov, 2014). This strongly suggests
that this fossa evolved in parallel in Late Cretaceous enantiorni-
thines and ornithuromorphs; alternatively, the fossa may repre-
sent a plesiomorphy of Ornithothoraces that was secondarily
lost in some Early Cretaceous enantiornithine lineages. The
capital ligament (or ligamentum terse) has a broad origin on
the pelvic elements (Bardakos and Villar, 2009); although few
studies have been performed to explore the biomechanical sig-
nificance of the capital ligament in living birds, clinical experi-
ment on fowls found that marked instability resulted from the
rupture of the capital ligament (Duff, 1985). Additionally,
research on mammals and humans has proposed that this liga-
ment contributes to the stability of the hip and restriction of
femur abduction (R
ali
s and McKibbin, 1973; Demange et al.,
2007; Bardakos and Villar, 2009). A stabilized hip joint would
be important to birds during both aerial and terrestrial
Wang et al.—Three-dimensional Jehol enantiornithine bird with ovarian follicles (e1054496-12)
Downloaded by [Jingmai K. O’Connor] at 06:41 15 January 2016

locomotion. This reveals another derived feature that evolved
in parallel to the ornithuromorph lineage as enantiornithines
continued to refine their skeleton for flight during their 65 mil-
lion years of recorded history.
ACKNOWLEDGMENTS
We thank D.H. Li for preparing the specimen and J. Zhang for
photographing. We also thank Z.H. Zhou for discussion and
commenting on the article. We thank Editor T. Worthy and one
anonymous reviewer for their constructive comments to improve
this article. This project is supported by the National Basic
Research Program of China (973 Program, 2012CB821906),
National Natural Science Foundation of China (41502002,
41172020, 41372014, and 41402017), State Key Laboratory of
Palaeobiology and Stratigraphy (Nanjing Institute of Geology
and Palaeontology, CAS, No.133115), National Science Founda-
tion for Fostering Talents in Basic Research of the National Nat-
ural Science Foundation of China (J1210008), and Science and
Technology Development Plan Project of Linyi (201312024).
LITERATURE CITED
Ashley, J. F. 1941. A study of the structure of the humerus in the
Corvidae. Condor 43:184–195.
Ballmann, P. 1976. Fossile Vogel aus dem Neogen der halbinsel Gargano
(Italien), zweiter Teil. Scripta Geologica 38:1–59.
Bardakos, N. V., and R. N. Villar. 2009. The ligamentum teres of the
adult hip. Journal of Bone and Joint Surgery 91:8–15.
Baumel, J. J., and L. M. Witmer. 1993. Osteologia; pp. 45–132 in J. J.
Baumel, A. S. King, J. E. Breazile, H. E. Evans, and J. C. Vanden
Berge (eds.), Handbook of Avian Anatomy: Nomina Anatomica
Avium, second edition. Nuttall Ornithological Club, Cambridge,
U.K.
Benton, M. J., Z. Zhou, P. J. Orr, F. Zhang, and S. L. Kearns. 2008. The
remarkable fossils from the Early Cretaceous Jehol Biota of China
and how they have changed our knowledge of Mesozoic life. Pro-
ceedings of the Geologists’ Association 119:209–228.
Chiappe, L. M. 1995. The phylogenetic position of the Cretaceous birds
of Argentina: Enantiornithes and Patagopteryx deferrariisi. Courier
Forschungsinstitut Senckenberg 181:55–63.
Chiappe, L. M., and J. O. Calvo. 1994. Neuquenornis volans, a new Late
Cretaceous bird (Enantiornithes: Avisauridae) from Patagonia,
Argentina. Journal of Vertebrate Paleontology 14:230–246.
Chiappe, L. M., and C. A. Walker. 2002. Skeletal morphology and sys-
tematics of the Cretaceous Euenantiornithes (Ornithothoraces:
Enantiornithes); pp. 240–267 in L. M. Chiappe and L. M. Witmer
(eds.), Mesozoic Birds: Above the Heads of Dinosaurs. University
of California Press, Berkeley.
Chiappe, L. M., S. A. Ji, and Q. Ji. 2007. Juvenile birds from the Early
Cretaceous of China: implications for enantiornithine ontogeny.
American Museum Novitates 3594:1–46.
Chiappe, L. M., J. P. Lamb, and P. G. P. Ericson. 2002. New enantiorni-
thine bird from the marine Upper Cretaceous of Alabama. Journal
of Vertebrate Paleontology 22:170–174.
Chiappe, L. M., M. A. Norell, and J. Clark. 2001. A new skull of Gobip-
teryx minuta (Aves: Enantiornithes) from the Cretaceous of the
Gobi desert. American Museum Novitates 3346:1–15.
Chiappe, L. M., S. Ji, Q. Ji, and M. A. Norell. 1999. Anatomy and system-
atics of the Confuciusornithidae (Theropoda: Aves) from the Late
Mesozoic of northeastern China. Bulletin of American Museum of
Natural History 242:1–89.
Chiappe, L. M., S. Suzuki, G. J. Dyke, M. Watabe, K. Tsogtbaatar, and R.
Barsbold. 2007. A new Enantiornithine bird from the Late Creta-
ceous of the Gobi desert. Journal of Systematic Palaeontology
5:193–208.
Clarke, J. A. 2004. Morphology, phylogenetic taxonomy, and systematics
of Ichthyornis and Apatornis (Avialae: Ornithurae). Bulletin of the
American Museum of Natural History 286:1–179.
Clarke, J. A., and M. A. Norell. 2002. The morphology and phylogenetic
position of Apsaravis ukhaana from the Late Cretaceous of Mongo-
lia. American Museum Novitates 3387:1–46.
Clarke, J. A., Z. Zhou, and F. Zhang. 2006. Insight into the evolution of
avian flight from a new clade of Early Cretaceous ornithurines from
China and the morphology of Yixianornis grabaui. Journal of Anat-
omy 208:287–308.
Demange, M. K., C. M. S. Kakuda, C. A. M. Pereira, M. H. Sakaki, and
R. F. D. M. E. Albuquerque. 2007. Influence of the femoral head
ligament on hip mechanical function. Acta Ortop
edica Brasileira
15:187–190.
Dial, K. P., G. E. Goslow, and F. A. Jenkins. 1991. The functional anat-
omy of the shoulder in the European starling (Sturnus vulgaris).
Journal of Morphology 207:327–344.
Duff, S. R. I. 1985. Hip instability in young adult, broiler fowls. Journal of
Comparative Pathology 95: 373–382.
Dyke, G., and A. O
sl. 2010. A review of Late Cretaceous fossil birds
from Hungary. Geological Journal 45:434–444.
Elzanowski, A. 1974. Preliminary note on the palaeognathous bird from
the Upper Cretaceous of Mongolia. Acta Palaeontologia Polonica
30:103–109.
Elzanowski, A. 2002. Archaeopterygidae (Upper Jurrasic of Germany);
pp. 129–159 in L. M. Chiappe and L. M. Witmer (eds.), Mesozoic
Birds: Above the Heads of Dinosaurs. University of California
Press, Berkeley.
Forster, C. A., L. M. Chiappe, D. W. Krause, and S. D. Sampson.
1996. The first Cretaceous bird from Madagascar. Nature 382:
532–534.
Goloboff, P. A., J. S. Farris, and K. C. Nixon. 2008. TNT: tree analysis
using new technology, Version 1.1 (Willi Hennig Society Edition).
Program and documentation. Available at www.zmuc.dk/public/phy
logeny/tnt. Accessed December 15, 2015.
Harris, J. D., M. C. Lamanna, H. You, S. Ji, and Q. Ji. 2006. A second
enantiornithean (Aves: Ornithothoraces) wing from the Early Cre-
taceous Xiagou Formation near Changma, Gansu Province, Peo-
ple’s Republic of China. Canadian Journal of Earth Sciences
43:547–554.
He, H., X. Wang, Z. Zhou, F. Wang, A. Boven, G. H. Shi, and R. X. Zhu.
2004. Timing of the Jiufotang Formation (Jehol Group) in Liaoning,
northeastern China, and its implications. Geophysical Research
Letters 31:L12605.
Hou, L., L. Martin, Z. Zhou, and A. Feduccia. 1999. Archaeopteryx to
opposite birds—missing link from the Mesozoic of China. Verte-
brata PalAsiatica 37:88–95.
Hou, L., Z. Zhou, Y. Gu, and H. Zhang. 1995. Confuciusornis sanctus,a
new Late Jurassic sauriurine bird from China. Chinese Science Bul-
letin 40:1545–1551.
Howard, H. 1929. The avifauna of Emeryville shell mound. University of
California Publications in Zoology 32:301–394.
Howell, A. B. 1937. Morphogenesis of the shoulder architecture: Aves.
Auk 54:364–375.
Jackson, B. E., and K. P. Dial. 2011. Scaling of mechanical power output
during burst escape flight in the Corvidae. Journal of Experimental
Biology 214:452–461.
Jasinoski, S. C., A. P. Russell, and P. J. Currie. 2006. An integrative phy-
logenetic and extrapolatory approach to the reconstruction of dro-
maeosaur (Theropoda: Eumaniraptora) shoulder musculature.
Zoological Journal of the Linnean Society 146:301–344.
Ji, S., J. Atterholt, J. K. O’Connor, M. C. Lamanna, J. D. Harris, D. Q. Li,
H. You, and P. Dodson. 2011. A new, three-dimensionally pre-
served enantiornithine bird (Aves: Ornithothoraces) from Gansu
Province, northwestern China. Zoological Journal of the Linnean
Society 162:201–219.
Jin, F., F. Zhang, Z. H. Li, J. Zhang, C. Li, and Zhou, Z. 2008. On the
horizon of Protopteryx and the early vertebrate fossil assemblages
of the Jehol Biota. Chinese Science Bulletin 53:2820–2827.
Lamanna, M. C., H. L. You, J. D. Harris, L. M. Chiappe, S. A. Ji, J. C. L€
u,
and Q. Ji. 2006. A partial skeleton of an enantiornithine bird from
the Early Cretaceous of northwestern China. Acta Palaeontologica
Polonica 51:423–433.
Linnaeus, C. 1758. Systema Naturae per Regna Tria Naturae, Secundum
Classes, Ordines, Genera, Species, cum Characteribus, Differentiis,
Synonymis, Locis. Volume 1: Regnum Animale. Editio decima,
reformata. Laurentii Salvii, Stockholm, 824 pp.
Longrich, N. R., T. Tokaryk, and D. J. Field. 2011. Mass extinction of
birds at the Cretaceous–Paleogene (K–Pg) boundary. Proceedings
of the National Academy of Sciences of the United States of Amer-
ica 108:15253–15257.
Wang et al.—Three-dimensional Jehol enantiornithine bird with ovarian follicles (e1054496-13)
Downloaded by [Jingmai K. O’Connor] at 06:41 15 January 2016

Marsh, O. C. 1872. Notice of a new and remarkable fossil bird. American
Journal of Science 4:344.
Maxwell, E. E., and H. C. E. Larsson. 2007. Osteology and myology of
the wing of the Emu (Dromaius novaehollandiae), and its bearing
on the evolution of vestigial structures. Journal of Morphology
268:423–441.
Mayr, G., and A. Manegold. 2013. Can ovarian follicles fossilize? Nature
499:E1.
Mayr, G., B. Pohl, S. Hartman, and D. S. Peters. 2007. The tenth skeletal
specimen of Archaeopteryx. Zoological Journal of the Linnean Soci-
ety 149:97–116.
Morschhauser, E. M., D. J. Varricchio, C. Gao, J. Liu, X. Wang, X.
Cheng, and Q. Meng. 2009. Anatomy of the Early Cretaceous bird
Rapaxavis pani, a new species from Liaoning Province, China. Jour-
nal of Vertebrate Paleontology 29:545–554.
O’Connor, J. K. 2009. A systematic review of Enantiornithes (Aves:
Ornithothoraces). Ph.D. dissertation, University of Southern Cali-
fornia, Los Angeles, 600 pp.
O’Connor, J. K., and L. M. Chiappe. 2011. A revision of enantiornithine
(Aves: Ornithothoraces) skull morphology. Journal of Systematic
Palaeontology 9:135–157.
O’Connor, J. K., A. O. Averianov, and N. V. Zelenkov. 2014. A confu-
ciusornithiform (Aves, Pygostylia)-like tarsometatarsus from the
Early Cretaceous of Siberia and a discussion of the evolution of
avian hind limb musculature. Journal of Vertebrate Paleontology
34:647–656.
O’Connor, J. K., K. Gao, and L. M. Chiappe. 2010. A new ornithuro-
morph (Aves: Ornithothoraces) bird from the Jehol Group indica-
tive of higher-level diversity. Journal of Vertebrate Paleontology
30:311–321.
O’Connor, J. K., X. Zheng, and Z. Zhou. 2013. Zheng et al. reply. Nature
499:E1.
O’Connor, J. K., L. M. Chiappe, C. Gao, and B. Zhao. 2011. Anatomy of
the Early Cretaceous enantiornithine bird Rapaxavis pani. Acta
Palaentologica Polonica 56:463–475.
O’Connor, J. K., X. Zheng, X. Wang, Y. Wang, and Z. Zhou. 2013. Ovar-
ian follicles shed new light on dinosaur reproduction during the
transition towards birds. National Science Review 1(1):15–17.
O’Connor, J. K., Y. G. Zhang, L. M. Chiappe, Q. Meng, Q. Li, and D.
Liu. 2013. A new enantiornithine from the Yixian Formation with
the first recognized avian enamel specialization. Journal of Verte-
brate Paleontology 33:1–12.
O’Connor, J. K., X. Wang, L. M. Chiappe, C. Gao, Q. Meng, X. Cheng,
and J. Liu. 2009. Phylogenetic support for a specialized clade of Cre-
taceous enantiornithine birds with information from a new species.
Journal of Vertebrate Paleontology 29:188–204.
Pan, Y., J. Sha, Z. Zhou, and F. T. F€
ursich. 2013. The Jehol biota:
definition and distribution of exceptionally preserved relicts of a
continental Early Cretaceous ecosystem. Cretaceous Research
44:30–38.
R
ali
s, Z., and B. McKibbin. 1973. Changes in the shape of the human hip
joint during its development and their relation to its stability. Jour-
nal of Bone and Joint Surgery 55:780–785.
Rosser, B. W. C. 1980. The wing muscles of the American coot (Fulica
americana Gmelin). Canadian Journal of Zoology 58:1758–1773.
Sanz, J., and J. F. Bonaparte. 1992. A new order of birds (Class
Aves) from the Lower Cretaceous of Spain; pp. 39–49 in K. E.
Campbell (ed.), Papers in Avian Paleontology. Honoring Pierce
Brodkorb. Natural History Museum of Los Angeles County,
Los Angeles.
Sanz, J. L., and A. D. Buscalioni. 1992. A new bird from the Early Creta-
ceous of Las Hoyas, Spain. Palaeontology 35:829–845.
Sanz, J. L., B. P. Perez-Moreno, L. M. Chiappe, and A. D. Buscalioni.
2002. The birds from the Lower Cretaceous of Las Hoyas (Province
of Cuenca, Spain); pp. 209–229 in L. M. Chiappe and L. M. Witmer
(eds.), Mesozoic Birds: Above the Heads of Dinosaurs. University
of California Press, Berkeley.
Sanz, J. L., L. M. Chiappe, B. P. P
erez-Moreno, A. D. Buscalioni, J. J.
Moratalla, F. Ortega, and F. J. Poyato-Ariza. 1996. An Early Creta-
ceous bird from Spain and its implications for the evolution of avian
flight. Nature 382:442–445.
Sereno, P. C., and C. Rao. 1992. Early evolution of avian flight and perch-
ing: new evidence from the Lower Cretaceous of China. Science
255:845–848.
Sereno, P. C., C. Rao, and J. Li. 2002. Sinornis santensis (Aves: Enantior-
nithes) from the Early Cretaceous of Northeastern China; pp. 184–
208 in L. M. Chiappe and L. M. Witmer (eds.), Mesozoic Birds:
Above the Heads of Dinosaurs. University of California Press,
Berkeley.
Walker, C. A. 1981. New subclass of birds from the Cretaceous of South
America. Nature 292:51–53.
Walker, C. A., and G. J. Dyke. 2009. Euenantiornithine birds from the
Late Cretaceous of El Brete (Argentina). Irish Journal of Earth Sci-
ences 27:15–62.
Walker, C. A., E. Buffetaut, and G. J. Dyke. 2007. Large euenantiorni-
thine birds from the Cretaceous of southern France, North America
and Argentina. Geological Magazine 144:977–986.
Wang, M. 2014. Taxonomical revision, ontogenetic, ecological and phylo-
genetic analyses of Enantiornithes (Aves: Ornithothoraces) of
China. Ph.D. dissertation, University of Chinese Academy of Scien-
ces, Beijing, 464 pp.
Wang, M., and D. Liu. 2015. Taxonomical reappraisal of Cathayornithi-
dae (Aves: Enantiornithes). Journal of Systematic Palaeontology.
DOI: 10.1080/14772019.2014.994087.
Wang, M., J. K. O’Connor, and Z. Zhou. 2014. A new robust enantiorni-
thine bird from the Lower Cretaceous of China with scansorial
adaptations. Journal of Vertebrate Paleontology 34:657–671.
Wang, M., Z. Zhou, and G. Xu. 2014. The first enantiornithine bird from
the Upper Cretaceous of China. Journal of Vertebrate Paleontology
34:135–145.
Wang, M., Z. Zhou, J. K. O’Connor, and N. V. Zelenkov. 2014. A new
diverse enantiornithine family (Bohaiornithidae fam. nov.) from
the Lower Cretaceous of China with information from two new spe-
cies. Vertebrata Palasiatica 52:31–76.
Wang, M., D. Li, J. K. O’Connor, Z. Zhou, and H. You. 2015. Second
species of enantiornithine bird from the Lower Cretaceous
Changma Basin, northwestern China with implications for the taxo-
nomic diversity of the Changma avifauna. Cretaceous Research
55:56–65.
Wang, X., A. W. A. Kellner, Z. Zhou, and D. de Almeida Campos. 2008.
Discovery of a rare arboreal forest-dwelling flying reptile (Pterosau-
ria, Pterodactyloidea) from China. Proceedings of the National
Academy of Science of the United States of America 105:1983–
1987.
Wang, X., J. K. O’Connor, B. Zhao, L. M. Chiappe, C. Gao, and X.
Cheng. 2010. New species of Enantiornithes (Aves: Ornithothora-
ces) from the Qiaotou Formation in Northern Hebei, China. Acta
Geologica Sinica 84:247–256.
Wang, X., J. K. O’Connor, X. Zheng, M. Wang, H. Hu, and Z. Zhou.
2014. Insights into the evolution of rachis dominated tail feathers
from a new basal enantiornithine (Aves: Ornithothoraces). Biologi-
cal Journal of the Linnean Society 113:805–819.
Wang, Y., J. K. O’Connor, D. Li, and H. You. 2013. Previously unrecog-
nized ornithuromorph bird diversity in the Early Cretaceous
Changma Basin, Gansu Province, northwestern China. PLoS ONE
8:e77693.
Xu, X., X. Zheng, and H. You. 2010. Exceptional dinosaur fossils show
ontogenetic development of early feathers. Nature 464:1338–1341.
You, H., J. K. O’Connor, L. M. Chiappe, and Q. Ji. 2005. A new fossil
bird from the Early Cretaceous of Gansu Province, northwestern
China. Historical Biology 17:7–14.
You,H.,M.C.Lamanna,J.D.Harris,L.M.Chiappe,J.K.
O’Connor, S. Ji, J. L€
u, C. Yuan, D. Li, X. Zhang, K. J. Laco-
vara, P. Dodson, and Q. Ji. 2006. A nearly modern amphibious
bird from the Early Cretaceous of northwestern China. Science
312:1640–1643.
Zhang, F., and Z. Zhou. 2000. A primitive enantiornithine bird and the
origin of feathers. Science 290:1955–1959.
Zhang, F., P. G. P. Ericson, and Z. Zhou. 2004. Description of a
new enantiornithine bird from the Early Cretaceous of Hebei,
northern China. Canadian Journal of Earth Sciences 41:1097–
1107.
Zhang, F., Z. Zhou, and G. J. Dyke. 2006. Feathers and ‘feather-like’
integumentary structures in Liaoning birds and dinosaurs. Geologi-
cal Journal 41:395–404.
Zhang, F., Z. Zhou, L. Hou, and G. Gu. 2001. Early diversification of
birds: evidence from a new opposite bird. Chinese Science Bulletin
46:945–949.
Wang et al.—Three-dimensional Jehol enantiornithine bird with ovarian follicles (e1054496-14)
Downloaded by [Jingmai K. O’Connor] at 06:41 15 January 2016

Zhang, Z., L. M. Chiappe, G. Han, and A. Chinsamy. 2013. A large bird
from the Early Cretaceous of China: new information on the skull
of enantiornithines. Journal of Vertebrate Paleontology 33:1176–
1189.
Zheng, X., L. D. Martin, Z. Zhou, D. A. Burnham, F. Zhang, and D.
Miao. 2011. Fossil evidence of avian crops from the Early Creta-
ceous of China. Proceedings of the National Academy of Sciences
of the United States of America 108:15904–15907.
Zheng, X., J. K. O’Connor, F. Huchzermeyer, X. Wang, Y. Wang, M.
Wang, and Z. Zhou. 2013. Preservation of ovarian follicles reveals
early evolution of avian reproductive behaviour. Nature 495:507–
511.
Zheng, X., J. K. O’Connor, F. Huchzermeyer, X. Wang, Y. Wang, X.
Zhang, and Z. Zhou. 2014. New specimens of Yanornis indicate a
piscivorous diet and modern alimentary canal. PLoS ONE 9:e95036.
Zhou, S., Z. Zhou, and J. K. O’Connor. 2013. Anatomy of the basal
ornithuromorph bird Archaeorhynchus spathula from the Early
Cretaceous of Liaoning, China. Journal of Vertebrate Paleontology
33:141–152.
Zhou, S., Z. Zhou, and J. K. O’Connor. 2014. A new piscivorous orni-
thuromorph from the Jehol Biota. Historical Biology 26:608–618.
Zhou, Z. 2002. A new and primitive enantiornithine bird from the Early
Cretaceous of China. Journal of Vertebrate Paleontology 22:49–57.
Zhou, Z. 2014. The Jehol Biota, an Early Cretaceous terrestrial Lager-
st€
atte: new discoveries and implications. National Science Review
1:543–559.
Zhou, Z., and L. Hou. 2002. The discovery and study of Mesozoic birds in
China; pp. 160–183 in L. M. Chiappe and L. M. Witmer (eds.),
Mesozoic Birds: Above the Heads of Dinosaurs. University of Cali-
fornia Press, Berkeley.
Zhou, Z., and Y. Wang. 2010. Vertebrate diversity of the Jehol Biota as
compared with other lagerst€
atten. Science China Earth Sciences
53:1894–1907.
Zhou, Z., and F. Zhang. 2001. Two new ornithurine birds from the Early
Cretaceous of western Liaoning, China. Chinese Science Bulletin
46:1258–1264.
Zhou, Z., and F. Zhang. 2003. Anatomy of the primitive bird Sapeornis
chaoyangensis from the Early Cretaceous of Liaoning, China. Cana-
dian Journal of Earth Sciences 40:731–747.
Zhou, Z., and F. Zhang. 2005. Discovery of an ornithurine bird and its
implication for Early Cretaceous avian radiation. Proceedings of
the National Academy of Sciences of the United States of America
102:18998–19002.
Zhou, Z., and F. Zhang. 2006a. A beaked basal ornithurine bird (Aves,
Ornithurae) from the Lower Cretaceous of China. Zoologica
Scripta 35:363–373.
Zhou, Z., and F. Zhang. 2006b. Mesozoic birds of China—a synoptic
review. Vertebrata PalAsiatica 44:74–98.
Zhou, Z., L. M. Chiappe, and F. Zhang. 2005. Anatomy of the
early Cretaceous bird Eoenantiornis buhleri (Aves: Enantior-
nithes) from China. Canadian Journal of Earth Sciences
42:1331–1338.
Zhou, Z., J. Clarke, and F. Zhang. 2008. Insight into diversity,
body size and morphological evolution from the largest Early
Cretaceous enantiornithine bird. Journal of Anatomy
212:565–577.
Zhou, Z., F. Jin, and J. Zhang. 1992. Preliminary report on a
Mesozoic Bird from Liaoning, China. Chinese Science Bulletin
37:1365–1368.
Zhou, Z., F. Zhang, and Z. Li. 2009. A new basal ornithurine bird (Jian-
changornis microdonta gen. et sp. nov.) from the Lower Cretaceous
of China. Vertebrata PalAsiatica 47:299–310.
Submitted December 7, 2014; revisions received April 8, 2015;
accepted April 24, 2015.
Handling editor: Trevor Worthy.
Wang et al.—Three-dimensional Jehol enantiornithine bird with ovarian follicles (e1054496-15)
Downloaded by [Jingmai K. O’Connor] at 06:41 15 January 2016