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A new small enantiornithine bird from the Jehol Biota,
with implications for early evolution of avian skull
Min Wanga, Han Hua & Zhiheng Lib
a 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
b Department of Geological Sciences, Jackson School of Geosciences, The University of
Texas at Austin, 1 University Station C1100, Austin, Texas, 78712, USA
Published online: 21 Aug 2015.
To cite this article: Min Wang, Han Hu & Zhiheng Li (2015): A new small enantiornithine bird from the Jehol
Biota, with implications for early evolution of avian skull morphology, Journal of Systematic Palaeontology, DOI:
To link to this article: http://dx.doi.org/10.1080/14772019.2015.1073801
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A new small enantiornithine bird from the Jehol Biota, with implications for early
evolution of avian skull morphology
*, Han Hu
and Zhiheng Li
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;
Department of Geological
Sciences, Jackson School of Geosciences, The University of Texas at Austin, 1 University Station C1100, Austin, Texas, 78712, USA
(Received 12 May 2015; accepted 11 June 2015)
Enantiornithes is the most diverse Mesozoic avian clade. Approximately half of the known global diversity of
Enantiornithes is from the Early Cretaceous Jehol Biota of China. The Jehol enantiornithines are usually articulated and
complete, but the bones are overlain by each other and preserved in two dimensions, severely limiting the number of
cranial characters that can be recognized. Here we describe a new enantiornithine bird, Pterygornis dapingfangensis gen.
et sp. nov., from the Jehol Biota. The new taxon has a unique sternal morphology with an external rostral spine and a pair
of craniolateral processes. Phylogenetic analysis resolves the new taxon in a derived position within Enantiornithes. The
specimen is disarticulated with several exceptionally well-preserved cranial bones, including the jugal and quadratojugal,
morphologies of which remain poorly understood for enantiornithines. Our results indicate that the quadratojugal is an
inverted L-shaped element, morphologically similar to that of more basal birds Archaeopteryx bavarica,Jeholornis prima,
Confuciusornis sanctus and Sapeornis chaoyangensis. Our ﬁndings also illustrate that the quadratojugal underwent large
modiﬁcations with the reduction of the caudoventral and squamosal processes sequentially during early avian evolution,
contributing to the reﬁnement of the cranial kinesis in early birds.
Keywords: Aves; Enantiornithes; jugal; Mesozoic; quadratojugal
Over the last three decades, the Early Cretaceous Jehol
Biota of China has yielded numerous and exceptionally
well-preserved vertebrate fossils, making it an important
atte for deciphering the evolution of
diverse terrestrial vertebrate groups, particularly the early
birds (Zhou et al.2003; Benton et al. 2008;Zhou2014).
Currently, more than 40 avian species have been named
from the Jehol Biota, spanning the whole spectrum of
major Mesozoic avian clades (Zhou & Zhang 2006a;
Zhou & Wang 2010). The Jehol bird-bearing deposits
consist of, in ascending order, the Huajiying, Yixian and
Jiufotang formations, which capture snapshots of over 10
million years of early avian history (130.7120.0 Ma;
Zhou et al. 2003; Jin et al. 2008; Pan et al. 2013). The
large number of complete skeletons, some of which pre-
serve feathers and in rare cases the traces of soft tissues,
have added signiﬁcantly to our knowledge about various
aspects of early avian evolution, including morphology,
biology, ontogeny and phylogeny (Zhang et al. 2006;
Zheng et al. 2011,2012,2013,2014; O’Connor et al.
2013a). More than half of the named Jehol birds are
referred to Enantiornithes, which constitutes the sister
group to Ornithuromorpha the clade giving rise to all
living birds (Zhou & Wang 2010; Wang et al. 2015).
Enantiornithes is the most speciose and successful Meso-
zoic avian clade with worldwide distributions (Chiappe &
Walker 2002; Longrich et al. 2011). The oldest record of
this clade is from the Huajiying Formation (130.7 Ma; He
et al. 2006; Jin et al. 2008), represented by Protopteryx
fengningensis Zhang & Zhou, 2000 and Eopengornis mar-
tini Wang, O’Connor, Zheng, Wang, Hu & Zhou, 2014.
The Jehol birds are usually complete and articulated, but
compressed in two dimensions. Consequently, key features
regarding some skeletal elements, particularly the gracile
skull bones, are obscured by crushed and overlying ele-
ments. Here we report a new enantiornithine bird from the
Jiufotang Formation near Dapingfang Town, Chaoyang
Country, in Liaoning Province, northeastern China.
Although incomplete, the skeleton is disarticulated and sev-
eral cranial elements are exquisitely well preserved in their
entirety, providing morphological information that had pre-
viously been poorly understood.
*Corresponding author. Email: email@example.com
ÓThe Trustees of the Natural History Museum, London 2015. All rights reserved.
Journal of Systematic Palaeontology, 2015
Downloaded by [Institute of Vertebrate Paleontology and Paleoanthropology], [MIN WANG] at 18:36 22 August 2015
CAGS-IG: Chinese Academy of Geological Sciences,
Institute of Geology, Beijing, China; CNU: Capital Normal
University, Beijing, China; LP: Institut d’Estudis Ilerdencs,
Lleida, Spain; IVPP: Institute of Vertebrate Paleontology
and Paleoanthropology, Beijing, China; STM:Shandong
Tianyu Museum of Nature, Shandong, China.
A phylogenetic analysis was performed using the data
matrix modiﬁed from Wang et al. (2014c). In addition to
the new taxon, four recently described enantiornithines
and basal ornithuromorphs were added: Eopengornis mar-
tini (STM24-1), Piscivoravis lii (IVPP V17078) and Itera-
vis hunchzemeyeri (IVPP V18958) were scored from their
holotypes; and the character scorings for Dunhuangia cuii
are after Wang et al. (2015). Rahonavis ostromi was
removed from the matrix, because recent studies have
indicated it was a dromaeosaurid rather than a bird (Norell
et al. 2006; Turner et al. 2007). The modiﬁed data matrix
consists of 60 taxa and 262 morphological characters (see
Online Supplementary Material). The phylogenetic analy-
sis was conducted using the TNT software package
(Goloboff et al. 2008), with the following settings: space
for 10,000 trees was set in the memory as the maxtrees;
all characters were equally weighted, and 33 characters
were treated ordered as in Wang et al. (2014c); an uncon-
strained heuristic search starting with Wagner trees was
used; 1000 replicates of random stepwise addition (branch
swapping: treebisectionreconnection, TBR) were per-
formed and 10 trees were kept at each step; branches were
collapsed to create polytomies if the minimum branch
length equalled zero; Bremer and bootstrap values were
calculated as indices of support; Bremer values were cal-
culated by using Bremer scripts embedded in TNT; and
the bootstrap value was retained by 1000 replicates using
the same setting in the primary search.
Class Aves Linnaeus, 1758
Ornithothoraces Chiappe, 1995
Enantiornithes Walker, 1981
Genus Pterygornis gen. nov.
Type species. Pterygornis dapingfangensis sp. nov.
Diagnosis. As for the type and only species.
Derivation of name. The genus name is derived from the
Latin word ‘pteryg’ (wing), intended to reﬂect its unique
wings with fully ankylosed alular and major metacarpus,
which distinguishes it from other known Early Cretaceous
enantiornithines and suggests reﬁned ﬂight capability.
Pterygornis dapingfangensis sp. nov.
Holotype. IVPP V20729, disarticulated and incomplete
skeleton, representing an adult individual based on the
complete fusion of the compound bones (Fig. 1;Table 1).
Derivation of name. The species name refers to the town
of Dapingfang, where the fossil was collected.
Occurrence and age. Dapingfang Town, Chaoyang
Country, Liaoning Province, northeastern China; Lower
Cretaceous, Jiufotang Formation (He et al. 2004).
Diagnosis. A small, sparrow-sized enantiornithine, dis-
tinguishable from other enantiornithines by the combina-
tion of the following morphologies: surangular with
rostroventrally sloping rostral margin, in contrast to the
rostrodorsal condition amongst other enantiornithines;
omal half shaft of coracoid curved medially; sternum
bearing an external rostral spine and a pair of craniolateral
processes, both features absent in most other enantiorni-
thines, e.g. Eoenantiornis buhleri,Vescornis hebeiensis
and Cathayornis yandica; alular and major metacarpals
fused with each other, a feature unknown in other Early
Cretaceous enantiornithines; and trochlea of metatarsal II
with well-formed ginglymoid articulation and a wide
articular furrow on its planar surface.
Anatomical terminology primarily follows Baumel &
Witmer (1993), using English equivalents of the Latin
terms. For structures not assigned preferred names therein,
this paper follows Howard (1929).
Only the right maxilla is preserved, and is in medial view.
The preserved jugal process is longer than the premaxil-
lary process (Fig. 1). The dorsal process is caudodorsally
directed and is craniocaudally compressed. A single tooth
is preserved in situ in the premaxillary process and it is
inclined rostrally. Caudally, a concavity may have repre-
sented an alveolus. A fragment carrying one tooth is pre-
served close to the maxilla, but the poor preservation
precludes determination of its identity. The nasals are
unfused medially; the bone is broad and tapers caudally,
with a short maxillary process and an elongated premaxil-
lary process. As in Eoenantiornis buhleri (Zhou et al.
2 M. Wang et al.
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2005), the maxillary and premaxillary processes deﬁne a
broad concave rostral notch, deﬁning the caudodorsal
margin of the external naris. The lacrimal is
T-shaped, with the descending ramus longer and stouter
than either the rostral or the caudal ramus. The rostral and
caudal rami are rostroventrally and caudodorsally orien-
tated, respectively. The dorsal margin of the lacrimal is
nearly straight, lacking the concavity reported in some
enantiornithines, including Pengornis houi,Longusunguis
kurochkini and Parabohaiornis martini (O’Connor &
Chiappe 2011; Wang et al. 2014c). Both jugals are pre-
served, and the bones are slender and rod-like (Figs 1,3).
The ventral margin of the maxillary process of the jugal
slopes rostrodorsally as it extends rostrally, reminiscent of
the morphology in Bohaiornis guoi,L. kurochkini and
Enantiornithes indet. LP4450. As in Cathayornis yandica
and B. guoi (Wang et al. 2014c; Wang & Liu 2015), the
caudal end of the jugal curves dorsally and tapers to a
pointed tip. In contrast, the jugal is forked caudally with
postorbital (ascending) and quadratojugal processes as in
some enantiornithines, including Shenqiornis mengi,
L. kurochkini and Enantiornithes indet. LP4450 (Sanz
et al. 1997; O’Connor & Chiappe 2011; Wang et al.
2014c). Two delicate and L-shaped bones are interpreted
as the quadratojugals (Fig. 3). Despite the fact that numer-
ous specimens have been discovered, little is known about
the morphology of this delicate element for enantiorni-
thines. The quadratojugal has been described in the non-
ornithothoracine birds Archaeopteryx bavarica,Sapeornis
chaoyangensis,Confuciusornis sanctus and the basal orni-
thuromorph Archaeorhynchus spathula (Elzanowski &
Wellnhofer 1996; Martin et al. 1998; Zhou & Zhang
2003,2006b). In IVPP V20729, the quadratojugal resem-
bles the morphology of the aforementioned taxa in that
Figure 1. Photograph of the holotype of Pterygornis dapingfangensis gen. et sp. nov. (IVPP V20729).
New Jehol enantiornithine bird 3
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the bone is an inverted L-shape with jugal and squamosal
processes, but it is more delicate. These two processes
deﬁne an acute angle approaching 90. The slender jugal
process is rod-like, and weakly tapers along its length.
The squamosal process is shorter and tapers dorsally. The
caudal end of the quadratojugal weakly protrudes caudally
rather than forming a distinct process as in dromaeosaur-
ids, in which this bone is shaped like an inverted T (Paul
1988;Xu&Wu2001). The right quadrate is exposed in
rostral view (Fig. 3). The orbital process is broken but
leaves its base along the entire height of the quadrate. The
otic process tapers dorsally. Although the dorsal tip is bro-
ken, the otic process is unlikely differentiated into the
prootic and squamosal capitulum as present in Neornithes
(Baumel & Witmer 1993), given that its preserved dorsal
end is considerably narrow. As in S. mengi, the madibular
process is bicondylar and the medial condyle is larger
than the lateral condyle (O’Connor & Chiappe 2011).
Unlike the condition in S. mengi and P. houi (Zhou et al.
2008; O’Connor & Chiappe 2011), the quadrate is imper-
forated by a foramen.
Only the left dentary is preserved in lateral view (Fig. 1).
The bone is typically enantiornithine in that the dorsal
margin is straight and the caudal end slopes caudoventrally
(O’Connor & Chiappe 2011). Four teeth are visible; how-
ever, the rostral end and the portion caudal to the preserved
fourth tooth are overlain by the rib and radius, preventing
the observation of additional teeth if they were present.
Figure 2. Interpretative line drawing of the holotype of Pterygornis dapingfangensis gen. et sp. nov. (IVPP V20729). Abbreviations: al-
1, the ﬁrst phalanx of alular digit; at, atlas; ax, axis; ca, caudal vertebra; cm, carpometacarpus; co, coracoid; cv, cervical vertebra; de,
dentary; dr, dorsal rib; fe, femur; ﬁ, ﬁbula; hu, humerus; ju, jugal; la, lacrimal; ma-1, the ﬁrst phalanx of major digit; mx, maxilla; mt I,
metatarsal I; na, nasal; pa, palatine; pp, pedal phalanx; py, pygostyle; qj, quadratojugal; qu, quadrate; ra, radius; rd, radiale; sc, scapula;
so, scleral ossicle; sp, splenial; sr, sternal rib; st, sternum; su, surangular; sy, synsacrum; ti, tibiotarsus; tm, tarsometatarsus; tv, thoracic
vertebra; ul, ulna; un, ulnare; l, left side; r, right side.
4 M. Wang et al.
The tooth is subconical and has a slightly caudally curved
occlusal tip. The left surangular is preserved in lateral view
(Fig. 3). The bone is robust with straight dorsal and ventral
margins. The rostral end of the surangular slopes
rostroventrally, a condition unknown amongst enantiorni-
thines, in which the rostral end slants rostrodorsally to
accommodate the distal end of the dentary which is caudo-
ventrally tapered (O’Connor & Chiappe 2011). The odd
Figure 3. Cranial elements of Pterygornis dapingfangensis gen. et sp. nov. (IVPP V20729). AD, jugal and quadratojugal; E, F, right
quadrate in rostral view. Abbreviations: al-1, the ﬁrst phalanx of alular digit; an, angular; jpq, jugal process of quadratojugal; ju, jugal;
lcq, lateral condyle of quadrate; mcq, medial condyle of quadrate; mpj, maxillary process of jugal; op, orbital process of quadrate; ot,
otic process of quadrate; pre, prezygapophysis; pos, postzygopophysis; qj, quadratojugal; qu, quadrate; rep, retroarticular process; spq,
squamosal process of quadratojugal; su, surangular; tv, thoracic vertebra.
New Jehol enantiornithine bird 5
morphology of the rostral end of the surangular indicates
that the dentary and surangular do not articulate via a
suture contact but in an overlapping manner in some enan-
tiornithines. No coronoid process is developed, as in many
enantiornithines with a few exceptions, including Rapaxa-
vis pani,L. kurochkini and Fortunguavis xiaotaizicus
(O’Connor et al. 2011;Wanget al. 2014a,c). Caudally, a
caudodorsally directed retroarticular process is developed
as in STM11-80 (Wang et al. in press). The angular is thin
and rod-like, ﬁrmly articulating with the ventral margin of
the surangular. The splenial is preserved in its entirety
(Figs 1,2). Due to imperfect preservation, the morphology
of this bone can only be observed in a few taxa amongst
enantiornithines. As in Vescornis hebeiensis, the splenial is
triangular with a long rostral ramus and a short caudal
ramus (Zhang et al. 2004). The ventral margin is straight,
but the dorsal margin slopes ventrally from its dorsal apex
towards both extremities. An isolated bone close to the left
nasal is tentatively interpreted as the palatine (Fig. 1). The
palatal elements are usually poorly preserved amongst
enantiornithines, particularly in the Jehol specimens that
are often more or less crushed, making their morphology
equivocal. The bone’s morphology resembles that of the
palatine of Gobipteryx minuta in that it is composed of a
wide paddle-like lamina and a slender rod-like portion
(Chiappe et al. 2001). If our interpretation is correct, then
the lamina represents the maxillary process and the rod-
like portion represents the pterygoid wing.
Figure 4. Photograph and line drawing of the atlas and the right coracoid of Pterygornis dapingfangensis gen. et sp. nov. (IVPP
V20729) and the coracoids of selected enantiornithines. A, B, Pterygornis dapingfangensis;C, Eoenantiornis buhleri;D, Vescornis
hebeiensis;E, Shenqiornis mengi. Line drawings in CE are transformed to the right coracoid in cranial view, and are not to scale.
Abbreviations: ac, acoracoid process; at, atlas; cf, condyloid fossa; co, coracoid; cp, costal process; if, incisura fossae; na, neural arch;
vf, vertebral foramen.
6 M. Wang et al.
The vertebral column is disarticulated and incomplete.
Eight cervical vertebrae are recognized including the atlas
and axis. The atlas is preserved in cranial view, and its
left portion is overlain by the right coracoid (Fig. 4). Due
to poor preservation, the morphology of the atlas has only
been described in the holotypes of Pengornis houi (IVPP
V15336) and Zhouornis hani (CNUVB-0903) amongst
enantiornithines (Zhou et al. 2008; Zhang et al. 2013). As
in these two taxa, and living birds, the bone is ring-like.
The neural arch is fused to the centrum. The dorsolateral
portion of the neural arch is wide and laminar, and the
arch narrows ventrally. A small process projecting lat-
erally from the arch is interpreted as the costal process,
also present in P. houi (see Zhou et al. 2008, ﬁg. 3b); how-
ever, this feature is lacking in Z. hani and most living
birds (Baumel & Witmer 1993). The condyloid fossa is
concave and faces craniodorsally, receiving the occipital
condyle of the skull. As in some living birds (e.g. Struthio
camelus and Meleagris gallapavo), the condyloid fossa is
excavated dorsally by the incisura fossae (Baumel &
Witmer 1993; Livezey & Zusi 2006). Therefore, the verte-
bral foramen is rounded with sharply constricted ventral
Figure 5. Photograph and line drawing of the synsacrum and the
left tarsometatarsus of Pterygornis dapingfangensis gen. et sp.
nov. (IVPP V20729). Abbreviations: ca, caudal vertebra; mt
IIV, metatarsal IIV; pc, pedal claw; pp, pedal phalanx; sy,
synsacrum; tr, transverse process; tv, thoracic vertebra.
Figure 6. Sternal morphology of Pterygornis dapingfangensis
gen. et sp. nov. in comparison with other enantiornithines. A, B,
holotype of Pterygornis dapingfangensis (IVPP V20729); C,
Houornis caudatus (modiﬁed from Wang & Liu 2015); D,
New Jehol enantiornithine bird 7
margin. Unfortunately, the corresponding area is overlain
by the odontoid process in the Z. hani holotype, and is
poorly preserved in the P. houi holotype. A short ventral
process is evident, but it is absent in Z. hani (see Zhang
et al. 2013, ﬁg. 3); whether it is present in P. houi cannot
be ascertained due to the poor preservation. The axis is
preserved in craniodorsal view and displaced close to the
right radius (Fig. 1). The prezygapophyses project less
cranially than the odontoid process, and the postzyga-
pophyses are well developed.
The preserved postaxial cervical vertebrae are approxi-
mately equal in length and width. The cranial articular
facet is heterocoelous, but the condition of the caudal
articular facet is obscured by preservation. The cervical
rib and transverse process are ankylosed to form the
enclosed transverse foramen. The spinous process is
absent. The postzygapophyses are longer than the prezy-
gapophyses and project caudally beyond the associated
centrum by a distance that is about half the centrum
length; the epipophyses are located on the postzygapophy-
ses and fail to reach their distal margins.
Seven thoracic vertebrae are discernible (Figs 1,2). The
centrum is longer than wide. The spinous process is tall,
exceeding the height of associated vertebral foramen.
Both the cranial and caudal articular facets are amphicoe-
lous. The vertical height of the cranial articular facet is
greater than half that of the vertebral foramen. A promi-
nent ventral process is present, approaching the height of
the spinous process. The centrum is excavated laterally by
a broad depression and the parapophysis is centrally
located, both conditions characteristic of Enantiornithes
(Chiappe & Walker 2002).
The synsacrum is composed of eight ankylosed sacral
vertebrae, more than in Iberomesornis romeralis (ﬁve),
Rapaxavis pani (six or seven) and Protopteryx fengningen-
sis (seven) (Zhang & Zhou 2000; Sereno et al. 2002;
O’Connor et al. 2011). The bone is exposed in ventral
view (Fig. 5). The cranial vertebral articulation of the ﬁrst
sacral vertebra is deeply concave, and is wider than high,
whereas the caudal articular surface of the synsacrum is
convex. The prezygapophyses of the ﬁrst sacral vertebra
project further cranially than its centrum. The transverse
processes of the cranial ﬁve sacral vertebrae are short, pos-
sibly truncated by postmortem crush, and are coalesced by
the transverse lamina. Comparatively, the transverse pro-
cesses of the caudal three vertebrae are elongated and
becoming increasingly caudally directed, as in other enan-
tiornithines (Wang et al. 2014c).
Six free caudal vertebrae are preserved (Figs 1,5).
Enantiornithes typically have six to eight free caudals
(Sanz et al. 2002; O’Connor et al. 2011; Wang et al.
2014b,c), and thus it is impossible to determine if addi-
tional caudals were present in the complete skeleton. The
transverse processes are caudolaterally directed, and are
Figure 7. Photograph and line drawing of the left carpometacar-
pus (dorsal view) of Pterygornis dapingfangensis gen. et sp.
nov. (IVPP V20729). Abbreviations: am, alular metacarpal;
mam, major metacarpal; mim, minor metacarpal.
Table 1. Selected measurements of the holotype of Pterygornis
dapingfangensis gen. et sp. nov., IVPP V20729.
Element Length (mm)
Alular metacarpal 2.4
Alular digit 1 4.4
Major digit 1 7.1
Metatarsal II 15.1
Metatarsal III 17.0
Metatarsal IV 15.6
Eocathayornis walkeri;E, Parabohaiornis martini (modiﬁed
from Wang et al. 2014a); F, Longipteryx chaoyangensis G,
Eoenantiornis buhleri;H, Cathayornis yandica (modiﬁed from
Wang & Liu 2015). Arrows in C and D indicate the rostral spine,
but whether it is the external or internal cannot be determined
due to preservation; arrow heads in E and H show that the rostral
spine is absent in many other enantiornithines, e.g. P. martini,
L. chaoyangensis,E. buhleri and C. yandica. Line drawings in
CH are not to scale. Abbreviations: clp, craniolateral process;
ers, external rostral spine; lt, lateral trabecula; mt, medial trabec-
ula; st, sternum.
8 M. Wang et al.
longer than their associated centrum width. The prezyga-
pophyses project cranially beyond the cranial articular
facet, whereas the postzygapophyses are absent. As in liv-
ing birds (e.g. Pucrasia macrolopha), the spinous process
is forked at its dorsal end. The pygostyle is fully anky-
losed, with its constituent vertebrae indistinguishable. The
bone is in lateral view and exhibits the dorsal and ventro-
lateral processes, as is typical of most other enantiorni-
thines (Chiappe & Walker 2002). The dorsal process is
restricted cranially, whereas the ventrolateral process
extends nearly along the entire length of the pygostyle.
The ribs are scattered in the slab (Fig. 1).
Both coracoids are exposed in cranial view. The coracoid
is strut-like and lacks the procoracoid process (Fig. 5). As
is the typical condition of enantiornithines, the lateral
margin is convex and the medial margin is concave
(Chiappe & Walker 2002). The strongly convex lateral
margin makes the omal end of the coracoid strongly
curved medially as in Cathayornis yandica,Eocathayor-
nis walkeri and Enantiornithes indet. CAGS-IG-02-0901
(Zhou 2002; Zhou & Hou 2002; You et al. 2005), whereas
the omal end is straight in other Jehol enantiornithines,
including Eoenantiornis buhleri and Vescornis hebeiensis
(Fig. 4). The coracoid expands rapidly from the rod-like
neck and forms the broad sternal end. The sternal margin
is concave, and the sternolateral process is not developed.
A medial groove runs along the medial margin of the
neck; however, whether a supracoracoidal nerve foramen
is present and opens into this groove, as in other enantior-
nithines (Chiappe & Walker 2002; O’Connor 2009), can-
not be determined due to preservation.
The scapulae are straight, lacking the sagittally curved
condition reported in some enantiornithines, including
Fortunguavis xiaotaizicus,Zhouornis hani and Dunhuan-
gia cuii (Zhang et al. 2013; Wang et al. 2014a,2015).
Although the proximal end is largely overlain by other
elements, a broad acromion is present and strongly proj-
The sternum is nearly complete except the xiphial
region (Fig. 6). The sternal body is nearly quadrangular.
Cranially, a small process projects from the middle of the
cranial margin of the sternum, and is continuous laterally
with the external labra of the coracoidal sulci, indicating
that it is homologous to the external rostral spine of mod-
ern birds (Baumel & Witmer 1993). A similar structure is
otherwise known only in Houornis caudatus and E. wal-
keri amongst enantiornithines; however, the poor preser-
vation makes it unclear whether it is the external or the
internal rostral spine in the latter two taxa (Wang & Liu
2015). A pair of craniolateral processes is developed
which are broad and triangular. The craniolateral pro-
cesses have so far been reported only in Concornis
lacustris and possibly Rapaxavis pani within enantiorni-
thines (Sanz et al. 2002; Zheng et al. 2012). As is typical
of enantiornithines, the caudal end of the sternum is
notched by two pairs of trabeculae. The lateral trabecula
is robust, with a fan-shaped distal expansion as in Houor-
nis caudatus and C. yandica. However, C. yandica bears a
short process extending from the proximal end of the lat-
eral trabecula (Wang & Liu 2015), but this feature is
absent in IVPP V20729. The medial trabecula is short,
robust and triangular and curves medially, resembling that
of Bohaiornis guoi (Wang et al. 2014c).
The left and right humeri are exposed in caudal and cra-
nial view, respectively (Fig. 1). The proximal margin of
the humerus is concave centrally, bounded by proximal
convexities dorsally and ventrally, a synapomorphy of
Enantiornithes (Chiappe & Walker 2002). The cranial sur-
face of the bicipital crest is poorly preserved, and thus a
pit-shaped fossa reported in some enantiornithines cannot
be determined (Chiappe & Walker 2002; Walker et al.
2007). Caudally, the ventral tubercle is well projected,
and separated from the caudal convexity of the humeral
head by a deep capital incision. There is no evidence of a
pneumotricipital foramen on the proximocaudal surface,
indicating that a diverticulum of the clavicular air sac pen-
etrating the humerus as in living birds is lacking (Chiappe
& Walker 2002). As in many other Jehol enantiornithines,
the deltopectoral crest is narrow and projects dorsally,
without cranial deﬂection. The ﬂexor process protrudes
well distally, making the distal surface of the humerus
proximodorsally angled. The dorsal and ventral condyles
are cranially located, and the ventral one is poorly pre-
served. As in most other enantiornithines, the caudal sur-
face of the distal end of the humerus is nearly ﬂat and
lacks both humerotricipital and scapulotricipital grooves
(Chiappe & Walker 2002; Wang & Liu 2015).
The ulna is slightly longer than the humerus. The bone
is bowed over the proximal half, but straight distally. The
bicipital tubercle and the brachial impression are appar-
ently lacking. The olecranon process is weakly developed.
The dorsal and ventral cotylae are adjacent and nearly
ﬂat. As in other enantiornithines and more basal birds,
quill knobs for the attachment of the secondary remiges
are absent (Chiappe et al. 1999; Chiappe & Walker 2002;
Zhou & Zhang 2003; Wang et al. 2014c). The radius is
straight and bears a longitudinal groove on its interosseous
surface of the proximal half shaft, a condition characteris-
tic of enantiornithines (Chiappe & Walker 2002). The
ulnare is nearly rectangular and exhibits a shallow meta-
carpal incision. The radiale is square-shaped and smaller
than the ulnare.
The left carpometacarpus is exposed in dorsal view
(Fig. 7). Proximally, the major and minor metacarpals are
New Jehol enantiornithine bird 9
fused to each other and also to the semilunate carpal. The
alular metacarpal is completely fused to the major meta-
carpal as in some Late Cretaceous enantiornithines
(Walker & Dyke 2009). In contrast, this bone, although
ankylosed proximally, is not fused to the major metacar-
pal distally in all known Early Cretaceous enantiorni-
thines. The alular metacarpal has a straight cranial
margin, indicating that an extensor process is absent. The
major metacarpal is rectangular. The minor metacarpal
extends distally beyond the major metacarpal, as is typical
of enantiornithines (Chiappe & Walker 2002). The minor
metacarpal becomes craniocaudally compressed distally,
and ﬁrmly articulates with rather than being fused to the
caudal surface of the major metacarpal. A faint intermeta-
carpal space is developed and is much narrower than the
midshaft width of the minor metacarpal. The manual pha-
langes are disarticulated and incomplete. Two elements
close to the left femur are interpreted as the ﬁrst phalanges
of the major and alular digits, based on comparisons with
complete hands of other enantiornithines. The ﬁrst pha-
lanx of the major digit lacks the craniocaudal expansion
reported in ornithuromorphs; the bone constricts just prox-
imal to its distal articular facet, as in Sulcavis geeorum
and Dunhuangia cuii (O’Connor et al. 2013b; Wang et al.
2015). The ﬁrst phalanx of the alular digit is slender and
shorter than that of the major digit. No pelvic elements
The left and right femora are exposed in cranial and
medial aspects, respectively. The shaft is slightly bowed
craniocaudally and measures about 83% the length of the
tibiotarsus. The femoral head projects medially and is sit-
uated on a short neck. The trochanteric crest extends prox-
imally to the level of the femoral head; comparatively, it
projects further proximally in Fortunguavis xiaotaizicus
and Martinavis sp. (Walker & Dyke 2009; Wang et al.
2014a). The proximal tarsals are fused to the tibia. Both
tibiotarsi are preserved in caudal view. The shaft slightly
expands at the proximal and distal ends. The ﬁbular crest
extends for the proximal third of the tibiotarsus. The prox-
imal end of the ﬁbula is transversely compressed. The
bone rapidly tapers distally to a slender split.
The distal tarsals are fused to the proximal ends of three
major metatarsals, but metatarsals IIIV are unfused dis-
tally, a condition known in most enantiornithines and
more basal birds (Chiappe et al. 1999; Chiappe & Walker
2002; Zhou & Zhang 2003; Wang 2014). Both tarsometa-
tarsi are exposed in plantar view. Metatarsal V is absent
(Fig. 5). The proximal articular surface of the tarsometa-
tarsus is wider than the combined widths of metatarsals
IIIV at the proximal end, and bears a low intercotylar
prominence. The shaft of the tarsometatarsus rapidly
narrows below the proximal margin and expands
mediolaterally when it approaches the trochleae. In plan-
tar view, there is no evidence of a caudal projection or
groove on the proximocaudal surface, indicating that the
hypotarsus of Neornithes is lacking. The proximal two-
thirds of metatarsals II and IV bear plantar projections,
rendering the plantar surface of the tarsometatarsus exca-
vated. Distally, the plantar projections of metatarsals II
and IV are reduced, and the plantar surface of the tarso-
metatarsus is nearly ﬂat. Metatarsal III is the longest,
closely followed by metatarsal IV, and metatarsal II
extends to the proximal margin of the metatarsal III troch-
lea. Metatarsals II and IV are approximately of the same
width; as in other enantiornithines (Chiappe & Walker
2002), metatarsal IV is thinner and its trochlea is reduced
to a single condyle. The metatarsal II trochlea is consider-
ably wider than that of metatarsal III, whereas these troch-
leae are subequal in width in some enantiornithines, such
as Houornis caudatus and Rapaxavis pani. The metatarsal
II trochlea has a well-formed ginglymoid articulation, and
a wide articular furrow is visible on its planar surface.
The lateral rim of the trochlea projects distally slightly
beyond the medial rim, reminiscent of but to a lesser
degree than in Vescornis hebeiensis and F. xiaotaizicus.
Proximal to the trochlea, the plantar surface of metatarsal
II lacks the fossa for metatarsal I. On its distal end, the
medial rim of the metatarsal III trochlea extends further
proximally and plantarly than the lateral rim; the lateral
rim is transversely wider. Both metatarsals I are pre-
served. The bone is straight in lateral view (the right one),
and P-shaped in craniolateral view (the left one) with a
mediocaudally deﬂected distal end for articulation with
the hallux. The pedal digits are disarticulated, making it
impossible to determine their assignments. The non-
ungual phalanges are spool-shaped with well-developed
pits for the attachment of the collateral ligament. The
unguals are recurved and laterally excavated by distinct
Comparison and phylogenetic analysis
IVPP V20729 is referrable to Enantiornithes by sharing
the following synapomorphies with this diverse clade: the
lateral margin of the coracoid is convex; the proximal
margin of the humerus is concave centrally, and rises dor-
sally and ventrally; the radius bears a longitudinal groove
on its interosseous surface; the minor metacarpal projects
further distally than the major metacarpal; the pygostyle
develops a pair of ventrolateral processes; and metatarsal
IV is thinner than metatarsals II and III (Chiappe &
Walker 2002). Compared with other equal-sized enantior-
nithines, IVPP V20729 is uniquely similar to Houornis
caudatus and Eocathayornis walkeri in having a rostral
spine of the sternum. In IVPP V20729, this structure can
10 M. Wang et al.
be identiﬁed as the external rostral spine, but whether it is
the external or the internal one cannot be ascertained in H.
caudatus and E. walkeri due to preservation (Wang & Liu
2015). A similar structure is so far unreported in other
enantiornithines (Zheng et al. 2012; Wang 2014). How-
ever, the sternum of IVPP V20729 differs from that of H.
caudatus and E. walkeri in having a pair of craniolateral
processes (Fig. 6). This feature is otherwise known only
in Concornis lacustris and possibly Rapaxavis pani
amongst enantiornithines (Sanz et al. 2002; O’Connor
et al. 2011). IVPP V20729 differs from these two taxa in
a number of morphological features. In C. lacustris (Sanz
et al. 2002), the craniolateral processes projects from the
proximal end of the lateral trabecula, more caudally posi-
tioned relative to that of IVPP V20729; in addition, meta-
tarsals II and IV are subequal in length in C. lacustris,but
metatarsal IV extends further distally in IVPP V20729.
Rapaxavis pani is characterized by a suite of features, e.g.
the sternal lateral trabecula is forked distally, the manual
digits are reduced and the pygostyle is constricted distally
(O’Connor et al. 2011). All these features are absent in the
new specimen. The complete fusion of the compound
bones, particularly that the alular metacarpal is fused to the
major metacarpal, and the smooth bone surface, indicate
that the specimen was adult at the time of death. Therefore,
the preserved morphologies are not subject to further
ontogenetic variations. The unique sternal morphology dis-
tinguishes the new specimen from the known enantiorni-
thines, supporting the erection of a new taxon, Pterygornis
dapingfangensis gen. et sp. nov.
The fully ankylosed alular and major metacarpals in P.
dapingfangensis are unique and warrant further discus-
sion. The fusion of these two bones is functionally beneﬁ-
cial for powered ﬂight, because the ankylosed alular
metacarpal would have stabilized the alular digit, which
serves the attachment of the bastard wing a critical
structure for slow ﬂight and manoeuvrability (Thomas
1993). However, these two bones are only fused proxi-
mally in other known Early Cretaceous enantiornithines,
and complete fusion is only present in Late Cretaceous
forms (Chiappe & Walker 2002; O’Connor 2009; Wang
et al. 2014c). One possible explanation is that the fusion
between the alular and carpometacarpus completes con-
siderably late amongst Early Cretaceous enantiornithines
such that no specimens ever reached this ontogenetic sta-
tus. However, numerous specimens consistently lack this
feature, particularly individuals with apparent adult osteo-
logical marks, e.g. all bone epiphyses are ossiﬁed, fused
tibiotarsus and tarsometatarsus, and fusion of the cervical
ribs to enclose transverse foramina, making this interpre-
tation implausible. Noticeably, the pelvic elements are
unfused in all known Early Cretaceous enantiornithines,
but are ankylosed in Late Cretaceous taxa (Chiappe &
Walker 2002; Walker & Dyke 2009). All these observa-
tions suggest that there is a general increase in the degree
of fusion in compound bones during the evolution of
Enantiornithes, and that the lack of fusion between the
alular and the major metacarpals in most Early Cretaceous
specimens is not resultant from ontogeny. Therefore, we
propose that the complete fusion of alular and metacarpals
represents an autapomorphy of P. dapingfangensis.
To determine the relationship of P. dapingfangensis rel-
ative to other enantiornithines, we performed a phyloge-
netic analysis using the data matrix modiﬁed from Wang
et al. (2014c; see Methods and Online Supplementary
Material). The phylogenetic analysis produced 370 most
parsimonious trees (MPTs) of 1046 steps, and an addi-
tional round of TBR search yielded 768 MPTs of equal
length. The strict consensus tree is largely resolved and
places P. dapingfangensis in a derived position within
Enantiornithes (Fig. 8). The new topology is generally
consistent with recent studies regarding the placements of
the major clades (Zhou et al. 2014a,b; O’Connor & Zhou
2013; Wang et al. 2014c,2015). In Enantiornithes, a large
polytomy composed of P. fengningensis, the Pengornithi-
dae and Longipterygidae is resolved in a more basal posi-
tion relative to other enantiornithines. The recently
established clades, including the Pengornithidae, Longip-
terygidae and Bohaiornithidae, were recovered here
(O’Connor et al. 2009; Wang et al. 2014c; Wang et al.
2014), but the interrelationships within the latter two
clades were incompletely resolved. Cathayornis yandica,
E. walkeri and P. dapingfangensis form the consecutive
outgroups to a small polytomy consisting of Vescornis
hebeiensis,Neuquenornis volans,Gobipteryx minuta,
Ealulavis hoyasi and the clade [Qiliania grafﬁni CC.
lacustris]. Ornithuromorpha is well resolved. As in previ-
ous studies, Archaeorhynchus spathula was recovered as
the basalmost ornithuromorph (O’Connor & Zhou 2013;
Wang et al. 2014c). The recently described Iteravis
hunchzemeyeri emerged in a more derived position than
other Jehol birds, corroborating the previous result that I.
hunchzemeyeri represents the most derived known Jehol
ornithuromorph (Zhou et al. 2014b).
Implications for early evolution of avian cranial
The known skull materials of Enantiornithes are largely
from the Jehol Biota, with a few reports from the Early
Cretaceous of Spain and the Late Cretaceous of Argentina
and Mongolia. The skull remains from Mongolia are
mostly referred to Gobipteryx minuta, and are preserved
in three dimensions but largely incomplete (Elzanowski
1977; Chiappe et al. 2001); and recently, Kurochkin et al.
(2013) reported an embryonic enantiornithine from Mon-
golia with poorly preserved cranial bones. For skull mate-
rial from Argentina, only one specimen, the holotype of
Neuquenornis volans, preserves the frontal, parietal and
occipital bones (Chiappe & Calvo 1994). The skull
New Jehol enantiornithine bird 11
Figure 8. Cladogram showing the phylogenetic position of Pterygornis dapingfangensis gen. et sp. nov. amongst Mesozoic birds. Boot-
strap and Bremer values are indicated to the corresponding nodes in normal and bold italic formats, respectively.
12 M. Wang et al.
material from Spain is represented by a single specimen
(Enantiornithes indet. LP4450), which is preserved in sim-
ilar condition to the Jehol birds (Sanz et al. 1997). The
Jehol enantiornithines are usually complete and articu-
lated. Unfortunately, the known Jehol enantiornithines are
mostly crushed and preserved primarily in two dimen-
sions. Consequently, the gracile cranial elements are over-
lapping and compressed, severely limiting the number of
morphological features that can be discerned. Therefore,
detailed cranial morphology remains largely unknown for
enantiornithines. However, the cranial bones of IVPP
V20729 are disarticulated and well preserved, allowing a
rare chance to reconstruct the morphology of certain cra-
nial elements, particularly the jugal and quadratojugal
The jugal is usually described as an arched rod-like ele-
ment in enantiornithines, but the morphology of its caudal
end can only be observed in a few taxa, including Shen-
qiornis mengi,Longusunguis kurochkini,Bohaiornis guoi,
Cathayornis yandica and Enantiornithes indet. LP4450,
and exhibits noticeable variations. As in L. kurochkini and
C. yandica, the caudal end of the jugal in the new bird is
unforked, tapered and dorsally curved (Figs 3,9;Wang
et al. 2014c;Wang&Liu2015). In contrast, it is bifur-
cated into the postorbital and quadratojugal processes in S.
mengi and Enantiornithes indet. LP4450 (O’Connor &
in non-ornithothoracine birds, including Archaeopteryx
bavarica,Jeholornis prima,Confuciusornis sanctus and
Sapeornis chaoyangensis (Fig. 9; Elzanowski & Well-
nhofer 1996; Chiappe et al. 1999; Zhou & Zhang 2002,
2003), but the jugal is more robust than in enantiornithines.
Interestingly, the forked jugal is also reported in a basal
ornithuromorph Schizooura lii but absent in sympatric orni-
thuromorph Yixianornis grabaui (Clarke et al. 2006; Zhou
et al. 2012). The forked condition in these early birds is
reminiscent of non-avian dinosaurs, but considerably
reduced, in which the postorbital and the jugal processes
are heavily built and elongated (Fig. 9;Paul1988; Currie
&Zhao1993;Xu&Wu2001; Norell et al. 2006).
Typically, the postorbital process in non-avian dino-
saurs contacts the jugal process of the postorbital, which
together separate the orbit completely from the infratem-
poral fenestra (Barsbold & Osmolska 1999; Weishampel
et al. 2004;Xuet al. 2004,2015). In basal birds such as
A. bavarica and Early Cretaceous taxa, the gracile postor-
bital process of the jugal may have failed to contact the
postorbital (Chiappe et al. 1999; Elzanowski 2002;
O’Connor & Chiappe 2011), although well-preserved
specimens are needed to test this hypothesis. In living
birds, the postorbital process of the jugal and the postor-
bital are absent (Baumel & Witmer 1993; Livezey & Zusi
2006). These ﬁndings indicate that the forked morphology
represents a plesiomorphic condition and that some enan-
tiornithines evolved the unforked jugal morphology in
parallel with ornithuromorphs.
The quadratojugal has only been brieﬂy mentioned in
one enantiornithine. In the holotype of Eocathayornis
Figure 9. Jugal and quadratojugal in dromaeosaurid and basal birds. A, Linheraptor exquisitus (IVPP V16923); B, the seventh skeleton
of Archaeopteryx (modiﬁed from Elzanowski & Wellnhofer 1996); C, Jeholornis prima (IVPP V13274); D, Sapeornis chaoyangensis
(IVPP V13275); E, Confuciusornis sanctus (modiﬁed from Chiappe et al. 1999); F, Archaeorhynchus spathula (IVPP V14287); G,
Schizooura lii (IVPP V16861); H, Pterygornis dapingfangensis (IVPP V20729); I, hypothetical morphological modiﬁcations of
jugalquadratojual in dinosaurbird transition: the caudoventral and squamosal processes of the quadratojugal reduced sequentially
(from T-shaped to L-shaped), and ﬁnally fused to the jugal in more advanced birds; and the caudal end of jugal is changed from forked
to unforked condition. Abbreviations: cvp, caudoventral process of quadratojugal; jpq; jugal process of quadratojugal; ju, jugal; ppj,
postorbital process of jugal; qj, quadratojugal; qpj, quadratojugal process of jugal; sqp, squamosal process of the quadratojugal.
New Jehol enantiornithine bird 13
walkeri, a short bone caudal to the jugal is tentatively
interpreted as the quadratojugal by Zhou (2002). Regard-
less of whether the quadratojugal is correctly identiﬁed in
this study, anatomical features of this element still remain
unknown. In Pterygornis dapingfangensis, the quadratoju-
gal is an inverted L-shaped element with jugal and squa-
mosal processes (Figs 3,9). Both processes are slender
and splint-like, and the jugal process is longer. Similar
morphology is also visible in A. bavarica,S. chaoyangen-
sis,C. sanctus and Archaeorhynchus spathula (Fig. 9;
Elzanowski & Wellnhofer 1996; Martin et al. 1998; Zhou
& Zhang 2006a; Martin 2010). By contrast, amongst the
closest relatives of birds such as the dromaeosaurids, the
bone is shaped like an inverted T with a distinct caudo-
ventral processes extending from the caudal end of the
quadratojugal (Fig. 9; Paul 1988;Xu&Wu2001; Norell
et al. 2006). This process is reduced and the caudal end of
the quadratojugal is blunt in A. bavarica and Early Creta-
ceous birds (Elzanowski & Wellnhofer 1996; Martin et al.
1998; Zhou & Zhang 2003,2006a). In basal birds such as
A. bavarica and Early Cretaceous forms, the squamosal
process of the quadratojugal is short and delicate, possibly
failing to contact the squamosal (Martin et al. 1998; Elza-
nowski 2002), whereas in dromaeosaurids the process is
stout and long, which contacts the quadratojugal process
of the squamosal, forming a completely delimited infra-
temporal fenestra (Paul 1988;Xu&Wu2001;Xuet al.
2015). In living birds, the quadratojugal is fused to the
jugal before hatchling, and the fused jugal bar is unforked
caudally (Baumel & Witmer 1993; Maxwell 2008a,b).
Therefore, all these observations reveal that the quadrato-
jugal underwent large modiﬁcations with the reduction of
the caudoventral and squamosal processes sequentially
during early avian evolution (Fig. 9).
The large modiﬁcations in jugal and quadratojugal reﬂect
the reﬁned cranial kinesis in basal birds relative to their
dinosaurian ancestors. Modern birds characteristically have
a kinetic skull in which the upper jaw or a part of it can be
moved with respect to the brain case, which is signiﬁcant in
the feeding behaviour (Zusi 1993). Such a functional prop-
erty involves a complicated mechanism and the reﬁnement
of the cranial elements (Zusi 1984). Compared with non-
avian dinosaurs, the most conspicuous modiﬁcations in
cranial elements pertaining to the skull kinesis of modern
birds are the absence of the postorbital, and of the
squamosalquadratojugal and the jugalpostorbital artic-
ulations, which enable the quadrate to rotate rostrocaudally,
pushing the jugal bar and the pterygoidpalate bar forward
or backward; in turn, the rostrum can be elevated or
depressed with respect to the brain case (Chiappe et al.
1999,2002). The reduced squamosal process of the quadra-
tojugal and the postorbital process of the jugal in P. daping-
fangensis and more basal birds indicate that reﬁnement for
cranial kinesis occurred early in avian evolution. However,
it is still unclear whether the squamosalquadratojugal
and/or the jugalpostorbital articulations are completely
lost in Early Cretaceous birds due to imperfect preservation,
which is critical to our knowledge regarding the evolution
of cranial kinesis of modern birds.
We thank Jie Zhang for taking the photographs. We are
grateful to two anonymous reviewers for their constructive
comments for improving the manuscript. This project was
founded by the National Science Foundation for Fostering
Talents in Basic Research of the National Natural Science
Foundation of China (J1210008), the National Basic
Research Program of China (973 Program, 2012CB821906)
and the National Natural Science Foundation of China
Supplemental material for this article can be accessed at:
Min Wang http://orcid.org/0000-0001-8506-1213
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