A New Enantiornithine Bird from the Lower Cretaceous of Western Liaoning, China, and Its Implications for Early Avian Evolution

Abstract

Recent studies have blurred the distinctness of two major avian groups: the Enantiornithes, a major radiation of early birds in the Cretaceous, and the Ornithuromorpha, the clade including extant birds. Here we describe a new enantiornithine bird from the Lower Cretaceous Jiufotang Formation of western Liaoning, China, Xiangornis shenmi, gen. et sp. nov., which further reduces the morphological gap between the two groups. Xiangornis shenmi has several enantiornithine features, including a furcula with a significantly elongated hypocleidium, a coracoid with a convex lateral margin, and a minor metacarpal that extends further distally than the major metacarpal. However, it also possesses some derived ornithurine features, such as a short alular metacarpal (about one-sixth as long as the major metacarpal) that is completely fused to the major metacarpal, a large extensor process on the alular metacarpal, proximal and distal fusion between the minor and major metacarpals, and an intermetacarpal space positioned significantly distal to the alular metacarpal. This new find indicates that a carpometacarpal morphology similar to that seen in modern birds probably evolved independently in enantiornithines and appeared earlier than in Ornithuromorpha, and demonstrates that character evolution in early birds was more complex than previously believed.

Full text

This article was downloaded by: [Dongyu Hu]
On: 06 May 2012, At: 17:49
Publisher: Taylor & Francis
Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House,
37-41 Mortimer Street, London W1T 3JH, UK
Journal of Vertebrate Paleontology
Publication details, including instructions for authors and subscription information:
http://www.tandfonline.com/loi/ujvp20
A new enantiornithine bird from the Lower Cretaceous
of Western Liaoning, China, and its implications for
early avian evolution
Dongyu Hu
a
, Xing Xu
a
b
, Lianhai Hou
a
b
& Corwin Sullivan
b
a
Paleontological Institute of Shenyang Normal University, 253 North Huanghe Street,
Shenyang, 110034, China
b
Key Laboratory of Evolutionary Systematics of Vertebrates, Institute of Vertebrate
Paleontology and Paleoanthropology, Chinese Academy of Sciences, 142 Xiwai Street,
Beijing, 100044, China
Available online: 03 May 2012
To cite this article: Dongyu Hu, Xing Xu, Lianhai Hou & Corwin Sullivan (2012): A new enantiornithine bird from the Lower
Cretaceous of Western Liaoning, China, and its implications for early avian evolution, Journal of Vertebrate Paleontology,
32:3, 639-645
To link to this article: http://dx.doi.org/10.1080/02724634.2012.652321
PLEASE SCROLL DOWN FOR ARTICLE
Full terms and conditions of use: http://www.tandfonline.com/page/terms-and-conditions
This article may be used for research, teaching, and private study purposes. Any substantial or systematic
reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to
anyone is expressly forbidden.
The publisher does not give any warranty express or implied or make any representation that the contents
will be complete or accurate or up to date. The accuracy of any instructions, formulae, and drug doses should
be independently verified with primary sources. The publisher shall not be liable for any loss, actions, claims,
proceedings, demand, or costs or damages whatsoever or howsoever caused arising directly or indirectly in
connection with or arising out of the use of this material.

Journal of Vertebrate Paleontology 32(3):639–645, May 2012
© 2012 by the Society of Vertebrate Paleontology
ARTICLE
A NEW ENANTIORNITHINE BIRD FROM THE LOWER CRETACEOUS OF WESTERN
LIAONING, CHINA, AND ITS IMPLICATIONS FOR EARLY AVIAN EVOLUTION
DONGYU HU,
*,1
XING XU,
*,1,2
LIANHAI HOU,
1,2
and CORWIN SULLIVAN
2
1
Paleontological Institute of Shenyang Normal University, 253 North Huanghe Street, Shenyang 110034, China,
hudongyu@synu.edu.cn; houlianhai@synu.edu.cn;
2
Key Laboratory of Evolutionary Systematics of Vertebrates, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese
Academy of Sciences, 142 Xiwai Street, Beijing 100044, China, xingxu@vip.sina.com; csullivan@ivpp.ac.cn
ABSTRACT—Recent studies have blurred the distinctness of two major avian groups: the Enantiornithes, a major radiation
of early birds in the Cretaceous, and the Ornithuromorpha, the clade including extant birds. Here we describe a new enan-
tiornithine bird from the Lower Cretaceous Jiufotang Formation of western Liaoning, China, Xiangornis shenmi, gen. et sp.
nov., which further reduces the morphological gap between the two groups. Xiangornis shenmi has several enantiornithine
features, including a furcula with a significantly elongated hypocleidium, a coracoid with a convex lateral margin, and a mi-
nor metacarpal that extends further distally than the major metacarpal. However, it also possesses some derived ornithurine
features, such as a short alular metacarpal (about one-sixth as long as the major metacarpal) that is completely fused to the
major metacarpal, a large extensor process on the alular metacarpal, proximal and distal fusion between the m inor and major
metacarpals, and an intermetacarpal space positioned significantly distal to the alular metacarpal. This new find indicates that
a carpometacarpal morphology similar to that seen in modern birds probably evolved independently in enantiornithines and
appeared earlier than in Ornithuromorpha, and demonstrates that character evolution in early birds was more complex than
previously believed.
INTRODUCTION
Enantiornithes and Ornithuromorpha represent two major
avian radiations. Enantiornithes is restricted to the Cretaceous,
whereas Ornithuromorpha is the sister taxon to Enantiornithes
and includes all living birds. The two groups were previously con-
sidered to differ in many aspects of their skeletal anatomy. How-
ever, new discoveries of basal birds (Norell and Clarke, 2001;
Clarke and Norell, 2002), particularly some recent finds from
the Lower Cretaceous Jehol Group of Liaoning Province, China
(Zhou and Zhang, 2005, 2006; Zhou et al., 2008), have substan-
tially reduced this morphological gap. During the 2005 field sea-
son, the partial postcranial skeleton of a new enantiornithine bird
was discovered at the Dapingfang Locality, Chaoyang County,
western Liaoning. This new taxon also exhibits some features
normally present in derived ornithurines, further blurring the dis-
tinctness of the two groups.
Institutional Abbreviations—IVPP, Institute of Vertebrate
Paleontology and Paleoanthropology, Beijing, China; PMOL,
Paleontological Museum of Liaoning, China; PVL, Paleontolog
´
ıa
de Vertebrados, Instituto Miguel Lillo, Tucuman, Argentina;
YPM, Peabody Museum of Natural History, Yale University,
New Haven, Connecticut, U.S.A.
SYSTEMATIC PALEONTOLOGY
AVES Linnaeus, 1758
ENANTIORNITHES Walker, 1981
XIANGORNIS SHENMI, gen. et sp. nov.
(Figs. 1, 2)
*
Corresponding authors.
Etymology—Generic name from ‘xiang,’ the Mandarin word
for ‘free flight,’ and ‘ornis,’ the Greek term for bird; specific name
from ‘shenmi,’ the Mandarin word for mysterious.
Holotype—PMOL-AB00245, partial postcranial skeleton in-
cluding nearly complete furcula, left coracoid, left carpometacar-
pus, and first phalanx of the left alular digit; partial sternum, and
left humerus, ulna, and radius. These skeletal elements are dam-
aged to varying degrees.
Horizon and Locality—Jiufotang Formation, Lower Creta-
ceous (Duan et al., 2006); Dapingfang Town, Chaoyang County,
Liaoning Province, China.
Diagnosis—Xiangornis can be referred to Enantiornithes
based on the following synapomorphies: ‘Y’-shaped furcula with
elongated hypocleidium; coracoid with convex lateral margin and
concave dorsal fossa; and minor metacarpal extending distally be-
yond major metacarpal. Differs from other enantiornithines in
having the following unique combination of features: large size;
coracoid with medially curved acrocoracoid process; proximally
convex humeral head; carpometacarpus longer than coracoid
and completely fused both proximally and distally; short alular
metacarpal (about one-sixth of the length of major metacarpal)
completely fused to major metacarpal; large flange-like extensor
process; and intermetacarpal space positioned significantly distal
to the alular metacarpal.
DESCRIPTION AND COMPARISON
Furcula
The furcula is exposed in ventral view (Fig. 1). The furcula
is ‘Y’-shaped, with a long hypocleidium as in other known
enantiornithines (Martin, 1995; Chiappe and Walker, 2002;
Zhou et al., 2008). The interclavicular angle and hypocleidium
are approximately 65 degrees and one-half of the length of the
clavicular r amus, respectively. This interclavicular angle is wider
639
Downloaded by [Dongyu Hu] at 17:49 06 May 2012

640 JOURNAL OF VERTEBRATE PALEONTOLOGY, VOL. 32, NO. 3, 2012
FIGURE 1. Holotype specimen of Xiangornis shenmi, gen. et sp. nov. (PMOL-AB00245). A, photograph; B, line drawing. Abbreviations: fu, furcula;
hy, hypocleidium; lcm, left carpometacarpus; lco, left coracoid; lhu, left humerus; lra, left radius; lul, left ulna; st, sternum; I-1, first phalanx of the alular
digit. Scale bars equal 20 mm.
than in the furculae of most known enantiornithines, particularly
the small taxa Iberomesornis (Sanz and Bonaparte, 1992),
Concornis (Sanz et al., 1995), Eoalulavis (Sanz et al., 2002),
Noguerornis (Chiappe and Lacasa-Ruiz, 2002), Longirostravis
(Hou et al., 2004), Vescornis (Zhang et al., 2004), and Shenqior-
nis (Wang et al., 2010). Although a hypocleidium is also present
in the ornithuromorph bird Hongshanornis (Zhou and Zhang,
2005) and the more basal bird Sapeornis (Zhou and Zhang,
2003), the furcula is ‘U’-shaped or boomerang-shaped in both
cases and bears only a short hypocleidium in Hongshanornis
(Zhou and Zhang, 2005). The clavicular ramus is mediolaterally
broad and dorsoventrally compressed as in the enantiornithines
Iberomesornis (Sanz and Bonaparte, 1992), Elsornis (Chiappe et
al., 2007), and Pengornis (Zhou et al., 2008), whereas the medial
surface of each clavicular ramus gradually widens towards the
omal end in the enantiornithines Longipteryx (Zhang et al., 2001)
and Bohaiornis (Hu et al., 2011). However, the lateral margin
of the clavicular ramus is prominently convex in Iberomesornis
and Pengornis, but relatively straight in Elsornis and Xiangornis.
The clavicular ramus appears to taper at the omal end, in
contrast to the laterally expanded omal end seen in Bohaiornis
(Hu et al., 2011).
Downloaded by [Dongyu Hu] at 17:49 06 May 2012

HU ET AL.—NEW CRETACEOUS BIRD FROM CHINA 641
Coracoid
The left coracoid is exposed in dorsal view. The coracoid is
strut-like with a length/width ratio of 2.1; it is proportionally
shorter than the coracoids of the enantiornithines Concornis
(Sanz et al., 1995), Eoalulavis (Sanz et al., 2002), and Enantiornis
(Walker and Dyke, 2010), in all of which the equivalent ratio is
more than 2.5. Although the more basal bird Confuciusornis has
also a strut-like coracoid, it has a length/width ratio of only 1.7
(Zhang et al., 2009) and is fused to the scapula. Proximally, the
acrocoracoid process is prominent, and has a considerable medial
curvature and a broad sulcus for the M. supracoracoideus, in
contrast to a small and straight process in most known enantior-
nithines (Martin, 1995; Chiappe and Walker, 2002; Zhou et al.,
2008). The acrocoracoid process is developed to a similar extent
only in relatively derived ornithuromorphs such as Gansus (You
et al., 2006) and Ichthyornis (Clarke, 2004). The presence of a
procoracoid process and a distinct supracoracoid nerve foramen
cannot be confirmed because the coracoid is damaged, but the
latter feature is probably located in a depressed area adjacent
to the medial margin. The sternal third of the lateral margin of
the coracoid is significantly convex as in the enantiornithines
Concornis (Sanz et al., 1995), Eoalulavis (Sanz et al., 2002), El-
sornis (Chiappe et al., 2007), and Pengornis (Zhou et al., 2008),
rather than slightly convex or straight as in the enantiornithines
Iberomesornis (Sanz and Bonaparte, 1992), Longipteryx (Zhang
et al., 2001), Rapaxavis (Morschhauser et al., 2009), and Bohaior-
nis (Hu et al., 2011). However, most known ornithuromorphs
other than Hongshanornis have a concave lateral margin of
the coracoid (Clarke et al., 2006). The lateral-most margin is
more depressed as in Pengornis (Zhou et al., 2008), suggesting
the presence of an incipient lateral process. The sternal third
of the dorsal surface of the coracoid clearly forms a fossa for
the M. sternocoracoideus as in most known enantiornithines
(Martin 1995; Chiappe and Walker, 2002; Chiappe et al., 2007),
in contrast to the flat or convex surface present in most known
ornithuromorphs (Clarke et al., 2006).
Sternum
The preserved portion of the sternum appears approximately
anchor-shaped, and a rounded segment of the margin is signifi-
cantly thickened compared with the rest of the bone. If this frag-
ment is interpreted as the anterior portion, then the sternum is
similar to those of most known enantiornithines such as Eoenan-
tiornis (Zhou et al., 2005) and Bohaiornis (Hu et al., 2011) in hav-
ing a rounded and thickened anterior margin for the articulation
with the coracoid. The posterior margin of the sternum also ap-
pears to be rounded in some ornithuromorphs such as Songlin-
gornis (Hou, 1997), Yanornis,andYixianornis (Zhou and Zhang,
2001). However, the posterior half of the sternum normally bears
a carina in basal birds, and the posterior margin is not especially
thick. The absence of a carina and the thickened margin of the
preserved sternal fragment of Xiangornis probably indicate that
the fragment is anterior. A suture runs along the midline of the
sternal fragment, suggesting that the left and right plates of the
sternum are incompletely fused together.
Humerus
The proximal half of the left humerus is present, and its
anterior surface is exposed. The head of the humerus obvi-
ously projects further proximally than the deltopectoral crest,
as in most ornithuromorphs such as Hongshanornis and Archae-
orhynchus (Zhou and Zhang, 2005, 2006) and the enantiornithine
Pengornis (Zhou et al., 2008), whereas the central portion of
its proximal margin is concave in most known enantiornithines,
such as Bohaiornis (Hu et al., 2011). The humeral head is sepa-
rated by a shallow notch from the bicipital crest, which is prox-
imodistally elongated and projects slightly ventrally. An incom-
pletely preserved transverse groove, probably representing the
sulcus ligamentum transversum, occurs near the proximal end of
the bicipital crest. The deltopectoral crest is proximodistally long,
and about as wide as the humeral shaft. It is not perforated, in
contrast to the condition in the more basal birds Confuciusornis
(Martin et al., 1998) and Sapeornis (Zhou and Zhang, 2003).
Ulna and Radius
The distal halves of the left ulna and radius are preserved, but
little can be said about their morphology except that the radius is
much more slender than the ulna.
Manus
Most of the left manus is preserved, although the proximal
carpals and most of the phalanges are absent. The semilunate
carpal and metacarpals are completely fused both proximally and
distally to form a carpometacarpus (Fig. 2). This element is ex-
posed in ventral view. Xiangornis resembles ornithuromorphs,
but differs from other enantiornithines, in that the carpometacar-
pus is longer than the coracoid (Table 1). The semilunate carpal
is laterally positioned, with a small contact with the dorsal por-
tion of the proximal surface of the alular metacarpal. The carpal
trochlea is strongly convex transversely.
The alular metacarpal is only about one-sixth as long as the ma-
jor metacarpal, approaching the condition in the Late Cretaceous
enantiornithine Martinavis
(Walker and Dyke, 2010) and the de-
rived ornithurine Iaceornis (Clarke, 2004). The alular metacarpal
is about one-fourth of the length of the major metacarpal in
most Early Cretaceous ornithothoracines, including Bohaiornis
(Hu et al., 2011) and Yanornis (Zhou and Zhang, 2001). In Xi-
angornis the alular metacarpal is completely fused to the ma-
jor metacarpal as in the Late Cretaceous enantiornithines Enan-
tiornis and Martinavis (Walker and Dyke, 2010) and derived
ornithurines such as Apsaravis (Clarke and Norell, 2002) and
Ichthyornis (Clarke, 2004), but a short groove is visible along the
distal part of the suture between the two metacarpals. In other
Early Cretaceous ornithothoracines, including Yanornis and Yix-
ianornis (Zhou and Zhang, 2001), the alular metacarpal is not
fused to the major metacarpal distally. The alular metacarpal has
a weakly ginglymoid distal end; the medial condyle is much nar-
rower transversely than the lateral condyle, but extends further
distally. The most unusual feature of the alular metacarpal is the
presence of a flange-like extensor process, a feature otherwise
unknown in Early Cretaceous birds and Late Cretaceous enan-
tiornithines. The process is formed by the rounded, prominent
TABLE 1. Measurements (mm) and proportions of the coracoid, car-
pometacarpus, and first phalanx of the alular digit of Xiangornis, gen. et
sp. nov. (PMOL -AB00245) compared with those of some early birds.
Co Cm I-1 Co/Cm I-1/Cm
Enantiornithes
Eoenantiornis (IVPP
V11537)
15.813.85.41.14 0.39
Bohaiornis (LPM-B00167) 23 22.79.51.01 0.42
Pengornis (IVPP V15336) 37.934.3— 1.10 —
Xiangornis
(PMOL–AB00245)
35 38.515.20.92 0.39
Ornithuromorpha
Yanornis (IVPP V12558) 30 35 17 0.86 0.49
Yixianornis (IVPP V12631) 23 25 11 0.92 0.44
Jianchangornis (IVPP
V16708)
32 36 29 0.88 0.80
Abbreviations: Co, coracoid; Cm, carpometacarpus; I-1, first phalanx of
the alular digit; —, missing values.
Downloaded by [Dongyu Hu] at 17:49 06 May 2012

642 JOURNAL OF VERTEBRATE PALEONTOLOGY, VOL. 32, NO. 3, 2012
FIGURE 2. Close-up photograph and line drawing of left carpometacarpus of Xiangornis shenmi, gen. et sp. nov. (PMOL-AB00245). Abbreviations:
daf, distal articular facet (of alular metacarpal); ep, extensor process; pp, pisiform process. Scale bars equal 10 mm.
proximomedial corner of the metacarpal plus an additional con-
vexity located further distally on the medial edge. There is neither
a sharp distinction between the extensor process and the shaft
of the alular metacarpal nor a sharp proximal embayment be-
tween the extensor process and the trochlear articular s urface of
the carpometacarpus, in contrast to modern birds and to the or-
nithurines Apsaravis (Clarke and Norell, 2002) and Ichthyornis
(Clarke, 2004). Its length covers about four-fifths of the medial
margin of the alular metacarpal and its width is slightly greater
than that of the distal end of the bone.
The major metacarpal is robust and slightly bowed laterally,
but this might be a preservational artifact. A prominence that
probably represents the pisiform process is present on the bound-
ary with the alular metacarpal and has the form of an approxi-
mately longitudinal crest, but only the medial surface is clearly
preserved. A distinct ridge arises from near its midpoint and ex-
tends transversely to the proximal end of the extensor process.
A deep fossa containing a shallow muscle scar is present on the
proximal surface of this ridge.
The minor metacarpal is strongly bowed laterally and extends
distally beyond the major metacarpal as in other known enan-
tiornithine birds (Martin, 1995; Chiappe and Walker, 2002; Zhou
et al., 2008). It is fused to the major metacarpal both proximally
and over a short interval near the distal end, in contrast to only
the proximal fusion in all known enantiornithines. The proximal
and distal fusion of the major and minor metacarpals is present
only in the early ornithuromorphs Yanornis and Yixianornis
(Zhou and Zhang, 2001) and most derived ornithurines (Clarke,
2004), and the major and minor metacarpals of all known enan-
tiornithines exhibit proximal fusion. A narrow intermetacarpal
space is present between the two regions of fusion, likely termi-
nating proximally at a level considerably distal to the end of the
alular metacarpal as in modern birds.
The one preserved phalanx is identified as manual phalanx
I-1 (Fig. 1). This phalanx is about 39% of the length of the
carpometacarpus, comparable to the equivalent value in most
known enantiornithines. In most basal ornithuromorphs from
Liaoning, however, phalanx I-1 is proportionally longer (Table
1). In Xiangornis the proximal end of phalanx I-1 is much deeper
than the distal end, and the distal part of the phalanx has a consid-
erable ventral curvature. The distal end appears not to be ging-
lymoid, but is robust enough to indicate the presence of an addi-
tional phalanx of the alular digit.
DISCUSSION
Phylogenetic Position
Xiangornis displays the following enantiornithine synapomor-
phies: ‘Y’-shaped furcula with long hypocleidium; coracoid with
convex lateral margin and concave dorsal fossa; and minor
metacarpal extending distally beyond major metacarpal (Martin
1995; Chiappe, 2002; Chiappe and Walker, 2002). These features
strongly support the identification of Xiangornis as an enantior-
nithine. However, Xiangornis also displays the f ollowing charac-
ter states previously considered diagnostic of Ornithuromorpha:
coracoid with medially curved acrocoracoid process; proximally
convex humeral head; carpometacarpus completely fused both
proximally and distally; short alular metacarpal (about one-sixth
of the length of the major metacarpal) completely fused to ma-
jor metacarpal; large extensor process; and intermetacarpal space
positioned significantly distal to alular metacarpal. The holotype
of Xiangornis shenmi is the first specimen to display this combi-
nation of features.
We conducted a phylogenetic analysis using the software pack-
age TNT (Goloboff et al., 2008) on a recently published data set
(Zhou et al., 2008) with Xiangornis added, and our analysis con-
firms the placement of Xiangornis within Enantiornithes (Fig.
3A). It is notable that the analysis places Protopteryx (Zhang
and Zhou, 2000) in a position basal to the Enantiornithine-
Ornithuromorph split. Accordingly, the morphological evidence
provided by Xiangornis further weakens the support for a
monophyletic Enantiornithes, at least as traditionally conceived
(Norell and Clarke, 2001; Zhou et al., 2008). Four character
states were optimized by our analysis as unambiguous synapo-
morphies of a monophyletic Enantiornithes, including humeral
distal margin angling strongly ventrally (124.1), ulnar distal end
with dorsal condyle significantly extended on posterior margin
(134.1), metacarpal III extending further distally than metacarpal
Downloaded by [Dongyu Hu] at 17:49 06 May 2012

HU ET AL.—NEW CRETACEOUS BIRD FROM CHINA 643
FIGURE 3. A, strict consensus tree illustrating the phylogenetic position of Xiangornis shenmi, gen. et sp. nov. (PMOL-AB00245). Phylogenetic
analysis was based on the data matrix f rom Zhou et al. (2008), consisting of 205 morphological characters (39 characters are ordered) in 30 taxa
including the newly added Xiangornis (see Supplementary Information S1 and S2; available online a t www.tandfonline.com/UJVP). The data matrix
was analyzed using a traditional search strategy in TNT, with default settings apart from the following: 10,000 maximum trees in memory and 1000
replications. Three most parsimonious trees (tree length = 478 steps, consistency index [CI] = 0.55, retention index [RI] = 0.79) were recovered by the
analysis, and their strict consensus is shown here. B, strict consensus resulting from the same phylogenetic analysis using the original matrix excluding
Xiangornis (tree length = 469 steps, CI = 0.56, RI = 0.80). Bremer and bootstrap support values computed in TNT for the nodes of the consensus
trees were labeled adjacent to their respective nodes to the left and right.
Downloaded by [Dongyu Hu] at 17:49 06 May 2012

644 JOURNAL OF VERTEBRATE PALEONTOLOGY, VOL. 32, NO. 3, 2012
FIGURE 4. Comparison of carpometacarpii of A, Xiangornis shenmi, gen. et sp. nov. (PMOL-AB00245); B, Early Cretaceous enantiornithine
Cathayornis (IVPP V9769) (Zhou and Hou, 2002); C, Late Cretaceous enantiornithine Enantiornis leali (PVL-4049) (Chiappe and Walker, 2002); D,
Early Cretaceous ornithuromorph Yixianornis (IVPP V12631); E, Late Cretaceous ornithurine Ichthyornis (YPM 1724) (Clarke, 2004); and F, modern
bird Apterornis defossor. Abbreviations: daf, distal articular surface; ep, extensor process; pp, pisiform process. Not to scale.
II (150.1), and manual phalanx II-1 longer than II-2 (153.1). Each
of these character states is also convergently present in some
other taxa, however. Re-running the analysis with Xiangornis ex-
cluded, a monophyletic Enantiornithes including Protopteryx was
recovered (Fig. 3B). The unambiguous synapomorphies support-
ing this clade include furcula with a long hypocleidium (82.2), fur-
cula laterally excavated (83.1), and scapular articular surface of
coracoid convex (87.1), with the last two character states being
unique to the group. We also used TNT to run Bremer support
and bootstrap analysis (1000 replicates) on the two matrices with
and without Xiangornis. Both the bootstrap and Bremer values
for Enantiornithes and Ornithuromorpha are lower in the analy-
sis with Xiangornis (Fig. 3A, B), and therefore confirm that the
discovery of Xiangornis has weakened the support for the mono-
phyly of both Enantiornithes and Ornithuromorpha.
Xiangornis is very similar to Pengornis (Zhou et al., 2008), in
size and various other morphological features such as the prox-
imally convex humeral head and the prominently convex lateral
margin of the coracoid, and both are from the same locality and
horizon. However, Xiangornis is clearly different from Pengornis
in having a straight lateral margin of the clavicular ramus, a dis-
tinctly curved acrocoracoid process, a carpometacarpus exceed-
ing the length of the coracoid, and a crest-like pisiform process
on the ventral surface of the carpometacarpus between the alular
and major metacarpals.
Manus Evolution
The discovery of Xiangornis suggests that a derived,
ornithurine-type carpometacarpus evolved independently within
Enantiornithines, and in fact appeared earlier in this group than
in Ornithuromorpha (Fig. 4). The large extensor process and
high degree of fusion in the carpometacarpus of Xiangornis are
also potential indicators of a degree of flight adaptation ex-
ceeding that seen in other enantiornithines. Fusion of the car-
pometacarpus presumably strengthens the manus against aero-
dynamic forces. In extant birds, the extensor process serves as a
point of attachment for the M. extensor metacarpi radialis and
for a branch of the propatagial ligament that extends from the
shoulder region to the wrist within the leading edge of the wing,
joined prior to its insertion by a tendon from the biceps (Vazquez,
1994). The M. extensor metacarpi radialis is the primary muscle
involved in adduction (‘extension’) of the avian wrist joint.
Ostrom (1976) proposed that a large extensor process might
either reduce the amount of energy required to counteract the
force of the airstream that tends to flex or fold the wing extrem-
ity, or allow rapid unfolding of the wing. The former function
is highly plausible. The extensor process would increase the mo-
ment arms of the propatagial ligament and M. extensor metacarpi
radialis with respect to adduction of the wrist, allowing them to
generate large torques that would resist the tendency of drag on
the feathered manus to abduct the wrist and collapse the wing.
However, the increased moment arm would conversely reduce
the ability of the M. extensor metacarpi radialis to bring about
rapid r otation at the wrist joint, so the large extensor process seen
in Xiangornis and derived ornithurines cannot be interpreted as
an adaptation for rapid wing unfolding. T he large extensor pro-
cess and distal fusion between the major and minor metacarpals
both seem to relate, in different ways, to stabilization of the dis-
tal wing during flight, implying that Xiangornis was converging
on ornithurine birds in some functionally significant aspects of its
wing structure.
ACKNOWLEDGMENTS
We thank the field crew of Shenyang Normal University for
collecting and preparing this specimen, R. Li for making these
drawings, P. O’Connor, R. L. Nydam, and A. Michel for their
edits, and G. J. Dyke and an anonymous reviewer for their re-
view and constructive suggestions. This study was supported by
the National Natural Science Foundation of China (41172026),
Natural Science Foundation of Liaoning Province, and Scientific
Research Fund of Education Bureau of Liaoning Province (grant
no. 2008S214). X. Xu’s work was also supported by the Chinese
Academy of Sciences.
LITERATURE CITED
Chiappe, L. M. 2002. Early bird phylogeny: problems and solutions;
pp. 448–472 in L. M. Chiappe and L. M. Witmer (eds.), Meso-
zoic Birds: Above the Heads of Dinosaurs. University of California
Press, Berkeley, California.
Chiappe, L. M., and A. Lacasa-Ruiz. 2002. Noguerornis gonzalezi (Aves:
Ornithothoraces) from the Early Cretaceous of Spain; pp. 230–239
in L. M. Chiappe and L. M. Witmer (eds.), Mesozoic Birds: Above
Downloaded by [Dongyu Hu] at 17:49 06 May 2012

HU ET AL.—NEW CRETACEOUS BIRD FROM CHINA 645
the Heads of Dinosaurs. University of California Press, Berkeley,
California.
Chiappe, L. M., and C. A. Walker. 2002. Skeletal morphology and sys-
tematics of the Cretaceous Enantiornithes (Ornithothoraces: Enan-
tiornithes); pp. 240–267 in L. M. Chiappe and L. M. Witmer (eds.)
Mesozoic Birds: Above the Heads of Dinosaurs. University of Cali-
fornia Press, Berkeley, California.
Chiappe, L. M., S. Suzuki, G. J. Dyke, M. Watabe, K. Tsogtbaatar, and
R. Barsbold. 2007. A new enantiornithine bird from the Late Cre-
taceous 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
Anatomy 208:287–308.
Duan, Y., L. Zhang, L. Li, and S. Cheng. 2006. Division and correlation
of unique fossil-bearing beds of Jiufotang Formation in Dapingfang-
Meileyingzi Basin of western Liaoning. Global Geology 25:113–119.
[Chinese]
Goloboff, P. A., J. S. Farris, and K. C. Nixon. 2008. TNT, a free program
for phylogenetic analysis. Cladistics 24:774–786.
Hou, L. 1997. Mesozoic Birds of China. Phoenix Valley Provincial Aviary,
Taiwan, 153 pp. [Chinese]
Hou, L., L. M. Chiappe, F. Zhang, and C. Chuong. 2004. New Early Cre-
taceous fossil from China documents a novel trophic specialization
for Mesozoic birds. Naturwissenschaften 91:22–25.
Hu, D., L. Li, L. Hou, and X. Xu. 2011. A new enantiornithine bird from
the Lower Cretaceous of western Liaoning, China. Journal of Ver-
tebrate Paleontology 31:154–161.
Linnaeus, C. 1758. Systema Naturae: Regnum Animale. Tenth edi-
tion. Reprinted by the British Museum (Natural History), London,
823 pp.
Martin, L. D. 1995. The Enantiornithes: terrestial birds of the Cretaceous.
Courier Forschungsinstitut Senckenberg 181:23–26.
Martin, L. D., Z. Zhou, L. Hou, and A. Feduccia. 1998. Confuciusor-
nis sanctus compared to Archaeopteryx lithographica. Naturwis-
senschaften 85:286–289.
Morschhauser, E. M., D. J. Varricchio, C. Gao, J. Liu, Z. Wang, X. Cheng,
and Q. Meng. 2009. Anatomy of the Early Cretaceous bird Rapax-
avis pani, a new species from Liaoning Province, China. Journal of
Vertebrate Paleontology 29:545–554.
Norell, M. A., and J. A. Clarke. 2001. Fossil that fills a critical gap in avian
evolution. Nature 409:181–184.
Ostrom, J. H. 1976. Some hypothetical anatomical stages in the evolution
of avian flight. Smithsonian Contributions to Paleobiology 27:1–21.
Sanz, J. L., and J. F. Bonaparte. 1992. A new order of birds (Class Aves)
from the Lower Cretaceous of Spain; pp. 38–49 in K. E. Campbell
(ed.), Papers in Avian Paleontology Honoring Pierce Brodkorb, Sci-
ence Series 36. Natural History Museum of Los Angeles County,
Los Angeles, California.
Sanz, J. L., L. M. Chiappe, and A. D. Buscalioni. 1995. The osteology of
Concornis lacustris (Aves: Enantiornithes) from the Lower Creta-
ceous of Spain and a reexamination of its phylogenetic relationships.
American Museum Novitates 3133:1–23.
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, California.
Vazquez, R. J. 1994. The automating skeletal and muscular mechanisms
of the avian wing (Aves). Zoomorphology 114:59–71.
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. 2010. Enantiornithine birds from the Late
Cretaceous of El Brete (Argentina). Irish Journal of Earth Science
27:15–62.
Wang, X., J.-M. O’Connor, B. Zhao, L. M. Chiappe, C. Gao, and X.
Cheng. 2010. A new species of Enantiornithes (Aves: Ornithotho-
races) based on a well-preserved specimen from the Qiaotou
Formation of northern Hebei, China. Acta Geologica Sinica 84:
247–256.
You, H., M. C. Lamanna, J. D. Harris, L. M. Chiappe, J.-M. O’Connor,
S. Ji, J. L
¨
u, C. Yuan, D. Li, X. Zhang, K. J. Lacovara, 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 Science 41:1097–1107.
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.
Zhang, Z., C. Gao, Q. Meng, J. Liu, L. Hou, and G. Zheng. 2009. Di-
versification in an Early Cretaceous avian genus: evidence from a
new species of Confuciusornis from China. Journal of Ornithology
150:783–790.
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.), Meso-
zoic Birds: Above the Heads of Dinosaurs. University of California
Press, Berkeley, California.
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. 2006. A beaked basal ornithurine bird (Aves,
Ornithurae) from the Lower Cretaceous of China. Zoologica Scripta
35:363–373.
Zhou, Z., L. M. Chiappe, and F. Zhang. 2005. Anatomy of the Early
Cretaceous bird Eoenantiornis buhleri (Aves: Enantiornithes) from
China. Canadian Journal of Earth Science 42:1331–1338.
Zhou, Z., J. Clarke, and F. Zhang. 2008. Insight into diversity, body size
evolution from the largest Early enantiornithine bird. Journal of
Anatomy 212:565–577.
Submitted April 5, 2011; revisions received August 28, 2011; accepted
December 18, 2011.
Handling editor: Patrick O’Connor.
Downloaded by [Dongyu Hu] at 17:49 06 May 2012