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A redescription of Chaoyangia beishanensis (Aves) and a comprehensive phylogeny of Mesozoic birds


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We review the enigmatic Chaoyangia beishanensis, one of the earliest birds described from the Jiufotang Formation, north-eastern China, and the first to be identified as an ornithurine (Aves: Ornithothoraces) and thus a member of the clade that includes living birds. A complete discussion of the validity of this taxon, which once included the holotype of Songlingornis, is provided, along with a revised diagnosis. The morphology of Chaoyangia is described, including extensive comparison with better known, recently discovered ornithurines as well as several other groups of Mesozoic birds (Confuciusornithiformes, Sapeornithiformes, Enantiornithes). Although preserved information is limited, the large number of fused sacral vertebrae and presence of a distal dorsal process on the ischium are among the features supporting early hypotheses that the only known specimen of Chaoyangia represents an ornithurine. Unique among ornithurines, Chaoyangia possesses two dorsal processes on the ischium, and thus remains a valid taxon. We include this taxon in a cladistic analysis to test morphological hypotheses regarding its systematic position. Although the results of the analysis are highly resolved and support the referral of Chaoyangia and Zhongjianornis to Ornithurae, support for the tree overall is very low. Recently discovered taxa have blurred the once clear morphological gap separating the two ornithothoracine clades (Ornithurae and Enantiornithes), and thus the increase in taxonomic diversity has caused a decrease in the stability of hypothetical relationships.
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A redescription of Chaoyangia beishanensis (Aves) and
a comprehensive phylogeny of Mesozoic birds
Jingmai K. O’Connor
& Zhonghe Zhou
Key Laboratory of Evolutionary Systematics of Vertebrates, Institute of Vertebrate
Paleontology and Paleoanthroplogy, 142 Xizhimenwai Dajie, Beijing, 100044, PR China
Available online: 20 Jun 2012
To cite this article: Jingmai K. O’Connor & Zhonghe Zhou (2012): A redescription of Chaoyangia beishanensis (Aves) and a
comprehensive phylogeny of Mesozoic birds, Journal of Systematic Palaeontology, DOI:10.1080/14772019.2012.690455
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Journal of Systematic Palaeontology, iFirst 2012, 1–18
A redescription of Chaoyangia beishanensis (Aves) and a comprehensive
phylogeny of Mesozoic birds
Jingmai K. O’Connor
and Zhonghe Zhou
Key Laboratory of Evolutionary Systematics of Vertebrates, Institute of Vertebrate Paleontology and Paleoanthroplogy,
142 Xizhimenwai Dajie, Beijing 100044, PR China
(Received 13 July 2011; accepted 17 January 2012)
We review the enigmatic Chaoyangia beishanensis, one of the earliest birds described from the Jiufotang Formation, north-
eastern China, and the first to be identified as an ornithurine (Aves: Ornithothoraces) and thus a member of the clade that
includes living birds. A complete discussion of the validity of this taxon, which once included the holotype of Songlingornis,
is provided, along with a revised diagnosis. The morphology of Chaoyangia is described, including extensive comparison with
better known, recently discovered ornithurines as well as several other groups of Mesozoic birds (Confuciusornithiformes,
Sapeornithiformes, Enantiornithes). Although preserved information is limited, the large number of fused sacral vertebrae
and presence of a distal dorsal process on the ischium are among the features supporting early hypotheses that the only
known specimen of Chaoyangia represents an ornithurine. Unique among ornithurines, Chaoyangia possesses two dorsal
processes on the ischium, and thus remains a valid taxon. We include this taxon in a cladistic analysis to test morphological
hypotheses regarding its systematic position. Although the results of the analysis are highly resolved and support the referral
of Chaoyangia and Zhongjianornis to Ornithurae, support for the tree overall is very low. Recently discovered taxa have
blurred the once clear morphological gap separating the two ornithothoracine clades (Ornithurae and Enantiornithes), and
thus the increase in taxonomic diversity has caused a decrease in the stability of hypothetical relationships.
Keywords: Chaoyangia; Jehol; ornithurine; Zhongjianornis; Songlingornithidae
Since the first discoveries in the early 1990s, new species,
genera, subclades and lineages of archaic birds have contin-
uously been uncovered from the Early Cretaceous lake
deposits of the Jehol Group in north-easter n China (Chiappe
2007; Zhou & Wang 2010). This geological unit, which
is composed of three formations (lower Dabeigou, middle
Yixian and upper Jiufotang), has revealed more Early Creta-
ceous avian diversity than any other. Within the last three
decades alone, the Early Cretaceous Jehol Biota of north-
eastern China has produced an unprecedented amount of
vertebrate diversity, revealing the feathers of dinosaurs and
the largest known Mesozoic mammals, among other spec-
tacular discoveries ( Zhou et al. 2003). The Jehol biota has
been key in revealing the early evolution of Aves, represent-
ing the second oldest and most diverse Mesozoic avifauna
to date. The Jehol avifauna preserves a number of clades,
spanning the entire phylogeny of Mesozoic birds, coexisting
in a diverse forested coastal lake habitat. Known uniquely
from this biota are Sapeornithiformes, Confuciusornithi-
formes, Jeholornithiformes (Li et al. 2010) (although other
long-tailed birds are known in the Late Jurassic from the
Corresponding author. Email:
Solnhofen Limestones of Germany and the Late Cretaceous
from the Maehavaero Formation of Madagascar; Forster
et al. 1996; Elzanowski 2002; O’Connor & Forster 2010),
and the only transitional short-tailed non-pygostylian bird
(Zhongornis haoae, too poorly known to be placed in a
higher taxon; Gao et al. 2008). The Jehol avifauna also
preserves the earliest record of ornithothoracine birds,
including a huge diversity of the dominant Cretaceous
enantiornithines and their sister clade, the more derived
ornithurine birds (Zhou & Zhang 2006b). The origin and
early evolution of the latter clade is of particular signif-
icance because this marks the appearance of the lineage
leading to all living birds.
Prior to the numerous complete discoveries of basal
ornithurines (= Ornithuromorpha) from the Jehol Group,
the global record of ornithuromorph taxa was quite sparse,
limited to isolated, fragmentary, partial skeletons (e.g.
Ambiortus dejemetvi, Gansus yumenensis, Patagopteryx
deferransi; Kurochkin 1982; Hou & Liu 1984; Alvarenga
& Bonaparte 1992). Although these isolated materials
preserved advanced morphologies that indicated their
phylogenetic placement within Ornithuromorpha, they did
little to help to piece together the biology of the early
ISSN 1477-2019 print / 1478-0941 online
2012 The Natural History Museum
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2 J. K. O’Connor and Z. Zhou
ancestors of modern birds. While specimens from other
deposits continue to be largely incomplete (Bell et al.
2010), within the last decade the nearly complete discov-
eries from the Jehol (e.g. Yanornis martini, Yixianornis
grabaui, Archaeorhynchus spathula, Hongshanornis longi-
cresta, Jianchangornis microdonta) have revealed a wealth
of morphological information, as well as data concerning
the ecology, diet and integument of early members of the
clade (Zhou & Zhang 2001, 2005, 2006a; Zhou et al. 2004;
Zhou et al. 2009).
Early discoveries from the Jehol were typically incom-
plete and poorly prepared compared to more recent
discoveries (e.g. Liaoningornis longidigitrus, Boluochia
zhengi, Cuspirostrisornis houi; Zhou 1995; Hou 1997a, b;
O’Connor et al. 2011a). These birds were described and
assigned to a particular clade based on the knowledge of
early birds available at the time, usually without apply-
ing cladistic analysis. However, since these discoveries, a
wealth of new knowledge has been accumulated. With new
fossils uncovered at such a high rate, very little revision
has been conducted on early discoveries despite the poten-
tial for new information (O’Connor et al. 2011a). Here
we review one of the first birds discovered from the Jehol
Group, Chaoyangia beishanensis (Hou & Zhang, 1993),
which later became the first bird from this sequence to be
identified as an ornithurine (Hou et al. 1996). Despite the
lack of clear support and justification, this classification
is still widely used today (Zhou & Zhang 2006b; Zhou
et al. 2008b). In order to better understand this enigmatic
taxon, the morphology of the holotype specimen (IVPP
V9934) is compared to that of the purportedly closely
related taxa Yixianornis, Yanornis and Confuciusornis,as
well as new controversial taxa with morphological simi-
larities (e.g. Zhongjianornis). We also briefly redescribe
Songlingornis, and the other specimen formerly assigned
to Chaoyangia, IVPP V9937. All these taxa are treated
together in a single analysis for the first time in order to test
hypotheses regarding the phylogenetic position and inter-
relationships of these species.
Material and methods
Specimens were studied using a Leica S4E micro-
scope. Anatomical nomenclature mainly follows Baumel &
Witmer (1993) although certain structures not cited therein
follow Howard (1929). While the Latin terminology used
by Baumel & Witmer (1993) is retained for muscles and
ligaments, osteological structures are described using the
English equivalents of the Latin terms.
Institutional abbreviations
CAGS: Chinese Academy of Geological Sciences, Beijing,
China; IVPP: Institute of Vertebrate Paleontology and Pale-
oanthroplogy, Beijing, China; PKUP: Peking University
Paleontological Collection, Beijing, China.
Background information
The holotype of Chaoyangia beishanensis (Hou & Zhang,
1993), IVPP V9934 (Figs 1–4), comes from the Boluochi
locality of the Jiufotang Formation, Liaoning, nor th-eastern
China. At the time, only the enantiornithines Cathayornis
and Sinornis were known from the Jehol and available for
comparison (Sereno & Rao 1992; Zhou et al. 1992). Speci-
men IVPP V9934 is a single partial skeleton preserved in a
main slab with a small counter slab (that corresponds only
to the proximal portion of the main slab), poorly preserv-
ing the impressions of the caudal half of the axial skeleton,
the pelvis and proximal hind limbs (Figs 1–4). At the time
of the initial description, the specimen was considered to
be unique from known lineages, but not assigned to a new
group (Hou & Zhang 1993). Later, as Early Cretaceous
birds became better understood through additional discov-
eries, Chaoyangia was regarded as a fairly advanced bird
and assigned to Ornithurae (Hou et al. 1996; Hou 1997b;
Zhou & Hou 2002; Zhou et al. 2008b).
The taxonomic history of this species, however, is not as
straightforward as it appears: although the original descrip-
tion of Chaoyangia was based on a single specimen (IVPP
V9934), the justification for the assignment of this taxon to
Ornithurae was based almost entirely on characters derived
from referred specimens (IVPP V10913 and V9937; Figs
5, 6). These specimens do not preserve any overlapping
elements with the holotype (IVPP V10913 is an incom-
plete pectoral girdle, while IVPP V9937 represents a partial
foot), and their assignment was based on size, locality and
the inference that all specimens belonged to an ornithurine
bird (Hou et al. 1996). One of these specimens (IVPP
V10913; Fig. 5) was later used to erect a new genus and
species, Songlingornis linghensis Hou, 1997b, and publica-
tions after 1996 either split the two taxa (Hou et al. 1996;
Hou 1997b; Clarke & Norell 2001; Clarke 2002) or lumped
them together (Hou et al. 1996; Zhou & Hou 2002; Ji 2006).
The original assignment of IVPP V10913 to Chaoyangia
was never justified and currently where Songlingornis is
considered a distinct taxon, hypotheses differentially place
the two taxa in the same family and order, Chaoyangornithi-
dae and Chaoyangornithiformes (Zhou & Zhang 2006b), or
widely separate them into different clades using phyloge-
netic analysis (Clarke 2002). The second specimen assigned
to Chaoyangia beishanensis, IVPP V9937 (Fig. 6), is an
isolated partial foot that also does not preserve any over-
lapping elements with IVPP V9934. The morphology of
this specimen has never been discussed or figured in detail.
The original diagnosis of Chaoyangia was based entirely
on the holotype (Hou & Zhang 1993); this was later revised
but the updated diagnosis incorporated a large number of
features derived from the referred specimens IVPP V10913
and V9937 (e.g. the presence of teeth, paired fenestrae
on the sternum, reduced ungual on pedal digit I; Zhou &
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A redescription of Chaoyangia beishanensis 3
Figure 1. Photographs of the holotype specimen of Chaoyangia beishanensis (IVPP V9934). A, slab; B, counterslab. Scale bar = 1cm.
Hou 2002). Although morphological characters that unite
Chaoyangia with ornithurines rely heavily on the assigned
material (IVPP V10913 and V9937), derived characters
visible in the holotype (IVPP V9934) include the presence
of uncinate processes, a large number of fused sacral verte-
brae, and a proximocranially projecting cnemial crest (Zhou
& Hou 2002). Currently, uncinate processes are known
to occur in a wide range of taxa, including some non-
avian theropods (e.g. dromaeosaurids, such as Deinonychus
and Microraptor, oviraptorosaurs, such as Citipati; Codd
et al. 2008), basal birds (e.g. Confuciusornis, Zhongjianor-
nis), as well as more advanced birds within Ornithuro-
morpha (Tickle et al. 2007). The latter two characters that
place Chaoyangia in Ornithuromorpha are still consistent
with this clade; however, the holotype specimen is poorly
preserved (bones are absent, preserved as impressions) and
very incomplete and these morphologies are difficult to
confirm from published data.
A recently discovered nearly complete basal pygostylian,
Zhongjianornis zhengi (Zhou et al. 2010), is strikingly
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4 J. K. O’Connor and Z. Zhou
Figure 2. Photograph of the cast of the main slab of IVPP V9934. Scale bar = 1cm.
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A redescription of Chaoyangia beishanensis 5
Figure 3. Camera lucida drawing of the main slab of the holotype specimen of Chaoyangia beishanensis (IVPP V9934). White indicates
well-preserved bone and light grey represents poorly preserved bone. Anatomical abbreviations: cc, cnemial crest; dp, dorsal process; fc,
fibular crest; fem, femur; fib, fibula; ili, ilium; isc, ischium; ob, obturator process; pub, pubis; rib, ribs; syn, synsacrum; tbt, tibiotarsus;
thv, thoracic vertebrae; tmt, tarsometatarsus; up, uncinate process. Scale bar = 1cm.
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6 J. K. O’Connor and Z. Zhou
Figure 4. Camera lucida drawing of the counterslab of the holo-
type specimen of Chaoyangia beishanensis (IVPP V9934). Light
grey represents poorly preserved bone. For anatomical abbrevia-
tions see Fig. 3 caption. Scale bar = 1cm.
similar in appearance to Chaoyangia where preservation
allows comparison (Fig. 7). This taxon also shows some
morphological similarities with Confuciusornis (as does
Chaoyangia, noted by Clarke 2002), such as the edentulous
robust beak, and the quadrangular shape of the deltopectoral
crest of the humerus. Although Z. zhengi does not clearly
preserve the tail, cladistic analysis resolves Zhongjianornis
as a basal pygostylian, more derived than Jeholornis and
Sapeornis but basal to Confuciusornis and Ornithothoraces
(including Songlingornis; Zhou et al. 2010).
The relationships between Chaoyangia and other taxa
have never been fully explored through cladistic analy-
sis; most studies do not include the fragmentary Chaoyan-
gia and rarely include Songlingornis.Ofthefewphylo-
genetic analyses to include this taxon, one early study
confirmed the hypothetical placement of Chaoyangia as a
basal ornithurine but included morphological data derived
from the referred specimens as well as the holotype (Zhou
1999). In her comprehensive analysis of the phylogenetic
position of Ichthyornis, Clarke (2002) briefly addressed the
issues surrounding Chaoyangia. Using data only from the
holotype specimen, this analysis resolved Chaoyangia as a
basal pygostylian in a polytomy with some enantiornithines
and Confuciusornis (Clarke 2002). It was further suggested
that based on available morphological data, Chaoyangia
may be junior synonym of Confuciusornis (Clarke 2002).
The holotype of Songlingornis linghensis (IVPP
V10913), because it i s more complete and slightly better
preserved than the holotype of Chaoyangia (IVPP V9934),
has appeared in several recent cladistic analyses (Clarke
et al. 2006; Zhou et al. 2008a, 2009, 2010). These analy-
ses have all placed Songlingornis in a clade together with
the nearly complete and well-known ornithurines Yixianor-
nis grabaui and Yanornis martini (Zhou & Zhang 2001;
Clarke et al. 2006); this clade, called Songlingornithidae
(Hou 1997b), is one of the few recognized Early Cretaceous
ornithurine subclades. Although true for nearly all known
Mesozoic bird relationships, this clade is only weakly
supported; the original analysis optimized the clade based
on four unambiguous characters, none of which are actu-
ally unique to this group of taxa (i.e. presence of a procora-
coid process, absence of a medial groove on the coracoid,
and edentulous tip of premaxilla, which define a major-
ity of ornithuromorphs, and the presence of caudal ster nal
fenestrae, also seen in Gansus;Clarkeet al. 2006). Unam-
biguous support in more recent analyses is based entirely
on the similar morphology of t he sternum (with a pair of
caudal fenestra and only a single pair of free caudal trabec-
ulae). Although the relationship may not hold as taxonomic
diversity increases (e.g. the presence of caudal sternal
fenestrae in other basal ornithurines), the nearly complete
holotype specimens of Yixianornis grabaui
and Yanornis
martini allow for direct morphological comparison with
Chaoyangia, not possible with the holotype of Songlingor-
nis linghensis, to test the current phylogenetic position of
Chaoyangia within Ornithurae. The lack of agreement in
the phylogenetic position of Chaoyangia reflects the frag-
mentary nature of the only known specimen, a problem that
is exacerbated by the mosaic distribution of morphologies
among Mesozoic Aves (Chiappe 2007).
Systematic palaeontology
Class Ave s Linnaeus, 1758
Ornithothoraces Chiappe & Calvo, 1994
Ornithuromorpha Chiappe, 2002
Ornithurae Haeckel, 1866 sensu Gauthier & de Quieroz,
Genus Chaoyangia Hou & Zhang, 1993
Chaoyangia beishanensis Hou & Zhang, 1993
(Figs 1–4)
Revised diagnosis. A small basal ornithurine bird with the
unique combination of the following characters: synsacrum
composed of more than eight vertebrae; uncinate processes
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A redescription of Chaoyangia beishanensis 7
Figure 5. Holotype of Songlingornis linghensis IVPP V10913, formerly assigned to Chaoyangia beishanensis. A, photograph; B,
interpretative drawing. Light grey represents poorly preserved bone. Anatomical abbreviations (not listed in Fig. 3 caption): cmc,
carpometacarpus; cor, coracoid; den, dentary; fur, furcula; jug?, possible jugal; max, maxilla; pmx, premaxilla. Scale bar = 1cm.
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8 J. K. O’Connor and Z. Zhou
Figure 6. Specimen IVPP V9937, formerly assigned to Chaoyan-
gia beishanensis. A, photograph; B, interpretative drawing. Poorly
preserved bones indicated by light grey. Anatomical abbreviations
(not listed in Fig. 3 caption): Iph1, pedal digit I first phalanx; Iph2,
pedal digit I second phalanx; IIph1, pedal digit II first phalanx;
IIph2, pedal digit II second phalanx; IIph3, pedal digit II third
phalanx; IIph4, pedal digit II fourth phalanx; IVph4?, pedal digit
IV fourth phalanx?; IVph5, pedal digit IV fifth phalanx; vf, vascu-
lar foramen. Scale bar = 1cm.
on ribs long (crossing 1.5 ribs) and slender; uncinate
processes expanded basally, forming a 55
angle with
the rib; ischium with two, gradually expanding, dorsal
processes; ischia distally contacting; pubic symphysis
extending one-third length of the pubis; femoral neck,
poorly defined; proximocranially projecting cnemial crest
on proximal tibiotarsus (modified from Zhou & Hou, 2002).
Material. IVPP V9934, single slab with partial counter-
slab, preserving the impressions of bones.
Stratigraphical distribution. Jiufotang Formation of the
Jehol Group, Lower Cretaceous, 125–120 Ma (Swisher
et al. 2002; He et al. 2004; Zhu et al. 2007).
Geographical distribution. Xidagou, Boluochi, Chao-
yang, western Liaoning Province, north-eastern China.
Description and remarks. Description is based solely on
the holotype specimen (IVPP V9934); morphology was
taken from the slab and counterpart as well as a cast of the
main slab.
Axial skeleton. Only thoracic vertebrae and ribs and
the synsacrum are preserved (Figs 1–4); an estimated 11–13
Figure 7. Holotype of Zhongjianornis zhengi, IVPP V15900.
Boxed area approximates region that can be compared to the holo-
type of Chaoyangia, IVPP V9934.
thoracic ver tebrae are present. Several of the thoracic verte-
brae are preserved partially in articulation (preserved best in
the counter slab; Fig. 1B) and in lateral view (Fig. 1). The
vertebrae are spool-shaped, excavated laterally by broad
deep fossae, and bearing tall dorsal s pines. The parapophy-
ses appear to be cranially located, visible in the s econd to
last preserved thoracic.
The synsacrum is preserved as an impression of the
ventrolateral surface. Based on the number of transverse
processes, it appears nine vertebrae form this element;
however, the proximal and distal ends of the synsacrum
are unclear, and up to 11 vertebrae may have been incor-
porated. This large number of fused sacral vertebrae,
even higher than originally estimated, is consistent with
the derived placement inferred for Chaoyangia. Primi-
tive long-tailed birds typically possess five (Archaeopteryx;
Elzanowski 2002) or six sacrals (e.g. Rahonavis, Jeholor-
nis; Forster et al. 1996; Zhou & Zhang 2003b), while
the basal pygostylians Sapeornis and Confuciusornis both
possess seven sacral vertebrae (Chiappe et al. 1999; Zhou &
Zhang 2003a); the enantiornithine synsacrum is composed
of seven (e.g. Rapaxavis, Pengornis, Protopteryx)to
eight sacrals (e.g. Cathayornis, Longipteryx, Vescornis;
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A redescription of Chaoyangia beishanensis 9
O’Connor 2009). Members of Ornithuromorpha typically
possess a larger synsacrum formed by nine or more
vertebrae; Yixianornis and Yanornis possess nine fully
fused sacral vertebrae (Zhou & Zhang 2001), while the
more derived Gansus and the ornithurine clade of foot-
propelled divers, the Hesperornithiformes, possessed 10
fused sacral vert ebrae (You et al. 2006). However, the
more recently discovered basal ornithuromorph, Archae-
orhynchus, possesses only eight fused sacrals (Zhou &
Zhang 2006a), suggesting that basal ornithuromorphs,
like enantiornithines, had fewer fused sacral vertebrae.
The basal bird Zhongjianornis reportedly preserves no
more than eight sacral vertebrae (Zhou et al. 2010);
however, preservation is unclear, transverse processes are
not preserved, and the distal third is covered by the ilium
(IVPP V15900).
The synsacrum is not preserved fused to the pelvis (IVPP
V9934). Because the synsacrum is preserved at an angle, it
is difficult to make unequivocal statements about the rela-
tive lengths of the transverse processes (which appear to be
slightly longer among the central vertebrae) or mediolat-
eral width of the bone (which appears widest in the centre).
However, the transverse processes are all clearly directed
laterally except for the caudalmost one or two vertebrae
(Fig. 3). The synsacrum appears slightly dorsoventrally
bowed so that the dorsal surface would be convex, a feature
observed in other ornithurines (Clarke 2004). The proximal
synsacrum appears dorsoventrally thicker than its distal end.
The midline of t he ventral surface appears to have possessed
a f aint groove, only preserved on the distal half, which may
have been more extensive.
Ribs. Six pairs of ribs are preserved in articulation
with the thoracic vertebrae. Two more ribs (from the
other side) are disarticulated and preserved parallel to the
thoracic series. Additional rib f ragments are scattered over
the hip region. The ribs are slightly sigmoidal, (proxi-
mal half slightly cranially convex and caudal half very
slightly cranially concave) considered an autapomorphy
of the species (Zhou et al. 2008b). In most taxa where
preservation permits comparison (preserved in lateral view)
the ribs are broadly concave cranially (e.g. ornithuromorph
Yanornis IVPP V13358, enantiornithine Longipteryx IVPP
V12325). Zhongjianornis, however, does show a similar
morphology where the middle portion of rib is straight
(IVPP V15900), which contributes to their s igmoid shape
as in Chaoyangia (Figs 1, 3). The distal ends of the ribs
are covered in IVPP V15900 and it cannot be determined
if distally the ribs became concave dorsally as in Chaoyan-
gia. The ribs in a newly described specimen of Cathayornis
(Zhang et al. 2010) are also slightly sigmoidal, suggest-
ing that additional specimens are required before it can be
determined if this is a diagenetic effect.
Three uncinate processes are clearly preserved in the
main slab in articulation with the thoracic ribs (Figs 1–4);
some disarticulated fragments may also represent uncinate
processes. The smaller slab preserves the counterparts to
two of these processes (Fig. 1B). The contact between the
rib and the uncinate process is identifiable, indicating these
processes were not fully fused. The uncinate processes
are directed dorsally, defining approximately a 55
with the ribs. The base of the process is broad, expand-
ing proximally and distally along the rib. The uncinate
processes are relatively short, crossing only a single rib
(from their origin), tapering distally, with the distal margin
located just over halfway to the next rib (Fig. 8). Ossified
uncinate processes are known throughout Aves, as well as
in some related non-avian dinosaurs (Clark et al. 1999;
Norell & Mackovicky 1999; Zhou et al. 2000; Codd et al.
2008). These processes are absent (or unossified) in the
most basal known bird, Archaeopteryx (Mayr et al. 2005),
and other long-tailed birds (e.g. Jeholornis; IVPP V13353).
Ossified processes are present in the basal bird Confuciu-
sornis but are not preserved in any specimen of Sapeornis
(Chiappe et al. 1999; Zhou & Zhang 2003a). In Confu-
ciusornis, these processes are unfused, simple without an
expanded base, and less than two rib lengths (Chiappe
et al. 1999). Although reported in two enantiornithines
(Eoenantiornis buhleri (IVPP V11537) and Longipteryx
chaoyangensis (IVPP V12325); Zhang et al. 2000; Zhou
et al. 2005), the short, straight, free strap-like fragments
identified as uncinate processes in these specimens are
not morphologically consistent within a s ingle specimen
and no uncinate processes have been reported in any of
the referred specimens of Longipteryx (IVPP V12552),
suggesting that these bones may have been misidentified.
Uncinate processes are most common among ornithurines
(Yixianornis, Hongshanornis, Archaeorhynchus; Zhou &
Zhang 2005, 2006a; Clarke et al. 2006), although they are
absent (or unossified) in some taxa (i.e. Gansus;Youet al.
2006). This absence is considered real, not preservational,
given the large number of excellently preserved specimens
of this taxon (You et al. 2006). The uncinate processes in
Chaoyangia most resemble those present in the ornithurine
Yixianornis (Clarke et al. 2006). In this taxon, the processes
are slightly expanded at the base, and long, extending across
two ribs; it cannot be determined if they were fused to the
ribs (Clarke et al. 2006). I n Archaeorhynchus the uncinate
processes are shorter, approximately one rib length and L-
shaped, rather than expanding at the base in both directions
(IVPP V14287), while in Hongshanornis they are similar
in morphology but longer, crossing two ribs, and forming a
angle with the rib (IVPP V14533).
Pelvic girdle . The pelvis is nearly complete (Figs 1–3);
both ilia are preserved although they do not reveal many
morphological details. The right one is poorly preserved
and the left is slightly disarticulated. It appears the ilia were
not fused to the synsacrum, although the ilium, pubis and
ischium were partially fused at the level of the acetabulum.
The impression of the preacetabular wing of the right ilium
is deeply concave craniolaterally, however preservation
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10 J. K. O’Connor and Z. Zhou
Figure 8. Comparative anatomy of Mesozoic bird uncinate
processes: A, Chaoyangia; B, Yixianornis; C, Zhongjianornis.
Anatomical abbreviation: up, uncinate process. All scale bars
represent one centimetre.
makes it difficult to tell if this is the result of another
bone overlying this part of the ilium; Zhongjianornis IVPP
V15900 preserves a similar deep dorsolateral concavity
on the preacetabular wing of the right ilium. In the cast
of IVPP V9334, the preacetabular ilium is preserved
primarily in dorsal view (dorsolateral view); in this view,
the preacetabular ilium appears thickest proximally and
laterally excavated by a shallow fossa. What is preserved
of the left ilium appears narrow and tapered cranially in
both the slab and cast (Figs 1, 2), suggesting the rostral
margins of the ilia were sharp and tapered rostrally as in
Zhongjianornis (Zhou et al. 2010). The morphology of
the postacetabular wing of the right ilium is unclear due to
overlapping bone impressions (Fig. 1A).
The ischium is the most interesting element preserved in
this specimen; it bears two dorsal processes and possibly
a very small obturator process ( Fig. 2). Just distal to the
pubic peduncle of the ischium is a small ventrally directed
process, which may be the reduced obturator process; it does
not contact the pubis. The first dorsal process is located
at approximately the midpoint of the ischium; it is not a
distinct process like that of enantiornithines and Confu-
ciusornis, which is also more proximally located in both
groups (Chiappe et al. 1999; O’Connor et al. 2009), but
a gradual dorsal swelling that defines an obtuse triangular
process, very similar to that present in some ornithurine taxa
(e.g. Yixianornis (IVPP V12631), Gansus (CAGS-IG-04-
CM-002); absent in Archaeorhynchus (IVPP V14287) and
Hongshanornis (IVPP V14533)). The apex of the process
is not preser ved and the exact morphology is unclear;
however, the base of the proximal process accounts for
almost one-third the length of the ischium. The second
process is s imilar but smaller and located at the distal end of
the ischium; the corpus swells dorsally, forming the second
process, and then tapers to a triangular point (Figs 1–3).
The ischium in other ornithurines (e.g. Gansus (CAGS-IG-
04-CM-002), Hongshanornis (IVPP V14533), Yixianor-
nis (IVPP V12631) and Yanornis (IVPP V13358)) tapers
sharply to the distal end with no additional distally located
swelling; however, a second distal process is also present on
the ischium in Confuciusornis (IVPP V 11374, V13168),
although it is located slightly more proximal than that
preserved in Chaoyangia. The ischium in Zhongjianornis is
similar to that of ornithurines, with a distally located proxi-
mal process (Zhou et al. 2010); however, damage and poor
preservation prevents an accurate assessment of the distal
morphology. The ischium in this taxon, however, is strongly
concave ventrally, a morphology absent in Chaoyangia.
Distally, it appears the two ischia contact each other; a
portion of the left ischium is visible in contact with the
right one (Fig. 3).
The pubis forms the ventral two-thirds of the acetab-
ulum; the pubic pedicel of the ilium is more than twice
as wide as the narrow pedicel for the ischium (Fig. 3).
The pubis is nearly parallel to the ischium, but both bones
are directed caudoventrally demarcating an acute angle
with the post-acetabular ilium (as opposed to parallel in
advanced ornithurines). The articulation, although in place
and preserving the acetabulum, appears to be slightly
crushed (Fig. 2); still we estimate the pubis and ischium
were retroverted at an acute angle of less than 45
rostroventral to the acetabulum, the pubis appears to
form a robust pectineal process. The pubis is more than
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A redescription of Chaoyangia beishanensis 11
two-thirds the length of the ischium. The shaft has an oval
cross-section; proximally the orientation of the long axis
is unclear but distally the shaft appears to become more
robust and the long axis of the oval cross-section is angled
dorsolaterally–ventromedially. The distal third of the pubes
contact each other, although they remain incompletely
fused. The contact is expanded dorsoventrally, not forming
a distinct boot in which the expansion occurs primarily
dorsally, perpendicular to the shaft as in some enantior-
nithines (e.g. Longipteryx (IVPP V12325)). Portions of
the pubic shaft are pitted, on the right just proximal to the
symphysis and on the left on the proximal portion of the
symphysis (visible in the cast). The pubes of Chaoyangia
are more robust than in some ornithuromorphs (especially
relative to Yixianornis (IVPP V12631) and Hongshanornis
(IVPP V14533)), but fairly comparable to those preserved
in Zhongjianornis (IVPP V15900).
Pelvic limb. The hind limb is very incomplete; both
femora are preserved (the left is incomplete), but only the
right tibiotarsus (missing its distal end) and a fragment of
the right tarsometatarsus are present (Figs 1–3). The prox-
imal end of a distal condyle of the tibiotarsus is preserved,
allowing for an estimate of the total length of this bone.
The femur is fairly long: it is more than two-thirds the
estimated length of the tibiotarsus and nearly as long as
the pubis. The femur is straight and robust in Chaoyan-
gia, comparable to the morphology of Zhongjianornis (the
femur is bowed in most enantiornithines; O’Connor 2009);
in both specimens, the proximal head is fairly large, and
separated by a very shallow neck, which also character-
izes other basal ornithurines (e.g. Yanornis, IVPP V12558,
V10996). A well-defined posterior trochanter (Chiappe &
Walker 2002), as present in enantiornithines and some non-
avian theropods, is absent. Impressions of the condyles of
the right femur are preserved in the main slab; no indica-
tion of a fibular trochlea is apparent. The condyles are proxi-
modistally elongate narrow ovals, and are widely separated.
The medial condyle appears approximately 50% wider than
the lateral condyle, which is more poorly preserved (visible
in cast). The reduction in width of this outer condyle may
suggest the presence of an incipient fibular trochlea.
The right tibiotarsus appears to be in caudal view
(impression of cranial surface); the proximal end bears
a small cnemial crest that projects proximocranially and
laterally. The feature appears to be a true morphology
of the specimen, although a diagenetic origin cannot be
completely ruled out given the poor overall preservation
of the specimen. This crest is limited to the proximal 15%
of the shaft length. In the cast, a second ridge appears
visible, ending just distal to where the first crest ends
(Fig. 2). This second possible crest cuts laterally, and
for most of its length appears to be r unning underneath
(lateral to) the larger crest. This may represent a second
cnemial crest or a break in the l arge proximally project-
ing cnemial crest. Although small low cranial crests are
present in some enantiornithines (Chiappe & Walker 2002),
a proximally projecting cnemial crest is only known within
Ornithuromorpha (e.g. Gansus, Hongshanornis, Yixianor-
nis; O’Connor et al. 2011b). Basal pygostylians Sapeor-
nis and Confuciusornis are not known to possess cnemial
crests (Chiappe et al. 1999; Zhou & Zhang 2003a) and
the hind limb of Zhongjianornis is exposed in caudal view,
thus preventing identification (IVPP V15900). The lateral
margin bears a short fibular crest; it begins just distal to
the proximal crests and extends for less than one third of
the preserved tibiotarsus. A small triangular bone preserved
just medial to the proximal end of the tibiotarsus is inter-
preted as the fibula. It is incomplete and preserves no real
morphological information.
A fragment of the proximal right tarsometatarsus is
preserved at the edge of the slab, most clearly visible in
the cast (Fig. 2). The fragment, interpreted as the impres-
sion of the cranial surface, only preserves part of the tarsal
cap and the proximal-most bit of metatarsal IV, but these
elements appear well fused, characteristic of or nithurine
birds; intermetatarsal fusion is poor or absent in enantior-
nithines (O’Connor et al. 2011b).
Genus Songlingornis Hou, 1997b
Songlingornis linghensis Hou, 1997b
(Fig. 5)
Revised diagnosis. A small ornithurine bird with the
unique combination of the following characters: dentary
straight and toothed; sternum elongate with a pair of
caudally located proximodistally elongate fenestrae that
taper distally; sternum lateral margin, single large lateral
(zyphoid) process; sternum with single free pair of robust
lateral trabeculae with large asymmetrical distal expansion;
and furcula U-shaped, with a flat and broad base (modified
from (Zhou et al. 2008b).
Material. IVPP V10913, single slab preserving the
impressions of several skull bones, the nearly complete
pectoral girdle, and partial wing and hind limb elements.
Stratigraphical distribution. Jiufotang Formation of the
Jehol Group, late Early Cretaceous, 125-120 Ma (Swisher
et al. 2002; He et al. 2004; Zhu et al. 2007).
Geographical distribution. Xidagou, Boluochi, Chao-
yang, western Liaoning Province, north-eastern China.
Morphology and remarks. Specimen IVPP V10913,
formerly a referred specimen of Chaoyangia and now
the holotype of Songlingornis linghensis, is a partial,
disarticulated skeleton, preserving only the impressions of
bones (Fig. 5). The rostral half of the skull i s preserved
slightly disarticulated. The premaxilla preserves two teeth
but the rostral tip is edentulous as in Yixianornis and
Yanornis (Zhou & Martin 2011). The poorly preserved
toothed maxilla has a long and delicate nasal process
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12 J. K. O’Connor and Z. Zhou
and a short jugal process, approximately half the length
of the premaxillary process. The dentary is straight and
toothed there are approximately six to eight teeth,
widely spaced proximally, and more densely spaced caudal
in the jaw. The teeth are slightly recurved apically and
constricted at the base of the crown. Voids of several
thoracic vertebrae suggest that the vertebral foramen
was proportionately wide. Several thoracic ribs are
also preserved; although their morphology is unclear,
they do not appear to be sigmoidal, as in Chaoyangia
(IVPP V9934).
The furcula is delicate and nearly U-shaped, similar to
that in Yixianornis (Clarke et al. 2006); as in this t axon,
the sternal margin at the interclavicular symphysis (apoph-
ysis) is straight so that the distal margin is not curved
throughout. The coracoid has a proximally located trian-
gular procoracoid process, with a straight cranial margin,
tapering into the shaft distally. A procoracoid process is only
known among ornithurines, although one enantiornithine
possesses a similar feature (Protopteryx; Zhang et al. 2000).
Both the medial and lateral margins are concave; the ster-
nal margin is straight and laterally expanded to form a
rectangular lateral process that does not project cranially,
a morphology common among basal ornithurines (e.g.
Longicrusavis, PKUP V1069). The sternum is similar to
that in Yixianornis and Yanornis (Clarke et al. 2006); the
rostral margin forms a tall apex, bounded by triangular
craniolateral processes (Fig. 5). The dorsal margin of the
coracoidal sulcus is contiguous with this process. A rectan-
gular lateral (zyphoid) process projects laterally for approx-
imately the middle quarter of the lateral margin; Yixi-
anornis possesses two lateral processes, the proximal one
much smaller than the other (IVPP V12631). The lateral
trabecula is directed caudolaterally and distally bears a
large asymmetric expansion that is wider medially (Fig. 5).
The caudal margin is rounded; it encloses a pair of large,
fenestra, caudolaterally bounded by a thin strap of bone.
The long axis of the fenestra i s craniocaudally oriented,
slightly angled proximolateral–mediodistally as in Yanor-
nis (IVPP V13358), and the distal margin is tapered so
that the fenestra is lachrymiform. The fenestrae preserved
in both Yanornis (IVPP V13358) and Yixianornis (IVPP
V12631) are proportionately wider, and the distal margin
is less tapered.
A carpometacarpus is also preserved, however not much
information can be discerned.
Ornithuromorpha indet. Hou et al., 1996
(Fig. 6)
Material. IVPP V9937, single slab preserving the impres-
sion of a partial hind limb.
Stratigraphical distribution. Jiufotang Formation of the
Jehol Group, late Early Cretaceous, 125–120 Ma (Swisher
et al. 2002; He et al. 2004; Zhu et al. 2007).
Geographical distribution. Xidagou, Boluochi, Chao-
yang, western Liaoning Province, north-eastern China.
Morphology and remarks. The isolated partial foot IVPP
V9937 (Fig. 6) assigned to Chaoyangia is either lumped
with this taxon or ignored; it has never been described,
and like Chaoyangia, its assignment to the derived clade
of birds was loosely based on limited information (Hou
et al. 1996). The specimen is a single slab preserving
the voids of an incomplete left tibiotarsus and foot as an
impression of its caudal surface (Fig. 6). The tibiotarsus
is very poorly preserved, missing both the proximal and
distal ends; the fibular crest is the only feature that can
be identified. It is short and appears rounded, although the
latter is most likely an artefact of preservation. The fibula
is preserved next to the crest and is fat proximally and
tapers to a sharp point. It extends for more than half of
the preserved tibiotarsus (Fig. 6). The lateral margin bears
a small tubercle located nearly at the bone’s midpoint,
presumably the attachment site of the m. iliofibularis.
The tubercle appears laterally directed; however, given
the preservation (impression), cranial projection would
largely not be visible and caudal projection is difficult to
Only the distal half (approximately) of the tarsometatar-
sus is preserved; the metatarsals appear highly fused
compared to primitive birds (e.g. Sapeornithiformes, Enan-
tiornithes; O’Connor et al. 2011b), although fusion was
not complete and the margins of individual metatarsals
can easily be discer ned. Weak intermetatarsal fusion char-
acterizes derived enantiornithines and basal ornithurines
(O’Connor 2009). The third metatarsal is the longest,
followed by the fourth and then the second. The metatarsals
end in the same plane, proximally and distally; prox-
imally, the impression is shallowest centrally, suggest-
ing that the caudal surface may have been slightly exca-
vated in this region. The dorsal excavation caused by the
caudal displacement of metatarsal III common in most
ornithuromorphs (e.g. Yanornis (IVPP V12558), Hong-
shanornis (IVPP V14533)) cannot be determined. The first
metatarsal is located high on the caudomedial surface of
the t arsometatarsus. A distal vascular foramen is located
between metatarsals III and IV as in other ornithurines
(e.g. Yixianornis, Gansus;Clarkeet al. 2006; You et al.
2006), and a second foramen may also have passed between
metatarsals II and III.
The hallux is very short; the proximal digit is slightly
longer than the small claw it bears (Fig. 6). The second
digit is formed by three phalanges; the first is twice the
length of that in the first digit. The second phalanx is
two-thirds of its size, followed by a small claw, approxi-
mately 50% larger than that of the hallux. The third digit is
very robust; t he first phalanx is larger than all other pedal
phalanges in all dimensions. The following two phalanges
reduce in size distally and articulate with the largest claw in
the foot. The fourth digit appears incomplete; three small,
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A redescription of Chaoyangia beishanensis 13
short phalanges (approximately the size of the first hallucal
phalanx) and a small claw are all that is preser ved. The
claw associated with the ungual of this digit is the small-
est and most delicate ungual of the foot. All digits bear
deep extensor pits and all claws are relatively small and
unrecurved as in other Jehol ornithurines (e.g. Yixianornis
(IVPP V12631), Yanornis (IVPP V13358), Hongshanornis
(IVPP V14533)).
The relative lengths of the metatarsals, their arrangement
(III long, I high), pedal proportions (longest phalanx proxi-
mal in digit), robust size of digit III, and the small size of the
claws are all consistent with a cursorial ecological habitat
(Hopson 2001; Zhang 2006). Interpretations of this taxon
as cursorial also support the inferred phylogenetic position,
with Jehol enantiornithines showing arboreal adaptations
such as large, recurved pedal claws while ornithurines are
more highly adapted for the ground.
Phylogenetic analysis
Chaoyangia IVPP V9934 was scored using the O’Connor
et al. (2011b) character list; Zhongjianornis, two confuciu-
sornithids (Jinzhouornis zhangjiyingia and Confuciusornis
dui), the enantiornithine Boluochia zhengi, and the recently
discovered ornithurines Jianchangornis microdonta and
Schizooura lii were also added to the matrix (see Online
Supplementary Material). Dalianornis cuhe, a taxon whose
avian status is controversial, was removed. This analy-
sis thus included 60 taxa scored across 245 characters,
making it the largest sampling of Mesozoic birds within
a single analysis to date. The dataset was analysed using
TNT (Goloboff et al. 2008). Thirty-one characters were
treated as ordered; all characters were weighted equally.
We conducted a heuristic search retaining t he single short-
est tree from every 1000 trees followed by an additional
round of tree bisection and reconnection (TBR) branch
swapping. A Nelson strict consensus tree was generated
from the resulting trees (Fig. 9). In order to determine how
the most fragmentary taxa affect the resolution of the resul-
tant tree, strict reduced consensus trees (Wilkinson 1999)
were generated using TNT (Goloboff et al. 2008) indi-
vidually removing Vorona, Zhongjianornis, and Chaoyan-
gia. In order to test the strength of alternative hypotheses,
constraint trees were built using TNT; the analysis was run
using the same parameters as in the first analysis and the
difference in tree lengths were compared.
The heuristic search, retaining the single shortest tree from
every 1000 trees, returned 17 trees of 836 steps. An addi-
tional round of TBR revealed 162 trees, 835 steps long.
The strict consensus of these trees resolves both Chaoyan-
gia and Zhongjianornis as basal ornithurines (Fig. 9).
As in most other analyses, Archaeopteryx is resolved
as the most basal bird; all other long-tailed birds form
an unresolved polytomy with the clade that includes all
more derived birds. Sapeornithiformes form the basal
pygostylian clade and Zhongornis is resolved as the confu-
ciusornithiform outgroup (or basalmost confuciusornithid).
The Zhongornis + Confuciusornithiformes clade for ms the
ornithothoracine outgroup. Enantiornithes is well resolved,
forming a series of ingroups; however, these relation-
ships are only weakly supported. Notably, Boluochia and
Longipteryx form a relationship, supporting interpretations
that these taxa are closely related (O’Connor et al. 2011a),
although a monophyletic Longipterygidae is no longer
supported (O’Connor et al. 2009), and Liaoningornis is
resolved as an enantiornithine ( O’Connor 2012), rather than
an ornithuromorph (Zhou & Zhang 2006a). Otogornis,a
fragmentary, rarely analysed taxon, is resolved as a basal
enantiornithine, contra the suggestion this taxon may be
closely related to Ambiortus (Kurochkin 1999).
Ornithurae (or Ornithuromorpha) is well resolved,
except for a polytomy of taxa with mainly basal char-
acters, which unfortunately includes the taxa in ques-
tion here. Archaeorhynchus is resolved as the basalmost
ornithurine; Patagopteryx, Jianchangornis, Schizooura,
Vorona, Zhongjianornis and Chaoyangia form a polytomy
outside all more derived taxa (Songlingornithidae, Hong-
shanornithidae and derived or nithuromorphs). The basal
positions of these taxa have been supported i n previous
cladistic analyses (Clarke et al. 2006; Zhou et al. 2009,
2012; O’Connor 2012).
The basal ornithurines, including Chaoyangia, show the
least resolution; Chaoyangia and Vorona are known from
fairly incomplete specimens, while the nearly complete
holotype of Zhongjianornis is poorly preserved. TNT
(Goloboff et al. 2008) was used to create strict reduced
consensus trees (Wilkinson 1999), removing each of these
taxa individually in order to try to increase resolution in
this polytomy. Removal of either Vorona or Zhongjianornis
does not affect the polytomy. However, excluding Chaoyan-
gia does increase resolution in this region of the tree. Alter-
native hypotheses suggest Chaoyangia may be related to
confuciusornithiforms (Clarke 2002). However, in this anal-
ysis constraint trees indicate the tree would have to be four
steps longer to accommodate t his relationship. To force a
similar relationship for Zhongjianornis, which was origi-
nally described as a basal pygostylian, tree length would be
at least 14 steps longer.
Phylogenetic problems
A comprehensive morphological review of Chaoyangia
beishanensis, one of the first birds from the Jehol Group,
supports initial hypotheses that this taxon is an ornithurine
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14 J. K. O’Connor and Z. Zhou
Downloaded by [Jingmai K. O’Connor] at 00:44 25 June 2012
A redescription of Chaoyangia beishanensis 15
bird (Hou et al. 1996). Although the only valid known spec-
imen of Chaoyangia is extremely fragmentary and reveals
limited anatomical information, when placed in a cladistic
analysis the resulting hypothesis concurs with morpholog-
ical observations. The results also support morphological
inferences that this taxon may be closely related to the more
complete Zhongjianornis, which is here also resolved as a
basal ornithurine.
The phylogenetic hypothesis resulting from the current
cladistic analysis is very weakly supported (CI: 0.389; RI:
0.670); however, given the fragmentary nature of the taxa
we seek to understand (e.g. Chaoyangia) and the lack of
resolution typical of recent cladistic analyses targeted at
Mesozoic birds (O’Connor et al. 2011b), any resolution
at all is encouraging. Adding two steps to the consen-
sus tree (L = 837) causes Enantiornithes and Ornithuro-
morpha to collapse. In trees of equal length, poorly
preserved and primitive taxa, particularly Zhongjianornis
and Chaoyangia, begin to move between the two major
ornithothoracine clades, sometimes resolved as basal enan-
tiornithines. Despite the inability of the cladistic analysis
to support strongly this hypothesis, Chaoyangia preserves
distinct features, such as an elongate synsacrum and a well
developed cnemial crest that are only known within the
ornithurine clade, and thus the results of this study concur
with initial studies (Hou et al. 1996), contra more recent
hypotheses (Clarke 2002).
On the other hand, Zhongjianornis, although nearly
complete and superficially similar to Chaoyangia, does not
definitively preserve any clear ornithurine synapomorphies,
largely due to poor preservation. No cnemial crest can be
observed on the tibiotarsus, which is in caudal view, the
number of fused sacral vertebrae is unknown, details of
the furcula are unclear (although it appears robust, similar
to Schizooura, IVPP V16861), and no sternum or cora-
coid can be observed. However, while the taxon might shift
between the two ornithothoracine clades in trees only two
steps longer than the most parsimonious tree, the chances
this taxon will be resolved again as a basal pygostylian
(Zhou et al. 2010) are low; this analysis required an addi-
tional 14 steps in order to resolve Zhongjianornis as a
basal pygostylian, suggesting that this relationship is not
likely. Given the limited morphological information avail-
able from this largely complete specimen, the phylogenetic
position of this taxon may continue to fluctuate until more
data are available, and until then the taxon should not be
considered unequivocally to be a member of any particular
clade, although research here suggests this taxon is likely
not a basal pygostylian.
Although each node within the consensus tree is
supported by numerous synapomorphies, t hese are coded
ambiguously in some taxa due to bad preservation, while
others are homoplastic, and Bremer support values for
the consensus tree are extremely low (Fig. 9). Preser-
vational differences between key collections of fossil
birds make it nearly impossible to i dentify synapomor-
phies that can be scored in all taxa for a given clade.
Meanwhile, many of the existing synapomorphies have
collapsed in light of the discovery of new morphologi-
cal diversity. For example, one recently described basal
ornithurine, Schizooura lii, although clearly ornithurine,
possesses a Y-shaped enantiornithine-like furcula, the cora-
coid lacks a lateral process, and the cranial surface of
the humerus is flat (Zhou et al. 2012), all features that
were until recently, within Ornithothoraces, restricted to
the enantiornithines. Despite these primitive features, previ-
ously unknown among Early Cretaceous members of this
derived clade, the taxon preser ves a typically ornithurine
craniocaudally elongate and largely imperforate sternum
with an extensive keel, features absent in another basal
Figure 9. Cladogram of the strict consensus tree (length, 835 steps) showing the hypothetical phylogenetic relationships of these Mesozoic
birds. Note that Chaoyangia and Zhongjianornis are resolved as basal ornithurines. Only unambiguous synapomorphies are considered
here; all synapomorphies are strict, unless stated otherwise. Sapeornithiformes is s upported by two synapomorphies: 130, fenestrated
deltopectoral crest (homoplastic); 154, semilunate carpal fused to the major and minor metacarpal (coding uncertain in some taxa).
Confuciusornithiformes is supported by three synapomorphies: 173, ungual phalanx of major digit smaller than of the alular and minor
digits; 174, proximal phalanx of minor digit much shorter than the following phalanges; 232, J-shaped metatarsal I with articular surface
planes perpendicular (coding uncertain in some taxa). Ornithothoraces is supported by 11 ambiguous synapomorphies: 26, pneumatic
quadrate; 46, caudal mandibular fenestra absent; 56, 11–12 thoracic vertebrae; 61, thoracic vertebrae laterally excavated; 84, scapula
articulating below the shoulder end on coracoid; 92, supracoracoidal nerve foramen displaced medially; 105, interclavicular angle less
than 70
; 114, rostral margin of sternum broad and rounded; 150, semilunate ridge on dorsal condyle of ulna; 215, condyles of the tibiotarsus
equal in cranial projection; 244, alula present. Enantiornithes is supported by 11 synapomorphies (coding uncertain in some taxa): 34
dentary teeth present (reversal); 78, pygostyle distally constricted; 106, furcula dorsolaterally excavated; 107, elongate hypocleidium
present; 123, humerus proximal margin centrally concave, rising dorsally and ventrally; 126, ventral tubercle separated from humeral head
by a deep capital incision; 139, humerus distal margin angled to long axis of shaft (homoplastic); 142, humerus distal condyles weakly
defined; 167, minor metacarpal projects distally more than major metacarpal; 203, femoral posterior trocanter hypertrophied (reversal);
221, distal tarsals free (reversal). Ornithuromorpha is supported by four synapomorphies (coding uncertain in some taxa): 96, curved
scapular shaft (homoplastic); 160, shelf-like articular surface on alular metacarpal for alular digit; 168, alular digit short (homoplastic);
212, cnemial crests on tibiotarsus (homoplastic). Consistency index: 0.389; retention index: 0.670. Values listed at nodes indicate absolute
and relative Bremer support.
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16 J. K. O’Connor and Z. Zhou
ornithurine, Archaeorhynchus, whose sternal morphology
is reminiscent of enantiornithines (Zhou & Zhang 2006a).
This mosaic distribution of morphologies among taxa and
the dwindling number of clear morphological differences
between Enantiornithes and Ornithurae as basal taxa are
uncovered has diminished the number of synapomorphies
in support of each node, resulting in weak support for most
traditional clades (e.g. Enantiornithes, Ornithuromorpha,
Ornithothoraces) and a collapse in others (e.g. Pygostylia,
Longipterygidae). The only way to rectify this problem is to
identify new synapomorphies for each clade and increase
the amount of morphological data incorporated into the
character matrix, no easy task given the varying preserva-
tional limitations set by the known diversity and the rapid
rate of discovery in China. Currently, all synapomorphies in
support of Ornithothoraces, Enantiornithes, and Ornithuro-
morpha are ambiguous because of the large number of
taxa and substantial amount of preservational variability
between specimens.
Despite the fact that increasing the number of included
taxa causes a decrease in s upport at certain nodes, it
is also only because of this large taxonomic diversity
that Zhongjianornis and Chaoyangia were recognized
as ornithurine birds. When an analysis includes a small
number of complete taxa which only reflect more derived
ornithurines (e.g. Hongshanornis, Yixianornis , Apsar-
avis, Gansus, Ichthyornis), the analysis will be unable
recognize a relationship with very primitive members
and their disparate morphologies. The current analy-
sis included a very large number of basal ornithurine
taxa (ornithuromorphs), including recent discoveries
such as Archaeorhynchus and Schizooura that preserve
‘enantiornithine-like’ morphologies. Although the results
of this analysis exemplify the increasing resolution among
hypothetical Mesozoic bird relationships that results from
the increase in taxa and morphological data, the increase
in recently discovered taxa with previously unknown
morphological combinations of primitive and derived
characters have also reduced the strength of the resulting
hypothetical relationships.
Tooth loss
All modern birds possess a beak and no teeth, and thus
the loss of teeth among Mesozoic birds is an important
step in the evolution of the modern avian rostrum. Teeth
have been lost within Dinosauria on multiple occasions
(e.g. ornithomimosaurs, oviraptorosaurs), and several times
within Aves alone (Makovicky et al. 2004). Tooth loss
is common among basal birds, with Sapeornithiformes
and Jeholornithiformes both having reduced their denti-
tion, while Confuciusornithiformes have lost their teeth
entirely (O’Connor et al. 2011b); Zhongjianornis, which is
interpreted as a basal pygostylian, exemplifies this pattern.
Among basal ornithurines, several edentulous taxa are also
recognized: Archaeorhynchus, potentially the hongshanor-
nithids, and Zhongjianornis (Zhou & Zhang 2005, 2006a;
O’Connor et al. 2010). With basal taxa resolved in a poly-
tomy, it is impossible to determine the pattern of loss
within this clade; however, we can infer that teeth were lost
on multiple occasions: the edentulous Archaeorhynchus is
resolved as the basalmost taxon while derived ornithurines
Ichthyornis and Hesperornis retain teeth. Tooth loss among
enantiornithines, however, is not as common, with only one
Late Cretaceous taxon known to be edentulous and a clade
of Early Cretaceous taxa that have lost their maxillary teeth
(Elzanowski 1976; O’Connor et al. 2011a). This may reflect
dietary differences between the two ornithothoracine clades
that may relate to the eventual extinction of the larger and
more successful Mesozoic clade, Enantiornithes.
We thank Liu Xinzhen and Jia Liantao for prepar-
ing casts and photographs, respectively. We thank the
Chinese National Natural Science Foundation (Grant KA
210417, 41172020), the Fellowship for Young International
Scientists of the Chinese Academy of Sciences (Grant
KC 210201) and National Basic Research Program of
China (973 Program no. 2012CB821906) for funding this
Supplementary material
Supplementary material can be viewed online
doi:10.1080/14772019.2012.690455. [doi should be article
tag to title page on the website]
Alvarenga, H. M. F. & Bonaparte, J. F. 1992. A new flightless
landbird from the Cretaceous of Patagonia. Pp. 51–64 in K.C.
Campbell, Jr (ed.) Papers in Avian Paleontology Honoring
Pierce Brodkorb. Natural History Museum of Los Angeles,
Los Angeles.
Baumel, J. J. & Witmer, L. M. 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.
Bell, A., Chiappe, L. M., Erickson,G.M., Suzuki, S., Watabe ,
M., Barsbold, R. & Tsogtbaatar, K. 2010. Description and
ecologic analysis of Hollanda luceria, a Late Cretaceous bird
from the Gobi Desert (Mongolia). Cretaceous Research, 31,
Chiappe, L. M. 2002. Basal bird phylogeny: problems and solu-
tions. Pp. 448–472 in L.M. Chiappe and L.M. Witmer (eds)
Mesozoic Birds: Above the Heads of Dinosaurs. University of
California Press, Berkeley.
Chiappe, L. M. 2007. Glorified Dinosaurs: the Origin and Early
Evolution of Birds. John Wiley & Sons, Hoboken, 263 pp.
Chiappe, L. M. & Calvo, J. O. 1994. Neuquenornis volans,a
new Late Cretaceous bird (Enantiornithes: Avisauridae) from
Patagonia, Argentina. Journal of Vertebrate Paleontology, 14,
Downloaded by [Jingmai K. O’Connor] at 00:44 25 June 2012
A redescription of Chaoyangia beishanensis 17
Chiappe, L. M. & Walker, C. A. 2002. Skeletal morphology and
systematics of the Cretaceous Euenantiornithes (Ornithotho-
races: Enantiornithes). Pp. 240–267 in L. M. Chiappe & L. M.
Witmer (eds) Mesozoic Birds: Above the Heads of Dinosaurs.
University of California Press, Berkeley.
Chiappe, L. M., Ji, S., Ji, Q. & Norell, M. A. 1999. Anatomy and
systematics of the Confuciusornithidae (Theropoda: Aves)
from the Late Mesozoic of northeaster n China. Bulletin of
the American Museum of Natural History, 242, 1–89.
Clark, J. M., Norell,M.A.& Chiappe,L.M.1999. An ovirap-
torid skeleton from the Late Cretaceous of Ukhaa Tolgod,
Mongolia, preserved in an avianlike brooding position over
an oviraptorid nest. American Museum Novitates, 3265, 1–36.
Clarke, J. A. 2002. The morphology and systematic position of
Ichthyornis Marsh and the phylogenetic relationships of basal
Ornithurae. Unpublished PhD thesis, Yale University, New
Haven. 532 pp.
Clarke,J.A.2004. Morphology, phylogenetic taxonomy, and
systematics of Ichthyornis and Apatornis (Avialae: Ornithu-
rae). Bulletin of the American Museum of Natural History,
286, 1–179.
Clarke, J. A. & Norell, M. A. 2001. Fossils and avian evolution.
Nature, 414, 508.
Clarke, J. A., Zhou, Z. & Zhang, F. 2006. Insight into the evolu-
tion 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.
Codd, J. R., Manning, P. L., Norell, M. A. & Perry, S. F. 2008.
Avian-like breathing mechanics in maniraptoran dinosaurs.
Proceedings of the Royal Society of London, Series B, 275,
Elzanowski, A. 1976. Paleognathous bird from the Cretaceous of
central Asia. Nature, 264, 51–53.
Elzanowski, A. 2002. Archaeopterygidae (Upper Jurassic of
Germany). Pp. 129–159 in L. M. Chiappe & L. M. Witmer
(eds) Mesozoic Birds: Above the Heads of Dinosaurs.Univer-
sity of California Press, Berkeley.
Forster, C. A., Chiappe, L. M.
, Krause, D. W. & Sampson, S.
D. 1996. The fi rst Cretaceous bird from Madagascar. Nature,
382, 532–534.
Gao, C., Chiappe, L. M., Meng, Q., O’Connor, J., Wang , X.,
Cheng, X. & Liu, J. 2008. A new basal lineage of Early Creta-
ceous birds from China and its implications on the evolution
of the avian tail. Palaeontology, 51(4), 775–791.
Gauthier, J. & de Queiroz, K. 2001. Feathered dinosaurs, flying
dinosaurs, crown dinosaurs, and the name Aves’. Pp. 7–41
in J. Gauthier and L.F. Gall (eds) New Perspectives on the
Origin and Early Evolution of Birds. Peabody Museum of
Natural History, New Haven.
Goloboff, P. A., Farris, J. S. & Nixon,K.C.2008. TNT, a free
program for phylogenetic analysis. Cladistics, 24, 774–786.
Haeckel, E. 1866. Generelle Morphologie der Organismen.
Verlag von Georg Reimer, Berlin, 462 pp.
He, H. Y., Wang,X.L., Zhou,Z.H., Zhu, R. X., Jin, F.,
Wang, F., Ding, X. & Boven, A. 2004. 40Ar/39Ar dating
of ignimbrite from Inner M ongolia, northeastern China, indi-
cates a post-Middle Jurassic age for the overlying Daohugou
Bed. Geophysical Research Letters, 31(20), L20609.
Hopson, J. A. 2001. Ecomorphology of avian and nonavian
theropod phalangeal proportions: implications for the arbo-
real versus terrestrial origin of bird flight. Pp. 211–235 in J.
Gauthier & L. F. Gall (eds) New Perspectives on the Origin
and Early Evolution of Birds. Peabody Museum of Natural
History, New Haven.
Hou, L. 1997a. A carinate bird from the Upper Jurassic of western
Liaoning, China. Chinese Science Bulletin, 42, 413–416.
Hou, L. 1997b. Mesozoic Birds of China. Feng-huang-ku Bird
Park, Taiwan, 221 pp.
Hou, L. & Liu, Z. 1984. A new fossil bird from Lower Cretaceous
of Gansu and early evolution of birds. Scientia Sinica, Series
B, 27, 1296–1301.
Hou, L. & Zhang, J. 1993. A new fossil bird from Lower Creta-
ceous of Liaoning. Vertebrata Palasiatica, 31, 217–224.
Hou, L., Martin, L. D., Zhou, Z. & Feduccia, A. 1996. Early
adaptive radiation of birds: evidence from fossils from north-
eastern China. Science, 274, 1164–1167.
Howard, H. 1929. The avifauna of Emeryville shellmound.
University of California Publications in Zoology, 32(2),
Ji, S. 2006. Furculae of non-avian theropods and basal birds.
Pp. 115–128 in J. L
u, Y. Kobayashi, D. Huang & Y.-N. Lee
(eds) Papers from the 2005 Heyuan International Dinosaur
Symposium. Geological Publishing House, Beijing.
Kurochkin, E. N. 1982. New order of birds from the Lower Creta-
ceous in Mongolia. Paleontological Journal, 1982, 215–218.
Kurochkin, E. N. 1999. The relationships of the Early Cretaceous
Ambiortus and Otogornis (Aves: Ambiortiformes). Smithso-
nian Contributions to Paleobiology, 89, 275–284.
Li, D.-S., Sullivan, C., Zhou, Z.-H. & Zhang, F.-C. 2010. Basal
birds from China: a brief review. Chinese Birds, 1, 83–96.
Linnaeus, C. 1758. Systema naturae per regna tria naturae,
secundum classes, ordines, genera, species, cum charac-
teribus, differentiis, s ynonymis, locis. Vol. 1: Regnum animale.
Editio decima, reformata. Laurentii Salvii, Stockholm,
824 pp.
Makovicky, P. J., Kobayashi, Y. & Currie, P. J. 2004. Ornithomi-
mosauria. Pp. 137–150 in D. B. Weishampel, P. Dodson & H.
olska (eds) The Dinosauria. 2nd edition. University of
California Press, Berkeley.
Mayr, G., Pohl, B. & Peters,D.S.2005. A well-preserved
Archaeopteryx specimen with theropod features. Science,
Norell,M.A.& Mackovicky, P. J. 1999. Important features of the
dromaeosaurid skeleton II: information from newly collected
specimens of Velociraptor mongoliensis. American Museum
Novitates, 3282, 1–45.
O’Connor, J. K. 2009. A systematic review of Enantiornithes
(Aves: Ornithothoraces). Unpublished PhD Thesis, University
of Southern California, Los Angeles, 600 pp.
O’Connor, J. 2012. A revised look at Liaoningornis longidigitrus
(Aves). Vertebrata Palasiatica, 5(1), 25–37.
O’Connor, J. K., Wang, X . -R., Chiappe,L.M., Gao, C.-H.,
Meng, Q.-J., Cheng, X.-D. & Liu, J.-Y. 2009. Phylogenetic
support for a specialized clade of Cretaceous enantiornithine
birds with information from a new species. Journal of Verte-
brate Paleontology, 29, 188–204.
O’Connor, J. K., Gao, K.-Q. & Chiappe, L. M. 2010. A new
ornithuromorph (Aves: Ornithothoraces) bird from the Jehol
Group indicative of higher-level diversity. Journal of Verte-
brate Paleontology, 30, 311–321.
O’Connor, J., Zhou, Z.-H. & Zhang, F.-C. 2011a. A reappraisal
of Boluochia zhengi (Aves: Enantiornithes) and a discussion
of intraclade diversity in the Jehol avifauna, China. Journal
of Systematic Palaeontology, 9, 1–13.
O’Connor, J. K., Chiappe, L. M. & Bell, A. 2011b. Pre-modern
birds: avian divergences in the Mesozoic. Pp. 39–114 in G. D.
Dyke & G. Kaiser (eds) Living Dinosaurs: the Evolutionary
History of Birds.J.Wiley&Sons,NewJersey.
O’Connor, P. M. & Forster, C. A. 2010. A Late Creta-
ceous (Maastrichtian) avifauna from the Maevarano Forma-
tion, Madagascar. Journal of Vertebrate Paleontology, 30,
Downloaded by [Jingmai K. O’Connor] at 00:44 25 June 2012
18 J. K. O’Connor and Z. Zhou
Sereno, P. C. & Rao, C. 1992. Early evolution of avian flight and
perching: new evidence from the Lower Cretaceous of China.
Science, 255, 845–848.
Swisher, C. C., III, Wang, X., Zhou, Z., Wa n g , Y. , Jin, F.,
Zhang, J., Xu, X., Zhang, F. & Wang, Y. 2002. Further
support for a Cretaceous age for the feathered-dinosaur beds
of Liaoning, China: new 40Ar/39Ar dating of the Yixian
and Tuchengzi formations. Chinese Science Bulletin, 47(2),
Tickle,P.G., Ennos, A. R., Lennox, L. E., Perry, S. F. &
Codd, J. R. 2007. Functional significance of the uncinate
processes in birds. Journal of Experimental Biology, 210,
Wilkinson, M. T. 1999. Choosing and interpreting a tree for
the oldest Mammal. Journal of Vertebrate Paleontology, 19,
You, H.-L., Lamanna, M. C., Harris, J. D., Chiappe, L . M.,
O’Connor, J., Ji, S.-A., L
u, J.-C., Yuan, C.-X., Li, D.-Q.,
Zhang, X., Lacovara, K. J., Dodson, P. & Ji, Q. 2006. A
nearly modern amphibious bird from the Early Cretaceous of
northwestern China. Science, 312, 1640–1643.
Zhang, F., Zhou, Z., Hou, L. & Gu, G. 2000. Early diversification
of birds: evidence from a new opposite bird. Kexue Tongbao,
, 2650–2657.
Zhang, Y.-G. 2006. Morphology of the distal tarsometatarsus
and perching habits in birds. Sichuan Journal of Zoology, 25,
Zhang, Y.-G., Zhang, L.-F., Li, J.-J. & Li, Z.-H. 2010. New
discovery and flying skills of Cathayornis from the Lower
Cretaceous strata of the Otog Qi in Inner Mongolia, China.
Geological Bulletin of China, 29, 988–992.
Zhou, Z. 1999. Early evolution of birds and avian flight—
evidence from Mesozoic f ossils and modern birds. P. 216.
University of Kansas, Lawrence.
Zhou, S., Zhou, Z.-H. & O’Connor, J. K. 2012. A new toothless
ornithurine bird (Schizooura lii gen. et sp. nov.) from the
Lower Cretaceous of China. Vertebrata Palasiatica, 50(1),
Zhou, Z. 1995. Discovery of a new enantiornithine bird from the
Early Cretaceous of Liaoning, China. Vertebrata Palasiatica,
33, 99–113.
Zhou, Z. & Hou, L. 2002. The discovery and study of Meso-
zoic birds in China. Pp. 160–183 in L. M. Chiappe & L. M.
Witmer (eds) Mesozoic Birds: Above the Heads of Dinosaurs.
University of California Press, Berkeley.
Zhou, Z.-H. & Martin, L. D. 2011. Distribution of the predentary
bone in Mesozoic ornithurine birds. Journal of Systematic
Palaeontology, 9, 25–31.
Zhou, Z.-H. & Wang, Y. 2010. Major features of the vertebrate
diversity of the Early Cretaceous Jehol Biota and their paleoe-
cological implications. Journal of Earth Science, 21 (Special
Issue), 228–230.
Zhou, Z. & Zhang, F. 2001. Two new ornithurine birds from the
Early Cretaceous of western Liaoning, China. Kexue Tongbao,
46, 371–377.
Zhou, Z. & Zhang, F. 2003a. Anatomy of the primitive bird
Sapeornis chaoyangensis from the Early Cretaceous of Liaon-
ing, China. Canadian Journal of Earth Sciences, 40, 731–
Zhou, Z. &
Zhang, F. 2003b. Jeholornis compared to
Archaeopteryx, with a new understanding of the earliest avian
evolution. Naturwissenschaften, 90, 220–225.
Zhou, Z. & Zhang, F. 2005. Discovery of an ornithurine bird and
its implication for Early Cretaceous avian radiation. Proceed-
ings of the National Academy of Sciences, 102, 18998–
Zhou, Z.-H. & Zhang, F.-C. 2006a. A beaked basal ornithurine
bird (Aves, Ornithurae) from the Lower Cretaceous of China.
Zoologica Scripta, 35, 363–373.
Zhou, Z.-H. & Zhang, F.-C. 2006b. Mesozoic birds of
China a synoptic review. Vertebrata Palasiatica, 44,
Zhou, Z., Jin, F. & Zhang, J. 1992. Preliminary report on a Meso-
zoic bird from Liaoning, China. Chinese Science Bulletin, 37,
Zhou, Z.-H., Wang, X.-L. , Zhang, F.-C. & Xu, X. 2000.
Important features of Caudipteryx evidence from two
nearly complete new specimens. Vertebrata Palasiatica, 38,
Zhou, Z., Barrett, P. M. & Hilton, J. 2003. An exception-
ally preserved Lower Cretaceous ecosystem. Nature, 421,
Zhou, Z., Clarke, J., Zhang, F. & Wings, O. 2004. Gastroliths in
Yanornis: an indication of the earliest radical diet-switching
and gizzard plasticity in the lineage leading to living birds.
Naturwissenschaften, 91, 571–574.
Zhou, Z., Chiappe, L. M. & Zhang, F. 2005. Anatomy of the
Early C retaceous bird Eoenantiornis buhleri (Aves: Enantior-
nithes) from China. Canadian Journal of Earth Sciences, 42,
Zhou, Z., Clarke, J. & Zhang, F. 2008a. Insight into diversity,
body size and morphological evolution from the largest Early
Cretaceous enantiornithine bird. Journal of Anatomy, 212,
Zhou, Z., Zhang, F. & Hou, L.-H. 2008b. Aves. Pp. 337–378 in
J.Li,G.Wu&F.Zhang(eds)The Chinese Fossil Reptiles and
Their Kin. Science Press, Beijing.
Zhou, Z.-H., Zhang, F.-C. & Li, Z.-H. 2009. A new basal
ornithurine bird (Jianchangornis microdonta gen. et sp. nov.)
from the lower Cretaceous of China. Vertebrata PalAsiatica,
47, 299–310.
Zhou, Z.-H., Zhang, F.-C. & Li, Z.-H. 2010. A new lower creta-
ceous bird from China and tooth reduction in early avian
evolution. Proceedings of the Royal Society of London, Series
B, 277, 219–227.
Zhu, R., Pan, Y ., Shi, R., Liu, Q. & LI, D. 2007. Palaeomagnetic
and 40Ar/39Ar dating constraints on the age of the Jehol Biota
and the duration of depostion of the Sihetun fossil-bearing
lake sediments, northeast China. Cretaceous Research, 28,
Downloaded by [Jingmai K. O’Connor] at 00:44 25 June 2012
... In recent analyses, Bremer support is typically very low Wang et al., 2018a). This likely reflects similarities between early-diverging ornithuromorphs and enantiornithines that have blurred the distinction between these two major clades and not missing data (O'Connor and Zhou, 2013). Take, for example, the taxon Schizooura lii: although clearly a member of the Ornithuromorpha, this species possesses a Y-shaped enantiornithine-like furcula; the coracoid lacks a lateral process (at one time a synapomorphy of the Ornithuromorpha); and the cranial surface of the humerus is flat (Zhou et al., 2012). ...
... Chaoyangia preserves two features observed clearly only in ornithuromorphs, but sometimes is resolved in the Enantiornithes, and thus a wellresolved tree can be found only if it is excluded . In many recent analyses, Ornithothoraces forms a single clade in trees only one or two steps longer than the most parsimoni-ous solution (O'Connor and Zhou, 2013;Wang et al., 2018a). This mosaic distribution of morphologies among taxa and the dwindling number of clear morphological differences between the Enantiornithes and the Ornithuromorpha as early-diverging taxa are uncovered has diminished the number of synapomorphies in support of each node, resulting in weak support for most traditional clades Zelenkov, 2017). ...
... This mosaic distribution of morphologies among taxa and the dwindling number of clear morphological differences between the Enantiornithes and the Ornithuromorpha as early-diverging taxa are uncovered has diminished the number of synapomorphies in support of each node, resulting in weak support for most traditional clades Zelenkov, 2017). The only way to increase support is to identify new synapomorphies for each clade and increase the amount of morphological data incorporated into the character matrix, no easy task given the varying preservational limitations set by the known diversity and the rapid rate of discovery principally in China (O'Connor and Zhou, 2013), but also elsewhere (de Souza Carvalho et al., 2015;Atterholt et al., 2018). Currently, all synapomorphies in support of Ornithothoraces, Enantiornithes, and Ornithuromorpha are ambiguous because of the large number of taxa and substantial amount of preservational variability between specimens. ...
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... A keratinous beak was absent in the earliest bird, Archaeopteryx, which had a fully toothed rostrum (Elzanowski, 2002;Mayr et al., 2005;Rauhut et al., 2018). Tooth reduction and an edentulous rostrum evolved numerous times during the Mesozoic evolution of Aves given the phylogenetic distribution of edentulous clades and clades containing edentulous taxa (O'Connor et al., 2011(O'Connor et al., , 2016O'Connor and Zhou, 2013;. The oldest and most basal occurrence of a toothless rostrum in Aves is in the Early Cretaceous basal pygostylian clade, the Confuciusornithiformes, in the oldest and most primitive member of this clade -Eoconfuciusornis from the 131 Ma Huajiying Formation (Hou et al., 1995b;Zhang et al., 2008). ...
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The keratinous beak is inferred to have evolved multiple times in the Archosauria and in Aves. Unfortunately, this feature rarely preserves in the fossil record. Here we examine a collection of 603 specimens belonging to the Confuciusornithiformes, a clade of edentulous basal avians, only two of which preserve visible traces of the rhamphotheca. Preservation is very different between the two specimens, offering no clues as to the taphonomic conditions that are conducive to preservation of this feature. These differences suggest that preservation of the rhamphotheca is not limited to a very narrow set of specific chemical conditions. We suggest the more common preservation of feathers over rhamphotheca is due to the higher melanin content in the former. The well-preserved traces in one specimen described here suggests that the rhamphotheca covering the upper and lower jaws each may consist of a pair of right and left elements, thus differing from the condition in neornithines in which the premaxillary nail and mandibular nail covering the rostral half of the upper and lower jaws respectively each form a single unit.
... Although Protopteryx fengningensis (Zhang and Zhou, 2000) is arguably one of the most important enantiornithines, until recently very little was known about this taxon (Chiappe et al., 2019a). Not only is Protopteryx among the oldest known members of the Enantiornithes, but it is commonly resolved as the basal-most known species in this clade (Atterholt et al., 2018;O'Connor and Zhou, 2013;Wang et al., 2018a), commonly sharing this position with pengornithids (represented in the Huajiying Formation by Eopengornis) (Wang et al., 2014b) and Iberomesornis, a Spanish taxon from deposits interpreted to be only slightly younger (Barremian in age) (Sanz et al., 2002). For nearly two decades following the initial publication (Zhang and Zhou, 2000), little new morphological information surfaced regarding this important taxon despite major alterations in our interpretations of its geologic provenance (formerly regarded as Yixian Formation) (He et al., 2006;Pan et al., 2013;Yang et al., 2020) and the structure of the tail feathers (originally described as elongate scales) . ...
Protopteryx fengningensis is from the 130.7 Ma Huajiying Formation making it one of the oldest known enantiornithines. Contributing to its significance, this taxon is also commonly resolved as the basal-most enantiornithine in phylogenetic analyses. Protopteryx preserves several unusual morphologies that are otherwise absent in the Enantiornithes but common in the Ornithuromorpha such as the procoracoid and lateral processes on the coracoid and proximally convex humeral head. Thus, the morphology of this taxon hints at the morphology of the ornithothoracine common ancestor. Here we supplement existing data with information from a new specimen as well as new morphological data from the holotype and paratype. The new specimen preserves gaps in the right wing suggestive of a sequential molt. The presence of two gaps suggests that, unlike neornithines, primaries and secondaries molted simultaneously. This represents an intermediate condition between Microraptor, in which several feathers are growing simultaneously and sequentially, and modern birds with sequential molts, in which a single feather is replaced at a time. A single patch of feathers was sampled revealing preserved eumelanosomes, indicating that at least part of the remiges was darkly colored.
We describe six specimens consisting of cranial remains and associated partial presacral axial series belonging to ornithuromorph birds from the Changma locality of the Lower Cretaceous Xiagou Formation of northwestern Gansu Province, China. Comparison among specimens is limited by the paucity of overlapping elements, their differing exposed views, and, in some specimens, poor preservation. Despite this, three separate taxa are represented, evidenced by differences in their dentary dentitions: one specimen is edentulous, another has sharp, closely spaced, relatively high-crowned and peg-like teeth, and a third preserves blunt, relatively low-crowned teeth placed in a communal groove, a morphology previously reported among adult birds only in Hesperornithiformes. We propose that the high-crowned specimen may be referred to Gansus yumenensis based on shared similarities with the closely related Iteravis huchzermeyeri, including a very similar dentition and an edentulous premaxilla with elongate, unfused frontal processes and no palatal processes. The two other specimens are considered new taxa, for which we erect the names Meemannavis ductrix gen. et sp. nov. and Brevidentavis zhangi gen. et sp. nov. These new specimens confirm that the Changma locality is dominated by ornithuromorph birds and contribute to a better understanding of this important avifauna. The observed variation in dental morphology hints at trophic diversity like that observed in ornithuromorphs from the penecontemporaneous Jehol Group of northeastern China. This article is protected by copyright. All rights reserved.
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The ontogenetic development of extant birds is characterized by rapid growth, bone fusion and an early onset of flight ability. In contrast, little is known about how these ontogenetic traits evolved in the bird stem lineage, and the available data pertains primarily to Enantiornithes. Here, we describe an almost complete skeleton of a juvenile euornithine bird (LNTU-WLMP-18) from the Early Cretaceous Jiufotang Formation (Aptian), which was discovered near Lamadong Town (Jianchang County, Liaoning, China). Despite its completeness, bone preservation is rather poor. Thus, to increase the contrast between bone tissue and matrix, we used cyan-red-based autofluorescence photography. The specimen is more or less articulated and exposed in ventral aspect. The jaws are edentulous, the coracoid bears a procoracoid process, and the ischium lacks a proximodorsal process. The pedal unguals are short and barely curved, indicating a ground-dwelling lifestyle. Feathers, including long primaries, are present as carbonized traces. Several characters indicate that LNTU-WLMP-18 is a juvenile: the bone surface has a coarsely striated texture and no fusion is evident between the carpals and metacarpals, between the tibia and the astragalus and calcaneum, or among the metatarsals. Although juvenile characters have the potential to impede accurate identification of the specimen, morphological comparisons and cladistic analysis identify LNTU-WLMP-18 as most likely referable to the basal euornithine Archaeorhynchus, which would make the specimen the first juvenile bird from the Jehol Group that could be assigned to a specific taxon. Based on its size and the incomplete ossification of the bone surface, LNTU-WLMP-18 represents the smallest and therefore youngest known individual of this genus. A statistical comparison of limb proportions shows that the forelimbs of LNTU-WLMP-18 are significantly shorter than the hindlimbs, while the forelimbs are longer than the hindlimbs in subadult and adult individuals. This is different from the situation in some Enantiornithes, in which the forelimbs exceed the length of the hindlimbs even in hatchlings. Similar to Enantiornithes, Archaeorhynchus probably exhibit an early onset of flight ability, as indicated by the extensive wing plumage in LNTU-WLMP-18. Finally, the lack of gastroliths in the visceral cavity might indicate a dietary shift in Archaeorhynchus during ontogeny. As a small-bodied, ground-dwelling, seed-eating bird with a precocial ontogeny, Archaeorhynchus filled an ecological niche that later allowed early crown birds to survive the K-Pg mass extinction.
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Multiple factors involved in the evolutionary transformation of the manus across the maniraptoran radiation, including its current morphology in modern birds, remain unexplored. Specifically, the morphological disparity of the manus has never been studied quantitatively, and there are no hypotheses about the possible mechanisms and constraints underlying its evolution. Morphological disparity is best studied with shape-analysis tools based on Procrustes methods, because they guarantee the independence of shape from size while depicting the results in expressive graphics. However, this methodology compares fixed configurations of coordinates, preventing their use in highly articulated and movable structures such as the maniraptoran manus. Here, we propose a new protocol, the one-dimensional Procrustes analysis (OPA), for transforming the chord lengths of these bones into unidimensional Cartesian coordinates, enabling treatment of the data under the operational advantages of the Procrustes methods. Our results applying this new method on a sample encompassing 174 maniraptoran dinosaurs manus, including 79 fossils (both avialan and nonavialan taxa) and 95 extant paleognathans and neognathans, document the morphological transition between early-diverging maniraptorans, nonavialan paravians, and birds over morphospace, highlighting an unexpectedly low disparity in the crown group when compared to early-diverging taxa. Within this transition, we show a common trend of proportional reduction and loss of distal elements, mostly in the minor and alular digits. Furthermore, our study reveals an allometric pattern characterizing manus morphological variation between early-diverging maniraptorans and enantiornithine avialans that disappears in crown birds and their closest early-diverging counterparts. This previously unnoticed allometric trend suggests a complex interplay of developmental, functional, and historical constraints in the evolution of the maniraptoran manus.
Many specimens of the basal bird Jeholornis from the Early Cretaceous Jehol Biota of northeast China include one or two distinctive paddle-shaped skeletal elements preserved in the thoracic region. These ossifications have generally been identified as lateral trabeculae, paired processes of the sternum that are common within the derived avian clade Ornithothoraces. In extant birds, lateral trabeculae define membrane-filled embayments or fenestrae in the caudal portion of the sternum that contribute to the area available for attachment of the pectoralis musculature, which drives the downstroke in flight. The presence of lateral trabeculae in Jeholornis would thus suggest a proportionally larger M. pectoralis, and a more powerful downstroke, than in other non-ornithothoracine avians. However, previously undescribed specimens of Jeholornis reveal that the paddle-shaped elements are actually anomalously expanded sternal ribs, the caudalmost of four pairs in the ribcage. Accordingly, lateral trabeculae are absent in Jeholornis, dovetailing with other evidence that basal birds lack many components of the sophisticated flight apparatus typical of ornithothoracines. The expanded sternal ribs represent a striking, and somewhat functionally enigmatic, autapomorphy of Jeholornis. In many pterosaurs the sternal ribs bear multiple small prominences, the sternocostapophyses, that probably improved the mechanical advantage of ribcage musculature involved in ventilation and increased the area for muscle attachment. The sternal rib expansions seen in Jeholornis presumably served a similar purpose, and are among a suite of derived features of this taxon that appear to represent adaptations for the demands of powered flight but only partially parallel those independently acquired by ornithothoracines.
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The Cretaceous birds of Alberta are poorly known, as skeletal elements are rare and typically consist of fragmentary postcranial remains. A partial avian coracoid from the upper Campanian Dinosaur Park Formation of Alberta, Canada can be referred to the Ornithurae, and is referred to here as Ornithurine G (cf. Cimolopteryx). Its structure is similar to previously described ornithurine coracoids from Alberta and other localities in North America, particularly those belonging to the genus Cimolopteryx. A comparison of these elements indicates that the new coracoid is distinct; however, its preservation prevents complete diagnosis. As other Cimolopteryx are Maastrichtian in age, Ornithurine G (cf. Cimolopteryx) also represents the earliest occurrence of a Cimolopteryx-like anatomy. A pneumatized coracoid is a diagnostic trait of Neornithes, often associated with the presence of a pneumatic foramen. Ornithurine G (cf. Cimolopteryx) does not preserve this feature. CT and micro-CT scans of both pneumatic and apneumatic coracoids of modern birds show similar internal structures to Ornithurine G (cf. Cimolopteryx), indicating that pneumaticity of the coracoid cannot be determined in the absence of an external pneumatic foramen. A comparison between members of Cimolopterygidae, including Cimolopteryx and Lamarqueavis, raises questions about the assignment of Lamarqueavis to the Cimolopterygidae, and the validity of this family as a whole.
We describe a new taxon of advanced ornithuromorph bird, Khinganornis hulunbuirensis gen. et sp. nov., from the previously unreported Pigeon Hill locality of the Lower Cretaceous Longjiang Formation in the northern Greater Khingan Range area of Inner Mongolia, China. A cladistics analysis resolves K. hulunbuirensis as the sister group of a clade formed by Changzuiornis and Iteravis among ornithuromorphs. The osteohistological analysis indicates that K. hulunbuirensis is the first ornithuromorph that maintained an uninterrupted growth during a longer period characterised by slow deposition of low-vascularised and terminal avascular bone tissue. The relatively long hindlimbs and elongate pedal digits with long proximal phalanges suggest a wading and amphibious ecology for the new bird. The discovery of K. hulunbuirensis represents the first occurrence of Jehol birds in the Greater Khingan Range and documents the northernmost known geographic distribution of the celebrated avifauna in China. The new record implies more extended palaeogeographic range for the early diversification of Mesozoic birds on the eastern side of Laurasia.
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Ornithomimosauria is a group of medium to large, lightly built theropods that are mainly known from Cretaceous sediments of central Asia and western North America. This chapter examines the diagnostic features, evolution, and paleobiology, and phylogenetic relationships among ornithomimid taxa. Ornithomimosaurs are represented by Pelecanimimus, Gallimimus, Garudimimus, Ornithomimus, Struthiomimus, Harpymimus, Archaeornithomimus, Shenzhousaurus, and Anserimimus. They are characterized by short, delicate skulls, elongate forelimbs with a weak, nonraptorial manus, and long hindlimbs. The chapter also compares the biogeographic history of ornithomimosaurs within the broader context of several other dinosaur groups that display a predominantly Asian-North American distribution during the Cretaceous.
Birds evolved from and are phylogenetically recognized as members of the theropod dinosaurs; their first known member is the Late Jurassic Archaeopteryx, now represented by seven skeletons and a feather, and their closest known non-avian relatives are the dromaeosaurid theropods such as Deinonychus. Bird flight is widely thought to have evolved from the trees down, but Archaeopteryx and its outgroups show no obvious arboreal or tree-climbing characters, and its wing planform and wing loading do not resemble those of gliders. The ancestors of birds were bipedal, terrestrial, agile, cursorial and carnivorous or omnivorous. Apart from a perching foot and some skeletal fusions, a great many characters that are usually considered ‘avian’ (e.g. the furcula, the elongated forearm, the laterally flexing wrist and apparently feathers) evolved in non-avian theropods for reasons unrelated to birds or to flight. Soon after Archaeopteryx, avian features such as the pygostyle, fusion of the carpometacarpus, and elongated curved pedal claws with a reversed, fully descended and opposable hallux, indicate improved flying ability and arboreal habits. In the further evolution of birds, characters related to the flight apparatus phylogenetically preceded those related to the rest of the skeleton and skull. Mesozoic birds are more diverse and numerous than thought previously and the most diverse known group of Cretaceous birds, the Enantiornithes, was not even recognized until 1981. The vast majority of Mesozoic bird groups have no Tertiary records: Enantiornithes, Hesperornithiformes, Ichthyornithiformes and several other lineages disappeared by the end of the Cretaceous. By that time, a few Linnean ‘Orders’ of extant birds had appeared, but none of these taxa belongs to extant ‘families’, and it is not until the Paleocene or (in most cases) the Eocene that the majority of extant bird ‘Orders’ are known in the fossil record. There is no evidence for a major or mass extinction of birds at the end of the Cretaceous, nor for a sudden ‘bottleneck’ in diversity that fostered the early Tertiary origination of living bird ‘Orders’.
Charles Darwin commented that Ichthyornis, as one of the "toothed birds" from the Late Cretaceous of Kansas, offered some of "the best support to the theory of evolution" (in litt., C. Darwin to O.C. Marsh, August 31, 1880). Ichthyornis figures no less prominently today. It is one of the closest outgroups to crown clade Aves, and remains one of the only Mesozoic avialans known from more than a handful of specimens. As such, Ichtkyornis is an essential taxon for analyses of deep divergences within Aves because of its influence in determining the morphologies ancestral to the crown clade. Ichthyornis, however, has languished in need of new anatomical description and taxonomic revision. Many of the best Ichthyornis specimens were largely inaccessible, plastered into Yale Peabody Museum (YPM) exhibit Mounts for nearly a century. The focus of this study was the entire YPM Ichthyornis collection, the largest at any institution. The elements removed from the mounts were identified to the specimens with which they were originally associated. Detailed morphological study of the 81 YPM specimens yielded the following results: (1) there is evidence for only one species of Ichthyornis, rather than the eight previously proposed; (2) 78 specimens are part of this species, Ichthyornis dispar; (3) two previously identified species are not part of Ichthyornis; and (4) one new species is identified. This analysis also provided a case study in the application of phylogenetic nomenclature at the species level. The morphology of Ichthyornis dispar is described in detail from the holotype and referred specimens. Phylogenetic analyses of 202 morphological characters, scored for 24 terminal taxa, evaluated the relationships among Mesozoic ornithurines including Ichthyornis dispar and the newly identified taxa. Analysis of 23 core taxa produced two most parsimonious trees (L: 384, CI: 0.66). Marsh's "Ichthyornithiformes" is not monophyletic: Two previously named species of Ichthyornis as well as Apatornis celer are placed as more closely related to or as part of Aves. The results of the phylogenetic analyses have implications for previous hypotheses of the timing and pattern of the origin of Aves.
This paper describes a new fossil named Cathayornis chabuensis discovered in 2008, from Chabu, Otog Qi in Inner Mongolia, which also represents the second Cathayornis found in this area. The specimen preserves a complete sternum and furcula with some other clear skeleton impressions. A comparison of the new material with Eocathayornis walkeri, C. yandica and C. chabuensis shows that except the similarity between C. yandica and C. chabuensis, the later one displays some more advanced characteristics than E. walkeri and C. yandica. Besides, the functional morphological analysis related to flying skills supports that C. chabuensis is not only capable of flapping flight as C. yandica in the Early Cretaceous, but also possesses an advanced flying system indicating a stronger flying capability.