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ARTICLE
Received 6 Jan 2015 |Accepted 20 Mar 2015 |Published 5 May 2015
The oldest record of ornithuromorpha from the
early cretaceous of China
Min Wang1, Xiaoting Zheng2,3, Jingmai K. O’Connor1, Graeme T. Lloyd4, Xiaoli Wang2,3, Yan Wang2,3,
Xiaomei Zhang2,3 & Zhonghe Zhou1
Ornithuromorpha is the most inclusive clade containing extant birds but not the Mesozoic
Enantiornithes. The early evolutionary history of this avian clade has been advanced
with recent discoveries from Cretaceous deposits, indicating that Ornithuromorpha and
Enantiornithes are the two major avian groups in Mesozoic. Here we report on a new
ornithuromorph bird, Archaeornithura meemannae gen. et sp. nov., from the second oldest
avian-bearing deposits (130.7 Ma) in the world. The new taxon is referable to the
Hongshanornithidae and constitutes the oldest record of the Ornithuromorpha. However,
A. meemannae shows few primitive features relative to younger hongshanornithids and is
deeply nested within the Hongshanornithidae, suggesting that this clade is already well
established. The new discovery extends the record of Ornithuromorpha by five to six million
years, which in turn pushes back the divergence times of early avian lingeages into the Early
Cretaceous.
DOI: 10.1038/ncomms7987 OPEN
1Key Laboratory of Vertebrate Evolution and Human Origins of Chinese Academy of Sciences, Institute of Vertebrate Paleontology and Paleoanthropology,
Chinese Academy of Sciences, Beijing 100044, China. 2Institue of Geology and Paleontology, Linyi University, Linyi, Shandong 276000, China.
3Tianyu Natural History Museum of Shandong, Pingyi, Shandong 273300, China. 4Department of Biological Sciences, Faculty of Science, Macquarie
University, Sydney, New South Wales 2019, Australia. Correspondence and requests for materials should be addressed to M.W. (email: wangmin@ivpp.ac.cn)
or to Z.Z. (email: zhouzhonghe@ivpp.ac.cn).
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Ornithuromorpha is the clade of birds that all living birds
but not Enantiornithes nest in refs 1,2. Until now the
earliest record of this group was from the lower
Cretaceous Yixian Formation (125 Ma), the middle phase in the
evolution of the Jehol Biota—the most important and diverse
fossil avifauna known to science1,3,4. More than half the known
diversity of Mesozoic birds belongs to this biota, which includes,
from the oldest to the youngest, the Protopteryx horizon and the
Yixian and Jiufotang Formations, which together encompass over
ten million years of avian evolution (130.7–120 Ma)5. Bio- and
lithostratigraphic works confirmed that the Protopteryx-bearing
deposits in Sichakou basin of Fengning Country are referable to
the interbedded shales from the lower part of the Huajiying
Formation5,6. Recent 40Ar/39Ar dating produced a weighted
mean age of 130.7 Ma for this horizon7. Therefore, the Huajiying
Formation is the second oldest avian-bearing deposit in the
world, only after the Upper Jurassic Solnhofen Limestones that
preserve Archaeopteryx in Germany6. Only three avian taxa have
been collected from this horizon: the basal confuciusornithiform
Eoconfuciusornis and two enantiornithines Protopteryx
and Eopengornis8–10. Here we report on the first two
ornithuromorph fossils from the same locality as the holotype
of Protopteryx fengningensis in Sichakou basin8, which constitute
the earliest known record of Ornithuromorpha. These two
specimens are referable to a single taxon, which appears to be
deeply nested within the Hongshanornithidae, a fairly diverse
clade of small, specialized wading ornithuromorphs. Currently,
four hongshanornithids, Hongshanornis longicresta,Longicrusavis
houi,Parahongshanornis chaoyangensis and Tianyuornis cheni,
have been reported from the Yixian and Jiufotang Formations in
Inner Mongolia and Liaoning2,11–14. These new specimens
reported here push back the first appearance datum of
Ornithuromorpha by approximately six million years.
Results
Systematic paleontology.
Aves
Ornithothoraces
Ornithuromorpha
Hongshanornithidae
Type genus. Hongshanornis, Zhou and Zhang11.
Archaeornithura meemannae gen. et sp. nov.
Etymology. The generic name is derived from Greek
‘Archae’ and ‘ornithura’, meaning ‘ancient ornithuromorph’.
The specific name is in honour of Dr Meemann Chang for
her continuous support of the study of the Jehol Biota.
Holotype. An articulated partial skeleton with feathers
(STM7-145), housed at the Tianyu Natural History Museum
of Shandong (STM), China (Fig. 1).
Paratype. An articulated partial skeleton with feathers
(STM7-163; Supplementary Fig. 1).
Locality and horizon. Protopteryx horizon in Sichakou
basin, Fengning County, Hebei, northeastern China; Lower
Cretaceous Huajiying Formation6,7.
Differential diagnosis. The new taxon is referable to the
Hongshanornithidae and can be distinguished from the
known hongshanornithids by the following combined
features: it differs from Hongshanornis and Longicrusavis,
in that the cranial margin of the sternum is strongly vaulted;
it is distinguished from Hongshanornis and Parahongsha-
nornis, in that the zyphoid process of the sternum is
well developed and squared; it differs from other
hongshanornithids except Longicrusavis, in that the alular
digit extends further distally than the major metacarpal; it
is distinguishable from other hongshanornithids except
Parahongshanornis, in that the penultimate phalanx of the
major digit is longer than the preceding phalanx; and the
new taxon has proportionally shorter femur relative to the
tarsometatarsus.
Description. The skull is not well preserved in either specimen
(Fig. 1; Supplementary Fig. 1). The cervical vertebrae are poorly
preserved in articulation with the skull; 10 vertebrae are preserved
including the ring-like axis, although the exact position of
the cervicothoracic transition cannot be determined due to
poor preservation. The vertebrae are clearly not elongated,
being approximately equal in width and length, as in other
hongshanornithids (Figs 1 and 2b,c; Supplementary Fig. 1). The
thoracic vertebrae are only preserved in the counter slab of
STM7-145, covered by the sternum. The synsacrum appears
to comprise 9–10 vertebrae, although preservation makes this
estimate equivocal. Six free caudals are followed by a poorly
preserved pygostyle (Fig. 3e). The transverse processes of the
caudal vertebrae are less than the width of the centrum in length
and caudolaterally directed, at least in the first free caudal. Two
well-preserved uncinate processes are preserved in the counter
slab of STM7-163, and they are straight and tapered (Fig. 2a).
Although not in articulation with the ribs, we infer they would
have crossed at least one rib, reaching and potentially crossing a
second. Four sets of gastralia are preserved in articulation in
STM7-163 (Supplementary Fig. 2b).
The scapula is curved, as in other ornithuromorph birds, but
the distal end is not well preserved in either specimen (Figs 1
and 2c). The furcula is typically hongshanornithid: delicate,
U-shaped, with tapered omal margins and a small tubercle-like
hypocleidium as in Tianyuornis and Parahongshanornis12–14,
which, however, is short and sharply tapered in Hongshanornis
(Fig. 2)11. In contrast, a hypocleidium is absent from most other
Cretaceous ornithuromorphs, although a short one has been
reported in Schizooura15. The furcular symphysis is much
thicker craniocaudally compared with the omal rami as in
Hongshanornis, whereas the furcula appears to be nearly of equal
thickness throughout in Longirostravis and Tianyuornis12,13. The
coracoid is narrow along the proximal half, and wide distally with
a well-developed sternocoracoidal process (Fig. 2b), as in
hongshanornithids and most other ornithuromorphs2,12–14.
Although poorly preserved, a procoracoid process is visible on
the right coracoid in the counter slab of both specimens; it is
medially oriented although the distal half appears more cranially
directed (Fig. 2b). This process is perforated at the base by a small
circular supracoracoidal nerve foramen. The coracoid is preserved
in the dorsal view in the counter slab of STM7-163 (Fig. 2b); the
acrocoracoid is blunt, the scapular cotyla is deeply concave, and
the laterally positioned glenoid is developed as a weak convexity.
Distally, the corpus is concave, more so than the condition in
Yixianornis but not so deeply as in some Late Cretaceous
enantiornithines16. The sternum is not well preserved, but a
fragment in STM7-163 indicates the rostral margin is vaulted as
in Tianyuornis and Parahongshanornis (Fig. 2d,g,h)13,14,
but more pointed than in Longicrusavis and Hongshanornis,in
which the cranial margin is broad and parabolic (Fig. 2e,f)2,11,12.
A well-developed zyphoid process is present and squared in
shape, as in Longicrusavis and Tianyuornis (Fig. 2a,f,g)12,13,
whereas the process is absent in Hongshanornis and
Parahongshanornis, and the corresponding lateral margin only
bulges laterally (Fig. 2e,h)11,14. A second fragment in the same
slab indicates that the lateral trabecula was short and narrow
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as in other hongshanornithids, with a distinct triangular
distal expansion similar to that of Tianyuornis but smaller
(Supplementary Fig. 2a)13.
The humerus is short and robust with a large rounded
deltopectoral crest that extends 44% the length of the humerus
and slightly exceeds the width of the shaft, as in other
hongshanornithids (Fig. 3a). The distal margin is perpendicular
to the shaft. The condyles are well developed and bulbous, and a
dorsal supracondylar process is present as in other hongshanor-
nithids (Fig. 3a; Supplementary Fig. 2d)2,12; however, the process
has so far been reported only in Ichthyornis among other
Mesozoic birds2,17. The ulna is bowed and more robust than the
straight radius as in all basal birds. An olecranon process is not
developed. The carpometacarpus appears to be fused proximally
but not distally in STM7-145. All the metacarpals are straight,
and the minor metacarpal is less than half the thickness of the
major metacarpal. The alular metacarpal bears a small extensor
process that is less than half the width of the articular facet of this
metacarpal. The alular digit is long, with half of the ungual
extending just beyond the distal margin of the major metacarpal
as in Longicrusavis, whereas in other hongshanornithids, only the
tip of the ungual slightly surpasses the distal end of the major
metacarpal (Fig. 3a,c). The ungual phalanx of the alular digit is
larger and more recurved than that of the major digit, as in other
hongshanornithids2,11–14. The first phalanx of the major digit is
mediolaterally compressed and caudally expanded, as in other
ornithuromorphs. As in Parahongshanornis, the penultimate
phalanx is longer than the preceding phalanx, whereas these two
phalanges are subequal in length in other hongshanornithids
(Table 1). The minor digit only preserves a single reduced
wedge-shaped phalanx that tapers distally. A second phalanx,
which is extremely reduced in other hongshanornithids2,11–14,
may have being missing due to preservation. Similar to
other hongshanornithids, the forelimb is much shorter than
the hindlimb, with an intermembral index (humerus þulna/
femur þtibiotarsus) of B0.84 (Table 1), whereas the forelimb is
typically longer in other Early Cretaceous ornithuromorphs18,19.
The pelvic girdle is not well preserved in either specimen; the
ilium is displaced cranially in STM7-145. Visible in the main slab,
the cranial margin is convex, while the lateral margin proximal to
the acetabulum is concave; the two margins are separated by a
weakly developed ventral hook present in most ornithuromorphs
and some enantiornithines. The pubes are long and contact along
their distal tenth but remain unfused, as in Hongshanornis
(Supplementary Fig. 2c). Although incomplete, the distal ends of
pubes are well preserved in lateral and medial views in the
counter slab of STM7-163, revealing a small distally expanded
boot as in Hongshanornis and Parahongshanornis (unclear in
Tianyuornis and Longirostravis; Fig. 3d,e)2,14. The ischia appear
to be just over half the length of the pubes, straight, narrow and
tapered along their distal halves (Fig. 3e), lacking the low dorsal
process located mid-corpus and the concave ventral margin
present in most other ornithuromorphs, including Yixianornis
and Piscivoravis20,21.
The femora are short and fairly robust, approximately equal in
length to the tarsometatarsi; in contrast, the femur is considerably
longer than the latter in most other basal birds, including
Jeholornis,Sapeornis,Confuciusornis, enantiornithines and
ornithuromorphs18,19. The tibiotarsus is proportionally shorter
than other hongshanornithids relative to the tarsometatarsus. As
in Longicrusavis, the fibula is preserved bowing out from the
tibiotarsus, not appressed against it, and only appears to extend to
the midshaft of the tibiotarsus12. The proximal medial surface
bears a shallow excavation, visible on the left side in the counter
slab of STM7-163.
The tarsometatarsi are well preserved in the main slab of
STM7-163 (Fig. 3f). They are fully fused, although the individual
metatarsals can be distinguished. Overall, the foot is very similar
to other hongshanornithids2,11–14. The proximal half of
metatarsal III is plantarly displaced relative to metatarsals II
and IV, as in all ornithuromorphs. Metatarsal III is the longest
and metatarsals II and IV end approximately at the same level.
The hallux is small and placed above the trochlea of the
other digits as in most ornithuromorphs including other
hongshanornithids. The first phalanx is approximately as long
as metatarsal I itself; the ungual phalanx is more strongly
recurved than that of the other digits. As in other
hongshanornithids, the phalanges decease in length distally,
digit III is the longest and digit II is substantially shorter than IV.
Both specimens preserve nearly complete plumage (Figs 1
and 4; Supplementary Fig. 1). Six long asymmetrical primary
remiges are preserved in the left wing of the main slab in the
ba
cv
co
hu
ra
ul
al
ma
mi
fe
ti
fi
tm
d I
d II
d II I
d IV
fu
sc st
pu
re pr
ul
ra
hu
fe
ti
fi
tm
re
cv
Figure 1 | Holotype of Archaeornithura meemannae gen. et sp. nov., STM7-145. (a) Main slab; (b) counter slab. Anatomical abbreviations: al, alular
digit; ba, basicranium; co, coracoid; cv, cervical vertebrae; d I–IV, pedal digit I–IV; fe, femur; fi, fibula; fu, furcula; hu, humerus; ma, major digit; mi, minor
digit; pr, primary remiges; pu, pubis; ra, radius; re, rectrices; sc, scapula; st, sternum; ti, tibiotarsus; tm, tarsometatarsus; ul, ulna. Scale bars, 10 mm.
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holotype (Fig. 4a); the second and third feathers are the longest.
The primary remiges are overlain by a layer of short feathers,
which measure just under half the length of the primary remiges
themselves—we interpret these feathers as the dorsal coverts
(Fig. 4a,b). They appear to be symmetrical, definitely lacking the
strong asymmetry present in the primary remiges in which the
leading edge vane is less than one-third the width of the trailing
edge vane (Fig. 4a). Portions of a few secondary feathers are also
preserved; these appear to be narrower than the primary remiges
and symmetrical with rounded distal margins. An alula is
preserved in both specimens, composed of at least three feathers
in STM7-163, visible where the alular digit is disarticulated on the
left side (Fig. 4d). The rounded distal margins of three large
symmetrical pennaceous feathers are preserved near the right foot
in STM7-145 (Figs 1 and 4b). These feathers are staggered so that
each medial feather ends distal to the lateral feather, suggesting
that these feathers represent the distal portion of an incomplete
fan-shaped array of rectrices, like that present in Hongshanornis
(IVPP V14533 and DNHM D2945/6)2.
Short rachis-less covert feathers are found all over the body,
particularly well preserved in STM7-163 (Supplementary Fig. 1).
These feathers cover the head, neck, shoulders, extend off the
co
hu
fu
cv
zp
st
uc
fu
co
sl hy
pc
ne
sc
co
pc
hy
st
ca
fu
zp
lt
zp
hy
Figure 2 | Pectoral girdle and sternum of Archaeornithura meemannae gen. et sp. nov., in comparison with other hongshanornithids. (a) STM7-163,
counter slab (zyphoid process of the sternum is outlined by a dash line); (b) STM7-145, main slab; (c) photograph and (d) line drawing of STM7-145,
counter slab. Line drawing (not scaled) of furcula and sternum of other hongshanornithids: (e)Hongshanornis longicresta;(f)Longicrusavis houi;
(g)Tianyuornis cheni;(h)Parahongshanornis chaoyangensis. Anatomical abbreviations: ca, carina; co, coracoid; cv, cervical vertebrae; fu, furcula; hy,
hypocleidium; lt, lateral trabecula of the sternum; ne, supracoracoidal nerve foramen; pc, procoracoid process; sc, scapula; sl, sternocoracoidal process;
st, sternum; uc, uncinate process; zp, zyphoid process of the sternum. Scale bars, 5 mm.
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proximal ulna and humerus and line the caudal end of the body
(Fig. 4c; Supplementary Fig. 1). These feathers are notably absent
from the distal three-quarters of the tibiotarsus in both specimens
(Figs 1 and 4a; Supplementary Fig. 1), consistent with the wading
habitat inferred for hongshanornithids12.
Discussion
Archaeornithura is referable to the Hongshanornithidae, which is
distinguishable from other Cretaceous ornithuromorphs by
the following synapomorphies: the U-shaped furcula bears a
tubercle-like hypocleidium; the humerus has a well-developed
supracondylar process; the manus is longer than the humerus; the
forelimb is shorter than the hindlimb with an intermembral index
of about 0.8; and the femur and tarsometatarsus are subequal in
length, while the former is considerably longer in most other
basal birds. Phylogenetic analysis was conducted using a
comprehensive matrix targeted at Mesozoic birds (58 taxa
and 262 characters; Supplementary Data 1 and Supplementary
Data 2)22; the results confirm the close affinity between the new
specimens and younger hongshanornithids, resolving all
purported members together in a clade, the Hongshanornithidae
(Fig. 5; Supplementary Fig. 3). This represents the most diverse
recognized clade of Early Cretaceous ornithuromorphs.
Synapomorphies of the Hongshanornithidae retained from the
analysis include: teeth present throughout the premaxillary
(character 4:0); mandibular ramus sigmoidal in shape (character
42:1); acromion process of scapula nearly parallel to the scapular
shaft in costal or lateral view (character 98:1); dorsal
supracondylar process of humerus developed (character 134:2);
second phalanx of the major digit longer than the proximal one
(character 171:0); intermembral index between 0.7 and 0.9
(character 177:1); the claw of the fourth pedal digit smaller
than that of other digits (character 256:1); and the ratio (length of
del
ul
ra
hu
sp
am
al
ma
mim mam
mi
pu
pb pb
pu
pb
is
py
is
ti
tm
mt I d I
d II
d III
d IV
ca
1
2
3
4
5
6
Figure 3 | Detail anatomy of Archaeornithura meemannae gen. et sp. nov. (a) Photograph and (b) line drawing of the left wing, STM7-145, counter
slab; (c) line drawing of hands of other hongshanornithids (not scaled; from left): Hongshanornis longicresta,Longicrusavis houi,Tianyuornis cheni,
Parahongshanornis chaoyangensis;(d) STM7-163, counter slab; (e) STM7-163, main slab; (f) feet, STM7-163, main slab. Anatomical abbreviations:
al, alular digit; am, alular metacarpal; ca, caudal vertebrae (six vertebrae counted); del, deltopectoral crest; d I–IV, pedal digit I–IV; hu, humerus; is, ischium;
ma, major digit; mam, major metacarpal; mi, minor digit; mim, minor metacarpal; mt I, metatarsal I; pb, pubic boot; pu, pubis; py, pygostyle; ra, radius;
sp, supracondylar process; ti, tibiotarsus; tm, tarsometatarsus; ul, ulna. Scale bars, 10mm (a,f), 5 mm (d,e).
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tibiotarsus/tarsometatarsus) between 2 and 1.6 (character 257:1).
Archaeornithura is resolved to be the sister taxon to the younger
Tianyuornis and this clade is supported by two synapomorphies:
outermost trabecula of sternum with a simple bulb-like distal
expansion (character 113:1; Supplementary Fig. 2a) and
metatarsals II–IV partially fused with discernible sutural
contacts (222:1; Fig. 3f). It is notable that, despite being the
oldest recognized ornithuromorph, Archaeornithura is deeply
nested within the Hongshanornithidae, which itself is more
deeply nested within Ornithuromorpha than some taxa known
entirely from younger deposits15,17,18,21,22. These inconsistencies
between stratigraphy and phylogeny require the presence
of ghost lineages and a much earlier origination date for
the Ornithuromorpha, which in turn pushes back the
Table 1 | Comparative measurements of Archaeornithura meemannae gen. et sp. nov. and other hongshanornithid taxa.
Elements STM 7-145 STM 7-163 IVPP V 14533 DNHM D2945 PKUP 1069 PMOL-AB00161 STM7-53
Coracoid 15.4 12.7 11.7 12.7 14.7
Scapula 423.2 22.4 23.1 424.5
Humerus 25.9 27.5 26.0 22.9 26.0 29.4 25.4
Ulna 25.8 28.3 24.4 23.9 25.0 28.4 26.4
Radius 23.9 26.0 23.0 23.1 24.0 26.8 24.6
Carpometacarpus 13.1 13.8 11.8 12.6 13.1 11.4 13.2
Alular digit 1 6.0 7.6 6.3 6.6 6.9 6.7 6.6
Alular digit 2 3.0 3.9 2.8 2.8 4.3 2.7 2.9
Major digit 1 6.6 6.8 5.8 6.6 7.0 7.1 6.9
Major digit 2 7.6 7.0 5.9 6.8 7.3 8.0 7.0
Major digit 3 2.4 3.0 2.5 3.4 2.6
Minor digit 1 3.3 2.8 4.0 3.2, 3.5 3.3
Femur 23.8 22 24.3 24.8 24.8
Tibiotarsus 38.0 37.5 38 34.6 37.6 41.3 39.0
Tarsometatarsus 23.0 21.0 19.1 21.5 21.2 23.1
(Humerus þulna)/(femur þtibiotarsus) 0.84 0.84 0.82 0.87 0.81
Archaeornithura meemannae (STM7-145, STM7-163), Hongshanornis longicresta (holotype, IVPP V 14533; paratype, DNHM D2945), Longicrusavis houi (holotype, PKUP V1069), Tianyuornis cheni (holotype,
STM7-53) and Parahongshanornis chaoyangensis (holotype, PMOL-AB00161). Lengths are measured in millimetres.
dc
pr
pr
re af
Figure 4 | Plumage of Archaeornithura meemannae gen. et sp. nov. (a) Left wing, STM-7-145, main slab; (b) right wing, STM-7-145, main slab;
(c) covert feathers over the skull and neck, STM 7-163, counter slab; (d) alular feathers on the left alular digit, STM7-163, main slab. Abbreviations:
af, alular feather; dc, dorsal coverts; pr, primary remiges; re, rectrices. Scale bars, 10 mm (a–c), 5 mm (d).
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divergence time with enantiornithines and other primitive avian
lineages.
Archaeornithura preserves fairly advanced plumage including a
well-developed alula and fan-shaped rectrices (Figs 1 and 4;
Supplementary Fig. 1). Both the alula (bastard wing) and a fan-
shaped tail are aerodynamically important for living birds during
slow flight and increases manoeuvrability23,24. These advanced
feather structures are inferred to be plesiomorphic at least to
Ornithothoraces2,10; an alula is also present in the basal
enantiornithine Protopteryx from the same locality8. Because
the alular digit is well developed in both hongshanornithids and
Protopteryx (extends beyond the distal end of the major
metacarpal), the morphology of the alula would be expected to
somewhat differ from that in living birds. However, preservation
of the alula in a Mesozoic bird has never been clearer than as
preserved in STM7-163 (Fig. 4d), which reveals a morphology
that is remarkably similar to that in living birds: it is formed by at
least three feathers (three to five in living birds), with the short
proximal feather ending level with the alular digit and the longer
feathers extending to the end of the major digit. Both
Archaeornithura and Hongshanornis preserve a fan-shaped
array of rectrices2, a feature plesiomorphic to Ornithuromorpha
Eoconfuciusornis
Changchengornis
Dromaeosauridae
Archaeopteryx
Jeholornis
Confuciusornis dui
Jinzhouornis
Confuciusornis sanctus
Sapeornis
Protopteryx
Patagopteryx
Hongshanornis
Parahongshanornis
Yanornis
Yixianornis
Piscivoravis
Gansus
Apsaravis
Hesperornis
Ichthyornis
Longipteryx
Shanweiniao
Eoenantiornis
Rapaxavis
Longicrusavis
Tianyuornis
Archaeornithura
Eoalulavis
Concornis
Fortunguavis
Vescornis Neuquenornis
Gobipteryx
Longirostravis
Boluochia
Eocathayornis
Jianchangornis
Archaeorhynchus
Schizooura Vorona
Songlingornis
Vegavis
Enaliornis
Baptornis advenus
Baptornis varneri
Parahesperornis
Pengornis
Eopengornis
Cathayornis
Qiliania
Shenqiornis Sulcavis
Parabohaiornis
Longusunguis
Zhouornis
Bohaiornis
Neornithes
Aves
Pygostylia
Enantiornithines
Ornithothoraces
Ornithuromorpha
Confuciusornithidae
Pengornithidae
Bohaiornithidae
Longipterygidae
Hongshanornithidae
c
d
e
100
3
111
1112
2
1111
1
1
11
1
11
1
1
1
11
1
1
3
3
3
250/
1
e
d
c
b
a
a
b
54/159/3
54/4
80/2
70/1
82/2
90/3
69/1
62/2
99/11
Figure 5 | Cladogram showing the systematic position of Archaeornithura meemannae among Mesozoic birds. Bootstrap and bremer values are labelled
to the corresponding nodes in normal and bold italic formats, respectively.
NATURE COMMUNICATIONS | DOI: 10.1038/ncomms7987 ARTICLE
NATURE COMMUNICATIONS | 6:6987 | DOI: 10.1038/ncomms7987 | www.nature.com/naturecommunications 7
&2015 Macmillan Publishers Limited. All rights reserved.
and apparently lost in Enantiornithes10. Enantiornithines and the
Confuciusornithiformes typically have only a pair of elongated
rachis-dominant rectrices8,9,25,26. The rachis of these feathers is
proportionately wide and always preserves a longitudinal stripe,
which is interpreted as a central groove in some studies10,26. More
recently, the same striped morphology was recognized in the
primary feathers of Confuciusornis and enantiornithines,
supporting hypotheses that rachis-dominated feathers are
modified flight feathers10.Archaeornithura documents this
feather morphology for the first time in the Ornithuromorpha;
a medial stripe is visible in the rachises of some of the primary
remiges. Although evidence from Archaeopteryx indicates
modern feather morphology including fully pennaceous coverts
and rachises that clearly lacked a longitudinal groove27, these
features are absent in Jehol birds despite the huge wealth of
specimens25,26. This suggests that modern feather morphologies
evolved independently within the Archaeopteryx lineage and a
derived subset of ornithuromorphs.
Bird fossils are extremely rare in the Mesozoic fossil record,
and until the wealth of specimens discovered from Early
Cretaceous deposits in northeastern China, very little was known
about the early evolution of birds1,3,4. The Jehol Biota
encapsulates a unique window into the biology and morphology
of the oldest known avifauna; however, this fauna is clearly
already well within the diversification of birds, given that both
ornithothoracine clades are present3,28. Until now no
ornithuromorphs had been described from the Huajiying
Formation, which preserves very few fossil birds10;
because diversity is low and geographic area is restricted, the
Huajiying Formation is interpreted as the earliest stage in the
diversification of the Jehol Biota. However, the discovery of
a new species belonging to the specialized clade of waders—the
Hongshanornithidae, indicates that ornithuromorphs themselves
were already quite specialized at this point in their evolution. This
also strongly supports inferences that this clade originated in a
semi-aquatic environment1,29,30.
Methods
Provenance of the two specimens of A. meemannae.The two specimens
(STM7-145, 7-163) of A. meemannae were acquired by the Tianyu Natural History
Museum of Shandong from a fossil dealer. The dealer confirmed that the fossils
were collected from the same locality of the holotype of Protopteryx fengningensis
(IVPP V11665) in Sichakou basin of Fengning Country, Hebei Province, north-
eastern China. Lithostratigraphic and biostratigraphic fieldworks have been
performed in the basin for years, and confirm that the Protopteryx-bearing horizon
belongs to the Lower member of the Huajiying Formation5,6,8. The Cretaceous
Strata cropping out in Sichakou basin consist of the Huajiying Formation and the
overlying Qingshila Formation; the Huajiying Formation consists of lacustrine
deposits with abundant pyroclastics, and all the known fossil birds, including the
two specimens of A. meemannae, were unearthed from the lower part of the
Huajiying Formation (‘Sichakou sedimentary member’ in ref. 6). Currently, no
fossil birds have been reported from the Qingshila Formation. A weighted mean
age of 130.7 Ma was reported using 40Ar/39Ar dating of the K-feldspars samples
from the interbedded tuffs about 6 m below the Protopteryx-bearing layer7, largely
consistent with previous results using the SHRIMP U-Pb method31. The two
specimens of A. meemannae are preserved in slabs that are identical to the matrixes
containing the holotype of Protopteryx fengningensis,Eoconfuciusornis zhengi and
Eopengornis martini, in that all the slabs are composed of tufaceous siltstones,
which are grey in colour and rigid in nature, consistent with mineralogical
composition of the birds-bearing deposits from the lower part of the Huajiying
Formation6. We have compared hundreds fossil birds, housed in the Institute of
Vertebrate Paleontology and Paleoanthropology, which are unearthed from the
Yixian and Jiufotang Formations from a wide geological area in Jehol Biota.
We have noticed that these slabs are off-white (rather than grey as in the
Archaeornithura-bearing slabs) in colour and mainly composed of weakly
laminated siliciclastic sandstones and shales, which are conspicuously softer than
the bird-bearing slabs from the Huajiying Formation (including the slabs
containing A. meemannae). In addition, we have requested the dealer to show us
the exact locality where these two specimens were unearthed, and confirmed that
they were collected from the Huajiying Formation in Sichakou basin. Detail
comparisons and geological correlation indicate that the slabs preserving the two
specimens of A. meemannae are identical in all visible lithological features to the
sediments of the lower part of the Huajiying Formation. Therefore, the provenance
of the two specimens of A. meemannae can be justified. The two specimens of
A. meemannae are housed in the Tianyu Natural History Museum of Shandong
and are publicly accessible.
Phylogenetic analysis.Phylogenetic analysis was performed using the modified
data set of Wang et al.22, a comprehensive morphological character matrix
targeting the phylogeny of Mesozoic birds (Supplementary Data 1 and 2. Rahonavis
was removed from the data set, given the fact that recent studies indicate that
Rahonavis is an unenlagiine dromaeosaurid rather than a bird32,33. Two
enantiornithines, Elsornis and Iberomesornis, were removed because of their
incompleteness. Two recently reported Jehol birds, Eopengornis martini
(enantiornithine) and Piscivoravis lii (ornithuromorph), were added and scored
from their holotypes (STM24-1, IVPP V17078)10,21. All the known
hongshanornithids were included, and Archaeornithura,Parahongshanornis and
Tianyuornis were coded from their corresponding holotypes. The revised data
matrix consists of 58 taxa (55 are Mesozoic birds), scored across 262 morphological
characters. Phylogenetic analysis was conducted using PAUP software package
version 4.0b10 (ref. 34), with the following settings: all characters equally weighted;
unconstrained heuristic search starting with Wagner trees; 1,000 replicates of
random stepwise addition (branch swapping: tree-bisection-reconnection) holding
10 trees at each step; and branches are collapsed to create polytomies if the
minimum branch length is equal to zero. Bootstrap and Bremer values were
calculated as indices of support. Bootstrap values were performed using the TNT
software package (ref. 35) with default setting, except that 1,000 replicates were
used. Only nodes with bootstrap values greater than 50% are shown in Fig. 5.
Bremer values were calculated using the bremer scripts embedded in TNT.
The phylogenetic analysis produced four most parsimonious trees of 997 steps,
and had a consistency index of 0.367 and retention index of 0.684 (Supplementary
Fig. 3). The strict consensus tree is well resolved, and the new cladogram is
essentially consistent with previous studies with regards to the placement of
major clades10,17,18,22,29,36. In the strict consensus tree, Longicrusavis,
Parahongshanornis and Hongshanornis form the successive outgroups to
Tianyuornis þArchaeornithura clade, and these five taxa together constitute a
clade, the Hongshanornithidae (Fig. 5).
Nomenclatural Acts.This published work and the nomenclatural acts it contains
have been registered in ZooBank, the proposed online registration system for the
International Code of Zoological Nomenclature. The ZooBank LSIDs (Life Science
Identifiers) can be resolved and the associated information viewed through any
standard web browser by appending the LSID to the prefix ‘http://zoobank.org/’.
The LSIDs for this publication are: urn:lsid:zoobank.org:pub:B55C95A7-1AB4-
4645-BEA4-FC7EE139C4A7.
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Acknowledgements
We thank Zongda Zhang for the reconstruction of the specimen. This research was
supported by the National Basic Research Program of China (973 Program,
2012CB821906), the National Natural Science Foundation of China (41172020,
41372014, 41472023 and 41172016), the National Science Foundation for Fostering
Talents in Basic Research of the National Natural Science Foundation of China
(J1210008) and the Australian Research Council grant (DE140101879).
Author contributions
Z.Z., X.Z., M.W. and J.K.O’C. designed the project. M.W., Z.Z., J.K.O’C., G.T.L., X.W.,
Y.W. and X.W. performed the research. M.W. performed the phylogenetic analysis.
M.W., Z.Z., J.K.O’C. and G.T.L. wrote the manuscript.
Additional information
Supplementary Information accompanies this paper at http://www.nature.com/
naturecommunications
Competing financial interests: The authors declare no competing financial interests.
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How to cite this article: Wang, M. et al. The oldest record of ornithuromorpha
from the early cretaceous of China. Nat. Commun. 6:6987 doi: 10.1038/ncomms7987
(2015).
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