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The morphology of Chiappeavis magnapremaxillo (Pengornithidae: Enantiornithes) and a comparison of aerodynamic function in Early Cretaceous avian tail fans


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We provide a complete description of the skeletal anatomy of the holotype of Chiappeavis magnapremaxillo, the first enantiornithine to preserve a rectricial fan, suggesting that possibly rectricial bulbs were present in basal members of this clade. Notably, Chiappeavis preserves a primitive palatal morphology in which the vomers reach the premaxillae similar to Archaeopteryx but unlike the condition in the Late Cretaceous enantiornithine Gobipteryx. If rectricial bulbs were present, pengornithid pygostyle morphology suggests they were minimally developed. We estimate the lift generated by the tail fan preserved in this specimen and compare it to the tail fans preserved in other Early Cretaceous birds. Aerodynamic models indicate the tail of Chiappeavis produced less lift than that of sympatric ornithuromorphs. This information provides a possible explanation for the absence of widespread aerodynamic tail morphologies in the Enantiornithes.
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55卷 第1
pp. 41-58
gs. 1-8
古 脊 椎 动 物 学 报
The morphology of Chiappeavis magnapremaxillo
(Pengornithidae: Enantiornithes) and a comparison of
aerodynamic function in Early Cretaceous avian tail fans
Jingmai K. OCONNOR1 ZHENG Xiao-Ting2,3 HU Han1
WANG Xiao-Li2 ZHOU Zhong-He1
(1 Key Laboratory of Vertebrate Evolution and Human Origins of Chinese Academy of Sciences, Institute of Vertebrate
Paleontology and Paleoanthropology, Chinese Academy of Sciences Beijing 100044
(2 Institute of Geology and Paleontology, Linyi University Linyi, Shandong 276000)
(3 Shandong Tianyu Museum of Nature Pingyi, Shandong 273300)
Abstract We provide a complete description of the skeletal anatomy of the holotype of
Chiappeavis magnapremaxillo, the first enantiornithine to preserve a rectricial fan, suggesting
that possibly rectricial bulbs were present in basal members of this clade. Notably, Chiappeavis
preserves a primitive palatal morphology in which the vomers reach the premaxillae similar to
Archaeopteryx but unlike the condition in the Late Cretaceous enantiornithine Gobipteryx. If
rectricial bulbs were present, pengornithid pygostyle morphology suggests they were minimally
developed. We estimate the lift generated by the tail fan preserved in this specimen and compare
it to the tail fans preserved in other Early Cretaceous birds. Aerodynamic models indicate the
tail of Chiappeavis produced less lift than that of sympatric ornithuromorphs. This information
provides a possible explanation for the absence of widespread aerodynamic tail morphologies in
the Enantiornithes.
Key words Mesozoic, Jehol Biota, Aves, rectrix
Citation O’Connor J K, Zheng X T, Hu H et al., 2016. The morphology of Chiappeavis
magnapremaxillo (Pengornithidae: Enantiornithes) and a comparison of aerodynamic
function in Early Cretaceous avian tail fans. Vertebrata PalAsiatica, 55(1): 41–58
1 Introduction
Enantiornithes is the most diverse recognized group of Mesozoic birds, considered
the first major avian radiation. Although specimens have been collected from continental
and marine sediments on all continents with the exception of Antarctica, like other bird
fossils, these remains are typically isolated and fragmentary (O’Connor et al., 2011). The
major exception is the Early Cretaceous deposits in northeastern China that have produced
国家重点基础研究发展计划项目(编号:2012CB821906)和国家自然科学基金(批准号:41172020, 41372014,
42 Vertebrata PalAsiatica, Vol. 55, No. 1
the 130.7–120 Ma Jehol Biota (Pan et al., 2013), preserving the second oldest recognized
fossil avifauna surpassed only by the Late Jurassic Solnhofen Limestones in Germany that
produce Archaeopteryx (Wellnhofer, 2008). Despite its age, the Jehol avifauna accounts
for approximately half of the entire diversity of Mesozoic birds including a huge diversity
of enantiornithines (Wang M et al., 2014; Wang X et al., 2014; Zhou and Zhang, 2006). As
new species steadily continue to be discovered, several distinct clades have been recognized
(e.g., the Bohaiornithidae, Longipterygidae). The most temporally successful of these
enantiornithines lineages is the Pengornithidae. The rst specimen, the holotype of Pengornis
houi, was described by Zhou et al. in 2008 and already this group is one of the most diverse
enantiornithine clades in the Jehol avifauna. Currently there are ve specimens representing
four genera (Pengornis, Parapengornis, Eopengornis, and Chiappeavis) (Hu et al., 2015;
O’Connor et al., 2016; Wang X et al., 2014; Zhou et al., 2008). The holotype of Pengornis
houi is the largest known Early Cretaceous enantiornithine. Eopengornis is from the 130.7
Ma Protopteryx-horizon of the Huajiying Formation and all other taxa are from the 120 Ma
Jiufotang Formation. Pengornithids are the most recognizable enantiornithines, with their
characteristic numerous small, low-crowned teeth, hooked scapular acromion, bilaterally
formed sternum without intermediate trabeculae, elongate femur, unreduced bula, metatarsal
V, and elongate metatarsal I and hallux. These characters are mostly primitive features strongly
suggesting that pengornithids are basal within the Enantiornithes, consistent with recent
phylogenetic analyses and the fact Eopengornis is among the oldest known enantiornithines
(Wang X et al., 2014).
The most recently described pengornithid, Chiappeavis magnapremaxillo, preserves
the first clear evidence that some members of the Enantiornithes possessed rectricial fans
(Fig. 1), similar to those present in the basal pygostylian Sapeornis and members of the
Ornithuromorpha (Clarke et al., 2006; Zheng et al., 2013), the clade that includes all living
birds nested within. The unique shape of the pengornithid pygostyle, being relatively more
similar to that of ornithuromorphs and Sapeornis than other enantiornithines, suggests that
the rectricial fan evolves together with the rectricial bulbs necessary to control them, which
in turn shapes the pygostyle (O’Connor et al., 2016). The holotype and only known specimen
of Chiappeavis magnapremaxillo STM 29-11 was only briefly described with regards to
its skeletal morphology. Here we provide a complete description and further explore the
unique morphology of the pengornithid pygostyle. We reconstruct the tail fans of several well
preserved Jehol ornithuromorphs and compare the aerodynamic lift generated by different tail
shapes and discuss the signicance of this information.
O’Connor et al. -The morphology of Chiappeavis magnapremaxillo
Fig. 1 Photograph of the holotype and only known specimen of Chiappeavis magnapremaxillo STM 29-11
Scale bar equals 2 cm
2 Description
This description provides only new anatomical information regarding STM 29-11 (Fig. 2).
The enlarged premaxillary corpus and elongate nasal processes that distinguish Chiappeavis
from other pengornithids have already been described in detail (O’Connor et al., 2016). The
maxillary process of the premaxilla is robust, sharply tapered, and roughly equal to the length
of the corpus (Fig. 3). The premaxillae form a medial wedged articulation with the nasals
although the extent of this articulation is unclear due to poor preservation of the nasals. A
fragment of the left nasal is preserved articulating with the frontal; it appears narrower than the
nasal in Pengornis IVPP V 15336 (Zhou et al., 2008). Although the maxilla forms most of the
facial margin in Pengornis V 15336 (Zhou et al., 2008) and all other known pengornithids (Hu
et al., 2014, 2015; Wang X et al., 2014), only possible fragments are preserved in Chiappeavis
STM 29-11. Part of the scleral ring is preserved in the orbit. Other fragments may represent
pieces of the pterygoids. Ventrally, a thin, distally upturned rod-like element is identied as
44 Vertebrata PalAsiatica, Vol. 55, No. 1
the jugal. A robust fragment of bone is preserved dorsal and in parallel to the jugal; this bone
may be a piece of the jugal process of the maxilla but it appears unusually robust. Part of the
palate is visible through the left external nares (Fig. 3). Both vomers are preserved presumably
in dorsal view. As in Gobipteryx they appear to be fused along their rostral halves, caudally
diverging at a 15° angle (nearly parallel in Gobipteryx). This suggests that like Gobipteryx
the choana was rostrally located compared to neornithines (Chiappe et al., 2001). However,
unlike in Gobipteryx and neognathous birds, as preserved the vomers appear to retain the
plesiomorphic tetrapod condition, reaching and presumably articulating with the premaxillae,
as in paleognathous birds and potentially Archaeopteryx (Witmer and Martin, 1987). A
fragment of bone preserved between the left vomer and the maxillary process of the premaxilla
may be a piece of the maxillary contribution to the palate. The caudal half of the skull is
poorly preserved, crushed and heavily abraded, revealing no anatomical details. The tip of the
left dentary is blunt; barely visible, numerous small teeth are preserved in separate aveoli. The
Fig. 2 Interpretative line drawing of the preserved elements in STM 29-11
Anatomical abbreviations: ca. caudal vertebrae; ce. cervical vertebrae; cm. carpometacarpus; co. coracoid;
de. dentary; fe. femur; . bula; fu. furcula; ha. hallux; hs. horny sheath; hu. humerus; il. ilium; is. ischium;
l. left; lt. lateral trabecula; ma. major metacarpal; mi. minor metacarpal; mt I-IV. metatarsals I-IV; p. phalanx;
pb. pubes; pm. premaxilla; pt. proximal tarsals; py. pygostyle; r. right; ri. thoracic ribs; sc. scapula;
sr. sternal ribs; sy. synsacrum; tb. tibia; th. thoracic vertebrae; ul. ulna; un. ulnare
Scale bar equals 2 cm. Light grey indicates areas of bone that are broken or poorly preserved; dark grey
indicates soft tissue impression of feathers
O’Connor et al. -The morphology of Chiappeavis magnapremaxillo
postdentary bones are poorly preserved.
Approximately seven cervical vertebrae are poorly preserved in articulation with the skull
(Fig. 2). The cranial articular surfaces appear to be slightly concave. Proximally the cervicals
are preserved in ventral view; distally the series appears in caudal view. The third preserved
vertebra reveals small carotid processes. The costal processes are short and sharply tapered.
The proximal portion of the thoracic series is obscured by overlap with the thoracic girdle.
There are ve visible dorsal vertebrae; the rst two are disarticulated but the distal three are in
articulation with the synsacrum. The dorsal vertebrae show the typical enantiornithine condition
with the parapophyses located one-third from the proximal end and the lateral surface deeply
Fig. 3 Detail photograph (A) and line drawing (B) of the skull in
STM 29-11
Anatomical abbreviations not listed in Fig. 2 caption: f. frontal; j.
jugal; m. possible fragment of the palatal ramus of the maxilla; n.
nasal; np. nasal process of premaxilla; q?. possible quadrate;
sl. scleral ring; v. vomers. Scale bar equals 5 mm
excavated by a groove (Chiappe
and Walker, 2002). The neural
spines of the synsacrum are fused
into a continuous spinous crest,
which narrows and decreases in
height distally, as in V 15336.
The rst four transverse processes
are quadrangular, short and
wide; the last three are elongate
and caudolaterally oriented
and the fifth is intermediate in
morphology (Figs. 1, 2). Five free
caudal vertebrae are preserved,
which is fewer than reported in
other pengornithids (Hu et al.,
2014, 2015); the cranial articular
surface is exposed in the first
caudal vertebra revealing a weakly
concave surface. The transverse
processes are long, approximately
equal to the centrum width.
The neural canal is smaller than
the size of the exposed caudal
articular surfaces. The unfused
haemel arches are rectangular
with blunt distal margins.
s noted in a more detailed
study of the pygostyle (Wang and
O’Connor, in press) the pengornithid
pygostyle bears all the
46 Vertebrata PalAsiatica, Vol. 55, No. 1
characteristic features of other enantiornithines, although this clade differs in how these
morphologies are expressed. The pygostyle of Chiappeavis has a pair of ventrolateral processes
restricted to the proximal ventral half of the pygostyle whereas in other enantiornithines
these processes extend for most of the pygostyle length (Chiappe and Walker, 2002). The
ventrolateral processes project further ventrally and are limited to the proximal third of
the pygostyle in Pengornis V 15336 (Fig. 4B). Visible on the right, a small cranial fork is
present and continuous with a dorsolateral process that appears to extend the entire length of
the pygostyle (Fig. 4A). The dorsal surface between these dorsolateral processes is broadly
concave as in other pengornithids, whereas this concavity is narrow and deeper in other
enantiornithines, even when preserved dorsoventrally crushed (Wang and O’Connor, in press).
The left ramus of the furcula is preserved in dorsal view; the rami are slightly bowed
Fig. 4 Comparative photographs of the pygostyle
preserved in Chiappeavis STM 29-11 (A)
and Pengornis IVPP V 15336 (B)
Anatomical abbreviations not listed in Fig. 2 caption:
cf. cranial fork; dl. dorsolateral process;
vl. ventrolateral process. Scale bar equals 5 mm
medially similar to Pengornis V 15336
(Fig. 5). The dorsolateral excavation is
limited to the proximal 2/3 of the ramus; the
dorsal surface of the omal third is flat. The
omal tip tapers bluntly, as in Pengornis V
15336, and is pitted and striated suggesting
incomplete ossification of the articular
surfaces. A hypocleidium was present, as
in other pengornithids. As in Pengornis,
the process measures approximately half
the length of the furcular rami, whereas
the hypocleidium appears proportionately
longer in Parapengornis IVPP V 18687
(Fig. 5). Both coracoids are in articulation
with the coracoidal sulci of the sternum in
dorsal view; the dorsal lips of the sulci cover the sternal margin of the coracoids indicating that
the sulci are deep. The acrocoracoid, glenoid and scapular articular surface are weakly aligned,
as in other enantiornithines (Chiappe and Walker, 2002). The poorly developed glenoid and
scapular cotyla are separated by a deep pit, which may be an artefact of crushing and obscuring
the presence of an acrocoracoidal tubercle. Just distal to the scapular articular surface the
supracoracoid nerve foramen pierces the neck of the coracoid, separated from the medial margin
by a complete boney bar; it does not appear to open into a medially located groove as it does
in many other enantiornithines (Chiappe and Walker, 2002). The corpus makes up the distal
half of the coracoid. The distal quarter of the lateral margin is convex, expanding the width of
the sternal margin. The convex distal portion of the lateral margin appears distinctly thinner
and atter than the rest of the coracoidal corpus. This morphology of the lateral margin of the
coracoid is also observed in other pengornithids (Eopengornis, Parapengornis V 18687) as well
as bohaiornithid enantiornithines (Wang M et al., 2014). The corpus is weakly excavated by a
O’Connor et al. -The morphology of Chiappeavis magnapremaxillo
shallow dorsal fossa, also observed in some ornithuromorph birds (e.g., Yixianornis), inferred to
be the attachment of the m. supracoracoideus (Clarke et al., 2006).
Fig. 5 Pengornithid furculae
A. Chiappeavis STM 29-11; B. Pengornis IVPP V 15336; C. Eopengornis STM 24-11;
D. Parapengornis IVPP V 18687; E. Parapengornis IVPP V 18632
Note differences in Parapengornis: the straight furcular rami dene a greater angle in IVPP V 18632 and the
hypocleidium is proportionately longer in IVPP V 18687. Anatomical abbreviations listed in captions of Figs. 2, 4
The left scapula in lateral view overlaps the right in costal view, and where the two
shafts overlap the left is missing a piece of the shaft; both distal ends are unclear. The scapular
acromion process is slightly longer than the glenoid facet and hooked, as in other pengornithid
enantiornithines (Wang X et al., 2014). The cranial margin of the process is wide and at. The
scapular glenoid facet is large, concave, slightly tapered distally and forming a labum where it
contacts the scapular blade (Fig. 6). The body of the scapula is relatively wide and short as in
other pengornithids. The costal surface is smooth, lacking the groove present in more derived
enantiornithines (e.g. Elsornis, Neuquenornis) (Chiappe and Walker, 2002).
The straight coracoidal sulci meet at an 120° angle so that the rostral margin of the
sternum is weakly vaulted (Fig. 6). The craniolateral corners are weakly developed into slight
dorsolateral projections but no distinct craniolateral process is present. The entire lateral
margin of the sternum including the lateral trabecula is weakly concave. The dorsal surface of
each trabecula is keeled giving this process a triangular cross-section; distally the apex moves
from dorsolaterally located to centered on the dorsal surface and the distal third is at. The
distal ends of the trabeculae are weakly expanded this area of bone is also heavily pitted
and striated indicating ossification was incomplete. The lateral trabeculae extend distally
beyond the caudal margin of the xiphial region, as in V 18632 (level with caudal margin in
Eopengornis STM 24-11). The lateral margins of the median trabeculae are concave as the
sternal plates narrow caudally, whereas they are straight in Eopengornis and Parapengornis.
Compared to other known pengornithids, the xiphial region is more elongate and narrow in
STM 29-11 forming an incipient xiphoid process and dening approximately a 40° angle (75°
in Eopengornis and 70° Parapengornis). The xiphial region bears a short, straight caudal
margin, absent in Eopengornis and V 18632, in which the xiphial region defines a blunt
V-shaped margin (Hu et al., 2014; Wang X et al., 2014). Given the lack of maturity in all
specimens preserving sternal material, these apparent differences in the morphology of the
48 Vertebrata PalAsiatica, Vol. 55, No. 1
distal ends of the lateral trabeculae and proportions of the xiphial region may change with
the discovery of adult material. However, features like the concavity of the lateral margins in
Chiappeavis STM 29-11 are unlikely to change at this stage in maturity.
Fig. 6 Close up of the thoracic girdle in Chiappeavis STM 29-11
Anatomical abbreviations not listed in Fig. 2 caption: a. acromion
process of scapula; ap. acrocoracoid process; bc. bicipital crest;
cg. capital groove; dl. dorsolateral excavation of furcular rami;
dpc. deltopectoral crest; g. glenoid facet; hh. humeral head;
hy. hypocleidium; lg. lateral groove on thoracic vertebrae;
nf. supracoracoidal nerve foramen; ns. neural spine of thoracic
vertebrae; pr. pathologic rib; rc. rostral cleft of sternum; s. scapular
cotyla of coracoid; vt. ventral tubercle; xp. xiphial process
Scale bar equals 5 mm
Well-defined costal facets
are not visible but three robust
sternal ribs are visible articulating
on the right costal margin of the
sternum. The third rib is more
robust than the others and has an
uneven caudal margin that may
be pathological in origin (Fig. 6).
The left sternal ribs are displaced
over the dorsal surface of the
sternum they are short, robust,
and weakly curved. Several
disarticulated thoracic ribs are
preserved; a few are located
cranial to the sternum and a few
are associated with this element.
Compared to the cranially located
ribs, the ribs preserved near and
overlying the sternum are shorter,
more robust, and more weakly
curved, and probably articulated
with the sternal ribs.
The left humerus is preserved
in cranial view, while the right is in
caudal view. Proximally in caudal
view, the ventral tubercle is small,
separated by a wide, shallow
capital incision, and a pneumatic
fossa is absent. In cranial view,
a small bicipital crest is present,
weakly projecting cranially. The
width of the deltopectoral crest
is less than the width of the shaft
and extends along the proximal
third of the humerus. The shaft
weakly increases in width distally
O’Connor et al. -The morphology of Chiappeavis magnapremaxillo
from its narrowest point located midshaft, also observed in other pengornithids. The distal
caudal surface is poorly preserved revealing no anatomical details. The distal condyles are
small and located primarily on the cranial surface as in other birds. The circular dorsal condyle
is larger than the oval ventral condyle, although the two are approximately equal in diameter.
The long axis of the ventral condyle is transversely oriented. The round ventral epicondyle
is smaller than the ventral condyle, and located on the craniodistal surface of the ventrodistal
margin. The brachial fossa is not developed.
Both antebrachia are complete; the left is in caudal view and the right is cranially
exposed. As in other basal birds the ulnae are bowed along their proximal halves. The dorsal
cotyla is at and the ventral cotyla appears slightly concave. The radii are straight and more
than half the thickness of the ulna; crushing prevents identication of a longitudinal groove
like that present on the interosseous surface of some enantiornithines (Chiappe and Walker,
The ulnare is U-shaped; one ramus is bluntly tapered, while the other is short and more
robust, similar to that of Pengornis V 15336. The radiale is quadrangular but it is unclear which
surface is exposed. The semilunate carpal appears only partially fused to the metacarpals.
The right alular metacarpal is preserved unfused to the major metacarpal. It is narrow and
approximately 1/5 the length of the carpometacarpus. The proximal end is rounded and the
distal end appears ginglymous. As in V 15336 the proximal end of the minor metacarpal wraps
onto the ventral surface of the major metacarpal and the ventral surface of the proximal third
of the minor metacarpal forms a ridge rather than a distinct pisiform process, a morphology
common in Early Cretaceous enantiornithines (O’Connor, 2009). The first phalanx of the
major digit is incomplete but like other enantiornithines it maintains the plesiomorphic
theropod condition and lacks any caudal expansion like that present in ornithuromorph birds.
The penultimate phalanx is not preserved; the ungual phalanx is small and weakly curved. The
rst phalanx of the minor digit is wedge-shaped with a at cranial margin and convex caudal
margin, tapering to a blunt distal margin.
Both ilia are preserved in articulation with the synsacrum (Figs. 1, 2). The right ilium
is preserved in medial view while the left appears in dorsal view. In lateral view, the dorsal
margin is weakly convex. The ventral margins of the preacetabular and postacetabular alae
are straight. The pubic pedicel of the ischium is wider than the iliac pedicel. The preacetabular
wing is longer and dorsoventrally taller than the postacetabular wing and the postacetabular
wing is bluntly tapered as in V 18632 and most enantiornithines. The right ischium, preserved
in medial view, is long, delicate and gently tapered; the dorsal margin is concave and the
ventral margin is convex (Figs. 1, 2). The pubes have a thick oval cross section with a
craniodorsal-caudoventrally oriented long axis. The distal third is heavily pitted and striated.
Both femora are preserved although the right is overlain by the pubes and ischia and
the proximal end is not exposed on either side (Figs. 1, 2). As described, a small tibiobular
crest is present distally (O’Connor et al., 2016). The right tibia is in caudal view exposing the
50 Vertebrata PalAsiatica, Vol. 55, No. 1
popliteal tuberosity and lateral articular facet on the proximocaudal surface, also developed
in Pengornis and Eopengornis (Wang X et al., 2014). The exor fossa is weak or absent. The
left tibia is exposed in craniolateral view; the proximal tarsals are fused to each other forming
the condyles. The medial condyle is wider than the lateral condyle. They are separated by a
wide, shallow intercondylar incisure. The lateral margin of the lateral condyle and the medial
margin of the medial condyle are both straight and the opposing surfaces are strongly convex,
as in Pengornis V 15336. The lateral condyle is excavated by a deep concavity on the lateral
surface as in some enantiornithines (e.g., Qiliania) (Ji et al., 2011). The ascending process is
triangular, tapering proximally, and taller than the height of the condyles. Only the right bula
is preserved and it is incomplete so it cannot be determined if it reached the distal condyles as
in other pengornithids (Wang X et al., 2014).
No distal tarsals are preserved, as in other pengornithids. The metatarsals are unfused and
slightly disarticulated; the exposed surfaces are abraded, preserving very little information.
Metatarsal IV is thinner than metatarsal III, which is in turn thinner than metatarsal II. The
digit of metatarsal II is robust with a large ungual phalanx; the ungual phalanx in digit III
is long but not as robust as those of digits I and II. The digit IV ungual is the smallest. No
metatarsal V is preserved although it was likely present, as in other pengornithids (Wang X et
al., 2014).
Ontogenetic status STM 29-11 is clearly immature based on the incomplete ossication
of the periosteal surface of the bone evident from the striated pits that sparsely cover the
surface of most elements. As would be expected, fusion is incomplete in the sternum and
proximal carpometacarpus, and the compound bones of the hindlimb have yet to fully co-
ossify. The compound bones of the axial skeleton, the pygostyle and synsacrum, are fully fused
in all subadult enantiornithine specimens supporting the inference that the difference in the
number of sacral vertebrae is a true distinction between Chiappeavis and Pengornis. The age
of the specimen has not been explored through histology because there are no breaks in the
long bones of STM 29-11 to allow non-destructive sampling of this particularly nice specimen.
However, the sternum is fully fused in the subadult holotype of Eopengornis martini STM
24-1 and V 18632. This indicates that STM 29-11 is at a relatively earlier ontogenetic stage and
strongly suggests it would have increased in size with maturity. The sternum in Parapengornis
V 18687 is also medially unfused, despite its much smaller size (Table 1) and histology
conrms that this specimen is immature, with no remodelling present to indicate the individual
was mature or nearly so. Parapengornis sp. V 18632 has a fully fused sternum but is roughly
15% smaller than Parapengornis V 18687 indicating these specimens may represent different
species (see phylogenetic analysis). As preserved STM 29-11 is 20% smaller than the holotype
of Pengornis houi V 15336, although given the relative immaturity of the former specimen we
suggest the terminal body size in Pengornis and Chiappeavis would have been similar.
O’Connor et al. -The morphology of Chiappeavis magnapremaxillo
Table 1 Select measurements of published pengornithids (mm)
Pengornis Parapengornis Eopengornis Chiappeavis
IVPP V 15336 IVPP V 18632 IVPP V 18687 STM 24-1 STM 29-11
right left
Scapula (36.3) 34.9 46.3 27.2 (40.9) 45.2
Coracoid L 39 (17.4) 26.3 17.8 30.1
Coracoid W (18) 14 (9.7) 17.6
Sternum L (22.7) 33 22 38
Sternum W 32 22 31
Humerus 72 45.7 52.1 38 55.7 57.8
Ulna 78 49 54.9 42.4 63.4 63.5
Radius (66) 49 53.7 41.5 58.1 60.3
Carpometacarpus 34.2 23.8 30.7 23.3 30.9 30
Major metacarpal 29.1* 20.1 24.8 18.2 26.5 27.7
Minor metacarpal 31.4 19.7 27.4 20.1 29.8
Alular metacarpal 4.2 5.3 3.4
Alular digit ph1 10.7 11.4 9.5
Alular digit ph2 5.5 6.7 3.9 –
Major digit ph1 16 12.5 12.7 9.3
Major digit ph2 11.6 8.8 9.2 7.2
Major digit ph3 4.5 4.8 3.6 – 5.2
Minor digit ph1 6.9 6.3 8.1 6.3 – 8.4
Hand 56.8 45.9 1.2 38.3
Femur 53 34.8 39.8 27 42.9
Tibiotarsus 55 37.7 40.4 31 44.6 46.7
Femur/tibiotarsus 0.96 0.92 0.99 0.87 0.92
Fibula (28) (12) 34 29 (36) (40)
Metatarsal I 8.2 6.9 8.6 6.9 – 8.2
Metatarsal I ph1 6.7 9.2 7.8 10.4
Metatarsal II 24 18.9 19.5 15.9 (22.4)
Metatarsal III 26.6 20.5 17 (22.5)
Metatarsal IV 25 18 15.9 – 20.5
Pygostyle 18.2 7.5 10 5.1 15
Synsacrum 24 – – – 24
Pubis (31) 35 37.2 26 – 47.1
Ilium (14) 30 – 29 –
Ischium 21 21 (5.2) 25.4 –
Notes: W. width; L. length; ph. phalanx. * estimated measurement, ( ) indicate incomplete elements.
3 Phylogenetic Analysis
We investigated the phylogenetic placement of Chiappeavis using a modied version of
the O’Connor and Zhou (2013) dataset that includes the revised character 220 used by Wang
X et al. (2014). The dataset includes ve pengornithids: Eopengornis, Parapengornis IVPP
V 18687 and IVPP V 18632, Pengornis, and Chiappeavis. (Hu et al., 2014, 2015; O’Connor
et al., 2016; Wang X et al., 2014; Zhou et al., 2008). The matrix includes a total of 63 taxa,
24 of which are referable to the Enantiornithes. Using TNT software (Goloboff et al., 2008)
we conducted a heuristic search using tree-bisection reconnection (TBR) retaining the single
shortest tree out of every 1,000 replications. This produced 824 most parsimonious trees
52 Vertebrata PalAsiatica, Vol. 55, No. 1
with a length of 897 steps. A second round of TBR produced more than 10,000 trees of the
same length. In the strict consensus, all nodes collapsed except Aves itself. Investigation of
the MPTs revealed that in 78% of the trees Pengornithidae was resolved. The clade formed
by Jeholornis + all more derived birds collapses due to the basal position of the fragmentary
taxon Chaoyangia resolved by a small percentage of MPTs. In order to reduce the effects of
homoplasy (Goloboff et al., 2008), which strongly characterizes early avian evolution (Brusatte
et al., 2015), we reran the analysis with the same parameters using implied weighting (k = 1.0,
2.0, and 3.0) (Goloboff, 1993). With a k value of 1.0, the analysis produced 24 trees (TBR =
129.47). The strict consensus is well resolved with pengornithids forming successive outgroups
to all other enantiornithines. With higher k values (2.0, 3.0) Pengornithidae is resolved as a
clade that is sister taxon to all other enantiornithines (Fig. 7).
4 Discussion
Pengornithid diversity Five pengornithid specimens are now recognized, representing
at least four distinct genera (Chiappeavis, Eopengornis, Parapengornis, and Pengornis).
Pengornithids are unusual birds, differing from other enantiornithines in the morphology of the
sternum (e.g., ossifying from a pair of medially fused bilateral plates and having only a single
pair of caudal trabeculae), pygostyle (shorter, wider, with proximally restricted ventrolateral
processes, often having a midline invagination on the caudal margin), and ischium (slender
without a dorsal process). In addition, they possess features more typical of long boney-tailed
birds or basal pygostylians, such as the presence of a metatarsal V and an elongate bula. This
marked increase in homoplasy caused by the inclusion of ve pengornithids has thus resulted
in a collapse in weakly resolved relationships from previous analyses, making a strong case
for the use of implied weighting. Without the use of implied weighting Pengornithidae is only
resolved in 78% of the MPTs, but in 98% of all MPTs V 18632 and Eopengornis form a clade,
thus not supporting previous inferences that V 18632 should be referred to Parapengornis
(Hu et al., 2015). This is further supported by differences in body size between V 18632 and
Parapengornis V 18687 (see Ontogenetic status). Difference in size, morphology (Fig. 5), and
stratigraphic level also suggest V 18632 is not referable to Eopengornis martini. Because the
specimen is a subadult, Hu et al., (2014) originally refrained from naming V 18632 (Pengornis
sp.), later referring it to Parapengornis (Hu et al., 2015). Here we regard this specimen as
Pengornithidae indeterminate. Notably, Eopengornis and Parapengornis share a common
tail morphology consisting of a pair of elongate, fully pennaceous rachis dominated feathers
but are not found to be closely related; instead, Eopengornis is found to be more closely
related to Chiappeavis, despite their disparate tail morphologies. This may suggest that this
analysis does not accurately portray pengornithid relationships or that pengornithid plumage
was as evolutionarily labile as in extant avian families (Gluckman, 2014). In favor of the
former, the pygostyle of Chiappeavis is most similar to that of Pengornis with regards to
O’Connor et al. -The morphology of Chiappeavis magnapremaxillo
Fig. 7 Phylogenetic hypothesis of Mesozoic bird relationships using implied weighting (k=3.0)
54 Vertebrata PalAsiatica, Vol. 55, No. 1
proportions, whereas that of Parapengornis and Eopengornis are slightly shorter, suggesting
that Pengornis may have had a rectricial fan. This subtle interclade diversity is not captured by
the abstract morphologies encapsulated by this and other current character matrices used for
the phylogenetic analysis of Mesozoic birds.
Large body size (Table 1) and stratigraphic level (Jiufotang) suggest that Chiappeavis is
more closely related to Pengornis than to Parapengornis (smaller) or Eopengornis (smaller,
Huajiying), which is further supported by the morphology of the furcula (furcular rami curved
in Chiappeavis and Pengornis whereas they are straight in Parapengornis) (Fig. 5). The
sternum in Chiappeavis is proportionately more elongate (length greater than width) than in
Parapengornis and Eopengornis (length and width subequal). It further differs from smaller
pengornithids in the morphology of the xiphial region of the sternum: the lateral margins of
median trabeculae are concave in the new taxon, whereas they are straight in Eopengornis
and Parapengornis. Ontogenetic and preservational differences obfuscate comparison with
Pengornis V 15336. Postcranially, Pengornis V 15336 and Chiappeavis STM 29-11 are similar
but STM 29-11 has a greater number of sacral vertebrae despite its immaturity (although
the cranial margin of the synsacrum is obscured, clearly only seven sacrals are present in
Pengornis V 15336) and the proximal articular surface of the tibia is inclined. The increased
number of sacral vertebrae and expanded premaxillae suggest Chiappeavis is more advanced
than other pengornithids.
Tail-fan performance in Early Cretaceous birds Even in the Jehol Biota, at the
earliest known stage of pygostylian evolution with data limited by fossilization, there exist
observable differences in the shape and relative size of the rectricial fan between clades and
individual taxa. Compared to all Jehol ornithuromorphs preserving tail fans (Yixianornis,
Yanornis, Hongshanornis, Schizooura, Piscivoravis) (Chiappe et al., 2014; Clarke et al., 2006)
(Fig. 8), the tail is proportionately shorter relative to body length in Chiappeavis STM 29-
11 (Table 2). These taxa also differ in the degree of gradation (measured as the difference in
length between the longest and shortest rectrices). Subtle differences in tail shape and length
can be used to understand the selective pressures responsible for producing each phenotype.
Lift is determined by the maximum continuous width, therefore any elongation beyond this
point is considered the product of sexual selection, being not optimized for ight (Thomas and
Balmford, 1995). In one test area, 80% of all bird species were found to have tail displays of
some kind (Fitzpatrick, 1997). Although two tails of equal width have the same lift, longer tails
generate greater moments for turning; the trade-off is that longer tails require greater muscle
force and incur more drag (Thomas and Balmford, 1995). Thus the huge diversity of avian tail
morphologies represents the product of these and the numerous other selective forces that exist
in the varied ecologies and lifestyles occupied by birds. The graded morphology in Sapeornis
and even the round morphology in ornithuromorphs indicate that although capable of
generating lift, these tails were not optimized for aerodynamic function, being also shaped by
sexual/signal selection. The difference between the longest and shortest rectrices is highest in
O’Connor et al. -The morphology of Chiappeavis magnapremaxillo
Sapeornis and Chiappeavis suggesting this inuence was strongest in these taxa. Shorter tails
tend to be adapted for higher ight speeds and greater lift to drag ratios, whereas longer tails
increase maneuverability and are found in woodland birds where the cluttered environment
selects for increased maneuverability and high-speed flight is infrequent (Thomas, 1997;
Thomas and Balmford, 1995). Thus the presence of long round-tails in most ornithuromorphs
indicates these taxa well adapted for the forested Jehol paleoenvironment (Zhou, 2004).
Since longer tails require greater muscle force, the proportionately shorter tail in Chiappeavis
supports inferences based on pygostyle morphology that rectricial bulbs, if present, were
poorly developed in enantiornithines. Some extant birds have a pygostyle similar to that of
enantiornithines in which the dorsal surface is expanded (having a dorsal platform and thus no
dorsally blade-like pygostyle lamina) to provide additional surface area for the attachment of
enlarged caudal levator muscles, yet these taxa retain rectricial bulbs (Wang and O’Connor, in
press). Thus the absence of a pygostyle lamina does not exclude enantiornithines from having
this structure.
Fig. 8 Rectricial fan morphology in Early Cretaceous ornithothoracines
A. photograph of the tail impression preserved in Chiappeavis magnapremaxillo STM 29-11, scale bar equals 1
cm. Reconstructions are based on the following specimens: B. Yanornis STM 9-19; C. Hongshanornis DNHM
D 2945; D. Yixianornis IVPP V 12631; E. Chiappeavis STM 29-11. Rectricial fans and pygostyles are drawn
to scale; scale bar equals 2 cm
In order to more directly quantify aerodynamic differences in tail shape we reconstructed
the rectricial fan for several taxa based on the specimens most clearly preserving this feature
(Table 2) and estimated their lift (Thomas, 1993). We recognize that the preserved width is not
necessarily the optimal or maximal spread of the tail in ight, but like living birds we assume
56 Vertebrata PalAsiatica, Vol. 55, No. 1
a range of widths were possible at least in the Ornithuromorpha. We assume equal post-
mortem compression of the rectricial bulbs (or comparable tail musculature in Chiappeavis
and Sapeornis) resulting in a comparable degree of tail spread between Jehol specimens.
Specimens preserved in lateral view were considered unsuitable for analysis. For Jehol birds
these measurements represent conservative estimates of the tail’s lift capabilities. The tail fan
of Chiappeavis is estimated to have the least efficient tail shape, whereas the tails in most
Jehol ornithuromorphs have almost double the lifting power for their given body mass (Table
2). These measurements support our predictions based on the shape of the pygostyle and
associated rectricial fan. The limited function of the enantiornithine tail fan, quantied here
for the first time, provides support for the hypothesis that this is the cause of the restricted
distribution of this feature in the Enantiornithes. Paired with limited musculature (as inferred
from pygostyle morphology) and the potential absence of the ability to control the spread
of the tail fan, the enantiornithine aerodynamic rectricial fan may not have provided a great
enough reproductive advantage to be retained through natural selection. This is at odds with
derived skeletal features present in Chiappeavis (enlarged premaxilla, longer synsacrum),
which may alternatively suggest that a tail fan was independently evolved in the Chiappeavis
Table 2 Comparison of tail morphologies and their associated aerodynamic benets
between Early Cretaceous birds
rectrices morphology fan width (mm) body weight (g) delta lift (N) lift/mass (N/g)
Archaeopteryx frond 90 304 0.05 0.00016
Jeholornis 4–6 two-tail 80–103 606 0.04–0.07 0.00012
Chiappeavis 8graded 50 205 0.021 0.00010
Hongshanornis 10 round 40 44 0.013 0.00028
Yanornis 8round 75 314 0.052 0.00017
Yixianornis 8graded 57 148 0.028 0.00019
Columba 12 round 260 350 0.42 0.0012
Body mass was estimated using humeral length and the equations by Liu et al. (2012). Note that despite
differences in their tail morphology, long-tailed birds generated similar amounts of lift (O’Connor et al., 2013). The
tail in the neornithine Columba is estimated to generate a whole order of magnitude higher lift. Data for Columba was
taken from Gatesy and Dial (1996); measurements for the London Archaeopteryx were taken from Wellnhofer (2008).
Measurements from fossil specimens assume similar amounts of fanning due to comparable post-mortem compression
and probably do not represent maximum spread, thus representing conservative estimates of the tail’s lift capabilities.
Acknowledgements We thank SHI Ai-Juan (IVPP) for assistance with gures, T. Stidham
(IVPP) for useful discussions, WANG Min (IVPP) and LI Zhi-Heng (IVPP) for useful
comments on an earlier version of this manuscript, and WANG Min (IVPP) for editing the
Chinese abstract. This research was supported by the National Basic Research Program of
China (973 Program, 2012CB821906), the National Natural Science Foundation of China
(41172020, 41172016, 41372014), and the Chinese Academy of Sciences.
O’Connor et al. -The morphology of Chiappeavis magnapremaxillo
巨前颌契氏鸟 (鹏鸟科:反鸟类)的形态学描述及
邹晶梅1 郑晓廷2,3 胡 晗1 王孝理2,3 周忠和1
(1 中国科学院古脊椎动物与古人类研究所,中国科学院脊椎动物演化与人类起源重点实验室 北京 100044)
(2 临沂大学地质与古生物研究所 山东临沂 276000)
(3 山东省天宇自然博物馆 山东平邑 273300)
构在较原始的反鸟类中已经发育。详细描述了巨前颌契氏鸟(C. magnapremaxillo)正型标本
中图法分类号Q 915.865 文献标识码A 文章编号1000−3118(2017)01−0041−18
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... Although the fossil record of stem birds and their closest relatives has grown enormously over the past 3 decades (23), detailed information concerning palatal morphology in these taxa is extremely rare due to their delicate nature and the crushed, 2D preservation of most specimens. With only few exceptions, the palate is partially preserved in 2D in some specimens of the Late Jurassic Archaeopteryx (24)(25)(26), the Early Cretaceous enantiornithine Chiappeavis (27), the Late Cretaceous enantiornithine Gobipteryx (28,29), the Late Cretaceous ornithurine Ichthyornis (30), and ambiguously in Hesperornis (31,32). Consequently, despite great interest, the origin of the modern avian palate and cranial kinesis from the akinetic nonavian theropod condition remains poorly understood (8,30,32,33). ...
... Cladogram was simplified and modified from previous publications (2,19,35,(41)(42)(43). Palate of Incisivosaurus, Dromaeosaurus, and Sinovenator was reconstructed and modified from previous publications (35-37, 41, 44, 45) and the vomer extracted in this study; palate of Archaeopteryx, Chiappeavis, Gobipteryx, Hespeornis, and Tinamous was modified from previous publications (25,27,(46)(47)(48) Based on these results, we reconstructed 3D models of the vomer for 17 representatives of the 24 orders of neornithines in which the vomer remains (SI Appendix, Table S3). Using these models together with the data from Sapeornis and Sinovenator, we conducted a 3D geometric morphometric (GMM) analysis of the vomer with a generalized Procrustes analysis (GPA) and a principal component analysis (PCA) (for landmark locations, see SI Appendix, Fig. S1). ...
... Very little palatal data are available for the Enantiornithes, the dominant clade of Cretaceous terrestrial birds. The best data come from the Late Cretaceous Gobipteryx (28,29), and an element was ambiguously identified as the vomer in Early Cretaceous Chiappeavis (27). Despite the poor preservation, the overall mediolaterally extensive morphology of the vomer in Chiappeavis suggests a condition similar to that in Sapeornis and paleognaths. ...
Most living birds exhibit cranial kinesis—movement between the rostrum and braincase—in which force is transferred through the palatal and jugal bars. The palate alone distinguishes the Paleognathae from the Neognathae, with cranial kinesis more developed in neognaths. Most previous palatal studies were based on 2D data and rarely incorporated data from stem birds despite great interest in their kinetic abilities. Here we reconstruct the vomer of the Early Cretaceous stem bird Sapeornis and the troodontid Sinovenator , taxa spanning the dinosaur–bird transition. A 3D shape analysis including these paravians and an extensive sampling of neornithines reveals their strong similarity to paleognaths and indicates that morphological differences in the vomer between paleognaths and neognaths are intimately related to their different kinetic abilities. These results suggest the skull of Mesozoic paravians lacked the kinetic abilities observed in neognaths, a conclusion also supported by our identification of an ectopterygoid in Sapeornis here. We conclude that cranial kinesis evolved relatively late, likely an innovation of the Neognathae, and is linked to the transformation of the vomer. This transformation increased palatal mobility, enabling the evolution of a diversity of kinetic mechanisms and ultimately contributing to the extraordinary evolutionary success of this clade.
... 11,12 However, unlike those taxa, the mediorostral end of the ectopterygoid body strongly projects rostrally, suggesting a broad surface contacting the pterygoid. As typical of pengornithids, 7,8,13 the dentary is packed with numerous, blunt, and low-crowned teeth; 12 teeth are preserved on the left side. The postdentary mandibular elements are fused with one another, forming a rostroventrally sloping articulation with the dentary. ...
... The proximal phalanx of the hallux is the longest, but that of digit II is the most robust, as in other pengornithids. 8,13 The ungual phalanges are strongly recurved and bear deep medial and lateral grooves as in other enantiornithines, 2 suggesting an arboreal lifestyle. ...
Enantiornithes are the most successful group of Mesozoic birds, arguably representing the first global avian radiation,1, 2, 3, 4 and commonly resolved as the sister to the Ornithuromorpha, the clade within which all living birds are nested.1,3 The wealth of fossils makes it feasible to comparatively test evolutionary hypotheses about the pattern and mode of eco-morphological diversity of these sister clades that co-existed for approximately 65 Ma. Here, we report a new Early Cretaceous enantiornithine, Yuanchuavis kompsosoura gen. et. sp. nov., with a rectricial fan combined with an elongate central pair of fully pennaceous rachis-dominated plumes, constituting a new tail plumage previously unknown among nonavialan dinosaurs and Mesozoic birds but which strongly resembles the pintail in many neornithines. The extravagant but aerodynamically costly long central plumes, as an honest signal of quality, likely evolved in enantiornithines through the handicap process of sexual selection. The contrasting tail morphotypes observed between enantiornithines and early ornithuromorphs reflect the complex interplay between sexual and natural selections and indicate that each lineage experienced unique pressures reflecting ecological differences. As in neornithines, early avialans repeatedly evolved extravagant structures highlighting the importance of sexual selection in shaping the plumage of feathered dinosaurs, even early in their evolutionary history.
... Jeholornithiformes is an early-diverging bird group from the Early Cretaceous Jehol Biota of China, retaining numerous primitive features, such as a long, bony tail (Zhou & Zhang, 2002;O'Connor et al., 2012;Rauhut et al., 2018). Among Aves, they are resolved by almost all phylogenetic analyses as being the earliest diverging Cretaceous stem bird lineages, crownward only to the Late Jurassic Archaeopteryx Meyer, 1861 from the Solnhofen Limestones in southern Germany (Zhou & Zhang, 2007;Zhou, 2014;O'Connor et al., 2016O'Connor et al., , 2017Wang et al., 2019bWang et al., , 2020bWang et al., 2019a). Jeholornithiformes is the sister lineage of Pygostylia, a clade that includes the edentulous Confuciusornithiformes, Sapeornis Zhou & Zhang, 2002, in addition to the species-rich Enantiornithes and Ornithuromorpha (the lineage that gave rise to modern birds), with the last two of these clades together forming Ornithothoraces. ...
Jeholornis is a representative of the earliest-diverging bird lineages, providing important evidence of anatomical transitions involved in bird origins. Although ~100 specimens have been reported, its cranial morphology remains poorly documented owing to poor two-dimensional preservation, limiting our understanding of the morphology and ecology of the key avian lineage Jeholornithiformes, in addition to cranial evolution during the origin and early evolution of birds. Here, we provide a detailed description of the cranial osteology of Jeholornis prima, based primarily on high-quality, three-dimensional data of a recently reported specimen. New anatomical information confirms the overall plesiomorphic morphology of the skull, with the exception of the more specialized rostrum. Data from a large sample size of specimens reveal the dental formula of J. prima to be 0–2–3 (premaxillary–maxillary–dentary tooth counts), contrary to previous suggestions that the presence of maxillary teeth is diagnostic of a separate species, Jeholornis palmapenis. We also present evidence of sensory adaptation, including relatively large olfactory bulbs in comparison to other known stem birds, suggesting that olfaction was an important aspect of Jeholornis ecology. The digitally reconstructed scleral ring suggests a strongly diurnal habit, supporting the hypothesis that early-diverging birds were predominantly active during the day.
... Accordingly, it is unlikely that the expansion of sternal rib 4 had any effect on the ability of the gastralia to contribute to ventilation. Notably, the third and caudalmost preserved sternal rib in the pengornithid enantiornithine Chiappeavis STM29-11 also bears an expansion (Fig. 5B), although this feature is more distally located and much smaller than its counterpart on sternal rib 4 of Jeholornis (O'Connor et al., 2017). Despite being relatively poorly developed, the expansion of sternal rib 3 in Chiappeavis suggests that modification of the sternal rib basket to improve the mechanical performance of the associated musculature also occurred in at least some birds substantially more derived than Jeholornis. ...
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.
... (O'Connor et al., 2016;O'Connor et al., 2017); the ventrolateral margin forms a blunt projecting keel whereas the medial margin would have formed the acute apex of the triangle. The xiphial region (fused median trabeculae) (triangular medial process of Zhang& Zhou, 2000) defines a wide V (Chiappe et al., 2019a) of approximately 75 along the cranial half, and narrows demarcating an angle of approximately 30 along the caudal half (the distal most portion of the xiphial region is not preserved in STM7-143), bluntly tapering into a rounded caudal margin (IVPP V11844, BMNHC-Ph1060a). ...
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.
... The acrocoracoid process is straight as in most enantiornithines (H. O'Connor et al. 2017). The lateral margin is convex distally (Fig. 4B), being slightly less developed than that observed in the holotype but still distinctly more convex than in other bohaiornithids (M. ...
Bohaiornithidae is currently the most diverse recognized family of Early Cretaceous enantiornithines, with unique morphology of the rostrum and pedal digits. Here we describe a second specimen of the bohaiornithid Longusunguis kurochkini from the Jiufotang Formation. This specimen provides new anatomical information regarding this taxon, in particular clarifying uncertain aspects of enantiornithine cranial morphology. The rarely preserved postorbital is completely preserved on both sides of the skull, confirming the presence of a complete postorbital bar in some enantiornithines. This suggests that the plesiomorphic diapsid skull was retained by at least some basal enantiornithines and the infratemporal fenestra in Ornithothoraces may have been lost independently multiple times, providing a better understanding of cranial evolution from non-avian dinosaurs to modern birds.
... The fossil was collected by an IVPP team in the Lower Cretaceous Jiufotang Formation 25 near Chifeng, Inner Mongolia Autonomous Region, China. The presence of a femur nearly as long as the tibiotarsus, elongate fibula subequal in length to the tibia, presence of metatarsal V, and a proportionately elongate metatarsal I (38% length of metatarsal III; 33-42% in pengornithids) and hallux clearly allow referral of IVPP V15576 to the Pengornithidae, a diverse clade of basal enantiornithines 26 . This is the first pengornithid collected from Inner Mongolia, but without additional material for the specimen, it cannot be identified to the generic level. ...
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Living birds are unique among vertebrates in the formation of a female-specific bone tissue called medullary bone (MB) that is strictly associated with reproductive activity. MB is a rapidly mobilized source of calcium and phosphorus for the production of eggshell. Among living taxa, its skeletal distribution can be highly extensive such that it even exists in the ribs of some species. Due to its ephemeral nature MB is rarely fossilized, little is understood with regards to the origin of MB and its skeletal distribution in early taxa. Here we describe a new Early Cretaceous enantiornithine bird, Mirusavis parvus, gen. et. sp. nov., indicating that skeleton-wide distribution of MB appeared early in avian evolution. We suggest that this represents the plesiomorphic condition for the Aves, and that the distribution of MB observed among extant neornithines is a product of increased pneumatization in this lineage and natural selection for more efficient distribution of MB.
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New and important pennaraptoran specimens continue to be discovered on a regular basis. Yet, with these discoveries the number of viable phylogenetic hypotheses has increased, including ones that challenge the traditional grouping of dromaeosaurids and troodontids within a monophyletic Deinonychosauria. This chapter will cover recent efforts to address prevailing phylogenetic uncertainties and controversies, both between and within key clades, including deinonychosaurian monophyly, the phylogenetic position of anchiornithines and scansoriopterygids, and the interrelationships of enantiornithines. While recent discoveries mainly from Asia have created much of the latest uncertainty and controversy, new material, particularly from Asia, promises to rather fittingly address these issues. Further curatorship of long-standing phylogenetic datasets and more prevalent use of extended analytical protocols will be essential to meeting this challenge, especially for groups whose boundaries have been blurred. As it becomes increasingly difficult to study all fossil materials, owing to their growing numbers and ever disparate locations, broader use of digital fossils and online character databases for character coding is acutely needed to ensure that errors arising from remote, rather than firsthand, scoring are reduced as far as possible, particularly at this time of rapid data accumulation.
We describe the detailed cranial osteology of Sapeornis chaoyangensis based on information from previously described specimens and IVPP V19058, a specimen that was recently reported with regards to the palatal elements but not fully described. The skull in this specimen is entirely preserved in disarticulation, providing the most comprehensive glimpse into the morphology of the cranial bones and their articulations for this taxon. Based on the new information extracted from this specimen, we revise some interpretations of cranial elements in previously published Sapeornis specimens and provide a comprehensive description of the cranial osteology for this basal pygostylian. The results of this study demonstrate that the postorbital bar, jugal bar, nasal, quadrate, and palate in Sapeornis show the plesiomorphic rigid articulations among birds. The comparison of cranial features across Paraves suggests that major cranial modifications evolved at the base of Ornithothoraces, and primarily in the ornithuromorph lineage.
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The transformation from a long reptilian tail to a shortened tail ending in a pygostyle and accompanied by aerodynamic fanning rectrices is one of the most remarkable adaptations of early avian evolution. However, no fossils directly capture this transition, and information regarding the structural morphology and the early evolution of the pygostyle in Mesozoic birds and their integuments is relatively limited. Here we provide a review of the pygostyle morphology of Early Cretaceous birds with comparison to the structure in living birds. This study emphasizes the convergent evolution of distally co-ossified caudal vertebrae in non-avian maniraptorans and early birds. There further exist distinct differences in pygostyle morphology between Sapeornithiformes, Confuciusornithiformes, Enantiornithes, and Ornithuromorpha. The morphology of the pygostyle and rectrices in early ornithuromorphs appear similar to that of extant birds, whereas the pygostyle in more primitive birds does not appear morphologically capable of supporting the rectricial bulbs and musculature necessary to control an aerodynamic fan-shaped tail. The rectricial bulbs and rectricial fan appear to have coevolved with the plough-shaped pygostyle early in the evolution of the Ornithuromorpha. This study also shows that the confuciusornithiform pygostyle was more similar to that of enantiornithines than previously recognized, consistent with the presence of nearly identical ornamental tail feathers in both groups.
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Birds are one of the most recognizable and diverse groups of modern vertebrates. Over the past two decades, a wealth of new fossil discoveries and phylogenetic and macroevolutionary studies has transformed our understanding of how birds originated and became so successful. Birds evolved from theropod dinosaurs during the Jurassic (around 165-150 million years ago) and their classic small, lightweight, feathered, and winged body plan was pieced together gradually over tens of millions of years of evolution rather than in one burst of innovation. Early birds diversified throughout the Jurassic and Cretaceous, becoming capable fliers with supercharged growth rates, but were decimated at the end-Cretaceous extinction alongside their close dinosaurian relatives. After the mass extinction, modern birds (members of the avian crown group) explosively diversified, culminating in more than 10,000 species distributed worldwide today.
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We describe a new enantiornithine bird, Parapengornis eurycaudatus gen. et sp. nov. from the Lower Cretaceous Jiufotang Formation of Liaoning, China. Although morphologically similar to previously described pengornithids Pengornis houi, Pengornis IVPP V18632, and Eopengornis martini, morphological differences indicate it represents a new taxon of the Pengornithidae. Based on new information from this specimen we reassign IVPP V18632 to Parapengornis sp. The well preserved pygostyle of the new specimen elucidates the morphology of this element for the clade, which is unique in pengornithids among Mesozoic birds. Similarities with modern scansores such as woodpeckers may indicate a specialized vertical climbing and clinging behavior that has not previously been inferred for early birds. The new specimen preserves a pair of fully pennaceous rachis-dominated feathers like those in the holotype of Eopengornis martini; together with the unique morphology of the pygostyle, this discovery lends evidence to early hypotheses that rachis-dominated feathers may have had a functional significance. This discovery adds to the diversity of ecological niches occupied by enantiornithines and if correct reveals are remarkable amount of locomotive differentiation among Enantiornithes.
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Body mass or weight is a crucial biological parameter for an organism. It is influenced by development, reproduction, physiology and evolution. Therefore, mass estimates for fossil species are important for many kinds of analyses. In this project, eighteen bivariate regression analyses of different measurements of the appendicular skeleton plotted against body weight in a data set of 422 individual birds, representing 229 species in 21 orders, revealed high correlations between several skeletal parameters and body mass. R-squared values of eighteen bivariate equations are ranged from 0.50 for tibiotarsal length, indicating a relative poor fit, to 0.91 for humeral diameter. To test the 18 equations empirically, they were used to predict the body weight of an additional 64 extant bird specimens, and the accuracies of various equations were compared. This predictive test showed that three parameters are generally most accurate as predictors of body mass: humerus length, ulna diameter, and tibiotarsal diameter. However, the humeral length and ulna diameter tended to give accurate results for particularly songbirds, raptors and climbing birds. The tibiotarsal diameter tended to give accurate results for terrestrial birds, such like chicken and doves. It is probable that humerus length and ulna diameters are the more accurate parameter for arboreal taxa, while tibiotarsal diameter is more accurate for terrestrial ones. Closer examination of the results showed that different measurements correlated best with body mass in different avian orders. This variation appeared to result from differences in habitat and functional morphology across the avian orders represented in the data set. The weights of some Chinese Mesozoic fossil birds were estimated using the equations generated for humeral length and tibiotarsal diameter, because ulnar diameter was frequently difficult to measure. Humeral length and tibiotarsal diameter yielded dramatically different mass estimates for some taxa, with estimates based on humerus length generally being lower. The result shows that these Early Cretaceous birds experienced a significant diversification in body weight during evolutionary process.
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Previously known only from the holotype specimen, Pengornis houi is the largest known Early Cretaceous enantiornithine bird and important for understanding body size and character evolution in Ornithothoraces. We report on a new subadult specimen from the Lower Cretaceous Jiufotang Formation referred to Pengornis sp. The specimen preserves a nearly complete sternum, reminiscent of that in Protopteryx and the basal ornithuromorph Archaeorhynchus, confirming the basal position of Pengornis and shedding new light on the evolution of the sternum in ornithothoracines. Anatomical information suggests that despite its size, Pengornis was arboreal, like other enantiornithines. Since Enantiornithes was first recognized over three decades ago (Walker, 1981), dozens of new enantiornithine taxa have been discovered from the Lower Cretaceous Jehol Group of northeastern China (Benton et al., 2008). This fossil-rich lacustrine unit consists of the lower Dabeigou Formation, exposed only in Hebei, the middle Yixian Formation, and the overlying Jiufotang Formation (Zhou et al., 2003). Pengornis is the largest known Early Cretaceous enantiornithine bird. The holotype and only previously known specimen of Pengornis houi (IVPP V 15336) preserves features previously considered unique to Ornithuromorpha such as the relatively more globose humeral head and the hooked acromion process on the scapula, providing evidence for a complex pattern of character evolution in ornithuromorph and enantiornithine birds (Zhou et al., 2008). Although the holotype specimen of P. houi preserves a great deal of anatomical information, particularly regarding the skull, preservation obscures many anatomical details of the disarticulated forelimb and hindlimb, the thoracic and pelvic girdles are incomplete, and no plumage is preserved. Recently, a nearly complete subadult specimen (IVPP V 18632) was recovered from the Jiufotang Formation of Lingyuan, western Liaoning, very near the locality that produced the holotype of P. houi. Morphological comparisons between this new specimen and the holotype of P. houi show that the new specimen can be referred to Pengornis, and may
The most basal avians Archaeopteryx and Jeholornis have elongate reptilian tails. However, all other birds (Pygostylia) have an abbreviated tail that ends in a fused element called the pygostyle. In extant birds, this is typically associated with a fleshy structure called the rectricial bulb that secures the tail feathers (rectrices) [1]. The bulbi rectricium muscle controls the spread of the rectrices during flight. This ability to manipulate tail shape greatly increases flight function [2, 3]. The Jehol avifauna preserves the earliest known pygostylians and a diversity of rectrices. However, no fossil directly elucidates this important skeletal transition. Differences in plumage and pygostyle morphology between clades of Early Cretaceous birds led to the hypothesis that rectricial bulbs co-evolved with the plough-shaped pygostyle of the Ornithuromorpha [4]. A newly discovered pengornithid, Chiappeavis magnapremaxillo gen. et sp. nov., preserves strong evidence that enantiornithines possessed aerodynamic rectricial fans. The consistent co-occurrence of short pygostyle morphology with clear aerodynamic tail fans in the Ornithuromorpha, the Sapeornithiformes, and now the Pengornithidae strongly supports inferences that these features co-evolved with the rectricial bulbs as a "rectricial complex." Most parsimoniously, rectricial bulbs are plesiomorphic to Pygostylia and were lost in confuciusornithiforms and some enantiornithines, although morphological differences suggest three independent origins.
Modern birds have extremely short tail skeletons relative to Archaeopteryx and nonavialian theropod dinosaurs. Long- and short-tailed birds also differ in the conformation of main tail feathers making up the flight surface: frond shaped in Archaeopteryx and fan shaped in extant fliers. Mechanisms of tail fanning were evaluated by electromyography in freely flying pigeons and turkeys and by electrical stimulation of caudal muscles in anesthetized birds. Results from these experiments reveal that the pygostyle, rectrices, rectricial bulbs, and bulbi rectricium musculature form a specialized fanning mechanism. Contrary to previous models, our data support the interpretation that the bulbi rectricium independently controls tail fanning; other muscles are neither capable of nor necessary for significant rectricial abduction. This bulb mechanism permits rapid changes in tail span, thereby allowing the exploitation of a wide range of lift forces. Isolation of the bulbs on the pygostyle effectively decouples tail fanning from fan movement, which is governed by the remaining caudal muscles. The tail of Archaeopteryx, however, differs from this arrangement in several important respects. Archaeopteryx probably had a limited range of lift forces and tight coupling between vertebral and rectricial movement. This would have made the tail of this primitive flier better suited to stabilization than maneuverability. The capacity to significantly alter lift and manipulate the flight surface without distortion may have been two factors favoring tail shortening and pygostyle development during avian evolution.
We report on a new enantiornithine Eopengornis martini gen. et sp. nov. from the lowest horizon of the Jehol Biota in Hebei, China; dated at 130.7 Mya, this is the second oldest avian bearing fossil deposit in the world, recording the First Appearance Datum of Enantiornithes. The new specimen, only the second enantiornithine and third bird reported from this horizon, preserves numerous synapomorphies with the largest Lower Cretaceous enantiornithine Pengornis houi from the Jiufotang Formation dated at 120 Mya. Together, they form a new avian lineage that lasted over 10 Myr, which is longer than any known clade of Lower Cretaceous enantiornithine. Eopengornis reveals new information about basal enantiornithine morphology such as the presence of a metatarsal V, helping to clarify the early evolution of these dominant Cretaceous avians. Furthermore, Eopengornis preserves a previously unrecognized tail morphology: a pair of elongate fully pennaceous rachis dominated feathers. This discovery confirms hypotheses proposing that the rachis dominated racket-plumes in basal birds represent modified pennaceous feathers. We suggest that the ornamental racket-plumes in enantiornithines and Confuciusornis evolved independently from the basal pygostylian condition, which we infer was a tail formed of normal flight feathers. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113, 805–819.