1-F-20161213003-1 Introduction
Anchiornis huxleyi is a feathered theropod which was discovered in
the Middle–Late Jurassic Tiaojishan Formation of Jianchang County,
Liaoning Province, China (Xu Xing et al., 2009). The discovery of
this species provides great evidence for the origins of birds,
flight capabilities and feathers.
In 2009, skeleton and feather features of Anchiornis were described
and the systematic position of Anchiornis was discussed, based on
two specimens, IVPP V14378 (Xu Xing et al., 2009) which is the
holotype, and LPM B00169 (Hu et al., 2009). However, the skeleton
and feather characters need to be revised because the specimens
were incomplete and included controversial characters. The
systematic position of Anchiornis also requires further discussion
because of different points for the classification (Hu et al.,
2009; Xu Xing et al., 2009). 2 Geological Setting
Anchiornis is a member of Yanliao Biota, which is a Middle–Late
Jurassic terrestrial biota distributed in western Liaoning,
northern Hebei and southeastern Inner Mongolia of China (Fig. 1).
Yanliao Biota vertebrates
include lissamphibians, transitional pterosaurs, feathered
theropods and primitive mammals, indicating a close relationship
with the Early Cretaceous Jehol Biota (Guo Xiangqi et al., 2012;
Liu et al., 2012; Xu Xing et al., 2016;
Morphological and Phylogenetic Study Based on New Materials of
Anchiornis huxleyi (Dinosauria, Theropoda)
from Jianchang, Western Liaoning, China
GUO Xiangqi1, 2, *, XU Li3 and JIA Songhai3
1 Yunnan Provincial Museum, Kunming 650000, Yunnan, China 2
Institute of Geology, Chinese Academy of Geological Sciences,
Beijing 100037, China 3 Henan Geological Museum, Zhengzhou 450000,
Henan, China Abstract: Anchiornis huxleyi, which is a member of the
Middle–Late Jurassic Yanliao Biota, is the smallest feathered
dinosaur ever known. It has been described as a critical link
between feathered dinosaurs and birds. Recent studies, including
those of Anchiornis, Xiaotingia, Eosinopteryx and Aurornis,
challenged Archaeopteryx as the most basal bird. The new Anchiornis
huxleyi specimens that are described in this paper show some minor
different characters compared to previously reported Anchiornis
specimens, which has revised the character list of Anchiornis and
indicates a different phylogenetic point from former opinions. Key
words: Anchiornis, feathered dinosaur, non-avian dinosaur,
Middle–Late Jurassic, Yanliao Biota
Vol. 92 No. 1 pp.1–15 ACTA GEOLOGICA SINICA (English Edition) Feb.
2018
* Corresponding author. E-mail:
[email protected]
© 2018 Geological Society of China
Fig. 1. Localities of fossil vertebrates of the Yanliao Biota in
western Liaoning and adjacent areas (modified from Guo Xiangqi et
al., 2012, fig. 1). , localities of Anchiornis huxleyi; , other
localities of fossil verte- brates of the Yanliao Biota.
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Gao Fuliang et al., 2017). 3 Systematic Palaeontology Class
Theropoda Marsh, 1881
Order Maniraptor Gauthier, 1986 Genus Anchiornis Xu Xing et al.,
2009
Anchiornis huxleyi Xu Xing et al., 2009 4 Materials
Two nearly complete Anchiornis huxleyi specimens, 41HIII 0404 and
41HIII 0415 (housed in Henan Geological Museum), which were
discovered in the Middle–Late Jurassic Tiaojishan Formation of
Jianchang, Liaoning Province, China, as other Anchiornis specimens.
41HIII 0404, which is 57.4 cm long, is a nearly complete skeleton
missing the posterior part of skull, parts of the cervical and
dorsal vertebrae, shoulder girdle and partial pelvic girdle (Fig.
2). Fortunately, elegant feathers distributed over the region of
forelimbs, hind limbs, dorsal and caudal vertebrae and pelvic
girdle were preserved in this specimen. 41HIII 0415, which is 37.5
cm long, is a nearly complete skeleton that is missing parts of the
skull, mandible, vertebrae, shoulder girdle and pelvic girdle
(Fig.
3). The closed neuro-central sutures suggest these both specimens
are probably adult individuals. 5 Description and Comparison 5.1
Skull and mandible
The skulls in new specimens are triangular in lateral view and have
a relatively blunt snout, like LPM-B00169 (Hu et al., 2009). The
posterior part of skull is unidentifiable in the new specimens
(Fig. 4a). The length of the skull in 41HIII 0415 is 51.4 mm (Table
1). The maxillary process of the premaxilla extends posteriorly so
that the premaxilla does not compose the posterior border of the
external naris, different from some dromaeosaurids like
Sinornithosaurus (Xu et al., 1999) (Fig. 4b). Anchiornis bears four
sub-equal premaxillary teeth which are closely packed and are not
strongly bent posteriorly. There is no serration on the anterior
and posterior carine, as seen in some dromaeosaurids and
troodontids like Sinornithosaurus (Xu et al., 1999; Liu Jinyuan et
al., 2004), Xixiasaurus (Lü et al., 2010) and Microraptor (Xu et
al., 2000, 2003). As seen in LPM-B00169, the antorbital fossa
contains promaxillary fenestra, maxillary fenestra and antorbital
fenestra, similar to most dromaeosaurids and troodontids like
Sinornithosaurus (Xu et al., 1999; Liu
Fig. 2. Specimen 41HIII 0404 of Anchiornis huxleyi. (a), photograph
of specimen 41HIII 0404; (b), line drawing of specimen 41HIII 0404.
Scale bars equal 5 cm. Abbreviations: boc, basioccipital; cav,
caudal vertebrae; cev, cervical vertebrae; ch, chevrons; cr,
cervical rib; dr, dorsal rib; dv, dorsal vertebrae; ept,
eptipterygoid; fu, furcula; g, gastralia; hy, hyoid; last, left
astragalus; lcal, left calcaneum; lco, left coracoids; lde, left
dentary; lf, left femur; lfi, left fibula; lh, left humerus; lis,
left ischium; ll, left lachrymal; lm, left maxilla; ln, left nasal;
lp, left pubis; lpm, left premaxilla; lr, left radius; lsa, left
surangular; lsc, left scapula; lspl, left splenial; lt, left tibia;
lul, left ulna; mc, metacarpal; mt, metatarsal; rae, radiale; ran,
right angular; rast, right astragalus; rcal, right calcaneum; rde,
right dentary; rf, right femur; rfi, right fibula; rh, right
humerus; ril, right ilium; ris, right ischium; rm, right maxilla;
rp, right pubis; rpm, right premaxilla; rr, right radius; rsa,
right surangular; rsc, right scapula; rt, right tibia; rul, right
ulna; sec, ‘semilunate’ carpal; v, vomer.
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Jinyuan et al., 2004), Sinornithoides (Currie and Dong, 2001) and
Aurornis (Pascal et al., 2013a) but different from Bambiraptor
(Burnham et al., 2000) and Shanag (Turner et al., 2007a) (Fig. 4c).
The number of maxillary teeth is close to ten, which is less than
some dromaeosaurids and troodontids such as Xixiasaurus (Lü et al.,
2010), Tsaagan mangas (Norell et al., 2006), Austroraptor (Novas et
al., 2008), Sinornithoides (Russell and Dong, 1993), Sinusonasus
(Xu Xing and Wang Xiaolin, 2004b), Jinfengopteryx (Ji Qiang et al.,
2005) and Daliansaurus (Shen Caizhi et al., 2017). These teeth are
not closely packed and not curved strongly, unlike some
dromaeosaurids and troodontids like Microraptor (Xu et al., 2000,
2003), Sinovenator (Xu et al., 2002), Bambiraptor (Burnham et al.,
2000), Sinornithosaurus millenii (Xu et al., 1999) and Shanag
(Turner et al., 2007a). Furthermore, Anchiornis teeth lack
serrations on both the anterior and posterior carinae and there is
no distinct constriction between the crown and the root, as in
Changyuraptor (Han et al., 2014). A small internarial bar appears
at the joint part of the nasal area. The nasal area gradually
widens posteriorly, reaching the anterior region of lachrymal, to
be more specific, above the external nares, promaxillary fenestra,
maxillary fenestra and antorbital fenestra. Like most
dromaeosaurids and troodontids, such as NGMC-91 (Ji et al., 2001),
T. mangas (Norell et al., 2006), Bambiraptor (Burnham et al.,
2000), Linheraptor (Xu et al., 2010), Sinornithosaurus (Xu et
al.,
1999; Liu Jinyuan et al., 2004), Sinornithoides (Currie and Dong,
2001), Sinusonasus (Xu Xing and Wang Xiaolin, 2004b) and
Xixiasaurus (Lü et al., 2010), the lachrymal is T-shaped in a
lateral view. The maxillary process of the lachrymal is relatively
short and directed anteroventrally, forming part of the dorsal
border of the antorbital fenestra so that the shape of antorbital
fenestra is a sub-triangle in a lateral view. The prefrontal
process is shorter than the maxillary process and is directed
posterodorsally, different from Aurornis (Pascal et al., 2013a) and
Eosinopteryx (Pascal et al., 2013b). The lachrymal extends
transversely in a dorsal view and bears a lateral ridge. The left
and right frontal is sutured at the middle line and the joint
slightly protrudes dorsally. In a dorsal view, the width of the
posterior part of the frontal is about twice that of the anterior
part. The lateral border of the frontal is thick and forms the
upper boundary of the orbit.
The length of the mandible is at 80% of the femur length. Both new
specimens have a relatively complete well preserved mandible (Fig.
4d). The dentary length is at 67% of the mandible length. On the
lateral surface of the dentary lies a horizontal groove that
includes a row of neurovascular fenestra, resembling that of
Sinovenator (Xu et al., 2002), Mei (Xu and Norell, 2004), Troodon
(Currie, 1987), Byronosaurus (Makovicky et al., 2003), Austroraptor
(Novas et al., 2008), Sinusonasus (Xu Xing and Wang Xiaolin,
2004b), Aurornis (Pascal et al., 2013a) and Daliansaurus (Shen
Caizhi et al., 2017). What is
Fig. 3. Specimen 41HIII 0415 of Anchiornis huxleyi. (a), photograph
of specimen 41HIII 0415; (b), line drawing of specimen 41HIII 0415.
Scale bars equal 5 cm. Abbreviations: cav, caudal vertebrae; cev,
cervical vertebrae; dr, dorsal rib; dv, dorsal vertebrae; fr,
frontal; fu, furcula; lco, left coracoids; lde, left dentary; lf,
left femur; lfi, left fibula; lh, left humerus; lil, left ilium;
lis, left ischium; ll, left lachrymal; lm, left maxilla; ln, left
nasal; lpm, left premaxilla; lr, left radius; lsc, left scapula;
lt, left tibia; lul, left ulna; mc, metacarpal; mt, metatarsal; pa,
parietal; rae, radiale; rco, right coracoids; rde, right dentary;
rf, right femur; rfi, right fibula; rh, right humerus; ris, right
ischium; rpm, right premaxilla; rr, right radius; rsc, right
scapula; rt, right tibia; rul, right ulna; sec, ‘semilunate’
carpal.
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special is that the space between the fenestra increases
posteriorly and the width of the groove does not change in 41HIII
0404, unlike that observed in another Anchiornis
specimen LPM-B00169 (Hu et al., 2009), Xiaotingia (Xu et al.,
2011a) and Eosinopteryx (Pascal et al., 2013b). A deep Meckelian
groove is located on the labial surface of
Fig. 4. Skull, mandible and hyoid arch of specimen 41HIII 0404,
premaxilla and maxilla of specimen 41HIII 0415. (a), photograph and
line drawing of skull of specimen 41HIII 0404 (scale bar equals 1
cm); (b), photograph and line drawing of premaxilla of specimen
41HIII 0415 (scale bar equals 1 mm); (c), photograph and line
drawing of maxilla of specimen 41HIII 0415 (scale bar equals 5 mm);
(d), photograph and line drawing of mandible and hyoid arch of
specimen 41HIII 0404 (scale bar equals 1 cm). Abbreviations: aof,
antorbital fenestra; bhy, basihyoid; chy, ceratohy- oid; emdf,
external mandibular foramen; fr, frontal; hym, hyomandible; idp,
interdental plate; jp, jugal process; lap, lachrymal process; lde,
left dentary; ll, left lachrymal; lm, left maxilla; ln, left nasal;
lpm, left premaxilla; lspl, left splenial; mg, Meckelian groove;
mp, maxillary process; mxf, maxillary fenestra; np, nasal process;
nvf, neurovascular foramina; pa, parietal; prmf, promaxillary
fenestra; ran, right angular; rde, right dentary; rpm, right
premaxilla; rsa, right surangular; saf, surangular
foramen.
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the dentary, as in Shanag (Turner et al., 2007a). The posterodorsal
process does not obviously protrude and the posteroventral process
does not reach the external mandibular foramen. Like the maxillary
teeth, the dentary teeth are not closely packed, not strongly
curved posteriorly, lack serrations on the anterior and the
posterior carinae and do not have a distinct constriction between
the crown and the root. Furthermore, a distinct interdental plate
can be seen on the labial surface. The dentary has fourteen teeth,
similar to that of Sinornithosaurus haoiana (Liu Jinyuan et al.,
2004), Bambiraptor feinbergi (Burnhamet al., 2000), Shanag
(Turner et al., 2007a), Saurornitholestes langstoni (Sue, 1978),
Velociraptor mongoliensis (Barsbold and Osmólska, 1999) and
Changyuraptor (Han et al., 2014), more than Xiaotingia (Xu et al.,
2011a) which has fewer than 10 and fewer than Austroraptor (Novas
et al., 2008) which present 25 and 18 in Jinfengopteryx (Ji Qiang
et al., 2005). Most of the splenial covers the posterior part of
the Meckelian groove in a labial view. The blunt process is
directed posterodorsally and is in the posterior part of the upper
margin. The angular length is at 47% of that of the mandible. A
small, sub-round surangular foramen is located near the posterior
end of the surangular, unlike that in Xiaotingia (Xu et al.,
2011a), Anchiornis IVPP V14378 (Xu Xing et al., 2009) and V.
mongoliensis (Barsbold and Osmólska, 1999). There is a sub-oval
external mandibular foramen at the posterior part of the joint of
the angular and surangular. The basihyoid is a parallelogram in a
lateral view and is located in the anterior part of the hyoid arch.
A pair of slender bowed bones to the left and right sides of the
basihyoid are ceratohyoids. A small round bone located at the end
of the ceratohyoid is probably a hyomandible. 5.2 Vertebral
column
Most of centra and ribs are preserved in 41HIII 0404, the anterior
cervical and dorsal vertebrae are missing and sacral vertebrae are
unrecognizable due to poor preservation. Except for the atlas, the
other nine cervical vertebrae can be clearly distinguished in
41HIII 0415, but the rest of the axial skeleton is incomplete. The
centrum length in a cervical series decreases slightly posteriorly.
The prezygapophysis is relatively robust. The diapophyses in the
cervical vertebra are developed and semi-circular in a lateral
view. The length of rhe cervical rib is slightly longer than the
corresponding centrum, different from Aurornis (Pascal et al.,
2013a). The shaft of the cervical rib is nearly parallel to that of
the centrum. The height of the neural arch is about twice that of
the centrum. The neural spine points posterodorsally, but it is not
distally expanded. Diapophyses are obvious but parapophyses are
not. The centrum length is twice the height and shortens
posteriorly. No distinct pneumaticfossa can be observed. The dorsal
ribs contain a relatively slender capitulum and short tuberculum.
The fourth ribs are the longest at 59% of the femur, while the
eighth dorsal ribs are the shortest, at 30% of the femur. There is
no uncinate process on the ribs, different from that of Microraptor
zhaoianus (Xu et al., 2000) and S. haoiana (Liu Jinyuan et al.,
2004). The gastralia are preserved in pairs. The length of the
longest gastralia is at 36% of the femur and the shortest is at
11%. The caudal count is about 28 based on the complete
preservation of 41HIII 0404 (Fig. 5a), like Tianyuraptor
Table 1 Selected measurements (in mm) of 41HIII 0404 and 41HIII
0415 Skull length 41HIII 0404 41HIII 0415 – 51.4 Mandible length
52.7 – Caudal series length 290.6 – Scapula length – – 25.7 (L) –
Coracoid length – – 5 (L) – Furcula width 25.6 17.1 Furcula length
(each branch) 17.3 11.2 Humerus length 63.2 (L) – 43.8 (L) 42.8 (R)
Humerus deltopectoral crest length 15.9 (L) – 11.9 (L) – Ulna
length 52.9 (L) 52.9 (R) 37.3 (L) 34.6 (R) Radius length 51 (L) –
36.9 (L) 34.6 (R) ‘Semilunate’ carpal length 2.7 (L) – 1.7 (L) –
Metacarpal I length 11.2 (L) – 8.3 (L) 7.9 (R) Metacarpal II length
30.9 (L) – – 21.5 (R) Metacarpal III length 28.7 (L) – – – Manual
phalanx I-1 24.4 (L) 24.3 (R) 21.6 (L) 18 (R) Manual phalanx I-2
15.9 (L) – 8.2 (L) 8.6 (R) Manual phalanx II-1 19 (L) – – 12.5 (R)
Manual phalanx II-2 24.6 (L) – 18.6 (L) 19.3 (R) Manual phalanx
II-3 16.4 (L) 15.7 (R) 9.5 (L) 9.6 (R) Manual phalanx III-1 7.6 (L)
7.7 (R) – – Manual phalanx III-2 6.8 (L) 7.4 (R) – 6.4 (R) Manual
phalanx III-3 12.8 (L) 13 (R) – 10.4 (R) Manual phalanx III-4 13.8
(L) – – 7.7 (R) Ilium length – 36.3 (R) – – Pubis length – 53.7 (R)
– – Ischium length – 20.8 (R) 13.6 (L) – Femur length 65.6 (L) 66.8
(R) 46.8 (L) – Tibia length 92.5 (L) – – – Tibiotarsus length – 96
(R) 71.5 (L) 71.2 (R) Fibula length 90.6 (L) – – – Astragalus
length 2.1 (L) – – – Metatarsal I length 8.7 (L) – 4.8 (L) 3.9 (R)
Metatarsal II length 49.2 (L) 48.3 (R) 32.9 (L) 36.2 (R) Metatarsal
III length 52.8 (L) 49.5 (R) 35.7 (L) 37.2 (R) Metatarsal IV length
52.2 (L) 50.1 (R) 32.8 (L) 35.9 (R) Metatarsal V length 13.1 (L) –
– – Pedal phalanx I-1 length 6.6 (L) – 5.5 (L) 5.7 (R) Pedal
phalanx I-2 length 6.2 (L) – 2.7 (L) 3.6 (R) Pedal phalanx II-1
length 11.2 (L) – 7.7 (L) 8.6 (R) Pedal phalanx II-2 length 11.3
(L) – 7.8 (L) 7.8 (R) Pedal phalanx II-3 length – – 5.8 (L) – Pedal
phalanx III-1 length 13.4 (L) – 9.1 (L) – Pedal phalanx III-2
length 10.1 (L) 10.8 (R) 7.6 (L) 7.6 (R) Pedal phalanx III-3 length
– 9.4 (R) 7.2 (L) 6.9 (R) Pedal phalanx III-4 length – 13 (R) 6.4
(L) 5.7 (R) Pedal phalanx IV-1 length 9.8 (L) 9.8 (R) 5.8 (L) 7.5
(R) Pedal phalanx IV-2 length – 5.6 (R) 4.4 (L) 5.5 (R) Pedal
phalanx IV-3 length – 13.2* (R) 3.5 (L) 4.9 (R) Pedal phalanx IV-4
length – – 2.1 (L) 5.4 (R) Pedal phalanx IV-5 length – 12.1 (R) 4.1
(L) – Notes: *, the estimated complete length of a partial element;
abbreviations: L, left; R, right.
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ostromi (Zheng et al., 2009), which is more than 24 or 25 in
Microraptor (Xu et al., 2000, 2003), 23 in Jinfengopteryx elegans
(Ji Qiang et al., 2005) and 22 in Changyuraptor (Han et al., 2014).
The total length of the tail is about four times that of the trunk
and about 4.4 times that of femur, as seen in Tianyuraptor (Zheng
et al., 2009), which is comparatively shorter than Epidendrosaurus
(Zhang et al., 2002) but obviously longer than Mei (Xu and Norell,
2004) and Eosinopteryx (Pascal et al., 2013b). The eight anterior
caudals are elongated posteriorly and the 10 posterior ones are
shortened posteriorly. The transitional point is probably located
at the sixth to eighth vertebrae (Table 2). Transverse processes
can be seen in the anterior caudal vertebrae, as in the holotype
(Xu Xing et al., 2009). But notably, the transverse process of the
first vertebra is directed posteriorly where the others are
directed laterally. The
prezygapophysis of the vertebrae get longer posteriorly, indicated
by the length of the anterior prezygapophysis that is about one
fourth of the corresponding centrum and the posterior
prezygapophysis that is about half of the corresponding centrum.
The postzygapophysis length is slightly shorter than the
corresponding prezygapophysis, which is about one third that of the
corresponding centrum at the end of the tail. These prezygapophysis
and
Fig. 5. Caudal vertebrae, chevronsin, ‘Semilunate’ carpal, manus
and pelvic girdle of specimen 41HIII 0404. (a), photograph and line
drawing of caudal vertebrae and chevrons (scale bar equals 1 cm);
(b), photograph and line drawing of ‘Semilunate’ carpal (scale bar
equals 5 mm); (c), photograph and line drawing of manus (scale bar
equals 2 cm); (d), photograph and line drawing of pelvic girdle
(scale bar equals 1 cm). Abbreviations: bvf, brevis fossa; cup,
cuppedicus fossa; isp, ischial peduncle; lis, left ischium; lp,
left pubis; mc, metacarpal; obp, obturator process; puf, pubic
foot; pup, pubic peduncle; rae, radiale; ril, right ilium; ris,
right ischium; rp, right pubis; sac, supracetabular crest; sec,
‘semilunate’ carpal.
Table 2 Measurements (in mm) of the centrum length of the caudal
vertebrae of 41HIII 0404
cv length cv length cv length cv length 1 6.1 8 11.3 15 11.6 22 9.2
2 6.5 9 11.4 16 11.0 23 8.2 3 7.5 10 11.4 17 – 24 7.6 4 – 11 11.0
18 11.3 25 6.9 5 – 12 – 19 11.0 26 – 6 9.7 13 – 20 10.3 27 – 7 10.8
14 – 21 9.9 28 –
Note: Abbreviation: cv, caudal vertebrae.
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postzygapophysis characters are very different from dromaeosaurids,
like Bambiraptor (Burnham et al., 2000), Microraptor (Xu et al.,
2000, 2003), S. haoiana (Liu Jinyuan et al., 2004), Graciliraptor
(Xu Xing and Wang Xiaolin, 2004a), Linheraptor (Xu et al., 2010)
and Buitreraptor (Makovicky et al., 2005). A distinct groove
appears on the lateral surface of the middle and posterior
vertebrae, consistent with LPM-B00169 (Hu et al., 2009) and
Eosinopteryx (Pascal et al., 2013b). The length of the middle
caudal vertebrae is about twice that of the caudal vertebrae at the
end, similar to Tianyuraptor (Zheng et al., 2009), at 2.1 times
longer than the anterior vertebrae, as in Sinusonasus (Xu Xing and
Wang Xiaolin, 2004b) and Xiaotingia (Xu et al., 2011a), but greater
than Linheraptor (Xu et al., 2010) and the holotype specimen of
Anchiornis (Xu Xing et al., 2009). Chevrons shafts are parallel to
the centrum. Chevrons are only posteriorly extended and anteriorly
bifurcated, which is similar to that of the holotype (Xu Xing et
al., 2009) but different from Graciliraptor (Xu Xing and Wang
Xiaolin, 2004a), Buitreraptor (Makovicky et al., 2005),
Jinfengopteryx (Ji Qiang et al., 2005) and Sinusonasus (Xu Xing and
Wang Xiaolin, 2004b). Each chevron tapers distally. The length of
anterior chevrons is about half that of the relative centrum and
shortens posteriorly. 5.3 Forelimb and pectoral girdle
The total length of the forelimb (humerus + ulna + carpal +
metacarpal II + digit II) is at 78% of the hind limb, like
Sinornithosaurus (Xu et al., 1999; Liu Jinyuan et al., 2004),
greater than the 53% in the Tianyuraptor (Zhenget al., 2009), but
much shorter than the 96% in the Changyuraptor (Han et al., 2014).
The scapula length is at 59% of the humerus, resembling the
holotype, slightly less than the 63% in S. millenii (Xu et al.,
1999) and 65% in S. haoiana (Liu Jinyuan et al., 2004) and
considerably less than the 77% in the Buitreraptor (Makovicky et
al., 2005) and 88% in the Tianyuraptor (Zheng et al., 2009). The
scapula to ulna length ratio is 70%, which is less than the 77% of
S. millenii (Xu et al., 1999) and 81% of S. haoiana (Liu Jinyuan et
al., 2004). The length of scapula is at 55% of the femur, which is
less than the 70% in Linhevenator (Xu et al., 2011b). The acromial
process is not obvious, differing from the distinct acromial
process types seen in Unenlagia comahuensis (Novas and Puerta,
1997), Rahona (Forster et al., 1998), Buitreraptor (Makovicky et
al., 2005), Jinfengopteryx (Ji Qiang et al., 2005) and Xiaotingia
(Xu et al., 2011a). The scapula does not expanded distally,
different from Jinfengopteryx (Ji Qiang et al., 2005), Linhevenator
(Xu et al., 2011b) and Epidendrosaurus (Zhang et al., 2002). The
glenoid cavity is located laterally, as seen in U. comahuensis
(Novas and
Puerta, 1997), Microraptor (Xu et al., 2000, 2003), Sinovenator (Xu
et al., 2002) and Mei (Xu and Norell, 2004). The coracoid tubercle
appears on the lateral surface of the coracoid which bears a
distinct sub-glenoid fossa, like Eosinopteryx (Pascal et al.,
2013b). The length of each furcula branch is at 26% of the femur,
which is relatively shorter than that of the holotype (Xu Xing et
al., 2009). There is no hypocleidium in the furcular. The length of
the humerus is at 95% of the femur, like Epidexipteryx (Zhang et
al., 2008), but is longer than many deinonychosaurians, like U.
comahuensis (Novas and Puerta, 1997), Austroraptor (Novas et al.,
2008), Linheraptor (Xu et al., 2010), Linhevenator (Xu et al.,
2011b), Epidendrosaurus (Zhang et al., 2002), Aurornis (Pascal et
al., 2013a) and Daliansaurus (Shen Caizhi et al., 2017) (Table 3).
The deltopectoral crest is not obviously protruding, being one
fourth the length of the humerus, as in other Anchiornis specimens
(Hu et al., 2009; Xu Xing et al., 2009), relatively shorter than
those in Unenlagia paynemili (Calvo et al., 2004), Luanchuanraptor
(Lü Junchang et al., 2007) and Linhevenator (Xu et al., 2011b). The
length of the ulna is at 83.7% of the humerus, similar to the
holotype (Xu Xing et al., 2009), Changyuraptor (Han et al., 2014)
and Epidendrosaurus (Zhang et al., 2002), but different from the
much longer ulna in Microraptor (Xu et al., 2000, 2003),
Jinfengopteryx (Ji Qiang et al., 2005), Xixiasaurus (Lü et al.,
2010), Rahona (Forster et al., 1998), Graciliraptor (Xu Xing and
Wang Xiaolin, 2004a) and NGMC91 (Ji Qiang et al., 2001). The ulna
is straight and the radius is relatively curved, like Eosinopteryx
(Pascal et al., 2013b). The ulna is only slightly thicker than the
radius. The olecranon process is not obvious. The ‘semilunate’
carpal in the new specimens is semi-circular, covering the proximal
surface of metacarpal I and half of metacarpal II. This is
inconsistent with the holotype, whose ‘semilunate’ carpal lies on
the surface of metacarpal II and metacarpal III and fuses with
these metacarpals, as is also seen in M. zhaoianus (Xu et al.,
2000), S. haoiana (Liu Jinyuan et al., 2004), Jinfengopteryx (Ji
Qiang et al., 2005) and Tianyuraptor (Zheng et al., 2009) in which
a larger part of the ‘semilunate’ carpal covers metacarpal II (Fig.
5b). The length of the manus is at 137% of the femur, including
metacarpal II, the longest metacarpal, which is at 49% of the femur
length (Fig. 5c). Metacarpal III is a little shorter, at 93% of
metacarpal II. Metacarpal I is at 36% of metacarpal II, which is
very similar to IGM100/44 (Barsbold et al., 1987) and Eosinopteryx
(Pascal et al., 2013b), slightly shorter than Jinfengopteryx (Ji
Qiang et al., 2005) but longer than S. haoiana (Liu Jinyuan et al.,
2004), Changyuraptor (Han et al., 2014) and
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Graciliraptor (Xu Xing and Wang Xiaolin, 2004a). Metacarpal II is a
little wider than metacarpal I and III. The ligament fossa in the
phalanges are deep, differing from Xiaotingia (Xu et al., 2011a)
whose ligament fossa are not obvious. The phalanges in digit II are
wider than those in other phalanges. Metacarpal II is longer than
phalanx I-1 but is shorter than metacarpal I plus phalanx I- 1.
Phalanx II-2 is the longest phalanx at 1.3 times that of II -1.
Phalanx II-3 is distinctly shorter than phalanx II-1, different
from NGMC91 (Ji et al., 2001) whose phalanx II -3 and II-1 are
almost the same length. Phalanx III-1 and III-2 are the shortest
phalanges. Phalanx III-1 is at 40% of phalanx II-1 and a little
longer than III-2, unlike that in Sinornithosaurus (Xu et al.,
1999; Liu Jinyuan et al., 2004), Microraptor gui (Xu et al., 2003),
Graciliraptor (Xu Xing and Wang Xiaolin, 2004a), Tianyuraptor
(Zheng et al., 2009) and Xiaotingia (Xu et al., 2011a), whose
phalanx III-1 is obviously longer than phalanx III- 2. The first
ungual is the largest in 41HIII 0404 and bear the largest
curvature, but ungual sizes in 41HIII 0415 look the same. 5.4 Hind
limb and pelvic girdle
The total length of the hind limb (femur + tibiotarsus + metatarsal
III + digit III) is at 126% of the forelimb. The short ilium is at
55% of the femur, shorter than the 60% in Sinovenator (Xu et al.,
2002) and 75% in Tianyuraptor (Zheng et al., 2009). The anterior
border of the
preacetabular is flat and slightly ventrally directed, different
from Epidexipteryx (Zhang et al., 2008), Epidendrosaurus (Zhang et
al., 2002), Xiaotingia (Xu et al., 2011a) and Tianyuraptor (Zheng
et al., 2009), which bear a projecting anterior border (Fig. 5d).
The cuppedicus fossa is obvious in the ilium, like U. comahuensis
(Novas and Puerta, 1997) and Luanchuanraptor (Lü Junchang et al.,
2007), and different from Mahakala (Turner et al., 2007b) and
Hesperonychus (Longrich and Currie, 2009), which do not have an
obvious cuppedicus fossa. Postacetabular tapers posteriorly, like
in most of the deinonychosaurians. The pubic peduncle is located
anteroventrally and the ischial peduncle is located
posteroventrally. The width of the pubic peduncle is longer than
the acetabulum and ischial peduncle. The supracetabular crest is
obvious. The pubis is nearly perpendicular to the ilium, whose
shaft is at 81% the length of the femur. The middle part of pubis
is robust and widens medially, being possibly a pubic apron. The
distal joint is flat and is directed posteriorly, forming the pubis
foot, like Rahona (Forster et al., 1998), Bambiraptor (Burnham et
al., 2000) and Tianyuraptor (Zheng et al., 2009), but is different
from the undeveloped type like that in Linheraptor (Xu et al.,
2010), Luanchuanraptor (Lü Junchang et al., 2007), Sinornithoides
(Russell and Dong, 1993) and Epidexipteryx (Zhang et al., 2008).
The pubis foot is at 12% the length of the pubis. The ischium is
relatively flat, the shaft is directed posteroventrally, and
it
Table 3 Selected ratios of 41HIII 0404, 41HIII 0415, IVPP V14378,
LPM-B00169 of Anchiornis and other relative Paraves
Anchiornis 41HIII 0404
Anchiornis 41HIII 0415
Aurornis YFGP-T5198
Eosinopteryx YFGP-T5197
Forelimb length/Hindlimb length 0.81 0.78 0.78* 0.82 – 0.81 0.73
Scapula length/Humerus length – 0.59 0.65* 0.66 0.77 0.63 0.63
Humerus length/Femur length 0.95 0.94 0.96* 1.04 0.85* 0.88 0.78
Ulna length/Femur length 0.8 0.77 0.86* 0.83 – 0.86 0.87
Humerus+Ulna length/Femur length 1.75 1.71 1.82* 1.87 – 1.74 1.65
Radius length/Femur length 0.77 0.79 – 0.82 0.75* – – Manus
length/Femur length 1.37 1.34 1.38* 1.56 0.93* 1.09 1.17 Metacarpal
I length/Metacarpal II length 0.36 0.38 – 0.37 0.42 0.35 –
Metacarpal I+Manual phalanx I-1 length/Metacarpal II length 1.15
1.3 – 1.14 1.29 1.15 – Metacarpal III length/Metacarpal II length
0.93 – – 0.9 1 1.01 – Manual phalanx II-2 length/Manual phalanx
II-1 length 1.29 1.52 – 1.29 1.67 – – Manual phalanx III-1
length/Manual phalanx II-1 length 0.41 – – 0.34 0.53 – – Manual
phalanx III-2 length/Manual phalanx III-1 length 0.92 – – 1.13 0.5
– – Manual phalanx III-3 length/Manual phalanx III-1 length 1.68 –
– 1.97 1.88 – – Ilium length/Femur length 0.55 – 0.61* 0.54 0.62*
0.53 0.52 Pubis length/Femur length 0.81 – – 0.93 – 0.83 0.72
Ischium length/Femur length 0.31 0.29 – 0.34 0.33* – 0.28
Tibiotarsus length/Femur length 1.45 1.53 1.57* 1.61 – 1.37 1.43
Tibia length/Femur length 1.4 – – – – – – Metatarsal III
length/Femur length 0.77 0.78 – 0.83 – 0.67 0.73 Metatarsal I
length/Metatarsal III length 0.17 0.12 – 0.2 – – – Metatarsal V
length/Metatarsal III length 0.26 – – 0.35 – – – Pedal phalanx II-2
length/Pedal phalanx II-1 length 1.01 0.96 – 1.06 0.75 – – Pedal
phalanx III-2 length/Pedal phalanx III-1 length 0.78 0.84 – 0.86
0.76 0.54 0.81 Pedal phalanx III-3 length/Pedal phalanx III-1
length 0.7 0.77 – 0.81 – 0.5 0.74 Pedal phalanx IV-1 length/Pedal
phalanx II-1 length 0.88 0.82 – 0.94 – – – Notes: *, the estimated
ratio by the estimated length; abbreviations: IVPP, Institute of
Vertebrate Paleontology and Paleoanthropology; LPM, Liaoning
Paleontological Museum; STM Shandong Tianyu Museum of Nature; YFGP,
Yizhou Fossil & Geology Park.
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is at 39% the length of the pubis, unlike Bambiraptor (Burnham et
al., 2000), Sinusonasus (Xu Xing and Wang Xiaolin, 2004b) and
Epidexipteryx (Zhang et al., 2008), whose ischium is longer than
half of the pubis. The pubic peduncle is nearly perpendicular to
the iliac peduncle. The anterior border of the ischium is flat but
the posterior border is straight and thick. A distinct obturator
process appears at the distal 1/3 part of the posterior border in
41HIII 0404 but at the middle of the posterior border in 41HIII
0415. No proximodorsal process were observed, unlike U. comahuensis
(Novas and Puerta, 1997), Rahona (Forster et al., 1998), S.
millenii (Xu et al., 1999), Bambiraptor (Burnham et al., 2000),
Buitreraptor (Makovicky et al., 2005), M. gui (Xu et al., 2003),
Sinovenator (Xu et al., 2002) and Mei (Xu and Norell, 2004). The
femurs are slightly anteriorly bent and the distal part is more
robust, the same as the holotype (Xu Xing et al., 2009). An obvious
femoral head is directed dorsomedially. The femoral neck and a
shallow trochanteric fossa can be seen in 41HIII 0404. A small
fourth trochanter appears at the middle of the femur shaft,
different from U. comahuensis (Novasand Puerta, 1997), Bambiraptor
(Burnham et al., 2000) and Buitreraptor (Makovicky et al., 2005),
which do not have a fourth trochanter. The length of the
tibiotarsus is at 149% of the femur, close to the 150% in the
holotype (Xu Xing et al., 2009) but longer than U. comahuensis
(Novas and Puerta, 1997), M. zhaoianus (Xu et al., 2000), Rahona
(Forster et al., 1998), Tianyuraptor (Zheng et al., 2009),
Linheraptor (Xu et al., 2010), Sinusonasus (Xu Xing and Wang
Xiaolin, 2004b), Epidexipteryx (Zhang et al., 2008) and
Eosinopteryx (Pascal et al., 2013b). The tibia is straight and the
middle part is slightly narrower than both ends. The fibula is a
little shorter than the tibia. The width of the proximal end of the
fibula is slightly less than that of the tibia. The middle part of
the fibula is extremely slender, about 1/6 the size of the middle
of the tibia, like Rahona (Forster et al., 1998) and S. millenii
(Xu et al., 1999). The body of the astragalus is sub-rounded in a
lateral view. Tha ascending process, which is at 73% the length of
the astragalus, is straight and tapers proximally, different from
Utahraptor (Kirkland et al., 1993) whose ascending process forms a
sub-triangle surface, and in Talos (Zanno et al., 2011) whose
ascending process covers the surface of the tibia. Metatarsal III
is the longest metatarsal at 77% the length of the femur and is an
arctometatarsus, like Graciliraptor (Xu Xing and Wang Xiaolin,
2004a), Saurornithoides junior (Barsbold, 1974), Tochisaurus
(Kurzanov and Osmólska, 1991), Mei (Xu and Norell, 2004), NGMC91
(Ji et al., 2001), Neuquenraptor (Novas and Pol, 2005), M.
zhaoianus (Xu et al., 2000), Linhevenator (Xu et al., 2011b),
Sinusonasus (Xu Xing
and Wang Xiaolin, 2004b) and the holotype (Xu Xing et al., 2009).
Metatarsal I is the shortest metatarsal at 16% the length of
metatarsal III. Metatarsal I is located at the distal 1/4 part of
metatarsal II, like M. zhaoianus (Xu et al., 2000), NGMC91 (Ji et
al., 2001) and Epidendrosaurus (Zhang et al., 2002), but differing
from the holotype (Xu Xing et al., 2009) and Linhevenator (Xu et
al., 2011b) whose metatarsal I is located at the middle of
metatarsal II. The length of metatarsal V is at 25% of metatarsal
III, much shorter than Changyuraptor (Han et al., 2014). The distal
end of metatarsal II bears a distinct ginglymoid. Metatarsal IV
bears an obvious ridge in anterior view, resembling Neuquenraptor
(Novas and Pol, 2005), M. zhaoianus (Xu et al., 2000), Mei (Xu and
Norell, 2004) and S. millenii (Xu et al., 1999). The width of
metatarsal IV is equal to the metatarsal II. The length of
metatarsal IV is slightly longer than metatarsal II. The first
digit is not reversed and is located at the posterior of other
digits. Phalanx I-1 is about the half length of phalanx III-1. The
length of phalanx II-1 is nearly equal to phalanx II-2 which has a
distinct proximal heel like Mahakala (Turner et al., 2007b),
Austroraptor (Novas et al., 2008), Byronosaurus (Norell et al.,
2000) and Linhevenator (Xu et al., 2011b). The third digit is the
longest and contains phalanx III-1, which is at 1.3 times length of
phalanx III-2, and phalanx III-3 is the shortest phalanx in digit
III. Phalanx IV-2, IV-3 and IV-4 are the shortest phalanges. The
height of the first ungual is about half that of the second one.
The second ungual is only slightly larger than the other unguals in
41HIII 0404, as in the holotype (Xu Xing et al., 2009), and is not
strongly curved, as seen in Hesperonychus (Longrich and Currie,
2009), IGM100/44 (Barsbold et al., 1987) and Borogovia (Osmólska,
1987). This differs from the strongly curved ungual in Rahona
(Forster et al., 1998), Pyroraptor (Allain and Taquet, 2000),
Microraptor (Xu et al., 2000, 2003), S. haoiana (Liu Jinyuan et
al., 2004), Graciliraptor (Xu Xing and Wang Xiaolin, 2004a),
Neuquenraptor (Novas and Pol, 2005), Sinusonasus (Xu Xing and Wang
Xiaolin, 2004b), Mei (Xu and Norell, 2004), Anchiornis IVPP V14378
(Xu Xing et al., 2009), Linhevenator (Xu et al., 2011b) and
Pedopenna (Xu and Zhang, 2005). However, in 41HIII 0415, the third
ungual is the largest in terms of height and length. 5.5
Feathers
Distinct feather prints are preserved in 41HIII 0404 and cover the
back, tail, regions of the ulna, metacarpals, manual phalanges,
tibiofibula, metatarsals and pedal phalanges (Fig. 6). None of the
feathers have a rachis, except those at the posterior part of the
tail. This is different from Anchiornis LPM-B00169 (Hu et al.,
2009)
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which has a distinct distribution of contour feathers at the
forelimb and hind limb regions. These differences may not be
individual or be in development, so more Anchiornis specimens are
needed for further clarification. The feathers covering the back
are obviously unusual. They are fibrous plumulaceous feathers,
averaging 41mm in length and the longest feather which is at 1.6
times the length of forelimb feathers in this specimen. These
feathers may not
be forelimb feathers based on the preservation location and length.
No such feathers are seen in other feathered dinosaurs and their
function remains unknown.
The tail feathers are very different between the anterior and
posterior parts. The anterior feathers (at the point of vertebrae
1–10) are fibrous plumulaceous feathers that shorten distally, from
31.5 mm to 12.7 mm. Furthermore, the arrangement of these feathers
is abnormal, they are
Fig. 6. Feathers of specimen 41HIII 0404. (a), feathers at the
back; (b), feathers at the forelimb; (c), feathers at the hind
limb; (d), feathers at the anterior tail; (e), feathers at the
posterior tail. Scale bars equal 5 cm.
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anteriorly radial but posteriorly parallel and perpendicular to the
tail. The posterior feathers (at the point of 14–27 vertebrae) are
asymmetric pennaceous feathers, perhaps rectrices, preserving an
unclear rachis but distinct vanes. There are about 20 pairs of
pennaceous feathers that are arranged posteriorly and point along
the posterior tail at an angle of 30 degrees. These feathers are
sub-oval and have a small distance from the tail, indicating a long
quill or a different pigment between the proximal and distal
feathers. The feathers distributed at the ulna are nearly
perpendicular to the ulna and average 25 mm in length and at 47%
the length of the ulna. The feathers distributed at the metacarpals
are average 20.5 mm in length and are at 66% the length of
metacarpal II. However, these feathers are at an angle of 45
degrees with the shaft of the metacarpals and point to the distal
part. Except for the unguals, the manual phalanges also have a
distribution of plumulaceous feathers that are average 4.8 mm in
length.
The feathers at the hind limb region are relatively dense, average
6.6 mm in length at the tibiotarsus region, 7.7 mm at the
metatarsus region, 1.5 mm at the pedal phalanges region and the
unguals have none. They are also plumulaceous feathers that are
distally pointed at an angle of 60 degrees to relative bones. 6
Discussion
These two specimens, 41HIII 0404 and 41HIII 0415, can be referred
to Anchiornis based on the following characters: their skulls are
triangular in a lateral view and have a relatively blunt snout; the
teeth are unserrated; the antorbital fossa contains the
promaxillary fenestra, maxillary fenestra and antorbital fenestra;
transverse processes can be seen in the anterior caudal vertebrae
and a distinct groove appears at the lateral surface of middle and
posterior caudal vertebrae; the chevrons are only posteriorly
extended and anteriorly bifurcated; the length of scapula is at 59%
of the humerus; the humerus has a relatively short deltopectoral
crest; the ulna is only slightly thicker than the radius; the
length of the ulna is at 83.7% of the humerus; the ischium is short
and at 30% of the femoral length; the femurs are slightly
anteriorly bent and the distal part is more robust; the length of
the tibiotarsus is at 149% of the femur; metatarsal III is the
longest metatarsal, it is at 77% the length of the femur and is an
arctometatarsus; the length of pedal phalanx II-2 is close to that
of pedal phalanx II-1.
By researching these two new Anchiornis specimens and comparing
them to IVPP V14378 and LPM-B00169, we have revised the characters
of Anchiornis as follows: the maxillary process of premaxilla and
maxillary process of the nasal form the posterior border of the
external nares;
the external nares expand posteriorly to the anterior border of the
antorbital fossa; the round maxilla fenestra is large and the
sub-oval promaxillary fenestra is relatively small; the lachrymal
is T-shaped in a lateral view, bearing a short prefrontal process
which forms a subtriangular antorbital fenestra with the maxilla
and nasal; they have a large lateral quadrate foramen; an array of
neurovascular foremen appear at the labial surface of the dentary
in a horizontal groove, and the interval between these foremen
widens posteriorly; distinct pneumathodium appear at the lateral
surface of cervical vertebrae; caudal vertebrae number about 28 and
anterior caudal vertebrae bearing transversal processes and
posterior caudal vertebrae bearing grooves are present at lateral
surfaces; the chevrons at the middle and posterior part of the tail
branch anteriorly, are directed posteriorly and are about half the
length of relative caudal vertebrae; the scapula does not have a
distinct acromial process, being flat and not extended distally; a
lateral tubercle appears at the coracoid; the length of the
deltopectoral crest is about 1/4 of the humerus; the ulna is only
slightly thicker than the radius; the ilium bears an obvious
supracetabular crest, cuppedicus fossa and brevis fossa, and the
pubic peduncle is wider than the ischial peduncle; the pubis points
anteroventrally and is distally posteriorly bent; the length of the
tibiotarsus is at 1.5 times that of the femur; astragalus whose
ascending process tapers at the end is not fused with tibia;
metatarsals are arctometatarsus, metatarsal I is located at the
distal 1/4 part of metatarsal II; the second ungual is only
slightly larger than other unguals.
However, 41HIII 0404 and 41HIII 0415 have some characters which
differ from previously reported Anchiorins specimens, indicating an
individual difference or different preservation situation. The
sub-round surangular foramen is quite small in the new materials.
Dentary teeth are not closely packed at the joint region. The
interclavicular angle of furcular is obviously different in these
specimens, at 77 degrees for 41HIII 0404 and 120 degrees for 41HIII
0415, which is close to IVPP V14378. Numerous small pits are
located on the ventral surface of the coracoid, which is described
as an Anchiornis characteristic, were not seen in the new
materials. The ‘semilunate’ carpal is located at the proximal end
of metacarpal I and II but not II and III in IVPP V14378. The
length of the ischium is at 30% of the femur, which is
comparatively longer than IVPP V14378 and LPM- B00169.
Four Paraves, Anchiornis, Xiaotingia, Aurornis and Eosinopteryx,
which are four small non-avian dinosaurs that have been found in a
similar location, have close relationship. Most of their characters
are quite similar,
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indicated by some bone length ratios (Table 3). Previous articles
allocated them into different clades, like Troodontidae, at the
base of Avialae, or forming a single group in Deinonychosauria,
because they share characters with the Dromaeosauridae,
Troodontidae and basal birds (Hu et al., 2009; Xu Xing et al.,
2009; Xu et al., 2011a; Pascal et al., 2013a; Pascal et al.,
2013b). Here we coded Anchiornis based on the character list
synthesised 41HIII 0404 and 41HIII 0415, into a recently published
phylogenetic analysis of basal Paraves, replacing the character
list of Anchiornis in that paper (Pascal et al., 2013a) (Appendix
1). The data matrix, using Dilophosaurus, Dubreuillosaurus,
Monolophosaurus and Sinraptor as outgroups, was analysed by TNT
(Goloboff et al., 2008). A total of 1500 characters and 100 taxa
were included in this research (Sinovenator was excluded because of
the wrong code list in that article), using the traditional
research of 1000 replicates. The 650 most parsimonious trees were
found to build a strict consensus tree (tree length = 4581,
consistency index=0.310 and retention index = 0.563) (Fig. 7). Our
results place Anchiornis, Xiaotingia, Aurornis, Archaeopteryx,
Eosinopteryx and part of Troodontidae at the base of Avialae. Other
Troodontidae were placed as a sister group with Avialae. That means
that the currently defined Troodontidae may not be a monophyletic
group and it has a closer relationship with Avialae than with
Dromaeosauridae. Yanliao Biota members, including
Anchiornis, Xiaotingia, Aurornis, Eosinopteryx and
Scansoriopterygidae being composed of Epidendrosaurus and
Epidexipteryx, have the closest relationship with Aves, indicating
that the Avialae had a rapid evolution during the Middle–Late
Jurassic period.
Noticeably, 275 characters of Anchiornis included in the 1500
characters were identified in the former character list (Pascal et
al., 2013a) and 399 characters are identified in this paper.
However, 39 character codes are different when comparing the two
character lists, which equates to 14% of the former character list
(Pascal et al., 2013a) (Appendix 1). Similarly, the ratios were
16%, 10%, 8% and 11% when compared with Archaeopteryx, Aurornis,
Eosinopteryx and Xiaotingia, respectively. These ratios show that
differences between Anchiornis individuals of are usually greater
than those between different species, a phenomenon which is not
inconsistent with natural laws. The incomplete data (963 of
Archaeopteryx, 289 of Aurornis, 265 of Eosinopteryx and 275 of
Xiaotingia) should be the most important reason for this
phenomenon. Species belonging to the Aurornis, Eosinopteryx and
Xiaotingia were built based on a unique specimen resulting in
insufficient data, and individual differences were difficult to
identify. That is why sometimes the relationships with
dromaeosaurids, troodontids, scansoriopterygids and other avians
are quite different when a new species is discovered. Another
reason to explain the phenomenon may be the questionable
Fig. 7. The strict consensus tree of the 650 most parsimonious
trees.
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character list. The feather characters should not be included in
the list because we could not identify feather gender differences.
Moreover, if a group of species have some apomorphic characters
that are listed in the character list but other species do not,
these characters may weaken the power of other common characters.
The weakened power will greatly influence the result of a
phylogenetic analysis when a great number of data are missing. As a
result, the results from a phylogenetic analysis based on an
incomplete character list are questionable.
Thousands of Anchiornis specimens have been discovered. We need to
synthesise the information from these specimens, identify the
differences between individuals and shape a relatively complete
character list so that conclusions are more reliable. 7
Conclusions
(1) The feathered dinosaur, Anchiornis huxleyi, provides
significant information on the evolution from dinosaurs to birds.
We revised species characters by collecting more data from two new
specimens, 41HIII 0404 and 41HIII 0415.
(2) We found some minor character differences between new materials
and former ones, caused by individual differences or a different
preservation situation. The different feather patterns from
previously studied materials showed that the diversity may not be
due to individual or developmental differences.
(3) The results from a phylogenetic analysis placed Anchiornis at
the base of Avialae and indicated that currently defined
Troodontidae may not be a monophyletic group. That means that the
relationship between Avialae, Troodontidae and Dromaeosauridae is
far more complex than previously imagined and that the Avialae had
a rapid evolution during the Middle–Late Jurassic period.
(4) Limited data from unique specimens and the questionable
character list weakens the reliability of phylogenetic analysis
results in dinosaur research. More specimens and more data may be
the only way to obtain more reliable results.
Acknowledgements
The authors thank Shu-an Ji and Ye Peng for commenting on the
manuscript and Chunjun Zeng and Guihai Cui for preparing the
specimens. The National Natural Science Foundation of China (grant
No. 41372026) and China Geological Survey (grant No. DD20160120)
supported this research.
Manuscript recived Dec. 13, 2016 accepted Jun. 12, 2017 edited by
Fei Hongcai
References Allain, R., and Taquet, P., 2000. A new genus of
Dromaeosauridae (Dinosauria, Theropoda) from the Upper Cretaceous
of France. Journal of Vertebrate Paleontology, 20 (2):
404–407.
Barsbold, R., 1974. Saurornithoididae, a new family of small
theropod dinosaurs from central Asia and North America.
Palaeontologia Polonica, 30: 1–22.
Barsbold, R., and Osmólska, H., 1999. The skull of Velociraptor
(Theropoda) from the Late Cretaceous of Mongolia. Acta
Palaeontologica Polonica, 44(2): 189–219.
Barsbold, R., Osmólska, H., and Kurzanov, M., 1987. On a new
troodontid (Dinosauria, Theropoda) from the Early Cretaceous of
Mongolia. Acta Palaeontologica Polonica, 32(1–2): 121– 132.
Burnham, D.A., Derstler, K.L., Currie, P.J., Bakker, R.T., Zhou
Zhonghe, and Ostrom, J.H., 2000. Remarkable new birdlike dinosaur
(Theropoda, Maniraptora) from the Upper Cretaceous of Montana. The
University of Kansas Paleontological Contributions, New Series 13:
1–14.
Calvo, J.O., Porfiri, J.D., and Kellner, A.W.A., 2004. On a new
maniraptoran dinosaur (Theropoda) from the Upper Cretaceous of
Neuquén, Patagonia, Argentina. Arquivos do Museu Nacional, Rio de
Janeiro, 62(4): 549–566.
Currie, P.J., 1987. Bird-like characteristics of the jaws and teeth
of troodontid theropods (Dinosauria, Saurischia). Journal of
Vertebrate Paleontology, 7(1): 72–81.
Currie, P.J., and Dong Zhiming, 2001. New information on Cretaceous
troodontids from the People’s Republic of China. Canadian Journal
of Earth Sciences, 38(12): 1753–1766.
Forster, C.A., Sampson, S.D., Chiappe, L.M., and Krause, D.W.,
1998. The theropod ancestry of birds, new evidence from the Late
Cretaceous of Madagascar. Science, 279: 1915–1919.
Gao Fuliang, Jiang Yang, Zhang Guoren, Pan Yuqi, Wu Zijie and Wang
Xuan, 2017. Location and new found of Yanliao Biota in western
Liaoning. Geological Review, 63(3): 770– 780 (in Chinese with
English abstract).
Goloboff, P.A., Farris, J.S., and Nixon, K.C., 2008. TNT, a free
program for phylogenetic analysis. Cladistics, 24: 774–786.
Guo Xiangqi, Han Jiangang and Ji Shu’an, 2012. Advances in the
study of vertebrate fossils of the Middle Jurassic Yanliao Biota in
western Liaoning Province and adjacent areas. Geological Bulletin
of China, 31(6): 735–742 (in Chinese with English abstract).
Han Gang, Chiappe, L.M., Ji Shu’an, Habib, M., Turner, A.H.,
Chinsamy, A., Liu Xueling and Han Lizhuo, 2014. A new raptorial
dinosaur with exceptionally long feathering provides insights into
dromaeosaurid flight performance. Nature Communications, 5, Article
number: 4382.
Hu Dongyu, Hou Lianhai, Zhang Lijun and Xu Xing, 2009. A
pre-Archaeopteryx troodontid theropod from China with long feathers
on the metatarsus. Nature, 461: 640–643.
Ji Qiang, Norell, M.A., Gao Keqin, Ji Shu’an and Ren Dong, 2001.
The distribution of integumentary structures in a feathered
dinosaur. Nature, 410: 1084–1088.
Ji Qiang, Ji Shu’an, Lü Junchang, You Hailu, Chen Wen, Liu
14 Vol. 92 No. 1 ACTA GEOLOGICA SINICA (English Edition)
http://www.geojournals.cn/dzxben/ch/index.aspx Feb. 2018
Yongqing and Liu Yanxue, 2005. First avialian bird from China.
Geological Bulletin of China, 24(3): 197–210.
Kirkland, J.I., Burge, D., and Gaston, R., 1993. A large
dromaeosaur (Theropoda) from the Lower Cretaceous of eastern Utah.
Hunteria, 2(10): 1–16.
Kurzanov, S.M., and Osmólska, H., 1991. Tochisaurus nemegtensis
gen. et sp. n., a new troodontid (Dinosauria, Theropoda) from
Mongolia. Acta Palaeontologica Polonica, 36(1): 69–76.
Liu Jinyuan, Ji Shu’an, Tang Feng and Gao Chunling, 2004. A new
species of dromaeosaurids from the Yixian Formation of western
Liaoning. Geological Bulletin of China, 23(8): 778– 783. (in
Chinese with English abstract)
Liu Yongqing, Kuang Hongwei, Jiang Xiaojun, Peng Nan, Xu Huan and
Sun Huiyi, 2012. Timing of the earliest known feathered dinosaurs
and transitional pterosaur older than Jehol Biota. Palaeogeography,
Palaeoclimatology, Palaeoecology, 323–325: 1–12.
Longrich, N.R., and Currie, P.J., 2009. A microraptorine
(Dinosauria–Dromaeosauridae) from the Late Cretaceous of North
America. PNAS, 106(13): 5002–5007.
Lü Junchang, Xu Li, Liu Yongqing, Zhang Xingliao, Jia Songhai and
Ji Qiang, 2010. A new troodontid theropod from the Late Cretaceous
of central China, and the radiation of Asian troodontids. Acta
Palaeontologica Polonica, 55(3): 381–388.
Lü Junchang, Xu Li, Zhang Xingliao, Ji Qiang, Jia Songhai, Hu
Weiyong, Zhang Jiming and Wu Yanhua, 2007. New dromaeosaurid
dinosaur from the Late Cretaceous Qiupa Formation of Luanchuan
area, western Henan, China. Geological Bulletin of China, 26(7):
777–786.
Makovicky, P.J., Apestegua, S. and Agnoln F.L., 2005. The earliest
dromaeosaurid theropod from South America. Nature, 437:
1007–1011.
Makovicky, P.J., Norell, M.A., Clark, J.M., and Rowe, T., 2003.
Osteology and relationships of Byronosaurus jaffei (Theropoda:
Troodontidae). American Museum Novitates, 3402: 1–32.
Norell, M.A., Makovicky, P.J., and Clark, J.M., 2000. A new
troodontid theropod from Ukhaa Tolgod, Mongolia. Journal of
Vertebrate Paleontology, 20(1): 7–11.
Norell, M.A., Clark, J.M., Turner, A.H., Makovicky, P.J., Barsbold,
R., and Rowe, T., 2006. A new dromaeosaurid theropod from Ukhaa
Tolgod (Ömnögov, Mongolia). American Museum Novitates, 3545:
1–51.
Novas, F.E., and Pol, D., 2005. New evidence on deinonychosaurian
dinosaurs from the Late Cretaceous of Patagonia. Nature, 433:
858–861.
Novas, F.E., and Puerta P.F., 1997. New evidence concerning avian
origins from the Late Cretaceous of Patagonia. Nature, 387:
390–392.
Novas, F.E., Pol, D., Canale, J.I., Porfiri, J.D., and Calvo, J.O.,
2009. A bizarre Cretaceous theropod dinosaur from Patagonia and the
evolution of Gondwanan dromaeosaurids. Proceedings of the Royal
Society B, 276: 1101–1107.
Osmólska, H., 1987. Borogovia gracilicrus gen. et sp. n., a new
troodontid dinosaur from the late Cretaceous of Mongolia. Acta
Palaeontologica Polonica, 32(1–2): 133–150.
Pascal, G., Andrea, C., Hu Dongyu, François, E., Wu Wenhao, and
Gareth, D., 2013. A Jurassic avialan dinosaur from China resolves
the early phylogenetic history of birds. Nature, 498:
359–362.
Pascal, G., Helena, D., Gareth, D., Hu Dongyu, François, E., and
Philippe, C., 2013. Reduced plumage and flight ability of a new
Jurassic paravian theropod from China. Nature Communications, 4,
Article number: 1394.
Russell, D.A., and Dong Zhiming, 1993. A nearly complete skeleton
of a new troodontid dinosaur from the Early Cretaceous of the Ordos
Basin, Inner Mongolia, People’s Republic of China. Canadian Journal
of Earth Sciences, 30: 2163–2173.
Shen Caizhi, Lü Junchang, Liu Sizhao, Kundrát, M., Brusatte, S.L.,
and Gao Hailong, 2017. A new troodontid dinosaur from the Lower
Cretaceous Yixian Formation of Liaoning Province, China. Acta
Geologica Sinica (English Edition), 91 (3): 763–780.
Sues, H., 1978. A new small theropod dinosaur from the Judith River
Formation (Campanian) of Alberta Canada. Zoological Journal of the
Linnean Society, 62: 381–400.
Turner, A.H., Hwang, S.H., and Norell, M.A., 2007a. A small derived
theropod from Öösh, Early Cretaceous, Baykhangor Mongolia. American
Museum Novitates, 3557: 1–27.
Turner, A.H., Pol, D., Clarke, J.A., Erickson, G.M., and Norell,
M.A., 2007b. A basal dromaeosaurid and size evolution preceding
avian flight. Science, 317: 1378–1381.
Xu Xing and Norell, M.A., 2004. A new troodontid dinosaur from
China with avian-like sleeping posture. Nature, 431: 838
–841.
Xu Xing and Wang Xiaolin, 2004a. A new dromaeosaur (Dinosauria:
Theropoda) from the Early Cretaceous Yixian Formation of western
Liaoning. Vertebrata Palasiatica, 42(2): 111–119.
Xu Xing and Wang Xiaolin, 2004b. A new troodontid (Theropoda:
Troodontidae) from the Lower Cretaceous Yixian Formation of western
Liaoning, China. Acta Geologica Sinica (English Edition), 78(1):
22–26.
Xu Xing and Zhang Fucheng, 2005. A new maniraptoran dinosaur from
China with long feathers on the metatarsus. Naturwissenschaften,
92: 173–177.
Xu Xing, Wang Xiaolin and Wu Xiaochun, 1999. A dromaeosaurid
dinosaur with a filamentous integument from the Yixian Formation of
China. Nature, 401: 262–266.
Xu Xing, Zhou Zhonghe and Wang Xiaolin, 2000. The smallest known
non-avian theropod dinosaur. Nature, 408: 705–708.
Xu Xing, You Hailu, Du Kai and Han Fenglu, 2011a. An
Archaeopteryx-like theropod from China and the origan of Avialae.
Nature, 475: 465–470.
Xu Xing, Norell, M.A., Wang Xiaolin, Makovicky, P.J., and Wu
Xiaochun, 2002. A basal troodontid from the Early Cretaceous of
China. Nature, 415: 780–784.
Xu Xing, Tan Qingwei, Sullivan, C., Han Fenglu and Xiao Dong,
2011b. A short-armed troodontid dinosaur from the Upper Cretaceous
of Inner Mongolia and its implications for troodontid evolution.
PLoS ONE, 6(9): e22916.
Xu Xing, Zhou Zhonghe, Sullivan, C., Wang Yuan and Ren Dong, 2016.
An updated review of the Middle–Late Jurassic Yanliao Biota:
Chronology, taphonomy, paleontology and paleoecology. Acta
Geologica Sinica (English Edition), 90(6): 2229–2243.
Xu Xing, Zhou Zhonghe, Wang Xiaolin, Kuang Xuewen, Zhang Fucheng
and Du Xiangke, 2003. Four-winged dinosaurs from China. Nature,
421: 335–340.
Xu Xing, Zhao Qi, Norell, M., Sullivan, C., Hone, D.,
Erickson,
ACTA GEOLOGICA SINICA (English Edition)
http://www.geojournals.cn/dzxben/ch/index.aspx Feb. 2018 Vol. 92
No. 1 15
G., Wang Xiaolin, Han Fenglu and Guo Yu, 2009. A new feathered
maniraptoran dinosaur fossil that fills a morphological gap in
avian origin. Chinese Science Bulletin, 54(3): 430–435.
Xu Xing, Choiniere, J., Pittman, M., Tan Qingwei, Xiao Dong, Li
Zhiquan, Tan Lin, Clark, J.M., Norell, M. A., Hone, D.W.E., and
Sullivan, C., 2010. A new dromaeosaurid (Dinosauria: Theropoda)
from the Upper Cretaceous Wulansuhai Formation of Inner Mongolia,
China. Zootaxa, 2403: 1–9.
Zanno, L.E., Varricchio, D.J., O’Conner, P.M., Titus, A.L., and
Knell, M.J., 2011. A new troodontid theropod, Talos sampsoni gen.
et sp. nov., from the Upper Cretaceous western interior basin of
North America. PLoS ONE, 6(9): 1–20.
Zhang Fucheng, Zhou Zhonghe and Xu Xing, 2002. A juvenile
coelurosaurian theropod from China indicates arboreal habits.
Naturwissenschaften, 89: 394–398.
Zhang Fucheng, Zhou Zhonghe, Xu Xing, Wang Xiaolin and Sullivan,
C., 2008. A bizarre Jurassic maniraptoran from China with elongate
ribbon-like feathers. Nature, 455: 1105– 1108.
Zheng Xiaoting, Xu Xing, You Hailu, Zhao Qi and Dong Zhiming, 2009.
A short-armed dromaeosaurid from the Jehol Group of China with
implications for early dromaeosaurid evolution. Proceedings of the
Royal Society B, 277: 211–217.
About the first author GUO Xiangqi, Male; born in 1987,
Heilongjiang, China;
graduated from Chinese Academy of Geological Sciences (M.Sc.) in
2012 and Nanjing University (B.Sc.) in 2007; assistant museologist
at Yunnan Provincial Museum; research interests is in vertebrate
palaeontology. Email:
[email protected].
Appendix 1 Data matrix of Anchiornis based on 41HIII 0404 and
41HIII 0415 1-10 10-20 20-30 30-40 40-50 50-60 60-70 70-80 80-90
90-100
1-100 0110---100 ----2---20 110--1-1-- --1011---0 -12--00---
0--100--02 1-0------- -00--0-001 -0-------- ---------- 100-200
---------- ---------- ---------- ---------- --------0- 10--000-20
2--0-01--0 01-----100 ----0--00- -1-100---- 200-300 -----1-00-
-----2---- 00-0-----0 -02------- -----0-0-- 20---1-101 ---2-10---
01--0-000- 2-0---0000 01-021-111 300-400 22-1-10101 0002-21---
10-10011-- 2-12------ ---------- -21--3--01 -01000---0 0-2-0--0-1
11100--0-1 20012-01-1 400-500 0-----0-2- 0-----10-- 2-----0---
-2----0-1- -------0-- ------1012 0------03- -----011-- 0-1-1-0011
00110-2-11 500-600 100-011--- 1010112-0- -------00- 00----0-0-
1--01-11-1 --1------- ---1--0--0 0--------0 ----1----- ------00--
600-700 ---0--000- -11--11-00 00--0--100 ---------- 0----01--1
--0-2--01- 10-0-0---- -----1--0- ---0--10-- 00-----0-- 700-800
--0------- ------1-00 --0--1---- --0------- ---------- ----------
--------0- ---1------ --11-1--1- -1--0110-0 800-900 --0--10---
-0--1---0- ----0--010 --------10 --------1- -----0-0-0 -------00-
-0-------- ----210--- -----1---1
900-1000 0--------0 ---------- ---00-0--- ---------- ---1-0-12-
------1--- -0-------- ---------- -------00- ---0--0--- 1000-1100
0-0---0--- ---------0 -0---1---- 1--------- ------0--- ----1----1
------0--0 ---0------ --1------- --100---01 1100-1200 -1--0---1-
---------- 0--------- 0--10----- --0---11-0 ---------- ----------
---------- ---------- --1------- 1200-1300 -----0---- ----------
---------- 0-------1- --1--1---- -0-------- ---------- ----------
1---0--0-- ---------- 1300-1400 ---------- ----0----- -------0--
---------- ---------0 -----0000- 0--10----- -0-------0 ---10-11--
-------0-- 1400-1500 --0------- ---------0 --0------- -1-----10-
--0-002-11 1--------- -----0---- ---------1 ----------
--------0-