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A new species of Microraptor from the Jehol Biota of northeastern China

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Herein we describe a new species of Microraptor from northeastern China that provides new information on the characteristics of the genus and anatomical details suggesting a gliding behaviour. Although specimens of Microraptor have been known for at least a decade, the completeness of the new fossil provides additional morphology that highlights the uniqueness of this taxon. The new specimen, Microraptor hanqingi, is the key to understanding the evolutionary significance of hindlimb wings. A four-winged structure present on an organism sharing an evolutionary lineage leading to modern birds implies that gliding was a stage in the development of avian flight. M. hanqingi represents the largest known microraptorian from China with a total length of approximately 1 m, and was closely-related to the venomous form, Sinornithosaurus.
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Palaeoworld
21
(2012)
81–91
A
new
species
of
Microraptor
from
the
Jehol
Biota
of
northeastern
China
En-Pu
Gonga,
Larry
D.
Martinb,c,
David
A.
Burnhamb,,
Amanda
R.
Falkd,
Lian-Hai
Houe,f
aDepartment
of
Geology,
Northeastern
University,
11
Lane
No.
3
Wenhua
Road,
Shenyang
110004,
China
bNatural
History
Museum
and
Biodiversity
Institute,
University
of
Kansas,
1345
Jayhawk
Boulevard,
Lawrence,
KS
66045-7593,
USA
cDepartment
of
Ecology
and
Systematics,
University
of
Kansas,
1345
Jayhawk
Boulevard,
Lawrence,
KS
66045-7593,
USA
dDepartment
of
Geology,
University
of
Kansas,
1475
Jayhawk
Boulevard,
Lawrence,
KS
66045-7594,
USA
eInstitute
of
Vertebrate
Paleontology
and
Paleoanthropology,
Chinese
Academy
of
Sciences,
No.
142
Xi-Zhi-Men-Wai
Street,
Beijing
100044,
China
fPaleontological
Institute
of
Shenyang
Normal
University,
253
North
Huanghe
Street,
Shenyang
110034,
China
Received
12
July
2011;
received
in
revised
form
23
April
2012;
accepted
9
May
2012
Available
online
19
May
2012
Abstract
Herein
we
describe
a
new
species
of
Microraptor
from
northeastern
China
that
provides
new
information
on
the
characteristics
of
the
genus
and
anatomical
details
suggesting
a
gliding
behaviour.
Although
specimens
of
Microraptor
have
been
known
for
at
least
a
decade,
the
completeness
of
the
new
fossil
provides
additional
morphology
that
highlights
the
uniqueness
of
this
taxon.
The
new
specimen,
Microraptor
hanqingi,
is
the
key
to
understanding
the
evolutionary
significance
of
hindlimb
wings.
A
four-winged
structure
present
on
an
organism
sharing
an
evolutionary
lineage
leading
to
modern
birds
implies
that
gliding
was
a
stage
in
the
development
of
avian
flight.
M.
hanqingi
represents
the
largest
known
microraptorian
from
China
with
a
total
length
of
approximately
1
m,
and
was
closely-related
to
the
venomous
form,
Sinornithosaurus.
©
2012
Elsevier
B.V.
and
Nanjing
Institute
of
Geology
and
Palaeontology,
CAS.
All
rights
reserved.
Keywords:
Dromaeosaurid;
Microraptor;
Archaeopteryx;
Gliding;
Arboreal
1.
Introduction
The
Early
Cretaceous
Jehol
forests
in
northeastern
China
contained
a
variety
of
arboreal
and
gliding
taxa
including
draco-
like
lizards,
gliding
mammals,
pterosaurs,
microraptorian,
and
primitive
birds
such
as
the
confuciusornithids
and
a
variety
of
enantiornithines.
This
paleoecology
and
faunal
diversity
is
con-
sistent
with
the
gliding
habits
proposed
by
the
original
authors
for
Microraptor
gui
(Xu
et
al.,
2003).
Our
new
species
pro-
vides
additional
osteological
support
for
four-winged
gliding
in
Microraptor.
Liaoning
gives
an
insight
into
the
beginning
of
ecologies
with
a
more
modern
aspect
resembling
in
particular
the
ecological
structure
of
Southeast
Asia
today.
The
nearly
com-
plete
absence
of
angiosperms
is
the
most
significant
difference.
This
gymnosperm
canopy
forest
provided
numerous
opportu-
nities
for
animals
that
could
climb
tree
trunks
and
glide.
That
gliding
was
an
important
phase
in
the
evolution
of
avian
flight
as
Corresponding
author.
Tel.:
+1
785
864
3917;
fax:
+1
785
864
5335.
E-mail
addresses:
gongep@mail.neu.edu.cn
(E.-P.
Gong),
ldmartin@ku.edu
(L.D.
Martin),
dinosaur@ku.edu
(D.A.
Burnham),
afalk@ku.edu
(A.R.
Falk),
houlh@yahoo.cn
(L.-H.
Hou).
envisioned
by
Beebe
(1915)
is
now
strongly
supported
by
fossil
evidence
(Xu
et
al.,
2003;
Xu
and
Zhang,
2005;
Xu
and
Guo,
2009;
Hu
et
al.,
2009)
and
more
recently
by
gliding
experiments
performed
on
an
anatomically
accurate
model
based
largely
on
the
specimen
described
in
this
paper
(Alexander
et
al.,
2010).
1.1.
Institutional
abbreviations
IVPP,
Institute
of
Vertebrate
Paleontology
and
Paleoanthro-
pology,
Chinese
Academy
of
Sciences,
Beijing,
China;
LHV,
Department
of
Land
and
Resources
of
Liaoning
Province;
STM,
Shandong
Tianyu
Museum
of
Nature;
KU,
Kansas
University
Division
of
Mammology.
2.
Stratigraphic
setting
All
known
taxa
of
Microraptor
occur
in
the
Early
Cretaceous
Jiufotang
Formation
of
Liaoning
Province,
northeastern
China
(Xu
et
al.,
2000,
2003;
Hwang
et
al.,
2002;
Wang
and
Zhou,
2003).
The
Jiufotang
is
a
formation
in
the
Jehol
Group
that
is
underlain
by
the
Yixian
Formation
(Jiang
and
Sha,
2006).
The
new
specimen,
LHV
0026,
occurs
in
buff-coloured,
lacustrine,
1871-174X/$
see
front
matter
©
2012
Elsevier
B.V.
and
Nanjing
Institute
of
Geology
and
Palaeontology,
CAS.
All
rights
reserved.
http://dx.doi.org/10.1016/j.palwor.2012.05.003
82
E.-P.
Gong
et
al.
/
Palaeoworld
21
(2012)
81–91
volcanic
paper
shale,
matching
that
of
other
specimens
from
this
particular
Jehol
deposit.
3.
Materials
and
methods
The
specimen
was
mechanically
prepared
under
a
binocu-
lar
microscope
and
transfer
techniques
were
used
to
reveal
the
underside.
After
the
top
(left)
side
was
embedded
in
optically
clear
acrylic
(CastoliteTM AP),
the
right
side
of
the
skeleton
was
uncovered
showing
well-preserved
skeletal
elements
and
details
not
evident
on
the
original
surface.
Casts
were
produced
from
both
sides
of
the
specimen
and
the
halves
put
back
together
so
that
it
was
possible
to
reconstruct
the
skeleton
in
three
dimen-
sions.
The
resulting
model
could
be
articulated
in
a
variety
of
postures.
The
original
specimen
was
studied
microscopically
with
regular
and
UV
lighting
and
scanned
with
CT
and
stereo
X-radiographs.
No
ambiguous
artefacts
or
restoration
was
found
on
this
specimen
and
we
are
confident
of
its
integrity.
We
use
the
Linnaean
system
where
taxa
have
diagnoses
and
are
not
defined
solely
by
some
presumed
phylogeny.
4.
Systematic
paleontology
Family
Dromaeosauridae
Matthew
and
Brown,
1922
Subfamily
Microraptorinae
Revised
diagnosis:
The
following
combination
of
charac-
ters
distinguish
the
Microraptorinae
from
other
dromaeosaurids;
narrow-waisted
coracoid;
large
tear-drop-shaped
coracoid
fen-
estra;
post
acetabular
ilium
bent
sharply
ventrally;
pelvis
opisthopubic
with
boot
bent
sharply
backwards;
prominent
lat-
eral
tuberosity
on
pubis;
nearly
vertical
ischium
with
enlarged
obturator
process;
femur
with
elevated
head
(above
greater
trochanter);
metatarsal
V
over
50%
length
of
metatarsal
IV;
metatarsal
I
more
proximally
situated
than
other
known
dro-
maeosaurids;
dorsally
situated
articular
surface
on
manus
unguals.
Remarks:
Senter
et
al.
(2004)
recognized
a
clade
consist-
ing
of
Sinornithosaurus,
Microraptor,
and
Bambiraptor
that
was
informally
referred
to
as
the
Microraptoria.
Sereno
et
al.
(2005)
created
a
“definitional
taxon”
that
they
termed
the
Micro-
raptorinae,
defining
it
as
the
“most
inclusive
clade
containing
Microraptor
zhaoianus
but
not
Dromaeosaurus
albertensis,
Velociraptor
mongoliensis,
Unenlagia
comahuensis,
or
Passer
domesticus”.
Sereno
et
al.
also
state
that
Sinornithosaurus
mil-
lenii
and
Bambiraptor
feinbergi
are
members
of
this
clade,
suggesting
that
his
concept
of
the
Microraptorinae
is
very
simi-
lar,
if
not
identical,
to
that
of
Senter
et
al.
(2004).
Longrich
and
Currie
(2009)
revised
the
Microraptorinae
and
placed
Bambirap-
tor
in
a
new
clade,
the
Saurornitholestinae,
and
added
Shanag
as
a
member.
Alternatively,
it
has
been
suggested
that
the
Maniraptora
nested
within
Aves
(Martin,
2004;
James
and
Pourtless,
2009).
Czerkas
et
al.
(2002)
also
considered
the
Maniraptora
within
Aves
and
placed
the
newly
named
dromaeosaurid
Cryptovolans
pauli
accordingly.
Microraptor
Xu
et
al.,
2000
Revised
diagnosis:
Skull
lacks
surface
ornamentation
of
Sinornithosaurus
as
well
as
sub
fenestral
fossa;
longer,
more
slender
ischium;
slightly
bowed
tibia;
first
phalanx
of
digit
III
longer
than
the
penultimate
phalanx.
Microraptor
hanqingi
n.
sp.
Etymology:
In
honor
of
the
late
Marshall
Zhang
Xueliang
who
was
the
founder,
president,
and
later
Honorary
President
of
Northeastern
University,
China;
Hanqing
is
his
alternate
name.
Type:
Department
of
Land
and
Resources
of
Liaoning
Province
LVH
0026,
a
single
slab
containing
a
nearly
complete
individual
(Fig.
1).
The
cranial
elements
comprise
a
skull
and
mandible
that
are
mostly
disarticulated
but
closely
associated.
Most
of
the
postcranial
skeleton
is
in
hard
articulation
although
the
pectoral
girdle
and
left
forearm
have
separated
from
the
body.
Both
hindlimbs
have
been
disassociated
from
the
pelvis
but
remain
in
articulation.
Most
of
the
tail
is
articulated;
how-
ever,
some
proximal
caudal
vertebrae
are
dislodged
and
lay
near
the
base
of
the
tail
and
pelvic
area
(Fig.
2).
The
tail
may
be
miss-
ing
the
terminal
caudal.
There
are
crural
feathers
associated
with
the
right
metatarsals
(Fig.
1)
and
vestiges
of
feathers
preserved
near
the
left
hindlimb
and
near
the
distal
end
of
the
tail.
Manual
and
pedal
unguals
have
claw
sheaths
preserved
(Fig.
3).
For
the
most
part,
the
rib
cage
and
gastralia
were
dislodged
and
moved,
probably
by
gas
formed
during
decay.
Some
ribs
are
still
artic-
ulated
to
dorsal
and
cervical
vertebrae.
Total
body
length
on
the
slab
approaches
1
m
measured
from
the
anterior
tip
of
the
dentary
to
the
proximal
end
of
the
tail.
Diagnosis:
Largest
known
species
of
Microraptor;
sternals
not
fused;
robust
pubis
with
squared
distal
end
(more
pointed
in
M.
gui)
and
not
as
bent
backwards
as
in
M.
gui;
pubic
boot
tapering
posteriorly;
ischia
with
posterior
edge
straight
and
ventral
edge
concave
while
in
M.
gui
they
are
sinuous
and
flat;
differs
from
M.
zhaoianus
and
resembles
M.
gui
in
having
a
proportionally
short
manual
digit
I;
metatarsals
II
and
IV
about
the
same
length
(mt
II
slightly
shorter);
differs
from
M.
gui
in
having
fewer
caudal
vertebrae
(23).
4.1.
Description
of
the
skull
The
skull
is
at
least
92.5
mm
long
based
on
the
length
of
the
mandible
(see
Table
1).
Preservation
of
the
skull
varies,
and
the
cranial
bones
that
can
be
identified
include
the
right
and
left
max-
illa,
remnants
of
both
premaxillae,
nasals,
lacrimal,
squamosal,
both
dentaries,
posterior
mandibular
elements
including
the
articular,
surangular,
prearticular,
angular,
and
splenial.
The
occipital
region
is
separated
from
the
rest
of
the
skull
and
can
be
observed
in
a
posterior
view.
In
Microraptor
hanqingi,
only
remnants
of
the
premaxillae
are
preserved
and
no
premaxillary
teeth
can
be
documented
among
the
isolated
teeth
on
the
slab.
The
left
maxilla
is
about
43.5
mm
long
and
projected
to
be
20.6
mm
high
at
its
tallest
point.
Its
triangular
outline
indi-
cates
that
the
skull
has
a
sloping
anterior
margin
similar
to
Archaeopteryx
and
Sinornithosaurus.
The
antorbital
fossa
is
E.-P.
Gong
et
al.
/
Palaeoworld
21
(2012)
81–91
83
Fig.
1.
Photographic
plate
of
the
holotype
LVH
0026,
Microraptor
hanqingi
(A);
scaled
ruler
equals
approximately
50
cm.
Line
drawing
of
the
holotype
(B);
scale
bar
=
5
cm.
Inset
(C)
photograph
of
the
feathers
from
the
left
metatarsals.
about
34.5
mm
long
and
about
16.4
mm
tall
extending
across
the
lateral
surface
of
the
maxilla
and
is
roughly
triangular
in
out-
line.
Within
this
fossa,
there
is
a
large
antorbital
fenestra
with
a
straight
anterior
border,
an
elliptically
shaped
maxillary
fen-
estra
unlike
Sinornithosaurus
which
has
a
semi-lunate
shaped
maxillary
fenestra
(fig.
3
of
Xu
and
Wu,
2001),
and
a
smaller
oblong
promaxillary
fenestra.
The
maxilla
contains
14
aveoli
but
only
four
teeth
are
pre-
served
in
position.
A
tooth
in
mid-position
has
minute
serrations
on
the
posterior
keel.
The
longest
tooth
seems
to
be
the
one
in
position
7.
The
maxillary
teeth
are
longer
and
more
recurved
than
the
dentary
teeth.
The
teeth
near
the
midpoint
of
the
max-
illary
are
significantly
longer
than
the
teeth
anterior
or
posterior
to
them
as
is
the
case
in
Sinornithosaurus.
Microraptor
resem-
bles
rear-fanged
snakes
in
the
general
arrangement
of
its
tooth
sizes.
The
nasals
are
35
mm
long
and
are
thin,
paired
elements
that
widen
anteriorly
and
posteriorly.
They
are
widest
(9.2
mm)
across
the
anterior
portion
of
the
bone
just
before
the
concave
border
of
the
nares.
The
lacrimal
is
T-shaped
and
about
19.5
mm
tall.
The
anterior
ramus
is
10.7
mm
long;
the
posterior
ramus
is
much
shorter.
The
dentary
is
ventrally
bowed
as
in
a
referred
specimen
of
Microraptor
zhaoianus
(IVPP
V
13475;
fig.
19
of
Xu,
2002)
and
Bambiraptor
feinbergi
(AMNH
30556
[FIP
001];
fig.
1
of
Burnham
et
al.,
2000).
The
tooth
count
of
M.
hanqingi
cannot
be
precisely
determined
for
the
dentary;
however,
the
aveoli
that
can
be
seen
are
arranged
closely
together
and
there
is
room
for
perhaps
as
many
as
16
teeth.
The
dentary
teeth
are
short
and
broad
as
compared
to
the
maxillary
teeth
and
seem
to
be
uniform
in
size.
The
medial
view
of
the
left
ramus
shows
an
upward
directed
prearticular
much
like
the
one
figured
by
Norell
et
al.
(2006,
see
fig.
14)
for
Tsaaganmangas.
It
is
articulated
to
the
surangular
but
the
posterior
mandible
is
separated
from
the
anterior
lower
jaw
at
the
intermandibular
hinge.
There
is
a
short,
triangular
84
E.-P.
Gong
et
al.
/
Palaeoworld
21
(2012)
81–91
Fig.
2.
X-ray
of
the
holotype
LVH
0026,
Microraptor
hanqingi,
pelvis
in
left
lateral
view;
arrow
points
to
acetabulum.
Abbreviations:
femur
(fem)
and
pubis
(p).
Scale
bar
=
5
cm.
Fig.
3.
X-ray
of
the
holotype
LVH
0026,
Microraptor
hanqingi,
showing
the
skull,
occiput,
vertebrae
(arrow
points
to
pleurocoel),
and
manus.
Abbreviations:
maxilla
(mx),
occipital
condyle
(oc)
and
cs
(claw
sheath).
Scale
bar
=
1
cm.
Table
1
Length
measurements
(in
mm)
of
the
holotype
of
Microraptor
hanqingi
for
selected
skeletal
elements
and
body
parts.
Element
Left
Right
Axial
Maxillary
length 45.0b
Lower
jaw
length
92.5a
Dentary
length
48.9b
Femur
111.7
109.8
Tibiotarsus
137.1
137.9
Tarsometatarsus
75.4
77.7
Pes
digit
II
33.9
34
Pes
digit
III 45 48b
Pes
digit
IV
41.3
43b
Humerus 93.5
92.6
Radius 77.9b79.5
Ulna
81.9b82.5
Scapula
54.9
59.9
Coracoid
27.3
Middle
metacarpal
52
Middle
digit
113
Sternal
plate
47.3
Furcula
73
Ilium
length
60
Ischium
length
36
Pubis
length
78
Dorsal
series
length
132b
Sacrum
length
43.6
Trunk
length 179b
Tail
length 535b
Total
length
950b
Hindlimb
length
380
Forelimb
length
231
Metacarpal
II
12.98
Metacarpal
III
54.88
Metacarpal
IV
48.17
II-1
32.44
Ungual
II
21.98
III-1
23.21
21.96
III-2
24.72
24.2
Ungual
III
20.56
IV-1
17.7
IV-2
4.66
IV-3 13.1
Ungual
IV
9.35
aIndicates
a
significant
portion
of
the
bone
measured
was
missing.
bIndicates
an
approximate
measurement.
splenial
in
articulation
with
the
medial
side
of
the
dentary.
We
did
not
observe
an
external
mandibular
fenestra.
The
occiput
is
represented
by
the
occipital
condyle
and
the
paraoccipital
processes.
The
occipital
condyle
is
saddle-shaped
and
the
foramen
magnum
is
roughly
oval.
The
paraoccipitals
are
not
downturned.
4.2.
Description
of
the
postcranial
elements
We
estimate
that
Microraptor
hanqingi
has
23
presacral
ver-
tebrae
comprising
ten
cervicals
and
13
dorsals.
The
cervical
vertebrae
are
articulated,
but
the
anterior
ones
are
not
easily
dis-
tinguished
due
to
post
mortem
damage.
Their
centra
appear
to
be
obliquely
angled
as
in
Deinonychus
antirrhopus
and
Bambi-
raptor
feinbergi
(Ostrom,
1969;
Burnham,
2004).
The
dorsals
are
well
preserved
and
articulated
except
for
the
posterior
ones
E.-P.
Gong
et
al.
/
Palaeoworld
21
(2012)
81–91
85
Fig.
4.
Line
drawing
of
the
reconstructed
skull
of
the
holotype
LVH
0026,
Microraptor
hanqingi.
Shaded
areas
are
bones
easily
recognized
on
the
actual
specimen.
that
are
slightly
dislodged
from
the
sacral
area.
From
the
radio-
graphs,
we
can
see
that
four
of
the
anterior
dorsals
have
small
openings
(pleurocoels)
in
lateral
side
of
their
centra
(Fig.
3).
The
height
of
the
dorsal
vertebrae
falls
within
the
range
typical
of
dromaeosaurs.
The
sacral
vertebrae
are
not
clearly
exposed
since
they
lay
between
the
pelvic
bones.
The
tail
is
approximately
535
mm
long
and
has
remnants
of
feathers
preserved
on
the
distal
end.
There
are
23
caudal
vertebrae,
although
the
proximal
caudals
are
disarticulated
the
surrounding
matrix
is
intact
through
the
sacrals
although
the
very
distal
caudal
may
be
missing
(Microraptor
zhaoianus
has
less
than
26
caudals;
M.
gui
has
approximately
26
caudals;
Crypto-
volans
pauli
has
28–30
caudals).
The
articulated
portion
of
the
tail
is
preserved
with
a
downward
curve
(Fig.
1).
The
six
anterior
most
caudal
vertebrae
are
significantly
shorter
than
the
others,
and
have
transverse
processes
that
become
less
pronounced
pos-
teriorly
until
the
processes
on
the
fifth
and
sixth
caudal
are
only
slight
ridges.
The
articular
facets
of
the
prezygapophyses
on
the
anterior
caudals
are
vertically
oriented.
The
longest
cau-
dals
are
in
the
mid-tail
region
and
the
caudals
decrease
in
length
from
this
point.
Rods
formed
by
elongated
prezygapophyses
and
chevrons
are
present
along
the
entire
length
of
the
tail
approach-
ing
the
first
few
proximal
caudals;
that
is
also
the
condition
found
in
Bambiraptor.
In
other
dromaeosaurids
such
as
Velociraptor
mongoliensis,
the
rods
are
not
as
extensive
and
do
not
approach
the
base
of
the
tail
(Norell
and
Makovicky,
1999).
Deinonychus
and
Velociraptor
have
tails
that
comprise
more
caudal
vertebrae,
and
intersegmental
mobility
was
not
eliminated
since
there
are
transverse
processes
up
to
the
twelfth
caudal
and
the
zygapophy-
ses
retain
articular
facets
the
entire
length
of
the
tail
(Ostrom,
1969).
Both
scapulae
and
coracoids
are
articulated
forming
a
scapu-
lar
arch
of
about
90
degrees
as
in
Archaeopteryx
and
most
other
birds
(Fig.
4).
The
scapula
is
long
and
strap-like
being
bowed
in
lateral
view.
As
in
Microraptor
gui,
the
scapula
and
coracoid
are
fused,
and
the
glenoid
faces
laterally.
There
is
a
large
fenes-
tra
present
on
the
coracoid.
Interestingly,
Bambiraptor
feinbergi
Fig.
5.
X-ray
of
furcula
of
the
holotype
LVH
0026,
Microraptor
hanqingi.
Abbreviations:
furcula
(fur),
coracoid
foramen
(cf)
and
scapula
(sc).
Scale
bar
=
3
cm.
has
a
similar
scapular
arch
except
that
the
fenestra
is
absent
and
the
bones
are
not
fused.
One
of
the
ossified
sternal
plates
is
preserved.
It
has
a
sim-
ilar
morphology
to
Microraptor
gui
and
M.
zhaoianus
(Hwang
et
al.,
2002),
as
well
as
Bambiraptor
feinbergi.
Facets
on
the
anterolateral
margin
are
present
for
at
least
three
sternal
ribs.
In
M.
gui
and
in
Cryptovolans
pauli
the
sternal
plates
are
fused.
There
is
a
boomerang-shaped
furcula
with
flattened
cross
section
and
sulcated
as
in
Archaeopteryx
and
Bambiraptor.
The
interclavicular
angle
is
approximately
80
degrees,
similar
to
other
specimens
referred
to
this
genus
(Hwang
et
al.,
2002);
however,
a
referred
specimen
of
Microraptor
gui
has
a
much
larger
angle
(O’Connor
et
al.,
2011).
The
X-radiograph
indi-
cates
that
our
furcula
is
thin-walled
and
reinforced
with
bony
struts
(Fig.
4).
There
is
no
evidence
of
a
hypocleideum
and
the
width
of
the
furcula
is
5.9
mm
at
this
point
tapering
distally
with
the
epicleidia
being
2.6
mm
wide.
There
are
no
foramina
or
pneumatopores
evident.
Both
humeri
are
preserved
although
the
condyles
on
either
end
are
difficult
to
observe.
The
humeral
length
(Table
1)
is
less
than
the
scapular
length
and
the
humerus
has
a
deltopectoral
crest
that
is
39%,
of
the
humeral
length,
as
compared
to
36%
in
the
holotype
of
Microraptor
gui.
The
ulnae
are
bowed
and
thicker
in
diameter
than
the
radii
(Fig.
5);
both
radii
and
ulnae
are
articulated.
This
and
some
post-mortem
damage
makes
positive
identification
of
a
biceps
tuberosity
on
the
radius
difficult.
The
holotype
of
Microraptor
86
E.-P.
Gong
et
al.
/
Palaeoworld
21
(2012)
81–91
gui
has
a
prominent
biceps
tuberosity
(Xu
et
al.,
2003);
however,
this
can
only
be
seen
because
the
radius
is
slightly
disarticulated.
Although
reported
as
a
diagnostic
character
for
M.
gui,
it
is
not
observed
on
the
articulated
forearms
of
M.
hanqingi.
The
right
wrist
in
Microraptor
hanqingi
is
articulated
and
the
semilunate
carpal
is
a
comparatively
large
bone
as
compared
to
the
other
carpals.
There
appears
to
be
a
total
of
four
carpals
(Fig.
5);
however,
the
contacts
are
ambiguous
due
to
their
close
articulation
and
post-mortem
damage.
The
semilunate
carpal
appears
to
partially
cover
the
first
two
metacarpals.
As
in
Microraptor
gui,
the
first
metacarpal
is
one-fourth
the
length
of
the
second
metacarpal;
the
third
metacarpal
is
slen-
der
and
although
the
bone
is
fractured,
there
is
no
evidence
that
it
is
bowed.
The
first
phalange
on
the
second
manual
digit
is
broadened—possibly
to
support
feathers
(Paul,
2002).
The
penultimate
phalange
on
the
third
digit
is
bowed
as
in
M.
han-
qingi
and
M.
gui.
All
the
manual
unguals
are
highly
recurved
and
the
unguals
on
the
left
manual
digits
two
and
three
preserve
the
keratinous
sheaths
(Fig.
3).
The
pelvis
is
well-preserved
and
articulated
in
right
lateral
view
providing
a
clear
view
of
the
acetabulum
(Figs.
1
and
2).
The
acetabulum
is
partially
closed
and
there
is
no
supracetabular
shelf
or
crest
on
the
lateral
surface
of
the
ilium
(Longrich
and
Currie,
2009)
have
pointed
this
out
for
microraptorians
and
oth-
ers.
The
preacetabular
portion
of
the
ilium
is
similar
to
other
microraptorians.
Posteriorly
the
iliac
blade
is
sharply
down-
turned,
extending
past
the
pubic
and
is
chial
peduncles
and
tapers
to
a
point.
The
type
of
Microraptor
zhaoianus
also
has
a
down-
turned
ilium;
however,
this
portion
of
the
ilium
is
not
preserved
on
M.
gui.
The
distal
end
of
the
ischium
extends
anteriorly
to
form
an
elongate
and
tapered
obturator
process.
This
feature
can
also
be
seen
on
the
holotypes
of
M.
zhaoianus
and
M.
gui
although
the
ischium
of
M.
hanqingi
is
not
as
slender
as
in
those
species.
The
pubis
is
swept
back
posteriorly
about
115
degrees
which
is
comparable
to
the
M.
gui
pubis
where
it
is
swept
back
120
degrees
(Xu
et
al.,
2003).
The
pubis
of
M.
zhaoianus
is
preserved
in
anterior
view
and
is
missing
the
distal
portion.
Both
femora
are
preserved
in
Microraptor
hanqingi.
The
right
femur
is
complete
and
exposed
in
a
lateral
view
(Fig.
2).
The
left
femur
is
exposed
in
medial
view
and
broken
with
the
proximal
portion
remaining
close
to
articulation
in
the
acetabu-
lum.
The
femur
appears
to
thicken
distally
although
crushing
in
this
area
obfuscates
any
measurement.
The
femora
are
slightly
bowed
laterally
and
anteriorly
as
in
most
other
dromaeosaurs.
The
accessory
crest
pendant,
noted
by
Xu
et
al.
(2000)
for
M.
zhaoianus,
cannot
be
confirmed
in
this
specimen
of
M.
hanqingi.
As
in
the
holotype
M.
gui,
the
tibiae
are
also
bowed
anteriorly
and
the
distal
ends
are
medially
twisted.
The
inner
condyle
is
larger
and
rounded
than
the
outer
condyle.
The
distal
end
is
compressed
and
not
significantly
wider
than
the
shaft.
The
foot
and
ankle
bones
of
our
specimen
are
nearly
com-
pletely
preserved
and
are
especially
noteworthy.
Left
metatarsal
I
lie
behind
metatarsal
II
(Fig.
6)
but
not
as
distally
positioned
on
the
foot
as
in
the
holotype
of
Microraptor
zhaoianus
(Xu
et
al.,
2000).
The
metatarsals
II,
III
and
IV
are
fused
proximally
and
metatarsal
III
is
laterally
compressed
between
metatarsals
II
and
IV.
Metatarsal
V
is
thin
and
long
as
in
other
microraptorians.
Fig.
6.
X-ray
of
the
right
arm
of
the
holotype
LVH
0026,
Microraptor
hanqingi.
Digits
are
labelled
II,
II
and
IV.
Abbreviations:
ulna
(ul)
and
radius
(ra).
Scale
bar
=
3
cm.
The
distal
tarsals
III
and
IV
are
apparently
fused
on
the
prox-
imal
surface
of
metatarsal
IV
and
have
a
concave
articular
surface.
The
proximal
end
of
the
tarsometatarsus
is
inclined.
There
does
not
appear
to
have
been
any
other
distal
tarsals.
As
in
all
deinonychosaurs,
the
2nd
pedal
ungual
is
the
largest.
The
ramphotheca
on
that
claw
is
highly
recurved
and
elongated
as
in
other
microraptorians
(Burnham
et
al.,
2011).
The
ram-
photheca
is
also
preserved
on
digit
three
of
the
left
foot
further
E.-P.
Gong
et
al.
/
Palaeoworld
21
(2012)
81–91
87
Fig.
7.
X-ray
of
lower
hindlimbs
of
the
holotype
LVH
0026,
Microraptor
hanqingi.
Abbreviations:
tibia
(ti),
metatarsal
(mt)
and
claw
sheath
(cs).
Scale
bar
=
1
cm.
demonstrating
a
highly
recurved
morphology
on
pedal
claws
for
Microraptor.
Compared
to
the
homologous
phalanges
in
a
chicken
(of
similar
body
weight)
the
Microraptor
digits
are
much
less
robust.
This
relative
weakness
of
the
pedal
digits
is
also
characteristic
of
pterosaurs
(figures
on
p.
57
of
Wellnhofer,
1991).
Feathers
are
easily
distinguished
on
the
foot
of
our
spec-
imen
showing
characteristic
rachis
and
barbs
(Fig.
1C).
5.
Discussion
Although
Microraptor
has
been
known
for
a
decade,
not
many
clear
diagnostic
features
have
been
offered,
making
iden-
tification
of
specimens
and
placing
them
in
taxonomic
positions
problematic.
The
type
specimen
of
Microraptor
zhaoianus
is
unfortunately
incomplete
in
many
respects;
the
following
char-
acters
seem
to
be
clearly
present:
metatarsals
comprising
the
tarsometatarsus
are
nearly
equal
in
length;
downturned
poste-
rior
ilium;
lengths
of
mid-caudals
much
longer
than
dorsals.
The
diagnosis
of
Microraptor
gui
must
ultimately
stand
on
fea-
tures
visible
on
the
type.
The
features
of
the
referred
specimen
of
Microraptor
zhaioanus
differ
enough
from
the
holotype
to
lead
us
to
wonder
if
this
referred
specimen
is
actually
conspecific.
Some
caution
should
be
applied
when
using
it
to
extrapolate
diagnostic
features
for
that
species.
We
are
confident
that
our
new
specimen
is
best
treated
as
a
new
species
of
Microraptor
rather
than
Sinornithosaurus,
as
it
lacks
the
specializations
of
the
teeth
and
maxillary
characteristic
of
that
genus
as
well
as
the
proportions
of
manual
digit
three.
The
holotype
(IVPP
V
12330)
of
Microraptor
zhaoianus
was
published
with
only
a
brief
description
of
the
cranial
material
(Xu
et
al.,
2000).
The
holotype
of
M.
gui
has
a
skull,
but
the
anterior
portions
are
dubious
and
the
posterior
cranial
elements
are
too
badly
crushed
to
reconstruct
the
cranium
although
it
con-
firms
the
presence
of
a
tri-radiate
postorbital
in
this
genus
(Xu
et
al.,
2003).
The
postorbital
of
M.
hanqingi
(Fig.
3)
is
similar.
A
referred
specimen
of
M.
sp.
(IVPP
V
13320)
has
a
nearly
complete
skull
but
also
suffers
from
post-mortem
damage.
This
skull
has
been
briefly
described
as
being
relatively
small
(com-
pared
to
femur
length),
heterodont
(Xu,
2002),
with
the
teeth
lacking
serrations.
Serration
pattern
varies
in
almost
all
of
the
known
skulls
and
is
ambiguous
in
our
new
specimen.
We
were
unable
to
document
the
presence
of
a
mandibular
fenestra
and
were
not
able
to
find
one
in
several
other
specimens
of
Micro-
raptor;
nor
is
one
indicated
in
the
tiny
reconstruction
on
the
88
E.-P.
Gong
et
al.
/
Palaeoworld
21
(2012)
81–91
Microraptor
skull
shown
in
Xu
et
al.
(2011)
in
their
phylogram.
Sinornithosaurus
is
illustrated
by
Xu
and
Wu
(2001)
as
having
a
mandibular
fenestra
and
this
seems
to
be
correct
providing
an
additional
difference
between
it
and
Microraptor.
Microraptor
hanqingi
has
a
total
reconstructed
length
of
approximately
95
cm.
This
is
larger
than
both
M.
zhaoianus,
which
has
a
total
length
of
48
cm
and
M.
gui,
which
has
a
total
length
of
78+cm.
We
estimate
the
body
mass
of
the
animal
to
be
approximately
2
kg
based
on
water-displacement
tests.
In
com-
parison,
the
more
robust
juvenile
Bambiraptor
feinbergi
has
a
reconstructed
length
of
94
cm.
The
ratio
of
tibial
length
to
femur
length
is
1.23
whereas
in
Microraptor
gui
the
ratio
is
1.289.
We
estimate
the
trunk
length
(TL)
in
our
specimen
to
be
179
mm
yielding
a
femur:TL
ratio
of
0.624
compared
to
0.614
reported
in
M.
gui
(Table
1).
Trunk
length
of
M.
hanqingi
is
short
and
estimated
to
be
179
mm
yield-
ing
a
femur:TL
ratio
of
0.624
compared
to
M.
zhaoianus
0.614
and
M.
gui
(0.44–0.50),
showing
M.
hanqingi
has
a
somewhat
longer
trunk.
6.
Significance
and
conclusions
Our
investigations
show
that
there
is
a
considerable
diversity
of
predatory
four-winged
gliding
birds
in
the
Liaoning
Forest
of
the
Early
Cretaceous.
The
only
predatory
gliders
today
are
small
and
eat
insects
(Draco,
etc.).
The
gliders
most
similar
to
Micro-
raptor
(flying
squirrels
and
dermopterans)
in
modern
tropical
forests
are
frugivorous.
The
abundance
of
primitive
birds
with
limited
flight
capabilities
and
arboreal
mammals
probably
pro-
vided
the
four-winged
gliders
with
a
unique
opportunity
for
a
predatory
lifestyle
(Larrson
et
al.,
2010;
O’Connor
et
al.,
2011).
Our
new
anatomical
information
has
produced
several
con-
verging
lines
of
evidence
demonstrating
that
the
original
describers
of
Microraptor
(Xu
et
al.,
2003)
were
correct
in
their
interpretation.
This
evidence
shows
that
the
microraptorian
four-winged
gliders
were
directly
analogous
in
morphology
and
presumably
lifestyle
to
the
most
specialized
mammalian
glid-
ers
and
are
in
fact,
a
close
ecomorph
to
gliding
dermopterans,
Cynocephalus.
The
acetabulum
is
visible
in
a
number
of
specimens
and
has
sloping
sides
with
the
articular
surface
extending
on
to
the
lateral
side
of
the
ilium
allowing
the
femur
to
orient
at
an
angle
of
nearly
75
degrees
(Fig.
8A
and
C).
The
inner
surface
of
the
acetabulum
is
too
nearly
closed
to
permit
the
femur
to
easily
articulate
with
the
shaft
held
vertical
(parasagittal)
and
no
dorsal
shelf
exists
to
support
such
a
position
(Fig.
8B).
The
femur
has
a
very
short
neck
with
the
head
significantly
elevated
above
the
trochanter
as
can
be
seen
from
other
referred
specimens
of
Microraptor
such
as
STM5-225
(Fig.
9).
It
is
in
many
respects
similar
to
the
dermopteran
femur
(Fig.
10A
and
B)
which
is
also
elongated.
In
fact,
dermopterans
provide
the
best
model
for
the
articulation
of
the
leg
and
its
position
in
Microraptor
while
gliding
or
climbing
(Fig.
10C).
The
sprawling
posture
of
the
hindlimb
is
confirmed
by
an
inclined
ankle
joint
that
is
seen
in
many
of
the
known
specimens.
This
is
an
unusual
morphology
that
precludes
the
normal
fore-aft
hinge
seen
in
animals
with
erect
parasagittal
legs.
Fig.
8.
Photograph
of
Microraptor
sp.
femur
(STM5-225).
Abbreviation:
femoral
head
(fh).
Scale
bar
=
1
cm.
The
morphology
of
the
foot
indicates
an
arboreal
habitat;
the
hallux
is
posteriorly
positioned
(Xu
et
al.,
2000;
O’Connor
et
al.,
2011)
and
capable
of
opposing
the
other
toes;
the
claws
are
highly
recurved
as
in
other
microraptorian;
lengthening
of
the
4th
toe
making
it
subequal
with
the
3rd
toe
(Storer,
1971).
Middleton
(2003)
examined
the
holotype
of
Microraptor
zhaoianus
and
confirmed
that
metatarsal
I
lies
in
a
position
behind
the
tarsometarsus
but
considered
this
a
non-perching
foot
since
he
could
not
see
if
the
metatarsal
was
twisted.
Although
one
of
us
(Martin,
1991)
was
the
first
to
point
out
that
modern
perch-
ing
birds
had
a
twisted
metacarpal
I,
we
do
not
expect
to
find
this
condition
in
the
progenitors
of
perching
birds
and
suspect
these
animals
were
using
a
variety
of
perching
mechanisms.
E.-P.
Gong
et
al.
/
Palaeoworld
21
(2012)
81–91
89
Fig.
9.
Detailed
features
of
pelvic
anatomy
related
to
leg-sprawling
in
Microraptor
hanqingi.
Oblique
ventral
view
of
sprawled
leg
and
hips
(A);
right
lateral
view
of
pelvis
(B);
oblique
dorsal
view
with
femur
articulated
(C).
Deceechi
and
Larrson’s
(2011)
report
on
the
ungual
phalanx
did
not
show
a
significant
difference
between
arboreal
and
cur-
sorial
animals
in
many
respects.
Their
data
on
claw
morphology
are
inconsistent
with
ours
and
others
(Xu
et
al.,
2000,
2003)
and
are
flawed
by
restriction
to
the
bony
core
rather
than
the
ramphotheca
as
the
functional
claw
shape
is
determined
by
the
latter.
Fortunately
the
material
from
China
preserves
numerous
examples
of
the
horny
ramphotheca
around
the
claws.
It
is
the
shape
of
this
ramphotheca
that
provides
information
about
the
Fig.
10.
Left
femur
of
IVPP
V
12662,
Microraptor
sp.
(A);
scale
bar
=
1
cm.
Left
femur
of
KU
165788,
Cynocephalus
(B);
scale
bar
=
1
cm.
Ventral
view
of
Cynocephalus
pelvic
area
with
femur
sprawled
(C);
the
femoral
head
does
not
fit
deeply
inside
the
acetabulum
when
the
leg
is
sprawled
for
gliding
as
shown
by
the
exposed
ventral
surface
of
the
articulated
femoral
head;
scale
bar
=
1
cm.
90
E.-P.
Gong
et
al.
/
Palaeoworld
21
(2012)
81–91
lifestyle
of
the
animal.
Unfortunately
this
shape
cannot
be
pre-
dicted
from
that
of
the
bony
core
and
attempts
to
use
the
core
have
met
with
poor
success
(Ostrom,
1986;
Glen
and
Bennett,
2007).
The
manual
and
pedal
claws
of
Microraptor
are
strongly
compressed
laterally
and
highly
recurved
corresponding
to
the
trunk-climbing
morphology
described
by
Yalden
and
Feduc-
cia
(Yalden,
1985,
1997;
Feduccia,
1993).
Claws
designed
for
predatory
grasping
may
not
be
distinguishable
from
climbing
claws
by
claw
angle
alone
but
are
easily
separated
by
a
thicker
base
that
tapers
towards
the
tip
(Pike
and
Maitland,
2004).
The
manual
claws
of
Microraptor
correspond
to
the
tree
climbing
morphology
and
were
surely
only
used
for
climbing
as
a
prey
held
at
the
tips
of
the
long
fingers
could
not
be
reached
by
the
mouth.
Manual
claw
three
has
a
curvature
of
180
degrees,
this
places
it
beyond
the
observed
range
for
predatory
birds
(Pike
and
Maitland,
2004)
and
within
the
range
for
the
pedal
claws
of
the
most
advanced
modern
climbers
such
as
woodpeckers,
and
slightly
above
the
manual
claws
of
Archaeopteryx.
The
pedal
claw
for
digit
three
measured
138
degrees,
placing
it
within
the
highest
range
for
modern
perching
birds
and
well
within
the
range
of
modern
trunk
climbing
birds
(Burnham
et
al.,
2011).
Also
the
extreme
lateral
compression
seen
in
the
claws
of
Micro-
raptor
is
only
matched
by
modern
trunk
climbing
mammals
and
birds,
such
as
squirrels,
dermopterans,
fruit
bats
and
woodpeck-
ers
(Yalden,
1985)
and
is
unlike
terrestrial
archosaurs
such
as
the
Upper
Jurassic
Compsognathus
with
flattened
pedal
claws
resembling
those
of
terrestrial
birds
being
broader
than
deep
giv-
ing
a
distinctly
hoof-like
impression
(Glen
and
Bennett,
2007).
Dromaeosaurids
are
characterized
in
part
by
an
enlarged
claw
on
the
second
pedal
digit.
A
stout
truncated
penultimate
phalanx
permits
this
claw
to
be
retracted.
In
later
forms
this
is
thought
to
be
part
of
a
unique
predatory
complex,
although
it
has
been
argued
recently
that
they
functioned
for
grasping
rather
than
as
a
killing
instrument
(Senter,
2006).
Microraptor
has
such
a
claw
and
the
holotype
of
M.
hanqingi
preserves
the
horny
sheath
in
anatomical
position
(Fig.
7)
showing
that
it
was
enormously
elongated
and
recurved.
However,
it
also
shows
the
extreme
lateral
compression
found
in
trunk
climbing
birds
and
mammals
as
well
as
the
subapical
constriction
and
needle-like
tip
unique
to
trunk
climbing
birds
(Peters
and
Gorgner,
1992).
This
suggests
that
it
was
not
a
predatory
device,
but
was
used
in
climbing.
It
may
have
opposed
the
claw
on
the
first
digit
(reduced
but
with
an
enlarged
claw
sheath)
and
perhaps
also
the
fourth
digit
which
is
able
to
swing
laterally
and
is
often
preserved
in
that
position
in
the
specimens
so
that
the
foot
could
firmly
grip
branches.
The
predatory
functions
of
this
complex
probably
evolved
after
the
loss
of
flight
in
this
lineage.
The
stiffened
tail
might
have
provided
additional
support
for
trunk
climbing
analogous
to
the
stiffened
tail
feathers
in
modern
woodpeckers
(Chatterjee,
1997).
Larger
dromaeosaurs
probably
had
more
lateral
flexibility
along
the