ARTICLE
Received 28 Sep 2016 | Accepted 13 Jan 2017 | Published 1 Mar 2017
DOI: 10.1038/ncomms14576
OPEN
Basal paravian functional anatomy illuminated
by high-detail body outline
Xiaoli Wang1,*, Michael Pittman2,*, Xiaoting Zheng1,3, Thomas G. Kaye4, Amanda R. Falk5, Scott A. Hartman6
& Xing Xu7
Body shape is a fundamental expression of organismal biology, but its quantitative
reconstruction in fossil vertebrates is rare. Due to the absence of fossilized soft tissue
evidence, the functional consequences of basal paravian body shape and its implications
for the origins of avians and flight are not yet fully understood. Here we reconstruct the
quantitative body outline of a fossil paravian Anchiornis based on high-definition images
of soft tissues revealed by laser-stimulated fluorescence. This body outline confirms
patagia-bearing arms, drumstick-shaped legs and a slender tail, features that were probably
widespread among paravians. Finely preserved details also reveal similarities in propatagial
and footpad form between basal paravians and modern birds, extending their record to
the Late Jurassic. The body outline and soft tissue details suggest significant functional
decoupling between the legs and tail in at least some basal paravians. The number of
seemingly modern propatagial traits hint that feathering was a significant factor in how basal
paravians utilized arm, leg and tail function for aerodynamic benefit.
1 Institute of Geology and Paleontology, Linyi University, Linyi City, Shandong 276005, China. 2 Vertebrate Palaeontology Laboratory, Department of Earth
Sciences, University of Hong Kong, Pokfulam, Hong Kong, China. 3 Shandong Tianyu Museum of Nature, Pingyi, Shandong 273300, China. 4 Foundation for
Scientific Advancement, 7023 Alhambra Drive, Sierra Vista, Arizona 85650, USA. 5 Department of Biology, Centre College, 600 West Walnut Street,
Danville, Kentucky 40422, USA. 6 Department of Geoscience, University of Wisconsin-Madison, Lewis G. Weeks Hall for Geological Sciences, 1215 West
Dayton Street, Madison, Wisconsin 53706-1692, USA. 7 Key Laboratory of Vertebrate Evolution and Human Origins of Chinese Academy of Sciences,
Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing 100044, China. * These authors contributed equally to this
work. Correspondence and requests for materials should be addressed to M.P. (email: mpittman@hku.hk) or to X.W. (email: wang_7355@163.com).
NATURE COMMUNICATIONS | 8:14576 | DOI: 10.1038/ncomms14576 | www.nature.com/naturecommunications
1
ARTICLE
NATURE COMMUNICATIONS | DOI: 10.1038/ncomms14576
L
aser-stimulated fluorescence (LSF) imaging can broaden
the scope of data available from fossils by revealing
morphological details that are otherwise invisible under
white or ultraviolet light conditions1. In this study, LSF imaging is
performed on the four-winged dinosaur Anchiornis2,3, one of a
few key basal paravian theropods—including Microraptor and
Archaeopteryx—whose osteology, feathering and aerodynamics
have made profound contributions to the understanding of avian
origins and early flight evolution3–8. Anchiornis is especially
suited for this study because its contribution to understanding
avian and flight origins has not been fully realized. As the
earliest four-winged paravian with long tibial and metatarsal
feathers, Anchiornis shares a key feature with gliding-capable
Microraptor3,5,9. Anchiornis is also represented by 229 þ
specimens10, which greatly improves the chance of discovering
rare soft tissue preservation with minimal taphonomic damage.
The LSF data collected was used to produce and describe the
quantitative outlines of portions of the fossil paravian body. In
providing much needed fossilized soft tissue evidence, the scope
of indirect skeletal and feather evidence in determining basal
paravian body shape will be better understood. Additionally, the
utility of body shape inferences based on an extant phylogenetic
bracket (EPB) approach can be gauged. The reconstructed leg
and tail outlines of Anchiornis suggest significant functional
decoupling between these body parts, as was likely the case in
many other basal paravians. The traits of the reconstructed
patagia-bearing arms hint that feathering was a significant factor
in how basal paravians utilized their appendages for aerodynamic
benefit.
Results
Body outline. LSF imaging recovered high fidelity outlines of the
arms, legs and tail for Anchiornis, but head, neck and thorax
outlines could not be reliably imaged (Fig. 1). The body parts
imaged under fluorescence were highly representative of the
original tissues, but no chemical analysis was done to determine if
they were organic or mineral in nature. For descriptive purposes
in this paper, standard anatomical references are used until such
time that a thorough analytical assessment of the preservation
allows for more accurate vernacular.
Forelimb outline. The slender arm outline is widest across the
propatagia (Figs 1 and 2). The latter are preserved at 69°–94° of
elbow extension and are less widely extended than the smaller
postpatagia (Supplementary Fig. 1; Supplementary Table 1).
STM-127
There is no obvious alular patagium, unlike enantiornithine
MCCMLH31444 (ref. 11). The propatagial surface is covered
in almost evenly spaced—but not scattered11—spots that
occasionally contain brown filamentous structures. The third
manual digit is covered in small rounded reticulate scales
(Supplementary Fig. 2). The outline interpreted as the margin
of the soft tissue is approximately twice as thick as the phalanges
of the third digit and has a smooth ventral surface without thick
fleshy pads, as in the fingers of oviraptorosaur Caudipteryx
(Fig. 1, plate II of ref. 12).
Hindlimb outline. The leg outlines are known up to the proximal
end of the tibia and fibula and are widest at the proximal
two-thirds of the latter (Fig. 1), the same shape found in
birds13,14. The feet have bird-like plantar footpads with interpad
grooves exhibiting the typical arthal condition of theropods15,16
(Figs 1 and 3). The footpads are covered in pebble-shaped
reticulate scales (Fig. 3), but the dorsal foot scales are minimally
discernible. There are pebble-shaped tibia scales and equivocal
ankle scales (Supplementary Fig. 3).
Tail and pelvic outline. The slender tail outline hugs the
caudal vertebrae, but at its base it forms a gently concave margin
from the third caudal to the region around the posterior ramus
of the ischium (Figs 1 and 4a; the ischium is not preserved in
STM-0-114, but its position is inferred from STM-0-118 and
other specimens). The body outline follows the shape of the pubic
boot and then ascends at a steep angle towards the distal end of
the ischium.
The bird-like body outline reconstruction in Fig. 1 confirms
existing skeleton and feather-based inferences and supports
EPB-based studies of leg and tail shape17,18. The drumstickshaped legs of Anchiornis (Fig. 1), and probably of most
theropods, are concordant with the relatively slender foot and
distal portion of the tibia and fibula as well as the broader
proximal portion of the latter bones and the robust femur. The
slender tail (Figs 1 and 4a) also fits the shallow and narrow caudal
centra and their shallow chevron depths. The observed leg and
tail outline are also in agreement with reconstructed theropod
musculature using fossil bones studied through an EPB-based
approach, validating this method. However, future studies will
benefit from the new data in helping to better constrain leg
muscles such as the M. fibularis longus and M. gastrocnemius
lateralis and tail muscles such as the M. transversospinalis and
M. ilio-ischio caudalis13,17–21 (Figs 1 and 4). Scales from the tibia
STM-114
STM-118
2 cm
3 cm
STM-144
10 cm
4 cm
STM-133
STM-144 cs
STM-147
2 cm
2 cm
STM-132
2 cm
2 cm
5 cm
Figure 1 | Reconstructed body outline of basal paravian Anchiornis using LSF images. Coloured areas represent different specimens and black ones are
approximated from equivocal data. Skeleton predominantly reconstructed from STM-118 and its scale is 5 cm. The inset specimen images have different
scales: in STM-127, 132, 147 and 144CS it is 2 cm, in STM-118 it is 3 cm, in STM-144 it is 4 cm and in STM-114 it is 10 cm. See Methods.
2
NATURE COMMUNICATIONS | 8:14576 | DOI: 10.1038/ncomms14576 | www.nature.com/naturecommunications
ARTICLE
NATURE COMMUNICATIONS | DOI: 10.1038/ncomms14576
a
Periligamentous
tissue
Skin
texture?
Propatagia
b
Periligamentous
tissue
Covert
feather
follicles
Propatagia
c
Periligamentous
tissue
Covert
feather
follicles
Propatagia
Figure 2 | Shallow propatagium of Anchiornis STM-0-127 at 95° of elbow
extension. Almost regularly spotted skin texture are covert feather follicles.
Scales are 1 cm. (a) White light image, (b) LSF image and (c) LSF image
with rank filter applied.
to the feet suggest that Anchiornis had podotheca like modern
birds15 and other tetanurans13,16 (Supplementary Fig. 3). The toe
pads in particular are of modern avian aspect (Figs 1 and 3).
Between the tail and legs, there is a potential cartilage-supported
pubic callosity that may have been suited for partially supporting
the animal as it rested on the ground (Fig. 4b). However, it could
simply indicate that the individual (STM-0-118) had yet to reach
maturity, although there are no clear indications of ontogenetic
stage elsewhere in the specimen.
Discussion
The Anchiornis propatagia observed in this study are the
first direct examples among four-winged dinosaurs (see
Supplementary Note 1 for a purported example in
Archaeopteryx22) and were associated with symmetrical
feathering in life3. They show shape discrepancies with the
halos preserved in the matrix around the bones, suggesting that
the latter should not be taken at face value as fossilized soft tissues
without complementary evidence such as preserved feathering
(Microraptor: Supplementary Figs 2 and 4; Fig. 2 of ref. 23).
Modern avian propatagia form the leading edge of the aerofoil
and help give it a cambered profile24. Propatagia make major
contributions to lift generation proximal to the wrist without
which birds cannot fly25. This function may have been possible in
Anchiornis given that we already know that the movement of
some four-winged dinosaurs through the air was limited by wing
area6, a property that propatagia help to increase. However, some
living flightless carinate birds have similar propatagial muscle
complexes to their volant relatives26. Propatagia also have a deep
non-flight-related non-avian theropod origin for example, those
in Caudipteryx (Fig. 4 of ref. 23; see Supplementary Note 1).
Specimens STM-0-114, 127 and 132 have the best preserved
propatagia and their shallow depth (1.2–1.5 cm) even at obtuse
elbow angles indicates that the arm was not nearly fully extended
when these individuals died. This implies that the propatagium
was kept taut either by a form of ligamentum propatagiale27,28
or by other portions of the propatagial muscle complex. The
propatagia also suggest that Anchiornis could produce a relatively
straight arm, a posture broadly found in many living gliding birds
(for example, comorants, albatrosses and pelicans). This indicates
a previously unknown aspect of arm morphology differentiation
at the earliest stages of paravian evolution (at least by the
Oxfordian stage of the Late Jurassic3) that may even have
been widespread. The aforementioned differentiation in arm
morphology among basal paravians implies functional diversity
that is in keeping with the diversity of arm feathers seen in
four-winged paravians: symmetrically vaned in Anchiornis3 and
asymmetrically vaned in Microraptor and Archaeopteryx5,9.
It also complements differences in the muscular control of
basal paravian arms as implied by the presumably weaker muscle
attachments to the non-ossified sterna of Anchiornis and
Archaeopteryx, and presumably stronger muscle attachments
to the ossified sterna of Microraptor10. The uncrossed and
skin-bound second and third manual digits of Anchiornis (Fig. 1,
Supplementary Fig. 5) formed a functionally didactyl hand, as in
Enantiornithes11. The latter trait presumably helped to stiffen
the postpatagium, but it is unclear whether it was present in
other four-winged dinosaurs too (for example, Microraptor:
Supplementary Fig. 4). A stiffer feathered postpatagium in
Anchiornis may have compensated for its aerodynamically
inferior arm feathers to some degree, providing another
example that basal paravians may have evolved multiple
solutions to similar locomotor needs and challenges. Improved
understanding of the interactions between functional parameters
is, therefore, a crucial step towards a more holistic understanding
of basal paravian function. However, it is clear that there was a
range of functional capabilities among basal paravian arms,
including those used for aerodynamic purposes.
The well-preserved propatagial surface of Anchiornis (Fig. 2)
shows the earliest known details of paravian covert feather
NATURE COMMUNICATIONS | 8:14576 | DOI: 10.1038/ncomms14576 | www.nature.com/naturecommunications
3
ARTICLE
NATURE COMMUNICATIONS | DOI: 10.1038/ncomms14576
Skin
texture?
Toepad
Toepad
Small,
rounded
reticulate
scales
Arthal-type
interpad
grooves
Toepad
Figure 3 | Plantar footpads of Anchiornis STM-0-147. These preserve reticulate scales and arthal-type interpad grooves. Scale is 1 cm. Inset images
of a footpad under white and laser light.
a
Adhesive
Adhesive
Caudal vertebrae
Proximal
tail outline
To tail tip
Middle
tail outline
b
Adhesive
To tail
base
Left
femur
Pubic
boot
Adhesive
Right
femur
Right
tibia
Pubic callosity
Leg outline
Cartilage
ia
Left tib
ula
Left fib
Leg
e
outlin
Figure 4 | Tail outline and outline of leg and pubic boot. (a) Tail outline of
STM-0-114. (b) Left leg and pubic boot outline of STM-0-118. The latter
forms a potential cartilage-supported (black band) callosity. Scales are 1 cm.
attachment and arrangement11,29. In Anchiornis, regularly-spaced
spots on the surface of the propatagium are interpreted as covert
feather follicles (Fig. 2). These are not arranged in tracts—unlike
modern birds—indicating little feather differentiation as seen in
its plumage3. These are not closely packed near the leading
edge of the wing which was covered in covert feathers that
were comparatively longer than those of most living birds
(Supplementary Fig. 5; ref. 13; Fig. 1 of ref. 24). However, the
diagonal orientation of these coverts (Fig. 1, Supplementary
Fig. 5) is shared with living birds24, indicating some degree of
4
leading edge camber in the wings of Anchiornis. This camber is
supported by the denser colouration of the propatagial leading
edge, a two-dimensional representation of the original threedimensional morphology30 (Fig. 2). Brown-coloured filamentous
structures associated with some of the feather follicles appear to
be fossilized in situ periligamentous tissue (Fig. 2). These
filaments suggest that these animals shared robust feather
attachments (Fig. 13 in ref. 24) with some Early Cretaceous
birds11,29 (and probably many feathered non-avian dinosaurs as
well). It is probable that other aspects of the modern avian dermal
system16 were already present in basal paravians, but this requires
further investigation. Current taxonomy refers Anchiornis to
basal Paraves2,3,8 and it has also been referred to Averaptora28.
Future soft tissue studies such as this one promise to further
refine our understanding of paravian patagial evolution.
The symmetry of the arm feathers and their regular, non-tractbased arrangement suggest that the arms were probably not used
in a comparably way to modern birds, despite striking similarities
in propatagium shape and camber. This suggests that
feathering—particularly its symmetry, size differentiation and
spatial arrangement—was highly significant towards how some
basal paravians utilized their arm (and likely leg and tail) function
for aerodynamic benefit.
Functional independence between the hind limb and tail of
living birds enables them to finely control their respective flight
surfaces and is the result of a continuous transition from hip to
knee-driven locomotion along the theropod lineage to birds17,18.
The new hind limb and tail outline results support the absence of
a large M. caudofemoralis in Anchiornis, as predicted by bone
morphology17,18. This indicates that Anchiornis had finer and
more independent control of its hind limb and tail (and the
feathers attached to them) compared with more basal
theropods17,18, although the detailed implications of these new
hind limb and tail constraints—particularly in comparing the
hind limb and tail function of basal paravians with that of
modern birds—requires future investigation using quantitative
biomechanical modelling.
The reconstructed body outline of Anchiornis is expected to be
similar to asymmetrically feathered basal paravians like Microraptor and Archaeopteryx based on their skeletal similarities.
This body outline study supports the modelled aerodynamic
performance of basal paravians4,6 and promises to reconstruct
even greater prowess in the future. This work, therefore, builds a
strong foundation for determining the aerodynamic capabilities
of Anchiornis be it ground-based or airborne3,7.
NATURE COMMUNICATIONS | 8:14576 | DOI: 10.1038/ncomms14576 | www.nature.com/naturecommunications
ARTICLE
NATURE COMMUNICATIONS | DOI: 10.1038/ncomms14576
Methods
Materials and taxonomy. The body outline in Fig. 1 and the other figures in the
manuscript show the details of nine basal paravian specimens (STM-0-7, 114, 118,
125, 127, 132, 133, 144 and 147) that can all be referred to Anchiornis. These
specimens are deposited in the Shandong Tianyu Museum of Nature in Pingyi,
China. Anchiornis has been referred to a basal bird2, a basal troodontid3,a basal
deinonychosaur8 or an averaptoran28 so in the absence of taxonomic consensus it
is referred more simply to a basal paravian in this study. Two diagnostic features of
Anchiornis huxleyi were included in the original description2 (IVPP V14378,
housed at the Institute of Vertebrate Paleontology and Paleoanthropology in
Beijing, China): extreme shortness of the ischium and a sculpturing pattern of
numerous small pits on the ventral surface of the coracoid. The ventral position of
the latter makes it a difficult feature to observe so it is no surprise that it has yet to
be confirmed in other Anchiornis specimens and in the nine aforementioned
specimens. An extremely short ischium is observed in STM-0-7, 118, 127 and 132,
but this character is not exposed in the other five specimens figured in the
manuscript. Unlike Xiaotingia, metacarpal III is thinner than metacarpal II in all of
the body outline specimens. Unlike Eosinopteryx, STM-0-114, 125 and 132 have
more than 23 caudal vertebrae, but this is uncertain in the six other figured
specimens. Unlike Aurornis, no evidence of an elongate metatarsal I is observed in
the body outline specimens, although in STM-0-133 the metatarsals are not well
exposed. The overall similarities in the exposed portions of all of the body outline
specimens indicate that these individuals can be referred to Anchiornis (for
example, a short deltopectoral crest, a straight ulna, and so on.); these characters
were also used to refer LPM-B00169 to this genus3 (housed at the Liaoning
Paleontological Museum in Shenyang, China).
LSF imaging protocol and theory. LSF images were collected using the protocol
of Kaye et al.1. Anchiornis specimens were imaged with 405 and 532 nm, 500 mw
lasers. An appropriate long pass blocking filter was used in front of the camera lens
to prevent image saturation by the laser. The laser was projected into a vertical line
by a Laserline Optics Canada lens, which was mechanically swept repeatedly over
the specimen during the photo’s time exposure in a dark room. The images were
post processed in Photoshop for sharpness, colour balance and saturation.
Fluorescence emanates from luminescent centres in the mineral lattice31.
The mineral lattice is not pure but incorporates organic and inorganic molecules
into the lattice at the time of formation32. The luminescent centre contains the
contaminating molecule in close association with the electron clouds of the
mineral31. Photons entering the lattice statistically transfer their energy to the
electron clouds and cause changes in electron excitation levels. The excited
vibrational energy states of the electrons then decay through multiple random
paths some of which emit photons while others do not. The excitation and decay
process is defined by ligand field theory which applies group theory and quantum
mechanics to electrostatic theory31. A full description of ligand field theory is
beyond the scope of this paper. Pertinent to fossil analysis, the contaminants of the
mineral structure are typically on a parts-per-million basis, which makes
fluorescence a sensitive analytical tool33. A colour change represents a different
electron decay process from a different atomic arrangement31. Due to the
complexity of the decay path, specific colours cannot be attributed to a particular
molecular arrangement just from an image31. However, differences in colours do
represent changes in the luminescent centre’s makeup. Additional complex
laboratory analysis can determine the nature of the luminescent centre which is the
target of further study.
Skeletal reconstruction. The skeletal reconstruction was illustrated in Adobe
Photoshop CC 2015. Individual bones were scaled from high-resolution photographs exhibiting minimal parallax using the Photoshop Ruler Tool. The virtual
scaling was set according to scale bars photographed in the same plane as the
specimens, using Photoshop’s Custom Scaling tool (Image -4 Analysis -4 Set
Measurement Scale). Bones were illustrated so that individual measurements end at
the edge of the white portion of the bone, as opposed to the middle or outside of
the black bounding line. The skeletal diagram is based primarily on STM-0-118.
Missing caudal elements were cross-scaled from STM-0-114. Major elements were
illustrated on separate layers to facilitate rotation and transformation into plausible
life positions. Presacral vertebrae provided the lengths and representative heights
of vertebral elements, but were not preserved with the lateral aspect visible in
sufficient quantities to determine the exact curvature of articulation in the neck and
back. Articulated and well-exposed presacral series of basal paravians (for example,
Jinfengopteryx) were used as supplementary guides for reconstructing vertebral
curvature in Anchiornis. Forelimb elements were articulated following the left
forelimb of STM-0-144, which is preserved with joint angles consistent with
contemporary biomechanics work. Hind limb elements of STM-0-118 and
STM-0–114 were preserved in articulation, and in good accordance with published
interpretations of theropod limb kinematics17,18, and were the basis for the pose
in Fig. 1.
Soft tissue reconstruction. Examples of soft-tissue preservation were inspected
for a lack of continuity and evidence of taphonomic distortion. To reduce
discrepancies between specimens of differing size, tissue depth was measured as a
percentage of bone width or length. Soft-tissue remains represented by multiple
specimens exhibiting similar depth and no signs of distortion were taken at face
value and reproduced directly in Fig. 1, including most distal limb elements. The
propatagium depth at the elbow varied in specimens based on the angle of the
elbow, a condition also seen in extant birds24,25, so the depth reconstructed in
Fig. 1 was matched to specimens of similar degrees of elbow flexion. Soft-tissue
elements that showed some degree of distortion were used as a qualitative guide for
reconstructing the remaining soft-tissue silhouette (represented in black in Fig. 1),
and other portions were based on dissections of birds and published theropod
myology13,20. We assigned anatomical terms of soft tissues based on the
morphology we observed, in accordance with traditional morphological
interpretations of vertebrate fossils (for example, bones, scales, feathers,
propatagium).
Data availability. The data that support the findings of this study are available
from the corresponding author upon reasonable request. The data reported in this
paper are detailed in the main text and in the Supplementary Information.
References
1. Kaye, T. G. et al. Laser-stimulated fluorescence in paleontology. PLoS ONE 10,
e0125923 (2015).
2. Xu, X. et al. A new feathered maniraptoran dinosaur fossil that fills a
morphological gap in avian origin. Chin. Sci. Bull 54, 430–435 (2009).
3. Hu, D. Y., Hou, L. H., Zhang, L. J. & Xu, X. A pre-Archaeopteryx troodontid
theropod from China with long feathers on the metatarsus. Nature 461,
640–643 (2009).
4. Xu, X. et al. An integrative approach to understanding bird origins. Science 346,
12532931–12532939 (2014).
5. Xu, X. et al. Four-winged dinosaurs from China. Nature 421, 335–340 (2003).
6. Palmer, C. The aerodynamics of gliding flight and its application to the arboreal
flight of the Chinese feathered dinosaur Microraptor. Biol. J. Linn. Soc. 113,
828–835 (2014).
7. Heers, A. M., Dial, K. P. & Tobalske, B. W. From baby birds to feathered
dinosaurs: incipient wings and the evolution of flight. Paleobiology 40, 459–476
(2014).
8. Xu, X., You, H. L., Du, K. & Han, F. L. An Archaeopteryx-like theropod from
China and the origin of Avialae. Nature 475, 465–470 (2011).
9. Foth, C., Tischlinger, H. & Rauhut, O. W. M. New specimen of Archaeopteryx
provides insights into the evolution of pennaceous feathers. Nature 511, 79–82
(2014).
10. Zheng, X. T. et al. On the absence of sternal elements in Anchiornis (Paraves)
and Sapeornis (Aves) and the complex early evolution of the avian sternum.
Proc. Natl Acad. Sci. 111, 13900–13905 (2014).
11. Navalón, G., Marugán-Lobón, J., Chiappe, L. M., Sanz, J. L. & Buscalioni, Á. D.
Soft-tissue and dermal arrangement in the wing of an Early Cretaceous bird:
Implications for the evolution of avian flight. Sci. Rep. 5, 14864 (2015).
12. Zhou, Z. H., Wang, X. L., Zhang, F. C. & Xu, X. Important features of
Caudipteryx—evidence from two nearly complete new specimens. Vertebrat.
PalAsiatic. 38, 241–254 (2000).
13. Baumel, J. J. in Handbook of avian anatomy: nomina anatomica avium.
Vol. 23, 777 (Nuttall Ornithological Club, 1993).
14. Pu, H. Y. et al. A new juvenile specimen of Sapeornis (Pygostylia: Aves) from
the lower cretaceous of Northeast China and allometric scaling of this basal
bird. Paleontol. Res. 17, 27–38 (2013).
15. Cuesta, E., Dı́az-Martı́nez, I., Ortega, F. & Sanz, J. L. Did all theropods have
chicken-like feet? First evidence of a non-avian dinosaur podotheca. Cretaceous
Res. 56, 53–59 (2015).
16. Stettenheim, P. R. The integumentary morphology of modern birds—an
overview. Am. Zool. 40, 461–477 (2000).
17. Hutchinson, J. R. & Allen, V. The evolutionary continuum of limb function
from early theropods to birds. Naturwissenschaften 96, 423–448 (2009).
18. Gatesy, S. M. in Mesozoic Birds: Above the Heads of Dinosaurs (eds Chiappe, L. M.
& Witmer, L. M.) 432–447 (University of Berkeley Press, 2002).
19. Carrano, M. T. & Hutchinson, J. R. Pelvic and hindlimb musculature of
Tyrannosaurus rex (Dinosauria: Theropoda). J. Morphol. 253, 207–228 (2002).
20. Hutchinson, J. R., Bates, K. T. & Allen, V. Tyrannosaurus rex redux:
Tyrannosaurus tail portrayals. Anat. Rec. 294, 756–758 (2011).
21. Persons, W. S. & Currie, P. J. The tail of Tyrannosaurus: reassessing the size
and locomotive importance of the M. caudofemoralis in non-avian theropods.
Anat. Rec. 294, 119–131 (2011).
22. Martin, L. D. & Lim, J. D. Soft body impression of the hand of Archaeopteryx.
Curr. Sci. 89, 1089–1090 (2005).
23. Feduccia, A. & Czerkas, S. A. Testing the neoflightless hypothesis: propatagium
reveals flying ancestry of oviraptorosaurs. J. Ornithol. 156, 1067–1074 (2015).
24. Brown, R. E., Baumel, J. J. & Klemm, R. D. Anatomy of the propatagium—the
great horned owl (Bubo virginanus). J. Morphol. 219, 205–224 (1994).
25. Brown, R. E. & Cogley, A. C. Contributions of the propatagium to avian flight.
J. Exp. Zool. 276, 112–124 (1996).
NATURE COMMUNICATIONS | 8:14576 | DOI: 10.1038/ncomms14576 | www.nature.com/naturecommunications
5
ARTICLE
NATURE COMMUNICATIONS | DOI: 10.1038/ncomms14576
26. McGowan, C. The wing musculature of the Weka (Gallirallus australis) a
flightless rail endemic to New Zealand. J. Zool. 210, 305–346 (1986).
27. Chiappe, L. M. & Lacasa-Ruiz, J. in Mesozoic Birds: Above the Heads of
Dinosaurs (eds Chiappe, L. M. & Witmer, L.) 230–239 (University of California
Press, 2002).
28. Agnolı́n, F. L. & Novas, F. E. Avian Ancestors: a Review of the Phylogenetic
Relationships of the Theropods Unenlagiidae, Microraptoria, Anchiornis and
Scansoriopterygidae (Springer, 2013).
29. Xing, L. D. et al. Mummified precocial bird wings in mid-Cretaceous Burmese
amber. Nat. Commun. 7, 12089 (2016).
30. Briggs, D. E. G. & Williams, S. H. The restoration of flattened fossils. Lethaia
14, 157–164 (1981).
31. Gaft, M., Reisfeld, R. & Panczer, G. Modern Luminescence Spectroscopy of
Minerals and Materials (Springer Berlin Heidelberg, 2005).
32. Shopov, Y. Y., Ford, D. C. & Schwarcz, H. P. Luminescent microbanding in
speleothems: high-resolution chronology and paleoclimate. Geology 22,
407–410 (1994).
33. Deneufville, J. P., Kasdan, A. & Chimenti, R. J. Selective detection of uranium
by laser-induced fluorescence: a potential remote-sensing technique. 1: optical
characteristics of uranyl geologic targets. Appl. Opt. 20, 1279–1296 (1981).
Acknowledgements
This study was supported by the Dr Stephen S.F. Hui Trust Fund (201403173007), the
Research Grant Council of Hong Kong’s General Research Fund (17103315), The Faculty
of Science of the University of Hong Kong and the National Science Foundation of China
(41688103, 41372014 and 41472023). Rui Pei is thanked for discussions about
Supplementary Table 1.
6
Author contributions
X.W., M.P., X.Z., T.G.K., A.R.F. and X.X. designed the project. All authors performed the
research. M.P., T.G.K., X.W. and X.X. wrote the manuscript.
Additional information
Supplementary Information accompanies this paper at http://www.nature.com/
naturecommunications
Competing financial interests: The authors declare no competing financial interests.
Reprints and permission information is available online at http://npg.nature.com/
reprintsandpermissions/
How to cite this article: Wang, X. et al. Basal paravian functional anatomy illuminated
by high-detail body outline. Nat. Commun. 8, 14576 doi: 10.1038/ncomms14576 (2017).
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in
published maps and institutional affiliations.
This work is licensed under a Creative Commons Attribution 4.0
International License. The images or other third party material in this
article are included in the article’s Creative Commons license, unless indicated otherwise
in the credit line; if the material is not included under the Creative Commons license,
users will need to obtain permission from the license holder to reproduce the material.
To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/
r The Author(s) 2017
NATURE COMMUNICATIONS | 8:14576 | DOI: 10.1038/ncomms14576 | www.nature.com/naturecommunications