ISSN 00310301, Paleontological Journal, 2010, Vol. 44, No. 12, pp. 15701588. Pleiades Publishing, Ltd.

, 2010
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INTRODUCTION
The first hypotheses for the origin of flight in birds,
which were formulated just after the discovery of
Archaeopteryx in the mid19th century, were diametri
cally opposite. The major alternatives were the
hypothesis of arboreal or trees down (Marsh, 1877) and
the hypothesis of cursorial or ground up development
of avian flight (Williston, 1879). According to the
arboreal hypothesis, birds evolved from thecodonts
(Seeley, 1866; Broom, 1913; Heilmann, 1926), while
the cursorial hypothesis implied that they evolved
from running theropod dinosaurs (Huxley, 1868;
Gegenbaur, 1878; Osborn, 1900). In the last in his life
time edition of The Origin of Species, Darwin (1872)
noted that Archaeopteryx is a strange bird, with a long
tail, as in lizards, each vertebra of which had a pair of
feathers, and wings, which had two free claws each; in
addition, he in general adhered to the idea that birds
descended from dinosaurs.
Birds are unique among terrestrial vertebrates in
the functioning of the locomotor system, with their
forelimbs adapted for flight and hind limbs adapted for
movement on land and water. In fact, the two systems
are adapted for movements in essentially different
environments. In the evolution of birds, the formation
of the system of air locomotion with the use of the
forelimbs and the evolution of their pelvic girdle and
hind limbs were tightly connected and correlated.
BRIEF REVIEW OF CONCEPTS
OF THE ORIGIN OF AVIAN FLIGHT
The problems of the origin of flight and the origin
of birds are fundamentally connected. All concepts of
the origin of flight have been reviewed in detail by
Shipman (1998) and Paul (2002). At present, two
major hypotheses of the origin of birds are discussed,
i.e., they evolved from either Triassic archosauromor
phs through Archaeopteryx or Jurassic theropod dino
saurs, also through Archaeopteryx. According to the
arboreal hypothesis, archosauromorph ancestors of
birds climbed trees, embracing the stem and branches
by the clawed manus, and descended by gliding and,
subsequently, turned from gliding to flapping flight
(Bock, 1965, 1986; Tarsitano and Hecht, 1980;
Feduccia, 1999; Martin, 2004, 2008). According to
the other variant of the arboreal hypothesis, avian
flight evolved through gliding of dromaeosaurids,
which climbed trees (Chatterjee, 1997b, 1999; Chat
terjee and Templin, 2007).
The dinosaurian hypothesis, which is supported by
many researchers and widely popularized by mass
Origin of Feathered Flight
E. N. Kurochkin
a
and I. A. Bogdanovich
b
a
Borissiak Paleontological Institute, Russian Academy of Sciences, Profsoyuznaya ul. 123, Moscow, 117997 Russia
email: enkur@paleo.ru
b
Schmalhausen Institute of Zoology, National Academy of Sciences of Ukraine,
ul. Bogdana Khmelnitskogo 15, Kiev, 01601 Ukraine
email: ibogdanovich@rambler.ru
Received March 15, 2010
AbstractThe origin of flight in birds and theropod dinosaurs is a manysided and debatable problem. We
develop a new approach to the resolution of this problem, combining terrestrial and arboreal hypotheses of
the origin of flight. The bipedalism was a key adaptation for the development of flight in both birds and thero
pods. The bipedalism dismissed the forelimbs from the supporting function and promoted transformation
into wings. For the development of true flapping avian flight, a key role was played by the initial universal ani
sodactylous foot of birds. This foot pattern provided a firm support on both land and trees. Theropod dino
saurs, archaeopteryxes, and some other early feathered creatures had a pamprodactylous foot and, hence,
they developed only gliding descent. Early birds descended by flattering parachuting with the use of incipient
wings; this gave rise to true flight. Among terrestrial vertebrates, only bats, pterosaurians, and birds developed
true flapping flight, although they followed different morphofunctional pathways when solving this task.
However, it remains uncertain what initiated the adaptation of the three groups for the air locomotion. Nev
ertheless, the past decade has provided unexpectedly abundant paleontological data, which facilitate the res
olution of this question with reference to birds.
Keywords: Aves, Enantiornithes, Archaeopteryx, Theropoda, Ornithurae, Mesozoic, origin of flight.
DOI: 10.1134/S0031030110120129
PALEONTOLOGICAL JOURNAL Vol. 44 No. 12 2010
ORIGIN OF FEATHERED FLIGHT 1571
media, has occupied a leading position and often
seems to provide a conclusive resolution of the prob
lem. Within the framework of this hypothesis, birds
acquired the flight through rapid running of terrestrial
theropods (Fig. 1), then, jumping and gliding, which
eventually resulted in the flight (Ostrom, 1976, 1979,
1997; Caple et al., 1983; Mller and Streicher, 1989;
Padian and Chiappe, 1998b) (Fig. 1).
A peculiar variant of the terrestrial hypothesis was
developed by Dial (2003b; Dial et al., 2008). As he
watched the rock partridge (Alectoris graeca) climbing
an inclined plane, he indicated that, as the angle of
inclination increased, the birds began flapping wings
and, as a result, moved successfully upwards even
when the plane was almost vertical. This was particu
larly typical of nestlings, which were virtually incapa
ble of flying. Similarly, the ancestors of birds could
have run on slopes by propulsion of movement using
flaps of the forelimbs, which subsequently trans
formed into wings equipped with the plumage. When
descending, rudimentary wings and hind limbs of
nestlings actively and synchronously worked, presum
ably as in remote ancestors of flying birds. This
hypothesis was named the hypothesis of the ontoge
netictransitional wing (OTW). This version of the
development of flight corresponds to a certain extent
to our reasoning developed below.
Biomechanical studies of the origin of flight based
on the study of Archaeopteryx, either reject the possi
bility of flight from the ground and at run (Rayner,
1985; OFarell et al., 2002; Norberg, 2004) or substan
tiate the origin of flight just in such a way (Caple et al.,
1983; Shipman, 1998; Burgers and Chiappe, 1999).
Garner et al. (1999) rejected both terrestrial (from
running) and arboreal hypotheses of the development
of flight. They proposed an alternative hypothesis of
pouncing proavis. This model implies that the flight
developed in predatory ancestors of birds and evolved
from pouncing on prey from an eminence or ambush.
In attacking proavises, the control of body movements
was improved as the distal part of the forelimbs and the
tail acquired simple feathers with bilaterally symmet
rical vanes. During subsequent evolution, natural
selection probably supported remiges with an aerody
namic structure producing lifting force. In this
hypothesis, a new approach to the analysis of the prob
lem of the origin of flight is applied, the initial adapta
tion for which is considered to be the ability of bipedal
ancestors of proavis to get on certain elevations and
pouncing on prey from above.
Peters (2002) proposed that climbing adaptations
of the forelimbs are incompatible with flying and
developed a variant of the terrestrial hypothesis of the
origin of flight through gliding jumps from an elevated
point (such as cliffs or steep slopes), with subsequent
flight. In his opinion, the climbing ability gave nothing
for the initiation of flight, while typical features of
avian anatomy, such as the reduction of teeth and
claws of fingers, horny beak, pygostyle, reduced fibula,
and secondary loss of flight repeatedly disappeared
and appeared in the evolution of birds (Peters, 2000).
All variants of the arboreal hypothesis coincide in
two conclusions, the presence of a gliding stage before
flapping flight and the recognition of Late Jurassic
Archaeopteryx from localities of Bavaria as the ances
tor of all later birds.
A novel hypothesis for the origin of avian flight was
developed by Thulborn and Hamley (1985) and
Loparev (1996) based on the analysis of the pelvic
structure of dinosaurs and birds and ontogeny of living
birds. According to this hypothesis, early birds devel
oped flight in shallow nearshore biotopes with thickets
Running with help of wings
Horizontal takeoff
Vertical
Aves
Maniraptora
takeoff
running with help of wings
Fig. 1. Stages of the development of avian flight according to the terrestrial hypothesis (reprinted from Chiappe, 2007, with
authors permission).
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KUROCHKIN, BOGDANOVICH
of emergent vegetation. When searching for food in
these biotopes, they spread widely the forelimbs to
form a shadow; as a result, the primary plumage trans
formed into wide flight feathers. When escaping from
predators, they ran on the water surface, using flap
ping movements of the forelimbs; having reached
thickets, they hid behind them. When moving in
thickets, the digits of the forelimbs equipped with
claws were used. This locomotion evolved in gliding
and, subsequently, flight above the water, which was
provided by the development of feathers on the fore
limbs; eventually, they acquired the cruising flight. It
should be noted that a similar hypothesis of the
appearance of Protoavis and avian plumage under
nearshore conditions was previously proposed by
LacasaRuiz (1993). Independently of these authors,
Saveliev (2005) developed the hypothesis for the origin
of birds and avian flight in nearshore habitats, based
on the supposition that the ancestors of birds could
have consumed rich aquatic food resources, run in
shallow water biotopes, and swum underwater using
the forelimbs; this provided special changes in the
central nervous system.
We have developed a compromise hypothesis of ter
restrialarboreal origin of flight, which is supported by
systemic changes in the locomotor apparatus of the
fore and hind limbs and plumage in the evolution of
archosauromorphs and early feathered reptiles and
based on morphofunctional analysis of the muscu
loskeletal system of living birds (Kurochkin and
Bogdanovich, 2008a, 2008b) and on the study of new
records of the earliest birds and feathered theropod
dinosaurs.
HIND LIMBS
Obligatory bipedal locomotion on land, with sup
porting digits of hind limbs, was acquired even by
ancestors of theropods and birds (Gauthier, 1986).
However, the bipedal patterns of theropods and living
birds differ essentially (Bogdanovich, 2004; Hutchin
son and Allen, 2009). As a bird walks, the femur
remains almost immobile, and the step length is deter
mined by the amplitude of movements of the tibia and
tarsometatarsus. In theropods, the step length is deter
mined by movements of all three segments of the hind
limb (femur + tibia + metatarsus); however, the step
length is approximately the same as in birds (Jones et
al., 2000). These differences in locomotion suggest
very early and independent divergence of birds and
theropods at the level of archosauromorphs (Jones et
al., 2000). The combination of cursorial features and
long heavy tail in bipedal theropods and a number of
ornithischians has attracted considerable interest
(Coombs, 1978). The balancing function of the tail
was understood rather early, for example, by Nopsca
(1907) and became generally accepted. Certainly, a
heavy tail counterbalanced the anterior part of the
inclined trunk of running bipedal animals (Fig. 2).
A probable reason for the development of bipedal
ism and standing posture was the necessity for
decreasing the load on the femoral curve, as the body
weight increased in some early archosauromorphs,
which became larger (Kubo and Benton, 2007). Tran
sition to facultative bipedalism in lizards is considered
to correlate with prevalence of the support on hind
limbs at an accelerated trot, as short forelegs could not
keep up with hind legs (Sukhanov, 1968). In addition,
it should be noted that, in lizards, with their sprawling
limbs, an increase in efficiency of bipedal running is
Fig. 2. A bipedal archosauromorph, ancestor of ornithuromorph birds; reconstructed by E. Kurochkin, drawn by O. Orekhova
Sokolova.
PALEONTOLOGICAL JOURNAL Vol. 44 No. 12 2010
ORIGIN OF FEATHERED FLIGHT 1573
probably connected with the absence of trunk undula
tion, which accompanies a quadrupedal locomotion.
In contrast to lizards, the limbs of progressive thec
odonts and early theropods were not spread apart, but
were positioned in an almost parasagittal plane (Sen
nikov, 1989; Carrano, 2000), with a constant bipedal
ism in some of them. Under these conditions, transi
tion to bipedalism does not provide an advantage. In
addition, it is difficult to imagine a relatively rapid and
maneuverable bipedal running combined with the
presence of a long heavy tail, since the muscular
energy expended for the maintenance of statodynamic
balance increases considerably under these condi
tions. Among terrestrial vertebrates which have devel
oped bipedal locomotion, a long and heavy tail is only
retained in lizards, some archosauromorphs (Ornitho
suchidae), crocodilomorphs (Sphenosuchidae), many
dinosaurs, and early birdlike feathered creatures.
Doubt about rapid running of large dinosaurs is based
on the study of theropod tracks and biomechanical
analysis (Farlow et al., 2000; Hutchinson and Gatesy,
2006; Hutchinson and Allen, 2009). These data sug
gest that they usually walked, while rapider gaits were
infrequent.
The bipedalism with a parasagittal position of hind
limbs, which dismissed the forelimbs from supporting
function and promoted the development of jumping
locomotion (Caple et al., 1983; Nessov and Yarkov,
1989), is regarded as the primary key adaptation for
specialized air locomotion of birds (Gatesy and Dial,
1996b). In the MiddleLate Triassic, when theropods
and birds probably appeared (Kurochkin, 2006a), all
land masses were united in a single continent (Pan
gea), with humid biotopes and extensive vegetation at
the periphery and open arid, and even superarid,
deserted landscapes in the depth of this huge continent
(Yasamanov, 1985; Golonka, 2000). Under conditions
of extensive dry and open landscapes (Irisov, 1992) and
thin xerophytic forests (Nessov and Yarkov, 1989), as
the authors cited believe, bipedal ancestors of birds
emerged. Certainly, it is highly probable that bipedal
locomotion was formed in open landscapes, which
required rapid running over long distances, with min
imized energy costs. However, available estimates sug
gest that bipedalism is as good as quadrupedal loco
motion with reference to energy economy (Schmidt
Nielsen, 1984). It is more important that bipedalism
dismissed the forelimbs from supporting function,
providing them with other functions. Another prereq
uisite for the use of hind limbs as the major support was
possibly a high position of the head, which was
required for better orientation in dense high plants. All
the above and the reasoning set forth below almost
equally concern the ancestors of true birds and the first
theropod dinosaurs, since, in our opinion, in contrast
to the alternative points of view (Chiappe, 2002), basal
birds and theropods from the very beginning of the
appearance of bipedal forms and, then, evolved for a
long time in parallel under the same landscape condi
tions (Kurochkin, 2006b). At the same time, structural
features of the forearm phalanges, humerus, and pha
langes of toes strongly suggest that birds (Aves) and
winged dromaeosaurid (Microraptor) independently
developed flight and arboreal mode of life (Senter
et al., 2004).
TRANSFORMATION
OF THE FORELIMBS INTO WINGS
The fact that the forelimbs were dismissed from the
supporting function was attributed to various func
tional reasons. They participated to a greater or lesser
extent in manipulative function, although some fea
tures, such as the reduction of digits IV and V and their
metacarpals and the other digits tightly adjoining each
other, are in contrast with the manipulative function of
the manus. Ostrom (1976) hypothesized that the fore
limbs of terrestrial ancestors of birds and theropods
were used as a net for catching insects, as they brought
together their forelimbs covered with featherlike
structures. However, it is hardly possible to capture
prey using such a net, since it would be pushed out by
the air flow as the two planes of the forelimbs were
brought together. Note that later Ostrom (1997) aban
doned this theory.
Martin (1983) provided cogent arguments against
this point of view and proposed that the locomotor
system of ancestors of birds was divided into two
essentially different parts because of adaptation to
movements in trees by leaping and clinging. Referring
to the example of arboreal primates, Martin proposed
that this specialization explained the combination in
Archaeopteryx of arboreal lifestyle with the develop
ment of fused tarsals and elongated tibiotarsus, which
are usually regarded as adaptations for running. Even
if the features indicated are attributable to such a spe
cialization, the adaptation of the forelimbs for climb
ing trees (embracing stems and branches by the
manus) is difficult to propose as a preadaptation to the
formation of wings (Peters, 2002), as is usually
accepted by the proponents of the arboreal origin of
avian flight. Arboreal vertebrates usually develop a
grasping limb, with two foot digits, or only the first,
opposed to the others, with forearm digits and the
entire manus elongated mostly by their phalanges and
strengthening of the flexors of the shoulder and elbow
joints (Kovtun, 1984). A variant of this limb type is
observed in arboreal Triassic Megalancosaurus
(Renesto, 1994). As a pentadactyl plantigrade limb
was initial to archosauromorph ancestors of reptiles
and birds and it changed because of similar functional
causes (in this case, in mammals and birds), it is pos
sible to propose basically parallel development of the
morphotype of arboreal limbs in these groups.
We propose different trends in the transformation
of the forelimb into avian wing. Protoavis (P. texensis)
from the Late Triassic of the United States (Chatter
jee, 1991, 1999) provides a notable example of a tran
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KUROCHKIN, BOGDANOVICH
sitional condition. Note that flapping directional flight
requires not only long remiges with suitable aerody
namic structure. A downward stroke must be followed
by an upward movement of the wing to a position at
least slightly higher than the dorsum. This is only pos
sible in the condition of appropriate orientation of the
glenoid of the scapulocoracoid articulation at the
point of articulation with the humerus. In Archaeop
teryx and even Confuciusornis, the glenoid is oriented
such that it was impossible to raise the wing above the
dorsum (Senter, 2006). However, judging from the
structure of the scapulocoracoid articulation, Pro
toavis was able to raise the wing above the dorsum
(original data), although we believe it could not fly
(Kurochkin, 1995, 2001). In the manus of Protoavis, the
number of digits is reduced to three, metacarpals III and
IV show initial fusion, and the carpals are partially
fused with the metacarpals (Fig. 3). Flexion and
extension in the carpometacarpal articulation of Pro
toavis occurred in the plane of the manus. The forma
tion of these structural features of the manus could not
be connected with the presence of an arboreal (climb
ing) stage of the limb, although Chatterjee (1999) pro
posed just this stage of climbing tree stems in manirap
torans, with the use of lengthened forelimbs and a firm
tail as a support.
The character of articulation between the coracoid
and scapula of Protoavis suggests the presence of the
supracoracoid muscle (Chatterjee, 1995, 1999; Kuro
chkin, 1995, 2001), which is usually regarded as a leva
tor of the forelimb. However, experimental and elec
tromyographic studies have shown that the basic func
tion of the supracoracoid muscle is rapid supination of
the humerus and the entire wing at the initial phase of
raising the wing (Ostrom, 1997; Ostrom et al., 1999).
ANISODACTYLOUS FOOT AND TAIL
The development of bipedal locomotion was
accompanied by the change in the body posture,
reduction of the forelimbs, and caudal shift of the cen
ter of gravity of the body. Apparently, under these con
ditions, the heavy, rigid tail initially performed both
the primary balancing function and the function of a
facultative support. This facilitated considerably the
maintenance of equilibrium, as the body acquired a
vertical position, with the anteriorly directed digits,
leaning on the ground, combined with the general
lengthening of the hind limb and partial reduction of
digits.
We believe that further progress directed to orni
thuromorph birds was connected with the improve
ment of the supporting function of the foot by the
development of anisodactyly, with three digits directed
anteriorly and the first (internal) digit directed strictly
posteriorly because of articulation with rudimentary
metatarsal I on its plantar (ventral) side (Bogdanovich,
2000). The anisodactylous foot type is probably ances
tral to the class Aves (Raikow, 1985; Zinoviev, 2008).
The data on Protoavis definitely corroborate this evo
lutionary scenario. The foot of this animal has a well
developed first digit, which is positioned opposite to
and at the same level as three anterior digits (Fig. 3).
Hence, the anisodactyly is already characteristic of the
grade of Protoavis. This is an essential character, since
the opposition of digit I at the initial stage of bipedal
locomotion increased the static stability of animal and
relieved the tail, providing the opportunity to reduce
it. The reduction of the tail (an unnecessary counter
balance in cursorial ancestors of birds, which inhab
ited mountain slopes) was supported by Irisov (1992),
although he did not provide detailed substantiated.
Dementiev (1940) indicated that the hind limb of
birds, with the initially anisodactylous foot, is in gen
eral better adapted for walking than for climbing.
However, the opposed position of even one welldevel
oped digit provides a clasping function of such a limb.
In general, the anisodactyly was probably the initial
pattern in the class Aves, which allowed simultaneous
bending of anterior digits and hallux (posterior digit),
providing adaptation to both embracing branches and
walking and running (Raikow, 1985; Zinoviev, 2008).
Living birds with the primary anisodactylous foot can
easily move on both land and branches. Thus, such a
foot shows certain functional universalism, which
could have given rise to all other types of avian foot.
In general, the majority of archosauromorphs, as
many tetrapods, have a pentadactyl foot, with five dig
its directed anteriorly; in the former, digit V is only
partially reduced (Ostrom, 1976). Further reduction
of foot digits in the course of improvement of terres
trial locomotion, which was connected with transition
from plantigrade to digitigrade limb (Severtsov, 1939),
is possible to trace using ornithopod and theropod
dinosaurs as an example. They developed a tetradactyl
tdIV
rad
II
IV
III
I
uln
II
IV
III
(a) (b)
cd2
cd3
Fig. 3. Protoavis texensis Chatterjee, 1991 (after Chatter
jee, 1995, modified): (a) manus and (b) foot. Designations:
(cd2) and (cd3) carpalia distalia 2 and 3, (rad) radiale,
(uln) ulnare, (tdIV) tarsale distale IV, and (IIV) digits.
PALEONTOLOGICAL JOURNAL Vol. 44 No. 12 2010
ORIGIN OF FEATHERED FLIGHT 1575
foot, with the medially projecting first digit. This foot
type is termed pamprodactylous (Bock and Miller,
1959; Zinoviev, 2008). In theropods, it allowed the
adaptation of the foot for rapid terrestrial locomotion.
However, it did not provide firm support on a perch
(tree branches), as they adapted to the overground lay
ers of plants.
All proponents of the arboreal hypothesis for the
origin of avian flight believe that, as proavis climbed
up vertical tree stems, it embraced them by the fore
limbs. In our opinion, this assumption is a simple fal
lacy, since the external orientation of the claw curva
ture in Archaeopteryx and other early birdlike feath
ered creatures, such as Jeholornis, along with
theropods, prevented setting on vertical stems. In
addition, the character of Triassic and Jurassic trees
precluded free upward movements along their stems.
The only way up was leaping on lower branches of trees
and subsequent upward jumps or movements by grasp
ing one branch after another. Thus, the hypothetical
proavis could leap onto the lower branches of trees
from the ground, as is observed in the most primitive
galliform curassow (up to 1.5 m without flying) (Bent,
1932) and many other representatives of this general
ized order, such as turkey, guineafowl, pheasants, and
wild hens (original observations), as they get onto trees
for overnight rest. It should be noted that leaps onto
trees or other eminences were repeatedly considered
5 cm
Fig. 4. Skeleton of the ornithuromorph Yixianornis grabaui Zhou et Zhang, 2001 from the Lower Cretaceous of China, with com
pletely opposed first digit of the foot and small pygostyle (indicated by arrows); photograph by E. Kurochkin.
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KUROCHKIN, BOGDANOVICH
as a step in the development of flight (Dementiev,
1940; Nessov and Yarkov, 1989; Cowen and Lipps,
1982; Caple et al., 1983); however, the initial aniso
dactyly has not been mentioned.
The anisodactylous foot, with simultaneously bend
ing three anterior and one posterior (hallux) digits pro
vided ancestors of birds with firm setting and equilibra
tion on tree branches. Theropods and their feathered
descendants with a pamprodactylous foot lacked a firm
seat on branches. By analogy with nestlings of living
birds, it is reasonable to assume that, in ancestors of
birds (or early birds), jumps on branches and, particu
larly, downward jumps were accompanied by synchro
nous flapping and flattering (as termed by Longrich,
2006) movements of the forelimbs, which were
intended to maintain equilibrium. When descending,
feathered theropods and Archaeopteryx used flatter glid
ing, which resulted in the formation of true flight, as
Long et al. (2003) concluded. Possibly, the distal seg
ments of the forelimbs of ancestors of birds were cov
I
II
III
IV
I
II
III
Fig. 5. Archaeopteryx grandis Elzanowski, 2001, Solnhofen (sixth) specimen, skeleton; arrows indicate claws of wing digits curved
externally and foot digit I oriented medially; Roman figures designate digits of the fore and hind limbs; photograph by E.N. Kuro
chkin.
PALEONTOLOGICAL JOURNAL Vol. 44 No. 12 2010
ORIGIN OF FEATHERED FLIGHT 1577
ered with lengthened contour feathers, which were used
in display behavior, similar to that of Caudipteryx or
Protarchaeopteryx from the Early Cretaceous of China
(Ji et al., 1998, 2001).
Consequently, the anisodactylous foot had a signif
icant effect on the trend of subsequent evolution of
bipedal ancestors of true birds and birds themselves.
This exaptation provided firm movements on land and
stable position on tree branches without the use of the
long tail formed of many vertebrae as a counterbal
ance. The following paleontological data verify this
hypothesis. In the Early Cretaceous Chinese ornithu
rines Yixianornis, Archaeorhynchus, Hongshanornis,
Jianchangornis, and Gansus, the caudal region is
formed of 57 short free vertebrae and a short
mediolaterally flattened pygostyle, while digit I of the
foot is distinctly opposed to the others (Fig. 4), so that
the first metatarsal comes onto the plantar side of the
tarsometatarsus (Gansus, Liaoningornis, Yanornis,
Yixianornis) (Hou and Liu, 1984; Hou, 1997; Zhou
and Zhang, 2001, 2005, 2006; Clarke et al., 2006; You
et al., 2006). Note that fossil tracks from Argentina
determined as Late Triassic birdlike footprints (Mel
hor et al., 2002) were produced by a completely aniso
dactylous foot. Yixianornis is so far the only Early Cre
taceous ornithuromorph that retains a relatively short
fanshaped tail, which was positioned on a flattened
pegshaped pygostyle (Clarke et al., 2006).
Theropods, archaeopteryxes, and enantiornithines
followed different pathways in the evolution of the
hind limb and tail. In particular, in dromaeosaurids,
digit I is not opposed to other digits, it is only slightly
displaced medially and lifted proximally (Norell and
Makovicky, 1997). In gliding Microraptor gui, digit I of
the foot is not opposed (Xu et al., 2003; original data).
In the new Late Jurassic fourwinged troodontid
Anchiornis huxleyi, the same condition of digit I is also
evident (Xu et al., 2009). There is no doubt that dro
maeosaurids and troodontids from the Upper Jurassic
and Lower Cretaceous of China were fourwinged
and displayed certain anatomical features, since sev
eral hundred fossil specimens have been recorded
(Alexander et al., 2010).
It is generally accepted that, in Archaeopteryx, digit
I was opposed to other digits of the foot (Feduccia,
1999; Feduccia et al., 2007). In fact, Archaeopteryx
shows incomplete opposition of digit I (Fig. 5). The
first metatarsal is located on the medial surface of the
second metatarsal; therefore, digit I is directed medi
ally; it could be abducted only slightly posteriorly
(Mayr et al., 2005; original data). Therefore, feathered
theropods, Archaeopteryx, and early birdlike taxa,
such as Zhongornis, Jinfengopteryx, and Jeholornis,
could not get rid of their long tail, since it was a coun
terbalance, as they leant on three anterior digits of the
foot, which provided insufficiently stable support on
both land and trees. The long digits with large curved
claws were probably preserved in the forelimbs of these
animals because of the same reason and were used for
clutching at branches, as they moved in trees (Fig. 6).
The short proximal and lengthened distal phalan
ges of wing digits (Zhou and Farlow, 2001) and exter
nal curvature of claws of Confuciusornis (as in Archae
opteryx) are poorly adapted for climbing vertical
stems, embraced by the forelimbs (Fig. 6). In addition,
the short and proximally shifted first digit of Confuciu
sornis prevented active movements in the tree crown
(Zinoviev, 2009). It remained uncertain for a long time
how Archaeopteryx used the externally curved claws
(which are distinctly seen in almost all specimens) for
climbing vertical stems of Jurassic trees. Surprisingly,
this point escaped attention of researchers. Moreover,
there were wide discussions concerning the extent of
claw curvature compared to living treeclimbing birds
and mammals, as a tool for sticking in tree stems. The
curved claws of wing digits are also externally oriented
in the Early Cretaceous dromaeosaurid Microraptor
(Fig. 7) and in Zhongornis and Jinfengopteryx of uncer
tain relationships (Ji and Ji, 2007; Gao et al., 2008).
However, this external orientation of claws looks nor
mal, taking into account that they were adapted for
clutching at tree branches, using the widely laterally
spread forelimbs. This assumption is supported by the
external orientation of the claw curvature in the allular
and first digits of the wing of hoatzin nestlings (Opis
thocomus), which move in trees clutching at tree
branches using the widely spaced wings (Heilmann,
1926). It is noteworthy that, even in Early Cretaceous
ornithurines (Ambiortus, Gansus, Yixianornis, Archae
orhynchus, and Hongshanornis), the ungual phalanges
of wing digits were small and only slightly curved
(Kurochkin, 1982, 1999; Zhou and Zhang, 2005,
2006a; You et al., 2006) (Fig. 8). They had no need of
large curved claws of wings, since the anisodactylous
foot provided firm seat of birds on branches. An excep
tion is provided by large Early Cretaceous Jianchang
ornis microdonta, in which the relatively large ungual
phalanges of allular and first digits are curved inside
and, in addition, the allular digit projects noticeably
distally beyond the edge of the carpometacarpus
(Zhou et al., 2009).
In enantiornithines from the Lower Cretaceous of
Spain and China, the caudal region of the vertebral col
umn and digit I (hallux) display different conditions.
Iberomesornis from the Lower Cretaceous of Spain has
eight relatively wide and long free caudal vertebrae; very
large and long pygostyle, which is expanded and flat
tened ventrally, formed of 1015 fused vertebrae; and
hallux, which is directed medially and can be turned
posteriorly (Sanz and Bonaparte, 1992; Sereno,
2000). In Early Cretaceous Concornis from Spain, the
reduced first metatarsal lies on the medial side of the
second metatarsal; the shape of the proximal articular
surface of digit I suggests that it was limited in poste
rior rotation (Sanz and Buscalioni, 1992; original
data); in the caudal region, only two anterior free ver
tebrae are preserved; therefore, it is impossible to
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PALEONTOLOGICAL JOURNAL Vol. 44 No. 12 2010
KUROCHKIN, BOGDANOVICH
reconstruct with certainty the general structure of the
caudal region. In the small enantiornithine Dalinghe
ornis (with a 2cmlong skull) from the Yixian Forma
tion (Liaoning, China), the tail is represented by a
2cmlong row of 20 free caudal vertebrae; digits I and
II are turned medially (Zhang et al., 2006). Another
small Chinese enantiornithine Cathayornis has eight
relatively large free caudal vertebrae and an elongated
pygostyle (15 mm long), which is flattened dorsoven
trally and has a wide bifurcating base (Zhou, 1995).
Unfortunately, the foot structure of this animal
remains uncertain, since the phalanges of its digits are
disarticulated and scattered. Cuspirostrisornis, a rela
tively small Early Cretaceous enantiornithine from
China, distinctly shows a large pygostyle and medially
positioned first digits of feet. In another enantiorni
thine, Rapaxavis, the pygostyle is even larger and more
widened, and the first digit is oriented distinctly medi
ally (Morschhauser et al., 2009). In other large and
small enantiornithines from the Lower Cretaceous of
China, the feet of which have been examined (Pro
topteryx, Sinornis, Eoenantiornis, and Vescornis), the
first metatarsal lies on the medial side of the second
metatarsal (Zhang and Zhou, 2000; Sereno, 2002;
Zhang et al., 2004; Zhou et al., 2005); this suggests
that the hallux was incompletely posteriorly turned.
Thus, in the majority of known enantiornithines, the
number of free caudal vertebrae is reduced to 58;
however, they are large, widened, and elongated, and a
long, massive, dorsoventrally flattened pygostyle is
attached to them. This suggests that the tail of enan
tiornithines was relatively heavy and elongated rather
Fig. 6. Carpal region of skeletons of Jeholornis prima Zhou et Zhang, 2002 (upper) and Confuciusornis sanctus Hou et al., 1995
(lower) from the Lower Cretaceous of China; arrows indicate claws of externally curved wing digits (after Hou, 1997); photograph
by E. Kurochkin.
PALEONTOLOGICAL JOURNAL Vol. 44 No. 12 2010
ORIGIN OF FEATHERED FLIGHT 1579
than fanshaped, with caudal feathers arranged in
sequential rows, at least, within the distal part of the
tail (Fig. 9); therefore, the tail structure was similar to
that of Archaeopteryx. In the foot of Early Cretaceous
enantiornithines, digit I was incompletely opposed to
other digits. In living ornithuromorph birds, the first
metatarsal usually lies on the medioplantar margin of
the second metatarsal. In Late Cretaceous enantiorni
thines, the tail was probably retained elongated and
heavy, as was reconstructed by Martin (1995). Nanan
tius from the Upper Cretaceous of Mongolia probably
had a rudimentary pygostyle in the shape of a short
rodlike structure (Kurochkin, 1996).
Evolutionary changes from the elongated leaflike
to short fanshaped tail were influenced by aerody
namic requirements. Gatesy and Dial (1996) have
shown that the lifting force produced by the fan
shaped tail of extant birds is several times as great as
that of the elongated leaflike tail of Archaeopteryx, all
other things (weight, surface area) being equal. In
addition, they developed the concept of three locomo
tor modules, i.e., the forelimbs, hind limbs, and tail,
which distinguish birds from the unimodular design of
their bipedal terrestrial ancestors (Gatesy and Dial,
1996b; Gatesy, 2002). In their opinion, each avian
module evolved independently. In contrast, we believe
that evolutionary changes in the three modules were
tightly correlated.
DISCUSSION
Thus, the model proposed for morphoecological
evolution of the ancestors of birds implies the initial
stage of terrestrial specialization, bipedalism, develop
ment of the upward leap (from ground to tree branches
or bushes), subsequent arboreal adaptation through
the movement along branches by leaping and descent
by flattering parachuting (Fig. 10). This evolutionary
scenario assumes the initial specialization of hind
limbs for bipedal locomotion based on the anisodacty
lous foot, which differs essentially from the foot of
theropods. A probable role of leaping, with the balanc
ing forelimbs for the origin of flight was repeatedly
proposed by supporters of both arboreal and terrestrial
hypotheses (Nopsca, 1907; Caple et al., 1983; Nessov
and Yarkov, 1989; Padian and Chiappe, 1998a).
The adaptation for the arboreal lifestyle of archo
sauromorph ancestors of birds is in need of explana
tion. We believe that this was intended not only for
expansion over new trophic niches but also for avoid
ance of terrestrial predators, in particular, during the
night and rest, and for the development of nesting
adaptations in trees or bushes, which undoubtedly
provided better defense than on the ground (Bock,
1986; Nessov and Yarkov, 1989; Dial, 2003a). New
trophic niches were developed later, after the forma
tion of true flight. Initially, these animals were appar
ently small; when leaping down from trees, they low
ered relatively slowly; this facilitated the development
of flight. Bock (1986) even proposed that the develop
ment of arboreal adaptations in the ancestor of birds
led to a decrease in size.
Turning to the arboreal origin of flight according
to the scheme from abovedownwards, from a climb
ing ancestor with the forelimbs embracing branches
and stems, it should be noted that this was connected
with certain rearrangements in the forelimbs, in par
ticular, with the formation of a prehensile manus,
which is incompatible with subsequent changes in the
plane of its bending and in the wing. The arboreal
hypothesis in pure form also implies the stage of glid
ing (Bock, 1986; Feduccia, 1999). However, the only
general pattern of the evolution of movements in the
air through the improvement of gliding is expansion of
Fig. 7. Skeleton of fourwinged Microraptor gui Xu
et. al., 2003 from the Lower Cretaceous of China; arrows
indicate remiges of advanced aerodynamic structure on
the fore and hind limbs and wing digits, with externally
curved claws; photograph by E. Kurochkin.
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KUROCHKIN, BOGDANOVICH
the flying membrane. Vivid examples of perfect gliders
are the flying lemur (Cynocephalus), flying squirrels
(Pteromys), marsupial cuscuses, and flying phalangers
can be supplemented by extant and extinct lizards,
Sharovipteryx, and Late Permian weigeltisaurids, the
earliest known gliders (Bulanov and Sennikov, 2006).
However, none of tetrapod groups are known to evolve
from gliding to flapping flight, that is, groups with
gliding primitive forms and advanced forms showing
flapping flight (Long et al., 2003). Gliding is provided
by an essentially different pattern of morphological
adaptations compared to active flight (Padian, 1983).
In gliders, the plane of the membrane (wing) probably
begins the formation from the body, from its proximal
regions in the distal direction. This design is initially
stronger and more efficient aerodynamically, since it
does not produce a slit between the flying surface and
body nor a narrowing between the left and right mem
branes. On the contrary, as the avian wing was devel
oped, the flapping plane most likely arose at the distal
end of the forelimb, beginning from digits; this is sup
ported by all presently known examples of the devel
opment of primary wings from the fore and hind limbs
in Mesozoic theropods and early birds: fourwinged
Microraptor and Anchiornis and some enantiornithines
(Xu et al., 2003; Zhang and Zhou, 2004; Hu et al.,
2009). In flapping wings, the distal regions are best
adapted for interaction with the air, making the major
contribution to the lifting force and moving more rap
idly than the proximal regions of the wing. Thus, glid
ing is incompatible with subsequent development of
flapping flight (Caple et al., 1983).
The formation of featherlike structures predeter
mined a different trend in the development of the loco
motor apparatus in the ancestors of birds. The wing, the
apex of which is formed of separate, mobile feathers
(wing with a split apex) provided a much greater angle
of attack without a burble; this produced sufficient lift
ing force to support the body in the air, even when the
wing moved at a low speed (Yakobi, 1966; Alexander,
1970). What was the reason for the formation of primary
feathers with symmetric vanes on the distal segments of
the forelimbs and tail of theropod dinosaurs and ances
tors of birds? We subscribe to the views of Cowen and
Lipps (1982) that such a plumage could have developed
by sexual selection as an element used for display behav
ior. This new formation was very useful to maintain
equilibrium, as animals moved on tree branches or
bushes. The flight, which was initiated by descend from
trees and evolved from flattering movements (Longrich,
2006) of the primarily feathered forelimbs, probably
contributed to the reduction of muscle mass of hind
limbs to a lesser extent than in the case of a continuous
flying membrane of bats; this favored further parallel
Fig. 8. Distal wing part of the ornithuromorph Ambiortus dementjevi Kurochkin, 1982 from the Lower Cretaceous of Mongolia;
arrows indicate rudimentary and slightly curved claw of wing digit I and imprints of remiges; photograph by E. Kurochkin.
PALEONTOLOGICAL JOURNAL Vol. 44 No. 12 2010
ORIGIN OF FEATHERED FLIGHT 1581
improvement of both systems. Note that, in Early Cre
taceous ornithuromorph birds, flying plumage on the
hind limbs has not been recorded. However, in gliding
troodontids, dromaeosaurs, enantiornithines, and
Archaeopteryx, the hind limbs had feathers, which
increased the total lateral surface, although they were
characterized by poor air locomotion (Feduccia, 1999;
Xu et al., 2003, 2009; Christiansen and Bonde, 2004;
Zhang and Zhou, 2004; Xu and Zhang, 2005; Long
rich, 2006; Hu et al., 2009).
Embryological studies of living birds have shown that
the foot and manus stop development as a pentadactyl
limb (because of fusion of skeletal elements) at approxi
mately the same stage; this also suggests relatively syn
chronous specialization of the fore and hind limbs in the
evolution of birds (Kovtun et al., 2003). It is usually
accepted that birds and saurischian dinosaurs were simi
lar in the initial evolutionary stage next to archosauro
morph ancestors (Romer, 1923; Walker, 1977). The two
groups probably evolved from different ornithosuchid
groups with the early acquired bipedalism.
Subsequent evolutionary events, which determined
distinctive characters of the ornithuromorph phyletic
lineage, probably involved the following features. The
reduced tail and strengthened thoracic musculature
caused a cranial displacement of the center of gravity.
To restore the optimum position (in birds, the center
of gravity is directly above the knee joint and the sup
porting foot), the position of the femur was changed.
In contrast to thecodonts and dinosaurs, the femur of
birds is positioned closer to the horizontal; this was
indicated earlier without special reasoning (Walker,
1977; Chiappe, 1995), and Gatesy (1990) provided a
functional explanation that involved the need to dis
place the foot under the center of gravity, which in
birds is shifted more cranially than in bipedal thero
pods. At the same time, an almost horizontal position
of the femora of birds requires a greater abduction of
these bones (a more lateral position to pass the body
by) and strengthening the muscles that restrict pro
tractionsupination of the femur to prevent sagging of
the body between the knee joints. The supination (out
ward rotation) of the femur combined with the pro
Fig. 9. Reconstructed appearance of the enantiornithine Nanantius valifanovi Kurochkin, 1996 from the Upper Cretaceous of
Mongolia; note lengthened tail and dorsoplantarly flattened tarsometatarsus, with medially directed first digits of the foot; recon
structed by E. Kurochkin, drawn by O. OrekhovaSokolova.
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KUROCHKIN, BOGDANOVICH
VIII
VI
V
VII
IV
III
II I
Fig. 10. Sequence of hypothetical stages of the development of flight in true birds: (I) bipedal terrestrial archosauromorph;
(II) development of anisodactyly in archosauromorph ancestor of true birds; (III) leaping on lower branches of trees and bushes;
(IV) firm seat on perches at the stage of completely formed anisodactylous foot and initial reduction of long tail; (V and VI) devel
opment of feathers with symmetrical vanes on the distal segments of the forelimbs and tail for display behavior; these feathers
could decrease the speed of descent by parachuting; (VII) formation of asymmetrical aerodynamic feathers on wings and reduc
tion of long tail; and (VIII) transition to true flapping flight; reconstructed by E. Kurochkin, drawn by O. OrekhovaSokolova.
traction (anterior displacement) provide a mechanism
that places the supporting foot in the projection of the
center of gravity to maintain equilibrium at the phase
of support on one hind limb (Stolpe, 1932; Hutchin
son and Gatesy, 2000). The protraction of the femur is
controlled by massive posterior femoral muscles
(according to the major function, retractors of the
femur), which are similar in birds and other bipedal
PALEONTOLOGICAL JOURNAL Vol. 44 No. 12 2010
ORIGIN OF FEATHERED FLIGHT 1583
archosaurs (Bogdanovich, 2005). Regarding the
restriction of supination, birds resolved this task
through the dorsal displacement of the iliotrochant
eric muscles along the lateral surface of the femoral
head and general strengthening of these muscles (the
majority of birds have three). These muscles are
homologous to the iliofemoral and puboischiofemoral
muscles of thecodonts and dinosaurs (Hutchinson,
2001). In birds, the strengthening and displacement of
these muscles (cranial or dorsocranial, respectively)
resulted in an increase in size of the preacetabular
region of the ilium, which is characteristic of Pro
toavis. Some researchers believe that the enlargement
of this part of the ilium is connected with the supinator
and protractor functions of the iliotrochanteric mus
cles, as the femur performed wobbling movements
during running (Hutchinson, 2001). However, the
topography and inner structure of these muscles in liv
ing birds (complex pinnate structure, with relatively
short fibers and a large angle of pinnation) and the
electromyographic study strongly suggest that they
function as pronators or extensors of the femur, when
turning movements are performed, and as stabilizers
of the femur in the static state (Gatesy, 1999); however,
the major function is restriction of supination (Sych
et al., 1985).
CONCLUSIONS
The above review of hypotheses for the origin of
flight and our morphofunctional analysis of terrestrial
and air locomotion and locomotor apparatus of birds
allows the development of a compromise hypothesis
for the origin of flight that combines elements of vari
ous variants of terrestrial and arboreal hypotheses with
new data and conclusions. This hypothesis is based on
the system approach to the appraisal of correlated evo
lutionary changes in the locomotor system and integ
ument of the ancestors of feathered creatures. The
only element adopted from the terrestrial hypothesis is
bipedalism, the key adaptation which dismissed the
forelimbs from the supporting function. In contrast to
the arboreal hypothesis in pure form, we propose that
transition of the ancestors of birds onto trees devel
oped through leaping on the lower branches with the
use of support on the hind limbs rather than through
climbing on the tree stem, with embracing by the fore
limbs. In the ancestors of birds, this was possible due
to the early development of the anisodactylous foot
and true intertarsal joint, which provided a stable sup
port on both the land surface and perches, with tight
embracing by completely opposed digit I. Thus, the
forelimbs remained freely flapping for the mainte
nance of equilibrium and development of a flapping
wing, as animals descended from trees. The anisodac
tylous foot, which provided a firm support on four
widely spaced digits, was the basis for the reduction of
long tail, formed of a series of vertebrae, which was
used by the ancestors of birds for the maintenance of
equilibrium on land and for arboreal locomotion. This
evolutionary scenario obviates the necessity of a glid
ing stage in the development of flapping flight, since
the wing and aerodynamic evolution of its plumage are
formed through equilibration by the forelimbs at leap
ing onto branches and through flattering movements
during descent.
The elaboration of this evolutionary scenario of the
origin of flight inevitably leads to the recognition of suc
cessive stages of the appearance of certain aberrations,
selection of which resulted in each new stage of the evo
lutionarily adapted equilibrium (Shishkin, 2005). How
ever, the mechanism of this process was not restricted to
isolated events; on the contrary, it involved correlated
systemic changes (Shishkin, 2006), including new for
mations in the fore and hind limbs, caudal module,
breathing, integument, behavior, and, eventually, in the
entire organization of the living system, as it adapted to
essentially new conditions.
The ecological aspect of our hypothesis raises the
question of under which conditions and why animals
were made to leap onto trees or bushes, equilibrate
using the primary wings, and descend by the flattering
flapping rather than gliding. In the Triassic and Juras
sic, the shrub and tree vegetation was dominated by
various gymnosperms, i.e., Coniferae, Bennettita
ceae, Pteridospermae, Cycadaceous, Gnetaceae, and
Ginkgoaceae. Many of these plants are characterized
by dense branching or feathering just from the ground
level and dense arrangement of branch whorls along
the stem (Takhtajan, 1956). It is rather difficult to
climb such trees and bushes along the stem, while
leaping or flying onto projecting branches or feathers
and upward jumps in these plants, clutching at
branches by wing digits with claws, are much easier
(Fig. 10). In addition, it was probably easy to build
primitive nests on these dense trees, so that the nests
were well hidden beyond the reach of terrestrial pred
ators. Moreover, the Coniferae, Ginkgoaceae, and
Gnetaceae provided animals with rich and diverse fruit
and seed food. As an animal descends from the tree, it
seems less efficient to spring downwards using the
same branches, while gliding with the help of rudi
mentary wings is difficult or even impossible. The
most suitable way in such a situation is almost vertical
parachuting, controlled by flattering flapping move
ments of the loaded forelimbs (primary wings). Nest
lings of extant birds, with the precocial or semipreco
cial developmental types (some anseriforms and
charadriiforms), descend from nests located on trees
or rocks using the same flatteringparachuting flight.
In early birds, such wings could have performed active
posterodorsal flaps, initiating progressive development
of the supracoracoid muscle. This is the ecological
basis and an additional functional aspect of the
hypothesis proposed for the origin of flight in true
ornithurine birds.
In theropod dinosaurs, digit I is not opposed to the
other digits of the foot; the same is true of their direct
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PALEONTOLOGICAL JOURNAL Vol. 44 No. 12 2010
KUROCHKIN, BOGDANOVICH
descendants, archaeopteryxes and microraptors. This
prevented the reduction of the long tail formed of verte
brae, since this foot did not provide a firm support on
branches nor when landing (Fig. 5). Therefore, they
could not develop a true flight, only some became good
gliders, with the supporting area enlarged by the feather
surfaces of the tail and hind limbs. In enantiornithines
(probable descendants of archaeopterygids), digit I of
the foot was incompletely opposed, and the tail
remained lengthened due to large extended free caudal
vertebrae and long massive pygostyle, the feathers of
which were arranged successively rather than formed a
fanshaped structure.
ACKNOWLEDGMENTS
We are sincerely grateful to L.P. Tatarinov,
A.N. Kuznetsov (Zoological Museum of Moscow
State University), N.V. Zelenkov, and A.K. Agadjan
ian (Borissiak Paleontological Institute, Russian
Academy of Sciences), and V.D. Gulyaev (Institute of
Animal Systematics and Ecology, Siberian Branch,
Russian Academy of Sciences) for useful advice and
remarks on the manuscript of this paper. We are thank
ful to the artist O. OrekhovaSokolova for producing
figures illustrating our concept and to Zhonghe Zhou
for the opportunity to study and take photographs of
Lower Cretaceous specimens housed in the Institute
of Vertebrate Palaeontology and Palaeoanthropolgy of
Chinese Academy of Sciences.
The study of E.N. Kurochkin was supported by the
Russian Foundation for Basic Research, project
no. 070400306.
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