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The evolution of flight in birds involves (i) decoupling of the primitive mode of quadrupedal locomotor coordination, with a new synchronized flapping motion of the wings while conserving alternating leg movements, and (ii) reduction of wing digits and loss of functional claws. Our observations show that hoatzin nestlings move with alternated walking coordination of the four limbs using the mobile claws on their wings to anchor themselves to the substrate. When swimming, hoatzin nestlings use a coordinated motion of the four limbs involving synchronous or alternated movements of the wings, indicating a versatile motor pattern. Last, the proportions of claws and phalanges in juvenile hoatzin are radically divergent from those in adults, yet strikingly similar to those of Archaeopteryx. The locomotor plasticity observed in the hoatzin suggests that transitional forms that retained claws on the wings could have also used them for locomotion.
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EVOLUTIONARY BIOLOGY
Hoatzin nestling locomotion: Acquisition of
quadrupedal limb coordination in birds
Anick Abourachid1*, Anthony Herrel1,2, Thierry Decamps1, Fanny Pages1, Anne-Claire Fabre1,
Luc Van Hoorebeke3, Dominique Adriaens2, Maria Alexandra Garcia Amado4
The evolution of flight in birds involves (i) decoupling of the primitive mode of quadrupedal locomotor coordi-
nation, with a new synchronized flapping motion of the wings while conserving alternating leg movements,
and (ii) reduction of wing digits and loss of functional claws. Our observations show that hoatzin nestlings move
with alternated walking coordination of the four limbs using the mobile claws on their wings to anchor them-
selves to the substrate. When swimming, hoatzin nestlings use a coordinated motion of the four limbs involving
synchronous or alternated movements of the wings, indicating a versatile motor pattern. Last, the proportions of
claws and phalanges in juvenile hoatzin are radically divergent from those in adults, yet strikingly similar to those of
Archaeopteryx. The locomotor plasticity observed in the hoatzin suggests that transitional forms that retained
claws on the wings could have also used them for locomotion.
INTRODUCTION
Birds are flying theropods that power their flight by flapping both
wings simultaneously. Developmental data indicate that the reduc-
tion of wing digits and the loss of claws are concomitant during bird
evolution (1) such that the wings lose their grasping function.
Although some birds such as chukars, ducks, rails, and owls re-
tain claws on the wing (2), they do not use them for locomotion.
Hoatzin (Opisthocomus hoazin) nestlings, however, retain functional
claws on the wing and have been suggested to use them to climb in
the vegetation. This is possibly one of the most remarkable but also
the least documented traits in this unusual bird. The first descrip-
tion of this behavior was provided by C. G. Young in 1888: “As soon
as the young escape from the egg, they creep about with the assist-
ance of these hands, stretching out their wings and digging these
claws into hooking on whatever they meet.” He further added that a
“specimen, by means of these claws walked out of a calabash” (3).
Another unusual trait in hoatzin nestlings is to escape by jumping
into the water below the nest and to swim back to the vegetation.
Although hoatzins are not rare, quantitative data on locomotion in
nestlings during either climbing or swimming have never been col-
lected and references to locomotion in these animals all refer back
to the original publication on their behavior (3).
Juvenile extant birds may provide key insights into our under-
standing of the evolutionary and functional transformations that
took place toward the evolution of modern birds (2). Before they are
capable of active flight, most juveniles flap their wings in the context
of wing-assisted incline running (WAIR) to move up steep slopes.
During WAIR, the wings generate aerodynamic forces that help the
animal ascend obstacles (4,5). As the synchronous wing coordina-
tion observed during flying and WAIR is shared by many birds
across the majority of clades, it is likely basal for the group (6). The
neuronal networks, functionally organized early during develop-
ment, drive the in-phase movements of the wings during bird loco-
motion. This determinism is so robust that the experimental substi-
tution of a brachial spinal cord segment by a lumbosacral segment
and vice versa during the early stages of development in chickens
leads to synchronized movements of the limbs connected to the
brachial segment of the spinal cord and alternated movements of
the wings connected to the lumbosacral segment (7). In that con-
text, the hoatzin is remarkable. Do hoatzin nestlings move using an
alternating quadrupedal walk, as suggested by Young’s description
(3), or do they use the wings and claws in an opportunistic reflex-
like way to grasp branches when possible, as when a newborn child
grasps a finger (8), or do they use a kind of WAIR behavior during
climbing, as do all other birds? Here, we provide the first quantita-
tive data on the locomotion of nestling hoatzins that inform on the
use of the claws and the coordination pattern of the limbs. We
filmed four nestlings, caught in nests along the Cojedes River in
Venezuela, while moving on an inclined substrate and while swim-
ming. Whereas movements were spontaneous in water, nestlings
needed to be encouraged to move on the inclined surface by touch-
ing their tail or hind feet. The inclined substrate was covered with a
towel, providing grip for the claws on the wings.
RESULTS
The limbs moved in an alternating fashion, with the movement
of a leg being followed by the movement of the contralateral wing,
then the other leg, and the other wing (Fig.1). The claws were
hooked onto the substrate and the wing flexed, pulling the body
upward. Locomotor cycles were most often irregular, as the lack of
an immediate attachment of the claws to the substrate destabilized
the nestling bird. When the claw did not hook into the substrate, the
motion of the wing continued further laterally until the claw at-
tached. If it did not, the wing was reversed and a new movement
cycle of the same wing was initiated. The quadrupedal locomotion
observed was rather irregular with birds stopping typically after two
or three cycles. However, the movements of the four limbs were
coordinated. The swing phase duration of the forelimbs was longer
than the swing phase duration of the hindlimbs (i.e., the wing duty
factor was smaller than the foot duty factor). The time lag between
1Département Adaptations du Vivant, UMR 7179 CNRS/MNHN, 57 rue Cuvier, Case
postale 55, 75231, Paris Cedex 5, France. 2Evolutionary Morphology of Vertebrates,
Ghent University, Campus Ledeganck, K.L. Ledeganckstraat 35, B-9000 Gent, Belgium.
3UGCT—Department of Physics and Astronomy, Ghent University, Proeftuinstraat
86, 9000 Ghent, Belgium. 4Centro de Biofı́sica y Biochı́mica, Instituto de Investigaciones
Cientı́ficas (IVIC), Caracas, Venezuela.
*Corresponding author. Email: abourach@mnhn.fr
Copyright © 2019
The Authors, some
rights reserved;
exclusive licensee
American Association
for the Advancement
of Science. No claim to
original U.S. Government
Works. Distributed
under a Creative
Commons Attribution
NonCommercial
License 4.0 (CC BY-NC).
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the movements was more irregular for the wings than for the legs.
However, the tendency is clearly to move the limbs in an alternating
way (Table1) (9), with a coordination typical of a quadrupedal
walking pattern [fore lag (FL), hind lag (HL), and pair lag (PL) close
to 0.5]. This suggests that the use of the wings is not limited to an
opportunistic grasping reflex.
The alternating coordination pattern of the wings also does not
correspond to WAIR, where the wings flap in phase to create aero-
dynamic forces. At hatching, chukars (Alectoris chukar) can ascend
slopes by crawling on all four limbs (6), but the wings, without claws,
cannot anchor to the substrate. No alternated wing coordination
has been reported. The hoatzin coordination pattern of the four
limbs is typical of a quadrupedal walking gait, a trait lost in all other
modern birds. This symmetrical gait (9) secures at least three points
of contact with the substrate and is the most stable of the quadrupedal
coordination patterns.
When placed in the pool, the nestlings swam vigorously and
with great ease, either under water or with the head kept outside of
the water. Irrespective of the coordination, the swimming cycles
were rather regular, even if a bit more variable for the wings com-
pared to the legs. The wing power phases were shorter than the
recovery phases, whereas they were longer for the legs. The coordi-
nation between the leg and the wing (PL) was variable (high SDs).
The movements of the legs were alternated (HL close to 0.5), while
the wings typically moved in phase (FL close to 0; Table1) (Fig.2).
Out of the 50 locomotor cycles observed, only 4 of them showed
an out-of- phase coordination pattern. The coordination during
most swimming cycles was thus generally similar to that ob-
served during WAIR (in other birds, but in a different mechanical
context).
In a more complex environment with branches, hoatzin nest-
lings used a quadrupedal walking coordination, but due to the
irregularity of the substrate, the coordination was far less regular
than on our experimental substrate. The head was also used as a
hook: It was flexed so that the base of the beak was positioned on the
branch, the neck appearing to pull the body upward and helping the
Fig. 1. Schematic illustration of a hoatzin nestling climbing on a 45° inclined surface. The x axis represents time. Each line represents the time when a leg is in contact
with the substrate. The movements of the four legs are alternating: The left wing moves and grips the substrate (A). Next, the right foot moves up and touches down (B),
followed by the right wing that moves forward (C). The left foot then moves forward and touches down (D), and the left wing moves again (E) followed by the right foot
(F). However, the left claw was unable to grip the substrate at its most forward position (star), resulting in it moving backward until gripping the substrate (E). The lateral
position of the wing perturbates the progression and changes the coordination pattern. The pattern is still alternated but with the left foot (G) moving before the right
foot (I) and the right wing (H) before the left wing (J). LF, left fore (wing); RF, right fore (wing); RH, right hind (foot); LH, left hind (foot).
Table 1. Gait characteristics and limb coupling during climbing and swimming. n, number of cycles analyzed.
Climbing
Cycle duration (s) Duty factor FL HL PL
RF LF RH LH RF LF RH LH
Mean 4.20 3.10 5.58 6.31 0.86 0.83 0.94 0.96 0.36 0.48 0.56
SD 1.61 2.27 2.25 2.97 0.10 0.05 0.04 0.01 0.33 0.10 0.22
n11 10 12 11 10 7 10 11 8 9 9
Swimming
In-phase coordination
Mean 0.77 0.82 0.75 0.74 0.43 0.41 0.54 0.53 0.05 0.42 0.32
SD 0.18 0.18 0.06 0.07 0.08 0.11 0.08 0.04 0.07 0.09 0.18
n12 12 15 13 12 12 15 13 9 9 10
Out-of-phase coordination
Mean 0.72 0.72 0.71 0.7 0.34 0.31 0.62 0.53 0.52 0.52 0.18
SD 0.16 0.06 0.07 0.08 0.05 0.07 0.07 0.06 0.13 0.12 0.16
n44444444444
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wings. The claws on the fingers were actively moved independent of
the movements of the rest of the hand skeleton. Contrast- enhanced
microcomputed tomography (CT) images of a late-stage embryo
show that the hoatzin has multiple muscles and tendons attaching
onto the finger bones, as observed in most other birds (1013).
However, an additional tendon of one of the digital flexor muscles
attaches onto the distal phalanx of the alula (Fig.3). This likely
allows the active gripping of the branches by the claws. A compari-
son of the proportions of the phalanges of the hoatzin nestlings with
those of Archaeopteryx (14) shows a remarkable similarity in pro-
portions between the two (Fig.4). The proportions in adult hoatzin
are, however, quite different from those observed in nestlings.
DISCUSSION
Quadrupedal locomotion requires a coupling of the forelimbs, a
coupling of the hindlimbs, and a coupling between the limb pairs at
the level of the spinal neuronal network (9,15). In vertebrates, loco-
motion is initiated at the level of the brainstem and generated by a
central spinal network (16). In mammals, which are able to use
in-phase and out-of-phase movements for each limb pair, two sets
of commissural interneurons are involved in the right-left coordi-
nation. An inhibitory pool of neurons is activated for alternating,
out-of-phase coordination, and an excitatory pool is activated for
synchronous, in-phase coordination (17). Their interplay depends
on the behavioral context and the associated locomotor speed. In
birds, the neural network is organized early during development
(7) and triggers in-phase movement of the wings. The in-phase flap-
ping of the wings could thus have arisen from either the loss of the
inhibitor commissural neuron pool or its silencing. The hoatzin
nestlings exhibit both in-phase movements during swimming and
out-of-phase movements during climbing. This suggests that they
have both excitatory and inhibitory connections between the inter-
neuronal networks of the limbs. The plasticity exhibited in the cou-
pling between the excitatory and inhibitory connections in the
hoatzin nestling could then arise either from descending drive or
from the effects of proprioceptive feedback, or both. The quadrupe-
dal coordination goes hand in hand with the presence of functional
claws on the wing (1), since without claws the wings cannot anchor
the body to the substrate and would thus be unable to generate the
locomotor forces. During slow movements, the locomotor mechanics
Fig. 2. Schematic illustration of a hoatzin nestling swimming. The x axis rep-
resents time. Each line represents the propulsive phase when the limb is moving
backward. The dorsal view shows a synchronized motions of the wings; the lateral
view shows the alternated motion of the limbs. LF, left fore (wing); RF, right fore
(wing); RH,right hind (foot); LH, left hind (foot).
Fig. 3. Musculoskeletal anatomy of a hoatzin shortly before hatching. Left: Fetus as positioned in the egg. Middle: Reconstructed mineralized parts of the skeleton of
the bird, showing the position of the wing skeleton (yellow circle). Right: Detailed reconstruction of the contrast-enhanced CT data of the wing (ventral view), with the
position of the additional tendon of the flexor digitorum profundus attaching to the alula digit illustrated. Inset: Detail of the alula digit, with the keratin sheet removed,
showing the claw-like distal phalanx. Blue, cartilage; yellow, bone; red, muscle; cyan, connective tissue sling of the muscle tendon; orange, keratin.
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require at least three anchoring points for stability, preventing
the coordination of wings into an in-phase motion. Proprioceptive
feedback may participate in the reactivation of a silent inhibitory
motoneuron pool during quadrupedal locomotion.
Birds originate from theropods, bipedal animals that did not use
the forelimbs for walking. Although the exact position of the hoatzin
in the bird tree of life remains controversial (1822), its divergence
seems to have occurred after the origin of Paleognaths, Galloanseres,
and other neoavian radiations (22). None of the species of these
clades are known to use the wings for climbing. Furthermore, the
forelimb in-phase coordination is determined early in the develop-
ment in the chicken (Gallus gallus) (7), a Galloanseres species from
a clade more basal than the Opisthocomiformes (22). The quadru-
pedal walking coordination of the hoatzin nestling thus represents
the reappearance of a trait lost during bipedal saurischian dinosaur
evolution (23), without the loss of a trait that has arisen later in the
evolution of birds (wing flapping during flight retained in adult
hoatzin). The quadrupedal coordination may be the expression of
the conservative nature of the central nervous system, with a
basic interneural network reactivation in response to proprioceptive
feedback, driven by the contact of the claws to the substrate. It is
possible that the interneuronal networks show greater plasticity and
diversity among birds than has been previously recognized due to
a sparse sampling of “model animal” species in neurophysiological
studies. As Archaeopteryx shows large claws on the wing similar in
proportion to those observed in the hoatzin nestlings, the latter
might be used as a functional analog to infer the locomotor reper-
toire in transitional forms like Archaeopteryx. Our results thus sug-
gest the existence of a larger locomotor repertoire in transitional
forms likely including both WAIR wing flapping and quadrupedal
limb coordination during climbing allowed by the presence of claws
on wings (24).
MATERIALS AND METHODS
Animals and filming
Animals were caught in October 2014 along the Cojedes River near the
town of El Baul under permit number 950 issued by the Venezuelan
government. Animals were transported back to the field labora-
tory and filmed with three HDR-CX740VE Sony cameras at 50 Hz.
Animals were induced to climb up an inclined surface covered with
a cloth to provide grip and then climb on branches. Subsequently,
animals were induced to swim in an aquarium (100 cm × 50 cm × 50 cm)
with a water depth of 15 cm. All the procedures were approved by
the ethics committees of the Muséum National d’Histoire Naturelle
(MNHN) (Comité Cuvier) and Instituto Venezolano de Investigaciones
Cientificas (IVIC) (COBIANIM).
CT scanning
A late-stage hoatzin embryo (egg length, 4.1 mm), four juveniles,
and two adults were CT-scanned at the Centre for X-ray Tomog-
raphy at Ghent University (UGCT). A first in toto scan of each
specimen was performed to get a complete overview of the mineral-
ized skeletal anatomy using the in-house developed HECTOR scanner
(25). A total of 2400 x-ray projections over 360° were taken at 120-kV
tube voltage and 20-W target power with a PerkinElmer detector
(pixel pitch, 0.2 mm; exposure time, 1000 ms per image), yielding an
isotropic voxel pitch of 20 m. Subsequently, the left wing was cut
off of the late-stage embryo and transferred to 50% ethanol and
phosphate-buffered saline (1 hour), after which it was treated with
2.5% phosphomolybdic acid for 1 week, to visualize soft tissues with
CT. The wing was then gradually transferred back to 70% ethanol
and scanned at HECTOR under similar settings (but at 100 kV and 10 W)
at an isotropic voxel pitch of 10 m. Virtual cross sections were
reconstructed using the in-house developed software Octopus
[version 8.8.2.1; (26)]. Bone and soft tissues were segmented and
visualized using Amira (version 6.0, FEI). Proportions of the pha-
langes and claws in Archaeopteryx were measured on the basis of
the illustrations of Griffiths (14).
Gait analysis
Climbing
On the videos, we noted the time when the limbs gripped the
cloth and stopped moving as well as the time when the claws were
released from the cloth. Even if the delays between the movements
may be long and the coordination may be perturbed by additional
grips, the coordination remained similar across the more than 20
locomotor cycles analyzed: The movement of a wing was followed
by the movement of the opposite foot, then the other wing moved
followed by the other foot. Last, the first wing moved again (Fig.1).
The movements were, however, very slow and irregular. For our
quantitative analysis, we kept only the cycles with stance phases
lasting less than 10 s and swing phases less than 2 s. As the birds
often stopped, we did not always have two successive complete cycles
so that we calculate the gait parameters for each limb even if it was
not possible to quantify all the parameters for all of them in a given
cycle. The swing phase was defined as the time when the limb is off
the substrate; the stance phase was defined as the time during which
the claw gripped the cloth. Cycle duration was quantified as the sum
of the swing phase duration plus the stance phase duration. The
duty factor was defined as the participation of the stance to the total
cycle duration (i.e., the stance duration divided by the cycle duration).
We also calculated coordination parameters (27): The FL was defined
as the time lag between the beginning of the two wing stance phases.
The HL was defined as the time lag between the beginning of the
two foot stance phases. Last, the PL was defined as the time lag
between the stance phase of a wing and the stance phase of the
ipsilateral foot.
Swimming
Fifty swimming cycles were observed. In four of them, the wings
moved in phase. In all the other cases, the wings and the feet moved
out of phase. We observed different coupling (Fig.2) between the
Fig. 4. Proportions of the digit phalanx in the Archaeopteryx compared to
three hoatzin developmental stages. Values are in percent of the digit length.
Variability is shown with white line.
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forelimbs and the hindlimbs. Because of the constraints of the field
experiments, we were not able to quantify all the cycles observed.
We selected the sequences when the birds moved parallel to the
camera in lateral view, allowing us to see the motion of both the
hindlimbs. The motion of the wings was visible but not accurate
enough to be measured on the lateral view. The two wings were
clearly visible on the dorsal views, but the hindlimbs were often hidden
by the wings or by reflections on the water. We selected sequences
where it was possible to synchronize the motion of the wings and
the legs for our quantitative analysis. We considered the power phase
of a limb to be the phase when it moved backward and the recovery
phase when it moved forward (hindlimbs) or laterally (wings).
SUPPLEMENTARY MATERIALS
Supplementary material for this article is available at http://advances.sciencemag.org/cgi/
content/full/5/5/eaat0787/DC1
Movie S1. Videos of the experimental conditions, climbing, and swimming in hoatzin nestlings.
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Acknowledgments: We would like to thank J. González-Fernández from Hato Mataclara and
the Hato Pinero staff for their support in the field, J. R. Cazalets and Ph. Janvier for their
remarks on the manuscript, and D. Geffard-Kuri for help with the illustrations. We also thank
the Ministerio Del Poder Popular para la Ecosocialismo, Habitat y Vivienda for the capture and
exportation permits. Funding: This work was supported by ATM MNHN, PEPS ExoMod CNRS
(A.A.), and IVIC grant no. 67 (M.A.G.A.). Author contributions: A.A. conceived the project;
M.A.G.A. organized the field work; A.A., A.H., T.D., A.-C.F., and M.A.G.A. participated in the field
work and the capturing and filming of the animals; A.A., A.H., T.D., D.A., and F.P. analyzed the
data; L.V.H. was responsible for the CT scanning of the specimens; D.A. and F.P. segmented
the CT data; A.A. and A.H. wrote the paper; all authors revised the paper. Competing
interests: The authors declare that they have no competing interests. Data and materials
availability: All data needed to evaluate the conclusions in the paper are present in the paper.
Additional data related to this paper may be requested from the authors. Hoatzin specimens
can be obtained from the Venezuelan Institute for Scientific Research pending scientific
review and a completed material transfer agreement. The CT scans for the specimens used in
this study are available upon request from the corresponding author.
Submitted 22 January 2018
Accepted 12 April 2019
Published 22 May 2019
10.1126/sciadv.aat0787
Citation: A. Abourachid, A. Herrel, T. Decamps, F. Pages, A.-C. Fabre, L. Van Hoorebeke, D. Adriaens,
M. A. Garcia Amado, Hoatzin nestling locomotion: Acquisition of quadrupedal limb coordination
in birds. Sci. Adv. 5, eaat0787 (2019).
on May 22, 2019http://advances.sciencemag.org/Downloaded from
Hoatzin nestling locomotion: Acquisition of quadrupedal limb coordination in birds
Adriaens and Maria Alexandra Garcia Amado
Anick Abourachid, Anthony Herrel, Thierry Decamps, Fanny Pages, Anne-Claire Fabre, Luc Van Hoorebeke, Dominique
DOI: 10.1126/sciadv.aat0787
(5), eaat0787.5Sci Adv
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REFERENCES http://advances.sciencemag.org/content/5/5/eaat0787#BIBL
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... Nestlings of the South American hoatzin (Opisthocomus hoazin) have claws on the thumbs and first fingers. Abourachid et al. (2019) recently showed that they were capable of a coordinated locomotor pattern of the four limbs typical of a quadrupedal walking gait, 'a trait lost in all other modern birds', during walking up a cloth-covered inclined plane. The nestlings could swim either with alternate or synchronised forelimb action. ...
... The nestlings could swim either with alternate or synchronised forelimb action. Abourachid et al. (2019) associated alternate forelimb action with the possession of mobile claws that secured attachment to the substratum. ...
... They demonstrate coordinated, alternate ipsilateral forelimb and hindlimb action, the classic mode of tetrapod terrestrial locomotion. The assertion of Abourachid et al. (2019) that the hoatzin (Opisthocomus hoazin) is the only modern bird species to be capable of this is evidently erroneous. Other high-latitude penguin species can also use such coordinated quadrupedal locomotion, at least for short distances in soft snow (for gentoo penguins see website 8, Table 1; for chinstrap penguins see website 9, Table 1). ...
... For example, no extant bats are secondarily flightless, probe in mud flats, wade along shores or swim beneath the sea and while hordes of bats fill caves across the world, there are no bats huddled for warmth on the Antarctic ice 42 . Birds, however, have converged at least somewhat upon most modes of life and phenotypic adaptations that bats have explored, including frugivory, sanguivory, nocturnal insectivory, echolocation, long-term torpor, quadrupedal climbing and lactation [73][74][75][76][77]. Live birth appears to be the sole characteristic from which birds are completely excluded. ...
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