Indian J. Anim. Res., 50 (4) 2016 : 476-483
Print ISSN:0367-6722 / Online ISSN:0976-0555
AGRICULTURAL RESEARCH COMMUNICATION CENTRE
www.arccjournals.com/www.ijaronline.in
Anatomical study of the ostrich (Struthio camelus) foot locomotor system
Rui Zhang*, Haitao Wang, Guiyin Zeng1, Changhai Zhou2, Runduo Pan3, Qiang Wang3 and Jianqiao Li
Key Laboratory of Bionic Engineering,
Ministry of Education, Jilin University, Changchun, China.
Received: 22-09-2015
Accepted: 11-01-2016
DOI:10.18805/ijar.9300
ABSTRACT
The Ostrich is a native bird of Africa, and is highly accomplished in terrestrial locomotion in desert and grassland
environments. The foot is an important segment in the ostrich body, critical for damping vibration, absorbing energy, and
maintaining balance; however, detailed information on the ostrich foot is sparse. In this study, the gross anatomy of locomotor
system of the ostrich foot was investigated using dissection and medical scan modeling. The paper contains a detailed
study of the organizational structure and relative positional relationship of bones, tendons, and ligaments, which can be
used for further three-dimensional (3D) reconstruction, providing a solid foundation for the research of high speed, heavy
load, and shock absorption mechanisms. The study also provides a theoretical basis for the research of robot travelling
mechanisms and vehicles traversing desert or planetary terrain.
Key words: Gross anatomy, Locomotor system, Medical scan modeling, Ostrich foot.
INTRODUCTION
The Ostrich (Struthio camelus) is the largest extant
avian biped; it lives in desert environments, exhibiting a
permanently elevated metatarsophalangeal joint and a large
stride (Rubenson et al., 2007; Schaller L. et al., 2009; Double
et al., 2012). The ostrich possesses superb cursorial abilities
primarily expressed by its extraordinary running speed and
endurance (Smith et al., 2013). The peculiar morphological
structure of the ostrich foot provides the mechanical basis
for its locomotor performance. The foot is the key part of
the ostrich locomotor system, making contact with the ground
directly to buffer ground reaction forces as well as stablilize
the center of gravity (Schaller et al., 2007). Dissections on
certain parts of the ostrich foot have been performed by both
domestic and foreign scholars. For example, dissections of
12 formalin-fixed ostriches were performed by Gangl D et
al (2004) to give anatomical descriptions of the pelvic limb.
El-Mahdy et al., (2010) studied the artery and nerve
distribution of the pelvic limb in detail. Kent et al., (2000)
highlighted how ostriches possess robust hind limbs vital to
their locomotor performance. A breakthrough was made
when Smith et al. (2006) studied the functional anatomy of
the ostrich pelvic limb in detail.
To our knowledge, it is not possible to view the
overall anatomical characteristics of each bone, cartilage,
ligament, and tendon by consulting the current literature.
We studied the anatomical structure of the ostrich foot
locomotor system in detail using gross anatomical dissection
(Tadjalli et al., 2009) combined with biomedical scan
modeling. This not only assisted in revealing its superior
locomotor mechanism, but also provided a reliable
morphological structure for the finite element (FE) model
construction of the ostrich foot locomotor system. The study
also provides a theoretical basis for research on robotic
traveling mechanisms and vehicles in extreme environments.
MATERIALS AND METHODS
Two healthy, freshly slaughtered adult African
ostriches were obtained from a breeding facility in Harbin
city, China. This facility keeps more than 50 ostriches yearround, and natural behavior and free exercise are allowed.
The ostrich feet were separated soon after slaughter
(Fig. 1A), and anatomical dissections performed under the
guidance of previous studies (Lucky et al., 2014). Once
preparation work was completed, the anatomical dissection
was formally performed. The ostrich foot was laid flat on
the autopsy table, and a linear imprint from tarsometatarsus
scored, which was then incised through the skin from the
initial point of the score line. The incision was clamped using
tweezers and the skin cut. With the skin peeled, anatomical
analysis was performed on tarsometatarsus, phalanx, and
articular cartilages, as well as the digital cushions.
CT and MRI scanning were performed on the
ostrich foot to obtain the precise distribution of the structures,
using a Light-speed 16 Plus spiral CT scanner and Discovery
MR750 3.0T MRI apparatus (Fig. 1B). The MRI scanning
process of the ostrich foot is depicted in Figure 1B. The
CT/MRI images were generated in DICOM format and then
processed with Mimics software. Following this they were
imported into RE processing software (Geomagic Studio)
for reconstruction.
*Corresponding author’s e-mail: [email protected]. 1Guangzhou Automobile Group Component Co., Ltd, Guangzhou, China. 2 College of Animal
Science, Jilin University, Changchun, China. 3Department of Radiology, the First Hospital, Jilin University, Changchun, China.
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Fig 1: Ostrich foot (A) and Discovery MR750 3.0T MRI apparatus (B).
To ensure the in vitro posture was consistent with
that of the living ostrich foot, the ankle joint of the in
vitro ostrich was fixed using a plastic string into a posture
similar to the standing posture of the in vivo ostrich before
CT/MRI scanning. The tightness of the string was adjusted
to change the loading force. This model enabled the
calculation of the mechanical interaction between ostrich
foot bones and articular cartilages for subsequent research
with FE simulation.
RESULTS AND DISCUSSION
Skin and Fascia Layer
Following the removal of skin from the ostrich
foot (Fig. 2A), it was evident that the tendons and
bones were covered by fascia (Fig. 2B), which has an
im port an t defen si ve functi on . To sepa ra te bon e,
tendon, ligament, and cartilage, the attached fascia was
then removed.
Synovial bursa: The synovial bursa is a capsule filled with
fibrous tissue, located between the apophysis and tendon
around articulations with greater friction. A small amount of
synovial fluid is contained inside the synovial bursa, which
functions by boosting articular glide as well as decreasing
friction between soft tissue and bone. The synovial bursa
was split along the long axis of the bone, and the synovium
clamped with tweezers (Fig. 3A), revealing tendons wrapped
inside the cavity of synovium.
Tendon sheath: Tendon sheath exists around articulations
(Fig. 3B), restricting the tendon as well as limiting friction
during tendon motion. Tendon sheath is composed of an outer
fibrous sheath and an inner synovial sheath (Norton et al.,
2013). Synovial fluid was found between these two layers
in the ostrich foot and there were two tendon sheath trochlea
of different sizes on the posterior aspect of the
metatarsophalangeal joint.
Fig 2: The removal of skin from the ostrich foot (1.Fascia)
Fig 3: Synovial bursa and tendon sheath (1.Synovium; 2.Fibrous sheath; 3.Synovial sheath).
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Digital cushion
forming an annular membrane. White matter, namely the
We found that, similarly to the elephant, there were dermis layer, was found between the digital cushion and
thick, soft fleshy digital pads on the plantar surfaces of the processus mastoideus group (Fig. 4B). Digital cushion
ostrich foot (Weissengruber et al., 2006). The ventral surface images in DICOM format generated from MRI were
of the digital pad was covered by numerous processus processed with Mimics to obtain the primary 3D model (Fig.
mastoideus running in different directions, and of different 5A). The relative location of the three digital cushions
lengths and thickness (EI-Gendy et al., 2011). The digital derived from Hypermesh was in accordance with the
pad of the third toe was thicker and bigger than that of the anatomical dissection (Fig.5B).
fourth toe. The digital pad was relatively easy to separate, Ostrich foot bones
with the internal structure of the digital pad encircled by
Bones serve a number of purposes, such as providing
independent fascia. We processed the digital pads of the third structure and bearing body weight. Nine phalanges and a
toe further, stripping off the superficial fascial membrane to tarsometatarsus provide the framework of the ostrich foot.
expose three banded structures of differing thickness and
length, namely the axial, middle, and abaxial (Fig. 4A). The Tarsometatarsus: The tarsometatarsus of the ostrich foot
largest structure in terms of mass and size was the middle was long and hard, triangular in outline and flattened dorsally
one, followed by the axial and abaxial. Similar to the third (Fig. 6A), making it an irregular bone (Charuta et al., 2013).
toe, dissection of the fourth toe also revealed three banded A shallow ditch was observed on the anteromedial surface
structures of different thickness and length. However the of the tarsometatarsus, traversed by nerves and blood vessels.
digital cushions of the fourth toe were relatively small We split the backbone of the tarsometatarsus crosssectionally
compared with those of the third. Further investigation found and found periosteum, compact bone, cancellous bone, and
that these three yellow objects, the digital cushions, were yellow marrow respectively from exterior to interior
composed of adipose tissue. The digital cushion is formed (Fig. 6B). The far portion of the tarsometatarsus was
composed of the lateral and medial malleoli, both
by a layer of connective tissue in the depth of the dermis of
articular surfaces of which were trochlea-shaped. The
the digital pad, the shape of which is irregular and tubular,
far end of the phalanx and tarsometatarsus constitute the
formed as a result of this species weightbearing only on the
metatarsophalangeal articulation, which consisted of two
tip of its toe.
parts: the medial malleolus of the tarsometatarsus and first
Following separation of the digital pad, incision into phalanx of the third toe formed the first articulation digitorum
the posterior section revealed an internal component that pedis of the third toe and the lateral malleolus of the
was bright red around the tip of the toe, gradually changing tarsometatarsus and first phalanx of the fourth toe formed
from bright red to orange in the direction from tip to posterior the first articulation digitorum pedis of the fourth toe. Each
foot. The outer ring was wrapped in white elastic material, articulation was connected and consolidated by numerous
Fig 4: Digital cushions (1.The middle one; 2.The axial one; 3.The abaxial one; 4.Dermis layer; 5.Processus mastoideus group).
Fig 5: Primary model of digital cushions derived from Mimics (A) and Hypermesh (B)
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Fig 6: The tarsometatarsus (A) and the crosssectionally view (B) (1.Periosteum; 2.Compact bone; 3.Cancellous bone; 4.Yellow marrow.)
sturdy ligaments to maintain its stability. The articular surface
of the proximal extremity of the tarsometatarsus provides
intertarsal articulation with the distal tibiotarsus.
Phalanx: The ostrich has formed a unique foot structure
secondary to adaptation to its permanent existence in a desert
environment. The ostrich foot has only two toes: the third
and fourth. The third toe, which is stout and well developed,
forms a 34° angle with the fourth toe (Schaller et al., 2011),
which is delicate and short. Our study revealed that the ostrich
toe was composed of eight or nine sections (Fig. 7A). The
third toe had four phalanges, from distal to proximal were
the fourth, third, second, and first phalanges with the first
phalanx the largest and the others decreasing in size in turn.
The proximal end of the first phalanx was connected with
the tarsometatarsus to form the metatarsophalangeal
articulation. The third toe had four or five phalanges and the
proximal end of the first small phalanx also connected with
the tarsometatarsus. A metatarsophalangeal pad was found
between the two toes, where the interphalangeal ligament
was distributed. The fifth phalanx of the fourth toe of some
ostriches is degenerated or disappeared.
phalangis was found to be trochlear-shaped, with articular
fossa found on the basis phalangis. The adjacent phalanges
were indirectly connected, enabling bones to move flexibly.
A three-dimensional model of the phalanges (Fig. 7B) was
obtained by importing the CT scan images in DICOM format
into Mimics software for trimming, and then importing them
into RE software (Geomagic Studio).
Articular cartilage: Articular cartilage covers the articular
surface, buffering bone vibration as well as decreasing
friction between articular surfaces (Schaller et al., 2009).
The ostrich foot is composed of numerous intertarsal,
metatarsophalangeal, and interphalangeal articulations.
Each phalanx is composed of basis phalangis,
corpus phalangis, and caput phalangis. In our study the caput
Interphalangeal articulation consists of an articular
surface, articular capsule, articular cartilage, and articular
cavity. Cartilage is distributed over all three articulation types
but is thickest on the intertarsal articulations, followed by
the metatarsophalangeal and interphalangeal. Additionally,
cartilage is thicker proximally on the joint and thinner over
the distal portion. Articular cartilage on the intertarsal
articulation is shown in Fig. 8A. The STL format image of
articular cartilage on the intertarsal articulation, obtained
by MRI and processed by Mimics software, is depicted
in Fig. 8B, with the magnification shown by a red arrow.
Fig 7: Phalanges (A) and the corresponding 3D model (B)
Fig 8: Articular cartilage on the intertarsal articulation (A) and the
corresponding outline obtained from Mimics (B)
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Tendons and Ligaments
Tendons have a continuous avascular collagen
structure (Mellett., 1994). Tendons are white, hard, and
composed of dense connective tissue without contraction
ability, and are always covered with bursa synovialis or
synovial sheath. Ligaments are elastic and bears good stretchproof.
Tendons on the plantar aspect of digits: The location of
the tendons of the ostrich foot could be clearly seen after the
removal of skin and fascia. We separated the flexor tendons
and numbered the tendons on the plantar aspect of the
phalanges (Fig. 9A). We concluded that the third and fourth
toe had three and two flexor digitorum longus pedis tendons,
respectively. These tendons originated as attachments to
muscles and terminated in connection with the phalanges.
For the third toe, the outermost flexor digitorum
longus pedis tendon had two small branches at the terminal
end. A porose portion of flexor tendon in the intermediate
layer also divided into two terminates at the inner and outer
plantar aspect of the proximal end of the third phalanx. The
deeply situated porose flexor tendon terminated at the root
segment of the toenail. These three flexor tendons separated
after passing through the tendon sheath trochlea on the
posterior aspect of the metatarsophalangeal joint, stretching
upwards after passing the tarsometatarsus.
For the fourth toe, porose flexor tendon was
distributed in the shallow layer and divided into three
branches (Fig. 9A), formed by a medial flexor tendon
terminating at the proximal end of the first phalanx, a middle
one significantly larger than the other two terminating at the
distal end of the first phalanx, and a distal flexor tendon
terminating at the distal end of the second phalanx. The flexor
digitorum longus pedis tendon of the fourth toe was found
in the deep layer, and was small in size. A porose flexor
tendon which thrust into the surface layer in the proximal
end of the first phalanx terminated at the distal phalanx of
the fourth toe, namely the fifth phalanx.
Tendon on the dorsal aspect of digiti pedis: Fig. 9B shows
the distribution of tendon on the dorsal aspect of the digiti
pedis. It is obvious that the number and size of the tendons
on the dorsal aspect was smaller than on the plantar aspect.
Pulling the extensor digitorum longus pedis tendons tight
resulted in the third and fourth toe extending, as the dorsal
aspect distributes the extensor tendons, and the plantar aspect
distributes the flexor tendons.
The extensor digitorum longus pedis tendon
extended downward along the dorsal aspect of
tarsometatarsus, and separated into two branches at the
proximal end of tarsometatarsus, inner and outer branches
that control the third and fourth toe, respectively. The inner
tendon terminated at the proximal end of the first phalanx of
the third toe, and the lateral tendon divided into two near
the ankle notch (labeled 1b1 and 1b2 in Fig. 9A). Tendon
1b1, shown extending towards the third toe, terminated at
the distal end of the fourth phalanx, while 1b2, extending
towards the fourth toe, terminated on the dorsal aspect of
the distal end of the fourth phalanx. The inherent flexor
tendon of the third toe terminated at the distal end of the
fourth phalanx of the third toe, with collateral ligaments
connecting the two phalanges found inside and outside the
second and fourth phalanges of the third toe.
Ligament between digiti pedis: Amplifying the digital
region, it became clear that annular ligament covered the
flexor tendon at the proximal end of the first phalanx of the
two toes; the annular ligament is labeled as 6 (Fig. 9A). Two
distinct interphalangeal ligaments could be seen after
dissection of the foot web, constituting a “triangle” structure
together with the phalanges and controlling range of motion
of the two phalanges. Mahdy et al (2010) concluded that the
included angle of the two toes was a maximum value of 34°
when the interphalangeal ligament is intact, by controlling
the extension of the two toes; however they only considered
the coarser medial interphalangeal ligament and ignored the
finer lateral interphalangeal ligament in the anatomy of the
lower extremity of the ostrich foot. We explored the effect
of the interphalangeal ligaments on the two toes. As part of
the experimental process, we kept the position of the third
toe unchanged and controlled the position change of the
Fig 9: (A) Tendon on the plantar aspect of digit (1.Porose flexor tendon; 2.Porose pieced flexor tendon; 3. Tendon flexor digitorum longus pedis;
4.Porose flexor tendon; 5.Tendon flexor digitorum longus pedis; 6. Annular ligament; 7. Interphalangeal ligament). (B) Tendon on the dorsal
aspect of digiti pedis (1.The extensor digitorum longus tendon(1a:medial aspect; 1b:lateral aspect; 1b1:terminates at the lateral aspect;
1b2:terminates at the lateral aspect) 2.The inherent extensor tendon; 3.The lateral collateral ligament).
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fourth toe with white cotton thread functioning as a tendon.
The medial and lateral interphalangeal ligaments both
become taut when pulled outward (Fig. 10A). The two
interphalangeal ligaments both became slack when the thread
was pulled inside (Fig. 10B). The finer lateral interphalangeal
ligament become slack and the coarser medial
interphalangeal ligament become taut when pulling along
the dorsal aspect of the toe (Fig. 10C). The finer lateral
interphalangeal ligament became taut and the coarser medial
interphalangeal ligament became slack when pulling along
the posterior aspect of the toe (Fig. 10D). This showed that
the two interphalangeal ligaments together control abduction
and adduction of the third toe, with only the medial
interphalangeal ligament limiting the toe moving dorsally,
and the lateral ligament limiting the position of the third toe
moving backward. When examining the function of each
interphalangeal ligament more closely, we found that the two
interphalangeal ligaments together controlled the movement
of the fourth toe, with the position of the toe controlled by
the lateral interphalangeal ligament, and the medial
interphalangeal ligament having almost no effect on it.
481
Collateral ligaments were found between the
phalanges of the third and fourth toe (Fig. 11A ,B),
reinforcing articular function. The interphalangeal
articulation was covered by the joint capsule, with collateral
ligaments were found on each side, maintaining the stability
of the interphalangeal joint during motion.
Prior work has documented anatomical information
on ostrich foot bones, muscle, and tendons (Baciadonna et
al., 2010; Hahulski et al., 1999; Pavaux et al., 1995; Smith
et al., 2010). However, no anatomical study on the phalanges
or the entire ostrich foot has been made, limiting
understanding of its internal structure and function as a
locomotor system entity. We studied the morphological
structure of ostrich foot using anatomical dissection and
medical imaging. We found eight or nine phalanges and a
tarsometatarsus, with the third and fourth toe having four
and five phalanges respectively. Tendon sheaths of different
sizes were found around the articulations, playing a role in
reducing the friction between tendon and bone. Two
interphalangeal ligaments constituted a triangular structure
together with the phalanges, controlling angle and range of
Fig 10: Response of the two interphalangeal ligaments under external force.
Fig 11: Ligament between the ostrich phalanges (1.Collateral ligaments; 2.Interphalangeal ligaments; 3.The cutting-off ligaments; 4.The intact ligaments).
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INDIAN JOURNAL OF ANIMAL RESEARCH
movement of the two toes. In summary, our study determined
the layout of each part of the ostrich foot, including skeleton,
articular cartilage, ligament, and tendon. The study report
not only contributes to revealing the superior locomotor
mechanism of the ostrich foot, but also provides a foundation
for further study of structural modeling and assembly in
ostrich foot motion system FE analysis. This has provided
preliminary preparation for the study of high-speed, energysaving bionic walking mechanisms and the bionic foot
structure of the bipedal robot.
However, some limitations are worth noting. The
complicated internal structure provided certain difficulties
for anatomical analysis, and limitations to experimental
conditions and time meant that articular cartilage was not
analyzed in detail. Articular cartilage reduces friction
between two adjacent bones and buffers shock in the process
of motion; further exploration of the ostrich foot should detail
this.
ACKNOWLEDGEMENTS
The authors are grateful for the financial support
by the National Natural Science Foundation of China
(No. 51275199) and the Science and Technology
Development Planning Project of Jilin Province of China
(Project No. 20140101074JC).
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