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Israel Journal of Veterinary Medicine  Vol. 70 (4)  December 2015 Ozudogru, Z. 46
A Study of the Morphological Structure of the Syrinx of the Sparrowhawk
(Accipiter nisus)
Ozudogru, Z.,
1
Balkaya, H.,
1
* Kara, A.
2
and Ozdemir, D.
1
1
Ataturk University, Faculty of Veterinary Medicine, Department of Anatomy, Erzurum, Turkey.
2
Ataturk University, Faculty of Veterinary Medicine, Department of Histology, Erzurum, Turkey.
*
Corresponding Author: Dr. Hulya Balkaya, Ataturk University, Faculty of Veterinary Medicine, Department of Anatomy, Erzurum, Turkey.
Tel: +90-442-2315532. E-mail: balkayaibrahim@hotmail.com
ABSTRACT
Sparrowhawks are commonly used for quail hunting in northeastern Turkey. Despite it is importance in
Turkey, there is a dearth of information concerning the anatomy of the syrinx in the sparrowhawk. Te
objective of this study was to assess the structure and morphological diferences of the sparrowhawk’s syrinx
from those of other avian species. Te syrinx, which is the main source for vocalization for birds is located
on the caudal end of the trachea. To the best knowledge of the authors this is the frst study of the syrinx
of the Sparrowhawk. Te syrinx of the sparrowhawk was found to be of the tracheobronchial type and
consists of four tracheosyringeal cartilages cartilage and fve bronchosyringeal cartilages. For the histological
specimens, syrinx tissues were stained with Crossman modifed triple stain for histological evaluation,
Verhoef’s elastic fbers stain for elastic fber density, and Alcian blue (pH: 2.5) and periodic acid Schif
(PAS) stain for mucopolysaccharide and neutral mucins, respectively. Te pessulus of hyaline cartilage was
found to be covered with pseudo-stratifed epithelium. Te medial labia and medial tympaniform membrane
consisted of double-ply layers of epithelium, which consisted of collagen and elastic fber layers. In addition,
the bronchosyringeales muscle consisted of extrinsic muscles only. In conclusion, the results of this study
may contribute to knowledge of morphologic and histologic structure and variations between bird species.
Keywords: Sparrowhawk; Accipiter nisus; Syrinx; Morphology; Vocalization
INTRODUCTION
Bird vocalization has an important role in distinguishing bird
species. Birds are classifed as passerine and non-passerine,
according to structural diferences of their vocal organs (1).
Te syrinx, known as the caudal larynx, is found in passerine
birds (2-4). Te syrinx lies between the trachea and primary
bronchi at the level of the second and third thoracic vertebrae
(5) and consists of three types of cartilage: tracheal, bronchial
and tracheobronchial, according to their origin (6-8). Te syr-
inx is the sound-producing organ, and it shows histological
and anatomical diferences according to bird species (9, 10).
Te syrinx creates a myoelastic-aerodynamic sound-source
for birds. Aerodynamic energy is converted into acoustic
energy with the help of active and passive components. Te
longitudinally located labia are held in a preliminary position
by syringeal muscles and creates a vibration when air passes
through, playing a crucial role in producing sounds (11-13).
Te syrinx consists of tympanum and tracheosyringeales
in the shape of a “C” and bronchosyringeales consisting of
half-rings of cartilage. Te pessulus in the cavum syringes
consists of a double-layer mucous membrane extending
dorso-ventrally from the primary bronchus’ median wall.
Syringeal muscles consist of two muscle structures: tra-
cheolateral and sternotracheal (14). However, histologic
diferences in the syrinx mucosa’s epithelium are present in
avian species and this epithelium consists of double-layer,
Israel Journal of Veterinary Medicine  Vol. 70 (4)  December 2015 47 Morphology of Sparrowhawk’s Syrinx
squamous (15), columnar (16) and ciliated pseudostratifed
columnar epithelium (10).
Quail hunting with sparrowhawks is a traditional sport
in northeaster Turkey and despite it is importance, there
is a dearth of information concerning the anatomy of the
syrinx in the sparrowhawk. Te current study was aimed to
investigate macroanatomical and histological structure of the
sparrowhawk’s (Accipiter nisus) syrinx. Structures detected in
this study included cartilage tissue and the distribution of
collagen and elastic fbers in the syrinx in addition to the
epithelial tissue covering its surface.
MATERIAL AND METHODS
Nine untreatable predatory sparrowhawks (Accipiter nisus)
whose wings or legs were broken were received from the
animal hospital at Ataturk University, Faculty of Veterinary
Medicine, Erzurum-Turkey between the years of 2011–2013.
Teir weights ranged from 150 to 250 g. Te sparrowhawks
were euthanized under ether anesthesia and syrinx tissues
were removed 3 mm cranial of tracheal bifurcation.
Syrinx tissues were fxed in neutral bufered 10% for-
malin fxative for 4 days. Te fxed tissues were dehydrated
in a graded series of ethanol and embedded in parafn.
Parafn-embedded tissues were serially sectioned with 5 µm
thickness. Te sections were stained with Crossman modi-
fed Mallory’s triple stain for histological examination. In
addition, Verhoef’s elastic fbers stain was used to determine
elastic-fber density, and Alcian
blue (pH 2.5) and Periodic acid
Schif (PAS) stains were used
to determine density of neutral
and mucopolysaccharide goblet
cells in the syrinx. Histological
micrographs were taken by
high-power light microscope
(Nikon Eclipse i50, Japan).
RESULTS
Te syrinx was observed to
be situated at the level of the
heart, at the level of the 14
th
cervical and 1
st
to 2
nd
thoracic
vertebrae. It was formed as a
result of modifcation of the
trachea’s terminal section and the beginning of the primary
bronchi (Figure 1A). In addition, the dorsal syrinx was con-
nected to the medial bronchial lumen beginning at the pes-
sulus, progressing ventrally and continuing to the medial labia
(ML), the sides of which were covered with epithelium and
the medial tympaniform membrane (MTM), both sides of
which, in turn, were covered with epithelium. At the medial
lumen, muscle fbers were connected to cartilagenous rings.
Also, it was observed that these muscle fbers were connected
to the ML and extending to the bronchial lumen on the ven-
tral side of syrinx (Figure 1). No goblet cells were observed in
MTM and ML epithelial tissue as judged by PAS and Alcian
blue (pH: 2.5) staining.
Te pessulus was observed as a hyaline cartilage divid-
ing the bronchial lumen into two parts dorsally and covered
with loose connective tissue (Figure 1B). Te lamina propria
consisted of loose thin connective tissue and its epithelial
tissue had a ciliated pseudostratifed columnar or respira-
tory epithelium. As a result of PAS and Alcian blue staining,
PAS-positive goblet cells in small quantities were seen in the
pseudostratifed columnar epithelial (Figure 1C).
Medial labia and medial tympaniform membrane: While
collagen fbers in the ML between two the epithelia and in
the MTM were observed as being vertically placed, it was also
observed that they formed a double-ply form [superfcial layer
(SL) and deep layer (DL)]. It was observed that collagen-fber
density increased throughout the bronchial lumen (Figure 2).
Figure 1: Micrographs of sparrowhawk syrinx, A: View of longitudinal drawing, B: Pessulus, medial
labia and medial trypanium membrane, C: Epithelium of pessulus, PAS staining. a1-a4: Cartilages of
tracheosyringeal rings, a2-a4: Tympanum rings, b1-b5: Cartilages of bronchosyringeal rings, ML: Medial
labia, MTM: Medial trypanum membrane, Ty: Tympanum, P: Pessulus, Arrow head: Goblet cells in the
epithelium of pessulus.
Research Articles
Israel Journal of Veterinary Medicine  Vol. 70 (4)  December 2015 Ozudogru, Z. 48
While the dorso-ventrally placed collagen fbers were encoun-
tered in the superfcial layer, both cranio-caudal and dorso-
ventrally placed collagen fbers were encountered in the deeper
layer. Elastic fbers were seen to be located the epithelial tissues
of the ML and MTM sections. It was also observed that elastic
fber density increased toward the interclavicular air-sac section
and that elastic fbers were situated between sub-epithelial
tissues. While these fbers showed a cranio-caudal placement,
it was observed that the fbers in the superfcial layer were
dorso-ventrally oriented (Figure 3).
Tracheal and bronchial (cartilagines bronchosyringeales)
rings: Hyaline cartilage was observed to cover the syrinx ex-
ternally. Tube-shaped tracheosyringeal cartilage commingled
with each other and with three other types of cartilage,
tracheal, bronchial and tracheobronchial, but not with the
hyaline cartilage, which was ossifed to create the tympanum.
It was observed that cartilagines bronchosyringeales consisted
of fve cartilage rings in the shape a “C”. It was also observed
that the lateral tympaniform membrane was located between
the last tympanum ring and the frst cartilage bronchosyrin-
geal ring (Figure 1 and Figure 4).
While extrinsic sternotracheal and tracheolateral muscles
were found in the syrinx, it was also observed that tracheo-
lateral muscles consisted of skeletal muscles with a circular
Figure 2: Micrograph of syrinx medial labia for collagen fbers, A and
B: Collagen fber of medial labia, SL: Superfcial layer, DL: Deep layer,
Crossman modifed triple staining.
Figure 4: Dorsal view of syrinx, a1-a4: Cartilages of tracheosyringeal
rings, a2-a4: Tympanum, b: Cartilages broncosyringeal rings, Black
arrows: Sternotracheal muscle, White arrows: Tracheolateral muscle,
MTM: Membrana tympaniformis medialis, MTL: Membrana
tympaniformis lateralis, P: Pessulus, (*): Ligamentum interbronchiale,
RB: Right bronchiole, LB: Left bronchiole, T: Trachea.
Figure 3: Micrograph of syrinx medial labia for elastic fbers, A and
B: Elastic fber of medial labia, SL: Superfcial layer, DL: Deep layer,
Verhoef’s elastic fbers staining.
Research Articles
Israel Journal of Veterinary Medicine  Vol. 70 (4)  December 2015 49 Morphology of Sparrowhawk’s Syrinx
appearance. In addition, it was observed that these muscles
were connected to bronchial cartilage rings playing a part in
preventing deformation of the bronchial labia during move-
ment (Figure 4).
DISCUSSION
In the current study, the anatomical and histological char-
acteristics of the syrinx were studied for the frst time in
sparrowhawks. Te morphologic structure of the syrinx has
been investigated in many previous studies (8, 17-19), but this
is the frst study in the syrinx of Sparrowhawk.
As found in many studies of other avian species (7, 8,
18-21), the syrinx of sparrowhawks was the tracheobron-
chial type. Te determination of the current study that the
lateral tympaniform membrane was found between the last
tympanum ring and the frst cartilage bronchosyringeal ring
agrees with data from other bird species such as long-legged
buzzard, male mallard and ostriches (7, 8, 18), but conficts
with the data for sea gulls (22), which found that the lateral
tympanum membrane was located between the frst and sec-
ond bronchosyringeal rings. It is appears that these varieties
arise from species diference.
It has been reported that the tympanum consists of fve
trachea rings in the chicken (14, 23), in the new world pigeon
(17), the duck (10) and in the seagull (24) and consists of
three trachea rings in the ostrich (18) and the long-legged
buzzard (8). Te current study determined that the spar-
rowhawk tympanum consisted of three trachea rings, like
the ostrich and the long-legged buzzard.
Our anatomical and histological data determined that
tracheolaryngeal cartilage was tube shaped and commingled
with each other and the three other types of cartilages,
tracheal, bronchial and tracheobronchial, but not with the
hyaline cartilage, which was ossifed to create the tympanum.
In addition, cartilagines bronchosyringeales consisted of fve
pieces of cartilage in the shape of a “C”. Frank et al. (25)
stated that cartilagines bronchosyringeales consisted of bron-
chial and tracheal rings that ossifed with age in male mal-
lards (25) and pigeons (26). Warner et al. (27) and Morejohn
(28) stated that the number of these cartilages varied from
one to six in chickens. Getty et al. (21) stated this cartilage
was in four pieces in the shape of a “C” and were connected
to the pessulus of fowl, duct, lizard and chicken (21, 27, 28).
It has been reported that the pessulus consists of connec-
tive tissue in the new world pigeon (17) and ostrich (18) and
consists of cartilage in chickens (29) and of an ossifed form
of cartilage in ducks (27) and passerines (30). In the current
study, it was observed that the pessulus consists of hyaline
cartilage resting on muscular mucosa. In addition, it was
determined that the pessulus was covered with respiratory
epithelium, and on histological analysis, PAS-positive (neu-
tral) goblet cells were seen interspersed within the epithe-
lium. It was also observed that this epitheliium of the lateral
pessulus’s was in the columnar form. Although Savart (31)
reported that diferent pessulus structures can be encountered
in avian species and that this structure contributes to voice
production, Warner (27) stated that the structure doesn’t have
vibratory ability, so it cannot be the source of sound.
Evaluation of data from the current study determined the
existence of elastic and collagen fbers between the medial
labia and medial tympaniform membrane tissues. It has been
reported that this double-ply structure found in labium plays
a part in tension of the labium (21). Previous studies have also
reported that the double-ply structure increases the elasticity
of dense elastic fbers, especially those found in deep lay-
ers of labium, and in this way it may ease frequency control
(30). Te current study concluded that density diferences
in double-ply elastic and collagen layers, situated between
two epithelial layers plays a role in creating the extracellular
matrixes of the visco-elastic structure.
From the present study it was determined that syrinx
muscles of the sparrowhawk consisted of extrinsically circular
skeletal muscles. It was observed that while these muscles
were connected to bronchial cartilage rings in the medial
lumen, they were also connected to ML extending up to
the bronchial lumen on the ventral side. Yildiz et al. (19)
reported that the syrinx muscles were extrinsic and intrinsic.
While it has been reported that intrinsic muscles were found
in passerines and parrots (32), it also has been reported that
extrinsic muscles were found in domestic fowls (33), which
agrees with our fndings about the sparrowhawk syrinx.
It can be understood that these diferences in muscle
structure contribute to the creation of diferent sounds among
bird species, since these muscle-structure diferences deter-
mine the characteristics of the vibrations that play a part in
sound creation. Te current study presents the characteristic
and morphologic features of the sparrowhawk’s syrinx, thus
diferentiating it from other bird species. Although the tissues
of the sparrowhawk’s syrinx showed some similarities with
Research Articles
Israel Journal of Veterinary Medicine  Vol. 70 (4)  December 2015 Ozudogru, Z. 50
some other passerine bird species, it was clear that distinct
histological and anatomic diferences do exist.
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