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Histomorphological Study of Syrinx of Black Francolin (Francolinus francolinus) in Iraq

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  • Faculty of Veterinary Medicine - University of Baghdad
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Histomorphological Study of Syrinx of Black Francolin (Francolinus francolinus) in Iraq

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Abstract | The syrinx of male and female adult black francolin was studied. Seven adult males and females weighted (300) gm to (265) gm respectively, were captured from the village of Baghdad. Macroscopic examination of syrinx was done under using stereomicroscope image analysis. Histological sections stained with heamatoxylin and eosin stain, Massson’s trichrom stain; Periodic acid schiff; Alcian blue stain; and combined Aldehyde fuchsin-Alcian blue stain. Results, the syrinx was tracheobronchial in type; it was consisted from: Tympanum, Tracho-Syringeal part, and Brancho-Syringeal part. In addition, there were lateral and medial vibrating membranes, pessulus and triangular voice. The syrinx was lined by the pseudostratified ciliated columnar epithelia with goblet cells. Groups of goblet cells are formed intra epithelia mucous glands with sulphated mucin. Complete cartilaginous rings were formed upper part of syringeal skeleton, whereas, C shaped cartilages formed its middle and distal parts. Medial and lateral labia were protruded into the syringeal lumen. Sexual dimorphism were obtained, the males had significantly narrow tympanum and right syringeal passage with thicker syringeal labia than female.
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INTRODUCTION
Birds have evolved a unique phonatory organ (syrinx),
which is highly variable in structure between species.
Like the mammalian larynx, regulates airow and action
inuences acoustic parameters of syrinx is controlled by
muscles during closing and opening of the passage air-
ways (Andersson, 1994; Podos et al., 2004; Edwards et al.,
2005). e classication of birds depended on presence or
absence the basis structure of syrinx or their musculature
(Tsukahara et al., 2008). Some birds vocalize all year long
while others call only during the mating season (Zhang et
al., 2009). And this is also accompanied by alteration in
the functional morphology of certain organs that respon-
sible for sound generation. Nevertheless, to what level of
gender dimorphism that aects the control vocal center, it
is still indistinct. Tympanum diers in birds, its consists
from two rings in the Japanese quails (Cevik-Demirkan
et al., 2007) and ve in the pigeons (Yildiz et al., 2005).
Histological and morphological syringeal variation in the
songbird has not been inspected. However, such chang-
es have been conrmed in mammalian species where they
lead to clear gender dimorphism in the characters of voice
(Suthers, 2004). In the songbirds the labia play a major
role in sound generators. Particularly, laterally location la-
bia are eective into vibration (Riede and Goller, 2010).
e wedge-shaped pessulus divided the airways of syrinx
(Kabak et al., 2007). e males black francolin have in
addition to its exterior dierences with female, they have
characteristic high loud voice especially in breeding season
unlike females that keep with inaudible sound (Prince et
al., 2011). ere is a dearth of information concerning the
anatomical and histological aspect of syrinx in this bird,
and whether there is any dierence between the sexes, es-
Research Article
Abstract | e syrinx of male and female adult black francolin was studied. Seven adult males and females weighted
(300) gm to (265) gm respectively, were captured from the village of Baghdad. Macroscopic examination of syrinx
was done under using stereomicroscope image analysis. Histological sections stained with heamatoxylin and eosin
stain, Massson’s trichrom stain; Periodic acid schi; Alcian blue stain; and combined Aldehyde fuchsin-Alcian blue
stain. Results, the syrinx was tracheobronchial in type; it was consisted from: Tympanum, Tracho-Syringeal part, and
Brancho-Syringeal part. In addition, there were lateral and medial vibrating membranes, pessulus and triangular voice.
e syrinx was lined by the pseudostratied ciliated columnar epithelia with goblet cells. Groups of goblet cells are
formed intra epithelia mucous glands with sulphated mucin. Complete cartilaginous rings were formed upper part
of syringeal skeleton, whereas, C shaped cartilages formed its middle and distal parts. Medial and lateral labia were
protruded into the syringeal lumen. Sexual dimorphism were obtained, the males had signicantly narrow tympanum
and right syringeal passage with thicker syringeal labia than female.
Keywords | Black francolin, Tympanum, Vibrating membrane, Syrinx, Labia
Muna Hussain al-aaMeli1, KHalid KaMil KadHiM2*
Histomorphological Study of Syrinx of Black Francolin (Francolinus
francolinus) in Iraq
Editor | Kuldeep Dhama, Indian Veterinary Research Institute, Uttar Pradesh, India.
Received | January 10, 2017; Accepted | February 16, 2017; Published | February 28, 2017
*Correspondence | Khalid Kamil Kadhim, Department of Anatomy and Histology, Faculty of Veterinary Medicine, University of Baghdad-Baghdad-Iraq; Email:
khalidkamkad@yahoo.com
Citation | Al-Aameli MH, Kadhim KK (2017). Histomorphological study of syrinx of black francolin (francolinus francolinus) in Iraq. Adv. Anim. Vet. Sci. 5(2):
92-99.
DOI | http://dx.doi.org/10.14737/journal.aavs/2017/5.2.92.99
ISSN (Online) | 2307-8316; ISSN (Print) | 2309-3331
Copyright © 2017 Al-Aameli and Kadhim. is is an open access article distributed under the Creative Commons Attribution License, which permits unrestrict-
ed use, distribution, and reproduction in any medium, provided the original work is properly cited.
1Department of Anatomy and Histology, Faculty of Veterinary Medicine, University of Kerbala-Kerbala-Iraq; 2De-
partment of Anatomy and Histology, Faculty of Veterinary Medicine, University of Baghdad-Baghdad-Iraq.
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pecially that males have characteristic high voice. For this
reason, this experiment was designed.
MATERIALS AND METHODS
Seven males and females of black francolin weighted (300)
gm to (265) gm respectively, which captured from the vil-
lage of capital Baghdad were used in this study. e birds
euthanized by intra muscular administration of diazepam
(1mg/1kg) combined with ketamine HCL (30Mg, 1Kg).
After thoracic incision, the syrinx are collected and xed in
the 10% neutral buer formalin. Anatomical examination
was done using dissection microscope (Kruss Ootronic,
Germany) provided by camera (SMZ 1500 digital cam-
era). Longitudinal and cross sections were prepared histo-
logically. Routine heamatoxylin and eosin stain were used
in addition to other special stain (Massson’s trichrom stain;
PAS; Alcian blue stain; Combined Aldehyde fuchsin-Al-
cian blue method) to give more histological details, and
Alcian blue-Alizarin red technique to recognize the ossi-
cation of hyaline cartilage (Bancroft and Stevens, 2012).
e parameters that have been measured are the diameters
of syringeal passages and diameters of the lateral trachealis
and sternotrachealis. In addition estimation of the thick-
ness of tympanic (vibrating) membranes, labia thickness,
pessulus and triangular voice area were done.
STATISTICAL ANALYSIS
e collected data were represented by mean ± standard
deviation. Comparisons were done between male and fe-
male. e mean of dierences between data were estimated
by independent t test using SPSS version 20.
RESULT AND DISSCUSION
Syrinx of black francolin was tracheobronchial in type;
it consists from three dierent groups: Tympanum, Tra-
cho-Syringeal part, Brancho-Syringeal part (Figure 1 and
2). In addition, there were branchidesmus (interbronchial
ligament), lateral and medial vibrating membranes, pessu-
lus and triangular voice. Similar to this syringeal division
was mentioned in turkeys (Khaksar et al., 2012). Mean-
while, in the other song birds, the syrinx is consisted from
either the tracheal or bronchial part or both (Seller, 2002).
ree incomplete rings were formed tympanum of fran-
colin syrinx. e last rings of tympanum bifurcate into two
modied rings to form the tracho-Syringeal part (three
rings), this followed by last part of syrinx (Brancho-Syrin-
geal) which consisted from four incomplete rings (Figure
3). Comparing with sea gulls, the tympanum is consisted
from ve rings (İnce et al., 2012), and in long-legged buz-
zard are two rings (Kabak et al., 2007).
Figure 1: Macrograph of black francolin syrinx (ventral
view): showing the parts of syrinx that formed by:
tympanum (tp); trachea-syringeal part (ts); broncho-
Syringeal part (bs); triangular voice (tv); ligament (ig);
sternotrachilis (st); lateral trachealis (lt); primary bronchi
(br).
Figure 2: Micrograph of syrinx of male black francolin
showing: trachea (t); tympanum cartilages (tc); trachea-
syringeal cartilages (ts); pessulus (p); right passage (r); left
passage (l); lateral labium (ll); medial labium (ml); lateral
vibrating membrane (lm); medial vibrating membrane
(mm); triangular voice (tv); sternotrachealis (st): ligament
(li). H&E.
In francolin, the tympanum was lined by the pseudostrat-
ied ciliated columnar epithelia with goblet cells, the later
however tended to aggregates in middle and lower parts
of syrinx to form intra epithelia mucous glands which ap-
peared in dierent numbers and sizes (Figure 4). ese
glands or the goblet cells showed positive reaction with
PAS stain and Alcian blue stain (Figure 5). However, these
glands appeared magenta due to its contains of sulphat-
ed mucin (Figure 6). In Bursa roller pigeon this mucosa is
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compose of pseudostratied prismatic epithelium or bis-
tratied squamous, columnar (Yıldız et al., 2005; Demir
kan et al., 2006) had recorded that the gland and goblet
cells increased toward the broncheo-syringeal part in bursa
roller pigeon. In birds, (Bacha and Bacha, 2000) and goose,
(Jeery, 2004) mentioned that plentiful goblet cells consti
tuted the intraepithelial glands which are contain mucin
with a predominance of sulphate ester salt for protection.
In the current study, the lamina propria-submucosa was
consisted from loose connective tissue with high amount
of elastic bers which showed continuity with the peri-
chondrium that surround the hyaline cartilage. e chon-
drocytes of the later located inside the lacunae and sur-
rounded by homogenous matrix. ese hyaline cartilages
were mostly ossied at its center (Figure 7). Similar results
were reported by (Aughey and Frye, 2001) however, there
was partly ossied perichondrium of the syringeal hyaline
cartilages in avian.
Figure 3: Macrograph of syrinx (dorsal view) of black
francolin: showing tympanum which formed by (1, 2, 3,
yellow color) C shaped cartilages; trachea-syringeal part
which formed by (1, 2, 3, black color) C shaped cartilages;
pessulus (p); ligament (lig.) Alcian blue-Alizarin red
technique.
e tympanum diameter showed no dierence between
genders (Figure 8). Meanwhile, the diameter of right
passage appeared signicantly (P<0.05) narrower in male
(Figure 9). In contrast, the left passage showed no dier-
ence between genders (Figure 10). ese data conceded
with (Suthers and Zollinger, 2004) report that in songbird,
the left passage is source sound produces lower than the
right side.
In the present study, the medial and lateral labia were thick-
ening of the mucous membrane that protruded into the
syringeal lumen between tympanum and the broncheo-sy-
ringeal parts of syrinx. e medial labia attached with the
pesselus cranially and continue with thin medial tympanic
(vibrating) membranes caudally, in which the later has at-
tached with the bronchial wall medially. Meanwhile, the
syringeal muscles attached directly with medial labia (Fig-
ure 11).
Figure 4: Micrograph of syrinx epithelium of black
francolin. Whereas, cilia (c); pseudostratied ciliated
columnar epithelia (ss); aggregation of goblet cells (intra
epithelia mucous glands) (g); lamina propria (lp); hyaline
cartilage (hc). Massson’s trichrom stain.
Figure 5: Micrograph of syrinx epithelium of black
francolin. Showing mucin reaction of the mucous epithelia
(upper with PAS) and (lower with Alcian blue stan),
whearas, trachea-syringeal part (ts); aggregation of goblet
cells (intra epithelia mucous glands) (g); lamina propria
(lp).
e epithelium lining these labia had characteristic fea-
tures, it not appeared as typical stratied columnar cells,
and these cells appeared lower in height and more com-
pact. is may be due to continues direct eects of the air
ow on this part of mucosa. e extra cellular matrix of
these labia was consisted mainly from collagen and smooth
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muscle bers. ese bers were oriented randomly particu-
larly in the supercial layers (Figure 12).
Figure 6: Micrograph: Medial vibrating membranes
(mvm) notice the folded; lateral vibrating membranes
(lvm); tracheo-syringeal cartilages (tsc); triangular voice
(tv); sternotrachealis ligament (lig). (Combined Aldehyde
Fuchsin-Alcian blue method).
Figure 7: Micrograph of male black francolin syrinx.
Showing ossication of the syringeal cartilages (bc);
pseudostratied ciliated columnar epithelia lining the
lateral vibrating membrane (lm) and medial vibrating
membrane (mm); right syringeal passage (rp); primary
bronchi (pb); triangular voice (tv); sternotrachealis (st).
Massson’s trichrom stain.
e right and left medial labia and right lateral labia of
male were signicantly (P<0.05) thicker than female (Ta-
ble 1). (Riede and Goller, 2015) recorded that the labium
is dier in shape and size between the female and male
which is generally thicker in male. Related to these results,
(Fee, 2002) suggested that in songbird, the labia of right
side is source of sound and has higher resonance peaks
Figure 8: Tympanum diameter in both male and female
black francolin. Values represent means±SD. Dierent
letters means signicantly (P<0.05) dierent. Where,
male (m); female (fe).
Figure 9: Diameter of the right syringeal passage in
both male and female black francolin. Values represent
means±SD. Dierent letters means signicantly (P<0.05)
dierent. Where, male (m); female (fe).
Figure 10: Diameter of the left syringeal passage in
both male and female black francolin. Values represent
means±SD. Dierent letters means signicantly (P<0.05)
dierent. Where, male (m); female (fe).
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Figure 11: Micrograph: Longitudinal section of the
syrinx in the male black francolin showing: medial labia
(ml); lateral labia (ll); lateral vibrating membranes (lvm);
medial vibrating membranes (mvm); tracheo-syringeal
part (ts); tracheo-syringeal cartilages (tsc); triangular voice
(tv); syringeal muscle (sm); broncheo-syringeal parts (bs).
(Combined Aldehyde Fuchsin-Alcian blue method).
Figure 12: Micrograph: Syringeal labia of the male black
francolin showing: medial labia (ml); lateral labia (ll);
epithelium (ep); lamina propria (lp); muscle bers (mf );
passage of the tracheo-syringeal part (ts). (Combined
Aldehyde Fuchsin-Alcian blue method).
than those of left side. Furthermore, (Gasser et al., 2006)
explained that the extra cellular matrix components (elas-
tic and collagen bers) of this labium were general fea-
ture design in organs to accommodate stress. In addition,
(Suthers, 2004) recorded that the labia of the syrinx in pas-
serine species appear as cushions of loose connective tissue.
In the current study, the bronchosyringeal part of black
francolin syrinx is consisted from four C shaped cartilages.
Whereas this part is composed from 7 cartilage rings in se-
Table 1: the thickness of syringeal labia of black francolinus
(male and female).
Thickness
left lateral
labia (µm)
Thickness
right lat-
eral labia
(µm)
Thickness
left medial
labia (µm)
Thickness
right me-
dial labia
(µm)
Male 170±6
a
191±26
a
176±19
b
193±10
a
Female 152±21
a
156±18
b
109±22
c
166±14
b
e data represented as (mean ± SD), (dierent letters) mean
signicant dierent at (P ≤ 0.05) within rows and between male
and female.
a gulls (İnce et al., 2012). In present study, the medial (in-
ternal) and lateral (external) vibrating membranes of the
brancheosyringeal part were lined by similar epithelia.
However, the medial vibrating membrane seemed more
folded than the lateral one, may be due to eects of mus-
cle contraction at this part when the hyaline cartilage had
replaced medially by thin layers of smooth muscles bers
with ne collagen and elastic bers (Figures 6). e ep-
ithelia of internal and external tympanic membranes in
male had dominantly thicker (P<0.05) than female (Fig-
ure 13 and 14). Concerning this result, (Tshifhiwa et al.,
2011) had suggested that these tympaniforum membrane
lined with a bands of connective tissue that varies in thick-
ness depended on species. And this connective tissue could
modify the syringeal lumen (Brown and Ward, 1990).
e syrinx had clear skeletal muscles bers which repre-
sented by lateral trachealis and sternotrachealis at each side
of the tympanum rings (Figure 1). e diameter of these
muscles through cross sections in males were signicantly
(P˂0.05) higher than females (Figure 15 and 16). ese
can be explained by the eects and action of these muscles
during generation of sound by stretching the syringeal car-
tilages and narrowing the passages. Increases in the diam-
eter of these muscle are recorded in zebra nch song and
Scaup Aythya marila, which is responsible for movements
of trachea (Daley and Goller, 2004; Pierko, 2008). Further-
more, the function of these muscles is thought to adjust the
length of the trachea during (inspiration and expiration)
and control rigidity of the cartilages of the vocal organ
(syrinx) during phonation (Burke et al., 2007).
e Triangular voice was triangular shaped space located
at the bifurcation of trachea between left and right prima-
ry bronchi. e inter-bronchial ligament deemed its base,
while the caudal aspect of pessulus composed its apex.
Meanwhile, the medial vibrating membranes were formed
the lateral borders of the triangle voice (Figure 2). e
male had signicantly (P˂0.05) greater area than females
(Figure 20). Similar Triangular voice shape was found in
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duck (Frank et al., 2007; Pierko, 2008) and in goose (Onuk
et al., 2010).
Figure 13: e lateral vibrating membrane thickness in
the syrinx of both male and female black francolin. Values
represent means±SD. Dierent letters means signicantly
(P<0.05) dierent. Where, male (m); female (fe).
Figure 14: e medial vibrating membrane thickness in
the syrinx of both male and female black francolin. Values
represent means±SD. Dierent letters means signicantly
(P<0.05) dierent. Where, male (m); female (fe).
Figure 15: ickness of sternotrachealis muscle in
both male and female black francolin. Values represent
means±SD. Dierent letters means signicantly (P<0.05)
dierent. Where, male (m); female (fe).
Figure 16: ickness of lateral trachealis muscle in
both male and female black francolin. Values represent
means±SD. Dierent letters means signicantly (P<0.05)
dierent. Where, male (m); female (fe).
Figure 17: Micrograph: e Pessulus (Longitudinal
section) of the syrinx in female black francolin. Notice,
elongate triangle pessulus showing ossication in most of
its parts. Masson´s trichrome stain.
Figure 18: Micrograph: e Pessulus (Longitudinal
section) of the syrinx in male black francolin. Notice, short
wide triangle pessulus showing ossication in most of its
parts. Masson´s trichrome stain.
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Figure 19: Pessulus area of syrinx in both male and female
black francolin. Values represent means±SD. Dierent
letters means signicantly (P<0.05) dierent. Where, male
(m); female (fe).
Figure 20: Triangular voice area of syrinx in both male
and female black francolin. Values represent means±SD.
Dierent letters means signicantly (P<0.05) dierent.
Where, male (m); female (fe).
rough the longitudinal sections of syrinx of black fran-
colin, the pessulus illustrated mostly as ossied cartilage.
It had long triangular shaped in female (Figure 17), while
it was short triangular in male (Figure 18). Despite that
males had greater pessulus area than female but these dif-
ferences were not signicant (P>0.05) (Figure 19). is
structure may help to amplify the sound that generated
from the syrinx. However, the dierences in pessulus shape
between genders were mentioned in birds (Aughey and
Frye, 2001). It is dagger shaped in domestic fowls (Tasbas
et al., 1994), half prism shaped in Japanese quail (Cevik-
Demirkan et al., 2007).
In conclusion to the data mentioned above, there was sex-
ual dimorphism which represented generally in male by
narrow tympanum and right passage of syrinx in male for
more laud sound generation. In addition, greater in syrin-
geal muscles bers and area of the pessulus and triangu-
lar voice that may be magnied the sound wave. e mere
presence of sexual dimorphism in these structures may be
explained how vocal dierences between males and fe-
males had arisen.
CONFLICT OF INTEREST
ere is no conict of interest.
AUTHORS’ CONTRIBUTION
Muna-Al aameli: sample collection, lab work, writing;
Khalid k kadhim: planning of research, writing, statistical
analysis.
REFRENCES
•Andersson M (1994).Sexual SelectionPrinceton, NJ: Princeton
University Press.
•Aughey, E., and F.L. Frye, 2001. Comparative Veterinary
Histology with Clinical Correlates. Manson Ltd. Lon. Pp
93-94. https://doi.org/10.1201/b15184
•Bacha WJ, Bacha LM (2000). Color Atlas of Veterinary
Histology 2nd (ed.): Lippincott Williams & Wilkins. Pp:
175-190.
•Bancroft JD, Stevens A (2012). eory and practice of
histological techniques. 7th edition. Churchill Livingstone.
Pp 127-129.
•Brown C, Ward D (1990). e morphology of the syrinx in the
Charadriiformes (Aves): possible phylogenetic implications.
Bonner ZDologische. Beitrage. 41: 95-107.
•Burke MR, Adkins-Regan E, Wade J (2007). Laterality in
syrinx muscle morphology of the Japanese quail (Coturnix
japonica). Physiol. Behav. 90: 682–686. https://doi.
org/10.1016/j.physbeh.2006.12.007
•Cevik-Demirkan A, Hazıroglu RM, Kurtul I (2007). Gross
Morphological and Histological Features of Larynx, Trachea
and Syrinx in Japanese quail. Anat. Hist. Embryol. 36: 215-
219. https://doi.org/10.1111/j.1439-0264.2007.00758.x
•Daley M, Goller F (2004). Tracheal length changes during
Zebra Finch song and their possible role in upper vocal tract
ltering. J. Neurobiol, 59: 319-330. https://doi.org/10.1002/
neu.10332
•Demirkan AC, Kurtul I, Haziroglu RM (2006). Gross
morphological features of the lung and air sac in Japanese
Quail. J. Vet. Med. Sci. 68(9): 909-913. https://doi.
org/10.1292/jvms.68.909
•Edwards SV, Kingan SB, Calkins JD, Balakrishnan CN, et al
(2005). Speciation in birds:genes, geography, and sexual
selection. Proc. Natl. Acad. Sci. USA. 102: 6550–6557.
https://doi.org/10.1073/pnas.0501846102
•Fee MS (2002). Measurement of the linear and non linear
mechanical properties of the Oscine syrinx: implications
for function. J. Comp. Physiol. A. 188: 829-839. https://doi.
org/10.1007/s00359-002-0349-z
•Frank T, Probst A, Konig HE, Walter I (2007). e syrinx
of the male mallard (Anasplatyrhynchos). Anat. Histol.
Embryol. 36(6): 121-126. https://doi.org/10.1111/j.1439-
0264.2006.00737.x
•Gasser TC, Ogden RW, Holzapfel GA (2006). Hyper elastic
NE
US
Academic Publishers
Advances in Animal and Veterinary Sciences
February 2017 | Volume 5 | Issue 2 | Page 99
modeling of arterial layers with distributed collagen ber
orientations. J. Royal. Soc. Interface 3: 15-35. https://doi.
org/10.1098/rsif.2005.0073
•İnce NG, PazvantG, Alpak H (2012). Anatomical features of
the syrinx in sea gulls. Ankara Üniv. Vet. Fak. Derg. 59: 1-3.
https://doi.org/10.1501/Vetfak_0000002492
•Jeery PK (2004). Structure and Function of Mucus-secreting
Cell of Cat and Goose Airway Epithelium. Exper. Eye.
Res.78(2): 187-96.
•Kabak M, Orhan IO, Hazıroglu RM (2007). e Gross
Anatomy of Larynx, Trachea and Syrinx in the Long-legged
Buzzard (Buteo runus). Anat. Histol. Embryol. 36: 27-32.
https://doi.org/10.1111/j.1439-0264.2006.00708.x
•Keskin N, Pınar L (2013). Glycohistochemistry of the lateral
tympanic membrane in the syrinx of the Denizli cock.
Department of Histology and Embryology, Faculty of
Medicine, Pamukkale University, Denizli, Turkey. Turk. J.
Vet. Anim. Sci. 37: 414-418. https://doi.org/10.3906/vet-
1210-44
•Khaksar Z, Kookhdan ET, Parto P (2012). Study on Anatomy
and Histological Structure of Larynx in Adult Male and
Female Turkeys, World J. Zool. 7(3): 245-250.
•Onuk B, Hazıroglu RM, Kabak M (2010). e Gross Anatomy
of Larynx, Trachea and Syrinx in Goose (Anser anser
domesticus). Kafka’s Uni. Vet. Fak. Derg. 16(3): 443-450.
•Pierko M (2008). Size of the upper respiratory tract with
reference to the body in Scaup Aythyamarila. Electronic J. of
Polish Agricultural Univ. (EJPAU) 11(4): 34.
•Riede T, Goller F (2010). Functional morphology of the sound
generating labia in the syrinx of two songbird species. J.
Anat. 216: 23–36. https://doi.org/10.1111/j.1469-
7580.2009.01161.x
•Riede T, Goller F (2015). Morphological basis for the evolution
of acoustic diversity in Oscine songbirds. Proc. R. Soc. 281-
306.
•Podos J, Huber SK, Taft B (2004). Bird song: the interface
of evolution and mechanism. Annu. Rev. Ecol. Evol.
Syst. 35: 55-87. https://doi.org/10.1146/annurev.
ecolsys.35.021103.105719
•Prince B, Riede T, Goller F (2011). Sexual dimorphism and
bilateral asymmetry of syrinx and vocal tract in the European
starling (Sturnus vulgaris). J. Morphology. 272: 1527-1536.
https://doi.org/10.1002/jmor.11007
•Seller TJ (2002). Birds respiration. Vol. 1CRS. Press, USA.
Pp.72-75.
•Suthers RA, Zollinger SA (2004). Producing song-the vocal
apparatus. Ann. A Y Acad. Sci. 1016: 109-129.
•Suthers RA (2004). Vocal mechanism in birds and Bats: a
comparative view. Annals of the Brazilian Acad. Of Sci. 76
(2): 247-252.
•Tasbas M, Hazıroğlu RM, Cakır A, Özer M (1994).
Morphological investigations of the respiratory system of
the Denizli cock. II. Laryx, trachea, syrinx. Ankara Univ. Vet.
Fak. Derg. 41: 135–153.
•Tshifhiwa G, Mandiwana N, Cecilia K, et al. (2011). A study
of gross morphological and histological syringeal features
of true francolins (Galliformes: Francolimls, Scleroptila,
Peliperdix and Dendroperdix spp.) and spurfowls (Ptemistis
spp.) in a phylogenetic context. Department of Botany,
University of Cape Town, Private Bag X3, Rondebosch
7701, South Africa, 82(2): 115-127.
•Tsukahara N, Yang Q, Sugita S (2008). Structure of the
syringeal muscles in jungle crow (Corvus macrorhynchus).
Anatomical Science fntemational. 83: 152-158.
•Yıldız H, Yılmaz B, Arıcan I (2005). Morphological structure
of the syrinx in the Bursa roller pigeon (Columba Lıvıa).
Bull. Vet. Inst. Pulawy. 49: 323-327.
•Zhang K, Siegmund T, Chan RW (2009). Predictions of
fundamental frequency changes during phonation based
on a biomechanical model of the vocal fold lamina
propria. J. Voice. 23: 277-282. https://doi.org/10.1016/j.
jvoice.2007.09.010
... Although it was stated in Yılmaz et al. 's [7] study that sulcus laryngeus was present in a narrow groove, sulcus laryngeus was not observed in our study. In the study presented in the aboral of mons laryngealis, in one row and succession, there are 5-6 rows of caudal-oriented papillae on each side, although in some studies [6,16,30,31,32], in the caudal part of mons laryngeus, 2 rows of rostral and caudal-oriented were seen. Onuk et al. [33] stated in their study that there were many papillae scattered and out of order. ...
... The discovery of two papilla-shaped protrusions on the caudal border of the glottis, with a median or even rather long and exceeding the level of mons laryngea, was similar to that of Al-aameli and Kadhim's study [32]. However, it was determined that papilla-like protrusions differ due to the level of mons laryngeus. ...
... In our study, 4 rings constituted tympanium. The last 5 to 7 tracheal rings in chickens [40], two rings in quail [39] and turkeys [41], 2 rings or more in domestic chickens [14], and 3 rings in Black Francolin birds [32]. It is stated that it forms a compact structure, tympanium. ...
... The topographical findings of the syrinx in male adult fowl in this study were similar to those of mallards [8,9] geese [ 10,11] Denizli roosters [12] pigeons [13,14] turkeys [15][16][17] guinea fowls [18] and ostriches [19]. It could be classified as tracheobronchial in type as described in most common birds such as pigeons [14] quails [20,21] mallards [8,9,22] geese [10,11] ostriches [19] long legged buzzards [23] Denizli roosters [12] guinea fowls [18] black francolins [24] and eagle owls [21]. ...
... As reported in pigeons and song birds, there were four C-shaped intermediate syringeal rings [14,27,34,35] while in the ostriches only last two rings were C-shaped and the first two were circled [46]. Two C-shaped intermediate rings were reported in guinea fowls [18] black francolins [24] and turkeys [31] two-three C-shaped intermediate rings in long legged buzzards [23]. ...
... Similar observation was also recorded in song birds [19] ostriches [32] guinea fowls [18] Denizli rosters [12] and turkeys [31]. It has been reported that it was consisted of first two bronchial half-rings as in quails [20,21] first four bronchial half-rings as in black francolins [24] and long-legged buzzards [23] first five half-rings as in pigeons [14] first five-six half-rings as in herring gulls [35] first six half-rings as in geese [9][10][11] first seven half-rings as in sea gulls [33]. ...
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Birds are considered a good model for studying the phonation process, the syrinx is a vocal organ in birds. The purpose of this study is to investigate the topographical and morphological characteristics of syrinx of male domestic fowl. In the current study we use the syringes of seven adult males. The study shows that the syrinx of investigated birds is tracheobronchial in type. It consists of; tympanum, tracheosyringeal and bronchosyringeal groups. In addition, there are interbronchial ligament (brachidesm), lateral and medial vibrating membranes as well as the pessulus at the tracheal bifurcation. Tympanum part forms the first part of the syrinx; it is formed of four tracheal rings. The tracheosyringeal part is located at the point of tracheal bifurcation just below the tympanum. It is formed of four highly modified incomplete tracheal rings. The bronchosyringeal part is formed of first three pairs of bronchial half-rings. The current study was presented the detailed morphological characteristics of syrinx in male domestic
... The morphological features of the syrinx have been described in several bird species by many authors (Myers, 1917;Nottebohm, 1976;Yildiz et al., 2003Yildiz et al., , 2005Frank et al., 2006;Khaksar et al., 2012;Keskin & Ili, 2013;Erdogan et al., 2015;Ozudogru et al., 2015;Al-aameli & Kadhim, 2017). However, these investigations did not constitute a coherent presentation for cellular organization and ultrastructural features of the syringes in different bird species. ...
... These findings suggested that the pessulus may help to amplify the sound that generated from the syrinx. Similar observation was also recorded in the males and females black francolin by Al-aameli & Kadhim (2017). ...
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Many studies have been carried out to investigate the morphological structure of the syrinx in many bird species. However, the cellular organization of the syrinx in the fowls and pigeons is still unclear. The current study revealed that in fowl and pigeon, the syrinx is formed of three main parts including tympanum (cranial) part, intermediate syringeal part, and bronchosyringeal (caudal) part, in addition to pessulus and tympaniform membranes. A great variation in the structural characteristics of syrinx of fowl and pigeon was recorded. In fowl, the tympaniform membranes showed a characteristic distribution of elastic and collagen fibers which increase the elasticity of tympaniform membranes. Moreover, the bony pessulus helps the medial tympaniform membranes to be stiffer, vibrate more strongly so that louder sound will be generated. In pigeon, the lateral tympaniform membrane is of greater thickness so that the oscillation of this membrane is reduced and the amplitude is lower. Moreover, the pessulus is smaller in size and is formed mainly of connective tissue core (devoid of cartilaginous or bony plates), resulting in the failure of stretching and vibrating of the medial tympaniform membranes, that leads to the generation of deeper sound. Electron microscopic examination of the syringes of fowls and pigeons revealed numerous immune cells including dendritic cells, plasma cells, mast cells, and lymphocytes distributed within syringeal mucosa and invading the syringeal epithelium. Telocytes were first recorded in the syrinx of fowls and pigeons in this study. They presented two long telopodes that made up frequent close contacts with other neighboring telocytes, immune cells, and blood capillaries.
... The obtained results reported that the first two cartilage rings of the tracheosyringeal cartilages were separate, while the rest of these cartilages were fused and ossified to form the tympanum, simulated that reported in goose (Onuk et al., 2010). However, the tympanum is formed by 2, 3, 4 or 5 rings in turkey, francolin, mallard and sea gulls ( Kookhdan et al., 2012;Yilmaz et al., 2012;Ince et al., 2012;Kadhim et al., 2017). ...
... The obtained results were parallel to those described in in goose ( Onuk et al., 2010) that the bronchosyringeal cartilages were 6 in number, while the bronchosyringeal cartilages are 3 in guinea fowl and francolin (Al-Bishtue, 2014;Kadhim et al., 2017), 4 in turkey ( Kookhdan et al., 2012), 5 in pigeon (Yildizet al., 2005) and 7 in sea gulls (Ince et al., 2012). ...
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Objective: The main purpose of this study was to give detailed information on the position and normal anatomical syringeal structure in goose which had received a little attention in the field of veterinary anatomy. Materials and methods: Six (3 females and 3 males) adult geese weighing 2-4 Kg were used. The goose was slaughtered and its body cavity was opened to detect in situ position of the syrinx. Then the syrinx were dissected and fixed in 10% formaldehyde for 48 h and then kept in 70% ethanol for 2 h. Results: Anatomical examination showed that the syringes of these birds were located in the thoracic cavity at the bifurcation of the trachea. The syrinx was tracheobronchial type formed by tracheosyringeal cartilages, bronchosyringeal cartilages, pessulus, medial and lateral tympaniform membranes, interbronchial ligament and foramen as well as extrinsic syringeal muscles. Conclusion: There were some similarities and some differences of the anatomical structures of the syrinx of goose and that of other bird species. No differences between male and female syrinx were observed. [J Adv Vet Anim Res 2017; 4(4.000): 343-347]
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Infection of falcon by aspergillus fumigatus, asp Flavus and asp Niger cause change in the voice, inability to vocalize or respiratory noises, due to the syrinx lesions, also severe dyspnea occur when obstruction happened. Due to the little available literatures about falcon anatomy, we have done this study to investigate the structure of the lesser kestrel syrinx as it is the voice box in birds which differ from a species to the other. Lesser kestrel (Falco naumanni) syrinx is tracheobronchial in type. The tympanum is composed of the last three cartilaginous tracheal simple complete rings. The tracheosyringeal group is formed of four fused single, ossified, special, characteristic rings just before tracheal bifurcation. The bronchosyringeal group is consisted of three paired cartilaginous C-shaped rings on both sides of the tracheal bifurcation; the edges of both first rings are single while the edges of the rest two bronchosyringeal rings are double. The first two bronchosyringeal rings are related medially to the medial tympanic membrane while the last one attached to the interbronchial ligament. The pessulus is a stretched triangle in shape, cartilaginous bar in the median plane of the trachea. The lateral and medial tympanic membranes are complete sheathes closing the trachea bronchial junction of syrinx laterally and medially. The lateral one is larger than the medial one, and both membranes are responsible for the sound production.
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In this study, larynx, trachea and syrinx of eight domestic mature geese (Anser anser domesticus) weighing 4500-5000g were examined. The larynx was formed by single cartilago (cart.) cricoidea and cart. procricoidea, and a paired cart. arytenoidea. Cartilagines trachea numbered 137-140 and variations in their diameters were detected along their courses. The cartilage rings localized near the middle of the trachea were in contact with the previous or following rings and formed H letter shape. Some rings were dorsally and some were ventrally forked. The syrinx was tracheobronchial type and formed by cartilagines (cartt.) tracheosyringeales and cartt. bronchosyringeales. Cartilagines tracheosyringeales were tube shaped and fused in both directions. Rings were completely ossified except the first two. Cartilagines bronchosyringeales were made up of six 'C' shaped cartilage rings. The open medial faces of the last four cartt. bronchosyringeales came closer to each other and facing left and right parts were tightly attached to each other by connective tissue smooth muscle. The membrane tympaniformes lateralis and medialis were observed. The membrane tympaniformes lateralis was between the tympanum and the first cart. bronchosyringealis, and the membrane tympaniformes medialis was between the pessulus and the second cart. bronchosyringealis. In conclusion, the cartilage rings in middle parts of trachea which seem to be H-shaped forked and also the tympanum which is completely fused and ossified characteristic for the goose.
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Molecular studies of speciation in birds over the last three decades have been dominated by a focus on the geography, ecology, and timing of speciation, a tradition traceable to Mayr’s Systematics and the Origin of Species. However, in the recent years, interest in the behavioral and molecular mechanisms of speciation in birds has increased, building in part on the older traditions and observations from domesticated species. The result is that many of the same mechanisms proffered for model lineages such as Drosophila— mechanisms such as genetic incompatibilities, reinforcement, and sexual selection—are now being seriously entertained for birds, albeit with much lower resolution. The recent completion of a draft sequence of the chicken genome, and an abundance of single- nucleotide polymorphisms on the autosomes and sex chromo- somes, will dramatically accelerate research on the molecular mechanisms of avian speciation over the next few years. The challenge for ornithologists is now to inform well studied exam- ples of speciation in nature with increased molecular resolu- tion—to clone speciation genes if they exist—and thereby evaluate the relative roles of extrinsic, intrinsic, deterministic, and stochastic causes for avian diversification.
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Considering that present a complete and comprehensive study on the structure hasn't been done in turkey's syrinx. In this study 10 adult male and female turkey's pieces were examined for macroscopic and then microscopic structure. The results showed that the male had exactly position on the base of the heart and between first and second intercostals space under the second cervical vertebrae. Syrinx also in female position was near the base of the heart, between first and second intercostals space under the second and third cervical vertebrae. In both sexes thin serous membrane connected to the esophagus ventral surface. Insurface. In microscopical examination results showed that the size of all parts of syrinx had increased in male than female and there was no difference in the epithelial layer between both sexes. Therefore there are some differences in position and structure between syrinx of adult male and female turkeys.
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The aim of this study was to investigate the topographical, anatomical and histological characteristics of the syrinx in 18 Bursa Roler Pigeons. The study showed that the syrinx in pigeons was of tracheobronchial type and was composed of tympanum, cartilagines tracheosyringeales, and cartilagines bronchosyringeales. Tympanum and cartilagines bronchosyringeales were formed from 5 cartilage rings, while cartilagines tracheosyringeales were formed from 4 C-shaped cartilage rings. The pessulus was made up of a double-folded mucous membrane extending dorsoventrally from median walls of the bronchus primarius into the cavum syringis. The membrana tympaniformis lateralis filled the distance between the third and fourth cartilagines tracheosyringeales rings. The membrana tympaniformis medialis covered the distance between the medial ends of the cartilagines broncho-syringeales rings. There were 2 syringeal muscles termed tracheolateral and sternotracheal. The lamina epithelialis of the mucosa was lined with non-cornified stratified squamous epithelium.
Book
Organized by body-system, this highly illustrated volume covers the normal histological appearance of tissues in a wide range of animals, both domestic and exotic species, with relevant clinical correlates emphasizing the need to appreciate the normal in order to recognize the abnormal. The breadth of coverage-farm animals, dogs, cats, horses, birds, reptiles, amphibians, and fish-and the integration of normal and abnormal tissue provide a reference of lasting value to veterinary students, veterinary practitioners, and pathologists.
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In the cat and goose, studies have been undertaken to determine the ultrastructure of airway epithelia, the concentration and distribution of the secretory cells which produce respiratory tract mucus, and the histochemistry of mucins located within cells and on their luminal surfaces. By electron microscopy all the 11 cell types so far described can be found in the airways of the cat but not the goose. Both goblet cells and submucosal glands are abundant in the cat whereas the trachea of goose lacks the latter, having instead abundant goblet cells many of which form 'intraepithelial glands'. Histochemically, the goblet cells of the cat and goose are similar in that they contain mucins with a predominance of sulphate esters. A surface mucosubstance can be demonstrated which, histochemically, is similar to that described in dog and man. Interestingly, this surface layer may be sloughed in response to an inhaled irritant such as ammonia and thereby contribute to the respiratory tract mucus recovered experimentally. Incorporation into macromolecules of radioactively labelled mucin precursors is assessed by autoradiography of tissue sections, and preliminary results of experiments designed to test the response of mucus-secreting cells to airway irritation and the parasympathomimetic drug, pilocarpine, are also presented.
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The syrinx of four sea gulls (Larus spp.) weighing 395-520 g were examined. The syrinx was a tracheobronchial type formed by the bronchosyringeal cartilages (cartilagines bronchosyringeales) and the tracheosyringeal cartilages (cartilagines tracheosyringeales). Five tracheosyringeal cartilages were fused completely and shaped tympanum. Bronchosyringeal cartilages were formed from 7-C shaped cartilage rings. Lateral and medial tympaniform membrane's which are important for vocalization were observed. The lateral tympaniform membrane was observed between 1st and 2nd cartilage rings of bronchosyringeales. Medial tympaniform membrane was placed between the pessulus and 7th bronchosyringeal cartilages. The interbronchial ligament (ligamentum interbronchiale) connects the left and right primary bronchi at the terminal part of the medial tympaniform membrane. Foramen interbronchiale was situated between the medial tympaniform membrane, pessulus and interbronchial ligament. The tracheolateral muscle (m. tracheolateralis) was attached to the 1st bronchosyringeal cartilages. Similarities and differences of syrinx between sea gulls and other avian species were determined in this study.
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▪ Abstract Bird song provides an unusually impressive illustration of vertebrate behavioral diversification. Research on bird song evolution traditionally focuses on factors that enhance song diversity, such as cultural transmission and sexual selection. Recent advances in the study of proximate mechanisms of vocal behavior, however, provide opportunities for studying mechanistic constraints on song evolution. The main goal of this review is to examine, from both conceptual and empirical perspectives, how proximate mechanisms might temper patterns of song evolution. We provide an overview of the two “substrates” of song evolution, memes and vocal mechanisms. We argue that properties of vocal mechanisms (control, production, and ontogeny) constrain vocal potential and may thus limit pathways of meme evolution. We then consider how vocal mechanisms may constrain song evolution under five scenarios of drift and selection and examine four specific song traits for which mechanistic constraints appear to counte...