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Received: 14 November 2017    Accepted: 18 November 2017

DOI: 10.1111/ahe.12336

REVIEW

Anatomy of the upper respiratory tract in domestic birds, with

emphasis on vocalization

C. Casteleyn1,2  | P. Cornillie1 | S. Van Cruchten2 | W. Van den Broeck1 | 

C. Van Ginneken2 | P. Simoens1

1
Department of Morphology, Faculty of
Veterinary Medicine, Ghent University, Summary
Merelbeke, Belgium This work reviews the anatomy of the upper respiratory tract in domestic birds includ-
2
Laboratory of Applied Veterinary
ing the chicken and pigeon. Non-­exhaustive additional information on other bird spe-
Morphology, Faculty of Pharmaceutical,
Biomedical and Veterinary Sciences, University cies, illustrating the extraordinary diversity in the biological class Aves, can be found in
of Antwerp, Wilrijk, Belgium
several footnotes. The described anatomical structures are functionally considered in
Correspondence view of avian sound production. In particular, the Syrinx is invaluable. Its most impor-
Christophe Casteleyn, Department of
tant structures are the Labia and the lateral and medial tympaniform membranes in
Morphology, Faculty of Veterinary Medicine,
Ghent University, Merelbeke, Belgium. non-­songbirds and songbirds, respectively. These structures produce sound by vibrat-
Email: christophe.casteleyn@ugent.be
ing during expiration and eventually inspiration.

1 |  ANATOMY OF THE UPPER (Fedde, 1998). In fowl, the nasal cavity can be divided into the rostral
RESPIRATORY TRACT Vestibulum nasi and the caudal Cavum nasi proprium. The former struc-
ture is lined by a squamous epithelium (Nickel, Schummer, & Seiferle,
1.1 | Nasal cavity 1977) and is encircled by a curved lamella that projects mediorostrally
from the caudal part of the dorsal cartilaginous plate, which partly cov-
The nasal cavity (Cavitas nasalis) of the chicken (Gallus gallus domesti-
ers the nasal opening, towards the nasal septum (Figure 2). This lamella
cus) and pigeon (Columba livia domestica) is dorsally bordered by the
should not be mistaken for a rostral nasal concha, which is absent in
frontal process (Processus frontalis) of the incisive bone (Os incisivum
the chicken and pigeon (Fitzgerald, 1969). In these two bird species, as
syn. Os premaxillare), the intermaxillary process (Processus intermaxil-
well as in many other bird species, the nasal cavity is completely parti-
laris) of the nasal bone (Os nasale) and the lacrimal bone (Os lacrimale).
tioned by the cartilaginous nasal septum (Septum nasi) into a left and
The lateral border is delineated by the maxillary process (Processus
right part, which is denoted by the term Nares imperviae (Figure 4).1
maxillaris) of the nasal bone. The floor of the nasal cavity is formed
The inhaled air flows medial to the lamella of the upper cartilagi-
rostrally by the maxillary process of the incisive bone and caudally by
nous plate and lateral to the nasal septum to reach the nasal cavity. In
the palatine bone (Os palatinum). The large orbits limit the nasal cavity
most avian species, including the chicken and pigeon, the nasal cavity
caudally (Figure 1).
contains a ventral and dorsal nasal concha (Figure 5). The ventral nasal
In most avian species, the nasal openings (Nares) are located
concha (Concha nasalis ventralis) is larger, more rostrally situated and
dorsolaterally at the basis of the upper beak. In the chicken, they
consists of a thin cartilaginous lamella lined by a mucociliary respi-
are enclosed by a dorsal and ventral cartilaginous plate. Both plates
ratory epithelium (Figure 6). This concha arises from the dorsolateral
join at their caudal borders where a shallow internal niche is formed
wall of the nasal cavity and extends in caudoventral direction towards
(Figure 2). The dorsal cartilaginous plate is covered by keratinized ep-
the choanae (Figure 5). Ventral to the ventral nasal concha, the naso-
ithelium denoted as the Operculum (McLelland, 1990). Furthermore, it
lacrimal duct (Ductus nasolacrimalis) discharges into the nasal cavity
may be raised by the cere (Cera) in some species, such as the domestic
by a slit-­like opening (Nickel et al., 1977). The smaller dorsal concha
pigeon and the budgerigar (Melopsittacus undulatus) (Figure 3). In the
(Concha nasalis dorsalis) originates on the ethmoid bone and projects
latter species, the colour of the cere is gender-­dependent.
The nasal openings are connected to the nasal cavity where the 1
In aquatic birds, such as the duck (Anas platyrhynchos), the nasal septum presents a large
inhaled air is filtered from the larger particles, warmed and moisturized aperture (Nares perviae) (King & McLelland, 1975).

Anat Histol Embryol. 2018;1–10. © 2018 Blackwell Verlag GmbH |  1

wileyonlinelibrary.com/journal/ahe  
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2       CASTELEYN et al.

F I G U R E   1   Left lateral view of the skull of a chicken showing the

bony limitations of the nasal cavity. 1 = Incisive syn. pre-­maxillary
bone, 1′ = frontal process, 1″ = maxillary process, 2 = maxillary bone,
3 = nasal bone, 3′ = intermaxillary process, 3″ = maxillary process,
4 = lacrimal bone, 5 = palatine bone

into the nasal cavity (Figure 5). Its rostral part is covered by a muco-
ciliary epithelium, whereas the caudal part is lined by an olfactory epi-
thelium involved in odour perception (Fitzgerald, 1969). This concha is
absent in the pigeon (Nickel et al., 1977).
The pyramidal infraorbital sinus (Sinus infraorbitalis) is lined by a
very thin mucosa and lies lateral to the nasal cavity, rostroventral to
the eye and caudal to the maxillary process of the nasal bone. The
infraorbital sinus is connected to the cavity enclosed within the dorsal
nasal concha by a mediodorsal fissure, which is broad in the duck and
goose (Anser anser) but narrow in fowl. Communication with the nasal
cavity takes place through a more ventral cleft in the medial mucosal
wall of the infraorbital sinus (Nickel et al., 1977; Figures 4 and 5). The
rostral compartment of the sinus is covered by a squamous epithe-
lium, whereas a ciliated cuboidal epithelium that comprises some gob-
let cells lines the more spacious caudal part of the sinus (McLelland,
1990).
The nasal cavity is connected with the oral cavity through the pala-
tine or choanal cleft (Choanae) that presents as a slender fissure in the
palate. Above this fissure lies the antorbital fossa (Fossa antorbitalis)
that contains the infraorbital sinus (Figure 6). The infundibular cleft
(Rima infundibuli syn. Tuba auditiva communis) is located caudal to the
F I G U R E   3   Rostral view of the head of a pigeon showing the
cere (1) at the basis of the upper beak which borders the nasal
openings caudally (2). The widely opened beak allows for inspection
of the choanal cleft (3) and the infundibular cleft (4). Adapted from
Casteleyn, Scheers, Simoens, and Van den Broeck (2011)
choanal cleft (Figure 3). Here, both auditory tubes (Tubae auditivae)
originate by a common cavity (Infundibulum tubarum). The soft tissues
surrounding the choanae and infundibular cleft contain lymphoid tis-
sue that corresponds with the pharyngeal tonsil (Figure 7; Casteleyn
et al., 2010; Salomon & Krautwald-­Junghanns, 2008).
1.2 | Larynx
The inhaled air that leaves the nasal cavity flows through the choanal
cleft towards the larynx (Larynx cranialis), which hampers the enter-
ing of larger particles into the trachea. It consists of a short cylindrical
structure that is composed of osseous, cartilaginous and musculomem-
branous components (Figure 8). Maceration of the soft tissues reveals
the presence of laryngeal osseous plates (Figure 9). In addition, only
the cricoid cartilage (Cartilago cricoidea) and paired arytenoid cartilages

F I G U R E   2   Left ventrolateral views of the left nasal opening of a chicken. (a) The dorsal (1) and ventral (2) cartilaginous plates surround the
nasal opening. Where they join caudally, a niche (asterisk) is formed. A lamella (3) branches off from the dorsal cartilaginous plate, which is also
called the operculum. (b) After detaching the operculum rostrally, the lamella becomes obvious
CASTELEYN et al.
F I G U R E   4   Left lateral view of the head of a chicken. The
cartilages surrounding the nasal opening have been removed
showing the cartilaginous nasal septum (1). The infraorbital sinus (2)
is visible in between the maxillary process of the nasal bone and the
eye. The probe shows the cleft through which the infraorbital sinus
communicates with the nasal cavity
(Cartilago arytenoidea) are present in birds. No epiglottis nor a thyroid
cartilage (Cartilago thyroidea) can be found (King & McLelland, 1975).
The cricoid is composed of a semi-­circular ventral cricoid plate and
dorsolateral wings that are connected to the plate by means of fibrous
tissue. As such, it forms a ring of fibrocartilaginous/fibroosseous tis-
sue. The arytenoid cartilages articulate dorsally with the cricoid. They
are composed of a caudal, ossified rod-­like part and a thin, cranial car-
tilaginous part that protrudes in cranial direction. The glottis (aditus
laryngis) that forms the entrance to the larynx is located in between
both arytenoids on the mons laryngis, which deviates the passage of
fluids laterally, thus avoiding choking (Figure 9). The dimensions of the
larynx can be adjusted by laryngeal muscles (Nickel et al., 1977).
1.3 | Trachea
The trachea originates at the larynx (Larynx cranialis) and is caudally
connected to the Syrinx or Larynx caudalis. Along its entire length, the
trachea is located in the median plane and is lined by a pseudostrati-
fied ciliary epithelium that contains some goblet cells. It crosses the
crop dorsally and enters the thoracic cavity between the rami of the
Furcula (Fitzgerald, 1969; Nickel et al., 1977). The oesophagus initially
lies dorsal to the trachea, but deviates to the right towards the cranial
thoracic aperture (Figure 10).
The length of the trachea varies between different bird species.
The trachea of the chicken consists of more than 100 closed tracheal
rings or Anuli tracheales. As these tend towards early ossification, the
term Cartilagines tracheales seems less appropriate. The consecutive
tracheal rings are connected to each other by elastic membranes
(Ligamenta anularia). Moreover, the rings overlap well as they comprise
a narrow and a wide part that are alternatingly located at the dorsal
and ventral side (Fitzgerald, 1969).
Furthermore, the tracheal rings are interconnected by several mus-
cles. The thin, striated Musculus (M.) tracheolateralis runs bilaterally
      3|
along the entire length of the trachea, thus from the Larynx cranialis to
the Larynx caudalis (McLelland, 1990). In the chicken and pigeon, the
left and right M. sternotrachealis originate on the craniolateral aspect
of the sternum and insert ventrally on the trachea in the median plane,
just cranial to the syrinx (McLelland, 1990) (Figure 11).2
1.4 | Syrinx
1.4.1 | Definition
The Syrinx, also called the Larynx caudalis, is in most bird species in-
valuable in sound production. It is located at the bifurcation of the
trachea into the primary bronchi. Its anatomical position is intratho-
racic at the basis of the heart, which is at the level of the first and sec-
ond thoracic vertebrae (Çevik-­Demirkan, Haziroğlu, & Kürtül, 2007;
Larsen & Goller, 2002; Suthers, Goller, & Pytte, 1999; Figure 11).
Furthermore, it is surrounded by the clavicular air sac (Vollmerhaus
& Sinowatz, 1992).
According to its structural components, three syringeal types can
be identified, viz. a tracheal, tracheobronchial and bronchial syrinx
(King, 1979). The majority of bird species, including the chicken, the
turkey (Meleagris gallopavo), the pigeon and mallard, possess a tracheo-
bronchial syrinx that is characterized by modifications of both the tra-
chea and the primary bronchi (Suthers & Zollinger, 2004; Yildiz,
Bahadir, & Akkoç, 2003).3
1.4.2 | Osseous and cartilaginous structures
The syrinx is supported by a number of cartilaginous rings (Cartilagines
syringeales) that succeed the proper tracheal rings and are conse-
quently termed tracheal syringeal rings (Cartilagines tracheales syringis)
(Figures 11, 13 and 14; King & McLelland, 1975). These are closely
assembled and as such form a firm cylindrical structure known as the
Tympanum (King, 1979). Furthermore, they are closed annular struc-
tures, just like the proper tracheal rings. Their number varies consider-
ably according to the species (eight in the chicken, up to 78 in some
members of the Ciconiidae) (King, 1979). Ossification is possible in a
few species such as the chicken, silver lark (Larus argentatus) and song-
birds (Vollmerhaus & Sinowatz, 1992).
The more caudal syringeal cartilaginous rings are called bronchial
syringeal rings (Cartilagines bronchiales syringis) and arise from the tym-
panum and form the basis of the partitioned tracheobronchial. As a
consequence, they are paired (King & McLelland, 1975). These cartilag-
inous rings are not entirely closed, but have a C-­like-­shaped profile
(Çevik-­Demirkan et al., 2007; King, 1979). The free margins face the
median plane and support the Membrana tympaniformis medialis or
2
In several bird species belonging to the Anserinae (e.g. geese (genus Anser and Branta) and
swans (genus Cygnus)), Gruidae (crane birds) and Paradisaeidae (birds-­of-­paradise), the trachea
is elongated, allowing for the formation of curves, curls and coils (Figure 12). This conforma-
tion enables vocalizations that contain louder, lower-­frequency sounds (Clench, 1978; Daley
& Goller, 2004; Frith, 1994).
3
The tracheal syrinx in the order Passeriformes (perching birds to which the suborder of the Oscines,
i.e. the true songbirds, belongs) or the bronchial syrinx that is present in the common cuckoo
(Cuculus canorus) shows adaptations of only the trachea or bronchi, respectively (King, 1979).
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4       CASTELEYN et al.

F I G U R E   5   Left lateral view of the head of a chicken visualizing the nasal cavity. (a) The cartilages of the nasal opening and the maxillary
process of the nasal bone have been removed, showing the nasal septum (1) and the antorbital fossa (2) that lies dorsal to the palatine cleft. The
infraorbital sinus (3) has been opened. (b) After removal of the nasal septum, the medial aspect of the right nasal cavity becomes visible. The
lamella of the right operculum (4), the large ventral nasal concha (5) and the small dorsal nasal concha (6) can be observed. The level at which the
histological cross section of the nasal cavity shown in Figure 6 is made is indicated by the double arrow

F I G U R E   7   Longitudinal histological section (haematoxylin–eosin

F I G U R E   6   Histological cross section of the nasal cavity of the
chicken (decalcified specimen; original size: 125 mm × 90 mm) at
the level of the corners of the beak. 1 = Nasal septum, 2 = antorbital
fossa, 3 = dorsal nasal meatus, 4 = cavity of the dorsal nasal concha,
5 = infraorbital sinus, 6 = nasolacrimal duct, 7 = frontal bone,
8 = palatine bone, 9 = jugal bone
interna (King, 1979). Where both medial tympaniform membranes join
cranially, the Pessulus, i.e. a pyramidal wedge-­shaped cartilage, can be
observed in many bird species including the chicken and pigeon. This
structure is, however, absent in the oscine songbirds (Çevik-­Demirkan
et al., 2007; King, 1979; King & McLelland, 1975; Figure 14).4
1.4.3 | Ligaments
A connective tissue strand links the medial aspects of the rostral parts
of the left and right primary bronchi. This Ligamentum interbronchiale
4 rings (King, 1979). It lacks in the duck (Frank et al., 2007), while its
The Bulla syringealis or Bulla tympanica is a confined expansion of the syrinx that is present in
some species (Figure 15). The archetypal tympanic bulla of the drake is a bell-­shaped exten-
sion at the left side of the syrinx that can present partial or complete ossification. It allows for
the sound to resonate and as such amplifies the volume of the produced sound (King &
McLelland, 1975; Vollmerhaus & Sinowatz, 1992).
staining) of the palate of a chicken showing the presence of lymphoid
tissue in the nasal mucosa bordering the choanal and infundibular
clefts. Some lymphoid follicles are indicated by the arrows. Adapted
from Casteleyn et al. (2010)
is called Bronchidesmus by King and McLelland (1975). The cavity
enclosed by the tracheal bifurcation cranial to this ligament is the
Foramen interbronchiale (King, 1979) (Figure 14).
1.4.4 | Membranes
The Membrana tympaniformis lateralis or externa is located bilaterally
in the lateral walls of the syrinx at the level of the tracheobronchial
junction (Fitzgerald, 1969). It can either extend from the Tympanum to
the first bronchial rings, as in the chicken and the pigeon (Gaban-­Lima
& Höfling, 2006; Pierko, 2007; Vollmerhaus & Sinowatz, 1992; Yildiz
et al., 2003; Figure 14), or can be composed of multiple short mem-
branes that are located in between the successive bronchial syringeal
presence is controversial in perching birds (King, 1979).5
5
In the tracheal syrinx type, the membrane is modified and accordingly termed Membrana
trachealis (King, 1979).
CASTELEYN et al. |
      5

F I G U R E   8   Dorsal view of the larynx (1) and cranial segment of

the trachea (2) of the chicken. The slit-­like laryngeal entrance that is
flanked by the protruding arytenoid cartilages (asterisks) is indicated
by the arrow

F I G U R E   1 0   Ventral view of the neck of a chicken showing the

localization of the trachea (1), oesophagus (2) and crop (3)

1.4.5 | Muscles
F I G U R E   9   Craniolateral view of a macerated larynx of a chicken
showing the laryngeal cartilages that are highly ossified in this specimen. The description below makes use of the nomenclature presented in
The entrance to the larynx is indicated by the arrow. The cricoid is
the Nomina Anatomica Avium (King, 1979). An alternative terminology
composed of the ventral cricoid plate (1) and the dorsolateral wings (2).
that complicates the comprehension of the anatomy of the muscles in-
The fibrous tissue that connects both parts has been macerated. Its
localization is indicated by the asterisk. The paired arytenoid cartilage volved in sound production can, however, be found in several literature
consists of a rod-­like caudal part (3) and a thin cartilaginous cranial part (4) reports. Nevertheless, two important clusters of muscles can be distin-
guished, i.e. the Mm. tracheales and the Mm. syringeales. The latter con-
The Membrana tympaniformis medialis bilaterally bridges the
sist of intrinsic syringeal muscles, which have their origin and insertion
Pessulus and the medial side of the primary bronchi. It dorsoventrally
on the syrinx. Extrinsic syringeal muscles have an attachment beyond
connects the medial free margins of the bronchial syringeal rings
the syrinx (King, 1979) and include some of the tracheal muscles.
(Kabak, Orhan, & Haziroglu, 2007; Yildiz et al., 2003). Both mem-
The Mm. tracheales comprise the M. tracheolateralis, M. sternotra-
branes form the lateral walls of the Foramen interbronchiale (Figure 14).
chealis, M. cleidotrachealis and M. sternohyoideus. The presence of this
The Labia are paired elastic strings located within the lateral and me-
entire repertoire in a particular species is exceptional. In most non-­
dial tympaniform membranes (Çevik-­Demirkan et al., 2007; King, 1979;
songbirds, which possess a tracheobronchial syrinx type, only the M. tra-
Suthers & Zollinger, 2004; Figure 14). These strings are in many cases
cheolateralis is described. Moreover, Ratites, Ciconiidae, Cathartidae and
the major source of sound (Frank, Walter, Probst, & König, 2006).6,7
some Galliformes lack tracheal muscles (Brackenbury, 1980; Çevik-­
Demirkan et al., 2007; Frank et al., 2006; Gaunt, 1983; King, 1979; Yildiz
6
Labia lack in some bird species, such as the silver lark and the long-­legged buzzard (Buteo
rufinus) (Kabak et al., 2007; King, 1979).
et al., 2003). The chicken and the pigeon possess both the M. sternotra-
7
In addition to the here-­described syringeal components, specific structures may be present chealis and M. tracheolateralis that both are extrinsic syringeal muscles
in other avian species. In the common quail (Coturnix coturnix), the mucosal membrane that
(Brackenbury, 1980; King, 1979; Vollmerhaus & Sinowatz, 1992;
covers the Pessulus protrudes into the tracheal lumen. As a result, a Membrana semilunaris is
formed (Fitzgerald, 1969; Frank et al., 2006). Since this structure cannot vibrate, it may play Figure 16). Most domestic bird species such as the chicken and pigeon
no role in sound production, in contrast to what was previously accepted (Frank et al., 2006). lack intrinsic syringeal muscles. However, some smooth muscle cells are
The Membrana tracheosyringealis is a paired membrane that is especially present in
Columbiformes and Psittaciformes (King, 1979). This membrane covers the inner wall of the present in the interbronchial area in the duck (Frank et al., 2006).8
trachea caudally and attaches to the Tympanum and the first bronchial rings (Gaban-­Lima &
8
Höfling, 2006). The Valvula syringealis that is present in diving ducks (Aythyinae) and mallards Passeriformes, Psittaciformes and the oilbird (Steatornis caripensis) possess well-­developed
(Anatinae) is a caudally oriented valve that originates on the inside of the lateral wall of the Mm. syringeales in addition to the tracheal muscles. Syringeal muscles are short and poorly
right primary bronchus. During diving, the contraction of the sternotracheal muscle allows for delineated. They include the Mm. tracheobronchialis dorsalis, ventralis et brevis and the Mm. sy-
this valve and the medial tympaniform membranes to protrude into the bronchial lumina and ringealis dorsalis et ventralis (Gaban-­Lima & Höfling, 2006; King, 1979; King & McLelland,
almost entirely block the airflow through both primary bronchi (Frank et al., 2006). 1975; Sherwood, Klandorf, & Yancey, 2004).
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6       CASTELEYN et al.

F I G U R E   1 2   Left craniolateral view of the cranial thoracic

aperture of a goose demonstrating the tracheal elongation that is
visible as a ventral loop. Adapted from Casteleyn, Michiels et al.
(2011)

F I G U R E   1 1   Ventral views of the thoracic cavity of a pigeon

after removal of the sternum. (a) The syrinx presents an intrathoracic
localization at the level of the first two thoracic vertebrae. It is
covered ventrally by the basis of the heart. (b) After caudal retraction
of the heart, the syrinx (boxed) that is located at the tracheal
bifurcation becomes visible. (1 = trachea, 2 = heart, 3 = lungs,
4 = liver, asterisks = sternotracheal muscles, arrows = tracheolateral
muscles.) Adapted from Casteleyn, Michiels, Van den Broeck, and
Simoens (2011)

2 |  VOCALIZATION F I G U R E   1 3   Ventral view of the chicken syrinx (boxed) that is

2.1 | Introduction
Mammals most commonly produce sound by means of their vocal
cords that are bilaterally present in the larynx. Although the latter
structure is also found in birds, vocal cords are lacking in these ani-
mals. Most bird species rely on their syrinx to vocalize.9
9
Since the syrinx is absent in some members of the Ratites, it is not surprising that they are
deficient in voice production. However, some species generate sound using the beak. Several
species of woodpeckers (Picidae) drum on tree trunks to mark their territory. Storks
(Ciconiidae), on the other hand, clatter by rapidly opening and closing the beak. Besides the
beak, feathers can generate sound as well. This is the case in a.o. the white-­bearded manakin
(Manacus manacus), the common snipe (Gallinago gallinago) and hummingbirds (Trochilidae).
The sound can either originate from wing snapping or from air turbulence around the feathers
(Clark, Elias, & Prum, 2011; Vuilleumier, 2002).
located in between the trachea (1) and the left and right primary
bronchi (2 and 2′, respectively). The sternotracheal muscles are
indicated by the asterisks. Adapted from Casteleyn, Michiels et al.
(2011)
According to the species, the vocal repertoire of birds varies from
simple sounds to more complex songs (Marler & Hamilton, 1966).
Several functions can be attributed to the birdsong, such as territory
marking and socialization of the offspring in female birds, and the lur-
ing of a mating partner in male birds. Additionally, it plays a role in the
reproductive cycle and the recognition of family members (Gorissen
& Eens, 2005; Marler & Hamilton, 1966). The text below focuses on
sound production in the syrinx.
CASTELEYN et al.
F I G U R E   1 4   (a) Longitudinal histological
section of the syrinx of a chicken (after
Casteleyn, Michiels et al., 2011). (b)
Schematic representation of the syrinx of
the blackbird (Turdus merula) adapted from
King (1979) and Vollmerhaus and Sinowatz
(1992). (1 = trachea, 2 = Tympanum,
3 = Pessulus, 4 = medial Labia, 5 = lateral
tympaniform membranes, 6 = lateral Labia,
7 = medial tympaniform membranes,
8 = interbronchial ligament, 9 = primary
bronchi, asterisks = sternotracheal muscles)
F I G U R E   1 5   Ventral view of the syrinx of a drake located in
between the trachea (1) and the left and right primary bronchi
(2 and 2′, respectively). The sternotracheal muscles are indicated by
the asterisks. The syringeal bulla (3) is clearly visible as a voluminous
extension at the left side of the syrinx. Adapted from Casteleyn,
Michiels et al. (2011)
2.2 | The mechanism of sound generation
In non-­songbirds, such as the chicken and the pigeon, the lateral
tympaniform membranes are responsible for the produced sound
(Elemans, Zaccarelli, & Herzel, 2008). The classical model states that
these membranes are initially relaxed, but when the air flows through
the syrinx during expiration, the membranes present a cyclic vibra-
tion that is the result of the Bernoulli forces created by the airflow
and the elastic restoring forces of the membrane itself (Ballintijn &
|
      7
Ten Cate, 1998; Gaunt, 1983). In this model, the pitch of the gener-
ated sound depends on the tension of the membranes, whereas the
volume is related to the amplitude of the vibration (Gaunt, 1983).
The structures that can influence these parameters are described
below.10
2.3 | Influence of the musculature
Non-­songbirds usually have no or only minor intrinsic syringeal
muscles (Frank et al., 2006; King, 1979). The sternotracheal and
tracheolateral muscles, both extrinsic syringeal muscles, have an-
tagonistic mechanical effects. The tracheolateral muscle indirectly
abducts or tenses the lateral tympaniform membrane by retracting
the syrinx in cranial direction. The sternotracheal muscle, on the
other hand, directly adducts or relaxes the membrane by drawing
the trachea caudally (Elemans et al., 2006; Gaunt & Gaunt, 1977;
Suthers & Zollinger, 2004). During the trill of the ring dove, the
lateral tympaniform membranes are adducted and abducted in and
10
Extrapolating the classical model to songbirds holds that the medial tympaniform
membranes are the sound-­g enerating structures since songbirds do not possess lateral
tympaniform membranes. However, the fact that songbirds are still able to produce
sound after their medial tympaniform membranes have been cut surgically could mili-
tate against the validity of the classical model in these bird species (Goller & Larsen,
1997b). After surgery, the sound is of lower intensity, but the individual sounds are still
mutable (Goller & Larsen, 1997b, 2002). Because of this observation, endoscopic re-
search has promoted the labial hypothesis or the pulse-­t one model that is most proba-
bly valid for a large number of songbird species (Goller & Larsen, 1997a; Suthers &
Zollinger, 2004). Prior to the production of the sound, the syrinx is displaced in cranial
direction and stretched. Consequently, the bronchi and the medial tympaniform mem-
branes are stretched (Goller & Larsen, 2002). The Bernoulli forces that arise during
expiration result in the subsequent displacement of the lateral and medial labia towards
the lumina of the bronchi (Goller & Larsen, 1997a, 2002; Larsen & Goller, 2002). Due
to their elasticity, a self-­o scillating system, referred to as a pneumatic valve, is set in
place (Goller & Larsen, 2002). An alternative hypothesis is the whistle hypothesis that
is based on aerodynamic principles. This model aims to clarify the production of tonal
sounds in the collared dove (Streptopelia decaocto) (Ballintijn & Ten Cate, 1998; Goller
& Larsen, 2002). When air travels at high velocity through a narrow passage, i.c. the
syringeal opening (Figure 14), turbulences arise in the airflow that, as in a whistle, act
as sound generators (Ballintijn & Ten Cate, 1998; Gaunt, 1983). However, recent stud-
ies have rejected this model because the fundamental frequency of the produced tones
failed to shift upwards when birds inhaled a lighter gas. Moreover, it was observed in
the ring dove (Streptopelia risoria) that the tracheal and syringeal muscles have a major
impact on the sound production (Elemans, Spierts, Müller, van Leeuwen, & Goller,
2004; Elemans et al., 2006).
 |
8       CASTELEYN et al.

out the syringeal lumen at a frequency of 24 Hz (Elemans et al.,

2004, 2006).11

2.4 | Influence of the respiration

In the majority of avian vocalizations, the sound is produced during
expiration (Suthers & Zollinger, 2004; Suthers et al., 1999). This can
especially be appreciated when observing the crowing of the rooster,
which is limited in time. The ring dove and the zebra finch, however,
can also generate inspirational sounds (Gaunt, Gaunt, & Casey, 1982;
Goller & Daley, 2001). During expirational sound production, the ex-
piratory muscles generate a specific airflow and pressure that are bi-
laterally present in the syrinx, even though the sound might be
produced unilaterally, a phenomenon known as lateralization of the
sound production (Suthers & Zollinger, 2004).12

2.5 | Influence of the suprasyringeal structures

The sound waves that are generated in the syrinx are modified
through their way out by the trachea, the oropharyngeal–oesophageal F I G U R E   1 6   Ventral view of the trachea of a pigeon showing
cavity, the tongue and the beak (Beckers, Nelson, & Suthers, 2004; the left and right sternotracheal muscle (1 and 1′, respectively) and
Riede, Suthers, Fletcher, & Blevins, 2006; Suthers et al., 1999). The the left and right tracheolateral muscles (2 and 2′, respectively). The
syrinx (boxed) is located at the tracheal bifurcation. Adapted from
trachea mutes or amplifies some frequencies. As mentioned above,
Casteleyn, Scheers et al. (2011)
the tracheas of geese and swans, crane birds and birds-­of-­paradise
present curves, loops or windings (Figure 12) that allow for generat-
ing louder sound of lower frequency (Clench, 1978; Daley & Goller, generated (Suthers, 2006). The degree of opening of the beak during
2004; Frith, 1994). The larynx and the hyoid bone can modify the vocalization is positively correlated with the frequency (Suthers et al.,
volume of the initial segment of the oesophagus (Riede et al., 2006). 1999). The tongue might seem of minor importance as it is a rather
When low-­frequency sounds are produced, the oesophagus and the rigid structure that is not suitable for articulation, as in humans (Wild,
oropharynx present a single cavity, i.e. the oropharyngeal–oesopha- 2004). However, it was recently demonstrated in northern cardinals
geal cavity. Its volume decreases when higher-­frequency sounds are (Cardinalis cardinalis) that tongue elevation lowers the resonance fre-
quency below 2 kHz by reducing the area of the passage from the
11
In songbirds, the M. tracheolateralis, which ends in front of the syrinx (McLelland, 1990),
stretches the syrinx and fits it in the appropriate position for sound production (Goller & Larsen,
oral cavity into the beak (Suthers, Rothgerber, & Jensen, 2016). The
1997a; Larsen & Goller, 2002). The M. syringealis dorsalis and the M. tracheobronchialis dorsalis tongue of Psittaciformes is exceptional as it can change the amplitude
adduct the medial and lateral labia, which results in the narrowing of the syringeal aperture
and frequency of the sound. This partly explains their capacity of mim-
(Elemans et al., 2006). This is important for the timing of the vocalisation within the appropriate
phase of the respiratory cycle (Larsen & Goller, 2002; Suthers & Zollinger, 2004). The M. tra- icking the human speech (Beckers et al., 2004).
cheobronchialis ventralis has the opposite function (Larsen & Goller, 2002). The lateral part of
the M. syringealis ventralis mainly influences the tension on the labia. As a result, this muscle has
impact on the pitch of the produced sound (Suthers & Zollinger, 2004). Finally, the M. sternotra-
chealis holds the syrinx in a stable position during the strong contractions of the intrinsic syrin- 3 | CONCLUSIONS
geal muscles that are necessary for the generation of high tones (Goller & Suthers, 1996).
12
Songbirds possess two independent sound sources because the musculature of each syrin-
Vocalization in birds is the result of the flawless synchronization of the
geal side is innervated by the ipsilateral Nucleus n. hypoglossi (Suthers et  al., 1999; Wild,
Williams, & Suthers, 2000). Both sources can function simultaneously or independently respiration and the muscle activation in the upper respiratory tract. In
(Suthers et al., 1999). Some bird species switch between both sides or use both sides simulta-
most species, the sound is created during expiration by the vibrations
neously (Suthers, 2001). Since the tones that are produced in the right side of the syrinx,
which has a smaller diameter bronchus (Luine, Nottebohm, Harding, & McEwen, 1980), have of the membranes and Labia that are present in the syrinx. Although
a higher frequency, the bird can cover a wider range of frequencies (Suthers, 2001). This two-­ the main principles of sound production in birds are well known, it
voice system is also present in non-­songbirds such as the king penguin (Aptenodytes patagon-
icus) and the emperor penguin (Aptenodytes forsteri) that are able to produce specific calls that should be noticed that variations exist in the fine-­tuning of the sing-
can be recognized individually (Aubin, Jouventin, & Hildebrand, 2000). Other species have a ing between species. Moreover, the anatomy of the sound-­producing
preference for one side of the syrinx (Suthers, 2001; Wade, Buhlman, & Swender, 2002; Wild
et al., 2000). If, for example, the left side of the syrinx produces sound during expiration, the
organs is variable as well.
right side is closed, but it opens after each syllable for a short inspiration. The longer the syl-
lable, the longer the duration of the inspiration is (Suthers & Zollinger, 2004). When a high
number of sound elements have to be generated, which is typical in the canary (Serenus), a AC KNOW L ED G EM ENTS
pulsating respiration is performed. Sound is produced by repeatedly opening and closing one
side of the syrinx, allowing the passage of air pulses that are each associated with one syllable
We would like to thank Katty Huybrechts and Gunther Vrolix for pro-
(Suthers et al., 1999). The advantage of the mini-­respiration lies in the fact that the bird can
continue singing for longer periods. viding the histological section shown in Figure 6.
CASTELEYN et al.
CO NFLI CT OF I NTE RE ST
None declared.
O RCI D
C. Casteleyn  http://orcid.org/0000-0003-2676-0756
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How to cite this article: Casteleyn C, Cornillie P, Van Cruchten S,
Van den Broeck W, Van Ginneken C, Simoens P. Anatomy of
the upper respiratory tract in domestic birds, with emphasis
on vocalization. Anat Histol Embryol. 2018;00:1–10.
https://doi.org/10.1111/ahe.12336