(1) Naris. The external aperture of the Cavum nasi. Terms for the form of the nostril are: Nares gymnorhinales, exposed nares; Nares perviae, open nares as in most birds; Nares imperviae, nares closed secondarily by growth of the horny beak as in some pelecaniforms, though these species breathe by secondary nares at the angle of the mouth (MacDonald, 1960). In sulids even the bony aperture is closed (Thompson, 1964:505; Topog. Annot. 21). Terms for the shape of the bony aperture (taxonomically significant) are: holorhinal, caudal margin rounded; schizorhinal, caudal margin a slit; amphirhinal, two bony openings on each side.

(2) Operculum nasale. The nasal operculum (Fig. 8.la) is a horny -flap dorsal to the nares in Gallus and some other species (Bang, 1971), and ventral to the nares in wrynecks (lynx) (Bang and Wenzel, 1985:2(0) (Topog. Annot. 21).

(3) Lamella verticalis naris. Synonymy: Atrial concha (Bang, 1971). The vertical lamella of the nostril (Fig. 8. I a) is a cartilaginous sheet arising from the ventral border of the Naris in Gallus (Bang, 1971; King, 1975: 1886) and a few other species e.g., members of Apodiformes and Tumix (Bang, 1971).

(4) Choana, Pars rostralis. A narrow rostral slit, possibly homologous to the median palatine suture of mammals (Heidrich, 1908).

(5) Choana, Pars caudalis. Synonymy: interpalatine cleft, Choana I (Lucas and Stettenheim, 1972: Fig. 362). The triangular opening, caudal to the maxillopalatine processes, between the palatine bones, and divided dorsally in the midline by the Vomer and Septum nasale (see Osteo. Fig. 4.7). Possibly homologous to the mammalian Choanae.

(6) Concha nasalis rostralis. Synonymy: Concha ventralis. Rostralis is preferred because in birds with a long nasal cavity (e.g., Hydrophasianus; Bang, 1971), there is no room for a ventrodorsal relationship between the conchae. The rostral nasal concha (Fig. 8.la) varies in form and is sometimes absent as in Sulidae (Bang, 1971).

(7) Concha nasalis media. Synonymy: maxillary concha (Bang, 1971); maxilloturbinal (Bellairs and Jenkin, 1960:285). Maxillary implies homology to the maxillary concha of mammals and other vertebrates, but this is uncertain and, therefore, the topographical term, middle nasal concha, is preferred. Its form varies (Fig. 8.lb). It is absent in very few birds, among them certain phalacrocoracids (Bang and Wenzel, 1985:203).

(8) Concha nasalis caudalis. Probably homologous with the single Concha of most reptiles (Bell airs and Jenkin, 1960:285). Very variable in form (Fig. 8.lc). In Gallus the caudal nasal concha is a hollow dome, its only exit being to the infraorbital [antorbital] sinus. It is typically covered with olfactory epithelium, and has a relatively great surface area in the highly olfactory Apteryx and Pagodroma. It is absent in only a few taxa, e.g., Sula, and Collocalia (Bang, 1971), and Psittacus (Pohlmeyer and Kummerfeld, 1989). In Collocalia the roof of the nasal cavity has an extensive olfactory epithelium (Bang and Wenzel, 1985; Osteo. Fig. 4.11).

(9) Concha nasalis septalis. Unique to petrels (e.g., Pagodroma), the septal nasal concha arises from the Seprum nasale and interdigitates with the Concha nasalis caudalis (Fig. 8.1c), its epithelium being olfactory (Bang, 1971).

(10) Meatus nasalis. The airway between the Conchae and the nasal walls (Figs. 8.1b, c). Since the three Conchae nasales lie in a rostrocaudal series, the mammalian terms, Meatus nasi dorsalis, medius, and ventralis are inapplicable.

(11) Valvula nasalis. The nasal valve is a paired crescentic mucosal fold attached to the Seprum nasale or to the adjoining roof of the. nasal cavity, level with the caudal end of the Concha media. Occurs in all water-feeding and diving birds with patent nostrils except Cincius, and in a few land species. It is forced into position by water pressure and then passively deflects water from the Regio olfactoria (Bang and Wenzel, 1985:205).

(12) Crista nasalis. Synonymy: Schwelle. The nasal crest is a ridge between the vestibular and respiratory regions in birds generally, but reduced or lacking in some species (Bang, 1971). It directs inspired air to the most rostral extension of the olfactory membrane (Bang and Wenzel, 1985:201).

(13) Regio vestibularis. Synonymy: nasal vestibule (Bang, 1971); vestibular zone, anterior zone (Sandoval, 1964). The vestibular region contains the Concha nasalis rostralis when this concha is present; it is lined by stratified squamous epithelium, and receives the secretion of the Glandula nasalis. It warms and humidifies the inspired air (Bang and Wenzel, 1985:2(0).

(14) Regio respiratoria. Synonymy: middle or respiratory area of Bang (1971) and Sandoval (1964). The respiratory region of the nasal cavity contains the Concha nasalis media. Its mucociliary epithelium is the primary defence against infection of the lower respiratory tract (Bang and Wenzel, 1985:203).

(15) Regio olfactoria. Synonymy: olfactory chamber (Bang, 1971); inner zone (Sandoval, 1964). The olfactory region contains the Concha nasalis caudalis and is lined by olfactory epithelium.

(16) Cisterna vestibularis. The vestibular cistern is a trough on the floor of the Regio vestibularis in many species. It catches secretion of the Glandula nasalis, thus humidifying the inspired air (Bang and Wenzel, 1985:2(0). Sinus septalis. The septal sinus (Fig. 8.lb) consists of bony spaces in the Seprum nasale which are continuous with the nasal cavity, occurring in a few species such as Rhea (Bang, 1971).

(17) Sinus infraorbitalis [Sinus antorbitalis]. Synonymy: orbital sac; subocular sac (Romanoff, 1960:537; BeUairs and Jenkin, 1960:290); maxillary sinus (Bang, 1971). The term "infraorbital sinus" is widely used in veterinary literature, the sinus being often infected. In Cacatua Ara, and Amazona the sinus has a capacious  extension into the upper beak, a transverse canal connecting the left and right sinuses, and a paired blind-ending cervical diverticulum (Pohlmeyer and Kummerfeld, 1989). The alternative term, Sinus antorbitalis, arises from homology with archosaurian reptiles and is widely used in paleontology (Osteo. Annot. 9).

(18) Sinus conchoinfraorbitalis [So conchoantorbitalis]. The concho infraorbital sinus occurs in the many species (e.g., Gallus) in which the Sinus infraorbitalis connects with the interior of the Concha nasalis caudalis (Bang, 1971).

(19) Apertura sinus infraorbitalis [A.s antorbitalis]. The opening of the Sinus infraorbitalis into the Cavum nasi.

(20) Glandula nasalis; Lobus medialis; Lobus lateralis. Synonymy: supraorbital gland (Beddard, 1898); salt gland. The nasal gland secretes salt in marine birds and in some desert species and raptors, but not in the large majority of terrestrial species (Peaker and Linzell, 1975:220). Therefore salt gland is not appropriate in birds  generally. Typically there is an independent Lobus lateralis and medialis (Technau, 1936). In Gallus, and closely related forms, only the Lobus medialis is present (Marples, 1932). See Osteo. Annot. 15.

(21) Diverticula cervicocephalica. Diverticula pneumatizing the skull, and sometimes other parts of the head and neck (Bignon, 1889; Groebbels, 1932:59; Coe, 1960; Bellairs and Jenkins, 1960:290; Romanoff, 1960:537; King, 1966:217). The cervicocephalic diverticula that invade the skull come from both the tympanic cavity and the nasal cavity (Osteo. Annot. 23,25). The cervical diverticulum of the psittacid infraorbital sinus (Annot. 17) is included; this extends as paired sacs nearly enclosing the vertebral column, surrounding the crop, and resting like a saddle over the shoulders (Walsh and Mays, 1984). In some birds, e.g., Leptoptilos, there are apparently major connexions between the nasal cavity and the air pouches of the neck (Coe, 1960; Akester, et aI., 1973) (which are examples of Sacci protrudentes (Topog. Annot. 28), and Osteo. Annot. 9, 23.

(22) Mons laryngealis. The conspicuous laryngeal mound carrying the opening into the larynx (Fig. 9.1).

(23) Glottis. The slit-like opening into the Cavum laryngis (Fig. 9.1). There were many synonyms in the early literarure (White, 1970:7), but this term is now used in amphibians and reptiles as well as birds (e.g., Marshall, 1962:403, 478, 585; Bock, 1978).

(24) Sulcus laryngealis. The prominent laryngeal sulcus, continuing the glottis caudally. Present in Anser and Gallus (White, 1970:8; 1975: 1891), and Corvus brachyrhynchos (Bock, 1978).

(25) Proc. rostralis; Corpus. The rostral process and body of the cricoid cartilage (Fig. 8.3). Incomplete, fused tracheal cartilages are attached ventrocaudally to the body in Columba (Zweers, et aI., 1981) and Corvus (Bock, 1978; White, pers. comm.).

(26) Crista ventralis. Synonymy: Proc. cricoideus medianus (Zweers and Berkhoudt, 1987). A median ossified ridge projecting dorsally from the Corpus of the Cart. cricoidea in Apteryx, Spheniscidae, Anas, Gallus, and Corvus (White, 1975: 1892; Zweers and Berkhoudt, 1987; McLelland, 1989:72).

(27) Ala; Cart. cricoidea dorsalis. In Accipitridae and Gallus (Fig. 8.3) each paired Ala (cricoid wing) is a cartilaginous plate attached dorsolaterally to the Corpus of the Cart. cricoidea by a strip of flexible cartilage; in Fulica and Pica attachment is  by a bony suture (see McLelland, 1989:72). In Corvus corax, C. orru and C. brachyrhynchos (Shufeldt, 1890:Fig. 10; White: pers. com.;. Bock, 1978) the Ala is represented by a separate, fully ossified, rod-like Cart. cricoidea dorsalis (Figs. 8.4, 7). In Corvus carone and C. monedula the dorsal cricoid cartilage is not totally separate, but rostrally has a small cartilaginous connexion to the rest of the cricoid cartilage (Zweers and Berkhoudt, 1987). The partial or complete separation of the dorsal cricoid cartilage may make the passeriform larynx more mobile, justifying a functional distinction between passeriform and non-passeriform larynges (Zweers and Berkhoudt, 1987).

(28) Cart. procricoidea. The small median procricoid cartilage intervenes between the two arytenoids, and between the two cricoid alae (Figs: 8.3, 6) or between the two dorsal cricoid cartilages (Figs. 8.4, 7). In Gallus (WhIte, 1970; 1975: 1892) and Columba (Zweers, et al., 1981) it is comma-shaped with a bony body(corpus) and a cartilaginous tail (cauda) (Fig. 8.2). In Corvus species (Fig. 8.4) it has no tail and is cuboidal (Bock, 1978; White, pers. comm.) or almost sphencal (Zweers and Berkhoudt, 1987). According to White (1970: 12) the term Cart. procricoidea was adopted by most earlier authors, but others regarded it as a part of the cricoid cartilage.

(29) Proc. caudalis. Synonymy: dorsal arytenoid (Bock; 1978). The caudal process of the arytenoid cartilage is variable, or even absent as in ratites and penguins (see McLelland, 1989:74). It forms a separate dorsal arytenoid cartilage in Corvus brachyrhynchos (Bock, 1978) as shown on the left side of Fig. 8.7, but not in Corvus orru and C. corax (White, pers. comm.) or in C. monedula and C. carone (Zweers and Berkhoudt, 1987).

(30) Juncturae laryngis [J. laryngeaIes]. There are four groups of articular structures of the larynx: (I) procricoid joints; (2) arytenoid joints;- (3) cricoid joints; and (4) extrinsic structures. Most of the laryngeaJ joints occur in all species studied, but in passerines the independent Cart. cricoidea dorsalis produces six additional joints (Zweers and Berkhoudt, 1987), all with names ending in "dorsalis". The terms are hyphenated to distinguish the two osteological constituents. For review see McLelland (1989:72-76).

(31) Juncturae procricoideae. The Cart. procricoidea articulates with the Cart. cricoidea and Cart. arytenoidea.

Artc. procrico-cricoidea. Synonymy: Artc. cricoprocricoidea (Zweers, et al., 1981). A synovial procrico-cricoid joint (Fig. 8.2) appears to be typical m nonpasserine species (spheniscids, Watson, 1883:201; Eudocimus albus, Baumel, pers.comm.; Gallus, White, 1975), but in Columba it is a syndesmosis, the elements connected by the Lig. procrico-cricoideum (Fig. 8;6).

Artc. procrico-cricoidea dorsalis. This synovial joint (Fig. 8.4) occurs in corvids between the procricoid and the dorsal cricoid cartilage (Bock, 1978; Zweers and Berkhoudt, 1987), being the homologue of the nonpasserine Artc. procrico-cricoidea. The joint is supported by the Lig. procrico-cricoideum dorsaIe (Fig. 8.7).

Artc. procrico-arytenoidea. Synonymy: Artc. arytaenoprocricoildea (Zweers and Berkhoudt, 1987). A synovial procrico-arytenoid joint (Figs. 8.2, 4, 6, 7) occurs in spheniscids (Watson, 1883:202), Gallus (White, 1975:1893), Columba (Zweers, et aI., 1981), and severaJ corvids (Bock, 1978; Zweers and Berkhoudt, 1987).

(32) Juncturae arytenoideae. The Cart. arytenoidea articulates with the Cart. procricoidea (Annot. 31), with the Ala of the Cart. cricoidea or with the homologous Cart. cricoidea dorsalis, and within its own components. Synd. aryteno-cricoidea. Synonymy: Artc. arytaenocricoidea (Zweers and Berkhoudt, 1987); Artc. cricoarytenoidea (NAA, 1979; McLelland, 1989:73). An aryteno-cricoid syndesmosis is formed in nonpasserines (spheniscids, Watson, 1883:202; Gallus, White, 1975: 1892; Columba, Zweers, et al., 1981; Strix, Baumel, pers. comm.), and corvids (Zweers and Berkhoudt, 1987), where the body of the arytenoid lies along the body and (in nonpasserines) the wing of the cricoid cartilage. The two cartilages are held together by the Lig. aryteno-cricoideum (Figs. 8.6, 7).

Synd. aryteno-cricoidea dorsalis. In corvids, the preceding syndesmosis is continued caudally by this additional syndesmosis, which is formed betwen the body of the arytenoid cartilage and the dorsal cricoid cartilage by the Lig. arytenocricoideum dorsale (Fig. 8.7) (Zweers and Berkhoudt, 1987).

Synd. intra-arytenoidea. The intra-arytenoid syndesmosis (Fig. 8.7) is a fibrous joint between the body and caudal process of the arytenoid cartilage in Corvus brachyrhynchos (Bock, 1978), but not in C. corax and C. arm (S. S. White, pers comm.) or C. carone and C. monedula (Zweers and Berkhoudt, 1987). See Annot. 29.

Synd. interarytenoidea. In Strix varia the caudal ends of the left and right Corpora arytenoidea articulate directly by fibrous tissue (see next paragraph), the interarytenoid syndesmosis (Baumel, pers. comm.).

Lig. interarytenoideum caudale. Synonym: arytenoarytenoid ligament (White, 1975: 1893). In Gallus (White, 1975) and Columba a strong unpaired caudal interarytenoid ligament (Fig. 8.6) joins the caudal ends of the left and right arytenoid cartilages (Zweers, et al., 1981). Presumably this ligament is the homologue of the fibrous tissue of the Synd. interarytenoidea.

Lig. interarytenoideum rostrale. Synonymy: Lig. intracricoideum rostraJe (Zweers and Berkhoudt, 1987). In certain corvids the rostral tips of the arytenoid cartilages are connected (Fig. 8.7) by a sheet of elastic fibres (Zweers and Berkhoudt, 1987).

(33) Juncturae cricoideae. The Cart. cricoidea articulates with the Cart. arytenoidea (Annot. 32), with the Cart. cricoidea dorsalis in passerines, and within its

own components.

Art. crico-cricoidea dorsalis. Synonymy: Artc. intracricoidea (Bock, 1978;

NAA, 1979; McLelland, 1979:72). The term Art. crico-cricoidea dorsalis comes

from Zweers and Berkhoudt (1987). Since it specifies the two components (Fig. 8.7),

it is preferred to the synonym. This synovial joint was recorded in several corvids

(Bock, 1978; White, pers. comm.; Zweers and Berkhoudt, 1987), but note the direct

cartilaginous connection mentioned in AnnO!. 27.

Synd. crico-cricoidea dorsalis. A syndesmosis in corvids between the caudal end

of the body of the cricoid cartilage and the dorsal cricoid cartilage, formed by the

Lig. crico-cricoideum dorsale (Fig. 8.7) (Zweers and Berkhoudt, 1987).

Synd. intercricoidea. In Strix varia (Baumel, pers. comm.), though not Columba

(Zweers, et aI., 1981), the caudal tips of the left and right Alae cricoideae articulate

directly in the midline.

Artc. intercricoidea dorsalis. A synovial joint in corvids formed by contact in the

midline of the caudal tips of the dorsal cricoid cartilages, bound by a strong Lig.

intercricoideum dorsaIe (Fig. 8.7) (Zweers and Berkhoudt, 1987). This joint is the

homologue of the preceding joint.

(34) Lig. trachoo-cricoideumj Lig. tracheo-cricoideum dorsalej Synd. cricobasibranchialisj

Lig. cricobasihyalej Lig. arytenoglossale. The Ligg. tracheocricoideum

and tracheo-cricoideum dorsale (synonym: Ligg. annulo trachealis

cricoideum and annulo trachealis cricoideum dorsale, Zweers and Berkhoudt, 1987)

connect the first three tracheal cartilages with the caudal border of the cricoid and

dorsal cricoid cartilages in corvids (Fig. 8.6) (Zweers and Berkhoudt, 1987). In

Columba and Strix varia the urohyal element of the hyoid bone is connected to the

ventral surface of the body of the cricoid cartilage by fibrous tissue, forming the

Synd. cricobasibranchialis (Baumel, 1979: 145). In some corvids an (elastic) cricobasihyal

ligament (Lig. cricobasihyale, synonym: Lig. hyocricoideum of Zweers and

Berkhoudt, 1987) connects the Crista dorsalis of the basihyal to the dorsal surface of

the cricoid cartilage. The Lig. arytenoglossale is a paired cord of elastic tissue in

Gallus, connecting the rostral process of the arytenoid cartilage with the cornu of the

paraglossal bone (White, 1975: 1894).

(35) M. dilator glottidisj M. constrictor glottidis. The dilator and constrictor

muscles of the .glottis are the intrinsic muscles of the larynx (Annot. 50). In Gal/us

(White, 1975:1894) and birds generally (Yarrell, 1833; Gadow'and Selenka, 1891;

Groebbels, 1932; White, pers. comm.) the dilator of the glottis is lateral and superficial,

running essentially from the wing and body of the cricoid to the arytenoid

cartilage (Fig. 8.5). The constrictor runs from the caudal midline of the larynx (typically

from the procricoid cartilage) to the arytenoid and cricoid cartilages (Fig. 8.5),

and has several divisions. In Gallus White (1975) distinguished three, i.e., medial,

lateral, and middle divisions, though their fibres intermingle.

In Columba the fibres of the constrictor muscle are attached not to the procricoid

but to the interarytenoid ligament (immediately dorsal to the procricoid) (Zweers,

et al., 1981). Bock (1978) distinguished three parts in the constrictor complex of

Corvus brachyrhynchos, and Zweers, et al. (1981) analysed the homologies of Bock's

three parts to the three divisions in Gallus of White (1975). Zweers, et al. (1981),

and Zweers and Berkhoudt (1987) identified five discrete muscles within the constrictor

complex of Columba (Fig. 8.5) and Corvus species, and established their homologies

within these two genera and in Gallus. In so doing, they suggested ten different

names for these two sets of five muscles.

These new srudies of the two intrinsic laryngeal muscles have not altered the original

interpretation of their function, which had been shown by electrical stimulation in

Gallus to dilate and constrict the glottis respectively (White and Chubb, 1967). These

functions have been confirmed cinematographically and electromyographically in

other species by Zweers, et al. (1981). Therefore it is proposed to retain dilation!

constriction of the glottis as the basis of the nomenclarure. With detailed knowledge

of these muscles in a wider range of species it may become advantageous to name the

individual components of the constrictor muscle (see Myol. Annot. 38).

(36) Cartt. tracheales. The tracheal cartilages are complete rings, closely interlocked,

with minimal intervals between them (Mclelland, 1965), and therefore the

Ligg. anularia of mammals are lacking; also there is no counterpart of the M. trachealis

of mammals. In sphenisciforms the trachea is divided into left and right channels

by a median seprum containing cartilaginous bars which are continuous with the

tracheal rings (Watson, 1883; Zeek, 1951). A seprum also occurs in certain procellariiforms

(Beddard, 1898:439,499). A longirudinal dorsal ridge resembling an incomplete

seprum, occurs in Casuarius sp. (Forbes, 1981).

Ansa trachealis. A tracheal loop or coil. One or several such loops occupy an

excavation in the sternum in Cygnus and gruids (see Johnsgard, 1961, for anseriforms,

and Mclelland, 1989:83, for review). In some other taxa the coils lie between

the skin and pectoral muscles, as in Platalea, Anseranas, Crax, and Aramus. Among

passerine birds, a coiled trachea occurs in the paradisaeid Manucodia (Ames,

1971:137) and Phonygammus (Riippell, 1933; Clench, 1978).

Saccus trachealis. In a few birds such as Dromaius (Murie, 1867) and Oxyura

jamaicensis (Wetmore, 1918) a tracheal sac opens from the trachea (Mclelland,

1989:87).

Bulbus trachealis. An expansion of the trachea, the tracheal bulb, occurs a short

distance rostral to the syrinx in the males of many anseriform species. A second

tracheal bulb occurs just caudal to the larynx in Melanitta fusca (see Mclelland,

1989:88, for review).

(37) Syrinx. Huxley (1877) introduced this term to replace "upper" and "lower"

larynx. Three types of syrinx, tracheobronchial, tracheal, and bronchial, were recognized

by nineteenth cenrury anatomists, according to the gross anatomical (not embryological)

distinction between the tracheal and the bronchial elements (Gadow,

1896:940; King, 1989:109). The tracheal elements are the direct continuation of the

trachea, and therefore lie in the midline and cranial to the bifurcation of the airway;

their skeletal components, i.e., the tracheosyringeal cartilages, typically are complete

rings. The bronchial elements lie caudal to the bifurcation of the airWay and are

therefore paired; their skeletal components, i.e., the bronchosyringeal cartilages,

constitute the skeleton of the most cranial part of the left and right primary bronchi

and are typically C-shaped half-rings.

The tracheobronchial syrinx (Fig. 8.8) has both tracheal and bronchial elements. It

occurs in the great majority of birds (Fiirbringer, 1888:1088; Gadow, 1896:941;

'Beddard, 1898:61; King, 1989:110). In the tracheal syrinx, specialization of the

tracheal elements dominates, as in the suboscine superfamily Furnarioidea. In this

taxon the wall of the tracheal part of the syrinx is largely membranous, the tracheosyringeal

cartilages being reduced to thin circlets embedded in the tracheosyringeal

membrane (Fig. 8.17) or absent (Fig. 8.18). Tracheal forms of syrinx occur in other

orders (King, 1989: 112). In the bronchial syrinx the bronchial elements are modified,

the syrinx of Steatomis being an extreme form (Fig. 8.9). Bronchial types of syrinx

also occur in sphenisciform and strigiform species (King, 1989: 115).

Ames (1971:14) classified the passeriform syringeal cartilages into "N' and "B"

types according to their shape. This system has proved its value in passeriform taxonomy

(e.g., Ames, 1971; Lanyon and Lanyon, 1989), but does not lend itself to the

general anatomical analysis of syrinxes. Although flawed (King, 1989: 117), the historical

method offers a simple anatomical basis for classifying the syrinx of many, if

not all, birds.

(38) Tunica mucosa respiratoria. The epithelial lining of the airways was reviewed

by King (1966), King and Molony (1971), Duncker (1971), Hodges (1974), Bang and

Wenzel (1985), and Mclelland (1989). The nasal cavity (except the Regio vestibularis),

larynx, trachea, syrinx, extrapulmonary primary bronchus, and intrapulmonary

primary bronchus have a basically similar respiratory epithelium, i.e.,

pseudostratified with ciliated columnar cells, goblet cells (Exocrinocyti callciformes),

basal cells, and simple alveolar mucous glands embedded in the epithelium.

The trachea also possesses a non-ciliated columnar cell characterised by microvilli

(Epitheliocytus microvillosus) (Mclelland, 1989:93), and in a few species the mucous

glands penetrate beneath the epithelium (Duncker, 1971:96). Where there is 

contact between membranes or movement, as in the larynx and syrinx, the epithelium

is modified. Thus, in the passerine syrinx (Setterwall, 1901), it changes to cuboidal

or stratified squamous on the lateral labium and simple squamous on the medial

rympaniform membrane (the primary vibrating membrane). In the roots of the secondary

bronchi the rypical respiratory epithelium of the primary bronchus changes

abruptly to a cuboidal epithelium without mucous elements, and then almost immediately

to a simple squamous epithelium which continues into the parabronchi.

Endocrinocyti respiratorii. Synonymy: neurite-receptor cell complex, Cook and

King, 1%9; granular cell, King, et al., 1974; granule-containing cell, McLelland and

Molony, 1983; neuroendocrine cell, Smith, et al., 1986; neuroepithelial cell, Cook,

et al., 1986a). Respiratory endocrine cells occur in the trachea and primary bronchus.

They contain membrane-bound dense-cored granules suggesting arninehandling

characteristics, and sometimes form synapses with presumptive afferent

axonal endings; they may therefore have a dual endocrine and receptor function (Cook

and King, 1969; King, et al., 1974; McLelland and MacFarlane, 1986; Cook, et al.,

1986a). In the intrapulmonary primary bronchus of Streptopelia risoria (McLelland

and MacFarlane, 1986), but not Gallus (King, et al., 1977), the endocrine cells form

large clusters resembling the pulmonary neuroepithelial bodies..of other vertebrate

classes.

(39) Tympanum. Synonymy: Trommel (Wunderlich, 1884); tracheal box (Gadow,

1896:941; Forbes, 1881; Beddard, 1898:289); drum (Ames, 1971: 15); rympanic box

or rympanic chamber (Warner, 1972b). The rympanum (King, 1989:125) is the rigid

cylinder formed by the close apposition or fusion of tracheosyringeal cartilages. Typically

its diameter exceeds that of the trachea. The Tympanum is a characteristic of the

tracheobronchial ryi>e of syrinx (Fig. 8.8). In most birds the most cranial cartilage of

the rympanum forms the cranial limit of the syrinx (Haecker, 1900). A rympanum is

also present in some tracheal rypes of syrinx (Figs. 8.17,18). In the most specialized

bronchial rypes of syrinx, as in StealOmis, the Tympanum is absent (Fig. 8.9).

(40) Bulla syringealis. Synonymy: Bulla tympanica. The rypical syringeal bulla is

an asymmetrical dilation of the left side of the rympanum (Figs. 8.12, 13) in males of

the subfamily Anatinae, except the Oxyurini (Johnsgard, 1961); in Tadoma tadoma

the dilation is greater on the right side (Gadow and Selenka, 1891:727; King,

1989: 133). In the males of most Anatini the bulla is largely or entirely osseous, but in

all Aythyini (Fig. 8.13) and most Mergini it is partly or extensively membranous

(Johnsgard, 1961; Warner, 1971).

(41) Cartt. tracheosyringeales. The most cranial of the tracheosyringeal cartilages

usually form the Tympanum. In a few taxa the cartilages become incomplete dorsally

and/or ventrally, as in Columbidae (Fig. 8.14), Psittacidae (Fig. 8.15), and Furnarioidea

(Figs. 8.17, 8.18) (King, 1989:128). Gaps thus created in the syringeal wall

are closed by Memm. tracheosyringeales.

(42) Cartt. bronchosyringeales. Synonymy: intermediary bars (Owen, 1866:331;

Miskimen, 1951); Halbringe. The bronchosyringeal cartilages are usually paired and

C-shaped. Compared with the true bronchial cartilages which follow them caudally,

they are broader, more irregular with expanded ends, and of greater diameter, but the

transition is gradual (King, 1989: 138). Their free ends rypically support the Mem.

rympaniforrnis medialis. In a few species bronchosyringeal cartilages immediately

caudal to the trachea are complete rings (King, 1989:138). The latter occur especially

in the bronchial rype of syrinx, where !O or more complete bronchosyringeal rings 

may follow the bifurcation of the trachea, as Steatomis (Fig. 8.9) (King, 1989: 138);

the complete rings are followed by several C-shaped cartilages bearing the Mem.

rympaniforrnis medialis.

(43) Pessulus. Synonymy: Steg (Haecker, 19(0). This median cartilage (Fig. 8.11)

splits the airway of the syrinx in most birds. It is absent in various taxa (King,

1989:141), including the oscine Alaudidae (Mayr, 1931), this being one of the two

significant deviations in the homogeneous structure of the oscine syrinx (Ames,

1971: 148).

(44) Mem. semilunaris. A projection of the. mucosa (Fig; 8.11) extending the Pessulus

cranially. Although often regarded as a component of the basic syrinx, the

semilunar membrane is erratically absent in both passeriform and non-passeriform

species (King, 1989: 165).

(45) Cartt. accessoriae. The accessory cartilages are small paired structures attached

to the medial rympaniform membrane or the tracheosyringeal and bronchosyringeal

cartilages.

Cart. membranosa dorsalis; Cart. membranosa ventralis. Synonymy: Cartt.

arytenoideae (Miiller, 1878; Owen, 1866:223); Cartt. tensores (Wunderlich, 1884);

Stellknorpel (Haecker, 1900); internal cartilages (Ames, 1971: 104, 144; Lanyon,

1984). These thin, paired, membrane cartilages of irregular shape nearly always lie in

the left and right medial rympaniform membranes, especially in Tyrannidae (Ames,

1971:104, 144). Haecker (1900) illustrated a dorsal cartilage in the oscine Pica (Fig.

8.10). KOditz (1925) believed that the ventral cartilage occurs in all oscines, a dorsal

cartilage being present in only some. A dorsal membrane cartilage was illustrated

by Miiller (1878:Plate V) in Anthracothorax dominicus (Trochilidae); Beddard

(1898: 191) described one at the ventral aspect of the first and second bronchosyringeal

cartilages of ramphastid species. These appear to be the only reports outside the

Passeriformes.

Proc. vocalis. This rather obscure term originated from Muller (1878:33), was

adopted by Garrod (1877) and Beddard (1898:69, 423), and reestablished by Ames

(1971:143). The term refers to a small paired cartilage rod or plate (Figs. 8.17, 18)

that appears to occur almost exclusively in the Furnarioidea (Garrod, 1877; Ames,

1971:143). It gives attachment to M. sternotrachealis, and in some genera also to

M. tracheolateralis and to the M. vocalis ventralis and/or dorsalis. Beddard (1898:69,

423) described a rudimentary Proc. vocalis in two species of Ciconiidae.

(46) Lig. interbronchiale. Synonymy: Bronchidesmus (Garrod, 1879; Myers,

1917). The term used by Wunderlich (1884) for the connective tissue bridge (Fig.

8.11) joining the left and right primary bronchi. The interbronchial ligament is

present in most but not all birds (King, 1989: 166).

Foramen interbronchiale. Synonymy: Subpessular air space (Warner, 1971,

1972a). The space between the bifurcation of the trachea and the Lig. interbronchiale

(Figs. 8.8, 11).

Lig. syringeale. The syringeal ligament is a loose fascial sheath originating from

the strong septum between the clavicles in Gallus (Youngren, et ai., 1974; Gaunt and

Gaunt, 1977). Contraction of the sternotrachealis muscle tenses the ligament and

rotates the pessulus, thus modifying the tension in the lateral rympaniform membrane

(Gaunt and Gaunt, 1977; Brackenbury, 1989:196).

(47) Mem. tympaniformis lateralis. Synonymy: Mem. tympaniformis externa

(Gadow, 1896:937; Greenewalt, 1968:27). One of the most difficult components of

the syrinx to define, the lateral tympaniform membrane is a membrane or series of

membranes between the lateral aspects of either the last tracheosyringeal cartilages

(Fig. 8.14) or the most cranial bronchosyringeal cartilages (Fig. 8.8b). Variants are

shown in Figs. 8.9, 16. In a few species such as Gallus it is well developed and a

major source of sound production. It appears to be absent in about as many nonpasseriform

species as it is present (King, 1989: 153). In oscines it is supposed to be the

region indicated in Fig. 8.11, but this is particularly controversial (King, 1989: 150-

159). Although authors have named this region the lateral tympaniform membrane,

Ames (1971: 16) and Warner (1972b) considered there to be no true membranous

areas in the lateral wall of the passeriform syrinx. Gaunt, et aI. (1973) pointed out the

proximity of the membrane to the lateral labium (Fig. 8.11); both components consist

of a thickened area of loose connective tissue in the lateral wall, so the anatomical

distinction between them is almost negligible (King, 1989:157, 165).

Mem. tracheosyringealis. The tracheosyringeal membrane or membranes contribute

to the dorsal and/or ventral wall of the tracheal element of the syrinx. They are

always associated with thinning or loss of tracheosyringeal cartilag!:s in the midline.

They occur especially in Columbidae (Fig. 8.14), Psittacidae (Fig. 8.15), and Furnarioidea

(Figs. 8.17, 8.18) (King, 1989:160).

(48) Mem. tympaniformis medlalis. Synonymy: Mem. tympaniformis interna

(Gadow, 1896:937; Ames, 1971:16; Warner, 1972b). The paired medial tympaniform

membrane (Figs. 8a, 11, 12, 14) seems to be present in the great majority of species,

being without question the primary vibrating membrane in many taxa (Greenewalt,

1968:28). The membrane is suspended between the free ends of the bronchosyringeal

cartilages. It is apparently absent in those few ciconiiform species which have a

tracheal type of syrinx wherein the bronchial rings are complete (King, 1989: 144). Its

presence in some psittacids has been questioned (Nottebohm, 1976; Gaunt and

Gaunt, 1985), but it is present in Aro arorouna (King, 1989: 144).

(49) Labium laterale; Labium medlale. Synonymy: labium externum, internum

(Haecker, 1900); .. inner and outer vocal cords", Setterwall, 190 1; Stimmpolster or

Stirnm1ippen (Ruppell, 1933). Paired connective tissue pads, projecting respectively

from the lateral and medial wall into the airway of the oscine syrinx (Fig. 8.11). The

lateral labium is one of the three "invariable features of the songbird syrinx", the

other two being the medial tympaniform membrane and perhaps the membrane cartilages

(Greenewalt, 1968). It is virtually indistinguishable from the lateral tympaniform

membrane (Annot. 47). Non-passerine species in general lack the lateral labium

(King, 1989: 164). The medial labium seems to occur only in passeriforms (King,

1989:165). .

Valvula syringealis. A crescentic syringeal valve projecting caudally from the lateral

wall of the right side of the tympanum in Anas (King, 1989: 149) and Aythya

ju/igu/a (Fig. 8.12) (Warner, 1971). A paired syringeal valve projects into the narrowest

part of the syringeal airway in Myiopsitta monachus (A. S. Gaunt, pers. comm.).

(50) Mm. laryngea1es; Mm. tracheales; Mm. syringeales. The muscles of the

airway between the larynx and lung are usually categorised as laryngeal, tracheal, and

syringeal muscles. A muscle that has extensive contact with the trachea could reasonably

be called a tracheal muscle; by pulling on the trachea such a muscle will almost

certainly act indirectly on the larynx at one end and on the syrinx at the other, and

could therefore be regarded also as a laryngeal or a syringeal muscle. Sometimes the

APPARATUS RESPIRATORIUS 273

muscles of the larynx, trachea, and syrinx are classified as extrinsic and intrinsic

muscles. An extrinsic muscle should have an attachment beyond the organ concerned,

whereas an intrinsic muscle should have all its attachments on the organ itself. This

distinction can be upheld for the larynx, the dilator and constrictor muscles being

clearly intrinsic and any other muscles extrinsic. However, in many species there can

be no truly intrinsic tracheal muscles, and unequivocal intrinsic syringeal muscles are

uncommon even in passeriforms (King, 1989:168, 172).

In the literature of the last two centuries many muscles have been associated with

the upper airways of birds. The same name has often been applied to nonhomologous

muscles, and different names have been applied to homologous muscles (George and

Berger, 1966:262). The basic problems are the small size of many of these muscles

and the occurrence of detailed interspecific variations. It can be difficult to decide

whether a fascicle of muscle fibres is a new muscle, a minor variant of a muscle

previously known, or a dissection artefact.

M. cleidohyoideus. In the NAA (1979), this muscle was named M. sternohyoideus.

Zweers (1982) established from the literature that, in birds examined so far,

there is a muscle that attaches to the clavicle at its caudal end, runs cranially in close

relationship to the skin of the neck and the trachea (though not directly attached to the

trachea), and attaches at its cranial end to the larynx or in some species the hyoid

bone; this is well attested in Tetroo urogallus by Yarrell (1833) (his furculo-tracheal

muscle), in Orus by Fisher and Goodman(l955) (their M. tracheohyoideus), in Nucifraga

by Bock, et aI. (1973) (their M. tracheohyoideus), in Calidridinae by Burton

(1974) (his M. cleidohyoideus), in Gallus by Gaunt and Gaunt (1977) (their M.

tracheohyoideus), and in Columba Livia by Zweers (1982) (his M. claviculohyoideus).

The term M. sternohyoideus, as in the first edition of the NAA, is a misnomer for this

muscle, because it has no attachment to the sternum. M. tracheohyoideus is equally a

misnomer, because it is not known to arise from the trachea in any species of bird.

Gaunt and Gaunt (1977) suggested that the best name would be M. cleidohyoideus,

which expresses the correct caudal attachment. An alternative would be M. cleidolaryngeus,

which would also describe the correct cranial attachment not only in Gallus

but in passeriforms as well (so far as is known). However, workers on the passeriform

larynx (e.g., Bock and his coworkers) have hitherto been content with the suffix

"-hyoideus" when naming this muscle. The adoption of M. cleidohyoideus rather

than cleidolaryngeus will therefore minimize disturbance among established terms.

M. sternohyoideus. Gadow and Selenka (1891:307) used the expression "System

des m. sterno-hyoideus" to cover a list of about 10 muscles. Most of these appear to

be synonyms for one muscle, but their use of "System" implied that some of these

names might relate to separate muscles. They then stated (p. 308) that a true M.

sterno-hyoideus, as seen in its primitive condition in reptiles, does still occur in

Apteryx. They also suggested (pp. 310, 730) that parrots possess a similar "sternohyoid"

muscle (except that it fails to reach the sternum). M. sternohyoideus will not

be listed in the NAA until its existence in birds is confirmed.

M. tracheohyoideus. The M. tracheohyoideus was not formally listed in the NAA

(1979), but Vanden Berge included it in his Table I. Zweers (1982) pointed out that

the M. tracheohyoideus of Fisher and Goodman (1955) in Orus americana and of

Bock, et aI. (1973) in Nucifraga are the same muscle as the cleidohyoideus of Burton

(1974) in charadriiforms and his own M. claviculohyoideus in Columba Livia; thus

these muscles are in fact the M. cleidohyoideus discussed two paragraphs above.

Zweers (1982) also revealed that at least one other group of recent authors has applied

the term tracheohyoideus to the M. tracheolateralis. M. tracheohyoideus will not

be listed in this edition of the NAA.

M. cricohyoideus. Zweers (1982) reported this muscle in Columba livia as running

between the cricoid and the hyoid bone; presumably it is an extrinsic laryngeal muscle

(Mclelland, 1989:76). In C. livia it consists of a small dorsal and a large ventral

component, the M. cricohyoideus dorsalis and ventralis, which arise respectively

from the dorsal and ventral aspects of the Os basibranchiale and insert together on the

ventral and ventrolateral aspect of the cricoid cartilage. Zweers interpreted the dorsal

component as representing the M. thyrohyoideus of George and Berger (1966:262) in

birds generally, of Fisher and Goodman (1955) in Grus, and of Bock, et al., (1973) in

Nucifraga, and representing the M. thyreohyoideus of Burton (1974) in Charadrii and

of Zweers et al. (1977) in Anas. In other species, apparently only one component is

present. Thus the dorsal component of this muscle, but not the ventral, was found by

Zweers and Berkhoudt (1987) in Corvus carone and C. monedula, and by Heidweiller

and Zweers (1990) in the estrildids Poephila guttata and Lonchura striata; in these

species the authors referred to it as either "M. cricohyoideus", or "M. cricohyoideus

(dorsalis)". Hornberger and Meyers (1989) also used the term M. cricohyoideus in

Gallus. However, they interpreted' their muscle as representing the combined

M. cricohyoideus ventralis and M. hyovalvularis of Zweers (1982) in Columba. In a

Thble of synonymies and homologies, Homberger and Myers identified in the literature

nine other names that had been applied to their M. cricohyoideus. This illustrates

the difficulty of codifying the terminology for such muscles with justice to all authors.

Moreover, the terminology is still in active evolution-see, e.g., the use of

M. thyreohyoideus in Anas by Zweers, et al. (1977), followed by the substitution of

M. cricohyoideus dorsalis for an apparently homologous muscle in Columba by

Zweers (1982). The selection of names in the NAA must inevitably be arbitrary, and

subsequent changes will probably be necessary as further knowledge becomes available.

For the pharyngeal functions of these muscles see Myol. Annot. 36.

M. tracheovalvularis. A very small muscle in Columba livia passing between the

first tracheal rings and the pharyngeal wall, and represented by Bock's (1978) cricohyoideus

posterior in Corvus, (Zweers, et al., 1981); an extrinsic laryngeal muscle

(Mclelland, 1989:76).

M. hyovalvularis. A muscle in Columba livia running along the dorsolateral aspect

of the larynx, between the hyoid bone and the pharyngeal wall (Zweers, et al., 1981),

and also present in Poephila guttata and Lonchuro striata (Heidweiller and Zweers,

1990). Interpreted by Zweers (1982) as represented by the M. dermoglossus and

M. thyrohyoideus of Grus (Fisher and Goodman, 1955), the M. cricohyoideus superior

of Nucifraga (Bock, et al., 1973), and the M. thyreohyoideus superior of Loxops

(Richards and Bock, 1973). Homberger and Meyers (1989) regard it as part of their

M. cricohyoideus in Gallus; this is an extrinsic laryngeal muscle (Mclelland,

1989:76). See Myol. Annol. 36.

M. sternotrachealis (Fig. 8.6). Owen (1886:224) regarded this as "the most constant

of all the muscles affecting the lower larynx", and George and Berger (1966:263)

believed that it "has apparently been found in all birds studied". Ames (1971: 1 09)

confirmed that it occurs in passerines generally. Beddard (1898:258) claimed its

absence in some psittaciforms, but Gaunt and Gaunt (1985) and King (1989:168)

found it in six psittacid species; feeble in oscines (Ames, 1975; Warner, 1972b).

M. cleidotrachealis (Fig. 8.13). Synonymy: M. ypsilotrachealis (Gadow and Se-

1enka, 1891:730; RuppeU, 1933; Lockner and Youngren, 1976). This synonym has

been very widely employed, but M. c1eidotrachealis has also been used for a long

time (e.g., Beddard, 1898:292). German veterinary anatomists have applied M. ypsilotrachealis

to the M. sternotrachealis; this term has therefore been used for two

entirely different muscles, and for this reason M. c1eidotrachealis is preferred. This

APPARATUS RESPIRATORIUS 275

muscle has been described in many members of the Anseriformes (Gadow, 1896:938;

Beddard, 1898:464; Riippel!, 1933; Lockner and Youngren, 1976; King, 1989:168).

It has also been reported in representatives of four other orders, e.g., Crypturellus,

Crax, and Tockus by Beddard (1898:222, 292, 487), and sphenisciforms by Watson

(1883). The essential characteristics of this muscle are its origin from the clavicle and

its direct insertion on the trachea, cranial to the insertion of M. sternotrachealis.

M. tracheolateralis (Fig. 8.8). Synonymy: M. contractor tracheae (Watson, 1883);

M. tracheobronchialis (Haecker, 1900); M. laryngosyringeus (KOditz, 1925); M.

bronchotrachealis (Ruppel!, 1933); M. trachealis lateral is (Zweers, 1982); M. cricotrachealis

lateralis (Zweers and Berkhoudt, 1987). This paired muscle occurs in the

great majority of avian orders, if not all (Fiirbringer, 1888: 1089; Beddard, 1898:62;

Gadow, 1896:938; Ames, 1971:105, 133). Complete loss of this muscle has been

claimed in some ratites, most ciconiids and cathartids, and some galliforms, but

sometimes the loss is "complete" only in the sense that the muscle ends wel! cranial

to the syrinx (King, 1989: 169). Typically it attaches caudally to the syrinx, forms a

lateral band along the whole of the trachea, and attaches cranially to the larynx. It is

sometimes divided into a dorsal and a ventral part, the former attaching cranially to

the larynx and the latter to the hyoid (respectively, M. tracheal is lateralis, pars cricoidea

and pars hyoidea of Zweers, 1982); or both parts attach to the larynx (the

M. cricotrachealis lateralis of Zweers and Berkhoudt, 1987). For further discussion

see Mclelland (1989:98) and King (1989: 169).

(51) Mm. syringeales. The principal sources on the passeriform syringeal muscles

are Ames (1971, 1975) and Warner (1 972b) , with contributions from Miskimen

(1951). The anatomy of the syringeal muscles in subpasseriforms is less wel! known.

However, the 19th century literature contains much information on the muscles of

subpasseriforms (see Fiirbringer, 1888: 1087; Gadow, 1896:937; and particularly

Beddard, 1898). For review see King (1989:169).

The syringeal muscles are very small, and not always sharply distinguished from

each other anatomically. This no doubt accounts for the different numbers of syringeal

muscles claimed by various authors in oscines, even though this taxon is noted

for the anatomical uniformity of these muscles (Ames, 1971:94; 1975); for example,

the maximum total number of paired, muscles (excluding M. sternotrachealis and M.

tracheolateralis) is four according to Ames (1971:89), five according to Warner (1972b),

seven according to Fiirbringer (1888: 1091), and eight according to KOditz (1925).

As noted by George and Berger (1966:268), Ames (1971: 10), and Warner (1972b),

the nomenclature most commonly used for the passeriform syringeal muscles originated

with Owen (1866:223); Ames employed this terminology. Fiirbringer's (1888)

nomenclature, however, was adopted by Gadow (1896:939) and Haecker (1900), and

has been closely followed by Warner (1972b) also. Among other major terminologies

are those of Wunderlich (1884), Setterwal! (1901), and KOditz (1925). Synonymy was

worked out by KOditz (1925), Ames (1971:90), and Warner (1972b), essentially as in

Table 8. 1. The terminology adopted here is based on that of Fiirbringer (1888).

M. tracheobronchialis dorsalis/brevis/ventralis; M. syringealis dorsalis and

ventralis. Synonyms: see Table 8.1. These syringeal muscles are present in oscines

as in Fig. 8.20. Ames (1971 :89-94) interpreted the M. tracheobronchialis dorsalis

and brevis as two parts of the same muscle, and considered the M. syringealis

dorsalis and ventralis, and the M. syringealis dorsalis also occur in the suborder

Menurae (Ames, 1971:85,87).

M. vocalis dorsalis and ventralis; M. obliquus ventralis and lateralis. These

occur in suboscine passeriforms as in Figs. 8.15, 16 and 17 (Ames, 1971:20-79).

M. syringealis superficialis/profundus; M. syringealis caudalis; M. syringealis.

The non-passeriform groups usually have no intrinsic syringeal muscles and only a

single paired (clearly) extrinsic syringeal muscle, the M. tracheolateralis, which typically

inserts on the tracheal or bronchial elements of the syrinx. This is the basic

tracheobronchial syrinx which is generally agreed to occur in the majority of nonpasserine

orders (Fiirbringer, 1888: 1089; Gadow, 1896:938; Beddard, 1898:61; Ames,

1971:133; King, 1989:175); it also occurs in several families of suboscine Passeriformes

as in Psarisomus (Eurylaimidae) (Ames, 1971:133). However, there are

certainly two pairs of short syringeal muscles in some psittacids (Gadow, 1896;

Evans, 1969:70; Nonebohm, 1976; Gaunt and Gaunt, 1985; King, 1989:176); it is

proposed to name these according to their topographical position, i.e., M. syringealis

superficialis and M. syringealis profundus (Figs. 8.15, 16). There is also a fully

authenticated single pair of true syringeal muscles in Steatomis ;:aripensis (Suthers

and Hector, 1985, their M. broncholateralis), which can reasonably be distinguished

by the term M. syringealis caudalis because of its unique position caudal to the

division of the airway (Fig. 8.7). The presence of one additional pair of short specialized

syringeal muscles in Gal/inago and Falco was mentioned by Wunderlich (1884),

Fiirbringer (1888: 1089), and Gadow (1896:939), but without full documentation.

Forbes (1881) reported with an illustration a very convincing single pair of true

syringeal muscles in Rhea. Any such single pairs of muscles would now be called

simply M. syringealis, until authenticated details of their topography and attachments

justify adding a descriptive adjective to the name. Hasty commitment to homologies

or functions should be avoided.

(52) Broncbus primarius, Pars extrapulmonalis; Cartt. broncbiales; Memm.

interanulares; Lig. bronchiale mediale. The term Bronchus primarius was introduced

by Juillet (1912). The extrapulmonary part of the primary bronchus lies between

the syrinx and the lung. ItS bronchial cartilages are C-sbaped, except in

Hirundinidae wbere they are complete rings (Warner, 1972b). The thin interannular

membranes connect adjacent bronchosyringeal and/or bronchial cartilages (Figs.

8.8b, 10). The thicker medial bronchial ligament completes the gap between the ends

of the bronchial cartilages (Fig. 8a) (King, 1989:23).

(53) Facies costa1is; Facies vertebralis; Facies septalis. The costal surface of the

lung adjoins the thoracic wall, its vertebral surface relates to the vertebrae, and its

septal surface faces the Septum horizontale (see Chap. 7).

(54) Sulci costales; Tori pulmonales; Tori intercostales; Tori marginales. The

ribs make costal sulci on the costal and vertebral surfaces of the lung. Between two

Sulci costales (Fig. 8.22) there is a Torus intercostal is (Quitzow, 1970) an approximately

transverse strip of lung tissue. Together, the intercostal and marginal tori

constitute the Tori pulmonales. The term Torus pulmonis was used by Schulze (1908)

and Groebbels (1932:44).

(55) Margo costovertebralis; Margo costoseptalis; Margo vertebroseptalis;

Margo cranialis; Margo caudalis; Angulus craniodorsalis; Angulus catidodorsalis;

Angulus cranioventralis; Angulus caudoventralis. Figure 8.21 shows the relationships

between the borders, angles, and surfaces (Quitzow, 1970) of the essentially

APPARATUS RESPIRATORIUS 277

quadrilateral lung of most birds. In primitive species with a poorly developed

Neopulmo (Annot. 57) the cranioventral and the caudoventral angles are indistinct,

making the lung triangular witb the apex pointing ventrally (Duncker, 1972).

(56) Planum anastomoticum; Linea anastomotica. Terms introduced by Locy and

Larsell (1916a). Synonymy: Linea serpta, Quitzow, 1970. The anastomotic plane and

its superficial Linea are caused mainly by the terminal anastomoses of the Parabronchi

of: (a) the medioventral and mediodorsal secondary bronchi (Figs. 8.22, 23), and

(b) the medioventral and lateroventral secondary bronchi (Fig. 8.23). The line is

visible on the surface (Fig. 8.21).

(57) Paleopulmo; Neopulmo. Terms proposed by Duncker (1971), to indicate a

phylogenetic relationship between the two main components of the lung. The Paleopulmo

is present in all birds. It consists (Fig. 8.23) of: (a) Bronchi medioventrales

andmediodorsales, and their Parabronchi; (b) the large Bronchus lateroventralis

which connects directly to the Saccus thoracicus caudalis; and (c) two or three

intermediate-sized Bronchi lateroventrales, which medially form Parabronchi joining

Parabronchi from the fourth Bronchus medioventralis at the Planum anastomoticum.

In supposedly primitive birds (e.g., sphenisciform species) the Paleopulmo forms the

whole of the lung.

In most birds the Neopulmo forms about one tenth of the lung. It is a network (Fig.

8.23) of anastomosing bronchi consisting of: (a) the Bronchi laterodorsales and their

Parabronchi; (b) laterally directed Parabronchi of the Bronchi lateroventrales; and

(c) the connexions of this network to the caudal air sacs. It was named the reseau anastomotique

by Campana (1875) and Locy and Larsell (1916a). McLelland (1989:234-

236) has summarized the progressive development of the neopulmo in various taxa.

(58) Bronchus primarius, Pars intrapulmonalis. The part of the primary bronchus

that lies within the lung is its intrapUlmonary part (Juillet, 1912). It ends caudally

by opening into the Saccus abdominalis (Fig. 8.22). A dilated mid-region, the

"Vestibulum" was described by Huxley (1882) and mentioned by many others, but is

not present in Gallus (Juillet, 1912; Payne and King, 1959; Akester, 1960; Quitzow,

1970) or in Anas and Columba (Akester, 1960). The term Vestibulum has also been

applied to the region of the Bronchus primarius where the Bronchi medioventrales

arise (Juillet, 1912; Groebbels, 1932:7), and even to the region of the Bronchus

primarius which is devoid of branchings (Duncker, 1971). The term Mesobronchus

was used by Huxley (1882) and a number of later authors for the region of the

Bronchus primarius which lies caudal to the supposed Vestibulum. In view of its

uncertain characteristics the term Vestibulum should not be used.

(59) Bronchi secundarii. These are the bronchi of the second order, and therefore

include all those that arise from the primary bronchus (Campana, 1875 :31; Locy and

Larsell, 1916a). The earlier authors (e.g., Campana, 1875; Schulze, 1908) named

them according to either the orientation of their origin from the primary bronchus, or

their subsequent direction, or both their origin and their direction. At that time, both

their orientation and their direction had been erroneously described (see Annot. 57 of

NAA, 1979), and so the resulting terminology was misleading. A further complication

has been the use of the same term for two or more different groups of secondary

bronchi, as with "ventrobronchi", "dorsobronchi", and "Iaterobronchi" (Table 8.2).

The resulting confusion pervaded the literature on the anatomy and physiology of

the avian lung. The NAA (1979) produced a new terminology, on the two following

principles: (1) all terms for the Bronchi secundarii should be based on the

lung territory which they supply, as in Figure 8.23 (a relatively neglected precept, 

Quitzow, 1970); (2) Terms which have already been in use, but with various meanings,

should be avoided. The following new terms for the secondary bronchi resulted:

Bronchi medioventrales, mediodorsales, lateroventrales, and laterodorsales. In the

decade following the NAA (1979) these terms have been widely adopted by anatomists

and physiologists. The same terms are listed here.

(60) Bronchi medioventrales. Synonymy: See Table 8.2. The medioventral bronchi

are the four (or five) secondary bronchi which supply the medial and ventral regions

of the lung (Fig. 8.23). They arise from the dorsomedial wall of the cranial region of

the Bronchus prirnarius (Fig. 8.22) (Fischer, 1905; King, 1966: 181; Quitzow, 1970).

Many of their main branches pass in the medial direction over the Facies septalis to

end by turning dorsally onto the Facies vertebralis.

(61) Bronchi mediodorsales. Synonymy: Table 8.2. The mediodorsal secondary

bronchi supply the medial and dorsal regions of the lung (Fig. 8.23). They arise from

the dorsal wall of the caudal part of the Bronchus primarius (Fig. 8.22), and then

travel dorsally (Duncker, 1971).

(62) Bronchi lateroventrales. Synonymy: Table 8.2. The lateroventral secondary

bronchi supply the lateral and ventral regions of the lung (Fig. 8.23). Their origins

are directly opposite to those of the Bronchi mediodorsales (Fig. 8.22), i.e., from the

ventral wall of the caudal part of the Bronchus prirnarius, and their course is ventral

or caudoventral (Payne and King, 1960; King, 1966: 181; Quitzow, 1970; Duncker,

1971). In birds generally, the large first or second bronchus coIi.nects with the Saccus

thoracicus caudalis. The subsequent two or three intermediate sized bronchi contribute

parabronchi to the Paleopulmo in all species; in species in which the Neopulmo is

developed these intermediate sized Bronchi lateroventrales, and yet other more caudal

and smaller ones, contribute parabronchi to the Neopulmo (Fig. 8.23).

(63) Bronchi laterodorsales. Synonymy: Table 8.2. These supply the lateral and

dorsal regions of the lung (Fig. 8.23). They form a large part of the Neopulmo; since

the degree of development of the Neopulmo varies greatly, the position, diameter, and

number of the Bronchi laterodorsales also vary (Campana, 1875; Locy and Larsell,

1916a; Groebbels, 1932; King, 1966; Quitzow, 1970). They arise from the lateral

wall of the caudal part of the Bronchus primarius and extend mainly laterally. The

firs! two or three are of large diameter (certainly in Gallus, see King, 1966: 182, and

in Cygnus, see Fig. 30b of Duncker, 1971). The more caudal of these secondary

bronchi are similar in diameter to Parabronchi; because of this, some authors (e.g.,

Akester, 1960; Duncker, 1971) excluded the whole of this group of bronchi from

those of the Bronchi secundarii and classified them as Parabronchi.

(64) Parabronchus. Synonymy: Bronchus tertiarius (Campana, 1875; Akester,

1960; King, 1966; Lasiewski, 1972); Lungenpfeife (Krause, 1922); Bronchi fistularii

(Quitzow, 1970; Gerisch, 1971). The Parabronchi are bronchi of the third or subsequent

orders of branching, i.e., they arise from the Bronchi secundarii or from the

subdivisions of the Bronchi secundarii (Fig. 8.22). The term Parabronchus is long

established, having been introduced by Huxley (1882), and is now in general use by

anatomists and physiologists. It includes both the parabronchial airway and the mantle

of exchange tissue which surrounds that airway; the boundary of the Parabronchus is

the Septum interparabronchiale (Annot. 70).

(65) Atrium. Synonymy: bronchiolus, vestibulum, fossa (see King, 1966: 195;

Gerisch, 1971:6). The term atrium was introduced by Krause (1922:295). The atria

are the polygonal chambers (Fig. 8.24) leading towards the air capillaries from the

APPARATUS RESPIRATORIUS 279

Parabronchi and from many secondary bronchi. The term is in general use, the many

alternatives having fallen into disuse. For species variations see Annot. 70.

(66) M. atrialis. The atrial muscles form a network of smooth muscle bundles (Fig.

8.24) around the openings into the atria (King and Cowie, 1969; Geriscfi and

Schwarz, 1972; West, et al., 1977; McLelland, 1989:237). See Annot. 70.

(67) Septum interatriale. The thin interatrial septa (Fig. 8.24) are the atrial walls,

separating adjacent atria (Gerisch, 1971). See also Annot. 70.

(68) Infundibulum. The term Infundibulum apparently originated from Krause

(1922:292). It refers to the funnel-shaped ducts that open from the floor of an Atrium

(Fig. 8.24) and lead to air capillaries. According to Gerisch (1971) the infundibula

also give rise to Rami respiratorii, which are intermediate in size between Infundibulum

and Pneumocapillaris. '

(69) Epitheliocytus granularis. Synonymy: Epitheliocytus magnus, Cellula granularis

(NAA, 1979; McLelland, 1989:246). The granular epithelial cell lines the

Atrium and contains osmiophilic laminated bodies (for review see King and Molony,

1971: 119). It is probably homologous to the the septal cell, great alveolar cell, type 2

epithelial cell, or granular pneumocyte of mammals.

(70) Septum interparabronchiale. The interparabronc;hial septa separate the exchange

tissue of adjacent Parabronchi. According to Duncker (1971), these septa, and

also the Atria and the Mm. atriales, are best developed in birds which fly poorly or

not at all. Maina, et al. (1982) found that all these structures are well developed in

anseriforms, galliforms, and charadriiforms, and poorly developed in columbiforms,

psittaciforms, cuculiforms, and passeriforms, the septa often being entirely lost. See

McLelland (1989:236) for review.

(71) Pneumocapillaris. Synonymy: Thbulus respiratorius, Ductulus respiratorius.

The term air capillary or Luftkapillaren has been widely used since the beginning of

the 20th century. Gerisch (1971) suggested Ductulus respiratorius, because he believed

that anastomoses are not sufficiently common to justify the term air capillary.

. Smith, et al. (1986) proposed "respiratory labyrinth" because anastomoses are so

profuse, but this term would be inapplicable to the individual tubules within the

complex. The profuse anastomoses and fluctuating calibres of the air capillaries, and

their interlocking relationships with the narrower and more uniform blood capillaries,

were established by Maina (1982, 1988), with observations also by West, et al. (1977)

and Fujii, et al. (1981). The quantitative morphology of the blood gas barrier and

many other pulmonary components has been reviewed by Maina (1989:307-368) and

Maina, et al. (1989).

(72) Epitheliocytus respiratorius. The respiratory epithelial cell which lines the

Pneumocapillaris is homologous to the similar cell in the mammalian alveolar wall

(the small alveolar cell, or type 1 epithelial cell), but it is much thinner than in

mammals and is also the only cell lining the barrier, thus minimizing barrier thickness

(Maina and King, 1982).

(73) Ostium. A term widely used but seldom defined. Muller (1908) and Schulze

(1908) applied it to the general zone of attachment of the air sac to the lung, enclosing

one or several actual orifices which open into the bronchi; King (1966:224) defined it

. explicitly in this way. Campana (1875:27) used Infundibulum for this general zone.

Quitzow (1970) introduced the term "Area saccopulmonalis" for the same region;

like Groebbels (1932) she restricted the term Ostium to the single opening from an air 

sac into a secondary (or the primary) bronchus. The older meaning of Muller (1908)

and Schulze (1908) was adopted in the NAA (1979), and is retained here (Fig. 8.22).

Within an Ostium there are two types of opening: (1) "Indirect connexion" which

connects the air sac to Parabronchi (the Bronchi recurrentes of Schulze, 1910; Juillet,

1912; and other authors, and the indirect connexions of King, 1966:223), and

(2) "Direct connexion" which connects the air sac to a secondary, or to the primary,

bronchus (the "bronche directe" and "orifice direct" of Juillet, 1912; the "direkt

Bronchen" and "direct Ostien" of Groebbels, 1932, and the "direct connexion" of

King, 1966:223). Terms that indicate the direction of air flow in these connexions

should be avoided, in view of the actual complexity of the flow (see Scheid and

Piiper, 1989:376-381 for review). This excludes Bronchi recurrentes, and probably

also the Bronchi pulmosaccales and saccopulmonales of Quitzow (1970). The terms

"direct" and "indirect connexions" do not suggest direction of flow, and have been

established for a long time. They are recommended for descriptive purposes, but not

listed as official terms. For a review of the Ostia and their connexions see McLelland

(1989:265-269) .

(74) Saccobronchus. This is an old term adapted to a new meaning by Duncker

(1971). It now refers to a single large funnel-like bronchus wl).ich collects many

parabronchi and connects with an air sac. The old meaning was applied (e.g., by

Schulze, 1910) to the many small parabronchial connexions of an air sac, the term

thus being synonymous with Bronchus recurrens; this older usage was retained by

some more recent authors (e.g., Quitzow, 1970).

A Saccobronchus (in the new sense) occurs only in the Saccus abdominal is and

Saccus thoracicus caudalis. The Saccus abdominalis has been found to possess one

such Saccobronchus in birds generally, except in Dromaiidae and Spheniscidae

(Duncker, 1971). A Saccobronchus is particularly well developed in both the Saccus

abdominal is and the Saccus thoracicus caudalis of Ciconia, Anas, and Pluvialis

(Duncker, 1971: Figs. 24-26, 32).

(75) Aa. interparabronchiales; Arteriolae intraparabronchiales. The general architecture

of the pulmonary circulation was established by Abdalla and King (1975).

The microanatomy of the vasculature and the terminal airways was described by

Maina (1982, 1988) and West, et aI. (1981), with contributions by Akester (1974)

and Fujii, et al. (1981). Radu and Radu (1971) provided information on the rami of

the left and right pulmonary arteries (Art. Annot. 2).

Each ramus of the pulmonary artery gives rise to many interparabronchial arteries.

These lie in the interparabronchial septa, and give off intraparabronchial arterioles

which give rise to blood capillaries (Fig. 8.24). The blood capillaries form an anastomosing

network interlocking with the network of air capillaries. The deoxygenated

blood from the pulmonary trunk is delivered at right angles to the long axis of each

parabronchus, causing a cross-current relationship between bulk parabronchial gas

flow and blood flow (Scheid and Piiper, 1970).

Vv. interparabronchiales; Vv. intraparabronchiales; Vv. atriales; Venulae septales;

Venulae intraparabronchiales. Some of the blood capillaries drain into septal

venules and then via atrial veins into intraparabronchial veins; most of them empty

via intraparabronchial venules into intraparabronchial veins, and thence into interparabronchial

veins (Fig. 8.24). See Yen. Annot. I. 2). 'There is no anatomical

evidence for arteriovenous anastomoses in the avian lung (Abdalla and King, 1976a).

R. bronchialis; V v. bronchiales. The paired bronchial rami arise from the A.

esophagotracheobronchialis (Abdalla and King, 1976b, 1977). In anseriform, galliform,

and columbiform species the bronchial veins of the extrapulmonary part of the

APPARATUS RESPIRA1URIUS 281

primary bronchus drain via esophageal veins into the V. esophagotrachealis and

thence into the cranial vena cava; the intrapulmonary part, and in Gallus the caudal

region of the extrapulmonary part, drain into the pulmonary vein. For reviews of the

pulmonary and bronchial circulation see West, et al. (1981:287-298) and Abdalla

(1989:281-306).

(76) Sacci pneumatici. In all birds air sacs arise from the lungs. The literature on

their anatomy is vast, much of it from the 19th century and not all of it reliable. Good

general surveys were made by Baer (1896), Schulze (1910), and especially Groebbels

(1932:54-76). More recent reviews are by King (1966:207-221) and McLelland

(1989:258-271). There are six primordial pairs of sacs, but in nearly all birds two

pairs fuse to form the median clavicular sac. The anatomy of the sacs varies greatly

between species.

(77) ~accus cervicalis. Synonymy: superior-posterior sac, Campana (1875); thoracocervlcal

sac, McLeod and Wagers (1939). The cervical sac consists of a pair of

main chambers and diverticula. The main chambers fuse to form a median compartment

in several orders (King, 1966:209), and rarely (e.g., Meleagris, King and Atherton,

1970) also fuse with the Pars lateralis of the clavicular sac to form a

cervicoclavicular sac. The'sac is absent in Gavidae and Podicipedidae (Gier, 1952;

Duncker, 1971).

(78). Diverticula vertebralia. The vertebral diverticula of the Saccus cervicalis pass

crarually and caudally along the vertebral column in birds generally (Groebbels

1932:56; King, 1966:209; Duncker, 1971:50). '

(79) Diverticula interrnuscularia. In some birds intermuscular diverticula of the

Saccus cervicalis penetrate between the cervical muscles and accompany branches of

the brachial plexus (Duncker, 1971 :50).

(80) Diverticula subcutanea. Extensive subcutaneous diverticula of the Saccus cervicalis

have been reported in Pelecaniformes and a few other species from other

orders (Groebbels, 1932:62-64; King, 1966:211) probably including Leptoptilos

(Akester, et al., 1973).

(81) Saccus clavicularis. Synonymy: thoracic sac (Sappey, 1847; superior-anterior

sac (Campana, 1875); ant. thoracic sac (McLeod and Wagers, 1939). The rival terms

Sacc~s ~lavicularis (Schulze, 1910) and Saccus interclavicularis (Juillet, 1912) have

had slfnilar usage, but the shorter S. clavicularis is preferred.

(82) Pars medialis; Pars lateralis. The Pars medialis and Pars lateralis of the Saccus

clavicularis are the primordial paired medial and lateral components of Locy and

Lars~ll (1916a, b). These four primordial sacs fuse in most species, to form a single

unpaired Saccus clavicularis. In Meleagris the Pars medialis persists as a pair of very

small separate sacs (King and Atherton, 1970) (see also Annot. 77). It has been

claimed that among the Ciconiiformes and Laridae the paired Pars medialis and Pars

lateralis remain separate, giving four separate Sacci claviculares in the adult (King

1966:214). '

(83) Diverticula intrathoracica. The intrathoracic diverticula of the Saccus clavicularis

extend variably around the heart (several Diverticula cardiaca) and along the

sternum (several Diverticula sternalia) (Groebbels, 1932:57, 74-76; King, 1966:

212; Duncker, 1971; King, 1975:1910).

(84) Diverticula extrathoracica. The extrathoracic diverticula of the clavicular sac

spread around the thoracic (pectoral) girdle (Groebbels, 1932:58, 74; King,

1966:212; Duncker, 1971; King, 1975:1911). Groebbels (1932:58) recognized four

main extrathoracic diverticula: Diverticulum subscapulare, between the scapula and

the thoracic cage; Diverticulum axlllare, between the muscles around the shoulder

region, and forming the Diverticulum humerale that invades the humerus in many

species (Osteo. Annot. 188, 189); Diverticulum subpectorale, under the pectoral

muscles; Diverticulum suprahumerale, covering the head of the humerus. Extensive

subcutaneous diverticula have been reported in pelecaniforms, ciconiiforms, and coraciiforms

(King, 1966:213). There is no agreement in the literature about the terminology

for these diverticula; very little is known about species variations, so revision

may be needed later.

(85) Saccus thoracicus cranialis/caudalis. Synonymy: ant./post. diaphragmatic

sacs (Sappey, 1847; Juillet, 1912; Groebbels, 1935); middle-superior, middle-inferior

sacs (Campana, 1875); ant., post. intermediate sacs (Locy and Larsell, 1916a, b);

pre-posrthoracic sacs (Schulze, 1910; Stresemann, 1934); ant., post. thoracic sacs

(Akester, 1960). The thoracic sacs (paired) are essentially intrathoracic. The cranial

sac is typically about one third the volume of the caudal sac, as in passeriforms; in

this group the cranial sac connects with the clavicular (Duncker, 1971). The caudal

thoracic sac is absent in Meleagris (King and Atherton, 1970). The thoracic sacs

typically have no diverticula, but in phalacrocoracids diverticula of the cranial thoracic

sac extend. along the esophagus (Duncker, 1971).

(86) Saccus abdorninalis. Synonymy: inferior sac (Campana, 1875); greater abdominal

sac, McLeod and Wagers, 1939). The abdominal sac typically lies in the

dorsocaudal region of the coelom. In many taxa (e.g., Fratercula) it is the largest sac,

but in others (e.g., the closely related Fulica, and particularly Apteryx and spheniscids)

it is one of the smallest (for reviews see King, 1966:216, and McLelland,

1989:264).

(87) Diverticula perirenalla; Diverticula femoralia. In many birds, the abdominal

sacs give off several perirenal diverticula that extend along the kidneys, invading the

adjacent vertebrae and pelvic girdle. Several femoral diverticula invade the bones and

muscles of the pelvic limb (Groebbels, 1932:59; King, 1966:216; Duncker, 1971;

King, 1975: 1912).

(88) Ossa pneumatica. The air sacs invade the postcranial skeleton in most species,

but the extent is extremely variable between species and even within species. Moreover,

it is difficult to prove that a bone is not pneumatic at all, and errors have

occcurred in the voluminous literature (King, 1966:223). In general the cervical sac

pneumatizes the vertebral ribs, and cervical and thoracic vertebrae; the clavicular sac

aerates the sternum, sternal ribs, thoracic girdle, and wing bones; and the abdominal

sac aerates the pelvis, synsacrum, and bones of the pelvic limb (King, 1966:222). No

bones are pneumatized by the thoracic sacs. The pneumatic bones of the postcranial

skeleton of Gallus have been thoroughly reinvestigated (Hogg, 1984), but the facts for

other species remain uncertain.

(89) Foramen pneurnaticurn; Pori pneumatici. The air sacs invade the skeleton

through either a large pneumatic foramen or small pneumatic pores.