Electronic Journal of Polish Agricultural Universities (EJPAU) founded by all Polish Agriculture Universities presents original papers and review articles relevant to all aspects of agricultural sciences. It is target for persons working both in science and industry,regulatory agencies or teaching in agricultural sector. Covered by IFIS Publishing (Food Science and Technology Abstracts), ELSEVIER Science - Food Science and Technology Program, CAS USA (Chemical Abstracts), CABI Publishing UK and ALPSP (Association of Learned and Professional Society Publisher - full membership). Presented in the Master List of Thomson ISI.
2010
Volume 13
Issue 4
Topic:
Biology
ELECTRONIC
JOURNAL OF
POLISH
AGRICULTURAL
UNIVERSITIES
Pierko M. 2010. STRUCTURAL ANALYSIS OF UPPER RESPIRATORY TRACT IN ANAS PLATYRHYNCHOS (L., 1758) AND CLANGULA HYEMALIS (L., 1758), EJPAU 13(4), #22.
Available Online: http://www.ejpau.media.pl/volume13/issue4/art-22.html

STRUCTURAL ANALYSIS OF UPPER RESPIRATORY TRACT IN ANAS PLATYRHYNCHOS (L., 1758) AND CLANGULA HYEMALIS (L., 1758)

Ma³gorzata Pierko
Department of Zoology, West Pomeranian University of Technology, Szczecin, Poland

 

ABSTRACT

This work aims at the anatomical-comparative description of the upper respiratory tract. The study comprised 212 adult ducks: 62 Anas platyrhynchos (32 males and 30 females) and 143 Clangula hyemalis (102 males and 48 females). Sex and age of the examined birds were assessed. The preparations of the studied organs were preserved in the 4% formaldehyde solution. The morpho-anatomical description comprised the larynx, the trachea, the syrinx, and the fore-fragments of the bronchi primarii. The tracheal cartilages were also counted. A considerable differentiation in the structure and the shape of the syrinx due to the sexual dimorphism was observed in both species. The syrinx in males was significantly well-developed as compared to the females. Both sexes differed in an average number of the tracheal cartilages provided there were more of them in the females. The interspecific comparisons also indicated differences in the syrinx, however solely in the group of the drakes. They mainly regarded a distinct shape of the bulla syringealis and the existence of tracheosyringeal membranes in Clangula hyemalis. A considerably higher average number of tracheal cartilages was indicated in the group of males in Anas platyrhinchos as compared to Clangula hyemalis. A regularity was noted, ie. the bigger and longer bulla syringealis, the shorter trachea containing fewer cartilages. A similar regularity in the group of females results rather from the interspecific differences of the body sizes and the neck lengths.

Key words: larynx, trachea, syrinx, bronchi primarii, Anas platyrhynchos (Mallard), Clangula hyemalis (Long-tailed Duck).

INTRODUCTION

The research on the avian respiratory tract focuses on several main areas, ie. bioacoustics, neuroanatomy, respirational physiology, histology, phylogenetic and morphological-ecological analyses of the relations between the structure of the respiratory tract and the lifestyle, and less frequently on the anatomical-comparative descriptions. Morpho-anatomical studies on the respiratory tract are scarce and usually of a contributory character and their topic constitutes most frequently the domestic fowl and the ornamental birds in captivity. There are considerably few publications on wildfowl and they mainly deal with birds of the order Passeriformes [1, 2, 3, 4, 5, 6, 7, 8, 11, 14, 15, 18, 19, 22, 23, 25, 26, 28, 29, 33, 35, 37, 38, 39, 40, 41, 42, 43, 44, 45, 49, 51, 53, 54, 56, 57, 58, 59, 60, 61, 62, 64, 65]. Morphology and morphometrics of the upper respiratory tract in connection with the disciplines mentioned above constitute a significant contribution to the increase of the taxonomic analyses and phylogenetic relations between various avian species. They are also important for the ecological studies revealing an extreme heterogeneity among birds also in this respect [1, 4, 5, 9, 15, 25, 29, 33, 34, 35, 43, 44, 49, 57, 59, 62, 65].

Flying ability, a faster rate of metabolism, and a wider range of thermoregulation determined the specificity of the structure and the function of the avian respiratory tract. Its efficiency coefficient in the representatives of this animal class is 10 times higher as compared to the mammals. This perfection causes the avian metabolism during a flight, can be even 20 times faster than in the state of repose. Due to such peculiarity of the structure of the respiratory and the blood-vascular systems, the complex mechanisms of respiration, the effective thermoregulation and the metabolic speed,  flying birds can actively fly in the air for a longer time without fatigue, while diving birds can dive for food. The avian respiratory system, evolved by birds, perfectly developed and efficient is mainly responsible for two important biological functions, ie. the very efficient and effective gas exchange (connected with thermoregulation) and the voice production [2, 5, 8, 11, 12, 13, 19, 22, 26, 27, 31, 36, 37, 46, 49, 52, 56, 57].

The avian upper respiratory tract consists of a larynx, a trachea, a syrinx and bronchi primarii. The first three, just mentioned, together with the oral cavity and the bill, form the so called vocal region. High specific variability in their structure results from an individual adaptation of birds to a variety of environmental conditions, different living habits and vocal communication [1, 2, 4, 5, 14, 15, 18, 22, 23, 25, 28, 29, 33, 35, 36, 37, 38, 43, 44, 49, 51, 52, 53, 54, 59, 61, 62, 63, 64, 65]. The avian sounds can be divided into two categories, ie. songs and typical communicative vocalizations. Responsible for the production of those is the syrinx [3, 4, 5, 8, 11, 12, 13, 15, 17, 18, 19, 22, 24, 26, 27, 37, 38, 39, 40, 43, 44, 46, 54, 56, 57, 58]. The remaining organs of the vocal region play an additional, somehow complementary role [5, 7, 12, 13, 14, 19, 22, 26, 27, 31, 37, 46, 48, 51, 53, 57]. There are three types of syrinx, ie. tracheobronchial, tracheal and bronchial. The most frequent in birds is the tracheobronchial syrinx. The syrinx consists of the last tracheal and/or the first bronchi primarii cartilages, and regarding their percentage in the syrinx structure the above classification has been conventionally made. The number of those cartilages varies specifically and dimorphically [2, 11, 37, 35, 38, 40, 44, 59, 62, 64, 65]. The most complex structurally is the syrinx of the singing birds (Passeriformes). This organ is considerably homogeneous within the group and its structural complexity regards mainly its musculature [28, 33, 45, 57, 61, 62]. Anseriformes, not belonging to the singing birds, also have a complex syrinx, yet its structure is not homogeneous and varies specifically. This distinguishes them from others, within that animal class, in a peculiar way. As a rule the Anseriformes have a tracheobronchial syrinx [10, 36, 37, 49]. A number of interspecific modifications exist in the structure and the length of  the trachea, intermediate to the larynx and the syrinx. Moreover, the Anseriformes differ from the remaining avian groups also in a number of cartilages which constitute the trachea and the bronchi primarii, as well as in the length of the trachea [1, 34, 37, 47]. Such organs of the respiratory tract as the larynx, the bronchi primarii, the lungs, and the air sacks, similarly to other birds, apart from the size and weight (which depend on the total body size) do not in general indicate any interspecific differences [36, 37, 49, 52, 63].

This work aims at the intraspecific description and interspecific comparison of the morpho-anatomical structure of the upper respiratory tract organs in the adult birds of both sexes in two palearctic wildfowl species, ie. Anas platyrhynchos and Clangula hyemalis.

MATERIAL AND METHODS

Both species belong to the order Anseriformes, suborder Anseres, family Anatidae, subfamily Anatinae, and two tribes: Anatini (genus AnasAnas platyrhynchos) and Mergini (genus ClangulaClangula hyemalis) – del Hoyo et al. [32].

Anas platyrhynchos occurs in Europe, Asia and Northern America. It is the most numerous breeding duck in Poland, encountered over shallow lakes, ponds, rivers and bogs. Apart from local populations which remain on the inhabited urban areas, the remaining ones, as a migratory species,  leave Poland to winter in the Balkans, Italy and France. They arrive in Poland in February and March and leave between August and December. Anas platyrhynchos hardly plunges and takes flight easily and adroitly. They fly fast with a characteristic flutter. As a rule they feed on the water surface and the bottom of shallows, submerging the head, neck and the fore part of the body (a typical trait of  Anatini). Their food consists of insects and their larvae, mussels and snails, crustaceans, aquatic and land plants, seed, as well as small amphibians, fish, and spawn to a lesser extent [20, 30, 32].

Clangula hyemalis breeds in the tundra of northern Norway and Sweden, on Greenland, Iceland, on the coast and islands of the Arctic Ocean and in the northern confines of Euroasia and North America. The European populations winter on the Baltic, North, and Black Seas. On the Baltic they winter in large flocks from October to April or the beginning of May. In Poland it is a migratory and wintering species belonging to the quantitative dominants among the wintering ducks (observed as the most numerous one on the Pomeranian and Gdañsk Bays). In winter it stays almost exclusively at sea. It flies lightly and deftly, swishing the wings loudly during frequent movements of them. It swims effortlessly and dives well (even to 60 m), can stay underwater even over 3 minutes. During the breeding period it prefers lakes and slow rivers of the tundra, and also fiords and off-shore islands. It mainly feeds on vertebrates during breeding season. During winter migrations it mainly feeds on mollusks and crustaceans, and less on fish, insects and larvae, annelids and sporadically on plant parts, provided it generally feeds at sea [20, 30, 32].

The upper respiratory tract of 212 adult specimens (over one-year-old, sexually mature, which had already bred) were analyzed, including 62 Anas platyrhynchos (32 males and 30 females) and 150 Clangula hyemalis (102 and 48, respectively). The birds were collected in north-western Poland (Western Pomerania). The specimens of Clangula hyemalis were collected in the fall-winter seasons between 1993–2001 from the fishing stations on the western coast of  the Baltic and on the Szczecin Bay. The birds died in the fishing nets in which they had got enmeshed while diving for food. The specimens of Anas platyrhynchos were collected from the hunters, shooting in the vicinity of Szczecin (north-western Poland) between 1997–2001 (September through December).

Taxonomic affinity of the studied birds was assessed on the basis of their appearance and the plumage coloration – ccording to del Hoyo et al. [32]. Afterwards, on the basis of the sexual organs their sex was assessed, according to the description in "Handbook of Avian Anatomy: Nomina Anatomica Avium" edited by King [36]. Due to the size of the bursa Fabricii, which achieves its developmental peak in the immature birds and disappears gradually through the achievement of full sexual maturity, the age was assessed – Siegel-Causey [55]. The preparations of upper respiratory tracts with the fore-fragments of bronchi primarii, according to the methods of Dingerkus & Uhler [21] and Cannell [16], were preserved in the 4% formaldehyde solution. Then they were described morpho-anatomically, including the larynx, the trachea, the syrinx, and the fore-fragments of bronchi primarii. The tracheal cartilages were counted (from the first located just behind the larynx to the last one just before the syrinx, not yet permanently fused with it).

Anatomical Latin names are used according to the obligatory nomenclature provided in the works of King & McLelland [37] and King [36]. The pictures and figures used in the work are the author's original, slightly and technical modeled upon the works of Ames [2] and King & McLelland [37].

RESULTS

The upper respiratory tracts in both sexes of Anas platyrhynchos are shown on Figure 1. The larynx, similar in both sexes of Anas platyrhynchos, of a cordate shape, lies at the bottom of the pharynx, constituting an entrance to the trachea. Its cartilaginous structure, covered with muscles is built of two cricoid cartilages, ie. cartilago cricoidea and cartilago procricoidea and an arytenoid cartilage (cartilago arytenoidea). It also contains a glottis and salivary glands (glandulae mucosae) arranged in rows. The entrance to the larynx leads through a rima laryngis surrounded by the right and left laryngeal labia (labium laryngeum dextrum et sinistrum). The larynx is muscularly joined to two hyoid bones (ossa hyoidea).

In the caudal direction, joined to the back of the larynx is the trachea. The number of tracheal cartilages equaled 127 in males and 130 in females, on an average. They are closed and form rings of various shape, partly overlapping. In the fore-part (closer to the larynx) they are elliptic, whereas on the other end of trachea they become more circular. These cartilages are joined with each other by a membrana interannularis. The trachea of Anas platyrhynchos is a single, straight pipe, muscled laterally, running along the neck. Along its entire length there are musculi tracheolaterales dexter et sinister. At the 4/5 of the trachea length attached are musculi cleidotracheales dexter et sinister, whereas just by the syrinx, musculi strnotracheales dexter et sinister. The fourth tracheal muscle, ie. musculus cleidohyoideus is located in the cranial part, just by the larynx. The caudal fragment of the trachea is joined to the syrinx.

The syrinx of the Anas platyrhynchos male is shown on Figure 2. It is a tracheobronchial syrinx. This organ in females is symmetrical, less complex and considerably smaller than in the males. The syrinx of the drakes consists of the fused last tracheal cartilages and fore- cartilages of bronchus primarius sinister, ie. cartilagenes bronchosyringeales and contains a bulla syringealis (also called a tympanum), which is absent in the females. The last tracheal rings fuse into a thick ring constituting the cranial part of the tympanum. The first rings of the bronchus primarius sinister constitute its caudal part. The number of rings constituting the tympanum in Anas platyrhynchos drakes cannot be assessed precisely as those rings are fused considerably with each other, and the borders between them are atrophic. The bulla syringealis in drakes of this species is exquisitely asymmetrical provided its larger part is always located on the left side what results from a considerable contribution of the fore-part of the bronchus primarius sinister in its structure. The tympanum consists of two chambers: the bigger one in the upper (cranial) part, and the smaller one in the lower (caudal) part.

Intermediate to the syrinx and the lungs are two bronchi primarii (Fig. 1). In both sexes of Anas platyrhynchos the syrinx is joined with the bronchi by a flaccid connective tissue, ie. the membrana tympaniformis lateralis, behind which (on the internal side of the bronchi) there are two elastic formations playing the role of the external vocal folds, ie. labium laterale and labium mediale. Moreover, in the very fore-part of bronchi primarii (in an angle between them, just by the syrinx) there is an osseous trabecula called a pessulus, which enters the inside diameter of the trachea. The pessulus is covered with a membrana semilunaris which passes further into the internal vocal folds (plicae vocales internale). Those folds in turn pass into a membrana tympaniformis medialis which constitutes their internal wall and connects the pessulus with bronchi primarii. The bronchi primarii cartilages, similarly to the tracheal ones, are joined with a membrana interannularis.  By the syrinx, the left and right bronchi are joined by a ligamentum interbronchiale, due to which, intermediate to it and the pessulus there is an elliptic space in the form of an opening foramen interbronchiale

The upper respiratory tracts of both sexes of Clangula hyemalis are presented in Fig. 1. A general scheme of the upper respiratory tract in both sexes of Clangula hyemalis does not differ from the detailed description, presented above for the males and the females of Anas platyrhynchos. The differences in the structure of the upper respiratory tract in Clangula hyemalis regard solely the syrinx and emerge from the sexual dimorphism. The male syrinx is shown in Fig. 3. The Clangula hyemalis drakes have the same type of the syrinx, considerably developed, with a tympanum, slightly bulging on its left side. It is significantly elongated along the cranial-caudal axis. The shape of its first (upper) chamber in the cranial part is exclusively characteristic for this species. In the natural position of the tympanum, on both sides of the first chamber dorsal side (Fig. 3A), and on the entire width on its ventral side (Fig. 3B), visible are the fragments of the last tracheal cartilages (constituting the upper part of the tympanum) not yet completely fused with each other. On the ventral side of the tympanum, the cartilages are narrowed and separated from each other by five (a, b, c, d, e) membrana tracheosyringeales (Fig. 3B) of relatively small area. On the other hand, the second (lower) chamber consists of two membrana tracheosyringeales – the first (g – Fig. 3A i B) bigger, and the second (f – Fig. 3A) smaller. A number of tracheal cartilages in Clangula hyemalis equaled on an average 69 in males and 74 in females.

Fig. 1. The upper birds respiratory tract of both sex of mallard (A) and Long-Tailed Duck (B) – the view of dorsal part (fot. original)
1 – larynx
2 – trachea
3 – syrinx
4 – primary bronchus bronchus primarius
5 – tongue bone ossa hyoidea
6 – musculus tracheolateralis
7 – musculus sternotrachealis
8 – musculus cleidotrachealis
9 – bulla tympaniformis syringealis otherwise called the bulla syringealis

Fig. 2. The male syrinx of Mallard: A – the view of dorsal part, B – the view of ventral
1 – trachea
2 – cartilagines
3 – the greater tympanum ventricle
4 – the smaller tympanum ventricle
5 – right primary bronchus bronchus primarius dexter
6 – left  primary bronchus bronchus primarius sinister
7 – membrana interannularis
8 – ligamentum interbronchiale
9 – foramen interbronchiale
10 – musculus tracheolateralis
11 – musculus sternotrachealis

Fig. 3. The male syrinx of Long-Tailed Duck: A – the view of dorsal part, B – the view of ventral part (ryc. original)
1 – trachea
2 – cartilagines
3 – the greater tympanum ventricle
4 – the smaller tympanum ventricle
5 – right primary bronchus bronchus primarius dexter
6 – left  primary bronchus bronchus primarius sinister
7 – membrana interannularis
8 – ligamentum interbronchiale
9 – musculus tracheolateralis
10 – musculus sternotrachealis
11 – membrana tympaniformis lateralis
12 – membrana tympaniformis medialis
a, b, c, d, e, f – membranes tracheosyringeales

The males of two analyzed species differed in the shape of the bulla syringealis, the existence and a number of tracheosyringeal membranes. In both species the tympanum of the drakes had a bulging on the left side of syrinx, provided this trait was more evident in Anas platyrhynchos. Moreover, in Anas platyrhynchos, along the cranial-caudal axis the syrinx was relatively short in comparison to its counterpart in Clangula hyemalis. In a natural position of the tympanum in Clangula hyemalis drake, on both sides seen from the dorsal side of the first chamber and on the entire width on its ventral side, visible were the fragments of the last tracheal cartilages constituting  the upper part of the tympanum, not yet fused completely with each other. Conversely, in Anas platyrhynchos drakes, those cartilages were almost completely fused with each other in those sites, and their borders almost invisible. Moreover, the tympanum of Clangula hyemalis drake consists of five relatively small and two large membranae tracheosyringeales, whereas the tympanum of Anas platyrhynchos drake was completely devoid of them. The females of both studied species did not differ in either the shape, nor the structure of analyzed organs of the upper respiratory tract. However, in both groups of females and males, the number of tracheal cartilages was considerably higher on an average in Anas platyrhynchos as compared to Clangula hyemalis.

DISCUSSION

In both analyzed species the differences connected with the sexual dimorphism regard mainly the structure and the shape of the syrinx. This determines the dissimilarity of voices produced by the birds of both sexes. The drake's voice has to be most efficient in the competition for the territory and in the wooing females during the breeding season [2, 3, 5, 6, 25, 7, 46, 49, 65]. It should be mentioned, however, that not in all avian species the structure of the syrinx in males considerably differs from that in the females (eg. in Columbiformes). Even an evident sexual dimorphism in the external morphology does not have to be reflected in the structure of this main vocal organ (eg. in Galliformes), what does not have to have repercussion on a poorer stock of sounds produced by the males [2, 3, 5, 6, 8, 11, 25, 37, 38, 46, 59, 60, 65]. The syrinx as an organ can be helpful in the assessment of the avian sex, particularly in the species which seasonally, or generally do not show dimorphic differences in their appearance. The process of the size and shape differentiation of the syrinx is initiated during the embryo stage. It is known to be determined hormonally (the so called masculinization), however, up to now a precise mechanism of it has not been recognized [42, 51, 54, 60, 61]. The parameters describing the syrinx vary, also between specimens and depend on the body size and the weight of particular birds [41, 61]. The description of the structure and the shape of syrinx in Clangula hyemalis drake, done on the basis of the visual examination of the organ as well as the original figures and photographs by the author is probably the first (if not unique) such a precise one, that has been published for this species. There are no similar examples in the available source literature. A few, considerably imprecise, figures done by hand, illustrating the syrinx only in drakes, accompanied by a vague description of its structure have been encountered [37]. Apart from the syrinx, both sexes differed in an average number of the tracheal cartilages; there were slightly more of them in females than males, what might have resulted from the difference of their syrinx sizes.

Indicated in this work, the interspecific differences also concerned the syrinx, provided the drakes of both species differed in the shape of the tympanum and the lack and/or the presence as well as the number of tracheosyringeal membranes. The evident interspecific differences result rather from a distant affinity of both studied species (each belongs to a different tribe of the subfamily Anatinae), and determine the dissimilarity of the voices produced by them. According to other analyses of the size and the shape of the syrinx, provided by other authors; together with the membranes constituting it, those traits significantly affect the increase of vocal abilities [3, 4, 5, 6, 8, 10, 11, 15, 17, 18, 19, 20, 22, 26, 27, 31, 37, 38, 39, 41, 42, 43, 44, 46, 54, 57, 58, 59, 61, 62, 64]. This is fully justifiable, as in this case Clangula hyemalis drakes produce a different voice as compared to the drakes of Anas platyrhynchos. The latter produce a low, harsh, muffled "khre khre khre", and a short whistle "fij" during the breeding period. On the other hand, the former produce distinct, rhythmic calls "au au aulik aulik" [20, 32]. It should be mentioned that the typical "quacking", commonly identified with the ducks, are produced by the females of Anas platyrhynchos. They are loud, spread on a broad-tone "quaack quaack", provided similar sounds are produced by a domestic form of Anas platyrhynchos, ie. Peking duck Anas platyrhynchos forma domestica [10, 20, 32].

The differences in the structure and the shape of the syrinx in males of certain species of the subfamily Anatinae have been described earlier, ie. Warner [63] regarding Anas platyrhynchos and certain selected species of Aythyini, Pierko [49] comparing Anas platyrchynchos with Aythya marila, and Biellier & Turner [10] comparing the dimorphism in males and females of Peking ducks. A few other analyses of this type in the males of Non-Passiformes were conducted in Gallus domesticus [3, 44], the representatives of Corvidae [18], Struthionidae [65], Columbiformes [64] and Falconiformes [29, 35]. These works assessed a degree of affinity between the studied species and the characteristics of phylogenetic relations between them. As certain taxonomists claim, the interspecific differences in the structure and the shape of the avian syrinx are significant taxonomically, because they not only characterize close and distant affinities, but also allow to isolate new populations within the species already determined [3, 6, 9, 15, 18, 23, 29, 33, 37, 41, 43, 44, 46, 59, 62, 64]. The pioneer in the syrinx anatomy, who classified various species of birds upon that, was a German anatomist Müller [45], who, similarly to his followers [2, 62] limited his research exclusively to Passeriformes. Another scientist, Beddard [9] extended his research also on other species. Nowadays however, when the possibility of genetic analyses is widespread [33], the morpho-anatomical comparisons of the avian respiratory tract have been considerably limited. Such research, however, should be continued, as a majority of species, particularly Non-Passeriformes, have not yet been described on that score [35, 37, 49]. Such analyses can be applied in numerous fields, eg. ecological studies, regarding the monitoring of population alterations connected with the migrations, the habitat changes and the expansion of species. Moreover, they can be helpful in the creation and/or the verification of the existing avian vocal models, which still remain controversial [4, 5, 6, 8, 12, 13, 14, 17, 19, 22, 24, 25, 27, 31, 35, 37, 39, 48, 50, 51, 53, 56, 58, 65].

As already stated, the males of both examined duck species have a tracheobronchial syrinx, consisting of a tympanum. Generally, apart from certain more detailed modifications, this is a typical trait of the Anseriformes. In certain species, the representatives of this order, the tympanum exists on both sides of the syrinx, as in eg. Tadorna tadorna (subfamily Anatinae, tribe Tadornini), however it is clearly asymmetrical and bigger on the right side. The bilateral asymmetry of the tympanum is most frequently encountered in the species of the subfamily Anatinae. Among the Anseriformes the bilaterally asymmetrical tympanum exists in Dendrocygnini (subfamily Anserinae), while in a few species of this avian group, the tympanum does not exist at all [10, 34, 37, 40, 54, 63]. This work indicates that the left side of the bulla syringealis in the males of both examined species was larger in relation to the right one. As other authors claim, that it is the left half of syrinx that is considerably larger and participates more in the voice production. Similarly to the muscles located on this side, which are responsible for the activity of the syrinx [3, 4, 6, 10, 11, 15, 26, 28, 37, 39, 40, 47, 48, 49, 50, 54, 56, 60, 65]. Both halves of the syrinx can at a given moment act simultaneously, and/or independently from each other, provided each half can produce the same sound, or both halves can generate a separate, sometimes a considerably distinct sound [4, 8, 10, 17, 22, 24, 26, 27, 31, 39, 46, 56].  This is particularly important for the birds nesting in flocks, helping them in a difficult mutual identity between parents themselves as well as between parents and chicks [4, 25, 28, 46, 56].

Apart from syrinx, the production and the emission of voice and its quality are also affected by nasal cavities, oral cavity and esophagus, larynx, trachea, bronchi, lungs and air sacks [7, 8, 19, 22, 25, 26, 27, 31, 34, 37, 46, 49, 51, 53, 57]. Beckers et al. [7] even concluded that the skill of mimicking human voice by parrots (order Psittaciformes, family Psittacidae, subfamily Psittacinae) is possible due to the adjustments enabling the tongue movements during the voice emission. This, however, is a peculiar trait exclusive for parrots, and probably also for Gracula religiosa (order Passeriformes, family Sturnidae), as generally the avian tongue is relatively stiff, what considerably limits its movements. It has also been indicated that in birds, quite significant is a change of the beak opening width and occasional movements of the head during the voice emission, what affects the size change of their vocal region. Nowadays it is assumed that the vocal region is responsible for the modulation intensity of the voice generated in the syrinx, yet the precise mechanism of the activity of the particular organs responsible for that has not been accurately recognized [4, 8, 12, 13, 14, 19, 22, 25, 26, 27, 28, 31, 34, 37, 46, 48, 50, 51, 53, 57]. Apart from the upper respiratory organs, the avian respiratory tract also includes the lungs (pulmones) and, exclusively for this class of animals, typical air sacks (sacci pneumatici). The tubular lungs of birds, besides the gas exchange, supply the air, causing its flow through the remaining organs. The role of air sacks in the emission of voice in birds has been least recognized [8, 26, 37, 46, 57].

The structure of the larynx is typical, uniform in all avian groups, therefore the lack of differences in its structure, observed in this work is justified. More modifications and interspecific differences are found in the structure of the trachea, located just behind it [1, 19, 34, 35, 36, 37, 47, 49, 50]. A higher average number of tracheal cartilages in Anas platyrchynchos in comparison to Clangula hyemalis, in the group of males results from the differences in the shape and the size (length) of their bulla syringealis. The following regularity occurred, ie. the larger and longer bulla syringealis, the shorter trachea with fewer cartilages. However, a similar regularity, observed in the female group of both species is striking. It could not have been affected by the bulla syringealis because the syrinx structure in this sex is considerably simple. This might rather result from the differences in the body size (Anas platyrhynchos is significantly larger than Clangula hyemalis, which belongs to the smallest species of ducks) and, most of all, in the length of the neck. The number of tracheal cartilages in birds depends on the length of the neck and amounts to about 30 in the small Passeriformes to about 350 in flamingos and cranes [37]. This work is devoid of histological analyses, however, it is evident from the available source literature, that the tracheal cartilages in the Anseriformes are built of the osseous tissue, while in other birds they are cartilaginous or hardly ossified [34,36,37,52,63]. The species, even quite closely affiliated with each other, within the Anseriformes can differ considerably in the number of cartilages in the trachea and the bronchi primarii as well as in the presence of the bulbus trachealis [36, 37, 47, 49, 52, 63], unobserved in both species, analyzed in this work. Usually there is only one dilatation, as in eg. Anas versicolor and Anas hottentota (tribe Anatini), Bucephala islandica and Mergus cucullatus (tribe Mergini), or Netta peposca (tribe Aythyini) [34, 37]. At times there are two such dilatations, as in certain representatives of the subfamily Anatinae, eg. Mergus merganser and Melanitta fusca (tribe Mergini), Netta rufina (tribe Aythyini), and/or Stictonetta naevosa (subfamily Anserinae, tribe Stictonettini) [37, 47, 49]. The trachea can also be quite long and form loops in the vicinity of the sternum, as in eg. Anseranas semipalmata (subfamily Anseranatinae), or Cygnus cygnus (subfamily Anserinae, tribe Anserini). Such a long trachea is also found in other species not belonging to the Anseriformes, eg. in Grus grus (order Gruiformes, family Gruidae). As has been mentioned earlier, the trachea acts generally as a resonator for the sound generated by the syrinx [37,53]. The increased length of the trachea allows for the amplification of the produced sound, due to which it becomes so loud to be heard at a distance of one kilometer and further. However, similarly to both of the species examined in this work, in the majority of the representatives of the class Aves, it has the shape of a straight pipe [1, 23, 34, 35, 36, 37, 49, 52]. There are also quite peculiar traits in the tracheal structure, eg. its juncture with the cervical air sacks by an elongated slit, as in Australian emu (order Casuariformes, family Dromaiidae); or its doubling along the entire length into two joint pipes (visible only in cross section), as in penguins (order Sphenisciformes, family Spheniscidae) and petrels (order Procellariiformes, family Procellariidae) [37]. As certain authors claim, the traits assessing the trachea size, such as length, number of cartilages, diameter of the cartilages, and the existence of bulbus trachealis in certain birds mentioned above, affect not only the quality of the produced voice, but also the breathing capacity [23, 36, 37, 43, 63]. The breathing capacity is closely related to the conducted lifestyle, and mainly to the feeding habits as well as the predispositions to flying and diving. Therefore the structure and the activity of the avian respiratory system affect the general abilities of the organism physical efficiency [37]. The feeding habits of both  analyzed species differ. Considerably less effort is put in it by Anas platyrhynchos, which dives quite shallow. Clangula hyemalis on the other hand dives down to 70 m and sometimes even deeper. Moreover, the latter flies over enormous distances during breeding seasons. Whereas such flights of Anas platyrhynchos are considerably shorter, while certain populations of this species do not migrate at all and winter at the very site of breeding; this particularly regards the specimens of the urban populations [20, 32]. The respiratory system of Clangula hyemalis, as a species considerably more active and forced to a greater physical effort as compared to Anas platyrhynchos, has to be distinguished by a more efficient lung ventilation and a higher breathing frequency.

The interspecific differences, indicated in this work, regarding the structure and the size of the syrinx in the male group, and the number of tracheal cartilages in birds of both sexes  suggest the usefulness of both organs for that type of comparisons. Since the females of both analyzed species did not differ in either the shape nor the structure of the remaining organs of their upper respiratory tract, the relations referring to their close affinity are hard to be sought. It means that such comparisons in the females can be less useful for this type of scientific analyses. It should be mentioned that the available source literature does not provide similar comparisons conducted in the females [49].

CONCLUSIONS

During the intraspecific comparisons in both analyzed species of ducks, a considerable differentiation was assessed in the structure and the shape of the syrinx, due to the sexual dimorphism. This organ can be quite useful for the assessment of sex in birds, particularly in the case of the species which do not show dimorphic differences in their appearance either seasonally nor in general. The only drawback of it, is the necessity to kill birds, because the recognition of sex due to the visual aspect and the size of the syrinx can only be done by autopsy. Apart from the syrinx, both sexes differed in an average number of the tracheal cartilages, ie. there were more of them in the females in comparison to the males, what was affected by the syrinx size.

The interspecific comparisons, conducted separately in the males and the females, indicated differences also in the case of the syrinx, however solely in the group of drakes. Those differences regarded mainly a dissimilar shape of the bulla syringealis and the presence of tracheosyringeal membranes in Clangula hyemalis drakes, absent in Anas ptlatyrhynchos drakes. The interspecific variability, assessed in this work, regarding the structure and the shape of the syrinx in drakes, indicates the helpfulness of this organ for the phylogenetic relationships between various species and populations, as well as for the taxonomy and the ecological studies to a certain extent.

A significantly higher average number of the tracheal cartilages in the group of males was indicated in Anas platyrhynchos as compared to Clangula hyemalis, what, in this sex, was affected by the differences in the shape and the size of the bulla syringealis. The following regularity occurred, ie. the larger and longer bulla syringealis, the shorter trachea with fewer cartilages. A similar regularity in the group of females of both species results rather from the differences of the body size and the length of neck (in favor of the bigger Anas platyrhynchos), because the female syrinx is not so well-developed.

As the females of Clangula hyemalis and Anas platyrhynchos, besides the number of the tracheal cartilages did not differ in either the shape nor the structure of the remaining organs constituting the upper respiratory tract, the comparisons in this sex seem to be hardly useful for this type of scientific analyses.

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Accepted for print: 17.11.2010


Ma³gorzata Pierko
Department of Zoology,
West Pomeranian University of Technology, Szczecin, Poland
Doktora Judyma 20, 71-466 Szczecin, Poland
Phone: 091 449 67 30
email: malgorzata.pierko@zut.edu.pl

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