MORPHOLOGICAL COMPARISON OF UPPER RESPIRATORY TRACT IN MALLARD ANAS PLATYRHYNCHOS AND SCAUP AYTHYA MARILA

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

ABSTRACT

The investigations comprised the upper respiratory tract in 100 adult ducks: 57 mallard Anas platyrhynchos (30 males and 27 females) and 43 scaup Aythya marila (26 males and 17 females). The work aimed at the anatomical comparison of the organs constituting the upper respiratory tract. Had the sex and age of the investigated birds been determined, the specimens of the upper respiratory tract, preserved in 4% formaldehyde solution, were described morphoanatomically including the larynx, trachea, syrinx and bronchi primarii. The interspecific comparisons of males and females of both species indicated a considerable divergence in the shape, size and structure of the syrinx. They refer, among others, to an extensive membrane, a constituent of the syrinx tympanum in the drakes of scaup which was absent in mallard.

Key words: mallard (Anas platyrhynchos), scaup (Aythya marila), larynx, trachea, syrinx, bronchi primarii.

INTRODUCTION

The upper respiratory tract in Aves consists of the larynx, trachea, syrinx and bronchi primarii. A considerable interspecific variability in the structure of these organs results from the adaptability of the individual species to various natural conditions as well as the distinct life habits and vocal communication. [1,2,4,5,7,14,15,16,22,23,35,36,42,].

The investigations of the respiratory tract concentrate on several aspects, ie. bioacoustics, neuroanatomy, respiratory physiology, histology, morphological-ecological analysis of the relation of the respiratory tract structure to the life habits, and rarely on the anatomical-comparative descriptions. Among the morphoanatomical investigations of birds, a certain attention is devoted to the studies on the respiratory tract, however they are rare and contributory in character. They mainly consider poultry and ornamental birds kept in captivity. There are rare publications on wild species and they mainly concern the Passeriformes [1,2,3,4,5,6,7,8,10,13,14,15,16,18,23,25,29,35,36,39,40,41,43].

Morphoanatomy of the upper respiratory tract in connection with other analyses (eg. bioacoustic, neuroanatomical, morphometric, or histological) can contribute, among others, to the precision of taxonomic analyses, the determination of the phylogenetic associations between various species of birds, as well as in the ecological studies to reveal an enormous variety of birds also in this respect [16,18,32,].

The goal of this work was the intraspecific description as well as the interspecific comparison of the morphological structure of the upper respiratory tract of adult birds of both sexes of two holoarctic species of wild ducks, ie. the mallard Anas platyrhynchos, and the scaup Aythya marila. Both investigated species belong to the order Anseriformes, suborder: Anseres, family: Anatidae, subfamily: Anatinae, and two tribes: Anatini (dabbling ducks), genus: Anas, species: Anas platyrhynchos (mallard) and Aythyini (pochards), genus: Aythya, species Aythya marila (greater scaup) – del Hoyo et al. [19].

Anas platyrhynchos inhabits the entire territory of Europe, Asia and North America. In Poland it is a predominant breeding duck encountered over shallow lakes, ponds, rivers and marshlands. It is also a migratory species, solely local urban populations remain on the habitat throughout a year, others migrate to their winter quarters south and southwest (Balkans and/or Italy and France). They fly back to Poland in February and March, whereas leave between August and December. Anas platyrhynchos slightly plunge in water and take off fast and dexterously. They fly fast with a characteristic flutter. They usually feed on the water surface and/or the bottom of shallows, submersing the head, neck and the front part of their bodies (characteristic of the Anatini). Their diet varies, including insects and their larvae, mollusks and snails, crustaceans, aquatic and terrestrial vegetation, seeds and occasionally small amphibians and fish, as well as their spawn [11,17,19,28,38].

Aythya marila migrates through Poland (south, September through November and north, March through May). It is numerous at the seacoast and sporadic on the distant offshore lakes. Its breeding biotope includes lakes and marshlands of tundra and taiga of Eurasia (Scotland, Scandinavia, Iceland and North Asia) and North America. It winters mainly on shallow coast waters and shielded bays of Europe and Southern Asia. It is a diving duck. It looks heavy and ponderous (both on water and in air). In the case of danger, contrary to Anas platyrhynchos, it prefers to dive, even to the depth of 30 m., whereas while feeding – to the depth of three to five meters, slightly deeper, occasionally. This duck feeds on plants and animals in various quantities subject to the season. Its fodder during the breeding season consists mainly of mollusks and crustaceans, insects, small fish in smaller quantities and vegetative parts of aquatic plants, their roots and seeds. Beyond the breeding season, however, it feeds on mollusks and crustaceans, rarely small fish and annelids as well as plants [11,17,19,27,38].

MATERIAL AND METHODS

The investigations comprised the upper respiratory tract of 100 adult ducks (over one-year-old, sexually mature, which have already bred): 57 Anas platyrhynchos (30 males and 27 females) and 43 Aythya marila (26 males and 17 females).

All the investigated birds were collected in north-western Poland (Western Pomerania). The Aythya marila specimens came from the fishermen’s bases along the Baltic coast (Międzywodzie, Dziwnów and Wisełka) and two bases on the Szczecin Bay (Stepnica and Wolin). Aythya marila were collected during fall-winter seasons between 1993-1998. The birds died in the fishing nets into which they got while diving for fodder. Anas platyrhynchos were the trophies of huntsmen from between 1997-1999, September-December, Szczecin surroundings.

The taxonomy of the investigated birds was determined (on the basis of their outward appearance and the color of feathers according to del Hoyo et al. [19]), their sex (selectively, on the presence of sex organs, according to the Handbook of Avian Anatomy: Nomina Anatomica Avium ed. By King [22]), and the age (on the basis of the appearance of the tertiary flight feathers, the wing coverts, and the size of bursa Fabricii). The development of bursa Fabricii achieves its peak in the adolescent specimens and gradually wanes towards the achievement of the sexual maturity [24,37].

The upper respiratory tracts prepared with the adjoining upper primary bronchi were preserved in 4% formaldehyde solution due to the method by Dingerkus & Uhler [12] and Cannell [9]. Then they were cleared of the fat tissue and external membranes tunices adventities and described morphoanatomically concerning the larynx, trachea, syrinx, and the first parts of primary bronchi.

The Latin anatomical terminology was due to King & McLelland [23] and King [22]. All figures (photographs and pictures) in this article are author’s originally, in a small degree imitated by Ames [2] and King and McLelland [23].

RESULTS

The upper respiratory tracts in mallard of both sexes are presented on the Fig. 1. The larynx in both sexes is similar, cardiac-like, located at the bottom of the pharynx forming the entrance to the trachea. It is built of a cartilaginous structure covered with muscles and consists of the glottis and glandulae mucosae arranged in rows. The larynx consists of two cricoid cartilages, ie. cartilago cricoidea and cartilage procricoidea as well as the cartilago arytenoidea. The entrance to the larynx leads through the rima laryngis surrounded by two labia, ie. labium laryngeum dextrum and labium laryngeum sinistrum. The larynx is linked muscularly with two hyoid bones ossa hyoidea.

The larynx caudally and directly opens to the trachea. The tracheal cartilages in mallard are closed rings partially overlapping each other. Their shape varies. Closer to the larynx they are elliptic whereas caudally – almost circular. These cartilages are linked with the membrana interannularis. The trachea is a straight singular tube extending along the neck. It hasn’t bends loops in the region of the sternum and bulbus tracheales, characteristic for certain species of ducks [22,23]. Both sides of the trachea are covered with muscles, ie. right and left musculi tracheolaterales (dexter et sinister). Close to the end of the trachea (4/5 of its length) there are right and left musculi cleidotracheales (dexter et sinister). At the very rear end of the trachea, by the syrinx there are right and left musculi sternotracheales (dexter et sinister). The trachea is moreover covered with the fourth muscle, ie. musculi cleidohyoideus which is located in the upper part of the trachea, by the larynx. The rear part of the trachea opens to the syrinx in both sexes. The syrinx of mallard male is presented on the Fig. 3 and 4.

The mallard have a tracheobronchial syrinx. In females this organ is symmetrical, of no complex structure, and considerably smaller than in males. In drakes the syrinx consists of the accreted finally cartilagines tracheales and first cartilages of the left primary bronchus (bronchus primarius sinister), so called cartilagines bronchosyringeales and contains bulla syringealis (also called the tympanum), nonexistent in females. The final rings of trachea accrete in a thick ring forming a superior part of the tympanum, whereas the first rings of the left bronchus form its caudal part. The exact number of the rings forming the tympanum is hard to determine due to their considerable accretion and the not sharp contours. The tympanum of the syrinx in males is visibly asymmetric, and his larger part is on your left side of the syrinx, which results from the considerable contribution of the first portion of the left bronchus in its structure. In drakes the tympanum consists of two chambers (Fig. 1,3,4): the larger one in the superior part (headlly) and the smaller one in the inferior part (caudally).

The syrinx ramifies into two bronchi primarii which open to the lungs. In both sexes of mallard the tympanum of the syrinx is linked with the bronchi by means of a limp connective tissue, ie. membrana tympaniformis lateralis. Behind this membrane there are two elastic formations located on the internal side of the bronchi performing the role of the external vocal fold, ie. labium laterale and labium mediale. Furthermore, at the first part of the bronchi, in an angle between them, by the syrinx, there is a bony trabecula, called pessulus, which enters the trachea. The pessulus is covered with membrana semilunaris, which transforms into plicae vocales internae. These folds transform into membrana tympaniformis medialis, which links the pessulus with the bronchi simultaneously forming their internal wall. The bronchial cartilages, similarly to the tracheal cartilages, are linked by the membrana interannularis. Close to the syrinx the right and left bronchi are linked by a ligamentum interbronchiale forming a foramen interbronchiale, a slit between the pessulus and this ligament. This slit is elliptical in both sexes of mallard.

The general structure of the upper respiratory tract in both sexes of scaup does not considerably differ from the above description for males and females of mallard. The upper respiratory tract in both sexes of scaup is presented on the Fig. 2. In both species the discrepancy in the structure of the upper respiratory tract emerge from the sexual dimorphism and concern solely the structure of the syrinx. The syrinx of the male of scaup is presented on Fig. 5 and 6. Also tracheobronchial, it is significantly developed and contains the tympanum which is missing in the females. The tympanum has a developed upper chamber with a large tracheosyringeal membrane membrana tracheosyringealis. The shape of the tympanum is characteristic. In its natural position, on the right of its dorsal side and the middle of the ventral side there are clearly visible fragments of the final tracheal cartilages forming the tympanum which did not accrete completely.

The males of both investigated species differ, above all, in the shape of the tympanum and the presence of the tracheosyringeal membrane in the males of scaup which constitute a part of the first (upper) chamber of the tympanum. In the males of mallard the tympanum is devoid of membranes. Moreover, the tympana in both species are characterized by a considerable protrusion of the wall on the superior (head) left side provided, it is greater in the males of mallard. The syrinx in the males of both species along the cranio-caudal axis is considerably short. In the males of scaup in the natural position of the tympanum on the right of the dorsal side and the middle of the ventral side there are visible fragments of the final tracheal cartilages which did not accrete completely. Whereas in the males of mallard these cartilages are accreted completely and their contours are hardly visible.

The females of both investigated species do not differ in the shape and structure of any of the analyzed organs of the upper respiratory tract, ie. larynx, trachea, syrinx and primary bronchi.

DISCUSSION

Sexual dimorphism concerning the structure and shape of the syrinx in both analyzed species determine the variety of the voices evoked by the males and the females. The most distinctive discrepancy in the structure and shape of the syrinx subject to the sexual dimorphism is observed in the Passeriformes and certain Anseriformes [2,23]. This trait allows for the effectiveness of the voice in males, eg. in competing for the territory and luring the females during the mating season. The males of the individual species produce distinct sounds of recurrently long and complicated song which is particularly characteristic for the Passeriformes [2,14,23,31]. Noteworthy is the fact that not in all species the structure of the syrinx in males and females differs considerably which does not often indicate a less inconspicuous stock of sounds in the latter, however, the studies on such comparisons are sporadic [2,3,6,22,23,39,40]. Such a distinct description of the structure and shape of the syrinx of the scaup drake based on the visual examination of the organ and the original illustrations by the author is probably the first published for this species as no such examples have been encountered in the available source literature.

The males of two investigated species differ in the shape and the structure of bulla syringealis constituting a part of the drake’s syrinx. The observed interspecific discrepancies may result from a remote affinity between both species (each belongs to a separate tribe of the subfamily Anatinae) and be also associated with the distinct voices evoked by them [11,23]. The discrepancies in the structure and shape of the syrinx in males of certain species of the subfamily Anatinae were earlier described by Warner (1971) depicting mallard and the selected species of the Aythyini (excluding scaup). Other, rare analyses of differences and similarities in the structure and shape of the syrinx in males of the Non-Passeriformes were conducted, among others, in the males of Gallus domesticus [30], representatives of the Corvidae (Chamberlain et al. 1968), the Columbiae [43] and the Falconiformes [16]. On the basis of the discrepancies in the morphological structure of the syrinx those works aimed at the genetic affinity between the investigated species and the characteristics of the phylogenetic associations among them. Due to certain taxonomists the discrepancies in the structure and shape of the syrinx in birds are very important taxonomically as they characterize not only the interspecific affinities but also allow for the isolation of new populations within a given species which may tend towards the assignation of a new subspecies [3,8,10,16,23,25,29,30,31,32,35,41,43]. Such detailed taxonomic specifications are very crucial in a number of fields, such as, the monitoring of population changes, especially the unfavorable ones, and/or the analyses aiming at the isolation of the sources of the environmental pollution and the estimation of its scope.

The males of two investigated species have a tracheobronchial syrinx containing a tympanum which is a characteristic trait of the Anseriformes. In certain species of this order the tympanum occurs on both sides of the syrinx, eg. in Tadorna tadorna (subfamily Anatinae, tribe Tadornini), however, it is evidently asymmetric and larger on the right side. In the species of the subfamily Anatinae the most frequent is the bilateral asymmetry of the tympanum. Among the Anseriformes the bilaterally symmetric tympanum is present in the Dendrocygnini (subfamily Anserinae), whereas it is totally absent in an inconsiderable percentage of species [21,23,42].

The females of both investigated species do not differ in the shape nor structure of the organs constituting the upper respiratory tract. Therefore no interdependencies due to a close affinity between them are possible to establish. It is evident that such comparisons in this sex can be less useful for the investigations of the affinity. Noteworthy is the fact that the available source literature does not provide such comparisons in females.

The larynx has always a typical uniform structure in all groups of birds [22,23], therefore an evident lack of interspecific and sexual dimorphism in its structure observed in this work is substantiated. More modifications and interspecific discrepancies are found in the structure of the trachea. The tracheal cartilages in the Anseriformes are built of an osseous tissue whereas in other birds they are cartilaginous and/or only partly ossified [22,23,26,34,42]. The species of the Anseriformes, even closely allied, can differ in a number of the tracheal and primary bronchial cartilages and also the presence of the so called bulbus trachealis [20,22,23,33,34,42], unobserved in both investigated species. Usually there is only one bulbus, as in eg. Anas versicolor and Anas hottentota (tribe Anatini), Bucephala islandica and Mergus cucullatus (tribe Mergini), or Netta peposca of the tribe Aythyini [21,23]. Occasionally there are two bulbiculi, as in certain specimens of the subfamily Anatinae, ie. Mergus merganser and Melanitta fusca (tribe Mergini), Netta rifina (tribe Aythyini), or Stictonetta naevosa of the subfamily Anserinae, tribe Stictonettini [23,33]. The trachea can be very long and form in the Anseriformes certain loops in the vicinity of the sternum, as in eg. Anseranas semipalmata (subfamily Anseranatinae) or Cygnus cygnus (subfamily Anserinae, tribe Anserini). However, similarly to both of the investigated species, in the majority of the specimens of the phylum Aves the trachea has the shape of a straight tube [1,13,20,22,23,34]. Certain authors openly claim that the size characteristics of the trachea, eg. length, number and diameter of the cartilages of which it is built as well as the presence of bulbiculi in certain species effect the effectiveness of breathing and partly the quality of the evoked voice [13,22,23,29,42]. The breath effectiveness is related to the distinct mode of life and predominantly to the feeding habits and the predisposition towards flying or diving of the individual species. Both of the investigated species differ in the feeding habits, as the less effort into this activity is put by mallard (the ancestor of our domesticated duck Anas domestica v. pekin), the scaup dives for fodder even to a considerable depth (30 m). Besides, scaup flies over significantly longer distances during the seasonal migrations than mallard [11,19,27,38]. The lack of visible discrepancies in the structure of trachea in both investigated species leads to the conclusion that the most helpful for the interspecific comparisons of the morphological structure of the organs constituting the upper respiratory tract is the syrinx in the males.

CONCLUSIONS

The intraspecific comparisons between mallard and scaup indicate a considerable discrepancy in the structure and shape of the syrinx connected with the sexual dimorphism.

The interspecific comparisons, conducted separately in males and females, indicate discrepancies in the structure and shape of the syrinx in drakes. In males these discrepancies referred mainly to the distinct shape of the syrinx tympanum in both species, and the presence of membrana tracheosyringealis (constituent of the tympanum) in the males of scaup which was absent in the males of mallard.

The observed interspecific mutability concerning the structure and shape of the syrinx in drakes may be useful for the analyses of the phylogenetic associations between various species and populations, and also for the taxonomy.

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Accepted for print: 17.10.2007

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