Microscopy: advances in scientific research and education (A. Méndez-Vilas, Ed.)
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1 Scanning electron microscopy investigation of the filter-feeding apparatus in the domestic goose (Anser anser f. domestica) and the domestic duck (Anas platyrhynchos f. domestica) K. Skieresz-Szewczyk and H. Jackowiak Department of Histology and Embryology, Faculty of Animal Breeding and Biology, Poznan University of Life Sciences, Wojska Polskiego 71C, Poznan, Poland Behavioral observations carried out in the Anseriformes in the laboratory environment by Van der Leeuw et al. [19] demonstrated three types of food intake, called grazing, pecking and filter-feeding. It is assumed that the geese are more adapted to the terrestrial style of life than to the aquatic one [17, 18]. Due to the fact of living predominantly on land, these birds, unlike ducks, are considered to be nonspecialist filter feeders [19]. The aim of the study is to compare microstructure of the filter-feeding apparatus in the domestic goose and in the domestic duck by using scanning electron microscopy. The filter-feeding apparatus in both species of Anseriformes is located on the lateral sides of the lingual body and is composed by large and small conical papillae of the body and filiform papillae. In the domestic goose in the rostral part of the lingual body are observed 11 pairs of small conical papillae and in the caudal part of the body are 4 pairs of large conical papillae. The processes of small conical papillae are directed sideways and slightly backwards. The processes of large conical papillae are pointed to the back of the tongue. The last large conical papilla was composed of two parts that differ in size: a larger lateral part and a smaller median part. Among the conical papillae of the body are arranged filiform papillae. In the domestic duck there are 14 pairs of small conical papillae and 6 pairs of the large conical papillae. The small conical papillae have shape of flattened plates which tips are frayed and arranged to the ventral side of the tongue. The large conical papillae are slightly flattened processes, which caudal surface has invagination and the rostral surface elongates into the lamina. Two others large conical papillae are in the form of frayed processes. The filiform papillae in the caudal part of the body are located, like in goose, between large conical papillae. In the rostral part of the lingual body, the location of the filiform papillae is completely different. The structure and arrangement of the filter-feeding apparatus in the domestic goose and duck is varied and speciesspecific, and indicate that the domestic ducks is adapted to life in the aquatic environment, and goose to live in the terrestrial environment. At the same time, the goose is still adapting to collect food from water and duck cutting grass on land. Keywords: SEM; tongue; birds; filtering-apparatus 1. Introduction Behavioral observations of food intake in birds showed that the structure of the beak and tongue are specialized organs for collecting, processing and transport of food into the esophagus [4, 14, 15, 19, 20]. The main factors influencing the wide diversity of morphological construction of tongue in birds are kind of food and method of food collection. Harrison in 1964 [5] distinguished three groups of tongues with special structural adaptations depending on their functions. The first group is tongues used to capture and food intake, which have strongly developed hyoid apparatus [1, 2, 3]. The second functional group is tongues adapted for crushing and manipulating of food with numerous stiff papillae on the dorsal surface [6, 7, 9, 10, 13]. The third group includes tongues that are used for holding food in the oral cavity before the stage of swallowing [8, 16]. This division, however, does not take into account morphological specialization created in response to the complex function of food intake, an example of which are birds of the family Anseriformes. In this group of birds, tongue and beak are involved in the three ways of getting food: pecking, grazing and filter-feeding [4, 14, 15, 19]. It should be noted that among Anseriformes, birds of the subfamily Anatidae exhibit a greater variety of food than birds belonging to the subfamily Anserinae. Among Anatidae are species feeding on green plants and seeds, as well as species specialized in the filtration of small aquatic organisms as shoveler (Anas clypeata), followed by species that feed on crustaceans and mollusks, as common pochard (Aythya ferina) or fish, as common merganser (Mergus merganser) and species whose main source of food are saltwater mollusks, an example of which is the shelduck (Tadorna Tadorna). In the subfamily Anserinae, which include e.g. bean goose and swan, diet consists mainly of vegetative parts of plants. On the basis of these differences, it is assumed that geese are more terrestrial birds than aquatic one [12, 19, 4]. Due to the fact of living predominantly on land, these birds, unlike ducks, are considered to be nonspecialist filter feeders [20]. 84
2 Diet of birds living in the breeding is somewhat limited and consists primarily of pre-cut forage, oat meal, wheat bran. During the autumn and winter they feed on carrots, steamed potatoes, fodder beets and sugar beets. Ducks having access to natural water also feed on aquatic plants and small invertebrates [12]. The aim of the study is to conduct comparative analysis of the microstructure of the filter-feeding apparatus in the domestic goose and duck by using scanning electron microscopy. 2. Material and methods The study was conducted using two tongues of adult females (9-month-old, average weight 5.5 kg) of the domestic goose and duck, collected from the local slaughterhouse. Immediately after dissection, the tongues were fixed in 10% formalin and then documented with a digital camera. For observations under the scanning electron microscope (SEM), the samples were dehydrated in a series of ethanol (70 100%) and acetone (96%-abs.), and subsequently dried at critical point using CO2 (Critical Point Dryer K850, Emitech). All specimens were mounted on aluminums stubs covered with carbon tabs, sputtered with gold (Sputter Coater S 150B, Edwards) and observed under the LEO 435 VP (Zeiss) at an accelerating voltage of kv. 3. Results The filter-feeding apparatus in the domestic goose and duck is located on the lateral side of the lingual body and is built of small and large conical papillae of the body and filiform papillae. The small conical papillae are in the rostral part of the body and large conical papillae are in the caudal part of the body. On the tongue in the domestic goose are present 11 pairs of small conical papillae and 4 pairs of large conical papillae (Fig. 1). In the domestic duck there are 14 pairs of small conical papillae and 6 pairs of the large conical papillae (Fig. 2). The filiform papillae are distributed along lateral side of the lingual body. Fig. 1 Dorsal view on the tongue in the domestic goose. Dashed line points the small conical papillae. Continuous line shows large conical papillae. Ap - apex, B - body, Lp lingual prominence, R root. Scale bar=0,5 cm. Fig. 2 Dorsal view on the tongue in the domestic duck. Dashed line points the small conical papillae. Continuous line shows large conical papillae. Ap - apex, B - body, Lp lingual prominence, R root. Scale bar=0,5 cm. 85
3 3.1 The small conical papillae The small conical papillae of the body in the domestic goose are in the form of cones with sharpened ends, and their length is 2,8 mm and the width is 0,3 mm (Fig. 3). Processes of these papillae are directed sideways and slightly caudally and are arranged, relative to the long axis of the tongue, at an angle of (Fig. 3). The small conical papillae in the domestic duck have the shape of flattened plates whose ends are sharpened, arranged to the bottom of the tongue at an angle of (Fig. 5). Their average length is 1,7 mm and a width of 0,9 mm. Fig. 3 Magnification of the small conical papillae (Sco) and the filiform papillae (Fi) of the tongue in the domestic goose. Fig. 4 Magnification of the large conical papillae (Lco) and the filiform papillae (Fi) of the tongue in the domestic goose. Arrow shows twisted processes of the filiform papillae. 3.2 The large conical papillae Processes of the large conical papillae in both species are directed caudally. In the domestic goose, these papillae are arranged at an angle of and in the domestic duck at an angle of (Figs. 4, 7). The large conical papillae in the domestic goose have the shape of cones with sharpened ends, which the average length is 5,5 mm and the average width is about 0,9 mm (Fig. 4). In the domestic duck 4 large conical papillae, from the side of the lingual prominence, are in the form of a slightly flattened cone, which the caudal surface has an invagination and the rostral surface elongates in the lamina (Fig. 7). The shape of these papillae resembles a nib of fountain pen. Their length is 2,7 mm and the width is 1,5 mm. Two other large conical papillae in the domestic ducks are in the form of cones with sharpened ends (Fig. 8). Fig. 5 Magnification of the small conical papillae (Sco) and the filiform papillae (Fi) of the tongue in the domestic duck. Scale bar=300 µm. Fig. 6 Magnification of the filiform papillae (Fi) forming dense bristle in the rostral part of the body in the domestic duck. Scale bar=1 mm. 86
4 3.3 The filiform papillae The filiform papillae both in the domestic goose and duck, have the shape of twisted processes, and are densely arranged in the form of simple and long processes distributed on median side of conical papillae (Fig. 4, 7, 8). The filiform papillae in the domestic goose, which are between small conical papillae, take the form of simple processes (Fig. 3). In the domestic duck, the filiform papillae form a dense bristles covering small conical papillae (Fig. 5). The average length of filiform papillae in goose is 1084,1 µm and the width is between 48,7 µm and 146,3 µm. In the domestic ducks filiform papillae are longer and reach a length of 1513,4 µm and the average width is 45,8 µm. Fig. 7 Magnification of the large conical papillae (Lco) and the filiform papillae (Fi) of the tongue in the domestic duck. Arrow shows the twisted processe of the filiform papillae. Arrow head points the invagination on the caudal part of the large conical papillae. Scale bar=1 mm. Fig. 8 Magnification of the large conical papillae (arrow heads) in form of cones and the filiform papillae (Fi) of the tongue in the domestic duck. Arrow shows the twisted processe of the filiform papillae. Scale bar=1 mm. 4. Discussion The process of food intake in vertebrates is complex and there are three stages: ingestion, intra-oral transport and swallowing [17]. Behavioral observations conducted in Anseriformes, showed that in goose and duck, the ingestion phase can be performed via pecking, grazing and filter-feeding [18, 19]. In the process of filter-feeding in the domestic goose and duck are mainly involved both kinds of mechanical papillae i.e. filiform papillae and also conical papillae, which form a spatial filter-feeding apparatus on lateral edges of tongue. The filter-feeding apparatus is getting in contact with inner border of serrate bill. Filtration of fluid with micro particles of food in goose is carried out in two phases and in duck during in a single cycle [18, 19]. After collecting the liquids, occurs lifting of the tongue and pressing it to the palate. Water is then removed outside oral cavity and food remains on the laminae of the beak and on surface of filiform papillae of tongue. Construction of filter-feeding apparatus vary in both studied species of birds. In goose all conical papillae of the body take the shape of elongated cones directed towards the caudal part of the tongue. Arrangement of papillae, which was observed in ducks is different, because only the large conical papillae are directed caudally and the rostral small conical papillae are pointed to bottom of the tongue. Also the arrangement of filiform papillae in both species is species-specific. In goose filiform papillae occur only in spaces between the large and small conical papillae of the body. Whereas in duck, the filiform papillae in the rostral part of the body completely overlap the small conical papillae and create dense bristles, which exactly wipe out small particles of food. In the caudal part of the body, the filiform papillae, are present between the large conical papillae as in goose. The comparison of the morphometric data shows significant differences in the size of the filiform papillae. Length of filiform papillae in duck is about 70% higher than in goose and the width is 50% smaller. These results provide additional comment for role of the filiform papillae, which is the main component of the filter-feeding apparatus. Longer and thinner filiform papillae in duck forming a dense bristle are undoubtedly more efficient filter-feeding apparatus, collecting smaller particles of food, compared to those structures in goose. It should be added that in duck filtration of food, is also assisted by a suitably shaped palate with a smooth surface and the construction of the lingual prominence, which front edges are raised. According to Van der Leeuw et al. in 2003 [19] these features support the suction-feed pump. 87
5 When describing structures of the filter-feeding apparatus it should be remembered that these structures are also involved in collecting food by grazing. From the latest publication by Jackowiak et al. in 2011 [11] structures that are directly related to the process of grazing, are large and small conical papillae of the body of the tongue. These papillae fit to horny lamina in the lower beak and together participate in cutting grass and green shoots of plants. As mentioned before, in both studied species of birds, was varied arrangement of conical papillae on the lateral edges of the body of the tongue, which is species-specific. Comparing sizes of conical papillae in both species of birds were found that the large and small conical papillae in goose are respectively, longer and narrower than in the duck. Metric analysis showed that the large conical papillae in goose are longer up to 50% than in duck and the width is about 37% lower than in duck. The small conical papillae in goose are 40% longer and up to 60% narrower than in duck. Such shapes and proportions of the size of the papillae may indicate that the longer and narrower conical papillae of the body in goose fit well to narrow gaps in the bottom of the beak and thus effectively cut grass. Differences in the structure of the filter-feeding apparatus in goose and duck can be considered as a structural feature indicating the adaptation of duck to life in the aquatic environment, and goose to live in the terrestrial environment. At the same time the structure of the filter-feeding apparatus in the domestic goose shows that the bird next to grazing food, is still also capable to filtering food from water. On the other hand the duck, which mainly filtering food from water, can also collect food by grazing. References [1] Emura S, Okumura T, Chen H. Scanning electron microscopic study of the tongue in the Japanese pygmy woodpecker (Dendrocopos kizuki). Okajimas Folia Anatomica Japonica. 2009; 86: [2] Emura S, Okumura T, Chen H. Comparative studies of the dorsal surface of the tongue in three avian species by scanning electron microscopy. Okajimas Folia Anatomica Japonica. 2010; 86: [3] Emura S, Okumura T, Chen H. Scanning electron microscopic study of the tongue in the rainbow lorikeet (Trichoglossus haematodus). Okajimas Folia Anatomica Japonica. 2011; 88: [4] Glatz PC, Miao ZH, Ru YJ. Feeding free-range poultry and pigs. In: Bels V, editor. Feeding in Domestic Vertebrates. From structure to behavior. CAB International, Wallingford. Oxfordshire, UK: CABI Publishing; p [5] Harrison JG. Tongue. A new dictionary of birds. Ed A.L. Thomson. Nelson, London; [6] Hassan SF, Moussa EA, Cartwright AL. Variations by sex in anatomical and morphological features of the tongue of Egyptian goose (Alopochen aegyptiacus). Cells Tissue Organs. 2010; 191: [7] Homberger DG, Brush AH. Functional-morphological and biochemical correlations of the keratinized structures in the African Grey Parrot, Psittacus erithacus (Aves). Zoomorphology. 1986; 106: [8] Iwasaki S, Kobayashi K. Scanning and transmission electron microscopical studies on the lingual dorsal epithelium of chickens. Acta Anatomica Nipponica. 1986; 61: [9] Iwasaki S, Asami T, Chiba A. Ultrastructural study of the keratinization of the dorsal epithelium of the tongue of Middendorff s bean goose, Anser fabalis middendorfii (Anseres, Antidae). Anatomical Record. 1997; 247: [10] Jackowiak H, Skieresz-Szewczyk K, Kwieciński Z, Trzcielińska-Lorych J, Godynicki S. Functional morphology of the tongue in the Nutcracker (Nucifraga caryocatactes). Zoological Science. 2010; 27:589-5 [11] Jackowiak H, Skieresz-Szewczyk K, Godynicki S, Iwasaki S, Meyer W. Functional morphology of the tongue in the domestic goose (Anser anser f. domestica). Anatomical Record. 2011; 294: [12] Kear J. The food of geese. International Zoo Yearbook. 1966; 6: [13] Kobayashi K, Kumakura M, Yoshimura K, Inatomi M, Asami T. Fine structure of the tongue and lingual papillae of penguin. Archive of Histology and Cytology. 1998; 61: [14] Kooloos JGM. A conveyer - belt model for pecking in the mallard (Anas platyrhynchos L.). Netherlands Journal of Zoology. 1986; 36: [15] Kooloos JGM, Kraaijeveld AR, Langenbach GEJ, Zweers GA. Comparative mechanics of filter feeding in Anas platyrhynchos, Anas clypeata and Aythya fuligula (Aves, Anseriformes). Zoomorphology. 1989; 108: [16] Rossi JR, Baraldi-Artoni SM, Oliveria D, Cruz C, Franzo VS, Sagula A. Morphology of beak and tongue of partridge Rhynchotus rufescens. Cienca Rural. 2005; 35: [17] Schwenk K. Functional and evolutionary morphology of lingual feeding in squamate reptiles: phylogenetics and kinematics. Journal of Zoology. 1989; 219: [18] Zweers GA, Gerritsen AFC, van Kranenburg Voogd PJ. Mechanics of feeding of the Mallard (Anas platyrhynchos L.; Aves, Anseriformes). Published in New York: Basel; [19] Van Der Leeuw AH J, Kurk K, Snelderwaard PC, Bout RG, Berkhoudt H. Conflicting demands on the trophic system of Anseriformes and their evolutionary implications. Animal Biology. 2003; 53: [20] Von Preuss F, Donat K, Luckhaus G. Functional study of the tongue in domestic fowls. Berliner und Munchener Tierarztliche Wochenschrift. 1969; 82:
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