Ultramorphological and histological studies on the

The Journal of Basic & Applied Zoology (2014) xxx, xxx–xxx

The Egyptian German Society for Zoology

The Journal of Basic & Applied Zoology www.egsz.org www.sciencedirect.com

Ultramorphological and histological studies on the tongue of the common kingfisher in relation to its feeding habit Sh.A. Al-Zahaby *, E.H. Elsheikh Department of Zool., Faculty of Science, Zagazig Univ., Egypt Received 9 May 2014; revised 16 August 2014; accepted 19 August 2014

KEYWORDS Ultramorphology of tongue; Lingual papillae; Lingual epithelium; Common kingfisher; River kingfisher; Little blue kingfisher; Alcedo atthis

Abstract The tongue of common kingfisher (Alcedo atthis, Alcedinidae, Aves) was investigated by means of light and scanning electron microscopy to elucidate its ultramorphological and histological features. The tongue of the studied bird is an elongated, tubby and consistent organ of triangular shape of about 8.9 mm in length. It drops in the posterior quarter of the lower part of the very long bill. It is composed of three successive regions; blunt apex, stocky body and root. In addition to the giant conical papillae demarcating the tongue’s body from root, numerous caudally directed spiny conical papillae are differently distributed on the dorsal and lateral surfaces of the lingual body and root. Both papillae appears to help catching and directly swallowing preys, however the apex is covered with superposed foliate papillae. By light microscope, the dorsal lingual epithelium is composed of a keratinized stratified squamous epithelium. The stratum basale is followed by a thick stratum spinosum of polyhedral cells containing some deeply embedded taste buds and gives rise to the stratum corneum cell layer. The loose connective tissue core (lamina propria) which embraces some blood vessels and melanocytes forms finger-like dermal papillae of different heights under the epithelium. It also contains branched tubulo-alveolar salivary glands mainly of massive gelatinous mucus secreted on the epithelial surface to facilitate food-intake indicating a close relationship of the lingual structure with the common kingfisher feeding habit which feeds mainly on fishes and aquatic arthropods. ª 2014 The Egyptian German Society for Zoology. Production and hosting by Elsevier B.V. All rights reserved.

* Corresponding author. E-mail address: [email protected] (S.A. Al-Zahaby). Peer review under responsibility of The Egyptian German Society for Zoology.

Production and hosting by Elsevier

Introduction Kingfishers are a group of small to medium sized brightly colored birds belonging to order Coraciiformes, suborder Alcedines which contains three families, Alcedinidae, Halcyonidae and Cerylidae. They have a cosmopolitan distribution occupying a wide range of habitats (Woodall, 2001).

2090-9896 ª 2014 The Egyptian German Society for Zoology. Production and hosting by Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.jobaz.2014.08.002 Please cite this article in press as: Al-Zahaby, S.A., Elsheikh, E.H. Ultramorphological and histological studies on the tongue of the common kingfisher in relation to its feeding habit. (2014), http://dx.doi.org/10.1016/j.jobaz.2014.08.002

2 From the 93 species distributed worldwide, only three species are locally found in Egypt especially; North coast, Nile Delta and Valley as well as Suez Canal area of Egypt. The common Kingfisher (Alcedo atthis, Linnaeus, 1758) of the present study is a noisy bird belonging to the first family, Alcedinidae (Tharwat, 1997). It is widely distributed and estimated to be the world’s third most common kingfisher (Fry and Fry, 2000). The common kingfisher (A. atthis) is also known as River Kingfisher, Little blue kingfisher and Eurasian kingfisher as it is widely distributed across Eurasia and North Africa (Woodall, 2001). It is a carnivorous (piscivorous) bird, eats mostly small fish, aquatic arthropods as well as Crustacea including freshwater shrimps and crabs (Campos et al., 2000). It hovers above the water to search for its prey then dives into the water to grab and catch it (Vilches et al., 2012). Birds live in the air, on land and around fresh or sea water, so with respect to their various life styles they have different feeding habits. Consequently shape and structures of their bills and tongues especially lingual epithelium might become adapted to dry conditions. Accordingly, keratinization of the lingual epithelium is a common feature of bird’s tongue (Kobayashi et al., 1998). Other characteristic features of the bird’s tongue that include the distinct median sulcus, convex lateral parts, different types of papillae, distribution of lingual glands and the crest of the backward giant conical papillae between the tongue’s body and root must be taken into consideration (Jackowiak and Godynicki, 2005; Emura, 2008). Such modifications result in differing tongue’s mobility and ability to slide out, extracting and manipulating food in the beak cavity (Emura et al., 2008a). Guimara˜es et al. (2009) revealed a close correlation between the structure of tongue and mechanism of food intake with respect to food type and source. The tongue which is the target of the present study, exhibits significant morphological adaptation to the different environmental conditions particularly feeding habits (Iwasaki, 2002). So, studies on the fine structure of the tongue’s surface in relation to feeding habits have been conducted on many avian species, such as white tailed eagle (Jackowiak and Godynicki, 2005), cormorant (Jackowiak et al., 2006), black kite (Emura, 2008), peregrine falcon and common kestrel (Emura et al., 2008a), northern goshawk (Emura et al., 2008b), spot-billed duck (Emura, 2009a), three species of herons (Emura, 2009c), Japanese pygmy woodpecker (Emura et al., 2009), blue-and-white flycatcher, hawfinch and Japanese white-eye (Emura et al., 2010a), common quail (Parchami et al., 2010a), rainbow lorikeet (Emura et al., 2011), scarlet macaw (Emura et al., 2012), muscovy duck (Igwebuike and Anagor, 2013), white-breasted kingfisher (El-Bakary, 2012), whitethroated kingfisher and common buzzard (El-Beltagy, 2013) and hooded crow (Elsheikh and Al-Zahaby, in press). The purpose of the present study is to investigate the dorsal lingual mucosa of the adult common kingfisher (A. atthis) which is commonly noticed around Abbasa ponds, Sharkia Province, Egypt. It is a sparrow-sized bird (about 16–17 cm long) renowned for its iridescent blue plumage, dumpy-body, large head, short tail and small red feet. This is done in relation to the bird’s feeding habits by using light and scanning electron microscopes and comparing results with those of previous studies.

S.A. Al-Zahaby, E.H. Elsheikh Materials and methods Tongues of four adult common kingfisher (A. atthis) collected from Abbasa ponds area, Sharkia province, Egypt, are used for the present investigations. For the Scanning Electron Microscope (SEM) the tongues were rinsed with 0.1 M phosphate buffer at pH 7.3. Post-fixation was made in 1% osmium tetroxide solution for two hours at 4 C. After dehydration through a graded ethanol series, specimens of tongue were subsequently dried with a Tousimis Autosamdri 815B critical point dryer. The dried specimen were mounted on aluminium stubs and coated by gold sputter coater (SPI-Module) and then examined with a Scanning Electron Microscope JEOL (JSM-5400 LV) in the Regional Centre of Mycology, Al-Azhar University, Cairo, Egypt. For the light microscope (LM), samples of the apex, body and root of the tongue were fixed in the 10% buffered paraformaldehyde (Merck, pH: 7.3) at room temperature for 48 h. Later the fixed specimens were submitted to dehydration process in a series of ethanol and embedded in paraplast. Histological sections of 5 lm thickness were stained routinely with Haematoxylin and Eosin (HE). Results The tongue of the adult common kingfisher (A. atthis) is an elongated, tubby and consistent organ of a triangular shape of about 8.9 mm total in length. It mimics and slightly drops in the bottom of the caudal quarter of the very long (40 mm), stout and pointed dagger-like bill. Morphologically, it is demarcated into the usual three successive regions of the avian tongues; non-tapered apex in front of medial stocky body and the hindmost root or radix, without any median sulcus on the dorsal surface (Fig. 1). SEM observations By SEM, the dorsal lingual surface of the studied bird is rough and keratinized with different degrees. The lingual apex is non-tapered or blunt. Its dorsal epithelium is eminent forming superposed ridges with intervening grooves giving the appearance of foliate papillae (Figs. 2 and 3). These papillae embrace some orifice of lingual glands. It is noted that the lateral posterior borders of the lingual apex, with its foliate papillae and desquamating superficial cells, extend back over the lingual body giving anarchy appearance (Figs. 4 and 5). However, the lingual body is dorso-ventrally flattened with transverse slightly raised dorsum, transverse eminence, in front of the papillary crest (Fig. 6). The latter, is of an inverted V shape and is formed of more than two rows of large or giant conical papillae, lying between the stocky body and root of the tongue. The apices of these giant papillae are posteriorly pointed, the longest are found at the lateral surfaces of the tongue, whereas papillae located medially are progressively smaller (Fig. 7). Nonetheless, on the dorsal and lateral surfaces of the body and root, other stout backward spiny conical papillae are scattered with different consistencies. In the anterior lateral part of the tongue’s body these spiny conical papillae are numerous and crowded (Fig. 5). The surface cells of the epithelium in the most anterior region of the lingual body

Please cite this article in press as: Al-Zahaby, S.A., Elsheikh, E.H. Ultramorphological and histological studies on the tongue of the common kingfisher in relation to its feeding habit. (2014), http://dx.doi.org/10.1016/j.jobaz.2014.08.002

Ultramorphological and histological studies on the tongue of the common kingfisher

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Fig. 3 Scanning electron micrograph of higher magnification of Fig. 2 showing; superposed foliate papillae (Fp) and orifices of the lingual gland (arrow). Scale bar 100 lm.

Fig. 1 Scanning electron micrograph of the whole tongue of the common kingfisher showing its; apex (A), body (B), root (R), transverse eminence (Te), laryngeal mound (Lm) and laryngeal ostium (Lo), giant conical papillae (Gcp) demarcating the body from root. Note that the dorsal surface of the apex is of a smooth aspect, however the body and root present a rough feature. Scale bar 1 mm.

Fig. 2 Scanning electron micrograph of the tongue’s apex of the studied bird showing; the characteristic superposed foliate papillae (Fp) and the most anterior region of tongue’s body (arrow) with an anarchy appearance. Scale bar 200 lm.

are desquamated or shed as clusters of plaques, so the surface appears frayed (Fig. 8), other cells demonstrate a delicate pattern of microridges (Fig. 9). Heading backward, stout spiny conical papillae appeared numerously especially in the lateral boundaries of the tongue’s body and root, at the expense of desquamating epithelial cells (Figs. 10 and 11). Orifices of lingual glands are evidenced also in between the posteriorly inclined spiny conical papillae

Fig. 4 Scanning electron micrograph of the anterior tongue’s border showing: Foliate papillae (Fp) distinguish the lingual apex and desquamating superficial epithelial cells (Dsc) giving an anarchy appearance in the most anterior region of the body. Scale bar 50 lm.

Fig. 5 Scanning electron micrograph of the antero-lateral region of the tongue’s body showing; numerous stout spiny conical papillae (Scp) outer to the mid region of the desquamating epithelial cells (Dsc). Scale bar 50 lm.

especially in the lingual root dorsum of the studied kingfisher (Figs. 12 and 13). Otherwise, the epithelium covering the most posterior extremity of the kingfisher’s tongue near the laryngeal mound, bounding the laryngeal cleft, demonstrates few prone or posteriorly inclined spiny conical papillae, lingual gland orifices and desquamating epithelial cells (Figs. 14 and 15). The posteriorly inclined spiny conical papillae and orifices of the lingual glands


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Fig. 6 Scanning electron micrograph of the tongue’s body (B) showing; transverse eminence (TE), papillary crest of giant conical papillae (Gcp) and spreading of spiny conical papillae (arrows). Scale bar 1 mm.

Fig. 7 Scanning electron micrograph showing; giant conical papillae (Gcp) between tongue’s body (B) and root (R), abundance of inclined spiny conical papillae (Scp) above and below the papillary crest. Scale bar 200 lm.

Fig. 8 Scanning electron micrograph of the anterior mid region of the tongue’s body showing; the desquamating superficial epithelial cells (Dsc), very rare spiny conical papillae (Scp), orifice of the lingual gland (arrow). Scale bar, 20 lm.

are more encountered posteriorly on both sides of the laryngeal cleft (Figs. 16 and 17). Light microscopical observations The tongue of the common kingfisher is covered by a normal stratified squamous epithelium mounting the dermis, on both

S.A. Al-Zahaby, E.H. Elsheikh

Fig. 9 Scanning electron micrograph of the anterior mid region of the tongue’s body little back of the previous one showing; desquamating superficial epithelial cells (Dsc), orifice of the lingual gland (arrow). Note the delicate pattern of microridges on the keratinized epithelial cell surface (arrow head). Scale bar 10 lm.

Fig. 10 Scanning electron micrograph of the posterior mid region of the tongue’s body showing; desquamating superficial epithelial cells (Dsc), few spiny conical papillae (Scp), orifice of the lingual gland (arrow), mucous granules (Mg). Scale bar 20 lm.

Fig. 11 Scanning electron micrograph of the posterior mid region of the tongue’s body showing; spreading of more inclined spiny conical papillae (Scp), desquamating epithelial cells (Dsc) orifice of the lingual gland (arrow), mucous granules (Mg). Scale bar 100 lm.

dorsal and ventral surfaces. By light microscope it is evident that, the dorsal lingual epithelium is composed of a keratinized stratified squamous epithelium. The cells of the single layered stratum basale are spherical to cuboidal with rounded nuclei.


Ultramorphological and histological studies on the tongue of the common kingfisher

Fig. 12 Scanning electron micrograph of the posterior region of the tongue’s body border showing; stout spiny conical papillae (Scp). Scale bar 100 lm.

Fig. 13 Scanning electron micrograph of the posterior region of the body near the border showing; numerous stout spiny conical papillae (Scp) and orifice of the lingual gland (arrow). Scale bar 50 lm.

Fig. 14 Scanning electron micrograph of the laryngeal mound (Lm) showing; desquamating epithelial cells (Dsc) and orifice of the lingual gland (arrow). Scale bar 100 lm.

To the outside, this cell layer is followed by a compacted thick stratum spinosum displaying typical polyhedral cells with prominent nuclei. They give rise to layers of flattened cells with horizontally elongated nuclei, constituting the stratum corneum (Figs. 18 and 19). Apart from the well keratinized covering epithelium, the lingual apex was predominated by foliate papillae (Figs. 20 and 21). However, the dorsal surface of the

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Fig. 15 Higher-magnification view of the previous figure showing; desquamating superficial epithelial cells (Dsc), few prone or inclined spiny conical papillae (Scp) and orifice of the lingual gland (arrow). Scale bar 50 lm.

Fig. 16 Scanning electron micrograph of the tongue’s root showing: orifice of the lingual gland (arrow) and inclined spiny conical papillae (Scp) at sides of the laryngeal mound. Scale bar 100 lm.

Fig. 17 Higher-magnification of the previous figure showing; lot of inclined spiny conical papillae (Scp) and orifice of the lingual gland (arrow) at the sides of the laryngeal mound. Scale bar 100 lm.

body and root of the kingfisher’s tongue demonstrate multiple, hard, pointed and backward directed processes (spiny conical papillae) (Fig. 22). These papillae are intensively running also at the lateral boundaries of the tongue with relatively longer lengths. Otherwise, numerous individual cells were seen to desquamate from the surface of the epithelium of the lingual


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Fig. 18 Light micrograph of a vertical section in the tongue of the common kingfisher showing: non-keratinized epithelium (Nke) of the tongue dorsum, a taste bud (Tb), stratum spinosum (Ss), stratum basale (Sb), short dermal papillae (Dp), loose connective tissue of the lamina propria (Lp) embracing melanocytes (arrow) and blood vessels (Bv).

S.A. Al-Zahaby, E.H. Elsheikh

Fig. 20 Light micrograph of a vertical section in the tongue’s apex showing: foliate papillae (Fp) with keratinized dorsal epithelium (Kde), lamina propria (Lp) gives long vertical dermal papillae (Dp), entoglossal cartilage (Ec) flanked by perichondrium sheath (Ps).

Fig. 21 Light micrograph of a vertical section in the tongue’s apex showing: foliate papillae (Fp) with keratinized epithelium (Kde), loose connective tissue of the lamina propria (Lp) with long vertical dermal papillae (Dp), non-keratinized ventral epithelium (Nkve) with very short dermal papillae.

Fig. 19 Light micrograph of a vertical section in the tongue of the studied bird showing: keratinized epithelium of the stratum corneum (Sc), keratin layer (Kl), imbedded taste buds spotted in the stratum spinosum (Ss), some melanocytes (arrow) lie in the lamina propria (Lp) beneath the stratum basale (Sb) and derma papilla (Dp).

body, a phenomenon previously illustrated in the SEM preparations (Figs. 8 and 10). Taste buds of bulbous form are spotted in the stratum spinosum of the tongue over the stratum basale especially in the tongue root (Figs. 18 and 19). However, gustatory papillae were not detected in the epithelium covering the tongue of the studied bird.

Fig. 22 Light micrograph of a vertical section in the tongue of kingfisher showing: keratinized dorsal epithelium (kde), stratum basale (Sb), stratum spinosum (Ss) and stratum corneum (Sc) emitted into spiny conical papilla (Scp), lamina propria (Lp) with short dermal papillae (Dp) and melanocytes (arrow).


Ultramorphological and histological studies on the tongue of the common kingfisher In the lamina propria, directly beneath the stratum basale, a large number of melanocytes are scattered (Figs. 18 and 19). Also, entoglossal hyaline cartilage extending ventrally even in the lingual apex is surrounded by a distinct perichondrium, skeletal muscle elements and loose connective tissue containing numerous blood vessels (Fig. 20). Connective tissue papillae of the lamina propria that penetrate the epithelial mucosa are relatively longer and often vertically oriented under the keratinized epithelium of foliate papilla (Fig. 21). The underlying irregular loose connective tissue layer (lamina propria) of the tongue is housed also with many glandular units. These lingual glands are of complex tubuloalveolar type, opening on the surface of the epithelium through mucus reservoirs of wide orifices especially in the caudal part of the tongue. These glands are surrounded by connectivetissue capsules, with septa dividing the glands into lobules (Figs. 23 and 24). The secreting mucus forms a thick, semitransparent gelatinous layer, strongly attached to the surface of the tongue.

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Fig. 24 Light micrograph of vertical section of the lingual mucosa showing: Non-keratinized epithelium (Nke), lamina propria (Lp), complex of the tubulo-alveolar gland (Lg) surrounded by connective tissue capsule (Ctc), mucus reservoir (Mr), lingual muscle (Sm), blood vessel (Bv).

Discussion Birds are adapted to their environment, compatible with their life style and have different models of bills and tongues. The tongue of birds is a highly diverse organ showing considerable variability in size, form and structure, much of which can be closely related to feeding habits (Kobayashi et al., 1998). The elongated triangular tongue of the common kingfisher (A. atthis) is composed of the three characteristic parts of the avian tongue; blunted apex, stocky body and the hindmost root without median dorsal sulcus. It fills the posterior quarter of the bill, as in the common African ostrich in which its tongue is also not more than quarter length of its bill (Tadjalli et al., 2008). Aside from kingfisher of the present study, the tongue of Anatidae (ducks, geese and swans) is specialized in grazing, pecking and filtration of food particles (Bels, 2006). Their tongues are elongated with a rounded apex and distinct median sulcus (Emura, 2009a) as was also recorded in common quail (Parchami et al., 2010a), red jungle fowl (Kadhim et al., 2011) and Muscovy duck (Igwebuike and Anagor, 2013). Contrastingly, in piscivorous birds such as common kingfisher of the present study, cormorant and stork (Jackowiak et al., 2006) and white-throated kingfisher

Fig. 23 Light micrograph of a vertical section in the tongue of the studied kingfisher showing: non-keratinized epithelium (Nke), lingual gland (Lg) surrounded by connective tissue capsule (Ctc), mucus reservoir (Mr), smooth lingual muscle (Sm).

(El-Beltagy, 2013) as well as in insectivorous birds such as brown-eared bulbul (Emura, 2009b), Jungle Nightjar (Emura et al., 2010b) and white eared bulbul (Parchami and Fatahian Dehkordi, 2013) their tongues showed length reduction without any median sulcus. In the common kingfisher which hunts and feeds mainly on fishes, the dorsal epithelial surface of its tongue is covered with a somewhat thick horny keratinized layer. It gives universally distributed spiny conical papillae, except on the anterior lingual apex. In this part the keratinized epithelium is organized in superposed foliate papillae with desquamating epithelial cells. However, in the tongue’s ventral surface, the stratified epithelia have a thinnest horny layer. This keratinization of the lingual epithelium was considered by Kobayashi et al. (1998) as a common avian feature. Iwasaki (2002) demonstrated a close relationship between the extent of lingual epithelial keratinization and avian feeding habit. A strongly keratinized lingual epithelium is seen mainly in herbivorous and granivorous birds as little tern and common buzzard (Iwasaki, 1992 and El-Beltagy, 2013, respectively). Nonetheless, a lesser degree of keratinization is found in birds living in aquatic habitats (Iwasaki, 2002) as also recorded in white throated kingfisher (El-Beltagy, 2013) and of course the common kingfisher of the present studies. The spiny conical papillae covering the kingfisher’s tongue with different degrees on the dorsal and lateral surfaces, may be considered as a species-specific trait for predator birds. Kobayashi et al. (1998) announced that, the tongue of many piscivorous bird species as penguin is adapted to hold the slippery preys by means of stiff, sharp, caudally-directed papillae (spiny conical papillae). The same authors presumed that, these papillae correspond to the filiform papillae of the mammalian species. Similarly, the tongues of the little egret, blackcrowned night heron and green-backed heron (Emura, 2009c) as well as white-throated kingfisher (El-Beltagy, 2013) feed on fish, most if not all, the dorsal epithelium of their tongue is covered with needle- like lingual papillae. However, in the Jungle Nightjar and scarlet macaw which feed on insects, the dorsal surface of their tongue’s apex and most of body presents a smooth aspect, but the conical papillae are observed only on


8 the posterior lingual body (Emura et al., 2010b, 2012, respectively). Nonetheless, zebra finch which is a seed and insect eating bird has many fine densely populated needle-like processes (papillae) in both lateral sides of the anterior lingual apex (Fatahian Dehkordi et al., 2010). El-Bakary (2011) declared that, these conical papillae facilitate holding and swallowing of the food items. This great variability is also recorded in the pattern of the posteriorly directed giant conical papillae, which in kingfisher are lined up in more than two rows arranged in a single papillary crest as those found in scarlet macaw (Emura et al., 2012). This pattern greatly varied from that found in other bird species like the white tailed eagle (Jackowiak and Godynicki, 2005), golden eagle (Parchami et al., 2010b), red Junglefowl (Kadhim et al., 2011), white-eared bulbul (Parchami and Fatahian Dehkordi, 2013), muscovy duck (Igwebuike and Anagor, 2013), cattle egret (Moussa and Hassan, 2013) and hooded crow (Elsheikh and Al-Zahaby, in press) having one recognizable row of giant conical papillae. Other species have definitely two rows of these giant papillae, they frequently have behind the smaller main row another additional one of larger papillae forming secondary papillary crest as observed in the nutcracker (Jackowiak et al., 2010) and common quail (Parchami et al., 2010a). Nonetheless, these posteriorly oriented giant conical papillae are totally absent in ostrich which eats almost anything such as invertebrates, small vertebrates and fruits (Jackowiak and Ludwig, 2008; Guimara˜es et al., 2009) as well as in woodpecker which feeds on small insects (Emura et al., 2009). However, the tongue of the little egret, black-crowned night heron, and green-backed heron which feed also on fish has only a pair of giant conical papillae (Emura, 2009c). Jackowiak and Godynicki (2005) claimed that, the occurrence of giant conical papillae, forming the papillary crest separating the body and root of the tongue, is a characteristic trait of modern birds, Neornithes. They act co-operatively and constitute mechanically resistance elements for sliding food items towards the oesophagus (Jackowiak et al., 2010; El-Beltagy, 2013). In kingfisher of the present study, complex of lingual salivary glands composed of tubulo-alveolar units is spread in the whole lamina propria of the tongue under the dorsal mucosa. The secretion of these glands does not pass directly to the outside surface but it is collected in the subepithelial chambers, where wide orifices provide effective evacuation of secretion as also stated by Jackowiak and Godynicki, 2005 in the white tailed eagle. Fatahian Dehkordi et al. (2010) in the zebra finch, proved that this salivary secretion of lingual glands is of glycoprotein nature, strongly positive with PAS reaction. El-Beltagy (2013) revealed that, in the white-throated kingfisher and common buzzard, the lingual salivary glands were made of mucoserous cells that elaborate acid and neutral mucosubstances. Recently, Mahmoud (2014) also found that, the salivary glands secretion in common Kestrel hunting on small mammals and Budgerigar feeds on seeds is mainly of mucous nature, strong PAS positive. This salivary mucopolysaccharide secretion is a moisturizing fluid that facilitates the ingestion of food as declared in ostrich (Jackowiak and Ludwig, 2008), nutcracker (Jackowiak et al., 2010) and hoopoe (El-Bakary, 2011). It may also act as inhibitor of some bacterial enzymes in the buccal cavity (Gargiulo et al., 1991). Otherwise, the microridges recognized on the superficial epithelial cells of the lingual body have been interpreted as structures

S.A. Al-Zahaby, E.H. Elsheikh that increase the adhesion of mucus to the epithelium (Jackowiak and Ludwig, 2008). On the other hand, as in other birds, little taste buds were found in the epithelium of the common kingfisher’s tongue. They are located in the deep area of the lingual epithelium as also stated by Ganchrow et al. (1991) and El-Beltagy (2013) in chick as well as in white-throated kingfisher and common buzzard, respectively. These taste buds are connected to the dorsal surface of the tongue through long ducts. It must also be mentioned that, the entoglossal cartilage is a cartilaginous rod that extends anteriorly in the lamina propria just under the lingual mucosa. It is an extension from the basihyal naturally developed in the avian tongue (Jackowiak and Ludwig, 2008). According to the given ultramorphological and structural features of the present study, the tongue of common kingfisher is typical for birds which swallow food items directly as that of the white tailed eagle, feeds mostly on fish, it tears the prey with its bill and swallows it directly (Jackowiak and Godynicki, 2005). The same authors claimed that, the presence of protruding transverse eminence in front of the papillary crest of the backward giant conical papillae serves to swallow preys directly and at the same time to prevent its regurgitation. Otherwise, because they are high on the food chain, kingfishers are susceptible to the effect of pollutants. So, they are important for ecosystem and represent a good indicator of freshwater community health (Bannerman, 1955 and Vilches et al., 2012). Nonetheless, anglers considered A. atthis a threat to fish resources and fish farms but they are not numerous enough to cause significant economic losses (Bannerman, 1955).

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