Morphological Adaptation of the Buccal Cavity in Relation to Feeding Habits of the Omnivorous ﬁsh Clarias Gariepinus: a Scanning Electron Microscopic Study

The Journal of Basic & Applied Zoology (2012) 65, 191–198

The Egyptian German Society for Zoology The Journal of Basic & Applied Zoology

www.egsz.org www.sciencedirect.com

Morphological adaptation of the buccal cavity in relation to feeding habits of the omnivorous ﬁsh Clarias gariepinus: A scanning electron microscopic study

A.M. Gamal, E.H. Elsheikh *, E.S. Nasr

Department of Zoology, Faculty of Science, Zagazig University, Egypt

Received 12 March 2012; accepted 9 April 2012 Available online 5 September 2012

KEYWORDS Abstract The surface architecture of the buccal cavity of the omnivorous fish Clarias gariepinus Taste buds; was studied in relation to its food and feeding habits. The buccal cavity of the present fish was inves- Buccal cavity; tigated by means of a scanning electron microscope. This cavity may be distinguished into the roof Scanning electron and the floor. Papilliform and molariform teeth which are located in the buccal cavity are associated microscope; with seizing, grasping, holding of the prey, crushing and grinding of various food items. Three types Surface architecture; of taste buds (Types I, II & III) were found at different levels in the buccal cavity. Type I taste buds Fishes were found in relatively high epidermal papillae. Type II taste buds were mostly found in low epidermal papillae. Type III taste buds never raise above the normal level of the epithelium. These types may be useful for ensuring full utilization of the gustatory ability of the fish. A firm consis- tency or rigidity of the free surface of the epithelial cells may be attributed to compactly arranged microridges. These structures protect against physical abrasions potentially caused during food maneuvering and swallowing. Furthermore, protection of the epithelium from abrasion is enhanced with mucous cell secretions which lubricate ingested food items. ª 2012 The Egyptian German Society for Zoology. Production and hosting by Elsevier B.V. All rights reserved.

Introduction ical from preys. Teleosts are reported to have the most taste buds of all vertebrates. Carnivorous fishes are endowed with In any vertebrate species, gustation contributes to the accep- taste buds, not only in the oral cavity including gill regions, tance or rejection of potential foods for survival, since taste but also on the lips, barbells, and external skin surface (Go- buds primarily function in the feeding behavior to detect chem- mahr et al., 1992). Literature on the surface ultra-structure of the buccal cavity in fish is scanty. Surface organization of the buccal cavity, * Corresponding author. using scanning electron microscope, was studied for some car- E-mail address: [email protected] (E.H. Elsheikh). nivorous fishes such as Gadus morhua (Bishop and Odense, Peer review under responsibility of The Egyptian German Society for 1966); Sparus aurata (Cataldi et al., 1987) and the surface Zoology. plankton feeder, Catla catla (Sinha and Chakrabarti, 1985). Meyer-Rochow (1981) described the distribution and surface morphology of taste buds on the tongue of a variety of habi- Production and hosting by Elsevier tats. Ezeasor (1982) described taste buds in the oropharyngeal

2090-9896 ª 2012 The Egyptian German Society for Zoology. Production and hosting by Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.jobaz.2012.04.002 192 A.M. Gamal et al. cavity of the active predator Salmo gairdneri. Hansen et al. (2002) reported the development of taste buds at different loca- tions including the oropharyngeal cavity of Danio rerio. More recently, Fishelson and Delarea (2004) and Fishelson et al. (2004) described the form and distribution of taste buds and dentition in the oropharyngeal cavity of several blenniid, gobiid and cardinal fish species. Devitsina (2005) studied the comparative morphology of intraoral taste apparatus in some fish. Also Yashpal et al. (2006), Raji and Norozi (2010) and El-Bakary (2011) described the structure of the buccal cavity in different fishes, Rita rita, the omnivorous catfish Clarias batrachus and Serrasalmus nattereri and in the juvenile and adult sea bass Dicentrachus labrax, respectively.

Materials and methods

This study was carried out on the mature cat fish Clarias gariepinus to demonstrate the gross morphological features. Five Figure 1 Scanning electron-micrograph of the surface architec- fishes were anesthetized with MS222 (0.02%;Tricain, Sandoz) ture of the roof of the buccal cavity of Clarias gariepinus showing and then decapitated .The heads were carefully washed in the upper lip (UL); upper band of teeth (UT); upper breathing physiological saline solution (Breipohl et al., 1973a,b) to re- valve (UV); ridge like structure (arrow); palatine region (PR) and move the mucus covering the surface and then fixed in 10% palate (P). formalin. After fixation, the head gut was opened by dividing the head into an upper and a lower half by cutting horizontally through the mouth to the esophagus. The two halves were washed again in physiological saline solution. This procedure was followed by a second fixation in 1% osmium tetroxide (Dalton, 1955) for at least 6 h. Specimens were then washed, and dehydrated in increasing concentrations of ethanol. The dehydrated specimens were dried with the critical-point drier Tousimis Audosamdri-815. The dried specimens were coated by gold sputter coater (SPI-Module) and observed under the scanning electron microscope JEOL (JSM-5500 LV) in the Re- gional Center of Mycology, Al-Azhar University, Cairo, Egypt. Then specimens were stored over silica gel, to be kept in a perfect condition for many weeks.

Results

In the present work the buccal cavity of C. gariepinus is spa- cious and opens anteriorly through a wide transverse mouth, which is bordered by upper and lower lips. The mouth cavity is divided into two regions: the dorsal roof and the ventral Figure 2 Scanning electron-micrograph of the buccal cavity of floor. Clarias gariepinus showing the ridge-like structure between the The roof of the mouth cavity comprised antero-posteriorly, upper breathing valve (R) and taste buds of type I (arrow). an upper jaw that consists of the upper lip, upper band of teeth, upper breathing valve (a thin fold at the inner boundary of the upper jaw), the palatine regions are supported bilaterally occurred between the lower band of teeth (Fig. 3). The ridge by the palatine bones; and the palate extends backward to the was narrow at the anterior edge and gradually widened toward pharynx (Fig. 1). The palatine regions, in general, were ovoid the posterior edge of the jaw (Fig. 3). The tongue consisted of in shape, separated from each other by a part of the palate; an anterior region and a major posterior region which extends they converged or even merged anteriorly (Fig. 1). In the upper to the pharynx. The middle part of the posterior region was an jaw, an elongated ridge-like structure occurred within the elongated ridge-like structure which is similar to that part upper breathing valve (Fig. 2). The ridge was narrow at its found between the lower teeth band (Fig. 4). anterior side and gradually widened toward its posterior side The palatine regions and the upper and lower bands of (Fig. 2). teeth were characterized by the presence of teeth (Figs. 5–7). The floor of the mouth cavity comprised antero-posteriorly In contrast, the upper and lower lips and breathing valves, a lower jaw that consists of the lower lip, lower band of teeth, the palate and the tongue were edentulous. In addition, the lower breathing valve (a thin fold at the inner boundary of the teeth were papilliform (conical in shape) on the upper and low- lower jaw). The tongue extends backward to the pharynx er bands of teeth (Figs. 5 and 6) and molariform (round in (Fig. 3). In the lower jaw, an elongated ridge-like structure shape) on the palatine regions (Fig. 7). Morphological adaptation of the buccal cavity in relation to feeding habits of the omnivorous fish 193

Figure 3 Scanning electron-micrograph of the surface architec- Figure 5 Scanning electron-micrograph of the buccal cavity of ture of the ﬂoor of the buccal cavity of Clarias gariepinus showing Clarias gariepinus showing higher magniﬁcation of upper band of the lower lip (LL); lower band of teeth (LT); ridge like structure teeth (UT), papilliform teeth (white arrow) and taste buds of type (R) and (arrow); lower breathing valve (LV) and tongue (T). II (black arrow).

Figure 4 Scanning electron-micrograph of the buccal cavity of Figure 6 Scanning electron-micrograph of the buccal cavity of Clarias gariepinus showing the ridge-like structure (R) on the Clarias gariepinus showing higher magniﬁcation of lower band of tongue (T) with clusters of mound-like epithelial elevations teeth (LT); papilliform teeth (white arrow) and taste buds of type separated by deep clefts. Taste buds (arrows). II (black arrow).

The epithelium of the buccal cavity consisted of a mosaic representing a taste hair, projected at the surface through the pavement of irregular polygonal epithelial cells of various taste pore (Fig. 8). dimensions (Fig. 8). The free surface of each epithelial cell In addition, the epithelium of the buccal cavity was charac- was characterized by the presence of a series of microridges. terized by the presence of a large number of prominent, irreg- The microridges of the cells appeared smooth, uniform in ularly distributed conical or papillate epithelial protrusions. width and sinuous. They were compactly arranged, extensive These structures were either isolated or found in groups (Figs. and often form maze-like patterns or extensively branched 9–13). On the basis of the degree of elevation and external sur- and interwoven to form web-like patterns (Fig. 8). face morphology, the taste buds were classiﬁed into three types Rounded or triangular crypts were evident probably be- (Type I, II & III). tween each 2–3 epithelial cells at irregular intervals. These The type I taste buds were prominently elevated being lo- crypts represented the mucous cell openings (Fig. 8) as well cated on epithelial protrusions, projected well above the sur- as the taste pores of the taste buds, which were either slightly face, often in the upper and lower lips (Figs. 11 and 12), on sunk or found at the level of the epithelium. The taste buds the palatine as shown in ﬁg. 7 (in the vicinity of molariform were characterized by the presence of several microvilli, each teeth), on the gill arch (Fig. 9), on the intermediate gill rakers 194 A.M. Gamal et al.

Figure 7 Scanning electron-micrograph of the buccal cavity of Figure 9 Scanning electron-micrograph of the buccal cavity of Clarias gariepinus showing palatine region (PR) bearing type I Clarias gariepinus showing type I taste buds on gill arch in a taste buds (black arrow), molariform teeth (white arrow) and proﬁle. palate (P).

Figure 8 Scanning electron-micrograph of the surface architecture of the epithelium of the gill arch of the ﬁsh Clarias gariepinus Figure 10 Scanning electron-micrograph of the buccal cavity of showing type III taste buds with taste hairs (white arrow); mosaic Clarias gariepinus showing type II taste buds on gill arch (white pavement of epithelial cells with distinct boundaries and com- arrow) and mucous cell opening (black arrow). pactly arranged microridges with characteristic invaginations (black arrow) and mucous cell apertures (double arrow). The characteristic ridge-like structures found between the (Fig. 14), on the ridge like structure found between the upper upper breathing valve and lower band of teeth (Figs. 2 and breathing valve and the lower band of teeth (Figs. 2 and 3) and 3) and on the posterior region of the tongue (Fig. 4) were also found on the tongue (Fig. 4). formed of clusters of large, conspicuous, irregularly polyhe- The type II taste buds were slightly elevated being found on dral, mound-like epithelial elevations, which were separated small, low-height epithelial protrusions, on the upper and low- from each other by deep clefts. On the surface of such eleva- er bands of teeth (Figs. 5, 6 and 15), on the upper and lower tions, several prominent papillate epithelial protrusions were breathing valves (Figs. 1, 3 and 16), on the palate (Fig. 7), evident (Fig. 4). on the tongue (Fig. 4), on the gill arch and gill rakers (Figs. The epithelial protrusions were covered with concentrically 10 and 13). The taste pores of these taste buds appeared in arranged epithelial cells (Fig. 8). The latter cells often showed slight depressions at the apices of the epithelial protrusions. shallow depressions or invaginations. At the peak of each pro- The type III taste buds were located either slightly sunk or trusion, a taste bud was located, with closely packed microvilli at the level of the general epithelium throughout the buccal serving as taste hairs, which are protruded to the surface cavity (Fig. 8). through a rounded taste pore (Fig. 8). Morphological adaptation of the buccal cavity in relation to feeding habits of the omnivorous ﬁsh 195

Figure 11 Scanning electron-micrograph of the buccal cavity of Clarias gariepinus showing surface architecture of the epithelia of Figure 13 Scanning electron-micrograph of the buccal cavity of the upper lip. Note type I taste buds (black arrow). Clarias gariepinus showing gill arch and gill raker bearing type II taste buds (white arrow).

Figure 12 Scanning electron-micrograph of the buccal cavity of Clarias gariepinus showing the surface architecture of the lower Figure 14 Scanning electron-micrograph of the buccal cavity of lip. Note type I taste buds (white arrows). Clarias gariepinus showing type I taste buds on intermediate gill raker (white arrow). Discussion et al., 2004). Teeth on jaws, similar to the papilliform teeth Irregularity and distribution of taste buds, mucous cells and of C. gariepinus, were also described in several other catfishes the patterns of microridges on the epithelial cells at different such as Mystus aor and Silonia silondia (Khanna, 1962), C. regions of the roof and floor of the buccal cavity of the fish batrachus (Sastry, 1973), Mystus gulio (Pasha, 1964), Hete- C. gariepinus could be considered as adaptations to various ropneustes fossilis (Chitray and Saxena, 1962), Andersonia lep- food preferences and feeding behavior of the fish. tura and Siluranodon auritus (Golubtsov et al., 2004). Most of The papilliform teeth which are found on the upper and these fishes are bottom-dwelling species and their food primar- lower bands of teeth may be associated with seizing, grasping, ily consists of small fish and invertebrates. Khanna (1962) re- holding and preventing the escape of small preys, occurring in ported pronounced, large, curved teeth on the jaws as well as the diet of C. gariepinus. Khanna (1962) using light microscopy on vomers and palatines of piscivores Muraenesox talabon. reported the presence of teeth on the premaxillae but not on This author suggested that such teeth are intended to hold se- the dentaries. Scanning electron microscope studies showed curely the prey in the mouth. Bishop and Odense (1966) also the presence of elongated conical and spine-shaped teeth on reported simple, pointed curved teeth in the mouth cavity of the jaws of some fishes that feed on, small preys such as Den- the carnivorous G. morhua and suggested that they help impale ticeps clupeoides (Sire et al., 1998), Atherion elymus (Sire and prey. In some herbivorous fishes such as Labeo horie (Girgis, Allizard, 2001) and several cardinal fish species (Fishelson 1952), Cirrhinus mrigala (Khanna, 1962; Sastry, 1973), Labeo 196 A.M. Gamal et al.

Hara (1994) reported that, sense of taste is an important property in fish for distinguishing from a variety of food available to them in an aquatic environment. In C. gariepinus of the present work, the presence of taste buds could be considered as an adaptation to its bottom dwelling and sluggish feeding behavior compensating for the restricted visibility in the foul turbid water habits. Khanna (1968) showed that, taste buds were rare or absent from the highly predaceous carnivorous- fish, Muraenesox telabon and Harpadon nehereus which rely more on their eyesight for detecting prey. The same author also found that, Channa striata feed both by sight and taste, has a better gustatory sense. Moreover in the hill stream carnivorous fish, Tor tor, which selects its food from the mud, has the best developed gustatory organ with numerous taste buds while, in the plankton feeder Ilisha filigera taste buds are present but less in number than T. tor. In addition, Meyer-Rochow (1981) noticed few taste buds on the tongue Figure 15 Scanning electron-micrograph of the buccal cavity of of Carapus mourlani and absence of them on the tongue of Clarias gariepinus showing type II taste buds on upper band of Diretmus sp. These two mesopelagic species possess poorly teeth in profile. developed taste receptors, for they inhabit areas of low prey abundance and diversity. In fish, food items seized, grasped, snapped, or nibbled with jaws, in general, are retained in the mouth cavity. During the retention period, food is subjected to final sensory judgment either rejected or swallowed (Kasumyan and Doving, 2003). In C. gariepinus of the present investigation, prominent taste buds may be useful in assessing the palatability of the food and decide whether to swallow or spit it out. The decision is made when food comes in contact with taste buds resulting in a mechanical impulse perceived and transmitted from the sensory cells to the brain centers (Reutter et al., 1974; Reutter and Breipohl, 1975). Furthermore, the location of the taste buds (type I and type II) at the summit of the conspicuous epithelial protrusions may increase the probability of contact between the receptors and the food items. This may enhance the efficiency in perception and sorting of food types as well as in assessing the quality and palatability of food items (Yashpal et al., 2006, 2009; Meyer-Rochow, 1981). These authors observed taste buds on distinct dome-like elevations on the surface of the tongue of several fish species, and they suggested that elevated taste buds could have a superior perception of Figure 16 Scanning electron-micrograph of the buccal cavity of taste rather than non-elevated ones or receptors sunken below Clarias gariepinus showing lower breathing valve bearing taste the level of the tongue. buds of type I (arrow). Structures similar to the type III taste buds in the mouth cavity of C. gariepinus were also observed on the snout, lips and barbell epithelium of G. morhua (Harvey and Batty, dero (Saxena, 1980), and Hilsa ilisha and Mugil corsula (Sastry, 1998), on the head, lips and gill rakers of Danio rerio (Hansen 1973), where holding or grasping of food is not required, the et al., 2002), on the lips and mouth of some blenniid and gobiid jaws are edentulous. fishes (Fishelson and Delarea, 2004) and in the oro-pharyngeal The present work revealed that, the molariform teeth with cavity in a number of cardinal fishes (Fishelson et al., 2004). rounded and blunt surfaces in the palatine region were previ- Furthermore, Fishelson et al. (2004) reported in addition to ously reported in the fish R. rita (Yashpal et al., 2006). These the taste buds belonging to the type III category another cate- structures may be associated with the crushing and grinding of gory of the taste buds known as type IV. hard body preys (e.g., mollusks, crustaceans). Bond (1979) The presence of ridge-like structures on the tongue and in suggested that in the fish Anarrhichichthys ocellatus, which feed between the upper and lower bands of teeth of C. gariepinus on shelled animals, molariform teeth are used to crush the and in R. rita (Yashpal et al., 2006) is important, which results shells. Molar-like or plated teeth were also reported in adult in the projection of taste buds above the level of the surface of S. aurata, which feed mainly on mollusks, polychaetes and the epithelium. In addition, the occurrence of taste buds on crustaceans (Cataldi et al., 1987). Molariform teeth may also these structures may be associated with the high degree of be used to compress food into a manageable lump, prevent competence of the fish in taste preference and selection of food. its escape and ensure its progress toward the throat Furthermore, these ridges may direct the food particles in the (Whitehead, 1977). buccal cavity toward the pharynx. Morphological adaptation of the buccal cavity in relation to feeding habits of the omnivorous fish 197

In C. gariepinus of the present investigation, the taste buds El-bakary, N.E.R., 2011. Comparative scanning electron microscope which are found on the upper and lower breathing valves may study of the buccal cavity in juvenile and adult sea bass (Dicen- serve to screen the quality of food before it is passed onto the trachus labrax). World Appl. Sci. J. 12 (8), 138–1133. mouth cavity. Similar results were reported by Yashpal et al. Ezeasor, D.N., 1982. Distribution and ultrastructure of taste buds in (2006) in R. rita. In addition, Fishelson et al. (2004) reported the oropharyngeal cavity of the rainbow trout, Salmo gairdneri.J. Fish Biol. 20, 53–68. a great number of taste buds in the oral valves in cardinal Fishelson, L., Delarea, Y., 2004. Taste buds on the lips and mouth of fishes. some blenniid and gobiid fishes: comparative distribution and The free surface of the epithelial cells found at different re- morphology. J. Fish Biol. 65, 651–665. gions such as lips, mouth cavity and gills of different fishes is Fishelson, L., Delarea, Y., Zverdling, A., 2004. Taste bud form and characterized by the presence of a series of microridges. In distribution on lips and in the oropharyngeal cavity of cardinal fish the present investigation, the microridges are organized in dif- species (Apogonidae, Teleostei), with remarks on their dentition. J. ferent ways to form intricate patterns. These structures are Morph. 259, 316–327. thought to be involved in various functions such as absorption, Girgis, S., 1952. The buccopharyngeal feeding mechanism in an secretion, mechanical protection and flexibility. These findings herbivorous bottom-feeding Cyprinoid, Labeo horie (Cuvier). J. may, therefore, confirm the observations of Mittal et al. Morph. 90, 281–315. Golubtsov, A.S., Moots, K.A., Dzerjinskii, 2004. Dentition in the (2004), Yashpal et al. (2006) and El-Bakary (2011). 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