Scanning Electron Microscopic Studies of Gill Arches and Rakers in Relation to Feeding Habits of Some Fresh Water ﬁshes

The Journal of Basic & Applied Zoology (2013) 66, 121–130

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

www.egsz.org www.sciencedirect.com

Scanning electron microscopic studies of gill arches and rakers in relation to feeding habits of some fresh water ﬁshes

E.H. Elsheikh *

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

Received 4 May 2013; revised 26 June 2013; accepted 23 July 2013 Available online 27 August 2013

KEYWORDS Abstract The surface ultrastructure of the gill arches and the gill rakers of the three concerned spe- Pharyngeal cavity; cies Oreochromis niloticus, Chrysichthys auratus and Clarias gariepinus was investigated by scanning SEM; electron microscopy. These structures show significant adaptive modifications associated with the Gill arch; food and feeding habits of these fishes. Short and tuberous type gill-rakers in O. niloticus, are a well Gill raker; interesting filter of food. In C. auratus gill rakers were short with broad base, they serve to strain Taste bud; water which was to bathe the gills and prevent any solid particles from passing over it. Gill rakers Fishes in C. gariepinus were long, cylindrical in shape and arising at acute angles to the arch, they help to strain food and other materials, thus protect gill filaments from damage. Prominent epithelial protuberances on the gill rakers and gill arches enable the taste buds, located at their summit, to project well above the surface of the epithelium. This could increase the efficiency of the taste buds in selective sorting of palatable food. Co-occurrence of teeth and taste buds on the epi-and hypopharyngeal bones (Types I–III) denotes that food processing and gestation occur simultaneously in the pharynx. Caniform, villiform and papilliform teeth on the epi- and hypopharyngeal bones of the three studied species respectively in O. niloticus, C. auratus andC. gariepinus were associated with a complex food-processing cycle. Mucous secretions, oozing through mucous cell openings, provide lubrication facilitating smooth passage of food through the pharynx. ª 2013 Production and hosting by Elsevier B.V. on behalf of The Egyptian German Society for Zoology.

Introduction

Oreochromis niloticus, Chrysichthys auratus and Clarias gariepinus are three of the most important fresh water fishes in * Tel.: +20 01281074849. E-mail address: [email protected]. the River Nile in Egypt. O. niloticus lives almost in inshore Peer review under responsibility of The Egyptian German Society for water and feeds mainly on periphytes and algae while C. aura- Zoology. tus lives in middle water, feeds on insects, crustacean, mollusks, nematodes, fish plants and bottom deposits were of minor importance. C. gariepinus was completely omnivorous, feeding on fish, insect larvae, mollusks, planktonic Production and hosting by Elsevier organisms, water weeds and bottom deposits. 2090-9896 ª 2013 Production and hosting by Elsevier B.V. on behalf of The Egyptian German Society for Zoology. http://dx.doi.org/10.1016/j.jobaz.2013.07.005 122 E.H. Elsheikh

Gills were the main sites of gas exchange in almost all fishes copy, three fishes from each species were used. Pieces of the gill (Moyle and Cech, 1996). In addition to their respiratory func- arches and gill rakers were taken, fixed in 10% formalin. This tion, the gills play an important role in the excretion of certain procedure was followed by a second fixation in 1% osmium waste products and in the maintenance of the fish salt balance tetroxide (Delton, 1955) for at least 6 h, washing and dehydra- (Norman, 1963). The gill dimensions and organization of gill tion in increasing concentrations of ethanol. The dehydration arches and rakers reflect the feeding habits of the fish samples were dried with the critical point drier Tousimis (Magnuson and Heitz, 1971; Hughes, 1980, 1984; Fernandes Audosamdri-815. The dried material was coated by gold and Rantin, 1986; Fernandes et al., 1995; Fernandes, 1996). sputter coater (SPI-Module) and samples examined by Among fishes, diversity of the food resources leads to the JEOL-JSM-5500 LV reflection scanning electron microscopy. evolution of various adaptive characters in the pharynx, which The material was stored over silica gel, so that it remained in plays an indispensable role in the retention, maneuvering and perfect condition for many weeks. transport of food for swallowing. The pharynx, in teleost, was characterized by the presence of gill arches. These were located Results at the boundary between the pharyngeal cavity and the opercular chamber on either side of the head. The gill arches in gen- The gill system in the three species, O. niloticus, C. auratus and eral were equipped with gill rakers toward their pharyngeal C. gariepinus had the form of a triangular mass with a caudally side and were considered to play an important role in feeding. directed base. The gill system consisted of four pairs of gills, A review of literature revealed that, the surface ultrastructure which were termed from lateral to medial as first (I), second of gill arches and gill rakers was derived from studies on fish (II), third (III) and fourth (IV) as shown in Figs. 1–3. In addi- species having different feeding habits that include plankton tion, C. gariepinus had a rudimentary fifth gill. feeder Rhinomugil corsula (Munshi et al., 1984), and Gadusia Each gill was semilunar in shape consisting of a gill arch chapra (Ghosh et al., 1988); filter feeder Brevoortia tyrannus that carried gill rakers on its concave aspect and gill filaments (Friedland, 1985); ilyophagous (periphyton feeder) Hyposto- on its convex aspect. The gill arch had two extremities; rostral mus commersonii (Eiras-Stofella and Charvet-Almeida, 1997), and caudal. The rostral extremity of each gill arch joined that Prochilodus scorfa (Eiras-Stofella and Charvet-Almeida, of the opposite side in a transverse median bridge. The bridges 1998), Mugil curema, Mugil liza and Mugil platanus (Eiras-Sto- of the gill arches united together forming an inter-branchial fella et al., 2001); omnivorous Fundulus heteroclitus and (Hoss- septum between the contra-lateral gills. This septum was flat- ler et al., 1985), Cyprinus carpio (Sibbing and Uribe, 1985; tened dorso-ventrally. The gills of both sides diverged caudo- Sibbing, 1988), and carnivorous fishes Anabas testudineus laterally leaving a triangular shaped area which was bounded (Munshi et al., 1984), Notopterous chitala (Ghosh et al., rostro-laterally, by the fourth pair of gills and was occupied 1988), Eugerres brasilianus (Eiras-Stofella and Charvet-Almei- by the floor of the pharynx. This floor was modified into da, 2000), and Cathorops strigosa (Fernandes et al., 2003). two distinct structures; hypo-pharyngeal bone (an anterior Kumari et al. (2005) described surface ultrastructure of gill ar- post-lingual organ) and lower pharyngeal jaw (a posterior ches and gill rakers in relation to the feeding ecology of a car- edentulous epithelium). The roof of the pharynx, opposite to nivorous catfish Rita rita. Vigliano et al. (2006) described the the lower pharyngeal jaw, was modified into an oval-shaped ultrastructural characterization of gills in Juveniles of the structure, the epi-pharyngeal bone (the chewing pad) covering argentinian silverside Odontesthes bonariensis. Also Pichugin the basioccipital region of the skull. The caudal extremities of and Sidorov (2006) explained the number and form of gill rak- the four gill arches curved dorsally, rostrally and slightly ers in Sakhalin trout Parahucho perryi. Mir and Channa (2009) used the SEM study to explain the gills of the snow Trout Schizothorax curvifrons Heckel. Kumari et al. (2009) described surface ultrastructure of gill arches and gill rakers in relation to feeding in a herbivorous bottom feeder fish of an Indian major carp Cirrhinus mrigala. Also Kumari et al. (2011) described the surface ultrastructure of the gill filaments and the secondary lamellae of the carp C. mrigala. The present study aimed to give more scanning electron microscopical information about the gill system of three species of fresh water fishes with different feeding habits which inhabit the River Nile; O. niloticus, C. auratus and C. gariepinus.

Material and methods

This study was carried out on fishes of O. niloticus, C. auratus and C. gariepinus. The length of fishes is 2, 7 and 5 cm, respectively. Five fishes from each species were used to demonstrate the gross morphological features. The opercular cavity was Figure 1 Scanning electron photomicrograph of Oreochromis opened; the specimens were washed very carefully in niloticus; showing four gill arches (A), numbered I–IV from lateral physiological saline (Breipohl et al., 1973a,b) to remove the to medial and gill rakers (R) which are arranged in two rows mucus on the surface and then fixed in 10% formalin, exam- lateral (L) and medial (M). The gill rakers appeared short, wide- ined grossly and photographed. For scanning electron micros- based and with tuberous end. Scanning electron microscopic studies of gill arches and rakers in relation to feeding habits of some fresh water fishes 123

Figure 2 Scanning electron photomicrograph of Chrysichthys auratus; showing four gill arches (A), numbered I–IV from lateral to medial and gill rakers (R) which are arranged in two rows lateral (L) and medial (M), which appeared short with broad-base Figure 4 Scanning electron photomicrograph of Oreochromis and processes with segmented tuberous end. niloticus; showing the surface epithelium of the gill arches. Arrow indicates microridges, thick arrow indicates microbridges and double arrow indicates mucous cells.

in Figs. 5 and 6). The boundaries between adjacent epithelial cells were demarcated by a well-defined double row of microridges (Figs. 4–6). The adjoining microridges on each epithelial cell were often interconnected with fine transverse connections, Viz., the microbridges (Figs. 4–6). In addition, mucous cells were scattered in between the arch epithelial cells, these cells were more numerous in C. auratus and C. gariepinus than in O. niloticus. These mucous cells were often filled with blobs of mucous secretion as shown in Figs. 4–6. In the investigated fish species the gill rakers differed in form, arrangement and length. In O. niloticus, they were arranged in two rows, medial and lateral. The rakers of the medial row were directed dorso-medially while those of the lateral row were directed dorso-laterally (Fig. 7). The rakers of Figure 3 Scanning electron photomicrograph of Clarias gariepinus; showing five gill arches(A), numbered I–V from lateral to medial and gill rakers (R) which are arranged in three rows (white arrow); lateral (L), intermediate (I) and medial (M). The gill raker is long, cylindrical in shape arising at acute angles to the arch. Its free end is curved rostrolaterally. ventrally where they are connected with each other. These arches were attached to the medial aspect of the operculum and the dorsolateral wall of the pharynx. In the three species, the gaps between the gill arches were generally wider in C. gariepinus than in O. niloticus and C. auratus, while in C. auratus these gaps were wider than in O. niloticus (Figs. 1–3). It was found that, the epithelium covering the gill arches of the three studied species demonstrated a mosaic of variable dimensions. The exposed surfaces of the epithelial cells were covered by microridges. These, in general, appear uniform in width and have a smooth surface, sinuous, or at times straight Figure 5 Scanning electron photomicrograph of Chrysichthys and compactly arranged (as in O. niloticus as shown in Fig. 4), auratus; showing the surface epithelium of the gill arches. Arrow lying parallel to each other or irregularly interwoven to form indicates microridges, thick arrow indicates microbridges and web like patterns (as in C. auratus and C. gariepinus as shown double arrow indicates mucous cells. 124 E.H. Elsheikh

Figure 6 Scanning electron photomicrograph of Clarias gariepi- Figure 8 Scanning electron photomicrograph of Chrysichthys nus; arrow indicates microridges, thick arrow indicates micro- auratus; showing gill rakers (R), which appeared short with broad- bridges, white arrow indicates deep invaginations and double base and processes with segmented tuberous end. arrow indicates mucous cells.

Figure 9 Scanning electron photomicrograph of Clarias gariepi- Figure 7 Scanning electron photomicrograph of Oreochromis nus; showing a higher magniﬁcation of gill arch(A) and gill rakers niloticus; showing gill arch (A) and gill rakers (R) which are (R). The gill rakers are arranged in three rows; lateral (L), arranged in two rows lateral (L) and medial (M). The gill rakers intermediate (I) and medial (M). The gill rakers are cylindrical in appeared short, wide-based and with tuberous end. The arch bears shape arising at acute angles to the arch. Its free end is curved group of taste buds (arrow). rostrolaterally.

intermediate row were few and short (Figs. 3 and 9). The rak- the adjacent gills were interdigitated (Fig. 1). The gaps between ers of the lateral row were present in all gills including the fifth the rakers of the same gill decreased to the epibranchial part. one, while those of the medial row were found only in the third The rakers appeared as relatively short, and wide-based pro- and fourth gills, being longer in the third one. The rakers of the cessed with tuberous ends (Fig. 7). intermediate row were found in the four main gills; they were It has been noted that the gill rakers in C. auratus, were ar- best developed in the third gill and were the weakest in the first ranged in two rows, medial and lateral (Fig. 3). The rakers of one. The rakers of the third, fourth and fifth gills were interdig- the medial row were directed ventro-medially, while those of itated (Fig. 3). The gaps between the rakers of the same gill the lateral row were directed ventro-laterally. The rakers decreased to the epibranchial part. The rakers appeared as of the adjacent gills were interdigitated (Fig. 2). The gaps be- cylindrical in shape arising at acute angles to the arch. Their tween the rakers of the same gill were equal in length. The rak- free ends were curved rostro-laterally as shown in Figs. 3 ers appeared as relatively short and broad-based processed and 9. with segmented tuberous ends (Fig. 8). The epipharyngeal bone (chewing pad) was divided into In C. gariepinus, they were arranged in three rows; medial, two rounded or oval structures as shown in Figs. 10–12 in intermediate and lateral (Figs. 3 and 9). The rakers of the the three concerned species. Each lobe appeared like half of medial and lateral rows were numerous with long processes a chewing pad with its surface bearing teeth amid epithelial arising from both sides of the gill arch, while those of the protuberances. Scanning electron microscopic studies of gill arches and rakers in relation to feeding habits of some fresh water fishes 125

Figure 10 Scanning electron photomicrograph of Oreochromis Figure 12 Scanning electron photomicrograph of Clarias gari- niloticus; showing the epipharyngeal bone (chewing pad). The epinus; showing a higher magniﬁcation of the chewing pad bearing anterior region is narrow and the posterior region is wide and taste buds of Types I and II (arrow) and papilliform teeth (thick bifurcated into two lobes (black arrow). The pores of the taste arrow). buds of type III (white arrow) lie within the epithelia between the rows of caniform teeth (thick arrow).

In O. niloticus, the teeth were caniform and the taste buds were of Type III (Figs. 13 and 16). In C. auratus, the teeth were villiform (Figs. 14 and 17). They were elongated, stout and conical with sharp pointed ends. The taste buds were of Types I and II (Figs. 18 and 19), respectively. In C. gariepinus, the teeth were papilliform (Figs. 15 and 20). They were elongated, with sharp pointed ends. The taste buds were of Types I and II (Fig. 20), respectively. The posterior region of the hypopharyngeal bone was known as the lower pharyngeal jaw. It was a narrow zone of edentulous epithelium as shown in the three species studied (Figs. 13–15).

Figure 11 Scanning electron photomicrograph of Chrysichthys auratus; showing the chewing pad, which formed of two lobes (thick arrow), bearing taste buds of Types I and II (white arrow) and villiform teeth (double arrow).

It has been noted that, in O. niloticus, the teeth were caniform (Fig. 10). The taste buds were of Type III, which do not project above the normal level of the neighboring epithelial cells as epithelial pores (Fig. 10). Whereas, in C. auratus and C. gariepinus, the pharyngeal teeth were villiform and papilliform respectively. Moreover, in the previous two species the taste buds were of Types I and II (Figs. 11 and 12). The hypopharyngeal bone (post-lingual organ and lower pharyngeal jaw) was distinguished into an anterior and a posterior region. The anterior region of the post-lingual organ was elongated and narrow. It widened gradually toward the poster- Figure 13 Scanning electron photomicrograph of Oreochromis ior region, which appeared somewhat triangular in outline niloticus; showing hypopharyngeal bones bearing caniform teeth (Figs. 13–15). The surfaces of the post-lingual organ were stud- (arrow) and taste buds of Type III (thick arrow) on the pharyngeal ied with teeth and a large number of taste buds, interspersed surfaces. Note a narrow zone of edentulous epithelium (white among the teeth. arrow). 126 E.H. Elsheikh

Figure 14 Scanning electron photomicrograph of Chrysichthys Figure 16 Scanning electron photomicrograph of Oreochromis auratus; showing hypopharyngeal bones bearing villiform teeth niloticus; showing hypopharyngeal bones bearing caniform teeth (arrow) and taste buds of Types I and II (thick arrow) on the (arrow) and taste buds of Type III (thick arrow) on the pharyngeal pharyngeal surfaces. Note a narrow zone of edentulous epithelium surfaces. Also showing the lower pharyngeal jaw or the edentulous (white arrow) between the bones. epithelium (white arrow).

Figure 15 Scanning electron photomicrograph of Clarias gari- Figure 17 Scanning electron photomicrograph of Chrysichthys epinus; showing hypopharyngeal bones bearing papilliform teeth auratus; showing a higher magniﬁcation of the hypopharyngeal (arrow) and taste buds of Types I and II (thick arrow) on the bones bearing villiform teeth (arrow) and taste buds of Types I pharyngeal surfaces. Note a narrow zone of edentulous epithelium and II (thick arrow). (white arrow) between the bones.

in herbivorous filter feeding, reported that the branchial sieve Discussion is made of short gill rakers, while those of zooplanktivorous fishes were long. Ojha et al. (1987) in plankton feeder mullet In the present investigation, the gill arches and gill rakers show R. corsula and Sicamugil cascasia; Guinea and Fernandez significant adaptive modifications, associated with the food (1992) in filter-feeders (four species of mullet), Liza aurata, and feeding ecology of the studied fishes. Liza saliens, Liza ramada and Chelon labrosus and Eiras-Sto- As most bony fishes, the three studied species possess four fella et al. (2001) in periphyton feeder M. curema, M. liza pair of gills. Although C. gariepinus has a rudimentary fifth and M. platanus, reported gill rakers with secondary and gill, without gill filaments. Each gill is formed of a curved gill tertiary structures to increase the efficiency of filtering mecha- arch carrying gill rakers on its concave aspect and gill filaments nism and the position and morphology of gill rakers in these on its convex surface. fishes act as a selective screen preventing the entrance of large In O. niloticus, the gill rakers were generally short and and undesirable organisms. widely spaced. The gill rakers could be considered to constitute The middle feeder C. auratus is able to expand its pharyn- the branchial sieve as an adaptation for the efficient filtering of geal cavity, thus accommodating large quantities of food or small food particles in the water gulped by the fish. Hyatt large size food items including mollusks, small fishes, crusta- (1979), Hoogenboezem et al. (1991) and Kumari et al. (2009) ceans, and insects. The arrangement of relatively short and Scanning electron microscopic studies of gill arches and rakers in relation to feeding habits of some fresh water fishes 127

Figure 18 Scanning electron photomicrograph of Chrysichthys Figure 20 Scanning electron photomicrograph of Clarias gari- auratus; showing a higher magniﬁcation of epithelial protuber- epinus; showing a higher magniﬁcation of the papilliform teeth in ances on the hypopharyngeal bones bearing Type I taste buds the hypopharyngeal bones (arrow) and taste buds of Types I and which are present in groups (arrow). II (thick arrow).

(1991), in an experimental study, noticed that the rakers act as a barrier to water flow rather than as a sieve. They change the direction of the water toward the roof of the oral cavity where food particles were trapped by its mucous covering be- fore being ingested. It is suggested that the gill rakers perform a dual function; they change the direction of the water as a first step and act as a sieve in a second step. The characteristic surface feature of the epithelial cells covering the gill arch and gill rakers in the three studied species is the presence of the microridges forming intricate patterns. These surface structures have also been reported in epithelia of gill arches and gill rakers in several fish species (Hossler et al., 1985; Ojha et al., 1987; Eiras-Stofella, 1994; Eiras-Stofella and Charvet-Almeida, 1998; Eiras-Stofella et al., 2001; Evans et al., 2005; Kumari et al., 2005, 2009, 2011). More recently, these microridges have been suggested to enhance mechanical flexibility and protection (Olson, Figure 19 Scanning electron photomicrograph of Chrysichthys 1995) and to impart a firm consistency to the free surface of auratus; showing a higher magnification of epithelial protuber- the epithelial cells (Mittal et al., 2004). Microbridges were of- ances on the hypopharyngeal bones bearing Type II taste bud with ten interconnecting together, that may enhance their consis- sensory protrusions projecting from the surface (arrow). tency or rigidity as suggested by Mittal et al., (2004) in their description of the opercular epidermis of Lepidocephalichthys guntea. broad base gill-rakers, serves to strain water which is to bathe In the present investigation, taste buds were present in a the gills and prevent any solid particles from passing over it. great number on the pharyngeal side of the gill arches and Magnuson and Heitz (1971), Durbin (1979) and White and on the gill rakers as well as on the epi and hypopharyngeal Bruton (1983) postulated that the number and shape as well as bones may be associated with their involvement in gestation spacing of rakers reflect the feeding habits of different fish spe- in the pharynx. These structures show significant adaptive cies. In this respect, C. gariepinus gill rakers were long, narrow modifications associated with the food and feeding ecology spaced and cylindrical in shape, arising at acute angles to the of the fishes. Prominent epithelial protuberances on the gill arch that helps to strain food and other materials as well as rakers and the gill arches enable the taste buds, located at their protect gill filaments from damage. The gill rakers were ar- summit, to project well above the surface of the epithelium. ranged in three rows; medial, intermediate and lateral. The This could increase the efficiency of the taste buds in selective structures of the intermediate gill rakers show significant adap- sorting of palatable food. Surface specializations of the post- tive modifications associated with the food and feeding ecology lingual organ were recognized with adaptive modifications of the fish, which serve as taste buds. This could increase the for selecting, trapping or holding food particles. Taste buds efficiency of the fish in selective, sorting of palatable food. Fur- have also been reported on the pharyngeal side of the gill thermore, Drenner et al. (1978) have assumed that gill rakers rakers and the gill arches in the carnivore Brachydanio rerio operate as passive sieves, retaining only those particles larger (Karlsson, 1983) and in F. heteroclitus (Hossler et al., 1985), than a given inter-raker spacing. However, Sanderson et al. mainly on the gill arches rather than the gill rakers in the car- 128 E.H. Elsheikh nivore N. chitala, on the gill rakers in the plankton feeder G. species may be involved in lubrication, assisting the smooth chapra and in the herbivore Labeo rohita (Ghosh et al., passage of food items through the pharynx, thus protecting 1988) and on the periphyton feeder M. curema, M. liza, and the epithelium from mechanical injury. The role of mucous M. platanus (Eiras-Stofella et al., 2001), and the carnivorous secretions in the lubrication of food during its passage in the Rhinelepis strigosa (Fernandes et al., 2003). More recently, gut in different fish species is widely accepted (Ezeasor and Eiras-Stofella and Charvet-Almeida (2000) and Eiras-Stofella Stokoe, 1980; Martin and Blaber, 1984; Anderson, 1986; Sinha and Fank-de-Carvalho (2002) observed taste buds on the gill and Chakrabarti, 1985; Park and Kim, 2001; Podkowa and rakers and the pharyngeal side of gill arches of ilyophagous Goniakowska-Witalinska, 2003; Yashpal et al., 2006; Kumari P. scrofa and the omnivorous E. brasilianus andCathorops spi- et al., 2005, 2009). Mucus in different fish species has also been xii, respectively. They suggested that the chemical receptors considered to play an important role in various food-process- might be used to help in food selection at swallowing. Kumari ing activities. These include absorption (Ezeasor and Stokoe, et al., 2005 in carnivorous fish R. rita, recorded the presence of 1980; Grau et al., 1992), lubrication of occluding tooth sur- a great number of taste buds on the pharyngeal side of the gill faces of the pharyngeal mill (Tibbetts, 1992), pregastric diges- arches, on the gill rakers and on the epi and hypopharyngeal tion (Murray et al., 1994), extraction of nutrients from plant bones. While, Kumari et al., 2009 in a herbivorous fish C. mri- material digested by fish (Tibbetts, 1997), reduction of adhe- gala the presence of a great number of taste buds on the gill sion, thereby ensuring their continued effectiveness (Tibbetts rakers, median ridges, and transverse flap-like septa between and Carseldine, 2003). the gill as well as on the postlingual organ and chewing pad The present work ascertains the mucous nature of the gill insure their role in food selection. surface epithelium. The presence of more mucous cells in the Occurrence of a great number of taste buds together with epithelium of C. auratus, and C. gariepinus than in O. niloticus, teeth on the epi-and hypopharyngeal bones in the three studied indicates a high mucous secreting character of the gills in these species suggests that food processing and gestation work species. This mucous nature is important not only as a protec- simultaneously in the pharynx and this may serve in the final tive barrier, but also has an ion regulatory function. This fact determination of the suitability of potential food items prior explains why C. auratus, and C. gariepinus survive longer to swallowing, as proposed by Linser et al. (1998) in Micropte- outside water. rus salmoides. Co-occurrences of teeth and taste buds within the pharyngeal cavity have also been reported in a variety of fish species (Reutter et al., 1974; Ezeasor, 1982; Sibbing, Acknowledgments 1982; Hossler and Merchant, 1983; Hossler et al., 1986; Northcott and Beveridge, 1988; Kumari et al., 2005, 2009). I thank Prof. A.E. EL-Attar, professor of comparative Slightly curved caniform, villiform and stout papilliform anatomy, Faculty of science, Zagazig University for his team’s teeth on the epi and hypopharyngeal bones in the three studied interest in critically going through the manuscript and making species respectively (O. niloticus, C. auratus, and C. gariepinus), many valuable suggestions. can be associated with a complex food processing cycle. Liem (1986) and Drucker and Jensen (1991) showed that during the References process of mastication or winnowing, surface debris is stripped from food particles and unpalatable material is fully dislodged Anderson, T.A., 1986. Histological and cytological structure of the as the food passes into the esophagus. Lauder (1983) reported gastrointestinal tract of the luderick, Girella tricuspidata (Pisces, that the pharyngeal jaw in Lepomis microlophus and Lepomis Kyphosidae), in relation to die. J. Morphol. 190, 109–119. gibbosus, is equipped with molariform teeth as an adaptation Breipohl, W., Bijvank, G.J., Zippel, H.P., 1973a. Rastermikro-skopi- to crush the snails which they feed on. Linser et al. (1998) sche untersuchungen der olfaktorischen rezeptoren im riechepithel reported the presence of straight and curved caniform pharyn- des goldfisches (Carassius auratus). Z. Zellforsch. 138, 439–454. geal teeth in piscivorous M. salmoides, and suggested that Breipohl, W., Bijvank, G.J., Zippel, H.P., 1973b. Die oberfla- those were more suitable for piercing flesh and removing scales chenstruktur der olfaktorischen drusen des goldfisches (Carassius than for crushing very hard objects such as snails. Tibbetts and auratus). Eine rastermikroskopische studie. Z. Zellforsch. 140, 567– Carseldine (2003), while describing the anatomy of the pharyn- 582. Delton, A.J., 1955. A chrome-osmium fixative for electron microscopy. geal mill in the herbivorous Arrhamphus sclerolepis krefftii, Anat. Rec., 121–281. suggested a model of pharyngeal jaw apparatus activity to Drenner, R.W., Strickler, J.R., O’Brien, W.J., 1978. Capture tentatively explain the sequence of treatment of food. This probability: the role of zooplankter escape in the selective included shredding, grinding of food, and rupturing cells of feeding of planktivorous fish. J. Fish. Res. Board of Canada 35, the tissues to release their contents. A high degree of macera- 1370–1373. tion derived from the activity of the pharyngeal jaw apparatus Drucker, E.G., Jensen, J.S., 1991. Functional analysis of a speciali-zed in different fish species was also reported by Kumari et al. prey processing behavior: winnowing by surfperches (Teleostei: (2005) in R. rita, they found villiform and caniform teeth in Embiotocidae). J. Morphol. 210, 267–287. the epi-and hypopharyngeal bones. Recently, Kumari et al. Durbin, A.G., 1979. Food selection by plankton feeding fishes. In: (2009) concluded the molariform teeth bone on the lower Clepper, H. (Ed.), Predator-Prey Systems in Fisheries Manage- ment. Sport Fishing Institute, Washington, DC, pp. 203–218. pharyngeal jaw of C. mrigala and a series of extensive regularly Eiras-Stofella, D.R., 1994. Variabilidade morfologica da regiao spaced ridges on the free surface of the chewing pad act as an faringea dos arcos branquiais de algumas species de peixes efficient pharyngeal mill in crushing, grinding and mastication (Teleostei), estudada atraves da microscopia eletronica de varreura. of food. Departamento de Zoologia, Universidade Federal do Parana, Mucus elaborated by mucous cells in the epithelium cover- Curitiba, Tese de Doutorado. ing the gill arches and the gill rakers of the three concerned Scanning electron microscopic studies of gill arches and rakers in relation to feeding habits of some fresh water fishes 129

Eiras-Stofella, D.R., Charvet-Almeida, P., 1997. Gills of the freshwa- Hossler, F.E., Harpole, J.H.J.R., King, J.A., 1986. The gill arch of ter fish Hypostomus commersoni Val., 1840 (Loricariidae) analyzed striped bass Morone saxatilis. I. Surface ultrastructure. J. Submi- through electron microscopy techniques. Braz. Arch. Biol. Technol. crosc. Cytol. 18, 519–528. 40, 785–792. Hughes, G.M., 1980. Morphometry of fish gas exchange in relation to Eiras-Stofella, D.R., Charvet-Almeida, P., 1998. Ultrastructure (SEM) their respiratory function. In: Ali, M.A. (Ed.), Environmental of the gills of Prochilodus scrofa steindachner (Pisces, Teleostei). Physiology of Fishes. Plenum Press, New York, pp. 33–56. Rev. Bras. Zool. 15, 279–287. Hughes, G.M., 1984. General anatomy of gills. In: Hoar, W.S., Eiras-Stofella, D.R., Charvet-Almeida, P., 2000. Gill scanning images Randall, D.J. (Eds.), Fish Physiology. Academic Press, New York, of the seawater fish Eugerres brasilianus (Gerreidae). Braz. Arch. pp. 1–72. Biol. Technol. 43, 421–423. Hyatt, K.D., 1979. Feeding strategy. In: Hoar, W.S., Randall, D.J., Eiras-Stofella, D.R., Fank-de-Carvalho, S.M., 2002. Morphology of Brett, J.R. (Eds.), . In: Fish Physiology, vol. VIII. Academic Press, gills of the seawater fish Cathorops spixii (Agassiz) (Ariidae) by New York. scanning and transmission electron micros-copy. Rev. Bras. Zool. Karlsson, L., 1983. Gill morphology in the zebrafish, Brachydanio rerio 19, 1215–1220. (Hamilton-Buchanan). J. Fish Biol. 23, 511–524. Eiras-Stofella, D.R., Charvet-Almeida, P., Fanta, E., Vianna, A.C.C., Kumari, U., Yashpal, M., Mittal, S., Mittal, A.K., 2005. Morpho-logy 2001. Surface ultrastructure of the gills of the mullets Mugil of the pharyngeal cavity, especially the surface ultrstructure of gill curema, M. liza and M. platanus (Mugilidae, Pisces). J. Morphol. arches and gill rakers in relation to the feeding ecology of the 247, 122–133. catfish Rita rita (Siluriformes, Bagridae). J. Morphol. 265, Evans, D.H., Piermarini, P.M., Choe, K.P., 2005. The multifunc- 197–208. tional fish gill: dominant site of gas exchange, osmoregulation, Kumari, U., Yashpal, M., Mittal, S., Mittal, A.K., 2009. Surface acid-base regulation, and excretion of nitrogenous waste. Physiol. ultrastructure of gill arches and gill rakers in relation to feeding of Rev. 85, 97–177. an Indian major carp, Cirrhinus mrigala. Tissue Cell 41, Ezeasor, D.N., 1982. Distribution and ultrastructure of taste buds in 318–325. the oropharyngeal cavity of the rainbow trout, Salmo gairdneri.J. Kumari, U., Mittal, S., Mittal, A.K., 2011. Surface ultrast -ructure of Fish. Biol. 20, 53–68. the gill filaments and the secondary lamellae of the cat–fish, Rita Ezeasor, D.N., Stokoe, W.M.A., 1980. Cytochemical, light and rita and the carp, Cirrhinus mrigala. Microsc. Res. Tech. 29. electron microscopic study of the eosinophilic granule cells in the Lauder, G.V., 1983. Functional and morphological bases of trophic gut of the rainbow trout, Salmo gairdneri Richardson. J. Fish. Biol. specialization in sunfishes (Teleostei, Centrarch- idae). J. Morphol. 17, 619–634. 178, 1–21. Fernandes, M.N., 1996. Morpho-functional adaptations of gills in Liem, K.F., 1986. The pharyngeal jaw apparatus of the Embiotoci- dae tropical fish. In: Val, A.L., Almeida-Val, V.M.F., Randall, D.J. (Teleostei): a functional and evolutionary perspective. Copeia, 311– (Eds.), Physiology and Biochemistry of Fishes of the Amazon. 323. INPA, Manaus, pp. 181–190. Linser, P.L., Carr, W.E.S., Cate, H.S., Derby, C.D., Netherton III, Fernandes, M.N., Rantin, F.T., 1986. Gill morphology of Cichlid fish. J.C., 1998. Functional significance of the co-localization of taste Oreochromis (Sarotherodon) niloticus (Pisces, Teleo-stei). Cienciae buds and teeth in the pharyngeal jaws of the large-mouth bass, Cult. 38, 192–198. Micropterus salmonides. Biol. Bull. 195, 273–281. Fernandes, M.N., Perma, S.A., Santos, C.T.C., Severi, W., 1995. The Magnuson, J.J., Heitz, J.G., 1971. Gill raker apparatus and food gill filament muscles in two Loricariid fish (genus Hypostomus and selectivity among mackerels, tunas and dolphins. Fish. B NOAA Rhinelepis). J. Fish. Biol. 46, 1082–1085. 69, 361–370. Fernandes, M.N., Castro, F.J., Mazon, A.F., 2003. Scanning electron Martin, T.J., Blaber, S.J.M., 1984. Morphology and histology of the microscopy of the gill raker of the Loricariid fish, Rhinelepis alimentary tracts of Ambassidae (Cuvier) (Teleostei) in relation to strigosa. Acta Microsc. 12, 511–512. the feeding. J. Morphol. 182, 295–305. Friedland, K.D., 1985. Functional morphology of the branchial basket Mittal, S.P., Mittal, A.K., 2004. Operculum of peppered loach, structures associated with feeding in the Atlantic Menhaden, Lepidocephalichthys guntea (Cobitidae, Cypriniformes): A scan- Brevoortia tyrannus (Pisces: Clupeidae). Copiea, 1018–1027. ning electron microscopic and histochemical investigation. Belg. J. Ghosh, T.K., Singh, O.N., Roy, P.K., Munshi, J.S.D., 1988. Zool. 134, 9–15. Morphometrics and surface ultrastructure of gill rakers of three Mir, I.H., Channa, A., 2009. Gills of the snow trout, Schizothorax Indian teleostean fishes. Proc. Indian Natl. Sci. Acad. B54, 331– curvifrons Heckel: A SEM study. Pak. J. Biol. Sci. 12 (23), 1511– 336. 1515. Grau, A., Crespo, S., Saraquete, J.S.D., Gonzalez, De., Canales, Moyle, P.B., Cech, J.J., 1996. Fishes: an introduction to Ichthyology, M.L., 1992. The digestive tract of the amberjack Seriola dumerili. third ed. Prentice Hall, Upper Saddle River, New Jersey. Risso: a light and scanning electron microscope study. J. Fish Biol. Murray, H.M., Wright, G.M., Goff, G.P., 1994. A study of the 41, 287–303. posterior esophagus in the winter flounder, Pleuronectes americ- Guinea, J., Fernandez, F., 1992. Morphological and biometrical study anus and the yellowtail flounder, Pleuronectes ferrugineus: mor- of the gill rakers in four species of mullet. J. Fish. Biol. 41, 381–397. phological evidence for pregastric digestion? Can. J. Zool. 72, Hoogenboezem, W., Van den Boogaart, J.G.M., Sibbing, F.A., 1191–1198. Lammens, E.H.R.R., Terlouw, A., Osse, J.W.M., 1991. A new Munshi, J.S.D., Ojha, J., Gosh, T.K., Roy, P.K., Mishra, A.K., 1984. model of particle retention and branchial sieve adjustment in filter- Scanning electron microscopic observation on the structure of gill feeding bream (Abramis brama, Cyprinidae). Can. J. Fish. Aquat. rakers of some fresh water teleostean fishes. Proc. Indian Natl. Sci. Sci. 48, 7–18. Acad. B50, 549–554. Hossler, F.E., Merchant, L.H., 1983. Morphology of taste buds on the Norman, J.R., 1963. History of Fishes, second ed., Geenwood, P.H., gill arches of the mullet, Mugil cephalus, and the Killifish Fundulus (Ed.). Perna, S.A., Fernandes, M.N., 1996. Gill morphometry of a heteroclitus. Am. J. Anat. 166, 299–312. facultative air-breathing Loricariid fish, Hypostomus plecostomus Hossler, F.E., Musil, G., Karnaky Jr., K.J., Epstein, F.H., 1985. (Walbaum) with special emphasis to aquatic respiration. Fish Surface ultrastructure of the gill arch of the Killifish, Fundulus Physiol Biochem., 15, 213–220. heterclitus from sea water and freshwater, with special reference to Northcott, M.E., Beveridge, M.C.M., 1988. The development and the morphology of apical crypts of chloride cells. J. Morphol. 185, structure of pharyngeal apparatus associated with filter feeding in 377–386. tilapias (Oreochromis niloticus). J. Zool. 215, 133–149. 130 E.H. Elsheikh

Ojha, J., Mishra, A.K., Munshi, J.S.D., 1987. Interspecific variations Sibbing, F.A., Uribe, R., 1985. Regional specialisations in the in the surface ultrastructure of the gills of freshwater mullets. Jpn. oropharyngeal wall and food processing in the carp (Cyprinus J. Ichthyol. 33, 388–393. carpio L.). Neth. J. Zool. 35, 377–422. Olson, K.R., 1995. Scanning electron microscopy of fish gill. In: Datta Sinha, G.M., Chakrabarti, P., 1985. On topological character- istics of Munshi, J.S., Dutta, H.M. (Eds.), Fish Morphology: Horizon of the mucosal surface in the buccopharynx and intestine of an Indian New Research. Oxford and IBH publishing Co. Pvt. Ltd., New freshwater major carp, Catla catla: a light and scanning electron Delhi, pp. 31–45. microscopic study. Zool. J. B. (Anat.) 113, 375–389. Park, J.Y., Kim, I.S., 2001. Histology and mucin histochemistry of the Tibbetts, I.R., 1992. The trophic ecology, functional morphology and gastrointestinal tract of the mud loach, in relation to respiration. J. phylogeny of the Hemiramphidae (Beloniformes). Ph. D. thesis, Fish Biol. 58, 861–872. University of Queensland, Australia. Pichugin, M.YU., Sidorov, L.K., 2006. On the number and form of gill Tibbetts, I.R., 1997. The distribution and function of mucous cells and rakers in Sakhalin trout Parahucho perryi. J. Ichthyol. vol. 46 (1), their secretions in the alimentary tract of Arrhamphus sclerolepis 133–135. krefftii. J. Fish Biol. 50, 809–820. Podkowa, D., Goniakowska-Witalinska, L., 2003. Morphology of the Tibbetts, I.R., Carseldine, L., 2003. Anatomy of a hemiramphid air-breathing stomach of the catfish Hypostomus plecostomus. J. pharyngeal mill with reference to Arrhamphus sclerolepis krefftii Morphol. 257, 147–163. (Steindachner) (Teleostei: Hemiramphidae). J. Morphol. 255, 228– Reutter, K., Breipohl, W., Bijvank, G.J., 1974. Taste buds type in 243. fishes. II. Scanning electron microscopical investigations on Vigliano, F.A., Aleman, N., Quiroga, M.I., Nieto, J.M., 2006. Xyphophorus helleri (Poecillidae, Cyprinodontiformes, Teleostei). Ultrastructural characterization of gills in juveniles of the Argen- Cell Tissue Res. 153, 151–164. tinian silverside, Odontesthes bonariensis (Valenciennes, 1835) Sanderson, S.L., Cech, J.J., Patterson, M.R., 1991. Fluid dynamics in (Teleostei: Atheriniformes). Anat. Histol. Embryol. 35, suspension-feeding blackfish. Science 251, 1346–1348. 76–83. Sibbing, F.A., 1982. Pharyngeal mastication and food transport in the White, P.N., Bruton, M.N., 1983. Food and feeding mechanisms of carp (Cyprinus carpio): a cineradiographic and electron micro- Gilchristella aestuarius (Pisces: Clupeidae). S. Afr. J. Zool. 18, 31– graphic study. J. Morphol. 172, 223–258. 36. Sibbing, F.A., 1988. Specializations and limitations in the utilize- ation Yashpal, M., Kumari, U., Mittal, S., Mittal, A.K., 2006. Surface of food resources by the carp, Cyprinus carpio: a study of oral food architecture of the mouth cavity of a carnivorous fish Rita rita processing. Environ. Biol. Fish 22, 161–178. (Siluriformes, Bagridae) Belg. J. Zool. 136 (2), 155–162.