Journal of the Persian Gulf (Marine Science)/Vol. 6/No. 19/March 2015/08/59-66

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1 Journal of the Persian Gulf (Marine Science)/Vol. 6/No. 19/March 2015/08/59-66 Anatomy and Histology of the Stomach and Pyloric Caeca in Mugilidae, Liza aurata (Risso, 1810), L. abu (Heckel, 1843) and Mugil cephalus (Linnaeus, 1758) Khayyami, Huseyn; * Zolgharnein, Hossein; Salamat, Negin; Movahedinia, Abdolali Deptement of Marine Biology, Faculty of Marine Science, Khorramshahr University of Marine Science and Technology, Khoramshahr, IR Iran Received: December 2014 Accepted: March Journal of the Persian Gulf. All rights reserved. Abstract Alimentary canal of fishes has a great variety of structural Peculiarities which are important in fisheries and biology. The aim of this study was to explain the anatomical and histological aspects of stomach and pyloric caeca in L. aurata, L. abu and M. cephalus (Mugilidae) from the Caspian Sea. Fifteen adult individuals of mugilidae; Liza aurata, L. abu and Mugil cephalus were collected from three fishing areas in the Caspian Sea, northwestern and the northeastern Persian Gulf. The length and diameter of stomach and the length, diameter and number of pyloric caeca were measured. L. aurata had larger stomach than L. abu. Anatomical and histological study showed stomach is U-shaped and gizzard like; it is divided into anterior cardiac and posterior pyloric portions, while pyloric caeca is a finger-like straight organ. In transverse section, the wall of the stomach and pyloric caeca is deeply folded with four-layered general structure. Lenght and diameter of stomach showed strong correlation with standard length of specimens. Keywords: Morphology, Epithelium, Muscularis, Gizzard. 1. Introduction The alimentary canal of fish is well developed and structurally adapted to accommodate a wide variety of diets. In fact, each fish species has its own structural peculiarities to the alimentary canal specially stomach towards its unique food habits (Chakrabarti and Ghosh., 2014). Knowledge of fish s alimentary canal morphology is becoming increasingly important in * huseyn22@gmail.com fish digestive physiology and improvement of nutrition protocols (Banan Khojasteh, 2012). Among large number of species, though the stomach is also defined as actual organ, consists of anterior cardiac region and posterior pyloric region (Chakrabarti and Ghosh., 2014). In Mugilidae family the stomach is a simple U- shaped sac which is divided into a thinwalled cardiac crop and a very thick- walled biconical pyloric gizzard (Thomson, 1997). The function of the gizzard in fishes is similar to birds; to grind or triturate 59

2 Khayyami et e al. / Anatomy and Histology of the Stomach and Pyloric caeca in Mugilidae, food (Wilson and Castro., 2010). The pyloric caeca are blind-endedd sphincterless ducts associated with the anterior intestine (Wilson and Castro., 2010). The pyloric caeca,i an importantt identification character, is found in various quantities and sizes in different species in Mugilidae family (Thomson, 1997). The pyloric caeca increase the surface areaa for digestion and absorption, but do not have a role in fermentation or storage (Buddington and Diamond., 1987). Liza aurata, L. abu and Mugil cephalus are commercial fishes of Mugilidae family which have an important role in feeding of many areas in Iran (Thomson, 1997; Ghelichi et al., 2004; Coad, 2008). Mullets (Mugilidae family) are very important marine species successful on all accessible foods (Mian et al., 2014). The aim of the present study was to explain the anatomical and histological aspects of stomach and pyloric caeca in L. aurata, L. abu and M. cephalus (Mugilidae). 2. Materials and Methods Fifteen adult individuals of mugilidae; Liza aurata, L. abu and Mugil cephalus (5 specimens each) were collected from three distant fishing area, in the Caspian sea (36 36' N, 52 10' E), Northwestern (30 25'N, 49 11'E) ) and the Northeastern (27 18'N, 56 26'E) Persian Gulf (Fig. 1). The fish were killed by blow to the head. For each specimen, the body cavity was cutt open through the ventral surface and the alimentary tract dissected out. The length and diameter (from thickest part) of the gizzard like stomach and pyloric caeca were measured (Fig. 2), and immediately fixed in 10% neutral buffered formalin. For histological study, the specimens were sent to the marine biology laborato ory of Khorramshahr University of Marine Science and Technology. The tissue was passed through graded ethanol, cleared in xylene, impregnated and embedded in paraffin wax by Tissue Processor model RX-11B, Tissue tek rotary. Sections 5µm thick were obtained with Leica microtome model LEICA-RM2245. They were stained with haematoxylin and eosin for light microscopy examination (Bancroft and Stevens, 1977). Photomicrographs were taken LITE camera attached a to Olympus Statistical analyses were performed using the SPSSS version 21 software packages and Excel with DINO microscope. Fig. 1: The map of Iran showing thee location of sampling regions, The The Caspian sea (1), Northwestern Persiann Gulf (2) and Northeastern Persian gulf (3). Fig. 2: Illustration off stomach and pyloric caeca inn Mugilidae. 1- Cardiac part, 2- Pyloric part, 3- Pyloric caeca, 4- Esophagus, 5- Intestine, 6- Length of o stomach andd 7- Diameter off stomach 60

3 Journal of the Persian Gulf (Marine Science)/Vol. S 6/No. 19/March 2015/08/ Results The stomachs of Liza aurata, L. abu and Mugil cephalus are U-shaped and gizzard-like, posterior pyloric portions. Mean length and diameter (±) standard deviations of and divided into anterior cardiac and stomach are illustrated in Table 1. The larger stomach belongs to L. aurata, according to its largest standard length, while L. abu has a small stomach followed by short standard length. In Histological study, in transverse section, there is a relationship between size of stomach and body size. The wall of the stomach is thick and deeply folded (Figs 3 and 4). It has a four-layered general structure: tunica mucosa which is of a single-layered columnar epithelium with a developed brush border and lamina propria in the form of connective tissue t network, submucosa which w is made up of thick t fibers of connective tissue, tunicaa muscularis; an extremely thick layer of smooth muscle and tunica serosa as an outer loose connective c tissue (Figs 3 and 4). The circular smooth muscle layer in the pyloric region tends to be more developed than in the cardiac region (Figs 3 and 4). 4 Histologically, aspects of stomach in L. aurata, L. abu and M. cephalus are very similar with no obvious difference between them. The pyloric caecas of L. aurata, L. abu and M. cephalus are finger-like straight organs. Mean length and diameter (±) standard deviations and number of pyloric caeca are illustrated in Table 1. Fig. 3: Micrograph of stomach wall; a: ( 40 resolution, Mugil cephalus) ); b: ( 40 resolution, Liza aurata ); c: ( 40 resolution, r L. abu ) and d: ( 100 resolution, M. cephalus). Foldss (FL), tunica muscularis (TM), lamina propria (LP), epithelium (EP) (H&E). 61

4 Khayyami et e al. / Anatomy and Histology of the Stomach and Pyloric caeca in Mugilidae, Fig. 4: Microhraphh of stomach wall;. a: (Mugil cephalus); c b and c: (Liza aurata) and d: (L. abu). Tunica muscularis (TM), lamina propria (LP), epithelium (EP) (H&E). Table 1. Characteristics of stomach and pyloric caeca cephalus (Linnaeus, 1758) L. aurata Mean ± SDD in Liza aurata (Risso, 1810), L. abu L. abu Mean ± SD (Heckel, 1843) and Mugil M. cephalus Mean ± SD Length of Stomach (cm) 5.16 ± ± ± 0.19 Diameter of Stomach (cm) 2.36 ± ± ± 0.12 Length of Pyloric Caecaa (cm) 2.08 ± ± ± 0.13 Diameter of Pyloric Caeca (cm) 0.64 ± ± ± Number of Pyloric Caeca Standard Length (cm) 47.1 ± ± ± 4.2 L. aurata has longest pyloric caeca and the largest diameter of pyloric caeca is for M. cephalus, while L. abu has small pyloric caeca. In histological study, in transverse section, the wall of the pyloric caeca is thin and deeply folded (Fig. 5). Pyloric caeca also has a four-layered general structure like stomach, s but its tunica muscularis has a thin layerr of smooth muscle (Fig. 5). 62

5 Journal of the Persian Gulf (Marine Science)/Vol. S 6/No. 19/March 2015/08/59-66 Fig. 5: Micrograph of pyloric caeca wall;. a: ( 40 resolution, Liza abu); b: ( 100 resolution, L. abu); c: : ( 40 resolution, Mugil cephalus) and d: ( 100 resolution, M. cephalus). Foldss (FL), tunica serosa (TS), tunica muscularis (TM), epithelium (EP) (H&E). In comparative study of histological aspects of In the data set as a whole R 2 for length of stomach pyloric caeca between L. aurata, L. abu and M. was and for diameter of stomach (Figs cephalus, no remarkable difference was recorded. 6 and 7). For all specimens, simple allometric equations provided a very good fit to the relationships between length of stomach - standard length and diameter of stomach- standard length (Figs 6 and 7). Fig. 7: The relationship between standard length and diameter of stomach in Liza aurata (Risso, 1810), L. abu (Heckel,( 1843) and Mugil cephalus (Linnaeus,( 1758). Fig. 6: The relationship between standard length and length of stomach in Liza aurata (Risso, 1810), L. abu (Heckel, 1843) and Mugil cephalus (Linnaeus, 1758). 4. Discussion In Liza aurata, L. abuu and Mugill cephalus, like 63

6 Khayyami et al. / Anatomy and Histology of the Stomach and Pyloric caeca in Mugilidae, other fishes of Mugilidae family, the stomach is U- shaped and gizzard-like (Thomson, 1997). This unique shape of stomach is one of the adaptative strategies in alimentary duct in Mugilidae. U-shaped stomach probably allows for stretching during food consumption and gizzard-like shape is adapted for grinding of coarse plant, sand and/or mud (Chakrabarti and Ghosh., 2014). Djadji et al. (2014), reported some species of Mugilidae family have a diet based on plant material or detritus. The digestive tract of teleost is well- adapted to modes of feeding and kinds of diet. The alimentary canal of fish exhibits a remarkable diversity of morphological and functional characteristics (Murray et al., 1996; Buddington et al., 1997; Banan Khojasteh, 2012; Khalaf Allah, 2013). The adaptation strategies of stomach in Liza aurata, L. abu and Mugil cephalus may have developed, because of feeding habit and environmental characteristics. In general, the teleost stomach shows a morphology which exhibits a distinct difference which correlates with diet, feeding habit, body shape and also environmental conditions (Reifel and Travill., 1978; Anderson, 1986; Winemiller et al., 1995). In fact, each fish species has its own structural adaptations of the stomach towards its unique food habit (Chakrabarti and Ghosh., 2014). The mucosal epithelium of the stomach of L. aurata, L. abu and M. cephalus is composed of a columnar wall which is similar to that of other teleosts. The mucosal epithelium and stomach wall histology in teleost are similar (Elbal and Agulleiro., 1986; Grau et al., 1992; Gargiulo et al., 1997; Arellano et al., 2001; Chakrabarti and Ghosh., 2014; Ghosh and Chakrabarti., 2015) and it is entirely composed of a columnar epithelium. In Liza aurata, L. abu and Mugil cephalus stomach is conical shaped which is more thickened in middle area. This shape is probably made because of form of muscle layer in middle area. The circular smooth muscle layer in the pyloric region tends to be more developed than in the cardiac region; however, extreme thickening assumes a globular or spindle-like shape giving the appearance of the gizzard (Kapoor et al., 1975; Thomson, 1997; Wilson and Castro., 2010). Liza aurata, L. abu and Mugil cephalus like other Mugildae have organs as pyloric caeca which is not unique in this family. Some fish also possess caeca which are located in the proximal gut adjacent to the pyloric sphincter (hence the name pyloric caeca). The pyloric caeca increase the surface area for digestion and absorption but do not play a role in fermentation or storage (Buddington and Diamond., 1987). The number and the structure of pyloric caeca is used for taxonomic separation of the genera of mullets by earlier workers (Thomson, 1954; Pillay, 1962; Thomson, 1966; Luther, 1977; Jayaram, 1999). The number is known to vary from 2 to 22 in the genus Mugil, while in the genus Liza it is between 2 and 17 (Luther, 1977; Kurma and Babu., 2013). In this study L. aurata had 9 and L. abu had 4 narrow and long pyloric caeca, while M. cephalus had 2 large pyloric caeca which conformed to Kurma and Babu (2013) and Thomson (1997). The pyloric caeca and proximal intestine are structurally similar and have the same function in digestion (Cataldi et al., 1987).The wall of pyloric caeca is thin and deeply folded and it has a four-layered general structure: tunica mucosa which is of a single-layered columnar epithelium with a developed brush border and lamina propria, submucosa, tunica muscularis; a thin layer of smooth muscle and tunica serosa as a loose connective tissue. As noted previously, the histological aspects of stomach and pyloric caeca of three species was similar with no differences. The folds of pyloric caeca perhaps increased surface area for digestion. The branched mucosal fold seen in the alimentary canal is an adaptation to increase surface area for digestion (Buddington and Diamond., 1987; Ikpegbu et al., 2013). In all fishes, four histologically similar basic layers are present with negligible differences in some species of lampreys (Wilson and Castro., 2010). Findings of this research, for example 64

7 Journal of the Persian Gulf (Marine Science)/Vol. 6/No. 19/March 2015/08/59-66 larger species of Mugilidae have larger stomach in correlation with standard length, confirmed Kramer and Bryant., (1995) Statement whom indicated between fish species with different body sizes, since more energy and nutrients are required to support larger species than small species, one might expect larger digestive organs in larger species. References Anderson, T.A., Histological and cytological structure of the gastrointestinal tract of the luderick, Girella tricuspidata, in relation to diet. Journal of Morphology. 190: Arellanol, J.M., Storch, V. and Sarasquetel, C., Histological and histochemical observations in the stomach of the Senegal sole, Solea senegalensis. Histology and Histopathology. 16: Banan Khojasteh, S.M., The morphology of the post-gastric alimentary canal in teleost fishes: a brief review. International Journal of Aquatic Science. 3(2): Bancroft, J.D. and Stevens, A., Theory and practice of histological techniques. New York, USA: Churchill Livingstone. Buddington, R.K. and Diamond, J., Pyloric caeca of fish: a new absorptive organ. American Journal of Physiology. 252: Buddington, R.K., Krogdahl, A., Bakke, M. and Kellep, A.M., The intestines of carnivorous fish: structure and function and the relations with diet. Acta Physiologica Scandinavica. 161: Catladi, E., Cataudella, S., Monaco, G., Rossi, A. and Tancioni, L A study of the histology and morphology of the digestive tract of the sea -bream, Sparus aurata. Journal of Fish Biology. 30: Chakrabarti, P. and Ghosh, S., A comparative study of the histology and microanatomy of the stomach in Mystus vittatus (Bloch), Liza parsia (Hamilton) and Oreochromis mossambicus (Peters). Journal of Microscopy and Ultrastructure. 2: Coad, B.W., Freshwater Fishes of Iran. Available at Djadji, E.L.G., Sylla, S., Konan, J.K., Atse, B.C. and Kouamelan, P.E., Similarity of Feeding Strategies of Two Mugilidae Liza falcipinnis (Linnaeus, 1758) and Mugil cephalus (Linnaeus, 1758) in Ebrié Lagoon (Ivory Coast). International Journal of Agriculture Innovations and Research. 3(2): Elbal, M.T. and Agulleiro, B., A histochemical and ultrastructural study of the gut of Sparus auratus (Teleostei). Journal of Submicroscopic Cytology and Pathology. 18: Gargiulo, A.M., Ceccarelli, P., Dallaglio, C. and Pedini, V., Ultrastructural study on the stomach of Tilapia spp (Teleostei). Anatomia, Histologia, Embryologia. 26: Ghelichi, A., Oryan, S., Ahmadi, M., Kazemi, R. and Hallajian, A., Histology of different stages of ovary development in the grey mullet and Gomishan shrimp. Journal of Agricultural Sciences and Natural Resources. 10: Ghosh, K.S. and Chakrabarti, P., Histological and histochemical characterization on stomach of Mystus cavasius (Hamilton), Oreochromis niloticus (Linnaeus) and Gudusia chapra (Hamilton): Comparative study. The Journal of Basic & Applied Zoology. 70: Grau, A., Crespo, S., Sarasquete, M.C. and González de Canales, M.L., The digestive tract of the amberjack Seriola dumerili, Risco: A light and scanning electron microscope study. Journal of Fish Biology. 41: Ikpegbu, E., Ezeasor, D.N., Nwogu, C., Nlebedum, U.C., Nnadozie, O. and Agbakwuru I.O., The Structure and Functional Significance of Branched Anastomosing Mucosal Folds in the Proximal Intestine of the Domesticated African Catfish ( Clarias gariepinus Burchell 1822). World Applied Sciences Journal. 28(11):

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