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INTERNATIONAL JOURNAL OF ENVIRONMENTAL SCIENCE AND ENGINEERING (IJESE) Vol. 7: 95- 104 (2016) http://www.pvamu.edu/research/activeresearch/researchcenters/texged/ international-journal Prairie View A&M University, Texas, USA

Comparative study on the histological structures of the intestine in some coral reef fishes in Hurghada, Red Sea, Egypt

Ragaa M.A. El-Deeb1, Samia M. Abd Elwahab2, Hassan M. M. Khalaf- Allah3, Mohamed M. Abu-Zaid3 and Walaa T.S. Shalaby2 1- Zoology Depart, Faculty of Science, Ain Shams University, Cairo, Egypt. 2- Zoology Department, Faculty of Science (girls), Al-Azhar University, Cairo, Egypt. 3- Marine Biology, Zoology Depart., Faculty of Science (boys), Al-Azhar University, Cairo, Egypt.

ARTICLE INFO ABSTRACT Article History The present work focuses on the variation of the histological structure of the Received: Dec. 5, 2016 intestine in some coral reef fishes (Siganus rivulatus, Mulloidichthys flavolineatus Accepted: Dec. 29, 2016 and ) in relation to food and feeding strategy. Fish specimens were Available online: Feb. 2017 collected from Abu Galawa Lagoon in Hurghada, Red Sea, during the period from ______December 2014 to November 2015. Keywords: The intestine of the herbivorous fish (S. rivulatus) is exceedingly long and Coral reef fishes variously convoluted. A character related to cellulose digestion, which requires a Intestine longer time in the intestine. While, the intestine of the carnivorous (M. Feeding strategy flavolineatus) and the piscivorous fish (T. choram) are short tubes. Ileo-rectal valve The ileo-rectal valve marked the beginning of the rectum and prevents the Red Sea passage of food particles into the posterior part before intestinal digestion and Histological structures absorption is completed. This valve is absent in the posterior intestine of herbivorous (S. rivulatus) and piscivorous fish, (T. choram). But, the posterior intestine of carnivorous fish (M. flavolineatus) was recognized by the presence of ileo-rectal valve. The duodenal mucosa of all studied is thrown into primary, secondary and tertiary folds. Such structures are short and few in number towards the ileum and are much thicker in the rectum. The epithelial lining of the intestine is consists of columnar and numerous large goblet cells. This may provide viscosity for both food and fecal materials. In conclusion, the intestine of studied species is subjected to diverse and significant variations and much modification in accordance to the food and feeding strategy. 1. INTRODUCTION From the economic importance of view, the Red Sea coasts constitute a very important sector in the Egyptian fisheries, both for significant total catch and a large number of economically important species. Research on reef fisheries and fish biology has a short history. Concurrently, reef fish biology flourished with numerous academic studies of small elements of reef fish communities. Coral reefs of the Red Sea support approximately 400 fish species which utilize corals for shelter, food and/or breeding ground. However, a little is known about the biology of the large variety of fish living in and around the coral reefs in the Red Sea (ERSR, 1998; Mohamed, 1999). ______ISSN 2156-7530 2156-7530 © 2011 TEXGED Prairie View A&M University All rights reserved

96 Ragaa M.A. El-Deeb et al.: Comparative study on the histological structures of the intestine in some coral reef fishes

The adaptations of the digestive organs understand the functional mechanisms of fish of the fish to their normal diet are digestive physiology and feeding strategy. particularly evident in the form, size, structure, abundance and limitation of the 2. MATERIAL AND METHODS microscopically elements such as dentition, 2.1. Specimens collection: mucous cells, taste buds, digestive glands A total of 26 specimens; 10 of rabbit and muscular coat in the esophagus, fish (Siganus rivulatus), 10 of yellow striped stomach, intestine and pyloric caeca in the goat fish (Mulloidichthys flavolineatus) and fish. 6 of needle fish (Tylosurus choram) formed All of these features are subject to the material for the present study. Fish diverse and significant variations and much specimens were collected from Abu Galawa modification in accordance with the feeding lagoon in Hurghada, Red Sea, during the habits (Dasgupta, 2000; Khalaf Allah, 2009). period from December 2014 to November Several studies are available on the 2015. Long lines nets were the main fishing adaptations of the alimentary canal of fish to method used to collect the fish. Wherever their food and feeding habits notably by possible fish were examined fresh or Kamel et al. (1995) on the Nile cat fish preserved in 10% formalin solution for latter (Bagrus docmac), Shehata (1999) on the examination. In the laboratory, fish were grass carp (Ctenopharyngodon idella), taxonomically identified, as far as possible Shehata et al. (1999) on the characinid fish up to genera according to Randall (1983) and (Alestes dentex), Khalaf-Allah (2001 and Lieske and Myers (2004). They were 2009) on the cichlid fish (Tilapia zillii), the identified, total length were measured to the mullet fish (Liza aurata), the sole fish (Solea nearest millimeters and recorded. solea), the spiny checked grunter (Terapon 2.2. Histological studies of the intestine: puta) and the striped sea bream For histological studies, small pieces (5 (Lithognathus mormyrus), Yashpal et al. mm) of intestine were removed from the (2006 and 2009) on the carnivorous fish dissected specimens and immediately fixed (Rita rita) and the carp (Cirrhinus mrigala), in alcoholic Bouin`s fluid for at least 48 Delashoub et al. (2010) on the bighead carp hours, dehydrated in ascending (Hypophthalmichthys nobilis), Gamal, et al. concentrations of ethyl alcohol, cleared in (2012) on the cat fish (Clarias gariepinus) xylene and embedded in paraplast wax and Deshmukh et al. (2015) on the cat fish (M.P.: 58°C). Transverse sections were cut at (Heteropneustes fossilis). the thickness of 4-6 µm, stained with However, information on the Harris`s haematoxylin and eosin and the morphological and histological adaptations histological procedures were completed for of digestive tube according to food and general structure (Humason, 1979). Sections feeding habits of coral reef fish in the were microscopically examined then Egyptian Red Sea are rare (Al-Hussini, 1947; photographed and described. Gohar and Latif, 1959; Khalf-Allah, 2013). Therefore, the present study aimed to 3. RESULTS provide comparative description on the 3.1. Siganus rivulatus: histological adaptations of the intestine in At the macroscopic observations level, some coral reef fish such as the rabbit fish the intestine of S. rivulatus is exceedingly (Siganus rivulatus) (Forsskål, 1775), the long and variously convoluted. It can be yellow striped goat fish (Mulloidichthys divided into three portions: anterior, mid and flavolineatus) (Lacepède, 1801) and the posterior intestine. The wall of each portion needle fish (Tylosurus choram) (Rüppell, is made up of the ordinary four layers: 1837) in Hurghada, Red Sea, Egypt in mucosa, submucosa, muscularis and serosa. relation to its food and feeding habits to Ragaa M.A. El-Deeb et al.: Comparative study on the histological structures of the intestine in some coral reef fishes 97

The microscopic observations revealed consists of simple squamous epithelium that the mucosal lining of the anterior (Plate III A&B). intestine is greatly folded. The villi are 3.2. Mulloidichthys flavolineatus: relatively short and closely set with tapering, At macroscopic observation level, the round and blunt tips. Small folds are present intestine of M. flavolineatus is differentiated at the bases of the crypts in between the into three regions (duodenum, ileum and comparatively large folds. The epithelial rectum). mucosa is made up of two kinds of cells: The microscopic observations showed columnar and mucus secreting cells. Mucus that the duodenal mucosa is greatly folded to secreting cells are few in number and have a form villi, which are enormously short and typical goblet outline. They are concentrated closely associated with shallow crypts. The at the sides of the folds, rarely on the crests. epithelial mucosa is made up of columnar While, in extensive areas along the bases, cells and numerous mucus-secreting cells, they are entirely absent (Plate I A&B). The which concentrated at the sides and bases of submucosa is comparatively thinner and the folds (Plate I C&D). The submucosa is composed of areolar connective tissue, richly comparatively thinner and composed of supplied with fibrocytes, lymphocytes and areolar connective tissue, penetrated by blood vessels. The muscularis consists of blood vessels and lymphocytes. Muscularis two layers: an inner circular and an outer mucosa is completely absent. The muscularis longitudinal muscle layers. Both of which consists of two layers: a thick inner circular are formed of unstriated muscle fibers. They layer and a thin outer longitudinal one of are held together by areolar connective unstriated type. The serous layer is made up tissue. The inner layer of muscle fibers is of simple squamous epithelium (Plate I relatively thicker than the outer one. The C&D). serosa consists of simple squamous The ilial mucosa is provided with epithelium (Plate I A&B). broad and long columnar cells. Mucous cells The histological structure of the mid are comparatively large. The submucosa intestine of S. rivulatus is almost similar to consists of fibrous connective tissue, richly that of the anterior one, except the villi, supplied with blood vessels. The muscularis which are enormously short with round or is well developed. The serosa consists of tapering tips. The epithelial lining is simple squamous epithelium (Plate II C&D). provided with broad and long columnar cells. The rectal folds are irregular in shape, Goblet cells are comparatively large. The being short and numerous. Mucus cells are muscularis is well developed. The serosa highly abundant. Lamina propria is consists of simple squamous epithelium and comparatively compact and contains small covering a thin layer of connective tissue lymph spaces. The muscularis is poorly (Plate II A& B). developed. The serous connective tissue The histological structure of the covered by a thin layer of simple squamous posterior intestine of S. rivulatus is similar as epithelium (Plate III C&D). far as the anterior one. But, some differences 3.3. Tylosurus choram: can be easily observed. Generally, the villi The intestine proper of T. choram is a are thicker and tend to be more slender short straight tube. It is divided into three towards the posterior end with round or portions (the anterior, middle and posterior). tapering tips. The mucosa is well developed The wall of each portion is made up of the and mucus cells are abundant (Plate III ordinary four layers: mucosa, submucosa, A&B). The submucosa is well developed and muscularis and serosa. lymph spaces, lymphocytes and large blood The mucosal folds in the anterior vessels are highly abundant. The muscularis portion of intestine are very long, numerous, is well developed and the inner layer is much more or less parallel to each other with thicker than the outer one. The serosa rounded tips. Small folds or buds are also 98 Ragaa M.A. El-Deeb et al.: Comparative study on the histological structures of the intestine in some coral reef fishes

present at the bases of the crypts. The stomach or intestinal bulb, duodenum, ileum, epithelial cells are of two kinds: absorptive rectum and anus. These parts may or may not and less frequently mucus secreting cells. be distinguished from each other in some The latters are saccular or spherical in shape fish, while in others there is clear (Plate I E&F). The submucosa is morphological distinction between these comparatively wider and consists of areolar chambers (Kumar and Tembhre, 1996). connective tissue supplemented by fibrous In this study, the intestine of the connective tissue. The muscularis is herbivorous fish (S. rivulatus) is exceedingly relatively thick and consists of two layers: an long and variously convoluted. This is inner circular and an outer longitudinal necessary for the amount of cellulose muscle layers formed of unstriated type. The materials, which requires a longer passage serosa consists of simple squamous and remain for considerable time in the epithelium (Plate I E&F). intestine. Therefore, the function of this part There is no line of demarcation is connected with the completion of the between the anterior and middle portions of digestion and absorption of the digested intestine in T. choram. However, some food. Externally, the intestine is not histological peculiarities can be easily differentiated into different distinguished demonstrated. The mucosa is thrown into regions due to the lack of any clear primary mucosal folds. The epithelial demarcation between them. Internally, mucosa is made up of a compact simple however, the intestine can be divided into columnar epithelium involved with large three portions: anterior, mid and posterior number of goblet cells (Plate II E&F). The intestine. These results are consistent with submucosa is wide and composed of fibrous previous studies by Almeida et al. (1993); connective tissue contains lymph spaces and Shehata (1997) and Khalaf-Allah (2001). numerous blood vessels. Muscularis and In the present study, the intestine in the serosa are similar in structure to those found carnivorous fish (M. flavolineatus) and the in the anterior portion of intestine (Plate II piscivorous fish (Tylosurus choram) are E&F). short tubes. These findings of the present The histological structure of the work are very similar to those described in posterior portion of intestine is similar as far other carnivorous fishes by Dasgupta (2002 as the middle one, but some differences can and 2004), Al-Abdulhadi (2005), El-Bakary be easily found. The mucosa is thrown into (2007), Khalaf-Allah (2009 and 2013) and deep primary mucosal folds. The folds are Hassan (2013). high, more tapering ends and branched into From the above mentioned results, it is secondary folds. Mucus secreting cells are clear that, the intestinal length is considered comparatively numerous, being saccular or as a significant feature considered in global in shape and distributed among the assessing the nature of diet and is varied columnar epithelium (Plate III E&F). The from species to another. The variations in the submucosa is well developed and made up of gut length of studied species may be due to areolar connective tissue supplemented by the fact that, the carnivorous (M. fibrous connective tissue. Lymphocytes, flavolineatus) and piscivorous (T. choram) lymph spaces and large blood vessels are fish have no need of storage food so a long highly abundant. The muscularis is relatively gut is unnecessary. These findings of the thicker. The serosa consists of simple present study are agree with the studies squamous epithelium (Plate III E&F). previously described by Al-Abdulhadi (2005), El-Bakary (2007), Khalaf-Allah 4. DISCUSSION (2009 and 2013) and Hassan (2013) on All parts of the alimentary canal from carnivorous fishes. On the other hand, the oesophagus to anus are known as gut. The food of herbivorous fish (S. rivulatus) gut is distinguished into oesophagus, contains more cellulose which requires Ragaa M.A. El-Deeb et al.: Comparative study on the histological structures of the intestine in some coral reef fishes 99 longer remains for digestion and large of the intestine, however, the villi are absorptive surface for the proper comparatively shorter, blunt and tend to be assimilation. Similar observations were more slender. Muscularis is well developed. reported by Almeida et al. (1993), Shehata Goblet cells are larger in size and higher in (1997) and Khalaf-Allah (2001). number. The presence of goblet cells in the On the other hand, the ileo-rectal posterior intestine has been considered valves were absent in the posterior intestine essential for fecal lubrication. Similar of herbivorous (S. rivulatus) and piscivorous observations were detected in most fish (Tylosurus choram) fish. But, the posterior described by Shehata (1997 and 1999), Alne- intestine of carnivorous fish (M. na-ei (1994), El-Bakary, (2007), Khalaf- flavolineatus) is recognized by the presence Allah (2009 and 2012) and Hassan (2013). of ileo-rectal valve as well as by increase in its diameter. The ileo-rectal valve, which is 5. REFERENCES more or less constant feature of teleost Agamy, E. I.; Soliman, F. M. and Lashin, F. intestine, marked the beginning of the E. (1992). Development of the terminal segment (the rectum). This valve digestive tube of the fresh water presumably prevents the passage of food teleost, Gambusia affinis holbrookii. particles into the posterior part before the IV- Intestine. J. Egypt. Ger. Soc. Zool., intestinal digestion and absorption is 8 (B): 523 – 558. completed. Similar observations were Al–Abdulhadi, H. A. (2005). 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102 Ragaa M.A. El-Deeb et al.: Comparative study on the histological structures of the intestine in some coral reef fishes

A B

D C

E F

Plate I: Photomicrographs of T.S. in (A&B) the anterior intestine of S. rivulatus, (C&D) duodenum of M. flavolineatus and (E&F) anterior intestine of T. choram showing muscularis (MUS), submucosa (SMU), mucosal fold (MU F), circular muscle fibers (CMF), longitudinal muscle fibers (LMF), areolar connective tissue (ACT), simple columnar epithelium (SCE) and mucous secreting cells (MU C). (H & E; A, C & E X40 and B, D & F X400).

Ragaa M.A. El-Deeb et al.: Comparative study on the histological structures of the intestine in some coral reef fishes 103

A B

C D

F E Plate II: Photomicrographs of T.S. in (A&B) the Mid intestine of S. rivulatus, (C&D) ileum of M. flavolineatus and (E&F) mid intestine of T. choram showing muscularis (MUS), submucosa (SMU), mucosal fold (MU F), circular muscle fibers (CMF), longitudinal muscle fibers (LMF), fibrous connective tissue (FCT), lamina properia (LP), simple columnar epithelium (SCE) and mucous secreting cells (MU C). (H & E; A, C & E X40 and B, D & F X400).

104 Ragaa M.A. El-Deeb et al.: Comparative study on the histological structures of the intestine in some coral reef fishes

A B

C D

F E

Plate III: Photomicrographs of T.S. in (A&B) the posterior intestine of S. rivulatus, (C&D) rectum of M. flavolineatus and (E&F) posterior intestine of T. choram showing muscularis (MUS), submucosa (SMU), mucosal fold (MU F), circular muscle fibers (CMF), longitudinal muscle fibers (LMF), fibrous connective tissue (FCT), simple columnar epithelium (SCE) and mucous secreting cells (MU C). (H & E; A, C & E X40 and B, D & X400).