sistem digesti ikan lele

AJBB Online Asian Journal Of Biology and Biotechnology 2014

Histology, histochemical and ultrastructural studies on Intestine of

Indian catfish, Clarias batrachus (Linn 1758)

Sudhir G. Chirde1 and Y. A. Gadhikar

1*

Department of Zoology, Govt. Vidarbha Institute of Science

Abstract: The aim of the present study was to describe the histological, histochemical and ultrastructural studies of the intestine of Clarias batrachus. Information about morphology, histology and ultrastructural studies is essential for a deeper understanding of the physiological approach of

intestine. The intestinal morphology is influenced by feeding habits. Clarias batrachus being an omnivorous fish, dwelling in muddy water, show a typical intestinal morphology. Histologically, the intestine wall of the investigated species consisted of mucosa, sub-mucosa, muscularis and serosa. Numerous intestinal folds were observed lined with absorptive columnar epithelium along with absorptive cells and mucous secreting goblet cells. The goblet cells were numerous in the distal intestine region of Clarias batrachus as compared to middle and proximal region of intestine. Histological analysis revealed that the intestine PAS and AB positive goblet cells. Ultrastructural studies of intestine showed the epithelial lining of absorptive cells with regular microvilli, tight junction complexes, lysosome, microtubules and mitochondria. This study gives deeper insight on the morphological functional output of the intestine of Clarias batrachus and will be the basic of comparison with other teleost fishes. Keywords: Histology, Histochemical, Ultrastructure, , Intestine, Teleost

and Humanities, Amravati (MS), India.

*Corresponding Author: Y. A. Gadhikar, e-mail id.: [email protected]

Introduction: The fish digestive system shows a marked

diversity of morphology and function (Cao and Wang, 2009; Khojasteh, et al., 2009). Better

information of intestinal morphology,

histological and ultrastructural study is essential for a deeper understanding of the

physiology and pathology of fish intestine. The

intestine is an organ involved in important

physiological function, being the primary site of

food digestion and nutrient uptake. Therefore

optimum utilization of dietary nutrients depends generally on the effectiveness of these functions (Caballero et al., 2003). The

intestinal morphology of fish can be influenced

by feeding habits, food intake frequency, as well as by body size and shape (Buddington et

al., 1997; Arellano et al., 2002). Depending on

diet, the fish intestine can vary morphologically

from short straight to long coil and complexly arranged (Govoni et al., 1986; Reinthal, 1989).

The feeding behaviors of fish are classified

according to the type of food consumed. In

simplest form, fish are either herbivore if they

eat plant material, carnivores if they consume

animal material or omnivores if they eat a

combination of plant and animal materials

(Evans, 1998). Clarias batrachus (walking catfish) is a

freshwater air breathing species of catfish

found in Central Asia, also known in English

walking catfish, and in Marathi Mangur, its Walk is wriggling motion with a snakelike movement, by using its pectoral fins to keep it upright. In the wild, the natural diet habit of this

creature is omnivorous (Mills, 1993). Walking

catfish has an elongate body shape. This

catfish has long-based dorsal and anal fins as

well as four pairs of sensory barbells, and the pectoral fins contain poisonous spines which

are especially stout on the male.

The present study aimed to study the general

histology and histochemical and ultrastructural

ajbbonline.com Volume:3 Issue (3) e301 ISSN 2278-9537 Page 1

AJBB Online 2014 Histology, histochemical and ultrastructural studies on Intestine

of Indian catfish, Clarias batrachus (Linn 1758)

distribution of mucosubstances in the intestine of walking catfish Clarias batrachus. This study

gives a deeper insight into the morphological and functional aspect of the intestine of Clarias

batrachus and will be the basis of the

comparison with other teleostean fish.

Material and methods 1 Collection and samples:Walking catfish

Clarias batrachus (Linn, 1758), (Order:

Siluriformes, Family: Clariidae) were used in

the present investigation. The adult walking

catfishes, ranging from 25 to 30 cm in length

and 250 to 300 gm in weight, were collected

alive from the fish market from the Amravati city (Maharashtra, India). They were killed and

dissected immediately in the laboratory.

2 Histological, histochemical and

ultrastructural studies

A. Histological and histochemical study:

Fresh adult specimens were carefully

dissected mid-ventral incision and small pieces

of intestine removed from the body. Small

pieces of intestine viz. proximal, middle and

distal parts of the intestine were fixed by immersion in 10% Formalin or Bouins fixative for light microscope studies. Samples were

routinely processed by dehydration in an

ethanol series and then embedding in paraffin.

Six micrometer thick histological sections were

cut by microtome, prepared according to standard protocol and then stained with

haematoxylin and eosin (H and E).

Histochemical techniques were applied for the

identification of mucous in the alimentary tract of the Clarias batrachus. Section were stain

with Periodic acid Schiff and alcian blue (PAS-AB) to demonstrate the full complement of

tissue proteoglycans and alcian blue (AB) stain

specifically acidic mucins while PAS stain

neutral one. Micrographs were taken with an

Olympus microscope. B. Ultrastructural study: Small pieces of the

proximal, middle and distal intestine tissues of Clarias batrachus were cut and fixed into the

2.5% glutaraldehyde as well as 2%

paraformaldehyde in 0.1 M sodium phosphate

buffer saline solution at pH 7.3 for an about 12 hours at 4

0 C. Samples were post-fixed in 1%

OsO4 for 1 hour at 40 C. The samples were

dehydrated in an ascending grade of acetone,

infiltrated and embedded in araldite CY 212

(TAAB, UK). Thick sections (1 m) were cut

with an ultra-microtome, mounted onto glass slides, stained with aqueous toluidine blue and

observed under a light microscope for gross

observation of the area and quality of the

tissue fixation. For electron microscope

examination, thin sections of grey-silver colour interference (70-80 nm) were cut and mounted

onto 300 mesh- copper grids. Sections were

stained with alcoholic uranyl acetate and

alkaline lead citrate, washed gently with

distilled water and observed under a Morgagni

268D transmission electron microscope (Fei Company, The Netherlands) at an operating

voltage 80 kV. Images were digitally acquired

by using a CCD camera (Megaview III, Fei

Company) attached to the microscope (AIIMS,

New Delhi, India).

Result

A. Histology and Histochemical study:

The intestine of Clarias batrachus divided into

three parts viz; proximal, middle and distal

intestine. The intestine wall layers which are

divided into mucosa, submucosa, muscularis

and serosa are similar to the other vertebrates

(Fig. 1). The mucosal surface of proximal

intestine part had numerous elongated and

deep finger-like folds called villi, lined by a

simple columnar epithelium consisting of

absorptive cells and mucus secreting goblet

cells (Fig. 2). The folds present in middle and

distal part of intestine are fewer and shorter.

There was tremendous increase in number of

goblet cells observed in the present study in

the distal part of intestine showing high

mucous secretion, as compared to proximal

and middle part of intestine i.e. duodenum

(Fig. 3, 4, 5). The goblet cells appeared like a

swollen circular-ovoid shaped which open on

the luminal exterior by a single pore. The free

borders of the columnar cells outline like a

brush border, which continue to the columnar

epithelium and interrupted only by the opening




of the goblet cells. Many lymphocytes usually

usually were observed to get aggregate at the

bases of the columnar epithelium while some

of them often appear in the free ends of the

cells. The lamina propria consists of loose connective tissue that penetrates as well as

supports the intestinal villi. The submucosa of

the intestine is formed of a vascularized loose

connective tissue that lies below the lamina

propria without separating line (Fig. 6). The muscularis of proximal, middle as well as

posterior intestine consists of two layers of

smooth muscle fiber; thick inner circular and

outer longitudinal muscle layer (Fig. 7). Many

nerve plexuses lie between these two muscle

layers. The serosa is an extremely thin layer of a simple squamous epithelium. These cells are

flattened with small amount of cytoplasm and

compressed oval nuclei. In proximal, middle as well as the distal intestinal part of Clarias

batrachus, the mucosal epithelium consists of

a series of goblet cells which were stained

strongly with positive AB and PAS (Fig. 8 and

9). This indicated the presence of the acidic as

well as neutral (carboxyl and phosphate

group) glycoprotein. B. Ultrastructural study: The ultrastructural studies of intestine of adult Clarias batrachus

(Control) were carried out in the present

investigation. TEM study showed the apical

border of the proximal epithelial lining of

intestine with presence of microvilli with normal

length, and no clear terminal web below the microvilli (Fig. 10). Fine filaments of the

microvilli extended in to the apical cytoplasm.

Many longitudinal oriented microtubules, small

vesicles and multivesicular bodies are present

in the apical cytoplasm (Fig. 11 and Fig. 12). Below the microvilli tight junction are present

(Plate Fig. 13). The endocrine cells with large

oval or spherical shape nucleus with prominent

nucleoli were located either at the base or the

center of the cell (Fig. 14 and Fig. 15). Ovoid

mitochondria were located to be scattered throughout the cytoplasm and basal to the

nucleus. The rough and smooth endoplasmic

reticulum located near the nucleus of cell (Fig.

15). Lamellar structures were observed in the

cytoplasm of columnar epithelial absorptive cells (Fig. 13). The apical end of middle

intestine bears numerous microvilli, tight

junction, and microtubules (Fig. 16).

Ultrastructuraly, long columnar epithelial

absorptive cells were observed in intestinal mucosa of C. batrachus (Fig. 17). The bulky

goblet cells were filled with numerous mucous droplets of low electron-density between

surface epithelial cells (Fig. 17). The epithelial

mucosa of intestine contained many endocrine

cells. They were characterized by irregular

hyper-chromatic nucleus and electron dense granules (Fig. 18). The enterocytes were

joined to the apical surface by the tight

junction complexes including the zonula

occludents and desmosoma (Fig. 16 and 19).

The distal intestine also showed apical end

covered with many microvilli, just below the microvilli tight junction complexes and some

microtubules were presence adjacent to goblet

cell (Fig. 20). Some round, elongated and

irregular type of enteroendocrine cells could

be established in the distal region of the intestine. These cells show presence of narrow

extension which is known as cytoplasmic

process and it contains longitudinal oriented

microtubules (Fig. 21 and 22). Based on the

transmission electron microscopically data,

some elongated and irregular open type of enteroendocrine cells could be established in

the proximal, middle as well as in the distal

intestine. Whereas some Closed type cells are observed in the middle and proximal

intestinal region (Fig. 14).

Cell type I with round morphology having the smallest secretory granules were located in

proximal, middle and distal parts of the

intestine (Fig. 14). Cell type II, with elongated

and round shape with secretory granules of

normal size were found in the proximal as well as the middle parts of the intestine region (Fig.

15 and 22). Cell type III with secretory

granules of nearly same size as those of the

Cell type II but with an irregular shape found in

proximal, middle as well as distal intestinal

region (Fig. 19 and 21). All the cell types seem to be open type that

means they have a secretory granules

containing base and long narrow extension to

the lumen. This dendrite-like cytoplasm

contains longitudinally oriented microtubules. Slight pinocytotic activity is observed in the

apical part of the endocrine cell, in which the




Figure 1-9: HE and PAS, AB study of

proximal, middle and distal intestine of

Clarias batrachus.

Fig. 1: Proximal part of intestine of Clarias

batrachus showing: MF (mucosal fold), M

(Mucosa), LP (Lamina propria), SM (Sub-

mucosa), CML (Circular muscle layer), LML

(Longitudinal muscle layer), S (Serosa). (HE

X10). Fig. 2: Mucosa of proximal intestine

showing: absorptive cell (arrowhead), goblet

cell (arrow), LP (Lamina propria). (HE X40).

Fig 3: Middle part of intestine Cl. batrachus

showing: M (Mucosa), SM (Sub-mucosa), LP

(Lamina propria), ML (Muscularis), GC (Goblet

cell). (HE X10). Fig. 4: Distal part of intestine

Cl. batrachus showing: M (Mucosa), SM (Sub-

mucosa), LP (Lamina propria), MF (Mucosal

fold, white arrow), ML (Muscularis). (HE X10).

Fig. 5: Mucosa of distal intestine showing:

goblet cell (arrow), LP (Lamina propria). (HE

X40). Fig. 6: Basal part of Intestinal fold

showing: GC (Goblet cell), LP (Lamina

propria), SM (Sub-mucosa), Loose connective

tissue (arrow). (HE X40). Fig. 7: Muscularis

layer of intestine showing: CML (Circular

muscle layer), LML (Longitudinal muscle

layer), Loose connective tissue (arrow). (HE

X40). Fig. 8 and Fig. 9: Mucosa of Intestine

showing: PAS and AB positive GC (Goblet

cell), LP (Lamina propria). (PAS and AB X40).




Figure 10-22: Ultrastructure of Proximal,

middle and distal intestine of Clarias

batrachus. Fig. 10: Ultrastructure of epithelial lining of

proximal intestine showing: MV (Microvilli). Scale bar 500nm. Fig. 11: Microtubule

extends towards the microvilli. Scale bar 200nm. Fig. 12: Many longitudinal oriented

microtubules (arrowhead), small vesicles

(white arrowhead), multivesicular bodies

(arrow) and mitochondria in the apical cytoplasm. Scale bar 500nm. Fig. 13: Apical

end showing tight junction (arrow),

microtubules (arrowhead) and lamellar structure (LS). Scale bar 1m. Fig. 14:

Endocrine cell showing: endoplasmic reticulum

(ER), L (Lysosome), Nucleus (N) electron dense granules (arrow). Scale bar 500nm. Fig.

15: Endocrine cell showing: Nucleus (N),

Mitochondria (MT), Endoplasmic reticulum

(ER), electron dense granules (G). Scale bar 500nm. Fig. 16: Epithelial border of middle

intestine showing: Microvilli (M), Tight junction

(arrow), Microtubules (arrowhead), Enterocyte cytoplasm (ET CP). Scale bar 2m. Fig. 17:

Apical end of middle intestine showing: Goblet

cell (GC), microvilli (MV), absorptive cell (AC),

nucleus (N), mitochondria (MT). Scale bar 2m. Fig. 18: Endocrine cell show irregular

hyper-chromatic nucleus (N) and electron dense granules (G). Scale bar 1m. Fig. 19:

Irregular shape endocrine cell showing:

Nucleus (N), mitochondria (MT), lysosome (L) and vacuoles (V). Scale bar 500nm. Fig. 20:

Apical end of distal intestine showing: microvilli

(MV), tight junction (arrow), microtubule

(arrowhead), goblet cell (GC). Scale bar 2m. Fig. 21: Endocrine cell with elongated

cytoplasm showing: Nucleus (N),, Mitochondria (MT), Cytoplasmic process (CP),

Microtubule (arrowhead), Golgi body (GB). Scale bar 2m. Fig. 22: Endocrine cell from

distal intestine region showing: Nucleus (N),

long cytoplasmic process (CP), electron dense

granules (G), microtubules (arrowhead). Scale bar. 2m.

Discussion: A. Histological and histochemical study:

The histological studies of the digestive tract




across species of fish are more valuable as

the interest in fish culture expands and

therefore more information necessitated with

regard to feeding and nutrition. The intestinal

mucosa acts as selective barrier to nutrients and also prevents many toxins and pathogens (Murray et al., 1994). Moreover, it plays a part

in the endocrine function, electrolytic balance and immune response (Buddington et al.,

1997). The fish species in present study

belongs to the family clariidae, showed oesophageal wall with a more regular structure

and longitudinal folds, which is related to the oesophagus of the silverside odontesthes

bonariensis (Diaz et al., 2006) and more

simple than those found in marine teleosts

(Abaurrea-Equisoain and Ostos-Garrido, 1996).

The intestine of Clarias batrachus is divided in

to three part; proximal, middle and distal

intestine. Long, numerous mucosal folds were

observed in the proximal intestine increasing

the surface area and enhancing the absorptive

activity (Khanna, 1971), while short in middle

and distal region. The mucosal folds of

intestine lined by a single layer of columnar

cells with numerous mucous secreting goblet

cells were consistent and in agreement with

the results obtained in other species

(Khojasteh et al., 2009; Abdulhadi et al., 2005;

Cataldi et al., 1986; Hernandez et al., 2009).

Columnar epithelial cells of the intestinal

mucosa may have an absorptive function as

reported in other fishes (Sis et al., 1979;

Clarke and Witcomb, 1980; Albrecht et al.,

2001). The pattern of muscularis layers

consisting of thicker inner circular and outer

longitudinal smooth muscle observed in

Clarias batrachus. This was also found similar

to that described for Ambassis sp. (Martin and

Blaber, 1984), for Tilapia (Gargiulo et al.,

1998), for Orthrias angorae (Sucmez and Ulus,

2005) and for Rhamdia quelen (Hernandez et

al., 2009. The thicker of the muscularis layer is

related with the storage and expulsion of fecal

material from the intestine (Grau et al., 1992).

Proximal region of intestine in Clarias

batrachus showed higher amount of folds

increasing the absorptive surface and

enhancing the absorptive activity. This is a

structural arrangement of the omnivorous

feeding habit by increasing efficiency,

whenmotility is increased. The complex folding of intestinal mucosa with increased surface

area aids in mixing of food with hepatic,

pancreatic juices as well as with mucous

secreted by goblet cells. Similar results and finding are reported in Mugil cephalus (El-

Bakary and El-Gammal 2010), in Seriola dumerili (Grau et al., 1992) and in teleostean

(Khanna, S.S. 1971). The amount of mucosal

fold in the middle and distal region were found

to be less as compared to proximal region in Clarias batrachus.

The intestine of Clarias batrachus contains

goblet cells in the mucosa of proximal, middle

and distal intestine. The population of goblet

cells increases toward the distal intestine

observed in the present study. This result of

increasing number of goblet cells is in accordance with the reports in fish such as rice field eel and flower fish Pseudophoxinus

antalyae (Cinar and Senol, 2006). The

increase amount of goblet cells may be

required for increased mucosal safety and lubricant for faecal exclusion (Dai et al., 2007).

These goblet cells react positively with PAS

and AB, representing that they contain neutral

as well as acidic glycoproteins (Cinar and Senol, 2006; Sucmez and Ulus, 2005, Bucke,

1971 and Radaelli 2000). Neutral mucosubstances combine with alkaline

phosphate involve in emulsification of food into

chyme in vertebrates. Acidic mucins act to

protect the intestinal epithelium against the enzyme glycosidase (Carrasson et al., 2006).

Thus, the present investigations of histological

studies of the intestine were similar to those

reported of other teleost, cat fishes and also

vertebrates. However there were some

variations observed in the presence of gastric

glands in pyloric region of stomach and goblet

cells were abundant towards the posterior

intestinal part of Clarias batrachus. The

histochemical finding showed positive for PAS

and AB in the intestinal region.

B. Ultrastructural study:

According to its feeding habits Clarias




batrachus may consider as an omnivorous cat

fish. Variation in the gut region is found generally in omnivorous fishes (Kapoor et al.,

1975). The ultrastructural study of intestine

show the epithelial lining of absorptive cell

from proximal intestine contains the usual organelles and the regular microvilli which

increase the surface area of the intestine. The

cytoplasmic channels, lysosomal system,

microtubules, small vesicles (pinocytotosis)

are typical features of the lining cells of the proximal, middle as well as distal intestine

region. In this study, the presence of microvilli,

tight junctional complexes, lysosome and

mitochondria in the enterocytes, are similar to

those observed in the freshwater fishes (Kuperman and Kuzmaina, 1994), in Solea solea (MacDonald, 1987), in Tilapia spp.

(Gargiulo, et al., 1998), in Solea senegalensis

(Arellano, 2002), in Orthrias angorae (Sucmez

and Ulus 2005) and in Oncorhynchus mykiss

(Banan Khojasteh et al., 2009).

The presence of the pinocytotic inclusion

provides evidence that an intracellular protein digestion in the intestinal region may be important in the fish species (Gargiulo et al.,

1998). Another feature of the mucosa of the

proximal, middle as well as the distal intestine of C. batrachus is the presence of the lamellar

structure in the cytoplasm. This structure is similar to those found in the cytoplasm detected in the Senegal sole intestine

(Arellano, 2002). While, they were extreme in

the intestine of different larvae as well as adult

fishes (Noaillac-Depyre and Gas, 1979; Calzada, et al., 1998). The lamellar structures

increase the surface area of membrane that

contact with the extracellular spaces maybe

facilitating lipoprotein transport.The

contribution of these intestinal membrane

infoldings in the transport of lipoprotein has been recommended (Deplano et al., 1991).

While in Sparus aurata, they are associated

with the mitochondria in the basal cytoplasm (Calzada et al., 1998). Moreover occurrences

is probably due to increase demand of energy

for process of osmoregulation, since the gut is the main organ for absorbing the water for

maintain the water as well as ion balance in

case of marine fish species (Tytler and Ireland,

1994)

The endocrine cells are restricted to the proximal intestine (Gargiulo et al., 1998)

whereas in the present study the endocrine

cells are found in the proximal, middle as well as in the distal intestinal region in C.

batrachus. We are first to report, the presence

of endocrine cells in the intestine of C. batrachus. On the basis of the present

ultrastructural result three types of

enteroendocrine cells can be distinguish in the

proximal, middle as well as the distal intestine of C. batrachus. Mainly these cells are of the

open type. This kind of cells may be receptor-sensory, receiving specific chemical

information from top so as to stimulate or

inhibits the secretion at the base (Fujita and

Kobayashi, 1974). This hypothesis is

supported by the presence of microvilli, small vesicles (pinocytosis) and longitudinal

microtubules in the apical end of the endocrine

cell. These features are also described in

receptor cells of taste buds (Murray, 1973).

Some closed types of endocrine cells are also found in the middle and proximal intestine.

Fujita and Kobayashi reported that this cell

type stimulate by the physiological stimuli

(Pressure, tension and temperature). Both

open and closed type of cells may be receiving

humoral stimuli from the bloodstream that influence the release of granules.

In conclusion, the histological, histochemical

and ultrastructural feature of the proximal

middle and the distal intestine of Clarias

batrachus revealed an adaptation for the

feeding habits and this is important for the

protection and increasing of the absorptive

processes.

Acknowledgment: We are special thanks to

Dept. of Anatomy, All India Institute of Medical

Science, New Delhi, (INDIA) for providing

Electron Microscope Facility.

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