Histopathology of respiratory organs of certain air-breathing fishes of India

Fish Physiology and Biochemistry - Tập 33 - Trang 441-454 - 2007
T. K. Banerjee1
1Histopathology Laboratory, Centre of Advanced Study in Zoology, Department of Zoology, Banaras Hindu University, Varanasi, India

Tóm tắt

Air-breathing fishes have evolved bimodal respiratory mechanisms for exploitation of water (through gills and highly vascularized skin) as well as atmospheric air (through aerial respiratory organs, ABO). Mucous cells in these respiratory organs of variously stressed fishes exhibit periodic fluctuations in their density and staining properties. The main types of damage in the gills include congestion of blood capillaries (BLCs), periodic lifting and sloughing of respiratory epithelia of the secondary lamellae causing haemorrhage, extensive fusion of secondary lamellae and hyperplasia of the respiratory epithelia due to uncontrolled regeneration leading to asphyxiation, altered excretion, and death of the fish. Haemolysis has also been observed following lead exposure. The damage in the ABO of Heteropneustes fossilis includes sloughing of the epithelial cells, leading to haemorrhage causing decreased red blood corpuscles density and degeneration of the secondary gill lamellae with reduced respiratory area. Subsequent hyperplasia of the respiratory epithelia and fusion of gill lamellae increase the respiratory barrier distance. The BLCs often bulge out and protrude into the lumen, bringing blood nearer to air. The ladder-like pillar cell (PLC)-BLC components of the gill lamellae frequently collapse. Damage to the ABO of Channa striata is less severe. Often haemorrhaging due to bursting of extensively stretched BLCs causes aerial respiratory failure. Chloride cells of the ABOs also show hyperplasia. While the highly mucogenic epidermis of C. striata shows less damage, the epidermis of Clarias batrachus and H. fossilis shows severe wear and tear, sloughing, and haemorrhage. Side-by-side regeneration continues, causing altered histomorphology of the epidermis. The different gland cells also show periodic fluctuations in their density and staining. The dermis also shows severe damage with loosening of their connective tissue fibres. These fibres give stronger reactions for sulfated mucin that not only retain additional water molecules for continuance of skin breathing, but also bind the toxic ambient pollutants.

Tài liệu tham khảo

Arillo A, Melodia F (1990) Protective effect of fish mucus against Cr (VI) pollution. Chemosphere 20:397–402 Banerjee TK (1993) Response of fish skin to certain ambient toxicants. In: Singh BR (ed) Advances in fish research, vol I. Narendra Publishing House, New Delhi, pp 185–192 Banerjee TK, Chandra S (2005) Estimation of toxicity of zinc chloride by histopathological analysis of the respiratory organs of the air breathing ‘murrel’ Channa striata (Bloch, 1797) (Channiformes, Pisces). Vet Arhiv 75:253–263 Banerjee TK, Mittal AK (1975) A cytochemical study of the chloride cells in the skin of a fresh water teleost (Channa striata (Bl.) Channidae, Pisces). Acta Histochem 52:126–135 Banerjee TK, Mittal AK (1976) Histochemistry and functional organisation of the skin of a ‘live-fish’ Clarias batrachus (Linn.) (Clariidae, Pisces). Mikroskopie 31:333–349 Banerjee TK, Parashar RS (2005) Histopathological analysis of toxic impact of lethal concentration of lead nitrate on the air-breathing organs of the ‘livefish’ Heteropneustes fossilis (Bloch). Acta Zool Taiwan 15:11–20 Banerjee TK, Paul VI (1993) Estimation of acute toxicity of ammonium sulphate to a fresh-water catfish, Heteropneustes fossilis II. A histopathological analysis of the epidermis. Biomed Environ Sci 6:45–58 Bradley RW, Sprague JB (1985) The influence of pH, water hardness, alkalinity on the acute lethality of zinc to rainbow trout (Salmo gairdneri). Can J Fish Aquat Sci 42:731–736 Burton DT, Jones AH, Caims J Jr (1972) Acute zinc toxicity to rainbow trout (Salmo gairdneri): confirmation of the hypothesis that death is related to tissue hypoxia. J Fish Res Board Can 29:1463–1466 Chandra S, Banerjee TK (2003) Histopathological analysis of the respiratory organs of Clarias batrachus (Linnaeus) subjected to the stress of air-exposure. Acta Zool Taiwan 14:45–64 Chandra S, Banerjee TK (2004) Histopathological analysis of the respiratory organs of Channa striata subjected to air-exposure. Vet Arhiv 74:37–52 Coombs TL, Fletcher TC, White A (1972) Interaction of metal ions with mucus from the plaice Pleuronectes platessa (L.). Biochem J 128:128–129 Dalela RC, Bhatnagar MC, Tyagi AK, Verma SR (1979) Histological damage of gills in Channa gachua after acute and subacute exposure to endosulphan and Rogore. Mikroskopie 35:301–307 Daoust PY, Wobeser G, Newstead JD (1984) Acute pathological effects of inorganic mercury and copper in gills of rainbow trout. Vet Pathol 21:91–101 Devi R, Banerjee TK (2003) Histopathological analyses of the toxic impact of the inorganic fertilizer, ammonium sulphate on the respiratory organs of the air breathing ‘murrel’ Channa striata (Bloch.) (Pisces). In: Proceedings of the. XXI symposium on reproduction. biology & comparative endocrinology. pp. 339–356 Devi R, Banerjee TK (2006) Analyses of toxicity rendered by lead nitrate on the skin (an accessory respiratory organ) of the air-breathing murrel Channa striata. Biochem Cell Arch 6:188–199 Dutta HM (1997) A composite approach for evaluation of the effect of pesticides on fish. In: Munshi JSD, Dutta HM (eds) Fish morphology: horizons of new research. Science Publishing Inc., USA, pp 249–277 Dutta HM, Munshi JSD, Roy PK, Singh NK, Adhikari S, Killius J (1996) Ultrastructural changes in the respiratory lamellae of the catfish, Heteropneustes fossilis after sublethal exposure to malathion. Environ Pollut 92:329–341 Fischer-Scherl T, Hoffmann RW (1988) Gill morphology of native brown trout, Salmo trutta, m. fario experiencing acute and chronic acidification of a brook in Bavaria, F.R.G Dis Aquat Org 4:43–51 Friberg LT, Vostal D (1976) Mercury in the environment. CRC Press, Cleveland, OH Glyun AW, Norrgren L, Mussener AC (1994) Differences in uptake of inorganic mercury and cadmium in the gills of the zebra fish, Brachydanio rerio. Aquat Toxicol 30:13–26 Handy RD, Eddy FB (1991) The absence of mucus on the secondary lamellae of unstressed rainbow trout, Oncorhynchus mykiss. J Fish Biol 38:153–155 Hart RK, Oglesby GB (1979) Toxin induced changes in the gill epithelium of rainbow trout (Salmo gairdneri). Scan Electron Microsc 3:355–361 Hemalatha S, Banerjee TK (1997a) Histopathological analysis of sublethal toxicity of zinc chloride to the respiratory organs of the air-breathing catfish Heteropneustes fossilis (Bloch). Biol Res 30:11–21 Hemalatha S, Banerjee TK (1997b) Histopathological analysis of acute toxicity of zinc chloride to the respiratory organs of the air-breathing catfish Heteropneustes fossilis (Bloch). Vet Arhiv 67:1–24 Hemalatha S, Banerjee TK (1997c) Estimation of sublethal toxicity of zinc chloride by histopathological analysis of fish (Heteropneustes fossilis, Bloch) epidermis. Curr Sci 73:614–621 Hemalatha S, Banerjee TK (2003) Estimation of acute toxicity of zinc chloride by histopathological analysis of the epidermal lining of the operculum of the live-fish Heteropneustes fossilis (Bloch). Toxicol Int 10:11–22 Hughes GM, Munshi JSD (1973) Nature of air-breathing organs of the Indian fishes Channa, Amphipnous, Clarias and Saccobranchus as shown by electron microscopy. J Zool Lond 170:245–270 Hughes GM, Munshi JSD (1979) Fine structure of the gills of some Indian air-breathing fishes. J Morphol 160:169–194 Karlsson-Norrgren L, Runn P, Haux C, Forlin L (1985) Cadmium-induced changes in gill morphology of zebra fish, Brachydanio rerio (Hamilton-Buchanan), and rainbow trout, Salmo gairdneri (Richardson). J Fish Biol 27:81–95 Karlsson-Norrgren L, Dickson W, Ljundberg O, Runn P (1986) Acid water and aluminium exposure: gill lesions and aluminium accumulation in brown trout, Salmo trutta L J Fish Dis 9:1–9 Kendall MW, Dale JE (1979) Scanning and transmission electron microscopic observations of rainbow trout (Salmo gairdnerii) gill. J Fish Res Board Can 36:1072–1079 Laurent P (1984) Gill internal morphology. In: Hoar WS, Randall DJ (eds) Fish physiology, Vol. X, Part A. Academic Press, New York, pp 73–193 Leino RL, McCormick JH (1984) Morphological and morphometrical changes in chloride cells of the gills of Pimephales promelas after chronic exposure to acid water. Cell Tissue Res 236:121–128 Leino RL, Wilkinson P, Anderson DG (1987) Histopathological changes in the gills of pearl dace, Semotilus margarita, and fathead minnow, Pimephales promleas, from experimentally acidified lakes. Can J Fish Aquat Sci 44:126–134 Lock RAC (1975) Uptake of methyl mercury by aquatic organisms from water and food. In: Koeman JH, Strick JJTWA (eds) Sublethal effects of toxic chemicals on aquatic animals. Elsevier, Amsterdam, pp 61–79 Lock RAC, Van Overbeeke AP (1981) Effects of mercuric chloride and methylmercuric chloride on mucous secretion in rainbow trout, Salmo gairdneri (Richardson). Comp Biochem Physiol 69:67–73 Mallatt J (1985) Fish gill structural changes induced by toxicants and other irritants: a statistical review. Can J Fish Aquat Sci 42:630–648 Mckone CE, Young RG, Bache CA, Lisk DJ (1971) Rapid uptake of mercuric ion by goldfish. Environ Sci Technol 5:1138–1139 Mittal AK, Banerjee TK (1975a) Histochemistry and structure of the skin of a murrel, Channa striata (Bloch, 1797) (Channiformes, Channidae). I Epidermis. Can J Zool 53:833–843 Mittal AK, Banerjee TK (1975b) Histochemistry and structure of the skin of a murrel Channa striata (Bloch, 1797) (Channiformes, Channidae). II Dermis and subcutis. Can J Zool 53:844–852 Mittal AK, Banerjee TK (1980) Keratinization versus mucus secretion in fish epidermis. In: Spearman RLC, Riley PA (eds) Skin of vertebrates. Academic Press, London, pp 1–14 Mittal AK, Munshi JSD (1971) A comparative study of the structure of the skin of certain air-breathing fresh-water teleosts. J Zool Lond 163:513–532 Mittal AK, Rai AK, Banerjee TK, Agarwal SK (1976) Lipids in the skin of a catfish Heteropneustes fossilis (Bloch)(Heteropneustidae, Pisces). A histochemical investigation. Histochemistry 48:177–185 Munshi JSD (1962a) The accessory respiratory organs of Clarias batrachus (Linn.). J Morphol 109:115–139 Munshi JSD (1962b) On the accessory respiratory organs of Heteropneustes fossilis Bloch. Proc R Soc Edinburgh 68:128–146 Munshi JSD (1962c) On the accessory respiratory organs of Ophicephalus punctuatus and Ophicephalus striatus. J Linn Soc Lond (Zool) 44:616–626 Munshi JSD (1980) The structure and function of the respiratory organs of air-breathing fishes of India Sectional (Zool. Entomol. and Fisheries) Presidential Address. In: Proceedings of the 67th session, Indian Sci. Cong. Association. Part II. pp 1–70 Munshi JSD (1993) Structure and function of the air-breathing organs of Heteropneustes fossilis. In: Singh BR (ed) Advances in fish research I. Narendra Publishing House, New Delhi, pp 99–138 Munshi JSD, Choudhary S (1994) Ecology of Heteropneustes fossilis (Bloch): an air-breathing catfish of South East Asia. Freshwater Biological Association of India, Bhagalpur Munshi JSD, Singh RK (1971) Investigation of the effect of insecticides and other chemical substances on the respiratory epithelium of predatory and weed fishes. Int J Zoot 22:127–134 Munshi JSD, Singh A (1992) Scanning electron microscopic evaluation of effects of low pH on gills of Channa punctata (Bloch). J Fish Biol 41:83–89 Ojha J (1993) Functional organization of teleostean gills. In: Singh BR (ed) Advances in fish research I. Narendra Publishing House, New Delhi, pp 71–98 Olson KR, Fromm PO (1973) A scanning electron microscopic study of secondary lamellae and chloride cells of rainbow trout (Salmo gairdneri). Z Zellforsch 143:439–449 Oronsaye JAO, Brafield AE (1984) The effect of dissolved cadmium on the chloride cells of the gills of the stickleback, Gasterosteus aculeatus L. J Fish Biol 24:253–258 Parashar RS, Banerjee TK (1999a) Effect of dehydration stress on the accessory respiratory organs of the air-breathing catfish Heteropneustes fossilis (Bloch). In: Val AL, Almeida-Val VMF (eds) Biology of tropical fishes. INPA, Manaus, pp 413–425 Parashar RS, Banerjee TK (1999b) Response of the aerial respiratory organs of the air-breathing catfish Heteropneustes fossilis (Bloch) to extreme stress of desiccation. Vet Arhiv 69:63–68 Parashar RS, Banerjee TK (1999c) Response of the gills of the air-breathing catfish Heteropneustes fossilis (Bloch) to acute stress of desiccation. J Exp Zool India 2:169–174 Parashar RS, Banerjee TK (1999d) Histopathological analysis of sublethal toxicity induced by lead nitrate to the accessory respiratory organs of the air-breathing teleost, Heteropneustes fossilis (Bloch). Pol Arch Hydrobiol 46:194–205 Parashar RS, Banerjee TK (2002) Toxic impact of lethal concentration of lead nitrate solution on the gills of the air-breathing catfish Heteropneustes fossilis (Bloch). Vet Arhiv 73:167–183 Pärt P (1983) Cadmium uptake in perfused rainbow trout gills. Acta Universitatis Upsaliensis, Dissertation from the Faculty of Science 707 Pärt P, Lock RAC (1983) Diffusion of calcium cadmium and mercury in mucous solution from rainbow trout. Camp Biochem Physiol 76:259–263 Paul VI, Banerjee TK (1995) Acute toxicity of ammonium sulphate to the air-breathing organs of the live fish Heteropneustes (Saccobranchus) fossilis (Bloch). Curr Sci 68:845–849 Paul VI, Banerjee TK (1996a) Ammonium sulphate induced stress related alterations in the opercular epidermis of the livefish Heteropneustes fossilis (Bloch). Curr Sci 70:1025–1029 Paul VI, Banerjee TK (1996b) Ammonium sulphate induced stress related changes in the epidermis of the livefish Heteropneustes fossilis (Bloch). J Fish Soc Taiwan 23:31–41 Paul VI, Banerjee TK (1996c) Analysis of ammonium sulphate toxicity in the catfish Heteropneustes fossilis using mucocyte indexing. Pol Arch Hydrobiol 43:111–125 Paul VI, Banerjee TK (1996d) Ammonium sulphate induced stress related alterations in the respiratory epithelium of the air-breathing organ of the live fish Heteropneustes fossilis (Bloch). J Biosci 21:519–526 Paul VI, Banerjee TK (1997) Histopathological changes induced by ambient ammonia (ammonium sulphate) on the opercular linings of the livefish Heteropneustes fossilis (Bloch). Dis Aquat Organ 28:151–161 Peuranen S, Vuorinen PJ, Vuorinen M, Hollender A (1994) The effect of iron, humic acids and low pH on the gills and physiology of brown trout (Salmo trutta). Ann Zool Fen 31:389–396 Playle R, Wood CM (1989) Water chemistry changes in the gill microenvironment of rainbow trout: experimental observations and theory. J Comp Physiol B 159:527–537 Powell MD, Speare DJ, Burka JF (1992) Fixation of mucus on rainbow trout Onchorhynchus mykiss (Walbaum) gills for light and electron microscopy. J Fish Biol 41:813–824 Prasad MS (1988) Sensitivity of branchial mucus to crude oil toxicity in a fresh water fish Colisa fasciatus. Bull Environ Contam Toxicol 41:764–758 Prasad MS (1991) Effect of crude oil on the air-breathing organs of the striped gourami, Colisa fasciatus. A SEM study. Ecotoxicol Environ Safety 18:211–218 Rajan MT, Banerjee TK (1991) Histopathological changes induced by acute toxicity of mercuric chloride on the epidermis of a freshwater catfish Heteropneustes fossilis (Bloch). Ecotoxicol Environ Safety 22:139–152 Rajan MT, Banerjee TK (1992) Acute toxic effects of mercuric chloride on the mucocytes of the epithelial lining of the accessory respiratory organ and skin of the air breathing catfish Heteropneustes fossilis (Bloch). Biomed Environ Sci 5:325–335 Rajan MT, Banerjee TK (1993a) Histopathological changes induced by acute toxicity of mercuric chloride on the air-breathing organ (branchial diverticulum) of the livefish Heteropneustes fossilis (Bloch). Acta Hydrochim Hydrobiol 21:316–322 Rajan MT, Banerjee TK (1993b) Histopathological changes in the respiratory epithelium of the air-breathing organ (branchial diverticulum) of the live-fish Heteropneustes fossilis exposed to sublethal concentration of mercuric chloride. J Freshwater Biol 5:269–275 Rajan MT, Banerjee TK (1993c) Histopathological changes in the epidermis of the air-breathing catfish Heteropneustes fossilis exposed to sub-lethal concentration of mercuric chloride. Biomed Environ Sci 6:405–412 Rajan MT, Banerjee TK (1994a) Toxicity of fish disinfectant, malachite green to Heteropneustes fossilis and induced changes in the mucocyte density of its skin. J Freshwater Biol 6:177–182 Rajan MT, Banerjee TK (1994b) Effect of mercuric chloride on the mucocytes of the air sac and skin of the air-breathing catfish, Heteropneustes fossilis. J Freshwater Biol 6:253–258 Roy PK, Munshi JSD (1986) Scanning electron microscopic evaluation of effects of saponin on gills of the climbing perch Anabas testudineus (Bloch) (Anabantidae, Pisces). Indian J Exp Biol 24:511–516 Roy PK, Munshi JSD (1991) Malathion induced structural and morphometric changes of a fresh-water major carp, Cirrhinus mrigala (Ham.). J Environ Biol 12:79–87 Sardet C, Pisam M, Maetz J (1979) The surface epithelium of teleostean fish gill: cellular and junctional adaptations of the chloride cell in relation to salt adaptation. J Cell Biol 80:96–117 Shrivastava J, Srivastava AK (1984) Histopathology of the gills of Channa gachua exposed to sublethal concentrations of malathion and chlordane. In: Kulshrestha SK (ed) Effects of pesticides on aquatic fauna. The Academy of Environmental Biology, Muzaffarnagar, India, pp 37–44 Singh A, Munshi JSD (1996) Scanning electron microscopic evaluation of the effects of short and long term exposure of copper and mercury on the gills of Channa punctata (Bloch). J Freshwater Biol 8:51–53 Singh S, Sahai S (1984) Effect of malthion on the mortality and behaviour of two freshwater teleosts. J Environ Biol 5:165–169 Singh BR, Guha G, Munshi JSD (1973a) Fat depot in the air-breathing organs of some teleosts. Z Mikrosk Anat Forsch 87:242–248 Singh BR, Guha G, Munshi JSD (1973b) Histophysiology of the respiratory muscle of the air-sac in an air-breathing siluroid fish- Saccobranchus fossilis (Bloch). Anat Anz 133:394–405 Skidmore JF (1964) Toxicity of zinc compounds to aquatic animals with special reference to fish. Quart Rev Biol 39:227–248 Speare DJ, Mirasalimi SM (1992) Pathology of mucous coat of trout skin during an erosive bacterial dermatitis; a technical advance in mucous coat stabilisation for ultrastructural examination. J Comp Pathol 160:201–211 Temmink JHM, Bouwmeister PJ, Delong P, van den Berg JHJ (1983) An ultrastructural study of chromate induced hyperplasia in the gills of a rainbow trout (Salmo gairdnerii). Aquat Toxicol 4:165–179 Tilney RL, Hocutt CH (1987) Changes in gill epithelia of Oreochromis mossambicus subjected to cold shock. Environ Biol Fish 19:35–44 Van der Putte I, Pärt P (1982) Oxygen and chromium transfer in perfused gills of rainbow trout (Salmo gairdneri) exposed to hexavalent chromium at two different levels. Aquat Toxicol 21:42–45 Varanasi U, Makey D (1977) Uptake and release of lead and cadmium in skin and mucus of Coho salmon (Oncorhynchus mykiss). Comp Biochem Physiol 60:187–191 Venugopal B, Luckey TD (1978) Metal toxicity in mammals. II. Chemical toxicity of metals and metalloids. Plenum, New York Webb HM (1979) The chemistry, biochemistry and biology of cadmium. Elsevier, Amsterdam Wendelaar Bonga SE (1997) The stress response in fish. Physiol Rev 77:591–625 Zaccone G, Fasulo S, LoCascio P, Ainis L, Ricca MB, Licata A (1989) Effects of chronic exposure to endosulfan on complex carbohydrates and enzyme activities in gill and epidermal tissues of the freshwater catfish Heteropneustes fossilis (Bloch). Arch Biol (Bruxelles) 100:171–185