Veterinarski arhiv 69 2

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VETERINARSKI ARHIV = 69 (2),=20 63-68, 1999

ISSN 1331-8055 Published = in=20 Croatia

Response of aerial = respiratory=20 organs of the
air-breathing catfish Heteropneustes fossilis=20 (Bloch)
to extreme stress of desiccation

Ram Sanehi Parashar = and Tarun=20 Kumar Banerjee*

Histochemistry and = Histopathology=20 Laboratory, Department of Zoology,
Banaras Hindu University, = Varanasi, India=20

* Contact address:
Dr. = Tarun Kumar=20 Banerjee,
Histochemistry and Histopathology Laboratory, Department = of=20 Zoology, Banaras Hindu University, Varanasi-221 005, India,
Phone: = 91-542=20 318 372; Fax: 91 542 317 074; E-mail: tarun@banaras.ernet.in

PARASHAR, R. S., T. K. = BANERJEE:=20 Response of aerial respiratory organs of the air-breathing catfish=20 Heteropneustes fossilis (Bloch) to extreme stress of desiccation. = Vet.=20 arhiv 69, 63-68, 1999.

ABSTRACT =

Histopathological = alterations caused by=20 desiccation stress in the aerial (accessory) respiratory organs (ARO) of = Heteropneustes fossilis which has a developed bimodal respiratory = mechanism for exploitation of water (through its gills) as well as air = (through=20 its ARO) have been described. The ARO assist the fish in surviving = extreme=20 drought conditions. When out of water, even though the fish survive for = about 16=20 h, their air sacs suffer extensive damage. In the initial stages the = fish very=20 frequently open their mouths to gulp in more air. The blood channels of=20 secondary lamellae of the ARO, engorged with ridged blood channels, = exhibit=20 extensive protrusion into the lumen where they form a network of very=20 thin-walled tube-like structures. Prolonged desiccation causes wear and = tear to=20 these greatly extended blood channels, leading to haemorrhaging into the = lumen.=20 Simultaneously, from the blind ends of the ARO, many of the ridges = approach very=20 close to each other and finally meet, leaving no free respiratory = surface in the=20 lumen to breathe aerially, ultimately resulting in failure of aerial = respiration=20 and the demise of the fish.

Key words: = accessory respiratory=20 organs, desiccation, Heteropneustes fossilis, histopatho-logy,=20 air-breathing catfish, India

Introduction =

Heteropneustes = fossilis, the=20 tropical air-breathing fish of the Indian subcontinent, inhabits = derelict water=20 bodies having poor O₂ conditions. These fish have a developed = bimodal=20 respiratory mechanism for exploitation of water (via its four pairs of=20 teleostean gills) as well as air (via air-breathing organs, ARO). Hence, = they=20 are able to withstand extreme drought conditions, especially when ponds = become=20 dried up during the long summer period (MUNSHI, 1962, 1963). Also, it = has been a=20 common practice to transport these fish in bamboo baskets, where they = remain=20 alive even when they are out of the water for several hours. ARO in this = fish=20 are a pair of sac-like structures which lie deeply embedded in the body = myotomes=20 at the trunk region of both sides of the vertebral column. The ARO are = adapted=20 to perform aerial respiration only and never come into direct contact = with the=20 aquatic environment.

Therefore, efforts were = made to=20 discover the histophysiological alterations taking place in the ARO of = the=20 air-breathing catfish Heteropneustes fossilis prior to their = death, while=20 combating desiccation stress and prevention of branchial respiration by=20 performing aerial respiration only when the fish are subjected to = extreme stress=20 of desiccation. The efficacy of ARO in maintaining life has also been = observed.=20

Materials and methods=20

Healthy specimens of = Heteropneustes=20 fossilis (35-40 g body mass, 18-20 cm in length) were collected from = a=20 single population at Varanasi and were acclimated for one month in tap = water=20 (having dissolved O₂, 6 mg/l, pH 7.5, water hardness 23.2 = mg/l and=20 water temperature 24=B12 =B0C) in large plastic aquaria in a laboratory. = They were=20 fed with minced goat liver on alternate days and the water was renewed = every 24=20 h, leaving no faecal matter, unconsumed food or dead fish, if any. = Feeding=20 ceased 24 h prior to the commencement of the experiment, with starvation = continuing throughout the period of the experiment.

Four groups of ten = acclimated fish=20 (15=B11 cm in length) were removed from water and placed on dry plastic = aquaria in=20 the laboratory for exposure to the air (atmospheric humidity 69%, room=20 temperature 27 to 30 ^oC) for 16 h, beyond which they rarely = survived.=20 Control groups of fish were retained in tap water.

After the expiry of 0, 6, = 12 and 16 h=20 of desiccation, five fish each from the experimental aquaria, as well as = from=20 the control aquaria, were sacrificed. The entire branchial diverticulum = (air=20 sac) from both sides of the fish was fixed in 10% neutral formalin and = aqueous=20 Bouin's fluid. Six =B5m paraffin sections were stained with Ehrlich's or = Harris=20 haematoxylin and alcoholic eosin (H/E) for routine histopathological = analysis.=20 Certain carbohydrate moieties were visualised by periodic acid-Schiff = (PAS)=20 after McManus, 1946, Alcian blue pH 2.5 (AB 2.5), AB 2.5/PAS, Alcian = blue pH 1.0=20 (AB 1.0) and salivary amylase/PAS (PEARSE, 1985) techniques.

Results and Discussion =

Control accessory = respiratory organ=20

The inner respiratory = surface of the=20 ARO, which is thrown into several folding or papilla-like ridges, is = lined at=20 its inner surface with stratified epithelium (Fig. 1) and consists of = vascular=20 and non-vascular areas. The vascular areas are characterised by the = presence of=20 small and large respiratory islets (MUNSHI 1962, 1980, 1993). An islet = (primary=20 lamella) is formed by double rows of secondary lamellae (SL), which hang = freely=20 into the lumen. In the transverse section, the SL penetrate = perpendiculary into=20 the stratified epithelium. The SL is composed of alternately arranged = blood=20 channels (BC) and pillar cells (PC). Within the blood channels, one or = two blood=20 cells are generally noticed. The single-layered respiratory epithelium = separates=20 the blood in the SL from the air in the lumen of ARO. Mucous cells (MCs) = (secreting non-sulphated acidic mucin) and epithelial cells (ECs) = constitute the=20 non-vascular areas. A thin layer of slime sometimes covers the = epithelial=20 surface.

Next to the epithelium, = and serially=20 arranged, are basement membrane, connective tissue, a thin membrane and = muscular=20 coat. The fish regularly raises its snout above the surface of the water = to=20 engulf air for aerial respiration and takes 40% of O₂ through = its air=20 sacs in saturated waters (bearing 3% O₂) (MUNSHI and = CHOUDHARY,=20 1994). Desiccation stress prevents normal branchial respiration. Hence, = gasping=20 for air in these fish increased during the initial stages of the = experiment.=20

Fig. 1. Transverse = section of the air=20 sac of control H. fossilis,
showing its structural = organisation. Note=20 the enormous space in the lumen (L). (PAS; =D735)
Fig. 2. Collapse of = the air=20 sac following 6 h of desiccation. Note the gluing of the respiratory = epithelia=20 of two approaching ridges. (HE; =D735)
Fig 3. Air sac of 16 h = desiccated fish,=20 showing disappearance of air space in the lumen (L) due to adhesion of=20 epithelial linings of closely approximated neighbouring ridges. Note the = strong=20 reaction in the mucous cells and the slimy secretion for sulphated=20 mucopolysaccharides. (Alcian blue/PAS reaction; = =D7200)

E=3Depithelium;=20 F=3Dfurrows, L=3Dlumen; MC=3Dmucous cells; P=3Dpigment cells; = R=3Dridges; S=3Dslime.=20

Desiccated accessory = respiratory=20 organ

Following desiccation the = structure of=20 the air sacs of the desiccated fish showed massive damage. The immediate = response to the ARO is manifested by an enormous increase in density of = RBC in=20 the channels of the SL, which become greatly extended and distend into = the=20 lumen. Thus, the blood channels of the SL protrude into the lumen as=20 balloon-like projections. Subsequently, these channels form a network of = very=20 thin-walled, blind tube-like structures over the epithelial surface. = More=20 engorging of the blood channels continues as desiccation progresses. The = gravity=20 of these thin-walled, tubular structures thus increases, causing the = bending of=20 the blood channels of the SL, bending at 90=B0 to lie flat on the inner = surface of=20 the air sac. The network of thin-walled vascular channels also spread = over the=20 non-vascular areas. The extensive network of the existing fine blood = vessels in=20 the connective tissue immediately below the respiratory epithelium=20 simultaneously becomes engorged with RBC. All these manifestations = substantially=20 decrease the barrier distance between the air in the lumen and the blood = in the=20 sac-like SL. It is thought possible that this may increase the efficacy = of the=20 air sac, albeit temporarily, by compensating for the failure of brachial = respiration. JOHANSEN et al. (1970) reported that when gill-breathing in = a=20 primitive air-breather, Amia calva varies reciprocally with = O₂=20 tension of the air-breathing organ because blood bypasses the gas = exchange blood=20 vessels of the gills where it is not the primary site for O₂ = uptake.=20 This is also true of H. fossilis, which could survive for several = hours=20 even though the blood channels in the gills (PARASHAR and BANERJEE, = 1998) also=20 show extensive engorgement with RBCs, mostly in the initial stages of=20 desiccation. Prolongation of dehydration beyond 16 h due to prolonged=20 desiccation causes wear and tear of these thin-walled extensively = stretched=20 blood channels of the SL of the gills of H. fossilis, leading to = severe=20 haemorrhaging and resulting in failure of branchial respiration = (PARASHAR and=20 BANERJEE, 1998).

From the blind end of the = air sacs,=20 many of the ridges come very close to each other and ultimately meet. = This=20 blocks the free surface of the respiratory epithelium, causing a = considerable=20 reduction in the volume of the lumen of the air sac and leaving very = little=20 space for aerial respiration (Fig. 2). Often, a slightly eosinophilic, = weakly=20 PAS positive viscous material of varying thickness glues the inner = surfaces of=20 the two approaching ridges and chokes the lumen (Fig. 3). The MCs of the = ARO of=20 the desiccated fish alter their staining property to secrete sulphated = mucin and=20 keep the surface of the ARO moist for longer periods. However, all these = attempts to keep the ARO moist in order to maintain aerial respiration = does not=20 last long, and the fish dies, ultimately due to haemorrhaging, = dehydration of=20 vital organ systems and the collapse of many vital physiological = processes (e.g.=20 CO₂ and N₂ elimination) resulting in total = asphyxiation=20 due to failure of (aerial) respiration. Regular sprinkling of water = increases=20 the survival period of the desiccating fish due to renewal of the water=20 molecules, which helps to maintain respiratory, as well as secretory = processes=20 through the skin and gills (PARASHAR and BANERJEE, 1998). The other = important=20 cause of death, which perhaps hastens the death, of this air-breathing = fish is=20 the retention of toxic metabolic substances, such as CO₂ and=20 N₂, which in fish/amphibians are generally eliminated via the = skin/gills (HUGHES, 1966) because H. fossilis releases very = little=20 CO₂ into the air through its air-sacs (R.Q. being only 0.17) = when it=20 respires in water (MUNSHI, 1993). Further, the CO₂ tolerance = limit of=20 H. fossilis is high in comparison to other (mostly pure = water-breathing)=20 fish. Thus, the gas exchange continues for a considerable length of = time, even=20 when the CO₂ level in the water body of this fish is high = (14.5% by=20 volume of air, MUNSHI, 1993), and the fish survive for longer periods.=20

Acknowledgements
This = work was=20 supported by a grant-in-aid from the University Grants Commission, = Government of=20 India, New Delhi. Research Project No. F 3-55/93 (SR-II)

References =

HUGHES, G. M. (1966): = Evolution between=20 air and water. In: Ciba Foundation symposium on Development of the lung = (A. V.=20 S. de Reuck and R. Porter, Eds.). Churchill Ltd., London. pp. 64-80. =

JOHANSEN, K., D. HANSON, = C. LENFANT=20 (1970): Respiration in a primitive air-breather, Amia calva. Res. = Physiol. 9, 162-174.

MUNSHI, J. S. D. (1962): = On the=20 accessory respiratory organs of Heteropneustes fossilis Bloch. = Proc Royal=20 Soc Edinberg. 68, 128-146.

MUNSHI, J. S. D. (1980): = The structure=20 and function of the respiratory organs of air-breathing fishes of India=20 Sectional (Zool. Entomol. and Fisheries) Presidential Address, Proc=20 67^th Session, Indian Sci. Association. Part II. pp. 1-70. =

MUNSHI, J. S. D. (1993): = Structure and=20 function of the air-breathing organs of Heteropneustes fossilis. = In:=20 Advances in Fish Research I (Singh, B. R., Ed.). Narendra Publishing = House.=20 Delhi India. pp. 99-138.

MUNSHI, J. S. D., S. = CHOUDHARY (1994):=20 Ecology of Heteropneustes fossilis (Bloch): an air-breathing = catfish of=20 South East Asia. Freshwater Biological Association of India Bhagalpur, = India.=20

PARASHAR, R. S., T. K. = BANERJEE (1998):=20 Response of gills of the air-breathing catfish Heteropneustes = fossilis to=20 desiccation stress. (in press)

PEARSE, A. G. E. (1985):=20 Histochemistry-Theoretical and applied. Vol. II. Edinburgh, London. = Churchill=20 Livingstone Inc. pp. 441-1055.

Received: 4 May = 1998
Accepted: 30=20 March 1999

PARASHAR, R. S., T. K. = BANERJEE:=20 Odgovor zracnih disnih organa ribe dvodihalice Heteropneustes = fossilis=20 (Bloch) na ekstremni stres isusivanja. Vet. arhiv 69, 63-68, 1999. =

SAZETAK =

Opisane su histopatoloske = promjene,=20 izazvane stresom isusivanja, zracnih (pomocnih) disnih organa u = dvodihalice=20 Heteropneustes fossilis koja je razvila dvostruki disni = mehanizam, i to=20 iz vode (putem skrga) i iz zraka (putem zracnih disnih organa). Ribe s = zracnim=20 disnim organima prezivljavaju ekstremne susne uvjete. Kada su izvan vode = prezivljavaju oko 16 sati i tada njihove zracne vrecice trpe opsezna = ostecenja.=20 U pocetnoj fazi, riba cesto otvara usta kako bi uzela vise zraka. Zracni = kanali=20 sekundarnih listica zracnih disnih organa obuhvaceni s grebenastim = krvnim=20 kanalima pokazuju znatnu protruziju u lumen gdje tvore mrezu cjevolikih=20 struktura vrlo tankih stijenki. Produljeno isusivanje uzrokuje trosenje = i=20 kidanje tih jako izduzenih krvnih kanalica i posljedicno krvarenje u = lumen.=20 Istovremeno u slijepim krajevima zracnih disnih organa mnogi se grebeni=20 medusobno priblizavaju i spajaju, te tako vise ne ostavljaju slobodnu = zracnu=20 disnu povrsinu s konacnim zakazivanjem zracnog disanja i ugibanjem ribe. =

Kljucne rijeci: = pomocni disni=20 organi, isusivanje, Heteropneustes fossilis, histopatologija,=20 dvodihalica, Indija

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