Effect of hypoxia, normoxia and hyperoxia conditions on gill histopathology in two weight groups of beluga (Huso huso)

Authors

1 Department of Fisheries , Faculty of Natural Resources, University of Guilan, Somehe Sara 1144,

2 1 *, 1, 2, 3

3 000

Abstract

The influence of dissolved oxygen concentration on gill histopathology of great sturgeon (Huso huso) was evaluated in two weight classes (initial weight 280.9?49.2 g and 1217.9?138.1 g respectively). Oxygen treatments included hypoxia (2-3 mg/l), normoxia (5-6 mg/l) and hyperoxia (9-10 mg/l). The fish were acclimated to experimental tanks for one week then randomly distributed into 9 tanks in each of the initial weight classes (3 and 6 fish per tank in higher and lower initial weight classes respectively) for 8 weeks. In order to find the histopathological changes, gill samples were collected, dehydrated through ethanol series, embedded in paraffin , sectioned at 7 ?m thickness using a Leitz microtome and stained with H & E. No mortality was observed over the 8 weeks of the experimental period. There were significant differences in weight and feed intake between treatments in the both weight classes (P<0.05). Fork length showed significant differences in lower initial weight class (P<0.05). The main histopathological changes were observed in gills including: Hyperplasia, loss of secondary lamellae, hemorrhage and congestion in primary and secondary lamellae, lamellar fusion, epithelial lifting in secondary lamellae, clubbing of secondary lamellae, telangiectases, increase in melanin pigments and numerous vacuoles in primary and secondary lamellae (in hyperoxia treatment). All these lesions may reduce gill functional surface of gaseous exchange, impairing respiratory function.

Keywords


Abel, PD and Skidmore, JF (1975). Toxic effects of an anionic detergent on the gills of rainbow trout. Water Research9, 759-765.

 

Agius, C and Roberts, RJ (2003). Melano-macrophage centers and their role in fish pathology (Review). Journal of Fish Diseases 26, 499–509.

 

Arellano, JM; Storch, V and Sarasquete, C (1999). Histological changes and copper accumulation in liver and gills of the Senegales sole, Solea senegalensis. Ecotoxicology and Environmental Safety 44, 62-72.

 

Barillet, S; Larno, V; Floriani, M; Devaux, A; Adam-Guillermin, Ch (2010). Ultrastructural effects on gill, muscle, and gonadal tissues induced in zebrafish (Danio rerio) by a waterborne uranium exposure. Aquatic Toxicology 100, 295-302.

 

Brauner, CJ; Seidelin, M; Madsen, SS and Jensen, FB (2000). Effects of freshwater hyperoxia and hypercapnia and their influences on subsequent seawater transfer in Atlantic salmon (Salmo salar) smolts. Canadian Journal of Fisheries and Aquatic Sciences 57, 2054-2064.

 

Buentello, JA; Gatlin III, DM; Neill, WH, 2000. Effects of water temperature and dissolved oxygen on daily feed consumption, feed utilization and growth of channel catfish (Ictalurus punctatus). Aquaculture 182, 339–352.

 

Caliskan, M; Erkmen, B and Yerli, SV (2003). The effects of zeta cypermethrin on the gills of common guppy Lebistes reticulatus. Environmental Toxicology and Pharmacology 14, 117–120. Cengiz, EI (2006).

 

Gill and kidney histopathology in the freshwater fish Cyprinus carpioafter acute exposure to deltamethrin. Environmental Toxicology and Pharmacology 22, 200–204.

 

Crampton, V; Hølland, PM; Bergheim, A; Gausen, M and Næss, A. 2003. Oxygen effects on caged salmon. Fish Farming International, June, 26–27.

 

Dabrowski, K; Lee, K; Guz, L; Verlhac, V and Gabaudan, J (2004). Effects of dietary ascorbic acid on oxygen stress Effect of Hypoxia, Normoxia and Hyperoxia...82(hypoxia or hyperoxia), growth and tissue vitamin concentrations in juvenile rainbow trout (Oncorhynchus mykiss). Aquaculture 233: 383–392.

 

De Silva, PMCS and Samayawardhena, LA (2002). Low concentrations of lorsban in water result in far reaching behavioral and histological effects in early life stages in guppy. Ecotoxicology and Environmental Safety53, 248–254.

 

Edsall, DA and Smith, C.E (1991). Performance of rainbow trout and Snake River cutthroat trout reared in oxygen saturated water. Aquaculture90, 251–259.

 

Erkmen, B; Caliskan, M and Yerli, SV (2000). Histopathological effects cyphenothrin gills of the Lepistes reticulatus. Veterinary & Human Toxicology 42, 5–7.

 

Foss, A; Vollen, T and Øiestad, V (2003). Growth and oxygen consumption in normal and O2 supersaturated water, and interactive effects of O2 saturation and ammonia on growth in spotted wolffish (Anarhichas minorOlafsen). Aquaculture 224, 105– 116.

 

Gisberta E, Rodrı ́guezb A, Cardonac L, Huertasa M, Gallardod MA, Sarasquetee C, Sala-Rabanald M, Ibarzd A, Sa ́nchezd J and Castello ́-Orvayb F (2004). Recovery of Siberian sturgeon yearlings after an acute exposure to environmental nitrite: changes in the plasmatic ionic balance, Na+–K+ ATPase activity, and gill histology. Aquaculture 239, 141–154.

 

Good, Ch; Davidson, J; Welsh, C; Snekvik, K and Summerfelt, S (2010). The effects of carbon dioxide on performance and histopathology of rainbow trout Oncorhynchus mykiss in water recirculation aquaculture systems. Aquacultural Engineering 42, 51-56.

 

Heisler, N (1993). Acid-base regulation in response to changes of the environment: characteristics and capacity. In “Fish Ecophysiology” (ed. J. C.Rankin and F. B. Jensen), New York: Chapman and Hall. pp. 207-230.

 

Hosfeld, CD; Engevik, A; Mollan, T; Lunde, TM; Waagbø, R; Olsen, AB; Breck, O; Stefansson, S and Fivelstad, S (2008). Long-term separate and combined effects of environmental hypercapnia and hyperoxia in Atlantic salmon (Salmo salar L.) smolts. Aquaculture 280, 146–153.

 

Korai, AL; Lashari, KH; Sahato, GA and Kazi, TG (2010). Histological Lesions in Gills of Feral Cyprinids, Related to the Uptake of Waterborne Toxicants from Keenjhar Lake. Reviews in Fisheries Science 18, 157-176.

 

Laurèn, DJ and McDonald, DG (1985). Effects of copper on branchial ionoregulation in the rainbow trout, Salmo gairdneri Richardson: modulation by water hardness and pH. Journal of Comparative Physiology B 155, 635-644.

 

Lillie, RD (1954). Histopathological Technique and Practical Histochemistry. New York: The Blakiston Company.

 

Lygren, B; Hamre, K and Waagbø, R (2000). Effect of induced hyperoxia on the antioxidant status of Atlantic salmon (Salmo salar L.) fed three different levels of dietary vitamin E. Aquaculture and Research 31, 401–407.

 

Macchi, GJ; Romanol, A and Christiansen, HE (1992). Melanomacrophage centers in white mouth croaker Micropogonias furneri, as biological indicators of environmental changes. Journal of Fish Biology 40, 971–973.

 

Mallatt, J (1985). Fish Gill Structural Changes Induced by Toxicants and Other Irritants: A Statistical Review. Canadian Journal of Fisheries and Aquatic Sciences 42 (4), 630-648.

 

Olson, KR; Fromm, PO and Frantz, WL (1973). Ultrastructural changes of rainbow trout gills exposed to methyl mercury or mercuric chloride. Federal Procedure, 32: 261. In: Evans, D.H., 1987. The fish gill: site of action and model for toxic effects of environmental pollutants. Environmental Health Perspectives 71,47–58.

Pane, EF; Haque, A and Wood, CM (2004). Mechanistic analysis of acute, Niinduced respiratory toxicity in the rainbow trout (Oncorhynchus mykiss): an exclusively branchial phenomenon. Aquatic Toxicology 69, 11-24. BagherzadehLakani et al., 83

 

Pichavant, K; Person-Le-Ruyet, J; Le Bayon, N; Severe, A; Le Roux, A and Boeuf, G (2001). Comparative effects of long-term hypoxia on growth, feeding and oxygen consumption in juvenile turbot and European sea bass. Journal of Fish Biology, 59 (4): 875 – 883.

 

Rafatnezhad, S and Falahatkar, B (2011). Nitrogenous compounds and oxygen concentration as the key density dependent factors to optimize growth of beluga, Huso huso (Actinopterygii: Acipenseriformes: Acipenseridae), in circular fiberglass tanks. Acta Ichthyologica. Piscaoriat. 41 (4): 285–291.

 

Reiser, S; Schroeder, JP; Wuertz, S; Kloas, WR and Hanel, W (2010). Histological and physiological alterations in juvenile turbot (Psetta maxima, L.) exposed to sublethal concentrations of ozone-produced oxidants in ozonated seawater. Aquaculture 307, 157-164.

 

Reiser, S; Wuertz, S; Schroeder, JP; Kloas, WR and Hanel, W (2011). Risks of seawater ozonation in recirculation aquaculture – Effects of oxidative stress on animal welfare of juvenile turbot (Psetta maxima, L.). Aquatic Toxicology 105, 508-517.

 

Ritola, O; Tossasvainen, K; Kiuru, T; Lindstorm-seppa, P; Molsa, H (2002). Effect of continuous and episodic hyperoxia on stress and hepatic glutathione levels in one-summer old rainbow trout (Oncorhynchus mykiss). Applied Ichthyology, 18, 159-164.

 

Rodrigues, RV; Schwarz, MH; Delbos, BC; Carvalho, EL; Romano, LA and Sampaio, LA (2011). Acute exposure of juvenile cobia Rachycentron canadumto nitrate induces gill, esophageal and brain damage. Aquaculture 322-323, 223-226.

 

Salas-Leiton, E; Cánovas-Conesa, B; Zerolo, R; López-Barea, J; Cañavate, JP and Albama, J (2009). Proteomics of juvenile Senegal sole (Solea senegalensis) affected by gas bubble disease in hyperoxygenated ponds. Journal of Marine Biotechnology 11, 473–487.

 

Schwaiger, J; Ferling, H; Mallow, U; Wintermayr, H and Negele, RD (2004). Toxic effects of the non-steroidal anti-inflammatory drug diclofenac. Part I. Histopathological alterations and bioaccumulation in rainbow trout. Aquatic Toxicology 68, 141-150.

 

Sharifpour, I; Rezvani Gilkolaei, S and Kazemi, R (2011). Histopathology of some important organs of perch (Sander lucioperca) and salmon (Salmo trutta caspius) in the southern Caspian Sea with emphasis on pollutants. Iranian Scientific Fisheries Journal 19, 77-86.

 

Thorarensen, H., et al., (2010). The effect of oxygen saturation on the growth and feed conversion of Atlantic halibut (Hippoglossus hippoglossus L.), Aquaculture 309, 96-102.

 

Van Heerden, D; Vosloo, A and Nikinmaa, M (2004). Effects of short-term copper exposure on gill structure, methallothionein and hypoxia-inducible factor- 1á (HIF-1á) levels in rainbow trout (Oncorhynchus mykiss). Aquatic Toxicology 69, 271-280.

 

Velasco-Santamaría, YM and Cruz-Casallas, PE (2008). Behavioural and gill histopathological effects of acute exposure to sodium chloride in moneda (Metynnis orinocensis). Environmental Toxicology and Pharmacology 25, 365-372.

 

Velmurugan, B; Selvanayagama, M; Cengiz, EI and Unlu, E (2007). Histopathology of lambda-cyhalothrin on tissues (gill, kidney, liver and intestine) of Cirrhinus mrigala. Environmental Toxicology and Pharmacology 24,286–291.

 

Wang, T; Lefevre, S; Huong, DTT; Cong, NV; Bayley, M, 2009. Effects of hypoxia on growth and digestion. In: Richards, J., Brauner, C.J., Farrell, A.P. (Eds.), Fish Physiology, Vol. 27. Academic Press, San Diego, CA, pp. 361–396.

 

Person-Le Ruyet, J., Pichavant, K., Vacher, C., Le Bayon, N., Sévère,A., Boeuf, G., 2002. Effects of O2 supersaturation on metabolismand growth in juvenile turbot (Scophthalmus maximus L.).Aquaculture 205, 373–383.