Copper induced alterations of biochemical parameters in the gill and plasma of Oreochromis niloticus

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Abstract

The main objective of this study was to determine the effects of copper exposure on copper accumulated in branchial tissue, gill Na+/K+-ATPase activity and plasma Na+, Cl, osmolality, protein, glucose and cortisol, in Oreochromis niloticus. Fish were experimentally exposed to 40 and 400 μg L 1 of waterborne copper and sacrified after 0, 3, 7, 14 and 21 days. Copper accumulation and Na+/K+-ATPase activity were determined in branchial tissue, whereas osmolality, Na+, Cl, protein, glucose and cortisol concentrations were measured in plasma samples. Gill copper accumulation increased linearly with exposure time and concentration, whereas gill Na+/K+-ATPase activity was maximally inhibited after 3 days of exposure and showed a significant negative correlation with copper tissue levels. Plasma Cl values decreased with time of exposure but only at 400 μg L 1 of copper. Plasma Na+, protein and osmolality decreased with exposure time at the highest copper concentration tested, whereas at 40 μg L 1 of copper this effect was only observed after 21 days of exposure. Plasma glucose and cortisol levels increased in a dose and time dependent manner, while showing complex fluctuations during the intermediate exposure times. In conclusion, copper induces an early maximum inhibition of gill Na+/K+-ATPase activity in O. niloticus. The subsequent slow decrease in ion plasma levels was related to compensatory mechanisms involving a non-specific stress response that appeared overcome at long-term exposures.

Introduction

Copper is one of the most abundant transition metals in nature and an essential constituent of all living tissues. However, when present at high concentrations, it becomes toxic to living organisms, including fish (Pelgrom et al., 1995b). Toxic concentrations of copper occur in nature mainly through mining and smelting, leaching from bedrock due to acid mine drainage and precipitation, and from industrial and agricultural activities (IPCS, 1998). Although the aquatic environment is frequently monitored, sublethal heavy metal concentrations may nevertheless be toxic to aquatic organisms. Subsequently, it has been suggested that the ideal aquatic pollution bio indicator relies in the study of heavy metal accumulation levels in fish organs (Handy, 1992).

Gills represent a thin and extensive surface (up to 90% of the total body surface) in intimate contact with water. They carry out three main functions, gas exchange, ion regulation and excretion of metabolic waste products. Due to the constant contact with the external environment, gills are the first target of waterborne pollutants (Perry and Laurent, 1993) and the main place for waterborne copper uptake (Campbell et al., 1999). Associated with copper accumulation, several histopathological changes occur in the branchial epithelium (Sola et al., 1995, Arellano et al., 2000, De Boeck et al., 2001, Mazon et al., 2002) followed by changes in systemic physiological parameters. The osmoregulatory disturbances induced by copper were associated with an increased epithelial permeability and inhibition of active ion uptake, subsequently to the reduction of Na+/K+-ATPase activity and a decrease in the number of active chloride cells (Laurén and McDonald, 1985, Laurén and McDonald, 1987a, Laurén and McDonald, 1987b, De Boeck et al., 2001).

Oreochromis niloticus is a widely used species in aquaculture for food supply and has been suggested as a bio indicator of water contamination (Almeida et al., 2002). The main purpose of this study is to determine the effects of copper exposure on copper accumulation, Na+/K+-ATPase activity in gill tissue, plasma ion levels, osmolality and protein and in stress response indicators such as plasma, glucose concentration and cortisol concentration, in O. niloticus.

Section snippets

Animals

Nile O. niloticus (Bouaké strain) were originally obtained from the Institute Nationale de Recherche Agronomique (Rennes, France) and raised in the Aquaculture Station of the University of Trás-os-Montes and Alto Douro (UTAD, Vila Real, Portugal) for three generations. Fish were kept in 100 L recirculating tanks (water flow rate of 5 L min 1) filled with dechlorinated tap water. Water composition was in agreement with European Community instructions (84/449/EEC Directives, Annex 5, method c1)

Gill dry weights

Gill dry weights were kept constant between groups at each time of exposure, except at day 21 where a significant decrease to controls was observed in the 40 μg Cu L 1 group (P = 0.003). Gill dry weights were also kept constant within each group along the time of exposure, with the exception of day 21 for the 40 μg Cu L 1 group, where significant decreases were observed from day 3 to day 14 (P = 0.043) and day 21 (P < 0.001) and between day 7 and day 21 (P = 0.003).

Gill copper accumulation

Copper accumulation in gill tissue

Gill copper accumulation

The basal copper concentrations found in O. niloticus gills were similar to those reported in Oreochromis mossambicus (Pelgrom et al., 1995a, Pelgrom et al., 1995b) and lower than those found in Tilapia zillii (Ay et al., 1999). Under exposure to sublethal copper concentrations, metal deposition levels were similar to those reported in Anguilla anguilla (Grosell et al., 1998b) and higher than those observed in O. mossambicus (Pelgrom et al., 1995a, Pelgrom et al., 1995b). A steady state in

Acknowledgements

This work was partially supported by the Portuguese Foundation for Science and Technology-FCT (SFRH/BD/6785/2001; UMIB) and the Spanish Ministerio de Ciencia y Tecnologia (BOS2001-4031-CO2-01).

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