Elsevier

Aquatic Toxicology

Volume 83, Issue 1, 5 June 2007, Pages 62-72
Aquatic Toxicology

Dietary copper exposure in the African walking catfish, Clarias gariepinus: Transient osmoregulatory disturbances and oxidative stress

https://doi.org/10.1016/j.aquatox.2007.03.014Get rights and content

Abstract

There are few dietary Copper (Cu) toxicity studies on warm water fish. We used the African walking catfish (Clarias gariepinus) to perform the first in vivo dietary Cu toxicity study on this species. We measured end points normally associated with metal toxicity (nutritional performance, haematology, histology, tissue Cu, Na+, and K+, Na+K+-ATPase activity) and add to the limited data on oxidative stress during dietary Cu exposure (thiobarbituric acid reactive substances or TBARS, and total glutathione). Clarias gariepinus were fed to satiation on a Cu-loaded diet (1500 mg Cu kg−1 dw feed), or a control diet (15 mg Cu kg−1 dw feed), for 30 days. Dietary copper exposure caused elevated Cu concentrations in the intestine (20 fold), liver (5 fold) and gills (4 fold) of Cu-exposed fish compared to controls after 30 days (ANOVA, P < 0.05). Copper-exposed fish showed a reduction in food intake and specific growth rate (SGR), but only very modest reductions in mean body mass at the end of the experiment (the latter not statistically significant). There were no treatment-dependent effects on food conversion ratio or proximate composition, and only transient disturbances to tissue electrolytes and Na+K+-ATPase activity. Haematology was normal throughout the experiment. Cu-exposed fish showed an increase in TBARS in the gill (1.5 fold) and intestine (2 fold increase) compared to the controls (ANOVA or Kruskal–Wallis, P < 0.05). Total glutathione content in the intestine of Cu-exposed fish doubled by the end of the experiment compared to controls, reaching 12.7 ± 2.85 μmol g−1 wet weight (mean ± S.E.M., n = 6, Student's t-test, P < 0.05). The liver showed some glycogen depletion consistent with reduced food intake, but no overt pathologies in the gills, liver or intestine were observed.

Introduction

There is now a considerable literature on dietary copper (Cu) exposure in fish (reviews, Handy, 1996, Clearwater et al., 2002, Handy et al., 2005) and laboratory studies have addressed several issues including Cu metabolism (Grosell et al., 1998), growth and survival (Clearwater et al., 2002), physiological and behavioural effects (Handy et al., 1999, Kamunde et al., 2001, Campbell et al., 2005), Cu levels for aqua feeds (Berntssen et al., 1999a, Berntssen et al., 1999b), and interactions of dietary salt and aqueous Cu exposure (Kjoss et al., 2005, Niyogi et al., 2006). However, most of this ecotoxicological research has been on temperate water species, especially trout and salmon. There are only a few reports of dietary Cu exposure in warm water species of fish.

The nutritional Cu requirements of a few warm-water fish have been suggested (e.g. Oreochromis hybrids, about 4 mg Cu kg−1 feed, Shiau and Ning, 2003). The nutritional Cu requirements of African walking catfish (Clarias gariepinus, Burchell, 1822) are uncertain, but the fish are healthy and grow on typical aqua feeds containing around 10 mg Cu kg−1, and their general nutritional requirements are broadly similar to other teleosts (Baker et al., 1997). The toxicological information on warm-water species is mostly limited to studies on growth performance. Dietary Cu levels of around 16 mg kg−1 food depress growth in the channel catfish, Ictalurus punctatus (Murai et al., 1981), and Nile tilapia fed 1500 mg Cu kg−1 dry weight (dw) of feed for 42 days showed decreased growth rate with post-exposure hepatic lipidosis (Shaw and Handy, 2006). Clarias gariepinus remains an important aquacultural species in Africa and Asia (Chimatiro, 1998, De Silva et al., 2006), and are grown in areas heavily contaminated from copper mines (Syakalima et al., 2001). This has prompted studies on aqueous Cu toxicity to African walking catfish (e.g. Kotze et al., 1999, Van Vuren et al., 1994), but apart from some in vitro studies on the gut (Handy et al., 2000, Handy et al., 2002), dietary Cu toxicity has not been systematically investigated in this species from an ecotoxicological perspective.

The overall aim of this study was to add to the sparse literature on dietary Cu toxicity to warm-water species of fish by overviewing the toxic effects of dietary Cu in vivo to the African walking catfish. The study also contributes to the limited literature demonstrating oxidative stress during dietary Cu exposure in fish (e.g. Baker et al., 1998, Berntssen et al., 2000) and partly compliments existing in vitro data on the intestinal Cu uptake models in this species (Handy et al., 2000, Handy et al., 2002).

Section snippets

Experimental design

African walking catfish weighing 89.1 ± 20.4 g (mean ± S.E.M., n = 360) were obtained from Sparsholt College (Winchester, Hampshire, UK) and held for 3 weeks in stock aquaria supplied with recirculating, aerated Plymouth tap water (see Section 2.7 below for water quality) and fed to satiation on a commercial fish food (standard No. 40, Skretting, Northwich, Cheshire, UK). Fish were then graded into six 250 l experimental aquaria (65 fish in each tank) supplied with recirculating Plymouth tap water

Copper accumulation

Exposure to copper via the oral route was confirmed by large increases in the copper content of the intestine and liver compared to fish on the control diet (Kruskall–Wallis, P < 0.05), while contamination in the gills remained low (Fig. 1). Over the entire experiment, Cu levels in the intestine and liver increased 20 fold and 4.7 fold, respectively, compared to controls (Fig. 1). Copper levels in the gills of control and Cu-fed fish showed a small (but statistically significant) decrease in Cu

Discussion

This study gives new data on the chronic dietary toxicity of Cu to African walking catfish in vivo. Overall we show that the fish accumulate Cu in the intestine and liver with only marginal reductions in growth rate (not statistically significant) that are associated with reduced food intake, and reflect some depletion of hepatic glycogen stores. Changes in tissue electrolytes, Na+K+-ATPase activity, and lipid peroxidation (TBARS) suggest these fish show transient disturbances to

Acknowledgements

This study was partly supported by a grant from the Leverhulme Trust to R. Handy. Technical support from Michael Hockings and Robert Serwata is appreciated.

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