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Copper metabolism in actively growing rainbow trout (Oncorhynchus mykiss): interactions between dietary and waterborne copper uptake

Collins Kamunde^1,*, Martin Grosell^1,, Dave Higgs² and Chris M. Wood¹

¹ McMaster University, Department of Biology, 1280 Main Street West, Hamilton, Ontario, Canada L8S 4K1 and
² Department of Fisheries and Oceans, West Vancouver Laboratory, 4160 Marine Drive, British Columbia, Canada V7V 1N6
Present address: The August Krogh Institute, Zoophysiological Laboratory, University of Copenhagen, DK-2100 Copenhagen, Denmark

View larger version (29K): [in a new window]   Fig. 1. (A) Effects on growth of exposure of juvenile rainbow trout to a combination of waterborne and dietary Cu levels ranging from deficient to excess. Values are cumulative mass gain per tank (means ± S.E.M., N=3). Diamonds, low waterborne Cu and low dietary Cu; triangles, low waterborne Cu and normal dietary Cu; open circles, normal waterborne Cu and low dietary Cu; filled circles, normal waterborne Cu and normal dietary Cu; squares, normal waterborne Cu and high dietary Cu level. (B) Effects of the exposure conditions on food conversion efficiency in actively growing rainbow trout. Values are means ± S.E.M. on a per tank basis, N=3 per data point. LL, low waterborne Cu and low dietary Cu; LN, low waterborne Cu and normal dietary Cu; NL, normal waterborne Cu and low dietary Cu; NN, normal waterborne Cu and normal dietary Cu; NH, normal waterborne Cu and high dietary Cu level. *Significant difference relative to group NN on normal water Cu and normal dietary Cu (ANOVA, P<0.05). No significant differences were observed with other comparisons of treatments.

View larger version (11K): [in a new window]   Fig. 2. Effects of dietary and waterborne Cu exposure conditions on whole body Cu concentration in actively growing rainbow trout. Values are means ± S.E.M., N=15 for weeks 0, 2 and 4, and N=9 for week 7 for each treatment. Diamonds, low waterborne Cu and low dietary Cu; triangles, low waterborne Cu and normal dietary Cu; open circles, normal waterborne Cu and low dietary Cu; filled circles, normal waterborne Cu and normal dietary Cu; squares, normal waterborne Cu and high dietary Cu level. *Significantly higher level, significantly lower level relative to the group exposed to normal water Cu and normal dietary Cu (ANOVA, P<0.05).

View larger version (14K): [in a new window]   Fig. 3. Patterns of whole body Cu concentration (y, µmol g–1 wet mass) with time (x, weeks) during exposure to low waterborne and low dietary Cu levels (A), and to normal waterborne and high dietary Cu levels (B). Values are means ± S.E.M., N=15 for weeks 0, 2 and 4, and N=9 for week 7 for each treatment. In A the negative relationship is best described by the exponential equation y=0.4268+0.6879exp(–0.5868x), r2=0.80, t1/2=1.18 weeks; in B, the positive relationship is best described by the linear equation, y=0.5897+1.407x, r2=0.80. Equations were derived from individual data points.

View larger version (17K): [in a new window]   Fig. 4. Gut tissue Cu concentration (µmol g–1 wet mass) over the exposure period and the proportional contribution (%) to total body Cu burden. Percentage data were transformed to arc sin for statistical analysis. Values are means ± S.E.M.; N=15 for weeks 0, 2 and 4, and N=9 for week 7 for each treatment. Diamonds, low waterborne Cu and low dietary Cu; triangles, low waterborne Cu and normal dietary Cu; open circles, normal waterborne Cu and low dietary Cu; filled circles, normal waterborne Cu and normal dietary Cu; squares, normal waterborne Cu and high dietary Cu level. *Significantly higher level, significantly lower level relative to the group on normal levels of water Cu and dietary Cu (ANOVA, P<0.05).

View larger version (16K): [in a new window]   Fig. 5. Liver Cu concentration (µmol g–1 wet mass) during the exposure period (A) and the proportional contribution of liver Cu to total body Cu (B). Percentage data were transformed to arc sin for statistical analysis. Values are means ± S.E.M.; N=15 for weeks 0, 2 and 4, and N=9 for week 7 for each data point per treatment. Diamonds, low waterborne Cu and low dietary Cu; triangles, low waterborne Cu and normal dietary Cu; open circles, normal waterborne Cu and low dietary Cu; filled circles, normal waterborne Cu and normal dietary Cu; squares, normal waterborne Cu and high dietary Cu level. *Significantly higher level, significantly lower level relative to group on normal levels of water Cu and dietary Cu (ANOVA, P<0.05).

View larger version (19K): [in a new window]   Fig. 6. Cu concentration in gills (µmol g–1 wet mass) during the exposure period (A) and the percentage contribution of the gill to total body Cu burden during the exposure period (B). Percentage data were transformed to arc sin for statistical analysis. All the values are means ± S.E.M., N=15 for weeks 0, 2 and 4, and N=9 for week 7 for each of the treatment. Diamonds, low waterborne Cu and low dietary Cu; triangles, low waterborne Cu and normal dietary Cu; open circles, normal waterborne Cu and low dietary Cu; filled circles, normal waterborne Cu and normal dietary Cu; squares, normal waterborne Cu and high dietary Cu levels. *Significantly higher level, significantly lower level relative to the group on normal levels of water Cu and dietary Cu (ANOVA, P<0.05).

View larger version (16K): [in a new window]   Fig. 7. Carcass Cu concentration (µmol g–1wet mass) during the exposure period (A) and the proportional contribution of the carcass to the total Cu burden during the exposure period (B). Carcass comprised whole body less gill, liver and gut. Percentage data were transformed to arc sin for statistical analysis. All the values are means ± S.E.M., N=15 for weeks 0, 2 and 4, and N=9 for week 7 for each of the treatment. Diamonds, low waterborne Cu and low dietary Cu; triangles, low waterborne Cu and normal dietary Cu; open circles, normal waterborne Cu and low dietary Cu; filled circles, normal waterborne Cu and normal dietary Cu; squares, normal waterborne Cu and high dietary Cu level. *Significantly higher level, significantly lower level relative to the group on normal levels of water Cu and dietary Cu (ANOVA, P<0.05).

View larger version (17K): [in a new window]   Fig. 8. Waterborne Cu uptake rates (means ± S.E.M., pmol g–1 h–1, N=9 per data point), measured using 64Cu at the end of the 7-week exposure for all the treatment groups. These measurements were carried out over a 12-hour period, at a range of waterborne copper concentrations. Diamonds, low waterborne Cu and low dietary Cu; triangles, low waterborne Cu and normal dietary Cu; open circles, normal waterborne Cu and low dietary Cu; filled circles, normal waterborne Cu and normal dietary Cu; squares, normal waterborne Cu and high dietary Cu level. *Significantly higher relative to the group on normal levels of water Cu and dietary Cu (ANOVA, P<0.05).

View larger version (12K): [in a new window]   Fig. 9. Effects of dietary and waterborne Cu exposure conditions on fish Cu content. Values are means ± S.E.M., N=15 for weeks 0, 2 and 4, and N=9 for week 7 for each treatment. Diamonds, low waterborne Cu and low dietary Cu; triangles, low waterborne Cu and normal dietary Cu; open circles, normal waterborne Cu and low dietary Cu; filled circles, normal waterborne Cu and normal dietary Cu; squares, normal waterborne Cu and high dietary Cu level. *Significantly higher level, significantly lower level relative to the group on normal levels of water Cu and dietary Cu (ANOVA, P<0.05).

View larger version (16K): [in a new window]   Fig. 10. (A) Relative contribution of dietary and waterborne Cu uptake to the total body Cu burden accumulated over 7 weeks of exposure to experimental regime. Open bars, contribution of the waterborne Cu uptake; hatched bars, contribution of the dietary Cu uptake; LL, low waterborne Cu and low dietary Cu; LN, low waterborne Cu and normal dietary Cu; NL, normal waterborne Cu and low dietary Cu; NN, normal waterborne Cu and normal dietary Cu; NH, normal waterborne Cu and high dietary Cu level. (B,C) True bioavailability of dietary Cu (% of Cu ingested in food and retained during the exposure period). (B) Bioavailability of dietary Cu in normal water. (C) Bioavailability of dietary Cu in low waterborne Cu. See text for details of the calculation