Abstract: We used field data from transplantation and caging studies with juvenile yellow perch (Perca flavescens) to test a kinetic bioaccumulation model for cadmium (Cd). The model, which considers both dietary and aqueous sources of Cd, was first used to predict the dynamics of Cd accumulation in perch exposed to high ambient Cd for 70 days. Model simulations for hepatic Cd agreed well with the observed time course of Cd accumulation in the liver, but for the gills and gut, the predicted accumulations after 70 days were about three times higher than the observed values, suggesting that these latter organs can alter their ability to take up and (or) eliminate Cd. The model was also used to predict steady-state Cd concentrations in the gills, gut, and liver of perch living in lakes along a Cd gradient. Agreement between predicted and observed steady-state Cd concentrations was reasonable in lakes with low to moderate Cd concentrations, but in lakes with high dissolved Cd (>1.5 nmol x [L.sup.-1]), the model overestimated Cd accumulation, particularly in the gills and gut. These results suggest that kinetic bioaccumulation models may better apply to some organs than to others. Because metal-induced toxicity is normally organ-specific, their application in a risk assessment context should be undertaken with caution.
Resume : Nous avons teste un modele cinetique de bioaccumulation du cadmium (Cd) chez la perchaude juvenile (Perca flavescens; branchies, intestin et foie) en nous servant de donnees obtenues dans le cadre d'experiences anterieures menees sur le terrain (transplantation; manipulation du regime alimentaire). Ce modele biodynamique tient compte de l'accumulation du Cd a partir de l'eau et de la nourriture et il a d'abord ete utilise pour predire l'accumulation du Cd chez des poissons exposes a des concentrations elevees en Cd pendant 70 jours. Les simulations pour le Cd hepatique se conformaient bien aux valeurs observees, mais pour les branchies et l'intestin, les valeurs predites a la fin de la periode de 70 jours etaient environ trois fois superieures a celles observees, ce qui suggere que ces organes peuvent changer leur capacite de prendre en charge ou d'eliminer le Cd. Le modele a egalement ete utilise pour predire les concentrations en Cd a l'etat stationnaire dans les branchies, l'intestin et le foie de perchaudes indigenes vivant dans des lacs situes le long d'un gradient en Cd. L'accord entre les simulations et les concentrations en Cd observees a l'etat stationnaire etait acceptable dans des lacs ayant des concentrations en Cd faibles ou moderees, mais dans les lacs les plus contamines en Cd ([Cd] > 1,5 nmol x [L.sup.-1]), le modele a de nouveau surestime l'accumulation, surtout dans les branchies et l'intestin. Ces resultats suggerent que les modeles cinetiques de bioaccumulation s'appliquent mieux a certains organes qu'a d'autres. Puisque la toxicite induite par les metaux varie generalement d'un organe cible a un autre, l'application de ces modeles dans l'evaluation des risques poses par les metaux dans l'environnement doit etre faite avec prudence.
Introduction
Kinetic bioaccumulation models have become powerful tools for explaining and predicting metal accumulation by aquatic animals (Blust 2001; Borgmann et al. 2005; Luoma and Rainbow 2005). Their strength comes from the fact that they are simple and thus practical to use and yet include enough mechanistic information to allow predictions of metal concentrations in animals living in the field (Luoma et al. 1992; Fisher et al. 2000; Croteau et al. 2002x). One reason for their success is that they explicitly consider metal uptake from water (e.g., via the gills) and from food (i.e., via the gut). For fish, it is particularly important to include both vectors for metal uptake, rather than assume that all of the metal is taken up from solution; metal bioaccumulation by many fish species is known to be influenced by dietborne metals (Harrison and Klaverkamp 1989; Mount et al. 1994; Kraemer et al. 2006).
One of the potential extensions to kinetic bioaccumulation models would be to use them to predict metal toxicity. However, to do so would require certain refinements, notably with respect to metal dynamics within the animal. Metal toxicity in animals is normally an organ-specific phenomenon, yet the current generation of field-tested metal bio-accumulation models does not consider metal distributions among various target organs (Luoma and Rainbow 2005).
In the present study, we used field data (Kraemer et al. 2005x, 2005b, 2006) describing Cd dynamics in yellow perch (Perca flavescens) to test the ability of a kinetic bio-accumulation model to predict Cd concentrations in individual organs. Data were available for Cd uptake from both food and water and for Cd loss. We chose Cd because of the toxic effects that it can exert on animals in mining areas (Campbell et al. 2003; Borgmann et al. 2004) and yellow perch because they are present in lakes covering a wide range of metal concentrations (Sherwood et al. 2000; Couture and Rajotte 2003; Giguere et al. 2004) and thus have great potential as a metal biomonitor. Recent work within our group (Giguere et al. 2005, 2006) and by others (Couture and Rajotte 2003; Levesque et al. 2003; Gravel et al. 2005) has demonstrated that although yellow perch can survive and reproduce in lakes with high ambient metal concentrations, they nevertheless manifest clear symptoms of metal-induced stress in a dose-dependent manner. We modeled Cd concentrations in several of its organs: the gills and gut, as they are important for Cd exchange with the external environment, and the liver, as it is an organ important for Cd storage (Giguere et al. 2004). We first tested the ability of a kinetic model to describe Cd dynamics in these three organs and then used the model to predict steady-state Cd concentrations in perch collected from lakes located along a Cd concentration gradient.
Our results demonstrate that the ability of metal accumulation and elimination experiments to predict steady-state concentrations in various organs of indigenous fish was dependent on the organ examined. Organs in contact with the external environment (i.e., the gills and gut) responded very differently than did the liver, presumably because of the ability of these "interface" organs to adjust their rates of metal uptake and (or) loss.
Materials and methods
The study lakes
The lakes that we studied are located in the Abitibi region near the city of Rouyn-Noranda, approximately 600 km northwest of Montreal, Quebec, Canada. A copper smelter has been in operation since 1927 in the city of Rouyn-Noranda, and although emissions are now largely controlled (Croteau et al. 2002b), lakes located downwind from this smelter are contaminated with metals such as Cd as a result of historical atmospheric deposition. In addition to these direct inputs from the smelter, some lakes in this region are also contaminated by runoff from mine tailings and mineralized outcrops. For model development, we chose two lakes: Lake Opasatica (OP, reference lake) and Lake Dufault (DU, metal-contaminated lake). For the subsequent testing of the model, in addition to these two lakes, we added one reference lake (OL, Ollier), one moderately contaminated lake (VA, Vaudray), and another highly contaminated lake (OS, Osisko). We also considered previously published data from six additional sites: Lakes Bousquet, Dasserat, and Heva from the Rouyn-Noranda area (gill, gut and liver data; Giguere et al. 2004) and Lakes Raft, Laurentian, Hannah, and Wavy from the Sudbury region (liver data only; Giguere et al. 2005).
Relative importance of dietary and aqueous Cd as metal sources for juvenile yellow perch
A detailed description of this experiment can be found in Kraemer et al. (2006). Briefly, juvenile yellow perch (1.5 [+ or -] 0.1 g dry weight, mean [+ or -] standard error (SE)) were collected from Lake Opasatica and held in cages located in both Lake Opasatica (two cages per treatment) and Lake Dufault (two cages per treatment). Each cylindrical cage (height 1.2 m, diameter 0.5 m) was made of Nitex netting (64 [micro]m mesh aperture) topped by Styrofoam floats and was anchored to the lake bottom (Munger et al. 1999). The floats held the cage opening well above the surface to prevent zooplankton from entering by wave action. Each cage initially contained 10 fish.
The cages were filled by passive entry of lake water through the netting, which prevented the entry of macrozooplankton. Yellow perch were allowed to acclimate to their cages for 24 h and were not fed during this time period. The caged fish in both lakes were then fed daily with macrozooplankton collected from either the reference lake (OP) or the Cd-contaminated lake (DU), creating four treatment regimes: reference lake water and reference diet (REF); reference lake water and contaminated food (FO); contaminated lake water and reference food (WO); and contaminated lake water and contaminated food (WF). Fish were sampled after 15 and 30 days of exposure, and the gills, gut, and liver were analyzed for Cd (see description of the analytical protocol below).
Cd uptake and efflux in juvenile yellow perch
Details of the Cd uptake and efflux experiments are outlined in Kraemer et al. (2005x) and Kraemer et al. (2005b), respectively. For the Cd-uptake experiments, juvenile yellow perch (<5 g fresh weight) were collected from a reference lake (OP) and held in cages in a metal-contaminated lake (DU) for up to 70 days. For the Cd-efflux experiments, juvenile yellow perch were collected from the contaminated lake (DU) and kept within cages in the reference lake (OP) for up to 75 days to measure Cd loss. Because this size class of perch feeds …
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