Jérémie D. Lebrun

Waterborne nickel bioaccumulation in Gammarus pulex: comparison of mechanistic models and influence of water cationic composition.

The biodynamic and saturation models offer promising lines of enquiry to predict the bioaccumulation of metals by aquatic organisms. However, in order to construct these models, the accumulation strategies have to be defined for each metal/organism couple in controlled conditions. This study aims at modelling the waterborne bioaccumulation of Ni and the influence of the waters geochemical properties on this process in a crustacean that is widely distributed in Europe, Gammarus pulex. In the laboratory, G. pulex was exposed to several Ni concentrations (from 0.001 to 100 mg L(-1)) in aquatic microcosms. Our results show that G. pulex is very tolerant to Ni (LC50(48 h)=477 mg L(-1) Ni). Time course experiments enabled the construction of a biodynamic model by determining the uptake (k(u)) and elimination (k(e)) rate constants. When the exposure concentration exceeded 1 mg L(-1) Ni, the metal uptake reached a maximum due to a limited number of binding sites for Ni. Therefore, the organisms maximal capacity to accumulate the metal (B(max)) and the half-saturation constant (K) were determined to establish the saturation model. We showed that the two models are comparable for the lowest exposure concentrations (<1 mg L(-1) Ni), with k(u)/k(e)=B(max)/K. Then, the bioaccumulation of Ni was recorded in waters exhibiting various concentrations of three major ions (Na(+), Mg(2+) and Ca(2+)). Only Ca had an inhibitory effect on the Ni uptake. This study reports for the first time the bioaccumulation of Ni in G. pulex. Because of its high tolerance to Ni and its high capacity to accumulate this metal, this crustacean could be used as an indicator of Ni bioavailability in freshwaters.

Essential metal contents in indigenous gammarids related to exposure levels at the river basin scale: metal-dependent models of bioaccumulation and geochemical correlations.

Biomonitoring, assumed to be an integrative measurement of the chemical exposure of aquatic organisms, is not straightforward for essential metals because they can be actively regulated by animals. Although increasing bioaccumulation with exposure levels is a crucial endpoint for the development of biomonitors, it is rarely verified in real environments, where the metal concentrations are rather low and vary little. This study was designed at the scale of a river basin to assess the ability of Gammarus pulex indigenous populations to accumulate Cu, Zn and Mn in realistic exposure conditions. During two annual campaigns, water and gammarids were collected at various sites contrasted in terms of physicochemistry and contamination. The results show significant relationships between metal concentrations in animals and in freshwaters established by conceptual models of bioaccumulation, but with patterns specific to each metal (base level, internal regulation and maximal accumulation). In particular, a saturation process of Cu accumulation occurs at environmental exposure levels, unlike Mn and Zn. Statistical analyses performed from field data show that Cu and Zn bioaccumulations may be influenced by a complex combination of geochemical variables, unlike Mn. We conclude that G. pulex is a useful candidate to monitor metal bioavailability in freshwaters due to its responsiveness to low exposures of surrounding environments. Nevertheless, a reliable quantification of bioavailability of essential metals requires characterizing some geochemical effects on metal bioaccumulation.

Bioaccumulation of polybrominated diphenyl ethers (PBDEs) in Gammarus pulex: relative importance of different exposure routes and multipathway modeling.

Characterizing the exposure routes of an organism and its ability to regulate accumulated contaminants is a crucial step toward developing a biomonitor. To date, very little data are available on the bioaccumulation kinetics of PBDEs in freshwater biota. This study aims at investigating the potential use of a litter-degrader widely distributed in European freshwaters, Gammarus pulex, as an indicator of exposure to PBDEs. In aquatic microcosms, gammarids were exposed to a mixture of brominated congeners (BDE-28, 47, 66, 85, 99, 100, 153, 154 and 183) to assess their ability to bioconcentrate PBDEs. Results show that all tested congeners are highly internalized by G. pulex and uptake rates of PBDEs are closely related to their partition coefficients (Kow). The determination of the elimination rate of BDE-47, the congener most readily accumulated by gammarids, indicated that metabolism and excretion of this congener are low in G. pulex, which argues in favor of its use as a quantitative biomonitor. Finally, bioaccumulation experiments were performed using contaminated leaves to determine the relative importance of dietary uptake in the contamination of gammarids. Even though water is the preeminent exposure route, a significant uptake of BDE-47 through food was observed (27%). We propose a biodynamic model that takes into account both exposure routes to describe BDE-47 bioaccumulation. This study supports the use of this ubiquitous amphipod as an early warning monitor of the bioavailable contamination of freshwaters by PBDEs.

Application of a multidisciplinary and integrative weight-of-evidence approach to a 1-year monitoring survey of the Seine River

Quality assessment of environments under high anthropogenic pressures such as the Seine Basin, subjected to complex and chronic inputs, can only be based on combined chemical and biological analyses. The present study integrates and summarizes a multidisciplinary dataset acquired throughout a 1-year monitoring survey conducted at three workshop sites along the Seine River (PIREN-Seine program), upstream and downstream of the Paris conurbation, during four seasonal campaigns using a weight-of-evidence approach. Sediment and water column chemical analyses, bioaccumulation levels and biomarker responses in caged gammarids, and laboratory (eco)toxicity bioassays were integrated into four lines of evidence (LOEs). Results from each LOE clearly reflected an anthropogenic gradient, with contamination levels and biological effects increasing from upstream to downstream of Paris, in good agreement with the variations in the structure and composition of bacterial communities from the water column. Based on annual average data, the global hazard was summarized as “moderate” at the upstream station and as “major” at the two downstream ones. Seasonal variability was also highlighted; the winter campaign was least impacted. The model was notably improved using previously established reference and threshold values from national-scale studies. It undoubtedly represents a powerful practical tool to facilitate the decision-making processes of environment managers within the framework of an environmental risk assessment strategy.

Behavioural and biochemical responses to metals tested alone or in mixture (Cd-Cu-Ni-Pb-Zn) in Gammarus fossarum: From a multi-biomarker approach to modelling metal mixture toxicity

Metals are usually present as mixtures at low concentrations in aquatic ecosystems. However, the toxicity and sub-lethal effects of metal mixtures on organisms are still poorly addressed in environmental risk assessment. Here we investigated the biochemical and behavioural responses of Gammarus fossarum to Cu, Cd, Ni, Pb and Zn tested individually or in mixture (M2X) at concentrations twice the levels of environmental quality standards (EQSs) from the European Water Framework Directive. The same metal mixture was also tested with concentrations equivalent to EQSs (M1X), thus in a regulatory context, as EQSs are proposed to protect aquatic biota. For each exposure condition, mortality, locomotion, respiration and enzymatic activities involved in digestive metabolism and moult were monitored over a 120h exposure period. Multi-metric variations were summarized by the integrated biomarker response index (IBR). Mono-metallic exposures shed light on biological alterations occurring at environmental exposure levels in gammarids and depending on the considered metal and gender. As regards mixtures, biomarkers were altered for both M2X and M1X. However, no additive or synergistic effect of metals was observed comparing to mono-metallic exposures. Indeed, bioaccumulation data highlighted competitive interactions between metals in M2X, decreasing subsequently their internalisation and toxicity. IBR values indicated that the health of gammarids was more impacted by M1X than M2X, because of reduced competitions and enhanced uptakes of metals for the mixture at lower, EQS-like concentrations. Models using bioconcentration data obtained from mono-metallic exposures generated successful predictions of global toxicity both for M1X and M2X. We conclude that sub-lethal effects of mixtures identified by the multi-biomarker approach can lead to disturbances in population dynamics of gammarids. Although IBR-based models offer promising lines of enquiry to predict metal mixture toxicity, further studies are needed to confirm their predictive quality on larger ranges of metallic combinations before their use in field conditions.

Comparison in waterborne Cu, Ni and Pb bioaccumulation kinetics between different gammarid species and populations: Natural variability and influence of metal exposure history

Kinetic parameters (uptake from solution and elimination rate constants) of Cu, Ni and Pb bioaccumulation were determined from two Gammarus pulex and three Gammarus fossrum wild populations collected from reference sites throughout France in order to assess the inter-species and the natural inter-population variability of metal bioaccumulation kinetics in that sentinel organism. For that, each population was independently exposed for seven days to either 2.5μgL-1 Cu (39.3nM), 40μgL-1 Ni (681nM) or 10μgL-1 Pb (48.3nM) in laboratory controlled conditions, and then placed in unexposed microcosms for a 7-day depuration period. In the same way, the possible influence of metal exposure history on subsequent metal bioaccumulation kinetics was addressed by collecting wild gammarids from three populations inhabiting stations contaminated either by Cd, Pb or both Pb and Ni (named pre-exposed thereafter). In these pre-exposed organisms, assessment of any changes in metal bioaccumulation kinetics was achieved by comparison with the natural variability of kinetic parameters defined from reference populations. Results showed that in all studied populations (reference and pre-exposed) no significant Cu bioaccumulation was observed at the exposure concentration of 2.5μgL-1. Concerning the reference populations, no significant differences in Ni and Pb bioaccumulation kinetics between the two species (G. pulex and G. fossarum) was observed allowing us to consider all the five reference populations to determine the inter-population natural variability, which was found to be relatively low (kinetic parameters determined for each population remained within a factor of 2 of the minimum and maximum values). Organisms from the population exhibiting a Pb exposure history presented reduced Ni uptake and elimination rate constants, whereas no influence on Ni kinetic parameters was observed in organisms from the population exhibiting an exposure history to both Ni and Pb. Furthermore Pb bioaccumulation kinetics were unaffected whatever the condition of pre-exposure in natural environment. Finally, these results highlight the complexity of confounding factors, such as metal exposure history, that influence metal bioaccumulation processes and showed that pre-exposure to one metal can cause changes in the bioaccumulation kinetics of other metals. These results also address the question of the underlying mechanisms developed by organisms to cope with metal contamination.