Cinétique d'accumulation et rétention d'espèces du mercure chez l'étoile de mer Leptasterias polaris: une expérience de transfert trophique à long terme Uptake kinetics and retention of mercury species in starfish Leptasterias polaris: a long term trophic transfer experiment

Résumé

Dans le cadre de travaux sur le rôle des échinodermes dans le cycle biogéochimique de certains métaux traces en milieu côtier, une étude de l'accumulation et de la rétention d'espèces chimiques du mercure a été menée avec l'étoile de mer Leptasterias polaris sur une période de 40 jours. Les étoiles de mer ont été divisées en deux groupes et nourries avec des moules contaminées soit au méthylmercure (MeHg) (14 mg.kg-1), soit au mercure inorganique (13 mg.kg-1). Les résultats montrent une vitesse d'accumulation dans le système digestif de 0,22 mg.kg-1.j-1 pour le Hg inorganique et 0,17 mg.kg-1.j-1 pour le MeHg. Ces vitesses sont 10 à 15 fois moins importantes dans les gonades et l'endosquelette. Pour le Hg inorganique, la charge relative dans les différents organes analysés se fixe après quelques jours et demeure stable jusqu'à la fin de l'expérience. Pour le MeHg, au contraire, cette charge relative passe progressivement du système digestif vers les gonades et l'exosquelette tout au long de l'expérience. Le pourcentage de rétention (%) demeure constant pour le Hg inorganique (51 ± 13%) mais il augmente régulièrement pour le MeHg, atteignant 90-95% vers la fin de l'exposition. L'application d'un modèle cinétique simple, basé sur un processus d'échange ionique, a permis de calculer des constantes de vitesse d'échange entre le digestat et le tissu digestif. Le MeHg s'échange plus vite entre la solution et les sites, mais semble mettre un peu plus de temps à voyager jusqu'aux organes de bioaccumulation. En conclusion, l'étoile L. polaris, par sa taille, sa longévité et sa grande efficacité à digérer tout ce qui est ingéré, semble en mesure de jouer un rôle important à la fois dans la séquestration du MeHg et la remise en solution du Hg inorganique.

Mots-clés:

• Échinodermes,
• étoile de mer,
• mercure,
• méthylmercure,
• prise en charge,
• rétention,
• échange ionique,
• modèle cinétique,
• constante de vitesse

Abstract

In spite of a large body of work on the uptake of trace metals in aquatic organisms in the last two decades, very little attention has been devoted to echinoderms (urchins, starfish, and sea cucumbers, among the most important ones), a large group of invertebrates forming a major component of most coastal ecosystems. In the course of our research program on the role of echinoderms in the biogeochemical cycling of some trace metals in coastal environment, an experiment has been conducted on the uptake and the retention of mercury species with starfish Leptasterias polaris over a 40-day exposure period.

Starfish were caught near Pointe-au-Père (Québec, Canada) and were acclimatized to laboratory conditions for 10 days in a flow-through aquarium. Forty stars (84 ± 14 g) were divided in two groups, kept in two aquariums, one for inorganic mercury and the other for methylmercury exposure. Animals were isolated from each other by mean of small 65-mm net cubicles allowing free circulation of seawater at a rate of 2 L.min-1. This flow rate provided a rapid renewal of seawater and ensured the elimination of any soluble mercury excreted during the course of the experiment. Control starfish receiving only uncontaminated mussels were also maintained in both aquariums to monitor the possible uptake of mercury from seawater. Blue mussels were collected in the vicinity of Pointe-au-Père and were contaminated following a technique described elsewhere (PELLETIER and LAROCQUE, 1987). Average levels of inorganic mercury and methylmercury (MeHg) in mussels were 13 ± 3 and 14 ± 4 mg.kg-1, respectively. Each starfish received one contaminated mussel per day over a 40-day period. Mussels were weighed before to be introduced in cages and their empty shells weighed again after ingestion by starfish in order to evaluate the amount of food and mercury taken up daily by each star. Two starfish were sampled in each aquarium every five days and dissected for pyloric caeca, gonads, and endoskeleton. Coelomic fluid was also collected. Both mercury species were analysed as total mercury (assuming a preservation level of ± 85-90% of the speciation during the course of the experiment) in biological tissues by cold vapour atomic adsorption spectrophotometry (detection limit=0.005 mg.kg-1 ww). The coefficient of variation was ± 15% and the recovery yield of MeHg-spiked samples was 92 ± 12%.

The concentration of inorganic mercury reached 7.56 mg.kg-1 (wet weight) in pyloric caeca and the uptake rate was 0.22 mg.kg-1.d-1. Concentrations in gonads and endoskeleton were 10 to 20 times lower than in caeca (Fig. 1). The uptake rate of MeHg (0.17 mg.kg-1d-1) was slightly slower and the maximum concentration reached in caeca was 5.34 mg.kg-1. Mercury concentrations found in coelomic fluid were low and at least 100 times smaller than those in ceaca. No mercury was found in tissues of control starfish indicating that mercury excreted by diffusion in water by contaminated starfish was not re-adsorbed by other starfish in aquariums. The mercury load in each organ of stars was calculated and expressed as a percent (%) of total Hg uptake for each chemical species (Fig. 2). The inorganic Hg loads in pyloric caeca, gonads and endoskeleton reached a steady-state after only 10 days and remained unchanged up to the end of the experiment. The behaviour of MeHg was totally different as the loads in caeca decreased from 95% to 65% but increased from almost zero up to 30% in endoskeleton. Finally, the retention (%) of mercury species was calculated by dividing the actual total amount of mercury in each starfish by the total amount of mercury received from mussels (Fig. 3). The retention of inorganic Hg was about 50% throughout the exposure period whereas the retention of MeHg increased up to 90-95% at the end of the experiment.

A kinetic model, based upon the assumption that the uptake process of Hg species in the digestive system is quite similar to an ion-exchange adsorption mechanism between a contamination solution and a solid surface, was developed. The integrated equation of the rate law was expressed as:

(ln(C₀-q))/q₀-q = K'(C₀m-q₀)t + ln (C₀m/q₀)

were Co is the initial concentration of mercury in the prey, qo is the maximun amount of mercury being absorbed, and m stands for the wet weight of the animal. This equation allowed the plot of its left-hand side against time and the slope provided an estimation of an apparent exchange rate constant for each mercury species (Fig. 4). The rate constant k'MeHg was slightly higher than k'Hg, indicating a faster exchange rate for MeHg between digested mussel tissues and binding sites (and also between sites) in caeca. However, a faster exchange rate do not mean a faster uptake rate because transport rate towards other organs also play an important role in the whole bioaccumulation process.

In conclusion, starfish, by its ability to digest all ingested tissues, seems to be in a position to play a major role in the sequestration of methylmercury (high retention) from mussels and from other potential preys and in recycling inorganic mercury in solution (low retention). Starfish can be seen as "marine digester" which engulfs bivalves and other invertebrates (following species) and sends back soluble metabolites and trace metals which have not been bioaccumulated.

Keywords:

• Echinoderms,
• starfish,
• mercury,
• methylmercury,
• uptake,
• retention,
• ion-exchange rate,
• kinetic model,
• constant rate