Oligotrophy as a major driver of mercury bioaccumulation in medium-to high-trophic level consumers: A marine ecosystem-comparative study

Abstract

Mercury (Hg) is a global contaminant of environmental concern. Numerous factors influencing its bioaccumulation in marine organisms have already been described at both individual and species levels (e.g., size or age, habitat, trophic level). However, few studies have compared the trophic characteristics of ecosystems to explain underlying mechanisms of differences in Hg bioaccumulation and biomagnification among food webs and systems. The present study aimed at investigating the potential primary role of the trophic status of systems on Hg bioaccumulation and biomagnification in temperate marine food webs, as shown by their medium-to high-trophic level consumers. It used data from samples collected at the shelf-edge (i.e. offshore organisms) in two contrasted ecosystems: the Bay of Biscay in the North-East Atlantic Ocean and the Gulf of Lion in the North-West Mediterranean Sea. Seven species including crustaceans, sharks and teleost fish, previously analysed for their total mercury (T-Hg) concentrations and their stable carbon and nitrogen isotope compositions, were considered for a meta-analysis. In addition, methylated mercury forms (or methyl-mercury, Me-Hg) were analysed. Mediterranean organisms presented systematically lower sizes than Atlantic ones, and lower δC and δN values, the latter values especially highlighting the more oligotrophic character of Mediterranean waters. Mediterranean individuals also showed significantly higher T-Hg and Me-Hg concentrations. Conversely, Me-Hg/T-Hg ratios were higher than 85% for all species, and quite similar between systems. Finally, the biomagnification power of Hg was different between systems when considering T-Hg, but not when considering Me-Hg, and was not different between the Hg forms within a given system. Overall, the different parameters showed the crucial role of the low primary productivity and its effects rippling through the compared ecosystems in the higher Hg bioaccumulation seen in organisms from oligotrophic Mediterranean waters.

Trace metal concentrations in the muscle of seven marine species: Comparison between the Gulf of Lions (North-West Mediterranean Sea) and the Bay of Biscay (North-East Atlantic Ocean)

“…Secondly, this pattern of generally higher metal concentrations in individuals from the GoL than from the BoB is consistent with previous studies on other contaminants such as Hg, which highlighted the prevalent effect of oligotrophy, driving higher contamination levels, lower organisms' size and lower C and N stable isotope ratios in the Mediterranean (i.e. lower biodilution effect of contaminants in general through the food web) (Chouvelon et al, 2018;Cossa et al, 2012;Harmelin-Vivien et al, 2009). This is also observed in this study where the majority of metal concentrations were on average higher in the GoL than in the BoB, along with lower total lengths and trophic levels, likely revealing the crucial role of sources of organic matter and primary producers at the base of the food web in the bioaccumulation and trophic transfer of metals (for more details, see (Chouvelon et al, 2018).…”

“…Hg (Chouvelon et al, 2018;Cossa and Coquery, 2005;Harmelin-Vivien et al, 2009) but also Cd and Pb (Damiano et al, 2011). In our study, only H. dactylopterus and N. norvegicus presented significant difference of metal concentrations between both locations (Table 3).…”

“…habitats of species; (Chouvelon et al, 2012)) and biotic factors (e.g. fish growth, trophic functioning of ecosystems; (Chouvelon et al, 2018;Cossa et al, 2012;Cresson et al, 2014) on Hg bioaccumulation in marine organisms, especially in commercial species. As such, several authors evidenced and partly explained the "Mediterranean Hg anomaly", i.e.…”

“…lower biodilution effect of contaminants in general through the food web) (Chouvelon et al, 2018;Cossa et al, 2012;Harmelin-Vivien et al, 2009). This is also observed in this study where the majority of metal concentrations were on average higher in the GoL than in the BoB, along with lower total lengths and trophic levels, likely revealing the crucial role of sources of organic matter and primary producers at the base of the food web in the bioaccumulation and trophic transfer of metals (for more details, see (Chouvelon et al, 2018). Thirdly, an increasing number of studies have documented relatively high levels of trace metal contamination in shelf-edge or deep species (Cronin et al, 1998;Hornung et al, 1993), especially when compared to neritic species (Chouvelon et al, 2012).…”

Spatial and taxonomic variation of mercury concentration in low trophic level fauna from the Mediterranean Sea

“…This could be driven in part by increased MeHg production in Mediterranean oligotrophic mixed layers due to changing phytoplankton composition enhancing methylation through the “microbial food web” (Heimburger et al 2010). In addition, Chouvelon et al (2018) implicate oligotrophy as a driver of higher Hg bioaccumulation at all trophic levels within the Mediterranean (Gulf of Lion) in comparison to the Atlantic Ocean (Bay of Biscay), which is consistent with our within-system observation of higher concentration with lower chl a . We also hypothesize that omnivorous euphausiids may preferentially graze on larger algae such as diatoms when it is highly abundant, but may feed at higher trophic levels (e.g.…”