An Arsenic-76 radiotracer to study the routes of assimilation, hemolymph distribution, and tissue inventories in the bioindicator organism Pomacea canaliculata.

The aim of this work was to study the absorption, distribution through the hemolymph, and bioaccumulation of arsenic by the freshwater Pomacea canaliculata using a short-lived tracer (76As, t1/2: 1.07 d) with high specific activity. Arsenic travels mainly dissolved in the plasma of the snail's hemolymph. This element is transferred from the hemolymph to the tissues (87%) 4 h after the inoculation of 50 µL of a 0.04 g/L of 76As radiotracer solution, being the digestive gland, kidney, and head-foot the main places of arsenical inventories. Snails exhibited a rapid arsenic accumulation response in a wide range of concentrations (from 1 to 1000 µg/L) of the metalloid dissolved in water and in a concentration-dependent manner. Also, snails incorporated As from the digestive system when they received a single safe dose of ~2 µg of 76As inoculated in a fish food pellet. The (semi) physiologically based toxicokinetic model developed in this study is based on anatomical and physiological parameters (blood flow, irrigation, tissue volume and other). Together, these findings make P. canaliculata an excellent sentinel organism to evaluate freshwater bodies naturally contaminated with As.

Zinc in an ultraoligotrophic lake food web.

Zinc (Zn) bioaccumulation and trophic transfer were analyzed in the food web of Lake Nahuel Huapi, a deep, unpolluted ultraoligotrophic system in North Patagonia. Benthic macroinvertebrates, plankton, and native and introduced fish were collected at three sites. The effect of pyroclastic inputs on Zn levels in lacustrine food webs was assessed by studying the impact of the eruption of Puyehue-Cordón Caulle volcanic complex (PCCVC) in 2011, by performing three sampling campaigns immediately before and after the PCCVC eruption, and after 2 years of recovery of the ecosystem. Zinc trophodynamics in L. Nahuel Huapi food web was assessed using nitrogen stable isotopes (δ15N). There was no significant increase of Zn concentrations ([Zn]) in L. Nahuel Huapi biota after the PCCVC eruption, despite the evidence of [Zn] increase in lake water that could be associated with volcanic ash leaching. The organisms studied exhibited [Zn] above the threshold level considered for dietary deficiency, regulating Zn adequately even under a catastrophic situations like PCCVC 2011 eruption. Zinc concentrations exhibited a biodilution pattern in the lake's food web. To the best of our knowledge, present research is the first report of Zn biodilution in lacustrine systems, and the first to study Zn transfer in a freshwater food web including both pelagic and benthic compartments.

Bioindication of mercury, arsenic and uranium in the apple snail Pomacea canaliculata (Caenogastropoda, Ampullariidae): Bioconcentration and depuration in tissues and symbiotic corpuscles.

Pomacea canaliculata is a mollusk potentially useful as a biomonitor species of freshwater quality. This work explores the ability of snail tissues and symbiotic corpuscles to bioconcentrate and depurate mercury, arsenic, and uranium. Adult snails cultured in metal-free reconstituted water were exposed for eight weeks (bioaccumulation phase) to water with Hg (2 µgL-1), As (10 µgL-1), and U (30 µgL-1) and then returned to the reconstituted water for other additional eight weeks (depuration phase). Elemental concentrations in digestive gland, kidney, symbiotic corpuscles and particulate excreta were determined by neutron activation analysis. The glandular symbiotic occupancy was measured by morphometric analysis. After exposure, the kidney showed the highest concentration of Hg, while the digestive gland accumulated mainly As and U. The subcellular distribution in symbiotic corpuscles was ∼71%, ∼48%, and ∼11% for U, Hg, and As, respectively. Tissue depuration between weeks 8 and 16 was variable amongst elements. At week 16, the tissue depuration of U was the highest (digestive gland = 92%; kidney = 80%), while it was lower for Hg (digestive gland = 51%; kidney = 53%). At week 16, arsenic showed a differential pattern of tissue depuration (digestive gland = 23%; kidney = 88%). The symbiotic detoxification of the three elements in excreta was fast between weeks 8 and 10 and it was slower after on. At the end of the depuration, each element distributed differentially in digestive gland and symbiotic corpuscles. Our findings show that symbiotic corpuscles, digestive gland and kidney P. canaliculata are sensitive places for biomonitoring of Hg, As and U.

Species- and habitat-specific bioaccumulation of total mercury and methylmercury in the food web of a deep oligotrophic lake.

Niche segregation between introduced and native fish in Lake Nahuel Huapi, a deep oligotrophic lake in Northwest Patagonia (Argentina), occurs through the consumption of different prey. Therefore, in this work we analyzed total mercury [THg] and methylmercury [MeHg] concentrations in top predator fish and in their main prey to test whether their feeding habits influence [Hg]. Results indicate that [THg] and [MeHg] varied by foraging habitat and they increased with greater percentage of benthic diet and decreased with pelagic diet in Lake Nahuel Huapi. This is consistent with the fact that the native creole perch, a mostly benthivorous feeder, which shares the highest trophic level of the food web with introduced salmonids, had higher [THg] and [MeHg] than the more pelagic feeder rainbow trout and bentho-pelagic feeder brown trout. This differential THg and MeHg bioaccumulation observed in native and introduced fish provides evidence to the hypothesis that there are two main Hg transfer pathways from the base of the food web to top predators: a pelagic pathway where Hg is transferred from water, through plankton (with Hg in inorganic species mostly), forage fish to salmonids, and a benthic pathway, as Hg is transferred from the sediments (where Hg methylation occurs mostly), through crayfish (with higher [MeHg] than plankton), to native fish, leading to one fold higher [Hg].

Silver bioaccumulation in chironomid larvae as a potential source for upper trophic levels: a study case from northern Patagonia.

Silver (Ag) is a pollutant of high concern in aquatic ecosystems, considered among the most toxic metallic ions. In lacustrine environments, contaminated sediments are a source of Ag for the food web. Chironomidae (Insecta: Diptera) are the most abundant, diverse, and representative insect groups in aquatic ecosystems. Chironomid larvae are closely associated to benthic substrates and link primary producers and secondary consumers. Given their trophic position and their life habits, these larvae can be considered the entry point for the transference of Ag, from the benthic deposit to the higher trophic levels of the food web. Previous studies in lakes from Nahuel Huapi National Park (Northern Patagonia) showed Ag enrichment over background levels (0.04-0.1 µg g-1 dry weight) both in biota (bivalves and fish liver) and sediments from sites near human settlements. The aim of this study was to analyze the role of chironomids in the transference of Ag from the benthic reservoir of Lake Moreno Oeste to the food web. The concentration of Ag in chironomid larvae tissue ranged from 0.1 to 1.5 µg g-1 dry weight, reaching a bioaccumulation factor up to 17 over substrates and depending on the associated substrate type, feeding habitats, larval stage, and season. The main Ag transfer to higher trophic levels by chironomids occurs in the littoral zone, mostly from larvae inhabiting submerged vegetation (Myriophyllum quitense) and sediment from vegetated zones. This study presents novel evidence of the doorway role played by chironomid larvae in Ag pathways from the sediments into food webs of freshwater ecosystems.

Mercury and selenium in the food web of Lake Nahuel Huapi, Patagonia, Argentina.

Despite located far from point sources of Hg pollution, high concentrations were recorded in plankton from the deep oligotrophic Lake Nahuel Huapi, located in North Patagonia. Native and introduced top predator fish with differing feeding habits are a valuable economic resource to the region. Hence, Hg and Se trophic interactions and pathways to these fish were assessed in the food web of this lake at three sites, using stable nitrogen and carbon isotopes. As expected based on the high THg in plankton, mercury did not biomagnify in the food web of Lake Nahuel Huapi, as most of the THg in plankton is in the inorganic form. As was observed in other aquatic systems, Se did not biomagnify either. When trophic pathways to top predator fish were analyzed, they showed that THg biomagnified in the food chains of native fish but biodiluted in the food chains of introduced salmonids. A more benthic diet, typical of native fish, resulted in higher [THg] bioaccumulation than a more pelagic or mixed diet, as in the case of introduced fish. Se:THg molar ratios were higher than 1 in all the fish species, indicating that Se might be offering a natural protection against Hg toxicity.

Heavy metal and trace elements in riparian vegetation and macrophytes associated with lacustrine systems in Northern Patagonia Andean Range.

Vegetation associated with lacustrine systems in Northern Patagonia was studied for heavy metal and trace element contents, regarding their elemental contribution to these aquatic ecosystems. The research focused on native species and exotic vascular plant Salix spp. potential for absorbing heavy metals and trace elements. The native species studied were riparian Amomyrtus luma, Austrocedrus chilensis, Chusquea culeou, Desfontainia fulgens, Escallonia rubra, Gaultheria mucronata, Lomatia hirsuta, Luma apiculata, Maytenus boaria, Myrceugenia exsucca, Nothofagus antarctica, Nothofagus dombeyi, Schinus patagonicus, and Weinmannia trichosperma, and macrophytes Hydrocotyle chamaemorus, Isöetes chubutiana, Galium sp., Myriophyllum quitense, Nitella sp. (algae), Potamogeton linguatus, Ranunculus sp., and Schoenoplectus californicus. Fresh leaves were analyzed as well as leaves decomposing within the aquatic bodies, collected from lakes Futalaufquen and Rivadavia (Los Alerces National Park), and lakes Moreno and Nahuel Huapi (Nahuel Huapi National Park). The elements studied were heavy metals Ag, As, Cd, Hg, and U, major elements Ca, K, and Fe, and trace elements Ba, Br, Co, Cr, Cs, Hf, Na, Rb, Se, Sr, and Zn. Geochemical tracers La and Sm were also determined to evaluate contamination of the biological tissues by geological particulate (sediment, soil, dust) and to implement concentration corrections.

Source and trophic transfer of mercury in plankton from an ultraoligotrophic lacustrine system (Lake Nahuel Huapi, North Patagonia).

The incorporation and trophic transfer of total and methyl mercury (THg, MeHg) were examined in three size classes of plankton (10-53, 53-200, and >200 µm size range) and a small planktivorous fish, Galaxias maculatus, from the large multi-branched Lake Nahuel Huapi (North Patagonia, Argentina). Three sites representing a large range of lake benthic-pelagic structures (based on depth and shoreline characteristics) and precipitation regimes were sampled. Nitrogen and carbon stable isotopes (δ(15)N, δ(13)C) were analyzed to assess Hg trophodynamics. Selenium concentrations were determined together with THg in order to consider its potential effect on Hg trophodynamics. High THg concentrations (0.1-255 µg g(-1) dry weight (DW)) were measured in plankton, largely in inorganic form (MeHg: 3-29 ng g(-1) DW, 0.02-7% of THg, in the two larger size classes). A trend of increasing THg concentrations, varying in two to three orders of magnitude, with decreasing plankton size was associated with precipitation measured prior to each sampling event. Passive adsorption of dissolved Hg(2+) from wet deposition and runoff is considered to be the principal Hg uptake mechanism at the base of the pelagic food web. Despite the initially high THg uptake in the smaller plankton classes, the transfer to G. maculatus, and consequently to the entire food web, is likely limited due to low proportion of MeHg to THg in plankton. Furthermore, evidence of G. maculatus with benthic feeding habits having higher impact on MeHg trophic transfer compared to the same species with more pelagic (e.g., zooplankton) feeding habits, was observed. Although there is a high THg uptake in plankton, limited amounts are incorporated in the entire food web from the pelagic compartment.

Differential mercury transfer in the aquatic food web of a double basined lake associated with selenium and habitat.

Food web trophodynamics of total mercury (THg) and selenium (Se) were assessed for the double-basined ultraoligotrophic system of Lake Moreno, Patagonia. Each basin has differing proportions of littoral and pelagic habitats, thereby providing an opportunity to assess the importance of habitat (e.g. food web structure or benthic MeHg production) in the transfer of Hg and Se to top trophic fish species. Pelagic plankton, analyzed in three size classes (10-53, 53-200, and >200 µm), had very high [THg], exceeding 200 µg g(-1) dry weight (DW) in the smallest, and a low ratio of MeHg to THg (0.1 to 3%). In contrast, [THg] in littoral macroinvertebrates showed lower values (0.3 to 1.8 µg g(-1) DW). Juvenile and small fish species feeding upon plankton had higher [THg] (0.2 to 8 µg g(-1) muscle DW) compared to large piscivore fish species (0.1 to 1.6 µg g(-1) muscle DW). Selenium concentrations exhibited a much narrower variation range than THg in the food web, varying from 0.5 to 2.7 µg g(-1) DW. Molar Se:Hg ratios exceeded 1 for the majority of organisms in both basins, with most ratios exceeding 10. Using stable nitrogen isotopes as indicator of trophic level, no significant correlations were found with [THg], [Se] or Se:Hg. The apparent lack of biomagnification trends was attributed to elevated [THg] in plankton in the inorganic form mostly, as well as the possibility of consistent Se supply reducing the biomagnification in the food web of the organic portion of THg.

Selenium species and their distribution in freshwater fish from Argentina.

The distribution and speciation of selenium (Se) in freshwater fish (muscle and liver tissue) from lakes in Argentina was investigated. Three introduced species, brown trout (Salmo trutta), rainbow trout (Oncorhynchus mykiss) and brook trout (Salvelinus fontinalis), and one native species, creole perch (Percichthys trucha), were investigated. Values for total selenium in muscle ranged from 0.66 to 1.61 µg/g, while in the liver, concentrations were much higher, from 4.46 to 73.71 µg/g on a dry matter basis. Separation of soluble Se species (SeCys(2), selenomethionine (SeMet), SeMeSeCys, selenite and selenate) was achieved by ion exchange chromatography and detection was performed by inductively coupled plasma-mass spectrometry. The results showed that in fish muscle, from 47 to 55 % of selenium was soluble and the only Se species identified was SeMet, which represented around 80 % of soluble Se, while in the liver, the amount of soluble Se ranged from 61 to 76 % and the percentage of species identified (SeMet and SeCys(2)) was much lower and ranged from 8 to 17 % of soluble Se.

Influence of dissolved organic matter character on mercury incorporation by planktonic organisms: an experimental study using oligotrophic water from Patagonian lakes.

Ligands present in dissolved organic matter (DOM) form complexes with inorganic divalent mercury (Hg2+) affecting its bioavailability in pelagic food webs. This investigation addresses the influence of a natural gradient of DOM present in Patagonian lakes on the bioaccumulation of Hg2+ (the prevailing mercury species in the water column of these lakes) by the algae Cryptomonas erosa and the zooplankters Brachionus calyciflorus and Boeckella antiqua. Hg2+ accumulation was studied through laboratory experiments using natural water of four oligotrophic Patagonian lakes amended witht'97Hg2+. The bioavailability of Hg2+ was affected by the concentration and character of DOM. The entrance of Hg2+ into pelagic food webs occurs mostly through passive and active accumulation. The incorporation of Hg2+ by Cryptomonas, up to 27% of the Hg2+ amended, was found to be rapid and dominated by passive adsorption, and was greatest when low molecular weight compounds with protein-like or small phenolic signatures prevailed in the DOM. Conversely, high molecular weight compounds with a humic or fulvic signature kept Hg2+ in the dissolved phase, resulting in the lowest Hg2+ accumulation in this algae. In Brachionus and Boeckella the direct incorporation of Hg from the aqueous phase was up to 3% of the Hg2+ amended. The dietary incorporation of Hg2+ by Boeckella exceeded the direct absorption of this metal in natural water, and was remarkably similar to the Hg2+ adsorbed in their prey. Overall, DOM concentration and character affected the adsorption of Hg2+ by algae through competitive binding, while the incorporation of Hg2+ into the zooplankton was dominated by trophic or dietary transfer.

Apple snails and their endosymbionts bioconcentrate heavy metals and uranium from contaminated drinking water.

PURPOSE: The differential ability of apple snail tissues, endosymbionts, and eggs to bioaccumulate several metals (Sb, As, Ba, Br, Zn, Cr, Fe, Hg, Se, and U) was investigated. METHODS: Metal concentrations were determined by neutron activation analysis in several tissues, endosymbionts, and eggs from mature apple snails cultured in either drinking water or reconstituted water (prepared with American Society for Testing and Materials type I water). RESULTS: The highest bioconcentration factors (BCFs) in the midgut gland were found for Ba, Zn, Se, As, U, Br, and Hg (in decreasing order), while the highest in the kidney were for Ba, Br, and Hg. The foot showed the highest BCFs for Ba, Hg, Br, and Se (in decreasing order). Calcified tissues (uterus, shell) and eggs showed low BCFs, except for Ba. Both C corpuscles and gland tissue showed statistically higher BCFs than K corpuscles for Ba, Fe, U, Br, and Sb. The concentration of most of the studied elements was significantly lower in tissues and endosymbionts obtained from snails cultured in reconstituted water instead of drinking water. Snails cultured in reconstituted water and then exposed or not to Hg, As, and U (at the maximum contaminant level allowed by the US Environmental Protection Agency) also resulted in high levels accumulated in midgut gland, endosymbionts and kidney. CONCLUSIONS: Our findings suggest that the midgut gland (and the symbionts contained therein), the kidney, and the foot of Pomacea canaliculata may be useful bioindicators of Hg, As and U pollution in freshwater bodies and that the unrestricted use of ampullariid snails as human and animal food must be considered with caution.