Bioaccumulation and trophic transfer of metals, As and Se through a freshwater food web affected by antrophic pollution in Córdoba, Argentina

https://doi.org/10.1016/j.ecoenv.2017.10.028Get rights and content

Highlights

  • Plankton showed the greatest capacity to bioaccumulate inorganic elements.

  • Aluminium, Cr, Mn, Fe, Ni, Cu, Zn, Ag, Cd, Pb, As and Se showed biodilution.

  • Mercury showed biomagnification throughout different components of the food web.

  • Elements thrown into environment can be biomagnified being back into human food.

Abstract

The concentration of metals (Al, Cr, Mn, Fe, Ni, Cu, Zn, Ag, Cd, Hg, Pb, U), As and Se in different ecosystem components (water, sediment, plankton, shrimp, and fish muscle) has been determined in a eutrophic reservoir in the Province of Córdoba (Argentina). Los Molinos Lake (LML) was sampled during the dry (DS) and wet seasons (WS) in order to examine the bioaccumulation and transfer of these inorganic elements through the food web. Stable nitrogen isotope (δ15N) was used to investigate trophic interactions. According to this, samples were divided into three categories: plankton, shrimp (Palaemonetes argentinus) and fish (Silverside, Odontesthes bonariensis). The bioaccumulation factor (BAF) was calculated for the organisms, and it was determined that the elements analyzed undergo bioaccumulation, especially in organisms such as plankton. The invertebrates were characterized by the highest BAF for Cu and Zn in both seasons, As (DS), and Cd and Hg (WS). The fish muscle was characterized by the highest BAF for Se (WS), Ag and Hg (DS). On the other hand, a significant decrease in Al, Cr, Mn, Fe, Ni, Cu, Zn, As, Se, Cd and U concentrations through the analyzed trophic web during both seasons was observed. Moreover, a significant increase in Hg levels was observed with increasing trophic levels in the DS, indicating its biomagnification.

Despite the increasing impact of metals, As and Se pollution in the studied area due to urban growth and agricultural and livestock activities, no previous study has focused on the behavior and relationships of these pollutants with the biotic and abiotic components of this aquatic reservoir. We expect that these findings may be used for providing directions or guidance for future monitoring and environmental protection policies.

Introduction

An aquatic ecosystem is a habitat for aquatic organisms and also a reservoir of potential persistent chemicals (Achary et al., 2017). The advance of technology, the increasing amount of waste materials and a growing population have often resulted in the transformation of lakes, rivers and coastal waters into waste depots, where the natural balance is severely upset and, in cases, totally disrupted (Sharma, 2014). Some of the severe pollutants that have drawn more attention are metals and the metalloid As. They are a global concern, due to their potential toxic effect, persistence and ability to bioaccumulate in aquatic ecosystems (Hall, 2002, David et al., 2012, Batvari et al., 2015).

The introduction of these contaminants into the aquatic system derives from various sources; they can be present due to naturally occurring deposits or through anthropogenic activities (Ekeanyanwu et al., 2010, Merciai et al., 2014). The latter might be from smelting processes, fuel combustion entering the system via atmospheric fallout, effluents and dumping activities, from runoff of terrestrial systems, land application of sewage materials and leaching of garbage. Metals and As tend to be trapped in the aquatic environment and accumulate in sediment, being directly available to benthic fauna or released to the water column through different ways, increasing the dissolved concentration in the environment and threatening the ecosystem (Pekey et al., 2004). In addition to sediment and water, this kind of elements can enter the food web through organisms taken as part of the diet (zooplankton, phytoplankton, and benthos) or by uptake through the gills and skin, and be potentially accumulated in edible fish in aquatic ecosystems (Ahmed et al., 2015). This mobilization means that they can be accumulated in the body tissues of living organisms (bioaccumulation) and transferred through aquatic food webs, increasing the concentration as they pass from lower trophic levels to higher trophic levels (biomagnification). In contrast, a number of studies have documented biodilution, whereby metal/loids concentration in tissues decreases with increasing trophic position (van Hattum et al., 1991, Van Hattum et al., 1996, Besser et al., 2001, Farag et al., 1998, Quinn et al., 2003). The link between the elements and their accumulation or dilution in aquatic organisms also depends on the species, toxic and physicochemical conditions, and exposure routes (Croteau et al., 2005). There is also influence of the biological and ecological factors of the species that make up the food chain, such as eating habits, habitat, age, sex, health and the mechanisms of detoxification (Soto-Jiménez, 2011).

Naturally occurring stable isotopes of carbon (δ13C) and nitrogen (δ15N) can be used as tracers to investigate the trophic relationships in foodwebs and any potential biomagnification of contaminants (Cui et al., 2011). A powerful tool to quantify the trophic position is δ15N, because its enrichment occurs incrementally across trophic levels with a constant rate (3–4‰). δ13C is generally used to provide information on spatial habitat use and carbon sources in addition to trophic relationships, and it is enriched in consumer tissues to a minor degree, approx. 1‰ among different trophic levels (Dehn et al., 2006). Thus, δ13C is also considered as a valuable biomarker for identifying different sources of primary production (Hobson et al., 2002, Hoekstra et al., 2003). Stable isotope analyses are widely used in ecotoxicological studies to elucidate contaminant behavior (e.g., bioconcentration and biomagnification) through the whole trophic chain (Cui et al., 2011).

Los Molinos Lake (LML) has been classified as mesotrophic to eutrophic, with recurrent cyanobacterial blooms and impaired water quality in summer and spring (Bazán et al., 2014). It was constructed for the purposes of providing drinking water, hydroelectrical power, irrigation, and flood control. In recent years, it has suffered natural impacts (fires and floods in the surrounding areas) and strong anthropogenic pressure by the growth of urban settlements and tourist facilities without planning or control. Currently, this water body represents a major touristic attraction for the region, and it is also used for recreational activities like fishing and water sports. The main activities performed in the catchment area are related to agriculture (soybean, corn and potato) and livestock, different animals (cows and horses) graze in the west coast of the reservoir and use it as a drinking trough (Rodriguez Reartes et al., 2016), providing a direct discharge of their manure into the water body. The treatment of domestic wastewater in LML is made through septic tanks and cesspools, which are insufficient due to the soil characteristics of the area, and the proximity of the dwellings to the reservoir (<50 m from the coast for some buildings) (Rodriguez Reartes et al., 2016). Aditionally, around the lake there are hundreds of rafts that are inhabited in a permanent way, which produce different types of wastes, which are directly thrown into the reservoir. Therefore, there is a large direct discharge of domestic effluents, i.e. without previous treatment, into the lake.

While some studies have analyzed the behavior and relationships of metals in the biotic and abiotic components of aquatic environments (Aderinola et al., 2009, Jara-Marini et al., 2009, Mathews and Fisher, 2008), most of the research on these pollutants has focused on isolated components, e.g. sediments (Aprile and Bouvy, 2008), water (Melgar et al., 2008), plants (Bayen, 2012) or fish (Malik et al., 2010). The bioavailability and the potential for bioaccumulation and biomagnification of inorganic elements in all components of an ecosystem are high; hence the importance to understand the pollutant dynamics in the aquatic environments.

One of the major pathways of human exposure to metal/loids is fish consumption, reaching > 90% compared to other routes of exposure, like dermal contact and inhalation (Griboff et al., 2017). Silverside (Odontesthes bonariensis) is a characteristic fish from the central region of Argentina in South America, and it is considered by different authors (Sagretti and Bistoni, 2001, Vila and Soto, 1986) as an omnivorous species, which is known to shift its diet depending on the size of the individual. The small ones (< 25 cm length) feed on plankton and invertebrates, while the big ones (>30 cm length) eat fish as primary food. This species is of economic importance, because it is widely used for commercial and sport fishing, being, for Argentina and Uruguay, the second most important fishery resource for local consumption as well as for exportation (Avigliano et al., 2015).

For all of the above, we consider it extremely important to evaluate the level of contamination in the reservoir, analyzing metals in abiotic and biotic samples. Therefore, the aims of this study are: 1) to determine metal, As and Se content in water, sediment, plankton, shrimp (Palaemonetes argentinus) and fish muscle (Odontesthes bonariensis) samples in LML to evaluate the influence of two contrasting climatic seasons (dry and rainy); and 2) to investigate the trophic transfer behavior of studied elements within an aquatic food web (water, plankton, shrimp and fish). Despite previous reports showing bioaccumulation or biomagnification of inorganic elements within aquatic ecosystems, our study aims to present the transfer of several elements (metals and metalloids) through a limited food web, showing similarities and discrepancies with previous reports, thus triggering the need for further research in this area.

Section snippets

Study area

LML (31°43’30’’S, 64°32’20’’W) is an artificial water body located in the fault-bounded valleys of Calamuchita, located 65 km SW of Córdoba city (Argentina) (Fig. 1). It is confined by the Sierras Chicas (East) and Sierras Grandes (West). The main tributaries are the San Pedro River, Los Espinillos River, del Medio River and Los Reartes River. It has just one effluent, Los Molinos River. The lake has an area of 21.1 km2, a maximum volume of 400 hm3, and a maximum depth of 52 m. Its retention time

Multi-element concentration in abiotic samples

In Table 2, concentrations of metals, As and Se in water (μg L−1) and sediment (μg g−1 dw) samples in the DS and WS are shown. On a temporal scale, the concentration of the inorganic elements in water was different; Al, Mn, Fe, Cu and As had higher concentrations during the WS, Ni and U were higher during the DS, and Cr, Se, Ag, Cd and Hg were below the detection limit in both seasons. Localized inputs like river and backwater inputs, atmospheric fall-out as well as variation in different

Conclusions

The concentration of metals, As and Se in water and sediment samples from the LML did not appear to be exerting toxic effects on the aquatic biota, considering that their levels were below the limits established by the appropriate legislation. Our current results indicate a significant difference in the concentration of some elements within and between studied organisms, being bioaccumulated in all studied organisms, especially in plankton. Mercury showed biomagnification through the different

Acknowledgements

Authors would like to acknowledge grants and fellows from the Agencia Nacional de Promoción Científica y Técnica (FONCyT/PICT-1411), CONICET (National Research Council PIP: 11220110101084), and Secretaría de Ciencia y Tecnología (PIP: 30720130100459 CB) from the National University of Córdoba (Argentina).

Conflict of interest

The authors declare that there are no conflicts of interest.

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