Accumulation of As, Cd, Pb, and Zn in sediment, chironomids and fish from a high-mountain lake: First insights from the Carnic Alps
Graphical abstract
Introduction
High-mountain lakes are among the most remote aquatic environments in Europe (Catalan et al., 2006). As such, they provide a natural laboratory for ecological assessment, since their food webs are relatively simple in structural network compared to lowland lakes (Sánchez-Hernández et al., 2015). Although remote, their small size and high turnover of surface waters render mountain catchments extremely receptive and vulnerable to anthropogenic impact (Pastorino et al., 2019a). Since the 1980s, they have been affected by global anthropogenic impacts and have become a receptor for medium-range atmospheric transported (MRAT) organic and inorganic contaminants (Ferrario et al., 2017; Pastorino et al., 2020a). In the European Alps, altitudinal transport can occur over relatively short distances from sources of pollution in the industrialized areas of Germany, Switzerland, Austria, and northern Italy (Poma et al., 2017).
Aquatic ecosystems host well-adapted species and are a reservoir for organic and inorganic contaminants (Fleeger et al., 2003). Trace elements contamination is a major problem due to the persistence and accumulation of metals in the biotic and abiotic components of aquatic ecosystems (Purves, 2012; Esposito et al., 2018). Trace elements enter the aquatic environment from a variety of sources. Although most occur naturally through biogeochemical cycles, rapid industrialization has accelerated their dispersion in the environment through human activities, especially the combustion of fossil fuels (Förstner and Wittman, 1981; Borrell et al., 2016). Furthermore, trace elements attached to fine aerosols can be transported hundreds of kilometers away from the original source, washed out into the aquatic ecosystems during precipitation events, and contaminate the water column and the sediment (Pan and Wang, 2015). Trace element levels have increased in remote areas as a result of atmospheric deposition, solubilization, and mobilization of sediments which form the major sink for environmental contaminants (Karadede-Akin and Ünlü, 2007) that aquatic organisms can take up (Priju and Narayana, 2007). High-mountain lakes are therefore excellent indicators of air pollution because they are not usually subject to other forms of disturbance (e.g., land-use) (Tornimbeni and Rogora, 2012).
Moreover, due to climatic and geographical factors, high-mountain lakes may be more vulnerable to contamination than lowland lakes (Mosello et al., 2002; Catalán et al., 2009; Rogora et al., 2013). Research in European mountain areas has focused on organic pollutants in abiotic compartments (Vilanova et al., 2001), however, limited information is available concerning trace element bioaccumulation in aquatic organisms (Köck et al., 1996; Yang et al., 2007; Pastorino et al., 2019a, Pastorino et al., 2020a). Far more is known about other ecosystems, especially the accumulation of trace elements by fish (Wagner and Boman, 2003; Elia et al., 2010; Squadrone et al., 2013, Squadrone et al., 2016) and macrobenthic invertebrates (Goodyear and McNeill, 1999; Santoro et al., 2009; Pastorino et al., 2019b) in freshwater ecosystems. In addition, trace elements trapped in sediments can enter the food web through organisms taken as part of the diet, e.g., fish that prey on benthic organisms (Alhashemi et al., 2012; Zulkifli et al., 2016; Palacios-Torres et al., 2020).
Fish are at the top of the trophic chain and can accumulate large amounts of certain trace elements (Squadrone et al., 2013; Avigliano et al., 2019). The accumulation patterns of contaminants in fish and other aquatic organisms are driven by uptake and elimination rates (Guven et al., 1999). Trace elements and their compounds are taken up differentially by organs because of the affinity between them and are found at different concentrations in various organs of the body (Bervoets et al., 2001). Fish assimilate trace elements via several routes: ingestion of particulate material suspended in water, ingestion of food, ion-exchange of dissolved metals across lipophilic membranes (e.g., the gills, and adsorption via tissue and membrane surfaces). Their distribution in tissues depends on dietary or aqueous exposure or a sum of the two (Jezierska and Witeska, 2006; Hauser-Davis et al., 2012; Pouil et al., 2018). However, in high-mountain lakes the concentrations of heavy metals in water are often not detectable. For example, Tornimbeni and Rogora (2012) showed how Pb and Cd concentration values in water from 32 Alpine lakes were often below the detection limits of the method (0.08 and 0.01 μg L−1, respectively). Thus, waterborne metals uptake can be considered negligible in these environments, especially in alkaline water where metals accumulate in sediments (Pobi et al., 2019).
Though fish muscle is not a target tissue for accumulation during acute exposure, it is a good indicator of chronic exposure (Has-Schön et al., 2006; Taweel et al., 2012). When contaminates exceed all biological defense barriers, trace elements begin to accumulate in muscle tissue (Kalay et al., 1999). But because muscle tissue is not always a good indicator of trace element accumulation in the entire body, other organs such as the liver need to be analyzed as well (Has-Schön et al., 2006).
No studies to date have investigated trace element accumulation from sediment to fish in high-mountain lakes in Alps. The aim of the present study was: a) to measure the levels of As, Cd, Pb, and Zn in sediment, the whole body of macrobenthic invertebrates (prey), and fish (predator) muscle and liver tissues; b) to determine the difference in trace element levels between these matrices; c) to evaluate the bioaccumulation factor (BAF) and the trophic transfer factor (TTF) values for prey and predator in a typical high-mountain lake (Dimon Lake) located in northeast Alps. The four trace elements (As, Cd, Pb, and Zn) were chosen based on available data for high-mountain lakes (Camarero et al., 2009; Pastorino et al., 2020a) and on their relevance for trophic levels in freshwater environments (Chernova and Lysenko, 2019).
Section snippets
Study site
Dimon Lake (46° 34′ 4.17″ N 13° 03′ 43.12″ E; Fig. 1) is a high-mountain lake located above the tree line in the Carnic Alps (municipality of Ligosullo, Udine Province, Friuli Venezia-Giulia, northeast Italy) at 1857 m a.s.l. Dimon Lake is a glacial-origin lake and is classified as a Site of Community Interest and Special Areas of Conservation (SCI/SAC-IT3320002 Monti Dimon e Paularo). The lake lies on sandstone and volcanic rock and has a maximum depth of 4.27 m. Originally fishless, fish were
Surface sediment
Fig. 2 shows the trace element levels (mean ± standard deviation) in the sediment samples from Dimon Lake. The mean concentration was in the order: Zn (138.8 ± 0.6) > Pb (109.6 ± 1.2) > As (39.5 ± 0.7) > Cd (0.61 ± 0.02) mg kg−1.
Macrobenthic invertebrates
The macrobenthic invertebrate community was composed chiefly of Hexapoda belonging to Diptera Chironomidae (75.2%) with four subfamilies (Prodiamesinae, Chironominae, Orthocladiinae, and Tanypodinae). The Prodiamesinae subfamily was represented by the single species
Discussion
High-mountain lake are precious ecosystems located far from industrialized area and provide habitat for few, but well adapted species. They are a sink for contaminants from the industrialized lowland regions (Camarero, 2003, Camarero et al., 2009). Dimon Lake is a receptor of trace element contamination originating from anthropic activities, dispersed in the atmosphere, and deposited via abundant annual precipitation throughout the year (Pastorino et al., 2019a).
Camarero et al. (2009) measured
Conclusions
This study presents first insights into trace element accumulation and transfer along a simple food chain from a high-mountain lake. Sediment is a major sink for As and Pb, whereas Diptera Chironomidae had the highest Cd and Zn levels. Trace element levels were lowest in fish tissues. BAF and TTF values were very low for all elements, suggesting a biodilution effect that merits future study. It is likely that fish regulate trace element intake and uptake from their environment. Environmental
CRediT authorship contribution statement
Paolo Pastorino:Conceptualization, Data curation, Investigation, Methodology, Writing - original draft, Writing - review & editing, Validation, Writing - review & editing.Marino Prearo:Conceptualization, Data curation, Investigation, Methodology, Supervision, Validation, Writing - review & editing.Marco Bertoli:Investigation, Methodology, Validation, Writing - review & editing.Maria Cesarina Abete:Data curation, Investigation, Methodology, Validation, Writing - review & editing.Alessandro Dondo:
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
The authors would like to thank the Ente Tutela Patrimonio Ittico del Friuli Venezia-Giulia and the Municipality of Ligosullo (UD) for their technical support.
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