Accumulation of As, Cd, Pb, and Zn in sediment, chironomids and fish from a high-mountain lake: First insights from the Carnic Alps

https://doi.org/10.1016/j.scitotenv.2020.139007Get rights and content

Highlights

  • Levels of As, Cd, Pb, and Zn were detected in a high-mountain lake dietary pathway.

  • Trace element concentration decreased with increasing trophic level.

  • The highest BAF values were recorded for Cd and Zn in Diptera Chironomidae.

  • Very low TTF values were recorded in fish muscle and liver.

  • Diptera Chironomidae seems to be a good matrix for trace element monitoring.

Abstract

Though mountain lakes are generally much less influenced by human activities than other habitats, anthropogenic threats can still alter their natural condition. A major source of global environmental pollution in mountain ecosystems is trace element contamination. For this study we investigated for the first time the accumulation of As, Cd, Pb, and Zn in sediment, Diptera Chironomidae (prey), and bullhead Cottus gobio (predator) in a typical high-mountain lake (Dimon Lake) in the Carnic Alps. Significant differences in trace element levels were observed between sediment, Diptera Chironomidae, and C. gobio liver and muscle samples (Kruskal-Wallis test; p < .03 for all elements). As and Pb levels were highest in sediment, Cd and Zn levels were highest in Diptera Chironomidae, and the lowest values for all elements were measured in C. gobio muscle and liver. Bioaccumulation factor values were much higher in Diptera Chironomidae than fish muscle and liver, with the highest values recorded for Cd (5.16) and Zn (4.37). Trophic transfer factor values were very low for all elements in fish muscle and liver, suggesting a biodilution effect along the food chain. Further studies are needed to expand on these first findings that provide useful insights to inform environmental monitoring and policy in remote high-mountain lakes.

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.

References (83)

  • M. Horváth et al.

    Sequential extraction studies on aquatic sediment and biofilm samples for the assessment of heavy metal mobility

    Microchem. J.

    (2013)
  • F.R. Khan et al.

    Zn-stimulated mucus secretion in the rainbow trout (Oncorhynchus mykiss) intestine inhibits Cd accumulation and Cd-induced lipid peroxidation

    Aquat. Toxicol.

    (2013)
  • M. Klavinš et al.

    Metal accumulation in sediment and benthic invertebrates in lakes of Latvia

    Chemosphere

    (1998)
  • J.C. McGeer et al.

    Cadmium

  • K.F. Mossop et al.

    Comparison of original and modified BCR sequential extraction procedures for the fractionation of copper, iron, lead, manganese and zinc in soils and sediments

    Anal. Chim. Acta

    (2003)
  • S. Niyogi et al.

    Interaction between dietary calcium supplementation and chronic waterborne zinc exposure in juvenile rainbow trout, Oncorhynchus mykiss

    Comp Biochem Physiol C Toxicol Pharmacol

    (2006)
  • Y. Palacios-Torres et al.

    Trace elements in sediments and fish from Atrato River: an ecosystem with legal rights impacted by gold mining at the Colombian Pacific

    Environ. Pollut.

    (2020)
  • P. Pastorino et al.

    Detection of trace elements in freshwater macrobenthic invertebrates of different functional feeding guilds: a case study in Northeast Italy

    Ecohydrology & Hydrobiology

    (2019)
  • P.S. Rainbow

    Trace metal concentrations in aquatic invertebrates: why and so what?

    Environ. Pollut.

    (2002)
  • J.R. Reinfelder et al.

    Trace element trophic transfer in aquatic organisms: a critique of the kinetic model approach

    Sci. Total Environ.

    (1998)
  • N. Roig et al.

    Metal bioavailability in freshwater sediment samples and their influence on ecological status of river basins

    Sci. Total Environ.

    (2016)
  • A. Ruus et al.

    Experimental results on bioaccumulation of metals and organic contaminants from marine sediments

    Aquat. Toxicol.

    (2005)
  • S. Squadrone et al.

    Heavy metals distribution in muscle, liver, kidney and gill of European catfish (Silurus glanis) from Italian Rivers

    Chemosphere

    (2013)
  • S. Squadrone et al.

    Presence of trace metals in aquaculture marine ecosystems of the northwestern Mediterranean Sea (Italy)

    Environ. Poll.

    (2016)
  • J. Usero et al.

    Heavy metals in fish (Solea vulgaris, Anguilla anguilla and Liza aurata) from salt marshes on the southern Atlantic coast of Spain

    Environ. Int.

    (2004)
  • R.M. Vilanova et al.

    Polycyclic aromatic hydrocarbons in remote mountain lake waters

    Water Res.

    (2001)
  • A. Wagner et al.

    Biomonitoring of trace elements in muscle and liver tissue of freshwater fish

    Spectrochim. Acta B

    (2003)
  • R. Yang et al.

    Accumulation features of organochlorine pesticides and heavy metals in fish from high mountain lakes and Lhasa River in the Tibetan plateau

    Environ. Int.

    (2007)
  • H. Agah et al.

    Accumulation of trace metals in the muscle and liver tissues of five fish species from the Persian Gulf

    Environ. Monit. Assess.

    (2009)
  • A.H. Alhashemi et al.

    Bioaccumulation of trace elements in different tissues of three commonly available fish species regarding their gender, gonadosomatic index, and condition factor in a wetland ecosystem

    Environ. Monit. Assess.

    (2012)
  • N. Arslan et al.

    Metal contents in water, sediment, and Oligochaeta-Chironomidae of Lake Uluabat, a Ramsar site of Turkey

    Sci. World J.

    (2010)
  • M.M. Authman et al.

    Use of fish as bio-indicator of the effects of heavy metals pollution

    J Aquac Res Dev

    (2015)
  • E. Avigliano et al.

    Arsenic, selenium, and metals in a commercial and vulnerable fish from southwestern Atlantic estuaries: distribution in water and tissues and public health risk assessment

    Environ Sci Pollut R

    (2019)
  • L. Camarero

    Spreading of trace metals and metalloids pollution in lake sediments over the Pyrénées

    J. Phys. IV France

    (2003)
  • L. Camarero et al.

    Trace elements in alpine and arctic lake sediments as a record of diffuse atmospheric contamination across Europe

    Freshw. Biol.

    (2009)
  • J. Catalan et al.

    High mountain lakes: extreme habitats and witnesses of environmental changes

    Limnetica

    (2006)
  • J. Catalán et al.

    Remote European mountain lake ecosystems: regionalisation and ecological status

    Freshw. Biol.

    (2009)
  • E.N. Chernova et al.

    The content of metals in organisms of various trophic levels in freshwater and brackish lakes on the coast of the Sea of Japan

    Environ. Sci. Pollut. Res.

    (2019)
  • M.J. Chowdhury et al.

    Tissue-specific cadmium and metallothionein levels in rainbow trout chronically acclimated to waterborne or dietary cadmium

    Arch Environ Con Tox

    (2005)
  • J.L. Crane

    Phase IV GIS-Based Sediment Quality Database for the St. Louis River Area of Concern-Wisconsin Focus. Overview of Sediment Quality Conditions in the St. Louis River Area of Concern

    (2006)
  • J.L. Crane

    Sediment Quality Conditions in the Lower St. Louis River, Minnesota/Wisconsin

    (2006)
  • Cited by (25)

    • Evaluation of levels of black in black-odor waters through absorption coefficient method

      2022, Science of the Total Environment
      Citation Excerpt :

      Therefore, the absorption coefficient method could sensitively evaluate the levels of black in waters. The Kruskal-Willis tests showed significant differences in αp(λ) and αt(λ) between dark, light, and no black waters at various wavelengths (p < 0.05, Table S5) (Pastorino et al., 2020). Hence, the wavelength did not affect the evaluation of levels of black through αp(λ) and αt(λ).

    • Metal contamination in alkaline Phantom Lake (Flin Flon, Manitoba, Canada) generates strong responses in multiple paleolimnological proxies

      2022, Science of the Total Environment
      Citation Excerpt :

      Midges (Chironomidae, Chaoboridae) have larval aquatic life stages that are well-preserved in the sedimentary record and have previously been used to examine trends in the deposition of past contaminants (Il'yashuk et al., 2003; Thienpont et al., 2016), food-web dynamics (Uutala, 1990), and deep-water oxygen conditions (Quinlan and Smol, 2001). Midge larvae can assimilate metals from detritus or sediment and transfer contaminants to higher trophic levels, such as important fish prey (Pastorino et al., 2020). They are often sediment-associated and would therefore be exposed to accumulated contaminants (Il'yashuk et al., 2003).

    View all citing articles on Scopus
    View full text