Elsevier

Environmental Pollution

Volume 159, Issue 10, October 2011, Pages 2861-2869
Environmental Pollution

Accumulation of mercury and methylmercury by mushrooms and earthworms from forest soils

https://doi.org/10.1016/j.envpol.2011.04.040Get rights and content

Abstract

Accumulation of total and methyl-Hg by mushrooms and earthworms was studied in thirty-four natural forest soils strongly varying in soil physico-chemical characteristics. Tissue Hg concentrations of both receptors did hardly correlate with Hg concentrations in soil. Both total and methyl-Hg concentrations in tissues were species-specific and dependent on the ecological groups of receptor. Methyl-Hg was low accounting for less than 5 and 8% of total Hg in tissues of mushrooms and earthworms, respectively, but with four times higher concentrations in earthworms than mushrooms. Total Hg concentrations in mushrooms averaged 0.96 mg Hg kg−1 dw whereas litter decomposing mushrooms showed highest total Hg and methyl-Hg concentrations. Earthworms contained similar Hg concentrations (1.04 mg Hg kg−1 dw) whereas endogeic earthworms accumulated highest amounts of Hg and methyl-Hg.

Highlights

► Hg and MeHg concentrations in mushrooms and earthworms at unpolluted forest soils. ► Mushrooms and earthworms contained similar Hg concentrations. ► MeHg was present in traces but four times higher in earthworms than in mushrooms. ► Ecophysiological group influenced Hg and MeHg concentration in both receptors.

Introduction

Mercury (Hg) is released in the atmosphere by natural (e.g. volcanic eruptions, forest fires, evaporation from soils and water) and anthropogenic processes (e.g. fossil fuel combustion, gold mining, ore roasting and processing) (Schroeder and Munthes, 1997, Pacyna et al., 2006, Swain et al., 2007). The annual global Hg input into the atmosphere is above 6000 tons (Swain et al., 2007) whereby the residence time of elementar Hg in the atmosphere is approximately one year (Fitzgerald and Mason, 1997). Therefore, Hg released to the atmosphere can be distributed over long distances and deposited in area far away from its source. Higher Hg contents in soils and water usually appear near mining areas (Kalač et al., 1996, Kocman et al., 2004, Swain et al., 2007) or chlor-alkali plants (Zagury et al., 2006, Gibičar et al., 2009).

Mercury and especially the organic form monomethylmercury (methyl-Hg) are highly toxic for microorganisms, animals and humans (Boening, 2000, Mason and Benoit, 2003). The lipophilic nature of methyl-Hg results in much more efficient accumulation in organisms compared to inorganic Hg. Different groups of organisms like bacteria and mushrooms showed the capacity to methylate Hg (Vonk and Sijpesteijn, 1973). Methylation of Hg was observed under different conditions but mainly under anoxic situations (St. Louis et al., 1996, Schwesig et al., 1999, Drott et al., 2007, Holloway et al., 2009). The contents of methyl-Hg in soils are low, whereas the percentage of methyl-Hg compared to total Hg contents in soils is nominal in a range between 0.5 and 1.5% (Boudou and Ribeyre, 1997).

In soils Hg is highly immobile and mainly accumulates in the top layers due to its strong affinity to organic matter and soil minerals thereby reducing the concentrations in the soil solution (Ravichandran, 2004). Therefore the bioavailability of Hg in soils is usually low (Tipping et al., 2010). Accumulation of Hg and methyl-Hg in soil organisms is important in particular with respect to the estimation of the risk of secondary poisoning (Ernst et al., 2008). Mushrooms and earthworms are interesting to examine different pathways of exposure to Hg from soil: (1) uptake from soil solution (predominantly mushrooms), (2) decomposition of litter and soil organic matter by mushrooms, and (3) ingestion of soil particles and litter by earthworms (Ernst and Frey, 2007). Mushrooms are well known to accumulate Hg (e.g. Stegnar et al., 1973, Byrne et al., 1976, Seeger and Nutzel, 1976, Minagava et al., 1980, Kalač et al., 1991, Kalač et al., 1996, Alonso et al., 2000, Falandysz et al., 2002, Falandysz et al., 2003, Cocchi et al., 2006, Svoboda et al., 2006) due to their filamentous mode of growth, branching and extra cellular release of enzymes and metabolites. In contrast, studies on the accumulation of methyl-Hg in mushrooms are a few (Stegnar et al., 1973, Minagava et al., 1980, Bargagli and Baldi, 1984, Fischer et al., 1995). Similarly, investigations on the accumulation of Hg (Burton et al., 2006, Ernst et al., 2008) and in particular of methyl-Hg in earthworms are also rare (Bull et al., 1977, Hinton and Veiga, 2002, Zhang et al., 2009). However, most studies regarding Hg accumulation in mushrooms and earthworms have been conducted in polluted sites, but investigations in non-contaminated sites, in particular forest soils, are rare (Stegnar et al., 1973, Ernst et al., 2008). Therefore, there is an urgent need to study the bioavailability of Hg and methyl-Hg in mushrooms and earthworms collected from non-contaminated forest soils to estimate the risk of secondary poisoning.

The aim of this study was to determine and compare total and methyl-Hg concentrations in two biological receptors from non-contaminated forest sites. In particular, we were interested on the accumulation of total Hg and methyl-Hg in the different ecophysiological groups of mushrooms (mycorrhizal, wood and litter decomposing saprotrophs) and earthworms (epigeic, endogeic, anecic).

Section snippets

Sampling and sample preparation

Earthworms and fruiting bodies of mushrooms were collected at 34 well characterized forest sites (Walthert et al., 2004, Blaser et al., 2005, Zimmermann et al., 2006) distributed over Switzerland (Fig. 1). Forest sites from the Swiss Alps were excluded due to their special climatic conditions. Except for three sites, all sampling points were non-contaminated forest soils with different physico-chemical characteristics. Smelters were located in the vicinity of two sites (Gerlafingen, Visp) and a

General soil properties and Hg and methyl-Hg concentrations

The investigated sites contained a wide range of soil and forest types (Table 1). Measured pH ranged from 2.9 (Krauchthal) to 7.2 (Neunkirch). The total Hg in soils ranged between 0.07 (Jussy) and 0.55 (Visp) mg Hg kg−1 dry soil by an average value of 0.18 mg Hg kg−1 dry soil. Three forest sites were expected to be contaminated because of the vicinity to a smelter industry (Gerlafingen, Visp) or a shooting range (Zuchwil). However, only one site (Visp) showed elevated Hg concentration

Mercury concentrations in forest soils

Former studies examining Hg concentrations in mushrooms and earthworms were mainly carried out in polluted soils. Total Hg concentrations in the top layer of our studied forest soils ranged between 0.07 and 0.55 mg Hg kg−1 dry soil (about 0.001–0.156 mg Hg g−1 organic matter), which were in accordance to observations of Byrne et al. (1976) reported from unpolluted sites (range between 0.08 and 0.33 mg Hg kg−1 dry soil) and were about 20–40 times lower than in studies from polluted soils (Bull

Conclusion

Mercury and methyl-Hg concentrations in mushrooms and earthworms from non-contaminated Swiss forest soils were low compared to literature. Both total and methyl-Hg concentrations in tissues were species-specific and dependent on the ecological groups of receptor. R. nigricans and L. rubellus were the only species which showed a significant correlation between Hg concentrations in soils and Hg tissue concentrations. Mushrooms and earthworms contained similar Hg concentrations, whereas methyl-Hg

Acknowledgements

We thank Stephan Zimmermann for soil and forest data support and Gregor Ernst for his help in classifying earthworms. We also are grateful to Roger Köchli for collecting soil and mushroom samples and to Neria Römer (Museo di storia naturale Ticino) for collecting and classifying mushrooms. We also thank Markus Meili (Dept. of Applied Environmental Science, Stockholm University) to perform analyses of total Hg on a direct mercury analyser for analytical comparisons. Technical assistance of Ms.

References (56)

  • P. Kalač et al.

    Concentrations of mercury, copper, cadmium and lead in fruiting bodies of edible mushrooms in the vicinity of a mercury smelter and a copper smelter

    The Science of the Total Environment

    (1996)
  • L. Liang et al.

    An improved speciation method for mercury by GC/CVAFS after aqueous phase ethylation and room temperature precollection

    Talanta

    (1994)
  • M. Meili et al.

    Critical levels of atmospheric pollution: criteria and concepts for operational modelling of mercury in forest and lake ecosystems

    The Science of the Total Environment

    (2003)
  • M.J. Melgar et al.

    Mercury in edible mushrooms and underlying soil: bioconcentration factors and toxicological risk

    Science of the Total Environment

    (2009)
  • D. Michelot et al.

    Update on metal content profiles in mushrooms-toxicological implications and tentative approach to the mechanisms of bioaccumulation

    Toxicon

    (1998)
  • E.G. Pacyna et al.

    Global anthropogenic mercury emission inventory for 2000

    Atmospheric Environment

    (2006)
  • M. Ravichandran

    Interactions between mercury and dissolved matter – a review

    Chemosphere

    (2004)
  • P. Stegnar et al.

    The accumulation of mercury by, and the occurrence of methyl mercury in some fungi

    Chemosphere

    (1973)
  • L. Svoboda et al.

    Contents of cadmium, mercury and lead in edible mushrooms growing in a historical silver-mining area

    Food Chemistry

    (2006)
  • E. Tipping et al.

    Critical limits for Hg(II) in soils, derived from chronic toxicity data

    Environmental Pollution

    (2010)
  • J. Alonso et al.

    Accumulation of mercury in edible macrofungi: influence of some factors

    Archives of Environmental Contamination and Toxicology

    (2000)
  • F. Bargagli et al.

    Mercury and methylmercury in higher fungi and their relation with the substrata in a cinnabar mining area

    Chemosphere

    (1984)
  • P. Blaser et al.

    Waldböden der Schweiz, Band 2. Regionen Alpen und Alpensüdseite

    (2005)
  • N.S. Bloom

    Determination of picogram levels of methylmercury by aqueous phase ethylation, followed by cryogenic gas chromatography with atomic fluorescence detection

    Canadian Journal of Fisheries and Aquatic Sciences

    (1989)
  • A. Boudou et al.

    Mercury in the food web: accumulation and transfer mechanisms

  • D.T. Burton et al.

    Bioaccumulation of total mercury and monomethylmercury in the earthworm Eisenia fetida

    Water, Air, and Soil Pollution

    (2006)
  • A. Drott et al.

    Importance of dissolved neutral mercury sulfides for methyl mercury production in contaminated sediments

    Environmental Science and Technology

    (2007)
  • J. Falandysz et al.

    Total mercury in mushrooms and underlying soil substrate from the Borecka forest, northeastern Poland

    Archives of Environmental Contamination and Toxicology

    (2002)
  • Cited by (102)

    • Bioremediation of heavy metals from aquatic environments by lactic acid bacteria

      2023, Lactic Acid Bacteria as Cell Factories: Synthetic Biology and Metabolic Engineering
    View all citing articles on Scopus
    View full text