Evaluation of the mercury contamination in mushrooms of genus Leccinum from two different regions of the world: Accumulation, distribution and probable dietary intake

Science of the Total Environment 537 (2015) 470–478

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Evaluation of the mercury contamination in mushrooms of genus Leccinum from two different regions of the world: Accumulation, distribution and probable dietary intake Jerzy Falandysz a,⁎, Ji Zhang b, Yuanzhong Wang b, Grażyna Krasińska a, Anna Kojta a, Martyna Saba a, Tao Shen c, Tao Li c, Honggao Liu d a

Gdańsk University, Laboratory of Environmental Chemistry & Ecotoxicology, 63 Wita Stwosza Str., 80-952 Gdańsk, Poland Institute of Medicinal Plants, Yunnan Academy of Agricultural Sciences, 650200 Kunming, China c College of Resources and Environment, Yuxi Normal University, 653100 Yuxi, Yunnan, China d College of Agronomy and Biotechnology, Yunnan Agricultural University, 650201 Kunming, China b

H I G H L I G H T S

G R A P H I C A L

A B S T R A C T

• Mushrooms are an important food in some regions of the world. • Mercury in mushrooms genus Leccinum from Yunnan, China and Poland was measured. • Mushrooms from mercuriferous belt in Yunnan showed elevated concentrations. • Mushrooms genus Leccinum efficiently accumulate geogenic Hg. • Consumption of mushrooms poses no health risk for either region.

a r t i c l e

i n f o

Article history: Received 18 May 2015 Received in revised form 30 July 2015 Accepted 31 July 2015 Available online 29 August 2015 Editor: D. Barcelo Keywords: Foraging Fungi China Poland Leccinum

a b s t r a c t This study focused on investigation of the accumulation and distribution of mercury (Hg) in mushrooms of the genus Leccinum that emerged on soils of totally different geochemical bedrock composition. Hg in 6 species from geographically diverse regions of the mercuriferous belt areas in Yunnan of SW China, and 8 species from the non-mercuriferous regions of Poland in Europe was measured. Also assessed was the probable dietary intake of Hg from consumption of Leccinum spp., which are traditional organic food items in SW China and Poland. The results showed that L. chromapes, L. extremiorientale, L. griseum and L. rugosicepes are good accumulators of Hg and the sequestered Hg in caps were up to 4.8, 3.5, 3.6 and 4.7 mg Hg kg−1 dry matter respectively. Leccinum mushrooms from Poland also efficiently accumulated Hg with their average Hg content being an order of magnitude lower due to low concentrations of Hg in forest topsoil of Poland compared to the elevated contents in Yunnan. Consumption of Leccinum mushrooms with elevated Hg contents in Yunnan at rates of up to 300 g fresh product per week during the foraging season would not result in Hg intake that exceeds the provisional weekly tolerance limit of 0.004 mg kg−1 body mass, assuming no Hg ingestion from other foods. © 2015 Elsevier B.V. All rights reserved.

⁎ Corresponding author at: Gdańsk University, 63 Wita Stwosza Str., PL 80-308 Gdańsk, Poland. E-mail address: [email protected] (J. Falandysz).

http://dx.doi.org/10.1016/j.scitotenv.2015.07.159 0048-9697/© 2015 Elsevier B.V. All rights reserved.

J. Falandysz et al. / Science of the Total Environment 537 (2015) 470–478

1. Introduction The low vapor pressure of element mercury (Hg) facilitates atmospheric distribution and persistence of this metal results in contamination of all environments. Natural sources of emission are volcanic eruptions and volatilization from biotic, water, and lithosphere based surfaces, while the anthropogenic sources of this toxic element are numerous (Schuster et al., 2002; UNEP, 2013). Mercury in the troposphere can undergo a long-range transport in the form of gaseous elemental mercury (GEM, HgO) and it can subsequently be oxidized to reactive gaseous mercury (RGM, Hg2 +-forms) that are more rapidly deposited. In the last two centuries, because of the anthropogenic emissions, Hg has become increasingly relevant as a contaminant of food and the environment (Liang et al., 2015; UNEP, 2013). China, with estimated 500–700 t of mercury emitted into the planetary boundary layer annually contributes significantly to the global anthropogenic emission of Hg (Fu et al., 2012). Between 2000 and 2010, the emission continuously increased from 356 to 538 t with an average annual increase of 4.2% (Zhang et al., 2015). In China, apart from anthropogenic sources, such as coal combustion, as well as in zinc and lead smelting, and cement production an important source of emissions are natural surfaces (Fu et al., 2012; Wu et al., 2014). This is because of the natural abundance of Hg in soils of China (Wen and Chi, 2007), and the use of Hg (cinnabar, HgS) deposits. Especially rich in HgS deposits is the southwestern region and the Guizhou Province of China (Qiu et al., 2012a,b). Accumulation of Hg in the form of inorganic Hg and methylmercury (MeHg) by vegetables and rice from soils enriched/polluted with Hg areas of natural enrichment in region of the Guizhou Province have been documented (Li et al., 2015; Rothenberg et al., 2014; Zhang et al., 2010). Litter and topsoil in forests can be specifically enriched in airborne anthropogenic Hg (Demers et al., 2007; Schuster, 1991). In a recent study, the content of airborne total Hg and methylmercury (MeHg) in montane topsoil along an elevational gradient transect on Mt. Leigong in subtropical southwestern China was reported to have distinctly increased with altitude (Zhang et al., 2013). In the Alpine Dimension Region of the Minya Konka (Mountain Gongga) on the Eastern Tibetan Plateau that is located far away from the industrial sources of emissions, Hg was found in elevated amounts in fruiting bodies of mushrooms (macrofungi) that have shallow mycelia and attains nutrients from leaf litter (Falandysz et al., 2014a). Mycelia of mushroom can efficiently mobilize Hg from soil, litter or wood substrate and translocate to the fruiting bodies where Hg is found at elevated amounts (Alonso et al., 2000; Árvay et al., 2014; Falandysz, 2002; Falandysz et al., 2001b, 2011, 2014b; Frankowska et al., 2010; Gucia et al., 2012; Melgar et al., 2009; Ostos et al., 2015). Nevertheless, mushroom species differ in their efficiency of take-up and sequestration of Hg in the fruiting bodies (Bargagli and Baldi, 1984; Falandysz et al., 2001a, 2002b,d, 2003c,d, 2004; Kojta et al., 2012; Melgar et al., 2009; Mielewska et al., 2008; Nasr and Arp, 2011; Nasr et al., 2012; Rieder et al., 2011; Řanda and Kučera, 2004; Vetter and Berta, 1997; Wacko et al., 2008). Mushrooms can be characterized depending on their life style either as saprophytic or mycorrhizal species. The mycorrhizal mushrooms, e.g. Leccinum mushrooms, absorb minerals and trace elements from soil and other substrata and share them with the symbiotic plants, while saprophitic species are self-dependent. Data on accumulation, distribution, and probable dietary intake of Hg with edible mushrooms foraged in the southwestern China are scarce (Wiejak et al., 2014). In the southwestern region of China, red and yellow lateritic soils are dominant (He et al., 2004), and naturally enriched with Hg in the mineral layer (Wen and Chi, 2007). This is because of the occurrence of Hg in the Circum-Pacific Mercuriferous Belt (Gustin et al., 1999), and the abundance of cinnabar deposits in some regions of southwestern China (Qiu et al., 2012b). Mushrooms of genus Leccinum are edible and popular in Yunnan, China, and in the Central and Eastern Europe, where they are traditionally foraged from

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the wild. However, there is a dearth of information on the capabilities of these mushrooms to bio-concentrate Hg from soils of the two distant and diverse regions, and the likely roles of the different soil bedrock geochemical composition; geography and climate; industrial emission of Hg and urbanization. Examination of edible mushrooms that emerged in two different regions of the world in China and Europe, which differ in content of geogenic Hg, atmospheric deposition of anthropogenic Hg, geography and climate could give new insight into sources and bioconcentration potential of this element by species. This study aimed at elucidating the bio-concentration potential, distribution and probable dietary intake of Hg from several species of mushrooms of genus Leccinum collected across Yunnan, China and in Poland. 2. Materials and methods Two hundred four specimens of 6 species of mushrooms of genus Leccinum were collected across Yunnan Province in China during the mushroom collection season (July–August) in 2011–2014, and 297 specimens of 8 species of the same genus were collected across Poland in the mushroom collection season (July–September) in 1998–2011 (Fig. 1). The forest topsoil layer (0–10 cm) beneath the fruiting bodies was also collected and Hg concentrations measured. The species collected in China were Leccinum atrostipiatum Smith et Watling, Leccinum chromapes (Forst.) Sing, Leccinum extremiorientale (L.Vass.) Singer, Leccinum griseum (Quél.) Sing, Leccinum rugosicepes (Peck) Sing and Leccinum versipelle (Fr.) Snell., and in Poland were Leccinum albellum (Peck) Singer, Leccinum duriusculum (Kalchbr. et Schul. in Fr.) Sing, Leccinum melaneum (Smotl.) Pilát & Dermek, Leccinum quercinum (Pil.) Green et Watl., Leccinum rufum (Schaeff.) Kreisel, Leccinum scabrum (Bull.) Gray, L. versipelle (Fr. & Hök) Snell and Leccinum vulpinum Watl. (Index Fungorum, 2015). All specimens of the fruiting bodies selected for study were in good “edible” body condition (not infested or eaten by insects) and well developed (old and “baby” specimens were not selected). Fresh fruiting bodies directly after pickup were cleaned up from any visible plant vegetation and soil debris with a plastic knife and the bottom part of stipe was cutoff. A whole fruiting bodies of mushrooms genus Leccinum, which are relatively large in size, before cooking are usually shortly rinsed using flowing water while sometimes are washed using a brush and water and further rinsed with water before being sliced and blanched or fried. This doesn't seem to affect Hg concentration because skin of a cap is resistant for water and also is hymenophore. Nevertheless, no study is available on this matter. Blanching (short time boiling for 10 min.) of halved fruiting bodies of mushroom Amanita fulva has little effect on Hg concentration (around 10% loss) when expressed on dry biomass basis (Falandysz and Drewnowska, 2015). The Leccinum mushrooms preserved by drying after dry clean-up are sliced and further before cooking are macerated (no washing) with cold water and a macerate and a solid part are used (for a soup or bigos) without discarding of a macerate. Dried fungal material (in pieces) is sometimes crushed (in hands) and added directly to bigos or is grounded and as a powder is used for making a sauce or a soup (cream or of other type) without any washing and does not affect Hg concentration. To get insight into distribution of Hg between two major morphological parts of the fruiting bodies of mushrooms, each specimen was separated into cap (with skin) and stipe (stem supporting the cap). Next, the individual cap and stipe samples were sliced into pieces using a plastic disposable knifes and pooled for each site (n = 5 to 15 individuals per pool) composite samples representing each species, sampling place and time of collection (Table 1) (Falandysz, 2014). Thereafter, the mushroom samples were placed into plastic basket of an electrically heated commercial dryers (dehydrator for mushrooms, fruits, vegetables and herbs; model: MSG-01; MPM Product, Milanówek, Poland and Ultra FD1000 dehydrator, Ezidri, Australia) and dried at 65 °C to constant mass. Dried fungal materials were pulverized in a porcelain mortar(s) that was cleaned by hand washing using

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J. Falandysz et al. / Science of the Total Environment 537 (2015) 470–478

Fig. 1. Localization of the sampling sites in China (1–18) and Poland (I–XI); for details see in Table 1.

laboratory brush, deionized water and detergent and further rinsed with distilled water and dried in an electrically heated laboratory dryer at 105 °C, and kept in brand new sealed polyethylene bags under dry conditions. Soil samples (top 0–10 cm layer with organic and inorganic horizon and without undecomposed leaf litter layer) were collected using plastic tools (knifes and spoons) at the site of mushrooms collection. Samples were free of any visible organisms, small stones, sticks and leaves, were packed into brand new sealed polyethylene bags and transported to the laboratory. Further, after opening of the polyethylene bags they were kept in vertical position and air dried at room temperature for 8–10 weeks (China) and 16–18 weeks (Poland) under dry and clean condition in the laboratory to obtain aerially dry material. Soil samples were ground in a porcelain mortar, sieved through a pore size of 2 mm plastic sieve and then stored until analysis for 1 to 4 weeks in brand new sealed polyethylene bags in closed plastic box under dry conditions in refrigerator. Soil samples collected in Yunnan where treated in the same manner and shipped to the analytical laboratory within 24 h at ambient temperature (around 5 to 19 °C) in dry condition. Sieves after use were washed, well rinsed with deionized water and dried before re-use.

Technology, Warsaw, Poland. The declared content of Hg for material CS-M-1 (dried mushroom powder Suillus bovinus) is 0.174 ± 0.018 Hg mg kg− 1 dm Hg and our result (n = 13) was 0.185 ± 0.011 mg kg−1 dm (recovery 106.3%), for CS-M-2 (dried mushroom powder Agaricus campestris) declared content is 0.164 ± 0.004 Hg mg kg− 1 dm and our result (n = 8) was 0.165 ± 0.005 mg kg−1 dm (recovery 100.6%), for CS-M-3 (dried mushroom powder Boletus edulis) declared content is 2.849 ± 0.104 mg kg−1 dm and our result (n = 2) was 2.840 mg kg−1 dm (recovery 99.7%), and for CS-M-4 (dried mushroom powder Leccinum scabrum) declared content is 0.465 ± 0.024 mg kg−1 dm and our result (n = 11) was 0.453 ± 0.026 mg kg− 1 dm (recovery 97.4%). The limit of detection (LOD) of this study was 0.003 mg Hg/kg dm, and the quantification limit (LOQ) was 0.005 mg Hg kg− 1 dm. One blank sample and one certified reference material sample were examined with each set of 3–10 samples studied. The computer software Statistica, version 10.0 (Statsoft Polska, Kraków, Poland), was used for statistical analysis of data and for graphical presentation of the results of two-dimensional multiple scatter plots relationships between the variables.

2.1. Mercury determinations

3. Results and discussion

All the reagents used in this study were of analytical reagent grade, unless otherwise stated. Double distilled water was used for the preparation of the solutions. Mercury standard solution of 1.0 mg Hg mL−1 was obtained from the 10 mg mL− 1 standard stock solution. Blank and 3, 5, 10, 15 and 20 μL (low mode) and 25, 50, 100, 150 and 200 μL (high mode) of 1.0 mg mL−1 Hg standard solutions were injected into the analyzer for the construction of a calibration curves, which were prepared fresh each week. The determinations of total Hg content of fungal and soils samples was performed using cold-vapor atomic absorption spectroscopy (CV-AAS) by a direct sample thermal decomposition coupled with gold wool trap of Hg and its further desorption and quantitative measurement at wavelength of 253.7 nm. The analytical instrument used was mercury analyzer (MA-2000, Nippon Instruments Corporation, Takatsuki, Japan) equipped with auto sampler and operated respectively at low (3 to 20 ng Hg per sample) and high (25 to 150 ng Hg per sample) mode (Brzostowski et al., 2011a,b; Jarzyńska and Falandysz, 2011; Nnorom et al., 2013). Analytical control and assurance quality (AC/AQ) was assessed through analysis of blank samples and certified fungal reference materials produced by the Institute of Nuclear Chemistry and

3.1. Hg in fruiting bodies Mushrooms of various species that emerged from the same localization differ in content of accumulated Hg and this is well documented based on sufficiently large collections of individuals (Alonso et al., 2000; Falandysz et al., 2002a,b,c,d; Melgar et al., 2009). Good accumulators of Hg, such as the species Boletus edulis and Macrolepiota procera, collected from background areas in Europe, showed in caps concentrations, respectively, 1.8 ± 1.4 to 7.6 ± 3.1 mg kg−1 dry matter (dm) and 1.1 ± 1.0 to 8.4 ± 7.4 mg kg− 1 dm. Moderate include species such as Leccinum scabrum and Leccinum rufum with concentrations from 0.38 ± 0.23 to 1.2 ± 0.4 mg kg− 1 dm and from 0.27 ± 0.07 to 1.3 ± 0.2 mg kg−1 dm, respectively (Falandysz and Borovička, 2013). Mushrooms such as L. chromapes, L. extremiorientale, L. griseum and L. rugosicepes from Yunnan showed high contents of Hg, which for the composite samples of caps range from 2.1 to 4.7 mg kg−1 dm and for stipes from 0.56 to 2.8 mg kg− 1 dm (Table 1). Two species, namely L. atrostipiatum and L. versipelle were available only from Pudacao in the Diqing County, and both contained less Hg than other species from other regions of Yunnan, i.e. in caps, 0.54–1.1 mg kg−1 dm and in stipes 0.43–0.70 mg kg−1 dm. The species, L. chromapes, L. extremiorientale,

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Table 1 Mercury content in Fungi genus Leccinum and soil substratum from China and Poland, quotient of Hg content in cap to stipe (QC/S), and quotient of Hg content in cap/stipe to soil beneath the fruiting bodies (BCF; bioconcentration factor); mean value ± SD, median value and range. Hg (mg kg−1 dry matter) Whole fruiting bodies Country, species and place and date of collection

BCF Soils

Caps

Stipes

n

Caps

Stipes

(7)⁎

1.1

0.70

0.48

1.6

2.3

1.6

(7) (10) (10)

3.6 2.6 4.8

2.8 0.85 1.4

WD WD WD

1.3 3.1 1.4

WD WD WD

WD WD WD

(10) (5) (9) (12) (11)

2.2 2.3 3.0 3.5 2.8

0.83 0.68 2.1 1.3 0.32

0.091 0.065 0.24 0.27 0.14

2.6 3.4 1.4 2.7 8.7

24 35 12 13 20

9.1 10 8.7 4.8 2.3

(7) (10)

3.6 3.2

0.83 0.70

WD WD

4.3 4.6

WD WD

WD WD

(10) (10) (10) (8) (10) (7) (10) (10) (7) (7) (10)

3.3 4.2 3.0 3.0 2.1 3.5 3.3 4.4 3.4 2.8 4.7

1.4 0.68 2.1 0.79 0.75 0.70 1.5 1.0 2.7 0.56 1.7

WD 0.31 WD 0.28 WD 0.33 0.33 0.58 WD 0.43 WD

2.4 6.2 1.4 3.8 2.8 5.0 2.2 4.4 1.3 5.0 2.7

WD 13 WD 11 WD 11 10 7.6 WD 6.5 WD

WD 2.2 WD 2.8 WD 2.1 4.5 1.7 WD 1.3 WD

(7)

0.54

0.43

WD

1.3

WD

WD

Poland Leccinum albellum (Peck) Singer [VII] Pomerania land, Pomlewo; 2011

3#

0.38 ± 0.16 0.43 0.20–0.50

0.37 ± 0.08 0.24 0.15–0.31

WD

1.5 ± 0.3 1.6 1.3–1.8

WD

WD

Leccinum duriusculum (Kalchbr. et Schul. in Fr.) Sing [XI] Warmia land, Puszcza Borecka; 1998

16

0.56 ± 0.20 0.48 0.31–1.0 0.35 ± 0.05 0.36 0.25–0.41

0.32 ± 0.09 0.31 0.20–0.47 0.21 ± 0.03 0.22 0.26–0.16

WD

1.7 ± 0.2 1.7 1.4–2.2 1.6 ± 0.2 1.6 1.2–2.0

WD

WD

10 ± 2 10 5.4–13

6.4 ± 1.0 6.4 5.4–7.7

China Leccinum atrostipiatum Smith et Watling [1] Pudacuo, Diqing; 2012 Leccinum chromapes (Forst.) Sing [2] Jiangchuan, Yuxi; 2012 [3] Fumin, Kunming; 2011 [4] Kunming city; 2011 Leccinum extremiorientale (L.Vass.) Singer [5] Nanhua, Chuxiong; 2013 [5] Nanhua, Chuxiong, 2013 [6] Jiulongchi, Yuxi; 2013 [7] Caoba, Yuxi; 2013 [8] Eshan, Yuxi; 2014 Leccinum griseum (Quél.) Sing [4] Kunming city; 2011 [9] Wuding, Chuxiong; 2011 Leccinum rugosicepes (Peck) Sing [10] Huize, Qujing; 2011 [3] Fumin, Kunming; 2011 [11] Anning, Kunming; 2012 [12] Shilin, Kunming; 2012 [13] Yimen,Yuxi; 2011 [13] Yimen, Yuxi; 2012 [14] Shiping, Honghe; 2012 [15] Midu, Dalil; 2012 [16] Weixi, Diqing; 2012 [17] Yuanmou, Chuxiong; 2012 [18] Pu'er city; 2011 Leccinum versipelle (Fr.) Snell. [1] Pudacuo, Diqing; 2012

[I] Pomerania land, Wysokie; 2006

15

QC/S

0.035 ± 0.011 0.033 0.026–0.049

Leccinum melaneum (Smotl.) Pilát & Dermek [VI] Pomerania land, Kozia Góra; 2011

9

0.62 ± 0.36 0.72 0.21–1.2

0.35 ± 0.13 0.40 0.15–0.51

WD

1.9 ± 0.6 2.2 0.76–2.5

WD

WD

Leccinum quercinum (Pil.) Green et Watl. [III] Pomerania land, Gdynia-Witomino; 2006

16(20)¶

1.0 ± 1.0 0.68 0.23–4.4 1.1 ± 0.4 0.98 0.80–1.8

0.60 ± 0.73 0.31 0.14–3.2 0.58 ± 0.15 0.58 0.34–0.84

0.080 ± 0.091 0.060 0.038–0.072 WD

2.0 ± 0.6 2.1 0.8–2.8 1.9 ± 0.3 1.7 1.7–2.3

19 ± 19 15 3.7–84 WD

11 ± 15 6.3 0.59–60 WD

1.5 ± 0.62 1.3 0.49–2.2 0.78 0.53 0.90

0.63 ± 0.32 0.51 0.29–1.1 0.61 0.39 0.64

WD

1.9 ± 0.5 1.7 1.2–2.9 1.3 1.4 1.4

WD

WD

WD WD WD

WD WD WD

0.32 ± 0.15 0.30 0.11–0.68 0.29 ± 0.21 0.22 0.043–0.61 0.38 ± 0.12 0.43 0.20–0.50

0.21 ± 0.17 0.17 0.07–0.75 0.16 ± 0.10 0.15 0.036–0.43 0.24 ± 0.07 0.24 0.15–0.31

0.018 ± 0.004 0.020 0.010–0.023 0.026 ± 0.01 0.020 0.0061–0.084 WD

1.8 ± 0.6 1.7 0.9–3.0 2.0 ± 1.5 1.5 0.8–7.6 1.6 ± 0.1 1.6 1.4–1.8

18 ± 12 17 5.5–54 17 ± 11 16 3.0–39 WD

12 ± 11 8.8 3.1–40 9.8 ± 6.6 8.0 1.8–25 WD

[VII] Pomerania land, Pomlewo; 2011

6

Leccinum rufum (Schaeff.) Kreisel [VII] Pomerania land, Pomlewo; 2011

7

[XIV] Pomerania land, Parchowo; 2010 [XII] Warmia land, Olsztynek; 2008 [XII] Podlasie land, Puszcza Białowieska, Białowieża; 1998 Leccinum scabrum (Bull.) Gray [II] Seaside Landscape Park; 2009

(15) (14) (15) 16

[II] Seaside Landscape Park; 2011

16

[V] Pomerania land, Szklana Góra; 2011

3

WD WD WD

(continued on next page)

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Table 1 (continued) Hg (mg kg−1 dry matter) Whole fruiting bodies Country, species and place and date of collection

BCF Soils

n

Caps

Stipes

[VI] Pomerania land, Kozia Góra; 2011

10

14

0.35 ± 0.12 0.40 0.40–0.51 0.65 ± 0.32 0.65 0.23–1.33

WD

[VII] Pomerania land, Pomlewo; 2011

0.76 ± 0.34 0.92 0.21–1.2 0.67 ± 0.32 0.69 0.20–1.23

Caps

Stipes

2.1 ± 0.6 1.9 1.5–2.4 1.1 ± 0.4 0.94 0.6–2.0

WD

WD

WD

WD

QC/S

WD

Leccinum versipelle (Fr. & Hök) Snell [VIII] Pomerania land, Bory Tucholskie; 2009 [II] Seaside Landscape Park, 2011

(15) 16

0.57 0.57 ± 0.38 0.38 0.19–1.39

0.39 0.46 ± 0.20 0.39 0.15–0.86

WD WD

1.5 1.2 ± 0.5 1.0 0.7–2.3

WD WD

WD WD

Leccinum vulpinum Watl. [IV] Pomerania land, Sulęczyno, 2006

15(26)

0.37 ± 0.13 0.34 0.18–0.59 0.58 ± 0.26 0.57 0.19–1.2 0.72 ± 0.24 0.64 0.50–1.1

0.28 ± 0.10 0.26 0.12–0.48 0.23 ± 0.08 0.22 0.082–0.37 0.52 ± 0.22 0.46 0.25–0.82

0.020 ± 0.010 0.018 0.013–0.029 0.059 ± 0.005 0.060 0.048–0.066 0.024 ± 0.014 0.020 0.013–0.054

1.4 ± 0.0 1.4 0.91–1.9 2.6 ± 0.7 2.5 1.4–3.6 1.4 ± 0.2 1.3 1.2–1.8

20 ± 10 16 8.9–44 9.9 ± 4.2 10 3.9–20 32 ± 13 31 17–54

14 ± 7 13 8.1–32 3.8 ± 1.3 3.8 1.6–6.5 24 ± 11 21 10–40

[X] Pomerania land, Kaszuny; 2002/2003

14

[IX] Pomerania land, Złotów, 2006

7

⁎ Composite samples. # Individual specimens. ¶ Number of samples and total number of specimens (in parentheses).

L. griseum and L. rugosicepes were available respectively from 2 to 11 spatially distantly distributed locations in China and all mushrooms showed a substantial content of Hg. Observed Hg concentrations in Leccinum spp. samples from China were higher than those from Europe (Table 1) and in other reports (Falandysz and Bielawski, 2001; Falandysz and Kryszewski, 1996; Melgar et al., 2009; Svoboda et al., 2006; Tüzen et al., 1998). Pooled samples of caps and stipes of L. versipelle from Yunnan and Poland showed moderate content of Hg, i.e. 0.54 mg kg−1 dm for caps and 0.43 mg kg−1 dm for stipes of samples from Yunnan; and 0.38-0.57 mg kg−1 dm (caps) and 0.39–0.39 mg kg−1dm (stipes) for samples from Poland (Table 1). Mushrooms L. rufum and L. quercinum collected in the northern part of Poland with Hg in caps of around 1.0 mg kg mg kg−1 dm were better accumulators when compared to L. albellum, L. duriusculum, L. melaneum, L. scabrum, L. versipelle and L. vulpinum, with an average Hg content about 0.5 mg kg−1 dm (Table 1). Caps of the Leccinum spp. from all locations in Yunnan, on average, contained higher concentrations than the stipes (p b 0.001; Mann–Whitney U test), and the values for caps to stipe Hg concentration quotient (QC/S), calculated for 23 composite samples and in a total of 204 fruiting bodies was 3.2 (range 1.3–8.7). This observation agree with the values of QC/S calculated in this study for L. albellum, L. duriusculum, L. griseum, L. melaneum, L. quercinum, L. rufum, L. scabrum, L. versipelle and L. vulpinum collected in Poland with range (median values) per species of from 0.94 to 2.5 (total 0.6–7.6) (Table 1). Similarly, in earlier studies, L. scabrum was reported to have higher Hg in caps compared to the stipes, i.e. mean value of QC/S was 2.1 ± 0.8 (range of 1.7 ± 0.4 to 2.9 ± 1.0 for twelve locations) while the median for 240 individual specimens was 2.0 (Falandysz and Bielawski, 2007). Similarly, L. rufum (L. aurantiacum) from Poland showed QC/S N 1, i.e. the mean values for nine locations range from 1.4 ± 0.1 to 2.3 ± 0.7 (1.0–5.6) while the median values range from 1.4 to 2.2 (Falandysz et al., 2012b). The value(s) of QC/S are rarely as high as determined in this study for Leccinum spp. from the Yunnan Province in other studies. For example for large collections of certain species of genus Amanita, Leccinum, Suillus and Xerocomus, and for Armillaria solidipes, Boletus edulis, Cortinarius caperatus, Macrolepiota procera, Paxillus involutus, Russula ochrolucea and Tricholoma flavovirens were the value of QC/S (Table 2). It is not clear what could be the reason for the observed discrepancies in the

value of QC/S for fruiting bodies of the same species of mushroom collected from different locations. Maturity state of hymenophore could be one of likely factors, and the occurrence of Hg as different chemical compounds in soil substratum and their different distributions within a horizon of soil as well as Hg availability are likely factors also. 3.2. Hg in soil substratum and fruiting bodies The composite samples of the soil substratum for red and yellow soils, which were available for twelve locations in Yunnan, showed Hg concentration of from 0.065 to 0.58 mg kg−1 dry mass (dm) (mean of Table 2 The values for caps to stipe Hg concentration quotient (QC/S). Species of mushroom (and number of individuals)

QC/S

Ref.

Amanita muscaria (n = 204) Amanita rubescens (n = 272) Amanita fulva (n = 831) Amanita vaginata (n = 92) Armillaria solidipes (n = 955) Boletus edulis (n = 173) Cortinarius caperatus (n = 715) Leccinum griseum (n = 110) Leccinum rufum (n = 126) Leccinum scabrum (n = 240) Macrolepiota procera (n = 348) Paxillus involutus (n = 181) Russula ochrolucea (n = 260) Suillus grevillei (n = 121) Suillus luteus (n = 383) Tricholoma flavovirens (n = 149) Xerocomus badius (n = 221) Xerocomus chrysenteron (n = 640) Xerocomus subtomentosus (n = 247)

1.9 ± 1.0 1.1 ± 0.4–1.7 ± 0.8 1.3 ± 0.4–2.5 ± 1.1 1.2 ± 0.4–2.1 ± 0.5 1.1 ± 0.4–1.7 ± 0.3 1.0 ± 0.7–3.2 ± 2.1 1.8 ± 0.4–3.2 ± 0.9 1.3 ± 0.7–2.3 ± 0.9 1.4 ± 0.1–2.3 ± 0.7 1.7 ± 0.4–2.9 ± 1.0 1.1 ± 0.2–4.6 ± 5.1 1.4 ± 0.5 1.3 ± 0.4–1.9 ± 0.4 3.1 ± 1.1 1.8 ± 0.4–3.3 ± 0.8 1.1 ± 0.1–1.9 ± 1.8 1.8 ± 0.8 0.86 ± 0.55–2.8 ± 2.5 1.0 ± 0.4–2.9 ± 1.8

A,B C D E F G,H I J K L,M N,O P,Q R S T V W X Y

Notes: Ref. A (Falandysz et al., 2007e), B (Falandysz et al., 2007f), C (Drewnowska et al., 2012a), D (Falandysz and Drewnowska, 2015), E (Drewnowska et al., 2014), F (Falandysz et al., 2013), G (Falandysz et al., 2007a), H (Falandysz et al., 2008a), I (Falandysz, 2014), J (Krasińska and Falandysz, 2015), K (Falandysz et al., 2012b), L (Falandysz and Bielawski, 2007), M (Falandysz et al., 2007d), N (Falandysz et al., 2007b), O (Falandysz et al., 2008b), P (Falandysz and Brzostowski, 2007), Q (Falandysz et al., 2007c), R (Drewnowska et al., 2012b), S (Chudzyński et al., 2009), T (Chudzyński et al., 2011), V (Maćkiewicz and Falandysz, 2012), W (Falandysz et al., 2012a) X (Dryżałowska and Falandysz, 2014), Y (Chojnacka et al., 2012, 2013).

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0.30 mg kg−1 dm). These values are, on the average, an order of magnitude greater than has been determined in brown soil and podzols sampled in Poland, for which median values of Hg at seven locations range from 0.018 to 0.060 mg kg− 1 dm (total range from 0.0060 to 0.084 mg kg−1 dm) (Table 1). Data on Hg contents of brown soils and podzols in this study can be considered as typical level for the upper 0–10 cm layer of soils in the forested areas in the northern and central regions of Poland, which is usually from b 0.05–b 0.1 mg kg− 1 dm or lower (Falandysz and Chwir, 1997; Falandysz et al., 1997, 2002a,c, 2003a,b; PIG, 2013; Romińska et al., 2008; Rompa et al., 2008). There is no reason to believe that mushrooms (fungi) are able to regulate the up-take and sequestration of Hg in fruiting bodies in the same way as is for essential metallic elements, e.g. potassium, which 40 undergoes homeostatic regulation and concentrations of K (also K) are within a narrow range for a species and morphological parts, while of Hg not (Falandysz and Borovička, 2013; Falandysz et al., 2015; JF, unpublished). Hence, the Hg contents of soil and the availability of its Hg compounds from soil is a major factor impacting absorption and sequestration of this element in fruiting bodies by mushroom. As mentioned, the atmospheric deposition loads of Hg increased in the industrial era because of emissions from anthropogenic sources (Schuster et al., 2002; UNEP, 2013) and this resulted in substantial enrichment of Hg in surface layer of forest soils. Hg deposited from atmosphere is highly retained in the surface layer (litter, fermentation layer and humus) of soils and when complexed with some organic ligands a small component could also infiltrate into deeper layers of soil mineral horizon (Demers et al., 2007). This seems to be the case for forest soils for the regions of Poland that is out the mercuriferous belt (exception seems to be the south-western corner of the country territory; see Gustin et al., 1999; observed also by Falandysz et al. 2007a, 2012a). The Hg content in the forest soil from the outskirts of the Włocławek town in Poland decreased by ~ 90% with increase in the depth from top 0–2 cm layer to 3–5 cm layer and by 98% to 5–15 cm layer (Falandysz et al., 1996). In case of soil sampled from the city Gdańsk, the Hg content decreased by 8% with increasing depth from top 0–5 cm layer to 10–15 cm layer, by 25% to 20–30 cm layer, by 84% to 50–70 cm layer and by 96% to 70–100 cm layer (Falandysz et al., 1996). Hence, in the regions of Poland, atmospheric Hg deposition could be an important source of Hg for mushrooms which mycelia live in litter and organic layer rather than geogenic sources. In a similar two studies of two soil horizons from mixed trees forests from Yunnan, the results differed compared to that mentioned for Poland. In montane soil from a remote rural site in region of Pu'er, the Hg content increased by 37% with increase in the depth from top 0–1 cm layer to 1–2 cm layer, decreased by 7.5% to 2–3 cm layer, decreased by 49% to 6–7 cm layer and remained almost unchanged from 7–8 cm to 12–13 cm layer. In a second study of forest soil from outskirts of the city of Yuxi, the Hg content decreased by 69% with increase in the depth from top 0–1 cm layer to 1–2 cm layer, decreased by 72% to 2–3 cm layer, decreased by 83% to 3–4 cm layer and slightly fluctuated but remained the same from 3–4 cm layer to 19–20 cm layer (JF; unpublished). Meanwhile, atmospheric deposition seem to be important source in the regions of Yunnan and Poland, while clearly geogenic sources due to the occurrence of mercuriferous belt are very important source in the regions of Yunnan, but not of Poland. The Leccinum spp. have mycelia deeper in soil horizon and this feature together with the relative abundance of Hg largely from geogenic sources and less from atmospheric deposition in Yunnan can explain the higher loads of Hg in fruiting bodies of the species collected in certain locations in Yunnan when compared to the situation in Poland (Table 1). The potential for mushrooms to take-up and sequester Hg (or any other element) in the fruiting body is assessed based on the value of the quotient of Hg in the cap, stipe or a whole fruiting body, and Hg in the myceliated layer of soil substratum that is defined as

475

bioconcentration factor (BCF) or transfer factor (TF). The values of BCF were high for certain mushroom species from some weakly polluted locations in Poland, e.g. N 100 for Macrolepiota procera (Falandysz et al., 2007b), while this value usually decreases with an increase in the Hg content of the soil substratum (Falandysz et al., 2012a,c). BCF values of Hg calculated for L. atrostipiatum, L. extremiorientale and L. rugosicepes from Yunnan and L. duriusculum, L. quercinum, L. scabrum and L. vulpinum from Poland were above 1 and despite the wide variation in Hg observed between soils from most of the locations in Yunnan and those from Poland. Hence, based on the relatively large set of samples of Leccinum spp. and soils with different content of geogenic Hg because of mercuriferous belt and lack of a belt and history of pollution with airborne Hg at the surface layer, these mushrooms that have mycelia not in fermented litter and upper organic layer but deeper in soil horizon have some potential to act as bioindicators of natural geogenic Hg levels in soil substratum and/or in soil layers having deposited/infiltrated Hg that accumulated over the last two centuries because of environmental pollution. The curve fit of Hg concentration in soil against the different parts of mushrooms (p b 0.001 for caps and p b 0.05 for stipes (Fig. 2)). No such pattern was observed when both data sets were examined separately and this could be attributed to the small number of observations for the regions alone (Figs. S1 and S2; Supplementary information). This result implies that fungi of the genus Leccinum has the potential and can be used as a bio-indicator for Hg in soil substratum. An earlier study showed that MeHg content in fruiting bodies is highly dependent on the MeHg content of the soil substratum (Fischer et al., 1995). Similarly, Hg content of certain species from some particular locations correlated positively with the Hg contents in soil, e.g. for caps of Agaricus arvensis and L. scabrum (Falandysz et al., 2003b), M. procera (Falandysz and Chwir, 1997) or A. rubescens (Drewnowska et al., 2012a), but these observations seemed to be location-specific at least in the case of Hg (no MeHg was determined in these referenced studies). Nevertheless, it is not easy to find a good general example, which could document the ability of mushroom(s) to quantitatively respond to Hg (or other Hg forms) contained in soil substratum.

3.3. Probable dietary intake of Hg In Yunnan that is agricultural land and highly forested, the edible mushrooms collected from the wild are popular food items and their minerals and trace element contents and composition are of human

Fig. 2. Relationships between Hg content in the caps and stipes of Leccinum spp. from locations in Yunnan and Poland and Hg in soil substratum (for caps: y = 0.87 + 6.0*x; r = 0.73, p = 0.0004; for stipes: y = 0.39 + 1.4*x; r = 0.50, p = 0.03).

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health concern. Both caps and stipes of the fruiting bodies of Leccinum mushrooms are edible. In the Chinese gourmet tradition, mushrooms of the genus Leccinum and Boletus are cooked using a Chinese pan called wok and a small portion of vegetable oil (Wang et al., 2014; Wiejak et al., 2014). The sliced fruiting bodies of Leccinum and Boletus mushrooms are fried for a short period (about 5 min) with hot oil and in the final step, small portions of the sliced vegetables and spices are added and the dish is further fried (for about 5 min). In the culinary experiment with Amanita fulva it was found that boiling (blanching) of fresh fruiting bodies for 10 min reduced the Hg content by 10% (Falandysz and Drewnowska, 2015), while blanching of L. versipelle did not result in a reduction in the Hg content (as expressed on dry matter content) (unpublished, JF). Thus it is expected that frying of mushrooms in the traditional Chinese manner using a wok will not reduce the Hg content. Contrary, this can enhance the Hg content, when expressed based on dry matter of cooked mushrooms, because they will lose some portion of water that will evaporate during cooking with hot oil. Both, the mushrooms and vegetables fried will absorb some portion of oil and usually a small portion of oil will remain, which is served with fried mushrooms. In Yunnan, the consumption of mushrooms collected in the wild is high and can reach up to 20–24 kg fresh fruiting bodies per capita annually in some locations (Zhang et al., 2010), while there are no detailed data for the regions of Yunnan. For the purpose of this work and estimation of probable dietary exposure for Hg with mushrooms consumed in Yunnan, the consumption rate of Leccinum spp. was estimated at 100 g for dinner per capita which seems reasonable with consumption frequency of up to three times in a week (3 × 100 g) during the mushroom seasonal abundance. The consumption can be greater for some individuals and families in the mushrooming season while the mushrooms can also be preserved and used later (Falandysz and Borovička, 2013). Nevertheless, in Yunnan it is also traditional to preserve mushrooms (by drying, freezing or with oil and salt) that can be used after mushrooming season, but there is a lack of quantitative data. The median value of Hg content in composite sample of caps for six species of mushrooms of the genus Leccinum from 23 locations in Yunnan Province in this study was 3.2 mg kg− 1 dm (that is 0.32 mg kg−1 fresh product assuming moisture content at 90%), and for samples from 17 locations in Poland was 0.57 mg kg−1 dm (equivalent to 0.057 mg kg−1 fresh product). Hence, based on the median contents of Hg, the estimated probable dietary intake of Hg with mushrooms of the genus Leccinum consumed in Yunnan at the rate of 100/day or 300 g in a week period is 0.032 mg and 0.096 mg per person (0.00053 mg and 0.0016 mg per kg body mass, assuming a 60 kg body mass). The corresponding values of probable dietary intake of Hg contained in Leccinum mushrooms from Poland are 0.0057 mg and 0.0017 mg per person (0.0000081 mg and 0.00024 mg per kg body mass, assuming a 70 kg body mass). For the assessment of potential risks from probable dietary intake of Hg in the fruiting bodies of Leccinum mushrooms a provisional tolerable weekly intake (PTWI) value of 0.004 mg kg−1 body mass (JECFA, 2010). Consumption of fresh caps of Leccinum from the locations in Yunnan at the rate of 300 g per week in the mushrooming season would not result in Hg intake value that exceeds the provisional tolerable weekly intake limit, assuming that no Hg from other foods is ingested. In spite of the elevated accumulation of Hg in edible fruiting bodies by certain mushrooms of the genus Leccinum from Yunnan, their consumption in moderate rates in foraging season with respect to current health standards can be considered safe. Selenium (Se) can provide protective role against MeHg (Ralston and Raymond, 2010), and possibly also against inorganic Hg ingested with food. In the recent concepts of assessments of risk from Hg (also MeHg) in foods, it is postulated that the co-occurrence of Se with the Hg need to be taken into account (Ralston and Raymond, 2014; Zhang et al., 2014). However, MeHg content is usually a small component

(b 5–b 10%) of total Hg in mushrooms (Falandysz and Borovička, 2013; Stijve and Roschnik, 1974). Thus, assessment of Se content in for risk assessment could be not useful. 4. Conclusions Mushrooms of the genus Leccinum in the regions of Yunnan due to the abundance of geogenic Hg in soils in the area of Circum-Pacific Mercuriferous Belt contain Hg at elevated concentration in edible fruiting bodies. Mushrooms of genus Leccinum seem to have the potential as an indicator of geogenic Hg in soil mineral horizon. In spite of elevated accumulation of Hg in edible fruiting bodies by certain mushrooms of genus Leccinum from Yunnan their consumption in moderate rates in the foraging season in the light of current health standards can be considered safe. Acknowledgements Part of this project was supported by the National Science Centre of Poland (UMO-2011/03/N/NZ9/04136) and the National Natural Science Foundation of China (No. 31260496, 31160409). Appendix A. Supplementary data Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.scitotenv.2015.07.159. References Alonso, J., Salgado, M., Garciá, M., Melgar, M., 2000. Accumulation of mercury in edible macrofungi: influence of some factors. Arch. Environ. Contam. Toxicol. 38, 158–162. Árvay, J., Tomáša, J., Hauptvogl, M., Kopernická, M., Kováčik, A., Bajčan, D., Massányi, P., 2014. Contamination of wild-grown edible mushrooms by heavy metals in a former mercury-mining area. J. Environ. Sci. Health B 49, 815–827. Bargagli, R., Baldi, F., 1984. Mercury and methyl mercury in higher fungi and their relation with the substrate in a cinnabar mining area. Chemosphere 13, 1059–1071. Brzostowski, A., Falandysz, J., Jarzyńska, G., Zhang, D., 2011a. Bioconcentration potential of metallic elements by Poison Pax (Paxillus involutus) mushroom. J. Environ. Sci. Health A 46, 378–393. Brzostowski, A., Jarzyńska, G., Kojta, A.K., Wydmańska, D., Falandysz, J., 2011b. Variations in metal levels accumulated in Poison Pax (Paxillus involutus) mushroom collected at one site over four years. J. Environ. Sci. Health A 46, 581–588. Chojnacka, A., Jarzyńska, G., Drewnowska, M., Nnorom, I.C., Falandysz, J., 2012. Yellowcracking Boletes (Xerocomus subtomentosus) mushrooms: content and potential to sequestrate mercury. J. Environ. Sci. Health A 47, 2094–3011. Chojnacka, A., Jarzyńska, G., Lewandowska, M., Nnorom, I.C., Falandysz, J., 2013. Multivariate analysis of minerals in Yellow-cracking Bolete (Xerocomus subtomentosus) collected at one site over three years. Fresenius Environ. Bull. 22, 2707–2712. Chudzyński, K., Bielawski, L., Falandysz, J., 2009. Mercury bio-concentration potential of Larch Bolete, Suillus grevillei, mushroom. Bull. Environ. Contam. Toxicol. 83, 275–279. Chudzyński, K., Jarzyńska, G., Stefańska, A., Falandysz, J., 2011. Mercury content and bio-concentration potential of Slippery Jack, Suillus luteus, mushroom. Food Chem. 125, 986–990. Demers, J.D., Driscoll, C.T., Fahey, T.J., Yavitt, J.B., 2007. Mercury cycling in litter and soil in different forest types in the Adirondack region, New York, USA. Ecol. Appl. 17, 1341–1351. Drewnowska, M., Jarzyńska, G., Kojta, A.K., Falandysz, J., 2012a. Mercury in European Blusher, Amanita rubescens, mushroom and soil. Bioconcentration potential and intake assessment. J. Environ. Sci. Health B 47, 466–474. Drewnowska, M., Jarzyńska, G., Sąpór, A., Nnorom, I.C., Sajwan, K.S., Falandysz, J., 2012b. Mercury in Russula mushrooms: bioconcentration by Yellow-ocher Brittle Gills Russula ochroleuca. J. Environ. Sci. Health A 47, 1577–1591. Drewnowska, M., Nnorom, I.C., Falandysz, J., 2014. Mercury in the Tawny Grisette. Amanita vaginata Fr. and soil below the fruiting bodies. J. Environ. Sci. Health B 49, 521–526. Dryżałowska, A., Falandysz, J., 2014. Bioconcentration of mercury by mushroom Xerocomus chrysenteron from the spatially distant locations: levels, intake and safety. Ecotoxicol. Environ. Saf. 107, 97–102. Falandysz, J., 2002. Mercury in mushrooms and soil of the Tarnobrzeska Plain, southeastern Poland. J. Environ. Sci. Health A 37, 343–352. Falandysz, J., 2014. Distribution of mercury in Gypsy Cortinarius caperatus mushrooms from several populations: an efficient accumulator species and estimated intake of element. Ecotoxicol. Environ. Saf. 110, 68–72. Falandysz, J., Bielawski, L., 2001. Mercury content of wild edible mushrooms collected near the town of Augustów. Pol. J. Environ. Stud. 10, 67–71. Falandysz, J., Bielawski, L., 2007. Mercury and its bioconcentration factors in Brown Birch Scaber Stalk (Leccinum scabrum) from various sites in Poland. Food Chem. 105, 635–640.

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