Mercury in wild mushrooms and underlying soil substrate from Koszalin, North-central Poland

Chemosphere 54 (2004) 461–466

www.elsevier.com/locate/chemosphere

Mercury in wild mushrooms and underlying soilsubstrate from Koszalin, North-central Poland

Jerzy Falandysz a,*, Aneta Jezdrusiaka, Krzysztof Lipka a,

Kurunthachalam Kannan b, Masahide Kawano c,Magdalena Gucia a, Andrzej Brzostowski a, Monika Dadej a

a Department of Environmental Chemistry and Ecotoxicology, University of Gda�nnsk,18 Sobieskiego Str., PL 80-952 Gda�nnsk, Poland

b National Food Safety and Toxicology Center, Michigan State University, East Lansing, MI 48824, USAc Department of Environmental Analytical Chemistry, Ehime University, 3-5-7 Tarumi, Matsuyama 790-8566, Japan

Received 25 February 2002; received in revised form 10 June 2002; accepted 8 July 2003

Abstract

Concentrations of total mercury were determined by cold-vapour atomic absorption spectroscopy (CV-AAS) in 221

caps and 221 stalks of 15 species of wild growing higher fungi/mushrooms and 221 samples of corresponding soil

substrate collected in 1997–98 in Manowo County, near the city of Koszalin in North-central Poland. Mean mercury

concentrations in caps and stalks of the mushroom species examined and soils varied between 30±31 and 920± 280,

17± 11 and 560±220, and 10±9 and 170±110 ng/g dry matter, respectively. Cap to stalk mercury concentration

quotients were from 1.0± 0.4 in poison pax (Paxillus involutus) to 2.8 ± 0.7 in slippery jack (Suillus luteus). Brown cort

(Cortinarius malicorius), fly agaric (Amanita muscaria), orange–brown ringless amanita (A. fulva), red-aspen bolete

(Leccinum rufum) and mutagen milk cap (Lactarius necator) contained the highest concentrations of mercury both in

caps and stalks, and mean concentrations varied between 600± 750 and 920± 280 and 370± 470 and 560± 220 ng/g dry

matter, respectively. An estimate of daily intake of mercury from mushroom consumption indicated that the flesh of

edible species of mushrooms may not pose hazards to human health even at a maximum consumption rate of 28 g/day.

However, it should be noted that mercury intake from other foods will augment the daily intake rates. Species such as

the sickener (Russula emetica), Geranium-scented russula (R. fellea) and poison pax (P. involutus) did not concentrate

mercury as evidenced from the bioconcentration factors (BCFs: concentrations in mushroom/concentration in soil

substrate), which were less than 1. Similarly, red-hot milk cap (L. rufus), rickstone funnel cap (Clitocybe geotropa) and

European cow bolete (S. bovinus) were observed to be weak accumulators of mercury. Fly agaric (A. muscaria) ac-

cumulated great concentrations of mercury with BCFs reaching 73± 42 and 38± 22 in caps and stalks, respectively.

Mercury BCFs of between 4.0± 2.3 and 23± 25 (caps) and 2.6± 1.9 and 14±12 (stalks) were noted for the other

mushroom species. Relatively great concentrations of mercury in fly agaric (A. muscaria) were due to preferential

uptake of this element by this species.

� 2003 Elsevier Ltd. All rights reserved.

Keywords: Fungi; Contamination; Heavy metals; Food; Daily intake

*Corresponding author. Tel.: +4858-3450372; fax: +4858-

3410357.

E-mail address: [email protected] (J. Fa-

landysz).

0045-6535/$ - see front matter � 2003 Elsevier Ltd. All rights reserv

doi:10.1016/S0045-6535(03)00700-8

1. Introduction

The fruiting bodies of many species of wild growing

edible and inedible higher fungi can contain great

ed.

462 J. Falandysz et al. / Chemosphere 54 (2004) 461–466

concentrations of toxic elements such as mercury, cad-

mium, arsenic or lead (Stegnar et al., 1973; Stijve and

Besson, 1976; Allen and Steinnes, 1978; Gast et al., 1988;

Zabowski et al., 1990; Kala�cc et al., 1991, 1996; Mejstrik

and Lepsova, 1993; Wondratschek and R€ooder, 1993;

Falandysz and Kryszewski, 1996; Slekovec and Irgolic,

1996; Falandysz and Chwir, 1997; Vetter and Berta,

1997; Alonso et al., 2000; Falandysz, 2002; Falandysz

et al., 2002), in addition to essential metallic elements

and metalloids such as potassium, iron, copper, zinc or

selenium (Bakken and Olsen, 1990; Stijve et al., 1998;

Falandysz et al., 2001). Mercury is an abundant element

in certain edible mushroom species of genera Agaricus,

Lepista, Calocybe, Macrolepiota, Lycoperdon and Bol-

etus (Kala�cc and Svoboda, 2000). Mushrooms collected

from polluted sites contained elevated concentrations of

heavy metals (Lodenius and Herranen, 1981; Bargagli

and Baldi, 1984; Zabowski et al., 1990; Kala�cc et al.,

1991, 1996). Methylmercury, a highly toxic form of

mercury, was found to be effectively absorbed by Boletus

sp. under field conditions. Under laboratory conditions,

methylmercury was effectively absorbed by saprophytic

mushrooms such as Coprinus comatus and C. radicus,

which were also able to methylate inorganic mercury

(Fischer et al., 1995). Information regarding chemical

forms of mercury in macromycetes is rather limited.

Proportion of methylmercury to total mercury concen-

trations in the fruiting bodies is usually low, in some

cases up to 15% of the total mercury concentrations

(Kala�cc and Svoboda, 2000).

Since wild growing edible higher fungi are attractive,

and are considered a delicacy, they are traditional to the

cuisine culture of various nations worldwide. Despite

their ability to accumulate toxic metals and their value

as a traditional food item, very few studies have exam-

ined the concentrations of toxic metals in mushrooms.

Several species of higher fungi are good accumulators of

elements such as vanadium (e.g. fly agaric, Amanita

muscaria), iron (e.g., variegated bolete, Suillus variega-

tus), arsenic (e.g. Laccaria sp.) or selenium (e.g. King

Fig. 1. The area of the mushroom collection

bolete, B. edulis, Albatrellus pes-caprae, Albatrellus sp.)

which makes them interesting objects for examining

unknown organometallic compounds (Watkinson, 1964;

Zabowski et al., 1990; Slekovec and Irgolic, 1996; Stijve

et al., 1998; Falandysz et al., 2001).

This is a part of a comprehensive nation-wide inves-

tigation to monitor mercury concentrations in higher

mushrooms and underlying substrate to understand

contamination status, accumulation features, possible

human intake rates and risk to local consumers in Poland.

2. Materials and methods

Fruiting bodies of 15 species of edible and inedible

mushrooms were collected from Manowo in the County

of Koszalin in North-central Poland in 1997–98 (Fig. 1).

The North-central part of Poland is mostly forested and

agricultural region without heavy industrial activities.

Therefore, environmental pollution by metallic elements

or metalloids is considered minimal in this region. In-

dividual specimens of mushroom species were collected

to cover a large area of land––up to several square

kilometres. Total mercury concentration was deter-

mined in 221 samples each of caps, stalks and underlying

soil substrate.

Fresh mushrooms, after removing plant and sub-

strate debris with a disposable plastic knife, were air-

dried for several days and then dried in an oven at 40 �Cfor 48 h, and pulverised in an agate mortar. Each pul-

verised sample was kept individually in clean (new)

polyethylene bags and further stored/archived in plastic

storage containers in a clean, dry room at darkness.

Subsamples (0.2–0.3 g) of dried and powdered samples

of individual specimens were wet digested with 6 ml of

concentrated nitric acid (Suprapoor�, Merck) in closed

PTFE vessels in a microwave oven (Automatic Diges-

tion System, MLS 1200). The digest was diluted to 10 ml

using double-distilled water, and further dilutions were

made, when necessary.

at the region of the city of Koszalin.

J. Falandysz et al. / Chemosphere 54 (2004) 461–466 463

Soil samples, after removal of plant material, small

stones and visible organisms, were air dried at room

temperature for approximately four weeks, and ground

in an agate mortar and further dried in an oven at 40 �Cfor 48 h. Each sample was kept individually in clean

(new) polyethylene bags and further stored/archived in

plastic storage containers in a clean, dry room at dark-

ness. Subsamples (�1 g) were wet digested with a mix-

ture of concentrated nitric and sulphuric acids in a glass

system, which consisted of round bottom flask, partial

condenser (30 cm long) and water cooler (Falandysz and

Chwir, 1997). The method of mercury measurement in-

volved cold vapour atomic absorption spectroscopy

(CV-AAS, Mercury Monitor 3200, Thermo Separation

Products, USA).

The digestion procedure was performed in a clean

hood facility. All glassware, Teflon vessels and tools used

were cleaned to avoid external contamination.With every

set of up to 50 mushroom or soil samples digested, two

blank samples were analysed daily and no contamination

was found in blanks. The method of mercury analysis has

been validated before (Falandysz, 1990; Falandysz and

Chwir, 1997) by participation in the international cali-

bration trials like GESM/Food Euro proficiency testing

exercise, analysis of certified reference plant material and

by running calibration procedure daily.

Relationships between mercury concentrations in

mushrooms and underlying soil substrate and biocon-

centration factor (BCF) values of mercury were tested

by linear regression analysis at p < 0:01 significance

level, while the other statistical analyses were performed

using t-test and ANOVA.

3. Results and discussion

Concentrations of mercury in surface soils are shown

in Table 1. Arithmetic mean, standard deviation, range

and median values of mercury concentrations in caps and

stalks of mushrooms and in underlying soil substrate of

15 mushroom species analysed are presented in Table 2.

BCF of mercury, calculated as the quotients of concen-

trations in caps/stalks to concentrations in soil and cap to

stalk concentration quotients are also given in Table 2.

Mean mercury concentrations in soils varied between

10± 9 and 79± 52 ng/g dry matter. Soil from which the

Table 1

Total mercury concentrations (ng/g dry matter) in underlying soil sub

Type of soil substrate N

Loose and weakly loamy sands with high content of humus

Light loamy sands and heavy loamy sands

Weakly loamy sands with low or high content of humus 1

Organic soils

Weakly loamy silty sand

mushroom species �the sickener� (R. emetica) was col-

lected, contained the greatest concentration of 170± 110

ng Hg/g. Soil type and texture varied depending on the

location. In most cases, soils were sandy with small

amount of humus. Most of the soil samples contained

total mercury concentration below 100 ng/g dry matter,

which is an average value for mercury concentration in

surface layers (0–10 cm) in forest soils in Poland (Fa-

landysz et al., 1996).

According to criterion proposed by Kala�cc and Svo-

boda (2000) none of the mushroom species analysed in

this study could be considered as good mercury accu-

mulator. Among edible species, red-aspen bolete (L.

rufum) contained the highest mercury concentrations of

up to 2400 ng/g dry matter in caps and up to 1500 ng/g

in stalks. Mean concentrations of mercury in the caps

of six other edible mushroom species varied between

99± 34 and 300± 110 ng/g, which is lower (p < 0:01)than that noted for red-aspen bolete (760± 590 ng/g).

Mercury concentrations in stalks of edible mushrooms

were 1.3–2.8 fold lower than those in caps. All inedible

mushrooms sampled had cap to stalk mercury concen-

tration quotients of greater than 1, except poison pax

(P. involutus) (Table 2).

BCFs of mercury varied among mushroom species

and the lowest BCF was in the sickener (R. emetica),

poison pax (P. involutus) and Geranium-scented russula

(Russula fellea). The sickener, was taken from a sub-

strate which was rich in humus (Table 2). Three mush-

room species mentioned above were weak mercury

accumulators because the BCF values were less than 1.

The fruiting bodies of fly agaric (A. muscaria) were

characterised by the highest BCFs reaching 73± 42 for

caps and 38± 22 for stalks. A relatively great concen-

tration of mercury in the fruiting bodies of fly agaric can

be explained by their great ability to accumulate mer-

cury (Table 2). For all the mushroom species investi-

gated, there were no statistically significant relationships

(p > 0:05) between total mercury content of the caps or

stalks and soil mercury content.

3.1. Allowable consumption estimates

Tolerance limits have been established for mercury in

many kinds of foodstuffs in Poland. However, there is

no specific tolerance limit for mercury in edible higher

strate of mushrooms collected near Koszalin, Poland

umber of samples Mercury concentration

48 130± 110 (26–370)

10 98± 54 (29–190)

48 32± 20 (6.0–95)

11 11± 38 (6.0–140)

4 5.9 ± 1.3 (5.0–7.7)

Table 2

Concentrations of mercury in mushrooms and soil substrate (arithmetic mean, SD, range and *median value, ng/g dry matter) near the city of Koszalin, mercury BCF in caps and

stalks, and cap to stalk (C/S) mercury concentration quotients

Species Number

of samples

Caps Stalks Soil

Hg BCF Hg BCF C/S Hg

Tamarack jack 15 220± 60 (80–320) 19± 13 (5.0–52) 130± 47 (65–240) 12±9 (3.0–36) 1.7 ± 0.3 20± 12 (5.0–49)

S. grevillei (Klotzsch) Sing. 220* 18 120 11 15

Slippery jack 15 130± 56 (61–230) 9.1± 5.3 (1.5–18) 54± 37 (17–160) 3.8 ± 3.1 (0.4–12) 2.8 ± 0.7 22± 23 (6.0–100)

S. luteus (L.) S. F. Gray 110 9.0 44 2.7 13

European cow bolete 11 200± 110 (90–410) 6.3± 4.3 (1.8–16) 77± 35 (38–150) 2.6 ± 1.9 (0.7–7.0) 2.5 ± 0.3 45± 32 (11–95)

S. bovinus (L.) O. Kuntze 170 5.4 67 2.0 35

Bay bolete 15 200± 70 (100–370) 12± 11 (1.8–33) 84± 28 (50–160) 4.8 ± 3.7 (0.7–11) 2.4 ± 0.5 30± 22 (7.0–78)

Xerocomus badius (Fr.) K€uuhn.ex Gilb.

180 7.2 81 3.1 25

Common scaber stalk 15 300± 110 (170–550) 10± 6 (3.0–23) 200± 70 (90–300) 6.7 ± 3.6 (1.3–13) 1.6 ± 0.5 40± 20 (12–77)

Leccinum scabrum (Bull.: Fr.) 250 10 180 7.2 36

Red aspen bolete 15 760± 590 (280–2400) 20± 21 (2.3–68) 540± 340 (160–1500) 13±12 (1.1–43) 1.4 ± 0.4 68± 57 (15–190)

L. rufum (Schaeff.) Kreisel 510 13 420 9.5 37

Poison pax 15 53± 32 (20–110) 0.94± 0.68 (0.15–2.3) 55± 28 (20–120) 1.0 ± 0.7 (0.15–2.7) 1.0 ± 0.4 77± 53 (26–180)

Paxillus involutus (Batsch.: Fr.)

Fr.

40 0.66 55 0.75 63

Rickstone funnel cap 15 99± 34 (50–180) 4.0± 3.2 (1.1–13) 74± 27 (47–160) 2.9 ± 1.8 (1.0–7.5) 1.3 ± 0.2 40± 20 (10–90)

Clitocybe geotropa (Bull.) Qu�eel. 90 2.6 68 2.4 30

Fly agaric 15 830± 290 (370–1400) 73± 42 (25–165) 420± 180 (190–790) 38±22 (10–72) 2.1 ± 0.5 10± 9 (5.0–32)

A. muscaria (L.: Fr.) Pers. 790 74 390 30 11

Orange–brown ringless amanita 15 780± 270 (440–1300) 23± 25 (5.3–90) 390± 150 (210–740) 11±11 (2.3–37) 2.1 ± 0.4 61± 33 (10–130)

A. fulva (Schaeff) Fr. 670 13 330 6.5 62

Brown cort 15 920± 280 (560–1600) 23± 19 (5–56) 560± 220 (130–1000) 14±12 (3.4–39) 1.5 ± 0.4 78± 66 (12–220)

Cortinarius malicorius 880 20 580 8.5 41

The sickener 15 30± 31 (7.0–140) 0.27± 0.24 (0.036–0.78) 17± 11 (8–54) 0.18± 0.17 (0.02–0.57) 1.6 ± 0.7 170± 110 (30–370)

R. emetica Fr. 22 0.17 15 0.12 180

Geranium-scented russula 15 51± 19 (30–100) 1.1± 1.2 (0.3–4.8) 34± 8 (19–49) 0.67± 0.58 (0.2–2.4) 1.5 ± 0.3 79± 52 (14–230)

R. fellea Fr. 45 0.6 34 0.5 75

Red-hot milk cap 15 44± 28 (20–130) 1.9± 1.8 (0.3–7.6) 37± 19 (14–88) 1.4 ± 1.3 (0.2–5.2) 1.2 ± 0.4 34± 23 (13–94)

Lactarius rufus (Scop.: Ft.) Fr. 40 1.5 35 1.0 22

Mutagen milk cap 15 600± 750 (63–2600) 19± 21 (2.0–79) 370± 470 (48–1600) 11±13 (1.1–49) 1.7 ± 0.3 35± 22 (11–80)

L. necator (Bull.: Fr.) P. Karst 300 12 180 8.0 28

464

J.Falandysz

etal./Chem

osphere

54(2004)461–466

J. Falandysz et al. / Chemosphere 54 (2004) 461–466 465

mushrooms. The tolerance limit set for mercury in fresh

vegetables and dried plant food items (>50% dry matter)

in Poland is 20 and 30 ng/g (Monitor Polski, 1993), re-

spectively. The concentrations of mercury in all edible

mushrooms exceeded the tolerance limit set for dried

plant foodstuffs. When the concentrations are expressed

on a fresh weight basis (moisture content of 90%, on

average), concentrations of mercury in slippery jack (S.

grevillei), European cow bolete (S. bovinus), bay bolete

(X. badius) and rickstone funnel cap (C. geotropa) were

below the tolerance limit (Table 2).

Wild growing mushrooms are attractive and popular

constituents of many meals traditional to the Polish

cuisine culture. Mushroom picking is a very popular

activity among the Poles. Nevertheless, there is no data

available on the collection and/or consumption rates of

wild or cultivated mushrooms in Poland. In the Czech

Republic, 72% of the families pick mushrooms at an

annual rate of 7 kg per household, with consumption

rates exceeding 10 kg per annum for some individuals

(Kala�cc and Svoboda, 2000). The rates of mushroom

collection and consumption estimates in Poland are ex-

pected to be similar to those in the Czech Republic.

Noncarcinogenic health effects may be estimated

using mercury reference dose value (RfD) of 0.0003 mg/

kg/day (US EPA, 1989; Kannan et al., 1998). The RfD is

an estimated single daily chemical intake rate, that ap-

pears to be without a risk if ingested over a lifetime. The

estimated dose (D) can be calculated as D ¼ C � I=W �1000 where C¼ concentration of mercury in mushroom

(lg/g wet wt), I ¼ ingestion rate of mushroom (g/day),

W ¼ average body weight (70 kg). The hazard index (H )

for the substance is the ratio of the dose (D) to the upper

level of daily substance intake rate over lifetime esti-

mated to be without toxic effects (i.e. RfD). If the Hvalue is less than 1, toxic effects are not expected to

occur. The H value can be calculated as a function of

ingestion rate and concentration of mercury ion in

mushrooms. The ingestion rates were chosen to repre-

sent average consumption rate per household member

(6.4 g/day) in the region of Koszalin (assuming 7 kg

annually per family/three family members) and the

highest consumption rate per individual (28 g/day; as-

Table 3

Hazard index for ingestion of mushrooms containing mercury

in the neighbourhood of the city of Koszalin

Ingestion rate

(g/day)

Hazard index (H)

Based on highest

Hg concentration

(0.076 lg/g wet

weight)

Based on mean

Hg concentration

(0.027 lg/g wet

weight)

6.4 0.02 <0.01

28 0.10 0.04

suming 10 kg annually). The H values were calculated

for ingestion of mushrooms containing the greatest (76

ng/g wet wt) and mean (27 ng/g wet wt) mercury con-

centrations for the examined species (Table 3). The re-

sults suggested that the consumption of mushroom

species analysed in this study is not hazardous at the

ingestion rates less than 280 and 700 g fresh product/

day, respectively, which would result in an hazard index

value less than unity.

Acknowledgements

Financial support from the Polish State Committee

for Scientific Research (KBN) under the grants no DS/

8250-4-0092-02 and PB 0705/PO6/2002/22 is acknowl-

edged.

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