Evaluation of Mercury Contamination in Fungi Boletus Species from Latosols, Lateritic Red Earths, and Red and Yellow Earths in the Circum-Pacific Mercuriferous Belt of Southwestern China
Evaluation of Mercury Contamination in Fungi Boletus Species from Latosols, Lateritic Red Earths, and Red and Yellow Earths in the Circum-Pacific Mercuriferous Belt of Southwestern China
Jerzy Falandysz 0 1 2
Ji Zhang 0 1 2
Yuan-Zhong Wang 0 1 2
Martyna Saba 0 1 2
Grażyna Krasińska 0 1 2
Anna Wiejak 0 1 2
Tao Li 0 1 2
0 1 Laboratory of Environmental Chemistry & ecotoxicology, Gdańsk University , Gdańsk , Poland , 2 Institute of Medicinal Plants, Yunnan Academy of Agricultural Sciences , Kunming, Yunnan , China , 3 Yunnan Technical Center for Quality of Chinese Materia Medical , Kunming , China , 4 Yuxi Normal University , Yuxi, Yunnan , China
1 Funding: This project in part was supported by the National Science Centre of Poland (UMO-2011/03/N/ NZ9/04136), the National Natural Science Foundation of China (Nos. 31460538, 31260496), and the Science Foundation of the Yunnan Province Department of Education , 2013Z074
2 Editor: Manuel Reigosa, University of Vigo , SPAIN
For the first time, highly elevated levels of mercury (Hg) have been documented for several species of the edible Fungi genus Boletus growing in latosols, lateritic red earths, and red and yellow earths from the Yunnan province of China. Analysis of Hg concentrations in the genus suggests that geogenic Hg is the dominant source of Hg in the fungi, whereas anthropogenic sources accumulate largely in the organic layer of the forest soil horizon. Among the 21 species studied from 32 locations across Yunnan and 2 places in Sichuan Province, the Hg was found at elevated level in all samples from Yunnan but not in the samples from Sichuan, which is located outside the mercuriferous belt. Particularly abundant in Hg were the caps of fruiting bodies of Boletus aereus (up to 13 mg kg-1 dry matter), Boletus bicolor (up to 5.5 mg kg-1 dry matter), Boletus edulis (up to 22 mg kg-1 dry matter), Boletus luridus (up to 11 mg kg-1 dry matter), Boletus magnificus (up to 13 mg kg-1 dry matter), Boletus obscureumbrinus (up to 9.4 mg kg-1 dry matter), Boletus purpureus (up to 16 mg kg-1 dry matter), Boletus sinicus (up to 6.8 mg kg-1 dry matter), Boletus speciosus (up to 4.9mg kg-1 dry matter), Boletus tomentipes (up to 13 mg kg-1 dry matter), and Boletus umbriniporus (up to 4.9 mg kg-1 dry matter). Soil samples of the 0-10 cm topsoil layer from the widely distributed locations had mercury levels ranging between 0.034 to 3.4 mg kg-1 dry matter. In Yunnan, both the soil parent rock and fruiting bodies of Boletus spp. were enriched in Hg, whereas the same species from Sichuan, located outside the mercuriferous belt, had low Hg concentrations, suggesting that the Hg in the Yunnan samples is mainly from geogenic sources rather than anthropogenic sources. However, the contribution of anthropogenically-derived Hg sequestered within soils of Yunnan has not been quantified, so more future research is required. Our results suggest that high rates of consumption of Boletus spp. from Yunnan can deliver relatively high doses of Hg to
Data Availability Statement: All relevant data are
within the paper.
Competing Interests: The authors have declared
that no competing interests exist.
consumers, but that rates can differ widely because of large variability in mercury
concentrations between species and locations.
Mercury is a ubiquitous trace element in the Earth’s crust. In some regions of the world, soils
are enriched in Hg in the form of HgS, because of geochemical anomalies causing
mercuriferous belts [
]. Today, the surface layer of forest and mountain topsoils worldwide is also
usually enriched in Hg due to atmospheric deposition from anthropogenic sources [
anthropogenically-caused enrichment of mercury in the organic layer of topsoils is a serious
environmental concern, with potential negative impacts on both the environment and human
]. Mercury typically occurs in biota and foods in trace amounts both in the form of an
inorganic (Hg+/2+) compounds and methylmercury, (MeHg, CH3Hg+), which is a persistent
and highly toxic compound that is the most common organic form of Hg. The ongoing process
of environmental spread of Hg because of anthropogenic activities is of consequence probably
not only for the forest topsoil but also for biota, especially marine organisms and upper
trophic-level species susceptible to bio-magnification [
Mercury is a semi-volatile metal and all its molecular forms are hazardous to human. The
molecular forms that are such as HgSe (mineral tiemannite), HgS (mineral cinnabar), and little
relevant environmentally Hg2Cl2 (calomel) are considered “safe” because they all have low
solubility in water; however, following ingestion they dissociate and/or are more soluble in the
highly acidic pH of gastric fluid after ingestion than in the water of a laboratory tube.
Although HgS is an ingredient in some medicinal preparations, including in Chinese
Traditional Medicine [
], mice exposed to HgS experienced symptoms of neurotoxicity [
Nevertheless, little information exists on the possible Hg intake and risks associated with the
consumption of mercury-contaminated medicine and foodstuff, such as edible mushrooms or
herbs from the mercuriferous belts [
The ubiquity of Hg in the environment and its occurrence in food has resulted in low-level
dietary intake of certain inorganic forms of Hg and MeHg, which are common trace-compounds
in foods. At a regional scale, because of anthropogenic pollution (e.g. Minamata Bay) or geology
(mercuriferous belts), exposure can be elevated for MeHg, as well as inorganic Hg, while
beneficious Se in food chain could be in deficit [
]. Traditionally, daily meals often include
wildgrown mushrooms as a small ingredient. Annual rates of intake of wild mushrooms are highly
variable across different regions of the world, varying with cultural and family traditions in places
such as the Czech Republic, Finland, the Yunnan of China, England, and Poland . Seafood is
viewed as a “source” of Hg to humans but is not a wild-grown and tasty mushroom, which
among biota often is the best accumulator of Hg from soil. Hence, mushrooms could be an
important local source of Hg to humans and the chemical form of Hg could be a crucial factor
mediating the effects of mercury-contaminated mushrooms on human health.
For example, in fish muscles Hg occurs nearly totally in the form of MeHg bound to thiols
(-SH) of cysteine (MeHg-cys) in proteins [
], and this is highly different when compared so
far to data published for wild-grown mushrooms [
]. Fish is considered a major source of
MeHg in humans but this can depend on the location and compositional structure of a diet
(ingredients and their geographical origin). For example, for some people in the Guizhou
Province of China neither, rice, rather than seafood, is the major source of dietary MeHg [
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Edible wild grown mushrooms that grew in locations far from industrial and urban regions
can be contaminated with Hg. This is because many mushrooms efficiently uptake this element
from soil substratum underneath the fruiting bodies. For example, Macrolepiota procera
(Parasol Mushroom) and Boletus edulis (King Bolete) are species whose mycelium efficiently absorbs
Hg from the soil substratum and accumulate it in fruiting bodies—frequently at level > 3.0 mg
kg-1 dm in areas with Hg in topsoil well below 0.05 mg kg-1 dm [
]. The Hg concentration
of fruiting bodies of several popular edible mushrooms foraged from “pristine” European
forests ranges from 0.27±0.07 to 8.4±7.4 mg kg-1 dry matter (with mean ranging from 0.027 to
0.84 mg kg-1 wet weight; assuming 90% moisture content) . Genus Boletus has many
]. Some Boletus species are called “real boletes”, such as. Boletus aereus, B. edulis, B.
pinophilus, and B. reticulatus, which have been found to be rich in Hg (and Se), while other
species have been found to be much less in Hg (and Se) when compared to the “real boletes”
(e.g. Bay Bolete B. badius (earlier called Xerocomus badius), Larch Bolete Suillus grevillei,
Variegated Bolete S. variegatus) [
Mushrooms growing in places with elevated concentrations of Hg in the topsoil due to
cinnabar (HgS) mining, processing of the non-ferrous metals, and other kinds of Hg hot spots
usually contain elevated concentrations of Hg that is up to 10~100 fold greater than the
amounts found in background areas (e.g., researchers found 20±42 mg Hg kg-1 dm in
Cantharellus cibarius, 23±24 mg kg-1 dm in M. procera, and 52±61 mg kg-1 dm in S. grevillei) [
Although the primary source of many inorganic compounds for fungi seem to be from the
substratrum (e.g. decaying litter, organic or mineral layer of soil, and dead or living vegetation),
the movement of water and vertical migration of water soluble compounds through the soil
horizon can also matter. Given the huge diversity of mushrooms (macrofungi), species-specific
genetic features, in addition to the mycorrhizal/saprophytic lifestyle, likely influence the uptake
and sequestration of certain mineral components in fruiting body of a given fungus. Some
fungi also have rhizomorphs—root-like structures that enhance the uptake of water and
watersoluble compounds [
]. For example, airborne pollutants such as Hg or radionuclide 134/137Cs
are well accumulated by some species with shallow mycelia—Hg by Gymnopus erythropus and
]. The nuclides 134/137Cs are better accumulated by Cortinarius spp.,
which richer in the stable caesium (133Cs) [
It is not well known which compound of Hg is the major constituent of total Hg in
mushrooms and where it is located in the fruiting body and/or cells. The highly toxic MeHg is
considered to be a minor fraction (< 5%) of the total Hg in mushrooms, although MeHg can be
more efficiently accumulated in fruiting bodies than inorganic forms of Hg that dominate in
flesh of mushrooms [
]. A low-level exposure to MeHg/total Hg is considered to not
have substantial negative health consequences because of the protection provided by dietary
selenium (Se) [
]. The beneficial role of Se, which can protect the cells from toxic action by
Hg, has been explained based on the replacement of Se in the selenocysteine comprising
selenoenzymes (e.g. gluthatione peroxidase; GPx) by the Hg in CH3Hg+ bound covalently to thiol
(-SH) of cysteine (MeHg-cys) and the formation of a strong bond of Hg-Se in Se-Hg-cys
]. The Se-Hg-cys complex is further degraded in lysosome to mercury-selenide
(HgSe) and this can lead to weakening of an activity of selenoenzymes and a deficit in the body
pool of Se, which is necessary for selenoenzyme synthesis.
Apart from Se there are also other possible ligands for Hg in fruiting bodies of mushrooms
like thiols (-SH) in amino acids. Cysteine is typical but a minor component of the exogenous
amino acids in mushrooms such as Pleurotus ostreatus and Agaricus bisporus [
cysteine is a possible ligand for MeHg in mushrooms. The seleno-compounds that have been
found in mushrooms are selenocysteine, selenomethionine, Se-methylselenocysteine, and
selenite, as well as several unidentified compounds. The concentrations of these compounds in
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mushrooms vary widely between species [
]. Sulphur [
], Se [
], and Hg [
] are the
elements specifically abundant in some Boletus spp. Hence, it is possible that a bulk of Hg
accumulated by mushrooms can be bound by S other than -SH of cysteine or by Se; however,
evidence is lacking. A recent study showed that the majority of Hg contained in fruiting bodies
does not leach during blanching, which suggesting it may strongly bind to functional groups or
be present as compounds that do not easily dissolve [
The latosols, lateritic red earths, and red and yellow earths in southwest China showed
geochemically-elevated concentrations of Hg when compared to some other regions in the country
]. Nevertheless, there is a lack of studies and data on the influence of the mercuriferous belt
on the accumulation and concentration of Hg in wild grown mushrooms, which are abundant
and popular foods in Yunnan. This study aimed to get an insight into the accumulation,
distribution and probable dietary intake of Hg contained in 21 species of Boletus mushrooms
collected in 32 locations across Yunnan Province and 2 locations in Sichuan Province in the
southwestern China. Topsoil samples underneath the fruiting bodies were collected from
certain locations alongside the mushrooms. An attempt was also made to assess the exposure to
Hg contained in those mushrooms using established safety criteria.
Materials and Methods
Mushrooms and topsoil samples
In order to investigate mushrooms representative of Yunnan, we chose species representing
widely distributed locations and collected several individuals from a species in a given location,
which were combined into composite samples for chemical analysis (Fig 1). No specific permits
Fig 1. Localization of the sampling sites (1–34; for details see in Table 1). The figure was created by DIVA-GIS 7.5 software.
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were required for the described field studies. No endangered or protected species were sampled,
and the localities where the samples came from are not protected in any way. Matured
mushrooms with small fruiting bodies are usually pooled before determination of trace element
]. Examination of such composite samples allows for a substantial
reduction of costs with limited loss of information and prevention of a bulk of sample material
for other analyses [
]. Hence, it is possible to obtain representative information on the
concentration of a given chemical element in fruiting bodies based on a composite sample instead
of the examination of individual specimens (15 individual samples is the minimum required
per location/population) [
In total, 968 specimens of 21 species of edible mushrooms of genus Boletus were collected in
forests from 32 locations across Yunnan and 2 places in Sichuan Province of China during the
collection season (June-September) in 2011–2014 (Fig 1). Soil samples of the forest topsoil
layer (0–10 cm) beneath the fruiting bodies were also collected. The species collected were
Boletus aereus Fr. ex Bull, Boletus amygdalinus (Thiers) Thiers, Boletus auripes Peck, Boletus bicolor
Peck, Boletus brunneissimus Chiu, Boletus calopus Fr, Boletus edulis Bull., Boletus ferrugineus
Schaeff, Boletus fulvus Peck, Boletus griseus Frost., Boletus impolitus Fr., Boletus luridiformis
Rostk., Boletus luridus Schaoff.:Fr., Boletus magnificus Chiu., Boletus obscureumbrinus Hongo,
Boletus pallidus Frost, Boletus purpureus Fr., Boletus sinicus W.F.Chiu, Boletus speciosus Forst.,
Boletus tomentipes Earle and Boletus umbriniporus Hongo [
]. The collected fruit bodies were
in good “edible” body condition (not injured by insects) and well developed (old and “baby”
specimens were not selected). Any visible plant vegetation and soil debris were cleaned off of
the fresh fruit bodies using a plastic knife. To get insight into the distribution of Hg between
two major morphological parts of the fruit bodies, each specimen was separated into cap (with
skin) and stipe. Next, the individual cap and stipe samples were sliced using a plastic knife and
pooled accordingly to obtain representative composite samples representing each species (with
5 to 21 individuals per pool), sampling place and time of collection (Table 1).
Thereafter, the mushroom samples were placed into the plastic basket of the electrically
heated commercial dryer for vegetables and dried at 65°C to constant mass. Dried fungal
materials were pulverized in a porcelain mortar and kept in brand new sealed polyethylene bags
under dry conditions. The soil samples, free of any visible organisms, small stones, sticks and
leaves were air dried at room temperature for several days under clean conditions and further
dried at 65°C to constant mass. Next, the soil samples were ground in a porcelain mortar,
sieved through a pore size of 2 mm plastic sieve and kept similarly to fungal materials.
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 100,
150, and 200 μL of 1.0 mg mL-1 Hg standard solutions were injected into the analyzer for the
construction of a calibration curve, which was prepared each week.
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The determinations of total Hg concentration of fungal and soils samples was performed
using cold-vapour 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 296 nm. Each sample was examined at least in duplicate and
most of the samples, because of unexpectedly high Hg concentrations, were examined in
triplicate. The analytical instrument used was a mercury analyzer (MA-2000, Nippon Instruments
Corporation, Takatsuki, Japan) equipped with an auto-sampler, and operated in low or high
modes, as appropriate [
A running analytical control and assurance quality (AC/AQ) was performed through the
analysis of blank samples and certified reference materials such as CS-M-1 (dried mushroom
powder Suillus bovinus), CS-M-2 (dried mushroom powder Agaricus campestris), CS-M-3
(dried mushroom powder Boletus edulis), and CS-M-4 (dried mushroom powder Leccinum
scabrum) produced by the Institute of Nuclear Chemistry and Technology, Warsaw, Poland
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 3–5 samples studied.
The bioconcentration factor (BCF) value (calculated for mushrooms as the concentration
quotient of fruiting body/cap or stipe to that of the underlying soil substrate) is used to estimate
possible influence. BCF allows us to estimate the elements that are actively accumulated
(BCF > 1) and those not actively accumulated, i.e. excluded (BCF < 1).
Results and Discussion
Hg in fruiting bodies
There is a scarcity of data on the accumulation and distribution of Hg in wild grown fungi
collected from the soils of the circum-Pacific mercuriferous belt of Yunnan [
] or outside
of the belt in China [
]. In general, the concentration of Hg in caps and stipes differed
substantially both between Yunnan locations and between species (Fig 1, Table 2). The
overall range of Hg concentrations in composite samples of the caps of Boletus spp. in this study
was from 0.13 mg kg-1 dm up to 22 mg kg-1 dm, the record high value reported for any
mushroom collected from the area (an area previously considered as background due to receiving
limited Hg pollution). In the stipes, the values of Hg ranged from 0.12 mg kg-1 dm to 8.4 mg
kg-1 dm (Table 2).
There is a high scarcity of data on the occurrence of Hg in Boletus mushrooms foraged in
Yunnan. Apart from a highly contaminated B. edulis specimen from the location Dayingie in
the central region of Yunnan (22 mg kg-1 dm in caps), mushrooms with high Hg
concentrations were found in: B. aereus from Yongren in the Chuxiong Autonomous Prefecture (13 mg
Hg kg-1 dm), B. bicolor from the Dayingie in the Yuxi City (at 5.5 mg kg-1 dm), B. ferrugineus
from the Dayingie in the Yuxi City (at 7.7 mg kg-1 dm), B. luridus from the Yuanmou in the
Chuxiong Autonomous Prefecture (at 11 mg kg-1 dm), B. magnificus from the Dayinjie in the
Yuxi City (at 13 mg kg-1 dm), B.obscureumbrinus from the Simao region in the Pu'er City (at
9.4 mg kg-1 dm), B. purpureus from the Lanping in the Nujiang Autonomous Prefecture (at 16
mg kg-1 dm), B. sinicus from the Jiulongchi in the Yuxi City (at 6.8 mg kg-1 dm), B. speciosus
from the Yuanmou in the Chuxiong Autonomous Prefecture (at 4.9 mg kg-1 dm), B. tomentipes
from the Dayingjie in the Yuxi City (at 13 mg kg-1 dm), and B.umbriniporus from the
Yuanmou in the Chuxiong Autonomous Prefecture (at 4.9 mg kg-1 dm) (Table 2).
Because of the large number of Boletus species examined here, for clarity of presentation the
results that follow are alphabetically ordered by species names.
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*(see Fig 1);
**(number of individuals);
WD (without data)
B. aereus. B. aereus prefers a warm climate. This fungus showed a capacity for
accumulation of Hg in the fruiting bodies and in this study the maximum was 13 mg Hg kg-1 dm in caps
and 4.2 mg kg-1 dm in stipes from the Yongren in the Chuxiong Autonomous Prefecture in the
northern part of Yunnan. For the specimens from the south of Yunnan in Dongshan in the
Wenshan Autonomous Prefecture, the values of Hg were an order of magnitude lower
Our results well agree with data on Hg in B. aereus from other parts of the world, which are
few and relate to individuals collected from the southern regions of Europe. Namely, in a recent
study B. aereus from Seville Spain showed Hg at 10 ± 3 mg kg-1 dm in the caps and 8 ± 3 mg
kg-1 dm in the stipes [
]. Another study from Lugo, Galicia Spain showed the Hg at 4.6 ± 2.3
mg kg-1 dm in hymenophore and at 3.3 ± 1.5 mg kg-1 dm in the rest of the fruiting bodies of B.
], while the mean value of Hg in whole fruiting bodies from the Reggio de Emilia
localization in Italy was 3.29 mg kg dm-1 [
The topsoil samples beneath the fruiting bodies of B. aereus contained Hg at 0.68 mg kg-1
dm in the Yongren location and 0.22 mg kg-1 dm in the Dongshan location, while the BCF
values of Hg were high for both areas, i.e. BCF at 19 and 7.3 for caps and at 6.2 and 4.4 for stipes
(although our sample size was only two per material). These high values of BCF demonstrate a
high capacity of the species to bio-include Hg even if the element concentration in soil was
elevated. The value of BCF showed that Hg up-take and sequestration by B. aereusis is higher for
soils with greater concentrations of Hg in the mineral horizon (Table 1).
Melgar et al. [
] reported a very high potential of B. aereus to bioconcentrate Hg (BCF at
315–424) for low polluted soil substratum—the Hg concentration of soil in Lugo was at ~ 0.01
mg kg-1 dm. It is worth noting that there are regions in both Italy and Spain that are under the
impact of mercuriferous belts [
]. Nevertheless, the Hg in soil substratum of B. aereus at the
Lugo locale was ~20 to 60-fold less than the soils in Yunnan. Unfortunately, there is no
information on Hg in soils substratum for the Reggio de Emilia or Sevilla.
B. amygdalinus, B. auripes, B. bicolor, B. brunneissimus, and B. calopus. Samples of B.
amygdalinus (former name Xerocomus amygdalinus), B. auripes, B. bicolor, B. brunneissimus,
and B. calopus, were available from a few places only. The pooled samples showed a range of
Hg concentrations in the caps, with 0.63 mg kg-1 dm for B. amygdalinus up to 5.5 mg kg-1 dm
for B. bicolor, and stipes were 50% less contaminated (Table 1). The relative high concentration
of Hg in B. bicolor sampled from the Dayingjie region in the county of Yuxi can be attributed
to the elevated concentration of the element in topsoil, as was noted for some other species
from this region (Table 1). All of these five boletus species are common in Yunnan, but there is
no information on the occurrence of Hg in fruiting bodies of these species from locations
B. bicolor sampled in the Sichuan Province of China from a place with Hg in topsoil
of < 0.1 mg kg-1 dm contained 0.19 mg Hg kg-1 dm in caps [
]. No other information is
available on accumulation and occurrence of Hg in B. amygdalinus, B. auripes, B. bicolor, B.
brunneissimus, and B. calopus.
B. edulis. B. edulis from all places sampled in Yunnan showed “elevated” concentration of
Hg, and the values ranged from 1.6 mg kg-1 dm to 22 mg kg-1 dm for the caps and from 0.85
mg kg-1dm to 8.2 mg kg-1 dm for the stipes. The median value of Hg for consignments of B.
edulis for 20 places scattered across Yunnan was 4.5 mg kg-1 dm for caps and 1.9 mg kg-1 dm
A few earlier data are also known on concentration of Hg, As, Cd, Pb, and Zn in B. edulis
from Liangshan in Sichuan with Hg at 0.28 mg kg-1 dm and at 1.8 mg kg-1 dm in sample from
mountains in Sichuan of China [
]. In another study in Sichuan, the Hg in caps of B.
edulis was 0.38 and in stipes 0.16 mg kg-1 dm, while in soil substratum was < 0.1 mg kg-1 dm [
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The B. edulis (King Bolete) from Europe has been well studied for Hg, many other trace
elements, and macro elements [
]. From the studies mentioned it is
known that in Europe B. edulis is efficient in the up-take and sequestration in flesh of Hg. For
example, B. edulis collected from many background locations contained Hg ranging from 1.1
±1.4 mg kg-1 dm to 7.6±3.1 mg kg-1 dm in the caps and from 0.82±0.71 to 3.8±1.8 mg kg-1 dm
in the stipes in Poland; 7.9±0.3 mg kg-1 dm in a whole fruiting bodies from the Precambrian
shale’s location in Bohemia of the Czech Republic and 2.7 (1.0–4.3) mg kg-1 dm in a whole
fruiting bodies in the Reggio Emilia and from 1.9±1.0 to 4.5±1.0 mg kg-1 dm in Tuscany of
Italy. This species collected in the region of Lugo in Galicia of Spain showed Hg in
hymenophore of 3.3±2.4 mg kg-1 dm and in the rest of fruiting bodies of 2.0±1.2 mg kg-1 dm.
B. fulvus, B. griseus, B. impolitus, and B. luridiformis. These four species (B. fulvus, B.
griseus, B. impolitus, and B. luridiformus) from Yunnan have not been so far studied for the
accumulation and contamination with Hg and they are without the BCF values. They all can be
considered as rich in Hg with maximum of up to 4.9 mg kg-1 dm in a pool of the caps of B.
griseus, while they seem not so efficient in up-take and sequestration of Hg as B. aereus and B.
edulis. In fruiting bodies of B. griseus sampled in 2006 from the Xichang region of the Sichuan
Province, the Hg was usually much lower than determined in present study, i.e. at 0.34 and
0.94 mg kg-1 dm [
] or in caps at 0.10 mg kg-1 dm [
]. No other data on occurrence of Hg in
B. fulvus, B. griseus, and B. luridiformis could be found in scientific literature. A specimen of B.
impolitus sampled from the Pb-Zn mine area in the Lanping County in north-western region
of Yunnan contained Hg in a whole fruiting body at 6.5 mg kg-1 dm [
Concentration of Hg determined in B. impolitus from Yunnan (Table 1) is almost the same
value as reported recent in a study in Poland. For a collection of the fruiting bodies of B.
impolitus from the localization situated far away from the mercuriferous belts in the north-eastern
region of Poland where Hg in soil substratum was at 0.042±0.014 mg kg-1 dm, the
concentration of Hg in the caps was at 1.8±0.6 mg kg-1 dm and in the stipes at 0.70±0.21 mg kg-1 dm
]. The values of BCF calculated for caps and stipes of the individuals from Yunnan were
respectively 4.4 and 2.3 (Table 1) and for individuals from the northern region of Poland were
an order of magnitude higher, i.e. 47 and 17 (median) [
]. This implies on a much better
absorption and sequestration by B. impolitus of Hg which contaminate the environment
because of a global anthropogenic fallout of Hg (a major or sole source of Hg in topsoil/soil in
Poland) than of the geogenic Hg from a geochemical anomaly.
B. luridus, B. magnificus, and B. obscureumbrinus. There are no previous records
available on Hg in B. luridus, B. magnificus, and B. obscureumbrinus from China. In this study, the
mushrooms B. luridus with up to 11 mg Hg kg-1 dm and B. magnificus with up to 13 mg Hg
kg1 are among those Boletus spp., which in several locations in Yunnan are highly contaminated
with Hg. Two collections of individual samples of B. obscureumbrinus were available only from
the Simao region in the Pu’er City on the south of the Yunnan and both mushrooms from
consignments were rich in Hg, which ranged from 6.3 to 9.4 mg kg-1 dm in the caps and from 3.6
to 6.0 mg kg-1 dm in the stipes (Table 1).
In case of B. luridus, B. magnificus, and B. obscureumbrinus mushrooms, the only previous
record available is for B. luridus collected from three spatially distantly distributed places in
Europe, which showed Hg in the caps of 0.40±0.10 to 0.89±0.40 mg kg-1 dm and 0.15±0.06 to
0.39±0.16 mg kg-1 dm in stipes [
]. The Yunnan’s B. luridus mushroom with Hg in the caps
of 2.1–11 and in the stipes of 0.67–4.2 mg kg-1 dm seems to pick-up Hg largely from the
mineral layer of soil horizon that is around 10-100-fold more enriched in Hg (Table 1), when
compared to concentration in topsoil substratum to B. luridus from Poland [
B. pallidus, B. purpureus, and B. sinicus. Mushroom B. pallidus was available from one
place and showed Hg in the caps of 1.3 mg kg-1 dm. It can be classified into the group of the
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Boletus mushrooms in Yunnan, which are less contaminated with Hg—may be because of low
bioconcentration potential for Hg compounds or because of low concentration of element in
soils (< 0.20 mg kg-1 dm) at the sampling locations. Both B. purpureus and B. sinicus from the
soils with elevated concentration of Hg, which showed contained from 2.4 to 4.3 mg Hg kg-1
dm, were substantially contaminated and concentration were up to 16 mg Hg kg-1 dm in the
caps and up to 6.8 mg Hg kg-1 dm in the stipes (Table 1). No data are available from the
scientific literature on Hg compounds in the fruiting bodies accumulation and distribution by B.
pallidus, B. purpureus and, B. sinicus.
B. speciosus, B. tomentipes, and B. umbriniporus. The species such as B. speciosus, B.
tomentipes, and B. umbriniporus are among the most popular edible fungi of genus Boletus in
Yunnan. They contained Hg in fruiting bodies at a wide range of concentrations which was
dependent on the geographical location. The B. speciosus with Hg in the caps ranged from 0.90
to 4.9 mg kg-1 dm, the B. tomentipes with from 0.13 to 13 mg kg-1 dm, and the B. umbriniporus
with from 0.54 to 4.9 mg kg-1 dm can be classified among the species in this study that are
substantially contaminated in view of the food toxicology philosophy.
In previous reports from the Sichuan Province of China, the reported concentration of Hg
in whole fruiting bodies of B. umbriniporus from the Liangshan place was 0.18 mg kg-1 dm
], and in caps and stipes of B. umbriniporus sampled elsewhere in the Sichuan, the Hg were
0.16 and 0.11 mg kg-1 dm for caps and stipes respectively [
The soil samples from the widely distributed locations in Yunnan showed Hg in 0–10 cm layer
at 0.073 to 3.4 mg kg-1 dm and most of the samples were well above 0.2 mg kg-1 dm, while in
two places in Sichuan were at 0.034 to 0.055 mg kg-1 dm (Table 1). The overriding source of
elevated concentration of Hg in the mineral layer of latosols, lateritic red earths and red and
yellow earths of Yunnan in this study is geochemical anomaly due to occurrence of the
circumPacific mercuriferous belt, while Hg deposited from the atmosphere is retained in a top 0–3 cm
layer of forest soil of Yunnan, which is black and rich in decaying litter and humus with organic
The red earths are the dominant highly weathered soil type in China and widely distributed
in the hilly and mountainous regions of northern part of Yunnan, while the lateritic red earths
are mainly distributed in areas bordering between the tropical and subtropical regions of
southeast part of Yunnan [
]. There is scarcity of data on Hg concentration of soils in
Yunnan. Wen and Chi [
] reported an average Hg concentration of 0.14 mg kg-1 dm (2,995
samples) in different types of sediments in southwest China (central and east Yunnan included), at
0.046 mg kg-1 dm (1,190 samples) from rain forest (south Yunnan included) and at 0.045 mg
kg-1 dm (1,183 samples) from alpine valleys (northwest Yunnan included). In south and
southwest China, median Hg concentrations in the C horizon and A horizons of soils (totally ~
12,000 samples) are 0.076 mg kg-1 dm (C) and 0.086 mg kg-1 dm (A) in yellow earth, 0.044 mg
kg-1 dm (C) and 0.069 mg kg-1 dm (A) in red earth, and 0.035 mg kg-1 dm (C) and 0.044 mg
kg-1 dm (A) in latosolic red earth [
In some other studies in China, in the Sichuan Province, which is largely the farmland
region, soils showed Hg in tea garden soil at 0.039 mg kg-1 dm (up to 0.37 mg kg-1 dm) [
and at 0.15 mg kg-1 dm (0.003–0.71 mg kg-1 dm) in 239 samples of topsoil from the central
region of the province [
]. There is no data available on speciation of Hg in soils of Yunnan.
In the active Xunyang Hg mine area in the south of the Shaanxi Province in China, which is in
northeast direction to Yunnan, the Hg and MeHg concentrations in riparian soils ranged
respectively from 5.4 to 120 mg kg-1 dm and from 0.0012 to 0.011 mg kg-1 dm [
12 / 19
Mercury can occur in organic and mineral layer of topsoil in various forms [
], such as
chelated (bound to organic substances), precipitated (in sulphide, carbonate, hydroxide,
phosphate and others), specifically and non-specifically adsorbed (because of covalent and
coordinative or electrostatic binding), and dissolved (free ion or soluble complex). In a study by
Rodrigues et al. [
], the geogenic Hg in soils from a mining area (Hg at 0.92 to 37 mg kg-1 dm)
was in a greater proportion as non-mobile forms that was less extractable, while more mobile
and semi-mobile Hg were in urban and industrial soil, which were better extractable by 0.1M
HCl or surrogates of human gastric fluid (pH 1.5) and human lung fluid (pH 7.4).
Data obtained in this study imply that B. edulis is very efficient in mobilization and
absorption of sparingly soluble forms of Hg (largely HgS) coming from the geogenic source in forest
soil of Yunnan. This is because mushroom B. edulis has mycelia deeper in soil substratum and
Hg concentration accumulated in fruiting bodies by this species seems to be more dependent
on the abundance of the geogenic or soil crust Hg from a deeper layer than airborne Hg from a
surface layer of soil horizon (this is known from accumulation of 137Cs by B. edulis after the
Chernobyl nuclear power plant catastrophe) [
]. The calculated values of Hg
bioconcentration factor (BCF), which is a quotient of element in cap, stipe, or a whole fruiting body to soil
concentration on dry matter basis, showed that all species for which both the fruiting bodies
and samples of soil substratum were available for study showed good potential to accumulate
Hg (BCF well above 1). Surprisingly, the values of BCF were relatively high even where
substratum was relatively rich in Hg due to geochemical anomaly (Table 1), and Hg concentration of
the caps and stipes of the fruiting bodies of B. edulis positively correlated with concentration in
soil—correlation coefficient (r) respectively at 0.89 and 0.92 (p < 0.005) (Fig 2). Also a highly
significant correlation was determined for relationship between Hg concentration of the caps
(0.78; p < 0.0001) and stipes (0.89; p < 0.0001) of the fruiting bodies and soil substratum for
all Boletus spp. (Fig 3). These results showed that B. edulis is a potential bioindicator of Hg
contained in soil substratum beneath the fruiting bodies and probably especially when the mineral
soil horizon is enriched in this element. In a wide study on occurrence and accumulation of Hg
and other metallic elements and minerals by B. edulis across Poland a weak positive
relationship could be found only for Cd in fruiting bodies and topsoil but not for Hg [
The results from present study and a sufficient number of published data from Europe imply
that B. edulis is able to efficiently up-take (BCF > 1) and sequester Hg in fruiting bodies at
elevated concentration when they emerge in the “background” areas (assuming lack of hot spot
anthropogenic Hg pollution), while this will be higher if they emerge from the latsols and red
and yellow soils which are naturally rich in Hg because of a geochemical anomaly. In other
words, the geogenic Hg in mineral layer of soil horizon seems to be for B. edulis an overriding
source of the element than the airborne Hg retained in organic layer above the mineral horizon.
The probable daily intake (PDI) of Hg with Boletus spp. in Yunnan
The Hg concentration in the caps and stipes of B. edulis ranged respectively from 0.16 to 2.2
mg kg-1 fresh product (fp) and 0.085 to 0.84 mg kg-1 fp (assuming moisture concentration of
90%), while for a whole set of mushrooms of genus Boletus in this study data were more
heterogeneous, i.e. from 0.013 to 2.2 mg kg-1 fp in caps and from 0.022 to 0.84 mg kg-1 fp in stipes.
Based on these figures, popularity of Boletus mushrooms in Yunnan and assessed consumption
rate by adult (60 kg body mass) as 100 g of fresh caps per meal taken up to three times in a
week in the mushrooming season and no Hg intake from other sources, the probable dietary
intake of Hg is estimated at between 0.016 and 0.22 mg (0.00027 and 0.0037 mg kg-1 bm) with
one meal composed of 100 g of caps of B. edulis and at between 0.048 and 0.66 mg (0.00081
and 0.011 mg kg-1 bm) with three meals in a week.
13 / 19
Fig 2. Relationships between Hg concentration in the caps (y = 2.2142 + 6.4298 * x; r = 0.9229; p < 0.0001; r2 = 0.8517) and stipes (y = 0.9553
+ 2.7493 * x; r = 0.8907; p < 0.0001; r2 = 0.7933) of the fruiting bodies of B. edulis from the Yunnan Province and soil beneath the fruiting bodies.
The body mass proportion between cap and stipe of an individual fruiting body of B. edulis
changes when it becomes matured with cap getting bigger in mature specimens. People
foraging for Boletus mushrooms usually collect both young and small in size and mature fruiting
bodies. In an attempt aiming to assess probable dietary intake of Hg by individuals eating
Boletus mushrooms a proportion between body mass of cap to stipe as 1:1 was used.
The value of provisional tolerable weekly intake (PTWI) of Hg is 0.004 mg kg-1 bm [
The Hg intakes calculated for most of Boletus mushrooms in Yunnan were below the PTWI
and without health risk, while in a few samples were higher than the standard even if no intake
of Hg from other food is considered. Limited is knowledge on impact of cooking on behaviour
of Hg contained in fruiting bodies of mushrooms [
], and unknown is bio-availability
from a meal and bio-accessibility at a cellular level of Hg from edible mushrooms. This is
because of a limited knowledge on concentrations of ligands antagonistic to Hg, e.g. Se, S,
contained in fruiting bodies of mushrooms and on the molecular forms of Hg and Se and possible
effect by Se. Selenium is usually present in elevated concentration in the “real boletes”, i.e.
Boletus spp. [
], and which in fact efficiently bio-concentrate also Hg. Selenium can have a role
as an agent diminishing biological impacts by Hg [
] but is so far little studied or known in
case of mushrooms relatively rich in Hg.
14 / 19
Fig 3. Relationships between Hg concentration in the caps (y = 1.4106 + 5.7865 * x; r = 0.7769 p < 0.0001; r2 = 0.6036) and stipes (y = 0.8913
+ 2.4557 * x; r = 0.7312; p > 0.0001; r2 = 0.5346) of the fruiting bodies of Boletus spp. from the Yunnan and Sichuan Provinces and soil beneath the
Hg in 21 species of the fruiting bodies of Boletus from Yunnan was measured and Hg levels for
B. edulis were found to be elevated over the background levels. The majority of the species have
no previous data on Hg content in fruiting bodies from either China or elsewhere. There was a
highly significant correlation between Hg content of the caps (0.89; p <0.005) and stipes (0.92;
p< 0.005) of the fruiting bodies and Hg content of the soil substratum for Boletus edulis. Hg
content in the soils is elevated above National Background due to Yunnan being located in the
Circum-Pacific Global Mercuriferous Belt.
Conceived and designed the experiments: JF YZW TL. Performed the experiments: JF JZ MS
GK AW. Analyzed the data: JF. Contributed reagents/materials/analysis tools: JF YZW TL.
Wrote the paper: JF. Participated in manuscript preparation: JZ.
15 / 19
16 / 19
17 / 19
18 / 19
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