Gdynia, Poland
Lodz, Poland
Gdynia, Poland
Introduction. Contamination by radiocaesium of edible wild mushrooms after major nuclear accidents is a long-lasting process in some regions of the world. Following greater awareness of radioactive pollution in Asia, particularly after the Fukushima accident, this study investigated the radioactivity of 137Cs and 40K contamination in edible wild mushrooms in China. Study objects and methods. The objects of the research were edible wild mushrooms collected during 2014 to 2016, from the Inner Mongolian and Yunnan regions of China. To obtain an insight into any environmental impacts to distant regions of mainland Asia, the mushrooms were analyzed for 137Cs activity. In parallel, the natural activity of 40K was also determined and used to estimate the content of total K. The topsoil underneath the mushrooms was also investigated from a few sites in Bayanhushu in Inner Mongolia in 2015. Results and discussion. The results showed that in 4 to 6 mushrooming seasons after the accident, mushrooms from both regions were only slightly contaminated with 137Cs, which implied negligible consequences. The activity concentrations of 137Cs in dried caps and whole mushrooms in 63 of 70 lots from 26 locations were well below 20 Bq kg–1 dry weight. Two species (Lactarius hygrophoroides L. and Lactarius volemus L.), from Jiulongchi in Yuxi prefecture showed higher 137Cs activities, from 130 ± 5 to 210 ± 13 Bq kg–1 dw in the caps. 40K activities of mushrooms were around two- to three-fold higher. A composite sample of topsoil (0–10 cm layer) from the Bayanhushu site (altitude 920 m a.s.l.) in Inner Mongolia showed 137Cs activity concentration at a low level of 6.8 ± 0.7 Bq kg–1 dw, but it was relatively rich in potassium (40K of 595 ± 41 Bq kg–1 and total K of 17000 ± 1000 mg kg–1 dw). Conclusion. Wild mushrooms from the Yunnan and Inner Mongolia lands only slightly affected with radioactivity from artificial 137Cs. Lack of 134Cs showed negligible impact from Fukushima fallout. Ionizing radiation dose from 137Cs in potential meals was a fraction of 40K radioactivity. The associated dietary exposure to ionizing irradiation from 137Cs and 40K contained in mushrooms from the regions studied was considered negligible and low, respectively. Mushroom species examined in this study are a potentially good source of dietary potassium.
Asia, forest, fungi, pollution, soil, radioactivity, radiocaesium, wild food
INTRODUCTION
Radiocaesium (134/137Cs), if not mention the shortlived
radioactive 131I (t0.5 = 8.02 days), is the main mass
and a long-term source of the toxic radiation, polluting
the Earth in the past from the nuclear weapon explosions
and nuclear power plant accidents [1, 2].
Macromycetes (fungi) can accumulate various
elements in their fruiting bodies, including radioactive
isotopes (134Cs, 137Cs, 40K, 210Po, 210Pb, 238Pu, 239+240Pu,
90Sr, 230Th, 232Th, 234U, 238U) emitting radiation of
various toxicities [3–9]. Many wild fungi are effective
accumulators of artificial radioactive cesium, which
circulates in forest ecosystems for years in contaminated
areas and can cause a potential health hazard from
ingestion of the mushrooms [2, 10–14].
Radiocaesium (137Cs) is an artificial and long-lived
(t0.5 = 30.1 years) nuclide, which appeared in mushrooms
after global fallout from nuclear weapons detonations in
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the atmosphere. High levels of radioactivity reappeared
following the collapse of the Chernobyl nuclear power
plant in 1986, including massive levels of 134Cs and
137Cs emissions [15]. The consequent radioactive fallout
caused a long-lasting and substantial contamination
with 137Cs of forest ecosystems including mushrooms in
regions surrounding the collapsed plant, especially in
the Ukraine, Belarus and Russia, as well as elsewhere in
Europe [16–23].
As in Chernobyl, a similar accident occurred
in Japan in March 2011, where, following a major
earthquake, a 15-meter tsunami disabled the power
supply and cooling systems of three Fukushima Daiichi
nuclear power plant reactors. All three cores largely
melted in the first three days, caused radioactive
contamination of the environment on a large scale,
including high 137Cs pollution of fungi growing in the
region [24–26].
The nuclear accidents caused long-term psychosocial
consequences on exposed individuals. One of the
consequences was that big game and domesticated
ruminants that eat contaminated mushrooms could
be also heavily loaded with 137Cs [27–29]. In humans,
mushrooms can be also the most important exposure
route to 137Cs when there is elevated consumption of wild
species [30]. As mentioned, contamination by 137Cs after
the Chernobyl accident as well as atomic weapon testing
is a long-lasting process in some mushroom species even
collected relatively away from this source [12–14].
The contribution of the 137Cs fallout from the
Chernobyl accident to ecosystems in distant places like
the Japanese islands was considered small compared to
the previous global fallout [31]. The Chernobyl fallout
had also some impacts on continental Asia. In China,
soils (layer 0–10 cm) sampled from 56 sites in the Inner
Mongolia province in 1982–1987 showed 137Cs mean
activity concentration of 13.6 ± 6.6 Bq kg–1 dry weight
(dw) (from 5.8 ± 4.4 to 23.4 ± 13.4 Bq kg–1 dw) [32]. Soil
from Yunnan province was also contaminated, showing
activity of 6.2 ± 5.4 Bq kg–1 dw (from 1.9 ± 0.3 to
31.6 ± 0.8 Bq kg–1 dw) in 1982–1987 [33].
The accident in the Fukushima nuclear power plant
caused a high alert on a direct and indirect radioactive
pollution consequences regarding to exposed staff
and local residents. It affected public health and foods
safety in Japan, as well as continental Asia from
serious accidental discharge and included studies on the
consequence to various types of environmental media
including soils, vegetation and wild growing mushrooms
[25, 34–46].
Edible mushrooms collected from the wild are
common foodstuffs in Yunnan, a land diverse in
climate, soil, forest types and landscape topography and
with a high biodiversity of mushroom species [47, 48].
Certain species are conditionally edible or medicinal
mushrooms, e.g. Caloboletus calopus (Pers.) Vizzini
or Tricholoma sejunctum (Fr. ex Sow.) Quél. Inner
Mongolia has an area of 1 183 000 km2 (457 000 sq mi)
with a landscape made up largely of meadows with an
abundance of saprobic mushrooms. This region is poor
in ectomycorrhizal mushrooms, a result of the limited
wooded areas, apart from the thickets along the Huang
He River [49].
To get greater awareness of radioactive pollution in
Asia, particularly after the Fukushima accident, this
study investigated the radioactivity contamination with
137Cs and 40K of edible wild mushrooms from the Inner
Mongolian and Yunnan provinces of China. The activity
concentrations of 137Cs and 40K were studied for the
first time in wild mushrooms (five species) from Inner
Mongolia and also in more than 26 species, including
taxa without previous data on 137Cs, from Yunnan,
collected during 2014–2016.
STUDY OBJECTS AND METHODS
Mushroom and topsoil samples. Mushrooms
were collected from the Inner Mongolia province
(approximate distance from Fukushima Daiichi power
plant site is 2500 km). They all represented saprobic
species and included Agaricus arvensis Schaeff,
Calocybe gambosa (Fr.) Donk, Calvatia gigantea
(Batsch) Lloyd, Macrolepiota excoriata (Schaeff.)
Wasser and Lepista personata (Fr.:Fr) Sing. The 26
species collected from Yunnan province (distance
from Fukushima is in the range of 3500 to 4500 km)
included Auricularia delicata (Fr.) Henn, Baorangia
bicolor (Kuntze), Boletus bainiugan Dentinger, Boletus
ferrugineus Schaeff., Hemileccinum impolitum (Fr.)
Šutara, Boletus reticulatus Schaeff., Butyriboletus
roseoflavus, Boletus tomentipes Earle, Caloboletus
calopus (previous name Boletus calopus Fr.), Neoboletus
brunneissimus (W.F. Chiu), Retiboletus griseus (Frost),
Rubroboletus sinicus (W.F. Chiu), Sutorius magnificus
(W.F. Chiu), Sutorius obscureumbrinus (Hongo),
Laccaria vinaceoavellanea Hongo, Lactarius deliciosus
(L.:Fr.) Gray, Lactarius hatsudake Tanaka, Lactarius
hygrophoroides Berk. & M.A. Curtis, Lactarius
volemus Fr., Lentinula edodes (Berk.) Pegler, Leccinum
rugosiceps (Peck) Singer, Morchella esculenta Pers.,
Russula compacta Frost and Tricholoma sejunctum. The
L. edodes samples were taken from cultivars from the
Wuding in Chuxiong and Longyang in Baoshan from
Yunnan, while solely composite samples were from
Baise in Guangxi province and the Northeast of China.
Soil samples were collected in parallel as two
pooled samples of topsoil (0–10 cm layer) beneath the
fruiting bodies of A. arvensis from grassy stands in
the Bayanhushu site in Inner Mongolia. Details of the
geographical locations of the sampling sites from which
mushrooms and topsoil were collected are given in Fig. 1
and Table 1.
Preparation of materials. To examine the
distribution of 137Cs and 40K and total K between the
morphological parts, individual fruiting bodies were
rinsed and separated into caps (with skin) and stipes,
but some were examined as whole (Table 1). Before
drying, the fungal materials were sliced into pieces
using a ceramic knife and pooled to create composite
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samples representing each species, sampling location
and time of collection. Mushroom parts were dried
at 65°C to constant mass (Ultra FD1000 dehydrator,
Ezidri, Australia), finely powdered in a porcelain mortar,
passed through an 80-mesh sieve, and stored in screw
sealed plastic (low density polyethylene) bags under dry
conditions.
Two pooled samples of topsoil (0–10 cm layer; 150 g
whole weight each) were cleaned from any visible
pebbles, leaves and twigs, soil samples, air dried
under clean condition, ground (porcelain mortar),
sieved (2 mm mesh plastic sieve), and stored in sealed
polyethylene bags.
Directly before analysis, the mushroom and soil
materials were prophylactically deep frozen and
lyophilized (Labconco Freeze Dry System, Kansas City,
MO, USA) for three days to ensure full dehydration.
Instrumental analysis. The analytical methodology
applied has been presented in detail before [43, 67,
68] but a summarized description is given below. In
brief, activity concentrations of 137Cs, 134Cs and 40K
were measured using a γ-spectrometer with a coaxial
HPGe detector with a relative efficiency of 18% and
a resolution of 1.9 keV at 1.332 MeV of 60Co (with
associated electronics) (Detector GC 1819 7500 SL,
Canberra Packard, Poland, Warsaw). The measurements
of the fungal materials in this study were preceded by
Figure 1 Localization of the sampling sites of mushrooms from the Inner Mongolia and Yunnan provinces in China
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Table 1 137Cs and 40K activity concentration (± an instrumental counting error) and estimated K in mushrooms collected from
the provinces of China
137Cs (Bq kg–1 dw) 40K (Bq kg–1 dw) K (g kg–1 dw)
(Whole sporocarps) (Whole sporocarps) (Whole sporocarps)
Province and species Location Year n# Caps Stipes Caps Stipes Caps Stipes
Inner Mongolia province Xilin Gol League
Agaricus arvensis West Ujimqin [1]* 2015 80 < 8.7 19 ± 4 2100 ± 240 1700 ± 250 72 ± 8 58 ± 8
A. arvensis Bayanhushu [2] 2015 60 7.2 ± 1.7 7.6 ± 1.7 875 ± 140 1100 ± 140 30 ± 1 37 ± 5
A. arvensis Bayanhushu [2] 2014 60 < 4.1 < 7.1 1500 ± 190 1100 ± 180 51 ± 6 37 ± 6
Calocybe gambosa Jinhe [3] 2015 14 9.7 ± 1.7 12 ± 2 1250 ± 100 1200 ± 120 43 ± 3 41 ± 4
Calvatia gigantea Bayanhushu [2] 2015 4 (10 ± 2) (1400 ± 170) (41 ± 5)
Macrolepiota excoriata Bayanhushu [2] 2015 2 15 ± 4 < 23 1600 ± 320 1400 ± 620 55 ± 11 48 ± 21
Lepista personata Baiyinhua [4] 2015 10 < 8.7 19 ± 4 1400 ± 93 1300 ± 110 48 ± 3 44 ± 4
L. personata Jinshan [5] 2015 10 6.4 ± 1.4 < 4.1 1200 ± 100 1200 ± 110 41 ± 3 41 ± 4
Yunnan province
Auricularia delicate Meng’a, Xishuangbanna [6] 2016 7 (< 1.4) (540 ± 61) (16 ± 2)
Baorangia bicolor Mojiang, Pu’er [7] 2015 5 4.9 ± 4.7 WD 1000 ± 200 WD 29 ± 6 WD
B. bicolor Yuxi [8] 2015 11 (< 3.6) (900 ± 100) (26 ± 3)
Boletus bainiugan Ning’er, Pu’er [9] 2016 5 < 2.8 2.7 ± 0.9 870 ± 88 520 ± 68 25 ± 3 15 ± 2
B. bainiugan Jiuxi, Yuxi [10] 2015 17 6.1 ± 1.2 6.6 ± 1.1 WD WD WD WD
B. bainiugan Dayingjie, Yuxi [11] 2015 12 < 2.9 WD 810 ± 76 WD 24 ± 2 WD
B. bainiugan Ning’er, Pu’er [9] 2016 30 5.3 ± 1.1 < 2.5 780 ± 89 690 ± 66 27 ± 3 24 ± 2
Boletus ferrugineus Midu, Dali [13] 2016 10 17 ± 1 13 ± 1 730 ± 85 600 ± 74 21 ± 2 18 ± 2
Boletus impolitus Jiuxi, Yuxi [10] 2016 2 41 ± 3 9.5 ± 1.8 1000 ± 130 910 ± 120 29 ± 4 27 ± 3
Boletus reticulatus Jiuxi, Yuxi [10] 2015 1 21 ± 6 < 3.1 1500 ± 440 2000 ± 850 44 ± 13 59 ± 25
Boletus speciosus Yuxi [8] 2015 7 (5.0 ± 1.1) (720 ± 74) (21 ± 2)
Boletus tomentipes Yuxi [8] 2015 12 (69 ± 4) (1300 ± 210) (38 ± 6)
B. tomentipes Hongta, Yuxi [12] 2015 7 35 ± 9 < 19 4000 ± 680 1800 ± 520 120 ± 20 53 ± 15
Caloboletus calopus Jiuxi,Yuxi [10] 2015 12 < 4.2 WD 960 ± 110 WD 33 ± 4 WD
C. calopus Hongta, Yuxi [12] 2015 10 9.8 ± 1.8 WD 1000 ± 110 WD 29 ± 3 WD
C. calopus Midu, Dali [13] 2015 11 7.2 ± 1.3 3.2 ± 1.2 640 ± 95 380 ± 78 19 ± 3 11 ± 2
Neoboletus brunneissimus Yuxi [8] 2015 11 (< 3.6) (1000 ± 95) (29 ± 3)
N. brunneissimus Midu, Dali [13] 2015 9 5.7 ± 1.3 9.6 ± 1.5 940 ± 87 960 ± 91 28 ± 3 28 ± 3
Retiboletus griseus Yuxi [8] 2015 10 (4.3 ± 1.4) (1400 ± 94) 41 ± 3
R. griseus Luohe, Yuxi [14] 2016 7 9.7 ± 2.7 < 5.4 1300 ± 250 950 ± 140 38 ± 7 28 ± 4
R. griseus Midu, Dali [13] 2015 14 9.4 ± 1.3 < 2.6 1100 ± 81 940 ± 73 32 ± 2 28 ± 2
Rubroboletus sinicus Jiuxi, Yuxi [13] 2015 9 < 6.2 13 ± 2 1100 ± 160 750 ± 140 37 ± 5 26 ± 5
R. sinicus Yuxi [8] 2015 11 < 4.9 WD 1100 ± 140 WD 33 ± 3 WD
R. sinicus Jiuxi, Yuxi [10] 2015 9 2.4 ± 0.3 WD 1000 ± 90 WD 32 ± 4 WD
Sutorius magnificus Dayingjie, Yuxi [11] 2016 7 18 ± 2 45 ± 3 1300 ± 120 1000 ± 120 38 ± 3 29 ± 3
Sutorius obscureumbrinus Yuxi [8] 2015 12 (3.9 ± 3.7) (1200 ± 130) (35 ± 4)
S. obscureumbrinus Gasa, Xishuangbanna [15] 2016 16 < 2.7 3.0 ± 0.7 1300 ± 100 975 ± 74 45 ± 4 33 ± 3
Laccaria vinaceoavellanea Baoshan city, Baoshan [16] 2016 7 (< 3.2) (1200 ± 93) (35 ± 3)
Lactarius deliciosus Zhengyuan, Pu’er [17] 2014 5 < 5.3 < 10 800 ± 150 1100 ± 290 23 ± 4 32 ± 8
L. deliciosus Lianhuachi, Yuxi [18] 2016 20 8.1 ± 1.6 17 ± 2 580 ± 110 720 ± 140 17 ± 3 21 ± 4
Lactarius hatsudake Lianhuachi, Yuxi [18] 2016 10 6.2 ± 1.3 15 ± 3 830 ± 80 710 ± 210 24 ± 2 21 ± 6
L. hatsudake Lianhuachi, Yuxi [18] 2016 4 12 ± 3 20 ± 5 1000 ± 160 1100 ± 350 29 ± 5 32 ± 10
Lactarius hygrophroides Lianhuachi, Yuxi [18] 2016 2 < 19 WD 1500 ± 64 WD 44 ± 2 WD
L. hygrophroides Lianhuachi, Yuxi [18] 2016 6 < 5.0 29 ± 7 1200 ± 140 1400 ± 500 35 ± 4 41 ± 15
L. hygrophroides Jiulongchi, Yuxi [19] 2016 9 130 ± 5 60 ± 5 920 ± 150 1300 ± 260 27 ± 4 38 ± 8
Lactarius volemus Jiulongchi, Yuxi [19] 2016 17 210 ± 13 67 ± 7 1000 ± 99 760 ± 97 30 ± 23 22 ± 3
L. volemus Yongping, Dali [20] 2016 8 < 3.5 6.1 ± 1.6 920 ± 100 830 ± 102 31 ± 3 28 ± 3
Lentinus edodes Wuding, Chuxiong [21] 2015 70 5.2 ± 1.4 12 ± 3 810 ± 110 910 ± 270 24 ± 3 27 ± 8
L. edodes Longyang, Baoshan [22] 2015 100 12 ± 2 22 ± 4 1200 ± 140 1100 ± 240 35 ± 4 32 ± 7
Lentinula edodes Northeast of China 2016 30+ 5.3 ± 1.4 4.5 ± 1.2 880 ± 110 640 ± 88 26 ± 3 19 ± 3
L. edodes Baise, Guangxi province [23] 2016 30+ 6.9 ± 1.7 < 3.6 790 ± 110 690 ± 82 23 ± 3 20 ± 2
Leccinum rugosiceps Ning’er, Pu’er [9] 2016 30 6.3 ± 1.1 4.0 ± 0.8 815 ± 84 781 ± 90 27 ± 3 27 ± 3
Morchella esculenta Midu, Dali [13] 2016 30 (< 3.4) (1200 ± 140) (35 ± 4)
Russula compacta Midu, Dali [13] 2016 5 (4.6 ± 1.0) (940 ± 80) (28 ± 2)
Boletus sp. Baoshan city, Baoshan [16] 2016 5 8.3 ± 1.4 9.3 ± 1.5 WD WD WD WD
Boletus sp. Midu, Dali [13] 2016 7 5.2 ± 1.2 1000 ± 83 29 ± 2
Boletus sp. Midu, Dali [13] 2016 6 5.9 ± 1.2 1200 ± 92 35 ± 3
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Boletus sp. Baoshan city, Baoshan [16] 2016 9 9.0 ± 1.2 690 ± 78 20 ± 2
Boletus sp. Baoshan city, Baoshan [16] 2016 5 < 2.7 3.0 ± 0.7 1300 ± 100 975 ± 74 39 ± 3 29 ± 2
Boletus sp. Midu, Dali [13] 2016 6 7.7 ± 1.7 1100 ± 130 32 ± 4
Boletus sp. Changning, Baoshan [24] 2016 5 5.7 ± 1.4 860 ± 98 25 ± 3
Boletus sp. Baoshan city, Baoshan [16] 2016 7 9.6 ± 1.4 760 ± 96 22 ± 3
Boletus sp. Baoshan city, Baoshan [16] 2016 6 < 4.1 780 ± 110 23 ± 3
Boletus sp. Changning, Baoshan [24] 2016 7 9.6 ± 2.2 1100 ± 150 32 ± 4
Boletus sp. Baoshan city, Baoshan [16] 2016 5 7.9 ± 1.4 790 ± 100 23 ± 3
Boletus sp. Midu, Dali [13] 2016 6 6.0 ± 1.5 1100 ± 120 32 ± 3
Boletus sp. Changning, Baoshan [24] 2016 6 4.4 ± 0.9 960 ± 73 28 ± 2
Boletus sp. Changning, Baoshan [24] 2016 5 7.4 ±1.4 810 ± 93 24 ± 3
Boletus sp. Changning, Baoshan [24] 2016 7 18 ± 2 990 ± 97 29 ± 3
Tricholoma sejunctum Liqi, Yuxi [25] 2016 14 7.7 ± 2.0 6.3 ± 2.0 1400 ± 140 1700 ± 170 41 ± 4 50 ± 5
T. sejunctum Yiwanshui, Yuxi [26] 2016 20 9.0 ± 1.4 23 ± 1 1400 ± 92 1200 ± 79 41 ± 3 35 ± 2
T. sejunctum Lianhuachi, Yuxi [18] 2016 5 20 ± 3 15 ± 4 2000 ± 270 1900 ± 340 59 ± 8 56 ± 10
*ID of the sampling site (see also in Fig. 1); #Quantity of specimens (fruit bodies) in a pool; WD – without data
background measurement (time 80 000 s) and counting
time was similar (> 22 h).
The instrument was calibrated using a multiisotope
standard by validated methodology. The
reference solution (Standard solution of gamma emitting
isotopes, code BW/Z-63/48/16), obtained from the IBJŚwierk
near Otwock in Poland, was used to prepare
reference samples for equipment calibration. The
radionuclides used in the reference solution during
equipment calibration were 241Am (1.2%), 109Cd (2.1%),
57Co (0.80%), 51Cr (1.55%), 113Sn (2.0%), 85Sr (1.2%),
137Cs (1.5%), 54Mn (1.55%), 65Zn (1.2%) and 60Co
(0.8%). The same geometry of cylindrical dishes with a
40-mm diameter was used for the analysis of the fungal
material extracts as well as for the reference samples
during equipment calibration organized by IAEARML-
2018-01. Detailed results of the intercalibration are
available in the publication [50].
Minimum detectable activity was determined
by the Currie method. This method is based on two
basic parameters: (a) critical level, which is defined
as a level below which the detection signal cannot be
reliably recognized and (b) detection limit specifying
the smallest signal that can be quantitatively reliable.
The measurement results obtained were recalculated
for dehydrated materials and decay corrected back to
the time of collection. Total potassium content was
calculated from the original 40K activity concentration
data (using mean value of 29.32 Bq g–1) in natural K,
which is in the range from 27.33 to 31.31 Bq g–1 of K
(percentage abundance of 40K atoms in natural K is
0.0117%) [51].
RESULTS AND DISCUSSION
137Cs and 134Cs in mushrooms and soil. All species
collected from Inner Mongolia in this study were
saprobic. 134Cs activity was not detected in any of the
study samples. It was possibly due to the negligible
impact from the Fukushima’s fallout in 2011 as wells as
a relatively short half-life of this isotope (t0.5 = 2.1 years)
and small impacts from the Chernobyl’s fallout in 1986
and preceding, the nuclear weapons detonations in the
atmosphere.
The values of the activity concentration of 137Cs
in caps and stipes of the fruiting bodies of Agaricus
arvensis, Calocybe gambosa, Lepista personata and
Macrolepiota excoriata and in the whole fruiting
bodies of C. gigantea were in the range from < 4.1 to
19 ± 4 Bq kg–1 dw (Table 1). There is no prior data
for these species from regions of Asia other than
Inner Mongolia [44, 53, 54]. The low levels of 137Cs
contamination in the studied mushrooms from the Inner
Mongolian region reflects low activities of this nuclide in
local soils as well as a lower potential of these species to
bio-accumulate this nuclide.
In this study, a composite sample of the upper
(0–10 cm) layer of soil collected in parallel with
A. arvensis from the Bayanhushu site (altitude 920
m a.s.l.) showed 137Cs activity concentration of
6.8 ± 0.7 Bq kg–1 dw. This result obtained for the sample
from 2015 is around 2 to 4-fold lower than earlier results
cited for topsoils collected in Inner Mongolia in 1982–
1987, and is close to the activity values reported in
1–5 cm layer of forest topsoils sampled from the
Changning and Mengman sites in Yunnan in 2016
(4.9 ± 0.6 and 7.5 ± 0.7 Bq kg–1 dw) [53].
Because of colder weather in the mountains,
soil and the mushrooms can be specifically affected
with radiocaesium, which is scavenged from the
contaminated plumes by wet precipitation [53–55].
Forest topsoil collected at 3000 m above sea level from
the Minya Konka (Gongga Shan) mountain in Sichuan
province of China in 2012 showed 137Cs at level from
41 ± 1 to 79 ± 2 Bq kg–1 dw. This result is well in excess
137Cs (Bq kg–1 dw) 40K (Bq kg–1 dw) K (g kg–1 dw)
(Whole sporocarps) (Whole sporocarps) (Whole sporocarps)
Province and species Location Year n# Caps Stipes Caps Stipes Caps Stipes
Continuation of the Table 1
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of what has been noted in topsoil from Inner Mongolia
in this study or other studies of soils from China [32,
33, 53].
As given in Table 1, the determined activity
concentrations of 137Cs in fruiting bodies of the saprobic
and perhaps a little parasitic species of Auricularia
delicate, the caps and stipes of fruiting bodies of the
saprobic decomposer Lentinula edodes, the saprobic
Morchella esculenta as well as over 20 species of
mycorrhizal mushrooms collected in Yunnan were low
and roughly in the range of values noted in mushrooms
from Inner Mongolia.
The only exception was individuals of Lactarius
hygrophoroides collected from the region of Jiulongchi
in Yuxi prefecture in central Yunnan in the summer of
2016. They showed activity concentrations of 137Cs from
130 ± 5 to 210 ± 13 Bq kg dw–1 in caps and from 60 ± 5
to 67 ± 7 Bq kg dw–1 in stipes (Table 1). These relatively
high levels of 137Cs activity in L. hygrophoroides
from the Jiulongchi site were in the range of
activities determined previously in several species
of ectomycorrhizal mushrooms collected at 2900–
3600 m above sea level from the Minya Konka summit
in 2012 [53].
Many other species of mushrooms collected from
the prefecture of Yuxi and across other regions from
Yunnan and elsewhere in China (Zhangzhou in the
Fujian province) in 2010‒2018 were substantially
less contaminated than L. hygrophoroides from the
Jiulongchi site or even mushrooms from the subalpine
regions on the eastern slope of the Minya Konka summit
[12, 16, 42, 44, 47, 52, 53, 56]. The exception was
Turbinellus floccosus (Schwein.) Earle ex Giachini &
Castellano [previous name Gomphus floccosus (Schw.)
Singer] collected from the region of Mangshi (98°24’ E,
24°22’ N) in the western part of Yunnan during August
2012 to July 2013, which showed a 137Cs activity
concentration of 212 (148–339) Bq kg–1 dw in the whole
fruiting bodies [44, 57].
Elevated activity concentrations of 137Cs in
L. hygrophoroides from the Jiulongchi site in this
study can possibly be explained by weather conditions
(episodic rain) scavenging nuclides from the radioactive
plume after the Fukushima (Japan) nuclear power plant
accident in early 2011.
The radioactive incident took place in Tongchuan,
Shaanxi Province, south of the central region of Inner
Mongolia (approximate distance from the sampling
sites mushrooms there is 1200 km). Some 137Cs from a
measuring instrument (lead ball – a major component of
a nuclear scale) when dismantling a cement factory has
gone missing. In a later investigation, radioactivity from
137Cs was found at a steel refinery in Shaanxi’s Fuping
county. Possibly, a lead ball with scrap metal was melted
down into the steel [58]. Information on possible, if any,
ground pollution in the region from this accident is not
available.
A recent (2021) study showed that the activity
concentration of 137Cs in 66 out of 68 of wild mushrooms
(17 species) collected from the northeast regions of
China in 2017‒2020 ranged from < 0.6 to 26 Bq kg–1 dw
(data rounded), and only in single Lactarius deliciosus
and Lepista nuda (Bull.) Cooke specimens collected in
2020, was 46 ± 3 Bq kg–1 dw and 130 ± 9 Bq kg–1 dw,
respectively [59].
The maximum activity concentration of 137Cs noted
in L. nuda in the above mentioned study was close to
values determined in Lactarius hygrophroides and
Lactarius volemus from Jiulongchi, Yuxi (Yunnan)
(Table 1), while the results are not very comparable
due to only two single specimens examined by Wang
et al. [59].
The radiocaesium contamination of land, the oceans
and biota, including edible wild growing mushrooms
has thus far, occurred in three main waves. The first
one arose from the nuclear weapons detonations in
the atmosphere in the period from 1945 to 1980 and
resulted in wide-spread aerial diffusion of radiocaesium
and other nuclides including 14C, 137Cs, 90Sr, 239–240Pu,
241Am and 3H [60]. With time, the resulting depositions
of longer lasting 137Cs affected every region of the
world [1, 60].
Data on radiocaesium in mushrooms for the
period before 1986 is scarce [10–13, 42, 61]. Fifteen
years before the Chernobyl accident, a solely
fruiting body of Tricholoma terreum collected
from the Czech Republic in 1971 showed 137Cs at
a level of 40 Bq kg–1 dw [61]. Additional historical
data on 137Cs in mushrooms was recorded in 1984,
in Poland for the Poison Pax (Paxillus involutus),
which showed 137Cs at a level of 2700 Bq kg–1 dw,
with lower levels noted for the King Bolete (Boletus
edulis) (95 and 104 Bq kg–1 dw) and Slippery Jack,
Suillus luteus (125 and 150 Bq kg–1 dw) collected in 1984
and 1985, respectively [10].
Data on the radiocaesium concentration activities
accumulated in wild mushrooms growing in Asia from
the period before the Chernobyl accident are absent in
the available literature. Effectively, there is also nothing
published on radiocaesium in wild mushrooms from
mainland Asia in the period between the Chernobyl and
Fukushima incidents.
The Chernobyl emission of radioactivity caused
an extreme and long-lasting radiocaesium pollution
of wild growing mushrooms in the regions of Europe,
and particularly in the neighbor areas collapsed
nuclear power plant [12, 16, 17, 62–65]. Japanese
researchers have published a large volume of data on
artificial radioactivity accumulated in wild mushrooms
growing in the country, both from the post-Chernobyl
and post-Fukushima emissions, which have recently
been evaluated by Komatsu et al. and Prand-Stritzko
and Steinhauser [25, 66]. The activity in these wild
mushrooms collected in the period up to March 2011
was largely from accumulated radiocaesium (137Cs) due
to the global fallout from nuclear weapons detonations,
with a small proportion being attributed to the
Chernobyl emissions [54]. The more recent emissions
92
Saniewski M. et al. Foods and Raw Materials, 2022, vol. 10, no. 1, pp. 86–96
from the Fukushima incident changed the pattern of
radionuclide contamination of wild mushrooms in Japan.
However, as shown in this study (Table 1) and in a few
other reports, the emissions could have only a small
impact on mainland Asia or elsewhere [44, 53, 68–69].
40K and K in mushrooms and soil. The topsoil from
the Bayanhushu site showed 40K activity concentration
of 595 ± 41 Bq kg–1 dw and total K content of 17 000 ±
1000 mg kg–1 dw, which were higher than previously
determined in topsoils sampled from several forested
areas in Yunnan (150 ± 14 to 340 ± 19 Bq kg–1 dw) [53].
In the study by Zhang et al., the means of 40K
activity concentrations in topsoils (0–10 cm) in
Inner Mongolia and Yunnan in 1982–1987 were
755 (866–1066 Bq kg–1 dw) and 487 Bq kg–1 dw
(149–1010 Bq kg–1 dw), respectively [70]. In another
national survey performed during 1983–1990, the
area-weighted mean and the point-weighted mean of
40K were 655.6 and 624.6 Bq kg–1 dw, respectively,
for soils in Inner Mongolia, while the two values for
soils from Yunnan were 532.0 and 518.6 Bq kg–1 dw,
respectively [71].
The activity concentrations of 40K in mushrooms
from Inner Mongolia were in the range of 875 ± 140 to
1600 ± 320 Bq kg–1 dw in caps and from 1100 ± 180 to
1400 ± 620 Bq kg–1 dw in stipes (Table 1). In the case
of mushrooms from Yunnan, A. delicate (ear-like
jelly fungus), which grows on wood, they had a lower
activity concentration of 40K (540 ± 61 Bq kg–1 dw)
than L. edodes (Table 1), which also grows on wood.
The L. edodes showed activities in the range of
790 ± 110 to 1200 ± 140 Bq kg–1 dw in the caps,
which are culinary valued, and from 640 ± 88 to
1100 ± 240 Bq kg–1 dw in the stipes, which are largely
discarded. This species collected from Yunnan
and examined by other authors, demonstrated the
mean value of 40K activity concentration to be
629 Bq kg–1 dw (from 396 to 1010 Bq kg–1 dw; n = 11)
[44]. 40K values in the caps of terrestrial mushrooms
from Yunnan were from 580 ± 110 Bq kg–1 dw in
L. deliciosus to 4000 ± 680 Bq kg–1 dw in Boletus
tomentipes, while stipes showed activities from 380 ±
78 Bq kg–1 dw in L. deliciosus to 1900 ± 340 Bq kg–1 dw
in Tricholoma sejunctum.
Potassium (total K) is the major metallic element
in mushrooms and occurs in dried fungal materials in
quantities of up to several percent, while the natural
nuclide 40K forms only a small proportion (makes up
0.012%) of the total. Hence, mushrooms collected from
areas that are only mildly affected by 137Cs depositions
or mushrooms without a high species-specific ability to
bioconcentrate this nuclide, e.g. like some species from
the genus Cortinarius, contained natural 40K in high
excess relative to 137Cs (Table 1) [12].
The amounts of K in the caps, stipes, or whole
fruiting bodies of the species in this study were
in the range 16 000 to 120 000 mg kg–1 dw (1.6 to
12 g kg–1 dw). Potassium is indispensable for
mushrooms, for the uptake and osmotic regulation
of water in the cytoplasm of cells and is a co-factor in
certain enzymes [72]. However, the same species, i.e.
A. arvensis, Boletus bainiugan, Retiboletus griseus,
Rubroboletus sinicus, Caloboletus calopus, L. hygrophoroides,
L. edodes and T. sejunctum collected from
different sites could differ around twofold in the content
of K (Table 1).
The daily adequate intake of K for adults is 2300 mg
for females and 3400 mg for males [73]. Thus, the
mushroom species examined in this study and assuming
absorption rate at around 90% could be considered as
potentially good sources of dietary potassium, especially
when stir-fried with oil, which is a common culinary
technique in SW China [67].
Potential risk from ionizing radiation doses. In
this study, a total of 70 lots of several species of edible
mushrooms collected from 26 locations in Yunnan
were examined and in 63 lots, the contamination
with 137Cs of the caps or the whole mushrooms was
well below 20 Bq kg–1 dw (Table 1). There were
three of 70 lots that were more contaminated with
137Cs than the others. Those lots were the gilled
mushroom B. tomentipes (of 69 ± 4 Bq kg–1 dw),
caps of the lamellar mushroom L. hygrophoroides
(130 ± 5 Bq kg–1 dw), and caps of lamellar L. volemus
(210 ± 13 Bq kg–1 dw) (Table 1). Assuming that the
moisture content in fruiting bodies is 90%, the estimated
137Cs activities in these three species were 6.9, 13, and
21 Bq kg–1 on a wet weight basis. Therefore, these
amounts were much lower than the maximum permitted
levels for import of mushrooms from third countries
[specific 13 countries affected by the Chernobyl’s
radioactive fallout for which the regulation applies] to
the European Union (600 Bq kg–1) [74].
In Yunnan, the main way to cook mushrooms is stirfrying
in vegetable oil in a wok pan [75]. It is interesting
that stir-fried mushroom meals showed about 2 to 5-fold
higher activity concentrations of 137Cs than the raw
mushrooms on a whole weight (wet) basis [67, 68].
Therefore, a 100-g portion of stir-fried L. volemus
caps from the most contaminated lot in this study
could include from 4.2 to 10.5 Bq of 137Cs (equivalent to
ionizing radiation dose from 56×10–3 to 140×10–3 μSv per
capita or 0.49×10–3 to 2.35×10–3 μSv per kg body mass;
60 kg body mass). These estimates are low, taking into
account the risk associated with the doses of ionizing
radiation received by consumers in Yunnan, even if stirfried
mushrooms are consumed daily for longer periods
during the mushrooming season.
In comparison, the natural 40K nuclide contained
in mushrooms (Table 1) introduces much higher doses
of ionizing radiation than 137Cs for locals in Inner
Mongolia and Yunnan provinces but is not considered as
a hazardous nuclide for consumers due to homeostasis of
K in human body.
CONCLUSION
The activity concentrations of 137Cs in lamellar
mushrooms from the Inner Mongolia province of China
and the local soil were low. 137Cs contamination of the
lamellar and gilled mushrooms from Yunnan province in
China was also low, i.e. well below one tenth of statutory
limits, and mushroom meals there can be considered as a
negligible source of 137Cs for their consumers.
In view of the results from this study, the accident
in the Fukushima nuclear power plant had little or
negligible effect on radioactive contamination of edible
and medicinal fungi in the regions of China. Natural
nuclide 40K contained in mushrooms is not considered
as hazardous for mushroom meal consumers. Wild
mushrooms can be considered as a good source of
dietary potassium for consumers.
CONTRIBUTION
Michał Saniewski: resources, methodology,
investigation, validation, data curation and analysis,
writing – review & editing. Jerzy Falandysz:
conceptualization, resources, investigation, formal
analysis, data curation, graphics, supervision, writing –
original draft, writing – review & editing. Tamara
Zalewska: resources, methodology, investigation,
validation, data curation and analysis.
CONFLICT OF INTEREST
The authors declare no conflict of interests regarding
the publication of this article.
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