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Radioactive Contamination of Ukrainian Mushrooms

Article in International Journal of Medicinal Mushrooms · January 2005


DOI: 10.1615/IntJMedMushr.v7.i3.490

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G.A. Grodzynska Sergey Syrchin


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Proceedings of the 7 International Conference on Mushroom Biology and Mushroom Products (ICMBMP7) 2011

RADIOACTIVE CONTAMINATION OF UKRAINIAN WILD-


GROWING MUSHROOMS

ANNA A. GRODZINSKAYA 1, SERGEY A. SYRCHIN 2, NIKOLAI D.


KUCHMA3, VIKTOR T. BILAY1

1- Departments of Phycology and Mycology, N.G. Kholodny Institute of Botany, NAS of Ukraine,
Tereshchenkivska Str., 2, Kyiv, 01601,
Ukraine,
agrodz@ukr.net
2- Departement of Physiology and Taxonomy of Micromycetes, D.K. Zabolotny Institute of
Microbiology and Virology, NAS of Ukraine,
Zabolotny Str. 20, Kyiv, Ukraine,
syrchin@ukr.net
3- Laboratory of Radioecological Monitoring of Institute of Agroecology, UAAS,
Metrologichna Str.12, 03143, Kyiv,
Ukraine

ABSTRACT

By the activity of accumulated radiocaesium mushrooms, especially mycosymbiotrophs,


prevail both plants and forest litter (which during the all post-Chornobyl period is the main
depot of radionuclides) by several to hundreds times. This fact allows to use species-
hyperaccumulators, for instance of radiocaesium, as bioindicators for radioactive
contaminated territories. They include certain representatives of Cortinariaceae, Russulaceae,
Boletaceae, Suillaceae, Hydnaceae, Paxillaceae, Tricholomataceae, Gomphidiaceae. Among
them, as widely spread edible species Boletus badius (Fr.) Kühn., and as common species
Lactarius rufus (Scop.) Fr. and Paxillus involutus (Batsch) Fr., not consumed by population
because of their inedibility and toxicity, had been recommended as most convenient objects
for long-term radioecological monitoring of contaminated territories of Ukrainian Polissya.
Accumulation of radiostrontium was in 10-102 times less than radiocesium. The use of
mushrooms-bioindicators let give the prognosis estimation of the situation with contamination
levels of soils, other wild-growing mushrooms and berries. At the same time it should be
noted that it’s not possible to use them for exact statistically reliable estimation of the
territories contamination levels taking into account the high level of variability observed even
in the samples of the same species in the same location.

Keywords: bioindication, 137Cs, 90Sr, the Chornobyl catastrophe.

INTRODUCTION
The Chornobyl catastrophe is unprecedented both by the territory of radioactive
contamination and by intensity of doses absorbed by biota objects. Even 25 years after the
accident radioactive contamination of mushrooms is quite significant, in some cases reaching
very high levels, and creates human health problems resulting from their nutritional and
medicinal use. The capacity of mushrooms to be concentrators of heavy metals and
radionuclides of natural and technogenous origin is well documented in special literature [1-
8]. A strong argument in favor of use of macromycetes as bioindicators is a clear prevailance
of radiocaesium contamination for the whole post-Chornobyl period in some macromycetes
species relative to forest litter (by several to hundreds times), which, in turn is the main

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Proceedings of the 7 International Conference on Mushroom Biology and Mushroom Products (ICMBMP7) 2011

radionuclides depot [9-11]. It must be noted that the radioactively polluted areas of Ukraine
are characterized by the mosaic pattern of contamination that complicates the estimation and
forecast of radionuclides uptake by biota objects. 137Cs (during the first post-catastrophe
period in combination with 134Cs) was confirmed to be the main doze-forming radionuclide
in the contaminated area, and that conditioned a priority given to the uptake of this element
by mushrooms. However, fruiting bodies having a high activity are only an insignificant part
of the total mycelial biomass which is situated in the organic soil layer. An essential
contribution of the macro-and micromycetes mycelia biomass and its ability to uptake and
retain radionuclides play a very important role in its migration and distribution processes.

MATERIALS AND METHODS


137
Cs activity in fruiting bodies of wild growing mushrooms (207 species) and substrates from
their habitats, collected in 1990-2010 at 159 locations of Kyiv (including the Chornobyl zone),
Chernihiv, Zhytomyr, Cherkassy, Volyn’, Rivne, Ivano-Frankivs’k, Poltava, L’viv, and
Zakarpattia regions of Ukraine have been studied using gamma-spectrometry. Some samples
were analyzed on 90Sr using radiochemical methods on the basis of the accumulation of 90Y.
Samples weighed from 1 to 200 g and had 3 to 30 fruiting bodies. Soil samples were taken at
the depth of 0-5 cm. Mushroom samples cleaned from soil and plant particles as well as
samples of soil (substrate) were dried at 40-50оС and ground to fine-dispersed condition. Then
they were dried at 80оС for 24 hours and placed in plastic Petri dishes, or plastic bags. The
counting time was 6-36 hours. Counting errors for the measurements of 137Cs were usually
lower than 20%. Average levels of soil surface contamination with 137Cs were defined during
field measurements, according to the maps presented in the National report [12], Atlas of
radioactive contamination of Ukraine and data in General dosimeter certification.

RESULTS AND DISCUSSIONS


Researches of radionuclide accumulation in mushrooms of Ukrainian Polissya which is the
most polluted region as a result of failure on Chornobyl Nuclear Power Plant (ChNPP) in 1986,
have shown that during all period after catastrophe mushrooms constantly demonstrated high
levels of radiocesium contamination. It is clear that mushrooms contamination levels is mainly
correlated with soil contamination levels. The maximum radiocaesium levels (up to millions Bq
per kg of dry weight) in species taken from the Chornobyl exclusion zone were observed in
mycosymbiotrophic species - P.involutus – 31 MBq/kg d.w.(Shepelychi forestry, 1996),
Boletus subtomentosus (L.) Quél.– 20 (Shepelychi forestry, 2004), Gomphidius glutinosus
(Schaeff.)Fr. – 17 ("Red"forest, 1993), Lactarius turpis (Weinm.) Fr. – 19 and Suillus luteus
(L.) Roussel – 15 (Kopachi, 2004), B. badius – 12 (“Red” forest, 1996), B. edulis Bull. - 11
MBq/ kg d.w. ( Janiv, 1998). In general, 90Sr uptake in wild-growing mushrooms is not as
intensive as that of radiocesium. Samples from that zone were shown have a ratio of 137Cs/90Sr
within the range 10-103 (mean - 102).
However, it is not the reason to ignore 90Sr, that element presenting a great danger for
the human organism. In cultivation condition it was shown increasing of radiostrontium
accumulation in edible and medicinal species such as Lentinula edodes (Berk.) Pegler and
Pleurotus ostreatus (Jacq.) Kumm. [13]. This phenomenon can be connected with higher
biological availability of 90Sr from mixed and watered substrates which are used in mushroom
industrial culture. It can be assumed that an increase of 90Sr activity in wood (observed last
years at the contaminated territories) will inevitable cause increase of its content especially in
lignotroph species. Therefore, the selective control of 90Sr accumulation in lignotrophs and
especially cultivated ones even at the areas with low surface soil contamination is strongly
recommended.

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Proceedings of the 7 International Conference on Mushroom Biology and Mushroom Products (ICMBMP7) 2011

The most numerous group of mushroom specimens was taken from region with the
surface contamination of 37 – 185 kBq/m2 (i.e.zone of an intensified radiation control).
Presently over 1.5 million people of Ukraine live at such contamination level [12]. Here,
despite the considerable variability of the obtained data, that is typical for radiobiological
research, quite high levels of radiocesium accumulation were observed. Coefficients of
accumulation (which are equal to the ratio between activity of radiocesium in mushrooms and
its activity in the substrate/soil in the location) reach tens, hundreds, and during the first post-
accident years even thousands. For instance, during the period from 2000 to 2005 the maximum
levels of radiocesium in the studied locations with this average levels of surface contamination
of soils with 137Cs have been observed in L. rufus – 375294 (vil.of Kolentzi), P. involutus –
282764 (vil.of Fenevychi), Cortinarius sp. – 269692 (vil. of Lutizh), Pluteus cervinus
(Schaeff.) P.Kumm.– 161643, B. badius - 120711, S. luteus – 117771 (near city of Ivankiv),
Hebeloma crustuliniforme (Bull.) Quél.– 100519 Bq/kg dry weight (settl.of Klavdievo-
Tarasove). High levels of radiocaesium uptake constantly were shown by B. badius from
different locations (Fig. 1). A considerable decrease in levels of radiocaesium was observed
only in drough-affected years. During all period of investigations accumulation of radiocesium
in wild growing mushrooms represents a damped wave process with rises in wet years and
lowest values in dry years.

Figure 1. Activity of 137Cs in fruiting bodies of B.badius from locations with average soil
surface contamination 37 – 185 kBq/m2 (I – city of Ivankiv, II – vil. of Shpyli, vil.of Lutizh,
Kyiv region).

The ratio 137Cs/90Sr was quite high (Fig.2).


On the whole, during the last years the levels of 137Cs contamination of up to 80% of
edible species samples (Boletus spp., Suillus spp., Leccinum spp., Cantharellus cibarius,
Lactarius deliciosus, Tricholoma spp. etc.) traditionally included into a diet of Slavic people
exceeded the maximum permissible norms accepted in Ukraine (2,5 kBq/kg d.w.).
At levels of 137Cs contamination ≤ 1 Сi/km2 in macromycetes also quite high level of
radiocaesium were observed.

Section: 563
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Proceedings of the 7 International Conference on Mushroom Biology and Mushroom Products (ICMBMP7) 2011

Figure 2. 137Cs and 90Sr activities in mushrooms in 2010 (vil.of Karpylivka, Chernihiv region).

Analysis of literature and our results of 1990-2010 monitoring allows concluding that
level of radionuclide accumulation in mushroom depends both on specific radioecological
situation in the area of mushroom sampling (quantitative and qualitative composition, forms of
radionuclides present in soil, moisture, pH, type of soil, climatic factors, landscape peculiarities
etc) and on mushroom species specificity, belonging to ecological trophic groups, depth of
mycelia location in soil. It must be noted that the tendency of increase of accumulation ability
in the sequence from lignotrophs →humus saprotrophs →litter saprotrophs
→mycosymbiotrophs, described earlier [9, 11] apparently concerns only the accumulation of
radiocesium. It is clear that in case of 90Sr this sequence will be of other kind.
In spite of positive correlation is marked between the level of contamination of soils,
humidity and level of contamination of mushrooms on the whole, mosaic pattern of
contamination of territory of Ukraine, complex of the controlled and non-controlled factors,
and especially extraordinarily high variability of mushrooms contamination levels (Table 1)
complicate the prognosis estimation of the dose loadings on the human as a result of
consumption of wild growing mushroom species.

Table 1. The estimation of variability of mushrooms contamination levels in 1990-2010

The average level of soil surface The range of mushrooms


contamination with 137Сs, kBq/m2 contamination with 137Cs, kBq/kg d.w.
3,7-18,5 BDL – 150
18,5-37 BDL – 300
37-185 BDL – 350
185-370 100 – 350
370-555 600 – 1 300
555 – 1480 4 000 – 17 000
>1480 Up to 32 000
BDL = below detection limit

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Proceedings of the 7 International Conference on Mushroom Biology and Mushroom Products (ICMBMP7) 2011

The conducted investigations on wild growing mushrooms of Ukrainian Polissya made


it possible to single out species with hyper-accumulative ability. Certain mycosymbiotrophic
representatives of families Cortinariaceae [Cortinarius spp., Rosites caperata (Pers.) P.Karst.,
Hebeloma crustuliniforme (Bull.) Quél.], Russulaceae (especially Lactarius spp.), Boletaceae
[Boletus spp., Leccinum scabrum (Bull.) Gray, Tylopilus felleus (Bull.) P.Karst.], Suillaceae
(Suillus spp.), Paxillaceae [Paxillus involutus (Batsch) Fr.], Hydnaceae [Sarcodon imbricatus
(L.) P.Karst., Hydnum repandum L.], Tricholomataceae [Tricholoma flavovirens
(Pers.)S.Lundell], Gomphidiaceae [Gomphidius glutinosus (Schaeff.) Fr. and G.rutilus
(Schaeff.) S.Lundell] have shown steadily high levels of contamination that makes it possible
to use them for bioindication purposes. Among them widely spread and common species in
Ukraine L.rufus and P.involutus may be regarded as the most convenient bioindicators since
inedibility of the first and toxicity of the second allow to reduce the influence of the
antropogenic factor in the estimation environmental radiocesium contamination. Use of B.
badius as the bioindicator is of some interest in terms of comparison with the data obtained for
other countries. The coefficients of accumulation of these three species reach tens and even
hundreds.
Mapping that involved bioindicative mushroom species (Figure 3) shows an evident
gradient of radioactive-induced contamination effects on mushroom fruiting bodies from
northern and northwest part to southern and central part of Kyiv region of Ukraine. Figures
show a coincidence, in general, of contamination intensity with the soil contamination levels
presented on maps published in the National report [12].

Figure 3. Mapping of Kyiv and part of Zhytomyr region with species-bioindicators.

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Proceedings of the 7 International Conference on Mushroom Biology and Mushroom Products (ICMBMP7) 2011

The use of selected mycoindicators is an express-technique that enable to assess and


extent of risk of mushroom consumption in that area, to forecast the development of situation
regarding contamination levels of soils, other wild-growing mushrooms and berries. At the
same time it should be noted that it is not possible to use them for exact statistically reliable
estimation of the territories contamination levels due to the high level of variability observed
even in the samples of the same species in the same location.
Literature data regarding a radioactive danger of mushrooms are numerous and as a
result it is quite natural to ask a question about the reasons of a mass character of wild-growing
mushrooms consumption by the population of Ukraine. In our opinion the reasons are several.
They lie in the traditional perception of «the gifts of forest», in lack or complete absence of
information concerning mushroom radioactive contamination in each area, in the syndrome of
«tiredness» of negative information published in mass media and in sense of being doomed that
in combination with a finance modest means of the majority of people living in the
contaminated areas form that vicious circle that is hard to get out from. It should be mentioned
that for some country people wild growing mushroom collection for sale forms a significant
part of their family’s budget. Thus, a specific scientific problem has deep social grounds.

CONCLUSIONS
The analysis of radiocesium accumulation dynamics in wild growing mushrooms gives
evidence of a long-term radiological risk resulting from their consumption as food and
medicine on the territory with 137Cs contamination more than 37 kBq/m2. It can be said that this
situation will remain dangerous for many years. In these conditions the only reasonable
alternative is to increase the industrial mushroom cultivation involving new perspectives with
species having high nutritional and medicinal properties on tested free from 137Cs and 90Sr
substrates.

ACKNOWLEDGEMENT
Authors express their gratitude to Professor Solomon P. Wasser (University of Haifa, Israel)
and Prof. Kurt Haselwandter (Institute of Microbiology, Innsbruck, Austria) for long-term
collaboration.

REFERENCES
[1] Grüter H. (1971). Radioactive fission product 137Cs in mushrooms in W.Germany during
1963-1970. Health Physics. 20: 655-656.
[2] Haselwandter K. & Berreck M. (1989). Accumulation of radiocaesium in fungi. In: Metal
ions in fungi. Pp 259-277, Winkelmann G. and Winge D.R., Eds. Marcel Dekker, N.Y., Basel,
Hong Kong.
[3] Fraiture A. et al. (1990) Interest of fungi as bioindicators of the radiocontamination in forest
ecosystems. In: G. Desmet, P. Nassimbeni, & M. Belli Eds. Transfer of radionuclides in
natural and semi-natural environments. Luxemburg: Elsevier Applied Science, pp 477-484.
[4] Wasser S.P., Grodzinskaya A.A. (1993). Content of radionuclides in macromycetes of
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[5] Mietelski J.W. et al. (1994). Radioactive contamination of Polish mushrooms. The Science
of the Total Environm. 157: 217-226.
[6] Yoshida S., Muramatsu Y. (1994). Accumulation of radiocaesium in basidiomycetes
collected from Japanese forests. Sci. Tot. Environ. 157: 197-205.

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Proceedings of the 7 International Conference on Mushroom Biology and Mushroom Products (ICMBMP7) 2011

[7] Kalač P. A Review of Edible Mushroom Radioactivity. (2001). Food Chemistry. 75: 29-35.
[8] Steiner M. et al. (2002). The role of fungi in the transfer and cycling of radionuclides in
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[9] Wasser S.P. et al. (1995). Accumulation of radionuclides by cryptogamic plants and higher
fungi of Ukraine (Eds.S.P.Wasser). Kyiv: 131 p. (in Ukr.)
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