Peculiarities of heavy metals’ accumulation by the fruit bodies of macromycetes in the conditions of the combined radiation and chemical contamination

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¹Bryansk state University named after academician I. G. Petrovsky

²Orel state University named after I. S. Turgenev

UCD 630.8 (581.19+574.3)

Peculiarities of heavy metals' accumulation by the fruit bodies of macromycetes in the conditions of the combined radiation and chemical contamination

¹Anishchenko L. N., Professor, doctor of agricultural Sciences

²Ladnova G. G., Professor, doctor in biology Sciences

²Frolova N.V., assistant professor, candidate in biology Sciences

Bryansk, Orel, Russian Federation

Introduction

Fungi like elements of supply chains provide biogeochemical migration of atoms including the dangerous substances - elements of the group of heavy metals (HM). It is known that fungi actively involve pollutants in migration processes, including radionuclides, HM [1, 2, 3].

It is noted that the absorption of pollutants in general is determined by the biological characteristics of macromycetes, the concentration of pollutants in the fruit bodies and mycelium is different when accounting for the dominance by weight of a vegetative body [4 - 6].

The dependence of radionuclide accumulation in different fractions of fungi depending on the type of soil, type of substrates populated by macromycetes and their morphological characteristics - osmotic method of absorbing substances, structure of hyphae, structure of cell wall, etc. has been defined [7-11].

The instability of holding radionuclides in the fruit bodies and mycelium of fungi, provided by the “aging” of pollutants, extreme variations in biomass fractions of macromycetes has been revealed [1, 3].

Intensively accumulating HM depending on the species, the macromycetes have an adverse effect on the biochemical apparatus. The concentration of HM in the majority of types of fungi is close to normal and only when exceeding the HM mobile forms in the substrates, the content of pollutants exceeds the background ones. The least concentration of HM is characteristic of saprotrophes, the highest is for symbiotrophes, however, these values vary geographically from the same species, depend on the age and the place of gathering of fruit bodies of macromycetes, so it is difficult to identify fungi-bioindicators in relation to HM [1, 2, 12-15].

HM as transboundary pollutants are chemically quite resistant, migrate in the soil and water profile and quickly integrate into the biological processes with the participation of macromycetes. According to the recommendations of the International programme on bio-indication, fungi are recommended to include into the monitoring of objects in the background and affected by the anthropogenic effects habitats [16]. Thus, identifying the fungi-bioindicators of HM in conditions of combined radiation-chemical contamination is a priority scientific and applied task which provides an analytical monitoring.

The aim of this work is to present the characteristics of macromycetes fruit bodies' absorption and accumulation of the elements of the group of heavy metals on the territory of the combined radiation-chemical contamination (on the example of forest habitats in the Dyatkovo district of the Bryansk region). In the course of achieving the aim the following tasks were being solved: the sampling of fruit bodies of the background species of macromycetes in habitats of combined radiation and chemical contamination; the determination of gross concentrations of metals in fruit bodies; the estimation of parameters of HM accumulation in various species of fungi; the identification of species-indicators of pollution.

Materials, methods, techniques and objects of the research

The Dyatkovo district of the Bryansk region is the most contaminated in chemical terms in connection with the largest source of emissions (OJSC “Maltsovsky Portlandcement”) and also with the density of radioactive contamination up to 10 Ci/km² [17].

In the selected area of the forest the ecological description of the sample area (100m2) and the sampling of soil, fruit bodies of macromycetes in the middle period of their development (from June to September for different species taking into account the vegetation period for each) was conducted [18, 19].

The soil was selected by the envelope method to a depth of 5 cm (the action horizon) near the studied fruit bodies of fungi-macromycetes. The knife sterilization was carried out by dipping it into the soil 5-6 times [20].

Fruiting bodies of Pileate mushrooms were cut with a knife, wherein the mycelium was not injured. Sporocarps and soil were subjected to drying first at room temperature and then in a drying closet until dry.

When selecting fungi a composite sample of various habitats of the site was being assembled. The mushrooms were cleaned from soil particles and plant residues, weighed and, if necessary, crushed [18].

The research and collection of fruiting bodies of fungi was carried out in the field season in 2014-2015 in the communities of the Association Vaccinio myrtilli-Quercetum roboris Bulokhov et Solomeshch 2003 (hard pines) and Aceri platanoidis - Piceetum Bulokhov et Solomeshch 2003 (immoral-herbal spruces).

In the soil samples and the fungi the TM content was determined using the method of x-ray fluorescence analysis on the device Spectroscan-Max with an appropriate sample preparation [21].

For the collected material we calculated the coefficients of biological absorption CBA (or the coefficients of accumulation - Ca), as the ratio of HM concentration in the fruit bodies of fungi and in the soil.

If the Ca is above 1, and therefore, HM is absorbed by macromycetes [22]. The total concentration of copper, lead, zinc, arsenic were compared with the norms, defined in accordance with sanitary and epidemiological regulation 2.3.2.1078-01-1 [23].

Results and their discussion

In the study of forest habitats in the territory of the Dyatkovo district forestry 37 species of fungi were discovered. Among them, 32 species belong to saprophytes, and 5 to parasites [24].

The analysis of the total content of the elements of the HM in the fruit bodies of macromycetes showed the following.

The highest total concentration of HM was observed in the fruit bodies of Russula mairei Singer, Boletus erythropus Krombh. and Leccinum scabrum (Bull.) Gray, typical fungi-saprotrophes.

The highest total contents (mg/kg) of lead and arsenic was in the fruit bodies of Calocybe gambosa (Fr.) Singer (Pb - 31,75±2,8, As was 3.22±0,8), Boletus edulis Rostk. (Pb - 38,94±2,8, As - 3,14±0,8), Russula adusta (Pers.) Fr. (Pb - 36, 25±2,8, As - is 3.08±0,8) and Xerocomus subtomentosus (L.) Quйl. (As - 3,20±0,7).

The maximum content (mg/kg) of zinc is observed in the fruit bodies of Russula alutacea (Fr.) Fr. (152,72±11,6), Xerocomus subtomentosus (121,40±9,2), Tricholoma equestre (L.) P. Kumm. (114,85±8,9), Russula adusta (111,50±9,3) and Boletus edulis (106,71±8,4).

The high total content (mg/kg) of copper and nickel is observed in the fruit bodies of Russula mairei (Cu - 40,30±3,6, Ni - 25,03±2,2), Leccinum scabrum (Cu - 44,45±3,8, Ni - 18,75±1,7), Boletus erythropus (Cu - 46,53±4,1, Ni - 22,70±1,9), Boletus edulis (Cu - 33,30±3,5, Ni - 18,50±1,6), Calocybe gambosa (Cu - 34,20±2,8, Ni - of 19.85±1,7).

A significant concentration (mg/kg) of cobalt, compared with all other types of fungi is observed in the fruit bodies of Russula alutacea (3,10±0,7), Xerocomus subtomentosus (2,11±0,5) and Paxillus involutus (Batsch) Fr. (2,40±0,5).

The greatest total content (mg/kg) of chromium is observed in the fruit bodies of Russula mairei (of 52.61±4,9), Paxillus involutus (31,85±3,6), Russula alutacea (49,50±4,4) and Boletus edulis (33,90±3,1).

Record-breakers for the accumulation of iron and manganese in the fruit bodies and the intensity of inclusion in the biogenic migration of these HM are Boletus erythropus (Fe - 29295±87,5, Mn - 489,98±13,7), Russula mairei (Fe - 10128,4±95,7, Mn - 982,95± 17,9) and Leccinum scabrum (Fe - 60675,25±101,5, Mn - 597,25±14,9), where the concentration of these metals is several times higher than their content in other studied fungi, and the CBA varies from 7.9 to 70.

The lowest concentrations of most of the HM, with the exception of cobalt and copper, were in the fruit bodies of poison pax (Paxillus involutus).

One of the main indicators of HM accumulation in organisms is the CBA or the Ca, allowing to judge about the degree of involvement of elements in the biological cycle, and it is used to assess the connection of the environmental and the physiological role of a chemical element, as well as to identify organisms-indicators and organisms- concentrators.

The accumulation coefficients of the individual elements of the HM in the fruit bodies of the studied species of fungi is presented in figure 1-3.

Figure 1 - Coefficients of accumulation of Co, Cu, Zn and Sr in the fruit bodies of the studied species of fungi

Рисунок 1: Рядовка майская - Calocybe gambosa;

Подгруздок черный - Russula adusta

Свинушка тонкая - Paxillus involutus

Белый гриб - Boletus edulis

Моховик зеленый - Xerocomus subtomentosus

Белый гриб - Boletus edulis

Сыроежка зеленая - Russula aeruginea

Свинушка тонкая - Paxillus involutus

Сыроежка Майра - Russula nobilis

Подберезовик обыкновенный - Leccinum scabrum

Дубовик крапчатый - Boletus erythropus

Xerocomus subtomentosus belongs to fungi-accumulators of Co, Cu, Zn, and Sr and it can be used as a bioindicator of environmental pollution by these HM in the conditions of the combined pollution. Cu, Zn and Sr accumulate Boletus edulis, Russula alutacea, Paxillus involutus, Russula mairei, Leccinum scabrum, Boletus erythropus and Russula adusta. Calocybe gambosa is an accumulator of Cu (CBA = 1,16). fungus macromycetes pollution radiation

Figure 2 - Coefficients of accumulation of Pb, As, Ni and Cr in the fruit bodies of macromycetes

Рисунок 2: Рядовка майская - Calocybe gambosa

Подгруздок черный - Russula adusta

Свинушка тонкая - Paxillus involutus

Белый гриб - Boletus edulis

Моховик зеленый - Xerocomus subtomentosus

Белый гриб - Boletus edulis

Сыроежка зеленая - Russula aeruginea

Свинушка тонкая - Paxillus involutus

Сыроежка Майра - Russula nobilis

Подберезовик обыкновенный - Leccinum scabrum

Дубовик крапчатый - Boletus erythropus

In the whole, Pb, As, Ni and Cr accumulate in the fungi with a slightly lower intensity than Co, Cu, Zn and Sr, with some exceptions. Arsenic is actively involved in the biological cycle Xerocomus subtomentosus (PCU (KN) = 7,9). Lead accumulates in the fruit bodies of Russula adusta, Paxillus involutus, Boletus edulis and Russula mairei. Nickel is accumulated in fruit bodies of Russula mairei, Boletus edulis и Leccinum scabrum, chrome is accumulated in Russula mairei.

Very intensive accumulation of iron and manganese (figure 3) were observed in fruit bodies of Russula mairei, Boletus erythropus and Leccinum scabrum, the CBA of Fe for these types of fungi is respectively 21,5; 20,5 and 7,9, the CBA of Mn 70; a 46,5 and 19,8.

Figure 3 - Coefficients of accumulation of Fe and Mn in the fruit bodies of the studied fungi species

Рисунок 2: Рядовка майская - Calocybe gambosa

Подгруздок черный - Russula adusta

Свинушка тонкая - Paxillus involutus

Белый гриб - Boletus edulis

Моховик зеленый - Xerocomus subtomentosus

Белый гриб - Boletus edulis

Сыроежка зеленая - Russula aeruginea

Свинушка тонкая - Paxillus involutus

Сыроежка Майра - Russula nobilis

Подберезовик обыкновенный - Leccinum scabrum

Дубовик крапчатый - Boletus erythropus

On the basis of the accumulation coefficients fungi are divided into three groups according to intensity of accumulation of metals: the first group consists of mushrooms accumulating heavy metals the most intensively - Russula mairei, Leccinum scabrum and Boletus erythropus; the second one is a group of fungi which are characterized by the average intensity of the HM accumulation- Xerocomus subtomentosus, Boletus edulis and Russula alutacea; the third group includes fungi which are characterized by a low degree of HM accumulation- Boletus erythropus, Russula adusta and Calocybe gambosa.

Conclusion

The analysis of the HM gross concentration showed that the maximum lead content was observed in the fruit bodies of Russula adusta, Boletus edulis and Calocybe gambosa. All fruit bodies of fungi, the total lead content exceeds the permissible sanitary-hygienic norms in 10,3-17,9 times, arsenic - in 3,4-12,1 times, zinc - in 1,5-11,7 times, copper - in 2,0-12,7 times. The total content of HM elements is maximum in the fruit bodies of Russula mairei, Boletus erythropus и Leccinum scabrum. The lowest concentrations of most of the HM, with the exception of Co and Cu, was in the fruit bodies of Boletus erythropus.

In most cases, the content of lead, nickel, arsenic and zinc, and copper in soils of the investigated sites exceeds the maximum permissible concentrations (MPC) and approximate permissible quantities (APQ).

Fungi-accumulators of Co, Cu, Zn, and Sr comprise Xerocomus subtomentosus proposed as a bioindicator. Pollutants Pb, As, Ni and Cr, in general, accumulate in the mushrooms with a slightly lower intensity than Co, Cu, Zn and Sr. However, arsenic is involved in the biological cycle of the green boletus (Xerocomus subtomentosus) (CBA = 7,9) quite actively. Studies of the absorption of HM by Paxillus involutus coincides with literature data [1, 2, 15, 25].

The identification of the peculiarities of the absorption and total content of HM in the conditions of combined radiation-chemical pollution has practical value. None of the species of fungi is recommended for use in food without pre-treatment: drying, soaking and boiling followed by draining of water.

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Annotation

UCD 630.8 (581.19+574.3)

Peculiarities of heavy metals' accumulation by the fruit bodies of macromycetes in the conditions of the combined radiation and chemical contamination. Anishchenko L. N., Professor, Department of ecology and environmental management, doctor of agricultural Sciences, Bryansk state University named after academician I. G. Petrovsky, 14 Bezhitskaya Str., Bryansk, Bryansk region, 241050, Russian Federation

Ladnova G. G., Professor, Department of ecology and biology, doctor in biology Sciences Orel state University named after I. S. Turgenev, 95 Komsomolskaya Str., Orel, Orel region, 302026, Russian Federation e-mail: gladnova@yandex.ru

Frolova N.V., assistant professor, Department of ecology and biology, candidate in biology Sciences Orel state University named after I. S. Turgenev, 95 Komsomolskaya Str., Orel, Orel region, 302026, Russian Federation

In the conditions of combined radiation and chemical contamination of forest habitats (Bryansk oblast) the cumulative activity of Pileate mushrooms in relation to heavy metals was revealed, the accumulation coefficients were calculated. The route methods of the soil research were used, the gross concentration of the elements was determined with the x-ray fluorescence method. The intensity of accumulation of heavy metals in fruit bodies of fungi were estimated using the accumulation coefficients.

The analysis of concentrations of gross pollutants showed that the maximum lead content was observed in the fruit bodies Russula adusta (Pers.) Fr., Boletus edulis Rostk. и Calocybe gambosa (Fr.) Singer, the concentration of arsenic - Calocybe gambosa, Boletus edulis, Russula adusta и Xerocomus subtomentosus (L.) Quйl. The maximum zinc content is observed in the fruit bodies of Russula alutacea (Fr.) Fr., Subtomentosus Xerocomus, Tricholoma equestre (L.) P. Kumm., Adusta Russula and Boletus edulis, copper and nickel content - Xerocomus subtomentosus, Leccinum scabrum, Boletus erythropus Krombh., Boletus edulis, Calocybe gambosa and Xerocomus subtomentosus, iron and manganese content - Boletus erythropus, Xerocomus subtomentosus and Leccinum scabrum. The total content of heavy metals (HM) in the fruit bodies of Xerocomus subtomentosus, Boletus erythropus and Leccinum scabrum is maximal.

On the basis of the accumulation coefficients fungi are divided into three groups according to intensity of accumulation of metals: the first group consists of mushrooms accumulating heavy metals the most intensively - Russula mairei, Leccinum scabrum and Boletus erythropus; the second one is a group of mushrooms which are characterized by the average intensity of the HM accumulation- Xerocomus subtomentosus, Boletus edulis and Russula alutacea; the third group includes mushrooms, which are characterized by a low degree of HM accumulation- Boletus erythropus, Russula adusta and Calocybe gambosa. Fungi accumulating Co, Cu, Zn and Sr is Xerocomus subtomentosus which is recommended as a bioindicator of environmental pollution with these metals. The obtained results are the basis of the potential for biomarker and eco-analytical research of migration of heavy metals with the participation of the components of forest ecosystems.

Key words: macromycetes, forest ecosystems, heavy metals, the total concentration of the accumulation coefficients, combined pollution, Bryansk region

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