Dynamics of annual growth of Pinus sylvestris on industrial wastes of mining companies

Svetlana Bakhtina·Yulai Yanbaev·Aleksey Kulagin·Nina Redkina·Ilgam Masalimov·Shamil Fayzrakhmanov

Abstract The development of the mining industry has led to the appearance in many parts of the world of vast technogenic territories from which toxic heavy metals enter the environment and food chains.Physical,chemical,and biological methods of cleaning industrial land due to technological complexity and high cost are relatively little used on a large scale.Natural forest overgrowth of mining sites and the removal of heavy metals by woody plants can be an effective form of recovery.Therefore,the study of this process is of significant scientific and practical interest.The analysis of the annual growth in height and width of the annual rings of the stem of Scots pine (Pinus sylvestris L.) in 2004–2019 was made on the territory of the Uchalinsky mining and processing plant (South Ural,Russia) contaminated with heavy metals.Relatively high concentrations of copper and zinc were found in soils,roots,bark,young shoots,comparable to exceeding the maximum allowable concentrations.Despite the spatial uniformity of the heavy metal content in the stands,the tree samples significantly differed in terms of annual growth.Results suggest that the lack of nutrients and not stress from exposure to heavy metals is the main reason for relatively low growth rates on slopes of industrial wastes.It was confirmed by studying the annual growth in height of the undergrowth in habitats with different soil cover conservation.The data prove the relatively high potential of Scots pine for the natural recovery of industrial lands polluted with heavy metals by mining enterprises.

Keywords Annual growth·Pinus sylvestris·Heavy metals·Phytoremediation

Introduction

Industrial pollutants cause significant harm to human health due to their toxicity,long-term circulation of substances,and the pollution of all components of natural ecosystems(Aelion et al.2009).Among them,heavy metals dominate which,together with mineral oils,are a source of pollution to 60% of soils of European Union countries.The total cost of solving this contamination is estimated at 6 billion euros(over USD 7 billion) per year (Panagos et al.2013).Similar monetary valuations in Russia have not been carried out.But there is information about the degree of pollution by heavy metals which is significant in Russia’s mining regions.The factories are major suppliers of concentrates of copper-pyrite ores to the metal enterprises of Russia,approximately 24.4%of the output of non-ferrous metallurgy in Russia (Abakumov et al.2015).Open-pit mining has led to a catastrophic change in natural environments,a source of heavy metals entering the environment,many times exceeding the maximum concentrations accepted in Russia (Abakumov et al.2015;Volkov et al.2019,Aidosov et al.2019).

Recovery of polluted lands by vegetation under these conditions is an effective and relatively inexpensive means of reducing the negative impact of heavy metals (Bolan et al.2011).It is relevant in places of open mining of fossil resources that are more prone to erosion and dispersion by chemical elements (Ngole-Jeme and Fantke 2017).Of particular interest is the use of woody plants due to their long life cycle,large biomass,and relatively high resistance to heavy metals (Cpuana 2011).Other methods for the restoration of soils contaminated with heavy metals,based on“dig-and-dump”or encapsulations,are costly and therefore can only be applied on a limited scale (Pulford and Watson 2003).

The response of plants to metal poisoning stress is often studied on seedlings,in cell suspensions,and in callus cultures (Cpuana 2011;Pietrzykowski et al.2014).But doubts arise about the validity of extrapolating these results to mature trees and their applicability in forestry practice.The sensitivity of plants to adverse conditions in the early stages of ontogenesis is much higher than in the later ones (Pulford and Watson 2003).For this reason,it seems justified to study adaptation to environmental pollution by heavy metals also in the generation of adult trees.

There are various laboratory and field methods for determining the vitality of trees–a key indicator in monitoring the impact of industrial pollution on the forest condition.These include biochemical analyzes of various plant tissues,estimates of crown foliage,and its structure Annual growth of trees in height and diameter of trunks are relatively inexpensive and affordable field measurements (Dobbertin 2005).These measurements are especially pounced for coniferous species with their easily determined annual rings or annual height growth y whorls of lateral branches.Annual growth is influenced by many factors.Interannual seasonal climatic conditions affect the entire stand (Suvanto et al.2017).At the same time,micro-heterogeneity of environmental conditions in space and time determining differences in treegrow is due to intra-and interspecific competition,differences in topography,fertility,soil moisture,availability of nutrients,temperatures and light.Annual growth rates vary even in habitats that are relatively uniform in environmental conditions,which indicates the genetic influence on growth of Scots pine (Yanbaev et al.2018).In technogenic deposits,primarily industrial dumps and tailing sites,and other sites with a disturbed surface,annual growth rates change due to the appearance of a new,powerful complex of environmental factors.There are effects of chemical toxicants on the metabolism of trees (leading to changes in the redox process,photosynthesis,reproductive processes,germination rates,and seed morphology).Under these toxic conditions,differences in individual genotypes and resistance to chemical toxicants are manifested (Pulford and Watson 2003).

The choice of the species of woody plants is a critical stage in the development of phytoremediation technologies for contaminated lands (Heckenroth et al.2016).In this study,Scots pine (Pinus sylvestris L.) was selected as it has been studied in considerable detail with regards to industrial pollution.The accumulation of heavy metals in the needles of Scots pine is recognized as an indicator of the state of the environment (Pajak et al.2017).Bioavailability,accumulation,and allocation of these metals have been studied in detail (Ots and Mandre 2012;Pietrzykowski et al.2014).There are also a limited number of studies addressing the dynamics of productivity of this species under environmental pollution by heavy metals.The growth in diameter of Scots pine affected by industrial gaseous pollutants,copper,and zinc has been studied in northern Russia (Chernen’kova et al.2014).The aim of this study is a comparative analysis of variability of the annual growth (diameter and height) in habitats of Scots pine on Uchalinsky Mining and Processing Plant sites when contaminated with heavy metals,differing in soil and topographic conditions,and proximity to industrial dumps.

Materials and methods

Study site

The Uchalinsky mining and processing plant (UMPP),which was formed in 1954,produces copper–zinc concentrates and sulfur flotation pyrite,and complexes in mineral and chemical composition of polymetallic ores.Its consumers are many large metal enterprises in Russia.The main component of the ores is pyrite (up to 78% of the ore mass),the primary source of copper and zinc.Thus,annual processing of about 5.5 million tons of ore results in 50 million tons of waste with volume of 25 million cubic meters (Abakumov et al.2015).Calculations show that 164.3 million m3of rock waste are stored on sites.Ore dressing waste from UMPP contains in tailing dumps relatively large concentrations of unrecovered heavy metals,including copper (0.2% of weight) and zinc (0.9%).It has been established that 120,396 and 247,389 tons of these metals,respectively,have been deposited since 1954 in the wastes of this site.This level has led to the accumulation of mobile forms of copper and zinc in a 5-km radius from the plant in the soil humus horizon of 22.5 and 2.6 the maximum permissible concentrations,respectively (Abakumov et al.2015).The waste sites of the Uchalinsky quarry (380 m deep,1800 m wide and 900 m long) are piled up to 30 m high with several ledges,plateaulike peaks,and steep slopes.During more than half a century of UMPP activity in the area of 1252 hectares,intensive regeneration of woody vegetation has taken place,mainly byBetula pendulaRoth.and Scots pine.One of the reasons for this observation is the large forest cover of the region(40.5% of the territory) and the dominance of these two species (74% by wood stock).Pine-birch forests surround the industrial plant and the adjacent town of Uchaly,for which UMPP has been a city-forming enterprise.Areas of forests are on mountain soils with a thin humus horizon as well as disturbed soils with soil-like properties with undeveloped profile,poor absorption and cleansing ability.There are two factories in the study area,Technoplex,which produces polystyrene boards and Nicole-Pak which produces corrugated paper and roof ing cardboard.However,their production volume and,consequently,environmental pollution are not comparable with the damage from UMPP activities.It was assumed that the effect of pollutants from these enterprises that the trees of the trial plots should be similar since they are located at approximately the same distance (Fig.1).

Fig.1 Location of trial plots in the technogenic zone of the Uchalinsky mining and processing plant

Sampling

An uncrewed aerial vehicle,DJI Phantom (SZ DJI Technology Co.,China),surveyed the north and north-east sides of the UMPP to select habitats for sampling (Fig.1).Trees 30–40 years old were abundant on technogenic or man-made lands.Pre-selected sites were inspected to select stands with similar age and density,and composition.Plot 1 is located 1.5 km from the plant territory in a stand without anthropogenic impact (Fig.1).The following habitats are located in the technogenic zone of the UMPP.Plot 2 is a stand on a level site;plot 3 was laid out at the base of industrial dumps where air pollution is supplemented by chemical toxicants entering the soil in sewage (Abakumov et al.2015).In these three plots,below a 1.5-cm thick litter layer,there is a thin clay soil up to 18-cm thick.The soil pH is 4.3,with low levels of phosphorus (2.05 mg per 100 g of soil),potassium (2.05 mg per 100 g of soil),and nitrogen (0.6 mg per 100 g of soil).Hydrolytic acidity is 8.45 mg.eq.per 100 g of soil.The total carbon content in the upper horizon is 1.0%of weight.Plot 4 is on a steep slope of overburden dumps where soil is absent and trees have populated the interunit spaces filled with weathering products of rocks and organic residues.Within each of the four plots,four biotopes,sites of uniform environment giving rise to a specific assembly of plants,were selected,relatively homogeneous in abiotic factors,soil thickness,light availability and stand characteristics (density,height,and diameter).

In each of these 16 biotopes,one model tree was selected from among 30 trees by measuring DBH (diameter at breast height) and harvested.Additionally,on a 1.2-km transect along the power line (Fig.1,test area 5) where intensive reforestation has taken place,60 samples of undergrowth were randomly selected (Fig.1,area 5).The plants were in habitats that differed in soil conservation–undisturbed(Sects.5.1,5.3 and 5.5),partially disturbed (5.5),and practically devoid of soil (5.2 and 5.4).In a similarly aged natural pine-birch stand 15 km from the UMPP,plot 6,control stand,was established.Age of trees was determined using a Haglof increment borer;density and composition of the stand were similar to those in the trial plots 1–4 (Table 1).In plot 6,20 trees with DBH close to the average were selected.

Table 1 Location and age of the plants selected for the study,the content of heavy metals in soil in the area of the trial plots

Measurements and laboratory tests

Using a binocular light microscope MБC-1 on sample cuts of 16 trees from plots 1–4 in two perpendicular directions,the annual diameter over 2004–2019 was measured within an accuracy of 0.5 mm.With a minimum accuracy of 1 cm,annual height growth of trees and undergrowth was metered.

The content of heavy metals of copper and zinc,the dominant heavy metals in the ores of the region,was determined by atomic absorption spectroscopy on the Contr-AA instrument (Analytik Jena AG,Germany).Soil samples from the upper 20-cm horizon were studied only in plots 1,2,3,and 6 because,in plots 4 and 5,soil was entirely or partially absent.For this reason,samples of roots,bark,wood of 1-,2-,3-year-old shoots,and needles of the last 3 years were taken in the summer only on sample trees in plots 1–3 and 6.The analysis of this material for heavy metal levels wascarried out using a certified inversion voltampermetric method (https://www.russi angos t.com/p-37243 4-mu-08-47136.aspx).Mass concentrations of elements were measured on a CTA analyzer (Russia).In total,42 and 96 samples of soil and plant material,respectively,were taken during the fieldwork.Measurements of annual growth and heavy metal contents in soils,organs,and tissues were processed using the STATISTICA 13.3 program.For average values,the relative error and the 95% confidence interval were calculated.The coefficient of variation C (%) was used as a measure of the variability of attributes.The statistical dependence between the variables was determined by building correlation matrices and assessing the reliability of the correlation coefficients.Statistical hypotheses were tested at significance levels of 5,0.1,and 0.01%.

Results

Differences in stands in terms of annual growth

Soil samples in plots 1,2,and 3 had a similar levels of copper and zinc;differences were not statistically significant.The total amount of heavy metals averaged 51.7 ± 10.8 (Cu)and 99.7 ± 4.4 (Zn) mg kg−1,which is higher than the Russian maximum permissible (23.0 and 85 kg−1,respectively).Despite the absence of regularities in the spatial distribution of heavy metals,the average annual growth in height and diameter decrease from plot 1 furthest from the industrial waste dumps to plot 2 located about 100 m from them(Figs.2 and 3).

In plot 3,located at the foot of the slag heaps where acidic waters with a high levels heavy metals enter (Abakumov et al.2015),these growth indicators are considerably reduced,especially annual height growth (Fig.2).The minimal growth in height and diameter is observed in plot 4,where the trees are on the steep slope of dumps devoid of soil and composed of overburden rocks.Annual height growth in these trial plots was 89.6,68.1,and 54.8%,respectively,of plot 1.Diameter growth decreases at approximately the same rate,87.5,84.4,and 50.0%.More detailed information is given in Tables 1 and 2.The differences in the samples are significant for height atp＜ 0.01(pair of plots 2–3) andp＜ 0.01 (pairs 1–3,1–4,2–3 and 3–4);for diameter,atp＜ 0.05 (pair 1–2),p＜ 0.01 (1–3)andp＜ 0.01 (1–4,2–4 and 4–4).

Fig.2 Annual height increment of Scots pine;C.I.–the boundaries of the 95% confidence interval

Dynamics of annual growth in stands

The sample trees differ in growth variability (Tables 2 and 3).Annual height increment is lowest in plot 1 (coefficient of variation 16.2%);in the other three plots,it is higher with values of 22.5–24.9%.These patterns are not due tothe different ages of the plots.Trees within the majority of plots on the UMPP lands differ little by age,18–19 plot 1,18–20 plot 2,and 37–38 plot 4.The trees of plot 3 differ in age to a greater extent (21–34 years old).Nevertheless,close and relatively small values of the coefficient of variation of diameter growth were established for plots 1 and 4 (23.1%and 22.6%).The variability of diameter growth is higher and close in plots 2 and 3 (31.8% and 31.1%).In the control plot 6,annual height increment averaged 38.7 ± 1.9 cm,and varied from 29.1 ± 4.2 to 57.4 ± 2.64,the coefficient of variation was 15.7% less than in plots 1 and -2 and above this in plots 3 and 4 (Table 2).The variability of 20 trees age 26–37 years old corresponds to the variability of heights under industrial conditions in plots 2 and 3;average coefficient of variation is 30.3 ± 2.2,which varies from 9.2 to 48.6% for individual trees.

Table 2 Dynamics and variability of the annual height increment of Scots pine in the sample plots

Table 3 Dynamics and variability of the annual diameter increment of Scots pine

Figures 4 and 5 show the dynamics over time of the growth of trees in the four plots.In plots 1 and 2,a synchronous variation in the average values of both annual height increment and diameter increment is observed.Trees of plot 3 mirror this trend to a lesser degree.On the steep slope of industrial dumps (plot 4),the variation practically disappears,especially in the annual diameter increment (Fig.3).

Fig.3 Annual diameter increment of Scots pine;C.I.–the boundaries of the 95% confidence interval

The increase in both heights and diameters in the plots under the man-made conditions of the UMPP varies on the whole;the correlation coefficient has positive values,statistically significant atp＞ 0.05 in pairs of plots 2–3 and 2–4.This feature manifests itself better in determining pairwise correlations of the growth of individual trees (Table 4).In plots 1 and 2 within the limits of the tree samples (Table 4,samples are marked with a bold line),and between them,annual growth in height is well synchronized–all correlations are statistically significant.In plot 3,the connection weakens because the growth of tree No.12 differs from the other three trees of the sample.In plot 4,the annual growth in height is not related,–the correlation between them is not statistically significant.Diameter growth partially repeats these correlations but to a lesser extent.The statistical significance of the synchronized dynamics of the diameter is expressed at lower levels,in plots 1–3,(only in 1 or 2 of 6 possible comparisons).On the other hand,the correlation of diameter,in contrast to annual height increment in plot 4,is statistically significant (p＜ 0.05) in half pairwise comparisons of the indicator values.

Fig.4 Dynamics of annual height increment of Scots pine under conditions of industrial pollution (the years are arranged in descending order,i.e.1-2019 and 16-2004)

Fig.5 Dynamics of annual diameter increment of Scots pine under conditions of industrial pollution (the years are arranged in descending order,i.e.1-2019 and 16-2004)

Heavy metal contents in samples

The accumulation of copper and zinc in soils of plots 1–3 were higher than the maximum permissible concentrations accepted in Russia (Cu–23.0 mg kg−1,Zn–85.0 mg kg−1).Copper concentrations in the UMPP site (51.7 ± 10.8 mg kg−1) is almost twice higher than under natural conditions (26.9 ± 1.2 mg kg−1).The metal in the soil accumulates in the roots of Scots pine (Table 5),decreasing by 2–4.4 times (p＜ 0.05) in bark-shoots-needles.Zinc in the roots is almost 1.8 times less than in soils.In the bark,the amount decreases slightly but decreases significantly by 2.5 times (p＜ 0.05) in shoots and needles.Other patterns are observed in the Scots pine stand that is 15-km from the plant (plot 6),the differences with plots 1–3 are statistically significant for copper (Zn levels are similar in undisturbed and technogenic lands).

The accumulations of zinc in roots,shoots,and needles are similar but an increased deposition of the metal in the bark are notable.Concentration of zinc,in comparison with the soil,is several times less in all tissues of Scots pine.The levels of the accessible form of copper and zinc is muchlower (2.7 ± 0.8 mg kg−1and 8.3 ± 0.8 mg kg−1,respectively) than in roots,bark,shoots,and needles (Table 5).

Table 4 Correlation matrix of annual increment of Scots pine under industrial pollution

Table 5 Content of heavy metals in the organs and tissues of Scots pine

Annual growth of the undergrowth

Significant differences in the sample trees of plots 1–3 in terms of growth are observed with a relatively uniform heavy metal levels in the plots.There is evidence that significant differentiation in annual height increment under these conditions exists in young regeneration in plot 5 (Fig.6).On average,for 2016–2019,heights are 26.5 ± 2.2 cm.Height changes significantly from individual to individual,from 4.5 ± 0.2 to 58.1 ± 7.1 cm.The increment up to 15 cm,15–30,30–45,and ＞ 45 cm have 24,11,9,and 15 trees,respectively.The transect passes through three sections with preserved soil.Under these conditions,the undergrowth has a relatively high annual height increment,in Sects.5.1 and 5.2 it was 47.0 ± 1.7 (changes within 37.0–57.4 cm,coeffi-cient of variation 11.5%),and 47.3 ± 1.8 cm (38.1–58.1 cm,12.0%),respectively.In plot 5.5 where the average annual height is lower,28.5 ± 1.5 cm (22.1–35.4 cm,18.1%),the density of undergrowth,and the competition of plants for access to light are less.The undergrowth of groups in Sects.5.2 and 5.4 has the lowest annual height increment,10.2 ± 0.8 cm (4.6–17.8 cm,35.4%) and 12.3 ± 1.7 cm(5.0–21.7 cm,40.2%),respectively.the undergrowth is in habitats where the soil is severely disturbed,and in some places,the rock is exposed.The average annual growth of most pairs of undergrowth differs significantly at a high level of significance (p＜ 0.001),except for pairs 5.1–5.3 and 5.2–5.4.

Fig.6 Annual increment of undergrowth in height under conditions of industrial pollution C.I.–boundaries of the 95% confidence interval

Discussion

The results show that yearly fluctuations in climatic conditions are a leading factor in the dynamics of the annual growth of Scots pine in height and diameter.It is indicated by the synchronism of changes in annual growth on plots 1–3 and,to a lesser extent,on plot 4.When planning the study,it was assumed that possible differences among the groups of trees in this parameter could not be caused significantly by climatic factors (temperature,precipitation) as they have to be relatively uniform within the area studied because its comparatively small size.It was expected that pollution by heavy metals as a result of UMPP activity would have a severe effect on plant growth due to the toxicity of these elements (Mukti 2014).In the study plots,high concentrations of copper and zinc were found in the soils,comparable with or exceeding maximum allowable concentrations.However,it turned out that significant differences in the groups of trees by annual increment were formed with a relatively uniform content of heavy metals in the plots (content of copper and zinc varied 46.1–62.7 mg kg−1and 91.6–105.1 mg kg−1,respectively).Soil samples from the plots of the technogenic zone did not differ in the content of these toxicants at a statistically significant level.Therefore,no concentration trend was found based on the distance from industrial dumps.In these conditions,the trees showed a relatively high annual increment in height and diameter,comparable to those under natural conditions.

There may be several non-conflicting causes of the identified phenomenon.Relatively high increments and relatively good vitality of trees in the technogenic zone may be because concentrations of the biologically accessible mobile forms of copper and zinc (the most dangerous for plants) is much lower than the total content (Pietrzykowski et al.2014).When they are absorbed by the trees,physical,physiological,biochemical,and molecular mechanisms of detoxification and protection may be involved (Dubey et al.2019).If these absorption barriers cannot protect plants from excessive intake of heavy metals,they can accumulate in physiologically less active organs (Krutil et al.2018).Perhaps,for this reason,we have identified relatively higher concentrations of copper and zinc in the bark than in young shoots and needles.

Another explanation for the relatively high increment of Scots pine in the technogenic zone may be the adaptation of the species to stress from exposure to heavy metals.During natural selection,a genetically determined metal resistance could be formed due to prolonged growth in soils with increased mineralization of rocks.For example,the content of zinc in 10 study plots of agricultural land in the Uchalinsky district (average 101.5 ± 3.5 mg kg−1,changes in the range 79.5–123.0 mg kg−1),were comparable with the concentration of zinc in the technogenic zone of UMPP.Such a relatively high natural background of environmental pollution by heavy metals can have genetic consequences.The reality of such a possibility has been shown by Chudzińska et al.(2016).When analyzing microsatellite DNA,it was found that the“stable”and“sensitive”sub-populations of Scots pine near a zinc plant in Upper Silesia were genetically different from each other at the level of differentiation of 42 populations previously studied in Poland.These two groups of trees also differed from each other in that the more adapted genotypes had a deficiency of heterozygotes in three of the four studied loci.These results,as well as the phenomenon of comparatively high growth rates of Scots pine in an environment contaminated with heavy metals,which we have identified,provide the promise of studying the genetic mechanisms of the formation of the stability of its populations.

Conclusion

The variability and the amount of the annual growth in height and diameter of Scots pine on lands of the Uchalinsky Mining and Processing Plant are determined primarily,as under natural conditions,by climatic factors and the availability of nutrients in soils.The level of contamination by the heavy metals,copper and zinc,in the study habitats does not lead to a significant decrease in annual growth.The reasons may be both the presence of mechanisms for reducing stress from exposure to heavy metals,and to the formation of genetically stable populations under conditions of natural mineralization.Scots pine has demonstrated high potential for the natural recovery of lands of mining enterprises pollutedwith heavy metals.Planting Scots pine represents a cost-effective and environmentally friendly alternative to artificial restoration technologies for disturbed lands.