Abstract
This paper examines the chemical composition of Scots pine litterfall in north taiga pine forests in background conditions and under the impact of emissions from the Severonikel copper–nickel industrial complex. In forests exposed to industrial airborne pollution, the content of fertilizer elements (Ca, Mg, Mn, and Zn) in coniferous litterfall decreases, while the content of heavy metals (Ni and Cu) and values of stoichiometric C/P and N/P ratios increase. This indicates that the quality of plant material to be decomposed by soil biota declines. In background conditions, intrabiogeocoenotic differences in the chemical composition of coniferous litterfall are manifested in a higher content of K and P (supplied with crown and trunk waters) under tree crowns; in intercrown spaces, concentrations of Fe, Zn, Ni, and Cu are higher due to background airborne pollution. In defoliating forests, coniferous litterfall under tree crowns contains more Ca, Mg, K, Mn, P, N, and S due to the intensive leaching of fertilizer elements from tree crowns by acidic precipitation and, as in the case of sulfur, due to its inflow with acidic precipitation. The elevated content of N, P, and K in coniferous litterfall of defoliating forests can be determined by high concentrations of these mobile elements in living needles falling off ahead of normal phenological terms. In background conditions, seasonal variability of the chemical composition of coniferous litterfall in defoliating forests is manifested in high Ca and Mn concentrations in needles due to their accumulation there by the end of the warm season. In sparse technogenic forests, Mg and K accumulate in coniferous litterfall by the end of the growing season, which indicates a disturbance of retranslocation processes under the impact of pollution. In all studied pine forests, the content of Fe and Zn in litterfall significantly decreases by the end of the warm season; in forests exposed to airborne pollution, the content of Ni and Cu decreases as well. This can be explained by their antagonism with Mn and leaching from needles by acidic precipitation during the warm season.
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INTRODUCTION
Fallen assimilating organs represent an active fraction of tree litterfall and act as a source of nutrients available to biota. The elemental composition of leaf/coniferous tree litterfall provides insight into the cycling of matter and soil formation patterns (Meier et al., 2005; Wood et al., 2006, 2009; Vesterdal et al., 2012; Osipov, 2017). Distinct features of the chemical composition of leaf and coniferous litterfall contribute to the formation of phytogenic zones of influence around trees, inhibit the growth of herbaceous plants, and affect the microbial activity and soil composition (Reshetnikova, 2011; Aponte et al., 2013; Chavez-Vergara et al., 2014; Ufimtsev and Egorova, 2016; Kolmogorova and Ufimtsev, 2018). The initial litterfall quality regulates its decomposition rate (Berg, 2000; Wardle et al., 2003; De Marco et al., 2007; Berg and McClaugherty, 2008; Zhang et al., 2008; Rahman et al., 2013; Tu et al., 2014; Lukina et al., 2017; Ivanova et al., 2019). The content of elements in litterfall depends on the tree species (Preston et al., 2006; Ukonmaanaho et al., 2008; Aponte et al., 2013; Jonczak and Parzych, 2014; Boev et al., 2018; Becker et al., 2018; Neumann et al., 2018), stand age (Trap et al., 2013), and topography (Bessonova et al., 2017). Seasonal features of the litterfall chemical composition remain poorly researched (Rautio et al., 1998b; Portillo-Estrada et al., 2013; Jonczak and Parzych, 2014; Chul’diene, 2017).
Within the Kola Peninsula and mainland Murmansk oblast, forest ecosystems are affected by both natural environmental factors (e.g., short growing season and low temperatures) and airborne technogenic pollution. A large mining and smelting enterprise, the Severonikel copper–nickel industrial complex (AO Kol’skaya GMK) is located in the central part of Murmansk oblast; the main components of its emissions are sulfur dioxide and polymetallic dust (Ni and Cu). In the 1990s, the volume of emissions from the Monchegorsk enterprise of Kol’skaya GMK had temporarily decreased (Tsvetkov and Tsvetkov, 2012). According to AO Kol’skaya GMK, Ni, Cu, and SO2 emissions amounted to 1400, 700, and 129 300 t yr–1, respectively, in 1995. Atmospheric pollution causes forest degradation, increases tree defoliation, and disrupts element retranslocation processes within trees (Lukina and Nikonov 1996, 1998; Nieminen and Helmisaari, 1996; Rautio et al., 1998a; Steinnes et al., 2000; Kiikkilä, 2003; Tarkhanov, 2009; Yarmishko and Lyanguzova, 2013; Sukhareva and Lukina, 2014; Vacek et al., 2016). An increase in the Ca inflow with pine litterfall compared to the control zone was registered in the impact zone of Sredneuralsky Copper Smelter (Yusupov et al., 1995). Due to the long-term impact of acidic precipitation and nitrogen saturation in spruce forests of the Czech Republic, concentrations of Ca, Mg, and Mn and the Ca/Al and Mg/Al ratios in the litterfall have decreased, while the N content and N/Mg ratio increased (Kopáček et al., 2010). The decomposition rate of spruce and pine litterfall has decreased in defoliating forests and sparse technogenic forests located in the Severonikel impact zone, and the quality of plant material declined: the initial content of heavy metals (Ni and Cu) increased, while the content of Ca, Mn, K, and Mg decreased (Lukina et al., 2017; Ivanova et al., 2019). To date, no comparative assessments of the chemical composition of tree litterfall components have been performed for a wide range of elements and parameters at the northern distribution limit of forests exposed to airborne technogenic pollution taking into account seasonality and intrabiogeocoenotic variability. Such data will make it possible to assess the state and functioning of forest stands and dynamics of biogeochemical cycles of carbon, nutrients, and heavy metals in forests.
The purpose of this study was to estimate the effect of airborne technogenic pollution from the Severonikel smelter on the chemical composition of pine needle litterfall taking into account the intrabiogeocoenotic and seasonal variability in pine forests at their northern distribution limit.
MATERIALS AND METHODS
The studies were conducted on permanent sampling plots of the Institute of North Industrial Ecology Problems, Kola Science Center, Russian Academy of Sciences, established in north taiga dwarf-shrub–lichen pine forests exposed to emissions from the Severonikel copper–nickel industrial complex (Monchegorsk) within the Kola Peninsula and mainland Murmansk oblast. Based on the pollution level and state of vegetation, the permanent sampling plots represent various stages of a digressive succession. They are located along the pollution gradient in the south-southwestern direction from the smelter at the following distances: 7–10 km from the emission source in sparse technogenic forests (STF), 20–100 km in defoliating forests (DF), and 100–200 km in forests formed in background automorphic conditions (BF) (Lukina and Nikonov, 1998). In terms of the stand composition, all studied objects are pine forests with an admixture of birch and spruce that had been affected by fires in the past.
Pursuant to the ICP Forests recommendations (Ukonmaanaho et al., 2016), litterfall was collected on sampling sites year-round into cotton bags attached to a solid frame at the bottom of the collecting funnel of the litterfall trap. The diameter of the upper part of the funnels is 82 cm; the litterfall trap depth is more than 0.5 m to prevent litterfall blowing-out from the traps. Collectors are installed at a height of 1–1.3 m above the ground to drain water from them. In 1994, litterfall traps were randomly installed in intercrown spaces on the sampling plots (10–15 units per plot); since 2013, they have been installed taking into account intercrown and undercrown spaces. At present, 7–8 litterfall traps are installed on each sampling plot between tree crowns and 4–5 litterfall traps under tree crowns. Sampling is performed twice a year: in early October prior to the permanent snow cover formation and in early June after the snowmelt. The pine needle fraction was isolated from the tree litterfall mass in the laboratory environment.
To determine the chemical composition of fallen Scots pine (Pinus sylvestris L.) needles after their isolation from litterfall samples in the laboratory environment, three mixed samples were taken—when possible separately for undercrown and intercrown spaces for analysis—for each of the sampling seasons (October–May and June–September) in 2014–2017; in total, 99 samples were analyzed. These data were supplemented by test results describing the initial composition of needle litterfall sampled once in September 1997 for a decomposition experiment conducted in 1997–1999; these samples were analyzed with a one- to fourfold replication. Computations were performed on an absolutely dry weight basis. The hygroscopic coefficient in the samples was determined by weighing them before and after drying in an oven at a temperature of 105°C. Prior to chemical tests, the studied plant material was crushed and wet ashing was performed using concentrated HNO3. Concentrations of metals (Ca, Mg, K, Al, Fe, Mn, Zn, Cu, and Ni) were determined using atomic absorption spectrometry (AAnalyst 800). The total N content was determined using the Kjeldahl method, total organic C content (Corg) using the Tyurin method, and total P content using the colorimetric method (Vorob’eva, 1998).
The V criterion (Husson et al., 2017) was used to estimate the intrabiogeocoenotic and seasonal variability of the pine needle litterfall chemical composition and the effect of airborne pollution (through the digression stage). The degrees of effect caused by airborne pollution (through digression stages), seasonal variability (warm and cold seasons of the year), and intrabiogeocoenotic spatial variability on the composition of coniferous pine litterfall was estimated taking into account the main elements of the micromosaic (undercrown/intercrown spaces) on the basis of the determination coefficient (R2) that reflects the contribution of a given factor to the total variance of the studied parameter. The V criterion was computed in the R statistical programming environment (R Core Team…, 2017).
RESULTS AND DISCUSSION
Chemical Composition of Pine Needle Litterfall in North Taiga Pine Forests at Different Digression Stages
Airborne pollution has the most significant effect on the content of Mn, Ni, Cu, S, Fe (R2 = 0.4–0.7), P, Ca, Al, and Mg and on the C/P ratio (R2 = 0.2–0.3) in Scots pine litterfall. To a lesser extent, the effect of airborne technogenic pollution is manifested for Zn and the N/P ratio (R2 = 0.1) (Table 1). In pine forests formed in background conditions, pine needle litterfall is distinguished by a relatively high content of Mg, Mn, and Zn and a low content of Al, Fe, Ni, Cu, and S (p < 0.05) (Table 2).
Changes in the elemental composition of fallen needles are observed in pine forests exposed to industrial airborne pollution. In defoliating forests, litterfall is distinguished by the lowest content of Ca and Mg, which is consistent with patterns identified under similar conditions for living needles (Lukina and Nikonov, 1998); concurrently, the P content is high (p < 0.05) (Table 2). The depletion of pine litterfall of nutrients (Ca, Mg) and the increase in the content of P capable of retranslocation in fallen needles can be explained by the effect of airborne pollution: in the vicinity of smelters, the age of needles on branches decreases, since they fall off not only in phenological terms, and retranslocation processes involving mobile elements are disrupted (Nieminen and Helmisaari, 1996; Lukina and Nikonov, 1998; Rautio et al., 1998a; Nikonov et al., 2004). A higher P content can also be associated with elevated K and N concentrations as a manifestation of a relationship in the N : P : K ratio: an increase in the concentration of one element leads to an increase in the content of others (Sazonova et al., 2005). Calcium and magnesium are less mobile elements, and a decrease in their content may be caused by their leaching from living needles on trees by acidic precipitation (Lukina and Nikonov, 1998). In sparse technogenic forests, litterfall formed by assimilating pine organs is distinguished by high concentrations of Ca, Al, Fe, Ni, Cu, and S and low concentrations of Mn, Zn, and P (p < 0.05) (Table 2). The increase in the content of heavy metals (Ni, Cu, and Fe), the main components of emissions from the Severonikel smelter, and a decrease in the content of Mn and Zn in living needles (Sukhareva, 2013) can be explained by antagonism between these elements (Rautio et al., 1998b; Steinnes et al., 2000; Lukina et al., 2005) and between Mn and Fe (Kabata-Pendias and Pendias, 1989; Lukina and Nikonov, 1996; Barber, 1998; Sukhareva and Lukina, 2014). Pollution disturbs the redistribution of mobile elements, which results in their higher content in assimilating organs (Sukhareva, 2013). However, a low P content is observed in coniferous litterfall of sparse technogenic light forests; apparently, this is due to its initially deficient level in pine needles (Sukhareva and Lukina, 2014) and antagonism with Ca, as it occurs in spruce needles at the intense defoliation stage (Lukina et al., 2008). The high content of Ca in pine litterfall and in living pine needles in sparse technogenic forests can be associated with the absorption of calcium from soil waters formed in horizons rich in this element and an inflow of mineral particles from dusty surfaces of technogenic wastelands. In the vicinity of the smelter, where sparse technogenic forests are formed, soil parent rocks contain gabbro- and gabbronorites that are rich in major cations (Lukina and Nikonov, 1996, 1998; Lukina et al., 2008; Anan’eva et al., 2012).
Airborne pollution significantly affects the C/P ratio and, to a lesser extent, the N/P ratio. These ratios characterize the plant material quality for soil biota, including microbial decomposers (Table 1). According to the literature data, the C/P and N/P ratios in Pinus banksiana Lamb. needle litterfall in Canada amount to 391 and 10, respectively (Moore et al., 2006). On sampling plots used in this study, the average C/P and N/P ratios in coniferous Scots pine litterfall reach in background conditions 1982 and 11, respectively. In defoliating forests, the C/P and N/P ratios statistically significantly feature the lowest values; while in sparse technogenic forests, these ratios are high. Taking that the N content and C content in litterfall are similar regardless of the digression stage, this phenomenon can be explained by a large difference in the phosphorus concentration: it is high in defoliating forests and low in sparse technogenic forests.
Overall, industrial airborne pollution has a significant effect on the chemical composition of litterfall formed by assimilating organs of pine trees: the quality of plant material to be decomposed by microorganisms declines due to a decrease in the content of fertilizer elements (Ca, Mg, Mn, and Zn) and an increase in the heavy metal content and C/P and N/P ratios.
Intrabiogeocoenotic Variability of the Pine Needle Litterfall Chemical Composition in Pine Forests at Different Digression Stages
As is known, the elemental composition of litterfall formed by assimilating plant organs and the presence of secondary metabolites in it contribute to the formation of phytogenic zones of influence around trees (Aponte et al., 2013; Kolmogorova and Ufimtsev, 2018). In background conditions, the spatial intrabiogeocoenotic variability of the coniferous litterfall composition is most pronounced for Zn, K (R2 = 0.3), Ni, Cu, and Fe (R2 = 0.2) and least pronounced for P (R2 = 0.1) (Table 1). Plant material sampled under tree crowns is distinguished by a higher content of mobile K and P (p < 0.05), which may be due to the inflow of potassium with crown and trunk waters and, possibly, due to a larger proportion of young needles in litterfall under tree crowns (Table 3). In intercrown spaces, fallen pine needles contain more Fe, Zn, Ni, and Cu (p < 0.05), which may be due to background airborne technogenic pollution caused by the transfer of pollutants in aerosols spreading over considerable distances (Ershov et al., 2019).
In defoliating pine forests, spatial variability is most pronounced for Ca and P (R2 = 0.4–0.5), Mg, Mn, K, N, and the C/P ratio (R2 = 0.2–0.3); by contrast, it is practically not manifested for S and the C/N ratio (Table 1). Needle litterfall in undercrown spaces is distinguished by a higher content of Ca, Mg, K, Mn, P, N, and S (p < 0.05) (Table 3), which is associated with their intensive supply with crown and trunk waters as a result of the leaching of fertilizer elements from tree crowns (Ca, Mg, K, Mn, and P) and the inflow of S with acidic precipitation. The C/N and C/P ratios are higher in intercrown spaces (p < 0.05) (Table 3) due to the lower P content there and similar C concentrations in litterfall and in undercrown spaces. On a waste rock heap (in reclaimed areas previously occupied by overburden rocks from a coal pit), the total P content in Scots pine litterfall also reaches the maximum in undercrown and near-crown zones of closed artificial stands (Kolmogorova and Ufimtsev, 2018). In sparse technogenic forests, spatial variability is clearly pronounced only for Ca (R2 = 0.3), whose content in coniferous litterfall is higher under tree crowns (p < 0.05) (Table 3), which may be associated with intense leaching of Ca from needles and its subsequent inflow into litterfall with precipitation. The absence of differences in the content of other elements and their ratios in sparse pine forests can be explained by a high transparency of their crowns damaged by the pollution impact.
Seasonal Variability of the Pine Needle Litterfall Chemical Composition in Pine Forests at Different Digression Stages
In background pine forests, seasonal variability is manifested to the greatest extent for Mn and Fe (R2 = 0.5–0.6) and to the least extent for P, Cu, Zn, Ca, and the C/P ratio (R2 = 0.2–0.3); for S, it is practically not manifested (Table 1). Plant material sampled after the cold season (October–May) is distinguished by a high content of Fe, Zn, Cu, P, and S; after the warm season (June–September), it is distinguished by high concentrations of Ca and Mn and a higher C/P ratio (p < 0.05) (Table 4). According to literature sources, the larch litterfall sampled in spring was 10% richer in N and 40% depleted of Ca compared to litterfall sampled in autumn (Chul’diene, 2017). Two main periods of C and N inflow into the soil with Scots pine litterfall were identified in forests of Finland: May–October and November–April; the inflow registered in the first period is greater with a maximum in September (Portillo-Estrada et al., 2013). In the year of 2007, the content of Mn and Zn in pine needle litterfall in pine forests of Poland was higher in autumn; in 2009, it was higher in spring (Jonczak and Parzych, 2014). According to Finnish researchers (Rautio et al., 1998b), first-year pine needles in Russian forests feature (similar to our case) a high content of Fe, Cu, P, and S in spring and Ca and Mn in autumn. It must be noted that the increase in the content of Zn and Fe in needle litterfall during the winter period is not consistent with patterns identified for living needles in background conditions of the Kola Peninsula: for 2 years, the content of zinc and iron in living needles there was higher in August compared to June (Lukina and Nikonov, 1996).
In defoliating pine forests, seasonal variability is more pronounced for the content of Ni, Fe, Cu, Mn, Zn (R2 = 0.4–0.9), Ca, and Al and for the N/P ratio (R2 = 0.2) (Table 1). Coniferous litterfall of the cold season features higher concentrations of Al, Fe, Zn, Ni, and Cu and a wide N/P ratio, while litterfall of the warm period, similar to the background conditions, is distinguished by high concentrations of Ca and Mn (p < 0.05) (Table 4). The elevated content of fertilizer elements in litterfall sampled after the growing season is determined by the more active absorption of elements from the soil and their redistribution within the tree during the warm period. The retranslocation of Ca and Mn inside trees is impossible; as a result, these elements accumulate during the warm season and remain in fallen needles in background conditions and in defoliating pine forests, which is consistent with patterns identified for living needles (Lukina and Nikonov, 1996).
In sparse technogenic forests, seasonal differences are most clearly manifested for Ni, Zn, Cu, and Fe (R2 = 0.4–0.7) and, to a lesser extent, for Mn, Mg, and K (R2 = 0.3) (Table 1). Coniferous litterfall of the cold period of the year contains more Fe, Zn, Ni, and Cu; pine needles fallen during the warm season, more Mg, K, and Mn (p < 0.05) (Table 4); while in living needles, K and Mg are mobile, and their content decreases at the end of summer (Lukina and Nikonov, 1996). The accumulation of K and Mg by the end of the growing season can indicate a disturbance of retranslocation processes under the impact of pollution (Nieminen and Helmisaari, 1996).
A significant (by almost two times) decrease in the content of Fe and Zn in litterfall after the end of the growing season in all studied pine forests and a decrease in the content of Ni and Cu (p < 0.05) (Table 4) in pine forests exposed to airborne pollution is not typical for aging but still living needles. In background conditions, this phenomenon can be explained by the potential antagonism between these elements and Mn ions (Lukina et al., 2008); in areas affected by airborne technogenic pollution, it is supplemented by their leaching and flushing from the needle surface by acidic precipitation during the summer season.
CONCLUSIONS
Industrial airborne pollution has a significant effect on the chemical composition of litterfall formed by assimilating organs of pine trees. It is established that in north taiga pine forests exposed to technogenic airborne pollution caused by emissions from the Severonikel copper–nickel industrial complex, the content of fertilizer elements (Ca, Mg, Mn, and Zn) in Scots pine litterfall decreases, while the content of heavy metals (Ni and Cu) and values of stoichiometric C/P and N/P ratios increase. This indicates that the quality of plant material to be decomposed by soil biota declines.
Both in background conditions and under the impact of airborne technogenic pollution, the chemical composition of litterfall formed by assimilating organs of pine trees is distinguished by a significant intrabiogeocoenotic variability. In background conditions, coniferous litterfall features a higher content of K and P (supplied with crown and trunk waters) under tree crowns; in intercrown spaces, concentrations of Fe, Zn, Ni, and Cu are higher due to background airborne pollution. In defoliating forests, higher concentrations of Ca, Mg, K, Mn, P, N, and S in coniferous litterfall under tree crowns are determined by their increased inflow with crown and trunk waters due to the leaching of compounds containing these elements by acidic precipitation.
Seasonal variability in the chemical composition of pine litterfall has common features in background pine forests and in pine forests exposed to airborne technogenic pollution. Both in background conditions and in defoliating forests, fallen needles that enter litterfall traps during the warm (June–September) season are distinguished by a high content of Ca and Mn, because the retranslocation of these elements inside trees is impossible and they accumulate during the growing season. In sparse technogenic forests, Mg and K accumulate in coniferous litterfall by the end of the growing season, which indicates a disturbance of retranslocation processes under the impact of pollution. A significant decrease in the content of Fe and Zn in litterfall after the end of the growing season in all studied pine forests and a decrease in the content of Ni and Cu in pine forests exposed to airborne pollution can be explained by the antagonism between elements and their leaching and flushing from the needle surface by acidic precipitation during the summer season.
Overall, airborne technogenic pollution affects the chemical composition of coniferous litterfall in pine forests of the north taiga forest zone and contributes to seasonal variability both in the redistribution of elements within trees and in spatial features of the inflow of elements with litterfall, which can directly affect the state of forest ecosystems in the north and the fulfillment of their ecosystem functions.
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ACKNOWLEDGMENTS
We are grateful to E.A. Belova, an engineer at the Laboratory of Terrestrial Ecosystems, Institute of North Industrial Ecology Problems, Kola Science Center, Russian Academy of Sciences, for maintaining the institute’s monitoring network and sampling ecosystem components, including tree litterfall.
Funding
This study was performed as part of the State Task of the Institute of North Industrial Ecology Problems, Kola Science Center, Russian Academy of Sciences, project no. 0226-2018-0111 (AAAA-A18-118021490070-5).
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Ivanova, E.A., Lukina, N.V., Smirnov, V.E. et al. Effect of Industrial Airborne Pollution on the Chemical Composition of Pine Needle Litterfall at the Northern Distribution Limit of Pine Forests. Contemp. Probl. Ecol. 15, 851–862 (2022). https://doi.org/10.1134/S1995425522070113
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DOI: https://doi.org/10.1134/S1995425522070113