Concentration of Heavy Metals in Dominant Moss Species as an Indicator of Aerial Technogenic Load

V. Sh. Barkana and I. V. Lyanguzova
Lapland State Biosphere Nature Reserve
ul. Zelenaya 8, Monchegorsk, 184506, Russia
E-mail: barcan.valery2010@yandex.ru
Komarov Botanical Institute, Russian Academy of Sciences
ul. Professora Popova 2, Saint-Petersburg, 197376, Russia

DOI 504.5:581.52:630*424.5
   
    Abstract
   
    The concentrations of nickel and copper were determined in mosses Hylocomium splendens and Pleurozium schreberi sampled in 1991 and 2011 at the same sites in the Lapland State Biosphere Reserve located in the impact area of atmospheric emissions from the Severonickel Smelter Combine (Monchegorsk, Murmansk Region, Russia). Both moss species have been confirmed to adequately reflect the levels of aerial technogenic load and can be used equally to monitor environmental pollution from heavy metals. It has been statistically proven that not only the volume of atmospheric emissions of polymetallic dust and the distance to the pollution source affect the concentrations of heavy metals in the studied moss species, but the wind rose and relief are also of importance.
   
    Keywords: heavy metals, Kola Peninsula, aerial technogenic pollution, bryoindication of pollution
   
    The use of mosses as indicators of airborne technogenic pollution is justified by their living features: Mosses lack roots, they attach to the surface layer of the litter only with rhizoids, so there is practically no contact between the living (green) part of moss and contaminated soil. At the same time, mosses obtain moisture, minerals, and pollutants, including dust particles of technogenic metal compounds, from the air. The absence or strong reduction of the cuticle in these moss species stipulates penetration of ions through the surface directly to the ion exchange sites on the cell walls. Since moss leaves have only a one-cell surface layer, they remain in very close contact with the surrounding atmosphere, and this way nutrients and heavy metals enter their tissues. Comparison of heavy metal accumulation by various plant species revealed a significantly higher accumulation level in lichens and especially in bryophytes in the impact area of non-ferrous metallurgy enterprises (Salemaa et al., 2004; Lyanguzova, 2010). In addition, tight branching allows mosses to filter the air effectively and absorb most dust from the atmosphere. Taylor and Witherspoon (1972) found about 100% initial intake of heavy metal was intercepted by mosses and about 20% can be washed off by rain later.
    Biomonitoring atmospheric pollution from heavy metals using various moss species became a frequent practice in Europe in the beginning of the 1970s. The studies in Sweden (Ruhling and Tyler, 1969, 1971, 1973), Norway (Steiness, 1977, 1985), Finland (Pakarinen and Tolonen, 1976; Makinen, 1983), and Poland (Grodzinska, 1978) have shown that two dominant moss species Hylocomium splendens and Pleurozium schreberi are interchangeable and can adequately reflect level of environmental contamination with heavy metals. After intercalibration of analytical procedures among the participating laboratories, one determined concentrations of nine elements in living parts of moss: copper, nickel, lead, chromium, iron, arsenic, cadmium, vanadium, and zinc, as well as found local anomalies of metal concentrations in mosses in the areas of ferrous and non-ferrous metallurgy enterprises of northern Sweden, Norway, and Finland, in addition to the far north of Norway and Finland in the areas adjacent to the copper-nickel combines of the former Soviet Union. Both Russian and foreign researchers (Onianwa, 2001; Nikodemus et al., 2004; Ermakova et al., 2004; Koroleva, 2004; Zhang et al., 2009; Blagnyte and Paliulis, 2010; Koroleva and Puhlova, 2012; Rukovodstvo ..., 2013; Ryzhakova et al., 2013) have continued developing the studies up to the present time. However, almost all surveys of contaminated areas were carried out once, often together with a study of heavy metal content in other components of terrestrial ecosystems. Only in recent years there have begun to appear works assessing the dynamic trend of heavy metal content in certain plant species following a significant reduction in aerial technogenic load (Dinamika ..., 2009; Zverev, 2009; Lianguzova, 2008, 2010, 2016; Sukharyova, 2013; Sukharyova and Lukina, 2014). The study goal was to compare the levels of accumulation of heavy metals (Ni, Cu) by two dominant moss species Pleurozium schreberi and Hylocomium splendens in the northern taiga ecosystems during the high (1991) and low (2011) aerial technogenic load.
   
    MATERIALS AND METHODS
   
    Founded in 1930, the Lapland State Biosphere Reserve lies in the impact area of the Severonickel Smelter Combine, the largest producer of metallic nickel in Europe, which began operations in 1938. The negative impact of the plant’s atmospheric emissions, which include sulfur dioxide and polymetallic dust containing mainly nickel and copper compounds, onto individual components of the forest ecosystems has been thoroughly studied and described in more than 2000 publications (Barcan and Kovnatsky, 1998; Kozlov and Barcan, 2000; Kozlov et al., 2009; Dinamika..., 2009; Lyanguzova, 2008, 2010, 2016).
    Figure 1 shows a scheme of the sampling area; a brief description of the 1991 and 2011 moss sampling sites is provided in Table 1. The moss sampling sites represented an open area from several up to ten square meters in the forest community, at least 300 m away from the roads. At each site, moss samples were collected from at least three places along a triangle with a side of 50-100 m long. Then individual samples were put into a combined sample, from which all accidental inclusions were removed.
    Unwashed moss samples were dried at 40°C; total dry sample mass was over 10 g. For the analysis one picked (with clean hands or in rubber gloves) the top three segments of each Hylocomium splendens specimen or green parts of each Pleurozium schreberi specimen. A test portion of air-dry moss sample was heated in a mixture of concentrated acids HNO3 and HCl at the ratio of 4:1. Cooled solution was filtered into polyethylene containers.
    The nickel and copper content in the solution was determined on the atomic absorption spectrophotometer AAS-36 in duplicates. The relative error in identification of each metal did not exceed 10-15%.
   

Fig. 1. Moss sampling sites in 1991 and 2011 (SSC, Severonickel Smelter Combine).

The statistical analysis was performed using the STATISTICA 10.0 package with dispersion and correlation analyses. Statistical significance of differences was determined by nonparametric Mann-Whitney test.

Table 1. Brief description of moss sampling points in 1991 and 2011 years
Nos. of moss sampling points	Place – names of sampling points	Ñoordinates		Distance from the smelter, km
		northern latitude	eastern longitude
3 á	Kurt–varench	67° 37' 40''	32° 44' 00''	34.0
8	Former Ñhuna settlement	67° 38' 10''	32° 36' 20''	34.4
9	El–yavr–way brook	67° 39' 00''	32° 40' 00''	32.2
5	Koos–nyark cape (the north shore of Chuna lake)	67° 38' 35	32° 31' 30''	34.9
2	Vuytem– nyark cape (the south shore of Chuna lake)	67° 38' 00''	32° 31' 00''	36.0
7	Portage Chuna lake–Okht lake	67° 34' 45''	32° 23' 30''	43.7
22	Ñordon Nyavka	67° 41' 20''	32° 03' 30''	43.1
23	Ñordon Mavra	67° 42' 30''	31° 53' 00''	47.9
16	House on the brook Lower Sylp way	67° 51' 00''	32° 15' 00''	27.1
4	Watch house Squirrel	67° 46' 00''	32° 11' 30''	33.4
37	North–west extremity of Chuna lake	67° 42' 00''	32° 18'° 00''	34.8
25	Left shore of Vitte river ñlose Seyd lake	67° 49' 45''	32° 40' 30''	13.7
10	1213 km of the road Saint–Petersbourg–Murmansk	67° 34' 30''	32° 35' 00''	41.2
11	1205 km of the road Saint–Petersbourg–Murmansk	67° 33' 30''	32° 27' 00''	44.8
12	1198 km of the road Saint–Petersbourg–Murmansk	67° 31' 00''	32° 21' 00''	50.8
19	Turn of the road Saint–Petersbourg–Murmansk to Apatity, 10-th km	67° 37' 00''	32° 59' 00''	35.2
20	Turn of the road Saint–Petersbourg–Murmansk to Apatity, 20-th km	67° 34' 40''	32° 13' 00''	41.9

RESULTS AND DISCUSSION
   
    Both in 1991 and 2011, the levels of heavy metal accumulation were comparable for Pleurozium schreberi and Hylocomium splendens at different sampling sites (Table 2). The nonparametric Mann-Whitney test found no interspecies differences in the content of heavy metals in the studied mosses both in 1991 and 2011. It followed that both moss species could be used equally for monitoring environmental contamination with heavy metals. The absence of species specificity of the two studied mosses has already been established (Ramenskaya, 1974; Ruhling and Tyler, 1973; Pilegaard et al., 1983; M?kinen, 1983; Steinnes, 1985). Analyzing microelement composition of the plants of the Kola Peninsula, Ramenskaya (1974) noted the nickel and copper concentrations in both moss species were 14 times higher their background levels in the Monchegorsk district.
    According to Ramenskaya (1974), regional background concentrations of nickel and copper in the studied moss species averaged 4-5 mg/kg of dry matter. Our data from various areas of the Kola Peninsula showed average concentration of nickel in the green parts of Pleurozium schreberi within the limits of 7.5-8.5 mg/kg and average copper content from 4.6 to 9.9 mg/kg. In 1991 in the Lapland Reserve, average nickel concentration was over 12 times its background content, and copper content, over 23 times. According to the nonparametric Mann-Whitney test, average concentrations of heavy metals in 2011 decreased significantly in both studied mosses (z = 2.74-4.53, p = 0.0000-0.006) and were only 4 times higher the background concentrations of each heavy metal. Thus, it was a sharp reduction in atmospheric emissions by the Severonickel Combine (Fig. 2) that led to a significant decrease in the content of heavy metals in both moss species, as the sampling sites remained the same during both periods of observation. Similar patterns in the dynamic trend of the levels of heavy metal accumulation by assimilation organs of higher plants were previously noted by us (Languzova, 2008, 2010, Dinamika..., 2009) and other researchers (Zverev, 2009; Sukhareva, 2013; Sukhareva and Lukina, 2014).
   

Table 2. Metal concentrations in moss samples from the same points by 1991 and 2011 years, ppm, dry matter *n.d., no data.
## of point sampling	Distance from smelter source, km	Ni				Ñu
		Pleurozium schreberi		Hylocomium splendens		Pleurozium schreberi		Hylocomium splendens
		1991 ã.	2011 ã.	1991 ã.	2011 ã.	1991 ã.	2011 ã.	1991 ã.	2011 ã.
36	34.0	139	31	n.d.*	n.d.	258	29	n.d.	n.d.
8	34.4	143	54	161	60	285	41	350	42
9	32.2	155	68	170	82	271	44	202	45
5	34.9	53	62	n.d.	n.d.	111	47	n.d.	n.d.
2	36.0	112	48	n.d.	n.d.	112	32	n.d.	n.d.
7	43.7	94	36	61	14	209	25	174	13
22	43.1	42	7	33	5	76	7	92	9
23	47.9	21	5	23	6	39	7	46	8
16	27.1	38	5	33	4	43	4	37	6
4	33.4	23	7	20	5	36	10	29	10
37	34.8	73	34	61	24	43	22	54	20
25	13.7	244	42	252	44	608	33	598	42
10	41.2	60	57	n.d.	n.d.	136	42	n.d.	n.d.
11	44.8	99	31	66	24	113	25	101	21
12	50.8	121	36	143	43	160	25	115	30
19	35.2	131	50	121	41	230	38	252	36
20	41.9	133	34	140	37	154	35	101	36

This study painted an ambiguous picture of the change in the level of the heavy metal accumulation by Pleurozium schreberi and Hylocomium splendens over two periods of observation. In almost all of the 1991 samples, copper content was higher than nickel content in both studied species, while in 2011 there was either a reversed ratio of concentrations of heavy metals or their concentrations were approximately equal (Table 2). However, the differences were not confirmed statistically by the Mann-Whitney test (z = -1.65 ... 1.45, p = 0.1 ... 0.78) for two observation periods and both moss species. At the same time, the volume of atmospheric emissions of nickel during 1990-2001 was significantly higher than those of copper (z = 2.83, p = 0.005); and during 2002-2013 the volumes of emissions of the metals did not differ significantly (z = -1.27, p = 0.204) (Fig. 2). Consequently, the ratio of nickel and copper concentrations in mosses was not always directly related to the ratio of the volumes of atmospheric emissions of heavy metals by the source of pollution, or may be due to internal properties of the moss species.
    For two observation periods, minimum concentrations of both metals in the studied mosses were found at sampling sites 4 and 16, located 27-33 km from the combine and at site 23, located 48 km from the combine (Table 2). The maximum nickel and copper concentrations in the studied moss species were detected at sites 5, 9, and 25, located 35, 32, and 14 km from the combine, respectively. However, the maximum concentrations of both metals were not always found at the same sampling sites. Thus, in 1991 the maximum nickel content in Hylocomium splendens was at site 9 and maximum copper content, at site 25; in 2011 the maximum nickel content in Pleurozium schreberi was at site 9, and maximum copper content, at site 5 (Table 2).

The correlation analysis of the data revealed a significant relationship only between the copper content in the studied moss species and the distance from the source of pollution, both in 1991 and 2011 (r = -0.64 ... -0.60, p <0.05); in all other cases the correlation between those parameters was absent. Thus, for example, at sampling site 12, the most remote from the smelter combine, concentrations of heavy metals in the studied moss species were not minimal during two observation periods. The lowest nickel concentration in both moss species was found at site 16, and the lowest copper content, at site 4, located 27-33 km from the smelter combine (Table 2). It follows that the levels of the heavy metal accumulation by mosses were apparently affected not only by the distance from the source of pollution, but also by the wind rose and relief, since sampling sites 4, 16, 22, 23, and 37 were located west of the combine and were shielded by the Chunatundra mountain range from the wind flow of pollutants (Fig. 1).
    The hypothesis was tested with variance analysis. The moss sampling sites were grouped into 2 sets: the first set included sites 4, 16, 22, 23, and 37; the second set had sites 8, 9, 10, 11, 12, and 37, located to the south of the smelter combine along the St.Petersburg-Murmansk Highway. One-way analysis of variance using the nonparametric Mann-Whitney test revealed significant differences between the sets: for Pleurozium schreberi (in 1991 and 2011) z = 2.74 ... 2.65 and p = 0.0062 ... 0.0081; for Hylocomium splendens z = 2.45 ... 2.46 and p = 0.0143 ... 0.0139. Thus, it confirmed the hypothesis of the wind and relief influence on concentrations of heavy metals in the studied moss species. Unfortunately, the available data did not allow for separation of the effects of the two factors on the levels of the heavy metal accumulation by moss.
    In 2011 the atmospheric emissions of the smelter combine decreased 7.7 times for nickel and 3.6 times for copper relative to those in 1991. The comparison of the order of decrease in concentrations of heavy metals in two moss species sampled at the same sites in 1991 and 2011 revealed a dissimilar decrease in concentrations of two metals and differences at various sampling sites (Fig. 3). In 2011 in Pleurozium schreberi nickel concentration decreased by an average of 3.4 times and copper content declined by 6.6 times in comparison with that in 1991, while the range of variation was from 0.9 to 7.6 times for nickel and from 2.4 to 18.4 times for copper. In 2011 in Hylocomium splendens nickel concentration decreased by an average of 4.1 times and copper content declined by 6.7 times with respect to their concentrations in 1991, while the order of decrease in nickel content was in the range of 2.1-8.3 times and in copper content, 2.7-14.2 times. It is noteworthy that the minimum and maximum orders of decrease in nickel and copper concentrations were observed at different sampling sites. For example, for both studied moss species, maximum decrease in nickel concentration was detected at site 16, located 27 km from the Combine, and in copper concentration, at site 25, located 14 km from the Combine (Fig. 3). For Pleurozium schreberi minimum decrease in concentrations of both nickel and copper was observed at site 5, located 35 km from the source of pollution; and for Hylocomium splendens minimum reduction in nickel concentration was noted at site 9, located 32 km from the plant, and in copper concentration, at site 37, located 35 km from the source of pollution. Thus, the decrease in nickel and copper concentrations of both moss species was disproportionate to the reduction in the volumes of atmospheric emissions of heavy metals by the Severonickel Smelter Combine. Earlier, we noted the disagreement between the time of change in the heavy metal concentrations in the higher plants and different levels of aerial technogenic load (Lianguzova 2016, in press).
    One can make several assumptions to explain such an ambiguous picture of accumulation of heavy metals by mosses and reduction in their concentration at the background of a decrease in dust emissions into the air by the Severonickel Smelter Combine. First, dust components in the Combine’s atmospheric emissions vary both in particle size and chemical composition. Fine polymetallic dust emitted into the atmosphere at different stages of the technological cycle contains mainly sulfides and metal oxides, as well as metallic nickel and copper (Barkan, 2008). These compounds have different solubility in water and acidified atmospheric fallout, and even more so in soil solution with pH = 4.0-4.5. It has been proved that spherical particles up to 5 ?m in size from the contaminated air occur in the organic horizon of podzols of the buffer and impact zones; their shape, surface morphology, and chemical composition are characteristic of the dust and gas emissions from matte or ore melting furnaces (Languzova et al., 2016, in press). The dust particles from the air are deposited on moss surfaces and can penetrate its tissues. Current chemical analysis method did not allow for separation of surface deposition of dust particles from metal concentration in tissues. Second, it was impossible to collect all moss samples over such a vast territory at the same time, therefore, some of the samples may have been collected during the dry season, and in some samples rain could have partially washed the dust off the moss surface. Third, it is well known as well as has also been presented by us, the relief and winds also play an important role in the distribution of air pollutants. Fourth, the rate of decrease in the nickel and copper concentrations in the studied moss species may be stipulated by the chemical nature of metals and their physiological role as vital microelements.
   
    CONCLUSIONS
   
    This study on the levels of heavy metal accumulation by two dominant moss species Pleurozium schreberi and Hylocomium splendens against the background of high (1991) and low (2011) aerial technogenic load showed that nickel and copper concentrations in living parts of the studied moss species adequately reflected the intensity of aerial technogenic pollution on the Lapland Reserve from the atmospheric emissions of heavy metals by the Severonickel Combine (Monchegorsk).
    Both studied moss species can be used equally to monitor aerial technogenic pollution from heavy metals due to the absence of significant differences in the metal content in the living parts of Pleurozium schreberi and Hylocomium splendens at the same sampling sites.
    The absence of a direct correlation between the levels of heavy metal accumulation by the studied moss species and the distance to the Severonickel Combine, as well as an ambiguous picture of the changes in nickel and copper concentrations in mosses during two observation periods confirm the influence of other factors (wind rose, relief) on the intake of heavy metals from contaminated air by bryophytes and heavy metal accumulation in plant tissues. In connection with this, when planning a network of monitoring sites, one should take into account not only the actual distance to the source of aerial technogenic pollution, but also the rose of prevailing winds in the given territory and its relief.
    The disproportionality and disagreement between the time of the decrease in the heavy metal concentrations in the studied moss species and the sharp reduction in atmospheric emissions from the non-ferrous metallurgy combine are due to numerous reasons, many still unknown and require further studies.
   
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Translated by Irina P. Goodrich