Changes in the vascular flora of a postflotation zinc–lead ore spoil heap of the “Orzeł Biały” mining and smelting works in Bytom (Silesian Upland) after 15 years

A study on vascular flora of a Zn–Pb ore spoil heap of the “Orzeł Biały” mining and smelting works in Bytom, Poland, was carried out in the 2017–2018 growing seasons. The aim of this study was to: (i) present the characteristics of current vascular flora that colonizes the Zn–Pb heap, (ii) describe its dynamic tendencies and directions of changes after 15 years, and (iii) identify species that can be useful for planting as a part of biological reclamation. Ninety-two mostly native species of vascular plants, belonging to 36 families and 77 genera, were found on the examined heap. In the spectrum of life forms, hemicryptophytes prevailed over therophytes and geophytes. The most numerous ecological groups were ruderal and meadow species. As regards life strategies, highly competitive species and taxa with mixed CSR strategies dominated. The basic mode of seed dispersal was anemochory. In terms of habitat preferences, species associated with moderately light, warm, fresh, neutral, and medium fertility soil dominated in the species composition of the studied flora. In 2017–2018 compared to the 2002 growing season, statistically significant differences were found in the origin, life forms, ecological groups, life strategies, mode of seed dispersal of species and their habitat preferences relative to light, temperature, pH, and productivity. Frequently recorded pseudometallophytes (Agrostis capillaris, Cardaminopsis arenosa, Daucus carota, Deschampsia caespitosa, Leontodon hispidus, Plantago lanceolata, Silene vulgaris, Rumex acetosa) can be used for planting as part of biological reclamation of the area.


Introduction
The history of extraction of ore-bearing dolomite deposits in the region of Bytom-Tarnowskie Góry dates back to the beginning of the twelfth century [1]. Because the deposits of galena (Pb-Ag ores) were shallow and easy-to-extract, they were depleted in the twentieth century. The increasing knowledge in the field of exploration of ores and the further development of mining technologies (including shafts and drainage systems) in the mid-fifteenth century meant that even deeper deposits of galena began to be extracted [2]. The exploitation of ore-bearing dolomites also increased because of the significant demand from metallurgy in the twentieth century, which meant that ores that were rich in Zn and Pb were quickly depleted and deposits that were poorer in Zn and Pb had to be enriched using a flotation process [3][4][5]. It is estimated that 36 mln Mg of postflotation wastes that contained 2.9% Zn and 0.6% Pb were stored on postflotation Zn-Pb spoil heaps situated in the Bytom region [6,7].

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The most frequent methods for managing these areas include sodding and afforestation. A higher content of heavy metals in wastes, the fine grain size of the substrate, which is easily carried by wind and water, nutrient deficiency, unfavorable air and water conditions, higher pH, and frequently salinity and insolation meant that these spoil heaps were slowly colonized primarily by herbaceous plants [8,9].
The process of spontaneous succession appeared to be the most successful. Studies that have been conducted on postindustrial sites have revealed that species that occur in the surrounding area, which constitute the local species pool, frequently play an important role in the initial stages of the formation of spontaneous vegetation cover [10]. The developing plant communities are poorer in species, and are frequently dominated by expansive or alien species. They are usually composed of common native taxa that are associated with meadow habitats, such as Achillea millefolium, Daucus [7,9,[11][12][13]. Plants that grow in metalliferous areas have developed different strategies that enable them to grow in hostile habitats in which there is high concentration of heavy metals in the soil substrate [14]. Most species (so-called excluders) bind toxic metal ions in the roots, thereby preventing them from being translocated into their aboveground parts. Other species, which are called accumulators, can accumulate a significant amount of metals in their aboveground parts [15].
Knowledge about the formation of plant cover on postflotation tailings has a practical aspect. The use of spontaneous succession in the reclamation of areas that have been degraded by Zn-Pb ore mining and processing permits sustainable and stable ecosystems to be created and the costs of reclamation to be reduced [10,16]. The aims of this research were to (i) present the current state of the vascular flora of the "Orzeł Biały" mining and smelting works dumping ground in Bytom, (ii) describe its directions of changes after 15 years, and (iii) identify the species that could be planted as a part of biological reclamation.

Study area
The lead and zinc spoil heap is located on the Bytom-Katowice Plateau in the Silesian Upland, Poland (N 50°20'20", E 18°56'35") ( Fig. 1). The climate of the mesoregion is characterized by a predominance of oceanic influences over continental ones as well as the sporadic interaction of tropical air masses from the southwest via the Moravian Gate. In the coldest part of the year, arctic cold air from the north also reaches the area. The relative air humidity ranges from 68% to 84%, the mean annual temperature is +8.12°C (January −3°C, July +16.8°C), and the annual precipitation is around 723 mm, with the most precipitation being recorded in July and the least precipitation in February [17]. The spoil heap lies beside the Lubliniec-Katowice railway route and national roads (No. 79 and 94). From the east, it abuts the "Żabie Doły" nature landscape complex, the main components of which are the water reservoirs that have been created in the subsidence basins because the areas above the sites where coal, lead, and zinc ores were extracted have collapsed [5,18] (Fig. 1).
The mosaic vegetation of this area is composed of rushes, some wet and fresh meadows, and agricultural crops [19]. The byproducts from the processing of lead and zinc ores by the "Orzeł Biały" mining and smelting works, which include 1.95 million tons of postflotation wastes containing 2.9% Zn and 1.1% Pb, were deposited on a truncated cone heap that covers 16.95 ha in the years 1926-1989. [7]. After the exploitation ceased, the heap was reclaimed three times: in the years 1971-1975, in 1987, and during the 1990s. The aim of the technical reclamation was to improve the habitat conditions of the heaps by correctly forming the top and slopes, covering them with a coarse substrate in order to improve the water conditions. Moreover, lime and fertilizers were used to improve the physicochemical parameters of the substrate [20].

Data sampling and analysis
Field studies were carried out on the postflotation zinc-lead spoil heap of the "Orzeł Biały" mining and smelting works in the 2017-2018 growing seasons. We made 53 phytosociological relevés (5 × 5 m) in the field, primarily on the sites where relevés were made in 2002 [7]. However, since some parts of the spoil heap that were covered by vegetation were destroyed by humans (e.g., by riding quads and secondary exploitation of the flotation tanks) or due to water and wind erosion, it was often not possible to do phytosociological research on the same sites. The nomenclature of the taxa follows Mirek et al. [21]. The vascular flora of the investigated spoil heap was analyzed in terms of the share of the species that belong to botanical families [21], the frequency of the occurrence of a species, the tolerance of the taxa to an increased Zn and Pb content in the soil [22][23][24], the shares of the geographical-historical groups [21,[25][26][27], life forms [22,25,26], ecological groups [25,26,28,29], life strategies [28,30,31], and the mode of seed dispersal [28]. The habitat preferences of the species were assessed based on the Ellenberg's indicator values (EIVs) for light (L), temperature (T), moisture (F), soil reaction (R), and productivity (N) [32,33]. We calculated average EIV for each phytosociological relevé as well as mean numbers of species with a given value of the indicator that occur in a given relevé.
In order to demonstrate any temporal changes in the species composition and diversity of the vascular flora of this metalliferous site after almost 15 years from the previous studies, the data that were presented in the work by Kompała et al. [7] and some unpublished data were also used for further analyses. In order to examine the significance of the differences in the species composition of the analyzed site between the 2002 and 2018 growing seasons, the nonparametric Mann-Whitney U test was used. All analyses were calculated in the STATISTICA 13.1 software [34].
It is worth emphasizing that there was an increase in the share of apophytes (from 77.0% to 80.4%). Kenophytes dominated among anthropophytes (13.0%). They were primarily represented by invasive species that are recorded quite often (frequency class III) such as Robinia pseudacacia and Solidago gigantea. The share of archaeophytes decreased (from 9.8% to 4.3%) (Fig. 2). There was a decrease in hemicryptophytes (from 62.3% to 46.7%) and therophytes (from 19.7% to 10.9%) in the spectrum of life forms. In contrast, the participation of geophytes (from 6.6% to 16.3%) and phanerophytes, including trees (from 6.6% to 13.0%) and shrubs (from 4.9% to 10.9%), increased considerably (Fig. 3).
In the ecological spectrum, there was a decrease in the share of meadow species (from 39.3% to 23.9%) and an increase in the share of ruderal (from 24.6% to 31.5%) and forest species (from 6.6% to 14.1%) (Fig. 4).
The share of species with a high competitive ability (C-strategists) (from 47.5% to 54.3%) as well as CS strategy (from 1.6% to 4.3%) increased. Conversely, the participation of taxa with mixed strategies such as CSR (from 26.2% to 21.7%) and SR (from 13.3% to 0%) decreased (Fig. 5).
The pattern in the mode of seed dispersal did not change drastically between 2002 and 2018. Dispersal by wind (anemochory) decreased slightly from 70.5% to 67.4% and was dominant over the zoo-(from 14.8% to 17.4%) and autochorous (from 11.5% to 10.9%) modes (Fig. 6).   Taking into account the number of species with a given value of the indicator, the values of almost all indices decreased between years, except for indicators of poor soils and extremely rich soils, indicators of acid to moderately acid soils, dry and moist soils (Tab. 2).
Analysis of the habitat preferences of the species calculated for relevés in terms of light, temperature, soil reaction, and nutrients showed a decrease in mean values of temperature and soil reaction, whereas the mean values of the indices for light and nutrients increased during the examined growing seasons (Tab. 3).

Discussion
The postindustrial sites that are connected with the processing of zinc and lead ores are relatively difficult to colonize by plant species. They are often a kind of environmental island in the surrounding urban landscape. The composition of the vascular flora of these areas is undoubtedly affected by many abiotic factors such as the age of the spoil heap, the physicochemical conditions of the substrate, some reclamation activities as well as biotic factors. These include species richness and species diversity as well as functional diversity. It is connected with the species traits that are associated with persistence, dispersal and regeneration after disturbances, and the composition of local flora that occurs in the vicinity of the spoil heaps. Such traits constitute the life strategies of a species and enable them to adapt to given habitat conditions, and they also related to the advancement of succession [9,12,35,36].
The current vascular flora of the postflotation zinc and lead ore spoil heap of the "Orzeł Biały" mining and smelting works comprises 92 species of vascular plants and is richer in species compared to the 2002 growing season when only 61 taxa were found. There was a decrease in common species (frequency class VI between years), whereas the number of rare species increased almost two-fold between the years examined.  We found statistically significant differences in the species composition of vascular flora between the examined periods in relation to the origin, life forms, and life strategies of the species, share of ecological groups, mode of seed dispersal as well as in the preferences of the species in terms of light, temperature, pH, and nutrients.
During the succession that occurred on the lead and zinc spoil heaps, the number of native species (apophytes) increased. Similar results have also been obtained by other scientists who studied spontaneous succession on coal mine spoil heaps [37,38], sand and gravel pits [39,40], reclaimed and spontaneously vegetated Zn-Pb mine wastes in southern Poland [41,42], or serpentinite waste dumps [43]. The composition of the vascular flora of the postmining lead and zinc spoil heaps is connected with the local species pool. In the past, the area of "Żabie Doły" was covered by rushes and wet meadows, some segetal as well as ruderal communities, in the floristic composition of which native species were primarily found. These are frequently better adapted to habitat conditions on spoil heaps than alien species [43]. Among the alien species that occurred in the vascular flora that was studied, Solidago gigantea was found on the top as well as at the bottom of the spoil heaps; however, it only formed rather small patches. During the reclamation works, the alien species Robinia pseudacaccia as well as some shrubs and trees were planted in order to improve the soil conditions of hostile habitats as well as to initiate the reclamation of the land into a forest. The black locust is a fast growing legume that has a high survival rate, a wide ecological amplitude, and its saplings are easy and inexpensive to produce in tree nurseries [44]. However, it has a negative impact on the diversity of native flora, and therefore it should not be deliberately planted. Grasses are one of the most numerous functional groups (family) in the vascular flora of a spoil heap. Plastic and fast response of grasses to many environmental stresses as well as their colonization abilities enable them to survive in environments that have been transformed by man. That is beneficial in planning reclamation works since grasses can fulfill the antierosion, soilforming, as well as ornamental role [45]. Some of them have a well-developed root system (Deschampsia caespitosa, Festuca arundinacea) and are able to grow well in bad water and air conditions in the soil and can bind the fine material of a spoil heap, thereby protecting it from water and wind erosion. Some expansive grasses such as Calamagrostis epigejos can play the role of a dominant in some vegetation patches. It has the socalled internal nitrogen cycling, a wide ecological amplitude, reproduce both vegetatively and generatively, and produce a thick layer of dead organic matter [46]. Other grasses such as Festuca ovina or Agrostis capillaris are frequently found on lead and zinc spoil heaps and cover large areas [47,48]. They are tufted, often patch-forming grasses that can adjust to alkaline pH, salinity, as well as a higher content of heavy metals in the soils. The persistence and colonizing ability of Agrostis capillaris result from the diversity of its regenerative strategies, the mobility of seeds, and its capacity to lateral spread [49,50]. Another species that can adapt to the habitat conditions that exist on spoil heaps is Silene vulgaris. This species has some ecotypes that can grow in these habitats. The lack of water, a low nutrient content, and a higher content of heavy metals mean that this species has many morphological (small stature, small but thicker leaves compared to individuals from seminatural habitats), anatomical (palisade and sponge layer), and physiological adaptations (chlorophyll fluorescence) that have enabled it to survive in hostile habitats [51,52].

Growing season 2002 2018
Origin of species An increase in the fertility of the substrate made it possible for species to enter during the later stages of succession. These were mainly geophytes (e.g., Calamagrostis epigejos, Calystegia sepium, Carex hirta, Convolvulus arvensis, Epipactis helleborine, Equisetum arvense), whose share in the species composition of the examined flora increased almost threefold in the studied periods. Conversely, the share of hemicryptophytes and therophytes in the flora decreased since 2002 in favor of geophytes. Some trees (Betula pendula, Populus tremula, Sorbus aucuparia, S. intermedia) and shrubs (Frangula alnus, Hippohaë rhamnoides, Spiraea media) were only found in the northwest part of the heap. During succession, the participation of phanerophytes in the spectrum of life forms and the participation of forest species in the ecological spectrum of the flora increased. Most of these were introduced by humans during reclamation works [7,20]. Nevertheless, only in this part of heap was succession in the shrub-forest direction observed. This was probably due to the fact that the litter of deciduous trees and bushes is relatively easily decomposed, which enriches the soil with nutrients [10].
We expected that the number and frequency of meadow species as well as the taxa that are associated with sandy and xerothermic grasslands would increase during spontaneous succession since these species frequently overgrow these types of habitats and occur in similar natural conditions, e.g., xerothermic grasslands [10]. However, there was a decrease in the share of meadow species in favor of the ruderal taxa between 2002 and 2018. The meadow species were often dominated by common taxa, whereas rare species were dominant among the ruderal species. The decrease in the share of meadows species was probably connected with the fact that there is a lack of propagules of these species in the vicinity. Wet and fresh meadows that occurred in the vicinity of the Zn-Pb spoil heaps in 2002 have completely disappeared. The share of psammophilous and xerothermic grasslands species did not change between the years.
Anemochory appeared to be the most frequent seed dispersal mode in both the periods that were studied, followed by zoochory, which indicates the early stages of succession [37,38]. The first mode enables species to disperse for long distances as well as to get to the spoil heap from surrounding vegetation. Such a mode of dispersal is typical of some species from the Poaceae family as well as other forbs of both native and foreign origin (Conyza canadensis, Erigeron annuus, Solidago sp.). In turn, zoochory enables some shrubs and trees to be dispersed over a short distance [43].
As was already stated in another paper on succession at postindustrial sites, the trends can differ in respect to the life history traits [40,41]. Frequently, a transition from R-strategists to C-or S-strategists is observed in the latter stages of succession [31,53,54]. In our research, the number of C-strategists and CS-strategists increased, whereas the number of Rstrategists decreased between 2002 and 2018. Řehounková and Prach [40] found that ruderals only occurred in gravel sandpits at the beginning of succession; however, they did not expand very much because of the lack of nutrients and the acid pH of the sites. On the lead and zinc spoil heaps, the number of ruderals was also lower. Some disturbances that occurred at the beginning of the succession, open or bare sites, harsh habitat conditions as well as a lack of competitors enabled them to become established. The low level of diversity of the examined flora is probably connected with the unfavorable environmental conditions that still occur on the spoil heaps almost 50 years after the material ceased to be deposited after the period 1926-1970. The substrate of the spoil heaps still contains a higher concentration of heavy metals, mainly zinc, lead, and cadmium, which makes it difficult for vascular plant species to colonize them and grow there [7,55,56]. Long periods without precipitation and a higher average mean temperature have caused the surface and slopes of flotation tailings to undergo heavy erosion and therefore the existing plant cover has been depleted. Part of the flotation tank is currently being taken apart, which has caused further damage to the vegetation.  Moreover, the vegetation cover of the surface of the spoil heap was devastated because local residents practised various sports on them. About one-third species of the vascular flora of the lead and zinc spoil heap prefer an alkaline pH of the substrate. In alkaline soils, most heavy metals, even when their total content in the soil is high, occur in an insoluble form and therefore they are not available for plants. On the other hand, the pH in the root zone is usually lower than that outside of it, which can increase the availability of toxic metals for plants [35]. A high concentration of heavy metals in the soil also slows down the decomposition of organic matter and thus limits the availability of basic nutrients (nitrogen and phosphorus) for plants [36]. A sandy-clay substrate, which mainly consists of fine grains with a diameter of less than 0.5 mm, is characterized by poor water and air conditions [55,56]. Adverse graining reduces the infiltration of water during precipitation and also reduces the water uptake by soil capillaries from the deeper soil layers during drought. The consequences of this include the intensification of water erosion during precipitation and an increase of wind erosion during drought as well as large fluctuations in the temperature in the upper substrate layer [6,8]. In addition, small dried grains of substrate can be blown by the wind, which exposes the roots of some plants and completely overwhelms others [9]. Some species have adapted to colonize areas with an increased concentration of heavy metals and constitute spontaneous flora. A list of 145 species of vascular flora that are confined to metalliferous areas and occur with a high frequency and abundance was prepared by Rostański et al. [24]. On the studied Zn-Pb spoil heap, they are represented by pseudometallophytes such as Agrostis capillaris, Cardaminopsis arenosa, Daucus carota, Deschampsia caespitosa, Leontodon hispidus, Plantago lanceolata, Silene vulgaris, and Rumex acetosa [22][23][24]. The above-mentioned taxa were also often recorded by Rostański and Kapa [57] and Skubała [12], who explored the vascular flora of other Zn-Pb spoil heaps near the study area. These species have developed a metal-exclusion strategy and can grow on soil with an increased zinc and lead content [23]. The use of pseudometallophytes in the phytostabilisation of metalliferous postflotation Zn-Pb spoil heaps not only enables the cost of reclamation works to be reduced, but also more lasting effects to be obtained than is the case with conventional methods [58]. It is also worth to notice that several frequently occurring pseudometallophytes (e.g., Reseda lutea, Lotus corniculatus, Oenothera biennis, Silene vulgaris, Oenothera spp.) are important sources of food for pollinators [59][60][61].
Although many floristic and phytosociological works have been done in the areas connected with exploitation and processing of zinc and lead ores, there is a need to conduct long-term studies on such spoil heaps that will allow to capture changes in the flora and vegetation. Results of such studies can be important in planning proper management of such sites.