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Environmental Management (2014) 53:800–812 DOI 10.1007/s00267-014-0240-z

Relation Between Edaphic Factors and Vegetation Development on Copper Mine Wastes: A Case Study From Bor (Serbia, SE Europe) Dragana Rand¯elovic´ • Vladica Cvetkovic´ Nevena Mihailovic´ • Slobodan Jovanovic´

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Received: 5 April 2013 / Accepted: 16 January 2014 / Published online: 1 February 2014 Ó Springer Science+Business Media New York 2014

Abstract The relationship between edaphic characteristics and vegetation growing on mine wastes in the Bor region (East Serbia, SE Europe) was studied using multivariate statistical analysis. The influence of edaphic factors on the composition of plant life-forms was also investigated, since it could reflect strategies for the avoidance of or tolerance to disturbances of ecosystems. The goal was to provide potential models for the restoration and management of this and similar mine waste areas. The results of this study imply that soil textures, nitrogen contents, reclamation technology and the presence of hydrothermally altered andesite as the type of bedrock significantly influenced plant colonization and vegetation composition of the Bor mine wastes. These edaphic factors explained 30.3 % of the total variation in the vegetation data set. It was also revealed that the pattern of plant life-forms found on the considered site groups corresponded to the soil texture. Based on their relative abundance on the investigated sites and relationships with soil properties it is concluded that therophytes and geophytes are unsuccessful primary colonizers of the Bor mine wastes. Hemicryptophytes of psammophytic character were the most successful primary D. Rand¯elovic´ (&) V. Cvetkovic´ Department for Mineralogy, Crystallography, Petrology and Geochemistry, Faculty of Mining and Geology, University of Belgrade, Ðusˇina 7, 11000 Belgrade, Serbia e-mail: [email protected] N. Mihailovic´ Institute for the Application of Nuclear Energy (INEP), Banatska 31b, 11080 Zemun, Serbia S. Jovanovic´ Faculty of Biology, Institute of Botany and Botanical Garden Jevremovac, University of Belgrade, Takovska 43, 11000 Belgrade, Serbia

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colonizers and therefore potential candidates for anthropogenically-assisted natural recovery. This study suggested that an assessment of edaphic factors should be widely used in the characterization of mine wastes prior to reclamation. Estimation of their role in the development of existing mine vegetation should predate reclamation procedures. Thus, approaches based on adequate plant lifeforms should have a more prominent role in future mine reclamation schemes. Keywords Reclamation Plant colonization Multivariate statistics Soil texture Nitrogen Plant life-forms

Introduction Edaphic factors include processes related to the formation of soil and development of its physical, chemical and biological characteristics. They are recognized as playing a vital role in plant colonization processes (Fonge et al. 2011). Rangeland plant community distribution and species composition are known to be related to soil properties, with spatial variability of vegetation responses ranging from broad geographic distributions to local-scale sites (Leonard et al. 1988). Soil factors play an important role in plant growth, especially on bare grounds and reclamation surfaces, where they contribute as a strong driving force to ecosystem development and sustainability. The clarifying of the uncertainties related to ecosystem dynamics, structure and function in highly degraded areas is essential for the successful applications of restoration management. Understanding the patterns in species richness, composition and the distribution of plant life-forms along edaphic environmental gradients is particularly

Environmental Management (2014) 53:800–812

important for mine wastes because it can define the potential restoration planning models. Closer insights into the context-dependent interactions between plants and mine soils may essentially improve attempts to restore ecologically appropriate plant communities. This paper focuses on soils and plants overlying mine waste surfaces in the Bor region (East Serbia, SE Europe). This area hosts some of the largest active copper mine basins in Europe with ongoing mining activities since 1904, and is nowadays known as an environmental hot-spot. The main pollution sources in the Bor region are industrial facilities for copper ore processing, the activities of which have resulted in direct and indirect degradation of soil resources over a wider area. Major habitats created as a consequence of mining activities includes flotation tailing ponds, pits, and overburden piles. This study was aimed at finding the most influential edaphic characteristics of the present vegetated mine wastes and the implications that may be of use for further reclamation purposes. Given that there is a mutual relationship between plants and soil, this study also indicates the role of the present plant species and their functional groups in altering the soil characteristics and enhancing primary and secondary colonization, which could also provide valuable insights for future management of reclamation processes.

Materials and Methods The study Area and Site Conditions The study field is located in the suburban area of the town Bor (with coordinates 44°040 2500 N, 22°050 2600 E) covering an area of approximately 150 ha with elevations ranging between 335 and 475 m. It consists of flotation tailings and overburden piles resulting from ore exploitation and processing in the period 1912–1988 (Fig. 1). The mine waste in general consists of two lithological types of waste material. The first is overburden composed of volcanic rocks, predominantly of andesite (±dacite), and their volcaniclastic equivalents (Banjesˇevic´ 2006). The most common volcanic rock is hornblende-biotite andesite displaying holocrystalline porphyritic texture and massive fabric. The volcaniclastic rocks are volcanic conglomerates and sandstones, mostly representing epiclastic rocks, whereas relicts of autoclastic deposits are subordinate. Andesites are present as fairly fresh, partially or intensively hydrothermally altered rocks. The altered andesites contain abundant secondary minerals, such as chlorite, sericite, clay minerals, calcite and amorphous to cryptocrystalline silica as well as subordinate alunite, anhydrite and barite. The relative abundance of these secondary minerals depends on alteration types, e.g.

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potassic (sericite), argillitic (clay minerals) or prophylitic (chlorite, calcite) (Jankovic´ 1990). The altered andesites usually contain impregnations or veinlets of ore minerals, principally copper and iron sulphides. The whole area of overburden was subjected to non-selective deposition of extracted rock material, which resulted in distinctive heterogeneity of the volcanic material on the overburden surface. The second lithology is represented by flotation tailings formed by deposition of milled particles that were left behind after the processing of copper ores (Bogdanovic´ et al. 2011). In the area of the Bor mine wastes, sites with naturally growing herbaceous vegetation occur sporadically. A large proportion of the investigated area is bare and uncolonized. Due to such a situation, only habitat fragments where the process of spontaneous vegetation colonization had started (i. e. the sites inhabited by at least one species) after the final formation of the overburden piles in 1988 were analyzed. Distribution of such sites is quite irregular within the overburden area. This area was also subject to limited reclamation works, the remnants of which are nowadays present as rather isolated patchy vegetated islands. The reclamation works with allochthonous nitrogen-fixing tree species Robinia pseudoacacia L. were conducted with variable success. Most sites, including the investigated overburden sites, were reclaimed in the period 1982–1986 (Milijic´ 1997). The flotation tailing banks were covered with 30 cm of a soil layer prior to planting, in contrast to the areas with overburden, which were not covered by topsoil for the purpose of reclamation. The topsoil material was borrowed from the nearby degraded natural forests and was not fertilized in the reclamation process. According to the technical reports on reclamation activities at flotation tailings banks in Bor (RBN Bor) the reclamation work within the flotation tailings area was conducted during the period 1987–1989. The following three general types of vegetated sites were recognized in this study: non-reclaimed areas on overburden, reclaimed areas on overburden and reclaimed areas on flotation tailings covered with topsoil. The relative abundance of these types of sites is different. The most widespread are non-reclaimed overburden sites, while the other two types occupy a much smaller territory. The study area is characterized by a temperate continental climate with transitions to a sub-mountainous one. The mean annual air temperature is 10.3 °C, while the annual precipitation averages 547 mm. The surrounding landscape belongs to the potential vegetation zone of climatogenous Hungarian oak and Turkey oak communities (Quercetum farnetto-cerris Rud.), interleaved with subassociations of Eastern hornbeam (Quercetum farnettocerris Rud. subas. carpinetosum orientalis Jov.).

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Fig. 1 Map of Bor mine waste area showing the location of study sites numbered 1–25. Legend: closed circle reclaimed flotation tailings with 30 cm topsoil, planted in 1981–1987; closed triangle

reclaimed overburden, planted in 1987–1989; closed square nonreclaimed overburden, plant colonization started after 1988

Soil Sampling and Analysis

Vegetation Sampling

A total of 25 composite soil samples were taken from the upper 20 cm layer of the sampling plots. The soil samples were air-dried and sieved through a 2 mm sieve. A 1:2.5 soil–water solution was used for determining the active soil acidity. Organic carbon was measured by the method of Tjurin (1965). Total nitrogen contents were determined by the method of Kjeldahl (Benton and Jones 2001). The contents of plant-available forms of phosphorus and potassium were analyzed by the Al-method (Egner et al. 1960). Soil textural classes (sand, silt and clay) were examined by the international pipette-B method with sedimentation in water and previous dispersion with sodiumpyrophosphate.

The phytosociological investigation on the selected sites of the Bor mine waste was conducted in the period 2007–2011. Vegetation data were collected from 25 stands (releve´s) according to the Braun-Blanquet (1964) methodology. This methodology is accepted as a formal framework for naming and organizing vegetation units within syntaxonomic hierarchy of associations, alliances, orders and classes (Mucina 1997; Weber et al. 2000; Rodwell et al. 2002), and represents a basic resource for modern vegetation science (Dengler et al. 2011). The Braun-Blanquet combined abundance-cover alphanumeric scale is transformed into a numeric scale as proposed by Westhoff and van der Maarel (1973). The size of sampling plots was adjusted to the minimum areal size depending on

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vegetation type presented on site (Mueller-Dombois and Ellenberg 1974). It varied from 25–100 to 250–500 m2 for vegetation of wild growing sites and reclaimed sites, respectively. The life forms of the plants were determined according to Ellenberg and Mueller-Dombois (1967).

(Lausi et al. 1982) was calculated for all individual taxa in order to gain an objective assessment of their importance in the colonization processes. The Shannon–Weaver diversity index was calculated for the site groups.

Data Analysis

Results

Aimed at detecting the plant response along measured environmental gradients, detrended correspondence analysis (DCA) was preliminary performed on a given data set. The length of the first DCA axis was 3.395 standard deviation units, suggesting that unimodal response models should be used (Lepsˇ and Sˇmilauer 2003). Correspondence analysis (CA), an ordination technique set by Benzecri (1969), was used to represent the phytocoenological releve´s as a function of their species composition. Canonical correspondence analysis (CCA), a direct gradient analysis method, was used to search for patterns between edaphic characteristics and species compositions (ter Braak and Prentice 1988). Correspondence analysis (CA) of community data and canonical correspondence analysis (CCA) of community and environmental data were performed using the latest version of the ‘FLORA’ software package (Karadzˇic´ et al. 1998; Karadzˇic´ and Marinkovic´ 2009). Weighted average (WA) site scores were applied for the calculations (McCune 1997). Multicollinearity among the explanatory variables was determined by calculating variance inflation factors and a correlation matrix. Strongly correlated variables were recognized as variables with r2 C 0.7 and variance inflation factors C20 (ter Braak and Smilauer 2002). Soil textural classes were strongly correlated, having linear combinations which resulted in the formation of a singular matrix. Therefore, the clay and silt variables were removed, while the sand variable was kept for later analysis. Bedrock types were coded as dummy variables. In order to confirm the identified vegetation groups discriminant analysis in the FLORA software package was performed. Analysis of variance was conducted in the Statistica Version 8 StatSoft package in order to test the variability of each environmental factor between the vegetation groups. The per-site abundance of the main lifeforms was associated to the physical and chemical soil variables from the investigated areas via the general linear model (GLM). The significance level was Bonniferoni adjusted for multiple comparisons (Sokal and Rohlf 2000). Diagnostic species were statistically determined using the u coefficient as a statistical measure of fidelity (Chytry´ et al. 2002). The u coefficients for present site groups of unequal size were standardized in order to be directly compared across different site groups (Tichy´ and Chytry´ 2006). Species exceeding a set fidelity threshold (u [ 0.7) are considered to be diagnostic for a given habitat unit. A coverage index (Ic)

Soil Analysis The investigated sites showed differences in physical and chemical rhizospheric soil properties. The share of sand fraction (particles 0.02–2 mm) among all sites ranged from 42.8 to 98.4 %, while the clay fraction (particles \0.002 mm) ranged from 35.3 to 0.41 %. The contents of silt (particles 0.002–0.02 mm) ranged from 25.15 to 0.73 %, respectively. The sites on reclaimed flotation tailings with topsoil cover displayed a clay loam to sandy clay loam soil texture; the reclaimed overburden had sandy loam to sandy clay loam texture, while non-reclaimed, wild growing overburden exhibited sand soil texture. The soils overlying the wild growing overburden sites were generally low in nitrogen having an average of 0.03 %. Those from reclaimed overburden displayed more variable nitrogen concentrations with an average of 0.6 % of total N. The soils over reclaimed flotation tailings covered with topsoil contained 0.2 % nitrogen on average. The soils of non-reclaimed and reclaimed overburden sites showed generally lower contents of organic carbon (average 1.35 and 1.04 %, respectively), in comparison to soil of reclaimed flotation tailings with topsoil cover (average of 2.57 %). The contents of plant-available phosphorous varied substantially between the soils from non-reclaimed and reclaimed sites, displaying average values of 61 and 76 ppm, respectively. The plant available phosphorous contents were higher on the soil from reclaimed flotation tailings covered with topsoil, averaging up to 133 ppm. The available potassium contents showed only slightly lower average concentrations in the non-reclaimed areas (158 ppm) than in the reclaimed overburden (195 ppm) and in the flotation tailings covered with topsoil sites (204 ppm). The pH values of the soil solutions varied among the sites. The non-reclaimed overburden showed the widest pH range from acid to alkaline (pH 3.91–8.32); the reclaimed overburden showed slightly acid to slightly alkaline values (pH 5.6–7.85), while the reclaimed flotation tailings covered with topsoil had moderately acid to slightly alkaline values (pH 4.5–7.55). Floristic and Vegetation Analysis A total of 119 species of vascular plants from 91 genera and 28 families were recorded in 25 phytosociological

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releve´s. The most frequent families were: Asteraceae (25 sp.), Fabaceae (20 sp.), Poaceae (11 sp.), Rosaceae (9 sp.) and Caryophyllaceae (5 sp.), which is in accordance with their presence in the whole flora of the Balkan Peninsula (Turill 1929). The floristic richness per plot varied between two and 54 species. The species number from non-reclaimed overburden sites were in the range 2–13, on reclaimed overburden in the range 13–28, whereas in flotation tailings covered with topsoil it varied between 24–54 species. The Shannon biodiversity index varied from 0.61 to 3.82 between plots, reaching average values of 1.580 for nonreclaimed overburden, 2.279 for reclaimed overburden and 3.368 for flotation tailings covered with topsoil. Analysis of the biological spectrum of total flora for the Bor mine wastes revealed its hemicryptophytic character (with 69 species or 58 %), while therophytes (with 19 species or 15.9 %) and phanerophytes (with 17 species or 14.4 %), geophytes (with seven species or 6 %) and chemicryptophytes (with six species or 5 %) were significantly less abundant in the biological spectrum of this area (Fig. 2). Three different vegetation groups—floristical compositions can therefore be distinguished and, conditionally, marked as: (1) Agrostis stolonifera–Epilobium dodonaei stage of development (No. 1–17, on non-reclaimed overburden sites); (2); Robinia pseudoacacia–Cirsium

Fig. 2 Occurrence of plant life-forms on the Bor mine waste sites. Abbreviations and descriptions: Ch chamaephytae (plants whose buds are located within 25 cm of the soil surface, mostly prostrate or creeping shrubs); G geophytae (perennials that bear their buds below the surface of the soil in the form of bulbs, corms, rhizomes or some other subterranean organ); H hemicryptophytae (mainly perennial herbaceous plants whose buds are located at or near the soil surface); P phanaerophytae (perennial woody plants with buds located at more than 25 cm above the soil surface); T therophytae (annuals that complete their life-cycle from seed to seed production within one growth season)

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eriophorum stage of development (No. 18–21, on reclaimed overburden) and (3) Robinia pseudoacacia– Convolvulus arvensis stage of development (No. 22–25, on flotation tailings covered with topsoil). Diagnostically significant species of Agrostis stolonifera–Epilobium dodonaei stage of development (on non-reclaimed overburden sites) determined by measuring the fidelity index was Agrostis stolonifera (u = 0.73). Diagnostically significant species of Robinia pseudoacacia–Cirsium eriophorum stage of development (on reclaimed mine overburden), according the fidelity index were: Cirsium eriophorum (u = 0.82), Rubus idaeus (u = 0.80) and Robinia pseudoacacia (u = 0.75). Besides planted Robinia (u = 0.75), within Robinia pseudoacacia–Convolvulus arvensis development stage differential species such as Convolvulus arvensis, Achillea millefolium, Vicia cracca, Daucus carota, Apera spica-venti, Saponaria officinalis and Centaurea stoebe subsp. micranthos (u [ 0.80) could be distinguished. The species with high diagnostic value, significant presence and cover value in these vegetation stages are summarized in Table 1. Results of Statistical Analysis Gradient Analysis Two main groups of releve´s could be distinguished by CA. The first axis (horizontal) separates vegetation of wild growing sites from planted Robinia pseudoacacia stands (Fig. 3), which additionally explains approximately 15.87 % of total variance in the species data (Table 2). The sum of canonical eigenvalues in CCA measures the variation in the species data, which is explained by the constraining environmental data set of 11 edaphic variables (listed in Table 3). Approximately, 61 % of the calculated total variation of vegetation data set resulted from all edaphic factors included in the analysis. In order to select only statistically relevant explanatory variables from the full data set, a forward selection CCA procedure using the partial correlation measurements model was performed (Table 3). At each step, the statistical significance of the variable added was tested using a Monte Carlo permutation test (ter Braak and Prentice 1988). The percentage of sand and flotation tailings with topsoil cover, the amount of total nitrogen and the presence of altered andesite bedrock were found to be significant variables in this data set (Fig. 4). When this combination of variables was entered into the CCA model, the variance of data was 30.3 % from the calculated total variation of the vegetation data set. The Monte-Carlo permutation test was used for testing the significance of canonical axes and the explained variance by canonical axes for the first and second axis were 46.8 and 27.3 %, respectively.

Environmental Management (2014) 53:800–812 Table 1 The list of species with diagnostic value, significant presence and cover value of deliberated vegetation stages at Bor mine wastes

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Vegetation stage

Main species

Standardized u coefficient

Level of presence in all releves

Level of presence in site group

Laussi coverage index

Lifeform

Agrostis stolonifera– Epilobium dodonaei

Agrostis stolonifera

0.73

IV

V

38.56

H

Epilobium dodonaei

0.41

IV

V

33.99

H

Calamagrostis epigeios

0.20

III

III

26.80

H

Centaurea arenaria

0.10

II

II

12.42

H

Robinia pseudoacacia

0.75

II

V

86.11

P

Rubus idaeus

0.80

II

V

33.33

P

Sanguisorba minor

0.53

III

V

11.11

H

Linaria genistifolia

0.17

III

IV

38.89

H

Cirsium eriophorum

0.82

I

IV

8.33

H

Centaurea stoebe subsp. micranthos

0.53

II

IV

16.67

H

Taraxacum officinale

0.66

I

IV

11.11

H

Festuca valesiaca

0.48

II

IV

11.11

H

Robinia pseudoacacia

0.75

II

V

72.22

P

Convolvulus arvensis

0.93

I

V

44.44

G

Saponaria officinalis

0.80

II

V

27.78

H

Centaurea stoebe subsp. micranthos

0.80

II

V

25.00

H

Potentilla argentea

1.00

I

V

19.44

H

Sanguisorba minor

0.53

III

V

19.44

H

Apera spicaventi

0.82

I

IV

36.11

T

Vicia cracca

0.82

I

IV

27.78

H

Achillea millefolium

0.82

I

IV

25.00

H

Daucus carota

0.82

I

IV

22.22

H

Artemisia vulgaris Rumex crispus

0.82

I

IV

16.67

H

0.82

I

IV

11.11

H

Poa pratensis

0.64

I

III

27.78

H

Festuca valesiaca

0.21

II

III

27.78

H

Robinia pseudoacacia– Cirsium eriophorum

Robinia pseudoacacia– Convolvulus arvensis

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Fig. 3 Ordination diagram of the correspondence analysis for vegetation data at the Bor mine wastes area

Fig. 4 Ordination diagram of the canonical correspondence analysis showing statistically significant edaphic variables for vegetated sites at the Bor mine wastes area

Table 2 Eigenvalues and percentage of explained variance for the correspondence analysis axes CA axis

Eigenvalues

Explained variance (%)

1

0.7091

15.87

2

0.4532

14

3

0.3957

8.58

4

0.3737

8.36

Total eigenvalues: 4.4678

Table 3 Results of forward selection CCA analysis under partial correlation measurements model (* marked values are statistically significant for P\0.05) Variable

Eigenvalue

F statistic

p value

Fresh andesite

0.102

0.43

0.546

Altered andesite

0.296

1.14

*0.022

Conglomerates

0.257

0.56

0.174

Fine-grained overburden material

0.072

0.43

0.646

Topsoiled flotation tailing

0.365

0.44

*0.000

Sand

0.629

3.37

*0.000

pH

0.251

0.43

0.056

N

0.299

0.51

*0.028

C

0.305

0.72

0.172

P K

0.208 0.094

0.50 0.44

0.054 0.34

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Fig. 5 Ordination diagram of the discriminant analysis illustrating the ability to distinguish site groups at the Bor mine wastes area on the basis of their vegetation data

Discriminant Analysis Discriminant function analysis was employed for checking the previously delineated affinity for a given site group. Three vegetation groups recognized based on the previous reclamation history and type were clearly distinguished


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Fig. 6 Box plots obtained by univariate analysis of variance for edaphic factors on distinguished site groups. Legend: a fresh andesite, b altered andesite, c conglomerates, d fine-grained overburden material, e topsoiled flotation tailings, f sand, g clay, h silt, i pH,

j N, k C, l P, m K. Abbreviations: NRO non-reclaimed overburden sites, RFT reclaimed flotation tailings covered with topsoil, RO reclaimed overburden

(Fig. 5) and discriminant function analysis confirmed 96 % of the releve´s as correctly classified.

Discussion Soil Characteristics

Analysis of Variance Analysis of variance was conducted in order to access the magnitude of the edaphic differences between the distinguished vegetation groups. Box and whisker plots showing the mean and standard deviation values for the studied edaphic variables by each vegetation group were constructed. As illustrated in Fig. 6, the distinguished site groups exhibited statistically significant differences in the topsoiled sites, percentage of sand, clay, slit and total nitrogen contents.

The contents of clay are clearly higher on the reclaimed sites, being the product of vegetation development coupled with enhanced weathering of bedrocks or topsoil coverage. It has previously been recognized that the development of vegetation on reclaimed sites may affects the soil clay content, and that the phenomena is influenced by the age of revegetation (Cerqueira et al. 2012, Singh et al. 2012). The percentage of silt also increased from the non-reclaimed overburden sites, through reclaimed overburden sites, up to reclaimed flotation tailings sites with topsoil coverage.

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The reclaimed sites are characterized by relatively smaller variations in the soil pH, while the non-reclaimed sites exhibited stronger variations of soil pH, mostly as a consequence of diverse mineralogical and geochemical bedrock characteristics. Part of plant-available phosphorous was released through mineralization of organic material, whereas the rest of the phosphorous was related to weathering of the geological bedrock. The average content of P2O5 in fresh hornblende andesites from the Bor area is B0.2 wt% (e.g. Kolb et al. 2013), and similar contents were expected in altered andesites (Banjesˇevic´ 2006) and epiclastic volcanic conglomerates. The major repository of phosphorous in the Bor andesites and conglomerates is apatite, usually appearing as inclusions into hornblende and biotite crystals, and its possible dissolution was most probably influenced by the pH values of the soil solutions. The accumulation of potassium in a plant-available form is the result of decomposition of primary rock-forming minerals and its release from their crystal lattice, as well as biological accumulation of potassium from the decomposition of vegetation litter. The average K2O concentrations in the fresh Bor andesite is &2.2 wt% (Kolb et al. 2013), and similar contents were expected in conglomerates, given that various andesites are the most abundant clasts in these rocks. On the other hand, the potassium contents can be highly variable in hydrothermally altered andesites, depending on the type of alteration (Georgieva et al. 2012). The organic carbon contents of soil are the direct results of vegetation decomposition on mine waste sites and their average values were lower on the non-reclaimed and reclaimed overburden sites than on the reclaimed flotation tailings with topsoil cover. The total nitrogen contents, from which the plant available forms are released by mineralization and organic matter decomposition, also differ among all groups of sites as a consequence of their variable composition and development of vegetation. Vegetation Characteristics The predominance of hemicryptophytes coincides with the biological spectrum of Serbia and of the whole area of a temperate climate (Diklic´ 1984). Besides climate, the predominance of hemicryptophytes is favored by the openness of the studied non-reclaimed sites and by the relative openness of the canopy layer within the planted site. This also implies that the hemicryptophyte life-forms are crucial to processes of both primary and secondary plant colonization of the investigated sites. The small proportion of therophytes indicates that they are generally unsuccessful colonizers of the present habitat types. This is especially evident in the non-reclaimed overburden where only four annual plants were recorded, while one of them (Crepis foetida ssp. rhoeadifolia)

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alternates as a thero-hemicryptophyte. A similar role of therophytes in primary succession processes on gravel sand-pits and rocky outcrop sites was reported by Rˇehounkova´ (2007) and Messias et al. (2011). Except planted Robinia pseudoacacia, other phanerophytes have minor structural and cenological significance on the reclaimed sites. The present sand soil texture in combination with very low nitrogen contents seem to pose limiting factors for development of phanerophytes, especially on the non-reclaimed overburden where only Rubus caesius was sporadically recorded. Geophytes are generally less important in the colonization of the investigated habitats. However, certain representatives of this life-form, such as grass species Agropyron repens and Cynodon dactylon, or geophytic lines, Convolvulus arvensis, show larger abundances on the reclaimed sites, considering the fact that they represent some of the most adaptable rhizomatous ruderal species on anthropogenically created sites. Although generally weakly present, some chamaephyte species found in this area (Dorycnium herbaceum, D. germanicum and Coronilla coronata) can have potential impacts on the improvement of nutrient status of the investigated habitats due to their nitrogen-fixing ability. In general, a higher share of chamaephytes is typical for dry rocky habitats and rock crevices vegetation. The relative frequency of life-forms among the site groups proportionally increased starting from the nonreclaimed overburden areas through the reclaimed overburden and finally to the flotation tailings covered with topsoil sites (Fig. 2). There is a somewhat larger number of phanerophytes on the reclaimed overburden sites in comparison to other groups and the average the Serbian spectrum. They are present as seedlings or juvenile forms of low abundance and cover value, represented by autochthonous species which are spontaneously colonizing planted areas (Rubus idaeus, R. caesius, Crataegus monogyna, Quercus cerris, etc). This supports the opinion that the surrounding vegetation is an important factor in the colonization process of anthropogenically created or heavily ˇ ehounkova´ modified sites (Ninot et al. 2001; Prach and R 2006; Moreno-de las Heras et al. 2008). The flotation tailings sites covered with topsoil were the subject of sporadic illegal logging, which influenced their secondary colonization process. A higher number of herbaceous life-forms (compared to the reclaimed overburden sites) developed. This was probably caused by the combination of fine-textured topsoil cover of higher water-holding capacity in its upper layers and the presence of a seed bank that prospered on nutrients (especially nitrogen) pool and opened canopy of logged parts of Robinia stands. The influence of anthropogenic factors and management measures on the composition of plant life-form on different


areas was emphasized (Pandey and Verman 1990; McIntyre et al. 1995; Gastoń et al. 2006), implying its use in the prediction of ecosystem responses to disturbances, as they reflect strategies and traits for their avoidance or tolerance (McIntyre et al. 1999). Multivariate test of significance showed that the effect of sand variable (and, respectively, clay and silt) on the presence of the 5 main plant lifeforms (therophytes, geophytes, phanerophytes, chamaephytes and hemicryptophytes) was statistically significant (Fratio = 19.91, Pvalue = 0.000***). Differences in soil texture were also found to influence the composition of vegetation life-forms of semi-arid and arid areas on both the regional (Medinski et al. 2010; Huerta-Martıńez et al. 2012) and local scale (Rubio and Escudero 2000). Results of univariate analysis within GLM tests suggest that the presence of geophytes on non-reclaimed and reclaimed areas was influenced by soil texture (Fratio = 52.18, P = 0.000***), being larger on the sites with higher contents of clay and silt. A similar pattern was noticed by Medinski et al. (2010) for arid biomes in Africa. This suggests that soil texture may be one of the potential factors influencing the presence of geophyte life-forms. However, this should be taken with caution because it is hard to distinguish the influence of solely soil texture from the influence of other closely related soil factors (e.g., soil water-holding availability, nutrient retention, heavy metal content, etc.), which are beyond the scope of this study. The presence of therophytes within the study area was significantly related to amount of sand (Fratio = 10.75, P = 0.004) and of total nitrogen (Fratio = 11.50, P = 0.003), being larger on the sites with lower contents of sand particles and higher total soil nitrogen contents. The lower number of therophytes in this area generally corresponded to the reported small proportions of therophytes in the biological spectra of different outcrop sites (Conceiçaõ and Pirani 2005; Ribeiro et al. 2007). According to Ribeiro et al. (2007), some of the reasons for the scarcity of therophytes on bare rock surfaces are the combination of short growing seasons and low nutrient contents that inhibit their strategy of rapid establishment and growth. Further research for clarification of this phenomenon is required. Recognition of Edaphic Factors The strong positive correlation with the first CCA axis (r = 0.70) emphasizes that sand as a soil texture variable is the most influential edaphic factor for vegetation development at the Bor mine wastes. Flotation tailing material with topsoil cover is the second important variable, exhibiting negative correlation (r = -0.58) with the first CCA axis. Soil texture has been recognized as an important ecological factor that controls the presence of plant species in

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different environments (Medinski et al. 2010; Zare Chahouki et al. 2012); including copper mine wastes (Anawar and Freitas 2011). Soil particles of different sizes are known to regulate water infiltration and water holding capacity, retention of nutrients, as well as geochemical reactivity. Higher quantities of fine particles, for instance, can increase the geochemical reactivity and thereby increase the availability of heavy metals in the soil solution (Hansen et al. 2005). Although not directly included in the multivariate analysis due to co-linearity, silt and clay components also appear to be important parameters influencing vegetation stages in the investigated area. The flotation tailings were the subject of reclamation methods with topsoil coverage. Top-soiled substrates were found to show significant differences in the composition of vegetation and the succession they support in comparison to non-topsoiled sites (Martinez-Ruiz and Marrs 2007; Moreno-de las Heras et al. 2008; Alday et al. 2011). Nitrogen is considered as one of the primary limiting nutrients for plant growth in terrestrial ecosystems, and its content was found to be important in plant colonization processes. Effects on species richness and abundances in secondary succession processes have also been recorded along nitrogen gradients (Tilman and Cowan 1989). Different amounts of total nitrogen among investigated site groups were mainly influenced by the presence of nitrogenfixing Robinia pseudoacacia on the reclaimed sites. Altered andesite as bedrock type is characterized by strong mineralogical and geochemical variability, depending on the type of alteration. Abrupt changes in physical and chemical characteristics of this bedrock type could locally affect the overlying soils and plants and therefore potentially influence the change in the composition of plant species. Local pyrite impregnations present in some mineralized hydrothermally altered andesites might have induced a local decrease of pH in the soils. Besides their clear influence on mine reclamation processes (Cerqueira et al. 2012; Singh et al. 2012; Kumar and Kumar 2013), the high importance of soil texture and nitrogen content for plant colonization and vegetation development was also previously found in investigations of different succession processes on gravel sand pits (Prach ˇ ehounkova´ 2006) and volcanic landslides (Shiels and R et al. 2008). This suggests the prominent role of those edaphic variables for plant natural or assisted colonization on different kind of rocky grounds. Diagnostically and Ecologically Important Species The Agrostis stolonifera–Epilobium dodonaei stage of development was present on sites with sand soil textures (average 96.9 % of sand) and lacking nitrogen (average 0.03 %). Somewhat higher retention of water in parts of the

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studied habitats caused a significant spontaneous presence and high coverage of Agrostis stolonifera diagnostic species. A similar dependence on these edaphic factors is related to the coverage of typical pioneer species Epilobium dodonaei and Calamagrostis epigeios due to their significance in the primary colonization of these habitats (Table 1). The presence of highly xerophilic and mainly psammophytic species, such as Centaurea arenaria and Festuca valesiaca in dry and drained parts of the investigated area, implies a combination of high contents of sand and lower amounts of total soil nitrogen. The Robinia pseudoacacia–Cirsium eriophorum stage developed on sandy loam to sandy clay loam texture with elevated total nitrogen contents, where diagnostic mesotrophic to meso-eutrophic species are present. Cirsium eriophorum is common on clay soils and more disturbed grounds and has the most significant diagnostic value in this site group. Besides Robinia, the prominent role in secondary colonization of these areas belongs to the species of higher coverage index, such as: Linaria genistifolia, Rubus idaeus and Centaurea stoebe subsp. micranthos. Soils of development stage Robinia pseudoacacia– Convolvulus arvensis on the reclaimed flotation tailings sites covered with topsoil were characterized by the lowest percentage of sand, and increased contents of silt and clay and increased content of nitrogen. Differential species of this group are of ruderal–nitrophilic character. Significant coverage and abundance within secondary colonization process belongs to grasses Festuca valesiaca and Poa pratensis (Table 1). Although the soil pH value was not a statistically significant in the present study of edaphic variables for vegetation development, a clear alteration of basophilic species Linaria genistifolia and Sanquisorba minor with acidophillic species Rumex acetosella could be found growing on topsoiled flotation tailings, altered andesites and conglomerates. The ultimate cause of such occurrences remains to be clarified by some further investigations. Environmental Management Implications A greater understanding of the relation between edaphic factors and the structure of vegetation communities on mine waste areas could prove highly valuable in attempts to develop suitable reclamation models and restore the ecological functions of these complex environmental systems. Based on the results of this study, some major findings can be used for environmental management applications as follows: –

Employment of multivariate analysis models could aid in the quantification of the relationships between edaphic factors and vegetation development in the

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–

–

–

process of reclamation or colonization of mine waste areas. Results from this study suggest that this relationship is important factor for the Bor mine waste area. Assessment of the most relevant edaphic factors that affect vegetation patterns could be employed as a tool in the characterization of mine areas in terms of their reclamation potential. For example, some of the obtained results suggest that soil texture and bedrock type could be used in pre-defining the mine soil reclamation potential on the Bor mine waste area. These findings, in turn, could be operationalized through identification of management practices that would maintain or improve the state of the mine soil resource. Gaining insights into the relations of plant functional traits (e.g., plant life-forms, nitrogen-fixing ability) and edaphic factors could indicate to successful functional groups at the investigated area, the favoring of which could affect existing reclamation schemes or the creation of new ones in order to enhance the success of the reclamation. For instance, according to results of this particular study, therophytes and geophytes should be avoided when designing a reclamation schemes for the Bor mine waste area. Identification of the ecological traits of frequently found native plant species that respond to the most significant edaphic factors at a given area may aid in the determination of their precedence in processes of anthropogenically-assisted natural recovery. Usage of hemicryptophytes of psammophytic character, the presence of which corresponds with a prevalence of sand soil textures at non-reclaimed overburden areas in Bor, could result in the establishment of plant communities with greater ecological stability.

Incorporation of these recommendations into the design and application of different reclamation models could improve the environmental management efforts to achieve an effective reclamation and recovery of mine waste sites.

Conclusions The vegetation stages developed on the Bor mine wastes of different type and reclamation history show considerable differences in species richness and composition. The variability is principally governed by mine soil properties, anthropogenic factors, climate and surrounding vegetation. The percentage of the variation explained by a set of significant edaphic factors (30.3 %) indicates that mine soil properties are important factors determining their vegetation patterns.


The results of multivariate ordination methods and analysis of variance suggest that the soil textural class is most influential among the edaphic factors for development of vegetation stages. Therefore, it must be strongly considered when deciding about the ecologically appropriate type of restoration plant community on the Bor mine wastes. The flotation tailings with topsoil cover is also a significant explanatory variable, especially given the fact that this artificial substrate showed considerable differences compared to the bedrock types occurring in the investigated area. Altered andesite type of bedrock was found to be another significant explanatory variable, possibly due to the presence of abrupt changes in mineral and chemical composition which could influence the plant composition. The introduction of nitrogen-fixing species for reclamation purposes created strong plant-soil feedback. This was evident through the significant alteration of soil nitrogen supplies, affecting back floristic diversity and determining secondary colonization processes. The life-form composition of considered site groups corresponded to differences in soil texture. Therophytes and geophytes were unsuccessful primary colonizers of the Bor mine wastes. These forms are found to be significantly influenced by the contents of soil sand particles or, most probably, by the whole complex of edaphic properties governed by soil texture. Although having an overall lower significance in the secondary colonization processes on the Bor mine wastes, the presence of phanerophytes was recorded on sites with higher clay and nitrogen contents. The results reported in this study imply that edaphic characterization of the Bor mine wastes in terms of their reclamation potential could be partially based on significant factors such as soil texture and bedrock type, while the reclamation process could be enhanced or altered by the introduction of nitrogen-fixing species. Reclamation processes could also benefit if governed through the most adaptable life-forms at this area. Hemicryptophytes of psammophytic character (e.g. Agrostis stolonifera, Epilobium dodonaei, Calamagrostis epigeios and Centaurea arenaria) were found the most successful primary colonizers and, therefore, potential candidates for anthropogenically assisted natural recovery. Nitrogen-fixing chamaephyte species (Dorycnium herbaceum, D. germanicum), which are natural colonizers of rocky habitats, could also play a more prominent role in reclamation processes on the Bor mine wastes. Assessment of edaphic factors should be widely used in both characterization of mine wastes prior to reclamation, and estimation of their role in existing mine vegetation development. Simultaneously, an approach based on adequate plant life-forms should have a more prominent role in formation of mine reclamation schemes.

811 Acknowledgement This study was supported by the Serbian Ministry of Education, Science and Technological Development (Project Nos. 173030 and 176016). VC acknowledges the support of the Serbian Academy of Sciences and Arts (Project Geodynamics). The authors wish to thank Dr Branko Karadzˇic´ for his helpful comments on statistical analysis in FLORA software. The reviews by two anonymous reviewers and editorial handling of Ming Wong were very helpful and are gratefully acknowledged.

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