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Edaphic Filters and Plant Colonization in a Mine Revegetated with Sewage Sludge

ABSTRACT

We evaluated the recruitment of plant species and their relation with edaphic attributes in a mine revegetated with sewage sludge in the Brazilian Federal District. Plant species in the revegetated mine and in remaining portions of Cerrado (savanna) within the mined landscape were sampled and identified. Then, samples of revegetated substrate and soils from Cerrado portions were collected, analyzed for chemical attributes and submitted to statistical tests. Results indicated that the remaining portions of Cerrado were colonized by 91 species (22% allochthonous species), and the revegetated substrate housed 62 species (55% allochthonous species). Multivariate tests showed that the edaphic condition built from the incorporation of sewage sludge into the mining substrate acted as filter on the assemblage of plant species. Despite the two study sites shared the same landscape, the Cerrado portions and the revegetated substrate did not share similar plant communities after a decade from mine rehabilitation works.

Keywords:
plant recruitment; ecological restoration; biosolids; Cerrado

1. INTRODUCTION

Surface mining is one of the most severe forms of environmental degradation and anthropogenic alteration of habitats (Wijesekara et al., 2016Wijesekara H, Bolan NS, Vithanage M, Xu Y, Mandal S, Brown SL et al. Utilization of biowaste for mine spoil rehabilitation. Advances in Agronomy 2016; 138: 97-173. http://dx.doi.org/10.1016/bs.agron.2016.03.001.
http://dx.doi.org/10.1016/bs.agron.2016....
). Vegetation removal and soil excavation for reaching minerals drastically reduce ecosystem resilience and its functions (Domene et al., 2010Domene X, Mattana S, Ramírez W, Colón J, Jiménez P, Balanyà T et al. Bioassays prove the suitability of mining debris mixed with sewage sludge for land reclamation purposes. Journal of Soils and Sediments 2010; 10(1): 30-44. http://dx.doi.org/10.1007/s11368-009-0073-1.
http://dx.doi.org/10.1007/s11368-009-007...
; Corrêa et al., 2017Corrêa RS, Balduíno APC, Teza CTV, Baptista GMM, Silva DJ. Recuperação da cobertura vegetal e da atividade fotossintética em jazidas revegetadas no Distrito Federal. Revista Brasileira de Ciências Ambientais 2017; 46(46): 75-87. http://dx.doi.org/10.5327/Z2176-947820170208.
http://dx.doi.org/10.5327/Z2176-94782017...
). Surface mining in the Brazilian Federal District (BFD) is based on low investments in operations, small mining extensions, and poor control over mineral exploration, impact mitigation, and ecological restoration (Corrêa et al., 2004Corrêa RS, Bias ES, Baptista GMM. Áreas degradadas pela mineração no Distrito Federal. In: Corrêa RS, Mello Baptista GMM, editores. Mineração e áreas degradadas no Cerrado. Brasília: Universa; 2004.).

Substrates exposed to the surface by mining present inappropriate conditions for the establishment of plants and other organisms (Goedert & Corrêa, 2004Goedert WJ, Corrêa RS. Usos, degradação e qualidade do solo. In: Corrêa RS, Baptista GMM, organizadores. Mineração e áreas degradadas no Cerrado. Brasília: Universa; 2004.; Corrêa & Bento, 2010Corrêa RS, Bento MAB. Qualidade do substrato minerado de uma área de empréstimo revegetada no Distrito Federal. Revista Brasileira de Ciência do Solo 2010; 34(4): 1435-1444. http://dx.doi.org/10.1590/S0100-06832010000400039.
http://dx.doi.org/10.1590/S0100-06832010...
), and the incorporation of high rates of organic matter into substrates (> 50 Mg. ha–1 dry basis) has been the solution to build a suitable edaphic environment on mined sites. Thus, the rehabilitation of exploited mines involves physical, chemical, and biological amendments of exposed substrates that along with propagules of regional species should trigger the autogenic succession in the revegetated sites (Corrêa et al., 2007Corrêa RS, Melo B Fo, Baptista GMM. Avaliação fitossociológica da sucessão autogênica em áreas mineradas no Distrito Federal. Cerne [online]. 2007 [cited 2017 Apr 6]. 13(4): 406-415. Available from: http://www.redalyc.org /html/744/74413409/
http://www.redalyc.org ...
).

Due to economic reasons and to stimulate recycling, urban residues, such as sewage sludge, have been applied to exploited mines as source of organic matter and plant nutrients since 1994 in the BFD (Corrêa, 2009Corrêa RS. Recuperação de áreas degradadas pela mineração no Cerrado. 2. ed. Brasília: Universa; 2009.). Sanitary issues that limit the use of sewage sludge in agriculture are not impediments for using it in mines (Corrêa, 2009Corrêa RS. Recuperação de áreas degradadas pela mineração no Cerrado. 2. ed. Brasília: Universa; 2009.). Increase of organic matter content, nutrient concentrations, and microbial biomass (Domene et al., 2010Domene X, Mattana S, Ramírez W, Colón J, Jiménez P, Balanyà T et al. Bioassays prove the suitability of mining debris mixed with sewage sludge for land reclamation purposes. Journal of Soils and Sediments 2010; 10(1): 30-44. http://dx.doi.org/10.1007/s11368-009-0073-1.
http://dx.doi.org/10.1007/s11368-009-007...
; Gardner et al., 2010Gardner WC, Broersma K, Naeth A, Chanasyk D, Jobson AL. Influence of biosolids and fertilizer amendments on physical, chemical and microbiological properties of copper mine tailings. Canadian Journal of Soil Science 2010; 90(4): 571-583. http://dx.doi.org/10.4141/cjss09067
http://dx.doi.org/10.4141/cjss09067...
; Torri et al., 2014Torri SI, Corrêa RS, Renella G. Soil carbon sequestration resulting from biosolids application. Applied and Environmental Soil Science 2014; 2014: 1-9. http://dx.doi.org/10.1155/2014/821768.
http://dx.doi.org/10.1155/2014/821768...
; Wijesekara et al., 2016Wijesekara H, Bolan NS, Vithanage M, Xu Y, Mandal S, Brown SL et al. Utilization of biowaste for mine spoil rehabilitation. Advances in Agronomy 2016; 138: 97-173. http://dx.doi.org/10.1016/bs.agron.2016.03.001.
http://dx.doi.org/10.1016/bs.agron.2016....
), improvement of physical attributes (De Maria et al., 2007De Maria IC, Kocssi MA, Dechen SCF. Agregação do solo em área que recebeu biossólido. Bragantia 2007; 66(2): 291-298. http://dx.doi.org/10.1590/S0006-87052007000200013.
http://dx.doi.org/10.1590/S0006-87052007...
; Jordán et al., 2017Jordán MM, García-Sánchez E, Almendro-Gandel MB, Pardo F, Vicente AB, Sanfeliu T et al. Technosols designed for rehabilitation of mining activities using mine spoils and biosolids. Ion mobility and correlations using percolation columns. Catena 2017; 148: 74-80. http://dx.doi.org/10.1016/j.catena.2016.02.027.
http://dx.doi.org/10.1016/j.catena.2016....
), and spontaneous revegetation of surfaces (Andrés et al., 2007Andrés F, Walter I, Tenorio JL. Revegetation of abandoned agricultural land amended with biosolids. The Science of the Total Environment 2007; 378(1-2): 81-83. http://dx.doi.org/10.1016/j.scitotenv.2007.01.017. PMid:17306339.
http://dx.doi.org/10.1016/j.scitotenv.20...
; Borges et al., 2009Borges TA, Silva CB, Balduíno APC, Soares JA, Pereira CEB. Uso de biossólido na recuperação de área degradada no Distrito Federal. Revista AIDIS de Ingeniería y Ciencias Ambientales [online] 2009 [cited 2017 Apr 6]. 2(1): 66-75. Available from: http://www.revistas.unam.mx/index.php/aidis/article/view/13106/0
http://www.revistas.unam.mx/index.php/ai...
; Silva et al. 2013Silva LCR, Corrêa RS, Doane TA, Pereira EIP, Horwath WR. Unprecedented carbon accumulation in mined soils: the synergistic effect of resource input and plant species invasion. Ecological Applications 2013; 23(6): 1345-1356. http://dx.doi.org/10.1890/12-1957.1. PMid:24147407.
http://dx.doi.org/10.1890/12-1957.1...
) follow the incorporation of organic residues into mining substrates.

The processes that classify and restrict species establishment on a site during the course of ecological restoration are designated as ecological filters (Hulvey & Aigner, 2014Hulvey KB, Aigner PA. Using filter-based community assembly models to improve restoration outcomes. Journal of Applied Ecology 2014; 51(4): 997-1005. http://dx.doi.org/10.1111/1365-2664.12275.
http://dx.doi.org/10.1111/1365-2664.1227...
). The literature commonly identifies three major ecological filters: 1) limitations on seed dispersion or seed rain that prevent species to reach the restoration site (Funk et al., 2008Funk JL, Cleland EE, Suding KN, Zavaleta ES. Restoration through reassembly plant traits and invasion resistance. Trends in Ecology & Evolution 2008; 23(12): 695-703. http://dx.doi.org/10.1016/j.tree.2008.07.013. PMid:18951652.
http://dx.doi.org/10.1016/j.tree.2008.07...
; Oster et al., 2009Oster M, Ask K, Cousins SAO, Eriksson O. Dispersal and establishment limitation reduces the potencial for successful restoration of semi-natural grassland communities on former arable fields. Journal of Applied Ecology 2009; 46: 1266-1274. ); 2) abiotic local conditions that favor or difficult the establishment and survival of some group of species (Cleland et al., 2013Cleland EE, Larios L, Suding KN. Strengthening invasion filters to reassemble native plant communities: soil resources and phenological overlap. Restoration Ecology 2013; 21(3): 390-398. http://dx.doi.org/10.1111/j.1526-100X.2012.00896.x.
http://dx.doi.org/10.1111/j.1526-100X.20...
; Sollenberger et al., 2016Sollenberger D, Kadlec C, O’Shaughnessy J, Egerton-Warburton L. Environmental filtering mediates grassland community assembly following restoration with soil carbon additions. Restoration Ecology 2016; 24(5): 626-636. http://dx.doi.org/10.1111/rec.12362.
http://dx.doi.org/10.1111/rec.12362...
); 3) biotic interactions between species that limit (competition) or facilitate (facilitation) the establishment, persistence and abundance of some species on a site (Funk et al., 2008Funk JL, Cleland EE, Suding KN, Zavaleta ES. Restoration through reassembly plant traits and invasion resistance. Trends in Ecology & Evolution 2008; 23(12): 695-703. http://dx.doi.org/10.1016/j.tree.2008.07.013. PMid:18951652.
http://dx.doi.org/10.1016/j.tree.2008.07...
; Cleland et al., 2013Cleland EE, Larios L, Suding KN. Strengthening invasion filters to reassemble native plant communities: soil resources and phenological overlap. Restoration Ecology 2013; 21(3): 390-398. http://dx.doi.org/10.1111/j.1526-100X.2012.00896.x.
http://dx.doi.org/10.1111/j.1526-100X.20...
).

Although some studies have offered an expressive contribution to the advance of knowledge on the rehabilitation of areas degraded by the mining (Corrêa et al., 2007Corrêa RS, Melo B Fo, Baptista GMM. Avaliação fitossociológica da sucessão autogênica em áreas mineradas no Distrito Federal. Cerne [online]. 2007 [cited 2017 Apr 6]. 13(4): 406-415. Available from: http://www.redalyc.org /html/744/74413409/
http://www.redalyc.org ...
; Corrêa, 2009Corrêa RS. Recuperação de áreas degradadas pela mineração no Cerrado. 2. ed. Brasília: Universa; 2009.; Daws et al., 2013Daws MI, Standish RJ, Koch JM, Morald TK. Nitrogen and phosphorus fertilizer regime affect jarrah forest restoration after bauxite mining in Western Australia. Applied Vegetation Science 2013; 16(4): 610-618. http://dx.doi.org/10.1111/avsc.12046.
http://dx.doi.org/10.1111/avsc.12046...
; Nussbaumer et al., 2016Nussbaumer YV, Cole MA, Offler CE, Patrick JW. Identifying and ameliorating nutrient limitations to reconstructing a forest ecosystem on mined land. Restoration Ecology 2016; 24(2): 202-211. http://dx.doi.org/10.1111/rec.12294.
http://dx.doi.org/10.1111/rec.12294...
; Wijesekara et al., 2016Wijesekara H, Bolan NS, Vithanage M, Xu Y, Mandal S, Brown SL et al. Utilization of biowaste for mine spoil rehabilitation. Advances in Agronomy 2016; 138: 97-173. http://dx.doi.org/10.1016/bs.agron.2016.03.001.
http://dx.doi.org/10.1016/bs.agron.2016....
), few studies have investigated the role of edaphic filters in plant recruitment on sites revegetated with sewage sludge (Corrêa et al., 2017Corrêa RS, Balduíno APC, Teza CTV, Baptista GMM, Silva DJ. Recuperação da cobertura vegetal e da atividade fotossintética em jazidas revegetadas no Distrito Federal. Revista Brasileira de Ciências Ambientais 2017; 46(46): 75-87. http://dx.doi.org/10.5327/Z2176-947820170208.
http://dx.doi.org/10.5327/Z2176-94782017...
). Therefore, this study aimed to investigate the relation between edaphic filters and plant colonization in a gravel mine revegetated with sewage sludge, having remaining portions of the original soil and native vegetation within the mined landscape as references.

2. MATERIAL AND METHODS

The area of this study was located on the margin of the highway BR-060 (15°57'6.45” S, 48°10'40.42” W, Datum WGS 84) in the southwestern portion of the Brazilian Federal District (BFD), which extends for 5,814 km2 on the Brazilian Central Plateau. Regional topography varies from flat to gently sloped, with average altitude of 1,100 m. Climate is Tropical of Savanna (Aw – Köppen Geiger) with well-defined wet and dry seasons. Annual mean temperature ranges from 21 °C to 24 °C and annual rainfall ranges from 1,200 to 1,600 mm, with 95% of precipitation occurring between September and March.

Lateritic gravel was explored from the study site in 2001 and 2002, and mine operations left a 67 ha crater from 4 to 5 m bellow the original ground level (Figure 1). The original soil on the area was a Haplic Inceptisol – Cambissolo (EMBRAPA, 2013Embrapa Brasileira de Pesquisa Agropecuária – EMBRAPA. Sistema Brasileiro de Classificação de Solos. 3. ed. Brasília: Embrapa Informação Tecnológica; 2013.), which supported Cerrado sensu stricto vegetation type. Rehabilitation works involved the incorporation of 130 Mg ha–1 (dry basis) of domestic sewage sludge into the exposed substrate surface (0-15 cm) in 2002. Urochloa brizantha (7 kg ha–1) was sown on the rehabilitated substrate in 2005, and since then the area has been used as pasture for approximately thirty bovines. Remaining portions of the original soil and Cerrado vegetation (mounds) were left in the midst of the mined landscape, just 4 - 5 m above mined surface. The Cerrado vegetation on mounds continued to produce seeds and propagules dispersed to the neighborhood.

Figure 1
Location of the sampled 29 ha within the 67 ha mined site. Data source: Codeplan (2017)Companhia de Planejamento do Distrito Federal – CODEPLAN. Geo Serviço [online]. 2017 [cited 2017 Apr 6]. Available from: http://www.codeplan.df.gov.br/component/content/article/331-geo-servico/306-geo-servico.html
http://www.codeplan.df.gov.br/component/...
.

A floristic survey of species naturally recruited in the rehabilitated mine substrate and in the remaining portions of Cerrado (mounds) was done ten years after sewage sludge incorporation into the exposed mine surface. Stratified sampling was chosen for the floristic survey due to the presence of two biotopes within the same site. Remaining portions of Cerrado (mounds) were selected at random and circular areas of 15 m radius were delimited around them on the rehabilitated mine surface (Figure 2). Rarefaction curves periodically tested the sampling sufficiency for each of the two biotopes until curves tended to stabilization, which was reached after sampling 15 mounds and respective areas on the rehabilitated substrate around them – 15 sampling units (Figure 3). The extension effectively sampled was 1.88 ha, of which 0.12 ha on mounds and 1.76 ha on the rehabilitated mine surface. All recruited plant species were recorded and three composite samples of soil and substrate (five subsamples – 0 to 15 cm depth) were collected from each sampling unit. Plant species not identified on the spot were photographed and collected for further identification in herbarium.

Figure 2
Sampling unit designed according to mound locations (D1 to D15) and surround areas. The dark green circle regards to the area on mounds and the light green circle to the area on the revegetated substrate around mounds.
Figure 3
Rarefaction curves of plant species sampled on mounds and on the substrate rehabilitated with sewage sludge.

Names of sampled plant species were updated (Species Link, 2017Species Link. Sistema distribuído de informação que integra dados primários de coleções científicas [online]. 2017 [cited 2017 Apr 6]. Available from: http://splink.cria.org.br/
http://splink.cria.org.br/...
), and species were classified according to life form (grass, bindweed grass, subshrub, shrub, or tree), origin (autochthonous or alochthonous to Cerrado formations), and invasion capacity of natural environments, rural areas, and pastures (Lorenzi, 2008Lorenzi H. Plantas daninhas do Brasil: terrestres, aquáticas, parasitas e tóxicas. 4. ed. São Paulo: Instituto Pantarum; 2008.; Mendonça et al., 2008Mendonça RC, Felfili JM, Walter BMT, Silva MC Jr, Rezende AV, Filgueiras TS et al. Flora vascular do bioma Cerrado: Checklist com 12.356 espécies. In: Sano SM, Almeida SP, Ribeiro JF, editores. Cerrado: ecologia e flora. Brasília: Embrapa Informação Tecnológica; 2008. 2 vol. ).

Soil and substrate samples were air-dried, sieved (2 mm), and analyzed for organic matter (OM), total nitrogen (total-N), available phosphorus (available-P), exchangeable potassium (exchangeable-K), calcium (Ca2+), magnesium (Mg2+), active acidity (pH), potential acidity (H+ + Al3+), cationic exchange capacity (CEC), and base saturation (V%). The analysis of organic matter (OM) followed the method of humid combustion (Walkley-Black) and posterior titration with an ammoniac ferrous sulphate solution. Total nitrogen was analyzed by the Kjeldahl method. Available-P and exchangeable-K were extracted with Mehlich-1 solution and concentrations were respectively determined in a photocolorimeter and spectrophotometer of atomic absorption. Ca2+ and Mg2+ were extracted with KCl solution and analyzed by spectrophotometer of atomic absorption. Soil and substrate samples were shaken with 0.01 M CaCl2 solution and analyzed for active acidity in a pH meter. Potential acidity was determined by means of a buffered solution of calcium acetate and subsequent titration with NaOH. From the obtained results, CEC and V% were calculated according to Embrapa (1997)Embrapa Brasileira de Pesquisa Agropecuária – EMBRAPA. Manual de métodos de análise de solos. 2. ed. Rio de Janeiro: Embrapa Informação Tecnológica; 1997..

Results were submitted to analysis of variance, test of Student, and Mood Median test in Minitab 15 software. The influence of the edaphic attributes on the distribution of recruited plant species was investigated by using the Canonical Correspondence Analysis (CCA). The CCA examines responses of species and sampling units to environmental variables. Thus, unlike other ordination techniques, the CCA provides a direct analysis of gradients (Ter Braak, 1987Ter Braak CJF. The analysis of vegetation-environment relationships by canonical correspondence analysis. Vegetatio 1987; 69(1-3): 69-77. http://dx.doi.org/10.1007/BF00038688.
http://dx.doi.org/10.1007/BF00038688...
). To meet CCA prerequisites, data were organized into two matrices and processed in R 3.3.1 version software (R Core Team, 2016R Core Team. R: a language and environment for statistical computing [online]. Vienna: R Foundation for Statistical Computing; 2016 [cited 2017 Apr 6]. Available from: https://www.R-project.org/
https://www.R-project.org/...
). Plant species matrix contained categorical values (presence = 1 and absence = 0). We used only the species that occurred in at least two of the 15 sampled units and eliminated accidental species from the CCA (Dajoz, 2005Dajoz R. Ecologia geral. Porto Alegre: Artmed; 2005.). This procedure is recommended in ordination techniques, because accidental species do not significantly affect results but increase the volume of calculations and errors (Gauch, 1982Gauch HC. Multivariate analysis in community ecology. Cambridge: Editora Cambridge University; 1982. http://dx.doi.org/10.1017/CBO9780511623332.
http://dx.doi.org/10.1017/CBO97805116233...
). The metric values of the edaphic attributes constituted the second matrix. To test the probability of relation between the matrices of plant species and edaphic attributes, we used the Monte Carlo permutation test (Ter Braak & Prentice, 1988Ter Braak CJF, Prentice IC. A theory of gradient analysis. Advances in Ecological Research 1988; 18: 271-317. http://dx.doi.org/10.1016/S0065-2504(08)60183-X.
http://dx.doi.org/10.1016/S0065-2504(08)...
). Flora similarity between mounds and rehabilitated substrate was evaluated by Anosim test, and the correlation between ordinations of sampling units depending on species composition and edaphic conditions was analyzed by Procrustes test.

3. RESULTS

Rarefaction curves indicated that the sampling of 15 remaining portions of Cerrado (mounds) and the respective surroundings was enough to represent the flora of the study area (Figure 3). It was found 131 plant species colonizing the soil on mounds and the rehabilitated substrate ten years after the incorporation of sewage sludge into the exposed mined surface. Out the 131 plant species, 91 appeared on mounds, of which 76% were unique to this biotope, 22% allochthonous, 38% invasive, 45% trees, 18% shrubs, and 40% herbs/subshrubs. Sixty two species recruited on the rehabilitated substrate, of which 65% were unique to this other biotope, being 55% allochthonous, 83% invasive, 14% trees, 16% shrubs, and 73% herbs/subshrubs (Table 1).

Table 1
Sampled plant species in the study area.

Sewage sludge applied at 130 Mg ha–1 (dry basis) to the exposed substrate resulted in high fertility levels in relation to the values found in soils on mounds (Table 2). The concentration of available-P in the rehabilitated substrate, for instance, reached 46 times the value found in the original Cerrado soil (Table 2). The other edaphic attributes also presented significantly different values in the two biotopes, except potential acidity (H+ + Al3+) (Table 2).

Table 2
Edaphic attributes of soil on mounds (D) and of rehabilitated substrate (S).

Eigenvalues for axes 1 and 2 from the Canonical Correspondence Analysis (CCA) were 0.19 and 0.54, respectively. Axis 1 explained 16.2% of the variance and axis 2, 5.9% of the same. The low 22.1% variance is common in ecological data ordinations due to the complexity of factors involved in the determination of communities’ floristic compositions (Ter Braak & Prentice, 1988Ter Braak CJF, Prentice IC. A theory of gradient analysis. Advances in Ecological Research 1988; 18: 271-317. http://dx.doi.org/10.1016/S0065-2504(08)60183-X.
http://dx.doi.org/10.1016/S0065-2504(08)...
). Monte Carlo permutation test was significant for CCA (p = 0.001) and for axes 1 and 2 (p = 0.001 and 0.022, respectively). The CCA ordination diagrams (Figure 4) and ANOSIM groups test (p = 0.001) showed that the analyzed edaphic attributes were significantly different between the soil on mounds and the substrate rehabilitated with sewage sludge (Table 2). Likewise, the flora from these two biotopes was also significantly different. Procrustes test (p = 0.001) showed high correlation between the edaphic variables and the floristic compositions in the two study biotopes (r = 0.86).

Figure 4
Canonical Correspondence Analysis (CCA) ordination for distribution of sampling units (mounds = D1 to D15; and rehabilitated substrate = S1 to S15) according to edaphic attributes (Table 2), and distribution of species (Table 1) influenced by edaphic attributes (Table 2). The first four letters of the generic and specific epithets abbreviated the scientific names of species.

The ordination diagram of species as a function of edaphic conditions (Figure 4) formed two distinct floristic groups: the first group associated with low edaphic fertility was composed of Acanthospermum australe, Aegiphila lhotzkiana, Annona tomentosa, Borreria latifolia, Byrsonima coccolobifolia, Casearia Sylvestris, Connarus suberosus, Davilla elliptica, Diospyros burchellii, Hortia brasiliana, Hymenaea stigonocarpa, Jacaranda ulei, and Maprounea guianensis (Table 1). In this first group, 93% of species appeared exclusively on mounds and are autochthonous to Cerrado. The second group of plant species correlated with the fertility conditions present in the rehabilitated substrate (Table 2) and was composed of Asclepias curassavica, Cyperus surinamensis, Digitaria insularis, Ipomoea triloba, Malvastrum coromandelianum, Pennisetum setosum, Ricinus comunins, Senna obtusifolia, Sida rhombifolia, Sidastrum micranthum, Solanum falciforme, Solanum palinacanthum, Stachytarpheta elatior, Tagetes minuta, Triumfetta rhomboidea, Vernonanthura ferruginea, and Vernonia polyanthes. In this last group, 59% of species are allochthonous and invasive of savannic formations of Cerrado.

4. DISCUSSION

The Cerrado biome has different expressions of vegetation climax such as grasslands, savannas, and forests (Eiten, 1972Eiten G. The Cerrado vegetation of Brazil. Botanical Review 1972; 38(2): 201-341. http://dx.doi.org/10.1007/BF02859158.
http://dx.doi.org/10.1007/BF02859158...
). These vegetation physiognomies grow under the same climate and are molded by particular soil conditions (Ratter et al., 2003Ratter JA, Bridgewater S, Ribeiro JF. Analysis of the floristic composition of the Brazilian Cerrado vegetation III: comparasion of the woody vegetation of 376 areas. Edinburgh Journal of Botany 2003; 60(1): 57-109. http://dx.doi.org/10.1017/S0960428603000064.
http://dx.doi.org/10.1017/S0960428603000...
; Moreno et al., 2008Moreno MIC, Schiavini I, Haridasan M. Fatores edáficos influenciando na estrutura de fitofisionomias do Cerrado. Caminhos de Geografia [online]. 2008 [cited 2017 Apr 6]; 9(25): 173-194. Available from: http://www.ig.ufu .br/revista/caminhos.html
http://www.ig.ufu ...
; Neri et al., 2012Neri AV, Schaefer CER, Silva AF, Souza AL, Ferreira-Júnior WG, Meira-Neto JAA. The influence of soils on the floristic composition and community structure of an area of brazilian Cerrado vegetation. Edinburgh Journal of Botany 2012; 69(01): 1-27. http://dx.doi.org/10.1017/S0960428611000382.
http://dx.doi.org/10.1017/S0960428611000...
; Schaefer et al., 2015Schaefer CEGR, Nunes JA, Neri AV, Mendonça AF, Ferreira-Júnior WG, Arruda DM et al. Relações solo-vegetação em formações brasileiras: metodologia e estudos de caso. In: Eisenlohr PV, Felfili JM, Melo MMRF, Andrade LA, Meira-Neto JAA, editores. Fitossociologia no Brasil: métodos e estudos de casos. Viçosa: Ed. UFV; 2015. 2 vol.). Effective soil depth, course material along the soil profile, depth of the groundwater table, soil drainage degree, and soil fertility level define different Cerrado phytophysiognomies, vegetation expressions of the edaphic climax in the biome (Haridasan, 2008Haridasan M. Nutritional adaptations of native plants of the cerrado biome in acid soils. Brazilian Journal of Plant Physiology 2008; 20(3): 183-195. http://dx.doi.org/10.1590/S1677-04202008000300003.
http://dx.doi.org/10.1590/S1677-04202008...
). In addition to these variations, floristic composition, phytosociology, and productivity can differ within the same physiognomy due to variations in soil fertility and physical characteristics (Haridasan, 2008Haridasan M. Nutritional adaptations of native plants of the cerrado biome in acid soils. Brazilian Journal of Plant Physiology 2008; 20(3): 183-195. http://dx.doi.org/10.1590/S1677-04202008000300003.
http://dx.doi.org/10.1590/S1677-04202008...
). Despite the edaphic climax that rules the Cerrado flora, studies on the influence of edaphic conditions on plant colonization in mining sites are rather scarce (Starr et al., 2013Starr CR, Corrêa RS, Filgueiras TS, Hay JDV, Santos PF. Plant colonization in a gravel mine revegetated with Stylosanthes spp. in a neotropical savanna. Landscape and Ecological Engineering 2013; 9(1): 189-201. http://dx.doi.org/10.1007/s11355-012-0196-1.
http://dx.doi.org/10.1007/s11355-012-019...
).

Plant colonization starts with propagules entering a disturbed area, and these species must pass through abiotic filters prior to establishing an initial community in it (Hobbs & Norton, 2004Hobbs RJ, Norton DA. Ecological filters, thresholds, and gradients in resistance to ecosystem reassembly. In: Temperton VM, Hobbs RJ, Nuttle T, Halle S, editors. Assembly rules and restoration ecology: bridging the gap between theory and practice. Washington: Island Press; 2004.). The successful seedlings will be further submitted to biotic filters such as competition, facilitation, predation, and parasitism. In this sense, the intensity of each filter type will influence the level of environmental stress imposed on recovering communities during ecological succession (Hobbs & Norton, 2004Hobbs RJ, Norton DA. Ecological filters, thresholds, and gradients in resistance to ecosystem reassembly. In: Temperton VM, Hobbs RJ, Nuttle T, Halle S, editors. Assembly rules and restoration ecology: bridging the gap between theory and practice. Washington: Island Press; 2004.). Some studies suggest that edaphic limitations of exposed substrates and dominance of invasive grasses (Poaceae) are the major ecological filters restricting the establishment and growth of autochthonous species in areas degraded by mining activities (Goedert & Corrêa, 2004Goedert WJ, Corrêa RS. Usos, degradação e qualidade do solo. In: Corrêa RS, Baptista GMM, organizadores. Mineração e áreas degradadas no Cerrado. Brasília: Universa; 2004.; Martins et al., 2004Martins CR, Leite LL, Haridasan M. Capim-gordura (Melinis minutiflora P. Beauv.), uma gramínea exótica que compromete a recuperação de áreas degradadas em unidades de conservação. Revista Árvore 2004; [cited 2017 Apr 6]; 28(5): 739-747. Available from: https://www.researchgate.net/publication/ 262432754
https://www.researchgate.net/publication...
; Halassy et al., 2016Halassy M, Singh AN, Szabo R, Szili-Kovacs T, Szitar K, Torok K. The application of a filter-based assembly model to develop best practices for Pannonian sand grassland restoration. Journal of Applied Ecology 2016; 53(3): 765-773. http://dx.doi.org/10.1111/1365-2664.12618.
http://dx.doi.org/10.1111/1365-2664.1261...
; Sollenberger et al., 2016Sollenberger D, Kadlec C, O’Shaughnessy J, Egerton-Warburton L. Environmental filtering mediates grassland community assembly following restoration with soil carbon additions. Restoration Ecology 2016; 24(5): 626-636. http://dx.doi.org/10.1111/rec.12362.
http://dx.doi.org/10.1111/rec.12362...
).

In this study, portions of Cerrado vegetation remained on mounds and acted as sources of propagules within the mined landscape (Figure 2). Even though, only 17% of the total sampled species (22 species) were common to the floristic communities on the mounds and on the rehabilitated substrate. Of these 22 species, 8 (44%) were classified as autochthonous, and 10 (56%) were classified as allochthonous and invasive of savanna formations of Cerrado (Table 1). In addition to the edaphic characteristics of each sampled biotope (Table 2), roots and underground stems that remain buried in substrates after mine exploitation (Corrêa et al., 1998Corrêa RS, Leite LL, Bastos EK. A dinâmica da degradação e da regeneração. In: Corrêa RS, Baptista GMM, editores. Ecologia e recuperação de áreas degradadas no Cerrado. Brasília: Paralelo 15; 1998.) and low production and longevity of seeds from some Cerrado woody species (Salazar et al., 2012Salazar A, Goldstein G, Franco AC, Miralles-Wilhelm F. Seed limitation of woody plants in Neotropical savannas. Plant Ecology 2012; 213(2): 273-287. http://dx.doi.org/10.1007/s11258-011-9973-4.
http://dx.doi.org/10.1007/s11258-011-997...
) may have influenced the low floristic similarity between the two plant communities within the same mined landscape. Long-term ecological studies indicate that the similarity between plant communities of a natural area of Cerrado and other area regenerated from deforestation is higher than the similarity between the same natural area and other area regenerated from mining activity (Corrêa & Leite, 1998Corrêa RS, Leite LL. Desmatamento e mineração em unidades de conservação. In: Corrêa RS, Baptista GMM, editores. Ecologia e recuperação de áreas degradadas no Cerrado. Brasília: Paralelo 15; 1998.; Corrêa, 2009Corrêa RS. Recuperação de áreas degradadas pela mineração no Cerrado. 2. ed. Brasília: Universa; 2009.). Even in the absence of physical barriers, as it is the case of this study, species that inhabit closely neighboring locations can be allopatric (excluding) if soil conditions define different biotopes (Dajoz, 2005Dajoz R. Ecologia geral. Porto Alegre: Artmed; 2005.).

The number of plant species sampled on mounds (91) and on the rehabilitated substrate (62) (Table 1) was below the floristic richness found in savannic formations of Cerrado (Felfili et al., 2001Felfili JM, Sevilha AC, Silva MC Jr. Comparação entre as unidades fisiográficas Chapada Pratinha, Veadeiros e Espigão Mestre do São Francisco. In: Felfili JM, Silva MC Jr, editores. Biogeografia do bioma Cerrado: estudo fitofisionômico da Chapada do Espigão Mestre do São Francisco. Brasíla: Universidade de Brasília; 2001.; Munhoz & Felfili, 2006Munhoz CBR, Felfili JM. Fitossociologia do estrato herbáceo-subarbustivo de uma área de campo sujo no Distrito Federal, Brasil. Acta Botanica Brasílica 2006; 20(3): 671-685. http://dx.doi.org/10.1590/S0102-33062006000300017.
http://dx.doi.org/10.1590/S0102-33062006...
). However, the number of woody species sampled in the mine rehabilitated with sewage sludge (Table 1) was within the range registered for mines abandoned to natural regeneration in the Brazilian Federal District (Corrêa et al., 2007Corrêa RS, Melo B Fo, Baptista GMM. Avaliação fitossociológica da sucessão autogênica em áreas mineradas no Distrito Federal. Cerne [online]. 2007 [cited 2017 Apr 6]. 13(4): 406-415. Available from: http://www.redalyc.org /html/744/74413409/
http://www.redalyc.org ...
). Allochthonous and invasive species of savanna and grassland formations of Cerrado were found both on the mounds under Cerrado vegetation cover and on the rehabilitated substrate (Table 1). Allochthonous species can become invasive and cause negative impacts to invaded environments (Sampaio & Schmidt, 2013Sampaio AB, Schmidt IB. Espécies exóticas invasoras em unidades de conservação federais do Brasil. Biodiversidade Brasileira [online]. 2013 [cited 2017 Apr 6]; 3(2): 32-49. Available from: http://www.icmbio.gov.br/revistaeletro nica/index.php/BioBR/article/view/351/362
http://www.icmbio.gov.br/revistaeletro ...
) due to their higher ability to compete and dominate plant communities relative to autochthonous species (Valéry et al. 2008Valéry L, Fritz H, Lefeuvre JC, Simberloff D. In search of a real definition of the biological invasion phenomenon itself. Biological Invasions 2008; 10(8): 1345-1351. http://dx.doi.org/10.1007/s10530-007-9209-7.
http://dx.doi.org/10.1007/s10530-007-920...
).

Sewage sludge applied to the mined surface at 130 Mg ha–1 increased substrate fertility to levels far above those measured in the soil under the natural vegetation cover (Table 2) and in Cerrado soils under agricultural production (Correia et al., 2004Correia JR, Reatto A, Spera ST. Solos e suas relações com o uso e manejo. In: Souza DMG, Lobato E, editores. Cerrado: correção do solo e adubação. 2. ed. Brasília: Embrapa Informação Tecnológica; 2004.). The rehabilitated substrate was dominated by grass species (Poaceae) and, even in areas under savanna vegetation cover, additions of phosphorus and nitrogen have favored the dominance of invasive grasses to the detriment of autochthonous species (Bustamante et al., 2012Bustamante MMC, Brito DQ, Kozovits AR, Luedemann G, Mello TRB, Pinto AS et al. Effects of nutrient additions on plant biomass and diversity of the herbaceous-subshrub layer of a Brazilian savanna (Cerrado). Plant Ecology 2012; 213(5): 795-808. http://dx.doi.org/10.1007/s11258-012-0042-4.
http://dx.doi.org/10.1007/s11258-012-004...
; Lannes et al., 2015Lannes LS, Bustamante MMC, Edwards PJ, Venterink HO. Native and alien herbaceous plants in Brazilian Cerrado are (co-) limited by different nutrients. Plant and Soil 2015; 400(1-2): 231-243. http://dx.doi.org/10.1007/s11104-015-2725-9.
http://dx.doi.org/10.1007/s11104-015-272...
). Studies on plant nutrition have shown that the majority of autochthonous species of Cerrado are resistant or tolerant to the dystrophy condition of Cerrado soils (Haridasan, 2008Haridasan M. Nutritional adaptations of native plants of the cerrado biome in acid soils. Brazilian Journal of Plant Physiology 2008; 20(3): 183-195. http://dx.doi.org/10.1590/S1677-04202008000300003.
http://dx.doi.org/10.1590/S1677-04202008...
), and that high levels of soil fertility favor the establishment of allochthonous and invasive plant species in detriment of autochthonous ones (Holmes, 2001Holmes PM. Shrubland restauration following woody alien invasion and mining: Effects of topsoil depth seed source, and fertilizer addition. Restoration Ecology 2001; 9(1): 71-84. http://dx.doi.org/10.1046/j.1526-100x.2001.009001071.x.
http://dx.doi.org/10.1046/j.1526-100x.20...
; Foster et al., 2009Foster BL, Kindscher K, Houseman GR, Murphy CA. Effects of hay management and native species sowing on grassland community structure, biomass, and restoration. Ecological Applications 2009; 19(7): 1884-1896. http://dx.doi.org/10.1890/08-0849.1. PMid:19831077.
http://dx.doi.org/10.1890/08-0849.1...
; Daws et al., 2013Daws MI, Standish RJ, Koch JM, Morald TK. Nitrogen and phosphorus fertilizer regime affect jarrah forest restoration after bauxite mining in Western Australia. Applied Vegetation Science 2013; 16(4): 610-618. http://dx.doi.org/10.1111/avsc.12046.
http://dx.doi.org/10.1111/avsc.12046...
; Nussbaumer et al., 2016Nussbaumer YV, Cole MA, Offler CE, Patrick JW. Identifying and ameliorating nutrient limitations to reconstructing a forest ecosystem on mined land. Restoration Ecology 2016; 24(2): 202-211. http://dx.doi.org/10.1111/rec.12294.
http://dx.doi.org/10.1111/rec.12294...
). Colonization and dominance of invasive species seem to be a common side effect in exploited mines where substrate fertility has increased above dystrophic levels (Silva et al., 2013Silva LCR, Corrêa RS, Doane TA, Pereira EIP, Horwath WR. Unprecedented carbon accumulation in mined soils: the synergistic effect of resource input and plant species invasion. Ecological Applications 2013; 23(6): 1345-1356. http://dx.doi.org/10.1890/12-1957.1. PMid:24147407.
http://dx.doi.org/10.1890/12-1957.1...
).

5. CONCLUSIONS

The incorporation of sewage sludge into the mining substrate created an edaphic environment chemically distinct from the original soil of the study area. A plant community primarily composed of allochthonous and invasive species spontaneously recruited on such fertile environment in detriment to the plant species present in the remaining portions of Cerrado within the mined landscape. The edaphic environment built with sewage sludge acted as a filter in assembling a distinct plant community compared to the native Cerrado vegetation.

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Publication Dates

  • Publication in this collection
    2 May 2019
  • Date of issue
    2019

History

  • Received
    13 Oct 2017
  • Accepted
    12 Mar 2018
Instituto de Florestas da Universidade Federal Rural do Rio de Janeiro Rodovia BR 465 Km 7, CEP 23897-000, Tel.: (21) 2682 0558 | (21) 3787-4033 - Seropédica - RJ - Brazil
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