Topsoil depth influences the recovery of rupestrian grasslands degraded by mining

ABSTRACT

Close association of iron mining and ferruginous rupestrian grassland places this ecosystem in a special condition of vulnerability, with a large number of degraded areas requiring restoration. Seedling transplantation and topsoil translocation can be used to recover native vegetation in degraded areas. This study aimed to experimentally test the application of two different topsoil depths (0.20 and 0.40 m) in a degraded area. We assessed the vegetation’s natural recovery and the survival of transplanted native species from rescue operations in four 200 m² plots established in each topsoil depth. There was no influence of topsoil depth on the plant species survival, while the vegetation cover was greater on the thicker topsoil. However, exotic species with invasive potential contributed substantially to this vegetation cover, requiring management planning. Some planted native species stood out for their survival ability in the topsoil 49 months after planting. Application of 0.20 m topsoil layer showed to be able to provide native species’ natural recovery and survivorship.

canga; campo rupestre; ecological restoration; diferential survival; flora rescue

INTRODUCTION

Ecological restoration aims to develop effective methods to restore the structural and floristic characteristics of an ecosystem (Gann and Lamb, 2006). This is particularly important in tropical non-forest ecosystems where deforestation has been expanding rapidly, producing strong effects on ecosystem functioning (Fernandes et al., 2016a). Moreover, the knowledge of restoration and resilience in these ecosystems is still limited (Buisson et al., 2018). Seedling transplantation, in situ germination of native seeds, and propagule germination from the topsoil are ways to re-establish indigenous vegetation (Skrindo and Pedersen, 2004; Fernandes et al., 2016b; Gomes et al., 2017).

Topsoil can be defined as the upper layer of soil, with marked presence of biological activity and organic matter. Revegetation from topsoil is based on germination from the propagule bank followed by the natural succession, defined as the nonseasonal, directional and continuous pattern of colonization and extinction by species populations on a site (Skrindo and Pedersen, 2004). Topsoil translocation has been applied experimentally in a wide range of ecosystems and shows potential as a method for restoring species diversity (Tozer et al., 2012; Merino-Martín et al., 2017). Studies of topsoil application to restore biodiverse tropical grasslands are important for effective restoration guidance (Pilon et al., 2018; Onésimo et al., 2021). The process exploits propagules present in the topsoil of a donor site to recreate a similar species assemblage at a recipient site (Tozer et al., 2012). When topsoil removal is necessary for mining, the soil may then be used as a substrate and propagules source for the reclamation or restoration of degraded areas (Holmes, 2001; Mendonça, 2013; Ferreira et al., 2015). This technique enables transposing some ecological filters of the natural regeneration process, such as seed availability, dispersion, and germination (Ferreira et al., 2015).

The Iron Quadrangle (QF) is a large ore reserve located in southeastern Brazil, with approximately 7000 km². The region harbors the headwaters of important Brazilian watersheds and a vegetation complex associated with ferruginous substrates (Jacobi et al., 2007; Ataíde et al., 2011; Fernandes, 2016a; Schaefer et al., 2016). The ferruginous rupestrian grassland, also known as canga, comprises a huge plant species diversity and high rates of endemism (Viana and Filgueiras, 2008; Fernandes, 2016b). Regional mining activity strongly impacts biodiversity and ecosystem services (e.g., recharge and water regulation, pollinators, natural pest controllers, etc.), requiring restoration actions in a large number of degraded areas (Fernandes and Ribeiro, 2017). Currently, 44.09 % of Minas Gerais State (258610.7 km²) is under concession to mining companies (Rezende, 2016; Pena et al., 2017). The soil structure of ferruginous rupestrian grasslands determines peculiar thermal and water behavior, which favors the establishment of highly specialized vegetation, extremely sensitive to the loss of soil cover (Jacobi et al., 2007; Fernandes, 2016a,b). The environmental uniqueness, high diversity, low resilience and accelerated degradation of this ecosystem have created a conflicting context and an immediate challenge for its conservation and restoration (Fernandes et al., 2016b).

In this study, we experimentally tested the application of two different topsoil depths (0.20 and 0.40 m) in a degraded area at the Iron Quadrangule. We assessed the natural vegetation recovery and the survival of transplanted seedlings of native species obtained from rescue operations in both topsoil depths.

MATERIALS AND METHODS

Study area

The experiment was settled up in January 2009 at the mine Capão Xavier (CPX) - Vale, located in Iron Quadrangule, south portion of Espinhaço Range, southeastern Brazil (20° 2’ 59” S, 43° 58’ 43” W). The climate is Cwa, according to the Köppen classification system, with rainy hot summer and dry winters. The warmer month exceeds 22 °C and the coldest month is below 18 °C in average temperature (Reboita, 2015).

Topsoil

The experimental area was capped with the topsoil from a donor site in the same mine. The topsoil was mainly composed of ferruginous concretions and the following granulometry: 44 % coarse sand, 28 % clay, 19 % silt and 9 % fine sand. The topsoil was removed from the excavation area by surface scraping (0.00-0.40 m) with a crawler tractor. After transporting to the experimental area, the material was scattered using loader and backhoe. The final thickness adjustment of the topsoil was performed manually. It was systematically established four 200 m² (20 × 10 m) plots with 0.20 m topsoil and four with 0.40 m topsoil. The plots were 2 m apart from each other. Each plot was subdivided into four subplots (5 × 10 m) to receive the native species planting, as specified in the following subsection.

Small soil fertilization was carried out aiming at the basic replacement of macronutrients. A mixture of the following nutrients was prepared and manually incorporated into the topsoil in all plots: magnesium thermophosphate (soluble P₂O₅, citric acid 2 %, Ca 20 %, Mg 7 %, B 0.10 %, Zn 0.55 %, Mn 0.12 %, Cu 0.05 %, and Mo 0.006 %), magnesium sulfate (Mg 9 % and S 12 %), and NPK 20-0-8.

Species selection and planting

The species Arthrocereus glaziovii (K.Schum.) N.P. Taylor & Zappi, Sinningia rupicola (Mart.) Wiehler, Anthurium minarum Sakur. & Mayo, Hoffmannseggella crispata (Thunb.) H.G.Jones, Billbergia elegans Mart. ex Schult. & Schult.f., Epidendrum secundum Jacq., Pleroma heteromallum (D. Don) D.Don, Vellozia compacta Mart. ex Schult. & Schult.f., Vellozia caruncularis Mart. ex Seub., Vellozia graminea Pohl, Vriesea minarum L.B.Sm., Clusia arrudea Planch. & Triana ex Engl., Dyckia consimilis Mez, Paliavana sericiflora Benth. and Cupania sp. L. were selected for the experimental planting, according to previous floristic survey in the surrounding area and to seedling availability in the mining company’s greenhouse (data not shown). These seedlings were obtained from rescue operations in the Capão Xavier mine area. On the rescue system adopted by the company, part of the rescued plants was planted in woody boxes (0.50 × 0.30 × 0.20 m dimension) and kept in the greenhouse for 6 to 12 months before planting. The boxes were taken to the experimental area and the seedlings were separated manually for planting in each subplot. Seedling size and age varied among species, once they were from rescue operations in the field. Nevertheless, the plants were visually selected to avoid plant size heterogeneity between experimental units when planting.

A total of 800 seedlings manually planted in shallow pits (0.10 × 0.10 × 0.10 m). Each subplot received 25 seedlings in the same spatial arrangement, totaling 100 seedling per plot, as following: A. glaziovii (N = 20), S. rupicola (N = 4), A. minarum (N = 8), H. crispata (N = 20), B. elegans (N = 4), E. secundum (N = 4), P. heteromallum (N = 4), V. compacta (N = 4), V. caruncularis (N = 4), V. graminea (N = 4), V. minarum (N = 8), C. arrudea (N = 4), D. consimilis (N = 4), P. sericiflora (N = 4), and Cupania sp. (N = 4). The planting was carried out in the rainy season, between January 20 and February 5 of 2009. However, due to low rainfall after the planting, irrigation by water truck was needed, according to the company availability and logistics.

Vegetation assessment

After 49 months, planted seedling survival, and vegetation composition and cover were assessed in each topsoil depth treatment. Survival was calculated for each species as the percentage of living individuals in relation to the initial number of planted individuals, at plot level. The vegetation cover was measured by a visual qualitative-quantitative estimative of five randomly placed quadrats (1 × 1 m) in each subplot. Vegetation composition and cover were assessed by the Relevé Method (Braun-Blanquet, 1932). The sampling was taken by five quadrats (1 × 1 m) placed 2 m apart from each other along a 10 m transect, in each subplot. The relative cover of each species found was visually estimated in each quadrat. Scientific names of the plant species were verified at The International Plant Names Index (IPNI, 2020) and Flora do Brasil 2020 databases.

Statistical analyses

T-test was applied to evaluate total species survival and total plant cover in function of topsoil depth. The Mann-Whitney test was performed to evaluate the survival of each species in function of topsoil depth. All analysis were performed using the R 3.4.0 statistical platform (R Development Core Team, 2020).

RESULTS

Planted seedling survival

Plant survival was not influenced by topsoil depth, whether considering the total plants or each species. Nevertheless, seven species showed 50 % survival or more (Cupania sp., V. caruncularis, A. minarum, C. arrudea, B. elegans, D. consimilis, and P. heteromallum) in both topsoil depth treatments, while V. graminea and S. warmingii were not found in the study area after the 49 months (Table 1). The species V. caruncularis showed 100 % survival in the 0.20 m topsoil treatment.

Table 1
Mean survival rates (%) of native species 49 months after planting in the topsoil experiment in the mine Capão Xavier – Vale. Plant species were from flora rescue operations

Species	N per plot	0.20 m topsoil	0.40 m topsoil
Anthurium minarum	8	56.25	62.50
Arthrocereus glaziovii	20	31.25	35.00
Bilbergia elegans	4	56.25	81.25
Hoffmannseggella crispata	20	47.50	52.50
Clusia arrudea	4	56.25	50.00
Cupania sp.	4	81.25	87.50
Dickya consimilis	4	56.25	50.00
Epidendrum secundum	4	18.75	31.25
Paliavana sericiflora	4	25.00	6.25
Sinningia warmingii	4	0.00	0.00
Pleroma heteromallum	4	75.00	62.50
Vellozia caruncularis	4	100.00	75.00
Vellozia compacta	4	62.50	43.75
Vellozia graminea	4	0.00	0.00
Vrisea minarum	8	46.87	28.12

• N: number of individuals planted in each plot.

Vegetation cover and composition

After 49 months, the 0.40 m topsoil plots showed greater vegetation cover than the 0.20 m topsoil plots (t₍₃₀₎ = -4.38; p = 0.00013) (Figure 1). The non-planted species (plants that emerged from the topsoil and/or colonizers arrived from seed rain or secondary dispersal) that most contributed to the vegetation cover in the 0.20 m topsoil treatment was Achyrocline satureioides (Lam.) DC. with about 20 % relative cover, followed by Andropogon bicornis L., Axonopus siccus Kuhlm., and Microstachys corniculata (Vahl) Griseb (Table 2). On the other hand, the non-planted species that most contributed to the vegetation cover in the 0.40 m topsoil was the exotic Melinis minutiflora P.Beauv. with about 15 % relative cover, followed by M. corniculata, Triumfetta semitriloba Jacq., and A. satureioides (Table 2).

Figure 1
Vegetation cover in each topsoil depth after 49 months of topsoil application in an experiment in the mine Capão Xavier – Vale, for restoration of ferruginous rupestrian grassland. The Y-axis values are represented as percentages divided by 100.

Table 2
Relative coverage (%) of plant species present in the experimental area in the mine Capão Xavier – Vale, comprising two treatments of different topsoil depth, 49 months after topsoil application

Species	Relative Coverage
	0.20 m topsoil	0.40 m topsoil
	----------------- %----------------
Achyrocline satureioides	20.72	11.31
Ageratum conyzoides	0.08
Ageratum fastigiatum	1.43	3.55
Alternanthera brasiliana	0.48	0.32
Andropogon bicornis	11.11	1.34
Andropogon ingratu	0.95
Anturium minarum	0.48	0.24
Arthrocereus glaziovii	0.16
Axonopus siccus	10.94	8.21
Baccharis dracunculifolia	0.71	0.55
Bilbergia elegans	0.32	0.32
Bidens pilosa	0.56	0.55
Bulbostylis fimbriata	2.38	1.26
Cecropia pachystachya		0.08
Chamaesyce hyssopifolia	0.79	0.24
Chromolaena laevigata	0.08
Clusia arrudea	0.16
Conyza canadensis	0.87	0.63
Commelina erecta	0.48	6.85
Crocosmia crocosmiiflora	0.40
Cryptanthus schwakeanus	0.32	0.08
Cupania sp.		0.39
Cyperussp.	0.16
Dyckia consimilis	0.32	0.24
Emilia fosbergii	2.46	0.16
Epidendrum secundum		0.24
Eragrostis articulata	0.24
Eriope macrostachya	0.20	0.39
Eragrostissp.	0.08
Gnaphalium sp.	0.48
Hoffmannseggella crispata	1.03	0.08
Ipomoea ramosissima		0.47
Lippia gracilis	1.19	1.34
Lychnophora pinaster	0.24	0.08
Marsypianthes chamaedrys	0.32
Melinis minutiflora	3.57	15.16
Melinis repens	0.32
Mimosa calodendron	0.32	2.45
Myrtaceae indeterminada	1.51
Oxalis corniculata	0.16
Panicum sellowii	0.16
Phyllanthus rosellus	0.64
Pilea microphylla	0.24
Plantago major		0.08
Portulaca hirsutissima	0.08	0.16
Polygala paniculata	0.95	0.08
Microstachys corniculata	10.48	13.66
Senna obtusifolia	0.40	2.64
Setaria parviflora	0.16
Sida glaziovii	4.92	3.63
Sporobolus sp.	2.06	0.77
Spermacoce verticillata	0.71	2.73
Stachytarpheta glabra	1.83	1.34
Tagetes sp.	1.98	0.47
Thelypteris dentata	0.32	0.08
Pleroma heteromallum	3.65	1.66
Triumfetta semitriloba	2.78	13.66
Trachypogon spicatus	0.32
Vellozia albiflora	1.03	1.34
Verbena litoralis		0.32
Vellozia caruncularis	0.16	0.16
Vellozia compacta	0.79	0.24
Vellozia graminea	0.08
Vernonanthura phosphorica		0.37
Vrisea minarum	0.24	0.08

A total of seven non-native species were present in the 0.20 m topsoil (Bidens Pilosa L., Melinis minutiflora P.Beauv., Melinis repens (Willd.) Zizka, Crocosmia crocosmiiflora (Lemoine) N.E.Br., Oxalis corniculate L., Thelypteris dentata (Forssk.) E.P.St.John and Pilea microphylla (L.) Liebm.), and four in the 0.40 m topsoil depth (B. pilosa, M. minutiflora, Plantago major L. and T. dentata). All these species are exotic from Brazil, except T. dentata, that is native from Brazil but not from rupestrian grassland; it is a forest species. The non-native species contributed with 7 % to the 0.20 m topsoil cover and 19.42 % to the 0.40 m topsoil cover (Figure 2).

Figure 2
Coverage of native and non-native species in each topsoil depth after 49 months of topsoil application in an experiment in the mine Capão Xavier – Vale to restore ferruginous rupestrian grassland.

A total of 58 species (51 native) were recorded in the 0.20 m topsoil plots, while 45 species (41 native) were recorded in the 0.40 m topsoil plots. Typical species from ferruginous rupestrian grassland (Mimosa calodendron Mart. ex Benth., Stachytarpheta glabra Cham., Vellozia albiflora Pohl, Cryptanthus schwackeanus Mez, Lychnophora pinaster Mart., and Portulaca hirsutissima Cambess.) were recorded in the natural recovery at both topsoil depth.

Among the 15 planted species, 11 were found in the 0.20 m topsoil plots after 49 months (A. glaziovii, A. minarum, H. crispata, B. elegans, P. heteromallum, V. compacta, V. caruncularis, V. graminea, V. minarum, D. consimilis and P. sericiflora); while 10 species were found in the 0.40 m topsoil plots (A. minarum, H. crispata, B. elegans, E. secundum, P. heteromallum, V. compacta, V. caruncularis, V. minarum, D. consimilis and Cupania sp.).

DISCUSSION

Floristic and ecological studies on both flora rescue and topsoil use are important to increase the knowledge of restoration practices and vegetation establishment, especially in threatened ecosystems such as the ferruginous rupestrian grassland. Our study showed that the topsoil technique could support the recovery of native species and provide persistence of transplanted native species. Our findings suggest that 0.20 m topsoil may be enough to play this role. Results pointed a potential of, after four years from topsoil application, 57 % vegetation cover using 0.20 m topsoil, with 93 % contribution of 51 different native species; while 79 % vegetation cover using 0.40 m topsoil, with 80.6 % contribution of 41 native species.

Although total vegetation cover was greater in 0.40 m topsoil than in 0.20 m topsoil, it was under substantial contribution of non-native species (almost 20 % relative cover). Moreover, the highly invasive African grass M. minutiflora presented the higher relative cover in the 0.40 m topsoil treatment, more than four times if compared with its cover in the 0.20 m topsoil treatment. As invasive plants have fast growth and high competitive ability, they create adverse microclimatic conditions for the native species establishment, hindering their development (Blossey, 1999; Hilário et al., 2011). Therefore, attention to their control is needed in ecological restoration practices. The management of invasive species is fundamental for the success of the restoration process started by the topsoil use, also requiring long-term monitoring (Blossey, 1999; Ferreira et al., 2015; Gomes et al., 2017).

A greater species richness was found in the 0.20 m topsoil treatment, which can be due to the germination ability of rupestrian grassland native species. The germination conditions and the substrate characteristics in the restoring areas provide information about plant establishment (Vázquez-Yanes and Orozco-Segovia, 1993). Temperature and light are important factors that control germination and seed dormancy, being crucial for plant growth regulation and development (Baskin and Baskin, 1988). Many rupestrian grassland species have small seeds with photodormancy (Abreu and Garcia, 2005; Nunes et al., 2016); thus germination should be lower in deeper soils.

The survival performance of some native species can be highlighted, such as V. caruncularis, P. heteromallum, Cupania sp. and V. compacta (only in 0.20 m topsoil), with above 60 % mean survival rates 49 months after planting. Additionally, many saplings of P. heteromallum were found in the area, indicating its sexual propagation.

The recording of typical species of ferruginous rupestrian grassland, that were not introduced by planting (M. calodendron, S. glabra, V. albiflora, C. schwackeanus, L. pinaster, and P. hirsutissima), suggests that these species can form seed banks and/or propagate from the surrounding environment. The presence of these species reinforces the potential of the topsoil use for restoration in this ecosystem. They were able to emerge from and/or colonize the topsoil at both tested depths.

Among the non-planted species, including the exotic ones, 30 were also found by Mendonça (2013) in an adjacent area, which are: Ditassa linearis Mart., Oxypetalum appendiculatum Mart., Baccharis dracunculifolia DC., L. pinaster, Bulbostylis capillaris (L.) C.B.Clarke, Bulbostylis fimbriata (Nees) C.B.Clarke, Alchornea triplinervia (Spreng.) Müll.Arg., M. corniculata, M. calodendron, Eriope macrostachya Mart. ex Benth., S. warmangii, Myrcia splendens (Sw.) DC., Peperomia decora Dahlst., Microtea paniculate Moq., Andropogon ingratus Hack., A. siccus, Eragrostis rufescens Schrad. ex Schult., Eragrostis polytricha Nees, Eragrostis articulate (Schrank) Nees, Panicum sellowii Nees, Sporobolus metallicolus Longhi-Wagner & Boechat, Andropogon bicornis L., Setaria parviflora (Poir.) Kerguélen, Trachypogon spicatus (L.f.) Kuntze, P. hirsutissima, Portulaca mucronate Link, Calibrachoa elegans (Miers) Stehmann & Semir, Lantana fucata Lindl., Lippia gracilis Schauer, and S. glabra. These data indicate the potential role of the topsoil as a source of quality propagules and/or as functional receptor of surrounding propagules for the establishment of native species.

CONCLUSIONS

Use of topsoil for ecological restoration in ferruginous rupestrian grasslands has shown to be a potentially effective technique, but the management of invasive species is extremely necessary and essential to be considered in the restoration planning. The 0.20 m topsoil showed lower coverage by exotic species compared to the thicker topsoil.

The native species Vellozia caruncularis, Cuspania sp., and Pleroma heteromallum stood out for their performance in this experiment, being considered good candidates for planting with restoration purposes in ferruginous rupestrian grasslands. Studies that monitor species establishment and performance in the topsoil at a long-time scale are needed to improve the knowledge of the technique’s effectiveness and identify complementary restoration practices.

Overall results suggest that a topsoil depth of 0.20 m allows the establishment of a variety of native species, both transplanted from rescue operations and colonizing species (from topsoil propagule bank or surrounding dispersal). Native species cover and richness were greater in 0.20 m topsoil compared to 0.40 m topsoil.

REFERENCES

• Abreu MEP, Garcia QS. Efeito da luz e da temperatura na germinação de sementes de quatro espécies de Xyris L. (Xyridaceae) ocorrentes na Serra do Cipó, MG, Brasil. Acta Bot Bras. 2005;19:149-54. https://doi.org/10.1590/S0102-33062005000100014
  » https://doi.org/10.1590/S0102-33062005000100014
• Ataíde ES, Castro PTA, Fernandes GW. Florística e caracterização de uma área de campo ferruginoso no complexo minerário Alegria, Serra de Antônio Pereira, Ouro Preto, Minas Gerais, Brasil. Rev Arvore. 2011;35:1265-75. https://doi.org/10.1590/S0100-67622011000700013
  » https://doi.org/10.1590/S0100-67622011000700013
• Baskin CC, Baskin JM. Germination ecophysiology of herbaceous plant species in a temperate region. Am J Bot. 1988;75:286-305. https://doi.org/10.2307/2443896
  » https://doi.org/10.2307/2443896
• Blossey B. Before, during and after: The need for long-term monitoring in invasive plant species management. Biol Invasions. 1999;1:301-11. https://doi.org/10.1023/A:1010084724526
  » https://doi.org/10.1023/A:1010084724526
• Braun-Blanquet J. Plant sociology. New York: McGraw Hill; 1932.
• Buisson E, Le Stradic S, Silveira FA, Durigan G, Overbeck GE, Fidelis A, Fernandes GW, Bond WJ, Hermann JM, Mahy G, Alvarado ST, Zaloumis NP, Veldman JW. Resilience and restoration of tropical and subtropical grasslands, savannas, and grassy woodlands. Biol Rev. 2018;94:590-609. https://doi.org/10.1111/brv.12470
  » https://doi.org/10.1111/brv.12470
• Fernandes GW. The megadiverse rupestrian grassland. In: Fernandes GW, editor. Ecology and conservation of mountaintop grasslands in Brazil. Switzerland: Springer International Publishing; 2016a. p. 3-14. https://doi.org/10.1007/978-3-319-29808-5_1
  » https://doi.org/10.1007/978-3-319-29808-5_1
• Fernandes GW. Ecology and conservation of mountain-top grasslands in Brazil. Switzerland: Springer International Publishing; 2016b. https://doi.org/10.1007/978-3-319-29808-5
  » https://doi.org/10.1007/978-3-319-29808-5
• Fernandes GW, Coelho MS, Machado RB, Ferreira ME, Aguiar LMS, Dirzo R, Scariot A, Lopes CR. Afforestation of savannas: an impending ecological disaster. Nat Conservacao. 2016a;14:146-51. https://doi.org/10.1016/j.ncon.2016.08.002
  » https://doi.org/10.1016/j.ncon.2016.08.002
• Fernandes GW, Toma TSP, Angrisano P, Overbeck G. Challenges in the restoration of quartzitic and ironstone rupestrian grasslands. In: Fernandes GW, editor. Ecology and conservation of mountaintop grasslands in Brazil. Switzerland: Springer International Publishing; 2016b. p. 449-74. https://doi.org/10.1007/978-3-319-29808-5_19
  » https://doi.org/10.1007/978-3-319-29808-5_19
• Fernandes GW, Ribeiro SP. Deadly conflicts: mining, people, and conservation. Perspect Ecol Conserv. 2017;15:141-4. https://doi.org/10.1016/j.pecon.2017.09.002
  » https://doi.org/10.1016/j.pecon.2017.09.002
• Ferreira MC, Vieira DLM, Walter BMT. Topsoil translocation for Brazilian savana restoration: propagation of herbs, shrubs, and trees. Rest Ecol. 2015;23:723-8. https://doi.org/10.1111/rec.12252
  » https://doi.org/10.1111/rec.12252
• Flora do Brasil. Flora do Brasil 2020 em construção [internet]. Rio de Janeiro: Jardim Botânico do Rio de Janeiro; 2020 [cited 2020 Nov 22]. Available from: http://floradobrasil.jbrj.gov.br/
  » http://floradobrasil.jbrj.gov.br/
• Gann GD, Lamb D. Ecological restoration: a means of conserving biodiversity and sustaining livelihoods. Arizona: Society for Ecological Restoration International; 2006.
• Gomes VM, Negreiros D, Fernandes GW, Pires ACV, Silva ACDR, Le Stradic S. Long-term monitoring of shrub species translocation in degraded Neotropical Mountain Grassland. Rest Ecol. 2017;26:91-6. https://doi.org/10.1111/rec.12537
  » https://doi.org/10.1111/rec.12537
• Hilário RR, Castro SAB, Ker FTO, Fernandes G. Unexpected effects of pigeon-peas (Cajanus cajan) in the restoration of rupestrian fields. Planta Daninha. 2011;29:717-23. https://doi.org/10.1590/S0100-83582011000400001
  » https://doi.org/10.1590/S0100-83582011000400001
• Holmes PM. Shrubland restoration following woody alien invasion and mining: Effects of topsoil depth, seed source, and fertilizer addition. Rest Ecol. 2001;9:71-84. https://doi.org/10.1046/j.1526-100x.2001.009001071.x
  » https://doi.org/10.1046/j.1526-100x.2001.009001071.x
• International Plant Names Index - IPNI. The Royal Botanic Gardens, Kew, Harvard University Herbaria & Libraries and Australian National Botanic Gardens [internet]; 2020 [cited 2020 Nov 22]. Available from: http://www.ipni.org
  » http://www.ipni.org
• Jacobi CM, Do Carmo FF, Vincent RC, Stehmann JR. Plant communities on ironstone outcrops: a diverse and endangered Brazilian ecosystem. Biodivers Conserv. 2007;16:2185-200. https://doi.org/10.1007/s10531-007-9156-8
  » https://doi.org/10.1007/s10531-007-9156-8
• Mendonça MP. O resgate da flora da Canga. Belo Horizonte: Valor Natural; 2013. https://doi.org/10.1007/s10531-007-9156-8
  » https://doi.org/10.1007/s10531-007-9156-8
• Merino-Martín L, Commander L, Mao Z, Stevens JC, Miller BP, Golos PJ, Mayence CE, Dixon K. Overcoming topsoil deficits in restoration of semiarid lands: designing hydrologically favourable soil covers for seedling emergence. Ecol Eng. 2017;105:102-17. https://doi.org/10.1016/j.ecoleng.2017.04.033
  » https://doi.org/10.1016/j.ecoleng.2017.04.033
• Nunes FP, Dayrell RLC, Silveira FAO, Negreiros D, Santana DG, Carvalho FJ, Garcia QS, Fernandes GW. Seed germination ecology in rupestrian grasslands. In: Fernandes GW, editor. Ecology and conservation of mountaintop grasslands in Brazil. Switzerland: Springer International Publishing; 2016. p. 207-25. https://doi.org/10.1007/978-3-319-29808-5_10
  » https://doi.org/10.1007/978-3-319-29808-5_10
• Onésimo CMG, Dias DD, Vale Beirão M, Kozovits AR, Messias MCTB. Ecological succession in areas degraded by bauxite mining indicates successful use of topsoil. Rest Ecol. 2021;29:e13303. https://doi.org/10.1111/rec.13303
  » https://doi.org/10.1111/rec.13303
• Pena JCC, Goulart F, Fernandes GW, Rodrigues M. Impacts of mining activities on the potential geographic distribution of eastern Brazil mountaintop endemic species. Perspect Ecol Conserv. 2017;15:172-8. https://doi.org/10.1016/j.pecon.2017.07.005
  » https://doi.org/10.1016/j.pecon.2017.07.005
• Pilon NAL, Buisson E, Durigan G. Restoring Brazilian savanna ground layer vegetation by topsoil and hay transfer. Rest Ecol. 2018;26:73-81. https://doi.org/10.1111/rec.12534
  » https://doi.org/10.1111/rec.12534
• R Development Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria; 2020. Available from: http://www.R-project.org/
  » http://www.R-project.org/
• Reboita MS, Rodrigues M, Silva LF, Alves MA. Aspectos climáticos do estado de Minas Gerais. Rev Bras Clim. 2015;17:206-26. https://doi.org/10.5380/abclima.v17i0.41493
  » https://doi.org/10.5380/abclima.v17i0.41493
• Rezende VL. A mineração em Minas Gerais: uma análise de sua expansão e os impactos ambientais e sociais causados por décadas de exploração. Soc Nat. 2016;28:375-84. https://doi.org/10.1590/1982-451320160304
  » https://doi.org/10.1590/1982-451320160304
• Schaefer CE, Cândido HG, Corrêa GR, Nunes JA, Arruda DM. Soils associated with rupestrian grasslands. In: Fernandes GW, editor. Ecology and conservation of mountaintop grasslands in Brazil. Switzerland: Springer International Publishing. p. 55-69. https://doi.org/10.1007/978-3-319-29808-5_3
  » https://doi.org/10.1007/978-3-319-29808-5_3
• Skrindo AB, Pedersen PA. Natural revegetation of indigenous roadside vegetation by propagules from topsoil. Urban for Urban Gree. 2004;3:29-37. https://doi.org/10.1016/j.ufug.2004.04.002
  » https://doi.org/10.1016/j.ufug.2004.04.002
• Tozer M, Simpson CC, Mackenzie BDE, Blanche M. Topsoil translocation: an effective method for increasing plant species diversity in restored sites. Australas Plant Conserv. 2012;20:16-17.
• Vázquez-Yanes C, Orozco-Segovia A. Patterns of seed longevity and germination in the tropical rainforest. Annu Rev Ecol S. 1993;24:69-87. https://doi.org/10.1146/annurev.es.24.110193.000441
  » https://doi.org/10.1146/annurev.es.24.110193.000441
• Viana PL, Filgueiras TS. Inventário e distribuição geográfica das gramíneas (Poaceae) na Cadeia do Espinhaço, Brasil. Megadiversidade. 2008;4:99-116.

Edited by

Editors: José Miguel Reichert and Marcos Gervasio Pereira.

Publication Dates

• Publication in this collection
  08 Dec 2021
• Date of issue
  2021

History

• Received
  15 May 2021
• Accepted
  20 Sept 2021