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Floresta e Ambiente

Print version ISSN 1415-0980On-line version ISSN 2179-8087

Floresta Ambient. vol.26 no.4 Seropédica  2019  Epub Nov 07, 2019

http://dx.doi.org/10.1590/2179-8087.004719 

Original Article

Conservation of Nature

Soil Seed Banks in a Forest Under Restoration and in a Reference Ecosystem in Southeastern Brazil

Kelly de Almeida Silva1 
http://orcid.org/0000-0002-1471-0551

Sebastião Venâncio Martins1 
http://orcid.org/0000-0002-4695-987X

Aurino Miranda Neto1 
http://orcid.org/0000-0001-9674-5741

Aldo Teixeira Lopes2 
http://orcid.org/0000-0002-3701-6773

1Departamento de Engenharia Florestal, Universidade Federal de Vicosa, Viçosa/MG, Brasil

2Companhia Brasileira de Alumínio, Miraí/MG, Brasil

ABSTRACT

The current study aims to characterize the soil seed banks in a forest under restoration and in a seasonal semideciduous forest remnant, as well as to quantitatively and qualitatively compare them in order to evaluate the seed bank potential to influence the restoration process. In total, 60 samples of soil seed banks were collected in two adjacent forests (30 in a 2.18-ha forest undergoing restoration process based on the planting of seedlings belonging to different tree species, after the forest was subjected to bauxite mining activity; and 30 in a 5.30-ha preserved forest fragment). The soil seed bank of the forest undergoing restoration recorded higher density of emerged seedlings than that of the reference ecosystem. Although the shrub-tree species in the investigated forests lacked floristic similarity, the highly similar dispersal syndrome distribution and the successional category of shrub-tree species in them have indicated that both forests underwent ecological processes. Therefore, the restoration process implemented in the mined area has successfully recovered the soil seed bank after a few years.

Keywords:  Atlantic Forest; bioindicators; floristic similarity; forest restoration; mining

1. INTRODUCTION

Forest restoration processes create sustainable plant communities that represent the original composition and diversity of degraded areas (Jefferson, 2004; Courtney et al., 2009). The ecosystem restoration goal lies on promoting and expanding the possibility of implementing ecological restoration and natural succession processes, as well as on enhancing biodiversity and stability in a given region (Tres et al., 2007; Martins, 2016).

Soil seed banks play a key role in recovering different ecosystems and in preserving their resilience (Mackenzie & Naeth, 2010). The assessment of the density and richness of seed banks from different plant species is essential to support the decision making about the most appropriate restoration techniques to be adopted in restoration projects (Martins, 2016). Soil seed bank features are determined based on viable seeds found in the soil (Caldato et al., 1996; Schorn et al., 2013). The seed banks are dynamic systems presenting certain inputs (such as seed rains resulting from active seed dispersal mechanisms) and outputs (such as seed germination, seed viability loss, predation or seed death) (Caldato et al., 1996; Gasparino et al., 2006). Although herbs and grasses prevailed in the soil seed bank of degraded hillslopes in Southern Wello (Ethiopia), these plant species should not be ignored, since they can help covering degraded soils and reducing soil erosion (Kebrom & Bekele, 2000).

The composition and resilience of soil seed banks found in environments undergoing restoration process change due to degrading activities performed before restoration techniques and to the way restoration is conducted (Navarra & Quintana-Ascencio, 2012; Stroh et al., 2012). The high seed density and species richness found in seed banks help improving plant development in degraded environments (Ma et al., 2010).

It is important to evaluate areas undergoing restoration processes to help improving restoration techniques and to investigate the effectiveness of objectives outlined in restoration projects (Stanturf et al., 2014). In addition, it is essential to evaluate the remaining forest areas near the one undergoing restoration in order to compare data collected from both areas (Keddy & Drummond, 1996; Jaunatre et al., 2013).

Studies focused on investigating soil seed banks in restoring and fragmented forests in the Atlantic Forest domain have revealed different results regarding the density of emerging seedlings. In total, 554 seedlings m-2 were found in a given area after six restoration years, whereas 1,056 seedlings m-2 were recorded after nine restoration years (Sorreano, 2002). Previous studies had also found 857.6 seedlings m-2 in a secondary forest in a kaolin mining area located in Minas Gerais State, Brazil (Martins et al., 2008): 771 seedlings m-2 in an area were subjected to 40 restoration years (Miranda Neto et al., 2014), 357 seedlings m-2 in an area were subjected to 23 restoration years (Correia & Martins, 2015) and, finally, 2,489 seedlings m-2 in an area restored for 10 years after being subjected to bauxite mining activity (Miranda Neto et al., 2017). The variation in soil seed density in different areas is associated with several factors such as the history of the area, propagule source and dispersing fauna (Franco et al., 2012).

Thus, environmental mitigation measures to what extent the restoration of areas degraded by mining activities is necessary. The mining sector plays a key role in the Brazilian economy; however, its current social and environmental effects, as well as findings from previous studies about mining operations, should be taken into consideration at the time to assess viable alternatives to minimize possible damages caused by this sector (Barros et al., 2012).

Brazil is one of the largest ore producers and it holds the largest mineral reserves in the world (Magno, 2015). Bauxite mining has several negative and positive effects on the environment. For example, mining activities can present the following negative environmental effects: vegetation suppression, water quality degradation, ecosystem function loss, different effects on fauna, as well as noise, dust, and particulate emissions (Bebbington & Bury, 2009; Koch, 2015). However, other activities can decrease the negative impact of mining, mainly the ones resulting from topographical conditioning and revegetation processes (Guimarães et al., 2012).

Therefore, studies focused on using soil seed banks as indicators to evaluate and monitor forests undergoing restoration aim to help understanding the natural regeneration potential of areas facing different disturbances. (Calegari et al., 2013; Martins et al., 2015). Furthermore, it is essential to understand seed bank resources to substantiate the decision-making about future interventions focused on improving ecological processes taking place in restored ecosystems (Martins et al., 2015).

The current study aimed to characterize the soil seed bank found in a forest undergoing restoration after being subjected to bauxite mining and in a seasonal semideciduous forest remnant (reference ecosystem), as well as to quantitatively and qualitatively compare them in order to evaluate the seed bank potential to influence restoration processes.

2. MATERIALS AND METHODS

2.1. Study area

The study was conducted in two adjacent forests herein named as Forest 1 (a 2.18-ha forest undergoing restoration process based on the planting of seedlings belonging to different tree species, after it was subjected to bauxite mining activity) and Forest 2 (reference ecosystem - a 5.30-ha of preserved forest fragment at mid-successional stage).

The investigated forests are located in São Sebastião da Vargem Alegre County (21°04′20″S and 42°38′11″W), Minas Gerais State, Southeastern Brazil, whose local altitude ranges from 792 to 832 m above sea level. Grasslands, preserved secondary forest fragments, eucalyptus plantations and mining areas can be seen in the study site.

The region presents humid temperate climate with dry winters and hot summers, which is classified as Cwa, according to Köppen’s climate classification (Sá Júnior et al., 2012).

Seasonal semideciduous mountain forest is the typical vegetation in the region and it belongs to the Atlantic Forest domain. Forest 1 was subjected to bauxite extraction by Votorantim Metais in 2008; subsequently, the company implemented recomposition and restoration processes based on these stages: topographic recomposition, deposition of soil fertile layer (0.30 m of topsoil was collected and stored before mining, near the area where the mining activity took place), soil acidity correction, phosphate fertilization, basic fertilization and planting of tree species (Table 1), at 3.0 m x 2.0 m spacing and side dressing. The restoration process was concluded in 2010 and the study about the soil seed bank in Forest 1 was conducted in 2015.

Table 1 List of tree species used in the planting of Forest 1 (forest under restoration process). 

Botanical family Species SC DS
Anacardiaceae Schinus terebinthifolius Raddi P Zoo
Tapirira guianensis Aubl. ES Zoo
Apocynaceae Tabernaemontana laeta Mart. P Zoo
Bignoniaceae Jacaranda puberula Cham. ES Ane
Sparattosperma leucanthum (Vell.) K.Schum. ES Ane
Bixaceae Bixa orellana L. P Zoo
Boraginaceae Cordia trichotoma (Vell.) Arráb. ex. Steud. ES Ane
Cannabaceae Trema micrantha (L.) Blume P Zoo
Caricaceae Jacaratia spinosia (Aubl.) A.DC. P Zoo
Euphorbiaceae Croton floribundus Spreng. P Zoo
Joannesia princeps Vell. ES Auto
Fabaceae Anadenanthera macrocarpa (Benth.) Brenan ES Ane
Andira anthelmia (Vell.) Benth. ES Zoo
Apuleia leiocarpa (Vogel) J.F.Macbr. LS Ane
Enterolobium contortisiliquum (Vell.) Morong P Zoo
Erythrina falcata Benth. P Auto
Hymenaea courbaril L. LS Zoo
Inga edulis Mart. ES Zoo
Leucaena leucocephala (Lam.) de Wit * P NC
Machaerium nyctitans (Vell.) Benth. ES Ane
Peltophorum dubium (Spreng.) Taub. ES Ane
Piptadenia gonoacantha (Mart.) J.F.Macbr. ES Auto
Schizolobium parahyba (Vell.) Blake P Ane
Senna multijuga (Rich.) H.S.Irwin & Barneby ES Auto
Lamiaceae Aegiphila integrifolia (Jacq.) Moldenke ES Zoo
Lauraceae Aniba firmula (Nees & Mart.) Mez LS Zoo
Malvaceae Ceiba speciosa (A.St.-Hil.) Ravenna LS Ane
Luehea divaricata Mart. & Zucc. ES Ane
Melastomataceae Tibouchina granulosa (Desr.) Cogn. P Zoo
Meliaceae Cabralea canjerana (Vell.) Mart. LS Zoo
Cedrela fissilis Vell. LS Ane
Guarea guidonia (L.) Sleumer LS Zoo
Melia azedarach L. * P Zoo
Moraceae Artocarpus heterophyllus Lam. * NC Zoo
Morus nigra L. * NC Zoo
Myrtaceae Syzygium cumini (L.) Skeels * P Zoo
Eucalyptus sp. * P NC
Rosaceae Cydonia oblonga Mill. * NC NC
Eriobotrya japonica (Thunb.) Lindl. * LS Zoo
Rubiaceae Genipa americana L. LS Zoo
Sapindaceae Sapindus saponaria L. LS Auto
Solanaceae Solanum bullatum Vell. P Zoo
Solanum mauritianum Scop. P Zoo
Solanum paniculatum L. P Zoo
Vochysiaceae Callisthene fasciculata Mart. LS Ane

SC: Successional category (P: Pioneer, ES: Early secondary, LS: Late secondary); DS: Dispersal syndrome (Ane: anemochory, Zoo: zoochory, Auto: autochory); *Exotic species in Brazil.

Forest 2, which is a preserved remnant stretch of a secondary seasonal semideciduous forest at mid-successional stage, was used as reference ecosystem to help the Forest 1 assessment process. Forest 2 presents the following structural characteristics: average canopy opening of 19.07%; 2.62 tree individuals m-2 in the natural regeneration layer; and 6,339 kg ha-1 of mean accumulated litter on the forest floor (Silva et al., 2018).

2.2. Data collection and analysis

Thirty 2.0 m × 2.0 m plots were allocated for study in each forest (Forest 1 and Forest 2) in 2015; they were distributed in six rows with five plants, which were spaced 5 m between plots and 40 m between rows. Since these are adjacent areas without physical separation, they were distributed based on the delimitation of the investigated forests, wherein 30 plots in Forest 1 mirrored 30 plots in Forest 2. A 0.25 m × 0.30 m wooden frame was cast in the center of each plot, where surface soil samples were collected 5.0 cm down in the ground, by disregarding the non-decomposed plant litter. In total, 60 samples (30 samples in Forest 1 and 30 samples in Forest 2) were collected and subjected to soil seed bank analysis.

The 60 soil samples were placed in properly labeled transparent plastic bags and sent to the shade house of the Research Plant Nursery at Federal University of Viçosa, Viçosa County, Minas Gerais State, where they were transferred to 0.25 m × 0.30 m × 0.05 m plastic trays with drainage holes at the bottom and arranged on 1-m-high bench tops. The trays were covered with 50% shading cloth to avoid external contamination. Two trays filled with sterilized sand were also arranged on the bench tops and used as controls. Soil samples were subjected to scheduled sprinkler irrigation (four 3-min-long irrigations on a daily basis) for six months. The soil seed bank was evaluated throughout this period based on the indirect seedling emergence method (Brown, 1992). Emerging seedlings were counted and identified once every two weeks; next, they were promptly removed from the trays.

Species were classified into families, and all their scientific names and respective authors were updated, according to the Angiosperm Phylogeny Group IV (2016).

The Wilcoxon test for paired samples (p < 0.05) was used to compare mean values recorded for density of individuals and species richness in the forest undergoing restoration (Forest 1) to those recorded for the reference ecosystem (Forest 2).

Based on Gandolfi et al. (1995), samples were classified into successional categories for Brazilian seasonal semideciduous forests, as follows: pioneer, early secondary and late secondary species. They were also classified as zoochorous, anemochorous and autochorous species, based on propagule dispersal syndromes, according to van der Pijl (1982).

Floristic, dispersal syndrome and successional category similarities in bush-tree species between seed banks in Forest 1 and Forest 2, as well as species planted in Forest 1 and the ones found in Forest 2, were assessed. A floristic survey comprising Forest 2 species was conducted based on walking visits to forest sections, once a month for six months (Table 2).

Table 2 Floristics of the shrub-tree species from the Forest 2 (reference ecosystem). 

Botanical family Species SC DS Hb
Annonaceae Annona cacans Warm. LS Zoo T
Xylopia brasiliensis Spreng. LS Zoo T
Xylopia sericea A.St.-Hil. ES Zoo T
Araliaceae Schefflera morototoni (Aubl.) Maguire et al. P Zoo T
Arecaceae Euterpe edulis Mart. LS Zoo P
Syagrus romanzoffiana (Cham.) Glassman ES Zoo P
Asteraceae Piptocarpha macropoda (DC.) Baker P Ane T
Vernonanthura divaricata (Spreng.) H.Rob. P Ane T
Bignoniaceae Jacaranda micrantha Cham. ES Ane T
Boraginaceae Cordia sellowiana Cham. ES Zoo T
Clusiaceae Garcinia gardneriana (Planch. & Triana) Zappi LS Zoo T
Cyatheaceae Cyathea phalerata Mart. ES Ane P
Erythroxylaceae Erythroxylum deciduum A.St.-Hil LS Zoo T
Erythroxylum pelleterianum A.St.-Hil LS Zoo T
Euphorbiaceae Alchornea glandulosa Poepp. & Endl. P Zoo T
Alchornea triplinervia (Spreng.) Müll.Arg. P Zoo T
Aparisthmium cordatum (A. Juss.) Baill. ES Auto T
Croton urucurana Baill. P Auto T
Maprounea guianensis Aubl. ES Auto T
Fabaceae Apuleia leiocarpa (Vogel) J.F. Macbr. LS Ane T
Bauhinia forficata Link P Auto T
Dalbergia nigra (Vell.) Allemão ex Benth. ES Ane T
Machaerium nyctitans (Vell.) Benth. ES Ane T
Peltophorum dubium (Spreng.) Taub. ES Ane T
Piptadenia gonoacantha (Mart.) J.F.Macbr. ES Auto T
Pterogyne nitens Tul. ES Ane T
Tachigali rugosa (Mart. ex. Benth.) Zarucchi & Pipoly LS Ane T
Hypericaceae Vismia guianensis (Aubl.) Choisy P Zoo T
Lacistemataceae Lacistema pubescens Mart. ES Zoo T
Lamiaceae Aegiphila integrifolia (Jacq.) Moldenke P Zoo T
Lauraceae Nectandra oppositifolia Nees LS Zoo T
Ocotea corymbosa (Meisn.) Mez ES Zoo T
Malvaceae Pseudobombax grandiflorum (Cav.) A.Robyns ES Ane T
Melastomataceae Miconia cinnamomifolia (DC.) Naudin P Zoo T
Miconia pusilliflora (DC.) Naudin ES Zoo T
Meliaceae Cabralea canjerana (Vell.) Mart. LS Zoo T
Cedrela fissilis Vell. LS Ane T
Guarea guidonia (L.) Sleumer LS Zoo T
Trichilia catigua A.Juss. LS Ane T
Trichilia elegans A.Juss. LS Zoo T
Moraceae Sorocea bonplandii (Baill.) W.C.Burger et al. LS Zoo T
Myristicaceae Virola bicuhyba (Schott ex Spreng.) Warb. LS Zoo T
Myrtaceae Myrcia splendens (Sw.) DC. ES Zoo T
Nyctaginaceae Guapira opposita (Vell.) Reitz ES Zoo T
Primulaceae Myrsine coriacea (Sw.) R.Br. ex Roem. & Schult ES Zoo T
Myrsine umbellata Mart. ES Zoo T
Rosaceae Prunus myrtifolia (L.) Urb. LS Zoo T
Rubiaceae Amaioua guianensis Aubl. LS Zoo T
Bathysa nicholsonii K.Schum ES U T
Coffea arabica L. U U S
Guettarda viburnoides Cham. & Schltdl. LS Zoo T
Psychotria vellosiana Benth. LS Zoo T
Rutaceae Hortia brasiliana Vand. ex. DC. LS Zoo T
Zanthoxylum rhoifolium Lam. P Zoo T
Salicaceae Casearia decandra Jacq. ES Zoo T
Casearia sylvestris Sw. P Zoo T
Sapindaceae Allophylus edulis (A.St.-Hil. et al.) Hieron. ex Niederl. P Zoo T
Matayba elaeagnoides Radlk. ES Zoo T
Siparunaceae Siparuna guianensis Aubl. LS Zoo T
Urticaceae Cecropia glaziovii Snethl. P Zoo T
Urera baccifera (L.) Gaudich. ex Wedd. P Zoo T
Vochysiaceae Vochysia sp. U Ane T

SC: Successional category (P: Pioneer, ES: Early secondary, LS: Late secondary); DS: Dispersal syndrome (Ane: anemochory, Zoo: zoochory, Auto: autochory); Hb: Habit (T: Tree, S: Shrub, P: Palm tree); U: Uncharacterized.

Jaccard similarity coefficient was used to assess floristic similarity based on a qualitative matrix composed of data about the presence and absence of plant species. Morisita coefficient was used to assess the dispersal syndrome and successional category similarities based on a quantitative matrix composed of data about species density.

Unweighted Pair Group Method with Arithmetic Mean (UPGMA) was used to interpret floristic, dispersal syndrome and successional category similarities; similar samples were clustered, depending on the selected variables, in order to generate a dendrogram.

3. Results

3.1. Seed bank in the forest undergoing restoration (Forest 1)

In total, 4,872 seedlings from 61 plant species and 25 botanical families were identified in Forest 1 seed bank. Seven of the species were only identified at genus level, whereas one remained undetermined, although it was identified at family level (Table 3). Forest 1 seed bank had 2,165 propagules m-2, which were distributed as follows: 1,497 grasses m-2, 607 bushes m-2, 59 trees m-2, and two uncharacterized species m-2. No seedling emerged in the control trays; this outcome showed lack of contamination with seeds from external sources in the experiment.

Table 3 Floristics and phytosociology of the species from the F1 soil seed bank (restoration forest). 

Botanical family/species NI RD(%) RF(%) SC DS Hb
Amaranthaceae
Amaranthus blitum L. 17 0.35 0.87 U U H
Asteraceae
Adenostemma verbesiana (L.) Kuntze 3 0.06 0.65 U Ane H
Ageratum conyzoides L. 671 13.78 4.77 P Ane H
Baccharis dentata (Vell.) G.M.Barroso 3 0.06 0.43 P Ane S
Baccharis dracunculifolia DC. 38 0.78 3.04 P Ane S
Baccharis trinervis Pers. 3 0.06 0.43 P Ane S
Bidens pilosa L. 8 0.16 0.43 P Ane H
Chromolaena odorata (L.) R.M.King & H.Rob 2 0.04 0.43 U Ane S
Conyza bonariensis (L.) Cronquist 48 0.99 4.77 P Ane H
Conyza canadensis (L.) Cronquist 21 0.43 3.04 P Ane H
Emilia fosbergii Nicolson 19 0.39 2.17 P Ane H
Erechtites hieracifolius (L.) Raf. ex DC. 29 0.60 3.04 P Ane H
Eupatorium sp. 1 0.02 0.22 U Ane S
Gnaphalium purpureum L. 40 0.82 3.47 ES Ane H
Gnaphalium sp. 2 0.04 0.43 U Ane H
Lessingianthus glabratus (Less.) H.Rob. 2 0.04 0.22 P Ane S
Porophyllum ruderale (Jacq.) Cass. 9 0.18 1.52 P Ane H
Sonchus oleraceus L. 9 0.18 1.95 U Auto H
Vernonanthura phosphorica (Vell.) H.Rob. 877 18.00 6.51 P Ane S
Vernonanthura westiniana (Less.) H.Rob. 14 0.29 2.60 P Ane S
Vernonia sp. 3 0.06 0.65 P U S
Youngia japonica (L.) DC. 32 0.66 1.30 ES Ane H
Boraginaceae
Varronia curassavica Jacq. 2 0.04 0.43 P Zoo S
Brassicaceae
Raphanus raphanistrum L. 3 0.06 0.43 P Auto H
Cannabaceae
Trema micrantha (L.) Blume 96 1.97 3.04 P Zoo T
Cyperaceae
Cyperus esculentus L. 317 6.52 1.95 P Ane H
Cyperus haspan L. 35 0.72 1.30 P Ane H
Cyperus meyenianus Kunth 31 0.64 1.52 P Ane H
Kyllinga brevifolia Rottb. 33 0.68 1.74 P U H
Euphorbiaceae
Euphorbia heterophylla L. 6 0.12 0.43 U Zoo H
Fabaceae
Leucaena leucocephala (Lam.) de Wit 5 0.10 0.43 P U T
Indeterminate
Ideterminate 1 4 0.08 0.87 U U U
Lamiaceae
Marsypianthes chamaedrys (Vahl) Kuntze 1 0.02 0.22 P Auto H
Mesosphaerum suaveolens (L.) Kuntze 386 7.93 4.56 P Zoo S
Lauraceae
Nectandra lanceolata Nees 8 0.16 0.87 LS Zoo T
Lythraceae
Cuphea carthagenensis (Jacq.) J.Macbr. 28 0.57 1.95 U Ane H
Malvaceae
Sida rhombifolia L. 26 0.53 1.74 P Ane H
Triumfetta rhomboidea Jacq. 8 0.16 1.08 P Zoo S
Melastomataceae
Clidemia hirta (L.) D.Don 5 0.10 0.43 P Zoo S
Tibouchina sp. 1 0.02 0.22 U Zoo T
Onagraceae
Ludwigia tomentosa (Cambess.) H.Hara 6 0.12 0.43 P Ane S
Oxalidaceae
Oxalis corniculata L. 83 1.70 4.12 U Auto H
Phyllanthaceae
Phyllanthus tenellus Roxb. 903 18.54 5.42 ES Auto H
Plantaginaceae
Scoparia dulcis L. 469 9.64 3.04 P Ane H
Poaceae
Andropogon bicornis L. 13 0.27 1.52 P Ane H
Eleusine indica (L.) Gaertn. 1 0.02 0.22 P Ane H
Melinis minutiflora P.Beauv. 9 0.18 1.08 P Ane H
Melinis repens (Willd.) Zizka 1 0.02 0.22 P Ane H
Paspalum notatum Flüggé 1 0.02 0.22 P Ane H
Paspalum sp. 281 5.77 4.12 P Ane H
Setaria parviflora (Poir.) Kerguélen 16 0.33 0.87 P Ane H
Urochloa decumbens (Stapf) R.D.Webster 137 2.81 4.56 P Ane H
Urochloa sp. 4 0.08 0.43 P Ane H
Rosaceae
Rubus sp. 2 0.04 0.22 U Zoo H
Rubiaceae
Borreria latifolia (Aubl.) K.Schum. 4 0.08 0.43 ES Auto H
Scrophulariaceae
Buddleja stachyoides Cham. & Schltdl. 14 0.29 0.22 P U S
Solanaceae
Physalis angulata L. 1 0.02 0.22 P Ane H
Solanum americanum Mill. 56 1.15 3.90 P Zoo H
Solanum mauritianum Scop. 23 0.47 2.17 P Zoo T
Urticacaceae
Cecropia hololeuca Miq. 1 0.02 0.22 P Zoo T
Verbenaceae
Lantana camara L. 1 0.02 0.22 P Zoo S
Total 4,872 100.00 100.00

NI: Number of individuals; RD: Relative density; RF: Relative frequency; SC: Successional category (P: Pioneer, ES: Early secondary, LS: Late secondary); DS: Dispersal syndrome (Ane: anemochory; Zoo: zoochory; Auto: autochory); Hb: Habit (T: Tree, S: Shrub, H: Herb); U: Uncharacterized.

Botanical families Asteraceae, Phyllanthaceae, Plantaginaceae, Poaceae, Cyperaceae and Lamiaceae were significantly abundant and accounted for 91.79% of emerging seedlings. Family Asteraceae accounted for 37.64% of emerging seedlings; it was followed by family Phyllanthaceae (18.53%), which was only represented by species Phyllanthus tenellus Roxb.

Table 4 shows the distribution of species and individuals based on successional category and on dispersal syndrome.

Table 4 Distribution of species and individuals in relation to the successional category and to the dispersal syndrome from the F1 soil seed bank (restoration forest). 

Dispersal syndrome (%) Sucessional category (%)
Zoo Ane Auto U P ES LS U
Specie 21.31 59.01 9.84 9.84 72.13 6.56 1.64 19.67
Individual 12.21 65.64 20.59 1.56 76.50 20.10 0.16 3.24

P: Pioneer, ES: Early secondary, LS: Late secondary, Ane: anemochory, Zoo: zoochory, Auto: autochory, U: Uncharacterized.

3.2. Reference ecosystem seed bank (Forest 2)

In total, 764 seedlings from 58 plant species and 25 botanical families emerged in Forest 2 seed bank. Eight of these species were only identified at genus level, whereas three remained unidentified and were also not classified at family level (Table 5). Density measurements showed 340 propagules m-2, which were distributed as follows: 157 trees m-2, 104 grasses m-2, 78 bushes m-2 and two creepers m-2. There was not seedling emergence in the control trays; this outcome showed lack of contamination with seeds from external sources in the experiment.

Table 5 Floristics and phytosociology of the species from the F2 soil seed bank (reference ecosystem). 

Botanical family/species NI RD RF SC DS Hb
Asteraceae
Ageratum conyzoides L. 1 0.13 0.41 P Ane H
Baccharis dentata (Vell.) G.M.Barroso 1 0.13 0.41 P Ane S
Conyza bonariensis (L.) Cronquist 4 0.52 1.63 P Ane H
Eclipta prostata (L.) L. 1 0.13 0.41 P Ane H
Erechtites hieracifolius (L.) Raf. ex DC. 29 3.80 4.08 P Ane H
Eupatorium sp. 8 1.05 2.86 U Ane S
Gnaphalium purpureum L. 8 1.05 2.04 ES Ane H
Helichrysum elatum A.Cunn. ex DC. 1 0.13 0.41 ES Ane H
Vernonanthura divaricata (Spreng.) H.Rob. 1 0.13 0.41 P Ane T
Vernonanthura phosphorica (Vell.) H.Rob. 28 3.67 5.71 P Ane S
Vernonanthura westiniana (Less.) H.Rob. 26 3.40 6.93 P Ane S
Cannabaceae
Trema micrantha (L.) Blume 34 4.46 4.90 P Zoo T
Cyperaceae
Kyllinga brevifolia Rottb. 2 0.26 0.41 P U H
Scleria gaertneri Raddi 5 0.65 0.41 U Zoo H
Euphorbiaceae
Alchornea glandulosa Poepp. & Endl. 1 0.13 0.41 P Zoo T
Alchornea triplinervia (Spreng.) Müll.Arg. 15 1.96 3.67 P Zoo T
Maprounea guianensis Aubl. 12 1.57 2.86 ES Auto T
Fabaceae
Pseudopiptadenia contorta (DC.) G.P.Lewis & M.P.Lima 2 0.26 0.82 ES Ane T
Hypericaceae
Vismia guianensis (Aubl.) Choisy 7 0.92 2.86 P Zoo T
Indeterminate
Indeterminate 1 1 0.13 0.41 U U T
Indeterminate 2 1 0.13 0.41 U U C
Indeterminate 3 1 0.13 0.41 U U C
Lamiaceae
Aegiphila integrifolia (Jacq.) Moldenke 3 0.39 1.22 ES Zoo T
Mesosphaerum suaveolens (L.) Kuntze 1 0.13 0.41 P Zoo H
Malvaceae
Ceiba speciosa (A.St.-Hil.) Ravenna 1 0.13 0.41 LS Ane T
Sida sp. 1 0.13 0.41 P Ane H
Melastomataceae
Clidemia hirta (L.) D.Don. 96 12.58 6.11 P Zoo S
Leandra niangaeformis Cogn. 4 0.52 1.63 P Zoo S
Miconia cinnamomifolia DC. Naudin 4 0.52 1.22 P Zoo T
Miconia latecrenata DC. Naudin 2 0.26 0.82 P Zoo T
Miconia sellowiana Naudin 10 1.31 1.63 P Zoo T
Tibouchina granulosa (Desr.) Cogn. 20 2.62 4.49 P Zoo T
Meliaceae
Trichilia elegans A.Juss. 1 0.13 0.41 LS Zoo T
Myrtaceae
Myrcia splendens (Sw.) DC. 1 0.13 0.41 ES Zoo T
Oxalidadaceae
Oxalis corniculata L. 1 0.13 0.41 U Auto H
Phyllanthaceae
Phyllanthus tenellus Roxb. 3 0.39 1.22 ES Auto H
Phytolaccaceae
Phytolacca americana L. 3 0.39 1.22 P Zoo H
Piperaceae
Piper sp. 2 0.26 0.82 P Zoo S
Poaceae
Andropogon bicornis L. 6 0.79 1.63 P Ane H
Panicum sellowii Ness 15 1.96 2.04 P Ane H
Paspalum sp. 3 0.39 0.41 P Ane H
Urochloa sp. 139 18.20 2.86 P Ane H
Primulaceae
Myrsine parvula (Mez) Otegui 3 0.39 0.82 ES Zoo T
Rubiaceae
Coccocypselum aureum (Spreng.) Cham. & Schltdl. 1 0.13 0.41 U Zoo H
Coccocypselum sp. 2 0.26 0.82 U Zoo H
Genipa americana L. 4 0.52 1.22 LS Zoo T
Guettarda uruguensis Cham. & Schltdl. 1 0.13 0.41 ES Zoo S
Psychotria sp. 4 0.52 1.22 LS Zoo S
Rutaceae
Zanthoxylum rhoifolium Lam. 2 0.26 0.82 P Zoo T
Salicaceae
Casearia decandra Jacq. 4 0.52 1.63 ES Zoo T
Sapindaceae
Serjania laruotteana Cambess. 1 0.13 0.41 U Auto C
Solanaceae
Solanum americanum Mill. 8 1.05 1.63 P Zoo H
Solanum cernuum Vell. 18 2.36 3.27 P Zoo T
Solanum mauritianum Scop. 167 21.87 6.12 P Zoo T
Solanum paniculatum L. 5 0.65 1.22 P Zoo S
Styracaceae
Styrax sp. 1 0.13 0.41 U Zoo T
Urticaceae
Cecropia glaziovii Snethl. 7 0.92 2.04 P Zoo T
Cecropia hololeuca Miq. 31 4.06 4.90 P Zoo T
Total 764 100.00 100.00

NI: Number of individuals; RD: Relative density; RF: Relative frequency; SC: Successional category (P: Pioneer, ES: Early secondary, LS: Late secondary); DS: Dispersal syndrome (Ane: anemochory; Zoo: zoochory; Auto: autochory); Hb: Habit (T: Tree, S: Shrub, H: Herb, C: Climber); U: Uncharacterized.

Botanical families Solanaceae, Poaceae, Melastomataceae and Asteraceae stood out for their abundance; they accounted for 79.19% of emerging seedlings. Family Solanaceae accounted for 25.92% of emerging seedlings (species Solanum mauritianum Scop. was well represented in this family) and it was followed by family Poaceae (21.34%).

Table 6 presents the distribution of species and individuals based on successional category and on dispersal syndrome.

Table 6 Distribution of species and individuals in relation to the successional category and to the dispersal syndrome from the F2 soil seed bank (reference ecosystem). 

Dispersal syndrome (%) Sucessional category (%)
Zoo Ane Auto U P ES LS U
Specie 55.17 31.03 6.90 6.90 58.62 17.24 6.90 17.24
Individual 61.12 36.00 2.23 0.65 90.84 4.97 1.31 2.88

P: Pioneer, ES: Early secondary, LS: Late secondary, Ane: anemochory, Zoo: zoochory, Auto: autochory, U: Uncharacterized.

3.3. Comparison between forest undergoing restoration (Forest 1) and reference ecosystem (Forest 2)

The mean density of emerging seedlings (number of individuals m-2) deriving from the seed bank was different (Z=4.638; p<0.001) between the two investigated forests; the forest undergoing restoration recorded higher seedling emergence (2,165 ± 1,788 seedlings m-2) than the reference ecosystem (340 ± 324 seedlings m-2) (Figure 1).

Figure 1 Number of individuals m-2 (A) and species richness m-2 (B) in soil seed banks from the forest undergoing restoration (F1) and from the reference ecosystem (F2). SE = Standard error; SD = Standard deviation. Means followed by the same letter did not differ from each other in the Wilcoxon test (p>0.05). 

The mean species richness per m2 did not show significant difference (Z=0.462; p=0.643) between forests, the forest under restoration recorded 27.0 ± 5.6 species m-2, whereas the reference ecosystem recorded 25.7 ± 11.1 species m-2 (Figure 1).

There was not floristic similarity among Forest 1 and Forest 2 seed banks, species planted in in Forest 1, and adult shrubby-tree species found in Forest 2 (Figure 2). Forest 1 seed bank recorded the emergence of 22 shrub-tree seedling species, whereas 35 species were identified in Forest 2 seed bank. The following shrub-tree species were often found in the seed bank of both forests: Baccharis dentata (Vell.) G.M.Barroso, Cecropia hololeuca Miq., Clidemia hirta (L.) D.Don., Eupatorium sp., Solanum mauritianum, Trema micrantha (L.) Blume, Vernonanthura phosphorica (Vell.) H.Rob. and Vernonanthura westiniana (Less.) H.Rob.

Figure 2 Floristic similarity dendrogram generated through the unweighted pair group method with arithmetic mean (UPGMA), based on the Jaccard similarity coefficient for data about the absence and presence of shrub-tree species in Forest 1 and Forest 2 seed banks, species planted in Forest 1 (Forest 1 planting), and species found in Forest 2, São Sebastião da Vargem Alegre County, MG, Brazil. 

Both forests showed high similarity in dispersal syndrome; Morisita index values ranged from 0.84 to 0.99. The highest similarity was recorded between Forest 2 seed bank and Forest 2 flora (Figure 3).

Figure 3 Dispersal syndrome similarity dendrogram generated through the unweighted pair group method with arithmetic mean (UPGMA), based on Morisita coefficient from a matrix composed of quantitative density data about shrubby-tree species in Forest 1 and Forest 2 seed banks, species planted in Forest 1 (Forest 1 planting) and species found in Forest 2, São Sebastião da Vargem Alegre County, MG, Brazil. 

Both forests also presented highly similar successional category; Morisita index values ranged from 0.65 to 0.95, except between Forest 2 flora and Forest 1 seed bank (0.43). The highest similarity was observed between species in successional categories of Forest 1 plantings and Forest 2 flora (Figure 4).

Figure 4 Successional category similarity dendrogram generated through the unweighted pair group method with arithmetic mean (UPGMA) method, based on Morisita coefficient from a matrix composed of quantitative density data about shrubby-tree species in Forest 1 and Forest 2 seed banks, species planted in Forest 1 (Forest 1 Planting), and species found in Forest 2, São Sebastião da Vargem Alegre County, MG, Brazil. 

4. DISCUSSION

Soil seed banks in areas undergoing early succession process tended to have larger number of seeds, whereas the number of viable seeds decreased as the successional process advanced, as shown in several studies (Araújo et al., 2001; Baider et al., 2001; Sorreano, 2002; Franco et al., 2012).

The seed bank in the forest undergoing restoration presented the highest density of herbaceous individuals and herbaceous species richness; this outcome was similar to the ones found in other studies conducted in tropical forest areas undergoing secondary succession process (Martins et al., 2008; Calegari et al., 2013; Figueiredo et al., 2014; Oliveira et al., 2018). These species are essential to enable the succession process in altered areas during their first colonization stage (Araujo et al., 2004). Herbaceous species can adapt better to disturbed areas and improve soil conditions (Silva-Weber et al., 2012) by enhancing water retention; therefore, they help preventing soil erosion and increase the amount of organic matter in the soil. This improvement in soil conditions favors the development of pioneer bush-tree species.

The reference ecosystem seed bank recorded higher density of tree individuals and tree species richness because it was a well-preserved forest remnant at mid-successional stage. Herbaceous species density tends to decrease, and tree species density tends to increase in soil seed banks as the succession process advances (Baider et al., 2001; Calegari et al., 2013).

Family Asteraceae represented a particularly large number of species and individuals identified in Forest 1 seed bank; most of them presented herbaceous habit and anemochorous dispersal syndrome, a fact that significantly increased their dissemination and, therefore, their abundance in the seed bank. Franco et al. (2012) also found larger number of herbaceous species in their study site, mainly of species belonging to family Asteraceae, which stood out for the highest number of species in the analysis of the seed bank of a seasonal semideciduous forest stretch in Minas Gerais State. Similar findings were also reported in other surveys conducted in tropical forests of the Atlantic Forest domain (Baider et al., 2001; Sccoti et al., 2011; Figueiredo et al., 2014). Species belonging to family Asteraceae present efficient adaptive ability and can be found in different phytophysiognomies (Beretta et al., 2008). Family Asteraceae stands out among angiosperms for its great diversity, which results from the colonization of different habitats and from efficient pollination and seed dispersion methods (Beretta et al., 2008).

Notably, Melinis minutiflora P.Beauv., Urochloa decumbens (Stapf) R.D.Webster and Leucaena leucocephala (Lam.) de Wit, which are invasive exotic species that can negatively affect the forest succession process, were found in Forest 1. The high growth, reproduction and dissemination ability of these invasive species can hinder, or even prevent, the establishment of native species that play a key role in forest healing and succession processes; therefore it is important taking into consideration the risk of having these invasive species becoming established species in disturbed areas (Franco et al., 2012). Thus, controlling these species, which often find favorable resources available to their perpetuation in areas undergoing restoration, is crucial to avoid compromising the forest restoration process (DeMeester & Richter, 2009; Kettenring & Adams, 2011).

4.1. Successional categories and dispersal syndromes

Soil seed banks mostly comprise pioneer species, which form the persistent seed bank and maintaining viable seeds in the soil for a long period of time, until the environmental conditions are appropriate for germination (Araújo et al., 2001; Erfanzadeh et al., 2010). These pioneer species found in the seed bank are responsible for healing clearings in tropical forests (Pereira et al., 2010; Correia & Martins, 2015). Thus, the composition and density of the seed banks evaluated in the current study suggest that they can be resilient to forest disturbances. However, it is essential highlighting the importance of monitoring and, if necessary, controlling the incidence of invasive exotic species in these areas.

Species presenting anemochorous dispersal syndrome prevailed in Forest 1 seed bank due to high herbaceous species density and richness, a fact that facilitated their dissemination in the area. Conversely, Forest 2 seed bank showed predominance of species with zoochorous dispersal syndrome, since Forest 2 is a well-preserved forest remnant at mid-successional stage. Zoochorous dispersal is the dispersal mode most often found in tropical forests (Sansevero et al., 2011), mainly in larger areas and fragment aggregations (Jesus et al., 2012).

Guimarães et al. (2014) have investigated the seed bank of four areas undergoing restoration process in the seasonal semideciduous forest phytophysiognomy belonging to the Atlantic Forest domain; each area was subjected to different restoration method types. Based on their results, anemochorous dispersal syndrome was the most dominant dispersion type (43.5% species); families Asteraceae and Poaceae recorded the highest number of anemochorous species. Similarly, Miranda Neto et al. (2017) conducted a study in a forest undergoing restoration after being subjected to bauxite mining activity and found predominance of anemochorous dispersion species, which mainly comprised herbaceous species; Poaceae was the most abundant family in the investigated site.

According to the present study, most bush-tree species presenting zoochorous dispersal syndrome were found along the strata of Forest 2. Thus, forests undergoing restoration process should naturally experience seed and seedling bank enrichment over time, since this forest type is attractive to seed dispersing fauna. The large number of zoochorous species assessed in Forest 2 flora helps conserving the fauna associated with the phytophysiognomy (Coelho et al., 2016) investigated in the present study. Moreover, Forest 2 houses key species for the restoration of degraded areas, such as Euterpe edulis Mart. This species has great reproductive ability, since its fruits are very attractive to the wild fauna (Matos & Bovi, 2002), a fact that facilitates its regeneration in the understory of forests, as well as its secondary growth, in addition to accelerating ecological succession processes through natural enrichment (Ribeiro et al., 2011).

4.2. Similarities

Floristic dissimilarity among Forest 1 and Forest 2 seed banks, Forest 1 planting and Forest 2 flora may be explained by the fact that a large percentage of adult tree species found in Forest 2 belong to the successional groups of late and early secondary species. Most of these species do not often form seed banks because they have large seeds that cannot easily move in plant litter and, consequently, they are hardly incorporated in the soil (Martins et al., 2015) and get more exposed to predators such as small rodents and ants. The density of viable seeds in Forest 2 seed bank tended to decrease because Forest 2 is a forest remnant at mid-successional stage. Despite the dissimilarity between Forest 1 seed bank and Forest 1 planted species, the natural enrichment of the forest undergoing restoration based on mid-successional stage forest species should take place within a few years and, consequently, the floristic similarity between them should increase due to the proximity of the two forests.

Although there is no floristic similarity between shrub-tree species in the investigated forests, the high similarity in the distribution of dispersal syndrome and successional category of shrub-tree species indicates that similar ecological processes have taken place in Forests 1 and 2. Moreover, the forest undergoing restoration is comparable to the reference forest in terms of configuration and distribution of propagule dispersal modes and ecological groups. Ecological processes provide important information about whether a given area undergoing restoration process can be resilient and reverse biodiversity losses (Brancalion et al., 2010; Bullock et al., 2011), as well as about the necessary conditions for forest succession implementation (Scheller et al., 2007).

5. CONCLUSION

The soil seed bank in the forest undergoing restoration process after being subjected to bauxite mining activity recorded higher density of emerging seedlings than that of the reference ecosystem. The higher seedling density found in the soil seed bank of the forest undergoing restoration is mostly attributed to pioneer herbaceous and shrub species. This outcome suggests their resilience potential in case of natural or anthropic disturbances.

The highly similar dispersal syndrome distribution and successional category of shrub-tree species indicated that ecological processes have taken place in both forests.

Therefore, we conclude that the restoration performed in the mined area has successfully recovered the soil seed bank density after a few years, as well as that the enrichment of tree species in this seed bank will naturally happen due to its proximity to the reference ecosystem (mid-successional stage forest).

ACKNOWLEDGEMENTS

We thank the Companhia Brasileira de Alumínio for providing infrastructure and financial support for the project (Agreement CBA / LARF / SIF-UFV). We also thank the National Counsel of Technological and Scientific Development of Brazil - CNPq for the PhD scholarship for the first author and the Research Productivity scholarship for the second author.

FINANCIAL SUPPORT Companhia Brasileira de Alumínio, (Agreement CBA/LARF/SIF-UFV). Conselho Nacional de Desenvolvimento Científico e Tecnológico, (Grant/Award Number: 142415/2013-8).

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Received: March 20, 2019; Accepted: September 11, 2019

Kelly de Almeida SilvaDepartamento de Engenharia Florestal, Universidade Federal de Viçosa - UFV, Av. PH Rolfs, s/n, CEP 36570-900, Vicosa, MG, Brasil e-mail: kellyalmeidaenf@yahoo.com.br

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