Richness of Cerrado Woody Species Engaged in Ecological Restoration in the Brazilian Federal District

Willian Barros Gomes Rodrigo Studart Corrêa Alexander Paulo do Carmo Balduíno About the authors

Abstract

This study has evaluated the richness of Cerrado woody species engaged in ecological restoration in the Brazilian Federal District (BFD). A survey gathered information on plant species traded by local nurseries, species recommended in restoration plans (PRADs), species effectively introduced in areas under restoration, and species present in preserved fragments of Cerrado. Results summed 566 Cerrado woody species from 80 botanical families of which 171 species were traded by local nurseries, 277 were recommended in PRADs, 190 were effectively used in restoration projects, and 434 species were sampled in fragments of native Cerrado. We found low similarity between species composition available in nurseries, recommended in PRADs, used in restoration projects and present in preserved fragments of native Cerrado. Such results indicate a poor connection between steps related to the selection of native woody species that make up initial plant communities on sites under ecological restoration.

Keywords:
Cerrado; plant diversity; rehabilitation

1. INTRODUCTION

The Cerrado biome houses more than 11,000 species of vascular plants and is the richest savanna in plant species in the world (Mendonça et al., 2008Mendonça RC, Felfili JM, Walter BMT, Silva MC Jr, Rezende AV, Filgueiras TS et al. Flora vascular do bioma Cerrado. In: Sano SM, Almeida SP, Ribeiro JF, editors. Cerrado: ecologia e flora. Brasília, DF: Embrapa Informação Tecnológica; 2008. p. 421-1279.). This biome has undergone severe degradation from the 1960s (Rada, 2013Rada N. Assessing Brazil’s Cerrado agricultural miracle. Food Policy 2013; 38: 146-155. 10.1016/j.foodpol.2012.11.002
https://doi.org/10.1016/j.foodpol.2012.1...
) mainly to support agriculture, urbanization, and mining activities (Beuchle et al., 2015Beuchle R, Grecchi RC, Shimabukuro YE, Seliger R, Eva HD, Sano E, Achard F. Land cover changes in the Brazilian Cerrado and Caatinga biomes from 1990 to 2010 based on a systematic remote sensing sampling approach. Applied Geography 2015; 58: 116-127. 10.1016/j.apgeog.2015.01.017
https://doi.org/10.1016/j.apgeog.2015.01...
; Klink & Machado, 2005Klink CA, Machado R. Conservation of Brazilian Cerrado. Conservation Biology 2005; 19(3): 707-713. 10.1111/j.1523-1739.2005.00702.x
https://doi.org/10.1111/j.1523-1739.2005...
; Sano et al., 2010Sano EE, Rosa R, Brito JL, Ferreira LG. Land cover mapping of the tropical savanna region in Brazil. Environmental Monitoring and Assessment 2010; 166(1-4): 113-124. 10.1007/s10661-009-0988-4
https://doi.org/10.1007/s10661-009-0988-...
; Spera et al., 2016Spera SA, Galford GL, Coe MT, Macedo MN, Mustard JF. Land-use change affects water recycling in Brazil’s last agricultural frontier. Global Change Biology 2016; 22(10): 3405-3413. 10.1111/gcb.13298
https://doi.org/10.1111/gcb.13298...
). As a result, only 54% of the original area remains under natural vegetation cover (Brasil, 2015Brasil. Mapeamento do uso e cobertura do cerrado: Projeto TerraClass Cerrado. Brasília, DF: Ministério do Meio Ambiente; 2015.).

Huge environmental liabilities in Brazilian biomes have triggered the demand for ecological restoration plans and projects, which aim at implementing strategies to rehabilitate natural ecosystems, environmental services, and ecological sustainability on degraded sites (Chazdon, 2008Chazdon RL. Beyond deforestation: restoring forests and ecosystem services on degraded lands. Science 2008; 320(5882): 1458-1460. 10.1126/science.1155365
https://doi.org/10.1126/science.1155365...
). As such, restoration projects intend to recover ecological and structural characteristics of ecosystems close to the previous original conditions (Palmer et al., 2016Palmer MA, Zedler JB, Falk DA. Ecological theory and restoration ecology. In: Palmer MA, Zedler JB, Falk DA, editors. Foundations of restoration ecology. 2nd ed. Washington, DC: Island Press; 2016. p. 3-26.). Many techniques have been used to achieve restoration goals, such as natural regeneration, assisted regeneration, direct seeding, nucleation, and tree plantation, which is the most common and traditional practice of ecological restoration (Reis et al., 2010Reis A, Bechara FC, Tres DR. Nucleation in tropical ecological restoration. Scientia Agricola 2010; 67(2): 244-250. 10.1590/S0103-90162010000200018
https://doi.org/10.1590/S0103-9016201000...
).

When projects rely on tree plantation, species richness and composition are vital characteristics of plant communities that will start up ecological succession on sites under restoration (Crouzeilles et al., 2017Crouzeilles R, Ferreira MS, Chazdon RL, Lindenmayer DB, Sansevero JB, Monteiro L et al. Ecological restoration success is higher for natural regeneration than for active restoration in tropical forests. Science Advances 2017; 3(11): e1701345. 10.1126/sciadv.1701345
https://doi.org/10.1126/sciadv.1701345...
; Rodrigues et al., 2009Rodrigues RR, Lima RA, Gandolfi S, Nave AG. On the restoration of high diversity forests: 30 years of experience in the Brazilian Atlantic Forest. Biological Conservation 2009; 142: 1242-1251. 10.1016/j.biocon.2008.12.008
https://doi.org/10.1016/j.biocon.2008.12...
; Siqueira et al., 2015Siqueira G, Terra G, Garcia LC, Lima LR, Ivanaukas NM, Brienza S Jr. Ecossistemas de referência para restauração florestal. In: Brancalion PHS, Gandolfi S, Rodrigues RR, editors. Restauração florestal. São Paulo: Oficina de Textos; 2015. p. 71-102.). However, many projects that opted for tree plantation have selected a limited number of woody species to compose initial plant communities (Barbosa et al., 2003Barbosa LM, Barbosa JM, Barbosa KC, Potomatti A, Martins SE, Asperti LM et al. Recuperação florestal com espécies nativas no estado de São Paulo: pesquisas apontam mudanças necessárias. Florestar Estatístico 2003; 6(14): 28-34.; Brancalion et al., 2013Brancalion PHS, Lima LR, Rodrigues RR. Restauração ecológica como estratégia de resgate e conservação da biodiversidade em paisagens antrópicas tropicais. In: Peres C, Barlow J, Gardner T, Vieira IC, editors. Conservação da biodiversidade em paisagens antropizadas do Brasil. Curitiba: UFPR; 2013. p. 565-587.; Corrêa et al., 2015Corrêa, RS, Melo Filho B, Pinheiro CQ, Santos PF. Floristic wood composition of revegetated mining sites in the Brazilian Federal District. Bioscience Journal 2015; 31(3): 908-922. 10.14393/BJ-v31n3a2015-22986
https://doi.org/10.14393/BJ-v31n3a2015-2...
; Durigan et al., 2010Durigan G, Engel VL, Torezan JM, Melo AC, Marques M, Martins S et al. Normas jurídicas para a restauração ecológica: uma barreira a mais a dificultar o êxito das iniciativas? Revista Árvore 2010; 34(3): 471-485. 10.1590/S0100-67622010000300011
https://doi.org/10.1590/S0100-6762201000...
; Rodrigues et al., 2009Rodrigues RR, Lima RA, Gandolfi S, Nave AG. On the restoration of high diversity forests: 30 years of experience in the Brazilian Atlantic Forest. Biological Conservation 2009; 142: 1242-1251. 10.1016/j.biocon.2008.12.008
https://doi.org/10.1016/j.biocon.2008.12...
). Failures in restoration projects have often been attributed to low species richness and low diversity of initial plant communities (Barbosa et al., 2003Barbosa LM, Barbosa JM, Barbosa KC, Potomatti A, Martins SE, Asperti LM et al. Recuperação florestal com espécies nativas no estado de São Paulo: pesquisas apontam mudanças necessárias. Florestar Estatístico 2003; 6(14): 28-34.).

Based on such a scenario, our objectives were to evaluate the richness of Cerrado woody species that has been recommended, available, and used for ecological restoration in the Brazilian Federal District and analyze its implications.

2. MATERIALS AND METHODS

2.1. Study area

This work was developed in the Brazilian Federal District (BFD), which is located on the Brazilian Central Plateau (Oliveira & Pompermayer, 2012Oliveira IP, Pompermayer EF. O meio ambiente legal. Revista Faculdade Montes Belos 2012; 5(3): 1-31.). BFD’s altitude ranges from 1,000 m to 1,200 m (Martins et al., 2004Martins ES, Reatto A, Carvalho OA Jr, Guimarães RF. Evolução geomorfológica do Distrito Federal. Planaltina: Embrapa Cerrados; 2004. (Documentos; 122).), local climate is Tropical Savanna (Aw, in Köppen-Geiger classification) with dry winters, rainy summers, and an annual rainfall mean of 1,500 mm (INMET, 2018Instituto Nacional de Meteorologia - INMET. Normais Climatológicas do Brasil 1981-2010 [Internet]. Brasília, DF: INMET; 2018 [cited 2020 Apr. 10]. Available from: Available from: https://bit.ly/2XRwuSK
https://bit.ly/2XRwuSK...
). All the fourteen Cerrado phytophysiognomies occur in the BFD (Walter, 2001Walter BMT. Pesquisa botânica na vegetação do Distrito Federal, Brasil. In: Cavalcanti TB, Ramos AE, editors. Flora do Distrito Federal, Brasil. Brasília, DF: Embrapa Recursos Genéticos e Biotecnologia; 2001. p. 59-86.) and 38.0% of BFD’s territory was originally covered by savanna formations, 43.2% by grassland formations, and 18.8% by forest formations, from which 5% were gallery forests (UNESCO, 2002Organização das Nações Unidas para a Educação, a Ciência e a Cultura - UNESCO. Vegetação do Distrito Federal: tempo e espaço: uma avaliação multitemporal da perda de cobertura vegetal no DF e da diversidade florística da Reserva da Biosfera do Cerrado - Fase 1. 2nd ed. Brasília, DF: 2002.).

2.2. Data gathering

Data were gathered from (1) plant nurseries, (2) restoration plans (PRADs), (3) academic works on plant species introduced in areas under restoration, and (4) species naturally present in preserved fragments of Cerrado. These four categories of sources were surveyed until sampling sufficiency was achieved for each category. Names of Cerrado woody species from 21 nurseries, 35 PRADs, 21 implemented PRADs, and 10 fragments of Cerrado were organized for this work (Figure 1). Lists of woody species recommended in PRADs were compiled at the local environmental agency library (Instituto Brasília Ambiental - IBRAM) and at the website Biblioteca Digital (IBRAM, 2018Instituto Brasília Ambiental - IBRAM. Biblioteca Digital [Internet]. 2018 [cited 2020 Apr. 9]. Available from: Available from: https://bit.ly/2XU5MbY
https://bit.ly/2XU5MbY...
). Taxa names were updated online as per the nomenclature of the Missouri Botanical Garden (MOBOT, 2016). Botanical families were organized according to The Angiosperm Phylogeny Group et al. (2016)Angiosperm Phylogeny Group; Chase MW, Christenhusz MJM, Fay MF, Byng JW, Judd WS et al. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical Journal of the Linnaean Society 2016; 181(1): 1-20. 10.1111/boj.12385
https://doi.org/10.1111/boj.12385...
.

Figure 1
Location of surveyed nurseries, implemented restoration plans (PRADs) and fragments of native Cerrado in the Brazilian Federal District.

2.3. Data analysis

Rarefaction curves (Colwell et al., 2012Colwell RK, Chao A, Gotelli NJ, Lin SY, Mao CX, Chazdon RL, Longino JT. Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. Journal of Plant Ecology 2012; 5(1): 3-21. 10.1093/jpe/rtr044
https://doi.org/10.1093/jpe/rtr044...
) periodically tested sampling sufficiency for each of the four surveyed categories by using the software R Core Team version 3.5.1 (2017)R Core Team. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2017 [cited 2020 Apr. 9]. Available from: Available from: http://www.R-project.org/
http://www.R-project.org/...
. Plant species within surveyed categories were compared by using Vegan package, according to Ugland et al. (2003Ugland KI, Gray JS, Ellingsen KE. The species-accumulation curve and estimation of species richness. Journal of Animal Ecology 2003; 72(5): 888-897. 10.1046/j.1365-2656.2003.00748.x
https://doi.org/10.1046/j.1365-2656.2003...
), Colwell et al. (2004)Colwell RK, Mao CX, Chang J. Interpolating, extrapolating, and comparing incidence-based species accumulation curves. Ecology 2004; 85(10): 2717-2727. 10.1890/03-0557
https://doi.org/10.1890/03-0557...
, and Kindt et al. (2006Kindt R, Van Damme P, Simons AJ. Patterns of species richness at varying scales in western Kenya: planning for agroecosystem diversification. Biodiversity and Conservation 2006; 15(10): 3235-3249. 10.1007/s10531-005-0311-9
https://doi.org/10.1007/s10531-005-0311-...
). Interpolated and extrapolated estimates of species richness were run at 95% confidence level as permutation allows drawing average curves of species accumulation and their empirical confidence intervals (Schilling et al., 2012Schilling AC, Batista JLF, Couto HZ. Ausência de estabilização da curva de acumulação de espécies em florestas tropicais. Ciência Florestal 2012; 22(1): 101-111. 10.5902/198050985083
https://doi.org/10.5902/198050985083...
). Bootsrap species richness estimator was used for species analysis and categorical data matrices were generated from the occurrence of the presence of species in each surveyed category.

Species origin was checked according to Mendonça et al. (2008Mendonça RC, Felfili JM, Walter BMT, Silva MC Jr, Rezende AV, Filgueiras TS et al. Flora vascular do bioma Cerrado. In: Sano SM, Almeida SP, Ribeiro JF, editors. Cerrado: ecologia e flora. Brasília, DF: Embrapa Informação Tecnológica; 2008. p. 421-1279.) and Cerrado native species were categorized according to their natural occurrence in Cerrado phytophysiognomies (Ribeiro & Walter, 2008Ribeiro JF, Walter BMT. As principais fitofisionomias do bioma Cerrado. In: Sano SM, Almeida SP, Ribeiro JP, editors. Cerrado: ecologia e flora. Brasília, DF: Embrapa Informação Tecnológica ; 2008. p. 151-212.). Data were organized on a table for summarizing the total number and the percentage number of Cerrado woody species engaged in each of the four surveyed categories.

3. RESULTS AND DISCUSSION

The survey of Cerrado woody species in 21 nurseries, 35 PRADs, 21 implemented PRADs, and ten preserved fragments of Cerrado in the Brazilian Federal District (BFD) were enough for reaching stability tendency on rarefaction curves (Figure 2). Procedure on sampling sufficiency adopted in this study emphasizes the asymptotic response to successive samplings (Figure 2) since plant species data from tropical ecosystems do not usually achieve inflection points on rarefaction curves (Corrêa et al., 2015Corrêa, RS, Melo Filho B, Pinheiro CQ, Santos PF. Floristic wood composition of revegetated mining sites in the Brazilian Federal District. Bioscience Journal 2015; 31(3): 908-922. 10.14393/BJ-v31n3a2015-22986
https://doi.org/10.14393/BJ-v31n3a2015-2...
; Schilling et al., 2012Schilling AC, Batista JLF, Couto HZ. Ausência de estabilização da curva de acumulação de espécies em florestas tropicais. Ciência Florestal 2012; 22(1): 101-111. 10.5902/198050985083
https://doi.org/10.5902/198050985083...
) as also shown in our work (Figure 2).

Figure 2
Rarefaction curves of Cerrado native woody species for the four surveyed categories: (a): nurseries; (b): restoration plans (PRADs); (c): implemented PRADs, and (d): preserved fragments of Cerrado. Bootstrap confidence intervals of 95% by interpolation and extrapolation. Error bars indicate estimated errors of means and unfilled dots represent sampling units.

This survey summed 566 Cerrado species from 80 botanical families, which account for 13.2% of the Cerrado’s vascular plant species identified so far (Mendonça et al., 2008Mendonça RC, Felfili JM, Walter BMT, Silva MC Jr, Rezende AV, Filgueiras TS et al. Flora vascular do bioma Cerrado. In: Sano SM, Almeida SP, Ribeiro JF, editors. Cerrado: ecologia e flora. Brasília, DF: Embrapa Informação Tecnológica; 2008. p. 421-1279.). There were 171 species from 45 families traded by local nurseries, 277 species from 64 families recommended in PRADs, 190 species from 52 families effectively used in restoration projects, and 434 species from 72 families were sampled in fragments from native Cerrado (Table 1).

Table 1
Cerrado woody species available in nurseries, recommended in the restoration plans, effectively used in restoration plans, and present in preserved fragments of Cerrado in the Brazilian Federal District.

The number of woody species traded by local nurseries made up 39% of the same found in native fragments of Cerrado and it may be insufficient to meet the demand of restoration plans for achieving rich and diverse plant communities. However, this scenario is better than the one found by Oliveira et al. (2017Oliveira CD, Gonzaga LM, Carvalho JA, Melo LA, Davide AC, Botelho SA. Riqueza de mudas de espécies florestais nativas potencialmente produzidas na Bacia do Rio Grande, MG. Pesquisa Florestal Brasileira 2017; 37(90): 159-170. 10.4336/2017.pfb.37.90.1342
https://doi.org/10.4336/2017.pfb.37.90.1...
), who evaluated the availability of native species saplings in nurseries settled in the Rio Grande catchment area, Minas Gerais (Brazil) and found a species richness lower than 10% compared to the regional native vegetation. Cerrado is the species-richest savanna in the world (Mendonça et al., 2008Mendonça RC, Felfili JM, Walter BMT, Silva MC Jr, Rezende AV, Filgueiras TS et al. Flora vascular do bioma Cerrado. In: Sano SM, Almeida SP, Ribeiro JF, editors. Cerrado: ecologia e flora. Brasília, DF: Embrapa Informação Tecnológica; 2008. p. 421-1279.) and the relatively low species richness available in nurseries (39%) is attributed to difficulties in collecting seeds from a wide range of native species and the poor knowledge on germination and growth of many native plant species (Oliveira et al., 2016Oliveira MC, Ogata RS, Andrade GA, Santos DS, Souza RM, Guimarães TG et al. Manual de viveiro e produção de mudas: espécies arbóreas nativas do Cerrado. Brasília, DF: Rede de Sementes do Cerrado; 2016.; Oliveira et al., 2017Oliveira CD, Gonzaga LM, Carvalho JA, Melo LA, Davide AC, Botelho SA. Riqueza de mudas de espécies florestais nativas potencialmente produzidas na Bacia do Rio Grande, MG. Pesquisa Florestal Brasileira 2017; 37(90): 159-170. 10.4336/2017.pfb.37.90.1342
https://doi.org/10.4336/2017.pfb.37.90.1...
; Santos & Queiroz, 2011Santos JJ, Queiroz SE. Diversidade de espécies nativas arbóreas produzidas em viveiros. Enciclopédia Biosfera 2011; 7(12): 1-8.). The main obstacles for plant sapling production of Brazilian native species are seed shortage (80%), difficulties in trading plant saplings (75%), and poor training for the management of native species (65%) (Silva et al., 2017Silva AP, Schweizer D, Marques HR, Teixeira AM, Santos TV, Sambuichi RH et al. Can current native tree seedling production and infrastructure meet an increasing forest restoration demand in Brazil? Restoration Ecology 2017; 25(4): 509-515. 10.1111/rec.12470
https://doi.org/10.1111/rec.12470...
).

Species richness recommended in the surveyed PRADs achieved 63.8% of that naturally present in fragments of Cerrado. However, restoration plans represent only the intention of setting up highly-diverse plant communities that will trigger ecological succession in degraded areas (Corrêa et al., 2015Corrêa, RS, Melo Filho B, Pinheiro CQ, Santos PF. Floristic wood composition of revegetated mining sites in the Brazilian Federal District. Bioscience Journal 2015; 31(3): 908-922. 10.14393/BJ-v31n3a2015-22986
https://doi.org/10.14393/BJ-v31n3a2015-2...
). Examined PRADs showed superficial and incomplete approaches to the problems intended to tackle, as some plans mostly swerved around real characteristics of sites to be restored and many proposed plant species were not adequate to them. Therefore, some PRADs were rather instruments to comply with environmental laws than to outline effective ecological restoration (Lima et al., 2006Lima HM, Flores JCC, Costa FL. Plano de recuperação de áreas degradadas versus plano de fechamento de mina: um estudo comparativo. REM: Revista Escola de Minas 2006; 59(4): 397-402. 10.1590/S0370-44672006000400008
https://doi.org/10.1590/S0370-4467200600...
). There were lists of activities and plant species in these plans that did not match the availability of sapling species traded in BFD nurseries. Sánchez (2010Sánchez LE. Planejamento e gestão do processo de recuperação de áreas degradadas. In: Alba JM, editor. Recuperação de áreas mineradas. 2nd ed. Brasília, DF: Embrapa Informação Tecnológica ; 2010. p. 103-121.) pointed out three major problems associated with PRADs: i) they usually are improperly drawn up and it results in unsatisfactory restoration when applied in practice; ii) they should be periodically updated; iii) proposed measures in PRADs are vague, generic, and difficult to check.

Studies on Cerrado phytophysiognomies have found 63 woody species in a hectare of sub-arboreal Cerrado (Cerrado stricto sensu) and 155 woody species in Cerrado’s forest formations (Amaral, 2008Amaral AG. Mudanças estruturais e florísticas do estrato herbáceo-arbustivo em campo sujo e campo limpo úmido na Fazenda Água Limpa - DF após um período de sete anos [thesis]. Brasília, DF: Instituto de Ciências Biológicas, Universidade de Brasília; 2008.; Andrade et al., 2002Andrade LAZ, Felfili JM, Violatti L. Fitossociologia de uma área de Cerrado denso na RECOR-IBGE, Brasília-DF. Acta Botanica Brasílica 2002; 16(2): 225-240. 10.1590/S0102-33062002000200009
https://doi.org/10.1590/S0102-3306200200...
; Aquino et al., 2014Aquino FG, Pereira CS, Passos FB, Oliveira MC. Composição florística e estrutural de um Cerrado sentido restrito na área de proteção de manancial Mestre D’Armas, Distrito Federal. Bioscience Journal 2014; 30(2): 565-575.; Brant, 2011Brant HSC. A fitossociologia do cerrado sentido restrito no Parque Recreativo do Gama (Prainha) - DF [monography]. Brasília, DF: Departamento de Engenharia Florestal, Universidade de Brasília; 2011.; Braga & Rezende, 2007Braga FMS, Rezende AV. Dinâmica da vegetação arbórea da mata de galeria do catetinho, Brasília-DF. Cerne 2007; 13(2): 138-148.; Haidar, 2007Haidar RF. Fitossociologia, diversidade e sua relação com variáveis ambientais em florestas estacionais do bioma Cerrado no Planalto Central e Nordeste do Brasil [thesis]. Brasília, DF: Departamento de Engenharia Florestal, Universidade de Brasília; 2007.; Nunes et al., 2002Nunes RV, Silva MC Jr, Felfili JM, Walter BMT. Intervalos de classe para abundância, dominância e frequência do componente lenhoso do Cerrado sentido restrito do Distrito Federal. Revista Árvore 2002; 26(2): 173-182.; Silva, 2009Silva JS. Diversidade alfa, florística e fitossociologia na ARIE do Cerradão, na APA Gama e Cabeça de Veado, DF [thesis]. Brasília, DF: Instituto de Ciências Biológicas, Universidade de Brasília; 2009.; Silva & Sarmento, 2009Silva MC Jr, Sarmento TR. Comunidades lenhosas no Cerrado sentido restrito em duas posições topográficas na estação ecológica do Jardim Botânico de Brasília, DF, Brasil. Rodriguésia 2009; 60(2): 277-294. 10.1590/2175-7860200960204
https://doi.org/10.1590/2175-78602009602...
; Silva et al., 2001Silva MC Jr, Felfili JM, Walter BMT, Nogueira PE, Rezende AV, Moraes RO et al. Análise da flora arbórea de matas de galeria no Distrito Federal: 21 levantamentos. In: Ribeiro JF, Fonseca CEL, Souza-Silva JC, editors. Cerrado: caracterização e recuperação de matas de galeria. Planaltina: Embrapa Cerrados ; 2001. p. 143-185.). Our data show local nurseries traded 26 Cerrado woody species on average, PRADs recommended 20 woody species on average, and executed PRADs used only 24 Cerrado woody species on average (Artioli, 2011Artioli CG. Uso de biomantas na revegetação de um fragmento de Mata de Galeria no Jardim Botânico de Brasília, DF: sobrevivência e desenvolvimento de mudas [thesis]. Brasília, DF: Departamento de Engenharia Florestal, Universidade de Brasília; 2011.; Barbosa, 2008Barbosa ACC. Recuperação de área degradada por mineração através da utilização de sementes e mudas de três espécies arbóreas do Cerrado no Distrito Federal [thesis]. Brasília, DF: Departamento de Engenharia Florestal, Universidade de Brasília; 2008.; Carvalheira, 2007Carvalheira MS. Avaliação do estabelecimento de espécies de Cerrado sentido restrito, a partir do plantio direto de sementes na recuperação de uma cascalheira na Fazenda Água Limpa - UnB [thesis]. Brasília, DF: Departamento de Engenharia Florestal, Universidade de Brasília; 2007.; Corrêa et al., 2007Corrêa RS, Melo Filho B, Baptista GMM. Avaliação fitossociológica da sucessão ecológica autogênica em áreas mineradas do Distrito Federal. Cerne 2007; 13(4): 406-415.; 2015Corrêa, RS, Melo Filho B, Pinheiro CQ, Santos PF. Floristic wood composition of revegetated mining sites in the Brazilian Federal District. Bioscience Journal 2015; 31(3): 908-922. 10.14393/BJ-v31n3a2015-22986
https://doi.org/10.14393/BJ-v31n3a2015-2...
; Cortes, 2012Cortes JM. Desenvolvimento de espécies nativas do Cerrado a partir do plantio de mudas e da regeneração natural em uma área em processo de recuperação, Planaltina, DF [thesis]. Brasília, DF: Departamento de Engenharia Florestal, Universidade de Brasília; 2012.; Ferreira et al., 2015Ferreira MC, Vieira DLM, Walter BMT. Topsoil translocation for Brazilian savanna restoration: propagation of herbs, shrubs, and trees. Restoration Ecology 2015; 23(6): 723-728. 10.1111/rec.12252
https://doi.org/10.1111/rec.12252...
; Fraga, 2016Fraga LP. Efeitos da aplicação de biossólido e resíduos de poda na revegetação de área de empréstimo no Distrito Federal [thesis]. Brasília, DF: Instituto de Ciências Biológicas, Universidade de Brasília; 2016.; Leite, 2014Leite TVP. Sistemas agroflorestais na recuperação de espaços protegidos por lei (AAP e Reserva Legal): estudo de caso do Sítio Geranium, DF [dissertation]. Brasília, DF: Departamento de Engenharia Florestal, Universidade de Brasília; 2014.; Lima et al., 2016Lima PAF, Gatto A, Albuquerque LB, Malaquias JV, Aquino FG. Crescimento de mudas de espécies nativas na restauração ecológica de matas ripárias. Neotropical Biology and Conservation 2016; 11(2): 72-79. 10.4013/nbc.2016.112.03
https://doi.org/10.4013/nbc.2016.112.03...
; Monteiro, 2014Monteiro MM. Efeito do hidrogel em plantios de mudas nativas do Cerrado para recuperação de área degradada pela mineração no Distrito Federal [thesis]. Brasília, DF: Departamento de Engenharia Florestal, Universidade de Brasília; 2014.; Oliveira, 2013Oliveira AJF. Recuperação de uma área degradada do cerrado através de modelos de nucleação, galharias e transposição de banco de sementes [dissertation]. Brasília, DF: Departamento de Engenharia Florestal, Universidade de Brasília; 2013.; Oliveira, 2014Oliveira LSC. Sucessão secundária em área de Cerrado stricto sensu durante um período de 23 anos após intervenções silviculturais [dissertation]. Brasília, DF: Departamento de Engenharia Florestal, Universidade de Brasília; 2014.; Oliveira, 2015Oliveira MC, Ribeiro JF, Passos FB, Aquino FG, Oliveira FF, Sousa SR. Crescimento de espécies nativas em um plantio de recuperação de Cerrado sentido restrito no Distrito Federal, Brasil. Revista Brasileira de Biociências 2015; 13(1): 25-32.; Oliveira et al., 2015Oliveira LS. Utilização de lodo de esgoto associado a três espécies nativas do Cerrado na recuperação de áreas degradadas [thesis]. Brasília, DF: Departamento de Engenharia Florestal, Universidade de Brasília; 2015.; Pachêco, 2014Pachêco BS. Chuva de sementes como indicador de restauração ecológica em matas ripárias do Distrito Federal [thesis]. Montes Claros: Centro de Ciências Biológicas e da Saúde, Universidade Estadual de Montes Claros; 2014.; Pinheiro et al., 2009Pinheiro CQ, Corrêa RS, Silveira IM, Jesus RS, Jorge RRA. Análise fitossociológica do estrato arbóreo de uma cascalheira revegetada no Distrito Federal. Cerne 2009; 15(2): 205-214.; Sampaio & Pinto, 2007Sampaio JC, Pinto JRR. Critérios para avaliação do desempenho de espécies nativas lenhosas em plantios de restauração no Cerrado. Revista Brasileira de Biociências 2007; 5(S1): 504-506.; Sousa, 2016Sousa AP. Avaliação de um programa de restauração de uma bacia hidrográfica: execução e envolvimento dos proprietários [thesis]. Brasília, DF: Departamento de Engenharia Florestal, Universidade de Brasília; 2016.; Souza, 2002Souza CC. Estabelecimento e crescimento inicial de espécies florestais em plantios de recuperação de matas de galeria no Distrito Federal [thesis]. Brasília, DF: Departamento de Engenharia Florestal, Universidade de Brasília; 2002.; Venturoli et al., 2013Venturoli F, Venturoli S, Borges JD, Castro DS, Souza DM, Monteiro MM, Calil FN. Incremento de espécies arbóreas em plantio de recuperação de área degradada em solo de Cerrado no Distrito Federal. Bioscience Journal 2013; 29(1): 143-151.).

Low average of species richness recommended in PRADs and in executed PRADs may be a result of low availability of native species in individual nurseries, although the pool of 21 surveyed nurseries in BFD traded 171 Cerrado woody species as a whole. Thus the range of 20-24 species introduced as initial plant communities on restoration sites is not reasonable because plant species for a given PRAD can be purchased from more than one nursery. Surprisingly, we found 190 Cerrado wood species on sites where PRADs had been executed and such figure suggests that some species could have come from elsewhere besides local nurseries. The introduction of species from other populations may lead to genetic contamination, extinction of local populations, and loss of genetic biodiversity, which opposes one of the ecological restoration goals. Yet, introduction of tree saplings from distinct ecological regions brings back genes that natural selection had already banned from the receiving area or genes previously inexistent in it (Durigan et al., 2010Durigan G, Engel VL, Torezan JM, Melo AC, Marques M, Martins S et al. Normas jurídicas para a restauração ecológica: uma barreira a mais a dificultar o êxito das iniciativas? Revista Árvore 2010; 34(3): 471-485. 10.1590/S0100-67622010000300011
https://doi.org/10.1590/S0100-6762201000...
).

Species-rich plant communities may guarantee restoration success as some studies point out that increases in ecosystem functions follow increases of species richness (Cardinale et al., 2007Cardinale BJ, Wright JP, Cadotte MW, Carroll IT, Hector A, Srivastava DS et al. Impacts of plant diversity on biomass production increase through time because of species complementarity. Proceedings of the National Academy of Sciences 2007; 104(46): 18123-18128. 10.1073/pnas.0709069104
https://doi.org/10.1073/pnas.0709069104...
; Solan et al., 2009Solan M, Godbold JA, Symstad A, Flynn DFB, Bunker DE. Biodiversity-ecosystem function research and biodiversity futures: early bird catches the worm or a day late and a dollar short? In: Naeem S, Bunker DE, Hector A, Loreau M, Perrings C, editors. Biodiversity, ecosystem functioning and human wellbeing: an ecological and economic perspective. Oxford: Oxford University Press; 2009. p. 30-45.). Barbosa et al. (2003Barbosa LM, Barbosa JM, Barbosa KC, Potomatti A, Martins SE, Asperti LM et al. Recuperação florestal com espécies nativas no estado de São Paulo: pesquisas apontam mudanças necessárias. Florestar Estatístico 2003; 6(14): 28-34.) found 355 native species in 30 plant nurseries in São Paulo State, Brazil, and an average of 30 native woody species in executed PRADs. The authors have attributed the low species richness on sites under restoration to the low availability of species in local nurseries. By comparison with our data, it seems that a low number of plant species available in individual nurseries have translated into low species richness in areas under restoration (Barbosa et al., 2003Barbosa LM, Barbosa JM, Barbosa KC, Potomatti A, Martins SE, Asperti LM et al. Recuperação florestal com espécies nativas no estado de São Paulo: pesquisas apontam mudanças necessárias. Florestar Estatístico 2003; 6(14): 28-34.).

Qualea grandiflora Mart. was the most frequent species found in preserved fragments of Cerrado in BFD and it was present in 80% of the surveyed sites. Tabebuia roseoalba (Ridl.) Sandwith was the most frequent species available in local nurseries and it was sold by 86% of the surveyed traders. Caryocar brasiliense Cambess. was the most recommended species in PRADs and appeared listed in 49% of them. Finally, Copaifera langsdorffii Desf. was the most frequent species effectively introduced in degraded areas and it was sampled in 62% of sites under restoration. Such a figure reflects the poor connection between the stages necessary for achieving a sound ecological restoration: reference ecosystem (Cerrado fragments), planning (PRADs), necessary support (nurseries), and execution of restoration projects.

Stepwise management of PRADs is critical for achieving successful ecological restoration (Corrêa et al., 2015Corrêa, RS, Melo Filho B, Pinheiro CQ, Santos PF. Floristic wood composition of revegetated mining sites in the Brazilian Federal District. Bioscience Journal 2015; 31(3): 908-922. 10.14393/BJ-v31n3a2015-22986
https://doi.org/10.14393/BJ-v31n3a2015-2...
). Among the 566 species recorded in this work, only 69 species (12%) were shared in between nurseries, PRADs, executed PRADs, and Cerrado fragments. Nurseries supply plant saplings for restoration projects, and PRADs and environmental agencies cannot overlook plant species that are effectively available in local nurseries (Barbosa et al., 2003Barbosa LM, Barbosa JM, Barbosa KC, Potomatti A, Martins SE, Asperti LM et al. Recuperação florestal com espécies nativas no estado de São Paulo: pesquisas apontam mudanças necessárias. Florestar Estatístico 2003; 6(14): 28-34.; Brancalion et al., 2013Brancalion PHS, Lima LR, Rodrigues RR. Restauração ecológica como estratégia de resgate e conservação da biodiversidade em paisagens antrópicas tropicais. In: Peres C, Barlow J, Gardner T, Vieira IC, editors. Conservação da biodiversidade em paisagens antropizadas do Brasil. Curitiba: UFPR; 2013. p. 565-587.; Durigan et al., 2010Durigan G, Engel VL, Torezan JM, Melo AC, Marques M, Martins S et al. Normas jurídicas para a restauração ecológica: uma barreira a mais a dificultar o êxito das iniciativas? Revista Árvore 2010; 34(3): 471-485. 10.1590/S0100-67622010000300011
https://doi.org/10.1590/S0100-6762201000...
; Sánchez, 2010Sánchez LE. Planejamento e gestão do processo de recuperação de áreas degradadas. In: Alba JM, editor. Recuperação de áreas mineradas. 2nd ed. Brasília, DF: Embrapa Informação Tecnológica ; 2010. p. 103-121.). Approximately 37% of the BFD territory was originally covered by sub-arboreal Cerrado (Cerrado stricto sensu) and most of the degraded sites are located in this phytophysiognomy (UNESCO, 2002Organização das Nações Unidas para a Educação, a Ciência e a Cultura - UNESCO. Vegetação do Distrito Federal: tempo e espaço: uma avaliação multitemporal da perda de cobertura vegetal no DF e da diversidade florística da Reserva da Biosfera do Cerrado - Fase 1. 2nd ed. Brasília, DF: 2002.). But 63.7% of species available in local nurseries, 62.5% of species recommended in PRADs, and 63.7% of species introduced on sites under restoration are from gallery forests (mata de galeria) (Table 2).

Table 2
Percentage of Cerrado woody species and absolute number of species found in the four surveyed categories in the Brazilian Federal District, according to the phytophysiognomy of natural occurrence.

Of the 21 implemented PRADs surveyed in this work, five (23.8%) were executed in areas of gallery forest, six on mining sites (28.6%), and ten (47.6%) in areas of sub-arboreal Cerrado (Cerrado stricto sensu), which is the phytophysiognomy mostly affected by degradation in BFD (UNESCO, 2002Organização das Nações Unidas para a Educação, a Ciência e a Cultura - UNESCO. Vegetação do Distrito Federal: tempo e espaço: uma avaliação multitemporal da perda de cobertura vegetal no DF e da diversidade florística da Reserva da Biosfera do Cerrado - Fase 1. 2nd ed. Brasília, DF: 2002.). However, the number of plant species from sub-arboreal Cerrado (Cerrado stricto sensu) ranked the third position after gallery forest (mata de galeria) and arboreal Cerrado (Cerradão) in PRADs and implemented PRADs. Only a third of Cerrado woody species available in the surveyed nurseries are from sub-arboreal Cerrado (Cerrado stricto sensu), and it may explain the prevalence of forest species in PRADs and implemented PRADs. According to Silva et al. (2017Silva AP, Schweizer D, Marques HR, Teixeira AM, Santos TV, Sambuichi RH et al. Can current native tree seedling production and infrastructure meet an increasing forest restoration demand in Brazil? Restoration Ecology 2017; 25(4): 509-515. 10.1111/rec.12470
https://doi.org/10.1111/rec.12470...
), many species available in nurseries in Brazil are endemic and require a biome-specific approach for their use in restoration projects. Selection of native woody species for ecological restoration in BFD has shown some deficiencies, such as low species richness. Hence, implemented PRADs applied less than 40% of the species richness present in preserved fragments of Cerrado.

The low number of pioneer species in areas of executed PRADs may also be a problem as only 23.7% of plant species in such areas are pioneer species (Table 1). São Paulo State regulation SMA 32/2014 requires 40% of pioneer species to compose initial plant communities on sites that will undergo ecological restoration. Pioneer species usually grow faster than plant species of advanced ecological stages (Durigan et al., 2010Durigan G, Engel VL, Torezan JM, Melo AC, Marques M, Martins S et al. Normas jurídicas para a restauração ecológica: uma barreira a mais a dificultar o êxito das iniciativas? Revista Árvore 2010; 34(3): 471-485. 10.1590/S0100-67622010000300011
https://doi.org/10.1590/S0100-6762201000...
) and it hastens the development of vegetation cover, which is an essential step towards the restoration of ecosystems (Corrêa et al., 2018Corrêa RS, Balduíno APC, Teza CTV, Baptista GMM. Vegetation cover development resulting from different restoration approaches of exploited mines. Floresta e Ambiente 2018; 25(4): e20171116. 10.1590/2179-8087.111617
https://doi.org/10.1590/2179-8087.111617...
). Another critical issue on BFD ecological restoration refers to the widespread use of forest species in areas of previously inhabited savanna formations. Such practice will likely lead succession towards the formation of forest ecosystems (Overbeck et al., 2013Overbeck GE, Hermann JM, Andrade BO, Boldrini II, Kiehl K, Kirmer A et al. Restoration ecology in Brazil: time to step out of the forest. Natureza & Conservação 2013; 11(1): 92-95. 10.4322/natcon.2013.015
https://doi.org/10.4322/natcon.2013.015...
; Parr et al., 2014Parr CL, Lehmann CER, Bond WJ, Hoffmann WA, Andersen AN. Tropical grassy biomes: misunderstood, neglected, and under threat. Trends in Ecology & Evolution 2014; 29(4): 205-213. 10.1016/j.tree.2014.02.004
https://doi.org/10.1016/j.tree.2014.02.0...
; Veldman et al., 2015Veldman JW, Overbeck GE, Negreiros D, Mahy G, Le Stradic S, Fernandes GW et al. Tyranny of trees in grassy biomes. Science 2015; 347(6221): 484-485. 10.1126/science.347.6221.484-c
https://doi.org/10.1126/science.347.6221...
).

Production of woody saplings from many different native species is a factor that currently limits ecological restoration in many parts of Brazil (Silva et al., 2017Silva AP, Schweizer D, Marques HR, Teixeira AM, Santos TV, Sambuichi RH et al. Can current native tree seedling production and infrastructure meet an increasing forest restoration demand in Brazil? Restoration Ecology 2017; 25(4): 509-515. 10.1111/rec.12470
https://doi.org/10.1111/rec.12470...
). There is currently a lack of knowledge on the production of plant saplings for several Cerrado native species (Barbosa et al., 2003Barbosa LM, Barbosa JM, Barbosa KC, Potomatti A, Martins SE, Asperti LM et al. Recuperação florestal com espécies nativas no estado de São Paulo: pesquisas apontam mudanças necessárias. Florestar Estatístico 2003; 6(14): 28-34.; Oliveira et al., 2016Oliveira MC, Ogata RS, Andrade GA, Santos DS, Souza RM, Guimarães TG et al. Manual de viveiro e produção de mudas: espécies arbóreas nativas do Cerrado. Brasília, DF: Rede de Sementes do Cerrado; 2016.; Oliveira et al., 2017Oliveira CD, Gonzaga LM, Carvalho JA, Melo LA, Davide AC, Botelho SA. Riqueza de mudas de espécies florestais nativas potencialmente produzidas na Bacia do Rio Grande, MG. Pesquisa Florestal Brasileira 2017; 37(90): 159-170. 10.4336/2017.pfb.37.90.1342
https://doi.org/10.4336/2017.pfb.37.90.1...
; Santos & Queiroz, 2011Santos JJ, Queiroz SE. Diversidade de espécies nativas arbóreas produzidas em viveiros. Enciclopédia Biosfera 2011; 7(12): 1-8.). As a result, it is rather difficult to find a broad sort of woody species in commercial nurseries (Oliveira et al., 2016Oliveira MC, Ogata RS, Andrade GA, Santos DS, Souza RM, Guimarães TG et al. Manual de viveiro e produção de mudas: espécies arbóreas nativas do Cerrado. Brasília, DF: Rede de Sementes do Cerrado; 2016.). Seed collection and appropriate germination protocols for Cerrado species are other limitations for ecological restoration (Viani & Rodrigues, 2007Viani RA, Rodrigues RR. Sobrevivência em viveiro de mudas de espécies nativas retiradas da regeneração natural de remanescente florestal. Pesquisa Agropecuária Brasileira 2007; 42(8): 1067-1075. 10.1590/S0100-204X2007000800002
https://doi.org/10.1590/S0100-204X200700...
), although there are already studies on these issues (Young et al., 2005Young TP, Petersen DA, Clary JJ. The ecology of restoration: historical links, emerging issues and unexplored realms. Ecology Letters 2005; 8(6): 662-673. 10.1111/j.1461-0248.2005.00764.x
https://doi.org/10.1111/j.1461-0248.2005...
).

Besides the difficulties to produce plant saplings from Cerrado species and the low species richness in BFD nurseries and PRADs, our study shows the detachment between species composition along the line nurseries, PRADs, and executed-PRADs, as only 22.9% of species were common to these three categories.

4. CONCLUSION

Cerrado woody species available in nurseries established in the Brazilian Federal District (BFD) made up 39% of the species richness found in native fragments of Cerrado as a whole. However, species richness found on sites under restoration falls to 5.5% of it on average. Total number of plant species traded in nurseries (171) can support plant communities richer in species than the ones recommended in PRADs (20 on average) and found in areas under restoration (24 on average). Restoration plans should therefore rely on various nurseries to increase species richness in initial plant communities.

There was a higher number of Cerrado species recommended in PRADs (277) than available in BFD nurseries (171) or growing in areas of executed PRADs (190). Such a figure portraits the unrealistic nature of the surveyed restoration plans.

ACKNOWLEDGEMENTS

We would like to thank the Instituto Brasília Ambiental (IBRAM) for supporting the data collection.

REFERENCES

  • Amaral AG. Mudanças estruturais e florísticas do estrato herbáceo-arbustivo em campo sujo e campo limpo úmido na Fazenda Água Limpa - DF após um período de sete anos [thesis]. Brasília, DF: Instituto de Ciências Biológicas, Universidade de Brasília; 2008.
  • Andrade LAZ, Felfili JM, Violatti L. Fitossociologia de uma área de Cerrado denso na RECOR-IBGE, Brasília-DF. Acta Botanica Brasílica 2002; 16(2): 225-240. 10.1590/S0102-33062002000200009
    » https://doi.org/10.1590/S0102-33062002000200009
  • Angiosperm Phylogeny Group; Chase MW, Christenhusz MJM, Fay MF, Byng JW, Judd WS et al. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical Journal of the Linnaean Society 2016; 181(1): 1-20. 10.1111/boj.12385
    » https://doi.org/10.1111/boj.12385
  • Aquino FG, Pereira CS, Passos FB, Oliveira MC. Composição florística e estrutural de um Cerrado sentido restrito na área de proteção de manancial Mestre D’Armas, Distrito Federal. Bioscience Journal 2014; 30(2): 565-575.
  • Artioli CG. Uso de biomantas na revegetação de um fragmento de Mata de Galeria no Jardim Botânico de Brasília, DF: sobrevivência e desenvolvimento de mudas [thesis]. Brasília, DF: Departamento de Engenharia Florestal, Universidade de Brasília; 2011.
  • Barbosa ACC. Recuperação de área degradada por mineração através da utilização de sementes e mudas de três espécies arbóreas do Cerrado no Distrito Federal [thesis]. Brasília, DF: Departamento de Engenharia Florestal, Universidade de Brasília; 2008.
  • Barbosa LM, Barbosa JM, Barbosa KC, Potomatti A, Martins SE, Asperti LM et al. Recuperação florestal com espécies nativas no estado de São Paulo: pesquisas apontam mudanças necessárias. Florestar Estatístico 2003; 6(14): 28-34.
  • Beuchle R, Grecchi RC, Shimabukuro YE, Seliger R, Eva HD, Sano E, Achard F. Land cover changes in the Brazilian Cerrado and Caatinga biomes from 1990 to 2010 based on a systematic remote sensing sampling approach. Applied Geography 2015; 58: 116-127. 10.1016/j.apgeog.2015.01.017
    » https://doi.org/10.1016/j.apgeog.2015.01.017
  • Braga FMS, Rezende AV. Dinâmica da vegetação arbórea da mata de galeria do catetinho, Brasília-DF. Cerne 2007; 13(2): 138-148.
  • Brancalion PHS, Lima LR, Rodrigues RR. Restauração ecológica como estratégia de resgate e conservação da biodiversidade em paisagens antrópicas tropicais. In: Peres C, Barlow J, Gardner T, Vieira IC, editors. Conservação da biodiversidade em paisagens antropizadas do Brasil Curitiba: UFPR; 2013. p. 565-587.
  • Brant HSC. A fitossociologia do cerrado sentido restrito no Parque Recreativo do Gama (Prainha) - DF [monography]. Brasília, DF: Departamento de Engenharia Florestal, Universidade de Brasília; 2011.
  • Brasil. Mapeamento do uso e cobertura do cerrado: Projeto TerraClass Cerrado Brasília, DF: Ministério do Meio Ambiente; 2015.
  • Cardinale BJ, Wright JP, Cadotte MW, Carroll IT, Hector A, Srivastava DS et al. Impacts of plant diversity on biomass production increase through time because of species complementarity. Proceedings of the National Academy of Sciences 2007; 104(46): 18123-18128. 10.1073/pnas.0709069104
    » https://doi.org/10.1073/pnas.0709069104
  • Carvalheira MS. Avaliação do estabelecimento de espécies de Cerrado sentido restrito, a partir do plantio direto de sementes na recuperação de uma cascalheira na Fazenda Água Limpa - UnB [thesis]. Brasília, DF: Departamento de Engenharia Florestal, Universidade de Brasília; 2007.
  • Chazdon RL. Beyond deforestation: restoring forests and ecosystem services on degraded lands. Science 2008; 320(5882): 1458-1460. 10.1126/science.1155365
    » https://doi.org/10.1126/science.1155365
  • Colwell RK, Chao A, Gotelli NJ, Lin SY, Mao CX, Chazdon RL, Longino JT. Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. Journal of Plant Ecology 2012; 5(1): 3-21. 10.1093/jpe/rtr044
    » https://doi.org/10.1093/jpe/rtr044
  • Colwell RK, Mao CX, Chang J. Interpolating, extrapolating, and comparing incidence-based species accumulation curves. Ecology 2004; 85(10): 2717-2727. 10.1890/03-0557
    » https://doi.org/10.1890/03-0557
  • Corrêa RS, Balduíno APC, Teza CTV, Baptista GMM. Vegetation cover development resulting from different restoration approaches of exploited mines. Floresta e Ambiente 2018; 25(4): e20171116. 10.1590/2179-8087.111617
    » https://doi.org/10.1590/2179-8087.111617
  • Corrêa RS, Melo Filho B, Baptista GMM. Avaliação fitossociológica da sucessão ecológica autogênica em áreas mineradas do Distrito Federal. Cerne 2007; 13(4): 406-415.
  • Corrêa, RS, Melo Filho B, Pinheiro CQ, Santos PF. Floristic wood composition of revegetated mining sites in the Brazilian Federal District. Bioscience Journal 2015; 31(3): 908-922. 10.14393/BJ-v31n3a2015-22986
    » https://doi.org/10.14393/BJ-v31n3a2015-22986
  • Cortes JM. Desenvolvimento de espécies nativas do Cerrado a partir do plantio de mudas e da regeneração natural em uma área em processo de recuperação, Planaltina, DF [thesis]. Brasília, DF: Departamento de Engenharia Florestal, Universidade de Brasília; 2012.
  • Crouzeilles R, Ferreira MS, Chazdon RL, Lindenmayer DB, Sansevero JB, Monteiro L et al. Ecological restoration success is higher for natural regeneration than for active restoration in tropical forests. Science Advances 2017; 3(11): e1701345. 10.1126/sciadv.1701345
    » https://doi.org/10.1126/sciadv.1701345
  • Durigan G, Engel VL, Torezan JM, Melo AC, Marques M, Martins S et al. Normas jurídicas para a restauração ecológica: uma barreira a mais a dificultar o êxito das iniciativas? Revista Árvore 2010; 34(3): 471-485. 10.1590/S0100-67622010000300011
    » https://doi.org/10.1590/S0100-67622010000300011
  • Ferreira MC, Vieira DLM, Walter BMT. Topsoil translocation for Brazilian savanna restoration: propagation of herbs, shrubs, and trees. Restoration Ecology 2015; 23(6): 723-728. 10.1111/rec.12252
    » https://doi.org/10.1111/rec.12252
  • Fraga LP. Efeitos da aplicação de biossólido e resíduos de poda na revegetação de área de empréstimo no Distrito Federal [thesis]. Brasília, DF: Instituto de Ciências Biológicas, Universidade de Brasília; 2016.
  • Haidar RF. Fitossociologia, diversidade e sua relação com variáveis ambientais em florestas estacionais do bioma Cerrado no Planalto Central e Nordeste do Brasil [thesis]. Brasília, DF: Departamento de Engenharia Florestal, Universidade de Brasília; 2007.
  • Instituto Brasília Ambiental - IBRAM. Biblioteca Digital [Internet]. 2018 [cited 2020 Apr. 9]. Available from: Available from: https://bit.ly/2XU5MbY
    » https://bit.ly/2XU5MbY
  • Instituto Nacional de Meteorologia - INMET. Normais Climatológicas do Brasil 1981-2010 [Internet]. Brasília, DF: INMET; 2018 [cited 2020 Apr. 10]. Available from: Available from: https://bit.ly/2XRwuSK
    » https://bit.ly/2XRwuSK
  • Kindt R, Van Damme P, Simons AJ. Patterns of species richness at varying scales in western Kenya: planning for agroecosystem diversification. Biodiversity and Conservation 2006; 15(10): 3235-3249. 10.1007/s10531-005-0311-9
    » https://doi.org/10.1007/s10531-005-0311-9
  • Klink CA, Machado R. Conservation of Brazilian Cerrado. Conservation Biology 2005; 19(3): 707-713. 10.1111/j.1523-1739.2005.00702.x
    » https://doi.org/10.1111/j.1523-1739.2005.00702.x
  • Leite TVP. Sistemas agroflorestais na recuperação de espaços protegidos por lei (AAP e Reserva Legal): estudo de caso do Sítio Geranium, DF [dissertation]. Brasília, DF: Departamento de Engenharia Florestal, Universidade de Brasília; 2014.
  • Lima HM, Flores JCC, Costa FL. Plano de recuperação de áreas degradadas versus plano de fechamento de mina: um estudo comparativo. REM: Revista Escola de Minas 2006; 59(4): 397-402. 10.1590/S0370-44672006000400008
    » https://doi.org/10.1590/S0370-44672006000400008
  • Lima PAF, Gatto A, Albuquerque LB, Malaquias JV, Aquino FG. Crescimento de mudas de espécies nativas na restauração ecológica de matas ripárias. Neotropical Biology and Conservation 2016; 11(2): 72-79. 10.4013/nbc.2016.112.03
    » https://doi.org/10.4013/nbc.2016.112.03
  • Martins ES, Reatto A, Carvalho OA Jr, Guimarães RF. Evolução geomorfológica do Distrito Federal Planaltina: Embrapa Cerrados; 2004. (Documentos; 122).
  • Mendonça RC, Felfili JM, Walter BMT, Silva MC Jr, Rezende AV, Filgueiras TS et al. Flora vascular do bioma Cerrado. In: Sano SM, Almeida SP, Ribeiro JF, editors. Cerrado: ecologia e flora Brasília, DF: Embrapa Informação Tecnológica; 2008. p. 421-1279.
  • Missouri Botanical Garden - MOBOT. Tropicos database [Internet]. Saint Louis: MOBOT; 2017 [cited 2018 Jan. 3]. Available from: Available from: https://bit.ly/2XXi0AE
    » https://bit.ly/2XXi0AE
  • Monteiro MM. Efeito do hidrogel em plantios de mudas nativas do Cerrado para recuperação de área degradada pela mineração no Distrito Federal [thesis]. Brasília, DF: Departamento de Engenharia Florestal, Universidade de Brasília; 2014.
  • Nunes RV, Silva MC Jr, Felfili JM, Walter BMT. Intervalos de classe para abundância, dominância e frequência do componente lenhoso do Cerrado sentido restrito do Distrito Federal. Revista Árvore 2002; 26(2): 173-182.
  • Oliveira AJF. Recuperação de uma área degradada do cerrado através de modelos de nucleação, galharias e transposição de banco de sementes [dissertation]. Brasília, DF: Departamento de Engenharia Florestal, Universidade de Brasília; 2013.
  • Oliveira CD, Gonzaga LM, Carvalho JA, Melo LA, Davide AC, Botelho SA. Riqueza de mudas de espécies florestais nativas potencialmente produzidas na Bacia do Rio Grande, MG. Pesquisa Florestal Brasileira 2017; 37(90): 159-170. 10.4336/2017.pfb.37.90.1342
    » https://doi.org/10.4336/2017.pfb.37.90.1342
  • Oliveira IP, Pompermayer EF. O meio ambiente legal. Revista Faculdade Montes Belos 2012; 5(3): 1-31.
  • Oliveira LSC. Sucessão secundária em área de Cerrado stricto sensu durante um período de 23 anos após intervenções silviculturais [dissertation]. Brasília, DF: Departamento de Engenharia Florestal, Universidade de Brasília; 2014.
  • Oliveira LS. Utilização de lodo de esgoto associado a três espécies nativas do Cerrado na recuperação de áreas degradadas [thesis]. Brasília, DF: Departamento de Engenharia Florestal, Universidade de Brasília; 2015.
  • Oliveira MC, Ribeiro JF, Passos FB, Aquino FG, Oliveira FF, Sousa SR. Crescimento de espécies nativas em um plantio de recuperação de Cerrado sentido restrito no Distrito Federal, Brasil. Revista Brasileira de Biociências 2015; 13(1): 25-32.
  • Oliveira MC, Ogata RS, Andrade GA, Santos DS, Souza RM, Guimarães TG et al. Manual de viveiro e produção de mudas: espécies arbóreas nativas do Cerrado Brasília, DF: Rede de Sementes do Cerrado; 2016.
  • Organização das Nações Unidas para a Educação, a Ciência e a Cultura - UNESCO. Vegetação do Distrito Federal: tempo e espaço: uma avaliação multitemporal da perda de cobertura vegetal no DF e da diversidade florística da Reserva da Biosfera do Cerrado - Fase 1 2nd ed. Brasília, DF: 2002.
  • Overbeck GE, Hermann JM, Andrade BO, Boldrini II, Kiehl K, Kirmer A et al. Restoration ecology in Brazil: time to step out of the forest. Natureza & Conservação 2013; 11(1): 92-95. 10.4322/natcon.2013.015
    » https://doi.org/10.4322/natcon.2013.015
  • Pachêco BS. Chuva de sementes como indicador de restauração ecológica em matas ripárias do Distrito Federal [thesis]. Montes Claros: Centro de Ciências Biológicas e da Saúde, Universidade Estadual de Montes Claros; 2014.
  • Palmer MA, Zedler JB, Falk DA. Ecological theory and restoration ecology. In: Palmer MA, Zedler JB, Falk DA, editors. Foundations of restoration ecology 2nd ed. Washington, DC: Island Press; 2016. p. 3-26.
  • Parr CL, Lehmann CER, Bond WJ, Hoffmann WA, Andersen AN. Tropical grassy biomes: misunderstood, neglected, and under threat. Trends in Ecology & Evolution 2014; 29(4): 205-213. 10.1016/j.tree.2014.02.004
    » https://doi.org/10.1016/j.tree.2014.02.004
  • Pinheiro CQ, Corrêa RS, Silveira IM, Jesus RS, Jorge RRA. Análise fitossociológica do estrato arbóreo de uma cascalheira revegetada no Distrito Federal. Cerne 2009; 15(2): 205-214.
  • Rada N. Assessing Brazil’s Cerrado agricultural miracle. Food Policy 2013; 38: 146-155. 10.1016/j.foodpol.2012.11.002
    » https://doi.org/10.1016/j.foodpol.2012.11.002
  • R Core Team. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2017 [cited 2020 Apr. 9]. Available from: Available from: http://www.R-project.org/
    » http://www.R-project.org/
  • Reis A, Bechara FC, Tres DR. Nucleation in tropical ecological restoration. Scientia Agricola 2010; 67(2): 244-250. 10.1590/S0103-90162010000200018
    » https://doi.org/10.1590/S0103-90162010000200018
  • Ribeiro JF, Walter BMT. As principais fitofisionomias do bioma Cerrado. In: Sano SM, Almeida SP, Ribeiro JP, editors. Cerrado: ecologia e flora Brasília, DF: Embrapa Informação Tecnológica ; 2008. p. 151-212.
  • Rodrigues RR, Lima RA, Gandolfi S, Nave AG. On the restoration of high diversity forests: 30 years of experience in the Brazilian Atlantic Forest. Biological Conservation 2009; 142: 1242-1251. 10.1016/j.biocon.2008.12.008
    » https://doi.org/10.1016/j.biocon.2008.12.008
  • Sampaio JC, Pinto JRR. Critérios para avaliação do desempenho de espécies nativas lenhosas em plantios de restauração no Cerrado. Revista Brasileira de Biociências 2007; 5(S1): 504-506.
  • Sánchez LE. Planejamento e gestão do processo de recuperação de áreas degradadas. In: Alba JM, editor. Recuperação de áreas mineradas 2nd ed. Brasília, DF: Embrapa Informação Tecnológica ; 2010. p. 103-121.
  • Sano EE, Rosa R, Brito JL, Ferreira LG. Land cover mapping of the tropical savanna region in Brazil. Environmental Monitoring and Assessment 2010; 166(1-4): 113-124. 10.1007/s10661-009-0988-4
    » https://doi.org/10.1007/s10661-009-0988-4
  • Santos JJ, Queiroz SE. Diversidade de espécies nativas arbóreas produzidas em viveiros. Enciclopédia Biosfera 2011; 7(12): 1-8.
  • Schilling AC, Batista JLF, Couto HZ. Ausência de estabilização da curva de acumulação de espécies em florestas tropicais. Ciência Florestal 2012; 22(1): 101-111. 10.5902/198050985083
    » https://doi.org/10.5902/198050985083
  • Silva AP, Schweizer D, Marques HR, Teixeira AM, Santos TV, Sambuichi RH et al. Can current native tree seedling production and infrastructure meet an increasing forest restoration demand in Brazil? Restoration Ecology 2017; 25(4): 509-515. 10.1111/rec.12470
    » https://doi.org/10.1111/rec.12470
  • Silva MC Jr, Felfili JM, Walter BMT, Nogueira PE, Rezende AV, Moraes RO et al. Análise da flora arbórea de matas de galeria no Distrito Federal: 21 levantamentos. In: Ribeiro JF, Fonseca CEL, Souza-Silva JC, editors. Cerrado: caracterização e recuperação de matas de galeria Planaltina: Embrapa Cerrados ; 2001. p. 143-185.
  • Silva MC Jr, Sarmento TR. Comunidades lenhosas no Cerrado sentido restrito em duas posições topográficas na estação ecológica do Jardim Botânico de Brasília, DF, Brasil. Rodriguésia 2009; 60(2): 277-294. 10.1590/2175-7860200960204
    » https://doi.org/10.1590/2175-7860200960204
  • Silva JS. Diversidade alfa, florística e fitossociologia na ARIE do Cerradão, na APA Gama e Cabeça de Veado, DF [thesis]. Brasília, DF: Instituto de Ciências Biológicas, Universidade de Brasília; 2009.
  • Siqueira G, Terra G, Garcia LC, Lima LR, Ivanaukas NM, Brienza S Jr. Ecossistemas de referência para restauração florestal. In: Brancalion PHS, Gandolfi S, Rodrigues RR, editors. Restauração florestal São Paulo: Oficina de Textos; 2015. p. 71-102.
  • Solan M, Godbold JA, Symstad A, Flynn DFB, Bunker DE. Biodiversity-ecosystem function research and biodiversity futures: early bird catches the worm or a day late and a dollar short? In: Naeem S, Bunker DE, Hector A, Loreau M, Perrings C, editors. Biodiversity, ecosystem functioning and human wellbeing: an ecological and economic perspective Oxford: Oxford University Press; 2009. p. 30-45.
  • Sousa AP. Avaliação de um programa de restauração de uma bacia hidrográfica: execução e envolvimento dos proprietários [thesis]. Brasília, DF: Departamento de Engenharia Florestal, Universidade de Brasília; 2016.
  • Souza CC. Estabelecimento e crescimento inicial de espécies florestais em plantios de recuperação de matas de galeria no Distrito Federal [thesis]. Brasília, DF: Departamento de Engenharia Florestal, Universidade de Brasília; 2002.
  • Spera SA, Galford GL, Coe MT, Macedo MN, Mustard JF. Land-use change affects water recycling in Brazil’s last agricultural frontier. Global Change Biology 2016; 22(10): 3405-3413. 10.1111/gcb.13298
    » https://doi.org/10.1111/gcb.13298
  • Ugland KI, Gray JS, Ellingsen KE. The species-accumulation curve and estimation of species richness. Journal of Animal Ecology 2003; 72(5): 888-897. 10.1046/j.1365-2656.2003.00748.x
    » https://doi.org/10.1046/j.1365-2656.2003.00748.x
  • Veldman JW, Overbeck GE, Negreiros D, Mahy G, Le Stradic S, Fernandes GW et al. Tyranny of trees in grassy biomes. Science 2015; 347(6221): 484-485. 10.1126/science.347.6221.484-c
    » https://doi.org/10.1126/science.347.6221.484-c
  • Venturoli F, Venturoli S, Borges JD, Castro DS, Souza DM, Monteiro MM, Calil FN. Incremento de espécies arbóreas em plantio de recuperação de área degradada em solo de Cerrado no Distrito Federal. Bioscience Journal 2013; 29(1): 143-151.
  • Viani RA, Rodrigues RR. Sobrevivência em viveiro de mudas de espécies nativas retiradas da regeneração natural de remanescente florestal. Pesquisa Agropecuária Brasileira 2007; 42(8): 1067-1075. 10.1590/S0100-204X2007000800002
    » https://doi.org/10.1590/S0100-204X2007000800002
  • Walter BMT. Pesquisa botânica na vegetação do Distrito Federal, Brasil. In: Cavalcanti TB, Ramos AE, editors. Flora do Distrito Federal, Brasil Brasília, DF: Embrapa Recursos Genéticos e Biotecnologia; 2001. p. 59-86.
  • Young TP, Petersen DA, Clary JJ. The ecology of restoration: historical links, emerging issues and unexplored realms. Ecology Letters 2005; 8(6): 662-673. 10.1111/j.1461-0248.2005.00764.x
    » https://doi.org/10.1111/j.1461-0248.2005.00764.x

Publication Dates

  • Publication in this collection
    06 July 2020
  • Date of issue
    2020

History

  • Received
    17 Jan 2018
  • Accepted
    18 Feb 2019
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