Agroforest Syst DOI 10.1007/s10457-017-0095-4
Agroforestry systems reduce invasive species richness and diversity in the surroundings of protected areas Anaı¨s de Almeida Campos Cordeiro . Sara Deambrozi Coelho . Nina Celli Ramos . Joa˜o Augusto Alves Meira-Neto
Received: 24 May 2016 / Accepted: 30 May 2017 Springer Science+Business Media Dordrecht 2017
Abstract The Serra do Brigadeiro State Park (PESB) is one of the largest fragments of Brazilian Atlantic Rainforest, and it is relevant for native species conservation. However, monocultures settled around the Park resulted in extensive open areas that facilitate the establishment of alien species on the PESB perimeter, which may threaten native species conservation therein, since biological invasion is the second main cause of global biodiversity loss. In this region, there are also farmers planting agroforestry systems (AFS), characterized by tree-based intercropping, which are structurally more similar to the Atlantic Rainforest reminiscent fragments present in the region and may limit local occurrence of potentially invasive exotic weeds for several reasons, such as the high levels of shade provided by trees, the groundcover that result from loss of tree leaves and the increased competition for belowground resources. This study aimed to test whether AFS limit exotic species establishment when compared to monoculture systems. Accordingly, three coffee monocultures and three agroforestry coffee plantations around the PESB
were studied. In each of the six study areas, 30 plots of 1 m2 were established between the lines of coffee plantation, where all species present were surveyed. In both treatments, rarefaction curves were constructed to evaluate native and exotic richness, and diversity of these two categories was estimated through Simpson index inverse (1/D). All 13 sampled exotic species were present in monocultures, but only three of them occurred in AFS. Besides, alien diversity in monocultures (1=D = 2.173 ± 0.011) was significantly higher than in AFS (1=D = 1.031 ± 0.001). Such changes in alien plant community between land-use show that AFSs limit invasive species establishment. Therefore, when planted around protected areas, AFS may contribute to the control of biological invasions and to biodiversity conservation. Keywords Biological invasion Exotic species Agroforestry systems Atlantic Rainforest PESB
Introduction A. de Almeida Campos Cordeiro (&) S. D. Coelho N. C. Ramos J. A. A. Meira-Neto (&) Laboratory of Ecology and Evolution of Plants, Department of Plant Biology, Federal University of Vic¸osa, Vic¸osa, Minas Gerais 36570-900, Brazil e-mail:
[email protected] J. A. A. Meira-Neto e-mail:
[email protected]
Conversion of natural areas into areas for agricultural practices is a major cause of landscape change and habitat fragmentation (Peneireiro 1999; Phalan et al. 2011). In forest areas, such changes lead to a decline in biodiversity through habitat loss and subsequent reduction of ecosystem services and resources for wildlife (Dobson et al. 1997; Peneireiro 1999; Foley
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et al. 2005; Phalan et al. 2011; Bateman et al. 2013). These landscape transformations also favor the establishment, increasing distribution and abundance of alien species (Pauchard and Alaback 2004) that modify community composition and structure, which in turn jeopardizes ecosystem functioning. Biological invasion is the process by which exotic species (species originating from other regions) establish and spread in either natural or man-made ecosystems (Ramos et al. 2015). The impacts of biological invasion from land-cover changes are present in many tropical areas as well as in the Brazilian Atlantic Forest, where deforestation has taken place in order to settle agricultural production systems and urban areas. Biological invasion is the second main cause of the global biodiversity crisis faced today by ecosystems and has been recognized as one of the most serious causes of species declines and native habitat degradation (Perrings et al. 2000), lagging behind only habitat destruction. A set of characteristics of invasive species may cause competitive advantages over natives. For instance, invasives usually have high growth rates and high reproductive allocation (Baruch and Bilbao 1999; Grotkopp and Rejma´nek 2007), high phenotypic plasticity (Pattison et al. 1998; Rogers and Siemann 2002; Daehler 2003) and they do not have natural enemies, such as pathogens and parasites (Rogers and Siemann 2002; Daehler 2003). Besides, invasive species may exhibit self-reinforcing mutualism mechanisms, by which well-established exotics may facilitate the establishment and spread of newly arriving ones, which potentially increase biological invasion rates (Simberloff and Holle 1999). In a local scale, low diverse crops such as monocultures may facilitate dispersion of exotic species through removal of competitors and increases in light intensities in potential invasion sites (Parendes and Jones 2000). These environmental features underlying land cover change could, therefore, strongly favour threatening species with very high chance to widespread at new open sites. This situation is even more concerning when close to protected areas, such as Areas of Permanent Preservation, Legal Reserves and Conservation Units (CU), where invasive alien species have become increasingly significant management problems (Pauchard and Alaback 2004). In Brazil, CU are widely recognized as important to maintain species and
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ecological processes (Baeza and Estades 2010; Pinto 2014). The CU Serra do Brigadeiro State Park (PESB) is one of the 77 Brazilian Atlantic Rainforest remaining fragments bigger than 100,000,000 m2 (Ribeiro et al. 2009; SOS Mata Atlaˆntica and INPE 2014). Therefore, it is a reminiscent of continuous forest very relevant for species conservation. However, its neighboring areas have been suffering biodiversity simplification due to the establishment of agricultural lands, which has led to local disturbances, such as canopy openness and high soil exposure to sunlight. These disturbance regimes facilitate invasion by heliophytic alien species (Pattison et al. 1998; Daehler 2003; Bisseleua et al. 2013), which find in these open areas a gateway for their establishment in the Park. In this context, one of the possible ways to contribute to species conservation in the PESB is to improve the quality of the surrounding agricultural landscape’s matrix. Under the current high rates of land-cover change in the tropics, agroforestry systems are gaining increasing importance. These systems result from the management of perennial and woody plants intercropped with agricultural crops and/or animals (Montagnini and Jordan 2005; Deitenbach et al. 2008), aiming to improve crop production and to reduce harmful impacts upon the environment through plant diversity cultivation and management. Agroforestry systems constitute a landscape’s productive matrix structurally more complex than monoculture systems (Bisseleua et al. 2013). They provide a wide range of subsistence products to local people (i.e., food, medicines, timber, plant resins and fibers) (Rice and Greenberg 2000; Castro et al. 2009; Mendes et al. 2013), as well as may help to recover degraded areas and maintain regional biodiversity (Cardoso et al. 2001; Arau´jo et al. 2007; Jose 2009; Bisseleua et al. 2013). Besides, AFSs have already been reported as effective in decreasing the recruitment of invasive species, predominantly heliophytic, because the presence of trees modify the intensity, duration and quality of sunlight reaching the ground (Ramos et al. 2015). Reduction of weeds in AFS may also be attributed to the increase in interspecific competition for belowground resources, to the groundcover provided by loss of tree leaves and to potential allelopathy (Rao et al. 1997). Therefore, the establishment of agroforestry food production in agricultural lands surrounding
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protected areas may generate a buffer zone that limits exotic invasive species occurrence by several means. In the case of coffee (Coffea arabica L.) plantations, the implementation of intercropping trees doesn’t affect productivity because coffee is a wellsuited plant to a certain level of shading (DaMatta 2004; Miguel and Carvalho 2005; Baliza et al. 2012; Charbonnier et al. 2013). As a matter of fact, coffee biennial production decreases under shading conditions, leading to a more steady production along the years, and branch dieback decreases in shaded environments (DaMatta 2004). Understanding the potential invasiveness of alien plant species in different types of land-uses is a key factor for elucidating the mechanisms underlying invasiveness processes of exotic plants and for preventing from the risk of future exotic plants spreading. In this context, we aimed to assess how the richness and diversity of alien species differs between agroforestry systems and traditional agricultural monocultures, focusing on areas immediately surrounding protected areas. We hypothesized that exotic species richness and diversity are lower in agroforestry coffee plantations than in coffee monocultures.
subsistence and economic activities include the cultivation of coffee (Ferrari 2010) and other food crops for domestic consumption. In the Zona da Mata region, the process of agriculture industrialization increased deforestation rates and encouraged the use of monocultures (mainly for coffee production) with consequent large amounts of external inputs, which contributed to environmental (e.g., biodiversity, soil, water) deterioration (Cardoso et al. 2001). Therefore, the socio-agricultural context during the last decades changed the landscape composition from a continuous forest to a mosaic of patches of forests fragments, pastures, agricultural monocultures and, more recently, agroforestry systems. Aiming to reverse such environmental deterioration, alternative solutions have been applied. Since 1994, several projects from the Federal University of Vic¸osa have been implementing an intense awareness campaign for farmers in this region, through the adoption of agroforestry systems (Cardoso et al. 2001). The result of these projects is the actual existence of some farms with coffee production intercropped with arboreal species, constituting AFS. Data collection strategy
Materials and methods Study area This study was carried out in the surrounding area of the PESB, located in the Zona da Mata region, Southeastern of Minas Gerais State, Brazil (Fig. 1). The original vegetation of the Serra do Brigadeiro is Seasonal Semideciduous Forest and Dense Ombrophylous Forest, within the Atlantic Rainforest biome (Soares et al. 2006). The climate is mild mesothermal (Cwb) with hot, humid summers and cold, dry winters, when up to 50% of the trees lose their leaves (Soares et al. 2006). The mean annual precipitation and temperature are, respectively, 1500 mm and 18 C (Cardoso et al. 2001; Caiafa and Silva 2007). The dominant soil types in the Zona da Mata are Oxisols, characterized as deep, well drained, acidic and poor in nutrient availability (Cardoso et al. 2001). Local population is composed mostly by family smallholders representing the majority of the rural population in the region, for which the main
We selected three different farms located in the surrounding area of the PESB. Selected farms were characterized by coffee monocultures (CAF treatment) adjacent to agroforestry coffee systems (AFS treatment), both located at the same slope and with similar environmental conditions, such as soil type, sunlight exposure and altitude. Table 1 specifies geographical coordinates of the three farms and the predominant intercropping species in each AFS. In each farm, we sampled 60 circular plots (30 plots per treatment) of 1 m2, located between the coffee lines, side by side, with minimum distance of 5 m between plots. The distance between the coffee plantation lines was approximately two meters in both AFS and CAF. Pesticides were not used at all in any of the farms, and the weed control was not carried out between the lines of coffee plantations for more than a month before data collection. Sampling was performed between July and August 2012 and included all individuals taller than 4 cm present in the plots. Individuals were identified to the lowest possible taxonomic level according to the
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Agroforest Syst Fig. 1 Location of the State Park of Serra do Brigadeiro (PESB), Minas Gerais State, Southeastern Brazil
Table 1 Geographic location of the studied farms around the PESB, Minas Gerais State (Brazil), where samples were held, and predominant intercropping species in each agroforestry system Property Property #1
Geographic location 0
00
0
Dominant species in AFS 00
2039 23 S 4233 12 W
Avocado (Persea americana Mill.)
Property #2
20410 5400 S 42310 4600 W
Inga species (Inga spp.)
Property #3
20400 1400 S 42330 1800 W
Banana (Musa paradisiaca L.)
Angiosperm Phylogeny Group III classification system (APG III 2009). After identification, each species was classified as native or exotic, according to the online database Species List of Brazilian Flora (2016). As this database classifies species into native, naturalized or cultivated, the latter two categories were considered as exotic. A subsequent literature review was made on all sampled exotic species, in order to detect their invasiveness ability.
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Data analysis Rarefaction curves were constructed for native and exotic species in both treatments, with a 95% confidence interval, using the software EstimateS 9.1.0. Plots that contained no individuals were not included in the analysis. Richness difference between native and exotic species in AFS and CAF was assessed via overlapping of the rarefaction curves. Richness
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difference is statistically significant when there is no overlapping between the curve of the community with lowest richness and the confidence interval of the ´ rva et al. 2015). richest community (Magurran 2004; A The Simpson Index (D) was estimated to assess native and exotic diversity in each treatment. This index takes into account both species richness and relative abundance of each species. If expressed as 1/ D, the higher the index, the greater is the diversity of the sample (Magurran 2004; Somerfield et al. 2008). The formula used to calculate the index was: D1 ¼ Ps1 i¼1
p2i
; where s is the species richness in the
community and pi is the ith species proportion. An analysis of variance was subsequently used to assess the difference between the calculated index for exotic and native species in each treatment.
Results In total, 5504 individuals were sampled, belonging to 48 species and 22 families (see Table 2 in Appendix). A Venn diagram in Fig. 2 shows the total number of native and exotic species and individuals found in each treatment.
2288 sampled individuals belonged to 13 exotic species: Bidens sulphurea Sch. Bip., Dichondra repens J. R. Forst. & G. Forst., Drymaria cordata (L.) Willd. ex Schult., Elephantopus mollis Kunth, Galinsoga parviflora Cav., Lepidium ruderale L., Melinis minutiflora P. Beauv., Oxalis corniculata L., O. latifolia Kunth, O. martiana Zucc., Rumex obtusifolius L., Taraxacum officinale F. H. Wigg. and Thelypteris dentata (Forssk.) E. P. St. John. All of them were present in CAF treatment, but only three also occurred in AFS: D. repens, O. corniculata and O. martiana. The remaining 3216 individuals belonged to 35 native species, six of which were present only in AFS: Brunfelsia sp., Myrsine ferruginea (Ruiz & Pav.) Spreng., Nectandra lanceolata Nees & Mart., Psychotria sp., Richardia brasiliensis Gomes and Senna pendula (Humb. & Bonpl. ex. Willd.) H.S. Irwin & Barneby. Fourteen of the sampled native species occurred only in CAF: Bidens pilosa L., Chamaecrista nictitans Moench, Conyza bonariensis (L.) Cronquist, Desmodium uncinatum (Jacq.) DC., Dioscorea sp., Erechtites valerianifolius (Link ex. Spreng.) DC., Euphorbia heterophylla L., E. hirta L., Gnaphalium spicatum Mill., Ipomoea sp., Mitracarpus hirtus DC., Plantago tomentosa Lam., Sida urens L. and Sonchus
Fig. 2 Venn diagram showing richness and abundance of sampled native and exotic species in agroforestry systems (AFS) and monoculture coffee production (CAF) around the PESB, in the Zona da Mata region of Minas Gerais, Southeastern Brazil
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Simpson Index inverse (1/D)
oleraceus L. The remaining 15 sampled native species were present in both treatments. Overlapping of rarefaction curves for exotic species in each treatment showed that exotics richness was significantly higher in CAF than in AFS (Fig. 3). On the other hand, for native community there was no difference between overall accumulation of species in CAF and in AFS (Fig. 4), since natives accumulation curve in AFS was totally positioned inside the confidence interval of the rarefaction curve of monoculture stands. Simpson Index distribution for exotic species (Fig. 5) pointed out higher diversity of exotics in CAF than in AFS. This result was corroborated by the ANOVA that tested the difference between mean
3.5 3 2.5 2 1.5
Monocultures
1
Agroforestry systems
0.5 0
0
15
30
45
60
Plots
Fig. 5 Distribution of Simpson index inverse for exotic species sampled in monocultures and agroforestry systems around the PESB, Minas Gerais State, Southeastern Brazil. Dashed lines indicate the 95% significance interval
Exotic species number
18 14 10 6
Monocultures
2 -2
Agroforestry systems 0
10
20
30
40
50
60
Plots
Fig. 3 Rarefaction curves for exotic species sampled in monocultures and agroforestry systems around the PESB, Minas Gerais State, Southeastern Brazil. Dashed lines indicate the 95% significance interval for each curve Fig. 6 Boxplots of Simpson index of exotic species in agroforestry systems (AFS) and monocultures (CAF) around the Brigadeiro State Park, Brazil. Different letters mean significant difference tested by ANOVA results for comparison between diversity of exotic species sampled
Native species number
40
30
20
10
0
Monocultures Agroforestry systems 0
15
30
45
60
75
90
Plots
Fig. 4 Rarefaction curves for native species sampled in monocultures and agroforestry systems around the PESB, Minas Gerais State, Southeastern Brazil. Dashed lines indicate the 95% significance interval for each curve
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diversity values (1=D) calculated for exotic species (F = 5150.7, p \ 0.001) (Fig. 6). Estimated 1=D for exotics were 2.173 ± 0.011 in CAF and 1.031 ± 0.001 in AFS. On the other hand, Simpson Index distribution for natives (Fig. 7) indicates less diversity of these species in CAF than in AFS, as also shown by ANOVA results (Fig. 8; F = 32.535, p \ 0.001). The mean diversity values (1=D) calculated for natives were 1.168 ± 0.010 in monocultures and 1.312 ± 0.026 in agroforestry systems.
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Simpson Index inverse (1/D)
5 4.5 4 3.5 3 2.5 2
Monocultures
1.5 1
Agroforestry systems
0.5 0
0
15
30
45
60
75
90
Plots
Fig. 7 Distribution of Simpson index inverse for native species sampled in monocultures and agroforestry systems around the PESB, Minas Gerais State, Southeastern Brazil. Dashed lines indicate the 95% significance interval
Fig. 8 Boxplots of Simpson index of native species in agroforestry systems (AFS) and monocultures (CAF) around the Brigadeiro State Park, Brazil. Different letters mean significant difference tested by ANOVA results for comparison between diversity of exotic species sampled
Discussion This study shows that agroforestry systems not only limit potentially invasive exotic species establishment in agricultural lands originally covered by BraziliAmong all species sampled in the studied AFS, only 12.5% were exotic. Nevertheless, exotic species encompassed 34.7% of total sampled individuals in
AFS, which points out their great ability to reproduce. Among all 13 exotic species, nine have already been recorded for their invasiveness abilities: B. sulphurea, D. cordata, E. mollis, G. parviflora, M. minutiflora, O. corniculata, O. latifolia, R. obtusifolius and T. officinale (Estelita-Teixeira 1977; Klein and Felippe 1991; Neto and Gama 2005; Gasparino et al. 2006; Cardoso and Pereira 2008; Hoffmann and Haridasan 2008; Molina-Montanegro et al. 2010; Silva e Mueller 2010; Zenni and Ziller 2011; Medeiros et al. 2017). Three species are exotic but non-invasive: D. repens, L. ruderale and T. dentata (Santos and Sylvestre 2006; Schneider 2008; Colmanetti et al. 2015), and no records were found on the invasiveness ability of O. martiana. The lowest accumulation of exotic species in agroforestry coffee plantations indicates limited invasive species establishment therein. The study of Ramos et al. (2015), conducted at the same study areas, found lower phylogenetic diversity of exotic species in the agroforestry systems when compared to the monocultures, and related this phylogenetic diversity pattern to the difference in light incidence among treatments (24.54% of canopy openness at the AFS and 50.52% at the coffee monocultures; v2 = 6.436, p = 0.01). Other studies show that high sunlight incidence on exposed soil in monocultures facilitates invasive species establishment (Pattison et al. 1998; Daehler 2003; Bisseleua et al. 2013). Accordingly, lower accumulation of alien species in AFS can be at least partially attributed to the shading generated by trees. Still, the occurrence of three exotic species and 1661 exotic individuals in agroforestry plantations shows that some alien species are welladapted to lower levels of light incidence. Further studies are necessary in order to test whether other factors, such as groundcover and competition for belowground resources, also limit exotic species establishment in agroforestry systems. The Simpson Index distribution indicates greater exotics diversity in monocultures than in AFS, which was corroborated by ANOVA results. In general, low biodiversity cultivation practices, such as monocultures, remove competitors and predators from the ecosystem, making the area more vulnerable to biological invasions (Perrings et al. 2002; Bisseleua et al. 2013). The lower Simpson Index for exotic species in AFS corroborates the results of their limited
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establishment in these areas, where only few species of the exotic regional pool survive due to their ability to grow and to reproduce under high levels of shading (Ramos et al. 2015). There was no significant difference between native species richness in AFS and monocultures, and AFS showed higher natives diversity than monocultures. These results are consistent with the evolutionary history of native understory weeds, since these species naturally exhibit adaptive strategies to survive in shaded environments. They probably have good photosynthetic performance and satisfactory biomass production, being able to reproduce even in habitats with high canopy cover (Garcia and Couto 1991; Pattison et al. 1998; Daehler 2003). Therefore, agroforestry food production around protected areas seems not only to limit biological invasion, but also promotes some native biodiversity maintenance in these areas. In sum, our results support the hypothesis that AFS are high quality landscape matrices that may act as efficient buffer zones in agricultural landscapes surrounding protected forest areas. Favoring diversity of crop and planting agricultural areas structurally similar to forests seems to be an efficient way of controlling biological invasions (Moonen and Barberi 2008) and maintaining native understory weeds in regions of forest vegetation such as the Atlantic Rainforest domain. The use of agroforestry systems has important socio-environmental benefits. Agroforestry food production is a potential conciliator of an effective biological conservation with agricultural production in Brazil, representing a viable way of sustainable agriculture (Peneireiro 1999; Bisseleua et al. 2013; Charbonnier et al. 2013). AFS are sources of ecosystem services for local populations and seems to maintain the conservation value of these agricultural landscapes. Under a scenario of increasing pressure for agriculture industrialization, agroforestry management practices should be adopted by local farmers as well as by institutions in order to improve sustainability of the systems. Acknowledgements The authors thank CNPq, CAPES and FAPEMIG for grants and scholarships. JAAMN has CNPq productivity fellowship. We are also grateful to all farmers that allowed us to develop our fieldwork in their properties.
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Appendix See Table 2. Table 2 Floristic survey and abundance of species sampled in agricultural lands around the PESB, in Minas Gerais State, Southeastern Brazil Family/species
Category
Abundance AFS
CAF
Asteraceae Ageratum conyzoides L.
Native
2
249
Baccharis dracunculifolia DC.
Native
2
11
Bidens pilosa L.
Native
0
18
Bidens sulphurea Sch. Bip.
Exotic
0
1
Chaptalia nutans (L.) Pol. Conyza bonariensis (L.) Cronquist
Native Native
55 0
4 3
Elephantopus mollis Kunth
Exotic
0
2
Emilia sonchifolia (L.) DC.
Native
1
32
Erechtites valerianifolius (Link ex Spreng.) DC.
Native
0
1
Galinsoga parviflora Cav.
Exotic
0
1
Gnaphalium spicatum Mill.
Native
0
24
Sonchus oleraceus L.
Native
0
25
Taraxacum officinale F.H. Wigg.
Exotic
0
1
Exotic
0
495
Exotic
0
53
Brassicaceae Lepidium ruderale L. Caryophyllaceae Drymaria cordata (L.) Willd. ex Schult. Commelinaceae Commelina erecta L.
Native
27
809
Commelina sp.
Native
235
1045
Dichondra repens J.R. Forst. & G. Forst.
Exotic
6
48
Ipomoea sp.
Native
0
2
Native
165
100
Native
0
3
Convolvulaceae
Cyperaceae Cyperus rotundus L. Dioscoreaceae Dioscorea sp. Euphorbiaceae Euphorbia heterophylla L.
Native
0
1
Euphorbia hirta L.
Native
0
2
Chamaecrista nictitans Moench
Native
0
1
Desmodium uncinatum (Jacq.) DC.
Native
0
1
Fabaceae
Agroforest Syst Table 2 continued Family/species
References Category
Abundance AFS
Senna pendula (Humb. & Bonpl. ex Willd.) H.S. Irwin & Barneby
CAF
Native
1
0
Native
1
0
Native
8
4
Lauraceae Nectandra lanceolata Nees & Mart. Lythraceae Cuphea carthagenensis (Jacq.) J. F. Macbr. Malvaceae Sida lonchitis A.St.-Hil. & Naudin
Native
2
2
Sida urens L.
Native
0
1
Oxalis corniculata L.
Exotic
478
1113
Oxalis latifolia Kunth
Exotic
0
28
Oxalis martiana Zucc.
Exotic
1
15
Native
10
64
Native
0
1
Oxalidaceae
Phyllanthaceae Phyllanthus tenellus Roxb. Plantaginaceae Plantago tomentosa Lam. Poaceae Melinis minutiflora P. Beauv.
Exotic
0
11
Paspalum sp.
Native
190
82
Exotic
0
1
Native
2
0
Polygonaceae Rumex obtusifolius L. Primulaceae Myrsine ferruginea (Ruiz & Pav.) Spreng. Rubiaceae Psychotria sp.
Native
2
0
Richardia brasiliensis Gomes Mitracarpus hirtus DC.
Native Native
2 0
0 6
Native
2
2
Brunfelsia sp.
Native
1
0
Capsicum baccatum L.
Native
1
4
Solanum cernuum Vell.
Native
1
1
Solanum granuloso-leprosum Dunal
Native
5
3
Exotic
0
34
Salicaceae Casearia decandra Jacq. Solanaceae
Thelypteridaceae Thelypteris dentata (Forssk.) E.P. St. John
CAF coffee monoculture systems, AFS agroforestry systems
Apg III (2009) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot J Linn Soc 161(2):105–121 Arau´jo DD, Chiodi RE, Ribeiro AP et al (2007) Ana´lise da diversidade de espe´cies vegetais e sua relac¸a˜o com os solos de sistemas agroflorestais do Alto Jequitinhonha – MG. R Bras Agroecol 2(1):391–394 ´ rva D, Speczia´r A, Er} A os T, To´th M (2015) Effects of habitat types and within lake environmental gradients on the diversity of chironomid assemblages. Limnologica 53:26–34 Baeza A, Estades CF (2010) Effect of the landscape context on the density and persistence of a predator population in a protected area subject to environmental variability. Biol Conserv 143(1):94–101 ´ vila Baliza DP, Cunha RL, Guimara˜es RJ, Barbosa JPRAD, A FW, Passos AMA (2012) Physiological characteristics and development of coffee plants under different shading levels. R Bras Ci Agr 7(1):37–43 Baruch Z, Bilbao B (1999) Effects of fire and defoliation on the life history of native and invader C4 grasses in a Neotropical savanna. Oecologia 119:510–520 Bateman IJ, Harwood AR, Mace GM et al (2013) Bringing ecosystem services into economic decision-making: land use in the United Kingdom. Science 341(45):45–50 Bisseleua HBD, Fotio D, Yede Missoup AD, Vidal S (2013) Shade tree diversity, cocoa pest damage, yield compensating inputs and farmers’ net returns in West Africa. PLoS One 8(3):e56115 Caiafa AN, Silva AF (2007) Structural analysis of the vegetation on a highland granitic rock outcrop in Southeast Brazil. Rev Bras Bot 30(4):657–664 Cardoso VJM, Pereira FJM (2008) Germinac¸a˜o de sementes de Drymaria cordata (L.) Willd. ex Roem & Schult.: efeito do potencial hı´drico. Braz J Bot 31:253–261 Cardoso IM, Guijt I, Franco FS, Carvalho AF, Ferreira-Neto PS (2001) Continual learning for agroforestry system design: University, NGO and farmer partnership in Minas Gerais. Brazil Agric Syst 69(3):235–257 Castro AP, Fraxe TJP, Santiago JL, Matos RB, Pinto IC (2009) Os sistemas agroflorestais como alternativa de sustentabilidade em ecossistemas de va´rzea no Amazonas. Acta Amaz 39(2):279–288 Charbonnier F, Maire G, Dreyer E et al (2013) Competition for light in heterogeneous canopies: application of MAESTRA to a coffee (Coffea arabica L.) agroforestry system. Agric Forest Meteorol 181:152–169 Colmanetti MAA, Shirasuna RT, Barbosa LM et al (2015) Nonarboreal vascular flora in a reforestation implanted with native seedlings. Hoehnea 42:725–735 da Silva L, Mueller S (2010) Avaliac¸a˜o de coberturas vegetais no solo sobre a incideˆncia de plantas daninhas e na produtivi´ gora Rev Divulg Cientı´fica 17:12–19 dade de tomate. A Daehler CC (2003) Performance comparisons of co-occurring native and alien invasive plants: implications for conservation and restoration. Annu Rev Ecol Evol Syst 34:183–211
123
Agroforest Syst DaMatta FM (2004) Ecophysiological constraints on the production of shaded and unshaded coffee: a review. Field Crops Res 86:99–114 de Medeiros N, Seixas DP, Batista JC et al (2017) Densitydependent regulation in a weed Bidens sulphurea (Cav.) Sch. Bip. (Asteraceae). J Environ Anal Prog 2:7–10 Deitenbach A, Floriani GS, Dubois JCL, Vivan JL (2008) Manual agroflorestal para a Mata Atlaˆntica. OPUS Editora, Brası´lia Dobson AP, Bradshaw AD, Baker AJM (1997) Hopes for the future: restoration ecology and conservation biology. Science 277(5325):515–522 Estelita-Teixeira ME (1977) Propagac¸a˜o Vegetativa de Oxalis latifoliaKunth (Oxilidaceae). Bol Botaˆnica 5:13–20 Ferrari EA (2010) Agricultura Familiar Camponesa: estrate´gias de reproduc¸a˜o socioeconoˆmica e a contribuic¸a˜o da Agroecologia. Dissertation, Federal University of Vic¸osa Foley JA, DeFries R, Asner GP et al (2005) Global consequences of land use. Science 309(5734):570–574 Garcia R, Couto L (1991) Sistemas silvipastoris: Experieˆncias no estado de Minas Gerais. In: II Encontro Brasileiro de Economia e Planejamento Florestal. Anais… Centro Nacional de Pesquisa de Floresta da Embrapa, Curitiba Gasparino D, Malavasi UC, de Malavasi M, de Souza I (2006) Evaluation of seed bank under different soil uses. Rev ´ rvore 30:1–9 A Grotkopp E, Rejma´nek M (2007) High seedling relative growth rate and specific leaf area are traits of invasive species: phylogenetically independent contrasts of woody angiosperms. Am J Bot 94(4):526–532 Hoffmann WA, Haridasan M (2008) The invasive grass, Melinis minutiflora, inhibits tree regeneration in a Neotropical savanna. Austral Ecol 33:29–36 Jose S (2009) Agroforestry for ecosystem services and environmental benefits: an overview. Agrofor Syst 76(1):1–10 Klein AL, Felippe GM (1991) Efeito da luz na germinac¸a˜o de sementes de ervas invasoras. Pesqui Agropecua´ria Bras 26:955–966 Magurran AE (2004) Measuring biological diversity, 2nd edn. Blackwell Science, Malden Mendes MMS, Lacerda CF, Cavalcante ACR, Fernandes FEP, Oliveira TS (2013) Desenvolvimento do milho sob influeˆncia de a´rvores de pau-branco em sistema agrossilvipastoril. Pesqui Agropecu Bras 48(10):1342–1350 Miguel AE, Carvalho CHS (2005) Efeito do nı´vel de luz sobre o crescimento de seis cultivares de cafe´. In: IV Simpo´sio de Pesquisa dos Cafe´s do Brasil, Londrina. Anais… Embrapa Cafe´, Brası´lia Molina-Montenegro MA, Atala C, Gianoli E (2010) Phenotypic plasticity and performance of Taraxacum officinale (dandelion) in habitats of contrasting environmental heterogeneity. Biol Invasions 12:2277–2284 Montagnini F, Jordan CF (2005) Tropical forest ecology: the basis for management and conservation. Springer, Berlin Moonen AC, Barberi P (2008) Functional biodiversity: an agroecosystem approach. Agric Ecosyst Environ 127(1–2):7–21 Neto RMR, Gama JRV (2005) Biomassa acima do solo de espe´cies herba´ceas e subarbustivas com potencial medicinal em uma vegetac¸a˜o secunda´ria. Cieˆnc Florest 13:19–24
123
Parendes LA, Jones JA (2000) Role of light availability and dispersal in exotic plant invasion along roads and streams in the H. J. Andrews Experimental Forest. Oregon Conserv Biol 14:64–75 Pattison RR, Goldstein G, Ares A (1998) Growth, biomass allocation and photosynthesis of invasive and native Hawaiian rainforest species. Oecologia 17:449–459 Pauchard A, Alaback PB (2004) Influence of elevation, land use, and landscape context on patterns of alien plant invasions along roadsides in protected areas of South-Central Chile. Conserv Biol 18(1):238–248 Peneireiro FM (1999) Os sistemas agroflorestais dirigidos pela sucessa˜o natural: Um estudo de caso. Universidade de Sa˜o Paulo, Piracicaba, Brasil, Dissertac¸a˜o Perrings C, Williamson M, Dalmazzone S (eds) (2000) The economics of biological invasions. Edward Elgar Publishing, Cheltenham Perrings C, Williamson M, Barbier EB et al (2002) Biological invasion risks and the public good: an economic perspective. Conserv Ecol 6(1):1–7 Phalan B, Onial M, Balmford A, Green RE (2011) Reconciling food production and biodiversity conservation: land sharing and land sparing compared. Science 333(6047):1289–1291 Pinto LP (2014) Status e os novos desafios das Unidades de Conservac¸a˜o na Amazoˆnia e Mata Atlaˆntica. In: Lima GS, Almeida MP, Ribeiro GA (orgs.). Manejo e Conservac¸a˜o de A´reas Protegidas. Laborato´rio de Inceˆndios Florestais e de Conservac¸a˜o da Natureza, Vic¸osa Ramos NC, Gastauer M, Cordeiro AAC, Meira-Neto JAA (2015) Environmental filtering of agroforestry systems reduces the risk of biological invasion. Agrofor Syst 89(2):279–289 Rao MR, Nair PKR, Ong CK (1997) Biophysical interactions in tropical agroforestry systems. Agrofor Syst 1(3):3–50 Ribeiro MC, Metzger JP, Martensen AC, Ponzoni FJ, Hirota MM (2009) The brazilian Atlantic Forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biol Conserv 142(6):1141–1153 Rice RA, Greenberg R (2000) Cacao cultivation and the conservation of biological diversity. Ambio 29(3):167–173 Rogers WE, Siemann E (2002) Effects of simulated herbivory and resource availability on native and invasive exotic tree seedlings. Basic Appl Ecol 3:297–307 Santos MG, da Sylvestre LS (2006) Floristics and economics aspects of the pteridophytes of rocky outcrop from Rio de Janeiro State, Brazil. Acta Bot Bras 20:115–124 Schneider AA (2008) A flora naturalizada no estado do Rio Grande do Sul, Brasil: herba´ceas subespontaˆneas. Biocieˆncias 15:257–268 Simberloff D, Holle BV (1999) Positive interactions of nonindigenous species: invasional meltdown? Biol Invasions 1(1):21–32 Soares MP, Saporetti-Junior AW, Meira-Neto JAA, Silva AF, Souza AL (2006) Composic¸a˜o florı´stica do estrato arbo´reo de Floresta Atlaˆntica interiorana em Araponga – Minas ´ rvore 30(5):859–870 Gerais. Rev A Somerfield PJ, Clarke KR, Warwick RM (2008) Simpson Index. In: Jorgensen SE, Fath BD (eds) Encyclopedia of ecology, 1st edn. Elsevier, Oxford, pp 3252–3255
Agroforest Syst SOS Mata Atlaˆntica & INPE (2014) Atlas dos remanescentes florestais da Mata Atlaˆntica. http://mapas.sosma.org.br/. Sa˜o Paulo, Centro de Documentac¸a˜o e Pesquisa da Fundac¸a˜o SOS Mata Atlaˆntica, Brasil
Species List of Brazilian Flora (2016) Botanical Garden of Rio de Janeiro. http://floradobrasil.jbrj.gov.br/. Access 29 Jan 2016 Zenni RD, Ziller SR (2011) An overview of invasive plants in Brazil. Braz J Bot 34:431–446
123
