Abstract:
Cerrado remnants can hold an important diversity of plant species of environmental and ecological relevance. We presented a checklist of vascular plants based on 12 years of inventory carried out in 36 plots (10 m x 2 m; 0.18 ha in total) and during unsystematic walks in a remnant area of cerrado sensu stricto located at Itirapina municipality, state of São Paulo, southeastern Brazil. The list comprised 195 plant species, corresponding to 54 families and 131 genera. The richest families were Fabaceae (25 species), Asteraceae (16), Myrtaceae (16), Rubiaceae (11), Bignoniaceae and Malpighiaceae (10 each), Melastomataceae (9), and Erythroxylaceae, Sapindaceae and Annonaceae (6). Predominant life forms included shrubs and trees, with 68% of the species, followed by lianas with 12%, sub-shrub and herbs with 10% each. Bees were the dominant pollinators (67,5%) and the majority of species had seeds dispersed by animals (56.8%), mostly by birds, followed by wind (33.3%) and self-dispersed (11.2%). More than 60% of the total species were classified as “typical” Cerrado species. Bowdichia virgilioides was the only species classified as Near Threatened (NT) and 157 were regarded as Data Deficient (DD). Our dataset provides floristic, structural, and ecological information for one of the targeted areas for Cerrado survey at São Paulo state, contributing to the understanding of diversity patterns and future conservation and restoration actions in this threatened hotspot.
Keywords:
Brazilian savanna; hotspot; life form; functional traits
Resumo:
Apresentamos uma lista de verificação de plantas vasculares baseada em 12 anos de inventário realizado em 36 parcelas (10 m x 2 m; 0,18 ha no total) e caminhadas assistemáticas em uma área remanescente de cerrado sensu stricto localizada em Itirapina, município do estado de São Paulo, sudeste do Brasil. A lista é composta por 195 espécies de plantas, correspondendo a 54 famílias e 131 gêneros. As famílias mais ricas foram Fabaceae (25 espécies), Asteraceae (16), Myrtaceae (16), Rubiaceae (11), Bignoniaceae e Malpighiaceae (10 cada), Melastomataceae (9) e Erythroxylaceae, Sapindaceae e Annonaceae (6). As formas de vida predominantes incluíram arbustos e árvores (33,7% das espécies), seguidas por lianas (12%), arbustos e ervas (10%). As abelhas foram os polinizadores dominantes (67,5%) e o principal modo de dispersão foi a zoocoria (56,8%), representada principalmente por pássaros, seguida por vento (33.3 %) e auto (11.2 %). Mais de 60% das espécies encontradas foram classificadas como espécies “típicas” de Cerrado. Bowdichia virgilioides foi a única espécie pertencente a uma categoria de ameaça “Quase Ameaçada (NT)”, sendo 157 delas classificadas na categoria “Deficiente de Dados (DD)”. Nosso conjunto de dados fornece informações florísticas, estruturais e ecológicas para uma das áreas-alvo do levantamento do Cerrado no estado de São Paulo, sudeste do Brasil, contribuindo para a compreensão dos padrões de diversidade e futuras ações de conservação neste hotspot ameaçado.
Palavras-chave:
Savana brasileira; hotspot; formas de vida; características funcionais
Introduction
The Cerrado - the Brazilian savanna - is the second most extensive biome in South America. It is the source of many water springs encompassing the main hydrographic basins and the largest reservoirs of freshwater in this continent, the Guarani Aquifer (Pereira et al. 2021PEREIRA, L.C.; BALBINO, L.; MATUS, G.N.; DIAS, H.C.T. & TONELLO, K.C. 2021. Aspects of forest restoration and hydrology: linking passive restoration and soil-water recovery in Brazilian Cerrado. J. For. Res. 31:1-11. DOI:10.1007/s11676-021-01301-3.
https://doi.org/10.1007/s11676-021-01301...
). Cerrado is one of the 25 global hotspots (Myers et al. 2000MYERS, N.; MITTERMEIER, R.A.; MITTERMEIER, C.G; DA FONSECA G.A.B. & KENT, J. 2000. Biodiversity hotspots for conservation priorities. Nature 403:853-858. DOI: 10.1038/35002 501.
https://doi.org/10.1038/35002501...
) for biodiversity conservation (Mittermeier et al. 2005MITTERMEIER, R.A.; GIL, P.R.; HOFFMAN, M.; PILGRIM, J.; BROOKS, T.; MITTERMEIER, C.G.; LAMOREUX, J. & FONSECA, G.A.B. 2005. Hotspots revisited: earth’s biologically richest and most endangered terrestrial ecoregions. Washington, Conservation International.), and the most diverse neotropical savanna (Klink & Machado 2005KLINK, C.A. & MACHADO, R.B. 2005. Conservation of the Brazilian Cerrado. Conserv. Biol. 19: 707-713. DOI: 10.1111/j.1523-1739.2005.00702.x.
https://doi.org/10.1111/j.1523-1739.2005...
), providing diverse and important ecosystem services essential to sustain agricultural systems (Lambers et al. 2020LAMBERS, H.; COSTA, P.B. & OLIVEIRA, R.S. 2020. Towards more sustainable cropping systems: lessons from native Cerrado species. Theor. Exp. Plant Physiol. 32: 175-194. DOI:10.1007/s40626-020-00180-z.
https://doi.org/10.1007/s40626-020-00180...
). Due to the extensive land conversion to agriculture and the high susceptibility to climatic change (Strassburg et al. 2017STRASSBURG, B.B.N.; BROOKS, T.; FELTRAN‐BARBIERI, R.; IRIBARREM, A.; CROUZEILLES, R.; LOYOLA, R.; LATAWIEC, A.E.; OLIVEIRA-FILHO, F.J.B.; SCARAMUZZA, C.A.M.; SCARANO, F.R.; SOARES-FILHO, B. & BALMFORD, A. 2017. Moment of truth for the Cerrado hotspot. Nat. Ecol. Evol. 1: 0099. DOI:10.1038/s41559-017-0099.
https://doi.org/10.1038/s41559-017-0099...
), the Cerrado is also the most severely threatened biome in Brazil (Lopes et al. 2021LOPES, G.R.; LIMA, M.G.B. & DOS REIS, T.N.P (2021) Maldevelopment revisited: Inclusiveness and social impacts of soy expansion over Brazil’s Cerrado in Matopiba. World Dev. 139:105316. DOI:10.1016/j.worlddev.2020.105316.
https://doi.org/10.1016/j.worlddev.2020....
).
The Cerrado is a heterogeneous ecosystem regarding biodiversity and phytophysionomy: ranging from grassland with small and sparse shrubs, savanna with predominant woody vegetation (trees of approximately 6-7 m height) and discontinuous tree cover, to forest formation with a canopy height of 12-15 m (Coutinho 2006COUTINHO, L.M. 2006. O conceito de bioma. Acta Bot. Bras. 20: 13-2. DOI:10.1590/S0102-33062006000100002.
https://doi.org/10.1590/S0102-3306200600...
, Sano et al. 2008SANO, E.E.; ROSA, R.; BRITO, J.L.S. & FERREIRA, L.G. 2008. Mapeamento semidetalhado do uso da terra do Bioma Cerrado. Pesqui. Agropecu. Bras. 43: 53-156. DOI: 10.1590/S0100-204X2008000100020.
https://doi.org/10.1590/S0100-204X200800...
). This heterogeneity is indicated by a high endemism rate (44%), representing about 12% of all Brazilian species (Klink & Machado 2005KLINK, C.A. & MACHADO, R.B. 2005. Conservation of the Brazilian Cerrado. Conserv. Biol. 19: 707-713. DOI: 10.1111/j.1523-1739.2005.00702.x.
https://doi.org/10.1111/j.1523-1739.2005...
). The cerrado sensu stricto is considered one of the most common phytophysiognomies, occurring in approximately 70% of all territorial extensions of its domain (Eiten 1972EITEN, G. 1972. The Cerrado vegetation of Brazil. Bot Rev. 38: 201-341. DOI:10.1007/BF02859158.
https://doi.org/10.1007/BF02859158...
).
From 1990 to 2010, the net loss rate of Cerrado natural vegetation was around 117.870 km2 (Beuchle et al. 2015BEUCHLE, R.; GRECCHI, R.C.; SHIMABUKURO, Y.E.; SELIGER, R., EVA, H.D.; SANO, E. & ACHARD, F. 2015. Land cover changes in the Brazilian Cerrado and Caatinga biomes from 1990 to 2010 based on a systematic remote sensing sampling approach. Appl. Geogr. 58:116-127. DOI:10.1016/j.apgeog.2015.01.017.
https://doi.org/10.1016/j.apgeog.2015.01...
). However, more recent data from the Brazilian Annual Land Use and Land Cover Mapping Project (MapBiomas, Collection 5.0; https://mapbiomas.org) showed that the accumulated losses, ranging from 1985 to 2019, is in reality, 408,6 thousand hectare.
It is estimated that the Cerrado ecosystem may disappear by 2050 (Strassburg et al. 2017STRASSBURG, B.B.N.; BROOKS, T.; FELTRAN‐BARBIERI, R.; IRIBARREM, A.; CROUZEILLES, R.; LOYOLA, R.; LATAWIEC, A.E.; OLIVEIRA-FILHO, F.J.B.; SCARAMUZZA, C.A.M.; SCARANO, F.R.; SOARES-FILHO, B. & BALMFORD, A. 2017. Moment of truth for the Cerrado hotspot. Nat. Ecol. Evol. 1: 0099. DOI:10.1038/s41559-017-0099.
https://doi.org/10.1038/s41559-017-0099...
) if extensive farming expansion, including agriculture and cattle ranching, is not contained and if conservation and preservation programs of biodiversity are not adopted (Strassburg et al. 2017STRASSBURG, B.B.N.; BROOKS, T.; FELTRAN‐BARBIERI, R.; IRIBARREM, A.; CROUZEILLES, R.; LOYOLA, R.; LATAWIEC, A.E.; OLIVEIRA-FILHO, F.J.B.; SCARAMUZZA, C.A.M.; SCARANO, F.R.; SOARES-FILHO, B. & BALMFORD, A. 2017. Moment of truth for the Cerrado hotspot. Nat. Ecol. Evol. 1: 0099. DOI:10.1038/s41559-017-0099.
https://doi.org/10.1038/s41559-017-0099...
). In addition, a recent study concluded that both the hydrology and ecology of the Cerrado will be strongly affected considering climate change in the near future (Rodrigues et al. 2020RODRIGUES, S.J.A.; VIOLA, M.R.; ALVARENGA, L.A.; MELLO, C.R.; CHOU, S.C.; OLIVEIRA, V.A.; UDDAMERI, V. & MORAIS, M.A. 2020. Climate change impacts under representative concentration pathway scenarios on streamflow and droughts of basins in the Brazilian Cerrado biome. Int. J. Climatol. 40, 2511-2526.DOI:10.1002/joc.6347.
https://doi.org/10.1002/joc.6347...
).
The state of São Paulo presents the lowest area of Cerrado remnant cover indices, around 13% of the original distribution (Sano et al. 2010SANO, E.E.; ROSA, R.; BRITO, J.L.S. & FERREIRA, L.G. 2010. Land cover mapping of the tropical savanna region in Brazil, Environ. Monit. Assess. 166:113-124. DOI: 0.1007/s10661-009-0988-4
https://doi.org/0.1007/s10661-009-0988-4...
). Public and multi-stakeholder conservation programs can change this imminent extinction scenario, cooperating with national and international biodiversity safeguarding goals in the Cerrado (Strassburger et al. 2016STRASSBURG, B.; LATAWIEC, A. & BALMFORD, A. 2016. Urgent action on Cerrado extinctions. Nature 540: 199. DOI:10.1038/540199a3
https://doi.org/10.1038/540199a3...
, 2017). The first step to improving conservation and restoration actions is conducting plant inventories to assess species diversity and differences in the community composition and structure among areas through time and biogeographic patterns (Lima et al. 2020LIMA, N.E.; GUIMARÃES, R.A.; ALMEIDA-JÚNIOR, E.B.; VITORINO, L.C. & COLLEVATTI, G.G. 2020. Temporal trends, impact and partnership in floristic and phytosociology literature in the Brazilian Cerrado. Flora 273: 151721. DOI: 10.1016/j.flora.2020.151721.
https://doi.org/10.1016/j.flora.2020.151...
). After that, acquiring functional traits, for example, running qualitative or quantitative studies of pollination and seed dispersal syndromes associated with vegetation stratification is essential to preserve Cerrado’s dynamics (Gottsberger & Silberbauer-Gottsberger 2018GOTTSBERGER, G. & SILBERBAUER-GOTTSBERGER, I. 2018. How are pollination and seed dispersal modes in Cerrado related to stratification? Trends in a Cerrado sensu stricto woodland in southeastern Brazil, and a comparison with Neotropical forests. Acta Bot. Bras. 32: 434-445. DOI: 10.1590/0102-33062018abb0186.
https://doi.org/10.1590/0102-33062018abb...
) and guide future restoration actions (Buisson et al. 2020).
The remnant Cerrado studied was fragmented nearly 30 years ago. The total density is 15,522 individuals per hectare - with the largest diameter and maximum registered being 34.7 cm and 12 m, respectively. Myrtaceae, Fabaceae and Malpighiaceae as the richest families and Bauhinia rufa (Bong.) Steudel, Xylopia aromatica (Lam.) Mart., Miconia rubiginosa (Bonpl.) A.DC, Virola sebifera Aubl. and Myrcia guianensis (Aubl.) DC. are the species with highest abundance (Reys et al. 2013REYS P.; CAMARGO, M.G.G.; GROMBONE-GUARATINI, M.T.; TEIXEIRA, A.P.; ASSIS, M.A. & MORELLATO, L.P.C. 2013. Estrutura e composição florística de um Cerrado sensu stricto e sua importância para propostas de restauração ecológica. Hoehnea 40: 449-464. DOI:10.1590/S2236-8906201300030000.
https://doi.org/10.1590/S2236-8906201300...
). In the cerrado sensu stricto studied, the edge effect and cardinal orientation intensifies the reproductive phenophases and synchronizes individuals of Xylopia aromatica and Myrcia guianensis (Camargo et al. 2011CAMARGO, M.G.G.; SOUZA, R.M.; REYS, P. & MORELLATO, L.P.C. 2011. Effects of environmental conditions associated to the cardinal orientation on the reproductive phenology of the Cerrado savanna tree Xylopia aromatica (Annonaceae). An. Acad. Bras. Ciênc. 83: 1007-1019. DOI: 10.1590/S0001-37652011005000014.
https://doi.org/10.1590/S0001-3765201100...
, Vogado et al. 2016VOGADO, N.O.; CAMARGO, M.C.G.; LOCOSSELLI, GM. & MORELLATO, LPC. 2016. Edge Effects on the Phenology of the Guamirim, Myrcia Guianensis (Myrtaceae), a Cerrado Tree, Brazil. Trop. Conserv. Sci. 9:291-312. DOI: 10.1177/194008291600900115
https://doi.org/10.1177/1940082916009001...
). Also, the edges influence the structure of the liana community, increasing the species richness, abundance, and host occupancy (Melis et al. 2021MELIS, J.; CAMARGO, M.G.G.; CARVALHO, P.G.; MORELLATO, L.P.C. & GROMBONE-GUARATINI, M.T. 2021. Edge influence on liana community in a cerrado savanna. Austral Ecol. 46: 192-203. DOI:10.1111/aec.12968.
https://doi.org/10.1111/aec.12968...
). Climate seasonality directly affects leaf fall and flush, flowering, fruiting and germinative strategies (Camargo et al. 2013CAMARGO, M.G.G., CAZETTA, E., SCHAEFER, M., MORELLATO, L.P.C. 2013. Fruit color and contrast in seasonal habitats - a case study from a cerrado savanna. Oikos 122:1335-1342. DOI: 10.1111/j.1600-0706.2013.00328.x
https://doi.org/10.1111/j.1600-0706.2013...
, 2018CAMARGO, MGG, CARVALHO, G.A.; ALBERTON, B.; MORELLATO, L.P.C. 2018. Leafing patterns and leaf exchange strategies of a cerrado woody community. Biotropica 50: 442-454. DOI: 10.1111/btp.12552
https://doi.org/10.1111/btp.12552...
, Escobar et al. 2018ESCOBAR, D.F.; SILVEIRA, F.A.O. & MORELLATO, L.P.C. 2018. Timing of seed dispersal and seed dormancy in Brazilian savanna: two solutions to seasonality. Ann. Bot. 121: 1197-1209. DOI: 10.1093/aob/mcy006.
https://doi.org/10.1093/aob/mcy006...
, 2021ESCOBAR, D F.; SILVEIRA, F.A.O. & MORELLATO, L.P.C. 2021 Do regeneration traits vary according to vegetation structure? A case study for savannas. J. Veg. Sci 32: e12940. DOI: 10.1111/jvs.12940.
https://doi.org/10.1111/jvs.12940...
, Martins et al. 2021MARTINS, A.E.; CAMARGO, M.G.G. & MORELLATO, L.P.C. 2021. Flowering Phenology and the Influence of Seasonality in Flower Conspicuousness for Bees. Front. Plant Sci. 11: 1-11. DOI: 10.3389/fpls.2020.594538.
https://doi.org/10.3389/fpls.2020.594538...
), certainly shaping the floristic diversity found in the area. Although several ecological aspects of the cerrado study area have been investigated, an accurate list of the flowering plants, however, has not yet been published.
Here, we presented a checklist of vascular plants, and associated pollination and seed-dispersal systems, based on 12 years of inventory carried in a cerrado sensu stricto remnant on Southeastern Brazil, described as a priority area for survey and conservation in the state of São Paulo by Metzger & Rodrigues (2008)METZGER, J.P. & RODRIGUES, R.R. 2008. Mapas síntese de diretrizes para a conservação e restauração da biodiversidade no Estado de São Paulo. In: Diretrizes para conservação e restauração da biodiversidade no Estado de São Paulo. R.R., Rodrigues; C.A. Joly, M.W. Brito; A Paese; J.P. Metzger; L. Casatti; M.A. Nalon; N. Menezes; N.M. Ivanauska; V. Bolzani & V.L.R..Bononi. Governo do Estado de São Paulo, São Paulo, p. 130-136.. This study aims to provide a starting point to implement public policies to management, land use, conservation, restoration and future ecological studies.
Material and Methods
1. Study site
The study area is a remnant of Cerrado located in a private land at Itirapina municipality, state of São Paulo (22°10’31.41” S; 47°52’26.3” W), southeastern Brazil (Figure 1a). The average altitude of the area is 760 meters above sea level. The Cerrado is described as a savanna biome composed by different vegetation physiognomies, including the woody savanna, widespread in the neotropical region (Coutinho 2006COUTINHO, L.M. 2006. O conceito de bioma. Acta Bot. Bras. 20: 13-2. DOI:10.1590/S0102-33062006000100002.
https://doi.org/10.1590/S0102-3306200600...
). The cerrado sensu stricto is a typical dominant woody vegetation of the Cerrado (Coutinho 2006COUTINHO, L.M. 2006. O conceito de bioma. Acta Bot. Bras. 20: 13-2. DOI:10.1590/S0102-33062006000100002.
https://doi.org/10.1590/S0102-3306200600...
) and at the study area (Reys et al. 2013REYS P.; CAMARGO, M.G.G.; GROMBONE-GUARATINI, M.T.; TEIXEIRA, A.P.; ASSIS, M.A. & MORELLATO, L.P.C. 2013. Estrutura e composição florística de um Cerrado sensu stricto e sua importância para propostas de restauração ecológica. Hoehnea 40: 449-464. DOI:10.1590/S2236-8906201300030000.
https://doi.org/10.1590/S2236-8906201300...
). The study area is a rectangular fragment that has been anthropized for nearly 30 years, with sides facing the four cardinal points: west: a highway; east: a remnant of Cerrado and a pasture; south and north: sugarcane crops (Figure 1b).
Map and vegetation of the study site. (A) Geographical location of the Itirapina municipality, belonging to the Cerrado Eco Region (Olson et al. 2001), São Paulo State, Southeastern Brazil; (B) Satellite image of the cerrado sensu stricto fragment studied with a scheme of the sampled plots (red dots: sample plots according to Reys et al. (2013)REYS P.; CAMARGO, M.G.G.; GROMBONE-GUARATINI, M.T.; TEIXEIRA, A.P.; ASSIS, M.A. & MORELLATO, L.P.C. 2013. Estrutura e composição florística de um Cerrado sensu stricto e sua importância para propostas de restauração ecológica. Hoehnea 40: 449-464. DOI:10.1590/S2236-8906201300030000.
https://doi.org/10.1590/S2236-8906201300... ; green dots: sample plots of this study), Fazenda São José da Conquista; (C) Photograph showing the vegetation interior; (D) Photograph taken from the top of a phenological tower, showing the cerrado sensu stricto fragment from above. Red diamond represents the Itirapina municipality on the São Paulo State map. (Photographs by G. M. Marcusso and B. Alberton, respectively).
The cerrado vegetation surveyed presents a discontinuous tree cover around 6-7 meters high (emergent trees reaching up to 12 meters) and discontinuous herbaceous layer with grasses and some herbs, bromeliads, and palms (Camargo et al. 2011CAMARGO, M.G.G.; SOUZA, R.M.; REYS, P. & MORELLATO, L.P.C. 2011. Effects of environmental conditions associated to the cardinal orientation on the reproductive phenology of the Cerrado savanna tree Xylopia aromatica (Annonaceae). An. Acad. Bras. Ciênc. 83: 1007-1019. DOI: 10.1590/S0001-37652011005000014.
https://doi.org/10.1590/S0001-3765201100...
, Reys et al. 2013REYS P.; CAMARGO, M.G.G.; GROMBONE-GUARATINI, M.T.; TEIXEIRA, A.P.; ASSIS, M.A. & MORELLATO, L.P.C. 2013. Estrutura e composição florística de um Cerrado sensu stricto e sua importância para propostas de restauração ecológica. Hoehnea 40: 449-464. DOI:10.1590/S2236-8906201300030000.
https://doi.org/10.1590/S2236-8906201300...
) (Figure1c-d). The average canopy openness varies from 24% (edges) to 15% (interior) (Reys et al. 2013REYS P.; CAMARGO, M.G.G.; GROMBONE-GUARATINI, M.T.; TEIXEIRA, A.P.; ASSIS, M.A. & MORELLATO, L.P.C. 2013. Estrutura e composição florística de um Cerrado sensu stricto e sua importância para propostas de restauração ecológica. Hoehnea 40: 449-464. DOI:10.1590/S2236-8906201300030000.
https://doi.org/10.1590/S2236-8906201300...
). The climate of the cerrado study area is seasonal, with a dry cold season from April to September and a rainy warm season from October to March (Camargo et al. 2018CAMARGO, MGG, CARVALHO, G.A.; ALBERTON, B.; MORELLATO, L.P.C. 2018. Leafing patterns and leaf exchange strategies of a cerrado woody community. Biotropica 50: 442-454. DOI: 10.1111/btp.12552
https://doi.org/10.1111/btp.12552...
, Escobar et al. 2018ESCOBAR, D.F.; SILVEIRA, F.A.O. & MORELLATO, L.P.C. 2018. Timing of seed dispersal and seed dormancy in Brazilian savanna: two solutions to seasonality. Ann. Bot. 121: 1197-1209. DOI: 10.1093/aob/mcy006.
https://doi.org/10.1093/aob/mcy006...
). The mean annual temperature is 20 °C, with a maximum of 32 °C (February) and a minimum of 18 °C (July). The mean total annual rainfall is 1524 mm (Camargo et al. 2018CAMARGO, MGG, CARVALHO, G.A.; ALBERTON, B.; MORELLATO, L.P.C. 2018. Leafing patterns and leaf exchange strategies of a cerrado woody community. Biotropica 50: 442-454. DOI: 10.1111/btp.12552
https://doi.org/10.1111/btp.12552...
, Escobar et al. 2018ESCOBAR, D.F.; SILVEIRA, F.A.O. & MORELLATO, L.P.C. 2018. Timing of seed dispersal and seed dormancy in Brazilian savanna: two solutions to seasonality. Ann. Bot. 121: 1197-1209. DOI: 10.1093/aob/mcy006.
https://doi.org/10.1093/aob/mcy006...
). Soil is classified as Latosol-Argisol according to the Brazilian Soil Classification System (EMBRAPA 1999EMBRAPA - EMPRESA BRASILEIRA DE PESQUISA AGROPECUÁRIA. 1999. Sistema brasileiro de classificação de solos. Brasília, Embrapa Produção de Informação. Rio de Janeiro: Embrapa Solos., Reys et al. 2013REYS P.; CAMARGO, M.G.G.; GROMBONE-GUARATINI, M.T.; TEIXEIRA, A.P.; ASSIS, M.A. & MORELLATO, L.P.C. 2013. Estrutura e composição florística de um Cerrado sensu stricto e sua importância para propostas de restauração ecológica. Hoehnea 40: 449-464. DOI:10.1590/S2236-8906201300030000.
https://doi.org/10.1590/S2236-8906201300...
).
2. Data collection
First, we established 36 plots of 25 m x 2 m at least 50 meters apart and equally distributed throughout the south and east sides of the fragment: east edge (10 plots), south edge (10 plots), east interior (8 plots), and south interior (8 plots), as described by Reys et al. (2013)REYS P.; CAMARGO, M.G.G.; GROMBONE-GUARATINI, M.T.; TEIXEIRA, A.P.; ASSIS, M.A. & MORELLATO, L.P.C. 2013. Estrutura e composição florística de um Cerrado sensu stricto e sua importância para propostas de restauração ecológica. Hoehnea 40: 449-464. DOI:10.1590/S2236-8906201300030000.
https://doi.org/10.1590/S2236-8906201300...
(Figure 1b). The plots were arranged in two parallel lines on both sides, with one line on the edge - defined as the area of contact with the matrix - and another line 100 meters from the edge. Within the 36 plots we marked, sampled and identified all trees and scrubs with a diameter ≥ 3 cm at 30 cm from their ground base (Reys et al. 2013REYS P.; CAMARGO, M.G.G.; GROMBONE-GUARATINI, M.T.; TEIXEIRA, A.P.; ASSIS, M.A. & MORELLATO, L.P.C. 2013. Estrutura e composição florística de um Cerrado sensu stricto e sua importância para propostas de restauração ecológica. Hoehnea 40: 449-464. DOI:10.1590/S2236-8906201300030000.
https://doi.org/10.1590/S2236-8906201300...
). Later, in 2015, we added 10 more plots (2 m x 50 m, 20 m apart) in the same study area, adopting the rapid sampling method (Gentry´s 0.1-ha transects) created and used by Gentry (1982)GENTRY, A.H. 1982. Patterns of neotropical plant species diversity. Evolutionary Biology 15: 1-84., including all woody individuals with diameter at breast height ≥ 2,5 cm (Figure 1b).
Next, we collected floriferous branches and reproductive structures of tree, shrub, herb, and climber species during unsystematic walks, aiming to fully cover all Cerrado areas through monthly field trips from 2004 to 2018. We identified taxa according to specialized literature and taxonomic experts, compared them with herbarium collections and deposited fertile voucher specimens in the Herbarium Rioclarense (HRCB). We verified the species and family names using Flora do Brasil (2020)FLORA BRASIL 2020 Jardim Botânico do Rio de Janeiro. Available at: < http://floradobrasil.jbrj.gov.br/ >. Accessed on: 14 Apr. 2021.
http://floradobrasil.jbrj.gov.br/...
. The results are presented under APG (2009)APG ‒ Angiosperm Phylogeny Group (2009) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot. J. Linn. Soc. 161: 105-121. and APG IV (2016)APG ‒ The Angiosperm Phylogeny Group (2016) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Bot. J. Linn. Soc. 181: 1-20.. Finally, we divided species into four groups according to life form (trees, shrubs, sub-shrub and herbs, and climbers) and dispersal system (Escobar et al. 2018ESCOBAR, D.F.; SILVEIRA, F.A.O. & MORELLATO, L.P.C. 2018. Timing of seed dispersal and seed dormancy in Brazilian savanna: two solutions to seasonality. Ann. Bot. 121: 1197-1209. DOI: 10.1093/aob/mcy006.
https://doi.org/10.1093/aob/mcy006...
, Van der Pijl 1982van der PIJL, L. 1982. Ecological Dispersal Classes, Established on the Basis of the Dispersing Agents. In: Principles of Dispersal in Higher Plants. Springer, Berlin, Heidelberg. DOI:10.1007/978-3-642-87925-8_5.
https://doi.org/10.1007/978-3-642-87925-...
). We classified all species as “typical” Cerrado species or belonging to other physiognomies in accordance with Durigan et al. (2004DURIGAN, G.; BAITELLO, J. B.; FRANCO, G. A.C. & SIQUEIRA, M. F. 2004.Plantas do Cerrado Paulista: imagens de uma paisagem ameaçada. Páginas e letras Editora & Gráfica, São Paulo., 2012DURIGAN, G.; RAMOS, V.S.; IVANAUSKAS, N.M. & FRANCO, G.A.C. 2012. Espécies de fitofisionomias na transição CERRADO-MATA ATLÂNTICA no estado de São Paulo. Secretaria do Meio Ambiente do Estado de São Paulo.). We checked the degree of threaten plants in the International Union for Conservation of Nature (IUCN) Red List of Threatened Species and in the Official Red List of Endangered Species of the Brazilian Flora (Flora do Brasil 2020FLORA BRASIL 2020 Jardim Botânico do Rio de Janeiro. Available at: < http://floradobrasil.jbrj.gov.br/ >. Accessed on: 14 Apr. 2021.
http://floradobrasil.jbrj.gov.br/...
) and classified in (EW - Extinct in the Wild, CR - Critically Endangered, EN - Endangered, VU - Vulnerable, NT - Near Threatened, DD - Data Deficient, LC - Least Concern).
We characterized diaspores of the surveyed species and fit them into the dispersion syndromes as self-, wind- and animal-dispersed diaspores according to Escobar et al. (2018ESCOBAR, D.F.; SILVEIRA, F.A.O. & MORELLATO, L.P.C. 2018. Timing of seed dispersal and seed dormancy in Brazilian savanna: two solutions to seasonality. Ann. Bot. 121: 1197-1209. DOI: 10.1093/aob/mcy006.
https://doi.org/10.1093/aob/mcy006...
, 2021) and Van der Pijl (1982)van der PIJL, L. 1982. Ecological Dispersal Classes, Established on the Basis of the Dispersing Agents. In: Principles of Dispersal in Higher Plants. Springer, Berlin, Heidelberg. DOI:10.1007/978-3-642-87925-8_5.
https://doi.org/10.1007/978-3-642-87925-...
. The inference of pollinators was made based on an extensive bibliographic survey, searching by the pollinators of Cerrado species from our study site performed by Martins (2019)MARTINS, A.E. 2019. Flower Color Patterns and Pollination in Seasonal Vegetations. Dissertação de Mestrado, São Paulo State University, Rio Claro, SP. and Martins et al. (2021)MARTINS, A.E.; CAMARGO, M.G.G. & MORELLATO, L.P.C. 2021. Flowering Phenology and the Influence of Seasonality in Flower Conspicuousness for Bees. Front. Plant Sci. 11: 1-11. DOI: 10.3389/fpls.2020.594538.
https://doi.org/10.3389/fpls.2020.594538...
.
Results
The list of plants included a total of 195 species belonging to 54 families and 131 genera (99 monospecific). We could not identify to the species level nine plant morphotypes. The richest families were Fabaceae (25 species), Asteraceae (16), Myrtaceae (16), Rubiaceae (11), Bignoniaceae and Malpighiaceae (10), Melastomataceae (9), Erythroxylaceae, Sapindaceae and Annonaceae (6), corresponding to 58% of the total surveyed species. Moreover, 27 of the 54 families surveyed had only one species (50%), and 12 families (22%) had only two species (Table 1). Considering only taxa identified to the genus level, there was also a predominance of arboreal and shrub life forms (34%, 64 spp each), followed by lianas (12%, 23 spp), sub-shrub (10%, 20 spp), and herbs (10%, 19 spp) (Figures 2 and 3). Within our Cerrado remnant, there were 27 species considered as Least Concern (LC), one as Near Threatened (NT) - Bowdichia virgilioides Kunth -, and 157 as Data Deficient (DD) (Table 1). Besides that, the typical Cerrado species according to Durigan et al. (2004DURIGAN, G.; BAITELLO, J. B.; FRANCO, G. A.C. & SIQUEIRA, M. F. 2004.Plantas do Cerrado Paulista: imagens de uma paisagem ameaçada. Páginas e letras Editora & Gráfica, São Paulo., 2012DURIGAN, G.; RAMOS, V.S.; IVANAUSKAS, N.M. & FRANCO, G.A.C. 2012. Espécies de fitofisionomias na transição CERRADO-MATA ATLÂNTICA no estado de São Paulo. Secretaria do Meio Ambiente do Estado de São Paulo.) found in our study area are 62.7% of the species (123) surveyed at the remnant.
List of plant species recorded in the cerrado sensu stricto, Itirapina, São Paulo State, Southeastern Brazil, and their respective voucher number, life form, dispersion syndrome, pollinator system, typical Cerrado species according to Durigan et al. (2004DURIGAN, G.; BAITELLO, J. B.; FRANCO, G. A.C. & SIQUEIRA, M. F. 2004.Plantas do Cerrado Paulista: imagens de uma paisagem ameaçada. Páginas e letras Editora & Gráfica, São Paulo., 2012DURIGAN, G.; RAMOS, V.S.; IVANAUSKAS, N.M. & FRANCO, G.A.C. 2012. Espécies de fitofisionomias na transição CERRADO-MATA ATLÂNTICA no estado de São Paulo. Secretaria do Meio Ambiente do Estado de São Paulo.) and threat status according to the International Union for Conservation of Nature (IUCN) Red List of Threatened Species and in the Official Red List of Endangered Species of the Brazilian Flora (Flora do Brasil, 2020FLORA BRASIL 2020 Jardim Botânico do Rio de Janeiro. Available at: < http://floradobrasil.jbrj.gov.br/ >. Accessed on: 14 Apr. 2021.
http://floradobrasil.jbrj.gov.br/... ) and classified in (EW - Extinct in the Wild, CR - Critically Endangered, EN - Endangered, VU - Vulnerable, NT - Near Threatened, DD - Data Deficient, LC - Least Concern and typical cerrado species. Dispersal syndromes: Self= self-dispersed, Wind = wind-dispersed, Animal= Animal-dispersed; Pollination: butt = butterfly; dvi = diverse insects; hum = hummingbird, sph = sphingidae; ND = not determined, Y = yes, N= no. *most frequent species of the southern cerrado based on the woody flora list provided by Bridgewater et al. (2004)BRIDGEWATER, S.; RATTER, J.A. & FELIPE RIBEIRO, J. 2004. Biogeographic patterns, β-diversity and dominance in the Cerrado biome of Brazil. Biodivers. Conserv. 13: 2295-231.7 DOI: 10.1023/B:BIOC.0000047903.37608.4c.
https://doi.org/10.1023/B:BIOC.000004790... . ** pollinator based on plant genera.
Number of plant species by life form surveyed in the cerrado sensu stricto, Itirapina, São Paulo State, Southeastern Brazil. Number of species = 195.
Diversity of plant species and life-forms in the cerrado sensu stricto, Itirapina, São Paulo State, Southeastern Brazil. Liana: (A) Temnadenia violacea (Vell.) Miers - hummingbird pollination, (B) Amphilophium elongatum (Vahl) L.G.Lohmann - bee pollination and (C) Serjania lethalis A.St.-Hil. - bee pollination; Trees: (D) Copaifera langsdorffii Desf. - bee pollination, (E) Pouteria torta (Mart.) Radlk. - diverse insects’ pollination, (F) Ouratea spectabilis (Mart.) Engl. - bee pollination and (G) Anadenanthera peregrina (L.) Speg.- bee pollination; Sub-shrub: (H) Senna rugosa (G.Don) H.S.Irwin & Barneby - bee pollination, (I) Palicourea rigida Kunth - hummingbird pollination and (J) Banisteriopsis campestris (A. Juss.) Little - bee pollination; Shrub: (K) Talisia angustifolia Radlk. - diverse insects’ pollination, (L) Byrsonima intermedia A. Juss. - bee pollination and (M) Casearia sylvestris Sw. - fly pollination; Herb: (N) Mimosa gracilis Benth. - bee pollination., (O) Commelina erecta L. - bee pollination and (P) Gomphrena macrocephala A.St.-Hil. - bee pollination. (Photos MGG Camargo).
Bee pollination were the dominant system, corresponding to 133 plant species (68.2%), followed by diverse insects (6.2%, 12 spp), butterflies (3.1%, 6 spp), flies (3.6%, 7 spp), beetles (3.1%, 6 spp), moths (3.6%, 7 spp), wind (1.5%, 3 spp), wasps (2.6%, 5 spp), hummingbirds (1.5%, 3 spp), sphingid moths (2.1%, 4 spp) and bats (1%, 2 spp) (Figures 4 and 5).
Number of species by pollination system recorded in the cerrado sensu stricto, Itirapina, São Paulo State, Southeastern Brazil. Pollination systems: bee, diverse insects (dvi), fly, moth, beetle, butterfly, wasp, sphingidae (sph), hummingbird (hum), wind and bat
Examples of species by seed dispersal syndromes collected in the cerrado sensu stricto, Itirapina, São Paulo State, Southeastern Brazil. Wind-dispersed: (A) Piptocarpha rotundifolia (Less.) Baker, (B) Banisteriopsis stellaris (Griseb.) B. Gates, (C) Eriotheca gracilipes (K.Schum.) A. Robyns; Self-dispersed: (D) Bauhinia rufa (Bong.) Steud., (E) Anadenanthera peregrina var. falcata (Benth.) Altschul - with unripe fruit and a detail of the ripe fruits, (F) Lippia origanoides Kunth - with unripe fruit and a detail of the ripe fruits; Animal-dispersed: (G) Myrcia guianensis (Aubl.) DC., (H) Miconia rubiginosa (Bonpl.) DC., (I) Erythroxylum pelleterianum A.St.-Hil. (Photos MGG de Camargo).
As for the dispersal systems, the animal-dispersed diaspores predominated (55.4%, 108 spp), followed by wind (33.3%, 65 spp) and self-dispersion (11.2%, 22 spp). Animal seed dispersal was predominant in trees and shrubs (Figure 6) and presented birds as the main dispersion agents (LPC Morellato and collab. Unpublished information).
Number of plant species by seed dispersal syndromes according to the life forms collected in the cerrado sensu stricto, Itirapina, São Paulo State, Southeastern Brazil
Discussion
We found a species richness (195) similar to other studied remnants of cerrado sensu stricto in São Paulo state, which used comparable sampling effort and inclusion criteria. For instance, 254 species were listed in Assis, São Paulo, by Durigan et al. (1999)DURIGAN, G.; BACIC, M.C.; FRANCO, G.A.D.C. & SIQUEIRA, M.F. 1999. Inventário florístico do Cerrado na Estação Ecológica de Assis, SP. Hoehnea. 26 49-172., 141 in Santa Rita do Passa Quatro by Waiser & Godoy (2001), and 177 species in Botucatu by Ishara et al. (2008)ISHARA, K.L.; DÉSTRO, G.F.G.; RODELLA, R.C.S.M. & YANAGIZAWA, Y.A.N.P. 2008. Composição florística de remanescente de cerrado sensu stricto em Botucatu, SP. Rev. bras. bot. 31:575-586. DOI: 10.1590/S0100-84042008000400004.
https://doi.org/10.1590/S0100-8404200800...
. However, the taxonomy used in those papers did not follow the APG III classification (2009)APG ‒ Angiosperm Phylogeny Group (2009) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot. J. Linn. Soc. 161: 105-121., limiting a comprehensive floristic comparison. The proportion of species distribution by family found in our cerrado checklist was very similar to the pattern found in previous studies carried out in Brazilian Cerrado areas (Ratter et al. 2003RATTER, J.; BRIDGEWATER, S. & RIBEIRO, J. 2003. Analysis of the floristic composition of the brazilian Cerrado vegetation iii: comparison of the woody vegetation of 376 areas. Edinb. J. Bot. 60: 57-109. doi:10.1017/S0960428603000064.
https://doi.org/10.1017/S096042860300006...
, Gottsberger & Silberbauer-Gottsberger 2006GOTTSBERGER, G. & SILBERBAUER-GOTTSBERGER, I. 2006. Life in the Cerrado: A South American Tropical Seasonal Ecosystem. Vol. II. Pollination and Seed Dispersal., Mantovani & Martins 1993MANTOVANI, W. & MARTINS, F.R. 1993. Florística do cerrado da Reserva Biológica de Moji Guaçu, SP. Acta Bot. Bras. 20: 33-60. DOI: 10.1590/S0102-33061993000100003.
https://doi.org/10.1590/S0102-3306199300...
, Felfili et al. 2002FELFILI, J.M.; SILVA, P.E.N.D.; SILVA JÚNIOR, M.C.D.; MARIMON, B.S. & DELITTI, W.B.C. 2002. Composição florística e fitossociologia do cerrado sentido restrito no município de Água Boa-MT. Acta Bot. Bras. 16: 103-112. DOI: 10.1590/S0102-33062002000100012.
https://doi.org/10.1590/S0102-3306200200...
, Batalha & Martins 2001, Weiser & Godoy 2001WEISER, V.L. & GODOY, S.A.P. 2001. Florística em um hectare de cerrado sensu stricto ARIE - Cerrado Pé de Gigante, Santa Rita do Passa Quatro, SP. Acta Bot. Bras. 15: 201-212 DOI: 10.1590/S0102-33062001000200007
https://doi.org/10.1590/S0102-3306200100...
, Durigan et al. 2001DURIGAN, G.; NISHIKAWA, D.L.L.; ROCHA, E.; SILVEIRA, É.R.; PULITANO, F.M.; REGALADO, L.B.; CARVALHAES, M.A.; PARANAGUÁ, P.A. & RANIERI, V.E.L. 2001. Caracterização de dois estratos da vegetação em uma área de cerrado no município de Brotas, SP, Brasil. Acta Bot. Bras. 16: 251-262. DOI: 10.1590/S0102-33062002000300002.
https://doi.org/10.1590/S0102-3306200200...
, Fidelis & Godoy 2003FIDELIS, A.T. & GODOY, S.A.P. 2003. Estrutura de um cerrado stricto sensu na Gleba Cerrado Pé de Gigante, Santa Rita do Passa Quatro, SP. Acta Bot. Bras. 17: 531-539. DOI: 10.1590/S0102-33062003000400006.
https://doi.org/10.1590/S0102-3306200300...
, Ishara et al. 2008ISHARA, K.L.; DÉSTRO, G.F.G.; RODELLA, R.C.S.M. & YANAGIZAWA, Y.A.N.P. 2008. Composição florística de remanescente de cerrado sensu stricto em Botucatu, SP. Rev. bras. bot. 31:575-586. DOI: 10.1590/S0100-84042008000400004.
https://doi.org/10.1590/S0100-8404200800...
, Carvalho et al. 2010CARVALHO, M.B.; ISHARA, K.L. & MAIMONI-RODELLA, R.C.S. 2010. Vascular Flora of a Cerrado sensu stricto remnant in Pratânia, state of São Paulo, southeastern Brazil. Check List: 350-357., Reys et al. 2013REYS P.; CAMARGO, M.G.G.; GROMBONE-GUARATINI, M.T.; TEIXEIRA, A.P.; ASSIS, M.A. & MORELLATO, L.P.C. 2013. Estrutura e composição florística de um Cerrado sensu stricto e sua importância para propostas de restauração ecológica. Hoehnea 40: 449-464. DOI:10.1590/S2236-8906201300030000.
https://doi.org/10.1590/S2236-8906201300...
), with Fabaceae, Malpighiaceae and Rubiaceae always among the most representative families. Compared to Reys et al. (2013)REYS P.; CAMARGO, M.G.G.; GROMBONE-GUARATINI, M.T.; TEIXEIRA, A.P.; ASSIS, M.A. & MORELLATO, L.P.C. 2013. Estrutura e composição florística de um Cerrado sensu stricto e sua importância para propostas de restauração ecológica. Hoehnea 40: 449-464. DOI:10.1590/S2236-8906201300030000.
https://doi.org/10.1590/S2236-8906201300...
survey, the present species list has increased to 40% the number of species, indicating the need for long-term, extensive surveys.
We surveyed 59 out of the 100 most frequent woody species listed to the Cerrado in Southern floristic province in Brazil (include São Paulo, Paraná and Minas Gerais states) based on Bridgewater et al. (2004)BRIDGEWATER, S.; RATTER, J.A. & FELIPE RIBEIRO, J. 2004. Biogeographic patterns, β-diversity and dominance in the Cerrado biome of Brazil. Biodivers. Conserv. 13: 2295-231.7 DOI: 10.1023/B:BIOC.0000047903.37608.4c.
https://doi.org/10.1023/B:BIOC.000004790...
. Among the species described on the Bridgewater et al. (2004)BRIDGEWATER, S.; RATTER, J.A. & FELIPE RIBEIRO, J. 2004. Biogeographic patterns, β-diversity and dominance in the Cerrado biome of Brazil. Biodivers. Conserv. 13: 2295-231.7 DOI: 10.1023/B:BIOC.0000047903.37608.4c.
https://doi.org/10.1023/B:BIOC.000004790...
list as the most common species in number of individuals we found in our site: Qualea grandiflora Mart., Byrsonima coccolobifolia Kunth, Piptocarpha rotundifolia (Less.) Baker, Erythroxylum suberosum A.St.-Hil., Caryocar brasiliense Cambess., Xylopia aromatica (Lam.) Mart., Byrsonima intermedia A. Juss., Casearia sylvestris Sw., Annona coriacea Mart., Ocotea pulchella (Nees & Mart.) Mez and Qualea multiflora Mart. It is important to highlight that most of these plants have been studied due to therapeutic properties as a result of their chemical composition. For example, Qualea grandiflora presents bioactivity against Plasmodium falciparum (Cordeiro et al. 2017CORDEIRO, T.M.; BORGHETTI, F.; OLIVEIRA, S.C.C.; BASTOS, I.M.D.; SANTANA, J.M.; GRELLIER, P. & CHARNEAU, S. 2017. Brazilian Cerrado Qualea grandiflora Mart. leaves exhibit antiplasmodial and trypanocidal activities In vitro. Pharmacogn. Mag. 13: 668-672. DOI: 10.4103/pm.pm_100_17.
https://doi.org/10.4103/pm.pm_100_17...
). Flavonoids isolated from Casearia sylvestris and Byrsonima coccolobifolia have been described as possible leishmanicidal (Antinarelli et al. 2015ANTINARELLI, L.M.; PINTO, N.C.; SCIO, E.; COIMBRA E.S. 2015. Antileishmanial activity of some Brazilian plants, with particular reference to Casearia sylvestris. An. Acad. Bras. Ciênc. 87: 733-742. DOI: 10.1590/0001-3765201520140288.
https://doi.org/10.1590/0001-37652015201...
, Souza et al. 2014SOUSA, L.R.F.; RAMALHO, S.D.; FERNANDES, J.B.; SILVA, M.F.G.F; IEMMA, M.R.; CORRÊA, J.; SOUZA, D.H.F.; LIMA, M.I.S. & VIEIRA, PC. 2014 Leishmanicidal galloylquinic acids are noncompetitive inhibitors of arginase J. Braz. Chem. Soc. 25: 1832-1838. DOI: 0.5935/0103-5053.20140115
https://doi.org/0.5935/0103-5053.2014011...
). Antioxidant, anxiolytic, antiulcer, insecticide, and antiparasitic properties of Annona coriacea - a species which presents a diversity of secondary metabolites may be promising for pharmacological use (Rocha et al. 2020ROCHA, G.N.S.A.O.; DUTRA, L.M.; LORENZO, V.P. & ALMEIDA, J.R.E.S. 2020. Phytochemicals and biological properties of Annona coriacea Mart. (Annonaceae): A systematic review from 1971 to 2020. Chem.-Biol. Interact .336. DOI: 10.1016/j.cbi.2021.109390.
https://doi.org/10.1016/j.cbi.2021.10939...
) - have begun to be studied. Erythroxylum suberosum has been reported to have antifungal and antibacterial activities (Violante et al. 2012), as well. These results reinforce the assumption that the high biodiversity of the Cerrado found even in small fragments like our study site, can be a source of new compounds with possible applications in therapeutic resources and further solidify the argument that the studied area must be preserved.
The only species belonging to a Near Threatened (NT) class found in our study site was the Bowdichia virgilioides Kunth (Table 1) a species distributed across the Amazon Rainforest, Caatinga, Central Brazilian Savanna (Cerrado), Atlantic Rainforest and Pantanal domains (Flora do Brasil 2020FLORA BRASIL 2020 Jardim Botânico do Rio de Janeiro. Available at: < http://floradobrasil.jbrj.gov.br/ >. Accessed on: 14 Apr. 2021.
http://floradobrasil.jbrj.gov.br/...
). Circumstances such as deforestation and over-extraction (due to the use in construction and furniture), —associated with biological characteristics such as low density and dormancy of its seeds — contributes to its endangered status (Rosa-Magri & Meneghi 2014ROSA-MAGRI, M.M. & MENEGHI, S.R. 2014. Avaliação das características germinativas da espécie arbórea sucupira--preta (Bowdichia virgilioides Kunth - Fabaceae). Bioikos 28:3-10.). Extinction of plant species leads to a loss of many ecological functions, community stability, and resilience, aside from secondary extinctions as a function of loss of key interactions (Rossati et al. 2015ROSSATI, N.B.; SILVA, D.M. & BATALHA, M.A. 2015. Loss of phylogenetic and functional originalities of woody Cerrado species in simulated extinction scenarios. Austral Ecol. 40: 267-274. DOI: 0.1111/aec.12210.
https://doi.org/0.1111/aec.12210...
).
Our study highlights the elevated number of plant species surveyed classified as Data Deficient (DD) (Table 1), showing the relatively low amount of available data about this domain species and the necessity of many complementary studies. However, some studies have shown that the data-deficient species described in many inventories are of extreme conservation concern, usually including species with a great risk for extinction (Bland et al. 2015BLAND, L.M.; COLLEN, B.; ORME, C.D.L. & BIELBY, J. 2015. Predicting the conservation status of data-deficient species. Conserv. Biol. 29:250-9. Doi: 10.1111/cobi.12372.
https://doi.org/10.1111/cobi.12372...
), or naturally rare (Corlett 2016CORLETT, R.T. 2016. Plant diversity in a changing world: status, trends, and conservation need. Plant Divers 38: 10-16. DOI: 10.1016/j.pld.2016.01.001.
https://doi.org/10.1016/j.pld.2016.01.00...
, Roberts et al. 2016ROBERTS, D.L.; TAYLOR, L. & JOPPA, L.N. 2016. Threatened or data-deficient: assessing the conservation status of poorly known species. Divers. Distrib. 22: 558-565.). In addition, the Cerrado of South America has the highest number of rare species showing the urgent need to include them in conservation planning (Maciel & Martins 2021MACIEL, E.A. & MARTINS, F.R. 2021. Rarity patterns and the conservation status of tree species in South American savannas. Flora 285:151942. DOI: 10.1016/j.flora.2021.151942.
https://doi.org/10.1016/j.flora.2021.151...
). Due to the great heterogeneity within the Cerrado domain and the alarming rate of destruction in recent years (MapBiomas, Collection 5.0), it is imperative that we conduct additional studies to provide more floristic and functional data for the remaining remnants. A more comprehensive floristic survey will improve the knowledge, and fill gaps in biodiversity data (Roberts et al. 2016ROBERTS, D.L.; TAYLOR, L. & JOPPA, L.N. 2016. Threatened or data-deficient: assessing the conservation status of poorly known species. Divers. Distrib. 22: 558-565.) on this domain, allowing us to propose better management strategies and contribute to improve models of restoration for the Cerrado (Pelizzaro et al. 2017PELLIZZARO, K.F., CORDEIRO, A.O.O., ALVES, M. MOTTA, C.P.; REZENDE, G. M.; SILVA; R.R.P.; RIBEIRO, J.F.; SAMPAIO, A.B.; VIEIRA, D. L.M. & SCHMIDT, I.B. 2017. “Cerrado” restoration by direct seeding: field establishment and initial growth of 75 trees, shrubs and grass species. Braz. J. Bot. 40: 681-693. DOI: 10.1007/s40415-017-0371-6.
https://doi.org/10.1007/s40415-017-0371-...
, Buisson et al. 2017BUISSON, E.; ALVARADO, S.T.; LE STRADIC, S. & MORELLATO, L.P.C. 2017. Enhancing the role of plant phenological research in ecological restoration. Restor. Ecol. 25: 164-171. DOI: 10.1111/rec.12471f.
https://doi.org/10.1111/rec.12471f...
, 2018).The proportions of plants in each life form category were consistent with most of the previous studies that describe cerrado sensu stricto as a vegetation dominated by trees and shrubs (50% of wood cover) (Coutinho 2006COUTINHO, L.M. 2006. O conceito de bioma. Acta Bot. Bras. 20: 13-2. DOI:10.1590/S0102-33062006000100002.
https://doi.org/10.1590/S0102-3306200600...
, Silva et al. 2015SILVA, A.F.; RABELO, M.F.R. & ENOQUE, M.M. 2015. Diversidade de angiospermas e espécies medicinais de uma área de Cerrado. Ver. Bras. Pl. Med. 17: 1016-1030. DOI: 10.1590/1983-084X/ 14_115.
https://doi.org/10.1590/1983-084X/14_115...
). However, in an inventory carried out in Pratania, SP, Carvalho et al. (2010)CARVALHO, M.B.; ISHARA, K.L. & MAIMONI-RODELLA, R.C.S. 2010. Vascular Flora of a Cerrado sensu stricto remnant in Pratânia, state of São Paulo, southeastern Brazil. Check List: 350-357. listed 37.5% shrubs, followed by herbs (27.5%), trees (23%), and lianas (12%). These conflicting results are possibly due to the level of preservation of the studied area and frequency of fires (Durigan et al. 2007DURIGAN, G.; SIQUEIRA, M.F. & FRANCO, G.A.D.C. 2007. Threats to the Cerrado remnants of the state of São Paulo, Brazil. Sci. Agric. 64: 355-363. DOI:10.1590/S0103-90162007000400006.
https://doi.org/10.1590/S0103-9016200700...
).
A recent inventory has mapped only 1% of remnant areas of Cerrado vegetation protected for the São Paulo State (Instituto Florestal 2020INSTITUTO FLORESTAL. 2020. Projeto Inventário Florestal do Estado de São Paulo: Mapeamento da Cobertura Vegetal Nativa. Secretaria de Infraestrutura e Meio Ambiente do estado de São Paulo. Disponível em: https://smastr16.blob.core.windows.net/home/2020/07/mapa-inventario-florestal-esp-20.pdf
https://smastr16.blob.core.windows.net/h...
). This is alarming data, highlighting the need for more protective measures of conservation from what has left of this important vegetation domain. In terms of importance, even for a small patch of vegetation, our study has reported the occurrence of several endemic cerrado species, as: Caryocar brasiliense Cambess., Anacardium humile A.St.-Hil., Aspidosperma tomentosum Mart. & Zucc., Licania humilis Cham. & Schltdl., Erythroxylum tortuosum Mart., Dalbergia miscolobium Benth., Dimorphandra mollis Benth., Ouratea spectabilis (Mart.) Engl. e Stryphnodendron rotundifolium Mart. Plant species of a wider distribution, such as: Duguetia lanceolata A.St.-Hil., Guatteria australis A.St.-Hil., Peritassa campestris (Cambess.) A. C. Sm., Sapium glandulosum (L.) Morong, Pterodon emarginatus Vogel e Campomanesia pubescens (Mart. ex DC.) O. Berg., found in this study area, can also be observed in other vegetation physiognomies (e.g.: semideciduous forest and Rain Forest) and vegetation domains (e.g.: Atlantic rainforest and Pantanal) (Flora do Brasil 2020FLORA BRASIL 2020 Jardim Botânico do Rio de Janeiro. Available at: < http://floradobrasil.jbrj.gov.br/ >. Accessed on: 14 Apr. 2021.
http://floradobrasil.jbrj.gov.br/...
), since our cerrado site belongs to the ecotone region of Cerrado and Atlantic Rainforest.
Our cerrado sensu stricto species were pollinated mainly by bees, with more than a half of species presenting bee-pollinated flowers (Figure 4), as expected for Cerrado and other tropical vegetation systems (Gottsberger & Silberbauer-Gottsberger 2006GOTTSBERGER, G. & SILBERBAUER-GOTTSBERGER, I. 2006. Life in the Cerrado: A South American Tropical Seasonal Ecosystem. Vol. II. Pollination and Seed Dispersal., Monteiro et al. 2021MONTEIRO, B.L.; CAMARGO, M.G.G.; LOIOLA, P.P.; CARSTENSEN, D.W.; GUSTAFSON, S. & MORELLATO, L.P.C. 2021. Pollination of the campo rupestre: a test of hypothesis for an ancient tropical mountain vegetation. Biol. J. Linn. Soc. 133: 512-530. DOI: 10.1093/biolinnean/blaa205.
https://doi.org/10.1093/biolinnean/blaa2...
, Genini et al. 2021GENINI, J.; GUIMARAES JR, P.R.; SAZIMA, M.; SAZIMA, I. &MORELLATO, L.P.C. 2021. Temporal organization among pollination systems in a tropical seasonal forest. The Science of Nature - Naturwissenschaften 108: 34.) and stressing the relevance of preserving Cerrado remnants for this key ecosystem service. For the same community, Martins et al. (2021)MARTINS, A.E.; CAMARGO, M.G.G. & MORELLATO, L.P.C. 2021. Flowering Phenology and the Influence of Seasonality in Flower Conspicuousness for Bees. Front. Plant Sci. 11: 1-11. DOI: 10.3389/fpls.2020.594538.
https://doi.org/10.3389/fpls.2020.594538...
found that plant species with different flower colors presented distinct flowering peaks over the year but maintained color diversity over time. For example, while white flowers peaked in the transition between dry and wet season, matching with the community flowering peak, yellow flowers were distributed all year long, being an important resource during the dry season, when a reduced number of species is flowering (Martins et al. 2021MARTINS, A.E.; CAMARGO, M.G.G. & MORELLATO, L.P.C. 2021. Flowering Phenology and the Influence of Seasonality in Flower Conspicuousness for Bees. Front. Plant Sci. 11: 1-11. DOI: 10.3389/fpls.2020.594538.
https://doi.org/10.3389/fpls.2020.594538...
). The observed flowering pattern provide functional diversity over time, contributing to the presence of different groups of pollinators such as bees, small insects, flies and hummingbirds, and nocturnal pollinators such as Sphingidae moths and bats (Gottsberger & Silberbauer-Gottsberger 2006GOTTSBERGER, G. & SILBERBAUER-GOTTSBERGER, I. 2006. Life in the Cerrado: A South American Tropical Seasonal Ecosystem. Vol. II. Pollination and Seed Dispersal., Amorim et al. 2009AMORIM, F.W.; DE ÁVILA, R.S.; DE CAMARGO, A.J.A.; VIEIRA, A.L. & OLIVEIRA, P.E. 2009. A hawkmoth crossroads? Species richness, seasonality and biogeographical affinities of Sphingidae in a Brazilian Cerrado. J. Biogeogr 36:. 662-674. DOI:10.1111/j.1365-2699.2008.02033.x.
https://doi.org/10.1111/j.1365-2699.2008...
, Martins et al. 2021MARTINS, A.E.; CAMARGO, M.G.G. & MORELLATO, L.P.C. 2021. Flowering Phenology and the Influence of Seasonality in Flower Conspicuousness for Bees. Front. Plant Sci. 11: 1-11. DOI: 10.3389/fpls.2020.594538.
https://doi.org/10.3389/fpls.2020.594538...
).
The observed predominance of seed dispersal by animals is expected for woody-dominated Cerrado phytophysiognomies (Weiser and Godoy 2001WEISER, V.L. & GODOY, S.A.P. 2001. Florística em um hectare de cerrado sensu stricto ARIE - Cerrado Pé de Gigante, Santa Rita do Passa Quatro, SP. Acta Bot. Bras. 15: 201-212 DOI: 10.1590/S0102-33062001000200007
https://doi.org/10.1590/S0102-3306200100...
, Gottsberger & Silberbauer-Gottsberger 2006GOTTSBERGER, G. & SILBERBAUER-GOTTSBERGER, I. 2006. Life in the Cerrado: A South American Tropical Seasonal Ecosystem. Vol. II. Pollination and Seed Dispersal., Gottsberger & Silberbauer-Gottsberger 2018GOTTSBERGER, G. & SILBERBAUER-GOTTSBERGER, I. 2018. How are pollination and seed dispersal modes in Cerrado related to stratification? Trends in a Cerrado sensu stricto woodland in southeastern Brazil, and a comparison with Neotropical forests. Acta Bot. Bras. 32: 434-445. DOI: 10.1590/0102-33062018abb0186.
https://doi.org/10.1590/0102-33062018abb...
) and previously indicated for our study area (Camargo et al. 2013CAMARGO, M.G.G., CAZETTA, E., SCHAEFER, M., MORELLATO, L.P.C. 2013. Fruit color and contrast in seasonal habitats - a case study from a cerrado savanna. Oikos 122:1335-1342. DOI: 10.1111/j.1600-0706.2013.00328.x
https://doi.org/10.1111/j.1600-0706.2013...
, Escobar et al. 2018ESCOBAR, D.F.; SILVEIRA, F.A.O. & MORELLATO, L.P.C. 2018. Timing of seed dispersal and seed dormancy in Brazilian savanna: two solutions to seasonality. Ann. Bot. 121: 1197-1209. DOI: 10.1093/aob/mcy006.
https://doi.org/10.1093/aob/mcy006...
). Wind-dispersed species are the second most important seed dispersal system, followed by self- dispersed seeds. The fruiting pattern of our community is seasonal according to the dispersal system (Camargo et al. 2013CAMARGO, M.G.G., CAZETTA, E., SCHAEFER, M., MORELLATO, L.P.C. 2013. Fruit color and contrast in seasonal habitats - a case study from a cerrado savanna. Oikos 122:1335-1342. DOI: 10.1111/j.1600-0706.2013.00328.x
https://doi.org/10.1111/j.1600-0706.2013...
, Escobar et al. 2018ESCOBAR, D.F.; SILVEIRA, F.A.O. & MORELLATO, L.P.C. 2018. Timing of seed dispersal and seed dormancy in Brazilian savanna: two solutions to seasonality. Ann. Bot. 121: 1197-1209. DOI: 10.1093/aob/mcy006.
https://doi.org/10.1093/aob/mcy006...
). Animal-dispersed fruits are produced all over the year, but mainly during the wet season (Camargo et al. 2013CAMARGO, M.G.G., CAZETTA, E., SCHAEFER, M., MORELLATO, L.P.C. 2013. Fruit color and contrast in seasonal habitats - a case study from a cerrado savanna. Oikos 122:1335-1342. DOI: 10.1111/j.1600-0706.2013.00328.x
https://doi.org/10.1111/j.1600-0706.2013...
, Escobar et al. 2018ESCOBAR, D.F.; SILVEIRA, F.A.O. & MORELLATO, L.P.C. 2018. Timing of seed dispersal and seed dormancy in Brazilian savanna: two solutions to seasonality. Ann. Bot. 121: 1197-1209. DOI: 10.1093/aob/mcy006.
https://doi.org/10.1093/aob/mcy006...
). Some animal-dispersed species such as Miconia rubiginosa (Bonpl.) DC., Pouteria torta (Mart.) Radlk., Tocoyena formosa (Cham. & Schltdl.) K.Schum. and Xylopia aromatica (Lam.) Mart. produce fruits even in the dry season and are important to guarantee resources for the frugivores in the area (Escobar et al. 2018ESCOBAR, D.F.; SILVEIRA, F.A.O. & MORELLATO, L.P.C. 2018. Timing of seed dispersal and seed dormancy in Brazilian savanna: two solutions to seasonality. Ann. Bot. 121: 1197-1209. DOI: 10.1093/aob/mcy006.
https://doi.org/10.1093/aob/mcy006...
). Fruiting peaks of self- and wind-dispersed species are observed at the dry season, when the wind dispersal is more efficient (Camargo et al. 2013CAMARGO, M.G.G., CAZETTA, E., SCHAEFER, M., MORELLATO, L.P.C. 2013. Fruit color and contrast in seasonal habitats - a case study from a cerrado savanna. Oikos 122:1335-1342. DOI: 10.1111/j.1600-0706.2013.00328.x
https://doi.org/10.1111/j.1600-0706.2013...
, Escobar et al. 2018ESCOBAR, D.F.; SILVEIRA, F.A.O. & MORELLATO, L.P.C. 2018. Timing of seed dispersal and seed dormancy in Brazilian savanna: two solutions to seasonality. Ann. Bot. 121: 1197-1209. DOI: 10.1093/aob/mcy006.
https://doi.org/10.1093/aob/mcy006...
). The proportion of seed dispersal function groups and fruiting time has been recently related to germination strategies (Escobar et al. 2018ESCOBAR, D.F.; SILVEIRA, F.A.O. & MORELLATO, L.P.C. 2018. Timing of seed dispersal and seed dormancy in Brazilian savanna: two solutions to seasonality. Ann. Bot. 121: 1197-1209. DOI: 10.1093/aob/mcy006.
https://doi.org/10.1093/aob/mcy006...
, 2021ESCOBAR, D F.; SILVEIRA, F.A.O. & MORELLATO, L.P.C. 2021 Do regeneration traits vary according to vegetation structure? A case study for savannas. J. Veg. Sci 32: e12940. DOI: 10.1111/jvs.12940.
https://doi.org/10.1111/jvs.12940...
), a matter of key relevance for restoration and that needs further investigation for Cerrado species.
The cerrado remnant studied can be considered a conservation priority due to the high diversity of data-deficient species and the importance for ecosystem services. Our checklist pointed out a high diversity of data-deficient species, a category considered equivalent to threatened by extinction by some authors (Bland et al. 2015BLAND, L.M.; COLLEN, B.; ORME, C.D.L. & BIELBY, J. 2015. Predicting the conservation status of data-deficient species. Conserv. Biol. 29:250-9. Doi: 10.1111/cobi.12372.
https://doi.org/10.1111/cobi.12372...
, Corlett 2016CORLETT, R.T. 2016. Plant diversity in a changing world: status, trends, and conservation need. Plant Divers 38: 10-16. DOI: 10.1016/j.pld.2016.01.001.
https://doi.org/10.1016/j.pld.2016.01.00...
, Roberts et al. 2016ROBERTS, D.L.; TAYLOR, L. & JOPPA, L.N. 2016. Threatened or data-deficient: assessing the conservation status of poorly known species. Divers. Distrib. 22: 558-565.). Consequently, our study area may represent a conservation priority based on the degree of knowledge gap and extinction risk of some species, associated with high diversity and potential ecosystem services provided. Our survey also indicated that even a small remnant can congregate a richest collection of species, plant functional types and life forms representatives of the Cerrado and concentrate an enormous value for biodiversity conservation, ecosystem services and restoration, holding several culturally important species (Pellizaro et al. 2017, Lemes et al. 2020LEMES, L.; DE ANDRADE, A.F.A. & LOYOLA, R. 2020. Spatial priorities for agricultural development in the Brazilian Cerrado: may economy and conservation coexist?. Biodivers Conserv 29: 1683-1700. https://doi.org/10.1007/s10531-019-01719-6
https://doi.org/10.1007/s10531-019-01719...
).
Acknowledgements
We thank the owners of Fazenda São José and IAB - Instituto Arruda Botelho for allowing us to conduct the field work at the farm. Our research was supported by São Paulo Research Foundation (FAPESP) (grants: #2007/59779-6, #2009/54208-6, FAPESP-Microsoft Research Institute #2013/50155-0 and FAPESP-Vale grant #2010/51307-0) to LPCM. MGGC received CNPq-PDJ (grant #161293/2015-8), FAPESP scholarship (grant: #2015/10754-8) and from Coordination for the Improvement of Higher Education Personnel - Brazil (CAPES) (grant #88887.583309/2020-00 Finance Code 001). RB and BCV received a doctoral fellowship and additional financial support from CAPES - Coordination for the Improvement of Higher Education Personnel (CAPES) —Finance Code 001; AEM Received scholarships from FAPESP (#2017/15152-1) and from the National Council for Scientific and Technological Development (CNPq), and currently receives a scholarship from CNPq (140534/2020-2). LPCM receives research productivity fellowship and grant from CNPq (#311820/2018-2). We thank all at the Phenology Laboratory (UNESP) for their help during fieldwork and for scientific discussions.
References
- ABRAHAMCZYK, S.; KLUGE, J., GARECA, Y.; REICHLE, S. & KESSLER M. 2011. The Influence of Climatic Seasonality on the Diversity of Different Tropical Pollinator Groups. PloS ONE 6: e27115. DOI: 10.1371/journal.pone.0027115.
» https://doi.org/10.1371/journal.pone.0027115 - AMORIM, F.W.; DE ÁVILA, R.S.; DE CAMARGO, A.J.A.; VIEIRA, A.L. & OLIVEIRA, P.E. 2009. A hawkmoth crossroads? Species richness, seasonality and biogeographical affinities of Sphingidae in a Brazilian Cerrado. J. Biogeogr 36:. 662-674. DOI:10.1111/j.1365-2699.2008.02033.x.
» https://doi.org/10.1111/j.1365-2699.2008.02033.x - ANTINARELLI, L.M.; PINTO, N.C.; SCIO, E.; COIMBRA E.S. 2015. Antileishmanial activity of some Brazilian plants, with particular reference to Casearia sylvestris. An. Acad. Bras. Ciênc. 87: 733-742. DOI: 10.1590/0001-3765201520140288.
» https://doi.org/10.1590/0001-3765201520140288 - APG ‒ Angiosperm Phylogeny Group (2009) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot. J. Linn. Soc. 161: 105-121.
- APG ‒ The Angiosperm Phylogeny Group (2016) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Bot. J. Linn. Soc. 181: 1-20.
- BATALHA, M.A. & MARTINS, F.R. 2004. Reproductive phenology of the Cerrado plant community in Emas National Park (central Brazil). Aust. J. Bot. 52: 149-161.
- BEUCHLE, R.; GRECCHI, R.C.; SHIMABUKURO, Y.E.; SELIGER, R., EVA, H.D.; SANO, E. & ACHARD, F. 2015. Land cover changes in the Brazilian Cerrado and Caatinga biomes from 1990 to 2010 based on a systematic remote sensing sampling approach. Appl. Geogr. 58:116-127. DOI:10.1016/j.apgeog.2015.01.017.
» https://doi.org/10.1016/j.apgeog.2015.01.017 - BLAND, L.M.; COLLEN, B.; ORME, C.D.L. & BIELBY, J. 2015. Predicting the conservation status of data-deficient species. Conserv. Biol. 29:250-9. Doi: 10.1111/cobi.12372.
» https://doi.org/10.1111/cobi.12372 - BRIDGEWATER, S.; RATTER, J.A. & FELIPE RIBEIRO, J. 2004. Biogeographic patterns, β-diversity and dominance in the Cerrado biome of Brazil. Biodivers. Conserv. 13: 2295-231.7 DOI: 10.1023/B:BIOC.0000047903.37608.4c.
» https://doi.org/10.1023/B:BIOC.0000047903.37608.4c - BUISSON, E.; ALVARADO, S.T.; LE STRADIC, S. & MORELLATO, L.P.C. 2017. Enhancing the role of plant phenological research in ecological restoration. Restor. Ecol. 25: 164-171. DOI: 10.1111/rec.12471f.
» https://doi.org/10.1111/rec.12471f - CAMARGO, M.G.G.; SOUZA, R.M.; REYS, P. & MORELLATO, L.P.C. 2011. Effects of environmental conditions associated to the cardinal orientation on the reproductive phenology of the Cerrado savanna tree Xylopia aromatica (Annonaceae). An. Acad. Bras. Ciênc. 83: 1007-1019. DOI: 10.1590/S0001-37652011005000014.
» https://doi.org/10.1590/S0001-37652011005000014 - CAMARGO, M.G.G., CAZETTA, E., SCHAEFER, M., MORELLATO, L.P.C. 2013. Fruit color and contrast in seasonal habitats - a case study from a cerrado savanna. Oikos 122:1335-1342. DOI: 10.1111/j.1600-0706.2013.00328.x
» https://doi.org/10.1111/j.1600-0706.2013.00328.x - CAMARGO, MGG, CARVALHO, G.A.; ALBERTON, B.; MORELLATO, L.P.C. 2018. Leafing patterns and leaf exchange strategies of a cerrado woody community. Biotropica 50: 442-454. DOI: 10.1111/btp.12552
» https://doi.org/10.1111/btp.12552 - CARVALHO, M.B.; ISHARA, K.L. & MAIMONI-RODELLA, R.C.S. 2010. Vascular Flora of a Cerrado sensu stricto remnant in Pratânia, state of São Paulo, southeastern Brazil. Check List: 350-357.
- CORDEIRO, T.M.; BORGHETTI, F.; OLIVEIRA, S.C.C.; BASTOS, I.M.D.; SANTANA, J.M.; GRELLIER, P. & CHARNEAU, S. 2017. Brazilian Cerrado Qualea grandiflora Mart. leaves exhibit antiplasmodial and trypanocidal activities In vitro Pharmacogn. Mag. 13: 668-672. DOI: 10.4103/pm.pm_100_17.
» https://doi.org/10.4103/pm.pm_100_17 - CORLETT, R.T. 2016. Plant diversity in a changing world: status, trends, and conservation need. Plant Divers 38: 10-16. DOI: 10.1016/j.pld.2016.01.001.
» https://doi.org/10.1016/j.pld.2016.01.001 - COUTINHO, L.M. 2006. O conceito de bioma. Acta Bot. Bras. 20: 13-2. DOI:10.1590/S0102-33062006000100002.
» https://doi.org/10.1590/S0102-33062006000100002 - DURIGAN, G.; BACIC, M.C.; FRANCO, G.A.D.C. & SIQUEIRA, M.F. 1999. Inventário florístico do Cerrado na Estação Ecológica de Assis, SP. Hoehnea. 26 49-172.
- DURIGAN, G.; NISHIKAWA, D.L.L.; ROCHA, E.; SILVEIRA, É.R.; PULITANO, F.M.; REGALADO, L.B.; CARVALHAES, M.A.; PARANAGUÁ, P.A. & RANIERI, V.E.L. 2001. Caracterização de dois estratos da vegetação em uma área de cerrado no município de Brotas, SP, Brasil. Acta Bot. Bras. 16: 251-262. DOI: 10.1590/S0102-33062002000300002.
» https://doi.org/10.1590/S0102-33062002000300002 - DURIGAN, G.; BAITELLO, J. B.; FRANCO, G. A.C. & SIQUEIRA, M. F. 2004.Plantas do Cerrado Paulista: imagens de uma paisagem ameaçada. Páginas e letras Editora & Gráfica, São Paulo.
- DURIGAN, G.; SIQUEIRA, M.F. & FRANCO, G.A.D.C. 2007. Threats to the Cerrado remnants of the state of São Paulo, Brazil. Sci. Agric. 64: 355-363. DOI:10.1590/S0103-90162007000400006.
» https://doi.org/10.1590/S0103-90162007000400006 - DURIGAN, G.; RAMOS, V.S.; IVANAUSKAS, N.M. & FRANCO, G.A.C. 2012. Espécies de fitofisionomias na transição CERRADO-MATA ATLÂNTICA no estado de São Paulo. Secretaria do Meio Ambiente do Estado de São Paulo.
- EITEN, G. 1972. The Cerrado vegetation of Brazil. Bot Rev. 38: 201-341. DOI:10.1007/BF02859158.
» https://doi.org/10.1007/BF02859158 - EMBRAPA - EMPRESA BRASILEIRA DE PESQUISA AGROPECUÁRIA. 1999. Sistema brasileiro de classificação de solos. Brasília, Embrapa Produção de Informação. Rio de Janeiro: Embrapa Solos.
- ESCOBAR, D.F.; SILVEIRA, F.A.O. & MORELLATO, L.P.C. 2018. Timing of seed dispersal and seed dormancy in Brazilian savanna: two solutions to seasonality. Ann. Bot. 121: 1197-1209. DOI: 10.1093/aob/mcy006.
» https://doi.org/10.1093/aob/mcy006 - ESCOBAR, D F.; SILVEIRA, F.A.O. & MORELLATO, L.P.C. 2021 Do regeneration traits vary according to vegetation structure? A case study for savannas. J. Veg. Sci 32: e12940. DOI: 10.1111/jvs.12940.
» https://doi.org/10.1111/jvs.12940 - FELFILI, J.M.; SILVA, P.E.N.D.; SILVA JÚNIOR, M.C.D.; MARIMON, B.S. & DELITTI, W.B.C. 2002. Composição florística e fitossociologia do cerrado sentido restrito no município de Água Boa-MT. Acta Bot. Bras. 16: 103-112. DOI: 10.1590/S0102-33062002000100012.
» https://doi.org/10.1590/S0102-33062002000100012 - FIDELIS, A.T. & GODOY, S.A.P. 2003. Estrutura de um cerrado stricto sensu na Gleba Cerrado Pé de Gigante, Santa Rita do Passa Quatro, SP. Acta Bot. Bras. 17: 531-539. DOI: 10.1590/S0102-33062003000400006.
» https://doi.org/10.1590/S0102-33062003000400006 - FLORA BRASIL 2020 Jardim Botânico do Rio de Janeiro. Available at: < http://floradobrasil.jbrj.gov.br/ >. Accessed on: 14 Apr. 2021.
» http://floradobrasil.jbrj.gov.br/ - GENINI, J.; GUIMARAES JR, P.R.; SAZIMA, M.; SAZIMA, I. &MORELLATO, L.P.C. 2021. Temporal organization among pollination systems in a tropical seasonal forest. The Science of Nature - Naturwissenschaften 108: 34.
- GENTRY, A.H. 1982. Patterns of neotropical plant species diversity. Evolutionary Biology 15: 1-84.
- GOTTSBERGER, G. & SILBERBAUER-GOTTSBERGER, I. 2006. Life in the Cerrado: A South American Tropical Seasonal Ecosystem. Vol. II. Pollination and Seed Dispersal.
- GOTTSBERGER, G. & SILBERBAUER-GOTTSBERGER, I. 2018. How are pollination and seed dispersal modes in Cerrado related to stratification? Trends in a Cerrado sensu stricto woodland in southeastern Brazil, and a comparison with Neotropical forests. Acta Bot. Bras. 32: 434-445. DOI: 10.1590/0102-33062018abb0186.
» https://doi.org/10.1590/0102-33062018abb0186 - ISHARA, K.L.; DÉSTRO, G.F.G.; RODELLA, R.C.S.M. & YANAGIZAWA, Y.A.N.P. 2008. Composição florística de remanescente de cerrado sensu stricto em Botucatu, SP. Rev. bras. bot. 31:575-586. DOI: 10.1590/S0100-84042008000400004.
» https://doi.org/10.1590/S0100-84042008000400004 - INSTITUTO FLORESTAL. 2020. Projeto Inventário Florestal do Estado de São Paulo: Mapeamento da Cobertura Vegetal Nativa. Secretaria de Infraestrutura e Meio Ambiente do estado de São Paulo. Disponível em: https://smastr16.blob.core.windows.net/home/2020/07/mapa-inventario-florestal-esp-20.pdf
» https://smastr16.blob.core.windows.net/home/2020/07/mapa-inventario-florestal-esp-20.pdf - IUCN (2020). The IUCN Red List of Threatened Species. Version 2020-3. https://www.iucnredlist.org. Downloaded on 2021-01-15. https://doi.org/10.15468/0qnb58 accessed via GBIF.org on 2021-04-14.
» https://www.iucnredlist.org» https://doi.org/10.15468/0qnb58 - KLINK, C.A. & MACHADO, R.B. 2005. Conservation of the Brazilian Cerrado. Conserv. Biol. 19: 707-713. DOI: 10.1111/j.1523-1739.2005.00702.x.
» https://doi.org/10.1111/j.1523-1739.2005.00702.x - LEMES, L.; DE ANDRADE, A.F.A. & LOYOLA, R. 2020. Spatial priorities for agricultural development in the Brazilian Cerrado: may economy and conservation coexist?. Biodivers Conserv 29: 1683-1700. https://doi.org/10.1007/s10531-019-01719-6
» https://doi.org/10.1007/s10531-019-01719-6 - KÖPPEN, W. 1948. Climatologia. Fondo de Cultura Económica. México.
- LAMBERS, H.; COSTA, P.B. & OLIVEIRA, R.S. 2020. Towards more sustainable cropping systems: lessons from native Cerrado species. Theor. Exp. Plant Physiol. 32: 175-194. DOI:10.1007/s40626-020-00180-z.
» https://doi.org/10.1007/s40626-020-00180-z - LEMES, L.; DE ANDRADE, A.F.A. & LOYOLA, R. 2020. Spatial priorities for agricultural development in the Brazilian Cerrado: may economy and conservation coexist? Biodivers Conserv 29: 1683-1700. DOI:10.1007/s10531-019-01719-6.
» https://doi.org/10.1007/s10531-019-01719-6 - LIMA, N.E.; GUIMARÃES, R.A.; ALMEIDA-JÚNIOR, E.B.; VITORINO, L.C. & COLLEVATTI, G.G. 2020. Temporal trends, impact and partnership in floristic and phytosociology literature in the Brazilian Cerrado. Flora 273: 151721. DOI: 10.1016/j.flora.2020.151721.
» https://doi.org/10.1016/j.flora.2020.151721 - LOPES, G.R.; LIMA, M.G.B. & DOS REIS, T.N.P (2021) Maldevelopment revisited: Inclusiveness and social impacts of soy expansion over Brazil’s Cerrado in Matopiba. World Dev. 139:105316. DOI:10.1016/j.worlddev.2020.105316.
» https://doi.org/10.1016/j.worlddev.2020.105316 - MACIEL, E.A. & MARTINS, F.R. 2021. Rarity patterns and the conservation status of tree species in South American savannas. Flora 285:151942. DOI: 10.1016/j.flora.2021.151942.
» https://doi.org/10.1016/j.flora.2021.151942 - MANTOVANI, W. & MARTINS, F.R. 1993. Florística do cerrado da Reserva Biológica de Moji Guaçu, SP. Acta Bot. Bras. 20: 33-60. DOI: 10.1590/S0102-33061993000100003.
» https://doi.org/10.1590/S0102-33061993000100003 - MARTINS, A.E. 2019. Flower Color Patterns and Pollination in Seasonal Vegetations. Dissertação de Mestrado, São Paulo State University, Rio Claro, SP.
- MARTINS, A.E.; CAMARGO, M.G.G. & MORELLATO, L.P.C. 2021. Flowering Phenology and the Influence of Seasonality in Flower Conspicuousness for Bees. Front. Plant Sci. 11: 1-11. DOI: 10.3389/fpls.2020.594538.
» https://doi.org/10.3389/fpls.2020.594538 - MELIS, J.; CAMARGO, M.G.G.; CARVALHO, P.G.; MORELLATO, L.P.C. & GROMBONE-GUARATINI, M.T. 2021. Edge influence on liana community in a cerrado savanna. Austral Ecol. 46: 192-203. DOI:10.1111/aec.12968.
» https://doi.org/10.1111/aec.12968 - METZGER, J.P. & RODRIGUES, R.R. 2008. Mapas síntese de diretrizes para a conservação e restauração da biodiversidade no Estado de São Paulo. In: Diretrizes para conservação e restauração da biodiversidade no Estado de São Paulo. R.R., Rodrigues; C.A. Joly, M.W. Brito; A Paese; J.P. Metzger; L. Casatti; M.A. Nalon; N. Menezes; N.M. Ivanauska; V. Bolzani & V.L.R..Bononi. Governo do Estado de São Paulo, São Paulo, p. 130-136.
- MITTERMEIER, R.A.; GIL, P.R.; HOFFMAN, M.; PILGRIM, J.; BROOKS, T.; MITTERMEIER, C.G.; LAMOREUX, J. & FONSECA, G.A.B. 2005. Hotspots revisited: earth’s biologically richest and most endangered terrestrial ecoregions. Washington, Conservation International.
- MONTEIRO, B.L.; CAMARGO, M.G.G.; LOIOLA, P.P.; CARSTENSEN, D.W.; GUSTAFSON, S. & MORELLATO, L.P.C. 2021. Pollination of the campo rupestre: a test of hypothesis for an ancient tropical mountain vegetation. Biol. J. Linn. Soc. 133: 512-530. DOI: 10.1093/biolinnean/blaa205.
» https://doi.org/10.1093/biolinnean/blaa205 - MYERS, N.; MITTERMEIER, R.A.; MITTERMEIER, C.G; DA FONSECA G.A.B. & KENT, J. 2000. Biodiversity hotspots for conservation priorities. Nature 403:853-858. DOI: 10.1038/35002 501.
» https://doi.org/10.1038/35002501 - PELLIZZARO, K.F., CORDEIRO, A.O.O., ALVES, M. MOTTA, C.P.; REZENDE, G. M.; SILVA; R.R.P.; RIBEIRO, J.F.; SAMPAIO, A.B.; VIEIRA, D. L.M. & SCHMIDT, I.B. 2017. “Cerrado” restoration by direct seeding: field establishment and initial growth of 75 trees, shrubs and grass species. Braz. J. Bot. 40: 681-693. DOI: 10.1007/s40415-017-0371-6.
» https://doi.org/10.1007/s40415-017-0371-6 - PEREIRA, L.C.; BALBINO, L.; MATUS, G.N.; DIAS, H.C.T. & TONELLO, K.C. 2021. Aspects of forest restoration and hydrology: linking passive restoration and soil-water recovery in Brazilian Cerrado. J. For. Res. 31:1-11. DOI:10.1007/s11676-021-01301-3.
» https://doi.org/10.1007/s11676-021-01301-3 - RATTER, J.; BRIDGEWATER, S. & RIBEIRO, J. 2003. Analysis of the floristic composition of the brazilian Cerrado vegetation iii: comparison of the woody vegetation of 376 areas. Edinb. J. Bot. 60: 57-109. doi:10.1017/S0960428603000064.
» https://doi.org/10.1017/S0960428603000064 - REYS P.; CAMARGO, M.G.G.; GROMBONE-GUARATINI, M.T.; TEIXEIRA, A.P.; ASSIS, M.A. & MORELLATO, L.P.C. 2013. Estrutura e composição florística de um Cerrado sensu stricto e sua importância para propostas de restauração ecológica. Hoehnea 40: 449-464. DOI:10.1590/S2236-8906201300030000.
» https://doi.org/10.1590/S2236-8906201300030000 - ROBERTS, D.L.; TAYLOR, L. & JOPPA, L.N. 2016. Threatened or data-deficient: assessing the conservation status of poorly known species. Divers. Distrib. 22: 558-565.
- ROCHA, G.N.S.A.O.; DUTRA, L.M.; LORENZO, V.P. & ALMEIDA, J.R.E.S. 2020. Phytochemicals and biological properties of Annona coriacea Mart. (Annonaceae): A systematic review from 1971 to 2020. Chem.-Biol. Interact .336. DOI: 10.1016/j.cbi.2021.109390.
» https://doi.org/10.1016/j.cbi.2021.109390 - RODRIGUES, S.J.A.; VIOLA, M.R.; ALVARENGA, L.A.; MELLO, C.R.; CHOU, S.C.; OLIVEIRA, V.A.; UDDAMERI, V. & MORAIS, M.A. 2020. Climate change impacts under representative concentration pathway scenarios on streamflow and droughts of basins in the Brazilian Cerrado biome. Int. J. Climatol. 40, 2511-2526.DOI:10.1002/joc.6347.
» https://doi.org/10.1002/joc.6347 - ROSA-MAGRI, M.M. & MENEGHI, S.R. 2014. Avaliação das características germinativas da espécie arbórea sucupira--preta (Bowdichia virgilioides Kunth - Fabaceae). Bioikos 28:3-10.
- ROSSATI, N.B.; SILVA, D.M. & BATALHA, M.A. 2015. Loss of phylogenetic and functional originalities of woody Cerrado species in simulated extinction scenarios. Austral Ecol. 40: 267-274. DOI: 0.1111/aec.12210.
» https://doi.org/0.1111/aec.12210 - SANO, E.E.; ROSA, R.; BRITO, J.L.S. & FERREIRA, L.G. 2008. Mapeamento semidetalhado do uso da terra do Bioma Cerrado. Pesqui. Agropecu. Bras. 43: 53-156. DOI: 10.1590/S0100-204X2008000100020.
» https://doi.org/10.1590/S0100-204X2008000100020 - SANO, E.E.; ROSA, R.; BRITO, J.L.S. & FERREIRA, L.G. 2010. Land cover mapping of the tropical savanna region in Brazil, Environ. Monit. Assess. 166:113-124. DOI: 0.1007/s10661-009-0988-4
» https://doi.org/0.1007/s10661-009-0988-4 - SILVA, J.M.C. & BATES, J.M. 2002. Biogeographic patterns and conservation in the South American Cerrado: A tropical Savanna hotspot. Bioscience 52: 225-234. DOI:10.1641/0006-3568(2002)052[0225:BPACIT]2.0.CO;2.
» https://doi.org/10.1641/0006-3568(2002)052[0225:BPACIT]2.0.CO;2 - SILVA, A.F.; RABELO, M.F.R. & ENOQUE, M.M. 2015. Diversidade de angiospermas e espécies medicinais de uma área de Cerrado. Ver. Bras. Pl. Med. 17: 1016-1030. DOI: 10.1590/1983-084X/ 14_115.
» https://doi.org/10.1590/1983-084X/14_115 - SOUSA, L.R.F.; RAMALHO, S.D.; FERNANDES, J.B.; SILVA, M.F.G.F; IEMMA, M.R.; CORRÊA, J.; SOUZA, D.H.F.; LIMA, M.I.S. & VIEIRA, PC. 2014 Leishmanicidal galloylquinic acids are noncompetitive inhibitors of arginase J. Braz. Chem. Soc. 25: 1832-1838. DOI: 0.5935/0103-5053.20140115
» https://doi.org/0.5935/0103-5053.20140115 - STRASSBURG, B.B.N.; BROOKS, T.; FELTRAN‐BARBIERI, R.; IRIBARREM, A.; CROUZEILLES, R.; LOYOLA, R.; LATAWIEC, A.E.; OLIVEIRA-FILHO, F.J.B.; SCARAMUZZA, C.A.M.; SCARANO, F.R.; SOARES-FILHO, B. & BALMFORD, A. 2017. Moment of truth for the Cerrado hotspot. Nat. Ecol. Evol. 1: 0099. DOI:10.1038/s41559-017-0099.
» https://doi.org/10.1038/s41559-017-0099 - STRASSBURG, B.; LATAWIEC, A. & BALMFORD, A. 2016. Urgent action on Cerrado extinctions. Nature 540: 199. DOI:10.1038/540199a3
» https://doi.org/10.1038/540199a3 - van der PIJL, L. 1982. Ecological Dispersal Classes, Established on the Basis of the Dispersing Agents. In: Principles of Dispersal in Higher Plants. Springer, Berlin, Heidelberg. DOI:10.1007/978-3-642-87925-8_5.
» https://doi.org/10.1007/978-3-642-87925-8_5 - VOGADO, N.O.; CAMARGO, M.C.G.; LOCOSSELLI, GM. & MORELLATO, LPC. 2016. Edge Effects on the Phenology of the Guamirim, Myrcia Guianensis (Myrtaceae), a Cerrado Tree, Brazil. Trop. Conserv. Sci. 9:291-312. DOI: 10.1177/194008291600900115
» https://doi.org/10.1177/194008291600900115 - WEISER, V.L. & GODOY, S.A.P. 2001. Florística em um hectare de cerrado sensu stricto ARIE - Cerrado Pé de Gigante, Santa Rita do Passa Quatro, SP. Acta Bot. Bras. 15: 201-212 DOI: 10.1590/S0102-33062001000200007
» https://doi.org/10.1590/S0102-33062001000200007
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Publication Dates
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Publication in this collection
16 Sept 2022 -
Date of issue
2022
History
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Received
03 Dec 2021 -
Accepted
03 May 2022