Abstract
Cocoa agroforests like the cabrucas of Brazil's Atlantic forest are among the agro-ecosystems with greatest potential for biodiversity conservation. Despite a global trend for their intensification, cocoa agroforests are also being abandoned for socioeconomic reasons especially on marginal sites, because they are incorporated in public or private protected areas, or are part of mandatory set-asides under Brazilian environmental legislation. However, little is known about phylogenetic structure, the processes of forest regeneration after abandonment and the conservation value of former cabruca sites. Here we compare the vegetation structure and composition of a former cabruca 30–40 years after abandonment with a managed cabruca and mature forest in the Atlantic forest region of Espirito Santo, Brazil. The forest in the abandoned cabruca had recovered a substantial part of its original structure. Abandoned cabruca have a higher density (mean ± CI95 %: 525.0 ± 40.3 stems per ha), basal area (34.0 ± 6.5 m2 per ha) and species richness (148 ± 11.5 species) than managed cabruca (96.0 ± 17.7; 24.15 ± 3.9 and 114.5 ± 16.0, respectively) but no significant differences to mature forest in density (581.0 ± 42.2), basal area (29.9.0 ± 3.3) and species richness (162.6 ± 15.5 species). Thinning (understory removal) changes phylogenetic structure from evenness in mature forest to clustering in managed cabruca, but after 30–40 years abandoned cabruca had a random phylogenetic structure, probably due to a balance between biotic and abiotic filters at this age. We conclude that abandoned cocoa agroforests present highly favorable conditions for the regeneration of Atlantic forest and could contribute to the formation of an interconnected network of forest habitat in this biodiversity hotspot.
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References
Asare R, Afari-Sefa V, Osei-Owusu Y, Pabi O (2014) Cocoa agroforestry for increasing forest connectivity in a fragmented landscape in Ghana. Agrofor Syst 88:1143–1156
Bhagwat SA, Willis KJ, Birks HJB, Whittaker RJ (2008) Agroforestry: a refuge for tropical biodiversity? Trends Ecol Evo 23:261–267
Cassano CR, Kierulff MCM, Chiarello AG (2011) The cacao agroforests of the Brazilian Atlantic forest as habitat for the endangered maned sloth Bradypus torquatus. Mamm Biol 76:243–250
Cassano CR, Schroth G, Faria D, Delabie JHC, Bede L (2009) Landscape and farm scale management to enhance biodiversity conservation in the cocoa producing region of southern Bahia, Brazil. Biodivers Conserv 18:577–603
Colwell RK (2013) EstimateS: Statistical estimation of species richness and shared species from samples. User’s Guide and application published at: http://purl.oclc.org/estimates
Colwell RK, Chao A, Gotelli NJ, Lin SY, Mao CX, Chazdon RL, Longino JT (2012) Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. J Plant Ecol 5:3–21
Dale VH, Beyeler SC (2001) Challenges in the development and use of ecological indicators. Ecol Indic 1:3–10
Delabie JHC, Jahyny B, do Nascimento IC, Mariano CSF, Lacau S, Campiolo S, Philpott SM, Leponce M (2007) Contribution of cocoa plantations to the conservation of native ants (Insecta: Hymenoptera: Formicidae) with a special emphasis on the Atlantic Forest fauna of southern Bahia, Brazil. Biodivers Conserv 16:2359–2384
Ding Y, Zang R, Letcher SG, Liu S, He F (2012) Disturbance regime changes the trait distribution, phylogenetic structure and community assembly of tropical rain forests. Oikos 121:1263–1270
Faria D, Laps RR, Baumgarten J, Cetra M (2006) Bat and bird assemblages from forests and shade cacao plantations in two contrasting landscapes in the Atlantic Forest of southern Bahia, Brazil. Biodivers Conserv 15:587–612
Finegan B (1996) Pattern and process in neotropical secondary rain forests: the first 100 years of succession. Trends Ecol Evo 11:119–124
Gama-Rodrigues EF, Ramachandran Nair PK, Nair VD, Gama-Rodrigues AC, Baligar VC, Machado RCR (2010) Carbon storage in soil size fractions under two cacao agroforestry systems in Bahia, Brazil. Environ Manage 45:274–283
Gomes JML (2006) Regeneração natural em uma floresta ombrófila densa aluvial sob diferentes usos do solo no delta do rio Doce. Dissertação, Universidade Estadual Norte Fluminense, RJ, Brasil
Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:379–391
Griscom HP, Griscom BW, Ashton MS (2009) Forest regeneration from pasture in the dry tropics of Panama: effects of cattle, exotic grass, and forested riparia. Restor Ecol 17:117–126
Guariguata MR, Dupuy JM (1997) Forest regeneration in abandoned logging roads in lowland Costa Rica1. Biotropica 29:15–28
Guevara S, Purata SE, Van der Maarel E (1986) The role of remnant forest trees in tropical secondary succession. Vegetatio 66:77–84
Hammer Ø, Harper DAT, Ryan PD (2001) Paleontological statistics software package for education and data analysis. Palaeontol Electronica 4:9–18
Holl KD, Loik ME, Lin EHV, Samuels IA (2000) Tropical montane forest restoration in Costa Rica: overcoming barriers to dispersal and establishment. Restor Ecol 8:339–349
IUSS Working Group (2014) World Reference Base for Soil Resources 2014. International soil classification system for naming soils and creating legends for soil maps. World Soil Resources Reports No. 106. FAO, Rome
Johns ND (1999) Conservation in Brazil’s chocolate forest: the unlikely persistence of the traditional cocoa agroecosystem. Environ Manage 23:31–47
Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464
Kembel SW, Hubbell SP (2006) The phylogenetic structure of a neotropical forest tree community. Ecology 87:S86–S99
Lani JL (1998) Deltas dos rios Doce e Itapemirim: Solos, com ênfase nos tiomórficos, água e impacto ambiental do uso. Viçosa, MG, Universidade Federal de Federal de Viçosa, 169p, (PhD. Thesis)
Letche SG, Chazdon RL, Andrade AC, Bongers F, van Breugel M, Finegan B, Laurance SG, Mesquita RC, Martinez-Ramos M, Williamson GB (2012) Phylogenetic community structure during succession: evidence from three Neotropical forest sites. Perspect Plant Ecol Evol Syst 14:79–87
Lima RAF, Batista JLF, Prado PI (2015) Modeling tree diameter distributions in natural forests: an evaluation of 10 statistical models. Forest Sci 61:320–327
Mo X-X, Shi L-L, Zhang Y-J, Zhu H, Slik JWF (2013) Change in phylogenetic community structure during succession of traditionally managed tropical rainforest in southwest China. PLoS One 8:e71464
Mooney H, Cropper A, Reid W (2005) Confronting the human dilemma. Nature 434:561–562
Mori SA, Boom BM, de Carvalino AM, dos Santos TS (1983) Ecological importance of Myrtaceae in an Eastern Brazilian Wet Forest. Biotropica 15:68
Myers N, Mittermeier RA, Mittermeier CG, Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858
Oliveira LC, Hankerson SJ, Dietz JM, Raboy BE (2010) Key tree species for the golden-headed lion tamarin and implications for shade-cocoa management in southern Bahia, Brazil. Anim Conserv 13:60–70
Pardini R (2004) Effects of forest fragmentation on small mammals in an Atlantic forest landscape. Biodivers Conserv 13:2567–2586
Piasentin FB (2011) O sistema de cabruca no sudeste da Bahia: perspectivas de sustentabilidade. Dissertação, Universidade de Brasília, DF, Brasil
Piasentin FB, Saito CH (2014) Os diferentes métodos de cultivo de cacau no sudeste da Bahia, Brasil: aspectos históricos e percepções. Bol Mus Para Emilio Goeldi Ciênc Hum 9:61–78
Piasentin FB, Saito H (2012) Caracterização do cultivo do cacau na região econômica litoral sul da Bahia. Estud Debate 19:63–80
Piotto D, Montagnini F, Thomas W, Ashton M, Oliver C (2009) Forest recovery after swidden cultivation across a 40-year chronosequence in the Atlantic forest of southern Bahia, Brazil. Plant Ecol 205:261–272
Prinzing A, Durka W, Klotz S, Brandl R (2001) The niche of higher plants: evidence for phylogenetic conservatism. Proc R Soc B Biol 268:2383–2389
Raboy BE, Christman MC, Dietz JM (2004) The use of degraded and shade cocoa forests by endangered golden-headed lion tamarins Leontopithecus chrysomelas. Oryx 38:75–83
Rezende CL, Uezu A, Scarano FR, Araujo DSD (2015) Atlantic forest spontaneous regeneration at landscape scale. Biodivers Conserv 24:2255–2272
Rice RA, Greenberg R (2000) Cacao cultivation and the conservation of biological diversity. Ambio 29:167–173
Rigueira DMG, da Rocha PLB, Mariano-Neto E (2013) Forest cover, extinction thresholds and time lags in woody plants (Myrtaceae) in the Brazilian Atlantic forest: resources for conservation. Biodivers Conserv 22:3141–3163
Rodrigues RR, Lima RAF, Gandolfi S, Nave AG (2009) On the restoration of high diversity forests: 30 years of experience in the Brazilian Atlantic forest. Biol Conserv 142:1242–1251
Rolim SG, Chiarello AG (2004) Slow death of Atlantic forest trees in cocoa agroforestry in southeastern Brazil. Biodivers Conserv 13:2679–2694
Rolim SG, Ivanauskas NM, Rodrigues RR, Nascimento MT, Gomes JML, Folli DA, Couto HTZ (2006) Composição florística do estrato arbóreo da Floresta Estacional Semidecidual na planície aluvial do rio Doce, Linhares, ES, Brasil. Acta Bot Brasílica 20:549–561
Ruf F, Schroth G (2004) Chocolate forests and monocultures: a historical review of cocoa growing and its conflicting role in tropical deforestation and forest conservation. In: Schroth G, Fonseca GAB, Harvey CA, Vasconcelos HL, Gascon C, Izar AMN (eds) Agroforestry and biodiversity conservation in tropical landscapes. Island Press, Washington, DC, pp 107–134
Sala OE, Chapin FS, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, Huber-Sanwald E, Huenneke LF, Jackson RB, Kinzig A, Leemans R, Lodge DM, Mooney HA, Oesterheld M, Poff NL, Sykes MT, Walker BH, Walker M, Wall DH (2000) Global biodiversity scenarios for the year 2100. Science 287:1770–1774
Sambuichi RHR (2002) Fitossociologia e diversidade de espécies arbóreas em cabruca (mata atlântica raleada sobre plantação de cacau) na Região Sul da Bahia, Brasil. Acta Bot Brasilica 16:89–101
Sambuichi RHR (2006) Estrutura e dinâmica do componente arbóreo em área de cabruca na região cacaueira do sul da Bahia, Brasil. Acta Bot Brasilica 20:943–954
Sambuichi RHR, de Oliveira RLRM, Mariano Neto E, Thevenin JMR, Jesus Junior CP, Oliveira RL, Pelicao MC (2008) Conservation status of ten endemic trees from the Atlantic forest in the south of Bahia -Brazil. Natureza & Conservacão 6:208–225
Sambuichi RHR, Haridasan M (2007) Recovery of species richness and conservation of native Atlantic forest trees in the cacao plantations of southern Bahia in Brazil. Biodivers Conserv 16:3681–3701
Sambuichi RHR, Vidal DB, Piasentin FB, Jardim JG, Viana TG, Menezes AA, Mello DLN, Ahnert D, Baligar VC (2012) Cabruca agroforests in southern Bahia, Brazil: tree component, management practices and tree species conservation. Biodivers Conserv 21:1055–1077
Sansevero JBB, Prieto PV, Moraes LFD, Rodrigues JFP (2011) Natural regeneration in plantations of native trees in lowland Brazilian Atlantic Forest: community structure, diversity, and dispersal syndromes. Restor Ecol 19:379–389
Schroth G, Bede LC, Paiva AO, Cassano CR, Amorim AM, Faria D, Mariano-Neto E, Martini AMZ, Sambuichi RHR, Lôbo RN (2015) Contribution of agroforests to landscape carbon storage. Mitig Adapt Strategies Glob Chang 20:1175–1190
Schroth G, Faria D, Araujo M, Bede L, Van Bael SA, Cassano CR, Oliveira LC, Delabie JHC (2011) Conservation in tropical landscape mosaics: the case of the cacao landscape of southern Bahia, Brazil. Biodivers Conserv 20:1635–1654
Schroth G, Fonseca GAB, Harvey CA, Vasconcelos HL, Gascon C, Izar AMN (2004) Agroforestry and biodiversity conservation in tropical landscapes. Island Press, Washington, DC
Schroth G, Garcia E, Griscom BW, Teixeira WG, Barros LP (2016a) Commodity production as restoration driver in the Brazilian Amazon? Pasture re-agro-forestation with cocoa (Theobroma cacao) in southern Para. Sustainability Sci 11:277–293
Schroth G, Jeusset A, Gomes AS, Florence CT, Coelho NAP, Faria D, Läderach P (2016b) Climate friendliness of cocoa agroforests is compatible with productivity increase. Mitig Adapt Strategies Glob Chang 21:67–80
Schroth G, Lehmann J, Rodrigues MRL, Barros E, Macêdo JLV (2001) Plant-soil interactions in multistrata agroforestry in the humid tropics. Agroforest Syst 53:85–102
Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research. WH Freeman and Company, New York, NY
Suganuma MS, Durigan G (2015) Indicators of restoration success in riparian tropical forests using multiple reference ecosystems. Restor Ecol 23:238–251
Suguio K, Martin L, Domingues J, (1982) Evolução da planície costeira do Rio Doce (ES) durante o quaternário: influência das flutuações do nível do mar. In: Suguio K, De Meis MRM, Tessler MG (eds) Anais do IV Simpósio do Quaternário no Brasil. pp 93–116, Sociedade Brasileira de Geologia, Rio de Janeiro, RJ, Brasil
Tabarelli M, Peres CA (2002) Abiotic and vertebrate seed dispersal in the Brazilian Atlantic forest: implications for forest regeneration. Biol Conserv 106:165–176
Thomas W, Carvalho AMVDE, Amorim AMA, Garrison J, Arbeláez AL (1998) Plant endemism in two forests in southern Bahia, Brazil. Biodivers Conserv 7:311–322
Toyama H, Kajisa T, Tagane S, Mase K, Chhang P, Samreth V, Ma V, Sokh H, Ichihashi R, Onoda Y, Mizoue N, Yahara T (2015) Effects of logging and recruitment on community phylogenetic structure in 32 permanent forest plots of Kampong Thom, Cambodia. Philos Trans R Soc Lond B:Biol Sci 370:20140008
Tscharntke T, Clough Y, Wanger TC, Jackson L, Motzke I, Perfecto I, Vandermeer J, Whitbread A (2012) Global food security, biodiversity conservation and the future of agricultural intensification. Biol Conserv 151:53–59
Vaast P, Somarriba E (2014) Trade-offs between crop intensification and ecosystem services: the role of agroforestry in cocoa cultivation. Agroforest Syst 88:947–956
Vieira DLM, Holl KD, Peneireiro F (2009) Agro-Successional Restoration as a Strategy to Facilitate Tropical Forest Recovery. Restor Ecol 17:451–459
Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Evol Syst 33:475–505
Webb CO, Donoghue MJ (2005) Phylomatic: tree assembly for applied phylogenetics. Mol Ecol Notes 5:181–183
Wildi O (2013) Data analysis in vegetation ecology. Wiley-Blackwell, Chichester
Wood GAR, Lass RA (2001) Cocoa. Blackwell Science Ltd, Oxford
Zanne AE, Tank DC, Cornwell WK, Eastman JM, Smith SA, FitzJohn RG, McGlinn DJ, O'Meara BC, Moles AT, Reich PB, Royer DL, Soltis DE, Stevens PF, Westoby M, Wright IJ, Aarssen L, Bertin RI, Calaminus A, Govaerts R, Hemmings F, Leishman MR, Oleksyn J, Soltis PS, Swenson NG, Warman L, Beaulieu JM (2014) Three keys to the radiation of angiosperms into freezing environments. Nature 506(7486):89–92
Acknowledgments
We thank Domingos Folli and Jonacyr Souza for field assistence; and John Portress for preparation of Fig. 1. We thank C. Wheeler and one anonymous reviewer for helpful suggestions on manuscript. The views expressed in this document are those of the authors and do not necessarily reflect those of the United Nations Development Programme.
Author Contributions
SGR, MTN, JMLG performed the experiments; SGR analyzed the data; SGR, RHRS, GS, MTN, wrote and edited the manuscript.
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Rolim, S.G., Sambuichi, R.H.R., Schroth, G. et al. Recovery of Forest and Phylogenetic Structure in Abandoned Cocoa Agroforestry in the Atlantic Forest of Brazil. Environmental Management 59, 410–418 (2017). https://doi.org/10.1007/s00267-016-0800-5
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DOI: https://doi.org/10.1007/s00267-016-0800-5