Secondary Forests on Anthropogenic Soils in Brazilian Amazonia Conserve Agrobiodiversity

Biodivers Conserv DOI 10.1007/s10531-010-9813-1 ORIGINAL PAPER Secondary forests on anthropogenic soils in Brazilian Amazonia conserve agrobiodiversity Andre´ Braga Junqueira • Glenn Harvey Shepard Jr. • Charles R. Clement Received: 3 July 2009 / Accepted: 13 February 2010 Ó Springer Science+Business Media B.V. 2010 Abstract Throughout Brazilian Amazonia anthropogenic soils that are the product of pre-Columbian settlements are called Terra Preta de Ińdio (Indian Dark Earths, TPI). These soils are dramatically different from surrounding soils due to long-term human activity, but there is little information about how secondary forest succession is affected by these differences. We tested if community structure (density, richness and basal area), floristic composition and domesticated species’ richness and density were similar between TPI and non-anthropogenic soils (NAS) in 52 25 9 10 m secondary forest plots in different successional stages near three traditional communities along the middle Madeira River, Central Amazonia. We sampled 858 woody individuals on TPI (77 domesticated) and 1095 on NAS (27 domesticated); 550 understory palms on TPI (169 domesticated) and 778 on NAS (123 domesticated). We found 179 species on TPI (10 domesticated), 190 on NAS (8 domesticated), and 74 (25%) in both environments. Although community structure on TPI and NAS was fairly similar, they showed significantly distinctive floristic composi- tions, both for woody individuals and understory palms. The density and richness of domesticated species was significantly higher on TPI than on NAS for woody individuals, but not for palms. The intimate long-term association of TPI with human activity has lead to the formation of distinct secondary forests and has favored the concentration of domesticated populations of crop species. Hence, secondary forests on anthropogenic soils concentrate agrobiodiversity, offering advantages for in situ conservation of genetic resources, and are unique ecosystems that should be considered in conservation efforts. A. B. Junqueira (&) Á C. R. Clement Coordenaçaõ de Pesquisas em Cieˆncias Agronoˆmicas, Instituto Nacional de Pesquisas da Amazoˆnia, Avenida Andre´ Arau´jo, 2936, Manaus, Amazonas 69060-001, Brazil e-mail: [email protected] C. R. Clement e-mail: [email protected] G. H. Shepard Jr. Departamento de Antropologia, Museu Paraense Emı´lio Goeldi, Avenida Perimetral 1901, Bele´m, Para´ 66077-830, Brazil e-mail: [email protected] 123 Biodivers Conserv Keywords Community structure Á Amazonian dark earths Á Plant domestication Á Secondary succession Á Succession management Á Traditional resource management Abbreviations ANCOVA Analysis of covariance EMBRAPA (Empresa Brasileira The Portuguese acronym for the Brazilian de Pesquisa Agropecua´ria) Agricultural Research Corporation) IBGE (Instituto Brasileiro The Portuguese acronym for the Brazilian Institute de Geografia e Estatı´stica) of geography and statistics INPA (Instituto Nacional The Portuguese acronym for the National Research de Pesquisas da Amazoˆnia) Institute for Amazonia IUSS International Union of Soil Science. LTSP/INPA (Laborato´rio Tema´tico the Portuguese acronym for the Soil and Plant de Solos e Plantas) Thematic Laboratory of INPA MANOVA Multivariate analysis of variance NAS Non-anthropogenic soils. NMDS Non-metric multidimensional scaling PCA Principal components analysis TPI (Terra Preta de Ińdio) The Portuguese acronym for Indian black earths, also called Indian dark earths and Amazonian dark earths Introduction Throughout Brazilian Amazonia anthropogenic soils associated with pre-Columbian indigenous settlements are called Terra Preta de Ińdio (Indian Dark Earths, hereafter TPI; Woods and Denevan 2009). TPI is widely distributed in Amazonia, occurring in patches that may vary from a single hectare to hundreds of hectares (Smith 1980). TPI patches are especially common in Brazilian Amazonia (Sombroek et al. 2002), but they occur also in Colombia, Peru, Venezuela and the Guianas (Eden et al. 1984; Andrade 1986). Most TPI patches were formed between 500 and 2,500 years ago (Neves et al. 2003), but the specific cultural and ecological processes that created these soils are still poorly understood and are the focus of an intense, multidisciplinary scientific effort (Woods and Denevan 2009). Although edaphic conditions can be highly variable among different TPI patches (Falcaõ et al. 2009), a few properties are common to almost all of them when compared to adjacent soils: higher levels of phosphorous, calcium, organic matter, pH and cation exchange capacity (Lehmann et al. 2003a). These characteristics make these soils more suitable for agriculture than other upland (i.e., non-flooded) Amazonian soils (Glaser 2007), which generally have low fertility and soil organic matter contents (Chauvel et al. 1987; Lehmann et al. 2003a). For this reason, TPI is frequently associated with specific and more intensive forms of agriculture (German 2003a, b; Fraser and Clement 2008; Fraser et al. 2009), although fallows are still an important part of the agricultural systems. There are suggestions that the secondary forest succession on TPI occurs differently than on other upland soils (Clement et al. 2003). Early successional stages on TPI showed a higher percentage of soil coverage by new weeds, higher weed species richness, and a higher relative proportion of annual and leguminous plants when compared with adjacent non-anthropogenic soils (Major et al. 2005). When abandoned, swiddens on TPI are 123 Biodivers Conserv colonized by a characteristic group of aggressive weeds, including several species typically associated with human-disturbed environments (Major et al. 2005). Local farmers recognize diverse stages of forest regrowth on TPI through indicator plant species, even when vegetation is dense (Moran 1981; Sombroek et al. 2002; German 2003b). Farmers also recognize vegetation structural characteristics associated with TPI, such as lower canopies and denser understories (Woods and McCann 1999), smaller average diameter of adult trees, and a greater abundance of vines and plants with spines (German 2003b). In the Xingu River basin, the proximity to TPI patches was identified as one of the factors determining the occurrence of secondary forests dominated by lianas (Baleé and Campbell 1990). Preliminary observations by Samuel Almeida and colleagues (Clement et al. 2009) indicate that old-growth forests [at least 300 years old (Kern 1996)] on TPI at Caxiuana˜ (Para´, Brazil) show differences in forest structure and species composition when compared to old-growth forests on non-anthropogenic soils. On the other hand, Paz-Rivera and Putz (2009) found few differences in the density of 17 useful tree species when comparing old secondary forests (at least 140 years old, probably much older) on anthropogenic and non- anthropogenic soils in a lowland forest in Bolivia. However, these authors suggested that on anthropogenic soils large individuals of long-lived species may be remnants of ancient cultivation (Paz-Rivera and Putz 2009). Still, apart from the experimental study of Major et al. (2005), the preliminary observations by Samuel Almeida and colleagues (Clement et al. 2009) and the quantitative ‘‘useful-species-focused’’ approach of Paz-Rivera and Putz (2009), all other observations are derived from qualitative and ethnographic data, and lack more detailed ecological investigation to be validated. Clement et al. (2003) raised the hypothesis that TPI could act as agrobiodiversity reservoirs, areas that concentrate considerable genetic diversity of native and exotic species with domesticated populations due to TPI’s long-term association with human activity. There is a growing need to locate areas of high diversity of crop wild relatives, which may or may not also be areas of high landrace diversity, in order to propose adequate conservation strategies for these areas (Maxted et al. 2008). We used an ecological approach to test the hypothesis that secondary forests on TPI concentrate agrobiodiversity, predicting that these environments would show a greater abundance and richness of species with domesticated populations when compared to adjacent secondary forests on non-anthropogenic soils. This is the first study that addressed the question of secondary succession on TPI. We compared secondary forests in several successional stages on TPI and nearby non- anthropogenic soils (hereafter NAS) with regards to forest structure (density, species richness and basal area) and species composition. We also identified TPI indicator species and tested the hypothesis that secondary forests on TPI concentrate agrobiodiversity. Methods Study site The study was carried out in three riverside communities located in the municipality of Manicore´, on the middle Madeira River, Amazonas state, Brazil: A´ gua Azul (5°490 5700S; 61°3305600W); Barreira do Capana˜ (5°5005100S; 61°4001100W); and Terra Preta do Atininga (5°3801900S; 61°30600W; Fig. 1). The local climate is characterized as Af in the Ko¨ppen system, with mean annual temperatures between 27 and 28°C, and a main annual rainfall of about 2,500 mm, with a marked dry season from June to September. The natural vegetation 123 Biodivers Conserv Fig. 1 Location of study sites. White triangles represent the three communities where plots for secondary forest sampling were established, and the white circle indicates the town of Manicore´, located along the middle Madeira River, Amazonas, Brazil of the region is composed mainly

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