Hum Ecol (2011) 39:455464 DOI 10.

1007/s10745-011-9412-0

Population Structure of Brazil Nut (Bertholletia excelsa, Lecythidaceae) Stands in Two Areas with Different Occupation Histories in the Brazilian Amazon
Ricardo Scoles & Rogrio Gribel

Published online: 8 June 2011 # Springer Science+Business Media, LLC 2011

Abstract Here we hypothesize that the intensity of disturbances caused by human activities in Brazil nut stands (castanhais) is positively related with the regeneration of Brazil nut trees (Bertholletia excelsa H.B.K., Lecythidaceae) and consequently with a younger population structure of this species. In order to test this hypothesis we compared the population structure of Brazil nut trees in two areas of the Brazilian Amazon with different histories of land usage by humans. Archeological and historical data suggest that the region surrounding the Trombetas River was densely occupied in pre-Columbian times and experienced depopulation after European contact with Amerindian populations, especially in the 16th century. The 25 Brazil nut stands sampled in this region were dominated by old B. excelsa trees and had scarce recruitment in the understory. These very mature stands likely owe their origins to the interval between the depopulation of the indigenous peoples in the 16th17th centuries and the establishment of quilombos at the beginning of the 19th century. The second study area was in

the vicinity of the Madeira River (Capan Grande Lake), where the castanhais were more accessible and disturbed. In this site, a younger population structure and abundant regeneration of B. excelsa were observed in the 10 sampled stands. Historical data from this region indicate that indigenous populations were replaced gradually beginning in the 18th century, with no evidence of severe depopulation. We suggest that the different historical and contemporary land use patterns contributed to the current contrasting population structures of the castanhais at the two locations. The data also support the idea that the castanhais, even the ones considered to be pristine and native forests, result from anthropogenic influences. We found no evidence to support restrictions on seed harvesting as a means to improve regeneration rates of Brazil nut stands. Keywords Amazonia . Anthropogenic forest . Extractivism . Historical ecology . Regeneration . Brazil nut

Introduction
R. Scoles Universidade Federal do Oeste do Par, Rua Marechal Rondon s/n. CEP , 68040-070 Santarm, Par, Brasil e-mail: ricardscoles@yahoo.es R. Gribel (*) Coordenao de Pesquisas em Botnica, Instituto Nacional de Pesquisas da Amaznia (INPA), Manaus, AM, Brazil e-mail: rgribel@jbrj.gov.br Present Address: R. Gribel Diretoria de Pesquisas, Instituto de Pesquisas do Jardim Botnico do Rio de Janeiro, Rio de Janeiro, RJ, Brazil

One of the most important economic non-timber forest products of the Amazon region is the Brazil nut (Bertholletia excelsa H.B.K., Lecythidaceae). Stands of Brazil nut trees, commonly known as castanhais, are aggregations of hundreds to a few thousand trees in the upland (terra firme) Amazon forest. The castanhais are long thought to owe their origin to the pre-Colombian Amerindians (Ducke 1946; Bale 1989; Mori and Prance 1990). However, there is no clear historical or ecological evidence of a long-term human influence on the regeneration or population structure of the castanhais. The clumped distribution and the abundance of unusual size classes of B. excelsa have generated discussions concerning the reasons for these characteristics. For example,

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it is possible that openings in the forest created by Amerindian activities permitted the germination of many seeds that later became a stand (Mori and Prance 1990; Salomo 1991). On the other hand, agoutis, considered the sole natural seed dispersers of B. excelsa, may have gathered and stored seeds in middens (Tuck Haugaasen et al. 2010) that were later forgotten. The stored seeds may have germinated, forming stands (Peres and Baider 1997). The physical proximity of the castanhais to areas with dark earths and archaeological sites suggests that the Amerindian peoples were influential in determining their current pattern of distribution and abundance (Mller et al. 1980; Mller 1981; Posey 1985; Bale 1989; Clement et al. 2010). The difficulty of naturally dispersing the large, heavy fruit also favors this hypothesis. If this view is correct, then Brazil nut stands may be anthropogenic rather than having natural origins (Posey 1984, 1985, 1986, 1990; Anderson and Posey 1987; Bale 1989). If humans are major actors in the geographical distribution and stand creation of Brazil nuts, the relative roles of agoutis and humans in the castanhais maintenance and structuring at local scale remain poorly understood, as is the question of human intention. Humans collect and open fruits in the forest and then transport sacks or baskets of Brazil nut seeds for use and sale. Seeds occasionally fall during the fruit opening and transport, affording a dispersal opportunity if the seed germinates and grows in a favorable location. For example, forest clearings made by humans may provide the preferred environment for seed germination, seedling establishment and sapling development. Unfortunately, records of the active planting of Brazil nut trees by Amerindians are rare, possibly because of the long period required for seed germination (several months). Here we examine and compare the population structure of two sets of Brazil nut stands near communities in the Brazilian Amazon. These two areas are distant from one another and have different patterns of historical occupation and contemporaneous use. We examine whether evidence supports the hypothesis that the population structure of B. excelsa trees in the castanhais is due to human activities. We hypothesize that disturbances caused by continuous human activities in the forests, such as selective timber extraction, collection of nontimber products, understory openings, and eventual fires, increase the regeneration rate of the B. excelsa stands and shift them toward a younger population structure. The Species Bertholletia excelsa is widely distributed in non-flooded forests (terra firme) in the Amazon and Guiana Shield, from 14 S to 5 N (Mori and Prance 1990). The species is found in areas with 1,4002,800 mm of annual rainfall, 24

27C mean annual temperature and an average relative humidity from 79% to 86% (Diniz and Bastos 1974). The tree is emergent, reaching up to 50 m in height and a diameter at breast height (DBH) of >300 cm (Zuidema and Boot 2002; Salomo 2009). The trunk is straight, with no branches until near the top. The canopy is formed of wellspaced branches and may reach up to 50 m in diameter. The fruit, which contains the Brazil nut, is woody, indehiscent, and spherical; it weighs 5002,500 g and has a diameter of >10 cm. This woody fruit holds 1025 seeds that are edible after removal of the woody protective tegument (Mori and Prance 1990). The agouti (Dasyprocta spp.) is thought to be the sole important disperser of its seeds (Huber 1910; Ortiz 1995, 2002; Peres and Baider 1997; Tuck Haugaasen et al. 2010). Most reproductive Brazil nut trees are greater than 40 cm DBH, and the most productive trees are 80160 cm DBH (Viana et al. 1998; Zuidema and Boot 2002). Trees may live for hundreds of years in terra firme forests, and the adults have high survival rates (Zuidema and Boot 2002). Brazil nut populations often contain 75150 trees of >10 cm DBH (Peres and Baider 1997), with stands of relatively high densities for humid tropical forests (520 trees ha1) mixed with areas of low density (0.2 trees ha1 (Mori and Prance 1990)). Studies of the population structure of B. excelsa have found few trees >10 cm DBH that are not reproductive (Salomo 1991; Nepstad et al. 1992; DHV 1993). Populations are typically dominated by intermediate-sized trees (Zuidema and Boot 2002; Peres et al. 2003; Salomo 2009). Bertholletia excelsa is heliophytic (Salomo 1991; Scoles 2010) and depends on clearings for growth as well as the survival of seedlings and saplings (Mori and Prance 1990; Viana et al. 1998; Myers et al. 2000; Oliveira 2000). Plants appear in clearings as if they were pioneer species, but, unlike pioneers, they remain after the forest has grown into more advanced successional stages. For this reason, the species is considered to be a long-lived pioneer tree (Swaine and Hall 1987; Zuidema 2003). Many experimental studies have shown that Brazil nut trees grow best in well-lighted open areas (Fernandes and Alencar 1993; Yared et al. 1993; Tonini et al. 2008) and that growth is much slower in forest shade in the understory layer (Kainer et al. 1998; Myers et al. 2000; Pea-Claros et al. 2002; Scoles 2010). Study Areas The population structure was studied at two distinct sites: 1) Trombetas River (hereafter Trombetas), on the northern side of the Amazon River, near Oriximin and Obidos in the state of Par, Brazil; and 2) Capan Grande Lake (hereafter Capan Grande) on the Madeira River, near Manicor on the southern side of the river in the state of Amazonas, Brazil. These two areas are 800 km from each other (Fig. 1).

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Fig. 1 Map showing study areas within the Brazilian Amazon and the location of the sampled Bertholletia excelsa stands

The sampled castanhais in Trombetas are in conservation areas, the Rio Trombetas Biological Reserve, the SacarTaquera National Forest, the recently created Rio Trombetas State Reserve, and in Quilombola Territories. The Quilombola Territories were originally areas to which African slaves fled from their owners, but they have now become semiautonomous communities. The Quilombola areas in this study are on the Trombetas and Erepecuru Rivers, which are administered by the Remaining Quilombo Community Association of Oriximin (ARQMO). The castanhais in Capan Grande all occur within the Lake Capan Grande Extractive Reserve, which is a direct-use conservation unit co-governed by the riparian communities of the lake and the Chico Mendes Institute for the Conservation of Biodiversity (ICMBio). At Capan Grande, sampling units are located near each other (116 km apart) on the plateaus near the lake and the communities (1008,750 m). At Trombetas, the sampled castanhais extend over the Trombetas River and its western tributaries watersheds. Most sampling units are >10 km apart from the communities, and more than a third are difficult to reach due to topography and obstacles, such as river rapids and ravines. At Trombetas, the greatest distance between two sampling units is 112 km. In both areas, the climate is tropical, humid, and has a short dry season with <100 mm rainfall month1. Annual rainfall varies from 2000 to 2500 mm, temperature varies from 24 to 26C, and relative humidity is normally >80%

(Brasil 1979; SUDAM 1984). In Manicor, January to March is usually the rainiest period (monthly rainfall ~300 mm), and only July and August may be considered dry months (AGRITEMPO 2009). At Trombetas, rainfall is highest from MarchMay, and the dry season runs from AugustNovember (IBAMA 2004). In both regions, the Brazil nut stands occur in areas with yellow or yellowish red latosoils which are the predominant soil types associated to terra firme forest in the lower stretches of the Trombetas and Madeira rivers (IBGE 2006). Amerindian occupation and use differ between the two study areas. The lower Amazon lost most of its native population during the first two centuries of colonization (c. 15001700). By the early eighteenth century a large part of the Amerindian population had succumbed to massacre and epidemics. The remaining Amerindians fled to less-accessible areas. For example, in Trombetas, they went upstream above the rapids and waterfalls of the Trombetas, Cachorro, Mapuera, Acapu and Erepecuru Rivers. This period was followed by the slow repopulation of the area by neo-indigenous people who had been uprooted from their original homes and cultures and were incorporated into Brazilian society by religious missionaries (Porro 1992). During the 1800s, African slaves and their descendents fled the towns and farms of the state of Gro-Par and established quilombos in the middle and upper regions of the Trombetas and Erepecuru Rivers. The inhabitants descended to lower regions when

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slavery was finally abolished (1886) and commercial trade in extractive products, such as Brazil nuts and timber expanded (Acevedo and Castro 1998). Since approximately 1850, the quilombo communities have dominated the lower and middle regions of the Trombetas and Erepecuru Rivers, while the indigenous peoples have remained along the upper regions of these rivers. The colonial occupation of the Madeira River occurred later, during the 1800s, with the creation of the states of Amazonas (1850) and the rubber boom. Previous incursions of colonists were temporary and limited to extractive commerce and Jesuit missions (Menndez 1992). In the 1700s, the government, fearing that the Madeira River would serve as a route for contraband metals from the states of Minas Gerais and Gois, prohibited river navigation (in 1733) and spread rumors of dangerous Indians, such as the Mura, along the river margins (Amoroso 1992). This strategy deferred more intense contact between the colonists and the Amerindians. Expansion of extractive commerce during the latter half of the 1800s marked the beginning of the colonization of the Madeira River that would give rise to a society of mostly rural, mixed-race (caboclo) communities, which endure today.

80 cm), productive adults (80160 cm), mature adults (160200 cm), and old adults (>200 cm) (Viana et al. 1998; Zuidema and Boot 2002). Plants less than 10 cm were divided into two groups based on the presence of endosperm. If present, the plant was considered a seedling; if absent (absorbed), the plant was a sapling (Myers et al. 2000; Zuidema and Boot 2002). Canopy Openness The openness of the canopy was measured photographically (Engelbrecht and Herz 2001). A 19-mm wide-angle lens was used on a Ricoh GX100 camera. Pictures were taken at 130 cm above the ground using a tripod and with the camera pointed at the zenith. Pictures were taken early in the morning or late in the afternoon to avoid direct sunlight. One photograph was taken from a random location within each of the 50-m sections of the transects for a total of 20 photos per transect (Nicotra et al. 1999). Digital images were analyzed with Miramn 6.0, a program that counts pixels and then calculates the percentage of white pixels in all pixels in the photo. The calculated percentage was then considered the index of canopy openness. Data Analysis

Methods Data were gathered over three years at Trombetas (2007 2009) and one year at Capan Grande (2008). A total of 25 (125 ha) transects of 501,000 m were established within stands of Brazil nut trees at the Trombetas River and 10 (49 ha) at Capan Grande, the latter with one shorter transect (800 m) due to spatial limitations. In each transect, 10 plots of 1025 m, randomly placed at 100-m intervals, were established to measure smaller trees (<10 cm DBH). Within each plot, we identified all B. excelsa individuals >10 cm DBH and noted their coordinates within the transect. We measured the DBH (cm) and the diameter of the canopy (as twice the length of the longest branch and the next longest branch approximately perpendicular to the first (m)), and estimated tree height (m). When the canopy was irregular, we applied a conversion factor to adjust the area estimated in quadrants. For example, if the canopy was irregular because it had a particularly sparse or empty quadrant, we multiplied by 0.75; if another quadrant was missing, we multiplied it by 0.50; if most of the canopy was absent, we multiplied by 0.25. We also collected data on smaller Brazil nut trees (<10 DBH) in the 10 plots. We measured spatial coordinates, tree height, the DBH of all saplings >1.3 m in height, and the diameter at the ground for smaller saplings. Trees were placed in classes to facilitate analysis. Classes were young (1040 cm DBH), young adults (40 Experiments in the classical sense are generally impossible to apply on a large regional scale. The two historical situations compared here cannot be replicated over the Amazon. As a consequence, the 25 plots in Trombetas and the 10 plots at Capan Grande cannot be considered as independent replications used in classical experimentation; they must instead be technically classified as spatial pseudo-replications (Hurlbert 1984). Because of that, we did not use inferential statistics to compare the two treatments in this unreplicated natural experiment and our comparisons and conclusions, therefore, are of an inferential and inductive nature.

Results Patterns of Population Structure The large basal area (10.4 and 7.1 m2 ha1) and the high proportion of the canopy occupied by Brazil nut trees (29% and 34%) in Trombetas and Capan Grande, respectively, indicate that this species is dominant in both areas, and the forests can be classified as monodominant or oligarchic (i.e., dominated by one or a few species, Peters et al. 1989; Campbell et al. 2006). However, size distributions of the B. excelsa trees contrast greatly in the two areas, with intermediate to large sizes dominating at Trombetas and smaller sizes (<80 cm DBH) at Capan Grande (Fig. 2). Tree

Hum Ecol (2011) 39:455464 Fig. 2 Distribution of Brazil nut densities in 10 cm size class intervals at Trombetas (filled bars) and Capan Grande (white bars)
1,6

459

n=609 1,2 n=850

Density (tree ha-1)

0,8

0,4

0,0 10 30 50 70 90 110 130 150 170 190 210 230 250 270 >300

height was on average 3 m greater at Trombetas than in Capan Grande. Tree density was lower and the trees were older at Trombetas, with only 7% of trees too young to reproduce (Table 1). At Trombetas, most trees were in the 80160 cm DBH range, whereas at Capan Grande, most trees were <100 cm DBH (76%), and approximately 26% were not reproductive (DBH 1040 cm). The distribution of tree sizes at Capan Grande was asymmetric, favoring small sizes (Fig. 2). At Capan Grande, the most productive trees (80160 cm DBH) were less well represented in the total population than at Trombetas, even though their absolute density was greater (4.5 versus 3.7 trees ha1). The density of trees <130 cm
Table 1 Comparative analysis of population structure (means standard deviation, if%, maximum and minimum) of B. excelsa in two regions of Brazilian Amazon: Trombetas River Region (Oriximin, Obidos, PA) and Capan Grande Lake (Manicor, AM)

DBH was higher at Capan Grande, and the density of trees >130 cm DBH was higher at Trombetas (Fig. 2). Capan Grande thus exhibited a younger population structure, with few trees >160 cm DBH (4%). At Trombetas, 27% of trees were >160 cm DBH, and 10% of trees were old adults (DBH>200 cm, Fig. 3). Old adult trees were almost absent at Capan Grande (1%). At Trombetas, three trees were >300 cm DBH, whereas the largest tree at Capan Grande had a DBH of 267 cm. Recruitment and regeneration were much greater at Capan Grande than at Trombetas (Table 1). Recruitment was estimated by seedling density and regeneration by seedling, sapling and juveniles densities. Recruitment is thus a subset

Parameter Tree Density DBH>10 (tree ha1) Tree Density DBH>40 cm (tree ha1) Tree Density DBH 1040 cm (tree ha1) Seedlings ha1 Saplings ha1 % juveniles (DBH 1040/DBH>10) Seedlings adult1 Saplings adult1 Juveniles adult1 Tree DBH (cm) Trunk height (m) Basal area (m2 ha1) Crown area (m2 ha1) Occupation canopy forest (%) Mean Canopy Opening (%) Proportion of canopy gap forest (>20% canopy opening)

Trombetas River 6.84.1 6.33.9 0.50.8 4.88.7 1.03.1 7 (0.0, 33) 1.02.2 0.10.4 0.10.1 128.555.5 22.54.9 10.45.6 2.8651.250 28.7 (11.8, 51.3) 6.5 (49.5, 1.9) 0.01

Capan Grande 12.57.8 9.24.7 3.23.4 24.819.9 4.45.3 18 (0, 41) 2.91.9 0,50.6 0.30.2 73.144.2 19.24.0 7.12.5 3.3851.351 33.8 (7.2, 51.0) 6.6 (2.3, 30.1) 0.02

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Fig. 3 Ancient Brazil nut tree at Trombetas river region with >2 m DBH

of and an indicator of potential regeneration. The seedling density at Trombetas (mean 4.6 seedlings ha1) was five times lower than at Capan Grande (24.4 ha1). Similarly, the density of saplings (1.0 and 4.4 saplings ha1 at Trombetas and Capan Grande respectively) and juvenile trees (0.5 and 3.2 juveniles ha1 respectively) were also much lower at Trombetas. Both regions have very shaded understories with only 6 7% light entrance. At Capan Grande, however, there were more small clearings (2% of total ground area with>20% light) than in Trombetas (1%) (Table 1). Canopy openings with 1020% light entrance were twice as common at Capan Grande, and thus the probability of light reaching the forest floor was higher in Capan Grande.

Discussion In the Amazon basin, the density of Brazil nut trees varies from 1 to 23 trees ha1. The density of B. excelsa at Capan Grande (12.5 trees.ha1) is thus among the highest recorded in studies for this species in the Amazon, with the exception of stands in Cajari, Amap state, Brazil (Table 2). In other studies of castanhais, size class distributions are usually more similar to that found at Trombetas, with frequencies being greatest in intermediate classes (Zuidema
Table 2 Comparison of Brazil nut tree density (>10 cm DBH) in different regions of the Amazon basin, by increasing order of density

2003). This trend was found also in Bolivia (DHV 1993; Zuidema and Boot 2002), in the Brazilian state of Par (Salomo 1991, 2009) and in most of the studies examined in the meta-analysis carried out by Peres et al. (2003). The castanhais at Capan Grande are in other ways strikingly different, with a distribution strongly skewed to the left, favoring trees with DBH<80 cm (Fig. 2). While this pattern is atypical, it is not unknown in the Amazon. At Nova Esperana, Xapuri (in the state of Acre), 58% of Brazil nut trees have <80 cm DBH. At the Chico Mendes Extractive Reserve in Acre, ~60% of trees have <100 cm DBH (Wadt et al. 2005). Interestingly, on the Madeira River, those castanhais that are farthest from communities tend to have size distributions similar to that of the stands at Trombetas (Scoles 2010). At Capan Grande, trees tended to be smaller (mean DBH=73 cm) than at Trombetas (129 cm), which indicates a younger population at the former location. Populations of B. excelsa in the Amazon, like that of Trombetas, usually have an average DBH >100 cm (Peres et al. 2003). Conversely, stands closer to Amerindian or Extractive Reserves or that are known to be persistently used by local communities tend to have an average DBH similar to that of Capan Grande. For example, mean DBH at the Pinkaiti Indigenous Area in Par was 734 cm; at Nova Esperana, Acre, it was 744 cm, and at the Chico Mendes Extractive Reserve, Acre, it was measured 865 cm (Peres et al. 2003; Wadt et al. 2005). Seedling density at Trombetas (mean, 4.6 seedlings ha1) is the lowest published to date (Baider 2000; Zuidema and Boot 2002; Zuidema 2003; Wadt et al. 2008). The ratio of seedlings to adults is also the lowest reported to date in the literature. In contrast, seedling density at Capan Grande (24.4 ha1) is similar to densities reported elsewhere [29.8 ha1, Baider (2000) in Para; 3052 ha1, Zuidema (2003) in Bolivia]. Thus, the castanhais at Capan Grande seem to have a greater regenerative capacity than those at Trombetas because of the much higher density of juveniles, saplings, and seedlings. Castanhais in Capan Grande are intermediate in terms of regeneration (18% young), which is within the range of 152% found in other areas (Peres et al. 2003). Yet, that percentage increases inversely with distance from
Area (ha) 12 28.5 203.7 125 22.6 49 Density 1.7 4.8 5.6 6.8 12.2 12.5 Source Zuidema and Boot (2002) Peres and Baider (1997) Salomo (2009) This study Baider (2000) This study

Location Forest Reserve El Tigre, Beni, Bolvia Indigenous Area Pinkaiti, Par State, Brazil Sarac-Taquera Forest, Par State, Brazil River Trombetas Region, Par State, Brazil Cajari, Amap State, Brazil Lake Capan Grande, Amazonas State, Brazil

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communities; closer castanhais have 2140% young plants (in comparison to the usual 18%) and are similar to studied areas that have the greatest proportion of non-reproductive trees. This regeneration trend found in the Capan Grande area is clearly contrary to the conclusions of Peres et al. (2003), which postulated that more persistently harvested castanhais exhibited poor regeneration and that these intensely exploited populations may eventually succumb to recruitment bottleneck. The entirety of the population structure parameters found here shows that Brazil nut stands are younger and have greater regeneration potential at Capan Grande. In Trombetas, the canopy was more closed and higher, and the stand contained less-dense, older trees. What are the most likely explanations for differences in the population structure between the two areas? Although climate, soils and other abiotic factors may have some unmeasured importance, we believe that two anthropic factors seem most likely to explain these different patterns. The first relates to the current trends in occupancy and use of the castanhais, and the second relates to their historical occupation. At Trombetas, the castanhais are less often visited by local people. This pattern is certainly due to the greater distance of the stands from the communities, and thus the trees are only visited during harvesting (4 month yr1). In addition, at Trombetas, many of the castanhais are near rapids that must be crossed by canoe or in steep and difficult terrain. Thus, gathering and transporting the harvest is much more difficult. Additionally, staging sites for transport are often very far from where seeds are harvested. As a result, the product must be carried over relatively great distances. Finally, legal regulations restrict access to harvesting periods in 60% of the area within the Biological Reserve of Rio Trombetas. In the ten castanhais within the domain of the quilombos territories, people tend not to visit the stands outside of the harvest season due to limited accessibility. The situation is very different at Capan Grande, where castanhais are near the communities. Comparatively, these stands are much more accessible, and collection and transport of Brazil nuts is easier. Several stands are near small rivers that can be used during high water. Aside from Brazil nut collection, other extractive activities occur when Brazil nuts are not being harvested, including rubber tapping, fruit collection, collection of fiber from vines and tree barks, and timber exploitation. Also, many stands are in forest fragments that are separated by land used for agriculture. This fragmentation increases the availability of light in the understory and creates edge effects and other perturbations. Despite the similarity of average light levels in the two forests, the distribution of light is very different because more openings are found at Capan Grande.

In other studies in the southwestern Amazon, the size distribution (i.e., a large proportion of young trees, average 7080 cm DBH) is similar to that at Capan Grande but has a lower total tree density (Viana et al. 1998; Wadt et al. 2005). In other stands, seedlings are always present despite the low density of reproductive trees (Viana et al. 1998; Zuidema and Boot 2002; Wadt et al. 2005). The presence of younger plants of B. excelsa is usually attributed to open forests with plenty of light, as compared to closed, denser forests where light may be limiting (IBGE 2004; Wadt et al. 2005). Hence, this mechanism may explain recruitment in our study area at Capan Grande, where human activities and settlements have opened the forest, in comparison with Trombetas. The history of occupation is also very different in the two study areas and may explain the contrasting population structures of the B. excelsa stands. The TrombetasErepecuru watershed is a region particularly rich in archaeological sites (Magalhaes 2007), black earths (Kern and Kmpf 1989), pottery (Hilbert 1955), and rock paintings (Pereira 2003; Pereira et al. 2009). These archaeological findings suggest that this region probably supported dense Amerindian populations and, consequently, experienced extensive forest disturbance during pre-Columbian times. It is quite likely that the Brazil nut, which grows well in disturbed areas, was favored by the slash-and-burn agriculture of the pre-Colombian societies (Posey 1984, 1986, 1990; Peters 2000; Roosevelt 2000; Campbell et al. 2006). It is notable that a tree-ring study of 22 Brazil nut trees (87145 cm DBH) from the Trombetas region measured ages from 228 to 502 years (Schngart et al. unpublished data). These data suggest that the biggest trees found in the Trombetas area, those with DBH >300 cm, may reach ages of 600 years or more. Interestingly, the estimated age of the majority of the Brazil nut trees in this study was between 300 and 450 years, which probably coincides with a period of depopulation of the Amerindian people following European contact, especially along the lower and middle stretches of the main rivers (Porro 1992). The current population structure of B. excelsa likely owes its origins to the interval between land abandonment due to Amerindian depopulation (sixteenth-seventeenth centuries) and the establishment of the quilombos (nineteenth century). Thus, it appears that the abandonment of the Trombetas area resulted in the development of the current B. excelsa population structure, with a high proportion of old trees and scarce regeneration. In contrast, Capan Grande likely owes the formation of its castanhais to the growth in human presence that intensified in the late nineteenth century, following colonization of the Madeira River and the beginning of the rubber boom. This timing may explain the domination of trees <80 cm DBH (which are approximately 150 years old (Zuidema and Boot

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2002)) in this population. The early riverine communities were probably established around existing stands of rubber (Hevea brasiliensis) and Brazil nut trees, which would have then favored the rejuvenation of the castanhais as previously described. Therefore, we hypothesize that when native Amazonian populations were decimated post-conquest in the Trombetas, forest disturbance was reduced, allowing for the shift in demography toward over-mature stands. Those human populations in Trombetas never fully recovered; rather, they were replaced by low-density black and caboclo populations, each with different subsistence strategies. In the Madeira, the decimation occurred later, and the Amerindian replacement by caboclos was more gradual and complete. The Madeira region probably recovered preconquest population densities, whereas the Trombetas most likely did not. The contemporaneous stands in Capan Grande probably have a younger population profile, not only because the castanhais are expanding but also because tree death is higher due to the more intensive use of fire and other disturbances in the landscape. Forests once considered primary and pristine, such as the native castanhais in Trombetas, are now being recognized as regenerated forests that have recovered after the abandonment of lands that were previously used for agriculture. In tropical America, Africa and Asia, areas that were once considered virgin or pristine have been discovered to have been occupied and significantly perturbed by earlier human settlements that, once abandoned, allowed forests to regrow (Willis et al. 2004). In tropical Latin America, many monodominant forests are the consequence of management and manipulation of the original forests by pre-Colombian and subsequent societies (Anderson 1990; Peters 2000; Campbell et al. 2006). Today, it is thought that the occurrence of many high-density stands of fruit trees, monospecific stands of palms, and other anthropogenic forests are evidence that at least 11% of the Brazilian Amazon was anthropogenically modified (Bale 1989). Here, we suggest that the differences in the population structures of the Brazil nut stands in Trombetas and Capan Grande may be a consequence of pre- and postcolonial human occupation and manipulation of the forest. Confirmation of this hypothesis will require archaeological studies which would improve understanding of the impact of Amerindians on pre-colonial tropical forests. The Brazil nut stands at Capan Grande exhibit a younger structure likely due to more recent human perturbations. In contrast, at the Trombetas River, trees are older, and the current recruitment is much lower. The lower recruitment is in part due to the greater density of big trees (and the consequent low-light conditions in the understory for the past several centuries) and in part due to few recent perturbations.

Regeneration of the heliophytic, long-lived Brazil nut is therefore likely to be most influenced by ecological factors that allow light to reach the understory, such as lowintensity forest disturbances mediated by humans. In addition, the ages of the stands and population structure indicate a history of human influence, both old (precolonization) and recent (post-colonization). Hence, we suggest that these stands are anthropogenic forests that are distinctly influenced by humans. Finally, we found no scientific evidence that there should be restrictions on seed harvesting as a means to improve regeneration rates of the Brazil nut stands.
Acknowledgments We thank the Protected Areas Program of the Chico Mendes Institute for Biodiversity Conservation (ICMBio), the National Council for Scientific and Technological Development (CNPq), the Scholarship Program of the International Education Institution of Brazil (IIEB), the Brazil Nut Germplasm Bank project of the National Institute for Amazonian Research (INPA), the Minerao Rio do Norte Company (MRN), and the Chico Mendes Biodiversity Institute (ICMBio) for their logistical and financial support. We sincerely thank the team of ICMBio at Porto Trombetas and Manicor for their collaboration and logistical support during field work, especially Gilmar N. Klein, Altemar Lopes Silva, Vivian Mara Uhlig and V almir Raimundo Lopes da Silva. Thanks to Paulo M. Alencastro and to Carlos Palacio for the map, Charles Clement and Andr Junqueira for the literature on historical ecology and helpful discussions, David Bertran for suggestions for the analyses, Jochen Schngart for the data on the tree-ring studies, and James J. Roper and Maristerra R. Lemes for constructive comments on the manuscript. Our heartfelt thanks go to all the families of the communities that were involved in this project. Research Grant to RG was provided for CNPq.

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