human ecology - scoles & gribel_2011 (1)

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Population Structure of Brazil Nut ( Bertholletia excelsa,

Lecythidaceae) Stands in Two Areas with Different

Occupation Histories in the Brazilian Amazon

Ricardo Scoles & Rogério Gribel

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

Abstract Here we hypothesize that the intensity of distur-

bances 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 thisspecies. In order to test this hypothesis we compared the

population structure of Brazil nut trees in two areas of theBrazilian Amazon with different histories of land usage byhumans. Archeological and historical data suggest that theregion surrounding the Trombetas River was denselyoccupied in pre-Columbian times and experienced depopu-lation 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. Thesevery mature stands likely owe their origins to the interval

between the depopulation of the indigenous peoples in the16th – 17th 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 (Capanã Grande Lake),

where the castanhais were more accessible and disturbed. Inthis site, a younger population structure and abundant regeneration of B. excelsa were observed in the 10 sampledstands. Historical data from this region indicate that indigenous populations were replaced gradually beginningin the 18th century, with no evidence of severe depopulation.We suggest that the different historical and contemporaryland 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 theones considered to be pristine and “native” forests, result from anthropogenic influences. We found no evidence to

support restrictions on seed harvesting as a means toimprove regeneration rates of Brazil nut stands.

Keywords Amazonia . Anthropogenic forest .

Extractivism . Historical ecology. Regeneration . Brazil nut

Introduction

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;Balée 1989; Mori and Prance 1990). However, there is noclear historical or ecological evidence of a long-term humaninfluence on the regeneration or population structure of thecastanhais. The clumped distribution and the abundance of unusual size classes of B. excelsa have generated discussionsconcerning the reasons for these characteristics. For example,

R. ScolesUniversidade Federal do Oeste do Pará,Rua Marechal Rondon s/n. CEP,68040-070 Santarém, Pará, Brasil

e-mail: [email protected]

R. Gribel (*)Coordenação de Pesquisas em Botânica,Instituto Nacional de Pesquisas da Amazônia (INPA),Manaus, AM, Brazile-mail: [email protected]

Present Address:

R. GribelDiretoria de Pesquisas,Instituto de Pesquisas do Jardim Botânico do Rio de Janeiro,Rio de Janeiro, RJ, Brazil

Hum Ecol (2011) 39:455 – 464DOI 10.1007/s10745-011-9412-0



it is possible that openings in the forest created byAmerindian activities permitted the germination of manyseeds that later became a stand (Mori and Prance 1990;Salomão 1991). On the other hand, agoutis, considered thesole natural seed dispersers of B. excelsa, may have gatheredand 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 theAmerindian peoples were influential in determining their current pattern of distribution and abundance (Müller et al.

1980; Müller 1981; Posey 1985; Balée 1989; Clement et al.

2010). The difficulty of naturally dispersing the large,heavy fruit also favors this hypothesis. If this view iscorrect, then Brazil nut stands may be anthropogenic rather than having natural origins (Posey 1984, 1985, 1986, 1990;Anderson and Posey 1987; Balée 1989). If humans aremajor actors in the geographical distribution and stand

creation of Brazil nuts, the relative roles of agoutis andhumans 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 thentransport sacks or baskets of Brazil nut seeds for use andsale. Seeds occasionally fall during the fruit opening andtransport, affording a dispersal opportunity if the seedgerminates and grows in a favorable location. For example,forest clearings made by humans may provide the preferredenvironment 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 seedgermination (several months).

Here we examine and compare the population structure of two sets of Brazil nut stands near communities in the BrazilianAmazon. These two areas are distant from one another andhave different patterns of historical occupation and contem-

poraneous use. We examine whether evidence supports thehypothesis that the population structure of B. excelsa trees inthe castanhais is due to human activities. We hypothesize that disturbances caused by continuous human activities in theforests, such as selective timber extraction, collection of non-

timber products, understory openings, and eventual fires,increase the regeneration rate of the B. excelsa stands andshift them toward a younger population structure.

The Species

Bertholletia excelsa is widely distributed in non-floodedforests (terra firme) in the Amazon and Guiana Shield,from 14° S to 5° N (Mori and Prance 1990). The species isfound in areas with 1,400 – 2,800 mm of annual rainfall, 24 –

27°C mean annual temperature and an average relativehumidity from 79% to 86% (Diniz and Bastos 1974). Thetree is emergent, reaching up to 50 m in height and adiameter at breast height (DBH) of >300 cm (Zuidema andBoot 2002; Salomão 2009). The trunk is straight, with no

branches until near the top. The canopy is formed of well-spaced branches and may reach up to 50 m in diameter. The

fruit, which contains the Brazil nut, is woody, indehiscent, andspherical; it weighs 500 – 2,500 g and has a diameter of >10 cm.This woody fruit holds 10 – 25 seeds that are edible after removal of the woody protective tegument (Mori and Prance1990). The agouti ( Dasyprocta spp.) is thought to be the soleimportant 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 cmDBH, and the most productive trees are 80 – 160 cm DBH(Viana et al. 1998; Zuidema and Boot 2002). Trees may livefor hundreds of years in terra firme forests, and the adults havehigh survival rates (Zuidema and Boot 2002). Brazil nut

populations often contain 75 – 150 trees of >10 cm DBH(Peres and Baider 1997), with stands of relatively highdensities for humid tropical forests (5 – 20 trees ha−1) mixedwith areas of low density (0.2 trees ha−1 (Mori and Prance1990)). Studies of the population structure of B. excelsa havefound few trees >10 cm DBH that are not reproductive(Salomão 1991; Nepstad et al. 1992; DHV 1993). Popula-tions are typically dominated by intermediate-sized trees(Zuidema and Boot 2002; Peres et al. 2003; Salomão 2009).

Bertholletia excelsa is heliophytic (Salomão 1991;Scoles 2010) and depends on clearings for growth as wellas 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 growninto more advanced successional stages. For this reason, thespecies is considered to be a long-lived pioneer tree(Swaine and Hall 1987; Zuidema 2003). Many experimen-tal studies have shown that Brazil nut trees grow best inwell-lighted open areas (Fernandes and Alencar 1993;Yared et al. 1993; Tonini et al . 2008) and that growth ismuch slower in forest shade in the understory layer (Kainer et

al. 1998; Myers et al. 2000; Peña-Claros et al. 2002; Scoles2010).

Study Areas

The population structure was studied at two distinct sites: 1)Trombetas River (hereafter Trombetas), on the northern sideof the Amazon River, near Oriximiná and Obidos in the stateof Pará, Brazil; and 2) Capanã Grande Lake (hereafter CapanãGrande) on the Madeira River, near Manicoré on the southernside of the river in the state of Amazonas, Brazil. These twoareas are 800 km from each other (Fig. 1).

456 Hum Ecol (2011) 39:455 – 464



The sampled castanhais in Trombetas are in conservationareas, the Rio Trombetas Biological Reserve, the Sacará-Taquera National Forest, the recently created Rio TrombetasState Reserve, and in Quilombola Territories. The QuilombolaTerritories were originally areas to which African slaves fledfrom their owners, but they have now become semi-

autonomous communities. The Quilombola areas in thisstudy are on the Trombetas and Erepecuru Rivers, whichare administered by the Remaining Quilombo CommunityAssociation of Oriximiná (ARQMO). The castanhais inCapanã Grande all occur within the Lake Capanã GrandeExtractive Reserve, which is a direct-use conservation unit co-governed by the riparian communities of the lake and theChico Mendes Institute for the Conservation of Biodiversity(ICMBio).

At Capanã Grande, sampling units are located near eachother (1 – 16 km apart) on the plateaus near the lake and thecommunities (100 – 8,750 m). At Trombetas, the sampled

castanhais extend over the Trombetas River and its westerntributaries’ watersheds. Most sampling units are >10 kmapart from the communities, and more than a third aredifficult to reach due to topography and obstacles, such asriver 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 month−1. Annualrainfall varies from 2000 to 2500 mm, temperature variesfrom 24° to 26°C, and relative humidity is normally >80%

(Brasil 1979; SUDAM 1984). In Manicoré, January toMarch is usually the rainiest period (monthly rainfall~300 mm), and only July and August may be considereddry months (AGRITEMPO 2009). At Trombetas, rainfall ishighest from March – May, and the dry season runs fromAugust – November (IBAMA 2004). In both regions, the

Brazil nut stands occur in areas with yellow or yellowish redlatosoils which are the predominant soil types associated toterra firme forest in the lower stretches of the Trombetas andMadeira rivers (IBGE 2006).

Amerindian occupation and use differ between the twostudy areas. The lower Amazon lost most of its native

population during the first two centuries of colonization(c. 1500 – 1700). By the early eighteenth century a large

part of the Amerindian population had succumbed tomassacre and epidemics. The remaining Amerindiansfled to less-accessible areas. For example, in Trombetas,they went upstream above the rapids and waterfalls of

the Trombetas, Cachorro, Mapuera, Acapu and ErepecuruRivers. This period was followed by the slow re-

population of the area by neo-indigenous people whohad been uprooted from their original homes and culturesand were incorporated into Brazilian society by religiousmissionaries (Porro 1992). During the 1800s, Africanslaves and their descendents fled the towns and farms of the state of Grão-Pará and established quilombos in themiddle and upper regions of the Trombetas and ErepecuruRivers. The inhabitants descended to lower regions when

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

Hum Ecol (2011) 39:455 – 464 457



slavery was finally abolished (1886) and commercial tradein extractive products, such as Brazil nuts and timber expanded (Acevedo and Castro 1998). Since approximately1850, 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 occurredlater, during the 1800s, with the creation of the states of Amazonas (1850) and the rubber boom. Previous incur-sions of colonists were temporary and limited to extractivecommerce and Jesuit missions (Menéndez 1992). In the1700s, the government, fearing that the Madeira River would serve as a route for contraband metals from the statesof Minas Gerais and Goiás, prohibited river navigation (in1733) and spread rumors of dangerous Indians, such as theMura, along the river margins (Amoroso 1992). Thisstrategy deferred more intense contact between the colonistsand the Amerindians. Expansion of extractive commerce

during the latter half of the 1800s marked the beginning of thecolonization of the Madeira River that would give rise to asociety of mostly rural, mixed-race (caboclo) communities,which endure today.

Methods

Data were gathered over three years at Trombetas (2007 – 2009) and one year at Capanã Grande (2008). A total of 25(125 ha) transects of 50×1,000 m were established withinstands of Brazil nut trees at the Trombetas River and 10

(49 ha) at Capanã Grande, the latter with one shorter transect (800 m) due to spatial limitations. In each transect,10 plots of 10×25 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 thetransect. We measured the DBH (cm) and the diameter of the canopy (as twice the length of the longest branch andthe next longest branch approximately perpendicular to thefirst (m)), and estimated tree height (m). When the canopywas irregular, we applied a conversion factor to adjust thearea estimated in quadrants. For example, if the canopy was

irregular because it had a particularly sparse or emptyquadrant, we multiplied by 0.75; if another quadrant wasmissing, we multiplied it by 0.50; if most of the canopy wasabsent, we multiplied by 0.25.

We also collected data on smaller Brazil nut trees (<10DBH) in the 10 plots. We measured spatial coordinates, treeheight, the DBH of all saplings >1.3 m in height, and thediameter at the ground for smaller saplings.

Trees were placed in classes to facilitate analysis.Classes were young (10 – 40 cm DBH), young adults (40 –

80 cm), productive adults (80 – 160 cm), mature adults(160 – 200 cm), and old adults (>200 cm) (Viana et al. 1998;Zuidema and Boot 2002). Plants less than 10 cm weredivided 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 wasused 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 themorning 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 Miramón 6.0, a program that counts pixels and thencalculates the percentage of white pixels in all pixels in the

photo. The calculated percentage was then considered theindex of canopy openness.

Data Analysis

Experiments in the classical sense are generally impossible toapply on a large regional scale. The two historical situationscompared here cannot be ‘replicated’ over the Amazon. As aconsequence, the 25 plots in Trombetas and the 10 plots at Capanã Grande cannot be considered as independent repli-

cations used in classical experimentation; they must instead betechnically classified as ‘spatial pseudo-replications’ (Hurlbert 1984). Because of that, we did not use inferential statistics tocompare the two ‘treatments’ in this unreplicated naturalexperiment 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 ha−1) and the high proportion of the canopy occupied by Brazil nut trees (29%and 34%) in Trombetas and Capanã Grande, respectively,indicate that this species is dominant in both areas, and theforests 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, withintermediate to large sizes dominating at Trombetas andsmaller sizes (<80 cm DBH) at Capanã Grande (Fig. 2). Tree

458 Hum Ecol (2011) 39:455 – 464



height was on average 3 m greater at Trombetas than inCapanã Grande. Tree density was lower and the trees wereolder at Trombetas, with only 7% of trees too young toreproduce (Table 1).

At Trombetas, most trees were in the 80 – 160 cm DBHrange, whereas at Capanã Grande, most trees were <100 cmDBH (76%), and approximately 26% were not reproductive(DBH 10 – 40 cm). The distribution of tree sizes at CapanãGrande was asymmetric, favoring small sizes (Fig. 2). At Capanã Grande, the most productive trees (80 – 160 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 ha−1). The density of trees <130 cm

DBH was higher at Capanã Grande, and the density of trees >130 cm DBH was higher at Trombetas (Fig. 2).

Capanã Grande thus exhibited a younger populationstructure, 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 Capanã Grande (1%). At Trombetas, three trees were >300 cm DBH, whereas thelargest tree at Capanã Grande had a DBH of 267 cm.

Recruitment and regeneration were much greater at CapanãGrande 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 Trombetas River Capanã Grande

Tree Density DBH>10 (tree ha−1) 6.8±4.1 12.5±7.8

Tree Density DBH>40 cm (tree ha−1) 6.3±3.9 9.2±4.7

Tree Density DBH 10 – 40 cm (tree ha−1) 0.5±0.8 3.2±3.4

Seedlings ha−1 4.8±8.7 24.8±19.9

Saplings ha−1 1.0±3.1 4.4±5.3

% juveniles (DBH 10 – 40/DBH>10) 7 (0.0, 33) 18 (0, 41)

Seedlings adult −1 1.0±2.2 2.9±1.9

Saplings adult −1 0.1±0.4 0,5±0.6

Juveniles adult −1 0.1±0.1 0.3±0.2

Tree DBH (cm) 128.5±55.5 73.1±44.2

Trunk height (m) 22.5±4.9 19.2±4.0

Basal area (m2 ha−1) 10.4±5.6 7.1±2.5

Crown area (m2 ha−1) 2.865±1.250 3.385±1.351

Occupation canopy forest (%) 28.7 (11.8, 51.3) 33.8 (7.2, 51.0)

Mean Canopy Opening (%) 6.5 (49.5, 1.9) 6.6 (2.3, 30.1)

Proportion of canopy gap forest (>20% canopy opening) 0.01 0.02

Table 1 Comparative analysisof population structure (means ±standard deviation, if%, maxi-mum andminimum) of B. excelsa

in two regions of BrazilianAmazon: Trombetas River Region (Oriximiná, Obidos, PA)and Capanã Grande Lake(Manicoré, AM)

0,0

0,4

0,8

1,2

1,6

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

D e n s i t y ( t r e e

h a - 1 )

n=609

n=850

Fig. 2 Distribution of Brazil nut densities in 10 cm size classintervals at Trombetas( filled bars) and Capanã Grande(white bars)

Hum Ecol (2011) 39:455 – 464 459



of and an indicator of potential regeneration. The seedlingdensity at Trombetas (mean 4.6 seedlings ha−1) was five

times lower than at Capanã Grande (24.4 ha−1). Similarly, thedensity of saplings (1.0 and 4.4 saplings ha−1 at Trombetasand Capanã Grande respectively) and juvenile trees (0.5 and3.2 juveniles ha−1 respectively) were also much lower at Trombetas.

Both regions have very shaded understories with only 6 – 7% light entrance. At Capanã Grande, however, there weremore small clearings (2% of total ground area with>20%light) than in Trombetas (1%) (Table 1). Canopy openingswith 10 – 20% light entrance were twice as common at Capanã Grande, and thus the probability of light reachingthe forest floor was higher in Capanã Grande.

Discussion

In the Amazon basin, the density of Brazil nut trees variesfrom 1 to 23 trees ha−1. The density of B. excelsa at CapanãGrande (12.5 trees.ha−1) is thus among the highest recordedin studies for this species in the Amazon, with theexception of stands in Cajari, Amapá state, Brazil (Table 2).In other studies of castanhais, size class distributions areusually more similar to that found at Trombetas, withfrequencies being greatest in intermediate classes (Zuidema

2003). This trend was found also in Bolivia (DHV 1993;Zuidema and Boot 2002), in the Brazilian state of Pará(Salomão 1991, 2009) and in most of the studies examinedin the meta-analysis carried out by Peres et al. (2003).

The castanhais at Capanã Grande are in other waysstrikingly different, with a distribution strongly skewed tothe left, favoring trees with DBH<80 cm (Fig. 2). While

this pattern is atypical, it is not unknown in the Amazon. At Nova Esperança, Xapuri (in the state of Acre), 58% of Brazil nut trees have <80 cm DBH. At the Chico MendesExtractive Reserve in Acre, ~60% of trees have <100 cmDBH (Wadt et al. 2005). Interestingly, on the MadeiraRiver, those castanhais that are farthest from communitiestend to have size distributions similar to that of the stands at Trombetas (Scoles 2010).

At Capanã Grande, trees tended to be smaller (meanDBH=73 cm) than at Trombetas (129 cm), which indicatesa 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 ExtractiveReserves or that are known to be persistently used by localcommunities tend to have an average DBH similar to that of Capanã Grande. For example, mean DBH at the PinkaitiIndigenous Area in Pará was 73±4 cm; at Nova Esperança,Acre, it was 74±4 cm, and at the Chico Mendes ExtractiveReserve, Acre, it was measured 86± 5 cm (Peres et al. 2003;Wadt et al. 2005).

Seedling density at Trombetas (mean, 4.6 seedlings ha−1)is the lowest published to date (Baider 2000; Zuidema andBoot 2002; Zuidema 2003; Wadt et al. 2008). The ratio of

seedlings to adults is also the lowest reported to date in theliterature. In contrast, seedling density at Capanã Grande(24.4 ha−1) is similar to densities reported elsewhere[29.8 ha−1, Baider (2000) in Para; 30 – 52 ha−1, Zuidema(2003) in Bolivia].

Thus, the castanhais at Capanã Grande seem to have agreater regenerative capacity than those at Trombetas

because of the much higher density of juveniles, saplings,and seedlings. Castanhais in Capanã Grande are intermedi-ate in terms of regeneration (18% young), which is withinthe range of 1 – 52% found in other areas (Peres et al. 2003).Yet, that percentage increases inversely with distance from

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

Location Area (ha) Density Source

Forest Reserve El Tigre, Beni, Bolívia 12 1.7 Zuidema and Boot (2002)

Indigenous Area Pinkaiti, Pará State, Brazil 28.5 4.8 Peres and Baider (1997)

Saracá-Taquera Forest, Pará State, Brazil 203.7 5.6 Salomão (2009)

River Trombetas Region, Pará State, Brazil 125 6.8 This study

Cajari, Amapá State, Brazil 22.6 12.2 Baider (2000)

Lake Capanã Grande, Amazonas State, Brazil 49 12.5 This study

Table 2 Comparison of Brazilnut tree density (>10 cm DBH)in different regions of theAmazon basin, by increasingorder of density

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communities; closer castanhais have 21 – 40% young plants(in comparison to the usual 18%) and are similar to studiedareas that have the greatest proportion of non-reproductivetrees. This regeneration trend found in the Capanã Grandearea is clearly contrary to the conclusions of Peres et al.

(2003), which postulated that more persistently harvestedcastanhais exhibited poor regeneration and that these

intensely exploited populations may eventually succumbto recruitment bottleneck.

The entirety of the population structure parameters foundhere shows that Brazil nut stands are younger and havegreater regeneration potential at Capanã Grande. In Trombetas,the canopy was more closed and higher, and the standcontained less-dense, older trees. What are the most likelyexplanations 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 explainthese different patterns. The first relates to the current trends in

occupancy and use of the castanhais, and the second relates totheir historical occupation.

At Trombetas, the castanhais are less often visited bylocal people. This pattern is certainly due to the greater distance of the stands from the communities, and thus thetrees are only visited during harvesting (≤4 month yr −1). Inaddition, at Trombetas, many of the castanhais are near rapids that must be crossed by canoe or in steep anddifficult terrain. Thus, gathering and transporting theharvest is much more difficult. Additionally, staging sitesfor transport are often very far from where seeds areharvested. 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 theBiological Reserve of Rio Trombetas. In the ten castanhaiswithin the domain of the quilombos territories, people tendnot to visit the stands outside of the harvest season due tolimited accessibility.

The situation is very different at Capanã Grande, wherecastanhais are near the communities. Comparatively, thesestands are much more accessible, and collection andtransport of Brazil nuts is easier. Several stands are near small rivers that can be used during high water. Aside fromBrazil nut collection, other extractive activities occur

when Brazil nuts are not being harvested, including rubber tapping, fruit collection, collection of fiber from vines andtree barks, and timber exploitation. Also, many stands arein forest fragments that are separated by land used for agriculture. This fragmentation increases the availabilityof light in the understory and creates edge effects andother perturbations. Despite the similarity of average light levels in the two forests, the distribution of light is verydifferent because more openings are found at CapanãGrande.

In other studies in the southwestern Amazon, the sizedistribution (i.e., a large proportion of young trees, average70 – 80 cm DBH) is similar to that at Capanã Grande but hasa lower total tree density (Viana et al. 1998; Wadt et al.

2005). In other stands, seedlings are always present despitethe 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 openforests 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 inour study area at Capanã Grande, where human activitiesand settlements have opened the forest, in comparison withTrombetas.

The history of occupation is also very different in the twostudy areas and may explain the contrasting populationstructures of the B. excelsa stands. The Trombetas-Erepecuru watershed is a region particularly rich inarchaeological sites (Magalhaes 2007), black earths (Kern

and Kämpf 1989), pottery (Hilbert 1955), and rock paintings(Pereira 2003; Pereira et al . 2009). These archaeologicalfindings suggest that this region probably supported denseAmerindian populations and, consequently, experiencedextensive forest disturbance during pre-Columbian times. It is quite likely that the Brazil nut, which grows well indisturbed areas, was favored by the slash-and-burn agricultureof 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(87 – 145 cm DBH) from the Trombetas region measuredages from 228 to 502 years (Schöngart et al . unpublished

data). These data suggest that the biggest trees found in theTrombetas area, those with DBH >300 cm, may reach agesof 600 years or more. Interestingly, the estimated age of themajority of the Brazil nut trees in this study was between300 and 450 years, which probably coincides with a periodof depopulation of the Amerindian people followingEuropean contact, especially along the lower and middlestretches of the main rivers (Porro 1992). The current

population structure of B. excelsa likely owes its origins tothe interval between land abandonment due to Amerindiandepopulation (sixteenth-seventeenth centuries) and theestablishment of the quilombos (nineteenth century). Thus,

it appears that the abandonment of the Trombetas arearesulted in the development of the current B. excelsa

population structure, with a high proportion of old treesand scarce regeneration.

In contrast, Capanã Grande likely owes the formation of itscastanhais to the growth in human presence that intensified inthe late nineteenth century, following colonization of theMadeira River and the beginning of the rubber boom. Thistiming may explain the domination of trees <80 cm DBH(which are approximately 150 years old (Zuidema and Boot

Hum Ecol (2011) 39:455 – 464 461



2002)) in this population. The early riverine communitieswere probably established around existing stands of rubber ( Hevea brasiliensis) and Brazil nut trees, which would havethen favored the rejuvenation of the castanhais as previouslydescribed.

Therefore, we hypothesize that when native Amazonian populations were decimated post-conquest in the Trombetas,

forest disturbance was reduced, allowing for the shift indemography 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. Inthe Madeira, the decimation occurred later, and theAmerindian replacement by caboclos was more gradual andcomplete. The Madeira region probably recovered pre-conquest population densities, whereas the Trombetas most likely did not. The contemporaneous stands in Capanã Grande

probably have a younger population profile, not only becausethe 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 recognizedas regenerated forests that have recovered after theabandonment of lands that were previously used for agriculture. In tropical America, Africa and Asia, areas that were once considered virgin or pristine have been discoveredto have been occupied and significantly perturbed by earlier human settlements that, once abandoned, allowed forests toregrow (Willis et al. 2004). In tropical Latin America, manymonodominant forests are the consequence of management

and manipulation of the original forests by pre-Colombianand subsequent societies (Anderson 1990; Peters 2000;Campbell et al. 2006). Today, it is thought that theoccurrence of many high-density stands of fruit trees,monospecific stands of palms, and other anthropogenicforests are evidence that at least 11% of the BrazilianAmazon was anthropogenically modified (Balée 1989).

Here, we suggest that the differences in the populationstructures of the Brazil nut stands in Trombetas andCapanã Grande may be a consequence of pre- and post-colonial human occupation and manipulation of theforest. Confirmation of this hypothesis will require

archaeological studies which would improve understand-ing of the impact of Amerindians on pre-colonial tropicalforests. The Brazil nut stands at Capanã Grande exhibit ayounger structure likely due to more recent human

perturbations. In contrast, at the Trombetas River, treesare older, and the current recruitment is much lower. Thelower recruitment is in part due to the greater density of

big trees (and the consequent low-light conditions in theunderstory for the past several centuries) and in part dueto few recent perturbations.

Regeneration of the heliophytic, long-lived Brazil nut istherefore likely to be most influenced by ecological factorsthat allow light to reach the understory, such as low-intensity forest disturbances mediated by humans. Inaddition, the ages of the stands and population structureindicate a history of human influence, both old (pre-colonization) and recent (post-colonization). Hence, we

suggest that these stands are anthropogenic forests that aredistinctly influenced by humans. Finally, we found noscientific evidence that there should be restrictions on seedharvesting as a means to improve regeneration rates of theBrazil nut stands.

Acknowledgments We thank the Protected Areas Program of theChico Mendes Institute for Biodiversity Conservation (ICMBio), the National Council for Scientific and Technological Development (CNPq), the Scholarship Program of the International EducationInstitution of Brazil (IIEB), the Brazil Nut Germplasm Bank project of the National Institute for Amazonian Research (INPA), the MineraçãoRio do Norte Company (MRN), and the Chico Mendes BiodiversityInstitute (ICMBio) for their logistical and financial support. Wesincerely thank the team of ICMBio at Porto Trombetas and Manicoréfor their collaboration and logistical support during field work,especially Gilmar N. Klein, Altemar Lopes Silva, Vivian Mara Uhligand Valmir Raimundo Lopes da Silva. Thanks to Paulo M. Alencastroand to Carlos Palacio for the map, Charles Clement and AndréJunqueira for the literature on historical ecology and helpfuldiscussions, David Bertran for suggestions for the analyses, JochenSchöngart for the data on the tree-ring studies, and James J. Roper andMaristerra R. Lemes for constructive comments on the manuscript.Our heartfelt thanks go to all the families of the communities that wereinvolved in this project. Research Grant to RG was provided for CNPq.

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