Wednesday, 14 September 2016

Inter-site variation in allometry and wood density of Goupia glabra Aubl. in Amazonia

Published Date
Received: October 28, 2014; Accepted: December 18, 2014

Variação entre-sítios na alometria e densidade da madeira de Goupia glabra Aubl. na Amazônia

N. C. Siliprandia  , E. M. Nogueiraa  , J. J. Toledob  , P. M. Fearnsidea  , H. E. M. Nascimentoa  * 
aCurso de Pós-graduação em Ciências de Florestas Tropicais, Instituto Nacional de Pesquisas da Amazonia – INPA, Avenida André Araújo, 2936, Petrópolis, CEP 69067-375, Manaus, AM, Brazil
bCurso de Pós-graduação em Biodiversidade Tropical, Universidade Federal do Amapá – UNIFAP, Rodovia Juscelino Kubitschek, Km 02, Jardim Marco Zero, CEP 68902-280, Macapá, AP, Brazil

The present study aims to compare the allometry and wood density of Goupia glabra Aubl. (Goupiaceae) in two different terra-firme sites in Amazonian forest. A total of 65 trees ≥ 10 cm DBH was sampled in both sites, with 39 trees in Nova Olinda do Norte (NOlinda, near the Amazon River) and 29 trees in Apuí (near the southern edge of the Amazon forest). Except for the relationship between DBH (diameter at breast height) and Ht (total height), allometric relationships for G.glabra differed significantly between sites. Apuí had lower intercept and greater slope for log10 (DBH) versus log10 (Hs – stem height), and, conversely, greater intercept and lower slope for log10 (DBH) versus log10 (Ch – crown height). The slope differed significantly between the sites for DBH versus Cd (crown diameter), with greater slope found for NOlinda. Mean basic wood density in Apuí was 8.8% lower than in NOlinda. Our findings highlight the variation in adaptive strategy of Gglabra due to environmental differences between sites. This is probably because of different canopy-understory light gradients, which result in differentiation of resource allocation between vertical and horizontal growth, which, in turn, affects mechanical support related to wood density. We also hypothesize that differences in soil fertility and disturbance regimes between sites may act concomitantly with light.
Key words: allometric relationships; functional traits; phenotypic plasticity; tropical tree species
O presente estudo tem como objetivo comparar a alometria e a densidade da madeira de Goupia glabra em dois diferentes sítios de floresta de terra firme na Amazonia. Um total de 65 árvores com DAP ≥ 10 cm foi amostrado em ambos os sítios, sendo 39 árvores em Nova Olinda do Norte (NOlinda, próximo ao rio Amazonas) e 29 em Apuí (próximo à borda sul da Amazônia). Exceto para a relação entre o DBH (diâmetro a altura do peito) e a Ht (altura total), as relações alométricas para G. glabra diferiu significativamente entre os sítios. Apuí apresentou menor intercepto e maior inclinação para a relação log10 (DBH) versus log10 (Hs – altura do fuste) e, ao contrário, maior intercepto e menor inclinação para log10 (DBH) versus log10 (Ch – altura da copa). A inclinação diferiu significativamente entre os sítios para DBH versus Cd (diâmetro da copa), com maior inclinação encontrada para NOlinda. A densidade básica média da madeira in Apuí foi 8.8% menor do que em NOlinda. Os resultados deste estudo destacam a variação na estratégia adaptativa de G. glabra devido às diferenças ambientais entre os sítios. Isto é provavelmente consequência dos diferentes gradientes de luz o que resulta na diferenciação na alocação de recursos entre o crescimento vertical e horizontal o que, por sua vez, afeta o suporte mecânico relacionado à densidade da madeira. Nós também levantamos a hipótese de que as diferenças em termos de fertilidade e regimes de distúrbios entre os sítios podem agir concomitantemente com o regime de luz.
Palavras-Chave: relações alométricas; características funcionais; plasticidade fenotípica; espécies arbóreas tropicais
In tropical forests light is one of the most limiting resources for tree growth. The ability of a tree to assimilate light energy depends on the relationships between the size of the tree (height and diameter) and crown size (both vertical and horizontal dimensions), i.e., the tree allometry – the spatial distribution of its components along the vertical axis (King, 1996Poorter et al., 2006). Since there is a gradient of light availability ranging from a low light level in the understory to a high one in the forest canopy, allometric differences are expected among tropical tree species because of their differences in light requirements (Chazdon and Fetcher, 1984). In this sense, low-statured and shade-tolerant understory tree species, which are adapted to low light environments for establishment and growth, tend to have proportionally wider and shallower crowns in order to (i) increase their ability to assimilate light along the horizontal light gradient and (ii) avoid self-shedding. Conversely, shade-intolerant pioneer species, which only grow in gaps and/or are highly light demanding, invest proportionally more in height growth, increasing crown depth while reducing crown horizontal expansion (King, 1996Thomas, 1996Sterck et al., 2001Alves and Santos, 2002).
Interspecific variation in allometry may be related to wood density because density correlates with mechanical support (King, 1981Niklas, 1993Putz et al., 1983). Light-demanding pioneer species in gaps need to invest more in growth to reach the canopy rapidly and to better compete with other tree species. In contrast, shade-tolerant species allocate more energy to survival through greater investment in mechanical support. Therefore, there is a tradeoff in biomass allocation (and, by inference, wood density) due to the different costs of support between these two extremes. Pioneer trees require less investment in wood tissue to sustain their crown, giving them more rapid growth and lower support costs, whereas shade-tolerant species invest more in building tissues (and thus have higher wood density), decreasing their susceptibility to physical damage, which ultimately results in a greater survival advantage (Putz et al., 1983Thomas, 1996King et al., 2006Poorter et al., 2006).
Although the patterns of differentiation in architecture and wood density among functional groups of trees are widely recognized, studies assessing the variation in allometry and wood density of a single species growing in different environmental conditions are rare. Individual trees within a given species have been found to have lower wood density (Nogueira et al., 2007) and shorter height for any given diameter (Nogueira et al., 2008a) in southern Amazonia as compared to central Amazonia. To our knowledge, the present study is the first to develop species-specific allometric equations for populations of a species with parameters specific to each of these subregions. At the community level and at different spatial scales, several studies have shown significant correlations between wood density and environmental variables that are affected by variation in altitude, latitude and soils (Wiemann and Williamson, 2002Muller-Landau, 2004Baker et al., 2004Wittmann et al., 2006Nogueira et al., 2007Swenson and Enquist, 2007Slik et al., 2010).
The present study aimed to compare the architectural features and wood densities of Goupia glabra growing at two different sites in terra-firme (not seasonally flooded) lowland forest in Brazilian Amazonia, which differ mainly in terms of soil type and light condition. Our central hypothesis was that G. glabra would have distinct allometric relationships related to environmental site conditions, and that this may be reflected in its wood density.
2.1 Research sites
This study was carried out in two areas of commercial timber exploitation in the Brazilian Amazon - one located in the municipality of Apuí, called Fazenda Nova Era (59°56' W; 7°18' S), and the other located in the municipality of Nova Olinda do Norte (hereafter termed NOLinda), called Fazenda Apapazinho (58°22'W; 3°48'S). Both study sites are in the state of Amazonas and are about 400 km apart along a north-south gradient (Figure 1). Apuí is located near the southern edge of the Amazon forest in the “arc of deforestation,” while NOlinda is located in central Amazonia near the Amazon River.
Figure 1 Location of the municipalities of Apuí and Nova Olinda do Norte and of the forest sites where trees were collected and measured in this study. 
At both sites the average annual temperature is about 27°C and the mean maximum and mean minimum are 31°C and 23°C, respectively, while annual precipitation ranges from 2200 to 2300 mm with two distinct seasons (INMET, 2009, for a 30-year historical series). Precipitation is concentrated between December and April, when the mean monthly rainfall is over 200 mm. However, NOlinda is more uniformly wet, whereas Apuí has a more pronounced decline in precipitation between June and August. Moreover, the sites differ in terms of vegetation, soils and geological formation. The predominant vegetation type in Apuí is open montane wet forest and the soils are mainly Acrisols (red-yellow latosol in the Brazilian system; Santos et al., 2011). In Nova Olinda do Norte, the dominant vegetation is classified as evergreen lowland tropical moist forest and the predominant soils are Xanthic Ferralsols (allic yellow latosol in the Brazilian system), which are heavily weathered, acidic, and very poor in nutrients such as P, Ca, and K.
2.2 The studied species
The genus Goupia is monotypic with just Goupia glabra Aubl. (Goupiaceae). G.glabra is a canopy semideciduous species with ascending branches and cylindrical stem. The bark is gray, with chipped lengthwise lenticels. The bark is 1 cm thick and comes off in large slabs. G. glabra has a continuous pattern of flowering and fruiting, but flowering peaks usually occur at the end of the dry season and fruiting peaks in the early rainy season. The fruit is a globose berry from 3 to 6 mm in diameter. Seed number ranges from one to five per fruit. Seeds are approximately 1.5 mm long and 1 mm wide and are dispersed primarily by birds (Ribeiro et al., 1999Ferreira and Tonini, 2004).
G. glabra has a wide distribution, occurring from the tropical rainforests of Panama and Colombia to Amazonian terra firme forests. Trees can reach up to 40 m in height and up to 130 cm in diameter at breast height (DBH), growing preferentially either on clayey or well-drained sandy soils (Loureiro et al., 1979Ferreira and Tonini, 2004). This species is closely associated with gaps (Loureiro et al., 1979Boot, 1996) and is classified as a shade-intolerant pioneer species (sensuSwaine and Whitmore, 1988). Although its wood is heavy, with a density ranging from 0.7 to 0.9 g/cm3G. glabra has relatively high growth rates in sites with direct sunlight (Loureiro et al., 1979).
2.3 Data collection
We measured 29 individuals of G. glabra in Apuí and 36 in NOlinda. Individuals with damage to the canopy and/or trunk were avoided. At both sites, G. glabra trees were collected in logging concessions that encompass 452 ha and 820 ha in Apuí and NOlinda, respectively. We aimed to obtain a uniform distribution of the number of individuals across the DBH size classes at both sites.
For each sampled tree ≥ 10 cm DBH, the following data were recorded: DBH, stem height (Hs), total height (Ht), crown length (Ch), crown diameter (Cd), commercial volume (Vc), stem form factor (FF), and wood density (Dg). DBH was measured at 1.30 meters above ground level, or just above any buttresses. Hs is the vertical distancebetween the ground level and the height of the lowest living branch. Ch was defined as the difference between the first branch and final height of the crown, and Ht is the sum of Hs and Ch. Cd was estimated by measuring the horizontal distance from the trunk to the vertical projection of the crown edge in four compass directions 90o apart. Cd of a tree was calculated by the arithmetic mean of the two perpendicular directions of the crown. Vc was calculated by cubic scaling of the bole using the Smalian method for obtaining the areas of cross sections at 0.5 m, 1 m, 1.3 m, and 2 m and thereafter at 2-m intervals up to the first living branch. All measurements included the bark. FF was calculated as the ratio between the bole volume calculated by the Smalian formula and cylindrical volume with a cross-sectional area equal to the measured DBH.
Cross sections (5-cm thick) were cut with a chainsaw from each selected tree to determine wood density (Dg) at six positions: 0.5 m, 1 m, 1.3 m, 2 m, middle and top of the bole. The samples were divided into heartwood, sapwood and bark and were weighed in the field on a portable electronic balance. The volume of each sample was determined immediately after collection to avoid dehydration. The wood samples were fixed on a stylus and submerged in a container of water placed on a balance. According to the Archimedes principle, the volume of water displaced by the immersed sample without touching the container corresponds to the volume of the sample; the amount was recorded in grams, since the density of water is near 1 g/cm3 (ASTM, 2002). Subsequently, the samples were placed in paper bags and dried in an oven with forced air circulation at 105°C (ASTM, 2002). After a week, we began weighing each sample at intervals of 24 hours. The average basic wood density for each tree was calculated as the ratio between the dry weight and the volume of the fresh sample.
2.4 Data analysis
Dimensional relationships of G. glabra within each site were determined by least square linear regressions. Both untransformed and logarithmically-transformed (log10) regressions were performed; the latter substantially improved the fit for some relationships. For each allometric relationship, 95% confidence intervals around the intercepts and slopes were calculated using the bootstrap technique (Efron and Tibshirani, 1993). For each site, 1000 bootstrap samples were drawn with replacement. Bootstrapping was also used to indicate a p-value for statistically significant differences between sites in terms of intercept and slope. To achieve this, 1000 bootstrap sample pairs (each pair encompassing all 65 trees) were drawn in order to obtain the null distribution of no difference between sites (i.e, H0: Apuí - NOlinda = 0). The probability p for rejection of H0 was obtained by the proportion of cases in which the observed differences of the intercepts and slopes between Apuí and NOlinda were smaller than 0.05. In other words, the observed difference was large enough to state that it was not due to chance alone.
Exponential nonlinear models were tested to determine the relationship between tree size (DBH) and wood density for each site separately. Two-way analysis of variance was used to test the effects on wood density of site and of the position of the cross section along the length of the bole. The effect of position in this analysis was calculated for three positions: 1.30 m (the DBH measurement point), 50% (the midpoint of the bole) and the top of the bole. Because it is not appropriate to assume that samples are independent within the same bole, we randomly selected different trees to obtain the wood density of each bole position within each site.
3.1 Allometry
All linear regressions for DBH versus the other variables (Hs, Ht, Ch, and Cd) were significant, except log10 (DBH) versus log10 (Ch) for Apuí (Table 1Figure 2a). There was no significant difference between sites for DBH versus Ht. However, when DBH was regressed against the two variables that compose Ht (Hs and Ch), both intercepts and slopes were significantly different between sites (Figure 2b, c). Furthermore, Apuí had lower intercept and greater slope for log10 (DBH) versus log10 (Hs), and, conversely, greater intercept and lower slope for log10 (DBH) versus log10 (Ch). The slope differed significantly between the sites for DBH versus Cd, with greater slope found for NOlinda (Figure 2d). Both slope and the intercept differed between sites for the relationship between Cd and Ht, with greater intercept and lower slope for Apuí (Figure 2e).
Table 1 Regression coefficients, bootstrapped 95% confidence intervals (LL = lower limit and UL= upper limit) and probabilities (p) associated with the rejection of the null hypothesis of no difference between coefficients related to forest sites calculated by bootstrapping. Probabilities in bold denote significant differences between sites at p < 0.05. 
Bootstrapped 95% confidence intervals
DBH vs. HtApuí16.220.200.4412.0421.020.090.310.530.71
log DBH vs. log HsApuí0.190.540.57–0.080.490.360.690.0020.002
log DBH vs. log ChApuí0.870.140.020.471.34–0.170.420.0510.03
DBH vs. CdApuí3.870.190.802.
Htvs. CdApuí1.420.450.39–3.587.520.240.640.0240.015
log DBH vs. log VApuí–3.942.490.98–4.16–3.682.332.620.0030.003
Figure 2 Regression models fitted to data on DBH versus (a) Ht, (b) Hs, (c) Ch and (d) Cd, (e) Ht versus Cd and (f) DBH versus Vc. Regressions of DBH with Hs and Ch are log10-transformed for both axes. Regression coefficients are shown in Table 1
There was a significant difference in stem form factor (FF) between sites (t = 2.66, p = 0.01, GL = 63). The FF in Apuí (0.83 ± 0.082, mean ± standard deviation) averaged 7.8% higher than in NOlinda (0.77 ± 0.079). Volume fitted as a function of DBH was highly significant for both sites (Apuí: r2 = 99.7%; NOlinda: r2 = 96.5%, p<0.0001 for both cases, Table 1), and the model parameters differed significantly, with both greater slope and intercept for Apuí (Table 1Figure 2f).
3.2 Wood density
There was a significant positive relationship between DBH and wood density (F1,64 = 10.48, p = 0.001) for Apuí, for which DBH explained 35.8% of the variation in wood density. On the other hand, no significant relationship was found for NOlinda (F1,64 = 0.63, p = 0.403, Figure 3). ANOVA detected a highly significant site effect on wood density (F1,64 = 38.88, p < 0.001). Wood density in NOlinda (0.74 ± 0.033, mean ± standard deviation) was, on average, 8.8% higher than in Apuí (0.68 ± 0.042). The position of the sample in the bole also influenced wood density (F2,64 = 4.82, p = 0.012), with the wood density at 1.30 m differed significantly from that at the top of the bole (p = 0.009, Tukey test). Wood density decreased from the base to the top of the bole, with the pooled average for both sites being 0.74, 0.71 and 0.70 g cm-3 at 1.30 m, middle and at the top of the bole, respectively (Figure 4).
Figure 3 Relationship between DBH and wood density for trees at each forest site. 
Figure 4 Mean (± standard deviation) of wood density at different stem positions for each forest site. 
Our findings suggest that the allometry of G. glabra significantly differed between sites, especially regarding to the relationships of crown shape to DBH and height. These differences mirror the interspecific allometric variations within the same site in terms of adult stature (canopy/emerging species versus understory species) and/or demand for light (pioneer versus shade tolerant species) (e.g.King, 1996Sterck and Bongers, 1998Poorter et al., 2006). Thus, the allometric differences found in this study can be attributed to abiotic differences related mainly to the quantity and quality of light reaching the understory, as well as the variation in soil physical and chemical characteristics between sites.
Tree architecture within the same species may vary during ontogeny and depends on abiotic conditions (mainly light availability) in which individual trees grow. Rapid changes in the development of the crown may occur when a tree reaches the canopy due to an increase in light exposure (King and Maindonald, 1999Sterck and Bongers, 2001Osunkoya et al., 2007). Although G. glabra trees had similar Ht at both sites, this was not true for the relationship between DBH and Hs, indicating that trees in NOlinda invest more in stem elongation in the smaller size classes, but for larger trees the opposite pattern occurs: trees in Apuí invest more in stem elongation throughout tree ontogeny, which resulted in significantly higher regression slope and lower intercept at this site. Such high initial stem growth in NOlinda can be attributed to the fact that a tree growing in dense rain forest, where it is assumed that light incidence is lower when compared to the open forest in Apuí, needs to invest more in vertical growth at this stage to increase access to light.
The differences in growth in Cd and Ch corroborate the reduced growth found for Hs (in the initial phase) for trees in NOlinda, where they invest less in Ch and Cd, but have deeper and wider crowns when fully developed. In Apuí the relationship between DBH and Ch was not significant, indicating that Ch remains constant after stems reach a certain height, at least for trees ≥ 10 cm DBH. Because low light intensity implies a lower photosynthetic rate, perhaps it is a better strategy for a species growing in the dense rainforest to invest energy in early height growth to reach the canopy rapidly and, in later stages, to increase specific leaf area by expanding the canopy to intercept a larger quantity of light. In fact, the variation in bole volume between sites is a consequence of differences in taper (form factor) and Hs during ontogeny.
Increasing canopy height may result in higher self-shading of the leaves due to the packing of leaf layers (Sterck and Bongers, 2001). However, the opposite phyllotaxis and the small leaves of G. glabra can minimize the effect of canopy shading. In this case, the increase in canopy height could result in an increase in the number of layers of leaves and, by inference, the specific leaf area. Rather, the better light conditions experienced by trees in Apuí means that they do not need to invest large amounts of resources in increasing photosynthetic area. A deep and wide canopy does not necessarily imply a greater number of leaf layers, but the distribution and geometry (shape, size and orientation) of foliage can play a crucial role in the light interception (Poorter et al., 2006).
Allometric differences in this study corroborate the variation in wood density between sites. Wood density is directly related to mechanical structure, and by inference, the ability of a tree to support its own weight and to resist exogenous forces, such as wind and pushing over by other trees (King, 1981Putz et al., 1983Chave et al., 2009). However, recent studies have cast doubt on these ideas, showing that the same strength for supporting tree weight is achieved by a trunk with low wood density (with lower construction cost) than by one with higher wood density (Anten and Schieving, 2010). Larjavaara and Muller-Landau (2010) proposed that species with low wood density, such as pioneers, prioritize short-term gains over long-term costs, thereby not only evolving low wood density, but also low trunk and xylem resistance. Low light levels may induce tropical trees to reduce their diameter growth, thus resulting in higher wood density (Thomas, 1996). This also results in a greater investment in vertical growth and crown expansion at the expenses of stem thickness (Sterck et al., 2001Osunkoya et al., 2007Poorter et al., 2006). A thinner trunk with high wood density is more flexible than a thicker one with low wood density and equal strength, and flexibility can be advantageous in reducing sail area during short gusts of wind and in allowing the tree to bounce back after having been struck by falling trees or branches. In this sense, the greater crown expansion of G. glabra in NOlinda required more investment in strength and flexibility, and thus in higher wood density. In a rainforest in Borneo, Osunkoya et al. (2007) showed that the safety factor (a measure related directly to physical properties of the wood) had strong positive relationships with crown diameter and depth, indicating that trees (regardless of species) with greater horizontal or vertical crown expansion had higher safety margins against rupture (see also King, 1996Sterck and Bongers, 1998Alves and Santos, 2002).
The difference in taper between sites may also represent an adaptive strategy in terms of mechanical support because the increase in the stem base may improve support and fixation (Sposito and Santos, 2001). A larger taper in NOlinda can be related to decreasing risk of deflection of the stem as a result of the greater weight generated by the crown expansion. Therefore, we concluded that there are different adaptive strategies during the ontogeny of G. glabra acting on resource allocation and occupation of space mainly as a result of differences in light availability between sites. NOlinda trees need to invest heavily in initial height growth by allocating more carbon per unit volume of stem in this phase, so that an increase in the safety margin against breakage may be achieved when trees reach the canopy and start investing more in crown expansion. In contrast, trees in Apuí allocate less carbon per unit volume of stem during their ontogeny, as canopy expansion is significantly lower than in NOlinda. In fact, the non-significant relationship between DBH and wood density for NOlinda and the positive relationship for Apuí (Figure 4) demonstrate that carbon allocation to stems in NOlinda occurs equally throughout ontogeny, whereas for trees in Apuí the allocation of biomass changes as the tree grows, with an increase occurring at the end of ontogeny when horizontal crown expansion starts.
Among tropical tree species, tree growth is negatively related to wood density (Thomas, 1996Muller-Landau, 2004Nascimento et al., 2005King et al., 2006). In addition, within the same species wood density is higher in slow-growing trees than in fast-growing trees (Koubaa et al., 2000), indicating that G. glabra may have faster growth in Apuí and, as a result, there must be a difference between sites in the age of trees of same diameter. However, such a difference should be evaluated empirically, and we suggest this approach for future studies.
The distribution of life-history strategies, and particularly the wood density of tropical tree species, may vary among sites depending on environmental features such as climate periodicity, soil conditions, disturbance regimes and competition for light (Muller-Landau, 2004Nogueira et al., 2007Patiño et al., 2009). Sites with high disturbance regimes on relatively fertile soils may favor fast-growing species that have low wood density, while sites with lower frequencies of disturbance and with nutrient-poor soils reduce tree growth (Baker et al., 2004Muller-Landau, 2004). Patiño et al. (2009) have shown that branch xylem density varies considerably across Amazonia, and that 33% and 26% of this variation is attributable to phylogeny and environmental factors, respectively. The remaining 41% is attributable to intraspecific differences related to phenotypic plasticity in many tree species.
In the present study, the difference in wood density between sites is a straightforward consequence of the phenotypic plasticity of G. glabra in response to different environmental conditions. In seasonally flooded várzea(white water floodplain) forests in the Amazon, Wittmann et al. (2006) attributed the differences in wood density of two tree species, Tabebuia barbata and Hevea spruceana, to the level and duration of flooding, which leads to different water conditions and, consequently, to the reduction of tree growth during the aquatic phase, i.e., sites with higher levels and durations of flooding result in greater physiological stress that decreases tree growth and increases wood density. In the present study, differences in soil fertility and disturbance regimes between Apuí and NOlinda can also be considered as crucial factors for different strategies of G. glabra growth, and the subject is appropriate for future studies.
At the community level, allometric differences have been found in trees in different forest types in Amazonia and in other tropical forests (Nogueira et al., 2008aFeldpausch et al., 2011Banin et al., 2012). The results of the present study are unique because they show differences in allometric relations and in wood density for the same species growing in two forest types in Brazilian Amazonia. These allometric differences have implications for biomass estimates for this species and represent a warning of one more possible bias in biomass estimates generally when obtained by means of allometric equations. This even applies to those equations that include both tree height and wood density as explanatory variables but assume no differences in crown biomass. In the present study, the biomass of Goupia glabra will be higher at the NOlinda site (central Amazonia) than at the Apuí site (southern Amazonia) due both to denser wood in all trees (Figure 3) and to larger crowns in the case of the trees with large diameters and heights (Figure 3d, e). These height and density differences between central and southern Amazonia are consistent with the pattern for species studied by Nogueira et al. (20072008a, b).
This contribution is part of the first author’s Master thesis undertaken at the National Institute of Amazonian Research (INPA), with fellowships from the Amazonas Research Foundation (FAPEAM, process #143643/2008-8). We are grateful to the landowners, Antonio M. R. de Arrunda, Raimundo de S. Maia Filho, Sergio S. Souza (Fazenda Apapazinho) and Marcos V. Conceicao (Fazenda Nova Era) who provided us financial and logistic support for fieldwork. Our special thanks to Antonio Siliprandi, Norian C. Siliprandi, Nivaldo Carline, Ivone C. Siliprandi Michele Gusmao, Susy D. Souza, Manoel J.F. Mar, Pedro S. Silva and Joaquim G. Silva for assistance in the field.
(With 4 figures)

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