Soil Nutrients Limit Fine Litter Production and Tree ... - Springer Link

Ecosystems (2007) 10: 503–518 DOI: 10.1007/s10021-007-9042-y

Soil Nutrients Limit Fine Litter Production and Tree Growth in Mature Lowland Forest of Southwestern Borneo Gary D. Paoli,1,2,3,* and Lisa M. Curran3 1

Department of Ecology and Evolutionary Biology, University of Michigan, 830 N. University Ave, Ann Arbor, Michigan 48109, USA; Indonesian Resource Institute, Bogor, West Java, Indonesia; 3Yale School of Forestry and Environmental Studies, 205 Prospect Street, New Haven, Connecticut 06511, USA

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ABSTRACT Efforts to improve models of terrestrial productivity and to understand the function of tropical forests in global carbon cycles require a mechanistic understanding of spatial variation in aboveground net primary productivity (ANPP) across tropical landscapes. To help derive such an understanding for Borneo, we monitored aboveground fine litterfall, woody biomass increment and ANPP (their sum) in mature forest over 29 months across a soil nutrient gradient in southwestern Kalimantan. In 30 (0.07 ha) plots stratified throughout the watershed (340 ha, 8–190 m a.s.l.), we measured productivity and tested its relationship with 27 soil parameters. ANPP across the study area was among the highest reported for mature lowland tropical forests. Aboveground fine litterfall ranged from 5.1 to 11.0 Mg ha)1 year)1 and averaged 7.7 ± 0.4 (mean ± 95 C.I.). Woody biomass increment ranged from 5.8 to 23.6 Mg ha)1 year)1 and averaged 12.0 ± 2.0. Growth of large trees (‡60 cm dbh) contributed 38–82% of plot-wide biomass increment and explained 92% of variation among plots. ANPP, the sum of these parameters, ranged from 11.1 to 32.3 Mg ha)1 year)1 and averaged

19.7 ± 2.2. ANPP was weakly related to fine litterfall (r2 = 0.176), but strongly related to growth of large trees at least 60 cm dbh (r2 = 0.848). Adjusted ANPP after accounting for apparent ‘‘mature forest bias‘‘ in our sampling method was 17.5 ± 1.2 Mg ha)1 year)1.Relating productivity measures to soil parameters showed that spatial patterning in productivity was significantly related to soil nutrients, especially phosphorus (P). Fine litterfall increased strongly with extractable P (r2 = 0.646), but reached an asymptote at moderate P levels, whereas biomass increment (r2 = 0.473) and ANPP (r2 = 0.603) increased linearly across the gradient. Biomass increment of large trees was more frequently and strongly related to nutrients than small trees, suggesting size dependency of tree growth on nutrients. Multiple linear regression confirmed the leading importance of soil P, and identified Ca as a potential co-limiting factor. Our findings strongly suggest that (1) soil nutrients, especially P, limit aboveground productivity in lowland Bornean forests, and (2) these forests play an important, but changing role in carbon cycles, as canopy tree logging alters these terrestrial carbon sinks.

Electronic supplementary material: The online version of this article (doi:10.1007/s10021-007-9042-y) contains supplementary material, which is available to authorized users. Received 8 June 2006; accepted 11 December 2006; published online 5 April 2007. *Corresponding author; e-mail: [email protected]

Key words: ANPP; biomass increment; carbon; Dipterocarpaceae; fine litterfall; Kalimantan; land use change; nutrient limitation; phosphorus; sequestration; sinks.

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G. D. Paoli and L. M. Curran

INTRODUCTION Efforts to reduce uncertainties in regional carbon fluxes, and to assess the differential effects of land use change on terrestrial carbon pools, require a mechanistic understanding of how aboveground net primary productivity (ANPP) varies across tropical landscapes (Houghton and others 2001; DeFries and others 2002; Houghton 2005). Mature tropical forests contribute an estimated one-third of global terrestrial net primary productivity (Saugier and others 2001), but within this biome, ANPP ranges nearly tenfold (Clark and others 2001a). Much of this variation is explained by declining productivity with increasing elevation (Proctor and others 1989; Pendry and Proctor 1996), but even among lowland forests (400-fold; Figure 1a, Table 2). Biomass increment varied more widely among plots than litter production (Figure 1b, Table 2),

ranging from 5.8 to 23.6 Mg ha)1 year)1 and averaging 12.0 ± 2.0. Basal area growth ranged threefold (0.40–1.284 m2 ha)1 year)1) and averaged 0.73 ± 0.1. Within plots, basal area, and biomass growth varied significantly among tree size classes and was strongly dominated by trees at least 60 cm dbh (Figure 2). Biomass increment was weakly related to fine litterfall production (r2 = 0.176, P £ 0.05. Figure 3a), but strongly related to growth of trees at least 60 cm dbh (r2 = 0.917, P < 0.0001). ANPP, the sum of litterfall and biomass increment, ranged approximately threefold from 11.1– 32.3 Mg ha)1 year)1, and averaged 19.7 ± 2.2 (Figure 1a, Table 2). Total ANPP was significantly related to leaf litter production (r2 = 0.161, P < 0.001, Figure 3b), but this relationship was weaker than reported elsewhere (Clark and others 2001a). In contrast, ANPP was strongly related to growth of trees at least 60 cm dbh (r2 = 0.848, P < 0.0001, Figure 3c), reflecting the overwhelming contribution of large trees to biomass increment. Aboveground live biomass ranged fivefold across plots but was unrelated to fine litterfall (Figure 4a).

Aboveground productivity in Bornean rain forest

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Figure 1. Aboveground productivity in lowland tropical forest at Gunung Palung National Park, Indonesia. Tree growth and fine litterfall were monitored over 29 months in 30 (0.07 ha) plots. Litterfall was sampled in each plot using 8 litter traps (0.49 m2) collected twice each month. a Fine litterfall, biomass increment and aboveground net primary productivity (ANPP). b Separate litter fractions: leaves, coarse debris (bark plus twigs), fine debris and reproductive material. Each point is a separate plot.

Table 2. Aboveground Net Primary Productivity in Lowland Tropical Forest at Gunung Palung National Park, Indonesia Litter production

Tree growth

Leaves

Fine woody debris

Fine non-woody debris

Reproductive litter

4.8 ± 0.2 (3.5–6.4)

1.1 ± 0.02 (0.7–2.5)

1.4 ± 0.2 (0.7–2.3)

0.4 ± 0.2 (0.1–40.9)

Total

Basal area

Biomass

ANPP

7.7 ± 0.4 (5.1–11.0)

0.73 ± 0.10 (0.41–1.25)

12.0 ± 2.0 (5.8–23.6)

19.7 ± 2.2 (11.1–32.3)

Productivity was monitored over 29 months in 30 circular plots (0.07 ha; 30 m diameter) throughout an upland watershed underlain by alluvium, sedimentary and granite substrates. Litter production was monitored using eight traps (0.49 m2) collected twice each month in each plot (total sampling area = 117.6 m2 across 240 traps). Tree growth is based on all stems at least 10 cm dbh. Biomass was estimated from diameter increments using the moist tropical forest equation of Brown (1997). Estimated ANPP is the sum of litter production and tree biomass increment. Data are mean ±95% C.I. and range (parentheses). Units for litterfall and biomass increment are Mg ha)1 year)1; basal area increment is m2 ha)1 year)1.

Figure 2. Aboveground plot-wide tree growth by size-class in lowland tropical forest at Gunung Palung National Park, Indonesia. Tree growth of stems at least 10 cm dbh was monitored in 30 plots (0.07 ha) over 29 months. Growth was compared among size classes using oneway ANOVA on untransformed data. ***P £ 0.001.

Standing biomass was, however, significantly related to biomass increment (r2 = 0.328, P < 0.001, Figure 4b) and ANPP (r2 = 0.331, P < 0.001, Figure 4c). ANPP data for each plot are provided in Supplementary Document 4 (http://www.springerlink. com).

Nutrient Correlates of Fine Litterfall, Tree Growth and ANPP Fine litterfall was significantly positively related to extractable P (r2 = 0 .646, P £ 0.001, Figure 5), total bases (r2 = 0.459, P £ 0.01, Figure 5), and to lesser degrees exchangeable K, Ca, and Mg

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Figure 3. Relationships among fine litter fall, tree biomass increment and ANPP (litter fall plus biomass increment) at Gunung Palung National Park, Indonesia. Units for all axes are Mg ha)1 year)1. *P £ 0.05, ***P £ 0.001.

Figure 4. Relationships among living aboveground forest biomass and a fine litterfall, b aboveground stem biomass increment and c aboveground net primary productivity (the sum of fine litterfall and biomass increment) in lowland tropical forest at Gunung Palung National Park, Indonesia. ***P £ 0.001.

(Table 3). No significant relationships with soil texture were found. The strength of relationships with soil nutrients varied among fractions and was highest for fine woody debris and non-woody fractions (r2 = 0.611, Figure 5b) and lowest for reproductive material (r2 = 0.134, Table 3). Relationships with total nutrient pools were similar to, but generally weaker than, those of labile nutrient pools. A total of 33 significant relationships between litterfall and soil were observed, whereas at a = 0.05 only five such relationships would be expected from chance alone given the number of comparisons made. Basal area and biomass growth showed a strong positive relationship with soil nutrients, especially extractable P and CEC (Table 3; Figure 5). Relationships with individual nutrients differed between labile and total nutrient pools—tree growth was significantly related to exchangeable K, Mg, Fe, and Zn, but not total forms of these elements (Table 3). Total ANPP was most strongly

related to extractable P (r2 = 0.603, P £ 0.001, Figure 5) and CEC (r2 = 0.546, P £ 0.001); weaker significant relationships were found with extractable K and total C, N, and P (Table 3, Figure 5). A total of 28 significant relationships between soil nutrients and tree growth and/or ANPP were observed, whereas at a = 0.05 only four such relationships would be expected from chance alone given the number of comparisons made. Extractable P entered five of eight multiple linear regression models to estimate productivity and accounted for 52–100% of the total variance explained by such models (Table 4). Extractable P was the only parameter retained in a model predicting biomass increment, and also accounted for more than 80% of the variation in ANPP related to soil nutrients (Table 4). In some cases, however, inclusion of other nutrients in combination with P substantially increased explanatory power. For example, the addition of total K and Ca to a model based on extractable P nearly doubled the


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Figure 5. Significant relationships between productivity and soil nutrients were found for 75 nutrientproductivity combinations (Table 3), including examples shown here. Each point is one 0.07 ha plot; nutrient values are the mean of multiple samples per plot. Litter production and woody biomass increment were monitored over 29 months. **P £ 0.01, ***P £ 0.001.

percentage of leaf litterfall variance explained from r2 = 0.313 to 0.617 (Table 4). AGB was not retained in any of the forward selection models. Fine litterfall, biomass increment and ANPP were negatively correlated with elevation, but this appeared to reflect declining nutrients—N and P—with increasing elevation, rather than a direct effect of elevation per se. Using partial correlation analysis, the correlation between elevation and productivity was not significant after controlling for N or P, whereas correlations with N or P remained significant after controlling for elevation.

associations between biomass increment and soil nutrients occurred for trees at least 40 cm dbh; nine were for trees at least 60 cm dbh. The best predictors of biomass increment among trees at least 60 cm dbh were extractable P (r2 = 0.410, P < 0.001) and total N and C (r2 = 0.334, P < 0.001 for both; Table 5). Significant relationships between tree growth and nutrients also were found in smaller size classes (for example, subcanopy trees 20–30 cm dbh; Table 5), but were comparatively weak. Nutrient associations with basal area growth closely followed those of biomass.

Size-Dependent Associations of Tree Growth with Soil Nutrients

DISCUSSION

Associations between tree growth and soil nutrients were more common among large trees than small trees (Table 5). Thirteen of 20 significant

Aboveground net primary productivity varied widely across the 30 lowland forest plots monitored at GPNP, despite the small size (340 ha), limited elevational range (8–190 m a.s.l.) and uniform

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Table 3. Regression Analyses of Aboveground Productivity on Surface Soil Texture and Exchangeable and Total Nutrient Content in Lowland Forest at Gunung Palung National Park, Indonesia Litter production Parameter

Leaves

(a) Exchangeable K L 0.150 Ca NS Mg NS Mn L 0.140 Na NS Ni NS Fe NS Zn L 0.253 Total bases L 0.169 CEC L 0.201 Olsen P Ln 0.388 Al NS (b) Total nutrients K L 0.294 Ca Ln 0.286 Mg Ln 0.129 Mn Ln 0.181 Na L 0.147 Ni NS Fe NS Zn Ln 0.192 C NS N Ln 0.201 P Ln0 .241 (c) Soil texture % sand NS % silt NS % clay NS % coarse NS

Tree growth

Fine woody Fine non-woody Reproductive Debris debris material Total

Basal area Biomass

ANPP

L 0.396 L 0.352 L 0.488 NS NS NS NS NS L 0.530 L 0.263 L 0.292 L 0.152

Ln 0.348 L 0.161 L 0.302 NS NS NS NS NS L 0.353 Ln 0.378 L 0.611 L 0.240

NS NS NS NS NS NS NS NS NS NS NS NS

L 0.367 L 0.227 L 0.270 NS NS NS NS L 0.170 L 0.459 L 0.392 Ln 0.646 NS

Ln 0.313 NS Ln 0.195 NS NS NS L .169 Ln .200 L 0.128 L 0.490 L 0.437 NS

L 0.261 NS NS NS NS NS L 0.140 L 0.227 NS L 0.458 L 0.473 NS

Ln 0.358 NS Ln 0.207 NS NS NS L 0.155 L 0.262 Ln 0.244 L 0.546 L 0.603 NS

NS NS NS NS NS NS NS NS Ln 0.150 L 0.190 Ln 0.311

NS NS NS NS NS NS NS NS Ln 0.299 L 0.288 Ln 0.451

NS NS NS NS L 0.134 NS NS NS NS NS NS

Ln 0.136 Ln 0.155 NS NS NS NS NS NS Ln 0.224 L 0.307 Ln 0.458

NS NS NS NS NS NS NS NS L 0.438 L 0.278 L 0.300

NS NS NS NS NS NS NS NS L 0.348 L 0.313 Ln 0.301

NS NS NS NS NS NS NS NS L 0.385 L 0.384 Ln0.405

NS NS NS NS

NS NS NS NS

NS NS NS NS

NS L 0.146 NS NS

NS NS NS NS

NS NS NS NS

NS NS NS NS

Linear (L) and logarithmic (Ln) regression were performed, and significant relationships (p £ 0.05) are bold faced. If both forms of regression were significant, the form that explained more variance is shown. Variance explained (r2) is given for significant regressions, all of which had a positive slope. Productivity was unrelated to any soil texture parameter.

climate of the study area. Fine litterfall ranged more than twofold (5.1–11.0 Mg ha)1 year)1), approximating the global range for tropical forests reported by Vitousek (1984) and the more selective data set of Clark and others (2001a). Estimated biomass increment at GPNP ranged fourfold (5.8– 23.6 Mg ha)1 year)1) and, in absolute terms, showed broader variation than the pantropical data set of Clark and others (2001a) and the Neotropical data set of Malhi and others (2004). Our results at GPNP appear to reflect the influence of spatial heterogeneity of soil nutrients on tree growth, especially large trees, although some variation may also be attributed to inter-plot differences in aboveground biomass. These findings: (1) highlight

the magnitude of small-scale spatial variation in aboveground productivity present in lowland tropical forests; (2) indicate that soil nutrients, especially P, are a major determinant of this pattern; and (3) suggest an exceptionally high productive capacity for mature lowland Bornean forests on well-drained mineral soils.

Relationships Among ANPP Components Relationships among ANPP components observed here differ from those reported previously in the Neotropics. AGB increment at GPNP was, on average, 65% higher than fine litterfall (12.0 versus 7.7 Mg ha)1 year)1) and contributed up to 74.2%

Stepwise multiple linear regression was used to quantify relationships between aboveground productivity and a pooled data set of 27 soil parameters, including soil texture, pH and exchangeable and total soil nutrient content. The final model is shown with variables arranged in the order they entered the model. Total and variance related to the first independent variable in the model are shown. P values indicate significance of the overall regression. *P £ 0.05, **P £ 0.01, ***P £ 0.05.

*** 0.767 5.745 + 0.134 Pexch + 0.035 Mnexch + 0.0006 Ctot + 0.0097 Ptot

0.603

*** *** 0.473 0.490 0.473 0.707 6.67 + 0.202 Pexch 0.379 + 0.062 CEC + 0.003 Mntot - 0.0002 Catot–0.0003 Mgtot

*** *** *** * *** 0.313 0.531 0.611 0.134 0.563 0.617 0.531 0.916 0.134 0.844 + 0.0190 Pexch + 0.00002 Ktot + 0.0005 Catot + 0.001 Total bases + 0.025 Pexch +0.006 Mgexch–0.004 Kexch + 0.0004 Catot–0.001 Zntot + 0.042 Niexch – 0.000083 Natot + 0.049 Pexch + 0.004 Caexch + 0.0009 Catot–0.412 %coarse 3.712 0.329 0.999 0.783 8.303

Fine litter fall Leaf litter Fine woody debris Fine non-woody debris Reproductive material Total litter Tree growth Biomass Basal area Litter fall plus tree growth ANPP

p-value r2 first parameter Total r2 Regression equation Parameter

Table 4. Results of Multiple Linear Regression Analysis of Soil Nutrient Effects on Aboveground Productivity in Lowland Tropical Forest at Gunung Palung National Park, Indonesia


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of ANPP in individual plots. Variation in ANPP was therefore driven by differences in tree growth, not litter production. In contrast, two recent largescale, primarily Neotropical comparisons (Clark and others 2001a; Malhi and others 2004) found that the contribution of biomass increment to ANPP was on average 42% less than that of fine litterfall across sites. Further differences between GPNP and other tropical sites were observed in terms of the contribution of different size classes to forest-wide biomass increment. The growth of trees less than 30 cm dbh contributed the majority of AGB increment at two Neotropical sites (Chave and others 2003; Vieira and others 2004), whereas spatial patterns of biomass increment at GPNP were driven by growth of large canopy and emergent trees, not smaller classes. The importance of canopy and emergent tree growth to aboveground productivity at our site is most evident in the plot of large tree growth versus ANPP (Figure 3c). The overwhelming contribution of large trees to total ANPP does not imply that other components are trivial—the large positive y-intercept and moderate slope describing this relationship (y = 11.48 + 0.443x) indicates that fine litterfall and small tree growth contribute substantially to ANPP. But, from a methodological point of view, if this predictive relationship is consistent across Bornean sites with similar forest structure, it may prove useful for quantifying ANPP over large areas throughout the island, where continuous monitoring of litter production is not possible. This apparent difference between Bornean and Neotropical forests in terms of the contribution of small versus large tree growth to ANPP deserves further investigation (Paoli and others, in press). Such a fundamental difference in forest structure between regions would have important implications for understanding the impact of recent logging and land-use change on terrestrial carbon fixation in the tropics. We also found that the relationship between aboveground fine litterfall and biomass increment at GPNP (r2 = 0.176; Figure 3a) was much weaker than reported by Clark and others (2001a) for 11 tropical sites (r2 = 0.57) and Malhi and others (2004) for eight Neotropical sites (r2 = 0.76; note that axes in Figure 3a must be reversed for direct comparison with these studies). Malhi and others (2004) noted the striking similarity of slopes in this relationship between their data set (y = 1.719x) and that of Clark and others (2001a; y = 1.739x) when forced through the origin, but cautioned against concluding a general relationship, due to the under-representation of forests on rich soils in

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Table 5. Regression Analysis of the Relationship between Tree Growth (Basal Area or Biomass Increment) and Soil Factors by Size Class in Lowland Tropical Forest at Gunung Palung National Park, Indonesia. Basal area increment Soil parameter 10–20 Exchangeable nutrients P NS K NS Mg Ln 0.14 Zn NS Total bases NS CEC NS Al NS Total nutrients C NS N L 0.14 P NS Mn NS Ni NS Fe NS Soil texture Coarse (%) NS

Biomass increment

20–30

30–40 40–50

50–60 >60

L 0.17 NS NS NS NS L 0.23 Ln 0.17

NS NS NS NS NS NS NS



L 0.39 L 0.19 NS L 0.21 Ln 0.14 Ln 0.33 L 0.23

NS L 0.16 NS NS Ln 0.14 NS NS NS NS NS NS L 0.21 NS Ln 0.16

L 0.31 NS NS NS NS NS

NS NS NS NS NS NS

NS NS NS L 0.15 Ln 0.18 L 0.13

NS NS NS NS NS NS

Ln 0.25 L 0.31 Ln 0.20 NS NS NS

NS L 0.14 NS NS NS NS

L 0.31 NS NS NS NS NS

NS

NS

NS

NS

- L 0.16 NS

- L 0.14 NS

10–20

20–30

30–40 40–50 50–60 >60 NS NS NS NS NS NS NS

NS NS L 0.14 NS NS NS NS

L .16 NS NS NS NS NS NS

L 0.41 Ln 0.20 NS L 0.21 L 0.14 L 0.33 L 0.22

NS NS NS NS NS NS

NS NS NS L 0.15 L 0.18 NS

NS NS NS NS NS NS

Ln 0.23 Ln 0.33 Ln 0.23 NS NS NS

NS

NS

NS

Of the 27 chemical and texture parameters analyzed, 14 were significantly related to tree growth in one or more size classes. Linear (L) and logarithmic (Ln) regression were performed, and significant relationships (p £ 0.05) are bold faced. If both forms of regression were significant, the form that explained more variance is shown. Variance explained (r2) is given for significant regressions. All relationships were positive except for that with % coarse fraction (surface soil mineral fragments >2 mm diameter), which was negatively related to tree growth.

Figure 6. Relationship between aboveground fine litterfall and woody biomass increment for lowland rain forest at Gunung Palung National Park, Indonesia, and for the combined data sets of Clark and others (2001b) and Mahli and others (2004). Forced through the origin (following Malhi and others 2004), the slopes are b1 = 0.556 for Gunung Palung (r2 = 0.19, P < 0.01) and b1 = 1.727 for the other data set (r2 = 0.72, P < 0.001). The overall relationship is best described by a saturating power function (y = 3.58 + x0.339; r2 = 0.48, P < 0.001).

their data set. Surprisingly, the slope of this relationship at GPNP is much shallower (Figure 6), whether forced through the origin (y = 0.556x,

95% C.I. of slope = 0.474 – 0.638) or not (y = 6.44 + 0.105x, 95% C.I. of slope = 0.017 – 0.193). One possible explanation for such a different relationship between litterfall and tree growth at GPNP is the relatively high stand-level biomass increments observed at our site. Biomass increments recorded for GPNP extend far beyond the range analyzed by Malhi and others (2004), suggesting that the empirical relationship between fine litterfall and biomass increment may be a saturating function when a fuller productivity range is sampled (Figure 6). A saturating relationship could result, for example, from more efficient conversion of leaf production into tree biomass gain on more productive (that is, nutrient rich) sites due to higher canopy-level nutrient productivity (for example, Paoli and others 2005). Assessing generality of the litterfall–tree growth relationship and the mechanisms underlying its form will require simultaneous monitoring of litterfall and biomass increment across nutrient gradients throughout the tropics, especially Borneo.

Soil Nutrient Correlates of Aboveground Productivity Soil nutrients varied markedly throughout the watershed (Table 1), and were significantly asso-

Aboveground productivity in Bornean rain forest ciated with aboveground productivity at our site. Although causality is not demonstrated by the correlational approach used, repeated correlations between soil nutrients and multiple, independent measures of productivity strongly suggest a causal effect of soil factors on plant growth. The primary soil factor controlling spatial patterns of ANPP throughout the watershed appears to be soil P. Surface soil extractable P was identified in regression analyses as the best predictor of leaf, fine material and total litterfall; tree growth; and total ANPP. The finding that CEC was strongly related to biomass increment and ANPP may also be further evidence of a P effect: CEC was more strongly correlated with extractable P (r = 0.862, P < 0.001) than with total bases (r = 0.404, P = 0.027) or individual cations, of which only K, and to lesser degrees Zn and Mg, were related to productivity (Table 3). In multiple linear regression, soil P was also found to account for 60–100% of the variance explained by such models (Table 4). Together, these patterns strongly suggest that soil P is a primary driver of spatial patterns of ANPP throughout this landscape. Multiple linear regression also identified candidate nutrients that may co-limit productivity in combination with P. For example, a linear combination of extractable P, exchangeable Ca, and total Ca predicted total fine litterfall much better than P alone (r2 = 0.805 vs. 0.563; Table 4). These three parameters were uncorrelated, suggesting that Ca and P explained independent dimensions of litterfall variation throughout the watershed.

Effect of Soil Nutrients on Litterfall Versus Tree Growth In absolute terms, tree biomass increment varied more widely throughout the watershed than fine litterfall, reflecting the comparatively strong response of tree growth to soil P (Figure 7). The positive relationship between litterfall and soil P reached an asymptote of approximately 9 Mg ha)1 year)1, midway across the P gradient, whereas biomass increment increased steeply and linearly with soil P (Figure 7). Biomass increment thus accounted for an increasing proportion of total ANPP as soil P increased, indicating that the overall positive relationship between ANPP and soil P was driven mainly by the influence of soil P on tree growth compared to that of litter production. Given that canopy trees at least 60 cm dbh explained 92% of variation in biomass increment among plots, this implies that the observed relationship between ANPP and soil P throughout the watershed is

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Figure 7. Relationship between extractable soil P and the two components of aboveground net primary productivity: fine litterfall and stem biomass increment. Productivity was monitored over 29 months using 30 (0.07 ha) plots in lowland tropical forest at Gunung Palung National Park, Indonesia.

explained by the positive effect of P on growth of large trees. Future research at GPNP should investigate how nutrient availability and changes in plant functional attributes across the gradient jointly explain higher productivity on P-rich soils. The composition of tree communities varies across the nutrient gradient at GPNP, giving rise to distinct species assemblages on contrasting soils (Paoli and others 2006; Cannon and Leighton 2004). On nutrientpoor soils, plant growth is slower, but the efficiency of plant nutrient use and uptake is higher (Paoli and others 2005), and this appears to reflect intrinsic differences in growth strategy between dominant species in different habitats (Paoli 2006). Thus, spatial variation in (1) the availability of limiting resources, such as P, and (2) the intrinsic growth potential of dominant species may jointly determine spatial patterns of productivity throughout the watershed. Elucidating the joint effects of biotic and abiotic factors on productivity will enhance our understanding of controls on ecosystem dynamics (Baker and others 2003b) and improve predictive models of ecosystem response to compositional changes induced by anthropogenic and climatic disturbances.

ANPP at Gunung Palung Compared to Other Sites Mean estimated aboveground increment at GPNP was 12.0 ± 2.0 Mg ha)1 year)1. This rate is nearly twofold higher than maximum values reported by Clark and others (2001a) and slightly higher than

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the maximum (11.0 Mg ha)1 year)1) reported by Malhi and others (2004) across 104 Neotropical plots. We consider two possible explanations for this difference. First, higher productivity at GPNP partly reflects the comparatively large stature of Bornean forests compared to other tropical regions. Lowland forests on well-drained soils in Borneo are dominated by large, emergent trees in the Dipterocarpaceae (Whitmore 1984; Slik and others 2003), which produce a tall, multi-layered canopy structure (Ashton and Hall 1992) and exceptionally high basal area. For example, at GPNP, estimated mean basal area of woody plants at least 10 cm dbh across 30 (0.16 ha) plots is 39.6 ± 1.4 m2 ha)1 (G. Paoli, unpublished data). This value is typical of mature lowland Bornean forest (Proctor and others 1988; Pendry and Proctor 1996; Mirmanto and others 1999), but approximately 40% higher than the average of 227 forest inventory plots across Amazonia (Malhi and others 2006). Higher basal area on Borneo reflects the higher density of emergent and canopy trees. For example, based on an enumeration of 67 (100 · 30 m) belts randomly distributed throughout our study area (data from Curran and Leighton 2000), the density of trees at least 60 and at least 100 cm dbh at GPNP are 24 and 5 trees ha)1, respectively, more than twice that reported for Central and South American forests (Clark and Clark 2000; Chave and others 2003; DeWalt and Chave 2004). This suggests that high ANPP at GPNP compared to the Neotropics is partly explained by larger forest stature on Borneo. A second possibility is that the productivity plots we monitored are not strictly representative of the forest overall. Our plots were randomly stratified subject to the criterion that less than 30% of the plot area was in a recent gap, and three out of 30 candidate locations were rejected. Deliberate avoidance of large gaps overestimates forest-wide AGB and its increment, as well as variance around its mean, due to oversampling of large trees (Clark and Clark 2000; Clark and others 2001b; Chave and others 2003). We believe this upward bias is probably modest in the present study, however, because (1) only 10% of candidate plot locations were rejected, and (2) rates of tree mortality, and thus gap formation, are significantly lower in Borneo compared to the Neotropics (1.47 vs. 2.03% for stems ‡10 cm dbh, t = 2.432, P = 0.026; Supplementary Document 5, see http://www. springerlink.com), which would tend to lower the magnitude of ‘‘majestic forest bias‘‘ (Phillips 1996) on Borneo resulting from avoiding large gaps.

Nevertheless, we explored this bias by enlarging the forest dynamics plots from 0.07 to 0.16 ha (40 · 40 m) and quantifying forest structure based on a larger sample. The inclusion of more gap and building phase forest lowered mean estimated AGB by 29% from 718 to 518 Mg ha)1. The impact of lower AGB on biomass increment can be estimated by applying regression equations derived from Figure 4b relating biomass increment to AGB via the linear function: y = 4.045 + 0.011x. Revised biomass increment ranges from 7.3 to 14.9 Mg ha)1 year)1 and averages 9.7 ± 1.2, approximately 19% lower than the original estimate. Combined with fine litterfall, which did not vary with AGB (Figure 4a), forest-wide ANPP ranges from 12.4 to 24.0 Mg ha)1 year)1 and averages 17.5 ± 1.2. This estimate is still high in relation to other lowland sites, but falls within the upper range reported by Clark and others (2001a), who noted the absence of high biomass forests in their data set.

CONCLUSION The large stature and high productivity of a mature lowland Bornean forest reported here highlights the role of these forests in terrestrial biosphere carbon cycling and raises important questions about the impact of recent land use change on carbon emission from the region. Over the last 2–3 decades, mechanized commercial logging throughout more than 60% of lowland Indonesian Borneo land area has led to widespread declines in forest biomass, especially among large canopy trees in the Dipterocarpaceae, where losses of up to 97% of pre-felling densities have been observed (Curran and others 1999; Curran and Webb 2000). Because large dipterocarps contribute overwhelmingly to the productive capacity of these forests, the selective removal of 6–26 large trees per hectare during logging (Curran and others 1999; Curran and Webb 2000) immediately reduces short-term carbon fixation. Productivity declines may be temporary if growth of surviving trees under high light offsets declines in large tree growth (Cannon and others 1998; Chapman and Chapman 2004), but this seems unlikely for the majority of accessible sites on Borneo, especially those on rich soils, because of excessive logging damage, widespread illegal logging and government policies that promote conversion of logged forests into industrial oil palm plantations (Curran and others 1999, 2004). Further research is required to assess the aboveground productivity and biomass of logged and unlogged forest throughout Borneo, and its relationship to

Aboveground productivity in Bornean rain forest soil factors, especially P, in order to model the implications of recent land use change on biosphere carbon emissions from the region. The future integration of productivity data with geologic, soil, and topographic maps across Borneo will provide refined baselines of original productivity potentials across several forest types on the island. Coupled with land use change datasets, these estimates will allow predictions of change in regional terrestrial carbon pools based on a suite of environmental variables that capture the largescale environmental heterogeneity present in these landscapes.

ACKNOWLEDGMENTS We are grateful to the Indonesian Institute of Sciences (LIPI) and the Department of Forest Protection and Nature Conservation (PHKA) for granting permission to conduct research in Indonesia. We thank our Indonesian sponsor, the Center for Research and Development in Biology (PPPB), for logistical support, and the students and faculty of Universitas Tanjungpura, for participating as our research counterparts. Farizal, Hon, Tang and Morni provided vital assistance in the field, and A. Budiman, Sugarjito, Ibu Ina, N. Paliama, and M. Sinaga provided logistical support. We thank R. Houghton, L. De Mattia, D. Goldberg, A. Gorog, K. Judd, S. Trigg, J. Vandermeer, D. Zak and three anonymous reviewers for critical comments, and M. Hardiono and A. McDonald Pittman for GIS computations of geological substrate and land use categories. Financial support for G.D.P. from the Fulbright Indonesia Program and the University of Michigan and L.M.C. from NASA Earth Science Program (NAG 511335 and 511161), the University of Michigan and the Yale School of Forestry and Environmental Studies and the Santa Fe Institute.

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