Light environment and tree strategies in a Bolivian tropical moist forest:an evaluation of the light partitioning hypothesis

Lourens Poorter1,2,* and Eric J.M.M. Arets1,3

1Programa Manejo de Bosques de la Amazonía Boliviana (PROMAB), Casilla 107, Riberalta, Bolivia; 2ForestEcology and Forest Management Group, Department of Environmental Sciences, Wageningen University, P.O.Box 342, 6700 AH, Wageningen, The Netherlands; 3Department of Plant Ecology, Utrecht University, P.O.Box 80084, 3508 TB, Utrecht, The Netherlands; *Author for correspondence (e-mail:Lourens.Poorter@wur.nl; phone: +31-317478007; fax: +31-317478078)

Received 7 June 2001; accepted in revised form 2 September 2002

Key words: Bolivia, Hemispherical photographs, Irradiance, Niche differentiation, Sapling growth, Shade toler-ance

Abstract

Light partitioning is thought to contribute to the coexistence of rain forest tree species. This study evaluates thethree premises underlying the light partitioning hypothesis; 1) there is a gradient in light availability at the forestfloor, 2) tree species show a differential distribution with respect to light, and 3) there is a trade-off in speciesperformance that explains their different positions along the light gradient. To address these premises, we studiedthe light environment, growth, and survival of saplings of ten non-pioneer tree species in a Bolivian moist forest.Light availability in the understorey was relatively high, with a mean canopy openness of 3.5% and a meandirect site factor of 6.8%. Saplings of two light demanding species occurred at significantly higher light levelsthan the shade tolerant species. The proportion of saplings in low-light conditions was negatively correlated withthe successional position of the species. Light-demanding species were characterised by a low share of theirsaplings in low-light conditions, a high sapling mortality, a fast height growth and a strong growth response tolight. These data show that all three premises for light partitioning are met. There is a clear gradient in shade-tolerance within the group of non-pioneer species leading to a tight packing of species along the small range oflight environments found in the understorey.

Introduction

Tropical rain forests are characterised by a high spe-cies diversity. In the Peruvian Amazon, for example,up to 300 tree species were found in a single hectare(Gentry 1988). Several theories have been forwardedto explain this high species diversity. According to theniche differentiation hypothesis, species coexistenceis possible because each species is specialised for aspecific set of growth conditions (Grubb 1977; Rick-lefs 1977). If there is sufficient spatial and temporalvariation in growth conditions, then a differential re-sponse of the species to these conditions (in terms ofgermination, growth and survival) may eventually re-

sult in a differential spatial distribution of tree spe-cies.

In the understorey of tropical rain forest, irradianceis the most limiting resource for tree growth (Whit-more 1996). In general, only 1–2% of the incomingradiation reaches the forest floor of closed forest,which may be enhanced to up to 25% when a gap isformed in the forest canopy (Chazdon and Fetcher1984; Chazdon 1988). Tree species may differ exten-sively in the way they cope with this variation in lightconditions and it is, therefore, postulated that speciespartition the light gradient (Denslow 1980; Brokaw1985). If species are adapted to a certain light envi-ronment, then the commonness of a species depends,amongst others, on the commonness of that light en-

295Plant Ecology 166: 295–306, 2003.© 2003 Kluwer Academic Publishers. Printed in the Netherlands.

vironment. Yet, few studies have quantified at a land-scape level the spatial variation in irradiance at theforest floor (but see Clark et al. (1996) and Nicotra etal. (1999), Zagt (1997)).

Rain forest tree species have been classified intodifferent functional groups based on their light re-quirements (Swaine and Whitmore 1988). Pioneerspecies can germinate in the shade but need a highlight environment for successful growth and survival,whereas non-pioneer species are able to germinate,establish and persist in the shade (Peña-Claros 2001;Whitmore 1996). The non-pioneers can be subdividedinto truly shade tolerant species and non-pioneer lightdemanding species (Hawthorne 1995). These latterspecies have intermediate light-requirements; al-though they are able to persist in the shade, they needhigh light levels to grow successfully to larger sizes.

Despite its pivotal role as a working model in trop-ical forest ecology, little quantitative information isavailable on the light requirements of tree species indifferent stages of their life cycle. In Costa Rica, sap-lings of nine species occurred in a small range of lightenvironments with the two pioneer species occurringin significantly higher irradiance level than the non-pioneer species (Clark et al. 1993). It is well knownthat pioneer species have a quite distinct morphologyand performance compared to non-pioneer species(Ackerly 1996). However, these pioneer species re-present only a small fraction of the total pool of rainforest species. For understanding the coexistence ofthe many species in the forest we need to go beyondstudying the extremes, and show that resource parti-tioning also occurs within the group of non-pioneerspecies (Brokaw and Busing 2000; Hubbell et al.1999).

If light partitioning contributes to species coexist-ence, than three premises should be met (cf. Burslem(1996) and Brokaw and Busing (2000)); 1) there is agradient in light availability at the forest floor, 2) treespecies show a differential distribution with respect tolight, and 3) there is a trade-off in species perform-ance that explains their different position along thelight gradient.

To evaluate the three premises we studied the lightenvironment, growth, and survival of saplings of tennon-pioneer tree species in a Bolivian moist forest.

Methods

Study area

The research was carried out in forest reserve El Ti-gre (10°59� S, 65°43� W), the research site of Pro-grama Manejo de Bosques de la Amazonía Boliviana(PROMAB). Annual rainfall in the region is about1780 mm, with a distinct dry period (< 100 mm mo−1)from May till September. The forest in the region canbe classified as a lowland tropical moist forest, withsome of the canopy trees being deciduous during thedry season. Within the reserve a square four hectarepermanent sample plot (PSP) was established in 1995.The forest canopy in the PSP has a height between25 and 35 m, with some emergent trees attainingheights up to 45 m. The PSP (including only treeswith a diameter at breast height > 10 cm) has a treedensity of 544 trees ha−1, a basal area of 27.9m2 ha−1, and a species richness of at least 81 speciesha−1 (Poorter et al. 2001).

Study species

Ten tree species were selected based upon their shadetolerance and the presence of adult trees in the PSP.An initial classification of the shade-tolerance of thespecies was based on qualitative observations of re-searchers and field staff on the commonness of thetree species in disturbed, light-rich habitats or in theundisturbed forest understorey. Later this initial clas-sification was confirmed by data on the abundance,growth and successional position of the species(Peña-Claros 2001; Poorter et al. 2001; Table 1). Ingeneral, pioneer species are characterised by a lowabundance in mature forest, fast growth rates, and amaximal abundance early in succession. Shade-toler-ant species show the opposite set of characteristics,while the non-pioneer light demanding species take aposition in between. In total ten subcanopy and can-opy tree species were selected; five non-pioneer lightdemanding species and five shade-tolerant species(Table 1). The two species groups differ significantlyin their successional position (t-test on the succes-sional score, t = 3.68, df = 8, P < 0.05). For furtherexplanation see the legend of Table 1.

Light measurements

In the centre of the PSP a 10 m × 10 m grid systemwas established covering an area of 170 m × 170 m.

296

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297

In this way the study area was reduced to an area of1.96 ha, including 225 grid points. To characterise thelight environment, hemispherical photographs weretaken at 1.3 m height above each of the 225 gridpoints. Hemispherical photographs were taken in May1997 during or just after sunset, using a Canon AE1camera with a 7.5 mm 180° fish-eye lens mounted ona tripod. The photographs were scanned with a flat-bed scanner and the canopy openness and direct sitefactor (DSF) were calculated using Winphot 5.0 (terSteege 1997). Under cloudless conditions, the DSFindicates what percentage of direct radiation abovethe forest canopy reaches the forest floor based on theposition of gaps in the canopy relative to the courseof the sun-tracks. A spatial interpolation map wasmade from the canopy openness, using Surfer 5.0. Forthe same 225 grid points a modified version of Dawk-ins’ crown illumination index (Clark and Clark 1992;Dawkins and Field 1978; Table 2) was estimated. TheCrown Illumination Index (CII) is a visual estimateof the amount of light received by the tree crown. TheCII consists of an ordinal scale, with high CII valuesindicating high light levels. For a definition of the CIIclasses, see Table 2. Both the canopy openness anddirect site factor increased with the CII (Table 2, cf.Davies et al. (1998)) and the CII provides therefore arapid, repeatable and reasonable estimate of the lightenvironment.

While setting up the study, we assumed that thelight availability measured at a grid point would berepresentative for all saplings occurring within a cer-tain radius around the grid point. To verify this as-sumption we made for a random sample of 50 gridpoints additional photos at 2 and 4 m distance northof the grid point. Light availability was positivelycorrelated for points at 2 m distance (Pearson’s r =0.49 for canopy openness, and 0.45 for DSF, P <

0.001, n = 100 in both cases, data points for compari-son 0–2 m, and 2–4 m pooled), but only weakly cor-related for points at 4 m distance (Pearson’s r = 0.23,P > 0.05, n = 50 for canopy openness, and Pearson’sr = 0.28, P < 0.05, n = 50 for DSF). Given thesemoderate correlations, we decided to estimate thelight environment for each individual sapling usingthe CII.

Sapling inventory

In May 1997 we searched for saplings of the ten studyspecies in a 4 m radius around each of the 225 gridpoints. In this way, a total area of 1.13 ha was inven-toried. Only saplings that were between 0.7 and 1.9m tall were included. The abundance of saplings wassignificantly correlated with the abundance of largetrees, if P. laevis, which is an outlier, is excluded(Pearson’s r = 0.85, P < 0.01). Saplings were taggedand their stem height was measured. The number ofleaves or leaflets was counted, depending on whetherthe species had simple or compound leaves. The leaf-(lets) were classified into two different classes; lightlydamaged leaves (75–100% of the leaf area present),and heavily damaged leaves (50–75% of the leaf areapresent). Total leaf(let) number was calculated basedon the sum of lightly and heavily damaged leaves,weighted for the amount of damage present. For eachsapling the light environment was estimated using theCrown Illumination Index, henceforth referred to asCII 97. The CII 97 was estimated independently bytwo people. The two estimates were highly correlated,and did not differ significantly from each other (Ken-dall’s tau-b of concordance = 0.61, P < 0.001). Forfurther analyses, the lowest of the two CII estimateswas used. After two years sapling survival was evalu-ated, and the stem height and CII (henceforth referred

Table 2. Description of the Crown Illumination Index. The corresponding canopy openness and direct site factor (DSF) are given for asample of 225 points. Values in the same column followed by a different letter are significantly different at a P-level of 0.05 (Student-Newman-Keuls test). No data are shown for CII class 1, 4, 5 because there were no or too few observations.

Code Definition Openness (%) DSF (%)

1 No direct light – –

1.5 Low amount of lateral light 3.4 a 5.9 a

2.0 Medium amount of lateral light 3.4 a 6.3 a

2.5 High amount of lateral light 3.4 a 7.4 a

3 Part of the crown receives direct overhead light 6.0 b 16.9 b

4 Whole the crown receives direct overhead light — —

5 Crown completely exposed — —

298

to as CII 99) were measured again. All species butBrosimum show orthotropic growth. Brosimum growsplagiotropically with a very slender horizontal leadershoot. For Brosimum stem length instead of heightwas measured.

Statistics

Whether species differed in their median CII wastested with a Kruskal-Wallis test. Thereafter pairwisespecies comparisons were made using a Mann-Whit-ney U-test.

Saplings that showed clear signs of stem breakage,or had a height growth smaller than −2 cm y−1 (whichis likely to be caused by damage or measurement er-ror) were excluded from the height growth analysis.With a type III ANOVA for unbalanced design it wastested whether species differed in log-transformedheight growth. For each species the height growthwas correlated with the initial plant height, total leaf-(let) number and CII using Spearman’s rank correla-tion.

Growth, survival, and the growth response to lightdetermine to a large extent the success of a species ina given forest environment. To quantify the species’growth response to light, we used the correlation be-tween the growth and the CII 99. All three perform-ance measures were correlated with the shade toler-ance of the species. The shade tolerance was definedas the percentage of saplings of a species that occurin low-light conditions (CII 97 � 1.5). All reportedP-values pertain to 2-tailed statistical tests. All statis-tical analyses were carried out using SPSS 7.0 (Noru-sis 1997).

Results

Light availability

There was substantial spatial variation in canopyopenness at the forest floor (Figure 1a). The canopyopenness was on average 3.5% (range 0.2–10.6%;Figure 1b), and the DSF was on average 6.8% (range0–27.5%). Sites with a high canopy openness oc-curred mostly in canopy gaps and were relativelyrare; only 14.7% of the sites had a canopy openness> 5%. The CII varied from 1 to 3 (Figure 1c). How-ever, both extremes were very rare (< 1%) and mostof the sites in the understorey ( � 50%) had a CII of2.

Niche differentiation with respect to light

The species occurred in a similar range of light envi-ronments (Figure 2) but differed significantly in theirCII distribution (Kruskal-Wallis test, Chi2 = 74.5, df= 9, P < 0.001). Sclerolobium and Tachigali hadhigher levels of CII than the five shade-tolerant spe-cies (Mann-Whitney U-test, P < 0.05 in al cases, Fig-ure 2). In addition, Brosimum had a distributionskewed more towards higher CII (classes) than P.rigida. The percentage of saplings in low-light (CII97 � 1.5) varied from 23% for Sclerolobium to 51%for P. rigida. The shade-tolerant species had a largerpercentage of their saplings in low light than the non-pioneer light demanding species (t-test, t = 4.25, df =8, P < 0.01).

Survival and growth

Two-year mortality varied from 4% for Brosimum andP. laevis to 20% for Tachigali (Table 3). On average,the non-pioneer light demanding species were char-acterised by a higher mortality than the shade-toler-ant species (t-test on angular transformed data, t =2.86, df = 8, P < 0.05).

Species differed significantly in height growth(ANOVA, F9,1058 = 7.1, P < 0.001). Median annualheight growth varied from 2.7 cm y−1 for P. laevis to7.5 cm y−1 for Brosimum (Table 3). Strikingly enoughthe shade-tolerant Brosimum realised the fastestheight growth. This is caused by its typical growthform. Where all other species show clear orthotropicgrowth, Brosimum grows plagiotropically with a veryslender horizontal leader shoot. As a consequence itgrows faster in stemlength than the other species. Thegrowth of the non-pioneer light demanding specieswas therefore comparable to those of the shade-toler-ant species (t-test, t = 1.14, df = 8, P = 0.27). Thenon-pioneer light demanding species did show afaster height growth, however, when Brosimum wasexcluded from the analysis (t-test, t = 4.25, df = 7, P< 0.01).

For most species the height growth was positivelycorrelated with the CII. The correlations were stron-ger with the CII at the end than at the beginning ofthe growth period (compare correlations with CII 97and CII 99; Table 4), which is probably due to gapsthat were formed shortly after the start of the fieldstudy, or regrowth of the vegetation with time. Thenon-pioneer light demanding species showed a stron-ger correlation between growth and CII 99 than the

299

shade-tolerant species (t-test, t = 3.04, df = 8, P <0.05). For only four species the height growth wassignificantly and positively correlated with the num-ber of leaves present at the start of the evaluation pe-riod (Table 4). These species tended also to be theones with the largest number of observations.

Correlations with shade tolerance

What plant traits are associated with the shade toler-ance of the species? We defined the shade tolerance

of a species as the percentage of saplings that occurunder low-light conditions (CII 97 � 1.5). This mea-sure of shade tolerance was significantly correlatedwith the successional score of the species as derivedfrom a study on secondary forest succession (Spear-man’s r = −0.66, P < 0.05). Species that had a largeshare of their saplings under low-light conditions didalso show up late in secondary succession, as indi-cated by their low successional score (Figure 3).

All three measures of sapling performance werenegatively correlated with the shade tolerance of the

Figure 1. a) Spatial distribution map of canopy openness, b) frequency distribution of canopy openness, c) frequency distribution of CrownIllumination Index in the forest of El Tigre. The canopy openness was measured with hemispherical photographs. Hemispherical photographswere taken at every intersection of a 10 m × 10 m grid in the permanent sample plot (n = 225). In figure a the isolines connect sites with thesame value for canopy openness.

300

species. Shade tolerant species were characterised bya low mortality rate, a slow median height growthrate, and a weak height growth response to light(Spearman’s r < −0.65, P < 0.05 in all three cases,Figure 3).

Discussion

Light levels at the forest floor

Most of the forest understorey is characterised by alow light availability. As a consequence, saplings ofthe shade tolerant species tended to be more abundantthan those of the non-pioneer light demanding spe-cies. Nevertheless, the light availability at the forest

Figure 2. Relative frequency distributions of Crown IlluminationIndex in 1997 for saplings of 10 rain forest tree species. The spe-cies are ordered based on the proportion of saplings occurring un-der low light conditions (CII � 1.5). Species followed by a dif-ferent letter have a significantly different CII (Mann-WhitneyU-test based on pairwise comparisons, P < 0.008).

Table 3. Two-year mortality and median and 90th percentile of an-nual height growth for saplings of ten rain forest tree species. TheN0 refers to the sapling number at the start of the field study.

Species Mortality (%) N0 Growth (cm y−1)

Median 90th

Bertholletia 10 10 6.6 12.3

Cordia 5 22 5.6 51.2

Pourouma 14 28 6.0 34.1

Sclerolobium 15 315 7.3 47.1

Tachigali 20 181 3.9 24.6

Brosimum 4 109 7.5 18.5

P. laevis 4 23 2.7 16.7

P. rigida 6 167 3.8 11.9

Protium 5 179 4.7 16.7

Tetragastris 7 300 4.9 15.4

Table 4. Spearman’s rank correlation (r) between height growth,Crown Illumination Index at the start (CII 97) and the end (CII 99)of the growth period and total leaf number. N indicates the samplesize.

Species CII 97 CII 99 Leaf number N

r P r P r P

Bertholletia 0.22 ns 0.60 ns 0.57 ns 7

Cordia 0.02 ns 0.48 * 0.42 ns 17

Pourouma 0.37 ns 0.34 ns 0.04 ns 21

Sclerolobium 0.44 *** 0.58 *** 0.08 ns 235

Tachigali 0.18 * 0.54 *** 0.36 *** 123

Brosimum − 0.00 ns 0.22 * 0.20 * 91

P. laevis − 0.19 ns 0.34 ns 0.30 ns 19

P. rigida 0.08 ns 0.25 ** 0.16 ns 135

Protium 0.13 ** 0.45 *** 0.22 ** 159

Tetragastris 0.21 *** 0.34 *** 0.37 *** 258

*: P < 0.05, **: P < 0.01, ***: P < 0.001, ns = non-significant

301

floor in El Tigre is relatively high compared to othertropical forests. The canopy openness is 0.8 to 12times higher, the DSF is 2 to 10 times higher, and theTSF is 1 to 3 times higher compared to other tropicalforests (Table 5). The relatively high light availabilityis probably caused by the relative low, irregular, andopen canopy of the forest in El Tigre. Such a highlight availability should lead to a larger share of gap-dependent species in the vegetation (Denslow 1980).In El Tigre, pioneer species comprise 1.6% of thestems larger than 10 cm DBH (Poorter et al. 2001).

Canopy openness at El Tigre was significantly cor-related at a spatial distance of 2 m but only weaklycorrelated at a distance of 4 m. This is in line withthe findings for other forests, which show that at in-tervals of 2.5 m the light environment is spatially au-tocorrelated, whereas at distances larger than 5 m thisautocorrelation disappears (Becker and Smith 1990;Clark et al. 1996; Nicotra et al. 1999).

Sapling occurrence in relation to light

Although species occurred in largely overlappinglight ranges, there is also strong evidence that theypartition the light gradient. Two non-pioneer light de-manding species occurred in brighter light environ-ments than the shade tolerant species (Figure 2), andspecies showed a clear ranking in the proportion ofsaplings in low-light conditions, which was closelycorrelated with their successional position (Figure 3).It is likely that we even have underestimated the roleof light partitioning, as we only focused on non-pio-neer species, and used a rather coarse estimate of thelight environment. In a Costa Rican rain forest, Clarkand Clark (1992) found that saplings of 6 non-pioneerspecies differed in their CII, with two species occur-ring in brighter environments than some of the oth-ers. Davies et al. (1998) also found differences in CIIwithin a group of eleven Macaranga pioneer species.All species experienced increased light levels whenincreasing in size, because of mortality of low-lightindividuals and a closer proximity to the canopy ofthe surviving individuals. Interspecific differences inlight environment disappeared when species grewtaller and eventually recruited to the canopy. Species-specific shifts in light requirements may occur withontogeny and during different phases of the life cycle(Oldeman and van Dijk 1991; Clark and Clark 1992;Peña-Claros 2001) thus augmenting the variety ofways in which the light gradient can be partitioned.In a Guyanan rain forest, Rose (2000) compared the

Figure 3. Correlation between species’ shade tolerance and a) suc-cessional score, b) mortality rate, c) median height growth rate, d)height growth response to light. Spearman’s rank correlation andsignificance level are given. Non-pioneer light demanding speciesare represented by open symbols, and shade-tolerant species byfilled symbols. The shade tolerance of the species is defined as theproportion of saplings that occur under low light conditions (CII97 � 1.5). The successional position of the species is inferred fromthe time the species becomes abundant during secondary succes-sion (see Table 1), with a high score indicating an early-succes-sional species. To quantify the species capacity to respond to light,we used the correlation between the growth and the CII 99 (Table4).

302

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seedling light environment of 20 non-pioneer treespecies, using hemispherical photographs. Speciesshowed four different distribution patterns with re-spect to canopy openness, which suggest that the spe-cies occupy different niches along the light gradient.

Growth in relation to light and leaf area

For most species the height growth was positivelycorrelated with the CII. Other field studies also findan increase in sapling growth with an increase in ir-radiance (Dalling et al. 1998; King 1994; Wright etal. 1998; Zagt 1997). A light-dependent increase ingrowth is mainly caused by an increase in assimila-tion rate (Poorter 2001). Light-demanding specieshave a high photosynthetic plasticity, and thereforethey may show a stronger growth response to lightthan the shade-tolerant species (Poorter 1999; Rose(2000, Rose and Poorter (in press)). Sapling growthwas positively related with leaf area for 40% of thespecies evaluated (Table 4, cf. Oberbauer et al.(1988); Poorter (2001) and Zagt (1997)). This indi-cates that sapling growth is limited by the amount oflight interception, and that leaf loss due to herbivoryor leaf shedding might have important repercussionsfor plant growth (Anten and Ackerly 2001).

Plant strategies

Ultimately, the shade tolerance can be defined as thelowest light level at which a species is able to surviveand grow. This is difficult and time consuming tomeasure, and therefore we defined shade tolerancehere as the percentage of saplings of a species thatoccur under low-light conditions. In the absence ofdispersal limitation, a different distribution with re-spect to light should be evoked by environmental-in-duced differences in germination, growth and sur-vival.

Species that a-priori were presumed to differ inshade-tolerance could indeed be discriminated basedon a number of plant traits (Figure 3). Light demand-ing species were characterised by a low share of theirsaplings in low-light conditions, a high sapling mor-tality, a fast height growth and a strong growth re-sponse to light (Figure 3). Similarly, Davies (2001)found that within a group of 11 pioneer species themortality rate and diameter growth increased with themean CII of the species. Because of their high growthand mortality rates, it is relatively easy to find inter-specific differences amongst pioneer species. How-

ever, in a community-wide analysis of 142 rain foresttree species, Condit et al. (1996) also found a strongpositive association between growth, mortality, andthe tendency to colonise gaps. Most of the shade-tol-erant species were clustered at one end of this gradi-ent, while the rest were continuously distributed overa wide range.

These results indicate that rain forest tree specieshave different solutions to regenerate in a patchy for-est environment, with a predictable, low irradiance inthe understorey and an unpredictable, ephemeral oc-currence of high-light gaps (Van Steenis 1958). Aslow growth and high survival allow shade-tolerantspecies to persist in the understorey until a gap in theforest canopy is formed. In contrast, the inherentlyhigh growth rates, and stronger growth response tolight allows the non-pioneer light demanding speciesto profit from newly formed gaps by rapidly attaininga position in the canopy before the gap is closed. Yet,those plant traits that facilitate a high growth rate (lowleaf defence, high leaf turnover) do also lead to anincreased risk of mortality (King 1994; Kitajima1996; Poorter 1998).

Niche differentiation with respect to light hasserved for a long time as a working model to explainthe coexistence of a large number of tree species.Nevertheless, there is little empirical evidence howspecies can be graded according to their shade-toler-ance. As a result, the classification of rain forest spe-cies often falls apart into a quite distinct, well-knowngroup of a few pioneer species and a remaining groupof shade-tolerant species, which constitute the vastmajority of tropical tree species (Hubbell and Foster1986). This study has demonstrated convincingly thatall three premises for light partitioning are met; 1)there is a gradient in light availability at the forestfloor (Figure 1a), 2) tree species show a differentialdistribution with respect to light (Figure 2), and 3)there is a trade-off in species performance that ex-plains their different position along the light gradient(Figure 3). It is especially promising that there is aclear gradient in shade-tolerance within the group ofnon-pioneer species (Figure 3, cf. Agyeman et al.(1999)). This suggests that species show subtle varia-tions in their plant strategy, which may lead to a tightpacking of species along the small range of light en-vironments found in the understorey. Light partition-ing contributes therefore to the coexistence of treespecies, in concert with other mechanisms such aschance, density-dependent pests and recruitment lim-itation (cf. Wright (2002)).

304

Acknowledgements

We thank staff and personnel of Programa Manejo deBosques de la Amazonía Boliviana (PROMAB) forthe logistic support during this field study. We wouldlike to thank especially Bert van Ulft, MichaelDrescher, Nicolas Divico, Rene Aramayo, Luis Apazaand Miguel Cuadiay for their indispensable help withthe data collection. Frans Bongers, Marielos Peña-Claros, Tim Whitmore, Pieter Zuidema and an anon-ymous reviewer are acknowledged for their usefulcomments on the manuscript. This research wasfunded by grant BO 009701 from the NetherlandsDevelopment Assistance.

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