Strong biases in the spatial distributions of tropical tree species in relation to edaphic variation have been widely reported (Swaine 1996; Clark et al. 1998; Svenning 2001; Lee et al. 2002). However, very few tests of soil-related differences in tree performance have been conducted in the field (e.g. Davies 2001; ter Steege 1994). Soil-related habitat specialization, as shown by significant differences in seedling performance between soil types, was found in four of the six species investigated in this study. Dryobalanops lanceolata and Hopea dryobalanoides had spatial distribution patterns in natural forest biased toward higher-nutrient udult soils, and had significantly greater relative growth rates in udult soils. Shorea laxa and Swintonia schwenkii had the opposite pattern with spatial distribution biases and higher growth rates on nutrient-poor humult soils. In contrast, the growth of Dryobalanops aromatica, a species of humult soils, and Shorea balanocarpoides, a more widely distributed species, were not significantly affected by soil type in this experiment.
performance and allocation patterns
Despite significant among-species differences in growth response to soils, the rank order of species performance was similar between soil types (Table 8; Kendall's Coefficient of Concordance, W = 0.5, P = 0.06). In the forest understorey, growth rates did not differ significantly among species. In gaps on udult soil, udult-soil species significantly outperformed all other species, but, on humult soil, the humult-soil species did not significantly outperform the udult species (the udult species had similar mean growth rates to two of the humult species and had significantly higher growth rates than one of the humult species). Performance ranking on nutrient-poor humult soils was more strongly associated with allocation patterns than with soil preferences. Dryobalanops lanceolata, H. dryobalanoides and D. aromatica had the highest growth rates on both soils, and had significantly different allocation patterns to the other species. On udult soil in gaps, these three species had significantly greater relative leaf allocation (Fig. 4b), less root allocation, greater fine root allocation (Fig. 4d), and higher SLA and LAR than the other species (Table 6). On humult soils, these three species greatly increased allocation to roots, particularly to fine roots, and reduced leaf allocation. However, despite reduced allocation to leaves on humult soils, these species maintained greater LARs than the other three species, through the combined effects of greater leaf allocation and higher SLA (Table 6). On humult soils, RGRd was strongly positively correlated with both LAR (Spearman rs = 0.886, P = 0.012) and SLA (rs = 0.829, P = 0.042) among species. Greater LARs probably resulted in higher growth rates on humult soils, because photosynthetic rates of seedlings differ only slightly among the six species (Palmiotto 1998). RGR is strongly positively correlated with LAR and SLA across a wide range of plant species (Reich et al. 1992; Cornelissen et al. 1996), and species with higher RGRs tend to perform better in both low and high soil nutrient environments (Grubb et al. 1996; Huante et al. 1995).
Table 8. Rank of relative diameter growth rates among the six species grown in two soils and two light environments, with treatments pooled. Ranks are indicated from highest, 1, to lowest, 6, growth rates. Different letters after the ranks for GAP treatments indicate significant differences in mean growth rates among species. There were no significant differences in growth rates among species for understorey plants. Species are arranged as in Table 2. Letters after the species codes indicate species habitat associations: h − humult, u − udult, w − widely distributed
|DRYOLA||(u)||3||2||3 ab||2 b|
|HOPEDR||(u)||2||1||2 ab||1 a|
|SHORBA||(w)||6||3||5 c||4 d|
|DRYOAR||(h)||5||6||1 a||3 c|
|SHORLA||(h)||4||5||6 c||6 d|
|SWINSC||(h)||1||4||4 b||5 d|
The species with the highest RGRs, LARs, SLAs and the greatest plasticities (sensuStrauss-Debenedetti & Bazzaz 1991) in allocation patterns in this study were the species of the high-nutrient udult soils. This pattern has been reported from both temperate and tropical forests (Grime 1979; Chapin et al. 1986; Grubb et al. 1996). Species of low-nutrient, drought-prone soils typically have relatively thick, long-lived leaves, and low plasticities of SLA and root allocation (Coomes & Grubb 2000). Comparison of the species pairs that had significant soil-related growth responses in this experiment, D. lanceolata and H. dryobalanoides (udult species) vs. S. schwenkii and S. laxa (humult species), illustrates this pattern clearly. However, the humult-soil species, D. aromatica, did not fit the pattern. Although D. aromatica is a species associated with humult soils throughout its geographical range (Ashton 1964; Baillie et al. 1987; Potts et al. 2002), it had allocation patterns more similar to the udult species. Nevertheless, there were subtle differences between D. aromatica and the udult species that might explain their different distribution patterns. On udult soil in gaps, D. aromatica behaved similarly to the udult species, with greater survival, higher leaf allocation, higher SLA and consequently higher LAR than the other humult species, although it did not have significantly increased growth on udult soil. On humult soil it differed from the udult species in having somewhat lower SLA and LAR. This was especially the case for smaller seedlings on humult soils where the allometric relationship shows lower leaf and greater root allocation than in the two udult species (Fig. 6). This may provide D. aromatica with an advantage in the case of short-term drought on humult soil.
Figure 6. Comparison of allometric relationships between leaf and root biomass allocation for the three species with the highest relative growth ratess. Relationships are for seedlings grown in gaps in udult and humult soils. P-values indicate the significance of differences in the intercept of the allometric model among species. Slopes did not differ significantly for either soil (P > 0.3). Reduced major regression results were: D. aromatica (udult: r2 = 0.73, humult: r2 = 0.60), D. lanceolata (udult: r2 = 0.70, humult: r2 = 0.49), and H. dryobalanoides (udult: r2 = 0.83, humult: r2 = 0.60).
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The udult-soil species live in close proximity to the humult soil (Fig. 1), and disperse at least some of their seeds onto the humult soil. At Lambir, seedling establishment for the udult-soil species, D. lanceolata, is significantly lower on humult soils (Itoh 1995b), but some seedlings do survive there. Seedlings of this species that survive on humult soil are expected to have higher growth rates than co-occurring humult-soil species. However, the higher growth rates of udult species on humult soils may be relatively unimportant if these species suffer a long-term performance disadvantage on humult soils. The contrasting characteristics of udult and humult species in this study suggest that there is a trade-off between high RGR, SLA, LAR and plasticity, and some aspect of performance on humult soils. Although north-west Borneo has an aseasonal climate (Walsh 1996), infrequent droughts occur in the region which may significantly affect tree survival (Becker et al. 1998; Nakagawa et al. 2000; Delissio & Primack 2003; Potts 2003). As mentioned above, humult soils in Lambir have significantly higher sand contents and significantly lower water-holding capacity than udult soils (Palmiotto 1998). High leaf allocation and SLA may be a significant liability in the event of unpredictable drought in soils of low water-holding capacity. Mortality was significantly elevated on humult soils in this experiment for one udult species (D. lanceolata). However, D. aromatica (humult) and S. balanocarpoides (widespread) also had higher mortality rates on humult soils. During the almost 2 years of the experiment there was no significant dry period, and it seems unlikely that the seedlings experienced much drought stress. What caused these higher mortality rates on humult soils remains unknown.
performance and soil resources
The two udult-soil species, D. lanceolata and H. dryobalanoides, performed significantly worse on humult soils than on udult soils. Greatly increased allocation to roots, particularly to fine roots, on humult soils by these species suggested the lack of a soil resource. Humult soils had significantly lower levels of total P than udult soils prior to the experiment, and seedlings on humult soils had significantly lower leaf-tissue P concentrations than seedlings on udult soils at the end of the experiment. The experimental addition of P increased available P in the soil, and increased leaf and fine-root P concentrations, however, there was no evidence that P availability limited the growth of D. lanceolata or H. dryobalanoides in either soil or light environment. Furthermore, we found no evidence that variation in P availability constrains the distribution of any of the six species.
Responses to nutrient addition by both temperate and tropical tree species are known to depend on light availability (Latham 1992; Grubb et al. 1996; Bungard et al. 2000), with more positive responses usually occurring in moderate to higher light levels (Coomes & Grubb 2000). Seedlings in gaps in this experiment received around 17% of full sun (c. 7.6 mol m−2 day−1). This would have resulted in significant periods at or above photosynthetic light saturation for these species (Barker et al. 1997; Bungard et al. 2000). Although these species can grow faster in even higher light levels (Zipperlen & Press 1996), it seems unlikely that the lack of a growth response to P addition by the species in this experiment was due to limited light availability.
All five dipterocarp species in this experiment are ectomycorrhizal and S. schwenkii is endomycorrhizal (P. A. Palmiotto, personal observation). Earlier work with potted seedlings has suggested that P is not limiting seedling growth in undisturbed forest for species that are mycorrhizal (Burslem et al. 1995). Our results support this finding. In one species, D. lanceolata, lower RGRd on non-native humult soils was correlated with lower mycorrhizal colonization. However, humult soils also had significantly lower levels of several other essential nutrients including Ca, Mg, K, and N, and D. lanceolata leaf-tissue on humult soils had significantly lower concentrations of several nutrients. Any one or a combination of these differences may explain the soil effects on growth. Lower growth rates of the udult forest species on humult soils may also be explained by the unfavourable water status on the more freely draining humult soil, although there was no significant drought during the experiment. Further work with interactions between mycorrhizas and soil nutrients, and with water relations is required for the species specializing on different soils at Lambir.
The three humult-soil species grew either more slowly (S. laxa and S. schwenkii) or no differently (D. aromatica) on the more nutrient-rich udult soils than on humult soils. For both humult-soil species that were tested, S. laxa and D. aromatica, leaf tissue concentrations of P and several other nutrients were significantly higher on udult soils. In addition, none of the humult species responded to P addition on either soil. These results suggest that the differential soil response in these species was not related to nutrient availability. Possible explanations for the reduced growth of these species on the clay-rich, udult soils may include greater water-holding capacity of udult soil resulting in occasional anoxic conditions in the rooting zone (Silver et al. 1999), an alien mycorrhizal flora on the udult soil, or the toxic effects of higher Al or Fe concentrations on udult soils (Sollins 1998). Trenching experiments coupled with careful monitoring of the mycorrhizal community might elucidate the causes of these performance differences.
In addition to differences in soil nutrient concentrations and water-holding capacity, humult and udult soils differ significantly in the depth of the organic humus layer (Palmiotto 1998). Experimental removal of the humus layer (see Methods section) was expected to influence either soil moisture or nutrient availability particularly on humult soils where the humus layer is up to 15 cm thick. However, humus removal had no significant effect on soil nutrient concentrations, and there were no significant effects of this treatment on growth (data not shown). The potential role of the humus layer in buffering soil moisture in the upper soil layers during episodic drought thus needs further study.
The evidence presented here strongly supports the hypothesis that edaphic variation directly contributes to the spatial aggregation of tree species in the Lambir forest. The six species used in this study coexist within the lowland dipterocarp forest in Lambir in north Borneo. Five of the six species are spatially aggregated on either nutrient-rich or nutrient-poor ultisols, and four of them perform better on their own soil. We found no evidence that this edaphic specialization is related to soil P. Further field experimental work on seedling water relations and a broader range of potentially limiting nutrients, coupled with studies of the role of mycorrhizas in these systems is required. It has been estimated that c. 60% of the tree species in the Lambir plot have spatial distributions biased across edaphic and topographic gradients in the 52-hectare plot. Edaphic specialization is therefore likely to be important for the coexistence of species in this diverse tropical forest.