Variation in leaf chemistry within a tropical forest community
Substantial variation in foliage and litter chemistry was observed among 45 co-occurring neotropical rainforest tree species. Since all trees were sampled within a well-defined, homogeneous 0.98 ha area, environmental conditions such as climate and general soil characteristics can largely be ruled out as driving factors for the observed variation in leaf quality. Rather, the reported differences appear to reflect inherent species-specific characteristics.
Species identity-driven variation in leaf traits is supported by the small intraspecific variation observed in the subset of nine species from different experimental forest plots (Fig. 1), and the well conserved species-specific differences at the population level of four of the studied species (Fig. 2). This is in agreement with a study by Ricklefs & Matthew (1982) on temperate deciduous trees, where they concluded that the small variation among individuals within species can be ignored for among-species comparisons within a site. Variation within species is arguably less important than variation among species in highly species rich communities such as most tropical forests, with typically between 100 and 200 different tree species per hectare, and often only one individual canopy tree for the majority of species (Ter Steege et al., 2000). In forest ecosystems dominated by only one or a few tree species, however, intraspecific variation in litter traits can be significant for ecosystem-level processes (Madritch & Hunter, 2002; Schweitzer et al., 2004).
Functional groups of plant species sharing similar leaf traits, such as N-fixing legumes or conifers, can account for a large amount of variation in leaf chemistry (Aerts, 1996; Cornelissen et al., 1997; Perez-Harguindeguy et al., 2000; Quested et al., 2003). In our study, however, the majority of species examined belong to the rather well-defined functional group of evergreen trees with long-lived, leathery leaves. Although some of the highest N and P concentrations were measured for species from the Fabales, only four (I. alba, I. jenmanii, D. purpurea and T. paraense) out of the seven Fabales species, are actually believed to fix N (Roggy et al., 1999), and two of them (Diplotropis purpurea and Tachigali paraense) are not among the 10 N and P richest species. This suggests that N fixation contributes little to a functional explanation of the reported range in leaf chemistry in the forest ecosystem studied. The local variation in litter quality observed here is similar to that reported across different plant functional groups and along a wide climatic gradient in central Argentina (Perez-Harguindeguy et al., 2000). For example, litter C : N ratio that correlated well with decomposition in the central Argentina study, varied by a factor of 3.2 (between 16 and 51) among the functional groups of ‘woody deciduous’, ‘woody evergreen’, ‘aphyllous’, ‘bromeliads’, ‘succulents’, ‘graminoids’ and ‘herbaceous dicots’, including a total of 52 plant species (Perez-Harguindeguy et al., 2000). This compares to the difference in C : N ratio by a factor of 3.1 (between 25 and 77) in our study. A somewhat lower range in C : N ratio between 25 and 66, varying by a factor of 2.6, was reported for 22 mostly deciduous tree species from a relatively infertile dry tropical forest (Lal et al., 2001).
In conclusion, the widely different leaf traits reported here for a rainforest tree community dominated by broadleaf evergreen tree species does not readily fit the conventional concepts of plant functional groups and their segregation within a leaf trait matrix. A finer grained resolution of ‘functional groups’ based, for example, on a more detailed assessment of leaf life-spans within the group of ‘evergreens’, could perhaps contribute to a functional interpretation of the observed variation in foliage and litter chemistry.
C : N : P stoichiometry and plant nutrient use strategies
Mean foliage C : N, C : P, and N : P ratios of 37.5, 1982 and 54.3 (on a molar basis) reported here, compare well with the average molar ratios of 35.5, 2457 and 43.4 across several tropical forest studies summarized in McGroddy et al. (2004). Although we did not account for the relative abundance of species in the calculation of these data, they are approximately representative for the community studied, characterized by a low abundance of most species. Mean foliage stoichiometry is in accord with previous findings of relatively constant C : N ratios, and distinctly higher C : P and N : P ratios in tropical forests compared with other forest ecosystems at higher latitudes (Güsewell, 2004; McGroddy et al., 2004; Reich & Oleksyn, 2004). These broad global patterns across biomes indicate large-scale environmental constraints (e.g. P limitation in tropical ecosystems vs N limitation in temperate ecosystems; McGroddy et al., 2004; Reich & Oleksyn, 2004) and/or temperature related physiological processes leading to broadly different growth rates, and thus, to different N and P demands across climatic gradients (Elser et al., 2000b; Kerkhoff et al., 2005). However, such large-scale considerations might be too coarse-grained to understand evolutionary processes in nutrient use strategies. The large variance in foliage stoichiometry among canopy trees in a rather homogeneous environment at a small local scale reported here, suggest different adaptive responses to selection pressures related to nutrient limitation, and does not support the view of well-constrained terrestrial C : N : P ratios of autotrophs as was suggested by McGroddy et al. (2004). In line with our findings, Townsend et al. (2007) recently reported a strikingly large interspecific variation in green leaf N : P ratios at different tropical forest sites, and concluded that this diversity needs to be accounted for in order to understand ecosystem processes in species rich tropical forests.
Compared with green leaves, C : N : P ratios widened considerably in litter from the same individuals because of nutrient resorption, and C : P and N : P in litter showed a larger variance than in foliage (Fig. 7). Nitrogen and P concentrations were on average 30% and 65% lower in litter than in green leaves. This corresponds to an estimated mean N resorption efficiency of 40 ± 13% and a mean P resorption efficiency of 70 ± 13% across our studied species (calculated on a unit-lignin basis, data not shown). In agreement with our study, higher mean P than N withdrawal in 73 species from eastern Australian ecosystems (Wright & Westoby, 2003), and in the dominant tree species Metrosideros polymorpha in Hawaiian tropical montane forest ecosystems (Vitousek, 1998), was associated with P-poor soils suggesting higher resorption of the more limiting nutrient. Similar to the Australian study (Wright & Westoby, 2003), we reported lower litter P concentrations than most values previously published (Killingbeck, 1996), and lower than what has been observed in other tropical rainforests (Proctor, 1984; Scott et al., 1992; Chuyong et al., 2000).
The large variation in litter C : P and N : P ratios among species was driven by the considerable increase in variation of litter P concentrations (Fig. 6). The much higher variability in litter P than in green leaf P concentration contrasts with the initial hypotheses of converging interspecific differences in litter compared with foliage nutrient concentrations, and concomitantly decreasing variances in litter C : N : P compared with foliage. Phosphorus withdrawal during senescence seems to vary among species independently of their foliage P concentration (Fig. 5). If a constant proportion of foliage P was recycled from senescing leaves, as could be expected when the relative amount of mobile P is a function of total leaf P, we would expect a close correlation between foliage and litter P. Conversely, if the absolute amount of immobile P within a leaf was determined by species-independent general biochemical and/or biophysical constraints, we would expect a higher proportion of total P being recycled from comparatively high P leaves. According to our hypothesis, this would then result in converging litter P concentrations towards possible minimum values in all species and maximum P conservation under the supposedly P limiting conditions of the studied forest. Why did our data not support either one of these two predictions?
Several nonexclusive explanations might exist which would need further testing. The degree of P limitation might vary among species, which then could exhibit distinct P use strategies, including P resorption efficiencies. For example, a fertilization experiment in a secondary tropical forest indicated species-specific limitations by both N and P (Davidson et al., 2004). A common minimum P value across species might actually not exist because of multiple constraints in biochemical and biophysical processes during leaf ageing, nutrient transformation, phloem loading, and nutrient retranslocation, processes that are, at present, not well understood. Independently of any physiological processes during senescence, the amount of remaining P in fresh fallen litter may also be determined by leaf structural and morphological characteristics (e.g. thickness of cuticula). These might more or less protect P compounds from leaching during leaf senescence, thus masking potential patterns of P resorption across species. Possible differences in leaching losses from senescing leaves among species have not been assessed here; however, they are commonly not considered as a major nutrient flux (Aerts, 1996; Killingbeck, 1996).
In conclusion, the tremendous variation in nutrient proficiencies and leaf stoichiometries among neighbour trees within a single site, suggests a wide range of adaptive strategies among tree species at the level of green leaf functioning, plant nutrient acquisition, and nutrient resorption physiology, to apparent common environmental constraints. This is in contradiction to simple generalizations on plant nutrient economies based upon broad functional groups, and indicates that ecosystem-scale selection is of minor relevance for the evolution of plant nutrient use strategies.
Implications for ecosystem nutrient dynamics
The observed high variation in litter chemistry and stoichiometry among trees and the low abundance of individual species within the canopy implies a qualitatively highly heterogeneous litter input to the soil at small spatial scales. The wide range of C : N : P stoichiometry in litter, but also differences in C quality, will affect higher trophic levels of the decomposer community with varying constraints depending on the local species composition of the litter. This might have important consequences for nutrient dynamics during litter decomposition and subsequent nutrient availability, and could, thus, contribute to the larger than expected range of plant stoichiometry. Spatially separated resources can affect competitive interactions between microbes and plants (Jingguo & Bakken, 1997) and microsite dynamics in soils are fundamentally important for the understanding of whole soil processes (Jackson et al., 1989; Ettema & Wardle, 2002; Schimel & Bennett, 2004). Recent advances in microsite-based mineralization theory were mainly achieved on nitrogen dynamics in primarily N-limited northern ecosystems (Schimel & Bennett, 2004), whereas the role of functionally distinct microsites for P cycling in P-limited ecosystems is not well understood. Recent studies showed that experimental P additions to P-limited ecosystems can increase decomposition rates (Hobbie & Vitousek, 2000), as well as the mineralization of dissolved organic matter derived from litter (Cleveland et al., 2002, 2006). Whether the wide variation in litter P concentration among species observed in our study translates into spatially heterogeneous soil P availability with feedback effects on trees and their leaf nutrient concentrations remains to be tested in further studies.