Original articleLeaf structure vs. nutrient relationships vary with soil conditions in temperate shrubs and trees
Introduction
The concentrations of foliar N ([N], Sobrado and Medina, 1980, Reich and Walters, 1994, Schulze et al., 1994, Niinemets et al., 2002) and P ([P], Sobrado and Medina, 1980, Bongers and Popma, 1990, Reich and Walters, 1994, Niinemets et al., 2001) often increase with increasing specific leaf area (SLA, leaf area per dry mass). Such relationships may partly be explained by a larger fraction of support structures in thicker and denser leaves that possess a lower SLA, and accordingly by a reduced requirement for mineral nutrients for construction of foliage with low SLA Sobrado and Medina, 1980, Reich et al., 1992, Niinemets et al., 1998, Niinemets et al., 1999. Since the nutrient vs. structure relations are frequently observed, it has been suggested that they represent fundamental convergence in leaf formation and functioning (Reich et al., 1999). Provided such relationships occur for all combinations of environmental factors, they would have paramount significance in regional and global scaling of stand leaf area and foliage carbon gain capacities.
In some situations, SLA vs. nutrient relationships are poor, disagreeing with their fundamental nature. For instance, the strength of SLA vs. [N] relations may be different in communities of varying water availability (Wright et al., 2001). Such differences may partly be explained by modifications in support investments due to changes in water availability (Niinemets, 2001). However, the hypothesis of the scaling of leaf nutrient concentrations with SLA due to alterations in fractional support investments does not explain why in some instances there are strong relationships of SLA with both [N] and [P], but in other cases only with one of these nutrients. Depending on nutrient supply from the soil, mineral nutrient contents may vary largely at a common SLA (e.g., Thompson et al., 1992). This probably arises from the circumstance that not all the foliage P and N are associated with cell metabolic functions. In fact, the nutrients in excess may be stored in the vacuoles Rebeille et al., 1983, Leigh and Storey, 1991. This may further indicate that more severely limiting nutrients present in only functional cell compartments have the strongest relationships with SLA, while the concentrations of less limiting elements may more strongly fluctuate due to the presence of the non-metabolic storage.
Nitrogen is generally considered as the most limiting nutrient in earth ecosystems, but there is increasing evidence that phosphorus may be the primary limiting element in many communities on acidic soils. Severe P limitations have been observed in tropical forests on soils rich in iron and aluminum forming insoluble compounds with phosphate Vitousek and Sanford, 1986, Reich et al., 1995, in temperate fens and bogs, where the availability of P is limited by slow turnover of organic P compounds Wilson and Fitter, 1984, Wassen et al., 1995, Niinemets et al., 2001, in Mediterranean-type ecosystems (Niinemets et al., 1999) and in temperate forest communities (Prescott et al., 1992) where both P immobilization by soil micro-organisms and P occlusion on soil minerals may play a role. Phosphate salts with Ca and Mg are also poorly soluble at higher soil pH (Lindsay and Vlek, 1977), and accordingly, P availability may be low in alkaline calcareous soils as well (e.g., Clement and Gessel, 1985). However, little attention has been paid to this potential P limitation resulting from the low mobility of P in alkaline soils. So far, the leaf structure/nutrient relationships have been studied only in acidic soils, but gaining insight into the generality of these relations requires more advanced understanding of the potential variability of these relations in different soils.
To test the hypothesis that the correlations between foliar nutrient concentrations and SLA are dependent on the mineral nutrient supply from the soil, we studied foliar morphology and stoichiometry of mineral nutrients in widespread perennials in a wooded meadow on calcareous soils, in a bog on very acidic soils and in a flood plain on moderately acidic soils. Primary production of herbaceous vegetation has been previously shown to respond primarily to P rather than to N in the wooded meadow (Pork, 1979) and in the bog Paavilainen, 1980, Finér, 1992, while the flood plain vegetation is mainly limited by N (Pork, 1963). Thus, we hypothesized (1) that P is present in limiting concentrations in the foliage in the bog and wooded meadow, but not in the flood plain, that [P] and [N] are positively correlated, and that other mineral elements are in a satisfactory supply. We further suggested (2) that there is a stronger positive relationship between [P] and SLA, than between SLA and other mineral nutrients in the P-limited ecosystems.
Within the same community, foliar nutrient concentrations vary largely among different species and among different individuals of the same species despite similar soil conditions Ricklefs and Matthew, 1982, McJannet et al., 1995, but the plant and species characteristics responsible for this variability are still poorly understood. Although such species and plant effects may be superimposed by general constraints on variation of leaf structure and nutrient contents, they may significantly alter the strength and predictive ability of these relationships. Total height of sampled woody plants varied by two orders of magnitude across the species in the current study. Since the plant ability to capture less mobile soil nutrients such as phosphate strongly depends on extensive root systems exploring large soil volumes, but that of more mobile mineral nutrients such as nitrate does necessarily not (Sands and Mulligan, 1990), we suggested that (3) foliar concentrations of less-mobile soil mineral nutrients are greater in larger woody plants, and that (4) this pattern is more evident in the case of more limiting nutrients.
Section snippets
Study sites
The work was conducted in three sites of contrasting soil conditions in Estonia. The first site was an open woodland on calcareous alkaline soils in Laelatu (58°36′ N, 23°35′ E; elevation 2–5 m above sea level; Kull and Zobel, 1991). Species-rich herb layer is dominated by Briza media L., Carex flacca Schreb., Festuca rubra L., Filipendula hexapetala Gil., Schorzonera humilis L. and Sesleria coerulea (L.) Ard. (Kukk and Kull, 1997). Sparse shrub layer mainly consists of 2–4 m tall Cornus
Nutrient concentrations in relation to foliar morphology
In the wooded meadow, foliar [P] and SLA were positively correlated (Fig. 1), but the concentrations of other mineral nutrients were not related to SLA. [N] varied little among all plants, and was considerably less at higher values of SLA than expected on the basis of a general relationship derived from the data covering six earth biomes (Reich et al., 1999). The concentrations of foliar Ca, Mg and K varied two- to fourfold across the species and foliar morphologies (Fig. 1), suggesting either
Foliage nutrient concentrations in calcareous and acidic soils
In the wooded meadow, average [P] was just above the level (0.125–0.135%) considered limiting for tree species, foliar [N] was relatively low as well, but Ca, K and Mg concentrations (Table 1) were several-fold higher than the limiting concentrations (cf. Rode, 1993, for a review of leaf nutrients in temperate trees). Ca concentrations exceeded the limiting range by threefold, K by twofold, and Mg by ninefold. Clearly, the cation supply was lower in bog and flood plain plants, but it was still
Acknowledgements
Financial support was provided by the Estonian Science Foundation (Grants 859 and 2661 to K.K., and 4584 to Ü.N.) and the Estonian Ministry of Education and Science (grant 0182468As03). We thank Tiina Elvisto for providing the unpublished data of late-season foliar nutrient contents, and Angelika Portsmuth, Juhani Püttsepp and Ülle Püttsepp for assistance with plant and soil sampling. Thoughtful suggestions of the reviewers have significantly contributed to maturation of this paper.
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