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Over large areas of the tropics, savanna and forest vegetation coexist in a mosaic at landscape and regional scales. In general, forest vegetation is associated with greater nutrient or water availability (Furley 1992; Ruggiero et al. 2002), but often this association is imperfect or non-existent (Gillison 1983; Bowman 1992, 2000; Furley 1992; Haridasan 1992; Schwartz et al. 1996; Fölster et al. 2001). Several factors may explain a weak association between vegetation type and soil properties. First, savanna–forest boundaries are known to shift location in response to climate and fire regimes (Kershaw 1986; Hopkins 1992; Desjardins et al. 1996; Schwartz et al. 1996; Sanaiotti et al. 2002), so vegetation distribution is not expected to be always in equilibrium with soil properties. Additionally, the distribution of a forest may be limited by total nutrient stocks at the site, rather than the amount in the soil (Haridasan 1992). In the tropics, where a large fraction of ecosystem nutrient stocks resides in the vegetation, soil nutrient concentrations might give a poor reflection of overlying vegetation. Finally, the vegetation itself can substantially affect soil nutrient availability, with soils becoming enriched under trees due to higher litter inputs and reduced fire frequency (Kellman 1979; Belsky et al. 1989; Mordelet et al. 1993). Therefore, even where vegetation is strongly associated with soil properties, it is often unclear whether the soil determines the distribution of vegetation types or vice versa.
The boundary between savanna and evergreen forest is characterized by a transition not only in tree density, but also in tree species (Adejuwon & Adesina 1992; Felfili & Junior 1992), with few species being common to both environments. Savanna and forest tree species differ in fire tolerance, allocation patterns, stature, and requirements for seedling establishment (Hoffmann & Franco 2003; Hoffmann et al. 2003, 2004), yet studies on the determinants of savanna and forest have typically not acknowledged the role of species traits in governing vegetation structure and dynamics. Furthermore, although nutrient availability is often purported to determine the distribution of savanna and forest, little is known about differences in the nutrient requirements of savanna and forest species. Hoffmann & Franco (2003) did not find a difference between savanna and forest seedlings in response to nutrient availability; however, the levels of nutrient addition in that study appear to have been too low or too short (150 days) to elicit a strong growth response overall, making observation of differences in nutrient requirements among species unlikely. Other studies suggest a tendency for higher foliar concentrations of some nutrients in evergreen forest species relative to savanna species (Fensham & Bowman 1995; Högberg & Alexander 1995; Schmidt et al. 1998; Schmidt & Stewart 2003). These studies revealed considerable overlap in nutrient concentrations between the two groups of species, and none controlled for soil conditions, making it uncertain whether species traits or environment were responsible for observed differences. Similarly, Haridasan (1992) did not find clear differences in mean leaf nutrient concentration between cerrado savanna and cerradão, a vegetation type commonly classified as forest (Ribeiro & Walter 2001) but which typically contains a mixture of savanna and forest tree species.
Despite the ambiguity of previous results, we expect forest species to exhibit higher leaf nutrient concentrations than savanna species due to differences in specific leaf area (SLA: leaf area per unit leaf mass). In the Cerrado region of Brazil, forest species tend to have higher SLA than savanna species, at least as seedlings (Hoffmann & Franco 2003), while nutrient concentration is strongly and positively correlated with SLA (Reich et al. 1997). Although the relationship between SLA and foliar nutrients appears robust across biomes and growth forms (Reich et al. 1997), water availability can substantially alter this relationship (Wright et al. 2001). For a given value of SLA, plants on drier sites can exhibit higher foliar concentrations of N and P, possibly because higher concentrations of Rubisco permit more complete drawdown of internal leaf CO2 concentration (Wright et al. 2001). This would result in higher water-use efficiency (WUE) by allowing the plant to photosynthesize effectively with lower stomatal conductance (WUE, Field et al. 1983; Wright et al. 2001). Therefore, although we expect forest species, which should be adapted to higher water availability, to have higher leaf nutrient concentrations due to their greater SLA, we also expect that, after controlling for SLA, savanna species will have higher N and P concentrations than forest species. In partial support of this hypothesis, Franco et al. (2005) found cerrado savanna trees to have consistently higher maximum net assimilation rates (Amax) than expected from the universal relationship between Amax and SLA obtained across multiple biomes (Reich et al. 1997), but unfortunately a direct comparison with tropical forest species was not possible. Furthermore, we expect savanna species to exhibit higher WUE than forest species and that, among species, WUE will be positively correlated with N concentration. We tested these hypotheses within a phylogenetic context for tree species of the savannas and gallery forests of the Cerrado region of central Brazil, while controlling for site conditions by selecting only individuals that established in open savanna vegetation.
We also tested for differences in foliar δ15N between savanna and forest species growing under similar environments. Savanna species have been shown to have lower values of δ15N than forest species in Australia (Schmidt & Stewart 2003) and Africa (Högberg & Alexander 1995). This contrasts with the widely observed pattern that plants tend to have higher δ15N in dry, rather than wet, environments (Schulze et al. 1998; Austin & Sala 1999; Handley et al. 1999; Swap et al. 2004). In these studies, the authors attribute these trends in leaf δ15N to site differences in nutrient-cycling processes, rather than to genetically determined differences between savanna and forest species. Nevertheless, foliar δ15N can be strongly influenced by species traits, particularly by associations with N2-fixing bacteria, ectomycorrhizas or vesicular–arbuscular mycorrhizas (Högberg & Alexander 1995). As it is unclear whether differences in 15N concentration between savanna and forest are determined entirely by ecosystem-level differences in nutrient cycling, rather than species traits, we compare foliar 15N of savanna and forest tree species under similar environments.
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Overall, leaves of forest species had 17% higher N concentration, 32% higher P concentration and 37% higher K concentration than leaves of savanna species (Table 1). Savanna species had higher mean values of δ13C and N : P ratio than forest species (Table 1). The concentrations of other nutrients, as well as δ15N, did not differ between plant types when compared with a factorial anova including genus as the second factor (Table 1).
Table 1. Mean (± SE†) specific leaf area (SLA) and nutrient and isotope concentrations of leaves of savanna and forest trees
|Parameter||Savanna species||Forest species||Ptype‡||Pgenera‡|
|SLA (cm2 g−1)|| 57·3 (4·0)|| 87·1 (4·8)||<<0·001||0·16|
|N (%)|| 1·48 (0·16)|| 1·73 (0·14)|| 0·003||0·0001|
|P (%)|| 0·067 (0·0072)|| 0·089 (0·0077)|| 0·002||0·006|
|K (%)|| 0·57 (0·078)|| 0·79 (0·12)|| 0·04||0·015|
|Ca (%)|| 0·55 (0·061)|| 0·78 (0·13)|| 0·08||0·015|
|Mg (%)|| 0·16 (0·015)|| 0·18 (0·022)|| 0·35||0·0031|
|Fe (mg kg−1)|| 107·4 (10·8)|| 95·5(5·9)|| 0·37||0·062|
|Mn (mg kg−1)|| 214 (51)|| 115 (25)|| 0·08||0·31|
|Zn (mg kg−1)|| 24·3 (1·3)|| 26·5 (2·1)|| 0·45||0·09|
|Cu (mg kg−1)|| 7·43 (2·19)|| 9·01(2·92)|| 0·09||0·0002|
|N : P ratio|| 22·6 (1·1)|| 20·5 (1·9)|| 0·02||0·002|
|δ13C ()||−27·76 (0·25)||−28·44 (0·23)|| 0·02||0·14|
|δ15N ()|| 0·25 (0·50)|| −0·53 (0·77)|| 0·34||0·18|
Forest species had significantly greater SLA than savanna species in all but two of 14 genera (Fig. 2). Overall, the SLA of forest species was 52% greater than that of savanna species (Table 1). Across all species, foliar concentrations of N, P, K, Fe and Cu were positively correlated with SLA, while N : P ratio was negatively correlated with SLA (Fig. 3). In all cases except Fe, differences in SLA were sufficient to explain differences in mean concentrations between savanna and forest species, as there was no significant difference between savanna and forest species once SLA is taken into account with analysis of covariance. In the case of Fe, savanna species had higher concentrations than forest species after factoring out SLA (Fig. 3).
Figure 2. Mean specific leaf area (± SE) of congeneric savanna and forest species. Significance levels determined by t-test: *, P < 0·05; **, P < 0·01; ***, P < 0·001; ns, not significant.
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Figure 3. Relationship between specific leaf area (SLA) and nutrient content for savanna and forest species. Where no regression line is present there is no significant correlation between nutrient concentration and SLA. Where a single regression line is present the correlation is significant (P < 0·05), but the relationship does not differ between savanna and forest species. For iron, savanna species had a higher concentration (upper line) than forest species (lower line) after accounting for SLA.
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Although forest species had higher concentrations of several nutrients, savanna species tended to have higher nutrient content per leaf area. This difference was significant for N (2·6 vs 2·0 g m−2, P = 0·001); Mg (297 vs 213 mg m−2, P = 0·01); Fe (19 vs 11 mg m−2, P = 0·0007); Zn (4·5 vs 3·1 mg m−2, P = 0·003); and Cu (1·20 vs 0·97 mg m−2, P = 0·03, data not shown). For all elements except Cu, these differences can be explained by a significant negative correlation between SLA and nutrient content per area (P < 0·05, data not shown).
Phylogenetically independent contrasts confirmed most of the trends observed in the comparisons among species (Fig. 4). The contrasts for mass-based concentrations of P, K and N, as well as N : P ratio, were significantly and positively correlated with the contrast for SLA, although Cu was only marginally correlated with SLA (P = 0·057), and Fe was not (P = 0·44). When examined with phylogenetically independent contrasts, nutrient content on a leaf-area basis was negatively correlated with SLA for N, P, Ca, Mg and Fe (P < 0·05), but not for K or Cu (data not shown). The contrast for δ13C was negatively correlated with that for SLA (r2 = 0·43, P = 0·02; Fig. 4), although this relationship was largely dependent on a single point corresponding to the contrast between the two Schefflera species. When either of these taxa was removed from the analysis, the relationship was no longer significant.
Figure 4. Relationships between phylogenetically independent contrasts (PIC). All relationships shown have significant correlations (P < 0·05).
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Leaf δ13C was not correlated with N (r2 = 0·005, P = 0·73) or P (r2 = 0·012, P = 0·57) when tested across species, nor when tested with phylogenetically independent contrasts (r2 < 0·08, P > 0·16). When tested across all species there was a weak positive correlation between leaf δ15N and total N (Fig. 4, r2 = 0·17, P = 0·03), and between δ15N and P (Fig. 4, r2 = 0·20, P = 0·009). Both these relationships became non-significant when tested with phylogenetically independent contrasts (r2 < 0·12, P > 0·07). δ15N was negatively correlated with soil pH and positively related with available Al3+ (Fig. 5). These relationships were significant regardless of whether individual values or species means were used. Nevertheless, soil pH does not account entirely for observed species differences; when tested with ancova with soil pH as a covariate, there was significant variation among species (F24,51 = 3·18, P = 0·003).
Figure 5. Interspecific variation in δ15N. Filled circles, savanna species; open squares, forest species. All relationships were also statistically significant when tested among individuals, rather than among species as shown here.
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The study individuals occurred in acidic (mean pH = 5·0 in H2O) and dystrophic soils typical of cerrado savannas. The soils on which the study individuals of the savanna species occurred did not differ from soils on which the forest species occurred for N (P = 0·11), K (P = 0·08), Ca (P = 0·29), Mg (P = 0·21), Fe (P = 0·82), Mn (P = 0·47), Zn (P = 0·74), Cu (P = 0·09), pH (P = 0·19) and C (P = 0·13). However the forest species did tend to occur in soils of higher P (1·58 vs 1·15 p.p.m., P = 0·006).
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As expected, on a mass basis forest species had higher foliar concentrations of N, P and K than savanna species due to their higher SLA, combined with positive correlations between SLA and each of these three nutrients. However, contrary to predictions, savanna species did not have higher concentrations of any of these nutrients after factoring out SLA as a covariate (Fig. 3). In contrast, Wright et al. (2001) found that species from drier sites had higher N and P concentrations for a given SLA than species from wetter sites. In that study, comparisons were performed between sites with annual rainfall of 387 and 1220 mm, which probably represents a higher range of water availability than the different landscape positions typically occupied by our study species. Also, we controlled for resource availability by sampling only individuals that established in open savanna, whereas this was not possible in the study of Wright et al. (2001). Unfortunately we do not have corresponding data for forest species in their typical habitat, so it is unclear how this would affect the relationship between SLA and nutrient concentration. Finally, although savanna species tend to occupy drier sites, they typically do not exhibit substantial water stress during the prolonged dry season, as evidenced by high rates of transpiration and high predawn water potentials (Meinzer et al. 1999; Franco 2002). In the Cerrado, where upland soils are typically many metres deep and mean annual rainfall is well over 1000 mm, ample water is available to savanna trees due to their deep root systems, even after several months without precipitation. In short, there may be little selective pressure to increase WUE by increasing leaf nutrient concentrations, as water availability does not appear to strongly limit photosynthesis of established trees.
Nevertheless, the significantly higher values of δ13C among savanna species indicate that these species have higher WUE (Farquhar & Richards 1984; Farquhar et al. 1988; Ehleringer et al. 1993), although, contrary to our predictions, this did not arise from higher investment in leaf N. In fact, δ13C was not correlated with the concentration of N or any other nutrient, contrary to predictions. Instead, the higher δ13C of savanna species appears to arise from the negative correlation between δ13C and SLA, although the latter was weak and statistically significant only when examined with phylogenetically independent contrasts. Others have found similar relationships between δ13C and SLA, but across precipitation gradients that confounded the relationship (Schulze et al. 1998; Lamont et al. 2002). Here, however, the relationship is independent of precipitation, indicating that leaf structure rather than water availability might explain differences in WUE between savanna and forest species.
All the individuals studied were in savanna vegetation, which was possible because long-term fire suppression has allowed forest species to establish in savanna. Of the 12 soil variables measured, only P concentration was higher under forest species relative to savanna species, which might explain the lower foliar N : P ratio of forest species. This difference could be important as the mean N : P ratio was >20 (Table 1), indicating that P is more limiting than N to plant growth (Güsewell 2004). However, there was a negative relationship between N : P ratio and SLA, suggesting that differences in SLA, rather than nutrient availability, may be responsible for differences between species types.
For the remaining soil characteristics there was no significant difference in the soils underlying savanna and forest species. This lack of a difference reflects our sampling criteria that limited sampling to individuals occurring in savanna conditions, and therefore does not indicate that savanna and forest species have similar soil preferences. Similarly, the finding that savanna and forest trees are constrained by the same functional relationship between SLA and nutrient concentration does not suggest that their nutrient relations are similar. On the contrary, low SLA is a common trait in nutrient-poor environments, probably because it permits a longer leaf life span and increased nutrient-use efficiency (Reich et al. 1992). However, SLA is also under selection according to light and water availability (Gutschick 1999; Niinemets 2001), so the high irradiances and seasonal drought typical of savanna environments are likely to have contributed to the evolution of low SLA of savanna species. The SLA and nutrient concentrations tend to be correlated with litter nutrient concentrations (Wright & Westoby 2003), decomposition rate (Diaz et al. 2004), and palatability (Cornelissen et al. 2004), so the differences in leaf traits between savanna and forest species are likely to have important implications for carbon nutrient cycling in the respective habitats.
Despite the differences in nutrient concentrations between savanna and forest trees, there was no clear difference in δ15N that might have indicated differences in N relations between these two groups. Other studies comparing savanna and forest sites have shown forest species to have higher δ15N (Högberg & Alexander 1995; Schmidt & Stewart 2003), so the lack of a difference here suggests that differences found by others were due to ecosystem processes rather than species-level differences.
There was, however, a strong negative relationship between soil pH and leaf δ15N, independent of plant type. Soil pH is known to have large effects on N cycling in ecosystems, with nitrification being inhibited by acidic conditions (Ste-Marie & Pare 1999), and soil concentration sometimes becoming particularly high at low pH, relative to (Bigelow & Canham 2002). This is relevant because Garten (1993) found soil to have a higher δ15N than soil , and that leaf δ15N was strongly related to soil concentration. If similar effects of pH occur in cerrado soils, the more acidic soils would have a relatively higher abundance of isotopically heavy , which should be reflected in higher δ15N. Unfortunately we do not have corresponding data on soil δ15N and and concentrations to examine whether this is a plausible explanation for the negative relationship between soil pH and δ15N. Differences in the importance of mycorrhizas has been used to explain intersite variation in foliar δ15N (Hobbie et al. 2000), but it seems unlikely to explain the negative relationship with soil pH. We expect that mycorrhizas would become relatively more important under the acidic soils where Al3+ is more abundant. As N obtained from mycorrhizas is relatively depleted in 15N (Evans 2001), the opposite relationship with pH would be expected.
Despite the significant relationship between foliar δ15N and soil pH, the role of species-specific differences in N relations should not be dismissed, as there was significant variation among species after taking soil pH into account with ancova. This interspecific variation is consistent with the findings of Bustamante et al. (2004), who reported δ15N values for eight of the savanna species studied here. When tested among these species, there was a strong correlation between our values and theirs (r2 = 0·82, P = 0·002, data not shown).
Regardless of the factor responsible for these consistent differences in δ15N across species, it does not appear to be highly conserved at the genus level, as evidenced by a lack of significant differences among genera (Table 1). In contrast, variation among genera was responsible for much of the interspecific variation in the concentration of most nutrients (Table 1). Therefore these traits are conserved within genera, with some genera consistently exhibiting high concentrations of an element while others exhibit low values. Interestingly, however, this was not the case for SLA, indicating that this trait was determined more strongly by the habitat of a species than by its taxonomic affinity. Therefore the tendency of some genera to have high N concentrations, for example, is not due to these genera having consistently higher values of SLA. This contrasts with the comparison between savanna and forest species, where the higher foliar N concentration of forest species can be largely explained by their greater SLA. Instead, both species within a genus tend to occupy similar positions relative to the overall relationship between N and SLA. If one species has a higher N concentration than expected based on SLA, then the other species in the genus is likely to have a higher-than-expected N concentration. For Guapira, Aegiphila, Erythroxylum and Schefflera, both species in each genus had higher N concentration than expected based on SLA, while N concentrations of Miconia, Ouratea, Aspidosperma, Byrsonima, Myrsine, Symplocos and Pouteria were lower than expected. Only Tabebuia and Hymenaea countered this trend, whereby the N concentration of one species was higher than expected based on its SLA, while its congener was lower than expected. Similar trends emerged for all other minerals except Fe and Mn. This suggests that, while rather large shifts in leaf nutrient concentrations have arisen within genera due to divergence in SLA between savanna and forest species, other aspects of their nutrient economy may have been conserved at the genus level. We do not have additional information to suggest whether this reflects conservatism of symbiotic associations, nutrient-uptake capacity, allocation patterns, internal recycling or some other factor, but any of these could be important.
Much remains to be understood about soil–vegetation relationships at savanna–forest boundaries. It has been widely recognized that nutrients play an important role in determining the distribution of tropical savanna and forest, and that the vegetation itself may reinforce the disparity in soil nutrient concentrations due to the higher litter accumulation and reduced fire frequency in forests relative to savanna (Kellman 1989; Bowman 2000). However, little attention has been given to the possibility that species characteristics, not just total biomass and site conditions, may play an important role in soil–vegetation relationships at the savanna–forest boundary. The data presented here reveal fundamental differences in leaf traits and nutrient relations of savanna and forest species. Further work is needed to elucidate how these differences reflect nutrient requirements and species distributions, and how they influence nutrient and carbon cycling in these two extensive tropical biomes.