Little is known about decomposition rates of tropical plant species and the potential effects of land use change on decomposition. We first discuss how leaf and litter traits are associated, then evaluate what drives leaf decomposition rate, and conclude how traits and decomposition rates differ for species and communities from different land use types.
Association amongst leaf traits
Nearly half of leaf and litter traits (43 out of 91 possible pair-wise combinations) were significantly correlated (Table 2) and almost half of the variation in leaf and litter traits was explained by the first PCA axis (Fig. 1a). This axis was negatively related to leaf area, density, dry matter content, and toughness, and positively related to SLA and nutrient concentrations in leaves and litter. The first axis therefore represents the LES, with slow, conservative traits to the left, and fast, acquisitive traits to the right. In their analysis of the worldwide economics spectrum, Wright et al. (2004) focused on SLA, LNC, LPC and photosynthetic traits. Our current analysis shows that apart from SLA, other leaf defence traits (leaf density, dry matter content and toughness) form an integral part of this LES (cf. Díaz et al. 2004; Kitajima & Poorter 2010) and that this fast–slow continuum is mirrored in litter traits (e.g. litter nitrogen concentration, litter C : N ratio, Fig. 1a).
Leaf traits predicting decomposition
The multiple regression analysis indicated that of all individual leaf and litter traits, a combination of LNC or SLA with chlorophyll content were the best predictors of decomposition rate. The relation between LNC and SLA and decomposition rate is consistent with previous studies (LNC: Santiago 2007; Cornwell et al. 2008; Fortunel et al. 2009; SLA: Cornelissen et al. 1999; Vaieretti et al. 2005; Santiago 2007). Decomposers prefer nitrogen-rich leaves as nitrogen is an essential and limiting element for their metabolism. They might also prefer high SLA leaves, as decomposers can consume such litter more rapidly and easily, processing less leaf material per unit area or volume. In contrast, accessing C-rich and nutrient-poor material is more difficult, because decomposers need a variety of enzymes (Wieder, Cleveland & Townsend 2009).
Leaf nitrogen concentration was, surprisingly, better at predicting litter decomposition rate than litter nitrogen concentration, probably because a suite of correlated leaf traits affects decomposition rate, and LNC was a better indicator of this suite of correlated traits (as summarized in the LES) than litter nitrogen concentration (Fig. 1). LNC was, also surprisingly, a better predictor than LPC, despite the fact that tropical rainforest soils are thought to be limited in P, and despite the fact that most decomposition studies in lowland tropical forests find LPC to be more important for decomposition than LNC (Vitousek 1984; Aerts 1997; Hobbie & Vitousek 2000; Santiago 2007; Wieder, Cleveland & Townsend 2009). Limitation by nitrogen is not only indicated by the results of our decomposition experiment, but also by the relatively low N : P ratios of fresh leaves (13·7) and litter leaves (12·8). A N : P ratio smaller than 14 is generally a sign of N-limitation whereas a N : P ratio higher than 16 is indicative of P-limitation (Koerselman & Meuleman 1996). Moreover, the fact that the N : P ratio declines during senescence, points out that N is preferentially reabsorbed over P. Two factors might explain why nitrogen played a more significant role than phosphorus in our decomposition experiments. Although phosphorus is often the most limiting nutrient in decomposition processes in tropical forests (Cleveland, Townsend & Schmidt 2002), nitrogen seems to be limiting in the forest where we carried out our experiments. The study of Cleveland et al. is based on a forest on extremely old, highly weathered soils in Costa Rica, whereas La Chonta forest is located on inceptisol: a soil of relatively new origin and usually fertile. In addition, black anthropogenic forest soils are relatively frequent in La Chonta forest (Paz-Rivera & Putz 2009) and these so-called terra-preta soils are especially rich in phosphorus (Peña-Claros et al., unpublished data). Thus, limitation by nitrogen, as has been frequently found for temperate and high latitude forests, can also be found in tropical forests. A second explanation for the importance of N during decomposition is that nitrogen is most important during early stages of decomposition, whereas P is important later on (Santiago 2007). Decomposers feed preferentially first on nitrogen, but as [N] decreases, they switch to [P] on a certain point. Our experiment might simply not have lasted long enough to detect [P] influences on decomposition.
While chlorophyll content by itself is not correlated with decomposition, it explains in the multiple regression analysis a small additional part of variation in decomposition rate that is not explained by LNC or SLA. The positive effect of chlorophyll on decomposition, which to our knowledge has not been tested before, is surprising. Perhaps a high chlorophyll content is an indirect indicator of the nitrogen or magnesium concentrations in the leaf (as N and Mg are components of chlorophyll, which both directly affect decomposition rate), or an indirect indicator of SLA (as thick leaves with low LA will have a high chlorophyll content per unit leaf area). The effect of chlorophyll content suggests that it would be interesting to include it in decomposition studies, especially because it can readily and quickly be measured with the SPAD metre.
We found a negative, albeit non-significant relationship between force to punch and decomposition rate (r = −0·24; n = 23; P = 0·266). The weak relationship between leaf toughness and decomposability could be explained by a difference in what is measured and how decomposers perceive the plant material. Possibly, microbes are responding to the strength of chemical bonds between atoms, while puncture tests work on a larger scale and respond to the size and orientation of these molecules. For example, in Cornwell et al. (2008) mosses are very soft by any method of toughness measurement, but have a very low decomposition rate.
Not only individual leaf traits, but also species’ position on the LES was positively correlated with decomposition rate (r = 0·49; n = 23; P < 0·05; Fig. 3c), with species with ‘fast’ acquisitive leaf traits showing higher decomposition rates than species with ‘slow’ conservative traits. This suggests that selection for a suite of coordinated structural and chemical leaf traits that determine photosynthetic rate, productivity and leaf longevity has strong nutrient cycling consequences. Similar results have been obtained for 35 tropical rainforest species (Santiago 2007) and 108 temperate herbaceous and woody species from a Ponderosa pine forest (Laughlin et al. 2010). However, in contrast to our hypothesis, the LES as a multivariate descriptor of leaf traits was a weaker predictor of decomposition rate than individual components of the LES, such as LNC and SLA, and the LES was not selected by the multiple regression analysis. This suggests that individual components of the LES (LNC, SLA) are the real drivers of decomposition rate, rather than the LES itself.
Leaf decomposition rate was also related to the regeneration strategy of the species, albeit indirectly, with regeneration strategy determining leaf traits, which in turn define decomposition rate. Light-demanding pioneer species decomposed faster than long-lived pioneer and shade-tolerant species (Fig. 3d). This means that a plant’s strategy determines its entire life cycle: pioneer species, for instance, combine high nutrient uptake rates with fast growth, leaf turnover and litter decomposition rates. Such a positive plant–soil feedback loop might, in the case of pioneer species, enhance soil fertility (Wardle et al. 2004) and in this way adults of these acquisitive species may pave the road for a new generation. In other words, systems dominated by pioneer species push themselves to an overall more fertile and productive state (cf. Cornelissen et al. 1999; Wardle et al. 2004).
Land use, leaf traits and decomposition rates
Functional parameters of the plant species in each community that are important for decomposition changed with the intensity of land use. The communities of mature and secondary forests consisted of long-lived tree species with low LNC, while in agricultural fields this community had been replaced by assemblages composed of fast-growing herbaceous species with higher LNC (Fig. 4). This reflects disturbance intensity and frequency in the different land use types with land use being least intensive in mature forest and most intensive on agricultural fields. These results are in line with other studies, which found that higher disturbance selects for acquisitive plants with leaf characteristics at the faster end of the growth spectrum (Díaz et al. 1999; Garnier et al. 2007; Dorrough & Scroggie 2008; Fortunel et al. 2009). SLA and position on the LES did not differ significantly between species from different land use types, although they increase gradually from mature forest to agricultural field (Fig. 4b,c), like we expected. One reason can be the relatively low number of species per land use type, another that within mature forest species and secondary forest species there is a large interspecific variation in leaf traits, due to the presence of the palm species Attalea speciosa, Attalea phalerata and Syagrus sancona. If palms are excluded from the analysis, then SLA and LES do differ significantly between land use types (data not shown). Palm species are characterized by tough, long-lived leaves with very low LNC, SLA and extremely low scores on the LES axis (Fig. 1). A palm species like A. speciosa becomes very dominant in secondary forest fallows, when these are frequently burned through slash-and-burn activities, because it resists fire, as its apex is well-protected by surrounding leaves, and because it lacks a vascular cambium – an advantage, although there are, in other parts of the world, other, non-monocot species which are able to succeed in frequently burned environments despite the presence of a vascular cambium (Bond 2008). Herbaceous or woody ferns are known to become dominant in other early successional tropical and sub-tropical forests (Amatangelo & Vitousek 2008, 2009). Species from agricultural fields had a higher average litter decomposition rate than secondary and mature forest species (Fig. 4d). Secondary forests were hypothesized to show a higher decomposition rate than mature forest, but the abundance of palms lead to a lower decomposition rate than expected. This means that the value of secondary forests for increasing fertility can be questioned.
The CWM reflects the characteristics of an ‘average’ plant in the community. Secondary forests were hypothesized to occupy an intermediate position between mature forests and agricultural fields (in line with Fig. 4), because its communities are thought to consist of rapid growing and photosynthesizing pioneer tree species with high LNC and SLA. However, secondary forests turned out to have the lowest LNC and SLA (Fig. 5), which is again explained by the high abundance of palm species; they make up 55% of total basal area in secondary forests. The palm species A. speciosa alone represented 46% of the assembly. It would be interesting to compare this high palm abundance with other secondary forests, to see whether this feature is widespread or typical for the Guarayos region.
This study showed that land use change indirectly affects decomposition rate. The indirect pathway, along which global change influences the functional composition of a community, which in turn changes ecosystem functioning, is known to be more important than the direct pathway, in which changes in abiotic conditions influence processes in the ecosystem (Cornwell et al. 2008). The nature of this process has been shown for Mediterranean fields (Kazakou et al. 2006; Cortez et al. 2007; Fortunel et al. 2009), but this is, to our knowledge, the first time that it has been analysed for tropical land use types, which are very important in global carbon and local nutrient cycles.