The analysis of secondary succession may enable the identification and prediction of fundamental processes involved in community assembly (Lebrija-Trejos et al., 2010). The assembly of communities is defined by the colonization and interaction of species coming from a regional pool to form local communities and can be simultaneously driven by factors related to ecological filters (abiotic and biotic environment) and neutral forces (dispersal limitation, ecological drift) (HilleRisLambers et al., 2012; Rosindell et al., 2011), but their proportional importance can vary along the successional time. Meiners et al. (2015) recently presented a conceptual framework of successional drivers that simultaneously accounts for geographic and evolutionary contexts with filter models associated to local dynamics. The framework highlights how each level constrains lower levels (for example, how site conditions constrain species availability) and potential feedbacks among levels (for example, how species performance alters site conditions), considering a broad review of succession studies (Meiners et al., 2015).

Ecological filters in community assembly may result in patterns of both convergence (underdispersion) and divergence (overdispersion) in species traits (Pillar et al., 2009). Trait-convergence is related to a species ability to transpose abiotic filters, driving the assembly to be similar for particular functional traits. Such filters may act at the regional scale (defining the species pool), and then at the local habitat scale, selecting species that are able to get established under the prevailing environmental conditions (Meiners et al., 2015). During the process of succession, early species may change the local environmental conditions (e.g. improving shading) and interact with other species, facilitating or hindering the colonization of new species (Lebrija-Trejos et al., 2010; Schöb et al., 2013).

Pioneer species may facilitate colonization by species that have different traits or strategies, such as shade-tolerant species, influencing, thus, the community assembly of the next successional phase (Verdú et al., 2009). In this case, we can expect a trait divergence pattern between the species that are colonizing and those already established and also among the new recruits, since the species pool of secondary/late forests is larger than the pioneers, increasing the probability of trait-divergence. On the other hand, pioneer species can also delay the colonization of secondary species by, for example, a positive feedback in the recruitment mechanism (‘persistent-monodominance’), hindering the successional process and keeping the community at an alternative state (Norden et al., 2011). This mechanism would maintain a convergence pattern. However, as local environmental conditions change over the time through the increase in vertical structure and canopy, abiotic filters of each successional phase may still lead to patterns of trait convergence within the communities. Secondary and late successional forest trees have evolved to the commonest environmental conditions – shaded habitats – causing species to converge on similar traits (Hubbell, 2005), at least in terms of those associated with light demand.

Considering the above, we would expect patterns of trait convergence along the forest succession process. However, at the scale where the coexisting species are competing for resources, having different strategies to obtain them may be more effective (Silvertown, 2004), leading to patterns of trait divergence. Processes of limiting similarity enhance species diversity through a finer niche partitioning, therefore increasing functional alpha diversity, here measured by the trait dissimilarity between local species (De Bello et al., 2009). As both trait convergence and divergence can be found over forest succession, simple conclusions about patterns of functional diversity and functional composition in forest succession have not yet been consistent (Böhnke et al., 2014). Whereas functional diversity measure the value, range and relative abundance of functional traits in a community, the functional composition can be represented by the community weighted mean value of traits (i.e. CWM) (Díaz et al., 2007). The number and the nature of selected traits strongly influence such functional patterns, and the environmental gradient must be part of this choice (Pillar et al., 2009).

In this study we evaluated patterns of convergence and divergence of plant traits, investigating tree species in a successional chronosequence of Araucaria forest plots in southern Brazil, to answer the following questions: (1) How early successional stages differ from late ones in terms of species composition, considering both upper and lower strata? (2) Which functional traits are optimal for revealing patterns of trait-divergence and trait-convergence related to forest development? (3) What patterns of functional composition and functional diversity of both upper and lower strata become evident along forest succession?

We recorded 94 species in the plots, among which 36 species had more than 10% of frequency, and were included in the functional analyses (Table S2). The upper stratum was mainly characterized by Tibouchina sellowiana in the initial successional areas (47% of sampled individuals) and Myrcia retorta (19%) in the late forests. Daphnopsis fasciculata (58%) and Myrceugenia myrcioides (30%) best represented the lower stratum of initial and late forests, respectively. The Jaccard similarity between upper and lower strata within each forest stage presented higher values for late forests than initial forests (mean±SD for sampling units: 0.25±0.10 and 0.18±0.15, respectively). In addition, the lower stratum of initial forests was more similar to the lower stratum (0.30±0.15) than to the upper stratum (0.24±0.13) of late forests.

Table 1 presents all trait subsets that maximized either TDAP or TCAP for the upper stratum and the lower stratum of the communities, according to the forest development gradient (matrix E). Divergence and convergence patterns expressed by the PCoA ordinations of the fuzzy-weighted community composition matrix (X) clearly show differences between late and initial forests for both strata (Fig. 1). Individuals present in the upper stratum of late forests are mainly represented by zoochoric species with higher seed mass and wood density in comparison to those present in initial forest areas. Some areas had a higher participation of deciduous species with high SLA and LNC values (lower portion of Fig. 1A) and might be representing an intermediate successional stage (intermediate values of total basal area of trees). Lower stratum patterns (Fig. 1B) still discerned the successional stage of forests, but four initial areas were already more similar to late forests. The initial areas that stayed separated in the diagram were mostly represented by individuals of species with long, narrow leaves and with less influence of zoochoric dispersal compared to late successional forests. We did not see any significance of phylogenetic structured assembly related to the trait-divergence and convergence patterns for the selected set of traits (Table 1). The only influence of phylogeny was at the level of species for the set of traits that maximized TCAP of the lower stratum (leaf form, LNC, zoocoric).

Fig. 1.

PCoA ordination triplot of successional Araucaria forests in southern Brazil. The analyses were based on matrices X of 20 plots described by the species composition of the upper stratum (A) and the lower stratum (B) after fuzzy-weighting by species similarities in terms of functional traits that maximized TDAP (Upper stratum: deciduousness, SLA, zoochoric, seed mass; Lower stratum: Leaf form, LNC, zoochoric). Functional traits were projected on the diagram based on their correlation with the ordination axes, considering their community-weighted mean (CWM) values. The total basal area of trees of the upper stratum (BA/m2) was also projected based on their correlation values with the axes. Communities are identified according their priori successional stage classification and species labels can be seen in Table S1.

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Functional diversity based on trait subsets that have maximized TDAP (Table 1) showed a logarithmic pattern of increase with the forest development, stabilizing the values for areas of 30–40m2ha−1 of tree basal cover (Fig. 2). This pattern, however, was much less prominent in the lower stratum than in the upper.

Fig. 2.

Functional diversity (Rao Entropy) of upper and lower strata of Araucaria forest according to the forest development, measured as the stem cover of trees with at least 10cm DBH (see Fig. S1 for this relation and the priori stage classification). Trait subset used for estimating was that with higher congruence for TDAP in each stratum (see Table 1).

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Convergence pattern in the upper stratum was maximized by wood density and leaf nitrogen content (LNC), but only wood density CWM values have shown a sharp relation with the forest development (Fig. 3A). In the lower stratum, wood density, leaf dry matter content (LDMC), and leaf area composed the subset best related with the environmental gradient (r=0.67) and all of them showed clear patterns of community convergence along the forest development (Fig. 3B).

Fig. 3.

Relation between CWM trait values and forest development in Araucaria forest, considering functional traits that maximized the congruence for convergence patterns of upper (left) and lower (right) strata. Logarithmic line tendency in (A) is y=0.0364ln(x)+0.1075, r2=0.68012 for wood density and in (B) are y=0.0224ln(x)+0.1525, r2=0.69715 for wood density; y=0.0162ln(x)+0.1725, r2=0.60655 for LDMC; y=−0.039ln(x)+0.3431, r2=0.74141 for leaf area.

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Our results indicate strong trait-convergence and divergence in the assembly of the communities, revealing the relationship between patterns of the selected traits (optimal trait subsets) and the environmental gradient established over the forest development, not associated to the phylogeny of species. Successional changes linked to convergence patterns were mostly related to the acquisitive-conservative gradient (Chave et al., 2009): late forests had in average more individuals of species with higher wood density and LDMC, and lower leaf area and LNC (examples of conservative plant strategies) than those communities at initial succession. Conversely, an increase in trait-divergence through the development of forest was mainly related to deciduousness, specific leaf area, leaf form, dispersal by animals and seed mass. Potential associations between these traits and successional processes are discussed below.

Plant species assembled in the understory of the studied initial forests were more similar to the upper stratum of late forests than to their own, which may indicate turnover of species within the ongoing successional process. Adult individuals of pioneer species (e.g. T. sellowiana) may be favoring the colonization of secondary species in the understory (e.g. Myrceugenia spp.). Successional changes in the forest structure led to changes in the understory environment (Lebrija-Trejos et al., 2010), allowing the assembly of regenerating species to be more similar to the advanced areas. We could also observe some communities previously considered ‘initial’ very close to late forests, when regarding community similarity based on species composition fuzzy-weighted by the functional traits (matrix X, Fig. 1B). Over the successional time, an increased phylogenetic evenness has been linked to the recruitment of late-successional species (e.g. Letcher, 2010), which could, in turn, present functional convergence in traits, conferring adaptive value for regeneration in shade conditions (Hubbell, 2005). In the present study, we saw an increase of trait-divergence along the forest development, not related to the phylogeny.

The results of chosen trait subsets for trait-divergence assembly patterns (TDAP) may express one or both alpha and beta divergence along the environmental gradient (Pillar et al., 2009). Various leaf traits were selected for maximizing divergence patterns along the forest development studied here, i.e. species inside the same community and/or species in communities that are at similar successional stages seem to be overdispersed in terms of trait states of deciduousness, SLA, leaf form, and LNC. Such traits are related to the species fitness and, consequently, competition, especially in terms of resource acquisition under light limiting conditions and nutrient demand (e.g. Wright et al., 2010). Considering these leaf traits, we can assume that coexisting species should be more successful when leading different (contrasting) strategies for acquiring and stocking energy, resulting in higher alpha diversity with the ongoing succession (Fig. 2). Additionally, we can also assume that communities along the forest development gradient diverge more as they stray in terms of successional time, which results in a higher beta divergence (Silvertown et al., 2006).

Some reproduction traits were also associated with divergence patterns – seed mass and zoochory. They should be related to the high variability of seed attributes among the species established in the upper stratum of late forests and to a higher proportion of zoochory (since the state ‘1’ of our study expresses the amount of zoochoric individuals in the community) in both strata of advanced forests, when comparing to initial successional forests (Duarte et al., 2007; Zanini et al., 2014). Divergence pattern of seed mass was mainly associated to overdispersion inside the communities of intermediate development, where coexisting species presented greater amplitude of states (higher functional diversity when considering only the seed mass trait – data not shown). Despite the predominance of zoochoric dispersal in advanced areas, we saw that species assembled in initial areas were also represented by anemochory and autochory.

Convergence patterns, here expressed by the community-weighted mean of traits that maximized TCAP (LNC and wood density for the upper stratum; leaf area, wood density, and LDMC for the lower stratum), revealed the expected change from acquisitive to the predominance of conservative plant strategies in late forests. The acquisitive-conservative gradient reflects the resource economy and growth strategy of plant species and can be recognized by the leaf economic spectrum, which runs from fast to slow return on investments of nutrients and dry mass in leaves (Wright et al., 2004), and by the continuum between early and late species, which further includes reproductive features (e.g. from small to big seeds) (Lohbeck et al., 2013). The decreasing logarithm of leaf area, as the forest development increase, agrees with the forest type – Araucaria forest, where many typical species are small-leaf species, as Araucaria angustifolia itself, and other abundant Myrtaceae species (Bergamin et al., 2012). Such decrease in leaf area was also observed along succession in dry forests, but not in wet tropical forests (Lohbeck et al., 2013), which is related to different trade-offs either associated to water economy or light availability among the species in each forest type. The Araucaria forest distribution is mainly related to low mean annual temperature, frost frequency and cloud cover (highland conditions in southeastern Brazil), which in turn favors small-leaf species, with high dry matter content (LDMC) and high wood density. We can make up this picture by looking at the regenerating stratum in late forests, where we can expect to find a well-developed Araucaria forest in the future.

Initial and late Araucaria forests are highly different in terms of species composition, but the regenerating stratum of initial forests (20 years old) was already more similar to advanced forests, especially in terms of functional traits. Species assembly along the forest development was clearly related to functional traits that express acquisitive-conservative strategies (wood density, leaf nitrogen content, leaf area, and leaf dry matter content), which maximized convergence patterns. On the other hand, trait-divergence patterns were also significant. Specific leaf area, seed mass, deciduousness and dispersal mode were the traits that maximized divergence, expressing a logarithmic relationship between functional diversity and forest development. Therefore, successional communities have been assembled through the influence of environmental and biotic filters, but limiting similarity processes seem to increase with the advance of the succession, as shown by the higher trait divergence in late Araucaria forests.

The authors declare no conflicts of interest.