Intraspecific trait variability of trees is related to canopy species richness in European forests

Highlights

• Species traits are linked to species complementarity and competitive ability.

• The intraspecific component of functional diversity is high in European forests.

• Conspecific trees adjust leaf traits in response to canopy species richness.

• Conspecific trees have architectures more variable in richer communities.

• Species respond to canopy species richness promoting species complementarity.

Abstract

Functional diversity informs about biodiversity-ecosystem functioning relationships. The intraspecific component of functional diversity (i.e. the phenotypic space of each species) depicts individual differences in the resource use and fitness among conspecifics, and gives valuable information about the functional similarity (competition) or dissimilarity (complementarity) of coexisting species. Here, we quantified trait differences within tree species along local diversity gradients to shed light on the role that this intraspecific variability exerts on functional complementarity of tree species. We measured architectural traits in 5,036 individuals and leaf traits in 1,403 individuals from nine dominant tree species, surveyed in 92 plots located in three major European forest types (Mediterranean, temperate and boreal forests). In each forest type, plots were positioned along a canopy richness gradient, with every study species present in different species richness levels, including monocultures. Our results showed that the relative magnitude of intraspecific trait variability to community-level variability is high in these forests. At the species level, we found adjustments of species leaf traits (mean shifts) in response to neighbouring trees, suggesting the existence of processes that limit niche overlap. We also found higher variability in architectural traits of conspecific individuals in more diverse canopies, suggesting greater niche packing and a more efficient use of available space as the number of species in the canopy increases. Altogether, our results support the hypothesis that differential responses of individuals within a species promote species complementarity, suggesting that biodiversity-ecosystem functioning relationships cannot be properly estimated without accounting for the intraspecific level of functional variation.

Introduction

An increasing body of work shows the positive effect that plant diversity exerts on different ecosystem functions and services, accounted either individually (e.g. productivity, stability or resilience against pests or pathogen outbreaks) (Allan et al., 2013; Balvanera et al., 2006; Cardinale et al., 2012) or together (the so-called ‘multifunctionality’) (Gamfeldt et al., 2008; Lefcheck et al., 2015; van der Plas et al., 2016). For individual ecosystem functions, two additive mechanisms have been identified supporting this positive relationship: niche complementarity and selection effects (Loreau and Hector, 2001; Turnbull et al., 2013). The former assumes that diverse communities comprise species with different resource use (i.e. differences in resource requirements or spatial/temporal distribution); the latter assumes that competition leads high-yielding species to dominate in mixtures.

Including functional diversity, in addition to the number of species, gives further information about the biodiversity effect on ecosystem functioning as it can better capture species interactions in a community (Cadotte, 2017; Cadotte et al., 2011; Ebeling et al., 2014). Traits determine how individuals use resources from their environment (McGill et al., 2006), and provide information about species niche and fitness differences (Kraft et al., 2015). Species trait differences are therefore directly linked to the complementarity and competitive ability of coexisting species (Carroll et al., 2011; Loreau et al., 2012), key components of biodiversity that influence how an ecosystem operates or functions (Tilman, 2001). Since approximately 25% of total estimated trait variation in plant communities worldwide is found within species (Albert et al., 2010a, b; Siefert et al., 2015), intraspecific variability should not be ignored when quantifying biodiversity effects on ecosystem functioning (Aschehoug and Callaway, 2014; Ashton et al., 2010; Zhu et al., 2015). Accordingly, an increasing number of studies is revealing the importance of intraspecific variability for different ecological questions, including functioning of plant communities (Crutsinger et al., 2006; Lecerf and Chauvet, 2008), community assembly (Jung et al., 2010; Siefert, 2012), species distribution forecasting (Cochrane et al., 2015; Valladares et al., 2014), and mechanisms ruling species interactions and coexistence (Lichstein et al., 2007; Roscher et al., 2015).

Traits are measured at the individual level, and the distribution of trait values within a species identifies its functional trait space. Hence, considering trait variability between and within species entails that the functional space can be occupied continuously by all the individuals making up the community. Approaches based on species mean traits underestimate species interactions (by ignoring functional overlaps) and the utilisation of available resources (de Bello et al., 2013; Violle et al., 2012). The functional overlap among coexisting species reveals their similarity, i.e. the functional space they share (Violle et al., 2012). Thus, low trait overlaps in rich communities would support that species exploit different niches and are thus complementary in their resource use. Meanwhile, large overlaps would imply functional redundancy among coexisting species. Despite the large effort required to quantify and collate trait variation within species, several studies have tackled the relationship between species richness and trait distributions and overlaps in order to elucidate mechanisms that underpin the structure of natural communities (Bastias et al., 2017; Kumordzi et al., 2015; Le Bagousse-Pinguet et al., 2014). However, results are contrasting and there is no clear evidence of similar species-specific responses (trait adjustments) to changes in species richness and composition. Insights from biodiversity experiments (carried out primarily with herbaceous species) have revealed a potential role of intraspecific variability for fostering species complementarity (Ashton et al., 2010; Mitchell and Bakker, 2016; Zuppinger-Dingley et al., 2014; Zhu et al., 2015). For instance, Zhu et al. (2015) assessed that 64% of the total net biodiversity effect measured on light capture compared to monocultures in wheat and maize intercrops was due to species plasticity.

Here, we have quantified trait variation within tree species along diversity gradients of canopy trees in mature, European forests to address whether intraspecific trait variability enhances species complementarity. We have compared the intraspecific trait variability (hereafter ITV) of trees growing in pure vs. mixed stands in three contrasting forest types: a continental-Mediterranean, a mountainous mixed temperate and a boreal forest. First, we have evaluated the magnitude of ITV at the community level relative to the variability among species (intErspecific Trait Variation, hereafter ETV) across the forest types, and analysed its relationship with species richness of the canopy tree layer. We further analysed how this component of the variability at the community level varies with species richness.

Subsequently, we analysed the relationship between species richness and ITV at the species level, i.e. trait mean and variance among conspecific individuals, searching for species-specific responses to the diversity gradient. Given the contrasting results found in previous studies of how species richness affects ITV (Bastias et al., 2017; Kumordzi et al., 2015; Le Bagousse-Pinguet et al., 2014; Siefert et al., 2015), we posit three alternative hypotheses for this relationship (Fig. 1): i) species richness and ITV are not correlated, suggesting either full complementarity among species or non-saturated communities; ii) species richness and ITV are negatively correlated, implying a reduced ITV due to resource partitioning and avoidance of niche overlap with increasing species richness (McGill et al., 2006; Tilman, 1982); iii) species richness and ITV are positively correlated, entailing higher temporal or spatial heterogeneity in the community that provides new opportunities (new niche availability) and wanes competition among individuals (Stein et al., 2014). This positive correlation might arise either by an increment of intraspecific trait variability at the community level (changes in trait variance among conspecifics in two different communities), or by trait mean shift of a species.