Linking leaf economic spectrum to floral resources along an environmental gradient

Abstract

1 INTRODUCTION

Among the functional traits of plants, leaf traits are often used to evaluate adaptations to abiotic and biotic factors (Lavorel & Garnier, 2002). Several theories, such as the CSR strategy (Grime et al., 1997; Pierce et al., 2013, 2017) and the leaf economic spectrum (Wright et al., 2004), have been developed to explain the main axes of variation in leaf traits. The primary axis describes resource acquisition strategies, ranging from fast-growing and short-lived species (acquisitive) to slow-growing and long-lived species (conservative). This gradient reflects a trade-off between traits that promote a high net assimilation rate per unit of leaf mass and traits that support a long leaf lifespan (Wright et al., 2004). In addition to this axis, leaf size is recognised as a second, independent dimension of trait variability (Pierce et al., 2012).

Beyond leaf traits, studies have increasingly focused on understanding how other plant traits, such as below-ground and reproductive traits, relate to leaf traits (e.g. E-Vojtkó et al., 2022; Weemstra et al., 2016). Plants are shaped by complex interactions between abiotic and biotic factors across the ecology–evolution continuum (Opedal, 2019). The integration of multiple plant traits influenced by these factors provides a more holistic understanding of plant strategies (Ciccarelli et al., 2023) and enables the identification of predictors for rapid functional characterisation (Smart et al., 2017).

Among reproductive traits, floral traits exhibit greater diversity than leaf traits, reflecting the wide range of functions associated with flowers (Roddy et al., 2019, 2021). Floral traits differ significantly from leaf traits in terms of water transport capacity, stomata presence, vein density and mesophyll porosity (Roddy et al., 2013; Schreel et al., 2024). This has led to the hypothesis that leaf and floral traits may evolve under different selection pressures (E-Vojtkó et al., 2022; Roddy et al., 2013). However, while leaf traits are often assumed to be influenced by abiotic factors such as resource availability and floral traits by biotic factors such as pollinators, both leaf and floral traits can be influenced by a combination of abiotic and biotic factors (e.g. Descamps et al., 2021), suggesting that evolutionary pressures on these traits are not entirely independent.

This applies in particular to pollen and nectar, the most common rewards offered by flowering plants to their pollinators, which are influenced by both abiotic and biotic factors (Descamps et al., 2021). Although pollen plays a central role in attracting pollinators (Fantinato et al., 2021), it is still uncertain whether pollinator selection significantly alters pollen traits, such as quantity and nutritional profile (Ruedenauer et al., 2019). On the contrary, abiotic factors, such as temperature and nutrient availability, seem to have a direct influence on pollen production and traits (Arathi & Smith, 2023; Devlin, 1988; Quesada et al., 1995; Recart & Campbell, 2021). As for nectar, macroevolutionary relationships between nectar and pollinators suggest that nectar differentiation may have evolved through pollinator-driven selection, although abiotic factors, such as temperature, nutrient and water availability, also strongly influence nectar production (Pleasants & Chaplin, 1983; Petanidou et al., 1999; Parachnowitsch et al., 2019). Since both pollen and nectar traits are influenced by selection pressures that also affect leaf traits (e.g. nutrient and water availability), it is plausible that correlations exist between leaf traits and floral resources resulting from joint responses to environmental variation or from congruent variation due to integrated developmental pathways (Klingenberg, 2008).

Variation in plant functional traits and strategies across environmental gradients is a well-documented phenomenon in functional studies of plants (Kandlikar et al., 2022). Among the environmental gradients, those associated with coastal dune ecosystems exhibit significant correlations with plant traits and strategies. Similar plant functional traits in dune ecosystems are found in regions with different species compositions and climates, which is primarily due to habitat filtering (Mahdavi & Bergmeier, 2016). The differentiation of plant species along the shoreline–inland gradient with respect to leaf traits is established (Li et al., 2005). Plant species with high values of leaf area and specific leaf area generally dominate in the pioneer communities closest to the shoreline, such as drift line and shifting dune communities, whereas species with high values of leaf dry matter content dominate in the inland communities, such as the semi-fixed and fixed dune communities. However, the variation in floral traits along this gradient remains largely unexplored. Furthermore, the topology of plant–pollinator interaction networks exhibits a pronounced spatial gradient from the shoreline to the inland, potentially mediated by variation in floral resources (Fantinato et al., 2018). Plant species of the pioneer communities closest to the shoreline support a richer and more abundant community of pollinators than inland communities (Fantinato et al., 2018). These results suggest a potential decrease in the quantity of floral resources produced moving from the shoreline to inland communities.

To investigate the relationship between leaf traits and floral resources, we focused on 11 animal-pollinated species that show high fidelity to specific coastal dune communities that successively develop from the shoreline inland. We hypothesised that greater quantities of floral resources (i.e. pollen and nectar) would be associated with greater values of leaf area and specific leaf area and lower values of leaf dry matter content. We considered the quantity of floral resources because it directly reflects the resource allocation strategies of plants and emphasises investment in reproductive over vegetative functions. While nutritional value may reflect resource allocation in some cases, for example investment in higher-value floral resources, such as sugar-rich nectar (Maldonado et al., 2023), quantity captures the extent of resource investment more directly. To test this hypothesis, we analysed correlations between leaf traits and floral resources at multiple levels (flower, floral unit and individual plant) and investigated how abiotic factors (i.e. environmental selection), biotic factors (i.e. pollinator selection) and phenological traits were related to the variation in leaf and floral traits.