Tree species identity shapes the relationship between canopy cover and herb-layer species in temperate forests

Abstract

1 INTRODUCTION

In forest ecosystems, the understorey layer represents a huge proportion of plant biodiversity, up to 90% (Gilliam & Roberts, 2014; Thrippleton et al., 2016), and provides a variety of ecosystem services, such as nutrient cycling, carbon sequestration and energy flow (Landuyt et al., 2019; Mölder et al., 2008; Muller, 2014; Wang et al., 2021). It shapes the distribution of other species by providing habitat not only for groups of species, such as mammals and insects (Fayt et al., 2006; Marshall & Hawthorne, 2012), but also for trees by regulating their regeneration through the resource competition with germinating seedlings (Coomes & Grubb, 2000; Gilliam, 2007) or facilitation processes (e.g. microclimate buffering or exchange through mycorrhizal networks; Callaway & Walker, 1997; Zilliox & Gosselin, 2014). Grasping the drivers of herb-layer distribution is thus crucial to guide sustainable forest management and biodiversity conservation programmes (Köhl et al., 2020).

The herb-layer community responds to various factors ranging from land-use history to abiotic and biotic factors across different scales (Barbier et al., 2008; Ellenberg & Leuschner, 2010; Gilliam, 2007; Hermy & Verheyen, 2007). Climate influences its broad distribution and temporal change. At local scale, the availability of suitable micro-environment in the forest floor is a strong driver (Kelemen et al., 2014), including soil composition and condition, water and light availability or microclimate temperature (Depauw, 2020; Wei et al., 2020). Yet, these factors partly depend on forest structure and tree composition (Augusto et al., 2003). For instance, tree canopies intercept up to 99% of incoming light (Coomes & Grubb, 2000), compete strongly for below-ground resources (Coomes & Grubb, 2000; Germany et al., 2017) and modulate the microclimate (Gottschall et al., 2019; Lembrechts et al., 2019). Trees also can be associated with particular herbaceous species due to differences in their nutrient cycling, rainfall partitioning, shade-casting ability and quality of the light transmitted by their foliage (Barbier, Balandier, & Gosselin, 2009; Rawlik et al., 2018). Tree species identity can also lead to litter composition (e.g. allelopathic compounds) and accumulation, affecting germination and performance of herb-layer species (Bertin et al., 2003; Rodríguez-Calcerrada et al., 2011). Thus, various overstorey composition characteristics are well-known to impact understorey herb communities, but questions remain as to what extent they influence individual species distribution (Ampoorter et al., 2015; Barbier et al., 2008; Germany et al., 2021; Gilliam & Roberts, 2014).

The distribution, diversity and structure of forest tree species communities are largely influenced by management practices (Tinya et al., 2021), which also impact the herbaceous layer, such as in the case of edge management (Govaert et al., 2020). The diversity of tree species can positively impact its herb-layer counterpart by not only increasing environmental heterogeneity (resource heterogeneity hypothesis, Ricklefs, 1977) but also creating new environmental conditions through non-additive tree species richness effect (Ball et al., 2008). Yet, recent studies found that inconsistent results about species richness effect (Ampoorter et al., 2015; Both et al., 2011; Pasion et al., 2018) and tree species identity (Coppi et al., 2019; Corcket et al., 2020; Germany et al., 2021) or tree species abundance (Barbier, Chevalier, et al., 2009), can be more important drivers of herb-layer composition, biomass and phylogenetic diversity. This can be explained by the fact that considering tree identity could integrate their functional differences more directly than taxonomic species richness, making it a better predictor of potential theoretical ecological mechanisms influencing the distribution of the herb-layer species. Tree identity could be a better predictor (as different tree species capture a significant differential share of resources) of the site's potential abiotic limiting factor for the growth of each herbaceous species (i.e. Liebig's Law of Limiting Factors, Austin, 2007) and better capture potential niche heterogeneity by more accurately describing the functional complementarity of canopy trees (i.e. resource heterogeneity hypothesis). Additionally, if certain tree species exert greater competitive pressure on the herbaceous layer (e.g. high-nutrient or light-uptake species), this may lead to the establishment of herb-layer species better adapted to stress resistance, rather than those adapted to competition or disturbance (Grime's CSR strategy; Grime, 2006). Therefore, certain functional groupings of trees could also be more relevant for predicting the impact of the canopy on the herb-layer species. For instance, many coniferous species tend to accumulate litter, acidifying soils more than most broadleaf trees (Augusto et al., 2015; Díaz-Calafat et al., 2023), favouring acid-tolerant herbaceous species and limiting germination and survival of core-forest herbaceous species (Thomaes et al., 2013). However, Barbier et al. (2008) cautioned against simplifying the effects of coniferous versus broadleaf trees on herbaceous species in particular because some species do not share the same characteristics that are predominantly found in their groups (e.g. beech broadleaf trees that have thick litter that can acidify the soil). Moreover, alternative functional grouping based on tree identity could be more relevant for capturing the effect of this stratum on herbaceous species (e.g. Raunkiaer life form type, successional stage or Ellenberg affinity to soil acidity or humidity through competitive access to the substrate). Trees' Raunkiaer life form determines herb-layer species composition by modulating access to light, moisture, nutrients (Gilliam & Roberts, 2014; Maguire & Forman, 1983) and creating specific microsites (Glick & Matlack, 2021), such as tip-up mounds from taller trees (leading to specific herb-layer species composition; Spicer et al., 2018). Moreover, tree successional (or dynamic) stages can influence the composition and number of herbaceous species (Rybar et al., 2023) both directly (e.g. through changes in transmitted light quality and quantity), but also indirectly by impacting the abundance of organisms that influence this herb-layer, such as herbivorous insects (Hilmers et al., 2018). Nonetheless, Barbier et al. (2008) recommend exploring tree-understorey interactions as species-specific relationships, as the identity of tree species may influence herb-layer species through a combination of multidimensional functional characteristics and mechanisms not fully captured by the traits considered.

Species associations are challenging to retrieve due to datasets requirements, such as adequate resolution and high sample size (Vallé et al., 2023). Research focused on tree species identity is often restricted by a small sample size and limited spatial extent, resulting in the identification of only a few species-specific relationships (Bergès et al., 2017; Dölle et al., 2017; Nagel et al., 2019). Experimental studies exploring the underlying mechanisms of overstorey–understorey relationships can be time-consuming and require adequate designs (Both et al., 2011). As such, it is crucial to identify potential associations between a large pool of trees and herbaceous species. Several authors (Gilliam et al., 1995; Peet et al., 2014) also hypothesized that the overstorey–understorey linkage may only occur after a certain period of establishment (about 20 years of stand development), as the two layers primarily (and mainly) respond to distinct abiotic factors during early development (i.e. light availability for trees and water and nutrients availability for herb-layer species; Gilliam et al., 1995). Moreover, over time, the likelihood of new environmental conditions being created increases due to events, such as treefalls (Bartels & Chen, 2010). Additionally, the closure of the canopy from foliage growth leads to complementary crown architectures among species in the canopy space (Jucker et al., 2018; Williams et al., 2017). These findings could explain the difficulty of detecting the tree identity effect on understorey species through experimental studies (Germany et al., 2017, 2021). Moreover, several authors highlighted the lack of empirical evidence for positive associations (Carleton & Maycock, 1981; Ellenberg, 1988). This underscores the valuable contribution of large empirical data sets, including a great proportion of long-established stands.

Detecting potential associations between tree species and herb-layer species and assessing the magnitude of any tree species identity effects, can help us understand and predict spatial herb-layer distribution. In this study, we relied on a nation-wide dataset coupling overstorey–understorey sampling protocol describing tree canopy composition and herb-layer cover at fine resolution over mainland France (Vidal et al., 2005). This protocol benefits from detailed empirical environmental descriptions (abiotic and management parameters) of the sampling sites by skilled forest observers. This increases the likelihood that detected associations are not just due to species responding similarly to factors that are not considered in the analyses (Poggiato et al., 2021). Thus, we hypothesized that associations between herb-layer species and tree species cover identity can be detected (H1.a), while controlling for trees taxonomic species diversity effect and main measurable environmental factors known to influence the herb-layer distribution. We concurred with Barbier et al. (2008) and Barbier, Chevalier, et al. (2009) that the effect of tree identity cannot be sufficiently expressed through a simple binary classification of ‘broadleaf’ versus ‘coniferous’. Given the intricate array of mechanisms that interconnect these two layers, we propose that alternative tree functional groupings may offer a more comprehensive representation of the trees' influence on herbaceous plants, although no classification can fully encompass the entirety of the tree identity effect (H1.b). We also hypothesized that herbaceous species can also share a common response to tree species identity cover depending on their habitat preferences (H1.c). For instance, non-forest herb-layer species were found to have negative responses of higher magnitude with the identity of dominant tree species or their abundances compared with forest herb-layer species, in local extent observational studies either based on controlled site type sampling (Barbier, Chevalier, et al., 2009) or taking site type variables into account in the statistical model (Zilliox & Gosselin, 2014).

While the monitoring of canopy trees is facilitated by advances in remote sensing allowing recognition of many species and identification of many individuals, the herb-layer does not directly benefit from this tool. Our second hypothesis proposes that using canopy tree species identity cover could improve predictions on individual distribution of numerous herb-layer species using these species associations (Vallé et al., 2023; Wilkinson et al., 2021), in new sites (H2). This could indirectly leverage remote sensing advances and represent a major advancement in the understanding and spatial prediction of this layer, which is difficult and time-consuming to survey.