Tamm reviewsTamm review: Forest understorey and overstorey interactions: So much more than just light interception by trees
Introduction
Biotic and abiotic interactions are key processes driving ecosystem composition and dynamics. The balance of competition and facilitation (along with other types of interaction) has often been highlighted as a fundamental mechanism of species coexistence and ecosystem dynamics (Callaway, 1995). Understandably, the influence of the tallest trees has been emphasised in many forest ecosystems, because they intercept a large proportion of incident light. Many studies have reported the effects of overstorey trees on light availability in the understorey and related physical variables that define the microclimate (e.g. radiation, temperature, air humidity, wind velocity, e.g. Valladares et al., 2016, Wagner et al., 2011). Overstorey trees are also an important component determining the forest water balance, by both their evapotranspiration and their interception of rainfall (e.g. Aussenac, 2000). Their contribution to the cycling of the main nutrients (e.g. via litter inputs, leachates and root exudates) is also essential (e.g. Johnson and Turner, 2019). However, a forest has other strata: midstorey trees, understorey trees, shrubs and herbaceous vascular plants, bryophytes, and epiphytes. In many studies, their presence has been addressed from the standpoint of diversity (e.g. Barbier et al., 2008), and their functional roles have drawn less attention (but see Landuyt et al., 2019). Yet these strata also intercept light, contribute to understorey microclimate, intercept throughfall, and can represent a non-negligible part of the total ecosystem evapotranspiration (Balandier et al., 2022).
In the first part of this review, we briefly recall the role of over- and understoreys in structuring forest microclimate, mostly through light sharing (Fig. 1, bubble 1). However, the forest also has a hidden realm, that of belowground interactions. Probably owing to the difficulties studying belowground processes, the literature frequently minimises belowground interactions in the relationships between overstorey trees and understorey vegetation (but see the specific review of Coomes and Grubb, 2000). Understorey vegetation most often colonises the top horizons, and trees the deepest ones, suggesting a spatial complementarity, although this is not always observed. However, some early studies reported that overstorey trees could suppress understorey vegetation by belowground competition, to an extent that had been largely underestimated, in some cases surpassing competition for light (reviewed by Coomes and Grubb, 2000). Some understorey species can survive deep shade (Valladares et al., 2016, Vernay et al., 2019) yet may succumb to belowground competition. Competition for soil resources (water and nutrients) to the advantage of understorey vegetation and at the expense of overstorey trees has been considered in only a few studies (Li et al., 2012). The second part of this review will discuss this competition (Fig. 1, bubble 2).
Many other life forms interact with trees and understorey vegetation. This review does not seek to give an exhaustive account of all the many processes influencing the interactions between over- and understorey. We will focus on the roles of two significant actors, namely mycorrhizae and herbivores.
The over- and understorey extend belowground through their root systems, prolonged by the mycelia of symbiotic mycorrhizal fungi that scavenge soil resources (Fig. 1, bubbles 4 and 5). Mycorrhizal associations improve nutrient and water acquisition by host plants (86% of terrestrial plant species form mycorrhizal associations with fungi; Brundrett, 2009) and support their health and resistance to pathogens (Smith and Read, 2008). Forests mainly harbour (i) ectomycorrhizae (EcM) associated with most canopy tree families (e.g. Fagaceae, Pinaceae, Betulaceae) from seedling to adult stages, (ii) vesiculo-arbuscular mycorrhizae (AM) associated with most families of understorey mosses, grasses, and forbs along with some woody families (e.g. Malaceae, Rosaceae and other Rosales, Aceraceae), and (iii) ericoid mycorrhizae (ErM) associated with Ericaceae shrubs, most importantly in boreal forest ecosystems.
Herbivory is the consumption of living above- and belowground plant material. It is an ecological process that drives evolutionary adaptations in both plants and animals (Agrawal, 2007, Futuyma and Agrawal, 2009, Burkepile and Parker, 2017, Pausas et al., 2018). Although invertebrate herbivory is significant, this review focuses on how vertebrate herbivory operates in over- and understorey dynamics, more specifically that of large mammalian herbivores (hereafter LMHs, Fig. 1, bubbles 8 and 9). For interactions between invertebrate herbivory and understorey, readers can refer to two recent reviews that address effects on carbon storage and belowground responses (Piper et al., 2018, Kristensen et al., 2019).
Finally, we look at the implications for forest management in the current unstable period of climate and global changes facing our forest ecosystems and point out some issues that need more research (Fig. 1, bubbles 3, 6 and 7).
We recognise that considering other forest ecosystems in different climates would have enabled broader generalisation. However, for this review we opted to consider mostly boreal, temperate, and Mediterranean forest ecosystems. These three ecosystems share common features, contrasting seasons, and dominant families of tree species. However, soil fertility, understorey cover and development, and climate all vary among these three forest types. In this review, overstorey means the main tall trees composing the adult tree canopy. Understorey vegetation includes all plants below the overstorey, whether midstorey trees, shrubs, forbs, graminoids, ferns, or bryophytes.
Section snippets
Light interception: A key driver of microclimate
It has been amply demonstrated that light interception by overstorey trees controls the dimensions and composition of understorey vegetation (e.g. Barbier et al., 2008, Wagner et al., 2011, Valladares et al., 2016). Counterintuitively, many plant species can survive deep shade, or at least require much less light than, for example, the light requirement indicator value (L) given by e.g. Ellenberg et al. (1991). This ability can be viewed as a plant life strategy (sit-and-wait theory) to persist
The underestimated role of understorey
Most studies have related water balance in the forest ecosystem to tree cover. Trees are obvious key drivers: the greater the forest cover, the higher the evapotranspiration (ET) and rainfall interception (e.g. Aussenac, 2000, Barbier et al., 2009). Accordingly, an increase in soil water content (SWC) after tree thinning operations has been widely reported in different ecosystems (e.g. Bréda et al., 1995, Aussenac, 2000, Giuggiola et al., 2016).
Water consumption by trees can be detrimental to
The complex nature of interactions for nutrients
Increased light, water, and nutrients are often observed when overstorey cover is reduced (Wagner et al., 2011). These conditions often promote the development of understorey vegetation. It can take up a non-negligible proportion of available nutrients to the detriment of overstorey trees. This effect has for example been observed for phosphorus in Pinus radiata plantations, depending on the understorey species considered (such as Austroderia toetoe, buddleia sp., Cytisus scoparius,
What does all this mean for stand management?
Forest managers may be tempted to ignore understorey vegetation as an insignificant part of the ecosystem in comparison with overstorey trees. However, we demonstrate that the interactions between over- and understorey do not reduce to light pre-emption by the overstorey to the detriment of the understorey. The understorey can also compete for water and nutrients and affect overstorey growth, and through interactions with biotic factors such as mycorrhizae and herbivores it can modify fluxes
Unaddressed issues
We have shown that complex processes determine the interactions between over- and understorey. Light is clearly a structuring component of the aboveground strata of the forest, and competition for light determines the outcome of many processes. However, the hidden realm of the forest ecosystem, the belowground part, also plays an underestimated role in ecosystem structuration. Besides competing for water and nutrients, over- and understorey are linked through complex networks of mycorrhizal
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
The authors thank Thérèse Danieau for the picture summarising the paper, and for her constructive comments. They also thank two anonymous reviewers for their helpful comments on a first version of this manuscript.
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