Elsevier

Forest Ecology and Management

Volume 526, 15 December 2022, 120584
Forest Ecology and Management

Tamm reviews
Tamm review: Forest understorey and overstorey interactions: So much more than just light interception by trees

https://doi.org/10.1016/j.foreco.2022.120584Get rights and content

Highlights

  • Interactions between over- and understorey do not reduce to light pre-emption by the overstorey.

  • Besides light interception, overstorey controls the development of understorey vegetation by belowground competition.

  • In turn, understorey drives overstorey development by sharing belowground resources and common mycorrhizal networks.

  • Drought stress alleviation and nutrient sharing by mycorrhizae rely mostly on overstorey-driven processes.

  • Large mammalian herbivores modulate below- and aboveground resource sharing through complex indirect interactions.

Abstract

Plant interactions play a key role in forest ecosystem dynamics. The tallest plants, namely the overstorey trees, are obvious major drivers, particularly in competition for light. This process has already been amply described. However, the role played by lower strata has often been underestimated. In this review, we first briefly recall the role of over- and understoreys in structuring forest microclimate, mostly through light sharing. We then focus on belowground interactions between over- and understorey, where knowledge is more piecemeal, partly because of measurement difficulties. Even so, some studies show that competition for water and nutrients by the overstorey controls the development of understorey vegetation much more than competition for light. The reverse (overstorey limitation by the understorey) has also been encountered, but has been much less well researched. We also address the involvement of mycorrhizae, specifically their role in alleviating overstorey drought stress and contributing to nutrient cycling. We go on to show how another example of key ecosystem engineers, large mammalian herbivores, shape above- and belowground resources and intervene in over- and understorey interactions. In conclusion, for a better understanding of forest dynamics and adapted management, particularly in the context of global climate change, we advocate taking account not only of trees but of all forest components. Belowground processes need more research. The roles of mycorrhizal networks, root exudates, microbiota, and chemical cues need to be further explored to gain a finer understanding of the interactions between over- and understorey.

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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