Causes, Effects, and Consequences

This section describes different ways that a dense understory canopy can suppress regeneration. Because most studies fail to distinguish among these mechanisms, Muller (1969) proposed the term interference to describe the suppression of one species or layer on another species. In the following sections, the literature is briefly reviewed to evaluate the evidence for six different mechanisms of interference between the understory layer and co-occurring tree species. These mechanisms include: (1) resource competition, (2) allelopathy, (3) physically impeding seedling germination and growth, (4) through modifications of interspecific interactions (see figure at right). We suggest that the most efficient and cost-effective remediation of the deleterious effects of these recalcitrant understory layers will require a greater understanding of how these layers alter patterns of forest regeneration and succession.

In forested systems, perhaps the most prominent interference mechanism exerted by a recalcitrant understory layer would be direct competition for above- and below-ground resources. In closed canopy forests, dense understories exacerbate the degree of light attenuation caused by the midstory and canopy (Beckage and others 2000, de la Cretaz and Kelty 2002, Messier and others 1998, Nilsen and others 2001). Photosynthetically active radiation (PAR) levels can drop well below 5 percent of full sun beneath these layers (Aubin and others 2000, Clinton and Vose 1996, George and Bazzaz 1999a, Hill 1996, Horsley 1993a, Kelly and Canham 1992, Lei and others 2002, Lusk 2001, Nakashizuka 1987, Wada 1993, Walker 1994). Additionally, these dense, low canopies can reduce light quality, (e.g., red: far-red wavelengths), thereby preventing germination, altering internode elongation, and inhibiting flowering (Horsley 1993a, Mancinelli 1994, Messier and others 1989). Furthermore, dense, low canopies decrease the availability of sunflecks particularly for seedlings (Denslow and others 1991, Lei and others 2002, Nilsen and others 2001). Finally, if canopy gaps do form, they may not operate as gaps at all if seedlings remain trapped beneath a dense understory layer (Beckage and others 2000, Lusk 2001, Webb and Scanga 2001). Under this scenario, regeneration may be limited to only a few individuals of those few species that are highly shade-tolerant.

Dense understories may also exacerbate belowground competition (Dillenburg and others 1993, Messier 1993, Putz and Canham 1992). Some studies infer resource limitation by detecting increased growth or survival of target plants following fertilization or measuring lower nutrient and water concentrations in soil beneath dense understory cover vs. more open areas, (e.g., Inderjit and Mallik 1996, Messier 1993, Nilsen and others 2001, Yamasaki and others 1998). Similarly, vine-covered saplings often have lower foliar nitrogen levels, reduced preleaf water potential, and decreased diameter growth when compared to vine-free saplings (Dillenburg and others 1993, Perez-Salicrup and Barker 2000). The above studies are suggestive of resource limitation though they typically do not distinguish between competition for water vs. soil nutrients. Because nutrient and water availability covary, decoupling these two factors is difficult (Casper and Jackson 1997, Nambiar and Sands 1993). Additionally, few experiments use factorial manipulations to disentangle a dense understory layer’s aboveground vs. belowground effects and their interactions (McPhee and Aarssen 2001).

Horsley (1993a) experimentally tested the influence of aboveground vs. belowground competition. He tied back hay-scented fern fronds while leaving their roots and rhizomes intact, thereby reducing light competition and isolated seedlings within PVC tubes, thereby reducing root competition. He found that light attenuation, not belowground competition, was the mechanism of interference (Horsley 1977, Horsley 1993a, Horsley 1993b). Putz and Canham (1992) conducted similar aboveground and belowground manipulations. They found that a dense shrubby understory layer reduced tree regeneration primarily because of belowground competition (see also Christy 1986), although this varied with soil fertility. Belowground competition was more important in infertile sites, whereas aboveground competition was more important in fertile sites. Clearly well-replicated factorial experiments are required to ascertain the relative importance of aboveground vs. belowground competition, although other processes may confound the results of these experiments, (e.g., allelopathy; see section on allelopathy).

This section discusses the potential effects of the phenomenon called allelopathy: i.e., the inhibition of growth or survivorship of one plant species by chemicals produced by another species. Direct field evidence for allelopathy remains equivocal and elusive. In forests that have dense understories dominated by ericaceous shrubs, the phenolics and other phytochemical compounds produced by these shrubs can disrupt nitrogen mineralization and inhibit ectomycorrhizal fungi; this significantly reduces conifer growth and survivorship (Walker and others 1999; reviewed by Mallik 1995, 2003 and Wardle and others 1998). In these systems, Nilsson (1994) used factorial manipulations of aboveground and belowground competition and allelopathy to identify how the boreal shrub Empetrum hermaphroditum suppressed tree regeneration. She found that both belowground competition and allelopathy were important, but that belowground competition played the primary role. Similarly, Jäderlund and others (1997) found that Vaccinium myrtillus interfered with Norway Spruce (Picea abies) primarily through belowground competition. In forests where ferns form dense understories, bioassays and greenhouse studies have suggested the potential for strong allelopathic effects on tree regeneration (Gliessman and Muller 1972, Gliessman and Muller 1978, Horsley 1977); however, further field experimentation failed to find strong allelopathic effects (Den Ouden 2000, Dolling 1996, Horsley 1993b, Nilsen and others 1999). Despite these results, too few studies have tried to experimentally disentangle resource competition from allelopathy via field experiments. Future research must move beyond merely documenting the existence of phytotoxic exudates in greenhouse and laboratory studies (Fuerst and Putnam 1983, Inderjit and Callaway 2003, Weidenhamer 1996, Williamson 1990).

This section discusses how a dense understory layer can increase the activity of small mammals, thereby increasing the rate and impact of seed and seedling predation (Den Ouden 2000, George and Bazzaz 1999a, Gliessman 1978, Schreiner and others 2000, Wada 1993). This can create a situation where it appears that low seedling densities are caused by resource competition, (e.g., light attenuation) when, in fact, they are caused by seed and seedling predation (Connell 1990, Holt 1977, 1984). Connell (1990) defined this as a type of apparent competition (sensu Holt 1977, 1984). Experiments that use canopy removals confound the direct competitive release caused by the removal of the understory layer with the indirect benefits of removing this layer, particularly the decrease in seed and seed predation by small mammals (Reader 1993). Even though small mammals are abundant, forage preferentially beneath dense vegetative cover, and consume copious quantities of seeds, few experiments have attempted to evaluate the role of seed or seedling predators vs. resource competition. Nonetheless, long-term studies in other plant systems have documented that selective seed and seedling predation can lead to rapid changes in plant community composition, (e.g., Brown and Heske 1990, Gill and Marks 1991, Howe and Brown 2001, Ostfeld and Canham 1993).

A thick litter layer typically reduces plant species diversity and density through a wide variety of direct and indirect mechanisms (see Facelli and Pickett 1991). For example, George and Bazzaz (1999a) found that a thick fern litter layer directly limited the establishment of small-seeded tree species (see also Beckage and others 2000, Farris-Lopez and others 2004, Lei and others 2002, Veblen 1982). Alternatively, in boreal forests, the insulative properties of a dense grass litter layer results in decreased soil nitrogen mineralization, water uptake, and seedling photosynthetic rates, thus indirectly diminishing conifer growth and survival (Cater and Chapin 2000, Hogg and Lieffers 1991, Lieffers and others 1993). Aside from these examples, there are few experimental tests that unravel the many facets of litter interference or evaluate its importance relative to other mechanisms, (e.g., resource competition). However, in forests characterized by a recalcitrant understory litter layer, it is clear that this alternative remains a viable and potentially important mechanism.

A dense understory layer can reduce tree seedling regeneration via non-competitive, physical interference. Clark and Clark (1991) demonstrated that the passive shedding of branches and leaves of subcanopy palms smothered seedlings present in the understory. Similarly, collapsing Guadua bamboo culms can reduce tree seedling growth and survival (Griscom and Ashton 2003). Additionally, the physical weight of a large liana load may suppress tree seedling and sapling growth (Gerwing 2001, Putz 1991, Schnitzer and others 2004). If tree species respond differentially to these physical stresses, then this mechanism alone can potentially alter understory tree species composition and modify future successional trajectories, (e.g., Gillman and others 2003, Guariguata 1998).

This section discusses how the intensity and duration of any particular interference mechanism can vary temporally as a result of the species’ life history, whether evergreen, deciduous, or monocarpic. In fact, this trait may provide clues to understand both the strength and type of interference. For example, evergreen species may pose a greater impediment to tree regeneration as their effects are exerted throughout the year on all tree seedling life-history transitions (Givnish 2002). In contrast, herbaceous perennials that senesce in the fall or deciduous shrubby species only exert competitive effects during the growing season (e.g., de la Cretaz and Kelty 2002, Nilsen and others 2001). This delayed expansion of the recalcitrant understory layer provides a brief window of opportunity for evergreen tree species, species with early germination, (e.g., Acer rubrum), or species with early leaf expansion, (e.g., Betula lenta) to overcome the understory stratum’s deleterious effects on early establishment. This temporal advantage can provide sufficient photosynthetic and growth opportunity to enable trees to survive and eventually grow through a fern layer (de la Cretaz and Kelty 2002). Additionally, if the intensity of seed and seedling predation decreases with senescence of the low canopy, then the impact of pervasive seed predation may decrease in the fall. This timing of senescence may generate increased predation on early seed dispersers, (e.g., Quercus spp.) relative to later dispersers, (e.g., A. saccharum, Fagus grandifolia).