Many ecologists studying the invasion biology of exotic plants have adopted the Gleasonian view that plant communities are primarily structured on the basis of competitive individualistic interactions and are primarily not structured on the basis of interdependent interactions (i.e. direct and indirect facilitation) (e.g. Bruno et al., 2005). However, some have speculated that facilitative interactions affect plant invasions (reviewed in Simberloff & Von Holle, 1999); for example, some invasive grasses increase the prevalence of fires, which negatively affects resident species and indirectly facilitates additional invasion (D’Antonio & Vitousek, 1992). A literature survey reveals that competitive interactions may be overemphasized relative to their actual occurrence in nature compared with facilitative interactions; however, this conclusion is based primarily on studies describing associational patterns (Bruno et al., 2005). It is clear that many more studies have been conducted that have tested for competitive effects than have tested for facilitative effects (Bruno et al., 2005). Furthermore, most studies relating to invasion biology are based on associational patterns and relatively few have included rigorous field experiments that characterize individual direct and indirect interactions (Simberloff, 2004; Bruno et al., 2005). A clever and insightful study by Saccone and colleagues in this issue of New Phytologist (pp. 831–842) addresses this concern with manipulative experiments that help to elucidate the effects of direct and indirect interactions on the invasion process occurring in a European floodplain.
‘…A. platanoides was observed to actually reduce its internode lengths with reductions in R : Fr in an apparent attempt to ‘sit-and-wait’ rather than compete for light in an unfair duel with canopy trees.’
Saccone and colleagues performed a field experiment along a successional gradient and manipulated the effects of different canopy types and the presence of the understory herbaceous layer on juvenile tree species. Disturbance by flooding drives the successional gradient at the study site. Existing theory, on the organization of natural plant communities, predicts that direct facilitative effects are most likely in environments with a high level of physical stress (Bertness & Callaway, 1994). Consistent with this prediction, they found that the resident Salix alba tree canopy, in the early-seral habitat of the floodplain (Fig. 1), had direct facilitative effects on the invasive Acer negundo and the late-seral Fraxinus angustifolia. This was counterbalanced by the competitive effects of the herbaceous layer, and results suggest a net facilitative effect of the two vegetative layers on juvenile A. negundo and F. angustifolia. Establishment of exotic invaders is affected by two important processes: propagule supply processes and post-dispersal recruitment processes. The reported facilitative effects are believed to buffer the Acer recruits from the impacts of flood disturbance. This and the species’ ability to disperse via water appear to be essential for its invasion into the studied floodplain, while competitive effects exerted by the herbaceous layer help to limit their invasion into this zone of the floodplain (Fig. 1).
Saccone and colleagues report further that the invasive Acer populations facilitate their own continued presence by both direct facilitation and indirect facilitation effects of the Acer canopy on juveniles of this species. As the recruits grow, their population develops into reproductive trees that form a forest intermediate between the Salix and Fraxinus forests along the successional gradient (Fig. 1). The developing Acer-dominated forest accelerates structural changes along the successional gradient, leading to increased shading of the understory compared with the early-seral Salix forest (Fig. 1). A characteristic of other invaded systems is that they alter ecosystem processes and successional trajectories, which may negatively affect resident species while either directly or indirectly facilitating invasion (e.g. Reinhart et al., 2006; Dehlin et al., 2008). The increased shade caused by the Acer canopy appears to have a direct negative effect on the understory herbaceous layer and weakens the competitive effects of the herb layer on Acer juveniles. The Acer canopy, therefore, indirectly facilitates establishment of its recruits by ameliorating the negative effects of the herbaceous layer on its juveniles. Although not in an invasion context, Acer pseudoplatanus in its native European forests has also been observed to indirectly facilitate establishment of its seedlings by reducing the competitive effects of understory forbs on A. pseudoplatanus seedlings (Pagès et al., 2003). Other invasive tree species are known to reproduce in intact forests, and then to ‘sit-and-wait’ and rapidly exploit any newly formed canopy gaps with great efficiency compared with the resident natives (Closset-Kopp et al., 2007). Martin & Canham (2010) found variation among the survival characteristics of seedlings of native and invasive Acer species, indicating that variation among phylogenetically related species is important in determining which become invasive. Evidence is beginning to emerge suggesting a type of syndrome among some invasive plants that share the functional characteristic of shade tolerance and the ability of adults to alter canopy structure in systems where the resident species lack a similar combination of characters.
Parallels between the study by Saccone et al. and other studies suggest that invader-driven changes in the understory light environment, which differ from natural rates of succession and/or trajectories, may be a common mechanism by which invasive species disrupt natural communities and facilitate their own invasion (Reinhart et al., 2006; Dehlin et al., 2008; Valladares & Niinemets, 2008). Acer platanoides, which is native to Europe, has invaded North American forests, and in some invaded forests has caused canopy-driven changes that have quantitatively and qualitatively (red : far-red (R : Fr)) altered the understory light environment compared with uninvaded forests (Reinhart et al., 2006). The study by Reinhart et al. (2006) also provides suggestive support for indirect facilitation, as the invader-driven alteration of the understory light environment reduced the survival of many resident species while its seedlings were uniquely capable of surviving and optimally allocating resources. This change in understory light quantity and quality with canopy closure is not surprising; however, the plants’ responses to the change in R : Fr were relatively unusual. In response to reductions in R : Fr, most plants are thought to follow the shade avoidance syndrome and elongate their stems and increase their internode lengths in an attempt to aggressively compete for light with similar-sized neighbors (Smith, 2000). Much of this research, however, has focused on shade-intolerant and early-seral species in contexts where symmetric competition for light is likely. Seedlings that elongate in response to the light environment created by mature trees would probably experience increased mortality as a result of producing long slender stems. This may explain why A. platanoides was observed to actually reduce its internode lengths with reductions in R : Fr in an apparent attempt to ‘sit-and-wait’ rather than compete for light in an unfair duel with canopy trees (K. O. Reinhart, unpublished data). Different environmental cues are thought to elicit shade tolerance (photosynthetically active radiation (Smith, 1982) and blue light (Lin, 2000)) vs shade avoidance responses (R : Fr). Shade tolerance may depend on synergistic responses to the collinear changes in light quantity and R : Fr that help prolong survival until light conditions change and facilitate growth (Valladares & Niinemets, 2008).
Documenting associational patterns is likely to always be an important aspect of invasion biology. Advances in the field, however, are likely with studies that couple information on associational patterns with descriptions of species’ interactions. Incorporating a more mechanistic understanding that can account for direct facilitative and indirect effects will require manipulative experiments to better understand the complex of interactions shaping natural communities and plant invasions. Combining knowledge of associational patterns with more reductionist and mechanistic experimental approaches will advance our understanding of invasion biology and improve our ability to predict and manage invaders and improve restoration (Simberloff, 2004). Increasing evidence is accumulating that shows exotic plants are invading mature undisturbed forests (reviewed in Martin et al., 2008). However, the vast majority of invasion biology research has focused on early-seral habitats. Studies in these additional systems may be essential for building an understanding, especially if knowledge regarding early-seral environments is not transferable, as suggested in the above case of phenotypic responses to changes in R : Fr. Future studies are needed that continue to perform field experiments and advance our understanding of the interactions contributing to invader establishment, spread, and impact in multiple systems.