Mycorrhizal Symbioses and Plant Invasions

The factors that influence a plant’s ability to invade are not well understood. Many mechanisms are involved and the relative importance of different mechanisms depends on the specific invasion. Here we consider one factor—mycorrhizal symbioses. These symbioses are ubiquitous interactions involving the plants and soil fungi of most terrestrial ecosystems. We develop a conceptual framework for considering mycorrhizal symbioses in plant species invasions. The most critical aspects of this framework are: (a) the mycorrhizal status and (b) the growth response of the invading plant, (c) the ability of the plant to associate with different fungi, (d ) the quality of the plant as a host for local fungi and feedback dynamics, (e) the biogeography and dispersal of the fungi, ( g) the introduction and spread of the fungi, and ( g) the ecological consequences of the creation of novel mycorrhizas. These aspects can critically influence the trajectory of a plant invasion, and this symbiosis deserves more attention in plant invasion biology. 699 Review in Advance first posted online on September 23, 2009. (Minor changes may still occur before final publication online and in print.) A nn u. R ev . E co l. Ev ol . S ys t. 20 09 .4 0. D ow nl oa de d fro m a rjo ur na ls. an nu al re vi ew s.o rg by H A RV A RD U N IV ER SI TY o n 11 /0 9/ 09 . F or p er so na l u se o nl y. ANRV393-ES40-33 ARI 14 September 2009 19:58 AM: arbuscular mycorrhizal EM: ectomycorrhizal INTRODUCTION Many plant species have been introduced to new habitats throughout the world, and some also grow in abundance and extend beyond original points of introduction (Lockwood et al. 2007). Plant species that spread extensively in their novel habitats are termed invasive. Some invasive plants may have repercussions on the local, native, community and impact rare and threatened species (Wilcove & Master 2005, but see Gurevitch & Padilla 2004) or influence ecosystem properties (Razaida et al. 2008). When an invasive plant becomes a target of concern, management plans are drafted for its control. However, to craft an effective management plan, it is important to understand the mechanisms involved in the invasion process. A vast literature on plant invasions makes clear that no single mechanism can explain invasiveness. The potential for a plant species to become invasive can be influenced by its niche, competitive ability, reproductive potential, and the evolution of these traits in the novel habitat (Leger & Rice 2003, Blair & Wolfe 2004). A species’ ability to invade can also be influenced by characteristics of the habitat being invaded, including the novel biotic interactions that may occur in a new range (Mitchell et al. 2006). Specialist herbivores and pathogens have been the focus of research directed at these novel biotic interactions, and form the basis of the enemy release hypothesis (Mitchell & Power 2003, Torchin et al. 2003). Much less work has focused on the potential for mutualistic interactions to alter invasion success [but see reviews by Richardson et al. (2000) and Mitchell et al. (2006)]. Even so, mutualisms can be the central force shaping a species’ ecology (Herre et al. 1999), and mutualisms between pairs of exotic species may be at least as common as parasitisms (Simberloff & Von Holle 1999). As a result, the introduction of one species may facilitate subsequent invasions by other species (Mandon-Dalger et al. 2004). In this review, we focus on a common symbiosis that involves most plant species, the mycorrhizal symbiosis, and discuss how this symbiosis may affect the ability of a plant species to invade. When a plant species is associated with mycorrhizal fungi the symbiosis may constrain or facilitate the spread of the plant. Understanding if and how the mycorrhizal association influences plant invasion may be a key aspect of the ecology and management of invasive plant species, as well as the conservation biology of native habitats. Mycorrhizas are symbioses between plants and fungi. The association is ancient; fossil symbioses date to 460 Mya (Redecker et al. 2000). Nearly 95% of the world’s plant species belong to families that are characteristically mycorrhizal, and although the mycorrhizal status of most species has not been explicitly probed, 80% of surveyed land plant species are mycorrhizal (Smith & Read 2008, Trappe 1987, Wang & Qiu 2006). The fungi involved in the symbiosis are not a monophyleticentity and associations may involve any of four different fungal phyla. The symbioses are often classed as either arbuscular mycorrhizal (AM) or ectomycorrhizal (EM), and the different types are defined by both the taxonomy of the fungi as well as the structures formed in or around plant roots (Smith & Read 2008). In addition to AM and EM symbioses, mycorrhizal associations include arbutoid, monotropoid, ericoid, and orchid forms. Mycorrhizal symbioses are generally considered as mutualisms. Plants and fungi trade resources, often exchanging photosynthetically derived C for P and N scavenged from soils. Other benefits have been ascribed to the mutualism, for example, protection from soil pathogens (Borowicz 2001) and enhanced tolerance to drought (Augé 2001). As with most other mutualisms, the degree of benefit derived by each partner depends on the particular context of an association, and in some cases the symbiosis is a parasitism ( Johnson et al. 1997, Jones & Smith 2004). We identify critical aspects of the symbioses of plants and mycorrhizal fungi that will influence the trajectory of a plant species’ invasion. These aspects include: 700 Pringle et al. R E V I E W S