Parasitic plants are often viewed as no more than a curiosity by ecologists. Yet, they are integral to the complex trophic interactions of many communities, and their unusual features may put them at particular risk to exotic species invasions. Here we develop a hypothesis for a novel consequence of invasion that we have termed parasitism disruption.
The invasive plant species Alliaria petiolata (garlic mustard, Brassicaceae) is an abundant and aggressive component of many North American forest understories. High reproductive output, distastefulness to generalist herbivores, and shade tolerance contribute to the invasive potential of A. petiolata, but its widespread success is largely attributed to the production of novel chemical weapons (Stinson et al., 2006; Callaway et al., 2008). Among these weapons are two classes of compounds well known for their antifungal properties: glucosinolate-derived isothiocyanates and flavonoids.
Recent studies have revealed that naive North American mycorrhizae (i.e., those that have not coevolved with A. petiolata in Europe) are highly sensitive to the garlic mustard chemical cocktail (e.g., Stinson et al., 2006; Callaway et al., 2008; Wolfe et al., 2008). While the bulk of studies have focused on arbuscular mycorrhizae, ectomycorrhizal fungi are also impacted. Laboratory bioassays reveal zero growth of ectomycorrhizae in the presence of A. petiolata chemicals—and, in the field, A. petiolata-invaded sites exhibit significant reductions in ectomycorrhizal biomass (Wolfe et al., 2008).
Through release of antifungal compounds, A. petiolata can disrupt mycorrhizal mutualisms through two distinct processes: (1) hampering formation of new associations between native plants and mycorrhizae and (2) diminishing the effectiveness of existing connections (Hale et al., 2011). For forest tree seedlings, the establishment of mycorrhizal interactions is critical for growth and survival—and research shows that, when grown in A. petiolata-trained soils, tree seedlings produce less biomass as a result of reductions in the ectomycorrhizal network (Wolfe et al., 2008). Similarly, adult plants that are actively engaged in the network are expected to receive diminished resources following reductions in mycorrhizal biomass. While this has not yet been demonstrated for ectomycorrhizal plants, there is clear evidence from arbuscular mycorrhizal systems. When leaf tissue of A. petiolata is applied to soils in which adult forest herbs are growing, changes in resource availability drive declines in plant photosynthetic rates (Hale et al., 2011). This diminished carbon gain scales up and, over time, translates into declines in carbon storage and key plant vital rates, such as flowering frequency (Brouwer et al., in press).
Ultimately, the dramatic effects of A. petiolata on mycorrhizal associations are predicted to lead to disruptions in plant population processes and community diversity. Research on the direct effects of A. petiolata on mycorrhizal fungi indicates that subsequent indirect effects on seedling growth (Stinson et al., 2006) and plant carbon gain (Hale et al., 2011) represent forms of mutualism disruption.
Consideration of the complexity of trophic interactions in the forest understory suggests that mutualism disruption, in the context used here, is unlikely to solely affect the relationship between mycorrhizal plants and their fungal partners. We hypothesize that a breakdown in mycorrhizal networks will also alter the performance of co-occurring parasitic and saprotrophic plants, particularly species engaged in mycoheterotrophy.
The natural history of mycoheterotrophy was poorly understood for some time. In fact, it took more than a century of meticulous observations, methodical experimentation, and careful conjecture (reviewed by Bidartondo, 2005) for botanical scientists to elucidate the trophic role of the first species identified as mycoheterotrophic, Monotropa hypopitys (pinesap, Ericaceae). Clearly, this achlorophyllous forest wildflower was not photosynthetic and thus needed to acquire its carbon from some other source, yet attempts to confirm early assumptions that it was a parasite on nearby tree roots were confounded when no evidence of physical root-to-root connections could be confirmed. Numerous scientists weighed in on the evidence, with much of the discussion finally coming down to a simple question: How can this species be a parasite when it is not actually known to penetrate the roots of other plants? Eventually, the groundbreaking solution to the “Monotropa argument” became clear: this species and the other members of the temperate subfamily Monotropoideae were mycoheterotrophs tapping not into host plants, but into their mycorrhizal associates (Björkman, 1960).
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Species such as Monotropa hypopitys, M. uniflora (Indian pipe), and Pterospora andromedea (pinedrops) are each engaged in belowground tripartite relationships in which they pilfer carbon after host trees have transferred it to their mycorrhizal fungi. Unlike typical ectomycorrhizae (with hyphae remaining within intercellular spaces), these fungi (christened monotropoid mycorrhizae) employ specialized fungal pegs to invaginate cell walls within the roots of the parasitic plant (Finlay, 2008). The importance of this connection is paramount to the survival of monotropoid plants; they rely entirely on monotropoid mycorrhizae for both carbon and nutrients (Finlay, 2008).
Given these interactions, Monotropa and relatives may be considered epiparasites on forest trees and the mycorrhizal networks surrounding them (Björkman, 1960). With no need for photosynthesis, or the ability to conduct it, monotropoid plants typically enjoy little competition in densely shaded herb layers where low light availability excludes many photosynthetic herbs.
The shade tolerance of Alliaria petiolata, however, has meant that it is presently invading understory communities where monotropoid plants occur. By reducing mycorrhizal associates of forest trees in these communities, A. petiolata may be causing declines in the populations of associated monotropoids. As such, the mutualism disruption attributed to A. petiolata (Stinson et al., 2006; Hale et al., 2011) would also function as a “parasitism disruption” leading to reduced opportunities for mycoheterotrophs to acquire carbon and nutrients.
Parasitism disruption could lead to declines in monotropoid species that are already restricted in distribution to where their host trees (mainly conifers, but also some hardwoods) and specified host fungi occur. These limited, often disjunct, occurrences are cause for concern because of the potential to affect already-established monotropoid individuals/populations, but recruitment of new individuals is also likely to decline precipitously in sites where A. petiolatainvades. Monotropoid seeds germinate in response to fungal cues, then quickly make connections to mycorrhizal hyphae required for seedling survival (Bidartondo, 2005). This makes germination a “critical checkpoint” (Bidartondo, 2005) where the loss of mycorrhizal fungi would result in a consequent bottoming-out of germination rates and new seedling recruitment.
For monotropoid species that are already considered threatened and are known from limited numbers of localities, A. petiolata represents a critically proximal local extinction threat. As an example, populations of the infamously uncommon Pterospora andromedea (pinedrops) in the eastern United States have been recorded in less than 20 locations since 1970—with only three known populations in New England (Schori, 2002). In one of the few sites presently known from the state of New York, the species occurs under a denseThuja–hardwood canopy in a natural area where A. petiolata is abundant (C. T. Martine, personal observations). Protection of this species, and other mycoheterotrophs like it, requires that the forests where populations occur be actively managed for removal of and/or Early Detection and Rapid Response (EDRR) to A. petiolata incursions. Otherwise, the combined effects of mutualism disruption and parasitism disruption could hasten collapses in mycoheterotrophic plant populations, consequent with declines in mycorrhizal plants, wherever A. petiolata occurs.
Parasitism disruption by A. petiolata could also negatively affect co-occurring mixotrophic parasites (e.g., some orchids and other Ericaceous taxa likePyrola), but we might expect these species to fare better because of their ability to use both photosynthesis and mycoheterophy. Although mixotrophs would face stress and even decline, they may not experience the rapid localized extinctions predicted for sympatric achlorophyllous monotropoids.
Mounting evidence for negative effects of invasive plant phytochemicals on native mycorrhizal associations outside the Alliaria study system (e.g., Zhang et al., 2007; Meinhardt and Gehring, 2012; Ruckli et al., 2014) suggests that parasitism disruption has the potential to foster consequences beyond the specific example described here. Biological invasions have been recognized as the cause of a diverse suite of biodiversity impacts (Pyšek et al., 2012); future testing of the parasitism disruption hypothesis will help us understand whether it deserves a place among them