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The Invasive Plant Alliaria Petiolata (Garlic Mustard) Inhibits Journal of Ecology 2008, 96, 777–783 doi: 10.1111/j.1365-2745.2008.01389.x TheBlackwell Publishing Ltd invasive plant Alliaria petiolata (garlic mustard) inhibits ectomycorrhizal fungi in its introduced range Benjamin E. Wolfe1*, Vikki L. Rodgers2, Kristina A. Stinson3 and Anne Pringle1 1Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA; 2Department of Biology, Boston University, Boston, MA 02215, USA; and 3Harvard Forest, Harvard University, Petersham, MA 01366, USA Summary 1. Ectomycorrhizal (EM) fungi play key roles in forest ecosystems, but the potential effects of invasive plants on EM fungal communities have not been assessed. In this study, we tested whether the non-mycorrhizal herbaceous plant Alliaria petiolata (garlic mustard) can alter the abundance of EM fungal communities in North America. 2. In three forests in New England, USA, we compared EM root tip abundance in soils where A. petiolata had invaded to adjacent areas without a history of A. petiolata invasion. At one site, we also intensively sampled EM root tip abundance across the edges of A. petiolata patches to determine the spatial pattern of A. petiolata effects on EM fungi. In a glasshouse experiment, we experimentally invaded soils with A. petiolata and Impatiens capensis, a native species and compared EM fungal colonization of white pine (Pinus strobus) seedlings grown in both soils. We also measured the effect of the A. petiolata allelochemical benzyl isothiocyanate on the growth of three species of EM fungi in pure culture. 3. In the field, EM fungal root tip biomass was lower in invaded soils, with the strongest reductions observed in forests dominated by conifers. Alliaria petiolata invasion did not have a significant effect on total root biomass. The influence of A. petiolata on EM fungal abundance in the field was localized, with the strongest inhibition observed within 10 cm of the edge of A. petiolata patches. 4. Pine seedlings growing in soils that were experimentally invaded with A. petiolata also had lower EM fungal root tip biomass compared to uninvaded soils. The native species I. capensis caused sim- ilar reductions in EM fungal colonization. Growth of pure cultures of all three species of EM fungi was completely inhibited by benzyl isothiocyanate. 5. Synthesis. Alliaria petiolata inhibits the growth of EM fungi in forests of its introduced range. Changes in EM fungal communities caused by the invasion of A. petiolata may influence tree seedling establishment and biogeochemical cycling. Key-words: Alliaria petiolata, ectomycorrhizal fungi, exotic plant invasion, garlic mustard, invasive species, mycorrhizal fungi, Pinus strobus Journal of Ecology (2008) doi: 10.1111/j.1365-2745.2008.0@@@@.x species-specific responses to nutrient inputs (Peter et al. 2001; Introduction Lilleskov et al. 2002; Avis et al. 2003). Management practices As diverse and abundant constituents of forest microbial such as timber harvesting and prescribed burning can also communities, ectomycorrhizal (EM) fungi play key roles in cause changes in the composition and function of EM fungal the functioning of forest ecosystems (Aerts 2002; Read et al. communities (Jones et al. 2003; Lazaruk et al. 2005). 2004). Direct and indirect effects of human activities can alter The invasion of exotic plants into forests may be another the composition and function of EM fungal communities way by which human activities can indirectly impact EM by changing the abundance and composition of hosts and communities. Dominant native plant species have been properties of the soil. For example, studies in a number of shown to influence the abundance of EM fungi in the soil different ecosystems have shown that nutrient deposition and on roots of neighbouring plants through the production can alter the composition of EM fungal communities, with of inhibitory compounds or from competitive interactions (Nilsson et al. 1993; Walker et al. 1999; McHugh & Gehring *Correspondence author. E-mail: [email protected] 2006). When an exotic plant becomes dominant in a forest © 2008 The Authors. Journal compilation © 2008 British Ecological Society 778 B. E. Wolfe et al. community, it may also be capable of changing the com- Methods position and function of the EM fungal community using similar mechanisms. Although exotic plants have been EXPERIMENT 1: EFFECTS OF ALLIARIA PETIOLATA IN shown to affect other components of native soil communities THREE FORESTS (reviewed in Wolfe & Klironomos 2005), the potential impact We assessed the influence of A. petiolata invasion on EM fungi in of an exotic plant invasion on EM fungi has not been the field at three different forests in New England, USA. We chose assessed. our sites based on an abundance of A. petiolata at the sites and Allliaria petiolata (garlic mustard) is an exotic plant of dominance of these sites by EM tree species. The first site is a temperate latitudes that has the potential to alter EM fungal stand of P. strobus (hereafter called ‘Pine Stand’) in Falls Village, communities. It is an herbaceous biennial in the family CT. The understorey at this site consists of Trientalis borealis, Fragaria Brassicaceae that does not form mycorrhizal associations. virginiana and Arisaema triphyllum. The second site is a mixed It is one of the few plant species that has been able to success- deciduous conifer forest (hereafter called ‘Mixed Forest’) located in fully invade forest understorey plant communities of North Salisbury, CT with Tsuga canadensis, Quercus rubra and Populus America (Nuzzo 2000). In many forests A. petiolata can become deltoides as the dominant EM trees and Maianthemum canadense, the dominant understorey species, often forming distinct, Smilacina racemosa and Solidago spp. as understorey herbaceous plant species. The third site is an urban forest (hereafter called high density patches (Winterer et al. 2005). Previous studies ‘Urban Forest’) at the Arnold Arboretum in Boston, MA, where have shown that arbuscular mycorrhizal (AM) fungi are both native (T. canadensis) and exotic (Picea abies) conifers are the almost completely eliminated from the roots of tree seedlings dominant tree species and the understorey consists of Dennstaedtia growing in soils where A. petiolata had invaded (Roberts & punctilobula, Solidago flexicaulis and M. canadense. Anderson 2001; Stinson et al. 2006). This species has the Within an area approximately 40 × 40 m2 at each of the three sites, potential to degrade local mycorrhizal mutualisms leading to we established 1 m2 plots in twelve locations: six plots were in areas a positive feedback that favours its growth over those of invaded by A. petiolata and six plots were in adjacent areas without native mycorrhizal-dependent species (Vogelsang et al. 2005; A. petiolata. Uninvaded plots were at least 2 m but not greater than Reinhart & Callaway 2006). Previous work with A. petiolata 5 m from the nearest A. petiolata plant. To minimize major differ- was based on mycorrhizal associations resynthesized in the ences in soil characteristics uninvaded plots were placed near glasshouse. Therefore, the strength of the effects of A. petiolata invaded plots. Areas invaded by A. petiolata had densities of at least 100 plants m–2. on mycorrhizal fungi colonizing mature tree roots in the In the third week of June 2006, two cores (5 cm diameter to a field is unknown. Moreover, these studies were in forests depth of 5 cm) were taken from randomly selected locations dominated by AM fungi, so responses of EM fungi to within each plot. We chose this sampling depth because at these A. petiolata are unknown. Given that EM and AM fungi are sites A. petiolata root density and EM root tip density are greatest phylogenetically distinct (James et al. 2006) and functionally within the top 5 cm of soil (B. Wolfe, personal observation). The divergent (Aerts 2002), their responses to A. petiolata invasion cores were placed on ice in a cooler and moved to storage at 4 °C may be different. within 24 h. In this study, we characterized the interactions between Within 48 h of collection, coarse roots, including EM roots, were A. petiolata and EM fungi through experiments in the field, removed from each core and EM fungal root tips were separated glasshouse and laboratory. In the field, we measured the from the coarse roots using a dissecting scope. Both coarse roots abundance of EM fungal root tips in three forests in plots with and EM root tips were dried for 36 h in a drying oven and were weighed to obtain total dry weight root biomass and total dry and without A. petiolata. We predicted that plots invaded by weight EM root biomass. Values for coarse root biomass per core, A. petiolata would have a lower abundance of EM fungal EM root tip biomass per core and standardized root tip biomass per root tips. We also recorded the spatial extent of the effect of core (EM root tip biomass/mg total root tip biomass) of the two A. petiolata on EM fungi. Because the putative allelochemicals cores from each plot were averaged to generate a mean value for of A. petiolata are highly volatile (Vaughn & Berhow 1999), each plot. we predicted that the inhibitory effects of A. petiolata on EM Two-way fixed factor anovas were used to determine the effects fungi extend outside of A. petiolata patches. In a glasshouse of site and presence/absence of A. petiolata on (i) coarse root biomass, experiment, we assessed the effect of the experimental (ii) EM root tip biomass and (iii) standardized root tip biomass. To invasion of A. petiolata and a native weedy plant species improve normality, standardized root tip biomass was log(x + 1) Impatiens capensis on growth and EM colonization of Pinus transformed prior to analysis. Post hoc comparisons were done strobus (white pine) seedlings. We predicted that A. petiolata using Tukey HSD tests. would reduce the growth and EM colonization of seedlings and would have a greater effect than the native plant species.
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