Biol Invasions (2009) 11:663–671 DOI 10.1007/s10530-008-9281-7
ORIGINAL PAPER
Removal of invasive shrubs reduces exotic earthworm populations Michael D. Madritch Æ Richard L. Lindroth
Received: 31 October 2007 / Accepted: 5 May 2008 / Published online: 13 May 2008 ! Springer Science+Business Media B.V. 2008
Abstract Invasive species are a leading threat to native ecosystems, and research regarding their effective control is at the forefront of applied ecology. Exotic facilitation has been credited with advancing the success of several aggressive invasive species. Here, we suggest using the knowledge of exotic facilitations to control invasive earthworm populations. In northern hardwood forests, the invasive shrubs Rhamnus cathartica (buckthorn) and Lonicera x bella (honeysuckle) produce high quality leaf litter, and their abundance is positively correlated with exotic earthworms, which increase nutrient cycling rates. We performed an invasive plant removal experiment in two northern hardwood forest stands, one dominated by buckthorn and the other by honeysuckle. Removal of invasive shrubs reduced exotic earthworm populations by roughly 50% for the following 3 years. By targeting invasive species that are part of positive feedback loops, land managers can multiply the positive effects of invasive species removal. Keywords European earthworms ! Invasive species ! Invasion meltdown
M. D. Madritch (&) ! R. L. Lindroth Department of Entomology, University of Wisconsin, 237 Russell Labs, 1630 Linden Drive, Madison, WI 53706-1598, USA e-mail:
[email protected]
Introduction Invasive species are a leading environmental threat; they are responsible for roughly $120 billion damages annually in the United States and for nearly half of all threatened or endangered species declines (Pimentel et al. 2005). As a primary threat to global biodiversity, second only to habitat destruction (Wilcove et al. 1998), they have received increased attention in both the public and scientific communities. Nevertheless, control of invasive species remains a disheartening task for many land managers. Here we suggest that the application of ecological principles to invasive species management may aid in their effective control. For instance, mutual facilitation among exotic species may lead to ‘‘invasion meltdowns,’’ where invasive species facilitate each other resulting in increased invasion rates and replacement of the native community (Simberloff and Von Holle 1999; Simberloff 2006). Eventually invasion meltdowns have the potential to alter basic ecosystem functions, such as nutrient cycling, that influence all biota within the community. We propose that targeting plant species that facilitate invasion meltdowns may be an effective management technique, especially for invasive species that are not susceptible to physical removal. We focus on two invasive plant species, Rhamnus cartharica (common buckthorn) and Lonicera x bella (Bell’s honeysuckle) and a suite of invasive earthworms that have invaded forests in southern
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Wisconsin, USA. Common buckthorn is a fast-growing, bird-dispersed species, native to Europe (Godwin 1943) and introduced to North America in the 1800s as an ornamental (Possessky et al. 2000). It has since become naturalized throughout much of the northern half of North America. It is the dominant species in many forests in the upper midwest and northeastern United States, posing a serious threat to native biodiversity (Catling 1997; Knight et al. 2007). Buckthorn can create thick, closed canopies that shade out other species, thereby reducing native tree recruitment by more than 90% (Fagan and Peart 2004). The invasive honeysuckle hybrid complex, L. x bella, was also initially introduced to North America as an ornamental and is a very aggressive shrub commonly found in abandoned fields, forest edges, roadsides, and other open upland habitat. Lonicera spp. typically reduce native plant recruitment and biodiversity via competition, especially for light (Hutchinson and Vankat 1997; Gould and Gorchov 2000; Collier et al. 2002), and some honeysuckle species contain allelopathic compounds (Dorning and Cipollini 2006). Together, invasive buckthorn and honeysuckle dominate many disturbed and urban forests throughout southern Wisconsin, USA, and are commonly lumped together and referred to as ‘‘bucksuckle.’’ Earthworms native to the Great Lakes region were most likely extirpated by the Wisconsin glaciation during the Pleistocene epoch, 12,000 y.b.p. (Gates 1970; Callaham et al. 2004). Native earthworm recruitment from south of the permafrost line has not recolonized the region (James 2004). Earthworms that currently inhabit the region are non-native European species brought by early settlers via ballast and plant materials (Reynolds 1977; Gates 1982; James 2004). Of these, the most common exotics are Lumbricadae species that have significant detrimental effects on northern forests formerly devoid of earthworms (McLean and Parkinson 1997; Hale et al. 2005a; Bohlen et al. 2004a, b). The most striking ecosystem-level effect of invasive earthworms is the obliteration of soil horizonation and the elimination of the leaf litter layer (Hale et al. 2005a, b). While the specific ecological consequences vary by species, in general, invasive earthworms increase soil bulk density (McLean and Parkinson 1997; Bohlen et al. 2004a, b) and nutrient cycling rates in forested ecosystems, leading to reductions in soil carbon and nitrogen (Hendrix and Bohlen 2002; Hale et al.
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2005a). Lumbricus species have been linked to declines in native plant diversity as well as native soil micro- and mesofauna in northern hardwood forests (Frelich et al. 2006; Migge-Kleian et al. 2006; Holdsworth et al. 2007). As ecosystem engineers, earthworms have the capacity to alter basic ecosystem functioning, thereby exerting long-term impacts on plant and animal communities. Most control efforts focus on preventing the further spread of invasive earthworms (Callaham et al. 2006). Heneghan et al. (2007) report a positive correlation between buckthorn and invasive earthworm populations along a natural buckthorn gradient in northeastern Illionois, USA. They suggest that invasive buckthorn and earthworm species are part of a ‘‘modest invasional meltdown.’’ Similar positive relationships between invasive shrubs and earthworms have been observed in temperate (Kourtev et al. 1998) and tropical (Aplet 1990) ecosystems. Fast-growing shrubs with high quality leaf litter are likely to increase earthworm populations. Correspondingly, large earthworm populations are likely to favor fast-growing invasive shrubs by increasing nutrient cycling rates and availability. Here we report the results of a buckthorn/honeysuckle removal experiment to test the direct effect of invasive shrubs on invasive earthworm populations. If strong exotic facilitation does exist, then controlling aboveground invasive shrubs may be an effective management tool to reduce populations of ecosystem-altering, invasive earthworms.
Methods Our field sites were located at the University of Wisconsin Arboretum in Madison, WI, USA. We chose two mixed hardwood stands dominated by red oak (Quercus rubra) overstories: one with a buckthorn understory and one with a honeysuckle understory. Within each stand, we randomly chose ten 10 m2 plots. All standing aboveground invasive biomass was removed from five of the ten plots before leaf senescence in September 2003, and again after shoot emergence in the late spring of 2004, 2005, and 2006. Biomass was physically removed by cutting as close to the ground as possible. Roots were left intact, while aboveground biomass was weighed and removed from the site. We did not apply
Removal of invasive shrubs reduces exotic earthworm populations
herbicide after biomass removal, as recommended for bucksuckle control (Pergams and Norton 2006), because doing so would have confounded the removal treatments with herbicide application treatments. We monitored aboveground recruitment by woody species throughout the experiment after busksuckle removal. Hereafter, plots where biomass was removed are referred to as ‘‘removal’’ and plots where no biomass was removed are referred to as ‘‘control.’’ We established a litter decomposition experiment using freshly senesced leaf litter from 2003 to compare native and invasive litter decomposition rates. We collected freshly senesced litter from four sources: buckthorn, oak in the buckthorn plots, honeysuckle, and oak in the honeysuckle plots. From each source we collected three batches of leaf litter that were kept separate and air-dried. Two gram portions were then placed into 15 9 15 cm litterbags that had 0.5 cm2 mesh size to allow earthworm access. Each ‘‘removal’’ and ‘‘control’’ plot for each forest stand received 12 bags in April 2004. Litterbags were collected after 76 and 170 days (N = 2 buckthorn/honeysuckle stands 9 2 remove/control 9 5 plots 9 2 invasive/ oak litter types 9 3 litter batches 9 2 collection dates = 240 bags). A subsample of initial litter was taken from each batch and ground in a ball mill for analysis of total carbon (C) and nitrogen (N) with a Carlo Erba CNS analyzer. After each collection, litterbags were freeze-dried and weighed. In early July 2004 and November 2004 (after leaf senescence) we estimated earthworm abundance in each of the 20 plots using aqueous mustard extractions (Lawrence and Bowers 2002). A galvanized steel cylinder with a cross sectional area of 0.19 m2 was driven 5 cm into the soil. We then applied 2 l of a 9 g/l yellow mustard solution, waited 5 min, then applied another 2 l of mustard solution, and waited another 5 min. Earthworms that emerged during the mustard application were counted, collected, and freeze-dried for biomass measurements. We re-sampled 2 years later in July 2006, and attempted to sample again in November 2006 after leaf senescence, but the ground temperatures were too cold to effectively extract worms. At each earthworm collection date, we measured soil respiration to estimate general microbial activity, using a portable infra-red gas analyzer (PP Systems). We also measured temperature and moisture in the top 10 cm of soil.
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To further characterize the soil microbial community, we also collected three soil cores (2 cm diameter, 10 cm deep) from each plot (July 2004) for soil enzyme analysis. The three cores from each plot were mixed together and passed through a 2 mm sieve to provide one soil sample per plot. We measured the activity of six extracellular enzymes: cellobiohydrolase and b-glucosidase (involved with the degradation of cellulose), leucine aminopeptidase (involved with the degradation of proteins), phenol oxidase and peroxidase (involved with the degradation of aromatic compounds), and urease (degrades urea). Enzyme assays were based on the methods of Saya-Cork et al. (2002) and are described in detail by Madritch et al. (2007). Two grams of equivalent dry mass soil were homogenized in 15 ml of 50 mM acetate buffer. Four hundred microlitre of this soil extract were then added to 2 ml microcentrifuge tubes in duplicate for each of the six enzyme assays as well as a set for sample blanks. One hundred microlitre of 5 mM 4-pNP-b-D-cellobioside were used as cellobiohydrolase substrate, 100 ll of 40 mM pNP-b-glucopyranoside were used as b-glucosidase substrate, and 100 ll of 5 mM leucine p-nitroanilide were used as leucine aminopeptidase substrate. Soil extracts and substrates were allowed to react for 2 h at 29"C, then centrifuged at 3,000 rpm for 10 min to separate soil particles. Supernatant samples were removed and aliquoted in triplicate into 96-well microplates. After receiving 40 ll of 1.5 M NaOH, plates were read at 410 nm with a spectrophotometer. A p-nitrophenol standard curve was used for cellobiohydrolase, b-glucosidase, and leucine aminopeptidase. Phenol oxidase and peroxides activities were estimated in duplicate using 400 ll of soil extract and 100 ml of 20 mM L-DOPA with and without 40 ml of 0.3% H2O2. Soil extracts and substrates were allowed to react for 3 h at 29"C before centrifuging as above. We used a purified horseradish peroxidase standard curve as a reference and read absorbance at 460 nm. Urease was measured in duplicate by analyzing soil extract ammonium concentration before and after a 2 h incubation of 400 ll soil extract with 40 ml of 400 mM urea. Ammonium concentrations were determined colorimetrically using assays based on the indophenol blue method modified by Mulvaney (1996) using sodium dichloroisocyanurate as a hypochlorite source. All activities were converted to lM substrate/h/g soil before statistical analysis.
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All data were normalized, as necessary, prior to statistical analysis. Two-way repeated measures ANOVAs were used to test the independent and interactive effects of forest stand and removal treatments on earthworm populations and soil respiration data over time (SAS Jump v. 7). As we did not have replicated buckthorn- and honeysuckle-dominated stands, we could not separate the effects of ‘‘forest stand’’ from that of ‘‘invasive plant species’’. Thus, although we describe the two different stands as ‘‘buckthorn’’ and ‘‘honeysuckle,’’ we cannot attribute differences between the stands to differences in the predominant invasive species per se. We employed simple two-way ANOVAs to describe treatment effects on the amount of leaf litter remaining, earthworm biomass, and soil extracellular enzyme activity.
Results Both buckthorn and honeysuckle produced high quality leaf litter that decomposed much faster than did litter from the oak overstory in both forest stands (Fig. 1). Oak litter quality varied according to the
forest stand from which it was collected. Oak litter from the honeysuckle stand had a higher C:N ratio than did the oak litter collected from the buckthorn stand (C:N = 114.6 ± 3.9 and 91.0 ± 15.3, respectively). The C:N ratio of honeysuckle was twice that of buckthorn litter (C:N = 30.6 ± 0.3 and 15.5 ± 0.5, respectively), but both were much lower than that of either collection of oak litter. Oak litter decomposed slightly slower in removal plots than in control plots, however this trend was not significant in either forest stand. Removal treatments prevented high quality litter from entering the detrital pathway, influencing soil fauna for the following two and a half years. Earthworm abundance beneath plots where invasive shrubs had been removed declined by 63% for the buckthorn stand and 38% for the honeysuckle stand by the following summer, and remained depressed throughout the next 2 years (Table 1, Fig. 2). Earthworm abundance under the buckthorn removal treatments increased over time, but remained significantly lower than in control plots throughout the study period. Earthworm biomass also declined in 2004 with invasive shrub removal, especially in the buckthorn plots (Table 2, Fig. 3). However, declines in earthworm biomass were not as large as declines in
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Litter mass remaining (%)
70 60 50 40 30 20 10 0 Buck Control
Buck Removed
Oak Control
Oak Removed
Buckthorn
Fig. 1 Mass remaining after 170 days of decomposition in litterbags with 0.5 cm2 mesh. Oak litter decomposed slower than either buckthorn or honeysuckle litter (F2,119 = 384.0, P \ 0.001), oak litter from the honeysuckle stand decomposed slower than did oak litter collected from the buckthorn stand
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Honey Control
Honey Removed
Oak Control
Oak Removed
Honeysuckle
(F1,59 = 10.66, P = 0.002), and honeysuckle litter decomposed slower than did buckthorn litter (F1,59 = 8.79, P = 0.004). Each litter type was placed in control and removal plots, however there was no significant effect of the removal treatment on mass loss
Removal of invasive shrubs reduces exotic earthworm populations Table 1 Repeated measures ANOVA results for earthworm population and soil respiration meausurements
P [ 0.1 indicated as n.s.
Earthworm population F1,16 = 5.18, P = 0.037
F1,8 = 8.54, P = 0.019
Invasive removal
F1,16 = 18.29, P \ 0.001
n.s.
Stand 9 invasive removal
n.s.
n.s.
Time
n.s.
F3,6 = 72.79, P \ 0.001
Stand 9 time
F2,15 = 2.85, P = 0.089
F3,6 = 5.4, P = 0.038
Invasive removal 9 time
n.s.
F3,6 = 5.06, P = 0.044
Stand 9 invasive 9 time
n.s.
n.s.
16
Control
E a r t h wo r m m a s s ( g / m 2 )
Removed
120 100 80 60 40
14 12 10
20 0
Soil respiration
Forest stand
140
Earthworm abundance (no ./ m2)
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8 6 4 2 0
July 2004
Nov 2004
Buckthorn
July 2006
July 2004
Nov 2004
Honeysuckle
Fig. 2 Earthworm abundance beneath control and removal plots for both buckthorn and honeysuckle. Earthworm populations declined after invasive shrubs were removed. Bars represent average earthworm populations (N = 5 plots per treatment) with error bars representing ±1 SE. See Table 1 for repeated measures ANOVA results
earthworm abundance, in part because the average size of individual earthworms increased after bucksuckle removal (Control = 0.095 ± 0.013 g/worm, Removal = 0.140 ± 0.027 g/worm; Table 2), indicating that smaller earthworms were preferentially reduced. We expected temperature and moisture to vary between control and removal plots, but found no differences, most likely because all plots were beneath a closed canopy of mature oaks. We used soil respiration as a general measure of microbial activity. Soil respiration decreased in buckthorn and honeysuckle removal plots during November Table 2 ANOVA results for earthworm biomass
P [ 0.1 indicated as n.s.
Buckthorn Control
July 2006
Buckthorn Removed
Honeysuckle Honeysuckle Control Removed
Fig. 3 Earthworm biomass beneath control and removal plots for both buckthorn and honeysuckle forest stands during 2004. Bars represent average earthworm population densities (N = 5 plots per treatment) with error bars representing ±1 SE. See Table 2 for ANOVA results
measurements of both 2004 and 2006, but did not differ during the July measurements of either year (Table 1, Fig. 4). The November 2006 collection/measurement date was significantly colder than the November 2004 collection (3.4" and 13.2"C, respectively), accounting for the decrease in respiration, and the lack of earthworm data for November 2006. Decreased microbial activity in July 2004 beneath removal plots was also confirmed by reductions in b-glucosidase activities (control: 2807 ± 314 lmol/h/g, removal: 1768 ± 188 lmol/h/g, F3,19 = 5.81, P = 0.005). No other enzyme activity responded to the removal treatments. Due to the overall lack of treatment effects on microbial enzyme activity in 2004, we did not Biomass per m2
Biomass per individual
Forest stand
F1,19 = 17.77, P \ 0.001
F1,19 = 5.18, P \ 0.001
Invasive removal
F1,19 = 5.26, P = 0.036
F1,19 = 4.85, P = 0.043
Stand 9 invasive removal
n.s.
n.s.
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Soil respiration (g C/m2/hr)
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M. D. Madritch, R. L. Lindroth 1.2 1
Control Removed
0.8 0.6 0.4 0.2 0
July 2004
Nov 2004
July 2006
Buckthorn
Nov 2006
July 2004
Nov 2004
July 2006
Nov 2006
Honeysuckle
Fig. 4 Soil respiration beneath control and removal plots for both buckthorn and honeysuckle. Respiration rates declined after invasive shrubs were removed for November, but not July, measurements (invasive removal F1,15 = 5.30, P = 0.037 for November 2004 and F1,19 = 7.98, P = 0.011 for November 2006). Bars represent average soil respiration (N = 5 plots per treatment) with error bars representing ±1 SE. See Table 1 for repeated measures ANOVA results
measure enzyme activity in 2006, and instead relied on soil respiration data to estimate microbial activity. Both buckthorn and honeysuckle contain allelopathic chemicals (Dorning and Cipollini 2006; Knight et al. 2007) that inhibit plant growth. We observed no recruitment by woody native species in any of the removal plots in 2004 or 2006.
Discussion Removal of invasive shrubs significantly reduced the abundance and biomass of invasive earthworms, most likely by reducing inputs of high quality leaf litter. European earthworms generally favor high quality litter with low C:N values (Hendriksen 1990), and both buckthorn and honeysuckle produce very high quality litter compared with the native oak overstory. Reductions in earthworm biomass were not as pronounced as reductions in earthworm abundance because bucksuckle removal preferentially reduced small earthworm abundance, possibly due to competitive release and/or shifts in the earthworm community composition. While others have observed correlations between invasive shrubs and earthworm abundance (Aplet 1990; Kourtev et al. 1998; Heneghan et al. 2007), we show here that removing invasive shrubs has a direct, negative effect on earthworm abundance. Eliminating invasive litter inputs into the detrital pathway also influenced microbial activity. Soil
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microbial activity declined following the removal of both buckthorn and honeysuckle shrubs. Although earthworms are known to influence microbial activity directly (Groffman et al. 2004; Migge-Kleian et al. 2006), the reductions in microbial activity shown here are most likely due to the removal of high quality leaf litter inputs as demonstrated by soil respiration data. While soil respiration tended to be lower in removal plots during July of both 2004 and 2006, it was significantly lower only in November, after leaf senescence, in each year. Invasive plant species typically produce high quality leaf litter (Ehrenfeld 2003) and this likely leads to significant changes in important belowground processes such as nutrient cycling (Allison and Vitousek 2004). Invasive plants and earthworms can both have long-term effects on forest communities and nutrient cycling, particularly in sites with a long history of invasion. Plant-induced changes to the soil are especially long-lived (Kardol et al. 2007) and microbial communities have relatively long legacies (Bartelt-Ryser et al. 2005). For instance, native tree species commonly fail to recolonize years after honeysuckle removal (Luken et al. 1997; Collier et al. 2002), in part due to allelopathetic effects of honeysuckle leaf litter (Dorning and Cipollini 2006). Likewise, we observed no recruitment by any native woody species in any of our buckthorn or honeysuckle removal plots. Earthworms are archetypal ecosystem engineers, and recent studies of earthworm invasions into northern forests demonstrate significant changes in soil nutrient availability, soil structure, soil biotic communities, and aboveground plant communities (Bohlen et al. 2004a, b; Groffman et al. 2004; Frelich et al. 2006). Many of the negative effects of earthworm invasion result from the destruction of the litter layer (Hale et al. 2005a). However, litter decomposition did not differ significantly between removal and control plots, and after 2 years we saw no recovery of the native litter layer in the removal plots. Although we monitored removal plots for 2 years, this time period was likely not long enough to realize the full ecosystem responses of invasive plant removal or reductions in earthworm abundance. Even if earthworms could be entirely removed from a site, the organic layer would likely take many years to re-establish. While earthworms were not eliminated from these stands, their abundance was severely reduced (approximately 50%).
Removal of invasive shrubs reduces exotic earthworm populations
Their presence will still have large influences on soil structure and nutrient availability, but their negative effects will likely diminish with population size. We expected that removing the invasive understory might introduce confounding temperature and moisture effects. However, we found no difference in soil moisture or temperature between control and removal plots in either the buckthorn or the honeysuckle stand, most likely because of an intact oak canopy. Yet, it remains possible that our treatment effects were the effects of removing the understory, regardless of whether the understory was invasive. We maintain that a bucksuckle understory is significantly different from a native northern hardwood understory composed primarily of juvenile hardwoods. Although many species display significant ontogenetic shifts in leaf litter chemistry (Boege and Marquis 2005), the difference in litter chemistry between oak and buckthorn or oak and honeysuckle is much larger. Furthermore, forests invaded by bucksuckle have more understory biomass than do native understories; the honeysuckle biomass of severely invaded forests can approach the total productivity of native forests (Luken 1988). Given the difference in the quality and quantity of understory leaf litter between invasive and native northern hardwood forest understories, the treatment effects shown here are most likely specific to fast-growing shrubs. Current invasive earthworm management efforts focus on controlling the spread of earthworms via soil and bait movement (Callaham et al. 2006). Controlling the spread is the most promising management technique, as earthworms move only 7.5 m annually on their own accord (Hale et al. 2005a). Callaham et al. (2006) suggested that controlling the spread of invasive plant species may be an effective management technique to limit the spread of invasive earthworms, and we show here that removing the invasive bucksuckle shrub complex is an effective method to reduce earthworm populations that have already become established. While it is entirely possible that invasive earthworms primed the soil for invasive shrubs to become dominant by increasing nutrient cycling rates and removing the litter layer (Heneghan et al. 2007; Knight et al. 2007), removing the invasive shrubs breaks the positive feedback cycle that contributes to an invasion meltdown. Of concern in our study is that earthworm abundance declined more than did earthworm biomass. The persistent
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presence of earthworm biomass in removal plots likely prevented the buildup of the native litter layer as noted above. Ecosystem perturbations often persist long after invasive species removal, and it is unlikely that native forests will recover quickly following bucksuckle removal. However, reducing the abundance of invasive species is often an important management goal, despite the fact that the ecosystem consequences of invasive species may not decline linearly with population abundance. Targeting buckthorn for removal may have additional effects beyond exotic earthworm population control. Buckthorn also serves as the overwintering host of the invasive Asian soybean aphid (Aphis glycines; Ragsdale et al. 2004). In northern hardwood forests, targeting buckthorn will likely reduce: (1) the direct negative effects of buckthorn on forest communities, (2) the indirect effects achieved through exotic earthworm facilitation, and (3) the negative effects on agriculture by removing the winter host of an invasive pest. Given the limited resources available for invasive species control, land managers should focus on removing those species that are most likely to have extended ecosystem and community level effects. One effective strategy may be to identify and target key invasive species that facilitate the invasion and success of other exotic species. Acknowledgements Funding was provided by NSF DEB0344019 to RLL and MDM. We thank the UW Arboretum for site use permission, P. Zedler for sparking our interest in the topic, and K. Lawson for field assistance.
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