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Applied Soil Ecology
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he impact of garlic mustard on sandy forest soils
herri J. Morris ∗, Dustin L. Herrmann1, Jessica McClain, Jaclyn Anderson, Kelly D. McConnaughayepartment of Biology, Bradley University, 1501 W. Bradley Avenue, Peoria, IL 61625, United States
r t i c l e i n f o
rticle history:eceived 31 August 2011eceived in revised form 25 January 2012ccepted 4 February 2012
ey words:arlic mustardlliaria petiolata
nvasive specieslack locust
a b s t r a c t
Garlic mustard (Alliaria petiolata), an exotic biennial herb invasive to North American forests, has poten-tial to affect resource availability in invaded soils. Garlic mustard produces a suite of toxic chemicals thatimpact diversity both above and belowground and thus likely alter ecosystem processes. To examinethe effects of garlic mustard on soil biota and ecosystem processes, we sampled soil from invaded anduninvaded stands at a pine plantation on sandy soils in central Illinois. Several of the pine stands werealso planted with the N2-fixing tree black locust (Robinia pseudoacacia). Results indicate that pine soilsunderlying garlic mustard have higher pH, and exhibit higher rates of N mineralization, relative nitrifi-cation and soil respiration compared to soils without garlic mustard. Nitrogen turnover on pine invadedstands is more similar to pine soils with the black locust trees present than to uninvaded pine stands
mineralization mineralization
without black locust. Garlic mustard cover was much greater in stands with black locust trees planted,suggesting that garlic mustard may be attracted to high N sites. Catabolic response profiles, which providea measure of soil microbial function, indicated a shift in substrate use for one of the substrates tested inthe presence of garlic mustard. While many of the soil characteristics measured did not differ betweeninvaded and uninvaded stands, the differences with regard to N turnover were striking and will likelyhave long term effects on soil nutrient status, with potential to feedback to forest health.
. Introduction
Invasive species are of great ecological and economic concernMoser et al., 2009). Invasive species threaten native communi-ies by altering community structure and ecosystem function in
manner that can have long term impacts on species diversitynd net primary productivity (Mooney and Drake, 1986; Gordon,998; Gilliam, 2007). The mechanisms by which species become
nvasive and alter ecosystem characteristics are related to the phys-ological and structural characteristics of the invading species andre thus species specific (Ehrenfeld, 2003). Eradication of inva-ive species requires understanding of the mechanism by whichnvaders gain advantage in ecosystems. Furthermore, knowledgef the impacts of these species on ecosystem structure and func-ion may be required to restore systems once the invader has beenemoved (D’Antonio and Meyerson, 2002).
Garlic mustard (Alliaria petiolata, Brassicaceae), is a non-
ycorrhizal, shade-tolerant herb that invades both disturbed and
ndisturbed forests in its introduced range (Nuzzo, 1993). Intro-uced to North America from Europe in the mid 1800s, garlic
mustard had spread to 4 providences in Canada and 34 states inthe US by 2000 (Welk et al., 2002). The models developed by Welket al. (2002) suggested that garlic mustard had not yet spread toall likely habitats in North America. Garlic mustard proliferates inmesic deciduous forests with partial to full sun, but also inhab-its upland areas with well-drained sandy soils (Cavers et al., 1979).Once established, garlic mustard is highly persistent in forests, evenremaining through succession and forest transitions (McCarthy,1997; Meekins and McCarthy, 2001).
Many studies on garlic mustard document belowgroundimpacts following garlic mustard invasion. Studies have reporteddifferences in soil microbial community composition and innutrient turnover in areas associated with garlic mustard whencompared to uninvaded areas (Stinson et al., 2006; Rodgers et al.,2008; Wolfe et al., 2008; Anderson et al., 2010; Lankau, 2010). Aswith many invasive species these changes to soil microbial popula-tions may persist even following removal of garlic mustard from theaffected areas, complicating forest restoration efforts (D’Antonioand Meyerson, 2002).
Garlic mustard, like other plants in the mustard family, hassecondary chemicals, primarily glucosinolates, which are toxicto aerobic organisms, including potential herbivores and soil
microbes. The cyanide-like moiety that results from glucosino-late degradation in damaged garlic mustard tissues (Cipollini andGruner, 2007) is likely responsible for its anti-herbivore activ-ity and potential impacts on soils. In its introduced range, the
lucosinolates in garlic mustard have been held responsible forlant-fungal mutualism disruption and depression of seed ger-ination in native species as demonstrated in laboratory studies
McCarthy, 1997). As a result of microbial transformations, glucosi-olates appear to have limited persistence in soils, which may limitheir direct allelopathic effects per se (Barto and Cipollini, 2009).owever, exposure may result in changes to plant and microbialommunity structure in a manner that alters nutrient availabilitynd impacts other ecological relationships such as competition anderbivory. In terms of competitive relationships, garlic mustardas been associated with altered nutrient dynamics in its inva-ive range which may give it advantage over native species. It haseen associated with increases in N turnover and key soil-derivedlant nutrients, Ca, P, and Mg (Rodgers et al., 2008). Many reportsave documented negative effects of garlic mustard invasion onative plant species (McCarthy, 1997; Nuzzo, 1999). These impactsan occur directly as a consequence of suppressed germination ofatives or as mediated by impacts on nutrient uptake. In particu-
ar, garlic mustard has been shown to suppress arbuscular (Robertsnd Anderson, 2001; Stinson et al., 2006) and ectomycorrhizal fungiWolfe et al., 2008).
The concerted effects of garlic mustard invasion across soilutrient classes under the same climatic regime have not been welltudied. To uncover this dynamic, we examined multiple proposedffects of garlic mustard in a simple natural system at two fertil-ty levels. This design is unique from those previously field-testedecause it holds all factors constant except those affecting soil fer-ility. Garlic mustard has become widely established on a sandyine plantation with a low carbon and nitrogen soil matrix in cen-ral Illinois. Some stands within the pine plantation are interspersedith the N2-fixing tree black locust (Robinia pseudoacacia L.) whileominated by pine trees. The presence of black locust has presum-bly created greater soil fertility in some stands. Black locust hasreviously been demonstrated to enhance soil N pools and net Nineralization rates in a nutrient poor pine–oak forest (Rice et al.,
004). In general, the study forest has low plant diversity and covern the understory. These factors may lead to clear signals associated
ith garlic mustard establishment and persistence.We hypothesize that garlic mustard invaded soils will have
ifferent nutrient conditions and soil microbial activity than unin-aded soils. Specifically, we predict that garlic mustard infestationsill be associated with increased carbon and nitrogen turnover,
egardless of soil nutrient levels. However, the degree to which dif-erences in soil processes and properties are associated with garlic
ustard may vary across a fertility gradient.
. Methods
.1. Study location
The study was located at Sand Ridge State Forest (SRSF), nearanito, Illinois (approximately 3000 ha, 40.41◦N latitude, 89.87◦W
ongitude), a glacial floodplain consisting of alluvial deposits fromhe late Woodfordian era. SRSF was converted from sand prairiend agriculture to pine plantations in the 1930s. Some areas werentermixed with black locust at the time of planting to increase siteertility. For this study, three replicate stands of three stand typesere sampled: pine (pine), pine with garlic mustard (pineGM), andine with garlic mustard and black locust (pineGMBL). No standsould be found with black locust that did not also have garlic mus-ard. The pines stands studied contained monospecific stands of
ither red pine (Pinus resinosa) or eastern white pine (Pinus strobes).tands were separated by approximately 1 km on average. All soilsere of the Bloomfield–Plainfield association and had a loamy sand
exture.
cology 60 (2012) 23– 28
2.2. Plant survey
To determine if garlic mustard or herbaceous cover varied bystand type and fertility level (i.e., pine, pineGM, pineGMBL), under-story plant surveys were conducted in July 2007 in the areas wheresampling plots were established. One 25 m transect was estab-lished per replicate stand (=3 replicate transects per stand type).Random ¼ m2 plots were sampled at every meter along the tran-sect at 0–10 m distance perpendicular to the transect. In each plotthe % cover by bare ground, garlic mustard, other non garlic mus-tard weeds, and native herbaceous plants was recorded as coverageclass (Class 1: 0–1% cover, 2: 2–5, 3: 6–25, 4: 26–50, 5: 51–75, 6:76–95, 7: 96–100%) and percent cover per plot was quantified asthe mid-point cover for its respective class. Percent cover and rel-ative cover (cover as a percent of total cover) as transect meanswere analyzed using a one-way ANOVA (SAS 9.1; Proc GLM) on datatransformed using the arcsin transformation to meet assumptionsof normality, with stand type as the effect.
2.3. Soil properties
Soil samples were collected to assess basic properties and micro-bial activity in garlic mustard invaded vs. non-garlic mustard soil.Within each stand replicate, three 1-m2 plots were randomly estab-lished with at least 1 m distance from the nearest tree. In July2007, eight composited mineral soil samples from 0 to 10 cm depthwere taken with a 2.3 cm diameter soil corer for each plot. Plots instands with garlic mustard populations were established on cur-rently invaded soils with densities of living first and second yearplants not atypical of the stand. Samples were brought to the labo-ratory, sieved to 4 mm and visible organic (i.e., roots) and inorganic(i.e., rocks) matter was removed. Subsamples were oven-dried at105 ◦C to determine moisture content. Soil pH was determined froma 2:1 slurry of 0.01 M CaCl2 and 15 g air-dried soil. Total soil car-bon and nitrogen was determined by sieving a subsample of soil to2 mm and grinding to pass a 180 �m sieve. Samples were analyzedon a 30 mg subsample on a CE Instruments Flash 1112 Series EA NCSoil Analyzer.
2.4. Microbial activity
To determine N mineralization potential, samples were incu-bated at 70% field capacity at 25 ◦C for 0, 30, 62 and 120 days.Inorganic N was extracted in 0.5 M K2SO4 and analyzed for NO3
−
and NH4+ on a Lachat Instruments QuikChem® FIA+ 8000 series
(Robertson et al., 1999). N mineralization rates were determinedas the amount of ammonium plus nitrate produced at the endof the incubation minus that present at the beginning. Relativenitrification represents the amount of nitrate produced during theincubation divided by the N mineralized during that same period(Robertson et al., 1999). Soil respiration was determined by incu-bating 60 g soil at 70% field capacity at 25 ◦C. Soil CO2 flux wasmeasured over a 126-day period using a Li-Cor CO2 analyzer ModelLI-6252 (Paul et al., 2001; Robertson et al., 1999). Basic soil proper-ties were analyzed using one-way ANOVAs with forest type as theeffect. Some data required transformation to meet the assumptionsof ANOVA, including reciprocal transformation of C:N ratios. Theresults from C and N mineralization were analyzed using a repeatedmeasures ANOVA (ANOVAR; DataDesk) with the C mineralizationdata log transformed prior to analysis. The relationship between
relative nitrification and pH across treatments was evaluated usingpH as a covariate (ANCOVAR; DataDesk). All reported differencesare significant at p < 0.05 except where noted with n = 9 for all soilcharacteristics.
Soil Ecology 60 (2012) 23– 28 25
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Fig. 1. Percent cover of garlic mustard and total herbaceous cover (A) and relative
S.J. Morris et al. / Applied
.5. Functional potential of soil microbial community
A catabolic response profile (CRP) was performed in August 2007n freshly collected soils from the same locations. The technique aseveloped by Degens and Harris (1997), altered by Frey et al. (2004),nd further modified here provides a fingerprint of the microbialommunity’s functional potential by measuring responses (i.e., soilespiration) to 12 simple carbon substrates. Substrates included:wo carbohydrates (glucose and mannose), two amino acids (l-sparagine and l-histidine), and eight carboxylic acids (l-ascorbiccid, citric acid, �-ketobutyric acid, �-ketoglutaric acid, dl-maliccid, malonic acid, succinic acid and tartaric acid). The substratesere mixed in solution with diH2O at the following concentrations:
Garlic mustard and total herbaceous cover differed significantlycross stands, with cover greatest in the pineGMBL stands followedy the pineGM stands (Fig. 1A). Garlic mustard cover was greater,nd non weedy herbaceous cover was lower, relative to total herba-eous cover, in the pineGM stand compared to the uninvaded pinetands; however, there were no differences in the relative cover ofon garlic mustard weeds in any of the stands (Fig. 1B).
.2. Soil properties
There were significant differences in soil physical characteristicsmong the stand types studied. The pH was greatest in pineGM soils
nd lowest in pineGMBL; pine soils were intermediate betweenhe two (Table 1). Differences were significant at p < 0.05, exceptetween pine and pineGM soils which had a p-value of 0.06. Bulkensity was significantly greater under pine soils but did not differ
able 1roperties by stand type (GM = garlic mustard; BL = black locust) for soils from pinelantations at Sand Ridge State Forest, IL, reported as mean (±1 SE). Different lettersepresent significant differences at p ≤ 0.05 by row, except for pH between pine andineGM where p ≤ 0.06 and is noted with crosses (†). For all n = 9 except for pinend pineGMBL organic C, total N and C:N ratio where n = 8 and pine C:N ratio where
= 7.
Soil property Forest type
Pine PineGM PineGMBL
pH 5.20(0.10)a† 5.55(0.15)b† 4.74(0.14) c
Bulk density (g/cm3) 1.31(0.02)b 1.24(0.02)a 1.24(0.02)a
Organic C (mg/g soil) 8.38(0.93)a 8.10(0.65)a 11.30(1.27)b
Total N (mg/g soil) 0.42(0.07)a 0.50(0.04)a 0.85(0.09)b
C:N 18.65(0.96)a 16.61(0.99)a 13.75(0.63)b
cover of garlic mustard, other (non garlic mustard) weeds, and non weeds (B) in threestand types (pine, pineGM and pineGMBL) at Sand Ridge State Forest, IL, reportedas mean ± 1 SE (n = 3). Mean values differed significantly at p < 0.05.
between pineGM and pineGMBL soils. Soil organic C and total N(mg/g soil) were significantly greater in pineGMBL soils than inpine and pineGM soils, which did not differ (Table 1). Likewise, theC:N ratio held a similar relationship—lower in pineGMBL soils, butnot significantly different between pine and pineGM soils.
3.3. Microbial activity
There were differences in log cumulative C respired across timeand there was a time by stand type interaction. Cumulative Crespired per gram organic C was lowest in pineGMBL stands andhighest in the pineGM stands through day 65 (Fig. 2, p < 0.05 forall comparisons), thereafter pineGM soils differed from pine andpineGMBL soils which did not differ.
There were differences across time for total N mineralized(NO3–N + NH4–N) and a marginally significant difference for standtype (p ≤ 0.10). N mineralization rates were greater in PineGMBLsoil than the other stand types at day 30, but pine and pineGM didnot differ (Fig. 3). PineGMBL and pineGM soils had higher N min-eralization rates than pine soils at day 62, but did not differ fromeach other (Fig. 3). At day 120, cumulative N mineralization did notdiffer across stand types.
Relative nitrification differed significantly across time and there
was a significant time by stand type interaction. Relative nitrifica-tion was significantly greater in pineGM and pineGMBL soils thanin pine soils (Fig. 4) at day 30, however at day 62 relative nitrifi-cation was greater in pine soils than pineGM but neither differed
Fig. 2. Cumulative carbon respired in mg CO2–C/g organic C over a 126-day incu-bation by stand type (GM = garlic mustard; BL = black locust) for soils from pineplantations at Sand Ridge State Forest. Results are reported as mean ± 1 SE for alldays sampled (n = 9). Significant differences at p < 0.05 across all days for log trans-formed data. All treatments were significantly different from each other throughday 65. After day 65 pineGM differed from pine and pineGMBL which did not differ.
0
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Fig. 3. N mineralization rates as mg N/kg soil/day over a 120-day incubation bystand type (GM = garlic mustard; BL = black locust) for soils from pine plantationsfrom Sand Ridge State Forest, IL. Results are reported as mean ± 1 SE for days 30, 60aPa
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Fig. 5. The relationship between relative nitrification on day 30 and pH by standtype (GM = garlic mustard; BL = black locust) for soils from pine plantations at SandRidge State Forest, IL. The relationship was significant for pine and pineGM, and
nd 120 (n = 9). Treatments differed significantly at p < 0.10 and time at p < 0.05 withineGMBL differing from pine and PineGM at day 30, then pine differs from pineGMnd pineGMBL at day 60.
rom pineGMBL soils. The relationship of relative nitrification to pHas evaluated across stands (Fig. 5). Relative nitrification for pine
nd pineGM soils was strongly related to pH whereas there waso relationship between relative nitrification and pH on pineGMBL
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ig. 4. The proportion of mineralized N that is NO3− , or relative nitrification (i.e.,
O3−/NH4
+ + NO3−), on day 30 by stand type (GM = garlic mustard; BL = black locust)
or soils from pine plantations at Sand Ridge State Forest, IL. Results are reported asean ± 1 SE (n = 9). There were significant differences across time and forest typeith pine differing from pineGMBL and pineGM at time 30 only.
their regression equations were not significantly different. (ANCOVAR; p < 0.05). ThepineGMBL relationship was not significant.
soils. The linear regression lines for pine and pineGM were not dis-tinguishable statistically, and the non-significant pH vs. relativenitrification response for pineGMBL was not similar to either.
3.4. Functional potential of soil microbial community
Results of the variance analyses on the PCA components for theCRP data were all non-significant (data not reported). One-wayANOVAs by substrate identified differences in responses to individ-ual substrates for only the carboxylic acid, �-ketoglutaric acid. Thestandardized respiration response increased from pine at 3.9 ± 0.4(±1 SE), to pineGM, 5.1 ± 0.6, to pineGMBL, 6.3 ± 0.6.
4. Discussion
As hypothesized, garlic mustard invaded soils differed from soilswithout garlic mustard in several key parameters, however this wasnot the case for all soil or microbial characteristics measured. Plantcover data supports that the presence of garlic mustard on our plotswas greater in the pineGM and pineGMBL stands than the unin-vaded pine stands without differences in the relative cover of nongarlic mustard weeds providing a reasonable stand to test thesehypotheses. Specifically, we predicted that garlic mustard infes-tations would be associated with increased carbon and nitrogenturnover, regardless of soil nutrient levels. The data support thesepredictions. Specifically, C and N mineralization were significantlyhigher in GM invaded soils. In addition, the GM invaded soils exhib-ited significantly higher pH, and lower bulk density. These resultssuggest that garlic mustard either alters soil physical, chemical andmicrobiological properties, or is attracted to soils with differentproperties. In the case of pH, pineGM soils had higher soil pH thanpine, which is consistent with differences detected by Rodgers et al.(2008), the pineGM soils also had much higher pH than pineGMBLsoils. Rodgers et al. (2008) found garlic mustard populations corre-lated with increased pH and, in a lab experiment, demonstrated asignificant increase in pH caused by garlic mustard. Garlic mus-tard at SRSF did not have difficulty growing across a very widerange of pH values, suggesting that garlic mustard may indeed alterthis basic soil property. The black locust in contrast was associatedwith much lower pH values than for the invaded or uninvaded pinestands. Malcolm et al. (2008) found black locust stands on nutrient
poor sands in New York to have lower pH than the pine–oak com-munity on the same soil type and Rice et al. (2004) found evidencethat black locust increases weathering. Others have found N fix-ation and the consequent increase in nitrification associated with
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S.J. Morris et al. / Applied
ecreased soil pH (Van Miegroet and Cole, 1984; Paul and Clark,996).
PineGM soils were associated with increased C mineralizationhroughout the 126-day incubation. The early respiration data sug-ests differences in the labile pool associated with pine, pineGMnd pineGMBL soils (Paul et al., 2001; McLauchlan and Hobbie,004), with the black locust soils having the smallest labile poolnd the pineGM the largest. Increased C mineralization under gar-ic mustard is consistent with reports of increased N turnoverssociated with invasion of garlic mustard (Rodgers et al., 2008).ifferences in C mineralization rates have not yet translated intoeasurable differences in organic carbon pools. As garlic mustard
as only been in these stands for the last five years (personal obser-ation) it is not surprising, given the slow rate of change for soilarbon with land use change that changes in carbon have not yeteen detected (Paul et al., 2001). The relatively low C mineralizationates under black locust soils may be related either to decreasedicrobial activity under low pH or decreased decomposition as
escribed by Fog (1988) with N additions.The presence of garlic mustard was associated with increases
n N mineralization, specifically nitrate production, early duringhe incubations. PineGM soils had rates similar to the pineGMBLoils rather than the pine soils that had similar total N (Table 1;igures 3 and 4). Rodgers et al. (2008) found the same trend in
mineralization rates between invaded and non-invaded soilsithin sites for several regional forests of varying fertility and
anopy/soil structure. In our study, similar N mineralization ratesre found for different soil fertility levels, while having climate,ocation and parent material constant, on garlic mustard invadedoils. However, this does not account for the potential confound-ng factors associated with black locust presence. The greater N
ineralization potential on the black locust soils occurred with-ut an accompanying increase in soil respiration. This supportsither a larger, more efficient microbial community or a shift in theicrobial community diversity (e.g., increase in N fixing species
nd nitrifiers).In this study relative nitrification was related to pH. The rela-
ionship between pH and nitrification has been identified in aumber of other studies (Vitousek and Matson, 1985; Morris andoerner, 1998). On these soils, the relationship between pH andotal nitrification (data not shown) was weak, but the relationshipetween pH and relative nitrification was significant and positiveith the exception of soils underlying stands with black locustresent (Fig. 5) which suggests that the availability of ammoniumore tightly controls the production of nitrate in these stands
han pH. The presence of garlic mustard was associated with bothncreased N mineralization as well as an increase in pH, which couldogether be responsible for more efficient nitrate production frommmonium. However the lag between the first and second timeoints in the N incubation suggests that the nitrifying community
s present in pine soils, but possibly in lower numbers than in theineGM and pineGMBL soils. While it is possible that garlic mustard
s attracted to sites with high nitrification rates, it is also possiblehat the presence of garlic mustard enhances nitrifier populationsctively through exudate production, tissue production or otherechanism. In addition, increased soil pH following garlic mustard
nvasion could be a consequence of N nutrition in the microbialools. For example, one possible mechanism for the increase in pH
s an increased rate of NO3− uptake. Ehrenfeld et al. (2001) proposed
his mechanism for the forest invasion by Microstegium vimineumnd Berberis thumbergii. Uptake of NO3
− in acidic soils results in theoncurrent uptake of H+ and thereby increasing soil pH (Imas et al.,
997). Additionally, NO3
− reduction in plants produces OH− whichan be carboxylated and exuded by roots in the form of organicnions (Marschner, 1995; Touraine et al., 1990). Therefore, garlicustard may raise pH by rapid NO3
− uptake and through root
cology 60 (2012) 23– 28 27
exudate chemistry. Positive impacts on soil nitrification activityhave been demonstrated for other invasive species (Hawkes et al.,2005).
To test the functional differences in the soil microbial commu-nity in garlic mustard invaded vs. uninvaded soils, we measured soilrespiration responses to the addition of a series of simple carbonsubstrates. The results suggest that garlic mustard may not impactsoil microbial function holistically; rather, catabolic activity on oneor a few key compounds associated with garlic mustard specificchemistry may be critical to its establishment and proliferation.Only one substrate, �-ketoglutaric acid, was preferentially used bygarlic mustard soils. Toxicology research has demonstrated that �-ketoglutaric acid greatly increases, through antagonism, the LD50of cyanide on test animals (Moore et al., 1986). In invaded soils, if �-ketoglutaric acid acts to decrease the toxicity of cyanide, there maybe an increase in microbial activity as a result of suppression of thetoxin. PineGMBL soils had the greatest response to �-ketoglutaricacid, followed by pineGM soils. This high response to �-ketoglutaricacid has been demonstrated in the soils associated with an exoticAcacia tree (Remigi et al., 2008), similar to black locust evolution-arily, independent of garlic mustard presence. By extension, thepresence of black locust may cultivate portions of a soil microbialcommunity similar to those created by garlic mustard. In terms ofnitrogen transformations �-ketoglutarate is responsible for reduc-tive amination in both free-living (Benemann et al., 1971) andsymbiotic N-fixing bacteria (Bergersen, 1971) so, whenever NH4
+
is plentiful, such as whenever biological N fixation is occurring thiscarbon substrate would be in high demand.
Garlic mustard establishment and proliferation may be botha factor of its creation of soil conditions favorable to its successand facilitation by pre-existing soil environments. The relevance ofeither scenario may also be context dependent. There is certainlystrong evidence that garlic mustard is changing soil processes bydisrupting fungal mutualisms (Stinson et al., 2006; Wolfe et al.,2008) and increasing nutrient availability (Rodgers et al., 2008).However, its capacity to rapidly establish and, in some instances,become dense monocultures without these characteristics beinguniversal (Anderson et al., 1996) suggests that facilitation of inva-sion may be important. In this study, the presence of black locustmay have facilitated the dense coverage of garlic mustard in thesestands (Fig. 1). In an extensive search of SRSF there were no pinestands with black locust found that did not have garlic mustardpresent in high densities (personal observation). The long-termeffects of black locust on soil, primarily soil acidification and highNO3
− production, are analogous to the impacts of acid deposi-tion (Rice et al., 2004). If these conditions allow garlic mustard acompetitive advantage or are amenable to its establishment, thechronic deposition of nitric, and possibly sulfuric, acids on forestsoils in industrialized regions (e.g., eastern North America) mayfacilitate garlic mustard expansion. Interestingly, glucosinolates,the secondary compounds in garlic mustard putatively responsi-ble for herbivore deterrence and fungal suppression, require bothnitrogen and sulfur (Wallsgrove et al., 1998).
Overall, the impacts of garlic mustard on an invaded system arelikely context dependent. Pre-existing conditions may be favor-able to its colonization and the forest may not be significantlyaltered; other invaded systems may be susceptible to change andloss of function or native diversity. In general, a plant’s effects onecosystem properties and processes are a consequence of multipleplant traits (Eviner and Chapin, 2003) and can vary along ecolog-ical gradients (Ehrenfeld, 2003; Eviner and Hawkes, 2008); here,the multiple soil variables that change from pine to pine with black
locust highlight the potential for garlic mustard to exert ecosys-tem effects or merely occupy suitable habitat. Studies underwayare evaluating the impacts of garlic mustard as it colonizes previ-ously non-invaded soils of differing fertility levels, and quantifying
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ts use of existing pathways and differential performance withinhose pathways. Finally, the role of positive feedbacks in garlic mus-ard colonization appears central to its invasiveness; its capacityo regulate soil community structure and function is likely a keyactor determining local abundances. Future work should exploreinks between positive feedback mechanisms and the simultaneousuppression of native competitors.
cknowledgments
We thank D.S. O’Keefe, J. Koch, S. Pawula, S. Tun and Kimberlyang for assistance with lab and field work; Illinois Departmentf Natural Resources, and Billy Lowe, site manager at Sand Ridgetate Forest for access to field sites; and reviewers for sugges-ions to improve the manuscript. This research was sponsoredy the National Science Foundation grant Award DEB-0816621.errmann and McClain were supported by National Science Foun-ation Research Experiences for Undergraduates (REU) grantBI-0755278 to K.D. McConnaughay and S.J. Morris for muchf this work. This research was also sponsored by the Office ofcience (BER) U.S. Department of Energy grant number DE-FG02-4ER63890.
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