2013 NORTHEASTERN NATURALIST 20(2):275–288
Increased Springtail Abundance in a
Garlic Mustard-Invaded Forest
Anne B. Alerding1,* and Roy M. Hunter1,2
Abstract - Alliaria petiolata (Garlic Mustard) decreases diversity of native plants and
introduces novel litter inputs to forests, but whether Garlic Mustard’s presence influences
detritivores is unclear. Our goal was to determine if Garlic Mustard alters springtail (detritivore)
densities during early invasion. We obtained epigeal (litter, humus, and soil)
cores from invaded and uninvaded areas in a Pinus strobus (White Pine) forest and used
high-gradient dynamic sampling to extract springtails. Invaded areas contained nearly
three times more springtails than uninvaded areas, attributable to two springtail morphospecies
from Collembola families Tomoceridae and Entomobryidae. Higher pH in
invaded epigeal samples correlated with increased springtail abundance. pH alkalization
also correlated with increased proportion of juvenile rosettes in mixed stands. Our results
suggest a possible role for pH modulation of springtail abundance in response to Garlic
Non-native (invasive) plants are well known for their disruptive biotic impacts
on ecosystems. As invaders increase in abundance, measurable declines in density
and diversity of native plants occur concomitantly with physical restructuring of
plant biomass that alters niche utilization by animal inhabitants (Baiser et al. 2008,
Bultman and DeWitt 2008, Pearson 2009). Invasive plants are often chemically
distinct from native plants, as their tissues contain novel chemical toxins that deter
biomass loss to herbivores (Callaway and Ridenour 2004). The resulting increased
consumption of native plants by herbivores hastens biomass conversion to invasive
plant biomass (Carvalheiro et al. 2010, Eschtruth and Battles 2009, Schaffner
et al. 2011), which then enters the food web as litter. While it might be predicted
that chemically distinct invasive plant litter would also have slower rates of consumption
by detritivores (animals, fungi, and bacteria), surprisingly, invasive litter
frequently shows accelerated rates of decomposition (Allison and Vitousek 2004,
Knight et al. 2007, Liao et al. 2008, Standish et al. 2004). This apparent dichotomy
of lower consumption of living invasive biomass but enhanced turnover of invasive
litter suggests that native herbivores and detritivores can respond differently
to plant invasion (Kappes et al. 2007, Levin et al. 2006).
It is currently unknown if invasive litter inputs cause trophic shifts that
favor detritivore food webs in forests. In the northeastern United States, one
of the most successful temperate forest invaders is the herbaceous biennial Alliaria
petiolata (M. Bieb.) Cavara & Grande (Garlic Mustard; Rodgers et al.
1Department of Biology, Virginia Military Institute, 203 Maury-Brooke Hall, Lexington,
VA 24450. 2Current address - Virginia Department of Health, 600 Bedford Avenue, Bedford,
VA 24523. *Corresponding author - email@example.com.
276 Northeastern Naturalist Vol. 20, No. 2
2008a). Garlic Mustard grows in a patchy distribution in forest understories,
where it reaches densities as high as 350 plants per m2 (Stinson et al. 2007,
Winterer et al. 2005). Garlic Mustard living biomass is mainly avoided by native
herbivores because its tissues are defended by chemical toxins: cyanide,
glucosinolates, and cyanopropenyl glycosides (Barto et al. 2010, Cipollini and
Gruner 2007, Evans and Landis 2007, Freeland and Janzen 1974, Renwick
2002). Thus, the bulk of Garlic Mustard biomass enters the forest floor as litter,
and forests invaded by Garlic Mustard show accelerated rates of decomposition
(Rodgers et al. 2008b). A mechanism for enhanced decomposition is unknown
but may involve increased activity of detritivores living in the forest understory.
The objective of our research is to measure the detritivore response to Garlic
Mustard invasion in a Pinus strobus (L.) (White Pine) forest.
Collembola (springtails) is an important group of detritivores in White Pine
forests. Springtails facilitate decomposition by breaking litter into smaller pieces
as they feed on both the plant litter and the microflora (bacteria and fungi),
thereby increasing litter surface area for further decomposition (Seastedt 1984).
Springtails are also unaffected by glucosinolate chemical defenses (Kabouw et
al. 2010), such as those produced by Garlic Mustard. Springtail responses to
Garlic Mustard invasion are poorly characterized, the only information coming
from a study focused on carabid beetles. Dávalos and Blossey (2004) measured
carabid beetle prey abundance in two forests by sampling soil beneath the coverboards
and litter beside the coverboards on one occasion during a 6-month study.
One forest showed no change, but the other forest revealed an increase in springtail
abundance (64.6%). To improve accuracy of springtail abundance estimates
in our study, we used an epigeal sampling device to obtain litter, humus, and soil
(together) from each sampling location. We additionally conducted a temporal
analysis of springtail abundance over a 3-week period in early summer, when
both phases of Garlic Mustard (juveniles and adults) co-occurred in the forest.
We hypothesize that abundance of springtails, a vital detritivore in this White
Pine forest, will increase in response to Garlic Mustard invasion.
Invasive plants not only affect biotic interactions in ecosystems, but their presence
impacts the abiotic environment. Abiotic variables such as temperature, pH,
and moisture influence decomposition rates through their effects on detritivores
and microflora (Aerts 1997). In a meta-analysis conducted from 199 articles, it
was recently demonstrated that ecosystems experiencing plant invasion show
enhanced nutrient mineralization and increased levels of macronutrients (P, N)
that facilitate greater productivity of invasive plants (Vilà et al. 2011). While
soil moisture is generally unaltered during plant invasions, pH levels resulting
from interactions between water, soil, humus, litter, and the living biota show
an overall decrease, or acidification (Vilà et al. 2011). Garlic Mustard invasion
causes similar increases in nutrient mineralization in invaded soils, but the pH
response differs from the generalized (meta-analysis) response reported by Vilà
et al. (2011). Garlic Mustard has been shown to alkalize soils in both field and
laboratory experiments (Anderson and Kelley 1995, deHart and Strand 2012,
Rodgers et al. 2008b). Because springtails show high reproductive rates at pH
2013 A.B. Alerding and R.M. Hunter 277
5–6 (Hopkin 1997), a pH range that is characteristic of Garlic Mustard-invaded
soils (Meekins and McCarthy 2001), we investigated pH change as a possible
mechanism for enhanced springtail success during Garlic Mustard invasion. We
hypothesized that springtail abundance would correlate with pH levels known to
maximize their fitness.
In this study, epigeal cores were randomly sampled from a White Pine forest
experiencing early Garlic Mustard invasion. Garlic Mustard density surrounding
the cores was assessed, and samples were measured for pH, moisture, litter composition,
and springtail abundance. We present an exploratory analysis of abiotic
factors and developmental features of Garlic Mustard and their possible roles in
influencing springtail abundance during invasion.
This study was conducted in a mature White Pine forest adjacent to Washington
and Lee University in Lexington, VA. from June into July 2010. The 60-year-old
White Pine forest is undergoing secondary succession to a mixed deciduous canopy
dominated by Fraxinus americana L. (American Ash) and Platanus occidentalis
L. (American Sycamore) in the overstory and Lindera benzoin L. (Spicebush),
Microstegium vimineum (Trin.) (Japanese Stiltgrass), and Garlic Mustard in the
understory. At the time of the study, Garlic Mustard invasion was in its early stages,
with seed propagules spreading southward into the forest from an adjacent section
to the north that was separated from our field site by a walking trail.
We established two adjacent 20-m x 20-m sites, one invaded by Garlic
Mustard and one uninvaded, with similar canopy openness, understory plant
community structure, epigeal composition, slope, and aspect. A few Garlic Mustard
first-year juveniles were found in the uninvaded site during the course of the
study, consistent with the southerly movement of Garlic Mustard into this forest.
Garlic Mustard plants occurred in a patchy distribution within the invaded
site. Garlic Mustard densities in this forest (15–78 plants per m2) reflect low levels
of early-stage invasion, or between 5–20% of the density attained in a highly
invaded forest (Stinson et al. 2007). Abiotic measurements and epigeal samples
were collected over a three-week period, beginning in June 2010, when juveniles
and adults were fully grown and siliques were beginning to release seeds.
Epigeal samples taken included the O horizon (plant litter and humus) and
the first few centimeters of the A horizon (inorganic matter). Temporal changes
in abiotic (moisture and pH) and biotic epigeal variables (litter composition and
springtail abundance) were monitored from randomly collected epigeal cores that
were sampled at weekly intervals between June 28 and July 13 (a once per week
for three weeks sampling protocol). Each 20-m x 20-m field site was subdivided
278 Northeastern Naturalist Vol. 20, No. 2
into four equally sized quadrats. For each sampling date during the temporal
sampling period, five points were randomly selected from each quadrat using a
random number table and X, Y coordinates. One point was selected from each
of the four quadrats per field site, with the fifth randomly selected from any of
the four quadrats. Because Garlic Mustard cover was patchy, sampling locations
were chosen in the invaded quadrats when they contained Garlic Mustard within
a 1-m2 perimeter of the selected X, Y sampling points. Samples were collected
using a 10-cm-diameter hole cutter (foot extractor with outside edge scalloped
blade, Par Aide Products, Lino Lakes, MN). Two 5-cm deep cores were removed
at each sampling point: one to measure springtail abundance and the other for
epigeal composition, pH, and moisture. Samples were transferred from the hole
cutter to sealed plastic bags and stored at 4 °C until analysis, within 6 hours for
springtail abundance and within 24 h for abiotic measures. Depth of epigeal litter
was measured with a ruler inserted through the litter. Garlic Mustard density at
each sampling point was assessed as the number of juveniles and adults within
1 m2 surrounding each sampling point.
Epigeal characteristics (moisture, pH, and composition)
Reserved cores were sorted to remove living plant matter and mixed by hand
to achieve an even mixture of humus, litter, and clay soil. Moisture was estimated
in fresh epigeal mixtures using the gravimetric method of Gardner (1986). pH
was measured in air-dried epigeal mixtures according to McLean (1982) with the
following modifications. The amount of dd H2O added to 2 g epigeal samples
prior to pH measurement was adjusted to compensate for increased water absorption
by needle-leaf litter (10 mL) and less absorption by clay or humus (4 mL).
Composition of needle litter, humus, and clay in the epigeal mixture was determined
as relative abundance (%, v/v) in each sample.
Light intensity and air temperature
Light intensity just above the Garlic Mustard adult canopy was measured at
each sampling point in μmol.m-2.s-1 photosynthetically active radiation with a
Field Scout Light Sensor (Spectrum Technologies, Inc., Plainfield, IL). Air temperature
was measured with a Kestrel 4500 Weather Meter (KestrelMeters.com,
Sylvan Lake, MI).
Epigeal springtail abundance
A high-gradient dynamic extraction method was used to estimate springtail
abundance in epigeal core samples. Methods were modified from Winter and
Behan-Pelletier (2007) as described below. Two sets of five Tullgren funnel temperature
extractors processed the 10 springtail samples that we collected each
week. Each funnel contained an 11-cm-long by 8.8-cm-wide section of black ABS
pipe attached to an ABS pi278pe coupler fitted with a grid panel containing 4-mm
holes. The funnel was attached to 6.6 cm of drain pipe, and the extractor was completed
by inserting a plastic cup (11.5 cm by 9.3 cm) beneath the drain pipe. Heat
was applied to the top of the funnel using a vanity light fixture containing five light
sockets. Fixtures were attached to 8.8-cm x 13.2-cm x 2.2-cm wooden boards to
2013 A.B. Alerding and R.M. Hunter 279
suspend each light bank 8 mm above the top edge of the funnels. Light sockets
were fitted with 60-W bulbs and rheostats to generate precise heat gradients.
Epigeal samples were placed upside-down inside the black pipe of the funnel
on the evening of each sampling date, after the previous week’s samples were
processed. Collection fluid (100 mL of 70 % v/v ethanol) was placed into each
cup to preserve animals as they moved into the collection cups from the epigeal
samples. In our field site, springtails represented over 90% of the number of
animals collected by this method. Mites (Order Oribatidae) represented the remaining
≈10% of animals. Extraction temperatures began at 20 °C on the first day
and were increased by 5 °C per day to a maximum of 40 °C. On the seventh day,
the extraction was terminated by removing springtails from collection cups using
vacuum infiltration with Whatman #1 filter paper. Springtails were stored in
20-ml glass scintillation vials and counted using a dissecting microscope and fine
forceps. Density of springtails was calculated by converting the number per core
sample to number per m2 of epigeal surface area. Springtails were identified to
family using two online taxonomic keys accessed in December 2012 (Christiansen
and Janssens 2010, Christiansen et al. 2012). Preserved morphospecies were
photographed using a Nikon SMZ 1500 dissecting microscope with Nikon Sight
DS-Fi2 digital camera and NIS-Elements 4.00.07 software (Nikon Instruments,
Inc., Melville, NY). Voucher specimens for morphospecies shown in Figure 1
are curated at the Smithsonian Institution (National Museum of Natural History,
Department of Entomology, Washington, DC, reference number 2062591).
Minitab Statistical Software (v. 16) was used for all statistical analyses. We
used ANOVA (general linear model) to investigate effects of temporal sampling
time and presence/absence of Garlic Mustard on springtail abundance.
One-factor ANOVA was used to investigate differences of abiotic factors (light
intensity, air temperature, epigeal moisture, pH, composition, and litter depth)
between the field sites. Pairwise comparisons of means were assessed with Tukey
tests. Linear regressions were used to explore relationships between epigeal pH,
moisture, Garlic Mustard density, and springtail abundance. Additionally, we
investigated the relationship between epigeal pH (Rodgers et al. 2008b) and %
juvenile rosettes (Rodgers et al. 2008b) in northern hardwood-conifer forests by
Epigeal characteristics of invaded and uninvaded field sites
Relative amounts of the three components of epigeal core samples (clay, humus,
and litter) were similar between invaded and uninvaded sites (Table 1). Depth
of leaf litter was also statistically similar between the sites. Nearly 3 times more
light reached the forest floor in the uninvaded site (P = 0.049). Even with higher
light levels in the uninvaded plot, air temperature was slightly cooler (P = 0.04),
possibly related to evapotranspiration of plants photosynthesizing under higher
light conditions. At the ground level, epigeal moisture was significantly lower
280 Northeastern Naturalist Vol. 20, No. 2
(54%) in the invaded site. The most significant difference between the sites was enhanced
epigeal alkalinity in the invaded site. While both sites were slightly acidic
(pH 4.2 versus 5.5), the 30% higher alkalinity in the invaded site (P < 0.001) indicates
a lower concentration of hydrogen ions (by 105 mM) in epigeal substrates.
Relationships between epigeal characteristics and springtail abundance
Five springtail morphospecies representing two families, Tomoceridae
(morphs T1, T2) and Entomobryidae (morphs E1, E2, E3), were detected in this
White Pine forest (Fig. 1). With the exception of morphospecies E3, which was
present only in Garlic Mustard sites, all other morphospecies were present in
equal relative proportions in both invaded and uninvaded sites. The dominant
morphospecies was T1 (on average 52% of collected individuals per epigeal
Figure 1. Springtail morphospecies from family Tomoceridae (T1, T2) and Entomobryidae
(E1, E2, E3) present in epigeal samples from the White Pine forest (Scale bar in each
photo represents 100 μm).
Table 1. Abiotic characteristics of two field sites established in a White Pine forest understory.
Plots were either uninvaded or invaded by Garlic Mustard. Numbers represent the mean ± SE of
ten sampling points. Statistical results from one-factor ANOVA are presented as the F statistic and
P-value for each variable.
Uninvaded plot Invaded plot
Abiotic variable Mean (SE) Mean (SE) F statistic P-value
Light intensity (μmol.m-2.s-1) 126.8 (34.3) 45.9 (17.2) 4.45 0.049
Air temperature (˚C) 29.6 (0.2) 30.2 (0.2) 4.90 0.040
Epigeal moisture (%) 51.0 (10.8) 22.5 (1.2) 6.89 0.017
Epigeal pH 4.2 (0.1) 5.5 (0.1) 97.49 less than 0.001
Humus (% of epigeal core) 38.0 (6.3) 27.5 (4.4) 1.86 0.189
Clay (% of epigeal core) 26.5 (8.8) 38.5 (7.0) 1.14 0.301
Litter (% of epigeal core) 35.5 (8.7) 34.0 (9.6) 0.01 0.909
Litter depth (cm) 34.2 (3.2) 27.4 (2.9) 2.42 0.137
2013 A.B. Alerding and R.M. Hunter 281
sample), followed by E1 (32 %), E2 (8 %), T2 (5%), and E3 (3 %). Total springtail
abundance (of all morphospecies combined) was higher in the invaded forest
understory. We detected between 2–3 times more springtails in the epigeal cores
of the invaded forest understory site (F = 10.65, P = 0.003; Fig. 2). This finding
is likely related to significant increases in abundance of two springtail morphospecies
in invaded sites, T1 (F = 5.79, P = 0.029) and E2 (F = 5.13, P = 0.039).
Morphospecies E1 and T2 were found in equal abundance in invaded and uninvaded
sites (F = 0.20, P = 0.659 and F = 0.21, P = 0.65, respectively). Sampling
date had no effect on total springtail densities (F = 1.88, P = 0.174), as elevated
springtail abundance was noted in Garlic Mustard sampling sites on three occasions
during the months of June and July. However, when considered separately,
we noted that entomobryid densities as a whole were significantly greater at the
second sampling date (F = 6.02, P = 0.027), due to greater abundance of morphospecies
Exploratory regressions were performed to examine abiotic factors that differed
between the two sites (Table 1) and their relationships with total springtail
abundance. Three of the variables that differed between the plots showed no significant
relationship with springtails (light: F = 0.015, P = 0.904; air temperature:
Figure 2. Total springtails present in epigeal samples from White Pine understory sites either
invaded or uninvaded by Garlic Mustard. Each point represents the mean springtail density
(#.m-2) ± SE of five cores randomly sampled from each plot. Springtail density responses to
site location and sampling dates were determined by ANOVA (general linear model).
282 Northeastern Naturalist Vol. 20, No. 2
F = 2.10, P = 0.166; soil moisture: F = 2.69, P = 0.120). The fourth variable,
epigeal pH, positively related with total springtail abundance (F = 5.31, P =
0.0349; Fig. 3), a relationship that was only found for the dominant morphospecies,
T1 (F = 6.71, P = 0.02).
Relationships between epigeal characteristics and Garlic Mustard abundance
Invaded sites had on average 33 ± 4.6 SE individuals per m2, with juveniles
representing 50.1% of the total Garlic Mustard plants counted on the three sampling
dates shown in Figure 2. However, the percentage of juveniles varied from
0–87% of the total individuals when epigeal cores were considered separately.
To explore possible relationships between Garlic Mustard abundance and epigeal
pH, we performed regressions for the two sampling dates when abiotic factors
were most similar. For these regressions, July 13 results were not included because
the first rainfall to occur in five weeks took place on July 12, decreasing
soil pH to the same level as uninvaded sites (data not shown). Neither the density
of juveniles (F = 0.045, P = 0.836) nor adults (F = 0.300, P = 0.593) had
significant relationships with epigeal pH. However, when juvenile density was
expressed as a percentage of total Garlic Mustard plants, almost 80% of the variation
in epigeal pH correlated with increased presence of juvenile rosettes (F =
22.082; P = 0.002; Fig. 4). Using soil pH and % juvenile rosette values reported
separately in Figure 4 and Table 1, respectively, of Rodgers et al. (2008b), we
Figure 3. Relationship between epigeal pH and springtail density in a White Pine forest
understory. pH and springtails were sampled at 18 random points on two sampling dates
that occurred after weeks with no rainfall. Relationship between epigeal pH and springtail
density was investigated with regression analysis.
2013 A.B. Alerding and R.M. Hunter 283
found a similar positive relationship between juvenile abundance and soil pH.
Data from the Rodgers et al. (2008b) study, as re-analyzed and presented in Figure
5 in this study, show that for at least five other forests in the northeastern US,
increasing proportion of juveniles in mixed patches of Garlic Mustard is associated
with greater soil alkalinity (F = 12.362; P = 0.039).
Increased springtail abundance
We found springtail density to be nearly 3 times greater in the epigeal layer of
an invaded forest, a result that was consistently measured on three consecutive
sampling dates. These results support our hypothesis that springtail abundance
increases in response to Garlic Mustard invasion. Our finding that morphospecies
from two springtail families showed idiosyncratic responses to invasion (T1 and
E2 showing elevations, T2 and E1 remaining unchanged), while E3 was present
in only invaded sites, shows the importance of lower taxonomic-level responses
to plant invasion. Neither family- nor morphospecies-level responses to Garlic
Mustard were considered by Dávalos and Blossey (2004), which could explain the
different responses to invasion reported in their study. To our knowledge, our data
Figure 4. Relationship between juvenile rosettes of Garlic Mustard and epigeal pH in an
invaded White Pine forest. For each of the nine values obtained on 28 June 28 and 5 July
2010, epigeal samples were removed before counting the number of juveniles and adults
within a 1-m2 area of the sample. Rosettes are expressed as a percentage of the total number
of Garlic Mustard (GM) plants present for each epigeal sample. Relationship between
percent juveniles and epigeal pH was investigated with regression analysis.
284 Northeastern Naturalist Vol. 20, No. 2
represent the first temporal, morphospecies-level analysis of springtail abundance
in an invaded forest. Additionally, because springtails represent 90% of the total
detritivore densities in this forest, our results suggest Garlic Mustard has a profound
impact on the detritivore trophic level of the decomposer food web.
Whether elevated springtail abundance directly influences higher trophic
interactions remains to be determined. A recent study of food-web responses to
Garlic Mustard by deHart and Strand (2012) used stable isotopes to infer predator
dietary changes in a White Pine forest located a few kilometers from our forest.
Interestingly, predators in the Formicidae and Opiliones families showed changes
in stable isotope signatures, suggesting shifts in feeding preferences away from
springtails and toward Noctuidae caterpillars that were feeding solely on Garlic
Mustard inflorescences. Since springtail densities and predator feeding behaviors
were not measured by deHart and Strand (2012), it is unknown if this feeding shift
occurred as a direct response to altered abundance of Entomobryidae or Tomoceridae
springtails or indirectly because caterpillars were more apparent (and easier to
catch) on inflorescences. Moreover, we note that we followed published protocols
to measure epigeal densities of springtails, while deHart and Strand (2012) collected
arthropods non-randomly, using forceps. This difference in methodology may
explain why deHart and Strand (2012) did not capture springtails in invaded sites.
Figure 5. Relationship between juvenile rosettes of Garlic Mustard and soil pH in five
invaded hardwood-conifer forests in Massachusetts and Connecticut. Data presented in
this figure represent a novel analysis of results from Table 1 (% juvenile rosettes) and
Figure 3 (epigeal pH in invaded sites) from Rodgers et al. (2008b). Relationship between
percent juveniles and epigeal pH was investigated with regression analysis.
2013 A.B. Alerding and R.M. Hunter 285
Springtails and abiotic features of the epigeal environment
In our study, epigeal pH correlated with nearly 25% of the variation in total
springtails in this White Pine forest. Highest springtail densities were measured
in Garlic Mustard-invaded sampling points, with an average value of pH 5.5,
supporting our hypothesis that springtail abundance would be maximized at pH
levels known to enhance springtail growth and reproduction (Hopkin 1997). At
least two other invasive plant species have been shown to increase soil alkalization
(Japanese Stiltgrass and Berberis thunbergii (DC) [Japanese Barberry];
Ehrenfeld et al. 2001, McGrath and Binkley 2009, Nuzzo et al. 2009). It is unknown
if springtails respond similarly to soil alkalization in forests invaded by
these invasives. We did discover that alkalization in our study was not additionally
enhanced by the presence of Japanese Stiltgrass in our sampling sites (data
A precise mechanism relating pH alkalization to increased springtail abundance
is unknown, but one possibility is that higher pH levels in the epigeal
layer of invaded forests enhance ventral tube functioning. The ventral tube is a
characteristic structure protruding from the springtail abdomen that is involved in
maintaining water homeostasis and in adhering springtails to smooth substrates
through adhesive properties (Hopkin 1997). Proper functioning of the ventral tube
is thought to require precise amounts of water and pH levels in the environment,
with ranges varying among species (Hopkin 1997). In Tomoceridae, fluid uptake
through the ventral tube is strongly inhibited in acidic environments (pH 2–3)
and highest between pH 5–6 (Jaeger and Eisenbeis 1984). Our demonstration that
total springtail abundance (and in particular, Tomoceridae morphospecies T1)
increases in this White Pine forest in correlation with epigeal alkalization is suggestive
of enhanced functioning of the ventral tube as a mechanism facilitating
springtail growth in Garlic Mustard invaded forests.
Even though ventral tube functioning is reportedly sensitive to external
moisture levels (Hopkin 1997), we found no significant relationship between
epigeal moisture and Entomobryidae springtail abundance in this White Pine
forest. Because levels of epigeal soil moisture in this forest (on average 53.9%)
were similar to those reported for other temperate forests that support springtail
populations (Salamon et al. 2008), it is likely that levels of soil moisture were
sufficient to support springtail growth and reproduction in this forest. In addition,
our finding that epigeal moisture was similar between invaded and uninvaded
sites, consistent with its general non-responsiveness to plant invasion (Vilà et
al. 2011), suggests that moisture influence on ventral tube functioning may play
little, if any, role in springtail responses to Garlic Mustard invasion.
Invasion pH and Garlic Mustard juveniles
Garlic Mustard’s biennial life cycle has important consequences for its longterm
establishment. Co-occurrence of juveniles and adults in mixed patches
results in competition between the developmental stages, with most adults surviving
to reproduce at the expense of juveniles (Winterer et al. 2005). Results
from our study show a possible relationship between the proportionate increase
286 Northeastern Naturalist Vol. 20, No. 2
in juvenile rosettes in mixed patches and epigeal alkalization. Our results are
corroborated through original re-analysis of data presented in Rodgers et al.
(2008b) and thus may indicate a competitive mechanism of juveniles in mixed
patches. A mechanism for plant-mediated alkalization is currently unknown, but
it has been suggested that H+ uptake by Garlic Mustard roots may increase as a
compensatory response to rapid uptake of NO3
- in invaded soils (Ehrenfeld et al.
2001, Hewins and Hyatt 2010). It would be of interest to measure H+ and NO3
uptake in roots of juveniles and adults growing in mixed patches that differ in the
proportions of juveniles and adults. Perhaps juveniles have evolved faster uptake
rates of both ions as a mechanism to increase their survival in mixed patches.
Our research shows that Garlic Mustard invasion not only impacts plant communities,
but its presence in forests also affects animals, specifically detritivores.
Forests with well-established populations of Garlic Mustard show enhanced rates
of decomposition, lower amounts of litter, and increased levels of macronutrients
(Rodgers et al. 2008b), but mechanisms for increased decomposition remain
undetermined. Since springtail feeding enhances both decomposition and nutrient
mineralization (Seastedt and Crossley 1984), our correlative findings between epigeal
alkalization and enhanced springtail abundance suggest a possible mechanism
that should be examined in future studies. It would be interesting to explore the
nature of the relationship between springtail abundance and increased rates of litter
decomposition in invaded forests. Ultimately, by stimulating springtail population
growth, Garlic Mustard may provide greater supply of food for detritivores that
rely on energy inputs from the base of this understory food web.
Financial support was provided by the Virginia Military Institute Center for Undergraduate
Research and the Jackson-Hope Fund. We thank Matthew Waalkes and Sarah Strand
for assisting with field measurements, Leslie Joyce and Karen Fredenburg for ordering
equipment and chemicals, Megan Newman for expedited interlibrary loans, Peppy Kesler
for helping construct the Tullgren funnel apparatus, and two anonymous reviewers for providing
constructive feedback. Wade Bell assisted with springtail identification, and Dick
Rowe, Paul Moosman, and Emily Lilly provided critical readings of this manuscript.
Aerts, R. 1997. Climate, leaf-litter chemistry, and leaf-litter decomposition in terrestrial
ecosystems: A triangular relationship. Oikos 79:439–449.
Allison, S.D., and P.M. Vitousek. 2004. Rapid nutrient cycling in leaf litter from invasive
plants in Hawai’i. Oecologia 141:612–619.
Anderson, R.C., and T.M. Kelley. 1995. Growth of Garlic Mustard (Alliaria petiolata) in
native soils of different acidity. Transactions of the Illinois State Academy of Science
Baiser, B., J.L. Lockwood, D. La Puma, and M.F.J. Aronson. 2008. A perfect storm: Two
ecosystem engineers interact to degrade deciduous forests of New Jersey. Biological
2013 A.B. Alerding and R.M. Hunter 287
Barto, E.K., J.R. Powell, and D. Cipollini. 2010. How novel are the chemical weapons
of Garlic Mustard in North American forest understories? Biological Invasions
Bultman, T., and D.J. DeWitt. 2008. Effect of an invasive ground cover plant on the
abundance and diversity of a forest-floor spider assemblage. Biological Invasions
Callaway, R.M., and W.M. Ridenour. 2004. Novel weapons: Invasive success and the
evolution of increased competitive ability. Frontiers in Ecology and the Environment
Carvalheiro, L.G., Y. Buckley, and J. Memmot. 2010. Diet breadth influences how the
impact of invasive plants is propagated through food webs. Ecology 91:1063–1074.
Christiansen, K.A., and F. Janssens. 2010. Checklist of the Collembola: Key to the common
surface-dwelling Collembola from North America. Available online at http://
www.collembola.org/key/bugguide.htm. Accessed December 2012.
Christiansen, K.A., P. Greenslade, L. Deharveng, R.J. Pomorski, and F. Janssens. 2012.
Checklist of the Collembola: Key to the families of Collembola. Available online at
http://www.collembola.org/key/collembo.htm. Accessed December 2012.
Cipollini, D., and B. Gruner. 2007. Cyanide in the chemical arsenal of Garlic Mustard,
Alliaria petiolata. Journal of Chemical Ecology 33:85–94.
Dávalos, A., and B. Blossey. 2004. Influence of the invasive herb Garlic Mustard on
ground-beetle assemblages. Environmental Entomology 33:564–576.
deHart, P.A.P., and S.A. Strand. 2012. Effects of Garlic Mustard invasion on arthropod diets
as revealed through stable-isotope analyses. Southeastern Naturalist 11:575–588.
Ehrenfeld, J.G., P. Koutev, and W. Huang. 2001. Changes in soil functions following
invasions of exotic understory plants in deciduous forests. Ecological Applications
Eschtruth, A.K., and J.J. Battles. 2009. Acceleration of exotic plant invasion in a forested
ecosystem by a generalist herbivore. Conservation Biology 23:388–399.
Evans, J.A., and D.A. Landis. 2007. Pre-release monitoring of Alliaria petiolata (Garlic
Mustard) invasions and the impacts of extant natural enemies in southern Michigan
forests. Biological Control 42:300–307.
Freeland, W.J., and D.H Janzen. 1974. Strategies in herbivory by mammals: The role of
plant secondary compounds. The American Naturalist 108:269–289.
Gardner, W.H. 1986. Water content. Pp. 493–544, In E.A. Klute (Ed.). Methods of Soil
Analysis, Part 1. Physical and Mineralogical Methods: Agronomy Monograph No.
9, 2nd Edition. American Society of Agronomy and Soil Science Society of America,
Madison, WI. 1358 pp.
Hewins, D.B., and L.A. Hyatt. 2010. Flexible N uptake and assimilation mechanisms may
assist biological invasion by Alliaria petiolata. Biological Invasions 12:2639–2647.
Hopkin, P.S. 1997. Biology of the Springtails. Oxford University Press, New York, NY.
Jaeger, G., and G. Eisenbeis. 1984. pH-dependent absorption of solutions by the ventral
tube of Tomocerus flavescens (Tullberg, 1871) (Insecta, Collembola). Revue
D’Écologie et de Biologie du Sol 21:519–531.
Kabouw, P., W.H. van der Putten, N.M. van Dam, and A. Biere. 2010. Effects of intraspecific
variation in White Cabbage (Brassica oleracea var. capitata) on soil organisms.
Plant and Soil 336:509–518.
Kappes, H., R. Lay, and W. Topp. 2007. Changes in different trophic levels of litter-dwelling
macrofauna associated with giant knotweed invasion. Ecosystems 10:734–744.
Knight, K.S., J.S. Kurylo, A.G. Endress, J.R. Stewart, and P.B. Reich. 2007. Ecology and
ecosystem impacts of Common Buckthorn (Rhamnus cathartica): A review. Biological
288 Northeastern Naturalist Vol. 20, No. 2
Levin, L.A., C. Neira, and E.D. Grosholz. 2006. Invasive cordgrass modifies wetland
trophic function. Ecology 87:419–432.
Liao, C., R. Peng, Y. Luo, X. Zhou, X. Wu, C. Fang, J. Chen, and B. Li. 2008. Altered
ecosystem carbon and nitrogen cycles by plant invasion: A meta-analysis. New Phytologist
McGrath, D.A., and M.A. Binkley. 2009. Microstegium vimineum invasion changes soil
chemistry and microarthropod communities in Cumberland Plateau forests. Southeastern
McLean, E.O. 1982. Soil pH and lime equipment. Pp. 119–225, In A.L. Page, R.H.
Miller, and D.R. Keeney (Eds.). Methods of Soil Analysis, Part 2. Chemical and Microbiological
Properties: Agronomy Monograph No. 9, 2nd Edition. American Society
of Agronomy and Soil Science Society of America, Madison, WI. 1159 pp.
Meekins, J.F., and B.C. McCarthy. 2001. Effect of environmental variation on the invasive
success of a nonindigenous forest herb. Ecological Applications 11:1336–1348.
Nuzzo, V.M., J.C. Maerz, and B. Blossey. 2009. Earthworm invasion as the driving force
behind plant invasion and community change in Northeastern North American forests.
Conservation Biology 23:966–974.
Pearson, D.E. 2009. Invasive plant architecture alters trophic interactions by changing
predator abundance and behavior. Oecologia 159:549–558.
Renwick, J.A.A. 2002. The chemical world of crucivores: Lures, treats, and traps. Entomologia
Experimentalis et Applicata 104:35–42.
Rodgers V.L., K.A. Stinson, and A.C. Finzi. 2008a. Ready or not, Garlic Mustard is moving
in: Alliaria petiolata as a member of Eastern North American forests. BioScience
Rodgers V.L., B.E. Wolfe, L.K. Werden, and A.C. Finzi. 2008b. The invasive species
Alliaria petiolata (Garlic Mustard) increases soil nutrient availability in northern
hardwood-conifer forests. Oecologia 157:459–471.
Salamon, J.A., S. Scheu, and M. Schaefer. 2008. The Collembola community of pure and
mixed stands of beech (Fagus sylvatica) and spruce (Picea abies) of different age.
Schaffner, U., W.M. Ridenour, V.C. Wolf, T. Bassett, C. Müller, H. Müller-Schärer, S.
Sutherland, C.J. Lortie, and R.M. Callaway. 2011. Plant invasions, generalist herbivores,
and novel defense weapons. Ecology 92:829–835.
Seastedt, T.R. 1984. The role of microarthropods in decomposition and mineralization
processes. Annual Review of Entomology 29:25–46.
Seastedt, T.R., and D.A. Crossley, Jr. 1984. The influence of arthropods on ecosystems.
Standish, R.J., P.A. Williams, A.W. Robertson, N. A. Scott, and D.I. Hedderley. 2004.
Invasion by a perennial herb increases decomposition rate and alters nutrient availability
in warm temperate lowland forest remnants. Biological Invasions 6:71–81.
Stinson, K., S. Kaufman, L. Durbin, and F. Lowenstein. 2007. Impacts of Garlic Mustard
invasion on a forest understory community. Northeastern Naturalist 14:73–88.
Vilà, M., J.L. Espinar, M. Hejda, P.E. Hulme, V. Jarošík, J.L. Maron, J. Pergl, U. Schaffner,
Y. Sun, and P. Pyšek. 2011. Ecological impacts of invasive alien plants: A metaanalysis
of their effects on species, communities, and ecosystems. Ecology Letters
Winter, J.P., and V.M. Behan-Pelletier. 2007. Microarthropods. Pp. 399–414, In M.R.
Carter and E.G. Gregorich (Eds.). Soil Sampling Methods of Analysis, 2nd Edition.
Canadian Society of Soil Science. 1264 pp.
Winterer, J., M.C. Walsh, M. Poddar, J.W. Brennan, and S.M. Primak. 2005. Spatial and
temporal segregation of juvenile and mature Garlic Mustard plants (Alliaria petiolata)
in a central Pennsylvania woodland. American Midland Naturalist 153:209–216.