Download Experimental evidence for indirect facilitation among invasive plants

Journal of Ecology 2014, 102, 12–18
doi: 10.1111/1365-2745.12186
Experimental evidence for indirect facilitation among
invasive plants
S. Luke Flory1* and Jonathan T. Bauer2
1
Agronomy Department University of Florida, Gainesville, FL 32611, USA; and 2Department of Biology Indiana
University, Bloomington, IN 47405, USA
Summary
1. Facilitation among species may promote non-native plant invasions through alteration of environmental conditions, enemies or mutualists. However, the role of non-trophic indirect facilitation in
invasions has rarely been examined.
2. We used a long-term field experiment to test for indirect facilitation by invasions of Microstegium
vimineum (stiltgrass) on a secondary invasion of Alliaria petiolata (garlic mustard) by introducing
Alliaria seed into replicated plots previously invaded experimentally by Microstegium.
3. Alliaria more readily colonized control plots without Microstegium but produced almost seven
times more biomass and nearly four times as many siliques per plant in Microstegium-invaded plots.
Improved performance of Alliaria in Microstegium-invaded plots compared to control plots overwhelmed differences in total number of plants such that, on average, invaded plots contained 327%
greater total Alliaria biomass and 234% more total siliques compared to control plots.
4. The facilitation of Alliaria in Microstegium-invaded plots was associated with an 85% reduction
in the biomass of resident species at the peak of the growing season and significantly greater light
availability in Microstegium-invaded than control plots early in the growing season.
5. Synthesis. Our results demonstrate that an initial plant invasion associated with suppression of
resident species and increased resource availability can facilitate a secondary plant invasion. Such
positive interactions among species with similar habitat requirements, but offset phenologies, may
exacerbate invasions and their impacts on native ecosystems.
Key-words: competitors, disturbance, invasion ecology, invasional meltdown, plant invasion,
positive interactions, resource availability
Introduction
Facilitative interactions have received increasing attention as
potential drivers of plant community structure (reviewed by
Brooker et al. 2008). Positive interactions among plant
species might occur through protection from unfavourable
abiotic conditions or by altered effects of herbivores,
pathogens or competitors. These interactions can moderate the
effects of global environmental changes such as non-native
species invasions, climate change and habitat loss (Lortie
et al. 2004). However, positive interactions among species
may also exacerbate such problems if, for example, one
invasive species facilitates further invasions (Mitchell et al.
2006; Kuebbing, Nu~nez & Simberloff 2013). Interspecific
facilitation, leading to increasing numbers and impacts of
invasions, has been termed ‘invasional meltdown’ (Simberloff
& Von Holle 1999) but has very rarely been demonstrated
*Correspondence author. E-mail: flory@ufl.edu
experimentally in natural systems (Simberloff 2006; Green
et al. 2011).
Direct facilitation among invasive species may occur when,
for example, N-fixing invasive shrubs (Hughes & Denslow
2005) or herbs (Carino & Daehler 2002) increase soil nitrogen availability, which then benefits other non-native species.
Similarly, intraspecific facilitation can occur when adult invasive plants provide favourable abiotic conditions for offspring
(Reinhart, Maestre & Callaway 2006; Saccone et al. 2010).
Facilitation across trophic levels may also occur, such as
when an invasive plant provides habitat for consumers that
feed on native species (Orrock, Witter & Reichman 2008). In
contrast, indirect facilitation occurs when the indirect benefit
of one species on another, through suppression of a shared
competitor, is greater than direct competition between the
species. In natural plant communities, there is evidence that
indirect interspecific facilitation can influence species composition and structure (Levine 1999), but there are few examples involving non-native plant species (Siemann & Rogers
2003). To our knowledge, no study has experimentally tested
© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society
Indirect facilitation among invasive plants 13
for non-trophic indirect facilitation among invasive plant
species.
We performed a field experiment to test the strength of
indirect facilitation by Microstegium vimineum (Trin.)
A. Camus (stiltgrass; hereafter Microstegium) on Alliaria petiolata (M. Bieb) Cavara & Grande (garlic mustard; hereafter
Alliaria), two of the most aggressive and problematic nonnative invasive plant species in eastern North America. We
experimentally invaded half of our long-term field plots with
Microstegium. Then, after three growing seasons, we added
Alliaria seed to Microstegium-invaded and control plots
across three disturbance regimes to determine whether the first
invasion facilitated the second invader. We expected that
Microstegium would provide little direct competition because
the two species have offset phenologies (Morrison et al.
2007). Alliaria germinates and grows predominantly during
early spring (i.e. C3 species, Anderson, Dhillion & Kelley
1996) and Microstegium germinates in late spring and produces the greatest biomass in late summer (i.e. C4 species).
Furthermore, Microstegium suppresses native herbaceous species (Flory & Clay 2010a; Bauer & Flory 2011) and tree
regeneration (Oswalt, Oswalt & Clatterbuck 2007; Flory &
Clay 2010b). Thus, we hypothesized that Microstegium invasions would indirectly facilitate Alliaria by suppressing native
species that would otherwise compete with Alliaria early in
the growing season. Such dynamics would be consistent with
the indirect facilitation model of plant communities (Levine
1976).
Materials and methods
STUDY SPECIES
Microstegium is a C4 annual grass that colonizes roadsides, trails and
disturbed areas, but can also invade intact, closed-canopy forests and
riparian areas (Flory 2010; Warren, Wright & Bradford 2011). Microstegium was introduced to North America from Southeast Asia in the
early 1900s (Fairbrothers & Gray 1972) and now occurs in 25 eastern
US states (USDA & NRCS 2013). Microstegium invasions can have
dramatic negative effects on native plant communities (Flory & Clay
2010a,b; Warren, Wright & Bradford 2011), arthropods (Simao,
Flory & Rudgers 2010) and ecosystem processes (Lee, Flory &
Phillips 2012). It germinates in late spring or early summer, grows
predominantly in mid-to-late summer, and flowers and produces seed
in early fall.
Alliaria is a C3 biennial herb from Europe that is invasive in forest
understories throughout the eastern US (Rodgers, Stinson & Finzi
2008). Alliaria invasions can suppress spring ephemeral flora and tree
seedlings, likely not only through direct interactions, but also
indirectly through suppression of mycorrhizal fungi communities
(McCarthy 1997; Stinson et al. 2007; Herold et al. 2011). Like Microstegium, Alliaria can also reduce the diversity and abundance of
insects and alter abiotic soil properties (impacts of Alliaria invasion
reviewed by Rodgers, Stinson & Finzi 2008). Alliaria germinates
early in the growing season, before most native species, and grows as
a rosette for the first year. Although seedling densities are often high
(Anderson, Dhillion & Kelley 1996), rosettes are sensitive to both
inter- and intraspecific competition (Bauer, Anderson & Anderson
2010). In the second year, plants rapidly bolt and flower very early in
the growing season (Anderson, Dhillion & Kelley 1996), and the
growth and reproductive success of adult plants is dependent on light
availability early in the growing season (Engelhardt & Anderson
2011).
E X P E R I M E N TA L S I T E
We conducted the experiment near Bloomington, Indiana, at the Indiana University Research and Teaching Preserve, Bayles Road site
(39°13′9″ N, 86°32′29″ W). In September 2005, we randomly
arranged 14 plots (5.25 9 5.25 m) in a ~40 9 60 m field surrounded
by mature trees (i.e. a forest opening) at 2.5 m spacing. There were
no canopy trees in or among the plots. The field was historically bottomland forest but has been maintained for ecological research for
more than 30 years. We surrounded each plot with 60-cm-tall erosion
barrier buried 10 cm deep to prevent movement of seeds among plots
and release of seeds to surrounding areas. Then, we planted all plots
with seed from 12 native woodland herbaceous species and nine
native tree species (see Flory & Clay 2010a,b for species lists).
Finally, we sowed half of the otherwise identical plots (n = 7) with
50 g Microstegium seeds (~19 000) per plot corresponding to
observed seedling densities in locally invaded sites. Plots were not
weeded or manipulated after the initial planting but were naturally
colonized by trees and herbaceous species from the seed bank and the
surrounding area (Flory & Clay 2010a,b).
E X P E R I M E N TA L D E S I G N
To determine whether Alliaria was facilitated by Microstegium, we
added Alliaria seed into both Microstegium-invaded and control plots
under three disturbance regimes (Fig. 1). We established three sets of
three subplots, separated by 0.5–1 m, at the northwest, southwest and
southeast corner of each plot (nine total subplots per plot). Plot was
the level of replication. Each subplot consisted of a 25-cm-diameter
plastic pot cut in half horizontally and the bottom removed and then
sunk 5 cm into the soil to prevent movement of Alliaria seed outside
of the subplot. At each of the three locations within a plot (Fig. 1),
we subjected each subplot to one of the three disturbance treatments:
no disturbance, moderate disturbance (raked with a three-tine garden
tool) or heavy disturbance (raked and all litter removed). Existing
Microstegium and native vegetation was left in place.
We collected Alliaria seed from a naturally occurring invasive population approximately 1 km from the research site in July 2008. We
then added approximately 50 Alliaria seeds by weight (0.094 g) to
each plot in December 2008 immediately after disturbance treatments
were applied. Very few seeds germinated in spring 2009, so we
repeated disturbance treatments in November 2009 and added ~200
(0.38 g) more seeds from the initial collection to all subplots. We
repeated disturbance treatments for a third time in March 2011.
D ATA C O L L E C T I O N A N D A N A LY S I S
To quantify the response of Alliaria to the Microstegium invasion and
disturbance treatments, we counted the number of Alliaria rosettes
(i.e. first-year plants) in late spring 2011 and the number of Alliaria
adults (i.e. second-year plants) in 2012. A large number of Alliaria
seeds germinated in 2011, but very few Alliaria rosettes were found
in spring 2009, 2010 or 2012 so we chose to follow only the 2011
cohort throughout the experiment. In June 2012, after the plants had
been counted, we harvested all Alliaria adult plants, measured their
height and counted the number of siliques produced per plant, dried
© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society, Journal of Ecology, 102, 12–18
14 S. L. Flory & J. T. Bauer
for the spatial structure within our experiment. We used Proc MIXED
in SAS 9.4 for all the analyses. We tested for differences in the biomass
of native species, Microstegium, litter between Microstegium-invaded
and control plots and changes in responses over time, using repeatedmeasures ANOVA (RM-ANOVA). Differences in light availability between
Microstegium-invaded and control plots and changes over time were
analysed using RM-ANOVA (Proc GLM, SAS 9.4).
Results
Fig. 1. Diagram showing the experimental design of the Microstegiuminvaded and uninvaded plots including the location of the Alliaria
introduction subplots (not to scale) and the disturbance treatments.
Monthly biomass harvests were conducted randomly at least 1 m
from the Alliaria introduction subplots.
them to constant mass at 60 °C and weighed them. To evaluate patterns of Microstegium, resident species and litter abundance throughout the 2010 growing season, we harvested 1 25 9 25 cm square
quadrat randomly located in each plot in April, May, June, July and
August (Fig. 1). Harvested quadrats were located at least 1 m from
the Alliaria introduction subplots. Samples were sorted by Microstegium, resident species and litter, then dried and weighed. Resident
native biomass was not sorted by individual species, but previous
research in these plots has shown that declines in biomass and diversity in invaded plots were not due to only one or a few species (Flory
& Clay 2010a). To determine how the invasion treatments affected
light availability, we measured light at ground level, at 0.5 m, and
above the plant canopy (AccuPAR Linear PAR/LAI ceptometer;
Decagon Devices, Inc., Pullman, WA, USA; photosynthetic photon
flux density (PPFD); mol m 2 s 1) at each of the three locations in
each plot during the 2010 growing season (Fig. 1). We calculated
available light by dividing the light value at ground level and 0.5 m
by the measurement above the canopy at each location.
D ATA A N A LY S I S
We tested for the effects of disturbance (control, moderate, heavy) and
Microstegium invasion on the number of Alliaria rosettes in 2011 and
the number of Alliaria adults in 2012 using separate ANOVAs with
disturbance, invasion and their interactions as fixed effects. We used
additional ANOVAs to test for effects of disturbance, invasion and their
interaction on the total biomass and the average height and silique production per plant of Alliaria in each subplot. For both sets of models,
we included subplot nested within plot as a random effect to account
The numbers of Alliaria rosettes and adults were significantly
affected by both Microstegium invasion and the disturbance
treatment. In 2011, the number of Alliaria rosettes was greater in
control plots than Microstegium-invaded plots for the undisturbed and moderately disturbed treatments, but the number of
rosettes was similar between invasion treatments with heavy
disturbance (invasion 9 disturbance, F2,80 = 5.67; P = 0.005).
Within control plots, there were 96% more Alliaria rosettes in
moderately disturbed subplots than in heavily disturbed subplots,
and 30% more in undisturbed than moderately disturbed subplots
(Fig. 2a). This pattern persisted for Alliaria adults in control
plots in 2012 (invasion 9 disturbance, F2,80 = 4.52; P = 0.014),
but the differences among disturbance levels was smaller and
there were relatively greater numbers of adults in Microstegiuminvaded plots that were exposed to heavy disturbance than
control or moderately disturbed plots (Fig. 2b; see Table S1 in
Supporting Information).
Overall, there was a significant positive effect of Microstegium invasion on the performance of Alliaria adult plants.
The average biomass (F1,80 = 6.18; P = 0.015) and silique
production (F1,80 = 6.09; P = 0.016) of individual Alliaria
plants increased in invaded plots relative to controls, and
there was a marginal increase in adult plant height (Fig. 3,
F1,80 = 3.45; P = 0.067). Average biomass and silique production per plant increased by 696% and 385%, respectively,
over controls, overwhelming the differences in total number
of plants in control compared to invaded plots. As a result,
on average, invaded plots contained 73.7 g total Alliaria biomass, which produced 1284 total siliques as compared to only
17.3 g total Alliaria producing 384 total siliques on average
in control plots. There were no effects of disturbance or interactions between disturbance and invasion on the performance
of Alliaria (Fig. 3, see Table S2).
Microstegium-invaded plots had significantly lower biomass of native resident species compared to control plots
(RM-ANOVA; F1,12 = 18.68; P = 0.001; Fig. 4a) but resident
species biomass increased over the growing season in both
Microstegium-invaded and control plots (F1,24 = 5.63;
P = 0.026). There was an interaction between the Microstegium invasion treatment and time for Microstegium biomass
(F4,48 = 17.6; P < 0.0001; Fig. 4b) due to increasing biomass
over the growing season in Microstegium-invaded plots but
consistently absent or very low abundance of Microstegium in
control plots. There was a marginal effect of Microstegium
invasion on litter mass (F1,12 = 3.43; P = 0.089; Fig. 4c),
with a tendency for greater litter biomass in Microstegiuminvaded compared to control plots early and late in the season
© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society, Journal of Ecology, 102, 12–18
Indirect facilitation among invasive plants 15
(a)
(a)
(b)
(b)
(c)
Fig. 2. Number of first year Alliaria plants (least squares
means SE) in 2011 (a) and second-year plants in 2012 (b) in control and Microstegium-invaded plots under no, moderate (mod) and
heavy disturbance treatments. Different letters indicate significant post
hoc differences at P < 0.05.
and no difference during mid-season. Total plant biomass was
25–56% lower in Microstegium-invaded than control plots
(F1,12 = 8.75; P = 0.012). Total biomass increased over the
growing season (F4,48 = 11.8; P = 0.0001), but the difference
between Microstegium-invaded plots and controls was consistent throughout the growing season (time*invasion, F4,48 =
0.87; P = 0.45).
Percentage light availability at 0.5 m was consistently greater
in Microstegium-invaded than control plots, particularly early
in the growing season, but there was no overall statistically significant difference between the Microstegium invasion treatments (F1, 12 = 2.73; P = 0.11; Fig. 5a). At ground level, there
was a marginal reduction in percentage light availability due to
Microstegium invasion (F1,12 = 3.67; P = 0.079; Fig. 5b) and
light availability varied across time (F4, 48 = 4.04; P = 0.018),
with more light available at ground level in control plots in
April and August, but similar light levels in Microstegiuminvaded and control plots from May through July.
Discussion
Our study experimentally demonstrates that Microstegium
can facilitate Alliaria across a range of disturbance
regimes. Greater growth and reproduction of Alliaria in
Fig. 3. Biomass (g; a), height (cm; b) and number of siliques (c) produced per Alliaria adult (least squares means SE) in control and
Microstegium-invaded plots in 2012.
Microstegium-invaded plots may be indirectly facilitated by
Microstegium’s suppression of shared resident competitors
and associated increases in resource availability, although
other mechanisms are possible. Alliaria more readily colonized native-dominated than Microstegium-invaded plots, particularly in the absence of disturbance, but Alliaria adults in
Microstegium-invaded plots were nearly seven times larger and
produced almost four times more siliques than Alliaria in
control plots (Fig. 3). Microstegium-invaded plots had substantially less resident community biomass than control plots,
and very little Microstegium early in the growing season when
Alliaria is most productive (Fig. 4). Low amounts of resident
biomass in Microstegium-invaded plots were presumably due
to the direct effects of Microstegium in prior years (Flory &
Clay 2010a; Bauer & Flory 2011). Reduced total biomass in
Microstegium-invaded compared to control plots resulted in
significantly higher light levels early in the growing season
(Fig. 5). Offset phenologies of Alliaria and Microstegium,
reductions in shared competitors, greater light availability or
other unmeasured abiotic or biotic changes due to the invasion
may have contributed to the facilitation of Alliaria in
© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society, Journal of Ecology, 102, 12–18
16 S. L. Flory & J. T. Bauer
(a)
(a)
(b)
(b)
(c)
Fig. 5. Percentage ambient light (least squares means SE) at 0.5 m
(a) and ground level (b) in control and Microstegium-invaded plots
over the 2010 growing season. Asterisks indicate significant post hoc
differences within dates at P < 0.05.
Fig. 4. Resident species (a), Microstegium (b) and litter (c) biomass
(least squares means SE) in control and Microstegium-invaded
plots over the 2010 growing season. Asterisks indicate significant post
hoc differences within dates at P < 0.05.
Microstegium-invaded plots. Regardless of the underlying
mechanism, Alliaria performance was promoted by prior invasions of Microstegium, providing robust experimental evidence
for facilitation among these invasive plant species.
Few studies have evaluated the role of facilitation among
invasive plant species (Tecco et al. 2007; Cushman, Lortie &
Christian 2011; Wundrow et al. 2012), and to our knowledge,
this study is the only experimental example of facilitation
between two invasive plant species where there is evidence
for indirect facilitation via suppression of shared competitors
and increased resource availability. However, further experimental work is needed to determine the relative contributions
of different mechanisms for facilitation of Alliaria by Microstegium, including the possible roles of alteration of microbial
(Callaway et al. 2004) or herbivore (Parker, Burkepile & Hay
2006) communities. For example, invasive plants can alter
soil microbial communities or nutrient availability, thereby
providing more suitable conditions for conspecific (Lee, Flory
& Phillips 2012) or heterospecific (Von Holle et al. 2006)
non-native plants. Invasive plants may also provide protection
from herbivores (Cushman, Lortie & Christian 2011), host
shared pollinators (Molina-Montenegro, Badano & Cavieres
2008) or create abiotic conditions that are relatively more
favourable for their offspring than native competitors (Reinhart, Maestre & Callaway 2006). Much more common than
interactions among invasive plant species are examples of
native plant species facilitating invasions (e.g. Maron &
Connors 1996; Saccone et al. 2010) or facilitation across
trophic levels such as when animals facilitate invasive plants
(Nuzzo, Maerz & Blossey 2009). Despite the lack of examples thus far, ongoing introductions of species to novel habitats may increase the co-occurrence of species with different
phenologies or resource requirements (Fridley 2012) and
promote indirect facilitation among invasive plant species
(Kuebbing, Nu~
nez & Simberloff 2013).
Microstegium significantly enhanced performance of adult
Alliaria plants but colonization of rosettes was much greater
under undisturbed and moderately disturbed treatments in
uninvaded plots (Fig. 2). Reductions in resident community
biomass in invaded plots (Fig. 4) were associated with greater
light availability early in the growing season (Fig. 5), which
may have increased Alliaria performance. In addition to reducing resident herbaceous species biomass, Microstegium invasions can also alter the composition of herbaceous species
(Adams & Engelhardt 2009; Flory & Clay 2010a) and suppress
the natural regeneration of trees (Marshall, Buckley & Franklin
2009; Flory & Clay 2010b), which may have contributed to
increased light availability. Here, we did not evaluate the species richness or composition of the native herbaceous community, but future research could investigate whether particular
groups of native species that are susceptible to the competitive
© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society, Journal of Ecology, 102, 12–18
Indirect facilitation among invasive plants 17
effects of Microstegium are driving responses of Alliaria in
Microstegium-invaded plots. Other unmeasured resources
besides light, such as nutrients or water, may have also contributed to differences in Alliaria performance. Low Alliaria colonization in invaded plots could have been due to higher
amounts of litter (Fig. 3, Flory & Clay 2010b; Bartuszevige,
Hrenko & Gorchov 2007) and reduced light levels at the soil
surface (Fig. 5). Disturbance reduced or removed the improved
conditions for Alliaria colonization in control plots, possibly
because seeds desiccated on the soil surface due to excessive
sunlight when the litter layer was removed. The conditions at
this particular experimental site, a forest opening (i.e. a field)
with significant sun exposure much of the day, may have contributed to the differences among disturbance treatments. The
site conditions may have influenced the facilitative effects of
Microstegium on Alliaria adults as well and results under different environmental conditions, particularly sun exposure, may
vary. Both Alliaria (Nuzzo 1993) and Microstegium (Flory
2010) can invade a wide range of edge and forest habitats, so
further tests of facilitation among the species in various habitats
are needed (Kuebbing, Nu~nez & Simberloff 2013).
In our experiment, we introduced a small amount of Alliaria seed into relatively large plots (27 m2) that had been
either experimentally invaded or not invaded by Microstegium. This allowed us to evaluate the facilitative effects of
Microstegium on Alliaria and the possible underlying mechanisms of changes in resident native herbaceous competitors
and resource availability. However, because of the relatively
small scale of the Alliaria introductions, we were not able to
determine how Alliaria might affect the performance of Microstegium. One possibility is that, due to their offset phenologies, co-occurrence in the same habitat may be beneficial for
both species and particularly damaging for resident native
species. An alternative possibility is that there might be disproportionate interactions among the species such that Alliaria
suppresses Microstegium over time. Both species change soil
properties in ways that appear to facilitate their own longterm dominance of invaded areas (Klironomos 2002; Lee,
Flory & Phillips 2012). Furthermore, although we found
strong evidence here that Alliaria can be facilitated by Microstegium, we did not investigate facilitation or competition
among Alliaria plants at different life-history stages (i.e.
rosettes and adults). Recent work has shown that intraspecific
competition among Alliaria plants early in the growing season
limits the establishment of rosettes in patches dominated
by adult plants (Bauer, Anderson & Anderson 2010). Adult
Alliaria plants are unlikely to be strong competitors with
Microstegium because adult Alliaria plants have largely completed their life cycle before Microstegium begins its most
active growth stage during late summer months. Future work
on these two highly invasive and widespread species should
investigate inter- and intraspecfic interactions of Alliaria and
Microstegium over greater temporal and spatial scales.
Our study demonstrates that Microstegium can inhibit resident plant communities and increase resource availability,
suggesting Microstegium indirectly facilitated Alliaria. Other
studies have suggested that such indirect facilitation may
occur if pairs of competitors compete for different resources
or utilize different mechanisms to acquire those resources
(Levine 1999). Our results suggest that indirect facilitation
may also occur if species have offset phenologies and compete for the same or similar resources at different times. Facilitation among invasive species has received increasing
attention as a mechanism for invasions (Simberloff & Von
Holle 1999; Mitchell et al. 2006), but there have been few
experimental demonstrations (Simberloff 2006). This is likely
due to the ethical concerns with introducing or manipulating
non-native invasive species in natural settings. However, if
experiments can be conducted where there is little risk of
increasing the spread of invasive species, such tests will help
to identify the mechanisms driving the establishment and
impacts of biological invasions and to develop effective ecosystem restoration strategies. Facilitation of Alliaria by Microstegium highlights the need for integrated ecosystem
management and studies that encompass multiple invasive
species across varying environmental conditions. The generality of this phenomenon is yet to be understood, but this study
is a clear demonstration that rapid response management of
plant invasions may preclude additional problems in future.
Acknowledgements
We thank Kurt Reinhart, Lauren Smith and Janet Morrison for reviewing an
earlier draft of this manuscript. Funding was provided in part by the Indiana
chapter of The Nature Conservancy and the University of Florida. The authors
declare that they have no conflict of interests.
References
Adams, S.N. & Engelhardt, K.A.M. (2009) Diversity declines in Microstegium
vimineum (Japanese stiltgrass) patches. Biological Conservation, 142, 1003–
1010.
Anderson, R.C., Dhillion, S.S. & Kelley, T.M. (1996) Aspects of the ecology
of an invasive plant, garlic mustard (Alliaria petiolata), in central Illinois.
Restoration Ecology, 4, 181–191.
Bartuszevige, A.M., Hrenko, R.L. & Gorchov, D.L. (2007) Effects of leaf litter
on establishment, growth and survival of invasive plant seedlings in a deciduous forest. American Midland Naturalist, 158, 472–477.
Bauer, J.T., Anderson, R.C. & Anderson, M.R. (2010) Competitive interactions
among first-year and second-year plants of the invasive, biennial garlic mustard (Alliaria petiolata) and native ground layer vegetation. Restoration Ecology, 18, 720–728.
Bauer, J.T. & Flory, S.L. (2011) Suppression of the woodland herb Senna
hebecarpa by the invasive grass Microstegium vimineum. American Midland
Naturalist, 165, 105–115.
Brooker, R.W., Maestre, F.T., Callaway, R.M., Lortie, C.L., Cavieres, L.A.,
Kunstler, G. et al. (2008) Facilitation in plant communities: the past, the
present, and the future. Journal of Ecology, 96, 18–34.
Callaway, R.M., Thelen, G.C., Rodriguez, A. & Holben, W.E. (2004) Soil biota
and exotic plant invasion. Nature, 427, 731–733.
Carino, D.A. & Daehler, C.C. (2002) Can inconspicuous legumes facilitate
alien grass invasions? Partridge peas and fountain grass in Hawai’i. Ecography, 25, 33–41.
Cushman, J.H., Lortie, C.J. & Christian, C.E. (2011) Native herbivores and
plant facilitation mediate the performance and distribution of an invasive
exotic grass. Journal of Ecology, 99, 524–531.
Engelhardt, M.J. & Anderson, R.C. (2011) Phenological niche separation from
native species increases reproductive success of an invasive species: Alliaria
petiolata (Brassicaceae) – garlic mustard. Journal of the Torrey Botanical
Society, 138, 418–433.
Fairbrothers, D.E. & Gray, J.R. (1972) Microstegium vimineum (Trin.) A.
Camus (Gramineae) in the United States. Journal of the Torrey Botanical
Society, 99, 97–100.
© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society, Journal of Ecology, 102, 12–18
18 S. L. Flory & J. T. Bauer
Flory, S.L. (2010) Management of Microstegium vimineum invasions and
recovery of resident plant communities. Restoration Ecology, 18, 103–112.
Flory, S.L. & Clay, K. (2010a) Non-native grass invasion alters native plant composition in experimental communities. Biological Invasions, 12, 1285–1294.
Flory, S.L. & Clay, K. (2010b) Non-native grass invasion suppresses forest
succession. Oecologia, 164, 1029–1038.
Fridley, J.D. (2012) Extended leaf phenology and the autumn niche in deciduous forest invasions. Nature, 485, 359–362.
Green, P.T., O’Dowd, D.J., Abbott, K.L., Jeffery, M., Retallick, K. & Mac
Nally, R. (2011) Invasional meltdown: invader-invader mutualism facilitates
a secondary invasion. Ecology, 92, 1758–1768.
Herold, J., Anderson, M.R., Bauer, J.T., Borowicz, V. & Anderson, R.C.
(2011) Comparison of the effect of early and late removal of second-year
garlic mustard (Alliaria petiolata) on first-year plants and deciduous forest
spring and summer dominant herbaceous groundlayer species in central Illinois, USA. Ecological Restoration, 29, 225–233.
Hughes, R.F. & Denslow, J.S. (2005) Invasion by a N-2-fixing tree alters function and structure in wet lowland forests of Hawaii. Ecological Applications,
15, 1615–1628.
Klironomos, J.N. (2002) Feedback with soil biota contributes to plant rarity
and invasiveness in communities. Nature, 417, 67–70.
Kuebbing, S.E., Nu~
nez, M.A. & Simberloff, D. (2013) Current mismatch
between research and conservation efforts: the need to study co-occurring
invasive plant species. Biological Conservation, 160, 121–129.
Lee, M., Flory, S. & Phillips, R. (2012) Positive feedbacks to growth of
an invasive grass through alteration of nitrogen cycling. Oecologia, 170,
1–9.
Levine, S.H. (1976) Competitive interactions in ecosystems. American Naturalist, 110, 903–910.
Levine, J.M. (1999) Indirect facilitation: evidence and predictions from a riparian community. Ecology, 80, 1762–1769.
Lortie, C.J., Brooker, R.W., Choler, P., Kikvidze, Z., Michalet, R., Pugnaire,
F.I. & Callaway, R.M. (2004) Rethinking plant community theory. Oikos,
107, 433–438.
Maron, J.L. & Connors, P.G. (1996) A native nitrogen-fixing shrub facilitates
weed invasion. Oecologia, 105, 302–312.
Marshall, J.M., Buckley, D.S. & Franklin, J.A. (2009) Competitive interaction
between Microstegium vimineum and first-year seedlings of three central
hardwoods. Journal of the Torrey Botanical Society, 136, 342–349.
McCarthy, B.C. (1997) Response of a forest understory community to experimental removal of an invasive nonindigenous plant (Alliaria petiolata Brassicaceae). Assessment and Management of Plant Invasions (eds J.O. Luken &
J.W. Thieret), pp. 117–130. Springer, New York.
Mitchell, C.E., Agrawal, A.A., Bever, J.D., Gilbert, G.S., Hufbauer, R.A., Klironomos, J.N. et al. (2006) Biotic interactions and plant invasions. Ecology
Letters, 9, 726–740.
Molina-Montenegro, M.A., Badano, E.I. & Cavieres, L.A. (2008) Positive interactions among plant species for pollinator service: assessing the ‘magnet species’ concept with invasive species. Oikos, 117, 1833–1839.
Morrison, J.A., Lubchansky, H.A., Mauck, K.E., McCartney, K.M. & Dunn, B.
(2007) Ecological comparison of two co-invasive species in eastern deciduous forests: Alliaria petiolata and Microstegium vimineum. Journal of the
Torrey Botanical Society, 134, 1–17.
Nuzzo, V.A. (1993) Distribution and spread of the invasive biennial garlic mustard (Alliaria petiolata) in North America. Biological Pollution: The Control
and Impact of Invasive Exotic Species. Proceedings of a symposium held at
Indianapolis, Indiana, USA 25-26 October 1991 (ed. B.N. McKnight), pp.
137–146. Indiana Academy of Science, Indianapolis, IN.
Nuzzo, V.A., Maerz, J.C. & Blossey, B. (2009) Earthworm invasion as the
driving force behind plant invasion and community change in northeastern
North American forests. Conservation Biology, 23, 966–974.
Orrock, J.L., Witter, M.S. & Reichman, O.J. (2008) Apparent competition
with an exotic plant reduces native plant establishment. Ecology, 89, 1168–
1174.
Oswalt, C.M., Oswalt, S.N. & Clatterbuck, W.K. (2007) Effects of Microstegium vimineum (Trin.) A. Camus on native woody species density and
diversity in a productive mixed-hardwood forest in Tennessee. Forest Ecology and Management, 242, 727–732.
Parker, J.D., Burkepile, D.E. & Hay, M.E. (2006) Opposing effects of native
and exotic herbivores on plant invasions. Science, 311, 1459–1461.
Reinhart, K.O., Maestre, F.T. & Callaway, R.M. (2006) Facilitation and inhibition of seedlings of an invasive tree (Acer platanoides) by different tree species in a mountain ecosystem. Biological Invasions, 8, 231–240.
Rodgers, V.L., Stinson, K.A. & Finzi, A.C. (2008) Ready or not, garlic mustard is moving in: Alliaria petiolata as a member of eastern North American
forests. BioScience, 58, 426–436.
Saccone, P., Pages, J.P., Girel, J., Brun, J.J. & Michalet, R. (2010) Acer negundo invasion along a successional gradient: early direct facilitation by native
pioneers and late indirect facilitation by conspecifics. New Phytologist, 187,
831–842.
Siemann, E. & Rogers, W.E. (2003) Changes in light and nitrogen availability
under pioneer trees may indirectly facilitate tree invasions of grasslands.
Journal of Ecology, 91, 923–931.
Simao, M.C.M., Flory, S.L. & Rudgers, J.A. (2010) Experimental plant invasion reduces arthropod abundance and richness across multiple trophic levels.
Oikos, 119, 1553–1562.
Simberloff, D. (2006) Invasional meltdown 6 years later: important phenomenon, unfortunate metaphor, or both? Ecology Letters, 9, 912–919.
Simberloff, D. & Von Holle, B. (1999) Positive interactions of nonindigenous
species: invasional meltdown? Biological Invasions, 1, 21–32.
Stinson, K., Kaufman, S., Durbin, L. & Lowenstein, F. (2007) Impacts of garlic
mustard invasion on a forest understory community. Northeastern Naturalist,
14, 73–88.
Tecco, P.A., Diaz, S., Gurvich, D.E., Perez-Harguindeguy, N., Cabido, M. &
Bertone, G.A. (2007) Facilitation and interference underlying the association
between the woody invaders Pyracantha angustifolia and Ligustrum lucidum.
Applied Vegetation Science, 10, 211–218.
USDA & NRCS (2013) The PLANTS Database (http://plants.usda.gov).
National Plant Data Team, Greensboro, NC, USA.
Von Holle, B., Joseph, K.A., Largay, E.F. & Lohnes, R.G. (2006) Facilitations
between the introduced nitrogen-fixing tree, Robinia pseudoacacia, and nonnative plant species in the glacial outwash upland ecosystem of cape cod,
MA. Biodiversity and Conservation, 15, 2197–2215.
Warren, R.J. II, Wright, J.P. & Bradford, M.A. (2011) The putative niche
requirements and landscape dynamics of Microstegium vimineum: an invasive
Asian grass. Biological Invasions, 13, 471–483.
Wundrow, E.J., Carrillo, J., Gabler, C.A., Horn, K.C. & Siemann, E. (2012)
Facilitation and competition among invasive plants: a field experiment with
alligatorweed and water hyacinth. PLoS One, 7, e48444.
Received 10 September 2013; accepted 29 October 2013
Handling Editor: Yvonne Buckley
Supporting Information
Additional Supporting Information may be found in the online
version of this article:
Table S1. Mixed model ANOVA results for the effects of Microstegium
invasion and disturbance on the number of Alliaria rosettes and
adults.
Table S2. Mixed model ANOVA results for the effects of Microstegium
invasion and disturbance on Alliaria adult biomass, height and silique
production.
© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society, Journal of Ecology, 102, 12–18