Journal of Ecology 2010, 98, 1379–1388 doi: 10.1111/j.1365-2745.2010.01722.

Invasion of Solidago gigantea in contrasting

experimental plant communities: effects on soil
microbes, nutrients and plant–soil feedbacks
Deborah Scharfy1*†, Sabine Güsewell1, Mark O. Gessner1,2 and Harry Olde Venterink1
1
Institute of Integrative Biology, ETH Zurich, Universitätstrasse 16, 8092 Zürich, Switzerland; and 2Department of
Aquatic Ecology, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Überlandstrasse 133, 8600
Dübendorf, Switzerland

Summary
1. Plant–soil feedbacks can influence the success of non-native plant invasions. We investigated if
these feedbacks and the underlying invasion effects on soil microbes and nutrients depend on the
species composition of the invaded vegetation, and whether these effects are related to differences in
the invasibility of native plant communities.
2. We carried out a mesocosm experiment simulating the invasion of Solidago gigantea into three
wetland plant communities (Molinion, Magnocaricion and Filipendulion), each composed of five
plant species but differing in productivity. To study plant–soil feedbacks, we used different soil inoc-
ulum types from invaded and non-invaded field sites of the corresponding communities and a refer-
ence site. Invasion success was assessed by measuring the biomass of S. gigantea after three growing
seasons and by analysing soil properties several times during the experiment.
3. Invasion success varied significantly among communities and soil inoculum types. Solidago
gigantea produced more biomass in the Molinion than in the two more productive communities. In
all three communities, it exhibited a negative feedback upon itself, producing 31–46% less biomass
when the substrate was inoculated with soil from a stand invaded with S. gigantea.
4. The presence of S. gigantea did not influence total biomass in any community nor N and P avail-
ability in soil. However, it led to a decrease in soil bacterial and an increase in soil fungal biomasses.
These changes were similar in the three communities and unrelated to the biomass of S. gigantea
biomass in the invaded communities.
5. Synthesis. The experimental comparison between effects of an invasive plant species on soil prop-
erties in different native communities showed similar effects despite pronounced differences in the
ability of the invasive species to grow in the different communities. In this system, plant–soil interac-
tions may thus affect invasion, but not explain differences in the invasibility of different communi-
ties. The invasive species increased soil fungal biomass, particularly in its own soil, compared to
native species and experienced a negative feedback, suggesting that the course of its invasion might
be affected by species-specific soil pathogens.
Key-words: bacterial biomass, enzyme activities, fungal biomass, invasion success, invasive
plants, plant communities, plant–soil (below-ground) interactions, plant–soil feedback, soil
properties, Solidago gigantea

Putten, Klironomos & Wardle 2007). Exotic plants can change

Introduction
Plant–soil interactions play a critical role in exotic plant
invasions of natural communities (Wardle et al. 2004; Van der
*Correspondence author. E-mail: deborah.scharfy@env.ethz.ch
†Present address: Agroscope Reckenholz-Taenikon Research Station,
Reckenholzstrasse 191, 8046 Zürich, Switzerland.
the composition and functioning of microbial communities,
alter soil food web structures and influence nutrient cycling
(Ehrenfeld 2003; Belnap et al. 2005; Hawkes et al. 2005;
Peltzer et al. 2009). These effects may arise from differences
between native and invasive species in functional traits such as
growth rate, or the quantity and quality of litter and root exu-
dates (Wardle et al. 2004; Bais, Broeckling & Vivanco 2008;

 2010 The Authors. Journal compilation  2010 British Ecological Society


1380 D. Scharfy et al.
Broeckling et al. 2008). It has been argued that invasive plants
are most likely to be successful and alter soil properties (biota
and nutrients) if they differ functionally from the native species
(Mack, D’Antonio & Ley 2001; Levine et al. 2003; Moles,
Gruber & Bonser 2008). Thus, invasion effects on soil condi-
tions are likely to depend upon the dissimilarity between the
native and invading plant species, but we are unaware of any
study that has rigorously investigated this hypothesis.
Effects of invasive plants on soil biota or nutrients may also
feed back on the invaders’ biomass production. There are vari-
ous accounts of positive feedbacks by which invasive plants
alter soil conditions in ways that stimulate their own produc-
tivity. Such conditions include altered nutrient availability
(Ehrenfeld 2003; Vinton & Goergen 2006; Dassonville et al.
2007) or the promotion of beneficial microbes such as mycor-
rhiza or nitrogen-fixing bacterial symbionts (Vitousek &
Walker 1989; Richardson et al. 2000; Klironomos 2002).
However, positive feedbacks appear not to be a prerequisite
for invasion success, since there are examples of negative feed-
back, caused, for example, by pathogens accumulating in the
soil and restraining the growth of successful invaders
(Beckstead & Parker 2003; Nijjer, Rogers & Siemann 2007).
This feedback will still favour the invader, however, if the
native vegetation experiences stronger growth restraints
(Eppinga et al. 2006; Mangla, Inderjit & Callaway 2008). The
greater the alterations in soil caused by an invader, the greater
the feedback that could be expected. In accordance, invasion
should be greater in communities less similar to the invader,
and changes in soil properties should therefore be related to
invasion success. Since site history and invasion effect are con-
founded in observational field studies, controlled experiments
are needed to test for such effects and feedbacks of invasive
and native plants.
The aim of our study was to assess the effects and feedback
of an exotic plant species invading native plant communities
differing in productivity. We chose Solidago gigantea as a
model species to simulate invasion in a mesocosm experiment.
This perennial forb native to North America frequently
invades wetland communities in Europe (Weber & Jakobs
2005) of both low and high productivity (Güsewell, Zuberbüh-
ler & Clerc 2005). Since S. gigantea is a fast-growing rhizoma-
tous forb with tall stem production (Jakobs, Weber &
Edwards 2004; Weber & Jakobs 2005), we expected it to be
more similar in relevant functional traits (e.g. quantity and
quality of litter) to native species of highly productive habitats
than to those of low productivity. Accordingly, we hypothe-
sized that:
1. Solidago gigantea increases biomass production at commu-
nity level and accumulates highest biomass when invading
the least productive and functionally less similar native
community.
2. By increasing carbon and nutrient turnover and hence
resource supply for microbial growth, S. gigantea alters
abiotic and biotic soil properties; this effect will be most
pronounced in the community where it produces the most
biomass.
 2010 The Authors. Journal compilation  2010 British Ecological Society, Journal of Ecology, 98, 1379–1388
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3. Alterations of biotic and abiotic soil properties will feed
back on the growth of S. gigantea. The nature of the feedback
could be positive since S. gigantea is more efficient at capturing
abundant nutrients than the native species. Alternatively, the
feedback could be negative, which might indicate that micro-
bial pathogens affect the native species more than S. gigantea.
Materials and methods
NATIVE PLANT COMMUNITIES
We studied S. gigantea as an invader of three wetland plant commu-
nity types which under natural conditions form a productivity gradi-
ent from mesotrophic Molinion to intermediate Magnocaricion to
eutrophic Filipendulion communities (Delarze, Gonseth & Galland
1999). The native plant species associated with these communities dif-
fer in their nutrient requirements, but all three communities can be
invaded by S. gigantea (Güsewell, Zuberbühler & Clerc 2005; Scharfy
et al. 2009). We assembled these plant communities experimentally in
mesocosms that were each represented by three native graminoids
and two native forbs (with three individuals per species). Characteris-
tic species used for the Molinion were Molinia caerulea (L.) Moench,
Carex panicea L., Anthoxanthum odoratum L., Succisa pratensis
Moench and Centaurea jacea subsp. angustifolia Gremli; for the
Magnocaricion they were Carex elata All., Calamagrostis epigejos (L.)
Roth, Phragmites australis (Cav.) Steud., Lythrum salicaria L. and
Mentha aquatica L.; for the Filipendulion they were Carex acutiformis
Ehrh., Phalaris arundinacea L., Alopecurus pratensis L., Filipendula
ulmaria (L.) Maxim. and Valeriana officinalis L.. Treating the inva-
sion process as an addition of a foreign plant to native vegetation, we
used an additive rather than a replacement design. In doing so, we
assumed that initial differences in plant density (18 and 15 plants in
the invaded and uninvaded communities, respectively) would not
produce notable treatment effects by the end of our 3-year study.
Most plants were raised from seeds and grown for ten weeks in a
greenhouse, but species that were difficult to germinate (Carex species
and Molinia caerulea) were collected in the field, separated into single
shoots, and kept in tap water until they had produced new roots, at
which point they were transplanted.
EXPERIMENTAL DESIGN
The experiment was set up in May 2006 in an experimental garden at
ETH Zurich, Switzerland (4724‘ N, 830‘ E, 520 m a.s.l.), and ran
for three growing seasons until July 2008. Each plant community was
grown with and without S. gigantea. In addition, three inoculum soil
types were used in growth substrate: invaded and native soils from
paired field sites and a native reference soil. Specifically, we used soil
from sites covered by Molinion (close to Chabrey: 4656‘ N, 659‘ E,
a gleysol), Magnocaricion (close to Yverdon: 4647‘ N, 641‘ E, a
gleysol) and Filipendulion communities (close to Zurich: 4728‘ N,
832‘ E, a calcaric to gleyic cambisol). At each of these sites, we col-
lected invaded soil from stands of S. gigantea and native soil in nearby
native vegetation without S. gigantea. We used these soils to inoculate
the substrate of our assembled communities. The paired sites for
native and invaded soil were less than 20 m apart to minimize differ-
ences in soil characteristics caused by factors other than S. gigantea
invasion. The native reference soil was collected at a site close to
Zurich (4722¢ N, 828¢ E, a calcaric cambisol). It showed aspects
of all three communities (i.e. presence of Molinia arundinacea,
Carex panicea, Lythrum salicaria, Filipendula ulmaria, and Carex

Invasion of Solidago gigantea in contrasting experimental plant communities 1381
acutiformis) and was not invaded by S. gigantea. This soil was used as
a standard soil inoculum in all three communities. For simplicity, we
refer hereafter to only three types of soil inocula (invaded, native, and
reference). Each treatment was replicated four times for each plant
community, resulting in a total of 72 experimental units.
Plastic buckets (35 L) were filled with 30 L of a mixture of 90%
sand (Carlo Bernasconi AG, Zurich, Switzerland, grain size
1–1.7 mm) and 10% soil (air-dried and sieved to pass through a
4-mm mesh prior to inoculation). Each of these mesocosms was
planted with three individuals per species, resulting in 15 individuals
in mesocosms without S. gigantea and 18 individuals in mesocosms
with S. gigantea. These 15 or 18 individuals were planted in three
concentric circles, so that all species occurred once on the outer,
intermediate and central circle, respectively. The arrangement of
the mesocosms was randomized twice during the duration of the
experiment.
Plants were watered with tap water and fertilized with nutrient
solutions every 2 weeks from June to September 2006 and from April
to October 2007. All mesocosms received the same amounts of nutri-
ents, 800 mg N in the first year and 1600 mg N in the second year.
The other nutrients were supplied in ratios of 0.7 (N:K), 3 (N:Mg),
3.4 (N:Ca), 10 (N:P), 25 (N:Fe). In 2007, we replaced the Ca(NO3)2
solution by NH4NO3 solution after measuring pH values > 7 in
some of the pots. Mesocosms were not fertilized in 2008, so that nutri-
ent contents would reflect the acquisition and retention of nutrients
given in 2006–2007. In particular, we wanted to determine if nutrient
availabilities were altered by the presence of S. gigantea.
VEGETATION PROPERTIES
The performance of S. gigantea and the native species in the different
plant communities was assessed in July 2008 by determining above-
ground biomass in each mesocosm. The above-ground material was
separated into the living shoots of each species and the pooled dead
biomass. Total below-ground biomass was determined in two of the
four replicate mesocosms. This fraction included roots of S. gigantea,
since it was impossible to separate roots by species. Samples were
dried at 75 C for 48–72 h, weighed and ground (1-mm mesh screen)
for nutrient analyses.
Nitrogen and phosphorus concentrations were determined after
Kjeldahl digestion in shoots of S. gigantea, in the combined above-
ground biomass of the native species, and the total below-ground
plant biomass. Subsamples of 150 mg were digested with concen-
trated H2SO4 and a K2SO4-CuSO4 tablet (FOSS Kjeltab) for 1 h at
420 C. Concentrations in the digests were determined spectrophoto-
metrically in a flow-injection analyser (FIAstar 5000, Foss Tecator,
Höganäs, Sweden).
SOIL PROPERTIES
Bacterial biomass in soil samples pooled from five cores taken in
November 2006 and June 2008 from each pot (0–10 cm depth, 1 cm
diameter) was determined by epifluorescence microscopy. Four
grams of fresh soil were preserved with 10 mL of a 2% formaldehyde
solution buffered with Na4P2O7 (3.8 mM). Samples were shaken and
sonicated (Branson Sonifier 250, SKAN AG, Basel, Switzerland) for
5 min to detach bacterial cells from soil particles (Buesing & Gessner
2002). Aliquots of the suspension were diluted (50-fold) and filtered
through a 0.2-lm membrane filter (Anodisc 25, Whatman Interna-
tional Ltd., Maidstone, UK). Cells trapped on the filter were stained
with 100 lL of 2.5% SYBR Green II solution (Molecular Probes,
Eugene, OR, USA) and examined at 1000-fold magnification under a
 2010 The Authors. Journal compilation  2010 British Ecological Society, Journal of Ecology, 98, 1379–1388
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microscope (Zeiss Axioskop 2, Carl Zeiss AG, Feldbach, Switzer-
land) with an attached camera system (Sensys Digital CCD, Photo-
metrics, AZ, USA). Fifteen microscopic fields were photographed per
filter and bacterial numbers and the area and circumference of each
cell determined with an image analysis programme (Metamorph
4.6r3, Universal Imaging Corporation, West Chester, PA, USA).
From these data we first calculated cell length and width, and then,
by assuming that cells were either rods or cocci, calculated their bio-
volumes (Bratbak 1993). Cell biovolumes were converted to bacterial
carbon (C) using the empirically determined relationship:
C = 89.6 · V0.59 (Simon & Azam 1989).
Fungal biomass was determined as ergosterol (Gessner & Schmitt
1996); this method is suited to determine soil fungal biomass but in
the presence of other fungi does not well reflect vesicular-arbuscular
mycorrhizas (Gessner & Newell 2002). Pooled samples from five soil
cores taken per pot in November 2006 and June 2008 were analysed.
Three grams of fresh soil were preserved with 10 mL of KOH in
methanol (143 mM). Samples were heated for 30 min in a water bath
at 80 C and subsequently allowed to cool. The extract was passed
over conditioned solid-phase cartridges (SepPak Vac RC tC18,
500 mg, Waters Corp., Milford, MA, USA) and rinsed with a wash-
ing solution (0.4 M KOH in methanol:H2O, 6:4 by volume). The car-
tridges were dried under a stream of air before ergosterol was eluted
with five portions of 0.35 mL isopropanol. The eluates were analysed
for ergosterol by HPLC (Jasco PU-980, Jasco GmbH, Gross-Ums-
tadt, Germany) with a RP-18 column (LiChroSpher 100, Merck Inc.,
Darmstadt, Germany). Methanol was used as the mobile phase and
ergosterol detected by measuring UV absorbance at 282 nm. Ergos-
terol concentrations in the soil samples were derived from standard
curves prepared with pure ergosterol (Fluka Chemie GmbH, Buchs,
Switzerland, > 98% purity). For further details of the method see
Gessner (2005). Ergosterol contents were converted to fungal carbon
contents by using a conversion factor of 5 mg ergosterol per gram
fungal dry mass (Gessner & Newell 2002) and assuming a fungal car-
bon content of 46% (Ruzicka et al. 2000). Both fungal and bacterial
biomasses are expressed in fungal and bacterial C contents (mg
microbial C per g soil C).
Enzyme activities of b-glucosidase, b-N-acetylhexosaminidase (for-
merly b-glucosaminidase) and acid phosphatase, which are involved
in the cycling of C, N and P, respectively (Miller & Dick 1995;
Olander & Vitousek 2000; Sinsabaugh et al. 2008), were measured in
samples pooled from five soil cores taken in July 2007 and July 2008
from each pot (0–10 cm depth, 1 cm diameter). Two g of fresh soil
were mixed in a centrifuge tube with 4 mL buffer (Tris, pH 6.0, or
Na-acetate-trihydrate, pH 5.5) and 1 mL of the appropriate substrate
analogue (25 mM p-nitrophenyl-b-d-glucopyranoside, 10 mM
p-nitrophenyl-N-acetyl-b-d-glucosamidine, or 10 mM p-nitrophenyl-
phosphate) according to Parham & Deng (2000). After shaking for
1 h, 1 mL of 0.5 M CaCl2 and 4 mL of alkaline buffer (Tris, pH 12,
or 0.5 M NaOH) were added. The tubes were then centrifuged for
5 min at 1479 g before measuring absorbance at 410 nm. Standard
solutions of p-nitrophenol spiked with 0.2 mL of 2 M NaOH were
used for calibration. The amount of p-nitrophenol released by the
enzymes was expressed in lmol h)1 g)1 fresh soil.
Concentrations of total phenolics were determined in soil as an
indicator of potentially inhibitory substances derived from plants.
Soil samples were taken after harvesting the above-ground biomass
in July 2008 and kept at 4 C until processed (three weeks). We used a
modified method of Swain & Hillis (1959). One g of fresh soil was
extracted by adding 5 mL of 50% ethanol and placing samples on a
shaker (300 r.p.m.) for 1 h. Samples were then centrifuged and a 3-
mL aliquot of the extract was diluted with 2 mL H2O and mixed with
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1382 D. Scharfy et al.

100 lL Folin–Ciocalteu-reagent. After 8 min, 300 lL of 2 M
Na2CO3 was added, and absorbance at 760 nm was measured after
1 h. Phenolic concentrations were determined with a standard curve
prepared with tannic acid and expressed as lg tannic acid equivalents
per g fresh soil.
Soil carbon concentrations were determined in air-dried soil sam-
ples (mix of five cores of 1 cm diameter, 10 cm depth, taken after the
harvest in July 2008), using a CN-analyser (CNS-2000, Leco Corp.,
St. Joseph, MI, USA). N and P availabilities in soil were determined
by measuring adsorption of nitrate, ammonium and phosphate to
ion-exchange resins (IER). Resins were exposed in soil in each meso-
cosm during successive 2-month intervals between April 2007 and
May 2008. For analysis, these successive measurements were subdi-
vided into two periods: a fertilized (April–June, June–August,
August–October, October–December) and an unfertilized period
(December–February, February–March, March–May). One 25-cm2
nylon bag per pot (60-lm mesh size, Sefar Nitex 03-60 ⁄ 35, Sefar AG,
Thal, Switzerland) containing IER was placed at about 5 cm below
the soil surface. Each bag contained 2 g mixed-bed IER (Amberlite
IRN 150, H+- and OH)-form, Sigma Aldrich, Switzerland). Before
exposure, IER bags were shaken twice for 30 min with 1 M KCl to
saturate exchange sites with K+ and Cl). After exposure, nutrients
were extracted from the IER by placing the bags in 50 mL of 0.5 M
HCl for 1 h on a shaker. Ammonium and nitrate in IER extracts were
analysed using a flow injection analyser (FIAstar 5000). Phosphate
concentrations were determined in the IER extracts by the ascorbic
acid-molybdate blue method (Murphy & Riley 1962) and measuring
absorbance at 880 nm on a spectrophotometer (Uvi Light XT2, Seco-
mam, Ales, France).
DATA ANALYSIS
during the experiment (cf. Table 2). Variables were log-transformed
prior to analyses if necessary to meet assumptions of parametric tests.
All analyses were performed with JMP 7.0.1 (SAS Institute Inc., NC,
USA).
Results
GROWTH OF S. GIGANTEA AND NATIVE PLANTS IN THE
EXPERIMENTAL PLANT COMMUNITIES
Native species from the Molinion community produced the
least total biomass, those from the Magnocaricion community
were intermediate, and those from the Filipendulion commu-
nity produced the most total biomass (Fig. 1a, white bars).
Differences in biomass production were particularly
pronounced for the roots (see Table S1 in Supporting infor-
mation).
Solidago gigantea produced significantly more shoot bio-
mass in the low-productivity Molinion than in the Magnocari-
cion and Filipendulion community (Fig. 1b). This difference
was particularly apparent for the mesocosms that received the
native reference soil inoculum (white bars) and the native soil
of the different communities (grey bars). Similarly, the N pool
in S. gigantea shoots was substantially higher in the Molinion
than in the Magnocaricion and Filipendulion communities,
whereas the P pool in S. gigantea shoots did not differ among
communities (Table 1). Solidago gigantea did not affect the
total biomass production in any community or soil type
(Fig. 1a, Table 1)

Most vegetation and soil data were analysed by three-way analysis of

variance, with invasion, plant community type and soil inoculum type
as factors (cf. Table 1, 2). The effects of plant community type and
soil inoculum type on the performance of S. gigantea were analysed
by two-way anova (cf. Table 1). Soil N and P availabilities were analy-
sed separately by means of repeated-measures anova for fertilized
(four measurements) and unfertilized (three measurements) periods
EFFECTS OF S. GIGANTEA ON SOIL BIOTA, ENZYME
ACTIVITIES AND NUTRIENTS
The effects of S. gigantea on abiotic and biotic soil properties
were generally not significantly different between the three
plant communities (Table 2, hardly any significant I · C

Table 1. Effects of invasion by Solidago gigantea, plant community type, soil inoculum type, and interactions of these factors on characteristics
of the native species and total plant community (three-way anova), as well as effects of plant community type and soil inoculum type on
characteristics of S. gigantea (two-way anova). F-values and significance levels are indicated for each effect (*P < 0.05, **P < 0.01,
***P < 0.001). Significant effects relating to S. gigantea are in bold (P < 0.01). Three-way interactions are not shown; none of them was
significant (P > 0.1)

Plants Variable Invasion (I) Community (C) Soil (S) I·C I·S C·S

Native species Shoot biomass 34.2*** 52.3*** 29.1*** 1.31 0.27 6.97***
Native species Shoot N pool‡ 112.5*** 83.2*** 42.3*** 4.56* 1.82 7.36***
Native species Shoot P pool 15.7*** 139.4*** 8.52*** 1.03 0.24 6.89***
Whole community† Shoot biomass 1.86 38.8*** 26.2*** 0.36 1.92 5.57***
Whole community† Root biomass‡ 0.03 49.9*** 8.73** 0.36 0.78 1.49
Whole community† Total biomass‡ 0.00 36.5*** 8.29** 0.48 1.26 1.44
Whole community† Total N pool 0.06 26.1*** 6.48** 0.17 1.88 0.81
Whole community† Total P pool 1.74 10.7*** 1.01 0.05 0.24 1.10
S. gigantea Shoot biomass 13.5*** 6.00** 2.07
S. gigantea Shoot N conc 8.63** 0.11 1.83
S. gigantea Shoot N pool 8.48** 6.88** 2.37
S. gigantea Shoot P conc 8.93** 3.67* 2.20
S. gigantea Shoot P pool ‡ 3.54* 6.41** 1.82

†Includes S. gigantea.
‡ Variables were log-transformed prior to analysis.

 2010 The Authors. Journal compilation  2010 British Ecological Society, Journal of Ecology, 98, 1379–1388
 Table 2. Microbial, enzymatic and nutritional soil properties in the mesocosm experiment as affected by Solidago gigantea, the native plant communities and soil inoculum type. Means ± SE for invaded and
uninvaded communities are shown ()S. gigantea, +S. gigantea, calculated from replicate means), in combination with three-way anova results for the treatment effects as well as factorial interactions.
Different letters behind means indicate significant differences according to Tukey’s post hoc test (a = 0.05). F-values and significance levels are indicated for each effect (*) P < 0.1,* P < 0.05, **P < 0.01,
*** P < 0.001). Significant effects relating to S. gigantea are in bold (P < 0.01)

Means ± SE Means ± SE
Year of ) S. gigantea +S. gigantea
Soil property assessment (n = 9) (n = 9) Invasion (I) Community (C) Soil (S) I·C I·S C·S I·C·S

Bacterial biomass (mg C g)1 soil Corg) 2006 10.9 ± 0.6 11.6 ± 0.9 0.76 2.81 2.06 0.02 0.43 3.32* 0.98
2008 16.7 ± 1.2a 14.3 ± 0.8b 7.86** 12.54*** 0.50 1.13 0.09 1.97 0.93
Fungal biomass (mg C g)1 soil Corg)† 2006 46.5 ± 8.2 40.7 ± 6.8 2.13 3.38* 38.97*** 2.20 0.27 7.66*** 3.05*
2008 16.0 ± 2.1b 19.5 ± 2.2a 5.71* 10.03*** 9.32** 0.06 4.94* 2.92* 0.78
Fungal:Bacterial biomass ratio† 2006 4.55 ± 0.9 3.78 ± 0.6 4.02 5.22** 31.84*** 1.84 0.03 10.24*** 1.91
2008 0.99 ± 0.10b 1.45 ± 0.14a 12.81*** 0.74 7.59** 0.16 3.00 2.58* 1.30
b-glucosidase (lM g)1 soil h)1)† 2007 0.90 ± 0.07b 1.05 ± 0.05a 8.45** 11.66*** 2.25 2.47 0.09 3.86** 0.71
2008 1.15 ± 0.05 1.24 ± 0.09 0.68 0.78 5.03** 0.40 0.41 0.89 0.45
b-N-acetylhexosaminidase (lM g)1 soil h)1)† 2007 0.35 ± 0.02 0.33 ± 0.02 1.35 13.48*** 1.63 2.41 0.74 2.18 0.98
2008 0.72 ± 0.13 0.74 ± 0.07 0.83 14.63*** 2.54 0.15 0.80 2.90* 0.63
Acid phosphatase (lM g)1 soil h)1) 2007 3.14 ± 0.28 3.09 ± 0.15 0.10 16.16*** 2.56 5.07** 0.06 0.86 0.35
2008 3.23 ± 0.16 3.03 ± 0.20 1.94 8.38*** 0.81 0.13 1.62 3.84** 0.06
Phenolics (lg g)1 soil)† 2008 81.9 ± 8.9 81.9 ± 4.6 0.72 7.33** 0.93 1.55 0.98 0.37 0.81
Soil organic C (mg g)1 soil) 2008 2.09 ± 0.10 2.28 ± 0.09 3.82(*) 21.67*** 3.82* 0.69 0.67 4.11** 0.54
N availability in fertilized periods (lg g)1 IER)‡ 2007 488.5 ± 73.2 567.9 ± 70.7 1.93 7.06** 6.97** 2.01 2.58(*) 3.04* 0.33
N availability in unfertilized periods (lg g)1 IER)‡ 2008 16.9 ± 1.7 14.8 ± 1.5 1.20 3.02(*) 2.77(*) 0.88 1.85 0.91 0.62
P availability in fertilizced periods (lg g)1 IER)‡ 2007 74.7 ± 6.7 86.5 ± 8.3 3.37(*) 6.76** 8.11*** 0.75 3.34* 1.56 0.17
P availability in unfertilized periods (lg g)1 IER)‡ 2008 4.37 ± 0.48 5.12 ± 0.96 0.96 4.46* 4.12* 3.07(*) 0.32 0.71 1.14

 2010 The Authors. Journal compilation  2010 British Ecological Society, Journal of Ecology, 98, 1379–1388
†Variables were log-transformed prior to analysis.
‡Analysed with repeated-measures anova, including four measurements during the fertilized period and three measurements during the unfertilized period.
IER, Ion-exchange resin.
Invasion of Solidago gigantea in contrasting experimental plant communities 1383

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1384 D. Scharfy et al.

(a) 800 Solidago gigantea increased b-glucosidase activity in soil in

without S. gigantea
with S. gigantea 2007, but a year later this effect was no longer evident
600 (Table 2). Solidago gigantea did not affect b-N-acetylhexosa-
Total biomass (g)

minidase activity, and phosphatase activity was not influenced

400
either besides the mentioned interaction effect (i.e. increase in
the Filipendulion, decrease in the two other plant communities)
in 2007 (Table 2).
200
Solidago gigantea increased soil carbon concentration by
10% on average, but this difference was not a large enough to
0
Molinion Magnocaricion Filipendulion be significant (P = 0.056, Table 2). Solidago gigantea also
(b)
30
increased soil P availability in soil inoculated with native and
invaded soil by 30% (371 vs. 285 and 433 vs. 332 lg g)1 IER),
S. gigantea shoot biomass (g)

Reference soil
Native soil but decreased it in the reference soil by 17% (233 vs.
20
Invaded soil 280 lg g)1 IER). This interaction was observed only in the fer-
tilized period, however, whereas P availability in the unfertil-
ized period was not affected by S. gigantea (Table 2). Solidago
10 gigantea did not significantly affect soil N availabilities or phe-
nolic concentrations (Table 2).

0
Molinion Magnocaricion Filipendulion
EFFECT OF SOIL INOCULUM ON PLANT GROWTH: WAS
(c) 100 THERE A FEEDBACK?
Reference soil
Native soil We found evidence that growth of S. gigantea was affected by
Native community shoot

75 Invaded soil
a negative plant–soil feedback: shoot biomass of S. gigantea
biomass (g)

was 31–46% lower in mesocosms inoculated with invaded soil

50
25
0 did not differ in shoot biomass production (Fig. 1c), or N
Molinion
Fig. 1. Biomass production of plants in the Molinion, Magnocaricion
and Filipendulion communities: (a) total plant biomass with Solidago
gigantea present or absent (n = 3); (b) above-ground biomass of
S. gigantea in the three plant communities (n = 4); (c) above-ground
biomass of the native species within the three communities (n = 4,
S. gigantea absent). Shown are means + SE, calculated from
replicate means, except for S. gigantea biomass (b; calculated from all
treatments).
than in mesocosms with inoculum from uninvaded native soil
(comparison of grey and black bars in Fig. 1b), and the uptake
of N and P was 26–48% lower (see Table S1). The native spe-
cies growing in soil inoculated with either native or invaded soil
Magnocaricion Filipendulion
and P uptake (see Table S1). Plant growth of the native plants
differed between native reference soil and native soil (Fig. 1c,
comparison of white and grey bars), possibly indicating nega-
tive feedback for the native species as well, since the reference
soil was collected at another site and probably harbouring a
distinct microbial community.
Discussion

EFFECTS OF S. GIGANTEA IN DIFFERENT NATIVE

interactions). A significant interaction was only found for
phosphatase activity in 2007, which was decreased by the pres-
ence of S. gigantea in the Filipendulion, and increased in the
other two communities. Overall, S. gigantea reduced bacterial
biomass, increased fungal biomass and also increased the fun-
gal-to-bacterial ratio after three growing seasons in 2008
(Table 2). Within communities, as assessed by a priori con-
trasts, bacterial biomass was reduced by S. gigantea only in the
Filipendulion (Fig. 2a), while the increases in fungal biomass
were not significant (Fig. 2c). Yet, the increases in fungal-to-
bacterial ratio were significant within two of the three commu-
nities, Molinion and Filipendulion (Fig. 2e). While S. gigantea
did not decrease bacterial biomass within any soil type accord-
ing to the a priori contrasts (Fig. 2b), it increased fungal
biomass markedly in the invaded soil (Fig. 2d) and increased
the fungal-to-bacterial ratio in two of the three soil types
(Fig. 2f).
 2010 The Authors. Journal compilation  2010 British Ecological Society, Journal of Ecology, 98, 1379–1388
COMMUNITIES
Despite the fact that native communities and S. gigantea
within the communities differed in biomass production as
anticipated, the effects of S. gigantea on biotic and abiotic soil
properties were mostly similar in the three plant communities.
Hence, our results do not support our main hypothesis; i.e. we
did not observe that S. gigantea had a stronger effect on soil
properties when invading in a community with plants that had
different rather than similar traits (Molinion and Filupendulion
species, respectively).
The relative contribution of S. gigantea to above-ground
total plant biomass was considerably higher in the Molinion
(32%) than in the other communities (15–19%). Hence, inva-
sion success of S. gigantea as measured by final shoot biomass
was greatest in the least productive community as predicted,
though not clearly least in the most productive community.
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Invasion of Solidago gigantea in contrasting experimental plant communities 1385

(a) (b)
30 30

Bacteria (mg C g–1 soil Corg)

Bacteria (mg C g–1 soil Corg)
Without S. gigantea
With S. gigantea
ns ns
20 * 20
ns ns
ns

10 10

0 0
Molinion Magnocaricion Filipendulion Reference soil Native soil Invaded soil

(c) (d)
30 30
ns ns

Fungi (mg C g–1 soil Corg)

Fungi (mg C g–1 soil Corg)

***
ns
20 20
ns ns

Fig. 2. Effects of Solidago gigantea on soil 10 10

bacterial and fungal biomass as well as on
ratios of fungal-to-bacterial biomass: in
mesocosms with the experimental Molinion, 0 0
Molinion Magnocaricion Filipendulion Reference soil Native soil Invaded soil
Magnocaricion and Filipendulion communi-
ties (a, c, e) and inoculated with the (e) (f)
2 2
reference, native and invaded soil inoculum ***
ns ns
Fungal/Bacterial ratio

types (b, d, f). Shown are means + SE

Fungal/Bacterial ratio
(n = 3, calculated from replicate means). 1.5 * 1.5
Results for the community · invasion inter- * *
action and soil type · invasion interaction 1 1
are from a priori contrasts based on
within-community and within-soil type data. 0.5 0.5
Significance levels are indicated for each
effect (ns > 0.05, *P < 0.05, **P < 0.01, 0 0
***P < 0.001). Molinion Magnocaricion Filipendulion Reference soil Native soil Invaded soil

This pattern agrees with field observations from wetlands in
Switzerland, where S. gigantea could replace Molinion commu-
nities, but only reached up to 50% cover in Filipendulion com-
munities (Güsewell, Zuberbühler & Clerc 2005). We can not
infer S. gigantea’s success in the communities from its impact
on the soil, since the impact was similar across all three
communities. Its success reflects the competitive strength of
S. gigantea in comparison with the native plant species under
our experimental conditions.
Initial differences in plant individuals in the experiment
between communities with and without S. gigantea could have
influenced community development and competitive interac-
tions. Since biomass production of invaded and uninvaded
communities was not reduced, our a priori assumption was
supported that natural plant expansion and replacement pro-
cesses during the course of the experiment would weigh out
any initial differences in plant density.
A NEGATIVE PLANT–SOIL FEEDBACK
Solidago gigantea grew worse in sand inoculated by soil that
previously had been in contact with this species in comparison
to soil of native species (Fig. 1). Negative plant–soil feedbacks
have also been reported for other exotic invading plants
(Beckstead & Parker 2003; Knevel et al. 2004; Nijjer, Rogers
& Siemann 2007), but this is the first report for a Solidago
species. Bever, Westover & Antonovics (1997) postulated two
mechanisms of negative feedbacks by altered plant–soil
microbe interactions which would assume either (i) stronger
negative effects by pathogens on S. gigantea than on its native
competitors, or (ii) stronger growth stimulation by S. gigantea
of the mutualists of the native species than of its own mutual-
ists. The first mechanism is more likely than the second since
biomass of the native species was not affected by inoculation
with invaded soil (Fig. 1c). Negative feedbacks as observed in
our experiment have been related to fungal pathogens for sev-
eral plants (Mills & Bever 1998; Packer & Clay 2000; Bezemer
et al. 2006), including invasive species (Beckstead & Parker
2003; Nijjer, Rogers & Siemann 2007). Since S. gigantea
increased soil fungal biomass markedly in the invaded soil of
our experiment compared to the native species and the growth
of native species was not affected in the invaded soil, it is
conceivable that S. gigantea accumulated fungal pathogens,
possibly even species-specific ones, that restrained its growth.
A negative feedback through stimulation of S. gigantea-spe-
cific pathogens can not explain per se why this species is a
successful invader in European wetlands; this would require an
even greater negative impact of pathogens on the native plants,
which we did not observe (Fig. 1c). Are there other
mechanisms that could reconcile negative feedbacks with
invasiveness? One possibility is based on the observation that
negative feedbacks generally play a significant role in limiting
the density of a given species within an area (Bever, Westover
& Antonovics 1997; Packer & Clay 2000; Kulmatiski et al.
2008), and can encourage the expansion of clonal plants to
new, pathogen-free soil (Van der Putten, Van Dijk & Peters

 2010 The Authors. Journal compilation  2010 British Ecological Society, Journal of Ecology, 98, 1379–1388

1386 D. Scharfy et al.
1993; Bever 1994; Bonanomi et al. 2005) when the plants fail
to control pathogens in place (Van der Putten et al. 2001).
That pathogens involved in plant growth reduction can be part
of the invasion mechanism is counterintuitive, but conceivable
and could apply to S. gigantea, which forms large clonal net-
works.
The negative feedback observed for S. gigantea could have
been enforced by interspecific competition from native species
(Bever 2003). Inclusion of S. gigantea monocultures in our
experiment would have enabled us to test this possibility. Nev-
ertheless, the negative feedback we observed was apparent
across all three plant communities, and particularly when
S. gigantea competed with the slow-growing species of the
Molinion community. This suggests that the reduced growth of
S. gigantea exposed to invaded soil was more likely a soil-based
than a competition effect.
The negative feedbacks in S. gigantea might be particularly
strong under rather nutrient-poor conditions, as in our experi-
ment, and could be masked under nutrient-rich conditions.
For instance, Gustafson & Casper (2004) found that negative
plant–soil feedbacks could be neutralized by nutrient addition.
The negative feedback as an influencing factor in S. gigantea
invasion could therefore be of particular importance when S.
gigantea invades communities of nutrient-poor sites, such as
the Molinion, whereas other factors such as competitive traits
could be more important when S. gigantea invades communi-
ties of nutrient-rich sites, such as the Filipendulion. In favour of
this hypothesis would speak that S. gigantea appears to form
less compact and less well-defined stands in poor than in rich
sites (personal observation).
SOLIDAGO GIGANTEA AFFECTED SOIL MICROBIAL
COMMUNITIES
The observed shifts in bacterial and fungal biomasses induced
by S. gigantea in our experiment could be due to several mech-
anisms, four of which we discuss below:
1. Plant-mediated change in the quantity and quality of organic
carbon. Soil fungi have been found to be promoted when C is
supplied as cellulose or acetic acid, whereas bacteria profit
from glucose, glycine, starch and gelatine (Van der Wal et al.
2006; Meidute, Demoling & Bååth 2008; Rinnan & Bååth
2009). Solidago gigantea indeed increased the soil C concentra-
tion in both field conditions (Scharfy et al. 2009) and our
experiment, although this effect was only marginally signifi-
cant. Excretion of compounds by S. gigantea that preferen-
tially favour fungal growth (e.g. acetic acid) hence is a possible
mechanism accounting for the observed microbial community
shift (Rinnan & Bååth 2009), but we have insufficient data to
assess whether this was important in our experiment.
2. Plant-induced changes in soil nutrient levels or stoichiometry.
As fungi produce more biomass per unit nutrient (N or P) than
bacteria, high C:N, C:P and N:P ratios in soil favour fungal
over bacterial growth (Joergensen & Wichern 2008; Güsewell
& Gessner 2009). However, since S. gigantea did not signifi-
cantly influence soil N or P availabilities, and did not affect
 2010 The Authors. Journal compilation  2010 British Ecological Society, Journal of Ecology, 98, 1379–1388
13652745, 2010, 6, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/j.1365-2745.2010.01722.x by Cochrane Philippines, Wiley Online Library on [21/01/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
activities of N or P acquiring enzymes (i.e. b-N-acetylhexosa-
minidase and acid phosphatase) in the soil, changes in soil
nutrient levels or stoichiometry were unlikely to be a key factor
in our experiment.
3. Accumulation of root pathogens. As discussed above, S. gi-
gantea may have induced an accumulation of fungal pathogens
(Mills & Bever 1998; Van der Putten et al. 2001). It is impor-
tant to note in this context that vesicular-arbuscular mycor-
rhiza (VAM) was highly unlikely to account for the increased
fungal biomass we observed, since VAM fungi typically con-
tain only low amounts of ergosterol, which we used as an indi-
cator of fungal biomass.
4. Root exudation of antibacterial compounds. We cannot rule
out that specific antibacterial or fungus-stimulating root
exudates influenced the observed shift from bacterial to fungal
biomass in the presence of S. gigantea. However, although
shoots of S. gigantea are known to contain secondary plant
compounds (sesquiterpenes) with antimicrobial and antiherbi-
vore activity (Kalemba & Thiem 2004; Johnson, Hull-Sanders
& Meyer 2007), we are not aware of reports suggesting antimi-
crobial activities of the roots or rhizomes of this plant.
SYNTHESIS: A POSSIBLE INVASION MECHANISM BY
S. GIGANTEA
A plant-induced shift in soil microbial communities, as
observed for bacteria and fungi in the present experiment, can
play a major role in the invasion of plant species (Wardle et al.
2004; Van der Putten, Klironomos & Wardle 2007). The mech-
anisms and impacts obviously depend largely on the identity of
the affected microbes (e.g. whether soil pathogens or mutual-
ists are involved). We propose a number of arguments that
point to fungal pathogens, possibly species-specific, being stim-
ulated by S. gigantea. These arguments include the negative
plant–soil feedback we observed, increased soil fungal biomass
in the presence of S. gigantea, higher fungal biomass in the
‘invaded’ soil, and the lack of effect of the latter on native
species.
We propose the following hypothetical invasion mechanism
for S. gigantea in European wetlands, which involves a cascade
of ecological processes: (i) Solidago gigantea increases soil C,
(ii) the increased C stimulates fungal growth at the expense of
bacteria because either the type of C compounds or an altered
C:N:P stoichiometry favours fungi over bacteria, (iii) these
fungi (presumably pathogens) induce a negative feedback on
the growth of S. gigantea but do not harm the competing
native species (Fig 2), (v) the pathogens stimulate S. gigantea
to form longer rhizomes and expand its area, thereby promot-
ing its invasion into adjacent native vegetation. The first three
mechanisms are supported by the present experiment and
previous studies (Vanderhoeven et al. 2006; Scharfy et al.
2009), whereas the fourth is only a suggestion, as we are not
aware of studies demonstrating effects of soil pathogens on rhi-
zome growth. However, it is known that pathogens can affect
a plant’s morphology through effects on the production and
distribution of growth hormones (Lopéz, Bannenberg &

Invasion of Solidago gigantea in contrasting experimental plant communities 1387
Castresana 2008), so that effects on rhizome growth would be
possible.
Clonal expansion is a strategy described for many invasive
plants (Thompson, Hodgson & Rich 1995; Küster et al. 2008)
and increases in soil organic carbon have often been observed
in response to plant invasions (Scott, Saggar & Mc Intosh
2001, Fickbohm & Zhu 2006, Heneghan et al. 2006, Vila et al.
2006). However, we are not aware of any study linking clonal
expansion and modification of soil organic carbon into the
suggested negative plant–soil feedback mechanism. We pro-
pose that this mechanism is worth testing for S. gigantea and
other clonal invasive plants in order to understand their inva-
sion success in varying habitats.
Acknowledgements
We are grateful to the managers of two wetland conservation areas for permis-
sion to take soil samples (Groupe d¢étude et de gestion – Grande Cariçaie, and
Fachstelle Naturschutz Zürich – Flachmoor Winkler Allmend). We thank Rose
Trachsler, Britta Jahn-Humphrey, Marilyn Gaschen and Daniel Steiner for
assistance with laboratory analyses, and Martin Fotsch, Sara C. Bischof and
Monika Kuster for help in maintaining the experiment and data collection. The
manuscript was improved by comments of Peter J. Edwards, the Handling Edi-
tor and three anonymous reviewers. This research was funded by the Swiss
National Science Foundation through grant 2-77669-05.
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Received 19 November 2009; accepted 3 August 2010
Handling Editor: Peter Alpert
Supporting Information
Additional supporting information may be found in the online
version of this article:
Table S1. Comparison of biomass and nutrient characteristics of Soli-
dago gigantea and native species within the Molinion, Magnocaricion
and Filipendulion communities.
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