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Keywords:

  • allelopathy;
  • exotic invasive plants;
  • functional groups;
  • functional traits;
  • litter decomposition;
  • nutrients;
  • plasticity

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information
  • Exotic plant invasions can alter ecosystem processes, particularly if the invasive species are functionally different from native species. We investigated whether such alterations can be explained by differences in functional traits between native and invasive plants of the same functional group or by differences in functional group affiliation.
  • We compared six invasive forbs in Europe with six native forbs and six native graminoids in leaf and whole-plant traits, plasticity in response to nutrient supply and interspecific competition, litter decomposition rate, effects on soil nutrient availability, and allelopathy. All traits were measured in a series of pot experiments, and leaf traits additionally in the field.
  • Invasive forbs differed from native forbs for only a few traits; they had less leaf chlorophyll and lower phosphorus (P) uptake from soil, but they tended to have a stronger allelopathic effect. The invasive forbs differed in many traits from the native graminoids, their leaves had lower tissue densities and a shorter life span, their litter decomposed faster and they had a lower nitrogen-use efficiency.
  • Our results suggest that invasive forbs have the potential to alter ecosystem properties when invading graminoid-dominated and displacing native graminoids but not when displacing native forbs.

Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

Functional traits determine the ecological strategy of plants, their response to site conditions and their influence on ecosystems (Lavorel & Garnier, 2002; Garnier et al., 2007; Suding et al., 2008). The study of functional traits therefore plays an important role in research on the ecology of exotic plant invasions. While many external factors contribute to the spread and establishment of invasive plants (e.g. human dispersal, vegetation disturbance, nutrient enrichment), the trait equipment of plant species is crucial for their impact on vegetation and ecosystem properties (Wardle et al., 1998; Levine et al., 2003; McIntyre et al., 2005). The comparison of traits between coexisting invasive and native plant species can therefore help understanding success of invasion and its impact (Thompson et al., 1995; Funk & Vitousek, 2007).

Associations between plant functional traits and either invasiveness or invasion impact have been reported in many studies (McIntyre et al., 2005; Küster et al., 2008). However, there are also studies that found no relationship (Hastwell & Panetta, 2005). Many traits may contribute to successful invasion (life form, phenology, seed size, polyploidy level etc.) and the significance of individual traits is often context-dependent or species-specific (Thompson et al., 1995; Moles et al., 2008). In particular, traits promoting high reproduction rates and rapid spread are decisive for the colonization of open habitats while those promoting fast growth and resource acquisition are most important for the ability to establish, dominate and displace the resident vegetation (Lavorel & Garnier, 2002; Dietz & Edwards, 2006). Therefore, the most successful invaders are often species with high specific leaf area (SLA), high relative growth rates and high nutrient turnover (Smith & Knapp, 2001; Hamilton et al., 2005; Leishman et al., 2007); these traits are characteristic of a competitive–ruderal strategy in the sense of Grime (2001). Invaders therefore tend to have an advantage over native species under high nutrient supply (Kolb et al., 2002; Rickey & Anderson, 2004; Blumenthal & Hufbauer, 2007), whereas nutrient-poor conditions do not generally favour plant invasions.

Phenotypic plasticity in functional traits can allow invasive plants to benefit from changing environmental conditions, either by greatly increasing their performance under resource-rich conditions or by maintaining their performance under resource-poor conditions (Richards et al., 2006). Some studies found invasive species to be particularly successfully in acquiring and using nutrients under nutrient-poor conditions (Funk & Vitousek, 2007; Muth & Pigliucci, 2007). More often, however, invasive species showed a more plastic response to nutrient enrichment than native species (Milberg, 1999). A possible reason is higher root plasticity, which allows for a more rapid capture of nutrients in soil (Callaway et al., 2003).

The effects of invasive plants on the soil are also variable. Invasive species have often been found to increase soil nutrient availability (Allison & Vitousek, 2004; Vanderhoeven et al., 2005; Dassonville et al., 2007; Rodgers et al., 2008), to exert allelopathic effects (Callaway et al., 2005; Jarchow & Cook, 2009) or to alter the soil microbial community (Belnap et al., 2005), but none of these effects is ubiquitous. Effects on the soil are most likely to occur if invasive plants are functionally different from the native vegetation, especially in terms of litter production, root properties and secondary chemistry (Mack et al., 2001; Levine et al., 2003; Moles et al., 2008).

The role of differences in functional traits for the success of invasive plants and their impacts on ecosystems is partly confounded by the fact that exotic plant invaders often belong to a different functional type than the native vegetation. For example, in Central Europe, the most successful herbaceous plant invaders are annual or perennial forbs (Pyšek et al., 2009), whereas the native herbaceous vegetation is often dominated by perennial graminoids. This implies that functional differences between dominant native and invasive species may just reflect their belonging to different functional types. For example, even though grasses are often highly competitive under nutrient-rich conditions, they generally have tougher leaves than forbs, with a longer life span and lower litter decomposition rates (Cornelissen & Thompson, 1997; Grime et al., 1997; Craine et al., 1999; Dorrepaal et al., 2005). These inherent functional differences must be taken into account in the evaluation of invasion effects. The comparison of exotic forbs with native forbs might underestimate the potential impact of invaders on ecosystems that are naturally dominated by graminoids, whereas the comparison of exotic forbs with dominant native graminoids might overstate the relevance of their functional differences for competitive interactions. It thus seems important to compare plant invaders with native species of both groups to properly assess how different they are.

In this study, we compared major invasive forbs in Switzerland with potentially dominant native forbs and graminoids for functional traits, plasticity and effects on soil under controlled conditions. We cultivated six plants from each group in pots at low and high nutrient supply, either alone or in competition. With these 18 species, we tested the following hypotheses which might contribute to explaining the success of the invaders.

Invasive forbs differ from native species in having functional traits that are more typical of a competitive–ruderal strategy, which allow more efficient resource acquisition or use; they differ more from native graminoids than from native forbs in this respect. Invasive forbs are more plastic than native species in response to variation in nutrient supply (i.e. their biomass production and their competitive ability increase more with increasing nutrient supply); they differ less from dominant native graminoids than from (mostly not dominant) native forbs in this respect. Invasive species increase soil nutrient availability but inhibit the growth of native species through allelopathic effects; they differ more from native graminoids than from native forbs in this respect.

Materials and Methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

Investigated plant species

The invasive species selected for our study are abundant throughout the lowlands in Switzerland. They included three perennial forbs and three annual forbs (Table 1). Exotic graminoids were not included in the study, because they play a minor role as plant invaders in Switzerland; for example, no graminoid appears on the ‘black list’ of noxious plant invaders in Switzerland (http://www.cps-skew.ch/english/invasive_alien_plants/black_list_watch_list.html). The 12 native species were chosen to be dominant or at least abundant in the natural vegetation at moist to wet sites in northern Switzerland (Table 1). We selected two graminoid and two forb species from each of the following plant communities; Molinion (mesotrophic, dominated by perennial grasses), Magnocaricion (mesotrophic to eutrophic, dominated by perennial sedges) and Filipendulion (eutrophic, dominated by a combination of perennial forbs, grasses and sedges). Annual native plants are virtually absent from all these communities.

Table 1.   Species list for the three plant groups investigated in this study, their family and their native range
Plant groupSpeciesFamilyLife formNative range1
  1. 1Sources: Weber (2003)Invasive plant species of the world. A reference guide to environmental weeds. CABI Publishing, Wallingford, UK.

  2. Country occurrence data accessed by GBIF (global biodiversity information facility) data portal: http://data.gbif.org

Native graminoidsMolinia caeruleaPoaceaePerennialEurope
Carex paniceaCyperaceaePerennialEurope, East North America
Calamagrostis epigejosPoaceaePerennialEurope, East North America
Carex elataCyperaceaePerennialEurope
Phragmites australisPoaceaePerennialEurope, Atlantic Islands
Carex acutiformisCyperaceaePerennialEurope
Native forbsSuccisa pratensisDipsacaceaePerennialEurope
Centaurea angustifoliaAsteraceaePerennialEurope
Mentha aquaticaLamiaceaePerennialEurope, North America, West Asia
Lythrum salicariaLythraceaePerennialEurope, North Africa, Asia
Filipendula ulmariaRosaceaePerennialEurope
Valeriana officinalisValerianaceaePerennialEurope, North America
Invasive forbsSolidago giganteaAsteraceaePerennialNorthern America
Solidago canadensisAsteraceaePerennialNorthern America
Impatiens glanduliferaBalsaminaceaeAnnualTropical Asia
Impatiens parvifloraBalsaminaceaeAnnualNorth East Asia
Fallopia japonicaPolygonaceaePerennialTemperate Asia
Erigeron annuusAsteraceaeAnnualNorth America

Experimental design

The experiment was set up in an experimental garden in Zurich, Switzerland (47°24′ N, 8°30′ E at 520 m asl), and run for two growing seasons (of c. 7 months) starting in May 2006. Four treatments were applied in the experiment, combining two nutrient levels (low and high) and two competition levels – with and without competition by Holcus lanatus, a competitive perennial grass abundant in a wide range of moist grasslands (e.g. Edelkraut & Güsewell, 2006). Each treatment was replicated three times for each species, resulting in a total number of 216 pots.

Plants were precultivated from seeds in a glasshouse for 10 wk, except for species with low germination rates (Carex spp., Molinia caerulea and Fallopia japonica), which were cultivated from tillers sampled in the field. Plants were grown individually in 3-l pots filled with quartz sand (grain size 1–1.7 mm; Carlo Bernasconi AG, Zurich, Switzerland). For the competition treatment, three tillers of H. lanatus were planted around the target plants. Pots were arranged on pallets in a randomized block design in the experimental garden. Randomization was repeated three times during the experiment, in September 2006 and in March and June 2007. Holcus lanatus plants that died in winter 2006/2007, probably owing to frost, were replaced in spring 2007.

Plants were watered with tap water and fertilized with nutrient solutions bi-weekly from June to October 2006 and from April to October 2007. Plants received either 60 mg N per pot yr−1 or 300 mg N per pot yr−1. The fertilizer solutions had nutrient ratios of 0.7 (N : K), 3.0 (N : Mg), 3.5 (N : Ca), 10 (N : P), and 200–3000 for the micronutrients. Just before fertilization, appropriate amounts of fertilizer solution were added to 22 l of water, and each pot received 200 ml of the diluted solutions.

Measurements of plant traits

Leaf life span was determined by tagging young, fully developed leaves with light strings and monitoring them from July to December 2006. Leaves were regarded as ‘dead’ when 75% of the leaf was senesced or when it was dropped before 75% senescence. The observed life span was corrected for the age of leaves at the time of tagging by recording the time until a new leaf had fully developed.

Root phosphatase activity was measured in pots without competition in October 2006. Using a small borer, soil cores (1 cm diameter, 0–10 cm depth) were taken in all pots and stored at 4°C. Within 24 h after sampling, cleaned root pieces (100 mg) were incubated for 1 h at room temperature in reaction tubes with 5 ml of a 5 mM p-nitrophenyl phosphate (pNPP) solution buffered at pH 6 (Tabatabai & Bremner, 1969). The reaction was stopped by adding 500 μl of the sample to 3 ml of 2 N NaOH. The absorbance of the solution was measured at 410 nm using a spectrophotometer (Uvi Light XT2; Secomam, Ales Cedex, France) and converted into the amount of p-nitrophenol released per unit fresh root mass.

Specific root length (SRL) was determined for roots from the same soil cores with the line-intersect method (Tennant, 1975); SRL was expressed as root length per unit root fresh mass.

Leaf area was measured in August 2007 for one to six ‘middle-aged’ leaves per plant, using a leaf area meter LI-3100 (Li-Cor, Lincoln, NE, USA). The fresh leaf samples were weighed, dried at 75°C for 24 h and weighed again. We calculated SLA (leaf area per dry leaf mass), tissue density (dry leaf mass divided by fresh leaf mass), and leaf thickness (leaf fresh mass divided by leaf area).

Leaf chlorophyll content was measured in three middle-aged leaves per plant in May 2007, using a chlorophyll-meter (SPAD-502; Konica Minolta, Tokyo, Japan). Three measurements were taken on each leaf and the average of the nine SPAD-values was calculated for each plant.

Leaf litter was collected three times in 2006 from each pot and air-dried. A subsample of the litter was ground (1 mm). Litter carbon (C) and nitrogen (N) concentrations were measured using an elemental analyser (CNS-2000; Leco Corporation, St Joseph, MI, USA). Phenolics were extracted by shaking the litter with 50% ethanol for 1 h (Swain & Hillis, 1959) and analysed with the Folin–Ciocalteu method, using tannic acid for the calibration.

Litter decomposition was determined through laboratory incubation, based on experiments from Aerts & De Caluwe (1997) and Güsewell et al. (2006). The air-dried litter was cut into < 2 cm pieces, and 100 mg subsamples were weighed into 5 × 5 cm nylon litterbags with 1-mm mesh size. Dry weight of the leaf litter samples was determined on separate samples. The litterbags were placed in trays on a 5-cm thick layer of a sand–soil mixture. The soil, collected from a nutrient-poor grassland, was added to the sand as a source of decomposers and litterbags were also sprayed with a soil extract (of the same soil as used in the sand–soil mixture) at the start of the incubation. The substrate was kept wet during the study and contact between substrate and litterbags was ensured by a lid loosely placed on the top of the litterbags. The incubation took place in a dark climate cabinet at 20°C and 60% relative humidity. After 10 wk, litterbags were removed, cleaned manually, and dried at 75°C for 24 h. The remaining litter was weighed to determine litter mass loss during incubation.

The above-ground biomass of plants was harvested after two growing seasons in October 2007 and sorted into living shoots of the target species, dead tissue of the target species, and competitor biomass. Root biomass was only harvested in pots without competition because it was unfeasible to separate roots of the target plants from those of the competitor in the pots with competition. Biomass samples were dried for 48–72 h at 75°C, and weighed. Plant material of the three replicates was pooled for nutrient analyses. Subsamples of ground material were digested for 1 h at 420°C with concentrated H2SO4 and a K2SO4–CuSO4 tablet (Foss Kjeltab, Höganäs, Sweden). The N and phosphorus (P) concentrations in the digests were determined colorimetrically using a flow-injection analyser (FIAstar 5000; Foss Tecator, Höganäs, Sweden).

Allelopathy experiment

The sand from the pots without competition was used to study the effect of plants on soil fertility as well as possible allelopathic effects. During the harvest, roots were separated from the sand with a 4-mm sieve. The sand was kept at 4°C and processed within 2 wk. From each sand sample, we filled four 450-ml pots, and divided them among four treatments: with or without activated charcoal (18 g per 900 g sand), and with or without fertilizer (8 mg N, 0.8 mg P, 12 mg potassium (K), 2.6 mg magnesium (Mg) and corresponding amounts of micronutrients per pot supplied in six weekly additions). In addition to the harvested sand, pure, fresh quartz sand was subjected to the same four charcoal–fertilizer treatment combinations as the control. All pots were planted with 3-wk-old seedlings of Dactylis glomerata and put in a glasshouse chamber with 16h : 8h and 20°C : 16°C as day : night cycle at 70% relative humidity. Plants were watered with deionized water twice a week. Shoot and root biomass of the D. glomerata plants was determined after 6 wk.

Data analysis

All functional traits were analysed with ANOVA mixed models including ‘plant group’, ‘competition’ and ‘nutrient level’ as fixed factors and ‘species’ as random factor nested in ‘plant group’. For traits measured only in pots without or with competition (root traits, nutrient uptake, competitor biomass) the model was reduced by excluding the factor ‘competition’.

The competitive ability of each species was calculated by dividing the above-ground biomass produced in competition by that produced without competition in the same block. Plasticity in response to nutrient supply was calculated for each species by dividing above-ground biomass produced at high nutrient level with that at low nutrient level in the same block. The log-transformed ratios were compared among plant groups and between treatments with mixed models as described earlier.

Allelopathic effects were calculated for each of the 18 species as the difference between the mean biomass produced by D. glomerata with and without charcoal, adjusted for the difference in biomass production owing to charcoal addition in the control sand. We only used data from the fertilized pots because charcoal addition inhibited the growth of D. glomerata in the unfertilized pots, possibly by reducing nutrient availability (Lau et al., 2008).

All statistical analyses were performed in JMP 7.0.1 (SAS Institute Inc., Cary, NC, USA).

Ancillary field sampling

To verify whether plant traits measured in our growth experiment under artificial conditions (plants grown in sand and exposed to full sunlight) correspond with those under natural conditions, we also sampled the 18 study species at their natural growth sites in the field. In three regions of Switzerland (cantons Zurich, Schaffhausen and Schwyz), we searched for the 18 study species in an effort to include their full range of habitats according to Lauber & Wagner (2007) and our experience (dry or wet grasslands, road margin, river bank, forest edge, forest). Each species was sampled at 3–11 sites. To account for plastic responses to light conditions, we recorded the potential duration of direct sunshine at each sampling site with a horizontoscope (Institut für Tageslichttechnik, Stuttgart, Germany). Values varied from 0 (full shade in dense forest) to 16 (full sunlight in open, flat areas).

At each site we sampled 20 leaves of each study species that was present. Fully expanded, nonsenescent leaves were taken at approximately half of the plant’s height (or from rosettes for Erigeron annuus). The chlorophyll content of the leaves was measured immediately. Leaves were taken to the laboratory between wet paper. Their SLA, tissue density and N content were determined with the same methods as already described.

Differences in leaf traits among the three species groups measured in the ancillary field study were tested with mixed models including groups and insolation as fixed factors and species (nested within groups) as random factors. The group–insolation interaction was not significant for any of the variables and therefore excluded from the final model. To assess how traits in the field compared with those in the growth experiment, we calculated the expected values of leaf traits at mean insolation (with analyses of covariance including species and insolation) for each species and correlated these values with species means from the growth experiment.

Results

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

Comparison of functional traits among invasive and native plant groups

In the pot experiment, invasive forbs differed from both native forbs and graminoids in only one trait: leaf chlorophyll content was lower in invasive than in native species (Fig. 1a, Table 2). No other trait differed between the two groups of forbs, but many traits differed between invasive forbs and native graminoids (Table 2). The invasive forbs had shorter-lived leaves, and their leaves had a lower tissue density than the leaves of native graminoids. Furthermore, invasive forbs produced less biomass, and had a lower total N pool, lower N-use efficiency, and higher N concentrations in roots than the native graminoids (Table 2). Leaf litter decomposition rates were lowest for the native graminoids, intermediate for the invasive forbs and highest for the native forbs (Table 2).

image

Figure 1.  Comparison of functional leaf traits between native and invasive species grown in a pot experiment: mean + SE (n = 12) of (a) leaf chlorophyll contents and (b) specific leaf area (SLA) for the six species investigated in each group. In the group of invasive forbs, the three annual species are indicated in grey and the perennials in black.

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Table 2.   Plant functional traits, measures of plasticity and effects on soil properties and processes are compared between three plant groups, native graminoids (NG), native forbs (NF) and invasive forbs (IF)
Measurement ofVariablesNative graminoidsNative forbsInvasive forbsInvasive vs nativeTreatments
  1. Mean ± SE for the three plant groups were determined from six species per group, grown in pots in an experimental garden under two nutrient levels and with or without competition. Differences between plant groups are derived from two-or three-way ANOVA (see the Supporting Information, Table S1) and Tukey post hoc test. Mean values sharing superscript letters are not significantly different. Capital letters indicate plant group differences at α = 0.01, and lower case letters at α = 0.05 level. Significant effects (P < 0.01) of nutrient treatments (N) and competition treatments (C) are indicated in the last column. Some means include both nutrient and competition treatments and some include only nutrient treatments, because these traits were only measured in pots without competition (see Table S1).

Leaf traitSpecific leaf area (SLA) (cm2 g−1)129.2 ± 10.7140.9 ± 12.0167.4 ± 24.0 C
Tissue density0.43 ± 0.01A0.28 ± 0.02B0.28 ± 0.03BIF < NG 
Leaf thickness (mg cm−2)19.11 ± 1.57B27.71 ± 1.96A24.46 ± 1.92AB C
Leaf life span (d)127.5 ± 1.9A101.6 ± 2.4B107.6 ± 1.4BIF < NG 
Leaf chlorophyll content (SPAD)30.38 ± 1.53A29.63 ± 1.54A22.37 ± 1.93BIF < NF&NGN, C
Leaf litter carbon (C) (%)44.47 ± 0.3443.07 ± 0.3942.93 ± 0.67 N
Leaf litter nitrogen (N) (%)1.53 ± 0.171.68 ± 0.152.02 ± 0.38 N, C
Leaf litter C : N54.54 ± 4.1449.69 ± 4.1352.30 ± 9.23 N, C
Leaf litter phenolics (mg g−1)12.94 ± 1.7726.36 ± 9.6919.73 ± 4.59  
Whole-plant traitShoot biomass (g)5.66 ± 0.624.51 ± 1.731.93 ± 0.41 N, C
Litter biomass (g)2.10 ± 0.45a1.85 ± 0.22ab0.80 ± 0.28bIF < NGN, C
Below-ground biomass (g)44.12 ± 7.99A15.92 ± 3.63AB12.34 ± 5.92BIF < NGN
Total biomass (g)56.10 ± 8.28A26.68 ± 5.01AB17.26 ± 7.04BIF < NGN
Root mass ratio (%)77.24 ± 3.2859.15 ± 7.8152.60 ± 10.81  
Shoot N concentration (mg g−1)8.46 ± 1.4310.87 ± 2.779.02 ± 2.31  
Shoot P concentration (mg g−1)0.45 ± 0.070.67 ± 0.160.62 ± 0.23  
Root N concentration (mg g−1)3.19 ± 0.28b6.08 ± 1.01ab6.88 ± 1.04aIF > NG 
Root P concentration (mg g−1)0.49 ± 0.04B0.87 ± 0.12A0.56 ± 0.04AB  
Total N pool (mg)201.2 ± 19.7A132.8 ± 13.9AB93.2 ± 26.0BIF < NGN
Total P pool (mg)25.67 ± 5.13A15.68 ± 2.24AB7.99 ± 2.25BIF < NGN
Nitrogen-use efficiency (g biomass g−1 N)281.7 ± 21.5a198.5 ± 38.4ab146.6 ± 26.8bIF < NG 
Phosphorous-use efficiency (g biomass g−1P)2314.2 ± 192.81664.8 ± 314.91814.8 ± 306.3  
Specific root length (SRL) (m g−1)47.45 ± 11.5633.04 ± 5.7016.30 ± 1.79  
PlasticityResponse to nutrients3.46 ± 0.503.41 ± 0.343.52 ± 0.30  
Response to competition0.31 ± 0.090.19 ± 0.040.11 ± 0.01  
Effects on soilLitter decomposability (% mass loss)26.54 ± 1.79b37.69 ± 2.88a34.73 ± 3.51ab  
Root phosphatase activity (μM g−1 h−1)2.14 ± 0.351.61 ± 0.151.43 ± 0.54  
Soil total phenolics (μg g−1)34.43 ± 3.1036.21 ± 1.2832.19 ± 1.76 N
Soil N (mg kg−1 soil)0.80 ± 0.100.52 ± 0.090.84 ± 0.11  
Soil P (μg kg−1 soil)91.7 ± 19.2105.0 ± 16.7135.0 ± 19.8 N

In the field, the three plant groups differed significantly in leaf tissue density (36–40% lower in forbs than in graminoids) and chlorophyll content (27% lower in invasive forbs than in native graminoids; Table 3). The SLA and leaf N concentration did not differ significantly among the three groups despite a tendency (= 0.09) for higher SLA in the invasive forbs (Table 3). The tissue density, SLA, chlorophyll content and leaf or root N concentration of the 18 species correlated well between field samples and the growth experiment (R = 0.6–0.9, Table 3).

Table 3.   Comparison of leaf traits measured in the ancillary field study between native graminoids, native forbs and invasive forbs
 Means and SE per groupTest of effects (F, P)Correlation
Native graminoidsNative forbsInvasive forbsGroupInsolation(R, P)
  1. Mean ± SE were determined from the same six species per group that we used for the experiment. Measurements were conducted at on average six sites per species. The effects of species (nested within plant group), plant group and insolation were tested with mixed models. F-values and significance levels are indicated for each effect (*P < 0.05, **P < 0.01, ***P < 0.001). Differences between plant groups were determined with Tukey post hoc test (α = 0.05); values sharing the same letter are not significantly different. Correlations between field data and experimental data (mean values per species) are shown in the last column. Test results for the random factor species (group) are not shown.

  2. 1Calculated with log-transformed data.

  3. 2Correlation with the N concentration of roots in the growth experiment.

Tissue density (%)35.2 ± 2.3a22.6 ± 2.3b21.3 ± 2.1b11.5***41.6***0.944***
Specific leaf area (SLA) (cm2 g−1)1180 ± 27215 ± 31279 ± 362.867.7***0.745***
Leaf nitrogen (N) concentration (mg g−1)119.5 ± 2.820.4 ± 2.824.6 ± 3.01.031.4***0.622**2
Chlorophyll (SPAD)38.9 ± 2.1a33.0 ± 2.1ab28.5 ± 1.8b7.0**2.70.620**

Plasticity in traits: response to nutrients and competition

Nutrient level and competition significantly affected plant growth and traits (Table 2; see the Supporting Information, Table S1). The higher nutrient supply significantly increased biomass production but not nutrient concentrations (data not shown).

Plasticity in response to nutrient supply was similar for the three plant groups (no significant group × nutrient interactions in Table S1). On average, plants produced 3.5 times more biomass with the higher nutrient supply, and invasive forbs were not more plastic than the two other groups (Fig. 2a).

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Figure 2.  Plasticity of native graminoids, native forbs and invasive forbs, as measured in six species per group for above-ground biomass produced at a high compared with a low nutrient level (a) (open bars, low nutrients; closed bars, high nutrients; error bars represent means ± SE; n = 6), in competition compared with no competition (b) (open bars, single plant; closed bars, in competition; error bars represent means ± SE; n = 6) and for nitrogen (N) concentrations in the above-ground biomass in competition compared with no competition (c). Numbers next to bars indicate the mean increase or decrease in biomass production per group between the treatments; error bars represent means ± SE; n = 6.

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Competition by H. lanatus decreased above-ground biomass production (Fig. 2b) and nutrient concentrations in the biomass; this response mostly did not differ between the three plant groups (on average 70–85% reduction) but varied widely among species within groups (Table S1). Yet, litter biomass production was particularly reduced in the native forbs (not shown), and N concentrations in shoots were reduced only in the invasive forbs (Fig. 2c). This trend was similar for the shoot P concentrations, but not significant (P = 0.21). Individual species produced between 1.6 and 34 times less above-ground biomass with competition. The nutrient level had no significant effect on the response to competition (Tables 2, S1).

Effects on soil fertility and allelopathic effects

In the pots without fertilization or activated charcoal, biomass production of D. glomerata was higher in the soil where invasive forbs had grown than where native forbs had grown (Fig. 3).

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Figure 3.  Comparison of phytometer shoot biomass production in pure sand or in sand pre-grown by native graminoids, native forbs or invasive forbs; error bars represent means ± SE; n = 6; Control; error bars represent means ± SE; n = 5. The pre-grown sand was either fertilized or unfertilized, and activated charcoal (AC) was added to half of the samples to assess allelopathic effects. Letters are from one-way ANOVA and post hoc Tukey test (α = 0.05) comparing plant groups and the control within treatments.

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The addition of activated charcoal to pots with fertilizer generally increased the growth of D. glomerata. This effect was stronger in the precultivated sand than in the fresh (control) sand, suggesting that plants had released substances with allelopathic effects during the two growing seasons. Allelopathic effects (the relative increase in shoot biomass of D. glomerata owing to charcoal addition) tended to be stronger in invasive forbs than in the two native plant groups (P = 0.06; Fig. 4).

image

Figure 4.  Comparison of allelopathic effects between the 18 species investigated. Allelopathic effects were measured as the differences in shoot biomass production of the phytometer Dactylis glomerata between pregrown substrates with and without the addition of activated charcoal. In the group of invasive forbs, the three annual species are indicated in grey and the perennials in black. Error bars represent means ± SE; n = 6.

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Different effects of plant groups on the growth of D. glomerata were not reflected by measurable differences in sand chemistry. Root phosphatase activity, concentrations of soluble phenolics and concentrations of nitrate, ammonium or phosphate in the sand did not differ between the plant groups (Tables 2, S1).

Discussion

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

Differences in plant traits between invasive and native species

Overall, the invasive forbs in our study hardly differed in functional traits from the native forbs, but clearly differed from the native graminoids. This difference, which primarily reflects the growth form and anatomy of the plant functional groups (Cornelissen & Thompson, 1997; Grime et al., 1997; Cornelissen, 1999), is of ecological relevance as alien forbs invade ecosystems dominated by graminoids. The invasion of (exotic) forbs in graminoid-dominated vegetations will substantially change the functional trait composition of the vegetation, and potentially also its effect on soil processes (Pokorny et al., 2005; Chapuis-Lardy et al., 2006; Garnier et al., 2007; Suding et al., 2008; Scharfy et al., 2010). In particular, the faster litter decomposition of invasive plants could accelerate nutrient cycling in invaded grasslands (Emery & Perry, 1996; Ashton et al., 2005; Drenovsky & Batten, 2007; Garnier et al., 2007; Suding et al., 2008).

Leaf chlorophyll content was one of the few traits that differed between invasive forbs and native forbs. The lower chlorophyll content (per unit leaf area) of the invasive species might indicate a greater light-use efficiency. Such a strategy might help these invasive plants to grow in a wide range of light environments as it reduces the risk of light inhibition in full sunlight while reducing self-shading when light is scarce.

Invasive forbs further differed from native forbs in having a 50–70% lower P pool in the biomass. This result was opposite to our hypothesis that invasive forbs would take up more nutrients from the soil. It mainly resulted from the low biomass of the annual Impatiens species, whereas the two perennial Solidago species had equal or higher nutrient pools than the native forbs. These results concur with the observation that the Solidago species also invade nutrient-poor grasslands (Güsewell et al., 2005; Scharfy et al., 2009), whereas the Impatiens species colonize only nutrient-rich sites, naturally dominated by forbs (Andrews et al., 2005; Güsewell et al., 2005; Hejda & Pyšek, 2006).

A higher SLA in invasive compared with native plant species was observed in previous field studies (Smith & Knapp, 2001; Grotkopp et al., 2002; Lake & Leishman, 2004; Hamilton et al., 2005). This was not the case in the present study (cf. Fig. 1b), probably because several native forbs were also fast-growing species occurring naturally in nutrient-rich, moist sites.

Differences in plasticity; response to nutrients and competition

Invasive forbs were not more plastic in response to nutrient enrichment than native species, in contrast to our hypothesis, and to other studies (Milberg, 1999; Craine & Lee, 2003). A possible reason is that our high-nutrient treatment was not sufficiently high to bring about such a difference. Indeed, root mass ratios hardly differed between low and high nutrient treatments (−3%), whereas they normally decrease in response to nutrient enrichment (Aerts & Chapin, 2000). Also, the shoot N and P concentrations of native plants in this study were lower than average concentrations reported from field measurements for the same species (Güsewell & Koerselman, 2002). Our results, therefore, do not exclude the possibility that invasive species would be more responsive to extreme nutrient enrichment.

The three plant groups also responded similarly to competition by H. lanatus, which does not support our hypothesis that invasive forbs would be less affected by competition than native species at a high nutrient level. Furthermore, their ability to suppress the competitor was not greater than that of the native forbs and tended to be lower than that of the native graminoids (H. lanatus produced a shoot biomass of 6.6 ± 0.6 g in pots of invasive forbs, 6.1 ± 0.6 g in pots of native forbs and 4.9 ± 0.7 g in pots of native graminoids; F = 3.54, P = 0.055). Hence, our results suggest a lower, rather than higher, competitive ability of invasive forbs, under the nutrient conditions of the experiment.

Do the invasive forbs differ in impact on soil processes from native species?

All but one plant species investigated appeared to exert allelopathic effects on D. glomerata (Fig. 4). While allelopathic effects have been reported for a number of invasive plant species (Inderjit et al., 2008), including Solidago canadensis (Yang et al., 2007; Abhilasha et al., 2008), few studies have directly compared these effects with those of native species when both plant groups have been grown in monocultures. Our study highlights the necessity to do such a comparison, as allelopathic effects in invasive species may well be paralleled by similar effects in native species.

In our experiment, the invasive forbs tended (P = 0.06) to exert stronger allelopathic effects on the shoot growth of D. glomerata than the native plant groups. The strongest allelopathic effects were found for the two annual Impatiens species (Fig. 4). This might contribute to the ability of both species to invade perennial native vegetation – an unusual behaviour for annual species in Central Europe (Thompson et al., 1995). Phragmites australis was the only native species with a similar high allelopathic effect to the two Impatiens species. Phragmites australis is a competitive invader in wetlands worldwide, and its allelopathic effects on co-occuring plants have already been described (Zou et al., 2006). Overall, our results suggest that allelopathic effects may contribute to the invasiveness of the plant species studied, but the differences between native and invasive species were smaller than expected.

Conclusions

Differences in functional traits seemed to primarily depend on functional group and life form, as the largest differences were found between annual invasive forbs and perennial native graminoids. Therefore, exotic invasive plants most likely alter ecosystem processes when they displace native species of a differing functional group and life form, respectively (Allison & Vitousek, 2004). When invasive forbs displace native forbs, ecosystem processes may not necessarily change, but invasive forbs may benefit from an advantage because of novel weapons (allelopathy), facilitating their invasion.

Acknowledgements

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

We thank Rose Trachsler and Marilyn Gaschen for their help with nutrient analyses, Martin Fotsch for his help in maintaining the experiment, as well as Sophia Etzold, Myriam Poll and Daniel Schlaepfer for their help in plant processing and data collection. This research was funded by the Swiss National Science Foundation through grant 2-77669-05.

References

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

Supporting Information

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

Table S1 ANOVA results for the effects of plant species (within groups), groups, nutrient level and competition on plant functional traits, plasticity in these traits and on traits affecting soil properties and processes

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