SEARCH

SEARCH BY CITATION

Keywords:

  • Arion lusitanicus;
  • choose experiments;
  • clonal growth;
  • EICA hypothesis;
  • intraspecific comparisons;
  • herbivory;
  • palatability;
  • seedlings;
  • sexual reproduction;
  • vegetative reproduction

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. Supplementary material
  10. References
  • 1
    The EICA (evolution of increased competitive ability) hypothesis suggests that release from natural enemies and pathogens results in higher vigour of invasive plants as a result of the selection of less defended but rapidly growing genotypes. Slug diversity and abundance appear to be low in North America compared with Europe, and we therefore hypothesized that release from slug herbivory contributes to the invasiveness of European Brassicaceae species in North America.
  • 2
    In common garden and glasshouse experiments we compared life history and fitness parameters in native (NP) and introduced (IP) provenances of four invasive Brassicaceae species (Barbarea vulgaris, Bunias orientalis, Cardaria draba, Rorippa austriaca) that were subjected to herbivory by Arion lusitanicus. In climate chamber bioassays we investigated slug damage to seedlings and leaf discs using the same sources of plant material.
  • 3
    In all species except B. orientalis we found significant but not always consistent differences in growth and reproductive characteristics between IP and NP plants. Plants of B. vulgaris and R. austriaca from the introduced range had a considerably higher growth rate than those from the native range. While IP plants of the non-clonal B. vulgaris allocated more resources to seed production than NP plants, the IP plants of the clonal R. austriaca showed a decreased number of seeds.
  • 4
    Contrary to expectation, there were no differences between NP plants and IP plants in the number of damaged leaves and leaf area consumed by slugs, or in the proportion of seedlings damaged and killed. Nor were there interaction effects between slug treatments and provenance.
  • 5
    The results suggest that there are genetically based differences in growth and reproductive parameters between NP and IP plants. As there were no differences in herbivore damage between the provenances, this genetic differentiation is probably due to factors such as competition rather than herbivore effects.
  • 6
    In order to make progress in understanding why some species become invasive, more comparative experimental studies are needed that investigate how different kinds of antagonists (generalist and specialist herbivores and pathogens) influence the performance of plants at different life stages.

Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. Supplementary material
  10. References

It has often been observed that plants grow more vigorously and attain larger size in introduced areas than do conspecifics growing in the native range (Blossey & Nötzold 1995; Leger & Rice 2003; Jakobs et al. 2004). Amongst hypotheses proposed to explain this phenomenon are, first, that release from natural enemies and pathogens results in higher plant vigour (e.g. Coley et al. 1985; Herms & Mattson 1992; Keane & Crawley 2002; Wolfe 2002) and, secondly, that poorly defended but rapidly growing genotypes are selectively favoured in the absence of herbivores (evolution of increased competitive ability (EICA) hypothesis, Blossey & Nötzold 1995). To investigate whether differences in selection pressures have resulted in genetic differentiation between plants in the native and introduced range requires comparative experiments under standardized conditions (Wolfe et al. 2004).

There have been rather few such common garden experiments of invasive and native plant provenances (Blossey & Nötzold 1995; Willis et al. 2000; Siemann & Rogers 2001; Leger & Rice 2003; Wolfe et al. 2004). In particular, the EICA-hypothesis has been tested using real or simulated herbivore pressure for only a few invasive plant species (Sakai et al. 2001) and the results are contradictory (e.g. Siemann & Rogers 2003; van Kleunen & Schmid 2003; Bossdorf et al. 2004a,b; Hierro et al. 2004). Most investigations have either focused on differences in herbivore damage or on differences in growth patterns between provenances, and few have considered both aspects together (but see Wolfe et al. 2004; Stastny et al. 2005). However, differences in growth between provenances might be unrelated to herbivory or, conversely, differences in herbivore pressure may not be reflected in changes in plant growth, as postulated by the EICA hypothesis.

Plants differ in their palatability to generalist herbivores and in their ability to withstand herbivore damage (Louda et al. 1990; Oliveira Silva 1992; Mutikainen & Walls 1995). Hence, the impact of herbivory on plant growth and fitness may differ between species. It can also differ among plants of the same species but of different ages (for example, due to age-dependent accumulation of secondary compounds, Moens 1989). In general, successful invasive species are likely to have a particularly high capacity for compensatory growth, as well as flexible resource allocation (e.g. Schierenbeck et al. 1994). In Europe, and especially in north-western parts where winters are wetter and milder (South 1992), slugs are among the most important herbivores of low herbaceous vegetation (Rathcke 1985; Rees & Brown 1992; Hulme 1996; Rodríguez & Brown 1998) and can influence both the biomass and the species composition of plant communities (Oliveira Silva 1992; Hanley et al. 1995a; Hulme 1996; Bruelheide & Scheidel 1999; Buschmann et al. 2005). For plants invading such vegetation, resistance to or tolerance of slug herbivory may therefore be important.

In this study we compare growth characteristics and effects of herbivores on four species of Brassicaceae. Several perennial species of Brassicaceae native to south-east or central Europe have increased their range into northern and western Europe, and some are also invasive in North America (cf. Jalas & Suominen 1994; Jalas et al. 1996; USDA 2002). Slugs are known to be important herbivores of at least some Brassicaceae species and comparative studies have even shown that, despite the presence of mustard oils, some slug species have a preference for Brassicaceae over other families (e.g. Cates & Orians 1975; Dirzo 1980; Rathcke 1985; Briner & Frank 1998). Whereas several voracious slug species have long been abundant in Europe, high levels of slug herbivory appear to be a more recent phenomenon in some regions of the USA and are mainly due to just one species, Deroceras reticulatum (McCracken & Selander 1980). This slug was introduced approximately 150 years ago and is now expanding its range. In contrast, because of their relatively low abundance slug species native to North America are not usually considered to be serious pests (South 1992).

Against this background we hypothesize that the lower intensity of slug herbivory in the USA has contributed to an increased invasiveness of certain European species of Brassicaceae in this new area. In addition, we assume that young plants are not only more vulnerable to slug attack than adult established plants (cf. Dirzo 1980; Hanley et al. 1995b; Frank 1998) but also that the preferences for native and invasive populations may vary according to life strategy or plant morphology. For example, in populations of clonal species where there is a trade-off between clonal propagation and seed production (Eriksson 1997, references therein), the relative importance of seedling and adult stages for invading a new area may determine patterns of herbivory.

Three main questions were posed in this study. (i) Are the introduced plants found in the USA more severely attacked by slugs than their native conspecifics from Europe? (ii) To what degree do the populations from the introduced area differ from the native ones with respect to life-history characters and fitness? (iii) Do any differences between provenances in the impact of herbivores depend upon plant morphology and life stage or upon leaf palatability?

Three types of experiments were performed to investigate these questions: (i) established plants were exposed to slug herbivory under field-like conditions in a common garden (mesocosm) experiment; (ii) the susceptibility of seedlings or juvenile plants to slug herbivory was compared in microcosm experiments; and (iii) the palatability to slugs of leaf discs was investigated in food-choice bioassays. An important feature of our study was the use of several taxonomically related species differing in their invasiveness. By using this approach we hoped to obtain more general conclusions about the interactions between slug herbivory and plant invasion than could be obtained from the study of a single species (Buschmann et al. 2002).

Materials and methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. Supplementary material
  10. References

plant species characteristics

We studied four herbaceous species of Brassicaceae: Barbarea vulgaris R.Br., Bunias orientalis L., Cardaria draba (L.) Desv. and Rorippa austriaca (Crantz) Besser. Besides sharing the characteristic traits of this family (Hedge 1976), the species are relatively similar in life-form and habitat preference. All are polycarpic herbaceous perennials with a semirosette growth form and relatively deep storage roots, and all have a preference for moderately disturbed, open sites on nutrient-rich calcareous soils (Oberdorfer 1990). However, they differ in the relative importance of vegetative and sexual reproduction (Table 1), the longevity of individuals and the type of the seed bank (Hegi 1986; Dietz & Ullmann 1998; Dietz et al. 2002). Rorippa austriaca and C. draba show low seedling recruitment but can spread clonally by lateral root growth and can also regenerate from dispersed root fragments. In contrast, B. orientalis and B. vulgaris produce abundant seedlings but do not spread clonally. Barbarea vulgaris lives for only a few years and mostly dies after flowering (H. Dietz, unpublished data), while the other species are longer lived (Dietz & Ullmann 1998; Woitke 2001).

Table 1.  Main regeneration strategy, status of the study species (NP, native provenance; IP, invasive provenance) and collection scheme of plant material of three populations per provenance and species, with year of sampling given in parentheses. SE-Eur, south-eastern central Europe (SE of Vienna (Austria) in Achau, Laxenburg and Fischamend Markt); W-Eur, western central Europe (S of Würzburg (Germany) in Winterhausen, Thüngersheim and Randersacker); N-Am, North America (SE Michigan (Ann Arbor and Ypsilanti), Illinois (Peoria) and Wisconsin (Madison), all USA). The number of plant fragments collected in each population is given in parentheses
  Barbarea vulgarisBunias orientalisCardaria drabaRorippa austriaca
 RegenerationSexualSexualClonalClonal
SE-Europe (2000)Type of material collectedAdult plants (60 per population)Fragments of clones (90 per population)Fragments of clones (90 per population)
StatusNPNPNPNP
W-Europe (1998)Type of material collectedSeedsAdult plants (60 per population)
StatusNPIPIPIP
N-America (1999)Type of material collectedSeedsFragments of clones (60 per population)Fragments of clones (60 per population)
StatusIPIP (extinct?)IPIP

All species are native in south-eastern Europe (Table 1). Barbarea vulgaris is also native, or perhaps archaeophytic, in central Europe while B. orientalis, C. draba and R. austriaca have been introduced to at least the western parts of central Europe (Jalas & Suominen 1994; Jalas et al. 1996). All species were introduced to North America in the 19th century or earlier (cf. Voss 1985) where they are invasive to different degrees. However, B. orientalis seems to be virtually extinct in the USA now (cf. USDA 2002).

collection of plant material

Three populations per species and provenance were sampled in typical ruderal sites between 1998 and 2000. Native populations (NP) of B. orientalis, C. draba and R. austriaca were sampled in the Vienna area in Austria (south-eastern central Europe) and of B. vulgaris in northern Bavaria (western central Europe). Invasive populations (IP) were sampled in the southern Great Lakes region of the USA (B. vulgaris, C. draba, R. austriaca) and in northern Bavaria (B. orientalis, Table 1). For each species, populations at least 10 km apart were sampled. The detailed sampling scheme is given in Table 1. Sixty to 90 individuals per species and population were grown, either from seed (B. vulgaris) or from plant fragments (B. orientalis, C. draba, R. austriaca). The plants were raised in pots of 10 cm diameter filled with commercial potting soil and were kept in an unregulated glasshouse in Würzburg and later in Zurich.

choice and collection of slug species

For our herbivory experiments we chose to use Arion lusitanicus Mabille, one of the most common European slugs and an agricultural pest in some regions (Reischütz 1986; Fechter & Falkner 1989; Frank 1998). This species was found for the first time in North America in 1999 (R. Hammond, personal communication) and is not abundant there.

We first used leaf disc palatability assays to test for variation in feeding preference among slug populations sampled at ruderal sites in northern Bavaria and Zurich. There were no differences in the consumption index between slugs from Germany and Switzerland (t-test: t = −0.44, d.f. = 38, P > 0.66). Based on these results, and for practical reasons, only slugs from Switzerland were used for the experiments. These were collected as required from the surroundings of the experimental garden at Hönggerberg in Zurich (Switzerland).

common garden experiments

The common garden experiment was established in October 2000 and ran for 2 years. The site was a homogeneous, sunny area in the experimental garden with a base-rich, loamy soil.

‘Plant origin’ and ‘slug presence/absence’ were the treatment factors. There were three replicate plots per treatment. Using a split-plot design five plants chosen at random from each of the three populations of each provenance were planted 25 cm apart in each half of a plot. Care was taken to ensure that the plants from the different provenances were similar in size. The plots were surrounded by slug-proof frames (1 × 1 m2, height 30 cm and buried 5 cm into the soil) and were arranged in a regular grid with a spacing of 75 cm between neighbouring frames. After an establishing period of 5 weeks, during which dead individuals were replaced by new ones, five slugs each were introduced to half of the plots, chosen at random, in autumn 2000. A wooden shelter was placed in the middle of each plot to provide a refuge for the slugs and help to maintain their numbers (cf. Keller et al. 1999).

For each plant we measured the following characters related to life history, phenology and fitness: total number of leaves, number of grazed leaves (measured twice a year in spring and autumn), number of shoots, starting date of flowering, number of fruits formed, number of seeds per fruit, and seed mass (measured once a year in summer). The start of flowering was related to the main flowering period of Taraxacum officinale in the area so as to take account of climatic differences between the years. Twenty fruits of each plant were sampled randomly to measure the mean number of seeds and seed weight.

From March to November the numbers of Arion lusitanicus in the slug plots were monitored on a weekly basis and adjusted to five per plot by adding or removing animals as necessary. Any individuals of other mollusc species were removed. In September 2001 molluscicide (metaldehyde pellets) was applied to prevent slugs from entering the slug-exclosure plots.

seedling and root regenerate bioassays

The susceptibility to grazing of seedlings and root regenerates (i.e. small plants regenerating from root fragments) was tested in garden and climate chamber experiments. The seedlings and root regenerates of the clonal species (C. draba, R. austriaca) were grown in a glasshouse in Zurich from seeds and root fragments collected from surplus individuals of the plants that were cultured separately. For these plants care was taken to avoid gene flow between individuals obtained from different areas.

The garden experiments were performed in May and September 2002. Plastic flats (45 × 28 × 5 cm3) filled with potting soil were buried into the soil to ground level in the area of the common garden experiments. For each species, 100 seedlings (cotyledon stage) or root regenerates from each provenance were planted into each randomly chosen half of a flat. After 2 days, each flat was assigned randomly to one of two grazing treatments: exposure to ambient grazing pressure by slugs (the numbers of slugs observed in the flats or in the surroundings, and the species present, were noted at intervals during the experiment) and a control with no slugs (molluscicide treatment). There were 10 flats per treatment and for each plant species. The numbers of damaged and dead seedlings/root regenerates were scored after 4 days.

In the climate chamber experiment, seedlings and root regenerates were offered to the slugs in plastic boxes (20 × 10 × 5 cm3; 17 °C; 12 hours light : 12 hours dark) in spring 2002. The bottom of each box was covered with 2 cm of commercial potting soil. Forty-eight hours after transplanting the seedlings into the boxes, one slug was introduced to each box and allowed to feed for 24 hours. The numbers of damaged and dead seedlings/root regenerates were scored at the end of the experiment.

leaf disc palatability bioassays

A bioassay experiment was conducted in which individuals of A. lusitanicus in 135 mm diameter Petri dishes were presented with leaf discs from plants of native and invasive origin. The leaf discs were 11 mm in diameter and were cut from mature leaves from all populations of each species. In each Petri dish six leaf discs from both native and invasive populations of the same species were placed alternately in a circular pattern on a moist filter paper. In addition, three larger discs of Taraxacum officinale, one of the most palatable plants for slugs (Dirzo 1980; Rathcke 1985; Frank & Friedli 1999), were placed in the centre of each Petri dish as an additional source of food intended to ensure that the experimental material was not totally consumed.

In a previous feeding experiment we found no significant differences in feeding behaviour between fed and unfed slugs, but fed slugs showed a lower variation in the amount of consumed leaf material and a tendency to discriminate more strongly between plant species (cf. Briner & Frank 1998). Therefore, prior to the experiments each slug was placed in a separate plastic box and fed ad libitum with T. officinale for 24 hours (climate chamber; 17 °C; 12 hours light : 12 hours dark). Subsequently, one slug was introduced to the centre of each dish and was allowed to feed for 12 hours in the dark (17 °C) in a climate chamber. The bioassays were conducted once in autumn and once in spring, using adult and juvenile slugs, respectively. There were 20 replicate Petri dishes of each species though death or inactivity of some slugs sometimes reduced the effective number of replicates.

At the end of the experiments the amount of leaf area consumed was determined by image analysis (cf. Dietz & Steinlein 1996). Ten surplus leaf discs per species and provenance were collected and oven-dried at 70 °C for 24 hours to measure the dry weight. The fresh body weight of slugs was measured before and after the experiment and the data were transformed to dry weight using the calibration of Bullock & Smith (1971). Palatability was expressed as the consumption index CI (Waldbauer 1968):

  • CI = (F/(T × W)) × 1000

where F is the amount of food eaten (mg), T is the duration of the feeding period (hours) and W is the mean body weight of the test slug during the feeding period (mg).

data analysis

JMP 5.0 (SAS Institute 2002) was used for all analyses. For the common garden experiment, anova was used to test the effects of plant provenance and slug density on the plant parameters. Separate tests were run for each species and each parameter because we could not be certain that parameters were independent of each other.

For the bioassays t-tests were used to compare differences in the consumption of leaf disc material and the percentage of damaged and killed seedlings between native and introduced plants.

Prior to parametric tests the percentage values were arcsin-transformed.

Results

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. Supplementary material
  10. References

common garden experiment

General differences between the native (NP) and invasive (IP) provenances

In general, the data were highly consistent between years and we present here only results from the second year.

Mortality was low in all species, ranging from 0 to 13% over the course of the experiment. There were also no significant differences in survivorship between IP and NP plants for any species or treatment (P > 0.44, data not shown).

For all species except Bunias orientalis, plants originating from the introduced area grew more vigorously, i.e. they produced a higher number of leaves or a higher number of stems or both than those originating from the native area (Fig. 1, Table 2). In both years the numbers of leaves present were generally low in autumn and differences between the provenances and slug treatments were small. Therefore, we present here only the spring data. In all species the highest numbers of leaves and stems were recorded in the second year. In Barbarea vulgaris and Rorippa austriaca the numbers of leaves and stems were significantly higher for IP than NP plants (Fig. 1, Table 2). Plants from IP of Cardaria draba had approximately 40% more leaves than the plants from NP but there were no differences in the number of stems. There were no significant differences between provenances in B. orientalis.

image

Figure 1. Number of leaves and stems produced by the study species in the second year (plot means ± SE; n = 3 replicate plots). Treatment factors are provenance of the plants (invasive vs. native plants) and slug density (slug presence or absence). Significant main effects on vegetative plant traits, determined from an anova for the common garden experiment, are shown. There were no interaction effects for any species. Grey bars, native populations; black bars, invasive populations; filled bars, slugs absent; hatched bars, slugs present; P, provenance; S, slug density; ***P < 0.001; **P < 0.01; *P < 0.05.

Download figure to PowerPoint

Table 2.  Summary table of significant main effects (anova) of provenance of the plants (invasive vs. native plants) and slug density (slugs present vs. slugs absent in plots) on plant performance and fitness parameters (for details see Appendix S1 in Supplementary Material). There were no interaction effects. P, provenance; S, slug density; + indicates better performance of invasive plants or higher leaf damage in slug plots, o indicates no effect; – indicates better performance of native plants or higher leaf damage in slug exclosure plots; double symbols indicate stronger effects
 Barbarea vulgarisBunias orientalisCardaria drabaRorippa austriaca
PSPSPSPS
Leaf damageo++o++o+++
No. of leaves++++oo++o++++
No. of stems+ooooo+o
No. of fruits++oooo+
No. of seeds fruit−1++ooooooo
Seed massooooo+o
Date of flowering+oooo+

Differences in reproductive parameters between NP and IP plants were more pronounced than those between growth parameters, but the differences were not consistent between species (Fig. 2, Table 2). In R. austriaca NP plants produced significantly more fruits than IP plants (NP 4100, IP 2530), seed number per fruit did not differ, and seed mass was significantly lower in NP plants (IP 0.016 mg, NP 0.008 mg). In contrast, in C. draba seed mass was significantly lower in IP plants. Barbarea vulgaris showed significantly higher fruit production in IP than in NP plants; in the ungrazed plots IP plants produced twice as many and in the grazed plots 10 times as many fruits as did the corresponding NP plants. In addition, IP plants produced more seeds per fruit than NP plants in both the grazed and ungrazed plots (Fig. 2, Table 2). In B. orientalis there were no consistent differences in the reproductive parameters between provenances or treatments.

image

Figure 2. Reproductive parameters of the study species in the second year (plot means ± SE; n = 3 replicate plots). Other symbols and statistical conventions as in Fig. 1.

Download figure to PowerPoint

IP and NP plants did not differ significantly in the percentage of flowering in any species (data not shown) and there were also no consistent differences in flowering phenology between provenances. IP plants of B. vulgaris flowered 4–10 days earlier than NP plants, while R. austriaca showed a difference in the opposite direction. (Fig. 2, Table 2).

Effects of slug treatments

There were no significant differences between NP and IP plants in the percentage of damaged leaves (Fig. 3, Table 2, P > 0.5) except on one occasion when NP plants of R. austriaca had significantly higher leaf damage. However, there were strong differences between the four study species in the level of slug damage. As the plants had a relatively low number of leaves in autumn and because of highly consistent results in spring and autumn (except for R. austriaca in which up to 95% of the leaves were affected by slug grazing in autumn 2001) we present only the spring data on leaf damage. In B. vulgaris up to 60% of the leaves were damaged by slugs in spring 2002 while in B. orientalis about 30% and in R. austriaca and C. draba less than 20% of the leaves were damaged (Fig. 3).

image

Figure 3. Damaged leaves (%) in spring 2002 (plot means ± SE; n = 3 replicate plots). Other symbols and statistical conventions as in Fig. 1.

Download figure to PowerPoint

Barbarea vulgaris and R. austriaca produced more leaves in the grazed than in the ungrazed plots whereas slug herbivory had no significant effect on leaf number in the other two species (Fig. 1, Table 2). The number of stems was mostly not affected by slug damage, though grazed plants of B. vulgaris tended to produce more stems than ungrazed plants (Fig. 1, P < 0.1).

In some species slug herbivory had significant effects on flowering date and the number of fruits produced. Ungrazed plants of B. vulgaris produced significantly more fruits, while ungrazed plants of R. austriaca produced fewer fruits (Fig. 2, Table 2). Furthermore, in the plots with slugs, R. austriaca flowered significantly earlier (49 and 56 days after main flowering of T. officinale for NP and IP, respectively) than under slug exclosure (51 and 67 days after main flowering of T. officinale for NP and IP, respectively) while the other species showed a tendency for later flowering (1–5 days) in the slug plots (Fig. 2, Table 2).

seedling and root regenerate bioassays

In the climate chamber experiment in May 2002, slug herbivory caused considerable damage to seedlings. Both the percentage of damaged seedlings and the percentage of killed seedlings were similar between provenances (P > 0.15 for all species) but varied strongly among species (Fig. 4).

image

Figure 4. Percentage of killed and damaged seedlings in the common garden seedling and root regenerate bioassay conducted in spring 2002 and in the climate chamber bioassay (means ± SE; n = 10). Grey bars, native populations; black bars, invasive populations; filled bars, killed seedlings; hatched bars, damaged seedlings; Ba, Barbarea vulgaris; Bu, Bunias orientalis; Ca, Cardaria draba; Ro, Rorippa austriaca.

Download figure to PowerPoint

In the common garden experiment, the commonest slug species in the flats with ambient slug herbivory were Arion lusitanicus (Mabille) and Deroceras reticulatum (Müller). Other species found in smaller numbers included D. leave (Müller), A. distinctus (Mabille), Boettgerilla pallens (Simroth) and Limax cinereoniger (Wolf).

Slugs caused considerable damage to, and death of, seedlings in the ambient flats whereas no plants died in the ungrazed controls (data for controls are not shown). Due to the slugs being larger, seedling damage rates were higher in autumn than in spring (IP 91 vs. 30%, NP 82 vs. 32%), but the differences between species were generally consistent not only between the spring and autumn bioassays (data not shown) but also between the common garden and climate chamber experiments. However, R. austriaca, a species known to be preferred by the slug D. reticulatum (H. Buschmann, unpublished data), was attacked more in the common garden experiment. Again, there were no significant differences in grazing damage between plants (whether seedlings or root regenerates) from IP and NP (P > 0.12 for all species).

While in C. draba the percentage of damaged seedlings was much higher than the percentage of damaged root regenerates, R. austriaca showed the opposite pattern. In both species, mortality of root regenerates was lower than that of seedlings (Fig. 4).

leaf disc palatibility bioassays

The percentage of leaf-disc area consumed ranged from 18% for C. draba to 63% for B. orientalis. The consumption index was higher in autumn 2001 (NP 11–68, IP 8–45) than in spring 2002 (NP 8–39, IP 8–32, Fig. 5) for all species, and especially for R. austriaca. As in the experiments with seedlings and root regenerates, the slugs showed no preference for NP or IP plants (P > 0.4 for all species). Differences in the palatability of the various species were consistent with the results of the other experiments.

image

Figure 5. Leaf palatability of the study species calculated as consumption index (CI) from the results of the leaf disc bioassays conducted in autumn 2001 and spring 2002 (means ± SE; n = 15). Grey bars, native populations; black bars, invasive populations.

Download figure to PowerPoint

Discussion

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. Supplementary material
  10. References

main and interaction effects of provenance

Contrary to our expectations, there were no general differences in slug damage between provenances of the four Brassicaceae species in any of our experiments. Furthermore, the interaction between provenance and grazing intensity was not significant for any species or parameter. In contrast, there were differences in growth, reproductive effort and/or phenology between provenances and in some cases between slug treatments.

With the exception of B. orientalis, plants from IP showed higher performance than conspecifics from NP. The strongest differences were found in B. vulgaris, which was the first to be introduced to the north-western USA and is most invasive there. Cardaria draba was introduced later and, although widespread, is not very abundant (e.g. Voss 1985; USDA 2002), while R. austriaca was not known before 1941 but is now expanding its range (USDA 2002; H. Dietz, personal observation). It could therefore be that B. vulgaris has had more opportunity than the three other species to evolve in response to the new conditions in North America, especially as C. draba and R. austriaca mostly regenerate vegetatively.

Comparative data on growth performance of plants of native and invasive provenance are available for at least 12 other plant species (Blossey & Nötzold 1995; Daehler & Strong 1997; Willis et al. 2000; Siemann & Rogers 2001, 2003; Leger & Rice 2003; van Kleunen & Schmid 2003; Vilàet al. 2003; Wolfe et al. 2004; Stastny et al. 2005). In five species plants from invasive populations grew larger than those from native provenances, whereas in five species there were no differences, and in one case the growth rate was higher for native plants. In the remaining species there were even contrasting results in two different studies. Hence, it is clear that no simple generalizations can be made about invasive plants having a higher growth rate, particularly between species that vary strongly in respect to their life-history traits.

It is also not possible to generalize about the relative impact of pathogens or herbivores upon plants from native and invasive populations. Siemann & Rogers (2003) found that seedlings from invasive provenances of Sapium sebiferum lost a higher amount of leaf area to grasshoppers than native seedlings. In the experiments of Wolfe et al. (2004), plants from the introduced range of Silene latifolia had a higher susceptibility to fungal infection, fruit predation and aphid infestation than plants from the native range. Similarly, IP plants of Spartina alterniflora showed lower resistance to a specialist herbivore with associated reduced growth and higher mortality (Daehler & Strong 1997); however, the NP plants with higher resistance also showed a higher intrinsic growth rate. Bossdorf et al. (2004a) demonstrated a specialist herbivore to cause higher herbivore damage in invasive than in native provenances of Alliaria petiolata, but no differences between provenances emerged with respect to plant fitness after simulated herbivory. Stastny et al. (2005) presented experimental results in which invasive plants of Senecio jacobaea grew larger, had a higher reproductive output and were consumed more by a specialist herbivore than native plants. In contrast, in a study by van Kleunen & Schmid (2003) using the same simulated herbivory regime for both provenances, native Solidago canadensis plants did not grow or reproduce more strongly than IP plants. In addition, Willis et al. (1999) could not find significant intraspecific variation in herbivore resistance between NP and IP plants of Lythrum salicaria. These diverse results suggest that the responses of NP and IP plants to herbivory are species-specific and may also depend on the life stages of plants and on the herbivores used.

what is the basis of the differences between provenances?

It is unlikely that the observed differences in life-history traits between provenances were due to climatic differences (e.g. Modrzynski & Eriksson 2002; Olsson & Agren 2002; Jakobs et al. 2004) because the plants not only grow in similar habitats but also are found under similar climatic conditions. It is also unlikely that they are the result of maternal effects (Willis et al. 2000) because plants were raised from seeds or root fragments and cultivated for more than one year under the same conditions before being planted into the experimental plots. Furthermore, we only used plants with a similar rosette diameter. For seedling experiments only seeds from the F2 generation were used.

For all these reasons we suppose that there is a genetic basis to the differences we observed between NP and IP plants, as proposed by the EICA hypothesis. Only B. orientalis showed almost no differences between NP and IP plants, probably because of the relatively small spatial separation between the two study provenances in Europe. Furthermore, both sets of plants occur in very similar environmental conditions and are exposed to a similar suite of herbivores. For the other species, our results also suggest that slug herbivory is not one of the causal factors underlying the genetic differentiation, though this could be because the time since introduction has been too short for any differences in the level of herbivory to be reflected in genetic differences between the native and introduced provenances (cf. Janzen & Martin 1982; Williamson 1996). While the genetic differences may reflect a post-introduction evolutionary change, another possibility is that the genetic differences are the result of founder effects (e.g. Sakai et al. 2001; Stastny et al. 2005).

We suggest that factors other than herbivory, perhaps different competition conditions in the native and invasive ranges, were responsible for the differences between IP and NP plants in our set of species (cf. Müller-Schärer & Steinger 2003; Vilàet al. 2003). For instance, B. orientalis and R. austriaca are rather weak competitors, but show highly plastic growth, which helps them to escape from competition with neighbouring plants in Europe and which may be advantageous in unpredictable habitats (Dietz & Steinlein 1998; Dietz et al. 1999, 2002; Woitke & Dietz 2002). If increased plasticity causes costs (Schlichting 1986; Via 1994), one possibility is that it could be advantageous to reduce plasticity under lower competition pressure as probably present in human-disturbed habitats of North America (cf. Mack 1989) and to reallocate the resources to other favourable plant traits. This hypothesis is contradictory to the suggestions that increased phenotypic plasticity in general should be advantageous for the invasiveness of plants in the introduced range (e.g. Sakai et al. 2001) but is supported by some studies. For example, Bossdorf et al. (2004b) showed that native plants of Alliaria petiolata (Brassicaceae) from Europe outcompeted invasive ones from North America. They attributed this result to reduced competition pressure in the new range of the species (evolution of reduced competitive ability, ERCA).

effects of herbivores

A further reason for the lack of differences in grazing damage between provenances may be the choice of slugs as herbivores. Different species and types of enemies can have different impacts on host plants and lead to variable responses (Wolfe 2002), particularly due to feeding on other parts of the plant (e.g. Coleman & Leonard 1995). Bossdorf et al. (2004a) showed that feeding damage to Alliaria petiolata by a specialist weevil (Coleoptera: Curculionidae) was higher on plants of invasive provenance. However, when the authors used a generalist herbivore (caterpillar) there were no differences between plants of native and invasive provenance. In contrast, other studies showed that generalists, including slugs and snails, can have different impacts on plants taken from the native and introduced range (Cates 1975; Wolfe 2002) and can be suitable herbivores to test the EICA hypothesis (Siemann & Rogers 2003). In our study, we have some indication that we would not find differences due to provenance even if we had used a specialist herbivore. Adults of two species of herbivores specializing on Brassicaceae occurred spontaneously in the common garden experiment; one was the flea beetle Phyllotreta atra (F), found on B. vulgaris, and the other was P. undulata (Kutsch.), found on R. austriaca. In neither case, however, did the percentage of damaged leaves due to flea beetle herbivory vary between the NP and IP plants (in both cases between 20 and 40%) though there were differences between species.

Although the amount of slug herbivory varied considerably among species there were no differences between provenances in either damage to or death of plants due to slugs. There was also no evidence of longer term mortality effects due to possible interactions between herbivory and other factors such as competition and drought (cf. Fenner 1987). The differences among species were fairly consistent across the various experiments, suggesting that these results are robust. Furthermore, they correspond well with those of a parallel study that revealed high variation in slug herbivory among six Brassicaceae species but no significant differences between invasive and native species in central Europe (Buschmann 2004).

Most Brassicaceae produce a range of glucosinolate compounds (Fahey et al. 2001), some of which are known to function as feeding deterrents to slugs (e.g. Giamoustaris & Mithen 1995; Byrne & Jones 1996). Allocation of resources to chemical defence is widely seen as a trade-off associated with reduced growth rates for mature plants (Herms & Mattson 1992; Vrieling & van Wijk 1994). Our results suggest that there may be a lower investment in chemical defence in faster growing species such as R. austriaca, possibly as the result of such a trade-off. The lack of differences in grazing between native and introduced provenances may be a result of short-term deterrent production. However, if inducible defences did play a role in the feeding behaviour of the slugs in the common garden and seedling experiments we would expect differences between the provenances, particularly in the leaf disc experiments where only fresh leaf material from undamaged plants was used.

There was also considerable variation between species in their response to slug herbivory. Barbarea vulgaris showed a decreased number of seeds and delayed flowering after slug damage and was obviously not able to compensate for the loss of resources due to leaf area removal. Decreasing fecundity and later flowering after removal of leaf material have been reported in several other studies with non-clonal species, including some using slugs as herbivores (e.g. Cates 1975; Dirzo & Harper 1980; Crawley 1989, references therein; Strauss et al. 2002). In contrast, the clonal species C. draba and R. austriaca had the possibility to compensate for slug damage, probably drawing on stored resources in their lateral roots (cf. Dietz & Steinlein 2001, references therein).

the role of sexual vs. clonal propagation

Our data provide support for the idea of a trade-off between clonal propagation and seed production in clonal plant populations, as suggested by Eriksson (1997). In R. austriaca and C. draba, which propagate mainly by lateral roots, higher growth in the invasive populations was associated with lower fecundity or lower seed mass, suggesting that IP plants of these species tend to allocate more resources to growth rather than to sexual reproduction. Although the growth of lateral roots was not explicitly measured in our study we assume that higher vegetative growth indicates a higher investment to clonal propagation (cf. Konvalinková 2003). Similarly, the clonal grass Poa bulbosa exhibits mainly sexual reproduction in the native range, whereas it reproduces predominantly vegetatively in its introduced range (Novak & Welfley 1997). Pysek (1997) listed a number of factors promoting the invasion process of clonal plants compared with non-clonal plants. Among other things he pointed out that clonal spread is not delayed, as is reproduction by seed, by a more or less protracted pre-reproductive phase. A further argument that is supported by our results could be that root regenerates are less vulnerable than seedlings to predation. Although a higher proportion of root regenerates was damaged, at least in C. draba, we could show for both species that their survival after herbivory was higher than that of seedlings. It may be generally the case for invasive plants that root propagules are favoured over seedlings, especially in the early phase of an invasion and where there is strong pressure from generalist herbivores. Seedling recruitment may become more important later in the invasion process because it enables long-distance dispersal and the occupation of new habitats, for example to escape from local crowding (e.g. Nishitani et al. 1999). In contrast to our results, Auge & Brandl (1997) showed a high level of seedling recruitment in Mahonia aquifolium, a clonal shrub invasive in Europe; in this study up to 50% of new ramets in an invaded area originated from sexual reproduction. In addition, Jakobs et al. (2004) demonstrated that populations of the clonal Solidago gigantea invading Europe had both a higher seed production and a higher vegetative growth. A possible explanation would be that the clonal Brassicaceae species (C. draba, R. austriaca) are rather at the beginning of their invasion in America (e.g. Voss 1985; USDA 2002) while S. gigantea, for example, was introduced to Europe 250 years ago and started spreading after 100 years (Jakobs et al. 2001). Because there has been little time for microevolution to occur, C. draba and R. austriaca rely on dispersal through root fragments rather than on dispersal through seeds, as described by Dietz et al. (2002) for R. austriaca. Alternatively, competition pressure may be reduced in North America compared with Europe in habitats where these species mainly occur (cf. Baker 1986; Mack 1989; Bossdorf et al. 2004a), and this could favour clonal propagation of invasive plants in North America due to a diminished need to escape local crowding.

Conclusions

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. Supplementary material
  10. References

Our results show that for three out of the four species studied, the vegetative performance of plants from invasive provenances is higher than that of plants from native provenance. While these findings are consistent with the EICA hypothesis, there were no indications in any of the bioassay experiments of the predicted higher attractiveness of the IP plants to herbivores.

Time since introduction may have been too short for differences in herbivore pressure to have resulted in a loss of defensive traits. Alternatively, reduced competition pressure could favour vegetative propagation in clonal plants, at least during the early phase of invasion.

It is not yet possible to generalize about the importance of release from herbivory as a factor promoting invasion. There is a need for more comparative experimental studies to investigate the influence of antagonists (generalist and specialist herbivores and pathogens) on growth and reproduction of plants at different life stages and exhibiting contrasting reproductive strategies. Our understanding of invasions, for example, might be increased by studying herbivore effects on invasive plants under different competition regimes.

Acknowledgements

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. Supplementary material
  10. References

We thank Steffen Schürkens, Anja Klingenböck, Baptiste Laville, Rolf Debrunner, Stephanie Halsdorf, Markus Kläui and Stefan Kuhn for help in the field and laboratory. Johannes Kollmann, Sabine Güsewell, Lindsay Haddon and two anonymous referees provided helpful comments on the manuscript. This project was funded through grants from the German Research Foundation (DFG) and the Swiss Federal Institute of Technology Zurich (ETHZ) to HD.

References

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. Supplementary material
  10. References
  • Auge, H. & Brandl, R. (1997) Seedling recruitment in the invasive clonal shrub, Mahonia aquifolium Pursh (Nutt.). Oecologia, 110, 205211.
  • Baker, H.G. (1986) Patterns of plant invasion in North America. Ecology of Biological Invasions of North America and Hawaii (eds H.A.Mooney & J.A.Drake), pp. 4457. Springer-Verlag, Berlin.
  • Blossey, B. & Nötzold, R. (1995) Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. Journal of Ecology, 83, 887889.
  • Bossdorf, O., Prati, D., Auge, H. & Schmid, B. (2004a) Reduced competitive ability in an invasive plant. Ecology Letters, 7, 346535.
  • Bossdorf, O., Schröder, S., Prati, D. & Auge, H. (2004b) Palatibility and tolerance to simulated herbivory in native and introduced populations of Alliaria petiolata (Brassicaceae). American Journal of Botany, 91, 856862.
  • Briner, T. & Frank, T. (1998) The palatability of 78 wildflower strip plants to the slug Arion lusitanicus. Annals of Applied Biology, 133, 123133.
  • Bruelheide, H. & Scheidel, U. (1999) Slug herbivory as a limiting factor for the geographical range of Arnica montana. Journal of Ecology, 87, 839848.
  • Bullock, J.A. & Smith, P.H. (1971) The relation between dry and fresh weight in some caterpillars. Entomologia Experimentalis et Applicata, 14, 125131.
  • Buschmann, H. (2004) Studies of herbivory in native and invasive plant populations. PhD thesis. ETH, Zurich.
  • Buschmann, H., Edwards, P.J. & Dietz, H. (2002) Does herbivory by slugs influence the invasiveness of Brassicaceae? Bulletin of the Geobotanical Institute ETH, 68, 7381.
  • Buschmann, H., Keller, M., Porret, N., Dietz, H. & Edwards, P.J. (2005) The effect of slug grazing on vegetation development and plant species diversity in an experimental grassland. Functional Ecology, doi :10.1111/j.1365-2435.2005.00960.x
  • Byrne, J. & Jones, P. (1996) Responses to glucosinolate content in oilseed rape varieties by crop pest (Deroceras reticulatum) and non-pest slug species (Limax pseudoflavus). Annals of Applied Biology, 128, 7879.
  • Cates, R.G. (1975) The interface between slugs and wild ginger: some evolutionary aspects. Ecology, 56, 391400.
  • Cates, R.G. & Orians, G.H. (1975) Successional status and the palatability of plants to generalized herbivores. Ecology, 56, 410418.
  • Coleman, J.S. & Leonard, A.S. (1995) Why it matters where on a leaf a folivore feeds. Oecologia, 101, 324328.
  • Coley, P.D., Bryant, J.P. & Chapin, F.S. (1985) Resource availability and plant anti-herbivore defense. Science, 230, 895899.
  • Crawley, M.J. (1989) Insect herbivores and plant population dynamics. Annual Review of Entomology, 34, 531564.
  • Daehler, C.C. & Strong, D.R. (1997) Reduced herbivore resistance in introduced smooth cordgrass (Spartina alterniflora) after a century of herbivore-free growth. Oecologia, 110, 99108.
  • Dietz, H., Köhler, A. & Ullmann, I. (2002) Regeneration growth of the invasive clonal forb Rorippa austriaca (Brassicaceae) in relation to fertilization and interspecific competition. Plant Ecology, 158, 171182.
  • Dietz, H. & Steinlein, T. (1996) Determination of plant species cover by means of image analysis. Journal of Vegetation Science, 7, 131136.
  • Dietz, H. & Steinlein, T. (1998) The impact of anthropogenic disturbance on life stage transitions and stand regeneration of the invasive alien plant Bunias Orientalis L. Plant Invasions – Ecological Mechanisms and Human Responses (eds K.Edwards et al.), pp. 169184. Backhuys, Leiden.
  • Dietz, H. & Steinlein, T. (2001) Ecological aspects of clonal growth in plants. Progress in Botany, 62, 511530.
  • Dietz, H., Steinlein, T. & Ullmann, I. (1999) Establishment of the invasive perennial herb Bunias orientalis L.: an experimental approach. Acta Oecologica, 20, 113.
  • Dietz, H. & Ullmann, I. (1998) Ecological application of ‘herbchronology’: comparative stand age structure analyses of the invasive plant Bunias orientalis L. Annals of Botany, 82, 471480.
  • Dirzo, R. (1980) Experimental studies on slug–plant interactions. I. The acceptability of thirty plant species to the slug Agriolimax caruanae. Journal of Ecology, 68, 981998.
  • Dirzo, R. & Harper, J.L. (1980) Experimental studies on slug–plant interactions. II. The effect of grazing by slugs on high density monocultures of Capsella bursa-pastoris and Poa annua. Journal of Ecology, 68, 9991011.
  • Eriksson, O. (1997) Clonal life histories and the evolution of seed recruitment. The Ecology and Evolution of Clonal Plants (eds H.De Kroon & J.Van Groenendael), pp. 211226. Backhuys, Leiden.
  • Fahey, J.W., Zalcmann, A.T. & Talalay, P. (2001) The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry, 56, 551.
  • Fechter, R. & Falkner, G. (1989) Weichtiere. Mosaik Verlag, München.
  • Fenner, M. (1987) Seedlings. New Phytologist, 106, 3547.
  • Frank, T. (1998) Slug damage and numbers of the slug pests, Arion lusitanicus and Deroceras reticulatum, in oilseed rape grown beside sown wildflower strips. Agriculture, Ecosystems and Environment, 67, 6778.
  • Frank, T. & Friedli, J. (1999) Laboratory food choice trials to explore the potential of common weeds to reduce slug feeding on oilseed rape. Biology Agriculture and Horticulture, 17, 1929.
  • Giamoustaris, A. & Mithen, R. (1995) The effect of modifying the glucosinolate content of leaves of oilseed rape (Brassica napus ssp. oleifera) on its interaction with specialist and generalist pests. Annals of Applied Biology, 126, 347363.
  • Hanley, M.E., Fenner, M. & Edwards, P.J. (1995a) An experimental field study of the effects of mollusc grazing on seedling recruitment and survival in grassland. Journal of Ecology, 83, 621627.
  • Hanley, M.E., Fenner, M. & Edwards, P.J. (1995b) The effect of seedling age on the likelihood of herbivory by the slug Deroceras reticulatum. Functional Ecology, 9, 754759.
  • Hedge, I.C. (1976) A systematic and geographical survey of the old world Cruciferae. The Biology and Chemistry of the Cruciferae (eds J.G.Vaughan, A.J.MacLeod & B.M.G.Jones), pp. 145. Academic Press, London.
  • Hegi, G. (1986) Angiospermae: Dicotyledones 2. Teil 1. Illustrierte Flora Von Mitteleuropa. (eds H.J.Conert, U.Hamann, W.Schultze-Motel & G.Wagenitz). Paul Parey, Berlin.
  • Herms, D.A. & Mattson, W.J. (1992) The dilemma of plants: to grow or to defend. Quarterly Reviews in Biology, 67, 283335.
  • Hierro, J.L., Maron, J.L. & Callaway, R.M. (2005) A biogeographical approach to plant invasions: the importance of studying exotics in their introduced and native range. Journal of Ecology, 93, 515 .
  • Hulme, P.E. (1996) Herbivores and the performance of grassland plants: a comparison of arthropod, mollusc and rodent herbivory. Journal of Ecology, 84, 4351.
  • Jakobs, G., Weber, E. & Edwards, P.J. (2004) Introduced plants of the invasive Solidago gigantea (Asteraceae) are larger and grow denser than conspecifics in the native range. Diversity and Distributions, 10, 1119.
  • Jakobs, G., Weber, E., Meyer, G.A. & Edwards, P.J. (2001) Life-history and genetic variation of native vs. introduced populations of the perennial Solidago gigantea Ait. (Asteraceae). Bulletin of the Geobotanical Institute ETH, 67, 7378.
  • Jalas, J. & Suominen, J. (1994) Atlas Florae Europaeae, 10 – Cruciferae (Ricotia to Raphanus). Helsinki.
  • Jalas, J., Suominen, J. & Lampinen, R. (1996) Atlas Florae Europaeae, 11 – Cruciferae (Sisymbrium to Aubrieta) , Helsinki.
  • Janzen, D.H. & Martin, P.S. (1982) Neotropical anachronisms: the fruits the Gomphoteres ate. Science, 215, 1927.
  • Keane, R.M. & Crawley, M.J. (2002) Exotic plant invasions and the enemy-release hypothesis. Trends in Ecology and Evolution, 17, 164170.
  • Keller, M., Kollmann, J. & Edwards, P.J. (1999) Palatability of weeds from different European origins to the slugs Deroceras reticulatum Müller and Arion lusitanicus Mabille. Acta Oecologica, 20, 109118.
  • Van Kleunen, M. & Schmid, B. (2003) No evidence for an evolutionary increased competitive ability (EICA) in the invasive plant Solidago canadensis. Ecology, 84, 28162823.
  • Konvalinková, P. (2003) Generative and vegetative reproduction of Helianthus Tuberosus, an invasive plant in Central Europe. Plant Invasions: Ecological Threats and Management Solutions (eds L.E.Child et al.), pp. 289299. Backhuys, Leiden.
  • Leger, E.A. & Rice, K.J. (2003) Invasive California poppies (Eschscholzia californica Cham.) grow larger than native individuals under reduced competition. Ecology Letters, 6, 257264.
  • Louda, S.M., Keeler, K.H. & Holt, R.D. (1990) Herbivore influences on plant performance and competitive interactions. Perspectives in Plant Competition (eds J.B.Grace & D.Tilman), pp. 2749. Academic Press, New York.
  • Mack, R.N. (1989) Temperate grasslands vulnerable to plant invasions: characteristics and consequences. Biological Invasions A Global Perspective (ed. J.A.Drake, et al. ), pp. 155179. John Wiley, Chichester.
  • McCracken, G.F. & Selander, R.J. (1980) Self-fertilization and monogenic strains in natural populations of terrestrial slugs. Proceedings of the National Acadamy of Sciences of the USA, 77, 684688.
  • Modrzynski, J. & Eriksson, G. (2002) Response of Picea abies populations from elevational transects in the Polish Sudety and Carpathian mountains to simulated drought stress. Forest Ecology and Management, 165, 105116.
  • Moens, R. (1989) Factors affecting slug damage and control measure decisions. BCPC Monograph, no. 41. Slugs and Snails in World Agriculture. (ed. I.H.Henderson), pp. 227236.
  • Müller-Schärer, H. & Steinger, T. (2003) Predicting evolutionary change in invasive, exotic plants and its consequences for plant–herbivore interactions. Genetics, Evolution and Biology Control (eds L.E.Ehler, R.Sforza & T.Mateille), pp. 137162. CAB International, Wallingford.
  • Mutikainen, P. & Walls, M. (1995) Growth, reproduction and defence in nettles: responses to herbivory modified by competition and fertilization. Oecologia, 104, 487495.
  • Nishitani, S., Takenori, T. & Kachi, N. (1999) Optimal resource allocation to seeds and vegetative reproduction under density-dependent regulation in Syneilesis palmata (Compositae). Plant Ecology, 141, 179189.
  • Novak, S.J. & Welfley, A.Y. (1997) Genetic diversity in the introduced clonal grass Poa bulbosa (Bulbous bluegrass). Northwest Science, 71, 271280.
  • Oberdorfer, E. (1990) Pflanzensoziologische Exkursionsflora. Ulmer, Stuttgart.
  • Oliveira Silva, M.T. (1992) Effects of mollusc grazing on the development of grassland species. Journal of Vegetation Science, 3, 267270.
  • Olsson, K. & Agren, J. (2002) Latitudinal population differentiation in phenology, life history and flower morphology in the perennial herb Lythrum salicaria. Journal of Evolutionary Biology, 15, 983996.
  • Pysek, P. (1997) Clonality and plant invasions: can a trait make a difference. The Ecology and Evolution of Clonal Plants (eds H.De Kroon & J.Van Groenendael), pp. 211226. Backhuys, Leiden.
  • Rathcke, B. (1985) Slugs as generalist herbivores: tests of three hypotheses on plant choices. Ecology, 66, 828836.
  • Rees, M. & Brown, V.K. (1992) Interactions between invertebrate herbivores and plant competition. Journal of Ecology, 80, 353360.
  • Reischütz, P.L. (1986) Die Verbreitung der Nacktschnecken Österreichs (Arionidae, Milacidae, Limacidae, Agrolimacidae, Bottgerillidae). Catalogus Faunae Austriae Suppl. 2, 67159.
  • Rodríguez, M.A. & Brown, V.K. (1998) Plant competition and slug herbivory: effects on the yield and biomass allocation pattern of Poa annua L. Acta Oecologica, 19, 3746.
  • Sakai, A.K., Allendorf, F.W., Holt, J.S., Lodge, D.M., Molofsky, J., With, K.A. et al. (2001) The population biology of invasive species. Annual Review of Ecology and Systematics, 32, 305332.
  • SAS Institute (2002) JMP User's Guide. SAS Institute, Cary, North Carolina.
  • Schierenbeck, K.A., Mack, R.N. & Sharitz, R.A. (1994) Effects of herbivory on growth and biomass allocation in native and introduced species of Lonicera. Ecology, 75, 16611672.
  • Schlichting, C.D. (1986) The evolution of phenotypic plasticity in plants. Annual Review of Ecology and Systematics, 17, 667693.
  • Siemann, E. & Rogers, W.E. (2001) Genetic differences in growth of an invasive tree species. Ecology Letters, 4, 514518.
  • Siemann, E. & Rogers, W.E. (2003) Reduced resistance of invasive varieties of the alien tree Sapium sebiferum to a generalist herbivore. Oecologia, 135, 451457.
  • South, A. (1992) Terrestrial Slugs – Biology, Ecology and Control. Chapman & Hall, London.
  • Stastny, M., Schaffner, U. & Elle, E. (2005) Do vigour of introduced populations and escape from specialist herbivores contribute to invasiveness? Journal of Ecology, 93, 2737 .
  • Strauss, S.Y., Rudgers, J.A., Lau, J.A. & Irwin, R.E. (2002) Direct and ecological costs of resistance to herbivory. Trends in Ecology and Evolution, 17, 278285.
  • USDA (2002) The PLANTS Database, Version 3.5 (http://plants.usda.gov). National Plant Data Center, Baton Rouge, Louisiana, USA.
  • Via, S. (1994) The evolution of phenotypic plasticity: what do we really know? Ecological Genetics (ed. L.Real), pp. 3585. Princeton University Press, Princeton, New Jersey.
  • Vilà, M., Gómez, A. & Maron, J.L. (2003) Are alien plants more competitive than their native conspecifics? A test using Hypericum perforatum L. Oecologia, 137, 211215.
  • Voss, E.G. (1985) Michigan Flora, Part II. Dicots. Cranbrook Institute of Science, Bloomfield Hills, Michigan.
  • Vrieling, K. & Van Wijk, C.A.M. (1994) Cost assessment of the production of pyrrolizidine alkaloids in ragwort (Senecio jacobea). Oecologia, 97, 541546.
  • Waldbauer, G.P. (1968) The consumption and utilization of food by insects. Advances in Insect Physiology, 5, 229289.
  • Williamson, M. (1996) Biological Invasions. Chapman & Hall, London.
  • Willis, A.J., Memmott, J. & Forrester, R.I. (2000) Is there evidence for the post-invasion evolution of increased size among invasive plant species. Ecological Letters, 3, 275283.
  • Willis, A.J., Thomas, M.B. & Lawton, J.H. (1999) Is the increased vigour of invasive weeds explained by a trade-off between growth and herbivore resistance. Oecologia, 120, 632640.
  • Woitke, M. (2001) Artenkombination, Etablierungsstadium und anthropogenes Störungsregime als Einflussfaktoren auf die Bestandesentwicklung der invasiven Brassicaceae Bunias orientalis L. und Rorippa austriaca (Crantz) Besser in experimenteller Vegetation. PhD thesis. University of Würzburg, Würzburg.
  • Woitke, M. & Dietz, H. (2002) Shifts in dominance of native and invasive plants in experimental patches of vegetation. Perspectives in Plant Ecology, Evolution and Systematics, 5, 165184.
  • Wolfe, L.M. (2002) Why alien invaders succeed: support for the escape-from-enemy hypothesis. American Naturalist, 160, 705711.
  • Wolfe, L.M., Elzinga, J.A. & Biere, A. (2004) Increased susceptibility to enemies following introduction in the invasive plant Silene latifolia. Ecology Letters, 7, 813820.