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Year: 2009
Enhanced fitness due to higher fecundity, increased defence against a specialist and tolerance towards a generalist herbivore in an invasive annual plant
Abhilasha, D ; Joshi, J
Abstract: Aims: The superior performance of many non-indigenous species in a new range can be attributed to different factors such as pre-adaptation to environmental conditions in new areasorto factors inherent to displacement mechanisms such as loss of co-evolved pathogens and herbivores that increase the speed of evolutionary change towards a shift in allocation from defence to growth and reproduction. To assess the importance of the different mechanisms governing the success of Conyza canadensis, a globally successful invader, we simultaneously tested several recent hypotheses potentially explaining the factors leading to biological invasion. Methods: We tested (i) whether plants from the non-native range showed a higher fitness than plants from the native North American range, (ii) whether they differed in resistance against an invasive generalist herbivore, the slug Arion lusitanicus andagainst a recently established specialist aphid herbivore, Uroleucon erigeronense and (iii) experimentally assessed whether C. canadensis releases allelopathic chemicals that have harmful effects on competing species in the non-native range. We compared populations along a similar latitudinal gradient both in the native North American and invasive European range and analysed patterns of adaptive clinal variation in biomass production. Important Findings: The invasion success of C. canadensis in Europe cannot be attributed to a single trait, but to a combination of factors. Invasive plants benefited from increased growth and above all, increased reproduction (a key trait in an annual plant) and were less attacked by a co-migrated specialist enemy. The observed loss of defence against generalist slugs did not translate into a decreased fitness as invasive C. canadensis plants showed a high re-growth potential. In contrast to earlier invitro studies, we detected no allelopathic effects on the competing flora in the non-native range. The latitudinal cline in vegetative biomass production in the non-native range observed in our common garden study indicates a high adaptive potential. However, only further genetic studies will provide conclusive evidence whether the differentiation in the non-native range is caused by pre-adaptation and sorting-out processes of putatively repeatedly introduced populations of this composite, long-distance disperser with highly volatile seeds or evolved de novo as a rapid response to new selection pressures in the non-native range.
DOI: https://doi.org/10.1093/jpe/rtp008
Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-19868 Journal Article
Originally published at: Abhilasha, D; Joshi, J (2009). Enhanced fitness due to higher fecundity, increased defence against a specialist and tolerance towards a generalist herbivore in an invasive annual plant. Journal of Plant Ecology, 2(2):77-86. DOI: https://doi.org/10.1093/jpe/rtp008
2 Enhanced fitness due to higher fecundity, increased defence against a specialist and tolerance towards a generalist herbivore in an invasive annual plant
D. Abhilasha and J. Joshi1*
Institute of Environmental Sciences, University of Zurich, Winterthurerstrasse 190, CH-8057
Zurich, Switzerland; *Author for correspondence (Telephone: ++41 (0)44 635 4747, Fax:
++41 (0)44 635 5711, e-mail: [email protected])
1Present address: Institute of Biochemistry and Biology, Biodiversity Research/Botany,
University of Potsdam, Maulbeerallee 1, 14469 Potsdam, Germany
Running title: Fitness and defence in an invasive annual plant.
1 Abstract 2 3 Aims
4 The superior performance of many non-indigenous species in a new range can be attributed to
5 different factors such as pre-adaptation to environmental conditions in new areas or to factors
6 inherent to displacement mechanisms such as loss of co-evolved pathogens and herbivores
7 that increase the speed of evolutionary change towards a shift in allocation from defence to
8 growth and reproduction. To assess the importance of the different mechanisms governing the
9 success of Conyza canadensis, a globally successful invader, we simultaneously tested several
10 recent hypotheses potentially explaining the factors leading to biological invasion.
11 Methods
12 We tested 1) whether plants from the non-native range showed a higher fitness than plants
13 from the native North American range, 2) whether they differed in resistance against an
14 invasive generalist herbivore, the slug Arion lusitanicus, and against a recently established
15 specialist aphid herbivore, Uroleucon erigeronense, and 3) experimentally assessed whether
16 C. canadensis releases allelopathic chemicals that have harmful effects on competing species
17 in the non-native range. We compared populations along a similar latitudinal gradient both in
18 the native North American and invasive European range and analysed patterns of adaptive
19 clinal variation in biomass production.
20 Important findings
21 The invasion success of C. canadensis in Europe cannot be attributed to a single trait, but to a
22 combination of factors. Invasive plants benefited from increased growth and above all,
23 increased reproduction (a key trait in an annual plant) and were less attacked by a co-migrated
24 specialist enemy. The observed loss of defence against generalist slugs did not translate into a
25 decreased fitness as invasive C. canadensis plants showed a high re-growth potential. In
26 contrast to earlier in-vitro studies, we detected no allelopathic effects on the competing flora
27 in the non-native range. The latitudinal cline in vegetative biomass production in the non- 1 native range observed in our common garden study indicates a high adaptive potential.
2 However, only further genetic studies will provide conclusive evidence whether the
3 differentiation in the non-native range is caused by pre-adaptation and sorting-out processes
4 of putatively repeatedly introduced populations of this composite, long-distance disperser
5 with highly volatile seeds or evolved de novo as a rapid response to new selection pressures in
6 the non-native range.
7
8 Keywords Allelopathy, biological invasions, Conyza canadensis, EICA hypothesis, 9 generalist/specialist herbivory, latitudinal clines, biogeographic comparison, common garden
3 1 Introduction 2
3 The superior performance of many non-indigenous species in new areas can be attributed to a
4 range of economic, climatic, and life-history factors (Lin et al. 2007; Sax et al. 2007) such as
5 pre-adaptation to environmental conditions in the new range (Sax and Brown 2000) or to
6 factors inherent to the displacement mechanism (mainly the loss of co-evolved biota) that
7 increase the speed of evolutionary change towards a shift in allocation from defence to growth
8 and reproduction (Blossey and Nötzold 1995; Bossdorf et al. 2005). There is increasing
9 evidence that strong selection pressures can induce rapid adaptive genetic change provided
10 that ample additive genetic variation is present in populations (Thompson 1998; Bossdorf et
11 al. 2005; Carroll et al. 2005; Sax et al. 2007; Prentis et al. 2008). The sudden absence of
12 specialist natural enemies should impose a strong selection pressure towards genotypes with
13 reduced resource allocation to defence and high investment in traits associated with
14 competitive ability (Blossey and Nötzold 1995; Keane and Crawley 2002; Joshi and Vrieling
15 2005). Therefore, plants in the non-native range that are no longer attacked by specialised
16 herbivores (Mitchell et al. 2006) should grow with higher vigour or have a higher
17 reproductive output and lower levels of defensive metabolites if such defences are costly, than
18 plants of the same species in the native range (Muller and Martens 2005). If, however,
19 defences are not costly, and provide a selective advantage against generalist herbivores in the
20 new range, then invasive plants may still be well protected in their new range and have a
21 higher fitness than native competing species (Joshi and Vrieling 2005).
22 An alternative mechanism based on pre-adaptation that explains the establishment and
23 spread of invasive plants is the release of allelochemicals by the invader (Rabotnov 1982,
24 Callaway and Aschehoug 2000; Cappuccino and Arnason 2006). Allelopathic compounds that
25 have phytotoxic or at least fitness-reducing effects may be novel for plant competitors without
26 a co-evolutionary history (Hierro and Callaway 2003; Prati and Bossdorf 2004; Schenk 2006).
4 1 These non-coevolved competitors may be more susceptible to novel phytochemicals than
2 adapted plant neighbours in the native range (Callaway and Aschehoug 2000).
3 To date, most of the studies comparing life-history traits between successful plant
4 invaders in temperate native and non-native ranges have focused on perennial plants
5 (Bossdorf et al. 2005). Comparatively fewer studies have focused on life-history differences
6 between native and invasive populations of annual species (e.g. Novak et al. 1991; Prieur-
7 Richard et al. 2002; Kollmann and Banuelos 2004; Leger and Rice 2007; McKenney et al.
8 2007), which innately possess a range of weedy traits (Thébaud et al. 1996), especially if self-
9 compatible (Stebbins 1957; van Kleunen and Johnson 2005).
10 Canadian horseweed (Conyza canadensis L. Cronq.) is a winter-annual, self-
11 compatible species native to North America, which was introduced to mid-Europe and to the
12 Mediterranean about 350 years ago (Wein 1932; Lohmeyer and Sukopp 1992; Clement and
13 Foster 1994) and has recently become established in New Zealand and Asia (Webb 1987),
14 colonising to date even remote island habitats in New Caledonia, around Tasmania and
15 Mauritius (Rozefelds et al. 1999; N. Zuël pers. comm.). In the native North American range,
16 weedy C. canadensis plants is an increasing problem in agriculture as they have developed
17 resistance to glyphosate in cropland where glyphosate-resistant soybeans are grown (Dauer et
18 al. 2007).
19 To assess the relative significance of the different mechanisms governing the success
20 of invasive species it is necessary to simultaneously test the enemy release and other non-
21 mutually exclusive hypotheses such as the novel weapons hypothesis (see Liu and Stiling
22 2006). Therefore, we performed an array of experiments to elucidate the traits explaining the
23 invasion success of C. canadensis. In native North American populations and in invasive
24 populations from Europe, we studied whether invasive plants 1) have a higher competitive
25 ability in the new range, 2) show a shift in allocation from defence to growth, and/or 3)
26 release allelopathic compounds harmful to competing plant species in the non-native range.
5 1 We included a similar latitudinal gradient both in the native and non-native range in our
2 experimental design as adaptive clinal variation has been shown to influence establishment
3 and success of invasive species (Weber and Schmid 1998; Kollmann and Banuelos 2004;
4 Maron et al. 2004; Leger and Rice 2007; Colautti et al. 2008; Etterson et al. 2008; Montague
5 et al. 2008).
6
7 Materials and Methods
8 Study species
9 Conyza canadensis (L.) Cronq. (Synonym: Erigeron canadensis L.; horseweed or Canada
10 fleabane) is a diploid (Thébaud and Abbott 1995), self-compatible (Mulligan and Findlay
11 1970), winter-annual plant (Weaver 2001) with a high seed output (more than 100,000 seeds
12 per plant have been reported; Shields et al. 2006). The seeds are highly volatile to the extent
13 that they even reach the planetary boundary layer of the atmosphere (Shields et al. 2006). C.
14 canadensis is native to North America (Weaver 2001), but to date, it is globally distributed
15 along roadsides, field margins and abandoned fields (Corlett 1992; Rozefelds et al. 1999; Kim
16 2002; Weaver 2001; Prieur-Richard et al. 2002). In Europe, it has been recorded as early as
17 1646 in Germany and 1690 in London (Wein 1932; Lohmeyer and Sukopp 1992; Clement
18 and Foster 1994) and recently it has been reported as being introduced to New Zealand (Webb
19 1987). In Europe, C. canadensis is susceptible to mollusc and insect herbivory (Prieur-
20 Richard et al. 2002) and its defence chemistry is characterised by the presence of
21 monoterpenes and sesquiterpenes (Hrutfiord et al. 1988), which have been shown to have
22 anti-herbivore activity (Harborne 1993). Earlier experiments using powdered plant material or
23 aqueous extracts demonstrated that C. canadensis contains four phenolic compounds
24 exhibiting a range of allelopathic impacts on different crop plants (Shaukat et al. 2003).
25
26 Growth and reproduction
6 1 C. canadensis seedlings of eight native populations from North America, 20 invasive
2 populations from Europe, and two invasive populations from New Zealand were sown in July
3 2005 (Table 1) in controlled glasshouse conditions (25ºC day/18ºC night temperature, 60-80%
4 RH, natural light conditions). None of the populations sampled belonged to glyphosate-
5 resistant strains: In a pilot experiment, we sprayed two replicate plants per population (one
6 more set of unsprayed replicate plants were treated as controls) with two different
7 concentrations (2% and 1%) of glyphosate and compared survival to unsprayed plants. All the
8 sprayed plants died, whereas all unsprayed control plants survived.
9 Of each population, ten seedlings belonging to five maternal genotypes (two
10 individuals per maternal genotype) were randomly picked and transplanted into pots
11 measuring 11x11x12cm containing peat soil and sand (1:1). The pots were organized in five
12 blocks with each block containing two plants from each population. As native plants had a
13 higher mortality (see results) there were often three maternal genotypes left per population.
14 Mortality was assessed after three months and the final survival rate was recorded after one
15 year of plant growth. After three months, the (1) height of the plant, (2) the number of leaves,
16 and (3) the rosette diameter were recorded. Biomass measures were obtained from control
17 plants in the herbivory experiment (see below). Plants were harvested when senescence
18 began, i.e. at the seeding stage. The flowering parts of the plants were covered by white
19 perforated cloth in order to harvest the cumulative reproductive biomass including volatile
20 seeds.
21 The ploidy level of eight native American, 20 invasive European and two New
22 Zealand populations (one sample per population; Table 1) was determined by flow cytometry
23 with fresh leaf material (Partec, Münster, Germany: see Schlaepfer et al. 2008 for a
24 description of the ploidy determination). We found a putatively higher ploidy level in invasive
25 New Zealand Conyza plants. Mean peak values correlated with DNA content obtained by
26 flow cytometry averaged at 104.5 ± 5.3 in American and 115.3 ± 2.2 in European samples,
7 1 whereas New Zealand samples peaked at consistently higher values (213.6 ± 3.2) suggesting a
2 polyploidisation of New Zealand plants. Therefore, we excluded the New Zealand
3 populations from our analyses owing to the unresolved taxonomic identity and low number of
4 populations.
5 6 Herbivory experiments
7 Susceptibility to herbivory by generalist herbivores was tested using the generalist herbivore
8 slug Arion lusitanicus Mabille (Arionidae), which supposedly originates from the Iberian
9 Peninsula and was introduced to central Europe in the second half of 20th century by
10 international trade activities (Briner and Frank 1998; Keller et al. 1999). In a pilot study,
11 several native Swiss species of slugs were tested on C. canadensis and A. lusitanicus was
12 selected because it was the only species not showing a severely decreased fitness after feeding
13 on C. canadensis plants.
14 Susceptibility to specialist herbivory was tested using the invasive specialist herbivore
15 aphid Uroleucon erigeronense Thomas, 1878 (Aphididae) of Nearctic origin (Blackman and
16 Eastop 2006), which was first found in Europe in the 1950’s (Ripka 2004; Sefrová and
17 Lastuvka 2005) and has also been introduced to South America (Blackman and Eastop 2006).
18 This aphid is oligophagous and in the native North American range feeds and reproduces
19 preferably on the upper parts of the stems of Conyza (Sefrová and Lastuvka 2005; Blackman
20 and Eastop 2006). This aphid also feeds on closely related Erigeron species (Karban 1986;
21 Thébaud and Abbott 1995; Noyes 2000) and attacks other species within the Astereae tribe,
22 especially in the invasive South American range (Sholes 1984; Fagundes et al. 2005;
23 Blackman and Eastop 2006). In the temperate Western hemisphere, it has only been recorded
24 on C. canadensis (Blackman and Eastop 2006).
25 Using the same populations for testing the effects of generalist herbivory as for the
26 growth measurements (Table 1), we organized the pots in five blocks with each block
8 1 containing five maternal genotypes from each population. The generalist slugs (A. lusitanicus)
2 were collected in a garden in Winterthur, Switzerland and from meadows surrounding the
3 University of Zurich, Switzerland. Following collection, the generalist slugs were reared in
4 the glasshouse on a mixed diet consisting of C. canadensis, Trifolium, grasses and several
5 forbs. The initial weight of each slug was measured before the slugs were released to feed on
6 the C. canadensis plants in November 2005. The plants were individually covered with
7 plastic-cloth cages, which prevented the slugs from escaping to neighbouring plants. Slugs
8 were left to feed for three months. An equal number of caged plants without slugs served as
9 control. In February 2006, the 1) final weight of the slugs, 2) the number of leaves showing
10 marks of herbivory, 3) the height of the plant, 4) the number of leaves, and 5) the rosette
11 diameter was assessed.
12 The effect of specialist herbivory by aphids on C. canadensis was assessed between
13 August 2006 and December 2006 in an insect-proof glasshouse with natural light conditions.
14 C. canadensis seedlings of 16 populations (eight native North American and eight invasive
15 European) were selected based on the latitudes and climatic similarities of the sites of origin
16 (Table 1). Ten seedlings per population were transplanted into 10x10x11cm pots containing
17 peat soil and sand (1:1) and 1.5 g of “osmocote”, a slow release NPK fertilizer. In total, there
18 were 160 pots arranged in two blocks. In each block, five replicate plants per population were
19 used. The pots were arranged to form 16 different cross-shaped groups per block (five pots
20 per group). Each cross-shaped group comprised two plants from native origins and two plants
21 from invasive origins surrounding the centre plant. The groups were arranged at a distance of
22 0.5 m from each other. Within each block, eight cross-shaped groups had native plants in the
23 centre and eight groups had invasive plants in the centre. The positions of the groups were
24 randomised. Individuals of wingless specialist green aphids (Uroleucon erigeronensis)
25 spontaneously colonised pilot plants of C. canadensis in the glasshouse and were then
26 subsequently raised on a 1:1 mixture of native and invasive plants of all populations. Of these
9 1 aphid stock, U. erigeronensis individuals were carefully collected by tapping attacked source
2 plants and ten randomly selected healthy adult aphids were placed on each of the group-centre
3 source plants. These pots were covered with plastic-cloth cages for one week and then the
4 cages were removed allowing the free movement of the aphids between the C. canadensis
5 centre-source and the four peripheral sink plants of each cross-shaped group. After one week,
6 the initial total number of aphids on each plant was recorded. The final number of aphids was
7 counted after 42 days. Afterwards, the aphids were collected in Eppendorf tubes, lyophilised
8 for 24 hours and the aphid biomass was measured on an ultra sensitive microbalance (Mettler
9 MT5). In a pre-test for herbivory, New Zealand plants were not attacked at all by the
10 specialist aphid.
11 An additional leaf-choice experiment was conducted in Petri dishes (10 cm dimeter)
12 under glasshouse conditions (25ºC/18ºC day/night temperature, 60-80% RH, natural light
13 conditions). Plants were grown in the glasshouse until the appearance of the third whorl of
14 leaves. The oldest leaves from the third whorl were selected from two maternal genotypes of
15 18 populations in total (eight native populations from North America, ten invasive
16 populations from Europe; Table 1). The tips of the leaves from all plants were cut into pieces
17 of identical size. Two random leaf samples from different native populations and two leaf
18 samples from different invasive populations were equidistantly placed inside a Petri dish on
19 wet filter paper. In total, there were 140 different combinations in 35 Petri dishes with two
20 maternal genotypes and two replicates of each of these genotypes. One wingless adult of U.
21 erigeronensis was placed in the centre of each Petri dish before the dish was sealed with
22 Parafilm. The aphids were chosen randomly from both native and invasive source plants of C.
23 canadensis. The position of the aphid in each Petri dish was marked consecutively for the
24 next three days.
25
26 Assessment of presence of allelochemicals
10 1 To test whether the release of allelopathic compounds is responsible for the invasion success,
2 we planted C. canadensis with different competitor species from the European non-native
3 range (Lepidium campestre (L.) R. Br., Brassicaceae; Medicago lupulina L., Fabaceae; and
4 Triticum aestivum L., Poaceae) in soil with and without the addition of finely ground
5 activated carbon to the substrate. We expected the carbon addition to remove any potential
6 interference of allelopathic chemicals in the soils (Callaway and Aschehoug 2000). An
7 enhanced performance of competitor species in the presence of activated carbon is regarded as
8 an indication of the presence of allelopathic substances in the soil (Prati and Bossdorf 2004).
9 This pot experiment was performed at the experimental garden of the University of Zurich
10 (47° 33' N, 8° 37' E; 534 m a.s.l.) from April to September 2006. We mixed unsterilised
11 commercial peat soil (Tref Substrates Coervorden B.V. The Netherlands, pH 5.5) and sand
12 (1:1), added 2% (8 g) of finely ground activated carbon particle size < 0.8 mm (puriss. p.a.,
13 Fluka) and 1 g of “Osmocote”, a slow release NPK fertilizer, to each pot (11x11x12cm).
14 Fertilizer was added to each pot to minimise possible confounding effects of activated carbon
15 on nitrogen availability (Abhilasha et al. 2008; Lau et al. 2008). In each pot, we planted one
16 seedling of C. canadensis. In total, two maternal genotypes each of 30 populations (Table 1)
17 were used. For each maternal genotype, one individual was planted in pots with or without
18 activated carbon (control). Three common European potentially naïve native competitor
19 species: L. campestre, M. lupulina and T. aestivum (common wheat) were sown in the pots
20 around each C. canadensis plant (10 seeds/competitor species/pot; seeds were acquired from a
21 commercial distributor of local ecotypes, UFA Seed Company, Switzerland). The germination
22 rate of the competitor species was recorded after four weeks. After three months, final
23 aboveground vegetative and reproductive biomass of C. canadensis as well as the
24 aboveground biomass of the competitor plants were harvested and dried for 48 hours at 80°C.
25
26 Statistical analysis
11 1 Statistical analyses were conducted using R (version 2.1.1). We performed hierarchical
2 analyses of variance or deviance (sequential sum of squares or sum of deviance changes)
3 using a generalized-linear model approach to multiple regressions (e.g. Neter and
4 Wassermann 1974) and the results of the model-fitting sequences were summarized in
5 ANOVA tables (Green and Tukey 1960). The sequential analysis included the main effects of
6 block, treatment (either addition of activated carbon, generalist or specialist herbivory), native
7 vs. invasive populations (fixed factor), the spatial arrangement in the aphid choice experiment
8 (native vs. invasive plant as central source plant), as well as interactions of native-vs.-invasive
9 origin and treatment. The effects of block and population identity were considered random
10 factors. The effect of native vs. invasive populations was tested for significance with F-ratios
11 using the pooled variation among both invasive and native populations (term population) as
12 the denominator (see Joshi and Vrieling 2005). Significance tests were based on F-tests
13 (analysis of variance) or quasi-F-tests (analysis of deviance for binomial survival or hit/non-
14 hit data in the aphid Petri-dish experiment; see McCullagh and Nelder 1989). In the analyses
15 of growth related life-history traits, all plants that did not survive were excluded and latitude
16 was used as a covariate to test whether latitudinal clines were detectable and to correct for any
17 latitudinal bias in the sampling. The effect of latitude was tested against the variation among
18 populations (see Weber and Schmid 1998). For the analyses of the number of leaves attacked
19 by slugs, the initial number of leaves served as a covariate and was tested before all other
20 factors. The number of aphids on the centre (source) plant in the specialist herbivory
21 experiment was taken as a covariate in the analysis of aphid numbers per plant. In the aphid
22 leaf-choice experiment, each “hit” or “non-hit” of a leaf in a Petri dish was analyzed as a
23 function of leaf mixture within the Petri dish, origin of the aphid (reared on native vs. invasive
24 plants) and Petri dish identity. Where necessary, dependent variables were transformed prior
25 to statistical analysis to meet the analysis of variance assumptions of homoscedasticity and
26 normality.
12 1
2 Results and Discussion
3 Growth and reproduction
4 Plants with invasive origins had higher survival rates after one year of growth than those of
5 native origin (July 2005-July 2006; 83.2% vs. 56.4%; F1,27 = 10.15, P < 0.01). Under identical
6 environmental conditions, invasive C. canadensis also consistently produced more
7 reproductive biomass than Conyza plants from the species’ native range (Fig. 1; F1,22 = 4.57,
8 P < 0.05) indicating a fitness advantage in this crucial life-history parameter of annual plants.
9 The vegetative biomass of invasive plants was overall 20% higher than that of native plants
10 (3.3 ± 0.30 g dry mass vs. 2.71 ± 0.34 g; F1,22 = 4.51, P < 0.05). This difference in plant size
11 and reproduction of invasive compared to native conspecifics agrees with the general pattern
12 of increased growth and reproduction found in a meta-analysis of experimental studies
13 comparing life-history traits of invasive and native populations of 26 plant species (Hawkes
14 2007).
15 Latitudinal clines in reproductive biomass were not detected in the comparison between
16 native and invasive plants (P > 0.4). However, in both ranges, the vegetative biomass declined
17 with latitude (F1,22= 16.57, P < 0.001); in invasive areas with a steeper slope (latitude x native
18 vs. invasive populations F1,22 = 6.19, P < 0.05; Fig. 2). This steeper latitudinal decline in
19 vegetative biomass in Europe was mainly driven by the especially high plant biomass from
20 populations of southern latitudes, but lower biomass than in the native range at the most
21 northern sites (Fig. 2). This may indicate local adaptation at the northern latitudes in the
22 native, but not in the non-native range, whereas at southern latitudes in Europe Conyza
23 canadensis had a clearly higher performance than in the native range (Fig. 2). As the seed
24 material used in the study stemed from the original sites, the pattern observed may also partly
25 be attributed to maternal effects. However, a similar pattern of latitudinal trends in growth has
26 been reported in the annual invasive Impatiens glandulifera that shows an increase in size and
13 1 time until flowering at increasingly southern latitudes in the invasive European range
2 (Kollmann and Banuelos 2004). The re-establishment of clinal variation in life-history traits
3 of invading species as an adaptive response to climatic variation has also been reported for a
4 range of perennial species (Weber and Schmid 1998; Maron et al., 2004; Montague et al.,
5 2008). In Solidago altissima for example, the rapid differentiation in response to clinal
6 variation in the non-native range in Europe and Japan (Weber and Schmid 1998; Etterson et
7 al., 2008) has been suggested to stem from sorting of lineages due to multiple introductions
8 (Etterson et al., 2008). Multiple introductions from various origins of the native range may
9 also be expected in C. canadensis, because this weed species is easily dispersed as seed
10 contaminants (Weaver 2001).
11
12 Herbivory experiments
13 We tested whether plants from the non-native range showed higher fitness and reproduction
14 and whether they differed in resistance against a generalist and specialist herbivore. The
15 generalist slug Arion lusitanicus attacked twice the number of leaves on invasive as opposed
16 to native plants (29 ± 4.3 vs. 14 ± 3.2 leaves per plant; F1,24 = 5.72, P = 0.02). Accordingly,
17 the increase in weight of the slugs was significantly higher if they fed on invasives rather than
18 natives (+ 0.15 ± 0.025 g vs. + 0.06 ± 0.048 g; F1,22 = 4.41, P < 0.05; Fig. 3a). This putative
19 decrease in defence, however, did not clearly translate into lower growth of the more heavily
20 attacked invasive plants even though reduced survival, growth and fecundity with increasing
21 herbivory has earlier been reported for invasive European C. canadensis (Prieur-Richard et al.
22 2002). Though three months of slug herbivory led to an overall 40% decrease in leaf number
23 of the attacked versus the undamaged control plants (F1,89 = 117.52, P < 0.001) as well as a
24 15.4% and a 9.2% decrease in rosette diameter and plant height, respectively (F1,89 = 23.18, P
25 < 0.001; F1,89 =10.18, P < 0.01), attacked invasive plants did not suffer from a differential
26 reduction in fitness compared with attacked native plants (invasives vs. natives: leaf number P
14 1 > 0.14; rosette diameter P > 0.15; height P > 0.13). Nine months after slug feeding, slug
2 herbivory no longer had any noticeable effects on total biomass of native and invasive plants
3 (P > 0.3). However, reproductive biomass of invasive plants that had been attacked was twice
4 as high as that of native plants (1.74 g ± 0.15 vs. 0.86 g ± 0.15; F1,26 = 5.36, P < 0.05)
5 indicating a substantially higher regrowth potential of invasive plants, whereas the vegetative
6 biomass of attacked plants did not differ between European and native American plants (P =
7 0.3).
8 Invasive populations of C. canadensis benefited also from a lower susceptibility to the
9 co-migrating specialist herbivore aphid Uroleucon erigeronense. In an open plant-choice
10 experiment (see M&M), invasive European C. canadensis plants were significantly less
11 attacked by U. erigeronensis than native American plants (after 7 days: F1,14 =5.87, P < 0.05;
12 Fig. 3b; after 42 days: F1,14 = 3.98, P = 0.066; 6.28 ± 1.3 vs.15.34 ± 3.1 aphid
13 individuals/plant). Individual aphid biomass did not depend on the origin of the host plant (P
14 > 0.9), but total aphid biomass was lower on invasive than native plants (F1,14 = 3.98, P =
15 0.066; 2.36 ± 0.5 vs. 5.02 ± 1), which suggests a higher aphid reproduction on native plants.
16 As this specialised aphid, which is reportedly monophagous on C. canadensis at least in the
17 temperate Western hemisphere (Blackman and Eastop 2006) had lethal effects on heavily
18 infected plants (pers. observation), a protection against this specialist enemy might translate
19 into a significant fitness advantage in the field.
20 If, however, aphids in a Petri dish had a limited choice of four different leaves, they
21 were more attracted to invasive leaves. After the first day in the Petri dish, aphids were
22 present on a leaf in 45.7% of the Petri dishes. Aphids reared on invasive plants were rarer on
23 leaves than aphids reared on native plants (Fdev1,33 = 7.94, P < 0.01). This difference was not
24 significant for later observations (all P > 0.15; interaction aphid source x observation Fdev 2,419
25 = 27.84, P < 0.001). After 2 days, 74.3% of the aphids were present on leaves and on the third
26 day, all aphids were present on leaves. In each census, the specific mixture of leaves in the
15 1 Petri dishes had a significant influence on the choice of the aphids (Fdev1,419 = 9.13, P < 0.01).
2 Overall, aphids were less attracted to native leaves: in the final census, aphids were present on
3 native leaves in only 12 Petri dishes (= 34%), and in the second census, aphids were present
4 only in 5 Petri dishes on native leaves, but in 21 of the totally 35 Petri dishes on invasive
5 leaves. Hence, specialist aphids were attracted to the invasive leaf samples if they had a
6 limited choice, but their reproduction was higher in native plants as shown in the open plant-
7 choice experiment.
8 The EICA (evolutionary increase of competitive ability) hypothesis that originally has
9 been tested using specialized insects, which were recently introduced as biocontrol agents in
10 the non-native range (Blossey & Nötzold 1995), predicts that herbivores show an improved
11 performance on plant individuals originating from the introduced range that have lost their
12 defence during the invasion process and reallocated energy from defence to growth and
13 reproduction. Even though C. canadensis plants in the non-native range have some life-
14 history traits consistent with EICA predictions, such as lower defence against a generalist
15 herbivore and higher growth and reproduction, the observed increased resistance to specialist
16 herbivory and the high re-growth potential after generalist herbivory suggest that EICA can
17 not fully explain the success evident in the species’ non-native range. Partial support for the
18 EICA hypothesis has also been observed in other Asteraceae species such as Solidago
19 gigantea (Hull-Sanders et al. 2007) and Senecio jacobaea, which only lost protection against
20 specialist species not present in their new range, but were better protected against generalists
21 and showed a higher fitness than populations from the native range (Joshi and Vrieling 2005).
22 While enemy release, i.e. the escape from herbivory of noxious weeds in the introduced
23 compared to the native range seems to be a rather general pattern (Colautti et al. 2004), this
24 release did not necessarily translate directly into improved plant fitness in a comparison of 62
25 studies on plant invaders (Hawkes 2007). Our results are consistent with these findings and
26 suggest that EICA is a too simple explanation for the success of plant invaders.
16 1 While the high re-growth potential of invasive C. canadensis may be a beneficial side
2 effect of a generally higher growth rate, the mechanisms behind the higher resistance of
3 invasive C. canadensis against a co-migrating specialist enemy are more difficult to
4 understand. Genetic data may reveal whether this increased resistance against the specialist
5 aphid is due to maladaptation of the North American aphid that invaded Europe only about 50
6 years ago, due to pre-existing defence in Conyza, i.e. a chance effect of the introduction
7 history, or whether invasive populations can build-up an effective defence more easily due to
8 e.g. higher genetic diversity after repeated introductions (Dlugosch and Parker 2008).
9 Hybridization as a cause of enhanced genetic diversity (Prentis et al. 2008), has been ruled
10 out by Thébaud and Abbott (1995) who did not find any support of a hybridogenous origin of
11 invasive French Conyza populations.
12
13 Assessment of presence of allelochemicals
14 Some non-indigenous invasive species produce biochemical agents that function as powerful
15 allelopathic substances in a new (not co-evolved) environment, or as negotiators of new plant-
16 soil microbial interactions (Callaway and Aschehoug 2000; Callaway and Ridenour 2004;
17 Abhilasha et al. 2008). In contrast to allelopathic effects of other members of the Asteraceae
18 (e.g. Menelaou et al. 1992; Baruah et al. 1994; Bagchi et al. 1997; Ridenour and Callaway
19 2001), in invasive C. canadensis, there was no evidence for allelochemicals having an
20 inhibitory effect against seedling growth of the potentially naïve native competitors in the
21 invaded areas of Europe. The three plant species sown had different germination rates of 6%
22 (Lepidium), 32% (Medicago), and 87% (Triticum). There were no significant effects of
23 activated carbon addition on the germination rate, individual biomass, or total biomass per pot
24 of Medicago and Triticum (all P > 0.2), but the germination of Lepidium was positively
25 influenced by the addition of activated carbon. However, this effect occurred mainly in the
26 presence of native North American Conyza plants and was not observed in pots with Conyza 17 1 plants from the invasive European range (significant interaction carbon x native-vs.-invasive,
2 F1,28 = 10.94, P < 0.01). This effect translated into significant differences in total Lepidium
3 biomass per pot depending on the origin of Conyza and the addition of activated carbon
4 (carbon x native-vs.-invasive, F1,28 = 10.04, P < 0.01), but individual biomass of germinated
5 Lepidium plants did not differ between carbon treatments (P > 0.4). Previous studies have
6 shown that leaf extracts of C. canadensis and volatile compounds from the inflorescence of
7 invasive Conyza albida, a closely related species, exert significant inhibitory effects on the
8 germination and growth of several crop species (Economou et al. 2002; Shaukat et al. 2003).
9 However, in allelopathic species the effects often depend on the concentration and persistence
10 of the chemicals in the soil, on microbial interactions, and on the relative toxicity of the
11 allelochemicals to different plant neighbours and the probable interactions between different
12 secondary compounds (Ridenour and Callaway 2001; Thelen et al. 2005; Blair et al. 2006;
13 Weir 2007). Hence, more detailed studies are necessary to identify the environmental
14 interactions that may enhance or in contrast inhibit allelopathic effects of invasive plant
15 species.
16 In conclusion, the invasion success of C. canadensis in Europe cannot be attributed to
17 a single trait, but to a combination of factors. Whereas in contrast to earlier in-vitro studies,
18 no allelopathic effects on the competing flora in the non-native range were detected, invasive
19 plants benefited from an increased growth and above all, reproduction (a key trait in an annual
20 plant) and were less attacked by a co-migrated specialist enemy. The observed loss of defence
21 against generalist slugs did not translate into a decreased fitness as invasive C. canadensis
22 plants showed a high re-growth potential. The latitudinal clines observed in this common
23 garden study indicate a high adaptive potential. However, only further genetic studies will
24 provide conclusive evidence whether the adaptive differentiation in the non-native range is
25 caused by pre-adaptation and sorting-out processes of putatively repeatedly introduced
26 populations of this composite long-distance disperser with highly volatile seeds (Wein 1932,
18 1 Shields et al. 2006; Dauer et al. 2007) or whether alternatively, adaptation to abiotic and
2 biotic environmental conditions in the new range that evolved de novo as a rapid response to
3 new selection pressures may be responsible for the success of this global spreader.
4
5 Acknowledgements
6 This work was supported by a grant from Swiss National Science Foundation to J. J. (nr.
7 3100AO-104006). We are extremely grateful to all people who made the effort to collect seed
8 material for us: Ludwig Beenken, Reinhard Böcker, Thassilo Franke, Martin Hejda, Mark van
9 Kleunen, Jochen Krauss, Frank Lomer, Svata Louda, Honor Prentice, Susanne Renner, R.E.
10 Ricklefs, Daniel Schlaepfer, Giles Thelen, Montserrat Vilà, Klaas Vrieling and Anne
11 Weyand. Christine Müller and Jana Petermann determined the aphid species used and gave
12 valuable suggestions on the design of the aphid experiment. Many thanks to them and
13 especially also to Alexander Fergus, Kai Blaisdell, Ewald Weber and two anonymous referees
14 for valuable comments on the manuscript, Bernhard Schmid for advice on statistical analysis,
15 Theres Zwimpfer, Alex Schwendener, Katja Schächle and Sabine Probst for all their help in
16 the garden and the glasshouse and to the Experimental Station of the Institute of Plant
17 Sciences of ETH, Eschikon for use of their flowcytometer, and Daniel Schlaepfer for help
18 with the same.
19
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24 1 Figures
2 3 Fig. 1 Invasive Conyza canadensis plants from Europe produced significantly more
4 reproductive biomass than native American plants (F1,22 = 4.57, P < 0.05) resulting in a fitness 5 advantage in this crucial life-history parameter of annual plants. Vertical bars denote ± 1 6 standard error. 7 8 Fig. 2 In the native North American range as well as in the invasive European range the
9 vegetative biomass of Conyza canadensis individuals declined with latitude (F1,22 = 16.57, P < 10 0.001); a) in invasive areas with a steeper slope than in the native area (b); latitude x native
11 vs. invasive populations F1,22 = 6.19, P < 0.05). Overall, the vegetative biomass of invasive
12 plants was 20% higher than that of native plants (3.3 ± 0.3 g dry mass vs. 2.71 ± 0.34 g; F1,22 13 = 4.51, P < 0.05). 14 15 Fig. 3 a) Generalist Arion lusitanicus slugs increased significantly more in weight if they fed
16 on invasive rather than native plants (F1,22 = 4.41, P < 0.05; Fig. 3a). b) In contrast, the 17 invasive European Conyza canadensis plants were significantly less attacked by Uroleucon
18 erigeronensis than the native North American plants (after 7 days: F1,14 = 5.87, P < 0.05; 11.4 19 ± 2.18 vs. 23.0 ± 3.9 mean number of aphid individuals/plant). 20 21
25 1 Table 1 Locations of source populations of North American (native) and Europe (invasive) 2 Conyza canadensis populations used in the greenhouse and garden experiments. # Ploidy 3 determination; ● Growth analysis; * Assessment of presence of allelochemicals; † Generalist 4 herbivory; ** Specialist herbivory – open choice experiment; ∆ Specialist herbivory –Petri 5 dish experiment 6 Origin Regions Latitude Longitude Native range Canada#●*†**∆ Quebec 54.00 N 72.00 W Canada*∆ Manitoba 49.95 N 98.94 W Canada#●*†**∆ Vancouver Island 49.66 N 125.83 W Canada#●*†**∆ Montreal 45.63 N 73.52 W Canada#●*† Montreal 45.50 N 73.60 W USA#●*†**∆ Central Idaho 43.84 N 115.85 W USA#●*†**∆ Idaho, near Montana border 43.49 N 112.03 W USA#●*†** Nebraska 40.78 N 96.68 W USA#●*†**∆ St. Louis 38.66 N 90.32 W USA* **∆ Tennessee 35.30 N 84.53 W Non-native range Sweden#●*†**∆ Baltic Port of Kalmar 56.65 N 16.33 E Sweden#●*†∆ Lund 55.70 N 13.16 E Germany#●*†∆ Hamburg 53.55 N 10.00 E Germany#●*†** Hamburg 53.58 N 10.00 E Germany#●*† Berlin 52.53 N 13.41 E Germany#●*†∆ Potsdam 52.40 N 13.06 E The Netherlands#●*†**∆ Wassenaar 52.15 N 4.38 E Czech Republic#*† Pruhonice 49.46 N 14.39 E Czech Republic#●*† Hrncire 50.00 N 14.31 E Czech Republic#●*†**∆ Chotobuz 49.76 N 14.34 E Czech Republic#●*† NA 49.45 N 15.30 E Germany#●*†**∆ Munich 48.13 N 11.58 E Switzerland#●*† Embrach 47.50 N 8.60 E Switzerland#●*†** Winterthur 47.50 N 8.75 E
26 Switzerland#●*† Zurich 47.38 N 8.55 E Switzerland#●*† St. Sulpice 46.53 N 6.66 E Switzerland#●*† San Abbondio, Ticino 46.33 N 8.75 E Switzerland#●*†**∆ Bolle di Magadino, Ticino 46.16 N 8.80 E Switzerland#●*†**∆ Martigny 46.10 N 7.08 E Spain#●*†∆ Barcelona 41.41 N 2.16 E 1 2
27 1 2 Fig 1
3 4
28 1 Fig 2
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29 1 Fig. 3
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30