Corresponding author: Lena Y. Watermann (
Academic editor: Bruce Osborne
Biological invasions are considered a significant challenge both from an ecological and economical perspective. Compared to the native range, environmental conditions in the invasive range often favor more competitive genotypes. Little attention, however, has so far been paid to the possibility that these invasive and competitive genotypes might also be back-introduced into a species’ native range, where they could trigger a problematic increase in abundance or expansion. The frequency with which this occurs in the species´ native range might be an underestimated aspect in nature conservation. We transplanted native and invasive individuals of the biennial model species
Watermann LY, Rotert J, Erfmeier A (2022) Coming home: Back-introduced invasive genotypes might pose an underestimated risk in the species´ native range. NeoBiota 78: 159–183.
Invasive alien plant species pose a significant threat to biodiversity (
Given the increasing human mobility around the globe that allows plant species to overcome the first barrier in the invasion process (
In general, range expansions in any population, native or invasive, are associated with adaptations that facilitate high reproduction rates (
For example, species naturalized outside their native range often experience a release from natural enemies during the invasion process. Once exempt from the necessity to defend against specialist herbivores occurring in the plant species’ native range, resources can be used for other purposes (Enemy Release Hypothesis) (
Besides the often-addressed aboveground factors, such as herbivory, plant-soil-feedbacks (
Accordingly, both above- and belowground agents, such as aboveground herbivory and plant-soil feedbacks, should be considered jointly when trying to judge the success or failure of (exotic) populations. Yet, most studies usually have an either exclusively aboveground or belowground perspective. However, trophic interactions may affect all plant organizational components. Furthermore, common gardens are typically not established as in-site experiments within naturally occurring populations of a species under consideration. This is understandable for reasons of nature conservation. However, abstaining from this kind of test means disregarding the role of
The biennial model species
In the last two decades,
We carried out a transplant experiment in field sites of naturally occurring ragwort populations in the species’ native range. We aimed to test whether
Seed collection was carried out in the summer of 2018 in the Pacific Northwest (invasive range) and Central Europe (native range) at the same time. For species identification, we referred to “Rothmaler - Exkursionsflora von Deutschland” (
Six populations each by range of origin (invasive – native) were chosen according to seed quality and availability to be included in this experiment. In addition, we intentionally included populations varying in size and density in order to cover a broad range of variation within ranges. The sites in the native range served both as donor populations for seed sourcing and target sites for (re-)transplantation. For the selection of these six native populations, we thus additionally had to acquire permission from local authorities, landowners, and the tenant farmers for conducting a transplant experiment on their sites. All field sites for this experiment are owned by the Stiftung Naturschutz Schleswig-Holstein (for population information, s. Suppl. material
From each population, seeds from seven randomly selected seed families were sown in potting soil (TKS 2 pot Medium Coarse, Floragard Vertriebs-GmbH, Oldenburg, Germany) on germination trays in April of 2019. The seeds were covered by 1 cm of soil layer to prevent them from drying out. The germination trays were placed in a greenhouse cabinet with ambient temperature and a photoperiod of 12:12 (night/day) hours and watered daily in the following days. After four weeks, five seed families with the highest germination success within each population were chosen to be included in the experiment and seedlings were thinned to allow optimal growth. Once established, the germination trays were placed outside to allow acclimatization of the separated individuals to outdoor conditions.
The field experiment was designed to estimate performance of invasive individuals compared to native individuals in the species’ original native range. The location of the six native populations used for seed material sampling also served as transplantation sites. In each of these six sites, we established five experimental plots. Plot locations were assigned randomly within site with coordinates marking the southwest corner of each plot. Starting from this corner, an area of 0.9 m × 1.2 m was established, where transplants were arranged in 4 × 5 rows (all plants were 0.3 m apart) leading to a total of 20 planting positions. One individual from each of the six invasive populations and two individuals from each of the six native populations (and therefore also originating from the experimental sites (= at their population home)) were randomly assigned to the planting positions leaving out the southwest and northwest spots. Thus, a total of 18 individuals were planted per plot. Each two individuals from the six native populations were replicates from the same seed family. For each of those replicates, one individual was a priori randomly chosen for the present experiment while the second one was assigned to remain into the summer of 2020 as part of an additional experiment (s. Suppl. material
Planting was carried out starting June 15th 2019 (approx. 2 months after sowing). The vegetation in the plots was cut to approx. 0.3 m to reduce heterogeneity during early establishment of the experimental plants. Subsequently, experimental plants were brought out with the adhering potting soil and labelled for recognition. After planting, each experimental plot was watered with 10 l water right away and two additional times after one week to assure establishment and survival of the planted individuals.
Next to each of the five experimental plots, a 2 m × 2 m monitoring plot was established following the diagonal extension 5 m apart in a northeastern direction. The monitoring plots served for recording vegetation composition and structure, including information on overall vegetation height (as a measure for productivity), coverage using a modified Londo scale (
The monitoring of the field experiment ran from June 28th until September 28th. After 6 weeks and 14 weeks of experimental runtime, we determined specific leaf area (
The greenhouse experiment was set up analogous to the field experiment and ran from August 21st (approx. 4 months after sowing of seeds) to November 13th. To decouple the influence of soil biota effects from other environmental factors varying with the field sites, soil samples were taken from all six native field sites used in the field experiment. These soil samples served as an inoculum for soil-biota treatments to all native and invasive individuals. For this, soil material was sampled about 0.5 m south of the southwestern corner of each experimental plot. After careful sod removal, a volume of 1 l soil was taken per plot, sieved through a 2 mm mesh and collected in a sterilized bucket. Separate soil samples from all plots were pooled and merged by site and served as the site-specific donor substrate. Soil sampling equipment was sterilized between sites to avoid cross-contamination.
All 12 population origins incorporated in the field experiment were also used in the greenhouse with three seed families randomly chosen out of the five used in the field. For each seed family, each one individual was grown with soil addition from one of the six field sites or only using standard substrate (control). Standard substrate consisted of 60% fine sand provided by the Botanical Garden of Kiel University and 40% unfertilized potting soil (F.E. Typ Nullerde, HAWITA Gruppe GmbH, Vechta, Germany) constituting an environment especially low in nutrients. This led to a total of seven different treatments for each seed family, thus resulting in a total of 252 individuals in the greenhouse experiment. All individuals were transferred to 1.5 l planting pots filled with 1.26 l standard substrate supplemented either by 0.14 l of soil collected from one of the six field sites (9:1 standard substrate:field soil) or an additional 0.14 l standard substrate for the control group. The standard substrate was processed by an autoclave (Webeco Dampf-Sterilisator, Matachana Germany GmbH, Selmsdorf, Germany) to reduce already present soil biota to a minimum. Each pot additionally received 3 g slow-release fertilizer (2.14 g/l) (Basacote Plus 6M 16 + 8 + 12 (+ 2 + 5), Compo Expert GmbH, Münster, Germany) corresponding to low levels of nutrient availability as per the manufacturer’s specifications. Planting pots were put on saucers and distributed in the greenhouse. Their position on benches was randomized every week. Predatory mites and sticky traps were installed at the beginning of the experiment to reduce infestation risk with insects. After one month, an insecticide was used on all plants (Spruzit Schädlingsfrei, W. Neudorff GmbH KG, Emmerthal, Germany), and milk and neem oil were applied to all individuals to prevent the spread of mildew. Throughout the experiment all plants were watered with 75 ml of tap water every 1–3 days as needed. Excess water from the saucers was emptied after every watering.
After the experimental runtime, monitoring and biomass harvest were carried out analogous to the field experiment.
Statistical analyses were performed with R (Version 4.1.1) (
Similarly, for the greenhouse experiment, we fitted a lmer with origin and provenance of the soil (site) as fixed effects. As a covariate we included either the respective response variables’ value at the beginning of the experiment or the initial number of leaves if no starting value was available (for biomass variables,
The datasets generated during and/or analyzed during the current study as well as the code used for analysis are available from the corresponding author upon reasonable request.
After 14 weeks of experimental runtime, individuals originating from the invasive range had developed larger rosettes (Table
Field experiment – performance traits. Results from the ANOVA for the linear-mixed effects and generalized-mixed effects model (Herbivory and Survival) in the field experiment for performance traits. Significant effects (p<0.05) are printed in bold.
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Origin | 1 | 287.15 | 7.1117 |
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147.09 ± 216.97 | 194.14 ± 251.87 | 1 | 9.602 | 4.6268 | 0.058 | 7.29 ± 5.82 | 8.63 ± 6.76 |
Week 1** | 1 | 297.41 | 5.1658 |
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1 | 227.745 | 22.79 |
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C:N ratio | NA | NA | NA | NA | NA | NA | NA | NA | ||||
Max. vegetation height | NA | NA | NA | NA | NA | NA | NA | NA | ||||
Origin × C:N ratio | NA | NA | NA | NA | NA | NA | NA | NA | ||||
Origin × Max. vegetation height | NA | NA | NA | NA | NA | NA | NA | NA | ||||
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Origin | 1 | 286.431 | 0.5499 | 0.458 | 12.07 ± 6.48 | 13.94 ± 8.23 | 1 | 290.39 | 7.6368 |
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0.60 ± 1.95 | 1.01 ± 2.82 |
Week 1** | 1 | 298.693 | 10.7502 |
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1 | 303.44 | 10.4424 |
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C:N ratio | 1 | 7.334 | 6.8443 |
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NA | NA | NA | NA | ||||
Max. vegetation height | 1 | 16.219 | 5.289 |
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NA | NA | NA | NA | ||||
Origin × C:N ratio | 1 | 285.911 | 0.0208 | 0.885 | NA | NA | NA | NA | ||||
Origin × Max. vegetation height | 1 | 286.344 | 0.3022 | 0.583 | NA | NA | NA | NA | ||||
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Origin | 1 | 281.277 | 0.2909 | 0.590 | 0.51 ± 0.57 | 0.53 ± 0.52 | 1 | 290.009 | 0.0228 | 0.880 | 1.11 ± 2.47 | 1.54 ± 3.31 |
Number of leaves | 1 | 315.251 | 26.8191 |
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1 | 289.342 | 18.0332 |
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C:N ratio | 1 | 27.973 | 5.6967 |
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1 | 29.04 | 4.3788 |
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Max. vegetation height | 1 | 29.692 | 4.8105 |
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1 | 30.241 | 5.9063 |
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Origin × C:N ratio | 1 | 278.043 | 0.7901 | 0.374 | 1 | 278.227 | 0.1853 | 0.667 | ||||
Origin × Max. vegetation height | 1 | 279.297 | 0.0001 | 0.993 | 1 | 279.264 | 0.0392 | 0.843 | ||||
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Origin | 1 | 54.908 | 11.7481 |
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2.31 ± 2.27 | 1.76 ± 1.70 | ||||||
Number of leaves | 1 | 290.887 | 0.4528 | 0.502 | ||||||||
NA | NA | NA | NA | |||||||||
Max. vegetation height | NA | NA | NA | NA | ||||||||
Origin × |
NA | NA | NA | NA | ||||||||
Origin × Max. vegetation height | NA | NA | NA | NA | ||||||||
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Origin | 14.4039 | 2.317 |
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0.13 ± 0.34 | 0.11 ± 0.32 | 0.1614 | 0.403 | 0.687 | 0.86 ± 0.35 | 0.84 ± 0.36 | ||
Number of leaves | NA | NA | NA | NA | NA | NA | ||||||
-0.0381 | -1.487 | 0.137 | NA | NA | NA | |||||||
Max. vegetation height | 0.1737 | 2.821 |
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NA | NA | NA | ||||||
Origin × |
-0.0382 | -1.013 | 0.311 | NA | NA | NA | ||||||
Origin × Max. vegetation height | -0.1296 | -2.27 |
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NA | NA | NA |
Origin effects (field experiment). Response of performance (
Irrespective of origin, C:N ratio and maximum height of the vegetation in the monitoring plot displayed a significantly negative relationship with
For functional leaf traits, no significant origin effect could be detected (Table
Field experiment – functional traits. Results from the ANOVA for the linear-mixed effects in the field experiment for functional leaf traits. Significant effects (p<0.05) are printed in bold.
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Origin | 1 | 156.816 | 1.6254 | 0.204 | 21.84 ± 6.16 | 20.37 ± 4.17 | 1 | 43.488 | 3.1219 | 0.084 | 0.13 ± 0.03 | 0.13 ± 0.02 |
Number of leaves | 1 | 173.993 | 3.6489 | 0.058 | 1 | 170.423 | 0.8594 | 0.355 | ||||
α-Diversity | 1 | 7.592 | 12.0547 |
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NA | NA | NA | NA | ||||
C:N ratio | 1 | 5.373 | 5.8519 | 0.056 | NA | NA | NA | NA | ||||
Origin × α-Diversity | 1 | 139.819 | 6.3232 |
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NA | NA | NA | NA | ||||
Origin × C:N ratio | 1 | 155.856 | 0.4553 | 0.500 | NA | NA | NA | NA | ||||
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Origin | 1 | 284.181 | 1.4873 | 0.224 | 27.38 ± 7.54 | 27.29 ± 7.49 | 1 | 292.377 | 0.1939 | 0.660 | 0.11 ± 0.02 | 0.09 ± 0.02 |
Number of leaves | 1 | 299.233 | 1.469 | 0.226 | 1 | 255.374 | 0.7518 | 0.387 | ||||
Max. vegetation height | 1 | 31.503 | 5.1708 |
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NA | NA | NA | NA | ||||
Origin * Max. vegetation height | 1 | 276.967 | 1.435 | 0.232 | NA | NA | NA | NA | ||||
α-Diversity | NA | NA | NA | NA | 1 | 27.654 | 2.552 | 0.122 | ||||
C:N ratio | NA | NA | NA | NA | 1 | 16.52 | 3.7026 | 0.072 | ||||
Origin × α-Diversity | NA | NA | NA | NA | 1 | 276.883 | 6.7717 |
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Origin × C:N ratio | NA | NA | NA | NA | 1 | 280.836 | 0.0623 | 0.803 |
Number of Leaves was counted at initial monitoring one week after planting;
Origin effects × covariate (field experiment). Effects of origin in interaction with α-diversity (
In the greenhouse experiment, there was no difference in biomass depending on the origin of the individuals (Table
Greenhouse experiment – performance traits. Results from the ANOVA for the linear-mixed effects in the greenhouse experiment for performance traits. Significant effects (p<0.05) are printed in bold. Treatment refers to the provenance of the added soil. All soils originate from field sites within the species’ native range.
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Origin | 1 | 10.302 | 0.3555 | 0.563 | 515.6 ± 198.34 | 525.75 ± 185.82 | 0.343 | 1 | 0.558 | 26.35 ± 8.19 | 25.19 ± 8.42 | |
Treatment | 6 | 224.597 | 2.6195 |
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19.756 | 6 |
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Initialϯ | 1 | 224.9 | 3.93 | 0.090 | 19.2468 | 1 |
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Origin × Treatment | 6 | 224.529 | 0.9115 | 0.487 | 24.9001 | 6 |
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Origin | 1 | 10.007 | 3.462 | 0.092 | 17.83 ± 3.80 | 18.66 ± 3.83 | ||||||
Treatment | 6 | 200.665 | 3.9741 |
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Initialϯ | 1 | 220.839 | 16.663 |
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Origin × Treatment | 6 | 200.924 | 1.3928 | 0.219 | ||||||||
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Origin | 1 | 10.211 | 2.915 | 0.160 | 4.80 ± 2.15 | 5.39 ± 2.66 | 1 | 223 | 0.0646 | 0.800 | 8.77 ± 5.39 | 2.66 ± 8.77 |
Treatment | 6 | 225.441 | 2.0788 | 0.057 | 6 | 223 | 3.7241 |
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Number of leaves | 1 | 224.85 | 2.4574 | 0.118 | 1 | 223 | 0.0208 | 0.886 | ||||
Origin × Treatment | 6 | 225.216 | 1.1429 | 0.338 | 6 | 223 | 0.4702 | 0.930 | ||||
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Origin | 1 | 10.65 | 1.8419 | 0.203 | 12.24 ± 8.20 | 14.24 ± 8.78 | 1 | 36.516 | 0.3564 | 0.554 | 1.77 ± 1.25 | 1.65 ± 1.26 |
Treatment | 6 | 226.95 | 3.7727 |
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6 | 187.414 | 2.0053 | 0.067 | ||||
Number of leaves | 1 | 171.56 | 0.1229 | 0.726 | 1 | 190.777 | 0.0396 | 0.842 | ||||
Origin × Treatment | 6 | 226.55 | 0.9688 | 0.447 | 6 | 186.814 | 0.2409 | 0.962 |
Number of leaves was counted at initial monitoring. Initialϯ refers to the values of the response variable at the initial monitoring, e.g. for Rosette Expansion (week 12) this is the Rosette Expansion at the initial monitoring, Treatment refers to the provenance of the soil used.
Treatment effects on performance traits (greenhouse experiment). Effects of soil provenance in the greenhouse experiment. Data shown are predicted values from the model ± SE. Different colors represent different soil origins (only soil from native sites were included in this experiment). Different letter combinations in the panels indicate significant differences according to the Tukey post-hoc test. ALB = Albersdorf, ARB = Arpsdorf, BUN = Bünsdorf/Wittensee, Con = Control (no soil added from any field site), PRE = Preetz, ROT = Rotenhahn/Eidertal, VOL = Vollstedter See. For location information see Suppl. material
For the functional traits
Greenhouse experiment – functional traits. Results from the ANOVA for the linear-mixed effects in the field experiment for functional leaf traits. Significant effects (p<0.05) are printed in bold.
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Origin | 1 | 10.142 | 0.9933 | 0.342 | 23.99 ± 4.46 | 22.73 ± 3.55 | 1 | 9.911 | 0.1945 | 0.669 | 0.12 ± 0.00 | 0.12 ± 0.02 |
Treatment | 6 | 202.852 | 2.807 |
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6 | 203.173 | 3.3796 |
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Number of leaves | 1 | 235.607 | 3.1885 | 0.075 | 1 | 205.374 | 10.3484 |
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Origin × Treatment | 6 | 202.57 | 0.4798 | 0.823 | 6 | 202.779 | 1.0921 | 0.368 | ||||
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Origin | 1 | 10.214 | 1.6375 | 0.229 | 21.22 ± 3.33 | 19.95 ± 3.35 | 1 | 9.894 | 0.0999 | 0.759 | 0.20 ± 0.03 | 0.20 ± 0.04 |
Treatment | 6 | 200.084 | 3.7331 |
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6 | 200.154 | 1.2052 | 0.305 | ||||
Number of leaves | 1 | 232.749 | 8.0692 |
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1 | 219.386 | 1.3717 | 0.243 | ||||
Origin × Treatment | 6 | 199.909 | 0.2384 | 0.963 | 6 | 199.852 | 0.177 | 0.983 |
Treatment effects on functional traits (greenhouse experiment). Effects of soil provenance in the greenhouse experiment. Data shown are predicted values from the model ± SE. Different colors represent different soil origins (only soil from native sites were included in this experiment). Different letter combinations in the panels indicate significant differences according to the Tukey post-hoc test. ALB = Albersdorf, ARB = Arpsdorf, BUN = Bünsdorf/Wittensee, Con = Control (no soil added from any field site), PRE = Preetz, ROT = Rotenhahn/Eidertal, VOL = Vollstedter See. For location information see Suppl. material
Since its initial appearance in the Pacific Northwest about a century ago, there was, theoretically, ample time for adaptive evolutionary adjustment to occur in
There is some evidence that specialist herbivores prefer invasive individuals of
In contrast, the absence of any origin-dependent differences in the greenhouse experiment was unexpected given previous studies with
In the field experiment, the invasive individuals might also have benefitted from atypically high temperature and decreased precipitation during the experimental runtime (
In the present study, the provenance of soil (treatment) differently impacted
Knowledge about soil provenance × plant origin interactions in general is lacking for this model species to date and we found no signs for enemy release on the belowground level as shown for
In the present experiment, maximum vegetation height (strongly linked to light availability with r = - 0.62, p<0.001 with Pearson’s rank) was a relevant environmental factor for both origins, with the typical responses of increasing specific leaf area with decreasing light availability (
In summary, we cannot conclude explicitly which factors are the main drivers of increased performance of invasive transplants in the species’ native range (hypothesis II). It is, therefore, also difficult to accurately predict the long-term consequences of back-introduction of propagules or individuals of invasive origin into the species’ native range. However, genetic admixture might accelerate geographic expansion and invasion (
Invasive genotypes of
With regard to a possible cryptic invasion of
However, it is likely that cryptic invasions will occur more often than identified so far. To date, invasion research mostly focuses on the unidirectional introduction into the novel range, and little is known about the possibility of back-introduction. Furthermore, knowledge about the frequency with which back-introductions happen is so far lacking. Generally, pathways of biological invasions are complex and vary in their relative importance over time (
We thank P. Music and F. Meyer for helping to set up the field experiment and subsequent support in monitoring as well as H. Bülow for plant care in the greenhouse. For technical help, especially in soil sterilization, we want to thank I. Meyer and C. Plieth for providing the necessary equipment. We are grateful to the Stiftung Naturschutz Schleswig-Holstein and A. Huckauf, in particular, for providing permission and access to their field sites.
The study was financially supported by the Evangelisches Studienwerk Villigst e.V. with a Ph.D. scholarship awarded to LYW and with a Quick and Tiny grant from Kiel University awarded to JR and LYW. We acknowledge financial support by Land Schleswig-Holstein within the funding programme Open Access Publikationsfonds.
Supplementary information
images, tables (word document)
Population information. Schematic overview of one experimental plot with planting scheme. Transformations of variables. Mean values for performance traits (field experiment). Mean values for functional leaf traits (field experiment). Mean values for performance traits (greenhouse experiment). Mean values for functional leaf traits (greenhouse experiment). Origin effects (field experiment). Origin effects × covariate (field experiment). Treatment effects on performance traits (greenhouse experiment). Treatment effects on functional traits (greenhouse experiment).