Research Article |
Corresponding author: Maria Hock ( maria.hock@botanik.uni-halle.de ) Academic editor: José Hierro
© 2015 Maria Hock, Michael Beckmann, Rainer R. Hofmann, Helge Bruelheide, Alexandra Erfmeier.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Hock M, Beckmann M, Hofmann RW, Bruelheide H, Erfmeier A (2015) Effects of UV-B radiation on germination characteristics in invasive plants in New Zealand. NeoBiota 26: 21-37. doi: 10.3897/neobiota.26.4405
|
UV-B radiation represents a potentially selective, yet little studied environmental factor for plant invasions, especially with respect to germination characteristics and seedling establishment in areas of high UV-B exposure such as New Zealand. To explain invasive potential of plant species pre-adaptation and local adaptation to selection factors in the invaded range are two frequently consulted concepts. To test for the relevance of these mechanisms, it is necessary to compare both invasive and non-invasive species, as well as native and exotic origins of invasive species. In the present study, germination success of two congeneric species pairs of the genera Verbascum (Scrophulariaceae) and Echium (Boraginaceae) were investigated under high UV-B intensities. Each genus comprised one species that has successfully invaded New Zealand grasslands and one species that was introduced but has not been invasive in New Zealand. In an among-species approach, pre-adaptation was tested by comparing germination success of native (European) origins of all four species in relation to their different invasive success in New Zealand. In a within-species comparison, native (European) and exotic (New Zealand) origins of the two invasive species were compared to test for local adaptation to UV-B in the invaded range. In both approaches, UV-B radiation inhibited the germination success of all study species. However, the comparison of invasive and non-invasive species of the two genera showed no UV-B-specific pre-adaptation of invasive species to high UV-B intensities. Higher germination success of invasive species probably led to an establishment advantage during colonization of the invaded range. Although local adaptation of exotic populations to UV-B could not be demonstrated in the within-species approach, a genetic shift in germination velocity between native and exotic origins was found. These differences may be ascribed to other relevant environmental factors, e.g. overall irradiation and drought, inducing similar plant responses as under UV-B radiation.
Congeneric species pairs, Echium, invasive vs. non-invasive species, local adaptation, native vs. exotic origins, pre-adaptation, Verbascum
In the course of globalization, a plethora of species have managed to overcome geographic barriers and to successfully establish wild populations in the new environment. Most notably, this can be observed in previously isolated systems, such as Australia, New Zealand, Madagascar and other islands (
In the last decades, many studies have attempted to identify characteristics that explain species’ invasiveness. Frequently evoked characteristics are a large native range and the ability of fast dispersal, as induced by short generation times, high seed production, low seed weight and long seed persistence (
However, germination patterns have also been shown to differ between exotic and native populations, thereby providing evidence for the alternative explanation of local adaptation taking place in the invaded range. There are some examples of herbaceous and woody plants that indicate lower germination rates of native populations compared to exotic ones (e.g.
Invasive species have to face several biotic and abiotic selection factors in the invaded range, such as competition, herbivory, soil properties and climatic conditions (
Early stages of plant development and seedling establishment are particularly sensitive to biologically effective UV-B radiation including metabolic limitations or DNA damage, when appropriate protection measures are not yet fully developed. In particular, reduced seedling biomass, inhibited hypocotyl or root development and growth abnormalities (e.g. shoot curvature) have been observed in response to high UV-B intensities (
Hence, we conducted a germination experiment comparing pairs of invasive vs. non-invasive species of the genera Echium and Verbascum, and native vs. exotic origins of the respective successful invader. We tested for pre-adaptation to high UV-B levels in native populations of invasive species as compared to congeneric non-invasive species, and for effects or more recent evolutionary processes, that may hint at local adaptation of exotic populations from New Zealand in the germination responses. We addressed the hypotheses that a) UV-B radiation inhibits germination success in plants and b) that invasive species and exotic populations show higher germination success in comparison to non-invasive species and native populations of invasive species, respectively. In a first analysis, we compared the germination success in response to high UV-B radiation of species native to Europe that are currently invading New Zealand grasslands with non-invasive congeners that, as yet, have failed to spread to a similar degree in New Zealand. In a second analysis, we tested for within-species differentiation among native and exotic origins. Accordingly, we included seeds of native (European) and exotic (New Zealand) populations of Echium vulgare L. (blueweed) and Verbascum thapsus L. (common mullein), as well as native (European) populations of their non-invasive congeners Echium plantagineum L. (Paterson’s curse) and V. nigrum L. (dark mullein), respectively. This is the first study addressing the role of UV-B for seedling emergence and establishment for plants invasive in the southern hemisphere.
We used seeds of two pairs of congeneric species of the genera Echium (Boraginaceae) and Verbascum (Scrophulariaceae). All four study species are native to Central Europe or distributed in Eurasia and typical components of dry grasslands and ruderal habitats. They are characterized by high drought tolerance and a strong prevalence in open, unshaded habitats (
The germination experiment was conducted at Lincoln University in Lincoln, Christchurch (New Zealand) in March 2012, in a walk-in growth chamber (Type PGV36, Conviron). The UV-B treatment was induced by twelve UV-B tubes (UVB 313 EL, Q-Lab Corporation), which were installed in addition to a standard set of illuminants. Each UV-B tube was enveloped with UV-B-permeable cellulose acetate filter to exclude undesired wavelengths (i.e. UV-C). During the experiment UV-B intensity was measured continuously in the growth chamber by a UV-B sensor, thus, an electronic feedback system kept the intensity constant (
The germination test was done in seedling trays (i.e. plots) arranged in a split-plot design. Eight seedling trays, filled with sterilized, finely granulated substrate, were each sub-divided in 24 quadrats (5cm × 5cm) being separated aboveground. For origins of Echium and Verbascum, 12 and 25 seeds per population, respectively, were sown in each quadrat. Each of the 24 populations was sown once per plot, i.e. each population was replicated eight times in total. Half of the plots were exposed to UV-B exposure, whereas the other four plots served as a control, i.e., no UV-B. The plots were randomly positioned within the two UV-B treatments and randomization was repeated twice during the experiment, including reassignment of UV-B applications to the two sections within the chamber.
The seeds were sown on the wet substrate and slightly pressed in. The trays (i.e. plots) were placed in tubs, filled with water, to keep the substrate moist. In addition, the trays were sprayed with water every second day to prevent them from drying out. From the third day of the experiment onwards, the number of germinated seeds was initially recorded daily and later every other day (ten times in total). The last germination event was monitored on day 17. Newly emerged seedlings and cases of seedling mortality were assessed visually. At the end of the experiment, we counted the final number of seedlings in each quadrat and determined the germination success.
For data analysis, linear mixed models were applied in SAS 9.2 (
Data were analyzed according to an orthogonal design reflecting the hypotheses by first comparing invasive and non-invasive species (among-species approach: n = 15 populations) and secondly, comparing native and exotic origins of the two invasive species E. vulgare and V. thapsus (within-species approach: n = 17 populations).
For the among-species approach, germination data of native populations of all four investigated species (n = 120 quadrats) were included in the statistical analysis, testing maximum germination success as a response variable. The model included ‘genus’ (Echium, Verbascum), ‘status’ (invasive, non-invasive) and ‘treatment’ (UV-B, no-UV-B) as fixed factors, whereas ‘treatment × plot’ and ‘genus × status × population’ were considered random factors. In order to test for differences in germination velocity, a repeated measures analysis was done by adding ‘days’ (i.e., the date of seedling census) as a continuous variable and ‘genus × status × treatment × unit (location in a certain quadrat)’ as a random factor to the model.
For the within-species approach, germination data of native and exotic populations of the invasive species E. vulgare and V. thapsus were tested for potential differences in UV-B tolerance (n=136 quadrats), applying the same model. Therefore, maximum germination success was tested in a model containing ‘species’ (E. vulgare, V. thapsus), ‘origin’ (DE, NZ) and ‘treatment’ (UV-B, no-UV-B) as fixed factors. ‘Species × origin × population’ and ‘treatment × plot’ were included as random factors. Again, a repeated measures analysis was done for all ten censuses during the experiment, using a similar mixed model but also including ‘days’ as a continuous variable and ‘species × origin × treatment × unit’ as a random factor.
All figures were produced with R 3.0.0 (
Both genera differed significantly in germination success with a higher maximum germination of the Verbascum species (p < 0.001, Fig.
Maximum germination in the among-species approach testing for pre-adaptation of Echium and Verbascum seeds. a of invasive (grey) and non-invasive (white) species and b in response to UV-B radiation (grey) and no UV-B radiation (white) treatment.
Results of the mixed model analysis of the among-species approach testing for pre-adaptation. Degrees of freedom (dfN = numerator, dfD = denominator), F-statistics (F) and significance values (p) are given. ‘Plot × treatment’ and ‘genus × status × population’ interactions were considered random effects and a Z-value instead of F-value is provided. Bold numbers indicate significant p-values (p < 0.05).
Source | dfN | dfD | F/Z | p |
---|---|---|---|---|
treatment | 1 | 6 | 9.33 | 0.022 |
genus | 1 | 11 | 86.77 | <0.001 |
status | 1 | 11 | 11.35 | 0.006 |
genus × status | 1 | 11 | 0.70 | 0.421 |
genus × treatment | 1 | 95 | 11.41 | 0.001 |
status × treatment | 1 | 95 | 0.36 | 0.551 |
genus × status × treatment | 1 | 95 | 0.44 | 0.507 |
treatment × plot | 0.56 | 0.286 | ||
genus × status × population | 2.03 | 0.021 |
Repeated measures analysis confirmed these effects over time (Table
Germination development in the among-species approach testing for pre-adaptation of exotic (dashed line) and native species (solid line) of the genera Echium (circle) and Verbascum (triangle).
Results of the repeated measures analysis of the among-species approach testing for pre-adaptation. Degrees of freedom (dfN = numerator, dfD = denominator), F-statistics (F) and significance values (p) are given. ‘Treatment × plot’, ‘genus × status × population’ and ‘genus × status × treatment × unit’ interactions were considered random effects and a Z-value instead of F-value is provided. Bold numbers indicate significant p-values (p < 0.05).
Source | dfN | dfD | F/Z | p |
---|---|---|---|---|
treatment | 1 | 6 | 0.45 | 0.529 |
genus | 1 | 11 | 39.20 | <0.001 |
status | 1 | 11 | 4.67 | 0.054 |
genus × status | 1 | 11 | 0.32 | 0.584 |
genus × treatment | 1 | 95 | 0.32 | 0.575 |
status × treatment | 1 | 95 | 0.00 | 0.986 |
genus × status × treatment | 1 | 95 | 0.65 | 0.421 |
days | 1 | 1072 | 675.56 | <0.001 |
days × genus | 1 | 1072 | 44.62 | <0.001 |
days × status | 1 | 1072 | 6.42 | 0.011 |
days × treatment | 1 | 1072 | 3.83 | 0.051 |
days × genus × status | 1 | 1072 | 9.11 | 0.003 |
days × genus × treatment | 1 | 1072 | 6.98 | 0.008 |
days × status × treatment | 1 | 1072 | 0.09 | 0.764 |
days × genus × status × treatment | 1 | 1072 | 0.01 | 0.921 |
treatment × plot | - | - | ||
genus × status × population | 2.18 | 0.015 | ||
genus × status × treatment × unit | 4.42 | <0.001 |
V. thapsus had a higher maximum germination success than E. vulgare (p=<0.001, Fig.
Maximum germination in the within-species approach testing for local adaptation of Echium vulgare and Verbascum thapsus seeds. a of New Zealand (grey) and German (white) populations and b in response to UV-B radiation (grey) and no UV-B radiation (white) treatment.
Results of the mixed model analysis of the within-species approach testing for local adaptation. Degrees of freedom (dfN = numerator, dfD = denominator), F-statistics (F) and significance values (p) are given. ‘Treatment × plot’ and ‘species × origin × population’ interactions were considered random effects and a Z-value instead of F-value is provided. Bold numbers indicate significant p-values (p < 0.05).
Source | dfN | dfD | F/Z | p |
---|---|---|---|---|
treatment | 1 | 6 | 5.64 | 0.055 |
species | 1 | 13 | 135.30 | <0.001 |
origin | 1 | 13 | 12.25 | 0.004 |
species × origin | 1 | 13 | 4.63 | 0.051 |
species × treatment | 1 | 109 | 8.97 | 0.003 |
origin × treatment | 1 | 109 | 1.21 | 0.275 |
species × origin × treatment | 1 | 109 | 2.26 | 0.136 |
treatment × plot | - | - | ||
species × origin × population | 1.81 | 0.035 |
The repeated measures analysis confirmed these results over time and revealed a faster germination of Verbascum seeds compared to Echium seeds and also a higher germination velocity of exotic origins of both species than native ones (Table
Results of the repeated measures analysis of the within-species approach testing for local adaptation. Degrees of freedom (dfN = numerator. dfD = denominator). F-statistics (F) and significance values (p) are given. ‘Treatment × plot’. ‘species × origin × population’ and ‘species × origin × treatment × unit’ interactions were considered random effects and a Z-value instead of F-value is provided. Bold numbers indicate significant p-values (p < 0.05).
Source | dfN | dfD | F/Z | p |
---|---|---|---|---|
treatment | 1 | 6 | 0.23 | 0.646 |
species | 1 | 13 | 85.51 | <0.001 |
origin | 1 | 13 | 1.22 | 0.289 |
species × origin | 1 | 13 | 0.18 | 0.680 |
species × treatment | 1 | 109 | 0.14 | 0.706 |
origin × treatment | 1 | 109 | 0.02 | 0.890 |
species × origin × treatment | 1 | 109 | 0.38 | 0.542 |
days | 1 | 1216 | 899.12 | <0.001 |
days × species | 1 | 1216 | 2.14 | 0.144 |
days × origin | 1 | 1216 | 7.72 | 0.006 |
days × treatment | 1 | 1216 | 1.00 | 0.317 |
days × species × origin | 1 | 1216 | 4.12 | 0.043 |
days × species × treatment | 1 | 1216 | 4.84 | 0.028 |
days × origin × treatment | 1 | 1216 | 0.33 | 0.563 |
days × species × origin × treatment | 1 | 1216 | 0.17 | 0.678 |
treatment × plot | - | - | ||
species × origin × population | 2.13 | 0.017 | ||
species × origin × treatment × unit | 4.70 | <0.001 |
The among-species approach showed a higher maximum germination rate of invasive species compared to non-invasive congeners and an overall inhibiting effect of UV-B radiation on germination success independent of the species’ status. This positive association of rapid germination and high germination percentage of seeds of native origins with species’ invasiveness has been also described in preceding studies (
The present study also indicates a stronger inhibition of germination under UV-B for Echium species, whereas Verbascum seeds, especially of invasive Verbascum thapsus, seem to be more UV-B tolerant. The tissues surrounding an embryo might act as UV-B shield, which could be a possible explanation of seed UV-B tolerance (
The within-species approach addressed the role of local adaptation in the invaded range and revealed a higher germination success of exotic origins of the invasive species from New Zealand compared to the native German populations. Again, stronger differences in germination proportions between exotic and native provenances were encountered for the Echium species compared to Verbascum, in particular when considering progression with time.
The present study confirmed a distinctly inhibiting effect of UV-B radiation on germination of the studied species, but did not provide evidence for a UV-B specific pre-adaptation of invasive species or local adaption of exotic populations to UV-B in the invaded range. The overall reducing effect of UV-B radiation on germination suggests that UV-B represents an important selection factor in the invaded range, and particularly for alien species colonizing new habitats in parts of the southern hemisphere. Possibly, neither pre-adaptation nor local adaptation fully explains the invasive potential of the study species. Instead, the phenotypic plasticity to a broad range of environmental conditions in terms of a ‘general-purpose genotype’, as was already mentioned for Verbascum thapsus (
We thank Susanne Both for seed sampling and Stephen Stilwell for technical support in New Zealand. The seed import to New Zealand could be managed via the International Plant Exchange Network (IPEN), handled by Eva Bremer (Botanical Garden of Martin Luther University Halle-Wittenberg) and Sue Molloy (Christchurch Botanic Gardens).
The study was financially supported by a DAAD (German Academic Exchange Service) travel grant awarded to MH.