Cultivated alien plants with high invasion potential are more likely to be traded online in China.

Biological invasions have become a worldwide problem, and measures to efficiently prevent and control invasions are still in development. Like many other parts of the world, China is undergoing a dramatic increase in plant invasions. Most of the currently 933 established (i.e., naturalized) plant species, of which 214 are categorized as invasive, have been introduced into China for cultivation. It is likely that many of those species are still being traded, particularly online, by plant nurseries. However, studies assessing whether naturalized and invasive species are currently being traded more or less than nonnaturalized aliens are rare. We extracted online-trade information for 13,718 cultivated alien plant taxa on 1688.com, the largest website for domestic B2B in China. We analyzed how the presence in online-nursery catalogs, the number of online nurseries that offerred the species for sale, and the product type (i.e., seeds, live plants and vegetative organs) differed among nonnaturalized, naturalized noninvasive, and invasive species. Compared to nonnaturalized taxa, naturalized noninvasive and invasive taxa were 3.7-5.2 times more likely to be available for purchase. Naturalized noninvasive and invasive taxa were more frequently offered as seeds by online nurseries, whereas nonnaturalized taxa were more frequently offered as live plants. Based on these findings, we propose that, to reduce the further spread of invasive and potentially invasive plants, implementation of plant-trade regulations and a monitoring system of the online horticultural supply chain will be essential.

Constraints on the evolution of phenotypic plasticity in the clonal plant Hydrocotyle vulgaris.

The evolution of phenotypic plasticity of plant traits may be constrained by costs and limits. However, the precise constraints are still unclear for many traits under different ecological contexts. In a glasshouse experiment, we grew ramets of 12 genotypes of a clonal plant Hydrocotyle vulgaris under the control (full light and no flood), shade and flood conditions and tested the potential costs and limits of plasticity in 13 morphological and physiological traits in response to light availability and flood variation. In particular, we used multiple regression and correlation analyses to evaluate potential plasticity costs, developmental instability costs and developmental range limits of each trait. We detected significant costs of plasticity in specific petiole length and specific leaf area in response to shade under the full light condition and developmental range limits in specific internode length and intercellular CO2 concentration in response to light availability variation. However, we did not observe significant costs or limits of plasticity in any of the 13 traits in response to flood variation. Our results suggest that the evolution of phenotypic plasticity in plant traits can be constrained by costs and limits, but such constraints may be infrequent and differ under different environmental contexts.

Invasive alien plants benefit more from clonal integration in heterogeneous environments than natives.

What confers invasive alien plants a competitive advantage over native plants remains open to debate. Many of the world's worst invasive alien plants are clonal and able to share resources within clones (clonal integration), particularly in heterogeneous environments. Here, we tested the hypothesis that clonal integration benefits invasive clonal plants more than natives and thus confers invasives a competitive advantage. We selected five congeneric and naturally co-occurring pairs of invasive alien and native clonal plants in China, and grew pairs of connected and disconnected ramets under heterogeneous light, soil nutrient and water conditions that are commonly encountered by alien plants during their invasion into new areas. Clonal integration increased biomass of all plants in all three heterogeneous resource environments. However, invasive plants benefited more from clonal integration than natives. Consequently, invasive plants produced more biomass than natives. Our results indicate that clonal integration may confer invasive alien clonal plants a competitive advantage over natives. Therefore, differences in the ability of clonal integration could potentially explain, at least partly, the invasion success of alien clonal plants in areas where resources are heterogeneously distributed.

Clonal integration in homogeneous environments increases performance of Alternanthera philoxeroides.

Physiological integration between connected ramets can increase the performance of clonal plants when ramets experience contrasting levels of resource availabilities in heterogeneous environments. It has generally been shown or assumed that clonal integration has little effect on clonal performance in homogeneous environments. However, a conceptual model suggests that integration could increase performance in a homogeneous environment when connected ramets differ in uptake ability and external resource supply is high. We tested this hypothesis in a greenhouse experiment with the amphibious plant Alternanthera philoxeroides. Ramets in clonal fragments containing three rooted and two unrooted ramets were either left connected or divided into a basal part with two rooted ramets and an apical part with the other ramets. To simulate realistic, homogeneous environments of the species with different levels of resource supply, plants were grown at 0, 20, or 40 cm of water depth. Water depth had a positive effect on most measures of growth, indicating that resource supply increased with depth. Connection had negative to neutral effects on total growth of fragments at a water depth of 0 cm, and neutral to positive effects at 20- and 40-cm depths; effects on the apical part were generally positive and larger at greater depth; effects on the basal part were generally negative and smaller at greater depth. Results largely supported the hypothesis and further suggest that clonal integration of allocation and reproduction may modify benefits of resource sharing in homogeneous environments.

Transgenerational Herbivory Effects on Performance of Clonal Offspring of the Invasive Plant Alternanthera philoxeroides.

Interactions between alien plants and local enemies in introduced ranges may determine plant invasion success. However, little is known about whether herbivory-induced responses are transmitted across vegetative generations of plants and whether epigenetic changes are involved during this process. In a greenhouse experiment, we examined the effects of herbivory by the generalist herbivore Spodoptera litura on the growth, physiology, biomass allocation and DNA methylation level of the invasive plant Alternanthera philoxeroides in the first- (G1), second- (G2) and third-generation (G3). We also tested the effects of root fragments with different branching orders (i.e., the primary- or secondary-root fragments of taproots) of G1 on offspring performance. Our results showed that G1 herbivory promoted the growth of the plants in G2 that sprouted from the secondary-root fragments of G1 but had a neutral or negative effect on the growth of the plants in G2 from the primary-root fragments. The growth of plants in G3 was significantly reduced by G3 herbivory but not affected by G1 herbivory. Plants in G1 exhibited a higher level of DNA methylation when they were damaged by herbivores than when they were not, while neither plants in G2 nor G3 showed herbivory-induced changes in DNA methylation. Overall, the herbivory-induced growth response within one vegetative generation may represent the rapid acclimatization of A. philoxeroides to the unpredictable generalist herbivores in the introduced ranges. Herbivory-induced trans-generational effects may be transient for clonal offspring of A. philoxeroides, which can be influenced by the branching order of taproots, but be less characterized by DNA methylation.

Effects of soil nutrient heterogeneity on intraspecific competition in the invasive, clonal plant Alternanthera philoxeroides.

BACKGROUND AND AIMS: Fine-scale, spatial heterogeneity in soil nutrient availability can increase the growth of individual plants, the productivity of plant communities and interspecific competition. If this is due to the ability of plants to concentrate their roots where nutrient levels are high, then nutrient heterogeneity should have little effect on intraspecific competition, especially when there are no genotypic differences between individuals in root plasticity. We tested this hypothesis in a widespread, clonal species in which individual plants are known to respond to nutrient heterogeneity. METHODS: Plants derived from a single clone of Alternanthera philoxeroides were grown in the greenhouse at low or high density (four or 16 plants per 27·5 × 27·5-cm container) with homogeneous or heterogeneous availability of soil nutrients, keeping total nutrient availability per container constant. After 9 weeks, measurements of size, dry mass and morphology were taken. KEY RESULTS: Plants grew more in the heterogeneous than in the homogeneous treatment, showing that heterogeneity promoted performance; they grew less in the high- than in the low-density treatment, showing that plants competed. There was no interactive effect of nutrient heterogeneity and plant density, supporting the hypothesis that heterogeneity does not affect intraspecific competition in the absence of genotypic differences in plasticity. Treatments did not affect morphological characteristics such as specific leaf area or root/shoot ratio. CONCLUSIONS: Results indicate that fine-scale, spatial heterogeneity in the availability of soil nutrients does not increase competition when plants are genetically identical, consistent with the suggestion that effects of heterogeneity on competition depend upon differences in plasticity between individuals. Heterogeneity is only likely to increase the spread of monoclonal, invasive populations such as that of A. philoxeroides in China.

Parental effects driven by resource provisioning in Alternanthera philoxeroides-A simulation case study.

Parental environmental effects can be a rapid and effective means for clonal plants in response to temporally or spatially varying environments. However, few studies have quantitatively measured the ecological significance of parental effects in aquatic clonal plants. In this study, we developed a two-generation (parent-offspring) growth model to examine the parental effects of nitrogen (N) conditions on summed and mean performance of clonal offspring of one wetland species Alternanthera philoxeroides. We also examined the role of survival status and developmental stage of clonal offspring in the consequence of parental effects in aquatic clonal plants. Our results indicated direct evidence that (1) there were significant non-linear correlations between the performance of parental plants and initial status of clonal offspring (i.e., the mass and number of clonal propagules); (2) parental N effects on the summed performance of clonal offspring were content-dependent (i.e., there were significant interactions between parental and offspring N effects), while parental effects on the mean performance of offspring were independent of offspring conditions; (3) parental effects mainly occurred at the early development stage of clonal offspring, and then gradually declined at the late stage; (4) the context-dependent parental effects on the summed performance of clonal offspring gradually strengthened when offspring survival was high. The mathematical models derived from the experimental data may help researchers to not only deeply explore the ecological significance of parental environmental effects in aquatic clonal plants, but also to reveal the importance of potential factors that have been often neglected in empirical studies.

Modification by earthworms of effects of soil heterogeneity and root foraging in eight species of grass.

Spatial heterogeneity of soil nutrients and earthworm activity can each increase the performance of plant species, but their interactive effects have been little studied. The ability of plants to forage for nutrients by concentrating roots where nutrients are concentrated can partly explain the positive effects of nutrient heterogeneity, but whether root foraging can help explain the positive effects of earthworm activity is untested. We conducted a greenhouse experiment in which we grew eight species of Poaceae in homogeneous and heterogeneous soils with or without the earthworms Eisenia fetida and Metaphire guillelmi and measured net accumulation of plant mass and tillers. Effects of heterogeneity and earthworms on plant performance were positive in most species. The presence of earthworms reduced the directly measured effect of heterogeneity on total mass in some grass species. Most species showed root foraging ability. Ability showed no relationship to effects of heterogeneity or earthworms on final total dry mass. However, earthworms reduced foraging in some species, possibly by lessening heterogeneity. Earthworm activity in heterogeneous soil may thus reduce the benefits of root foraging for nutrients in plants.

A multi-species comparison of selective placement patterns of ramets in invasive alien and native clonal plants to light, soil nutrient and water heterogeneity.

A worth noticing pattern in current invasive biology is the clonal ability of many of the world's worst invasive plants. Selective placement of ramets (i.e. foraging behavior) can intensify ramet performance and allocation, and place more ramets in the more favorable microhabitats, which can maximum utilize resource and share risk in heterogeneous environments. Still little is known about whether invasive alien and native clonal plants differ in the selective placement patterns of ramets in invasive clonal plants or not. We used five congeneric pairs of naturally co-occurring invasive alien and native clonal plant species in China. In a glasshouse, we grew all species in pots under a homogeneous and three heterogeneous conditions (i.e. light, soil nutrients or water) subjected to resource-high or -low patches. All biomass parameters and number of ramets significantly increased in resource-high patches in all three types of heterogeneous environments. Interestingly, growth of invasive alien plants benefited significantly more from resource-high patches than native plants in all heterogeneous environments. Overall, invasive had higher biomass parameters per ramet than natives. Ramet parameters of invasive plants also benefited more from resource-low patches than natives. Three different selective placement patterns of ramets in resource-low patches were exhibited in invasive plants: ramet increasing shoot investment (above pattern), increasing root investment (below pattern) and increasing both investments (complete pattern) in the light, soil water and nutrient heterogeneity, respectively. Investment on less, larger ramet was the adaptive strategy of invasive plants in resource-poor patches. The results suggest that adaptively selective placement patterns of ramets promote a higher morphology plasticity and performance in invasive clonal plants over natives. When alien clonal plants spread new areas with light, soil nutrients or water heterogeneity, selective placement patterns of ramets might play an important role in plant performance and competitive superior by capitalizing more on additional resources.

Context-Dependent Parental Effects on Clonal Offspring Performance.

Parental environments may potentially affect offspring fitness, and the expression of such parental effects may depend on offspring environments and on whether one considers an individual offspring or all offspring of a parent. Using a well-studied clonal herb, Alternanthera philoxeroides, we first grew parent plants in high and low soil-nutrient conditions and obtained 1st generation clonal offspring from these two environments. Then we grew offspring of these two types of 1st generation clonal offspring also in high and low nutrient conditions. We measured and analyzed mean performance and summed performance of the four types of 2nd generation clonal offspring. High nutrient availability of parental environments markedly increased both mean performance (i.e., the average fitness measure across all individual offspring produced by a parent) and summed performance (i.e., the sum of the fitness measure of all offspring produced by a parent) of the 2nd generation clonal offspring. The positive parental effects on summed performance of the 2nd generation clonal offspring were stronger when the 1st generation clonal offspring grew in the high instead of the low nutrient conditions, but the positive parental effects on their mean performance did not depend on the nutrient environments of the 1st generation clonal offspring. The results provide novel evidence that parental environmental effects persist across vegetative generations and strongly depend on offspring environments and levels of plants.

Herbivory-induced maternal effects on growth and defense traits in the clonal species Alternanthera philoxeroides.

Plants have evolved a variety of defense traits against foliar herbivory, including the production of primary and secondary metabolites, the allocation of chemical compounds, and morphological plasticity. Using two vegetative generations of the invasive clonal species Alternanthera philoxeroides, we investigated the effects of maternal and offspring herbivory by Planococcus minor on the integrative defense strategy of plants. Herbivory severely inhibited leaf, stolon and root growth, as well as the production of primary metabolites (soluble sugars, starch, and total non-structural carbohydrates in stolons), and decreased average leaf area and specific leaf area of the second-generation A. philoxeroides. The changes in growth measures of the first-generation A. philoxeroides with herbivory were consistent with that of the second generation. By contrast, herbivory basically did not affect the concentration of non-structural carbohydrate compounds in the roots, and even increased the concentrations of N and total phenols in taproots. Furthermore, herbivory-induced maternal effects also reduced the growth of the second-generation plants. The results suggest that A. philoxeroides is capable of adapting to herbivory by P. minor, mainly via the allocation of available resources in belowground organs, and that the herbivory effect can persist across vegetative generations. These features may potentially improve the regeneration and tolerance of A. philoxeroides after a short-term herbivory.

Clonal integration increases tolerance of a phalanx clonal plant to defoliation.

Defoliation by herbivores commonly imposes negative effects on plants, and physiological integration (resource sharing) can enhance the ability of guerilla clonal plants to tolerate stresses. Here we examined whether physiological integration can increase the ability of phalanx clonal plants to withstand defoliation. On a high mountain grassland in southwestern China, we subjected the phalanx clonal plant Iris delavayi within 10cm×10cm plots to three levels of defoliation intensity, i.e., control (no defoliation), moderate (50% shoot removal to simulate moderate herbivory) and heavy defoliation (100% shoot removal to simulate heavy herbivory), and kept rhizomes at the plot edges connected (allowing physiological integration) or disconnected (preventing integration) with intact ramets outside the plots. Defoliation significantly reduced leaf biomass, root biomass and ramet number of I. delavayi. Clonal integration did not affect the growth of I. delavayi under control, but significantly increased total biomass, rhizome and root biomass under heavy defoliation, and leaf biomass and ramet number under moderate defoliation. We conclude that clonal integration associated with resource reallocation plays an important role in maintaining the productivity of the alpine and subalpine grassland ecosystems in SW China where clonal plants are a dominant component of the grasslands and are commonly extensively managed with moderate grazing intensity. Our results also help to better understand the adaption and tolerance of phalanx clonal plants subjected to long-term grazing in the high mountain environment.

Nutrient enrichment alters impacts of Hydrocotyle vulgaris invasion on native plant communities.

Nutrients may affect the invasiveness of alien plants and the invasibility of native plant communities. We performed a greenhouse experiment to investigate the interactive effect of invasion by a clonal herb Hydrocotyle vulgaris and nutrient enrichment on biomass and evenness of native plant communities. We established three types of plant communities (H. vulgaris alone, native plant communities without or with H. vulgaris) under low and high levels of nutrients. Native communities consisted of eight native, terrestrial species of three functional groups, i.e. four grasses, two legumes, and two forbs. Invasion of H. vulgaris had no effect on biomass of the native community, the functional groups, or the individual species. High nutrients increased biomass of grasses, but reduced evenness of the community. High nutrients also decreased the competitive effect, and the relative dominance index of H. vulgaris. Therefore, high nutrients reduced the competitive ability of H. vulgaris and enhanced the resistance of the native community to invasion. The results provide a basis for management strategies to control the invasion and spread of H. vulgaris by manipulating resource availability to support native communities.

[Effects of light intensity contrast on clonal integration of Spartina anglica].

We conducted a greenhouse experiment to test how clonal integration affected the growth responses of Spartina anglica to light intensity heterogeneity in light availability and whether such effects depended on contrast light intensity. The experiment had three homogeneous treatments and two heterogeneous treatments. In the homogeneous treatments, both ramets of a connected ramet pair were unshaded (high light intensity), moderately shaded (medium light intensity, 70% of the high light intensity) and deeply shaded (low light intensity, 30% of the high light intensity). In the heterogeneous treatments, one ramet of a pair was unshaded, but its connected ramet was either moderately shaded (low light intensity contrast) or deeply shaded (high light intensity contrast). In the homogeneous treatments, biomass of S. anglica was significantly higher in the high light intensity treatment than in the medium and low light intensity treatments. Number of leaves, root length, and total biomass were significantly higher in the shaded ramet in the heterogeneous treatment with low light intensity contrast than in the ramet in the homogeneous treatment with medium light intensity. Final size and mass were not significantly different between the unshaded ramet in the heterogeneous treatment with low light intensity contrast and the ramets in the homogeneous high light intensity treatment. These results suggested that clonal integration benefitted a shaded ramet with little cost to an unshaded ramet when contrast in light intensity was low. However, effects of clonal integration were not significant when contrast was high. It therefore appeared that effects of clonal integration on the growth of S. anglica did not increase with increasing light intensity contrast. In natural habitats, clonal integration might improve growth of S. anglica when its ramets are moderately shaded by other plants but not when they are deeply shaded.

Effects of heterogeneous competitor distribution and ramet aggregation on the growth and size structure of a clonal plant.

Spatially heterogeneous distribution of interspecific competitors and intraspecific aggregation of offspring ramets may affect the growth and size structure of clonal plant populations, but these have been rarely studied. We conducted a greenhouse experiment in which we grew a population of eight offspring ramets (plants) of the stoloniferous clonal plant Hydrocotyle vulgaris aggregately or segregately in two homogeneous treatments with or without a competing grass Festuca elata and a heterogeneous treatment with a patchy distribution of the grass. In patchy grass treatments, H. vulgaris produced markedly more biomass, ramets and stolons in open patches (without grasses) than in grass patches, but displayed lower size variations as measured by coefficient of variation of biomass, ramets and stolons among the eight plants. In open areas, H. vulgaris produced statistically the same amounts of biomass and even more stolons and showed higher size variations in patchy grass treatments than in open (no grass) treatments. In grass areas, H. vulgaris grew much worse and displayed higher size variations in patchy grass treatments than in full grass treatments. Ramet aggregation decreased the growth of H. vulgaris in open treatments and in both open and grass patches in patchy grass treatments, but had little effect in full grass treatments. Ramet aggregation had little effect on size variations. Therefore, heterogeneous distribution of competitors can affect the growth and size structure of clonal plant populations, and ramet aggregation may decrease population growth when they grow in open environments or heterogeneous environments with a patchy distribution of interspecific competitors.

Patchy distributions of competitors affect the growth of a clonal plant when the competitor density is high.

Environments are patchy in not only abiotic factors but also biotic ones. Many studies have examined effects of spatial heterogeneity in abiotic factors such as light, water and nutrients on the growth of clonal plants, but few have tested those in biotic factors. We conducted a greenhouse experiment to examine how patchy distributions of competitors affect the growth of a rhizomatous wetland plant Bolboschoenus planiculmis and whether such effects depend on the density of the competitors. We grew one ramet of B. planiculmis in the center of each of the experimental boxes without competitors (Schoenoplectus triqueter), with a homogeneous distribution of the competitors of low or high density, and with a patchy distribution of the competitors of low or high density. The presence of competitors markedly decreased the growth (biomass, number of ramets, number of tubers and rhizome length) of the B. planiculmis clones. When the density of the competitors was low, the growth of B. planiculmis did not differ significantly between the competitor patches and competitor-free patches. However, when the density of the competitors was high, the growth of B. planiculmis was significantly higher in the competitor-free patches than in the competitor patches. Therefore, B. planiculmis can respond to patchy distributions of competitors by placing more ramets in competition-free patches when the density of competitors is high, but cannot do so when the density of competitors is low.

Soil particle heterogeneity affects the growth of a rhizomatous wetland plant.

Soil is commonly composed of particles of different sizes, and soil particle size may greatly affect the growth of plants because it affects soil physical and chemical properties. However, no study has tested the effects of soil particle heterogeneity on the growth of clonal plants. We conducted a greenhouse experiment in which individual ramets of the wetland plant Bolboschoenus planiculmis were grown in three homogeneous soil treatments with uniformly sized quartz particles (small: 0.75 mm, medium: 1.5 mm, or large: 3 mm), one homogeneous treatment with an even mixture of large and medium particles, and two heterogeneous treatments consisting of 16 or 4 patches of large and medium particles. Biomass, ramet number, rhizome length and spacer length were significantly greater in the treatment with only medium particles than in the one with only large particles. Biomass, ramet number, rhizome length and tuber number in the patchy treatments were greater in patches of medium than of large particles; this difference was more pronounced when patches were small than when they were large. Soil particle size and soil particle heterogeneity can greatly affect the growth of clonal plants. Thus, studies to test the effects of soil heterogeneity on clonal plants should distinguish the effects of nutrient heterogeneity from those of particle heterogeneity.

Burial depth and stolon internode length independently affect survival of small clonal fragments.

Disturbance can fragment plant clones into different sizes and unstabilize soils to different degrees, so that clonal fragments of different sizes can be buried in soils at different depths. As a short-term storage organ, solon internode may help fragmented clones of stoloniferous plants to withstand deeper burial in soils. We address (1) whether burial in soils decreases survival and growth of small clonal fragments, and (2) whether increasing internode length increases survival and growth of small fragments under burial. We conducted an experiment with the stoloniferous, invasive herb Alternanthera philoxeroides, in which single-node fragments with stolon internode of 0, 2, 4 and 8 cm were buried in soils at 0, 2, 4 and 8 cm depth, respectively. Increasing burial depth significantly reduced survival of the A. philoxeroides plants and increased root to shoot ratio and total stolon length, but did not change growth measures. Increasing internode length significantly increased survival and growth measures, but there was no interaction effect with burial depth on any traits measured. These results indicate that reserves stored in stolon internodes can contribute to the fitness of the A. philoxeroides plants subject to disturbance. Although burial reduced the regeneration capacity of the A. philoxeroides plants, the species may maintain the fitness by changing biomass allocation and stolon length once it survived the burial. Such responses may play an important role for A. philoxeroides in establishment and invasiveness in frequently disturbed habitats.