The Invasive Plant Alternanthera philoxeroides Was Suppressed More Intensively than Its Native Congener by a Native Generalist: Implications for the Biotic Resistance Hypothesis

Prior studies on preferences of native herbivores for native or exotic plants have tested both the enemy release hypothesis and the biotic resistance hypothesis and have reported inconsistent results. The different levels of resistance of native and exotic plants to native herbivores could resolve this controversy, but little attention has been paid to this issue. In this study, we investigated population performance, photosynthesis, leaf nitrogen concentration, and the constitutive and induced resistances of the successful invasive plant, Alternanthera philoxeroides, and its native congener, Alternanthera sessilis, in the presence of three population densities of the grasshopper, Atractomorpha sinensis. When the grasshopper was absent, leaf biomass, total biomass, photosynthesis, and leaf nitrogen concentration of A. philoxeroides were higher than those of A. sessilis. However, the morphological and physiological performances of A. philoxeroides were all decreased more intensively than A. sessilis after herbivory by grasshoppers. Especially as the concentrations of constitutive lignin and cellulose in leaf of A. philoxeroides were higher than A. sessilis, A. philoxeroides exhibited increased leaf lignin concentration to reduce its palatability only at severe herbivore load, whereas, leaf lignin, cellulose, and polyphenolic concentrations of A. sessilis all increased with increasing herbivory pressure, and cellulose and polyphenolic concentrations were higher in A. sessilis than in A. philoxeroides after herbivory. Our study indicated that the capability of the invasive plant to respond to native insect damage was lower than the native plant, and the invasive plant was suppressed more intensively than its native congener by the native insect. Our results support the biotic resistance hypothesis and suggest that native herbivores can constrain the abundance and reduce the adverse effects of invasive species.     

No impact of a native beetle on exotic plant performance and competitive ability due to plant compensation

The novel associations between invasive plants and their natural enemies in the introduced range have recently received increasing attention; however, the effects of novel enemies on exotic plant performance and competition with native species remain poorly explored. Here, we tested the impact of herbivory by a native beetle, Cassida piperata, on the performance of the exotic species Alternanthera philoxeroides and competition with a native congener, Alternanthera sessilis, using common garden experiments in central China. We found A. philoxeroides was able to fully compensate for intense herbivory by C. piperata. Herbivory by C. piperata that released at the average density in this region had no impact on competition between the native and exotic plant species. Our results indicate that herbivory by novel enemies may not reduce exotic plant performance due to plant compensation. However, high tolerance to herbivory may not confer a competitive advantage for exotic species compared to less tolerant native competitors if the herbivore damage is below a certain threshold. Thus, it is necessary to assess the impact of novel enemies on exotic plant performance and competition with native plants along gradients of insect densities. This may lead to a better understanding of how best to exploit the role of native herbivores in facilitating or slowing plant invasions.     

The Invasive Wetland Plant Alternanthera philoxeroides Shows a Higher Tolerance to Waterlogging than Its Native Congener Alternanthera sessilis

Plant invasion is one of the major threats to natural ecosystems. Phenotypic plasticity is considered to be important for promoting plant invasiveness. High tolerance of stress can also increase survival of invasive plants in adverse habitats. Limited growth and conservation of carbohydrate are considered to increase tolerance of flooding in plants. However, few studies have examined whether invasive species shows a higher phenotypic plasticity in response to waterlogging or a higher tolerance of waterlogging (lower plasticity) than native species. We conducted a greenhouse experiment to compare the growth and morphological and physiological responses to waterlogging of the invasive, clonal, wetland species Alternanthera philoxeroides with those of its co-occurring, native, congeneric, clonal species Alternanthera sessilis. Plants of A. philoxeroides and A. sessilis were subjected to three treatments (control, 0 and 60 cm waterlogging). Both A. philoxeroides and A. sessilis survived all treatments. Overall growth was lower in A. philoxeroides than in A. sessilis, but waterlogging negatively affected the growth of A. philoxeroides less strongly than that of A. sessilis. Alternanthera philoxeroides thus showed less sensitivity of growth traits (lower plasticity) and higher waterlogging tolerance. Moreover, the photosynthetic capacity of A. philoxeroides was higher than that of A. sessilis during waterlogging. Alternanthera philoxeroides also had higher total non-structural and non-soluble carbohydrate concentrations than A. sessilis at the end of treatments. Our results suggest that higher tolerance to waterlogging and higher photosynthetic capacity may partly explain the invasion success of A. philoxeroides in wetlands.     

Phenotypic plasticity of invasive Alternanthera philoxeroides in relation to different water availability, compared to its native congener

Phenotypic plasticity and genetic differentiation are two possible mechanisms that plants use to cope with varying environments. Although alligator weed (Alternanthera philoxeroides) possesses very low genetic diversity, this alien weed has successfully invaded diverse habitats with considerably varying water availability (from swamps to dry lands) in China. In contrast, its native congener (Alternanthera sessilis) has a much narrower ecological breadth, and is usually found in moist habitats. To understand the mechanisms underlying the contrasting pattern, we performed a greenhouse experiment to compare the reaction norms of alligator weed with those of its native congener, in which water availability was manipulated. Our results revealed that the two congeners had similar direction of phenotypic plasticity. However, A. philoxeroides showed greater plasticity in amount than did A. sessilis in many traits examined during the switch from wet to drought treatment. Nearly all of the phenotypic variance in A. philoxeroides could be ascribed to plasticity, while A. sessilis had a much higher fraction of phenotypic variance that could be explained by genotypic variation. These interspecific differences in plastic responses to variable water availability partially explained the difference in spatial distribution of the two congeners.     

Effects of node position on regeneration of stolon fragments in congeneric invasive and native Alternanthera species in China

Vegetative regeneration plays an important role in the adaptation of clonal plants in frequently disturbed habitats, but few studies have compared vegetative regeneration capacity of invasive clonal plants with that of their native congeners. Vegetative regeneration capacity from shoot nodes can also be affected by the position of the nodes, but this appears little studied. We conducted a greenhouse experiment with Alternanthera philoxeroides, a highly invasive species in China, and its native congener A. sessilis to test the difference in vegetative regeneration capacity of stolon nodes at five different positions (i.e. 3rd, 4th, 5th, 6th and 7th node starting from the apex of the stolon). At the end of the experiment, we counted and harvested all regenerated plants and determined their biomass and allocation. Both species could successfully regenerate from stolon fragments and node position significantly affected regeneration rate and subsequent growth. However, the vegetative regeneration capacity of A. philoxeroides was not higher than that of A. sessilis. These results suggest that vegetative regeneration from stolon fragments may not be a trait that can explain the invasiveness of A. philoxeroides.     

Nitrogen addition increases intraspecific competition in the invasive wetland plant Alternanthera philoxeroides,but not in its native congener Alternanthera sessilis

Nitrogen is often released in pulses with different frequencies, and N supply pulses may affect growth, reproduction, and biomass allocation of plants. However, few studies have examined how N supply pulses affect intraspecific competition of clonal plants and whether such an effect depends on the N supply amount. We grew one (no competition) or 12 ramets (with intraspecific competition) of both an invasive clonal plant Alternanthera philoxeroides and its native congener Alternanthera sessilis in five different N treatments: control (no N addition), low/high amount with low/high frequencies (pulses). Nitrogen addition significantly increased the growth of both species, while intraspecific competition decreased it. Nitrogen addition significantly increased intraspecific competitive intensity of A. philoxeroides as measured by the log response ratio of growth traits, but did not affect that of A. sessilis. Despite the N supply amount, N pulses had little effect on the growth and thus intraspecific competition of the two species. Therefore, increasing N deposition may change population structure and dynamics and the invasion succession of A. philoxeroides, but changes in N pulses may not.     

History of exposure to herbivores increases the compensatory ability of an invasive plant

Release from natural enemies is frequently cited as an important factor contributing to plant invasions. But such effects are likely to be temporary—native herbivores can form new plant-herbivore associations and co-evolved insects might reach the new range. While the potential effects of the initial enemy release have been well studied, the consequences of any resumption of herbivory are poorly understood. Alternanthera philoxeroides is one of the most widespread invasive plants in China and is attacked both by a specialist herbivore introduced from the native range, Agasicles hygrophila, and a native beetle Cassida piperata Hope which has formed a new association. However, these insects are not found throughout the invaded range. To test the effect of the history of population exposure to herbivory on compensatory ability, plants were cultured from 14 populations around China that differed in whether A. hygrophila or C. piperata were present. Treatment plants were exposed to herbivory by A. hygrophila for a week until 50% of the leaf area was defoliated, then grown for 80 days. Plants from populations with prior exposure to herbivory (of any kind) accumulated more root mass than populations without prior exposure, indicating that prior exposure to insects can stimulate plant compensation to herbivory. We would recommend that potential changes in plant tolerance in response to prior exposure to herbivory are considered in invasive plant management plans that employ bio-control agents.     

Differences in interactions of aboveground and belowground herbivores on the invasive plant <Emphasis Type="Italic">Alternanthera philoxeroides</Emphasis> and native host <Emphasis Type="Italic">A. sessilis</Emphasis>

Plant invasions may result in novel plant-herbivore interactions. However, we know little about whether and how invasive plants can mediate native above- and belowground herbivore interactions. In this study, we conducted greenhouse experiments to examine the interaction between a native defoliating beetle, Cassida piperata, and a native root-knot nematode, Meloidogyne incognita, on the invasive alligator weed, Alternanthera philoxeroides. We also included their native host A. sessilis in the experiments to examine whether the patterns of above- and belowground herbivore interaction vary with host plants (invasive vs. native). We analyzed total carbon and nitrogen in leaves and roots attacked by M. incognita and C. piperata. M. incognita slightly negatively affected feeding by C. piperata on A. philoxeroides, and the leaf area damaged decreased as the number of M. incognita increased. M. incognita had a negative impact on total leaf nitrogen, but had no impact on total leaf carbon. M. incognita egg production on A. philoxeroides roots decreased as the amount of damage caused by C. piperata increased. Herbivory by C. piperata did not affect total root carbon or nitrogen. M. incognita and C. piperata did not affect each other on the native plant A. sessilis. These results suggest that invasive plants can mediate native above- and belowground herbivore interactions. The knowledge of how invasive plants affect those interactions is crucial for better understanding the impacts of biological invasions on native above- and belowground organisms.     

The influence of abiotic stress and phenotypic plasticity on the distribution of invasive Alternanthera philoxeroides along a riparian zone

Relatively few studies have compared invasibility and species invasiveness among microhabitats within communities, synchronously. We surveyed the abundance and performance of non-native Alternanthera philoxeroides (Mart.) Griseb. (alligator weed), its co-occurring native congener, Alternanthera sessilis (L.) DC. (sessile joyweed), and other species in a wetland community along a riparian zone in southeast China to test the hypotheses that: i) degree of invasion differs between different types of microhabitats within the community; and ii) microhabitat types that differ in invasibility also differ in soil resource availability or in sediment characteristics likely to affect resource availability; iii) phenotypic plasticity of A. philoxeroides may play a key role in its adaptation to diverse habitats as can be concluded from its extremely low genetic diversity in China. The study riparian zone comprises different types of microhabitats including wet abandoned field, swamp, marsh dunes and gravel dunes. Consistent with these hypotheses, cover of A. philoxeroides was high in abandoned fields (73 ± 2.9%) and swamps (94 ± 1.3%), which had high soil nutrients and water availability. On the contrary, cover of native A. sessilis was relatively high in marsh dunes and grave dunes, which had coarse gravel surfaces, low soil nutrients and low water availability. A. philoxeroides showed greater morphological plasticity in response to habitat variation. In abiotically harsh habitats, stems had limited growth, and were prostrate with weak adventitious roots at nodes, forming thin, scattered patches. In the two richer habitats, the highly branched plants spread over the water or soil surface, supporting dense stronger leaf-bearing stems which grew vertically. The growth pattern of A. sessilis among microhabitats did not exhibit significant variations. These results suggest that morphological plasticity and microhabitat types with high soil resources may facilitate invasions of A. philoxeroides.     

Responses of a native beetle to novel exotic plant species with varying invasion history

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施氮对空心莲子草(Alternanthera philoxeroides)和莲子草(Alternanthera sessilis)种间关系的影响

自然界的氮素释放总是呈现出空间和时间上的异质性,但关于异质性氮释放对于入侵植物和本地植物种间关系影响的研究相对较少。将入侵植物空心莲子草(Alternanthera philoxeroides)和同属本地植物莲子草(Alternanthera sessilis)分别进行单种种植(12株,无种间竞争)和混种种植(每种6株,有种间竞争),模拟大气氮湿沉降设置由两种不同施氮总量(15g N m~(-2)a~(-1)和30g N m~(-2)a~(-1))和两种不同施氮频率(每5天1次和每15天1次)交叉组成的4种施氮处理,并以不施氮为对照。施氮总量的增加显著促进了两种植物的生长,但对两种植物的种间竞争关系没有显著影响。施氮频率对两种植物的生长以及种间竞争关系都没有显著影响。两种植物在面对竞争时表现出不同的生物量分配策略,空心莲子草将更多的生物量分配到茎,而莲子草将更多的生物量分配到根。在全球变化的背景下,大气氮湿沉降可能会改变两种植物的种群结构和动态,但可能对这两种植物的种间关系影响较小。     

Climate warming increases biological control agent impact on a non‐target species

Climate change may shift interactions of invasive plants, herbivorous insects and native plants, potentially affecting biological control efficacy and non‐target effects on native species. Here, we show how climate warming affects impacts of a multivoltine introduced biocontrol beetle on the non‐target native plant Alternanthera sessilis in China. In field surveys across a latitudinal gradient covering their full distributions, we found beetle damage on A. sessilis increased with rising temperature and plant life history changed from perennial to annual. Experiments showed that elevated temperature changed plant life history and increased insect overwintering, damage and impacts on seedling recruitment. These results suggest that warming can shift phenologies, increase non‐target effect magnitude and increase non‐target effect occurrence by beetle range expansion to additional areas where A. sessilis occurs. This study highlights the importance of understanding how climate change affects species interactions for future biological control of invasive species and conservation of native species.     

Non-target plant testing of the flea beetle Agasicles hygrophila,a biological control agent for Alternanthera philoxeroides (alligatorweed) in China

Non-target plant selection tests using 20 representative species showed that Agasicles hygrophila could feed on Alternanthera sessilis, but the mature larvae did not pupate successfully. A. hygrophila could not complete their life cycle on the other plant species tested. Thus, A. hygrophila is safe for controlling Alternanthera philoxeroides in China.     

Olfactory response of a predatory mirid to herbivore induced plant volatiles: multiple herbivory vs. single herbivory

Plants infested with a single herbivore species can attract natural enemies through the emission of herbivore‐induced plant volatiles (HIPVs). However, under natural conditions plants are often attacked by more than one herbivore species. We investigated the olfactory response of a generalist predators Macrolophus caliginosus to pepper infested with two‐spotted spider mites, Tetranychus urticae, or green peach aphid, Myzus persicae, vs. plants infested with both herbivore species in a Y‐tube olfactometer set up. In addition, the constituents of volatile blends from plants exposed to multiple or single herbivory were identified by gas chromatography‐mass spectrometry (GC‐MS). The mirid bugs showed a stronger response to volatiles emitted from plants simultaneously infested with spider mites and aphids than to those emitted from plants infested by just one herbivore, irrespective of the species. Combined with results from previous studies under similar conditions we infer that this was a reaction to herbivore induced plant volatiles. The GC‐MS analysis showed that single herbivory induced the release of 22 additional compounds as compared with the volatiles emitted from clean plants. Quantitative analyses revealed that the amount of volatile blends emitted from pepper infested by both herbivores was significantly higher than that from pepper infested by a single herbivore. Moreover, two unique substances were tentatively identified (with a probability of 94% and 91%, respectively) in volatiles emitted by multiple herbivory damaged plants: α‐zingiberene and dodecyl acetate.     

The influence of abiotic stress and phenotypic plasticity on the distribution of invasive Alternanthera philoxeroides along a riparian zone

Relatively few studies have compared invasibility and species invasiveness among microhabitats within communities, synchronously. We surveyed the abundance and performance of non-native Alternanthera philoxeroides (Mart.) Griseb. (alligator weed), its co-occurring native congener, Alternanthera sessilis (L.) DC. (sessile joyweed), and other species in a wetland community along a riparian zone in southeast China to test the hypotheses that: i) degree of invasion differs between different types of microhabitats within the community; and ii) microhabitat types that differ in invasibility also differ in soil resource availability or in sediment characteristics likely to affect resource availability; iii) phenotypic plasticity of A. philoxeroides may play a key role in its adaptation to diverse habitats as can be concluded from its extremely low genetic diversity in China. The study riparian zone comprises different types of microhabitats including wet abandoned field, swamp, marsh dunes and gravel dunes. Consistent with these hypotheses, cover of A. philoxeroides was high in abandoned fields (73 ± 2.9%) and swamps (94 ± 1.3%), which had high soil nutrients and water availability. On the contrary, cover of native A. sessilis was relatively high in marsh dunes and grave dunes, which had coarse gravel surfaces, low soil nutrients and low water availability. A. philoxeroides showed greater morphological plasticity in response to habitat variation. In abiotically harsh habitats, stems had limited growth, and were prostrate with weak adventitious roots at nodes, forming thin, scattered patches. In the two richer habitats, the highly branched plants spread over the water or soil surface, supporting dense stronger leaf-bearing stems which grew vertically. The growth pattern of A. sessilis among microhabitats did not exhibit significant variations. These results suggest that morphological plasticity and microhabitat types with high soil resources may facilitate invasions of A. philoxeroides.     

Exotic weevil invasion increases floral herbivore community density,function, and impact on a native plant

Consumer communities are being re‐arranged through unprecedented rates of human‐mediated invasions and extinctions. Such changes in consumer diversity potentially alter community function and impact on resource populations. Although insect herbivore invasions are increasingly common, the influence of such species additions on native resident herbivore guilds, along with their individual and combined effects on native plant resources, are rarely investigated. Here, we used site‐to‐site and plant‐to‐plant variation in herbivore composition to examine how the addition of an invasive exotic weevil, Rhinocyllus conicus, combines with a guild of native floral herbivores (tephritid flies, pyralid moths) to influence two key components of herbivore community function – aggregate herbivore densities and cumulative levels of seed destruction – on a native thistle, Cirsium canescens. Invasion of a site by R. conicus more than doubled aggregate herbivore density, resulting in increased levels of seed destruction and a halving of seed production by the native thistle. Further, herbivore function was significantly higher on individual plants attacked by R. conicus, compared to plants attacked only by native herbivores. Insect densities and levels of seed destruction on plants attacked by multiple herbivore taxa never exceeded those observed for plants attacked by R. conicus alone, suggesting that increases in herbivore community function with invasion resulted from the inclusion of a functionally dominant insect rather than any complementarity effects. Some evidence for interference between insects emerged, with a trend towards reduced moth and weevil densities in two and three taxon mixtures compared with plants attacked by each taxon alone. However, density compensation was limited so that, overall, the addition of a novel herbivore to the floral guild was associated with a significant increase in herbivore community function and impact on seed production. The results suggest that invasion of a functionally dominant herbivore into an unsaturated recipient community can augment function within a resource guild.     

Above‐ and belowground herbivory jointly impact defense and seed dispersal traits in Taraxacum officinale

Plants are able to cope with herbivores by inducing defensive traits or growth responses that allow them to reduce or avoid the impact of herbivores. Since above‐ and belowground herbivores differ substantially in life‐history traits, for example feeding types, and their spatial distribution, it is likely that they induce different responses in plants. Moreover, strong interactive effects on defense and plant growth are expected when above‐ and belowground herbivores are jointly present. The strengths and directions of these responses have been scarcely addressed in the literature. Using Taraxacum officinale, the root‐feeding nematode Meloidogyne hapla and the locust Schistocerca gregaria as a model species, we examined to what degree above‐ and belowground herbivory affect (1) plant growth responses, (2) the induction of plant defensive traits, that is, leaf trichomes, and (3) changes in dispersal‐related seed traits and seed germination. We compared the performance of plants originating from different populations to address whether plant responses are conserved across putative different genotypes. Overall, aboveground herbivory resulted in increased plant biomass. Root herbivory had no effect on plant growth. Plants exposed to the two herbivores showed fewer leaf trichomes than plants challenged only by one herbivore and consequently experienced greater aboveground herbivory. In addition, herbivory had effects that reached beyond the individual plant by modifying seed morphology, producing seeds with longer pappus, and germination success.     

植物竞争和昆虫取食调节入侵植物对土壤细菌群落和功能的影响

以入侵植物空心莲子草(Alternanthera philoxeroides(Mart.)Griseb)、本土近缘种莲子草(Alternan-thera sessilis(L.)DC)、生防昆虫莲草直胸跳甲(Agasicles hygrophila(Selman&Vogt))和本地昆虫虾钳菜披龟甲(Cassida pi...     

Differences in physiological traits and resistances of <Emphasis Type="Italic">Alternanthera philoxeroides</Emphasis> after herbivory by generalists and specialists

Many researchers have surveyed damages caused by natural enemies of invasive plants in both native and introduced ranges to test the enemy release hypothesis. In this study, we report our findings on the physiological and morphological impacts of a co-evolved specialist insect (Agasicles hygrophila) and two generalist insects (Atractomorpha sinensis and Hymenia recurvalis) in introduced ranges on an invasive plant, Alternanthera philoxeroides, in both field trials and controlled environments. The resistance of A. philoxeroides against the generalists and the specialist was also studied. We obtained consistent results in both the field trials and the controlled treatments: both the generalists and the specialist decreased leaf biomass, photosynthesis, leaf nitrogen content, and total leaf non-structural carbohydrate content in A. philoxeroides. However, the specialist decreased leaf mass, photosynthesis, and leaf nitrogen content more acutely than the generalists. Moreover, A. philoxeroides increased both leaf lignin and cellulose concentrations upon the generalists’ attack but only increased cellulose concentration in response to the specialist. Our results showed that even under the same population density, the co-evolved specialists from original ranges caused more severe morphological and physiological damage to A. philoxeroides than the generalists in introduced ranges. This revealed that invasive plants released some herbivory stress before their co-evolved specialists were introduced, which may contribute to the superior performance of invasive plants in introduced regions.     

水淹胁迫诱导喜旱莲子草茎发生类环割效应

在水淹环境中,喜旱莲子草水面上未受淹的茎段常表现出增粗膨大的现象。遭受水淹的植物被淹没的组织和器官会面临氧气缺乏和能量供应不足的问题。植物体内碳水化合物的运输需要消耗能量,当因水淹而使植株被部分淹没（即地下部分全部和地上部分的一部分被淹没）时,由于水淹缺氧导致能量供应不足,碳水化合物在植物被淹组织内的运输可能受限从而在水面上的未淹茎段中积累并对未淹茎段的径向形态产生影响。为探究水淹环境中喜旱莲子草未受淹茎段增粗膨大是否与碳水化合物积累有关,对茎被水淹和茎不受水淹的喜旱莲子草进行对比研究,结果发现：（1）水淹的喜旱莲子草位于水面上的未淹茎段节间平均直径显著大于水面下受淹茎段节间平均直径,未淹茎段与受淹茎段相比发生显著的膨大现象;未水淹的喜旱莲子草其茎的上部茎段节间平均直径与下部茎段节间平均直径相比并无显著差异,上部茎段也无明显膨大现象。（2）水淹的喜旱莲子草位于水面上的未淹茎段碳水化合物含量显著高于未水淹的喜旱莲子草对应茎段的碳水化合物含量。本研究表明,水淹胁迫下喜旱莲子草位于水面上的未受淹茎段中碳水化合物发生积累,导致植株位于水面上的未受淹茎段发生与物理环割后类似的茎膨大现象。