Xinmin Lu

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.

Flooding compromises compensatory capacity of an invasive plant: implications for biological control

Plant compensatory growth is proposed to be insidious to biological control and known to vary under different environmental conditions. However, the effects of microsite conditions on compensation capacity and its indirect impacts on biological control of plant invaders have received little attention. Alligator weed, Alternanthera phioxeroides, is an invasive plant worldwide, growing in both aquatic and terrestrial habitats that are often affected by flooding. Biological control insects have been successful in suppressing the plant in many aquatic habitats but have failed in terrestrial habitats. To evaluate the impact of flooding on compensation capacity, we conducted common garden and greenhouse experiments in which plants were grown under different moisture conditions (aquatic versus terrestrial). Our results show that plants were able to fully recover from continued herbivory in the terrestrial habitat, but failed in the aquatic habitat, indicating a flooding-regulated plant compensatory capacity. Also, the grazed plants increased below-ground growth and reproductive root bud formation in the terrestrial habitat, but there was no such difference in the aquatic habitat. Our findings suggest that the differing plant compensatory capacity, affected by flooding, may explain the different biological control efficacy of alligator weed in aquatic and terrestrial habitats. Understanding mechanisms in plant invader compensation in different microsite conditions is important for improving management efficiency.

Effects of warming and nitrogen on above- and below-ground herbivory of an exotic invasive plant and its native congener

Warming and atmospheric nitrogen deposition could impact plant community composition by altering competitive interactions, however, the effects of these environmental changes on plant invasions via above- and below-ground herbivory are unknown. Here we report the effects of warming and nitrogen addition on aboveground insect defoliation and belowground root-knot nematode infection of a native plant and an introduced invasive congener. Warming increased belowground nematode infection only, while nitrogen addition increased both nematodes and defoliation. Defoliation rates were similar for the exotic invasive and native species and the increases with nitrogen addition were large (almost doubled) but comparable. However, roots of native plant were more intensively infected (i.e., knot density) than roots of the exotic invasive plant (~4-fold in ambient conditions) and this difference increased under elevated temperature (~30-fold higher) in which total nematode infection were nearly tenfold higher. Compared to the exotic invasive plant, the native plant had a higher proportion of fine roots and specific leaf area, but lower photosynthesis ability irrespective of warming and nitrogen deposition treatments. The nematode preferred fine roots to coarse roots for both plant species. Our study indicates that above- and below-ground herbivory of plants differ in their sensitivity to varying drivers of environmental change, which may alter plant interactions and makes it difficult to predict future community structure. Together with the dramatic response of belowground nematodes to warming, this suggests that future modeling or experimental studies on species’ responses to environmental change should simultaneously consider above- and below-ground communities.

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

The impact of plant invaders on the fitness of native insects has received increasing attention, but it remains unclear how native insects that have a taxonomic conservatism in host–plant use respond to novel hosts. In this study, an experimental approach was taken to this issue by comparing the preference and performance of a native beetle, Cassida piperata Hope, on native hosts Chenopodium album and Alternanthera sessilis, and non‐coevolved exotic hosts Alternanthera spinosus and Alternanthera philoxeroides of varying invasion history with choice and cross‐rearing experiments. In host choice experiments, adult beetles preferred to oviposit on the older invader A. spinosus to the same degree as it did the native hosts, but generally avoided the newer invader A. philoxeroides. However, in rearing experiments, larval beetles developed more slowly on the two exotic hosts than on the native hosts. The varying responses of adult beetles to invaders might be explained by their differing invasive history, and suggest that the beetle has adapted to the older invader behaviourally. However, the slower development of the beetle on the two invaders suggests that the beetle has failed to adapt physiologically to either species of invasive plant. These results offer insights into the temporal dynamics of a native insect adapting to plant invaders, and suggest that when testing the impact of exotic plant invasion on native insect fitness, it is necessary to consider the duration of novel association between the insect and the novel plant species.

Increased compensatory ability of an invasive plant to above- and below-ground enemies in monocultures.

Above- and below-ground enemies have prominent influence on plant invasions, and increasing evidence has shown that plant invasions are also affected by inter- or intraspecific interactions between individual plants. However, how these two factors interactively affect plant invasions has rarely been tested. Here, we examined the response of the invasive plant Alternanthera philoxeroides (Mart.) Griseb. to above- and below-ground enemies at varying plant densities in a greenhouse experiment in Wuhan, China. We found that both above- and below-ground enemies decreased the plant total and root mass at individual and population levels, but that of the two, below-ground enemies had a greater effect than above-ground enemies, and that the two guilds of enemies acted additively on the plant. However, their impacts decreased as the plant density increased, due to enhanced plant tolerance to both guilds of enemies. The increased plant tolerance may result from changes in plant resource allocation patterns, corresponding to a positive linear relationship between the ratio of fine root mass to total root mass and plant density. Given that forming dense monocultures in their new ranges is one of the most important characteristics of invasive plants, we propose that the high compensatory ability at dense monocultures may be an important mechanism underlying exotic species invasion.

Differences in interactions of aboveground and belowground herbivores on the invasive plant Alternanthera philoxeroides and native host A. sessilis

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.

Con-specific neighbours may enhance compensation capacity in an invasive plant.

Facilitation, both by inter- and intra-specific neighbours, is known to be an important process in structuring plant communities. However, only a small number of experiments have been reported on facilitation in plant invasions, especially between invasive con-specific individuals. Here, we focus on how con-specific neighbours of the invasive alien plant alligator weed affect the tolerance of alligator weed to herbivory by the introduced biological control agent, Agasicles hygrophila. We conducted greenhouse and garden experiments in which invasive plant density and herbivory intensity (artificial clipping and real herbivory) were manipulated. In the greenhouse experiment, artificial clipping significantly reduced plant biomass when plants were grown individually, but when con-specific neighbours were present in the same pot, biomass was not significantly different from control plants. Similarly, when compared to control plants, plants that were subjected to herbivory by A. hygrophila produced more biomass when grown with two con-specific neighbours than when grown alone. Real herbivory also resulted in an increased number of vegetative buds, and again when two con-specific neighbours were present this effect was increased (a 55.3% increase in buds when there was no neighbour, but a 111.6% increase in buds when two con-specific neighbours were present). In the garden experiment, in which plants were grown at high density (6 plants per pot), alligator weed fully recovered from defoliation caused by insects at levels from 20-30% to 100%. Our results indicate that the con-specific association may increase the compensatory ability to cope with intense damage in this invasive plant.

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.

Latitudinal variation in soil biota: testing the biotic interaction hypothesis with an invasive plant and a native congener

Soil biota community structure can change with latitude, but the effects of changes on native plants, invasive plants, and their herbivores remain unclear. Here, we examined latitudinal variation in the soil biota community associated with the invasive plant Alternanthera philoxeroides and its native congener A. sessilis, and the effects of soil biota community variation on these plants and the beetle Agasicles hygrophila. We characterized the soil bacterial and fungal communities and root-knot nematodes of plant rhizospheres collected from 22 °N to 36.6 °N in China. Soil biota community structure changed with latitude as a function of climate and soil properties. Root-knot nematode abundance and potential soil fungal pathogen diversity (classified with FUNGuild) decreased with latitude, apparently due to higher soil pH and lower temperatures. A greenhouse experiment and lab bioassay showed native plant mass, seed production, and mass of beetles fed native foliage increased with soil collection latitude. However, there were no latitudinal patterns for the invasive plant. These results suggest that invasive and native plants and, consequently, their herbivores have different responses to latitudinal changes in soil-borne enemies, potentially creating spatial variation in enemy release or biotic resistance. This highlights the importance of linking above- and below-ground multitrophic interactions to explore the role of soil biota in non-native plant invasions with a biogeographic approach.

Differing interactions between an introduced beetle and a resident root nematode mediated by an invasive plant and its native congener

Interactions between above- and below-ground herbivores play an important role in shaping plant competition and invasion, while the effects of non-native species invasions on above- and below-ground interactions remain unexplored. In this study, we report the interactions between an above-ground introduced beetle and a resident root nematode hosted by an invasive plant or its native congener with a laboratory bioassay and a greenhouse experiment in Wuhan, China. Nematode infections decreased beetle food conversion rates and larval biomass on the native plant, and increased beetle food conversion rates with no detectable impact on the larval biomass on the invasive plant. Beetle defoliation decreased nematode egg production on both the native and invasive plants. The interactions of the introduced beetle and the nematode were different by the invasive and native plants, which suggests that invasive plants and their introduced herbivores have the potential to alter above- and below-ground interactions and affect associated community members, which may in turn affect invasion processes and the safety of classical biocontrol practices.