Jianqing Ding

Biological control of invasive plants through collaboration between China and the United States of America: a perspective

For more than 100xa0years, classical biological control of invasive plants through screening, introducing and releasing of host-specific natural enemies from native regions has been regarded as one of the promising approaches to the management of invasive plants. Many invasive plants in the United States of America are native to China, and vice versa. China and the USA also share a number of invasive plant species, including water hyacinth (Eichhornia crassipes), alligator weed (Alternanthera philoxeroides) and cordgrass (Spartina spp.). Collaboration between the two countries on biological control benefits both the nations by reciprocal opportunities to research and exchange natural enemies, by exchanging information on common invasive species, and by providing training for students and professionals. Here we review the history of collaboration between China and the US on biological control of more than 20 invasive plants. Current collaborative projects associated with four plant species, Polygonum perfoliatum L., Trapa natans L. Pueraria montana (Lour.) Merr. var. lobata and Ailanthus altissima (Mill.) Swingle, are also covered. We prioritize 14 invasive plants as targets for future collaborative biological control based on information on their importance in introduced areas, natural enemy records, and their potential biocontrol risk to introduced ecosystems. They are: Ampelopsis brevipendunculata, Celastrus orbiculatus, Dioscorea oppositifolia, Euonymus alata, Euonymus fortunei, Ligustrum sinense, Melia azedarach, Paulownia tomentosa, Sapium sebiferum and Ulmus pumila for the US, as well as Spartina alterniflora, Ambrosia artemisiifolia, Ambrosia trifida and Solidago canadensis for China. In addition, we emphasize that we must very carefully consider any potential non-target effect when we intend to introduce and release new natural enemies. We anticipate that the high priority both countries have placed on control of invasive plants will stimulate increasing collaboration on biological control.

Assessing potential biological control of the invasive plant, tree-of-heaven, Ailanthus altissima

Abstract Tree-of-heaven, Ailanthus altissima, is a deciduous tree indigenous to China and introduced into North America and Europe. It is a serious threat to ecosystems in introduced areas, as the plant is very competitive, and also contains allelopathic chemicals that may inhibit growth of surrounding native plants. In addition, the plant contains secondary chemicals that make it unpalatable to some insects. In this paper we assess potential biological control of this plant by reviewing literature associated with natural enemies of the plant from both its native and introduced regions in the world. Our literature surveys revealed that 46 phytophagous arthropods, 16 fungi, and one potyvirus were reported attacking tree-of-heaven, some apparently causing significant damage in China. Two weevils, Eucryptorrhynchus brandti and E. chinensis, are major pests of the plant in China and are reportedly restricted to tree-of-heaven, showing promise as potential biological control agents. Nymphs and adults of a homopteran insect, Lycorma delicatula and larvae of two lepidopteran species, Samia cynthia and Eligma narcissus, may also cause severe damage, but they are not host specific. Two rust fungi, Aecidium ailanthi J. Y. Zhuan sp. nov. and Coleosporium sp. have been reported on tree-of-heaven in China and are also promising potential candidates for biological control of the plant. Nine insect herbivores and 68 fungi are associated with tree-of-heaven in its introduced range in North America, Europe, and Asia. An oligophagous insect native to North America, the ailanthus webworm, Atteva punctella, may be a potential biocontrol agent for the plant. Among the fungal species, Fusarium osysporum f. sp. perniciosum, caused wilt of tree-of-heaven in North America and may have the potential to control the plant, but its non-target effect should be carefully evaluated. Our review indicates that there is potential for using insects or pathogens to control tree-of-heaven.

Climate warming affects biological invasions by shifting interactions of plants and herbivores

Plants and herbivorous insects can each be dramatically affected by temperature. Climate warming may impact plant invasion success directly but also indirectly through changes in their natural enemies. To date, however, there are no tests of how climate warming shifts the interactions among invasive plants and their natural enemies to affect invasion success. Field surveys covering the full latitudinal range of invasive Alternanthera philoxeroides in China showed that a beetle introduced for biocontrol was rare or absent at higher latitudes. In contrast, plant cover and mass increased with latitude. In a 2-year field experiment near the northern limit of beetle distribution, we found the beetle sustained populations across years under elevated temperature, dramatically decreasing A.xa0philoxeroides growth, but it failed to overwinter in ambient temperature. Together, these results suggest that warming will allow the natural enemy to expand its range, potentially benefiting biocontrol in regions that are currently too cold for the natural enemy. However, the invader may also expand its range further north in response to warming. In such cases where plants tolerate cold better than their natural enemies, the geographical gap between plant and herbivorous insect ranges may not disappear but will shift to higher latitudes, leading to a new zone of enemy release. Therefore, warming will not only affect plant invasions directly but also drive either enemy release or increase that will result in contrasting effects on invasive plants. The findings are also critical for future management of invasive species under climate change.

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.

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 80xa0days. 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.

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.

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.

Warming benefits a native species competing with an invasive congener in the presence of a biocontrol beetle.

Climate warming may affect biological invasions by altering competition between native and non-native species, but these effects may depend on biotic interactions. In field surveys at 33 sites in China along a latitudinal and temperature gradient from 21°N to 30.5°N and a 2-yr field experiment at 30.5°N, we tested the role of the biocontrol beetle Agasicles hygrophila in mediating warming effects on competition between the invasive plant Alternanthera philoxeroides and the native plant Alternanthera sessilis. In surveys, native populations were perennial below 25.8°N but only annual populations were found above 26.5°N where the invader dominated the community. Beetles were present throughout the gradient. Experimental warming (+xa01.8°C) increased native plant performance directly by shifting its lifecycle from annual to perennial, and indirectly by releasing the native from competition via disproportionate increases in herbivory on the invader. Consequently, warming shifted the plant community from invader-dominated to native-dominated but only in the presence of the beetle. Our results show that herbivores can play a critical role in determining warming effects on plant communities and species invasions. Understanding how biotic interactions shape responses of communities to climate change is crucial for predicting the risk of plant invasions.