Herbivory of a biocontrol agent on a native plant causes an indirect trait‐mediated non‐target effect on a native insect. (15th May 2021)

• Record Type: Journal Article
• Authors: He, Minyan; Zhang, Jialiang; Siemann, Evan; Yi, Jiahui; Qin, Wenchao; Sun, Xiao; Ding, Jianqing; Huang, Wei
• Is Part Of: Journal of ecology. Volume 109:Number 7(2021)
• Page Start: 2692
• Page End: 2704
• Publication Date: 2021-05-15
• Subjects: biological control -- density‐mediated effect -- exploitation competition -- food web linkage -- invasive plant -- native insect -- plant–herbivore interactions -- trait‐mediated effect; Plant ecology -- Periodicals; 577.05
• DOI: 10.1111/1365-2745.13676
• Languages: English
• ISSNs: 0022-0477

Abstract

Abstract: Identifying food web linkages between biocontrol agents of invasive plants and native species is crucial for predicting indirect non‐target effects. Biocontrol insects can integrate into food webs within recipient habitats and influence native insects through apparent competition (altering shared natural enemies) or density‐mediated exploitation competition (changing density of native plants). However, whether and how trait‐mediated exploitation competition (modifying native plant chemicals and volatiles profiles) can produce indirect non‐target effects remains largely overlooked, despite plant phenotypic responses to insect herbivory being common and widely documented. The flea beetle Agasicles hygrophila was introduced into China for management of alligator weed Alternanthera philoxeroides, but it also attacks the native congener sessile joyweed Alternanthera sessilis, which may cause indirect non‐target effects on the native tortoise beetle Cassida piperata that also feeds on sessile joyweed. Here, we examined the relationships among abundances of the flea beetle and tortoise beetle, and coverage of sessile joyweed in the field. Then, we investigated the impact of flea beetle herbivory on tortoise beetle development and oviposition, as well as on sessile joyweed primary metabolites and leaf volatiles. Tortoise beetle abundance was not related to sessile joyweed coverage, but they were less abundant on plants with more flea beetles in the field survey, and produced fewer offspring on plants with more prior flea beetle damage in the field cage experiment. Tortoise beetle development was inhibited by prior flea beetle herbivory in bioassays in enemy‐free conditions and they preferred to oviposit on sessile joyweed that had experienced little or no flea beetle damage. Flea beetle herbivory decreased sessile joyweed foliar glucose and protein, and substantially changed its leaf volatile blend. Synthesis . Our results show that the flea beetle has major indirect non‐target effects on the tortoise beetle through trait‐mediated exploitation competition, rather than apparent competition or density‐mediated exploitation competition. Our results demonstrate a new example for indirect non‐target effects of biocontrol agents. Furthermore, our results indicate that minor brief negative impacts of biocontrol agents on non‐target plants might propagate to higher trophic levels and such negative impacts can strengthen with increasing intensity of the direct non‐target effect. Abstract : Our study reveals that the biocontrol agent of invasive plant has the potential to influence the native insect through exploitation competition on the shared native plant. Perhaps more importantly, such exploitation competition is likely due to trait‐mediated effects by reducing native plant nutritional value and inducing repellent volatile production, rather than density‐mediated effect via changing native plant density. Our results, therefore, demonstrate a new example that is responsible for indirect non‐target effect of biocontrol agent. 摘要: 识别和鉴定入侵植物生防昆虫与本地生物存在的可能联系对预测生防昆虫所产生的间接非靶标效应至关重要。生防昆虫可以通过表观竞争 (调节共有天敌) 或者密度介导的利用性竞争 (改变本地植物密度) 来影响本地昆虫。尽管植物在被昆虫取食后会产生大量的诱导反应, 但是性状介导的利用性竞争 (诱导本地植物的化学反应) 是否会影响本地昆虫, 进而产生间接的非靶标效应往往被忽视。 莲草直胸跳甲 ( Agasicles hygrophila ) 作为生防昆虫被引入中国对入侵植物空心莲子草 ( Alternanthera philoxeroides ) 进行生物防治, 但其也取食本地植物莲子草 ( Alternanthera sessilis ), 进而可能影响莲子草上的本地昆虫虾钳菜披龟甲 ( Cassida piperata ) 。本研究通过野外调查和同质园控制实验研究了莲草直胸跳甲、虾钳菜披龟甲和莲子草的互作关系, 通过生物测定研究莲草直胸跳甲对虾钳菜披龟甲个体发育和产卵选择的影响, 通过初生代谢产物和植物挥发物测定研究其内在化学调控机制。 野外调查和同质园控制实验发现虾钳菜披龟甲的多度与莲子草的盖度无显著相关性, 但与莲草直胸跳甲的多度呈显著的负相关。生物测定发现莲草直胸跳甲在莲子草上的取食危害显著降低虾钳菜披龟甲的发育, 并对虾钳菜披龟甲的产卵具有趋避作用。化学分析表明莲草直胸跳甲的取食危害显著降低莲子草营养物质的含量, 提高了排斥性叶片挥发物的释放。 本研究展示了一个全新的生防昆虫和本地昆虫互作通路: 生防昆虫可以通过性状介导的利用性竞争对本地昆虫产生间接的非靶标效应。研究结果表明生防昆虫对非靶标植物微小和暂时的负面影响可能会扩展至较高的营养水平, 从而产生间接的非靶标效应。此外, 这种间接的非靶标效应会随着直接非靶标效应的增强而增强。