Herbivory of a biocontrol agent on a native plant causes an indirect trait-mediated non-target effect on a native insect

Herbivory of a biocontrol agent on a native plant causes an indirect trait-mediated non-target effect on a native insect
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生物防治剂对本地植物的食草会对本地昆虫产生间接性状介导的非目标效应

DOI:
10.1111/1365-2745.13676
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发表时间:
2021-05-15
期刊:
影响因子:
5.5
通讯作者:
Huang, Wei
Huang, Wei
中科院分区:
环境科学与生态学1区
文献类型:
--
作者:
He, Minyan;Zhang, Jialiang;Huang, Wei

文献摘要

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确定入侵植物和本地物种的生物防治剂之间的食物网联系对于预测间接非目标效应至关重要。生物防治昆虫可以融入受体栖息地内的食物网,并通过明显的竞争(改变共同的天敌)或密度介导的开发竞争(改变本地植物的密度)影响本地昆虫。然而,性状介导的利用竞争(改变本地植物化学物质和挥发物特征)是否以及如何产生间接非目标效应仍然在很大程度上被忽视,尽管植物对食草昆虫的表型反应很常见并且被广泛记录。跳甲虫Agasicles hygrophila被引入中国用于管理鳄鱼杂草空心莲子草,但它也会攻击本地同源无柄快乐草空心莲子草sessilis,这可能会对也以无柄快乐草为食的本地龟甲虫 Cassida Piperata 造成间接非目标影响。在这里,我们研究了跳甲虫和龟甲虫的丰度与田间无柄快乐草的覆盖度之间的关系。然后,我们研究了跳甲食草性对龟甲发育和产卵,以及对无柄快乐草初级代谢物和叶片挥发物的影响。龟甲丰度与无柄快乐草覆盖度无关,但在田间调查中跳甲虫较多的植物上龟甲虫丰度较低,而在田间网箱实验中,在跳甲虫伤害较多的植物上龟甲虫产生的后代较少。在无敌条件下的生物测定中,龟甲虫的发育受到先前跳蚤甲虫食草性的抑制,并且它们更喜欢在几乎没有或没有受到跳蚤甲虫损害的无柄快乐草上产卵。跳甲虫食草性降低了无柄快乐草叶片的葡萄糖和蛋白质,并大幅改变了其叶片挥发性混合物的合成。我们的结果表明,跳甲通过性状介导的利用竞争,而不是表观竞争或密度介导的利用竞争,对龟甲虫产生主要的间接非目标效应。我们的结果证明了生物防治剂的间接非目标效应的新例子。此外,我们的结果表明,生物防治剂对非目标植物的轻微短暂负面影响可能会传播到更高的营养水平,并且这种负面影响会随着直接非目标效应强度的增加而加强。
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.