Earwig × Fruit fly × Parasitoid: Interactions

The earwig Euborellia annulipes (Dermaptera: Anisolabididae) is a generalist predator. It was recently observed in fruits infested with fruit flies, whose juveniles are frequently attacked by parasitoid wasps. However, the predation of these fruit flies by E. annulipes has not yet been recorded nor has their intraguild interaction with parasitoid wasps. In this study, we explored earwig-fruit fly-parasitoid interactions using the E. annulipes earwig, the Mediterranean fly Ceratitis capitata (Diptera: Tephritidae), and the parasitoid wasp Diachasmimorpha longicaudata (Hymenoptera: Braconidae). We hypothesized that (1) earwig adults prey on fruit fly larvae and pupae, and this predation depends on the earwig sex and prey density and developmental stage; (2) earwigs are able to recognize and avoid parasitized prey; and (3) chemical markings on the host left by the parasitoid are recognized by the earwigs. In laboratory experiments, earwig females and males preyed on second and third-instar larvae and pupae of C. capitata, and females predated more than males regardless of the stage of development of the prey. Predation was higher in second-instar larvae, followed by third-instar larvae and, finally, fruit fly pupae. Females and males exhibited a type II functional response. Males killed but did not consume their prey more than females, effectively contributing to the elimination of prey even when they were not consumed. In no-choice tests, parasitized and nonparasitized fruit fly larvae were consumed by adult female earwigs in similar proportions. However, in choice tests, the female earwigs avoided feeding on parasitized larvae. Subsequent tests indicated that the parasitized larvae were recognized by semiochemicals released by the parasitoids during parasitism of the larvae. This result indicates that this earwig has the ability to identify parasitized prey and prefers to avoid intraguild predation. These findings are unprecedented and indicate that E. annulipes has the potential for biological control of C. capitata and that by avoiding intraguild predation, this earwig will have an additive effect on pest mortality.环纹肥蠼螋（Euborellia annulipes，革翅目Dermaptera：蠼螋科Anisolabididae）是一种多食性捕食者。近期研究人员在被实蝇侵染的果实中发现了该物种，而实蝇幼体常遭寄生蜂攻击。但目前尚无关于环纹肥蠼螋捕食此类实蝇的记录，也未见其与寄生蜂之间的集团内互作（intraguild interaction）相关报道。本研究以环纹肥蠼螋、地中海实蝇（Ceratitis capitata，双翅目Diptera：实蝇科Tephritidae）以及长距茧蜂（Diachasmimorpha longicaudata，膜翅目Hymenoptera：茧蜂科Braconidae）为实验材料，探究蠼螋-实蝇-寄生蜂三者间的互作关系。本研究提出三项假说：其一，蠼螋成虫会捕食实蝇幼虫与蛹，且该捕食行为受蠼螋性别、猎物密度及猎物发育阶段调控；其二，蠼螋能够识别并规避被寄生的猎物；其三，蠼螋可识别寄生蜂在寄主体内留下的化学标记物。室内试验结果显示，雌性与雄性蠼螋均会取食地中海实蝇的2龄、3龄幼虫及蛹，且无论猎物处于何种发育阶段，雌性蠼螋的捕食量均高于雄性。捕食率在2龄幼虫组中最高，其次为3龄幼虫组，实蝇蛹组的捕食率最低。雌雄蠼螋均表现出II型功能反应（functional response）。雄性个体杀死但未取食的猎物数量多于雌性，即便未发生取食，雄性也能有效减少猎物种群规模。在非选择性试验（no-choice tests）中，雌性蠼螋对被寄生与未被寄生的实蝇幼虫取食比例相近。但在选择性试验（choice tests）中，雌性蠼螋会主动避开取食被寄生的幼虫。后续试验表明，蠼螋是通过寄生蜂在幼虫寄生过程中释放的信息化合物（semiochemicals）识别被寄生的幼虫。该研究结果证实，此种蠼螋具备识别被寄生猎物的能力，并倾向于避免集团内捕食（intraguild predation）。本研究发现尚属首次报道，结果表明环纹肥蠼螋具备对地中海实蝇的生物防治潜力，且其规避集团内捕食的行为可对害虫死亡率产生累加效应。