Institut de Recherche sur la Biologie de l'Insecte, UMR 7261, CNRS/Université de Tours, UFR Sciences et Techniques, Tours, France.
Department of Life and Environmental Sciences, Kyoto Prefectural University, Kyoto, Japan.
PLoS One. 2018 Dec 21;13(12):e0209485. doi: 10.1371/journal.pone.0209485. eCollection 2018.
Leaves represent the main resource for herbivorous insects and their performances are mainly a function of leaf nutritional quality. Two feeding strategies are known to optimize the exploitation of leaf resources: leaf-miners that selectively feed on tissues of high nutritional quality and gall-inducers that induce the development of a new tissue showing an enhanced nutritional value. Some leaf-miners are known to also manipulate their nutritional environment, but do not affect plant development. Cases of callus proliferation in leaf-mines have been reported, however, the direct role of the insect in the formation of additional plant cells and the nutritional function of this tissue have never been established. Using an experimental approach, we show that leaf-mining larvae of micromoth, Borboryctis euryae (Lepidoptera: Gracillariidae), that grow on Eurya japonica (Pentaphylacaceae), actively induce callus proliferation within their leaf-mine at the fourth instar. We experimentally demonstrated that, at this developmental stage, the larva feeds exclusively on this newly formed tissue and feeding of the tissue is essential for completing larval stage. Phenological census revealed considerable expansion and variation of fourth instar duration caused by the continuous production of callus. We propose here the "cornucopia" hypothesis which states that the newly produced callus induced by the leaf-mining larvae provides virtually unending nourishment, which in turn allows flexible larval development time. This represents the first example of a leaf-miner manipulating plant development to its benefit, like a gall-inducer. We propose to name this life style "mine-galler".
叶片是植食性昆虫的主要食物来源，其取食行为主要取决于叶片的营养品质。昆虫有两种取食策略可以最大限度地利用叶片资源：取食高营养组织的选择性叶食者，以及诱导形成具有更高营养价值新组织的虫瘿诱导者。已知有些叶食者会主动改变其营养环境，但不会影响植物的发育。然而，在叶片取食者中也有报道称会出现愈伤组织增生的情况，但昆虫在额外植物细胞形成中的直接作用及其营养功能从未得到证实。本研究采用实验方法，证明了在第四龄幼虫期，取食杨桐（Pentaphylacaceae）的 micromoth 潜叶蛾（Borboryctis euryae）（鳞翅目：潜叶蛾科）会主动诱导叶片潜道内的愈伤组织增生。实验表明，在这一发育阶段，幼虫仅取食新形成的组织，而这种组织的取食对于完成幼虫发育是必不可少的。物候学普查显示，由于不断产生愈伤组织，第四龄幼虫期的持续时间显著延长且变化较大。我们提出了“聚宝盆”假说，即由潜叶幼虫诱导产生的新愈伤组织提供了几乎源源不断的养分，从而使幼虫的发育时间具有灵活性。这是首例叶片取食者为自身利益而操纵植物发育的例子，类似于虫瘿诱导者。我们建议将这种生活方式命名为“潜叶瘿食”。
