Tri-Trophic Effects of Seasonally Variable Induced Plant Defenses Vary across the Development of a Shelter Building Moth Larva and Its Parasitoid

Plant chemical defenses can negatively affect insect herbivore fitness, but they can also decrease herbivore palatability to predators or decrease parasitoid fitness, potentially changing selective pressures on both plant investment in production of chemical defenses and host feeding behavior. Larvae of the fern moth Herpetogramma theseusalis live in and feed upon leaf shelters of their own construction, and their most abundant parasitoid Alabagrus texanus oviposits in early instar larvae, where parasitoid larvae lay dormant for most of host development before rapidly developing and emerging just prior to host pupation. As such, both might be expected to live in a relatively constant chemical environment. Instead, we find that a correlated set of phenolic compounds shows strong seasonal variation both within shelters and in undamaged fern tissue, and the relative level of these compounds in these two different fern tissue types switches across the summer. Using experimental feeding treatments, in which we exposed fern moth larvae to different chemical trajectories across their development, we show that exposure to this set of phenolic compounds reduces the survival of larvae in early development. However, exposure to this set of compounds just before the beginning of explosive parasitoid growth increased parasitoid survival. Exposure during the period of rapid parasitoid growth and feeding decreased parasitoid survival. These results highlight the spatial and temporal complexity of leaf shelter chemistry, and demonstrate the developmental contingency of associated effects on both host and parasitoid, implying the existence of complex selective pressures on plant investment in chemical defenses, host feeding behavior, and parasitoid life history.

植物化学防御（plant chemical defenses）可对昆虫植食者的适合度产生负面影响，同时还会降低植食者被捕食者取食的适口性，或是降低拟寄生者（parasitoid）的适合度，从而可能改变作用于植物化学防御生产投入以及宿主取食行为的双重选择压力。蕨蛾（Herpetogramma theseusalis）的幼虫栖息并取食自身构筑的叶巢（leaf shelters），其最主要的拟寄生天敌Alabagrus texanus会在宿主早龄幼虫体内产卵；拟寄生幼虫会在宿主发育的大部分阶段处于休眠状态，直至宿主化蛹前才快速发育并钻出宿主。据此，二者本应处于相对稳定的化学环境中。但我们的研究发现，一组具有相关性的酚类化合物（phenolic compounds）在叶巢内以及未受损伤的蕨类组织中均呈现显著的季节动态，且这两类蕨类组织中该类化合物的相对含量在整个夏季发生了反转。通过实验性取食处理——我们让蕨蛾幼虫在整个发育过程中暴露于不同的化合物浓度动态中——我们发现，发育早期暴露于该组酚类化合物会降低幼虫的存活率。然而，在拟寄生者快速生长阶段开始前暴露于该类化合物，却能提升拟寄生者的存活率。而在拟寄生者快速生长与取食阶段暴露于该类化合物，则会降低拟寄生者的存活率。这些研究结果凸显了叶巢化学环境的时空复杂性，并证实了其对宿主与拟寄生者的影响存在发育偶然性，这意味着植物化学防御投入、宿主取食行为以及拟寄生者生活史（life history）均面临着复杂的选择压力。