Department of Plant and Environmental Sciences, Clemson University, Clemson, South Carolina, 29678, USA.
Department of Entomology, Washington State University, Pullman, Washington, 99164, USA.
Ecology. 2018 May;99(5):1089-1098. doi: 10.1002/ecy.2192.
Plant defenses often mediate whether competing chewing and sucking herbivores indirectly benefit or harm one another. Dual-guild herbivory also can muddle plant signals used by specialist natural enemies to locate prey, further complicating the net impact of herbivore-herbivore interactions in naturally diverse settings. While dual-guild herbivore communities are common in nature, consequences for top-down processes are unclear, as chemically mediated tri-trophic interactions are rarely evaluated in field environments. Combining observational and experimental approaches in the open field, we test a prediction that chewing herbivores interfere with top-down suppression of phloem feeders on Brassica oleracea across broad landscapes. In a two-year survey of 52 working farm sites, we found that parasitoid and aphid densities on broccoli plants positively correlated at farms where aphids and caterpillars rarely co-occurred, but this relationship disappeared at farms where caterpillars commonly co-occurred. In a follow-up experiment, we compared single and dual-guild herbivore communities at four local farm sites and found that caterpillars (P. rapae) caused a 30% reduction in aphid parasitism (primarily by Diaeretiella rapae), and increased aphid colony (Brevicoryne brassicae) growth at some sites. Notably, in the absence of predators, caterpillars indirectly suppressed, rather than enhanced, aphid growth. Amid considerable ecological noise, our study reveals a pattern of apparent commensalism: herbivore-herbivore facilitation via relaxed top-down suppression. This work suggests that enemy-mediated apparent commensalism may override constraints to growth induced by competing herbivores in field environments, and emphasizes the value of placing chemically mediated interactions within their broader environmental and community contexts.
植物防御通常会影响相互竞争的咀嚼式和吮吸式食草动物是否会间接互惠或互害。双食性食草动物还会混淆植物信号，这些信号被专门的天敌用来定位猎物，从而进一步使食草动物-食草动物相互作用在自然多样化的环境中的净影响复杂化。虽然双食性食草动物群落在自然界中很常见，但对于自上而下的过程的后果尚不清楚，因为很少在野外环境中评估化学介导的三营养级相互作用。在开阔地中结合观察和实验方法，我们测试了一个预测，即咀嚼食草动物会干扰对甘蓝上韧皮部取食者的自上而下的抑制，这在广泛的景观中都适用。在对 52 个工作农场的为期两年的调查中，我们发现，在蚜虫和毛毛虫很少共同出现的农场中，小菜蛾上的寄生蜂和蚜虫密度呈正相关，但在毛毛虫常见共同出现的农场中，这种关系消失了。在随后的实验中，我们比较了四个当地农场的单食性和双食性食草动物群落，发现毛毛虫（小菜蛾）导致蚜虫寄生率降低 30%（主要是由小菜蛾蚜小蜂引起），并在一些地点增加了蚜虫群体（小菜蛾蚜）的生长。值得注意的是，在没有捕食者的情况下，毛毛虫间接抑制了蚜虫的生长，而不是促进了蚜虫的生长。在相当大的生态噪声中，我们的研究揭示了一种共生的模式：通过放松自上而下的抑制来促进食草动物-食草动物的相互作用。这项工作表明，在野外环境中，由天敌介导的看似共生关系可能会超过竞争食草动物对生长的限制，并强调了在更广泛的环境和群落背景下，将化学介导的相互作用纳入其中的价值。
