Dual‐guild herbivory disrupts predator‐prey interactions in the field

Abstract

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.

Caterpillar-induced rice volatiles provide enemy-free space for the offspring of the brown planthopper

“…HIPVs can also be detected by neighboring plants and help them to anticipate an incoming attack ( Arimura et al, 2000 ; Heil and Ton, 2008 ; Engelberth et al, 2004 ; Karban et al, 2014 ; Sugimoto et al, 2014 ; Nagashima et al, 2018 ). Hence, HIPVs provide information to all players in a plant’s ecological network and through these various effects, HIPVs play a major role in determining the composition of insect communities in the field ( Xiao et al, 2012 ; Zhu et al, 2015 ; Poelman and Dicke, 2014 ; Blubaugh et al, 2018 ; Schuman and Baldwin, 2018 ).…”

Bacteria and Competing Herbivores Weaken Top–Down and Bottom–Up Aphid Suppression

“…A competing chewing herbivore might dilute or constrain volatile signals exploited by aphid parasitoids to find their prey ( Vos et al, 2001 ), reducing top–down suppression. Indeed, our recent fieldwork in this system showed that co-herbivory by chewing herbivores reduced aphid parasitism as well as concentrations of secondary metabolites important in aphid-specific volatile signaling ( Blubaugh et al, 2018 ). This consistent pattern detected across a gradient of microbial diversity further emphasizes the importance of herbivore community structure in determining the outcome of tritrophic interactions.…”

“…capitata, cvs. Arcadia) are attacked by herbivorous aphids and caterpillars, while the aphids (but generally not the caterpillars) are in turn attacked by parasitoid wasps ( Snyder et al, 2006 ; Blubaugh et al, 2018 ). The cabbage aphid ( Brevicoryne brassicae ) is the dominant aphid on these plants, while Pieris rapae is the most common caterpillar species.…”

“…The cabbage aphid ( Brevicoryne brassicae ) is the dominant aphid on these plants, while Pieris rapae is the most common caterpillar species. The most abundant aphid parasitoid in the system is Diaeretiella rapae , which limits cabbage aphid population growth in the U.S. Pacific Northwest ( Blubaugh et al, 2018 ); however, parasitism of P. rapae is rare in the region ( Blubaugh et al, 2018 ). Caterpillars ( P. rapae ) used in our experiments came from a lab colony, and aphids ( B. brassicae ) came from a wild colony collected from a single kale plant ( Brassica oleracea var.…”

Tri‐trophic interactions: bridging species, communities and ecosystems

“…Open questions include whether natural enemies affect the strength or outcome of plant‐mediated herbivore interactions (e.g. De Rijk et al ; Blubaugh et al ), and whether plant indirect defence traits affect apparent competition among herbivores when the latter share enemies.…”