Natural enemies need not consume herbivores to suppress herbivore populations. Behavioral interactions can adversely impact herbivore fitness from reduced time feeding, investment in defense, or injury from failed attacks. The importance of such "nonconsumptive effects" for herbivore suppression may vary across species based on the specificity and intensity of the herbivore defensive response. In a series of manipulative studies, we quantified the nature and consequences of nonconsumptive interactions between two parasitoid wasps, Aphidius ervi Haliday and Aphidius colemani Viereck, on two aphid species, pea aphids (Acyrthosiphon pisum (Harris)) and green peach aphids (Myzus persicae (Sulzer)). Both wasps successfully parasitize green peach aphids, but only A. ervi parasitizes pea aphids. We observed A. ervi antennating and stinging pea aphids and documented a decrease in pea aphid longevity in response to stinging even when the aphid survived the interaction and no mummy formed. The primary defensive tactic of pea aphids in response to either wasp species was dropping from the host plant. Both wasp species antennated and stung green peach aphids, but they elicited unique defensive behaviors. Green peach aphids kicked or emitted cornicle secretions in response to A. colemani but spent more time off the plant in the presence of A. ervi. Green peach aphid longevity and fecundity were not affected by wasp stings when the aphid survived and no mummy formed. Our study demonstrates the complexity of behavioral interactions between parasitoids and their potential hosts and contributes to a mechanistic understanding of variation in the nonconsumptive suppression of herbivore populations.

Most studies investigating the importance of non-consumptive interactions for herbivore suppression focus on pairwise interactions between one predator and one prey, ignoring any community context. Further, the potential for non-consumptive interactions to arise between herbivores and non-enemy organisms is commonly overlooked. We investigated the relative contributions of consumptive and non-consumptive effects to aphid suppression by a wasp assemblage containing both enemies and non-enemies. We examined the suppression of two aphid species with different defensive strategies, pea aphids (Acyrthosiphon pisum), which drop from their host plant to the ground, and green peach aphids (Myzus persicae), which remain on the plant and merely walk away. The expectation was that riskier defensive behaviors, like abandoning the plant, would result in larger non-consumptive effects. We found that the outcome of multi-species interactions differed depending on the mechanism of suppression, with interference among wasps in their consumptive effects and additivity in their non-consumptive effects. We also found that, despite differences in defensive strategies, the non-consumptive effects of wasps on aphid abundance were significant for both aphid species. Furthermore, when part of a multi-species assemblage, non-enemies enhanced aphid suppression via complementary non-consumptive effects with lethal enemies, but this increase in suppression was offset by disruption in the consumptive suppression of aphids by lethal enemies. We conclude that non-consumptive effects arise from interactions with both enemy and non-enemy species and that both can contribute to herbivore suppression when part of a broader community. We predict that encouraging the presence of non-enemy organisms may provide insurance against fluctuations in the size of consumptive enemy populations and buffer against herbivore outbreaks.

Although crop rotation has been used for centuries to enhance agricultural production, there are surprisingly little data justifying the use of one rotation over another. Growers typically avoid growing plants in succession that belong to the same genus or family, but it is not clear whether closely related crops are indeed poor rotation partners and whether evolutionary history, overall, predicts legacy effects in agricultural soils. Here, we use a plant–soil feedback framework to test the relationship between species relatedness and crop growth. Using tomato Solanum lycopersicum as our focal crop, we determined how 36 common crop and weed species that vary along a spectrum of phylogenetic relatedness influence tomato growth in subsequent plantings. We also tested whether soil conditioning affects the performance of an above‐ground insect herbivore, the tobacco hornworm Manduca sexta. Phylogenetic relatedness did not predict plant–soil feedback effects on tomato biomass or hornworm performance; rather, impacts of soil conditioning were highly species‐ or family‐specific. For example, tomatoes growing in soil previously containing plants in the Asteraceae family were notably resistant to caterpillar feeding. There was also a disconnect between which plant species caused negative feedbacks on tomatoes vs. hornworms (e.g. thistle Cirsium discolor soil had strong negative effects on herbivory but no impact on plant growth). Hence, negative feedbacks on hornworms are likely due to enhanced defence instead of simply reducing leaf availability. Synthesis and applications. These data demonstrate that, despite being widely recommended by agronomists in most cropping systems, phylogenetic relatedness is a poor predictor for the success of crop pairings in rotation, especially in tomato. Better understanding of species‐specific effects of soil conditioning will lend insight into how polycultures can be better designed to optimize crop growth while reducing susceptibility to insect pests, which is particularly useful on diversified farms that cultivate a variety of crop species.

Agriculture has long employed phylogenetic rules whereby farmers are encouraged to rotate taxonomically unrelated plants in shared soil. Although this forms a central tenet of sustainable agriculture, strangely, this on‐farm “rule of thumb” has never been rigorously tested in a scientific framework. To experimentally evaluate the relationship between phylogenetic distance and crop performance, we used a plant–soil feedback approach whereby 35 crops and weeds varying in their relatedness to tomato (Solanum lycopersicum) were tested in a two‐year field experiment. We used community profiling of the bacteria and fungi to determine the extent to which soil microbes contribute to phenotypic differences in crop growth. Overall, tomato yield was ca. 15% lower in soil previously cultivated with tomato; yet, past the species level there was no effect of phylogenetic distance on crop performance. Soil microbial communities, on the other hand, were compositionally more similar between close plant relatives. Random forest regression predicted log10 phylogenetic distance to tomato with moderate accuracy (R2 = .52), primarily driven by bacteria in the genus Sphingobium. These data indicate that, beyond avoiding conspecifics, evolutionary history contributes little to understanding plant–soil feedbacks in agricultural fields; however, microbial legacies can be predicted by species identity and relatedness.

Understanding the factors that influence predator-prey dynamics requires an investigation of oscillations in predator and prey population sizes over time. However, empirical studies are often performed over one or fewer predator generations. This is particularly true for studies addressing the non-consumptive effects of predators on prey. In a previous study that lasted less than one predator generation, we demonstrated that two species of parasitoid wasps additively suppressed aphid populations through a combination of consumptive and non-consumptive effects. However, the non-consumptive effects of one wasp reduced the reproductive success of the other, suggesting that a longer-term experiment may have revealed antagonism between the wasps. The goal of our current study is to evaluate multi-generation consumptive and non-consumptive interactions between pea aphids (Acyrthosiphon pisum) and the wasps Aphidius ervi and Aphidius colemani. Aphidius ervi is a common natural enemy of pea aphids. Aphidius colemani is a non-consumptive enemy that does not consume pea aphids, but negatively affects pea aphid performance through behavioral disturbance. Large field cages were installed to monitor aphid abundance in response to the presence and absence of both species of wasp over four weeks (two parasitoid generations). We found that the non-consumptive enemy A. colemani initially controlled the pea aphid population, but control in the absence of parasitism was not sustainable over the long term. Aphidius ervi suppressed pea aphids through a combination of consumptive and non-consumptive effects. This suppression was more effective than that of A. colemani, but aphid abundance fluctuated over time. Suppression by A. ervi and A. colemani together was complementary, leading to the most effective and stable control of pea aphids. Therefore, promoting a diverse natural enemy community that contributes to pest control through consumptive and non-consumptive interactions may enhance the stability of herbivore population suppression over time.