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Multi-species suppression of herbivores through consumptive and non-consumptive effects.

ABSTRACT: 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.

SUBMITTER: Ingerslew KS

PROVIDER: S-EPMC5965886 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Publications

Multi-species suppression of herbivores through consumptive and non-consumptive effects.

Ingerslew Kathryn S KS Finke Deborah L DL

PloS one 20180523 5

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. W ...[more]

PMID: 29791456

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Project description: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.

Project description:Plants are often exposed to multiple herbivores and densities of these attackers (or corresponding damage intensities) often fluctuate greatly in the field. Plant-mediated interactions vary among herbivore species and with changing feeding intensity, but little is known about how herbivore identity and density interact to determine plant responses and herbivore fitness. Here, we investigated this question using Triadica sebifera (tallow) and two common and abundant specialist insect herbivores, Bikasha collaris (flea beetle) and Heterapoderopsis bicallosicollis (weevil). By manipulating densities of leaf-feeding adults of these two herbivore species, we tested how variations in the intensity of leaf damage caused by flea beetle or weevil adults affected the performance of root-feeding flea beetle larvae and evaluated the potential of induced tallow root traits to predict flea beetle larval performance. We found that weevil adults consistently decreased the survival of flea beetle larvae with increasing leaf damage intensities. In contrast, conspecific flea beetle adults increased their larval survival at low damage then decreased larval survival at high damage, resulting in a unimodal pattern. Chemical analyses showed that increasing leaf damage from weevil adults linearly decreased root carbohydrates and increased root tannin, whereas flea beetle adults had opposite effects as weevil adults at low damage and similar effects as them at high damage. Furthermore, across all feeding treatments, flea beetle larval survival correlated positively with concentrations of carbohydrates and negatively with concentration of tannin, suggesting that root primary and secondary metabolism might underlie the observed effects on flea beetle larvae. Our study demonstrates that herbivore identity and density interact to determine systemic plant responses and plant-mediated effects on herbivores. In particular, effects are species-specific at low densities, but converge at high densities. These findings emphasize the importance of considering herbivore identity and density simultaneously when investigating factors driving plant-mediated interactions between herbivores, which advances our understanding of the structure and composition of herbivore communities and terrestrial food webs.

Dataset Information

Multi-species suppression of herbivores through consumptive and non-consumptive effects.

Publications

Multi-species suppression of herbivores through consumptive and non-consumptive effects.

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