Mechanisms of non-consumptive effects of parasitoid wasps on aphid populations : enhancing aphid suppression by increasing natural enemy and plant diversity
Authors:   , Ingerslew Kathryn Suzanne 
Published: April 2021

Predators are typically evaluated for their potential effectiveness as natural biological control agents by examining traits related to their consumptive relationship with an herbivore. For example, voracious predators with a high prey attack rate or predators that specialize in consuming a particular pest species are considered ideal for biological control. However, there is a growing body of research demonstrating that predators also influence herbivore population size through non-consumptive interactions. Non-consumptive interactions include changes in prey behavior, morphology, or life-history traits in response to the presence of a predator that allow prey to survive a predator encounter but result in declines in prey fitness due to reduced availability of resources or expending energy that would have been otherwise used for growth or reproduction. The existence of non-consumptive effects is significant because it raises the possibility that a non-lethal organism (i.e. non-enemy) in the environment can also contribute to herbivore suppression if an herbivore inaccurately perceives an organism as a threat and engages in a defensive response. The goal of my dissertation research was to determine whether non-enemies contribute to natural biological control and enhance herbivore suppression beyond levels accomplished by consumptive natural enemies alone. Previous work in our lab demonstrated that pea aphids Acyrthosiphon pisum (Harris) respond to the non-enemy wasp Aphidius colemani Viereck by stopping feeding and dropping off of their host plant, resulting in a decline in pea aphid abundance even though pea aphids are not a host for A. colemani. My work evaluated whether this behavioral suppression of pea aphid populations by the non-enemy wasp is complementary with pea aphid suppression by the consumptive enemy Aphidius ervi Haliday. I investigated 1) the mechanisms responsible for and the magnitude of the non-consumptive effects of A. colemani and A. ervi on pea aphid populations, 2) the contributions of non-consumptive interactions to short-term and long-term suppression of aphid populations in the presence of consumptive natural enemies, and 3) the feasibility of increasing plant diversity in the field to enhance pea aphid suppression by facilitating behavioral non-consumptive interactions. I found that pea aphids respond to interactions with both wasp species, but they more frequently engaged in defensive behaviors such as dropping in the presence of the enemy A. ervi than the non-enemy A. colemani. The behavioral response of the pea aphid to the presence of the non-enemy was strong enough for A. colemani to suppress pea aphid populations in the short term, but this suppression was not maintained over the long term. When the non-enemy A. colemani was combined with the consumptive enemy A. ervi, there was some evidence for antagonism between the wasps over the short term. However, the non-enemy and enemy were complementary in their suppression of pea aphid populations over the long term, with more consistent and stable suppression when both wasps were present. I also demonstrated that increasing plant diversity in a field setting enhances suppression of pea aphid populations by promoting interactions between pea aphids and non-enemies. My work demonstrates that non-lethal organisms, or non-enemies, in the environment have an important role to play in influencing herbivore abundance, and that the addition of non-enemies to a community of lethal predators and parasitoids can lead to greater and more consistent suppression of herbivores in the long term.