Chemically mediated tritrophic interactions: opposing effects of glucosinolates on a specialist herbivore and its predators

1. The occurrence of enemy-free space presents a challenge to the top-down control of agricultural pests by natural enemies, making bottom-up factors such as phytochemistry and plant distributions important considerations for successful pest management. Specialist herbivores like the cabbage aphid Brevicoryne brassicae co-opt the defence system of plants in the family Brassicaceae by sequestering glucosinolates to utilize in their own defence. The wild mustard Brassica nigra, analternate host for cabbage aphids, contains more glucosinolates than cultivated Brassica oleracea, and these co-occur in agricultural landscapes. We examined trade-offs between aphid performance and predator impact on these two host plants to test for chemically mediated enemy-free space. 2. Glucosinolate content of broccoli B. oleracea and mustard B. nigra was measured in plant matter and in cabbage aphids feeding on each food source. Aphid development, aphid fecundity, predation and predator mortality, and field densities of aphids and their natural enemies were also tested for each food source. 3. Cabbage aphids growing on high glucosinolate plants like B. nigra contained more glucosinolates than aphids on lower glucosinolate B. oleracea. Aphids on B. nigra had shorter generation times and greater daily fecundity, while their predators (Diptera: Syrphidae) had lower feeding and higher mortality rates. Lower syrphid densities were found on B. nigra than on B. oleracea in the field. 4. Synthesis and applications. This study presents physiological and field evidence to suggest that weedy B. nigra may provide enemy-free space from an important predator. Habitat near crops should be examined for its potential to provide enemy-free space and compromise otherwise effective biological control. The issue of pest control must be considered from the bottom up as well as the top down.