Indirect Interactions in Biological Control of Insects: Pests and Natural Enemies in Alfalfa

Abstract

The population dynamics of insect pests in agroecosystems may often be linked to those of other phytophagous species through the foraging activities of natural enemies; these indirect interactions provide both opportunities and challenges for biological control. We conducted field experiments to explore indirect interactions in the biological control of the alfalfa weevil (Hypera postica) in northern Utah. Honeydew produced by pea aphids (Acyrthosiphon pisum) in alfalfa fields may be important as a source of nutrition for adults of the wasp Bathyplectes curculionis and may thereby enhance parasitism of the wasp's host, the alfalfa weevil. The presence of aphids may also promote aggregation of lady beetles, which consume weevil larvae in alfalfa. But by feeding heavily on pea aphids as well, these predators could indirectly enhance weevil survivorship by undercutting the wasp's capacity to parasitize its host. In one field experiment, we added pea aphids and/or adults of the lady beetle Coccinella septempunctata to caged field plots of alfalfa during the first (spring) hay crop. Adding aphids increased levels of parasitism among late‐maturing alfalfa weevil larvae. Adding lady beetles decreased numbers of late‐maturing weevil larvae, but also decreased levels of parasitism among these larvae. In another experiment, repeated application of artificial honeydew to caged alfalfa plots during the first crop increased levels of parasitism among weevil larvae. In a third experiment, a single application of artificial honeydew to open (uncaged) alfalfa plots in mid‐May also had a direct positive effect on rates of parasitism among larvae. However, this application had an indirect negative effect on parasitism as well: the presence of artificial honeydew caused aggregation of lady beetles and thus led to decreased aphid abundance. Consequently, provision of artificial honeydew as a food source for parasitoid adults was neutralized by a subsequent reduction in naturally occurring honeydew. These field experiments illustrate the complexity with which indirect interactions can affect exploiter‐victim relationships in biological control. They also raise questions concerning the long‐term consequences that may result from the purposeful introduction of the Old World lady beetle C. septempunctata to alfalfa and other crops in North America. Artificial honeydew may prove useful in enhancing parasitism of the alfalfa weevil, but frequent applications may be required to compensate for associated reductions in availability of naturally occurring aphid honeydew. The effects of honeydew producers on other herbivores through natural enemies fall under the general concepts of short‐term apparent competition and related ecological relationships among species, and highlight the importance of temporal and spatial factors in indirect interactions.