INDIRECT INTERACTIONS IN BIOLOGICAL-CONTROL OF INSECTS - PESTS AND NATURAL ENEMIES IN ALFALFA

The population dynamics of insect pests in agroecosystems may often be linked to those of other phytophagous species through the foraging ac tivities of natural enemies; these indirect interactions provide both opportunities and challenges for biological control. We conducted fiel d experiments to explore indirect interactions in the biological contr ol of the alfalfa weevil (Hypera postica) in northern Utah. Honeydew p roduced by pea aphids (Acyrthosiphon pisum) in alfalfa fields may be i mportant 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 o f lady beetles, which consume weevil larvae in alfalfa. But by feeding heavily on pea aphids as well, these predators could indirectly enhan ce weevil survivorship by undercutting the wasp's capacity to parasiti ze its host. In one field experiment, we added pea aphids and/or adult s of the lady beetle Coccinella septempunctata to caged field plots of alfalfa during the first (spring) hay crop. Adding aphids increased l evels of parasitism among late-maturing alfalfa weevil larvae. Adding lady beetles decreased numbers of late-maturing weevil larvae, but als o decreased levels of parasitism among these larvae. In another experi ment, repeated application of artificial honeydew to caged alfalfa plo ts during the first crop increased levels of parasitism among weevil l arvae. In a third experiment, a single application of artificial honey dew to open (uncaged) alfalfa plots in mid-May also had a direct posit ive effect on rates of parasitism among larvae. However, this applicat ion had an indirect negative effect on parasitism as well: the presenc e of artificial honeydew caused aggregation of lady beetles and thus l ed 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 expe riments illustrate the complexity with which indirect interactions can affect exploiter-victim relationships in biological control. They als o raise questions concerning the long-term consequences that may resul t from the purposeful introduction of the Old World lady beetle C. sep tempunctata to alfalfa and other crops in North America. Artificial ho neydew may prove useful in enhancing parasitism of the alfalfa weevil, but frequent applications may be required to compensate for associate d reductions in availability of naturally occurring aphid honeydew. Th e effects of honeydew producers on other herbivores through natural en emies fall under the general concepts of short-term apparent competiti on and related ecological relationships among species, and highlight t he importance of temporal and spatial factors in indirect interactions .