Ew. Evans et S. England, INDIRECT INTERACTIONS IN BIOLOGICAL-CONTROL OF INSECTS - PESTS AND NATURAL ENEMIES IN ALFALFA, Ecological applications, 6(3), 1996, pp. 920-930
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
.