also learn to prefer the odour of another substrate, but, unlike with
the generalistL. heterotoma, visits to these substrates always remained
shorter than visits to the natural substrates. Similar learning abilities may
be used for different purposes and therefore the effect of learning may
differ. The generalist L. heterotoma can achieve a great flexibility
in substrate selection, while the specialists may employ learning to
temporarily divert to less preferred substrates.
A high degree of flexibility through learning thus provides parasitoids
with an adaptive mechanism, and this mechanism expands beyond patch
finding. Both positive and negative reinforcement during foraging shapes
the subsequent decisions of the parasitoids on where to go and how long
to stay there. It helps parasitoids to assess spatial and temporal variation
in patch profitability, i.e. to estimate host quantity, quality and distrib-
ution and to track changes in these important parameters. In this phase of
searching, learning is essential for optimizing foraging decisions.A multitrophic approach to parasitoid behaviour
Parasitoids of plant-feeding insects function in a multitrophic world in
which plants play a central role in determining parasitoid development
and foraging behaviour (Vet and Dicke, 1992). Parasitoids of herbivores
are attracted to potential food plants of their hosts and, since the early
1990s, it has become clear that plants can play an active role in guiding
parasitoids to their potential victims (Turlingset al., 1990). Although an
uninfested plant may already be attractive to parasitoids, this attraction
is a magnitude larger when the plant is being attacked by herbivores,
suggesting evolutionary mutualism between desperately defending plants
and eagerly searching parasitoids. Vet (1999) discusses this important role
of the plant for the searching parasitoid, stating that it has important
evolutionary and ecological consequences for all trophic levels. For
the plant, selection for good signalling ability can potentially affect all
components of a plant’s defence strategy: the composition of the odour
blend, signal transduction and biosynthetic pathways, systemic responses
to herbivore damage or the relative investments in direct and indirect
defence. For the herbivore, the conspiracy between plant and parasitoid
is based on the feeding activity of the herbivore itself and selection
will act on the herbivore’s diet choice and feeding behaviour to reduce
the conveyance of information that reveals its presence. In addition,
herbivores can influence their chance of being parasitized through selec-
tion of feeding sites, when plant species, cultivars, genotypes or even
plant parts vary in their attractiveness to parasitoids. A less attractive
plant is searched less, which creates a partial refuge for the host, affecting
the spatial pattern of parasitism and thus the dynamics of the herbivore
and parasitoid populations. For the parasitoid, in the evolutionary setting
of real plant–parasitoid mutualism, parasitoids are selected to optimize
their response to those plant signals that indicate the presence of suitable44 L.E.M. Vetet al.