- is the actual encounter and oviposition in
or upon a suitable host (e.g. Dicke and Vet,
1999). In other words, all the other responses
in the foraging repertoire are of value only to
the extent that they contribute to such
encounters and oviposition.
A parasitoid can better perceive and use
stimuli emanating directly from a host or a
direct by-product of the host at close range
than at longer range (Vinson, 1988). It stands
to reason that the direct cues are more reli-
able indicators of host presence than indirect
cues, such as the odour of a particular plant
or other habitat odour. Of particular signifi-
cance is the fact that these direct cues would
be linked more consistently with hosts and
ovipositional success over parasitoid genera-
tions, as would be required by natural selec-
tion for them to become genetically fixed
(‘hard-wired’) responses. It is also apparent
that at close range the parasitoids can afford
to confine their responses to a more limited
scope of stimuli and thus respond in a more
homogeneous manner than at longer range
in response to indirect cues.
Further, we have often observed that para-
sitoids encountering closer-range cues are less
disrupted by other stimuli, such as light and
movement (even touch by the observer),
which reduces further the variations in behav-
iour at close range. This more focused behav-
iour at close range is similar to the tendency
of other organisms to be less easily disturbed
as they reach the immediate proximity of
food, mates or other targets of a searching
sequence (e.g. Steidle and van Loon, 2002).
At long range, the parasitoid, because of
limitations in its ability to detect direct cues,
must depend on indirect indicators, such as
certain types, ages and parts of plants or
other habitat cues typically indicating the
potential presence of suitable hosts (Vet and
Dicke, 1992). These indirect indicators may
be cues generally associated with host pres-
ence, but the reliability of such associations
within and among parasitoid generations
would not be as great as that of direct cues.
Moreover, at long range the parasitoids can
less afford to confine their emphasis to a lim-
ited group of cues and are obliged to explore
and sort a greater array of stimuli.
Consequently, the overall variety of cues to
be evaluated and the factors affecting the
magnitude of parasitoid response are greater
at longer range. Thus, there is a greater need
for parasitoids to adapt their longer-range
responses through learning as they
encounter different situations among and
within generations. Although both genetic
and learned responses are probably present
on both ends of the foraging sequence of
parasitoids, we contend that the need for
learning is greater at longer range. It is
important, however, to note possible limits
to our argument of more learning in the case
of less reliable, longer-range cues. In discus-
sions for other organisms, authors have sug-
gested that, in situations of extreme
unpredictability, learning may be of reduced
value in tracking changes, in which case a
fixed, mediocre alternative may be as suit-
able (Papaj and Prokopy, 1989).
As stated above, the greater variability in
long-range foraging behaviour of parasitoids- and consequently the greater difficulty of
its study – has resulted in a very limited
knowledge of longer-range foraging behav-
iour, especially mechanisms governing the
responses. Variability in long-range foraging
behaviour may also seriously limit the use of
parasitoids as dependable pest-control
agents unless we can understand and man-
age this variability. In other words, perhaps
we have the least information where the
need is greatest (see preface of Drost et al.
(1986) for further discussion of need for
studies of foraging behaviour of parasitoids
in response to airborne odours (Steidle and
van Loon, 2002)).
Applied Considerations
A primary determinant of the effectiveness
of parasitoids as biological control agents is
the behaviour of the ovipositing females.
Therefore, we must be able to ensure two
features of their behaviour: (i) efficient loca-
tion and attack of their hosts; and (ii) reten-
tion of females in the target area. To meet
these requirements we must understand and
manage the factors that influence the forag-
ing behaviour of the parasitoids. Predictably
effective performance of the parasitoids is a50 W.J. Lewiset al.