Abstract
Parasitic wasps are known to improve their foraging efficiency after learning of herbivore-induced plant volatiles (HIPVs) upon encountering their hosts on these plants. However, due to spatial and temporal variation of herbivore communities, learned HIPV cues can become unreliable, no longer correctly predicting host presence. Little is known about the potential fitness costs when memories holding such unreliable information persist. Here we studied how persistent memory, containing unreliable information, affects the foraging efficiency for hosts in Cotesia glomerata. Wasps were conditioned to associate one of two types of HIPVs with either P. brassicae frass, 1 single oviposition in P. brassicae, 3 ovipositions in P. brassicae spaced in time or they were kept unconditioned. The following day, wasps were allowed to forage in a wind tunnel, in an environment that either conflicted or was congruent with their learned plant experience. The foraging environment consisted of host (P. brassicae) and non-host (Mamestra brassicae) infested plants. The conflicting environment had non-hosts on the conditioned plant species and hosts on the non-conditioned plant species, whereas the congruent environment had hosts on the conditioned plant species and non-hosts on the unconditioned plant species. Wasps had to navigate through five non-host infested plants to reach the host-infested plant. Since C. glomerata wasps do not distinguish between HIPVs induced by host and non-host caterpillars, the conflicting foraging situation caused a prediction error, by guiding wasps to non-host infested plants. Especially wasps given 3 spaced oviposition experiences, tested in a conflicting situation, spent significantly more time on non-host infested plants and showed a high tendency to oviposit in the non-hosts. As a result, they took significantly more time to find their hosts. Conditioned wasps, which were tested in a congruent situation, were more responsive than unconditioned wasps, but there was no difference in foraging efficiency between these two groups in the wasps that showed a response. We conclude that persistent memories, such as formed after 3 experiences spaced in time, can lead to maladaptive foraging behavior if the contained information becomes unreliable.
Highlights
A high degree of spatial and temporal variation exists in herbivore communities, which makes it challenging for predators to find suitable prey
Since the congruent and conflicting survival curves of frass and a single oviposition show a high degree of overlap, the overall difference between congruent and conflicting foraging situations is mainly explained by the effect of spaced conditioning with 3 ovipositions (Figure 3)
The same pattern was observed for non-host oviposition, where wasps given spaced conditioning with conflicting information oviposited 3 times as often in non-hosts, but here the difference between the two spaced conditioning groups had a p-value of 0.063 (Figure 5)
Summary
A high degree of spatial and temporal variation exists in herbivore communities, which makes it challenging for predators to find suitable prey. Parasitoids are known to use a wide variety of olfactory, visual, auditory and tactile cues to obtain and store information on local host presence, distribution and abundance (Vet and Dicke, 1992; Turlings et al, 1993; Van Alphen and Bernstein, 2008; Ishii and Shimada, 2009) Acquisition of this information can be achieved through learning, in particular through associative ovipositional learning, where an oviposition in a host becomes associated with various environmental cues, such as herbivore-induced plant volatiles (HIPVs), resulting in associative memory (Bleeker et al, 2006). Parasitic wasps can temporarily adapt their foraging strategy to current local host and host-plant availability
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