Neighbouring resources have been found to either decrease or increase the likelihood that a consumer organism attacks a focal resource. These phenomena are referred to as associational resistance (AR) and associational susceptibility (AS), respectively. While associational effects have been observed in various field studies, little is known on how resource heterogeneity can cause associational effects. We used a laboratory approach in which we studied the effects of resource density and frequency in the search behaviour of Drosophila melanogaster as a model organism for olfactory-guided behaviour in insects. We first determined whether D.melanogaster could discriminate between odour sources that differ quantitatively. Secondly, we determined what the effect of resource density and frequency was on the search behaviour of D.melanogaster by combining these resources into various patch arrangements. Finally, we used the outcome of our experiments to disentangle the role of resource density and frequency in associational effects. We found that D.melanogaster has the ability to discriminate between quantitatively different resources, but that the attraction to resource density is constrained by an optimum after which attraction decreases. Furthermore, in heterogeneous environments, flies showed a strong preference towards the more apparent resource, leading to AS for the more apparent resources and AR for the less apparent resource. The strength of this interaction increased with a decreasing frequency of the more apparent resource. These results imply that D.melanogaster mainly selects patches at the level of individual resources. Consequently, when a patch contains qualitatively different resources, the more apparent resource will attract a higher number of flies than the less apparent resource irrespective of the frequency of the apparent resource within the patch. Our study shows that associational effects can be explained by determining the hierarchical level at which a consumer selects its resources. When a consumer selects resources at the individual level rather than at the patch level, our results can be used to explain the population dynamics of host plants and their associated consumers under field conditions.

Neighboring resources can affect insect oviposition behavior when the complexity of sensory information obscures information about host resource availability in heterogeneous resource patches. These effects are referred to as associational effects and are hypothesized to occur through constraints in the sensory processing of the insect during host search, resulting into suboptimal resource use. Because the possibilities to study these constraints on naturally occurring animals are limited, we instead used sensory mutants of Drosophila melanogaster to determine the importance of sensory information in the occurrence of associational effects. We found that oviposition was mainly governed by non-volatile chemical cues and less by volatile cues. Moreover, the loss of gustatory sensilla resulted in random resource selection and eliminated associational effects. In conclusion, our study shows that associational effects do not necessarily depend on constraints in the sensory evaluation of resource quality, but may instead be a direct consequence of distinctive selection behavior between different resources at small scales.

Many insects face the challenge to select oviposition sites in heterogeneous environments where biotic and abiotic factors can change over time. One way to deal with this complexity is to use sensory experiences made during developmental stages to locate similar habitats or hosts in which larval development can be maximized. While various studies have investigated oviposition preference and larval performance relationships in insects, they have largely overlooked that sensory experiences made during the larval stage can affect such relationships. We addressed this issue by determining the role of natal experience on oviposition preference and larval performance relationships in a tritrophic system consisting of Galerucella sagittariae, feeding on the two host plants Potentilla palustris and Lysimachia thyrsiflora, and its larval parasitoid Asecodes lucens. We firstly determined whether differences in host-derived olfactory information could lead to divergent host selection, and secondly, whether host preference could result in higher larval performance based on the natal origin of the insects. Our results showed that the natal origin and the quality of the current host are both important aspects in oviposition preference and larval performance relationships. While we found a positive relationship between preference and performance of natal Lysimachia beetles, natal Potentilla larvae showed no such relationship and developed better on L. thyrsiflora. Additionally, the host selection by the parasitoid was mainly affected by the natal origin, while its performance was higher on Lysimachia larvae. With this study we showed that the relationship between oviposition preference and larval performance depends on the interplay between the natal origin of the female and the quality of the current host. However, without incorporating the full tritrophic context of these interactions, their implication in insect fitness and potential adaptation cannot be fully understood.