Disentangling associational effects: both resource density and resource frequency affect search behaviour in complex environments

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.