Diet dependent experience and physiological state shape the behavior of a generalist herbivore

The performance of herbivorous insects depends on a balance of nutrient uptake and toxin avoidance. Whereas high concentrations of defensive plant metabolites impair both generalists and specialists, generalists are likely less adapted to particular hosts and thus more negatively affected by plant defense traits. Furthermore, resulting diet-dependent differences in the physiological state and the gained experience of an animal may shape its behavior. Here, we investigated the effects of life-long experience with leaves of different quality on the performance and various behavioral traits of the generalist leaf beetle Galeruca tanaceti. Rearing individuals continuously on three different diets [young leaves, old leaves, or leaves of different age of cabbage (Brassicaceae) in alternating order every other day], we found that relative growth rates (RGRs) of the larvae were higher when feeding on young leaves than when feeding on the other diets. Feeding on leaves of different age in alternating order reduced the performance of G. tanaceti, indicating costs involved in diet mixing. The experience gained by the respective food qualities shaped the preference behavior in adult beetles. Positive and negative feedbacks of animals reared on young or old leaves, respectively, led to a preference towards young leaves. In contrast, feedback was probably prevented for animals reared on alternating diet, which did not exhibit any preferences. Older adults did not show any diet-dependent differences in body mass due to physiological changes during adult development. A battery of behavioral tests with the older adults revealed that the behavior was consistent over context and partially over time but behaviors did not differ in dependence of the diet experience. We retrieved three personality dimensions for this species, namely boldness, activity, and exploration. The behavioral structure was very similar to earlier findings for another chrysomelid species, indicating a broader validity of the concept of personality dimensions in insects. Our results demonstrate the importance of both experience- and state-dependence when investigating behavioral phenotypes.