Cascading effects of caffeine intake by primary consumers to the upper trophic level.

Abstract

Secondary metabolites are central to understanding the evolution of plant-animal interactions. Direct effects on phytophagous animals are well-known, but how secondary consumers adjust their behavioural and physiological responses to the herbivore's diet remains more scarcely explored for some metabolites. Caffeine is a neuroactive compound that affects both the behaviour and physiology of several animal species, from humans to insects. It is an alkaloid present in nectar, leaves and even sap of numerous species of plants where it plays a role in chemical defences against herbivores and pathogens. Caffeine effects have been overlooked in generalist herbivores that are not specialized in coffee or tea plants. Using a host-parasitoid system, we show that caffeine intake at a relatively low dose affects longevity and fecundity of the primary consumer, but also indirectly of the secondary one, suggesting that this alkaloid and/or its effects can be transmitted through trophic levels and persist in the food chain. Parasitism success was lowered by ≈16% on hosts fed with caffeine, and parasitoids of the next generation that have developed in hosts fed on caffeine showed a reduced longevity, but no differences in mass and size were found. This study helps at better understanding how plant secondary metabolites, such as caffeine involved in plant-animal interactions, could affect primary consumers, could have knock-on effects on upper trophic levels over generations, and could modify interspecific interactions in multitrophic systems.