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.

Enhancing natural enemy performance through plant secondary metabolites: The role of caffeine for the parasitoid Snellenius manilae

“…As a result, we hypothesize that S. manilae may exhibit higher physiological performance and locomotion ability by consuming a suitable dose of caffeine solution. However, most literature has shown that caffeine and other secondary metabolites might have some negative effects on parasitoids (Hall et al., 2021; Poyet et al., 2017; Thurston & Fox, 1972; Tougeron & Hance, 2021), with a few studies revealing that alkaloids might have no effects on parasitoids (Kostenko et al., 2013; Krauss et al., 2007; Urrutia et al., 2007), which is in contrast to our findings. The main reason for the difference is that previous papers concentrated on the tri‐trophic or multi‐trophic level (Tougeron & Hance, 2021).…”

“…However, most literature has shown that caffeine and other secondary metabolites might have some negative effects on parasitoids (Hall et al., 2021; Poyet et al., 2017; Thurston & Fox, 1972; Tougeron & Hance, 2021), with a few studies revealing that alkaloids might have no effects on parasitoids (Kostenko et al., 2013; Krauss et al., 2007; Urrutia et al., 2007), which is in contrast to our findings. The main reason for the difference is that previous papers concentrated on the tri‐trophic or multi‐trophic level (Tougeron & Hance, 2021). For these trophic‐level studies, the experiments were tested on the parasitoids that parasitized the herbivores that fed on diets or plants containing alkaloids (Barker & Addison, 1996; Bultman et al., 2009, 2012; Campbell & Duffey, 1979).…”

“…However, only a few studies focus on the plant secondary metabolites feeding response of adult parasitoids. Despite the fact that caffeine is primarily regarded as a plant defence mechanism and can be toxic to herbivorous pests (Kim et al., 2006) and even parasitoids larvae (Tougeron & Hance, 2021), it is still worthy to investigate its potential benefits for the adult stage.…”