Caught between friends and foes : plant-mediated interactions between herbivores and flower visitors

Understanding the interplay between ecology and evolution in complex multispecies communities is a major challenge for ecologists. Most plant species are flowering plants, and to maximize their contribution to the next generation they need to deal with antagonistic herbivores while also engaging in interactions with mutualistic pollinators. Plants respond to attack by herbivores with phenotypic changes to repel or kill the attackers, and when plants are flowering, these changes extent to flower-trait expression. As a result, herbivore attack can alter interactions with pollinators and flower feeders. Knowledge on the specificity of herbivore-induced changes in flower traits, importance for the assembly of flower-visitor networks, and associated consequences for plant fitness is limited to date. The aim of this thesis project was to investigate how attack by a range of herbivore species affects plant interactions with mutualistic and antagonistic flower visitors and whether these interactions have consequences for plant fitness. I was especially interested in specificity of plant-mediated herbivore - flower-visitor interactions. The study used the Black mustard (Brassica nigra) plant and ten different herbivore species with different feeding behaviours: some choose to feed among their favourite tissues, others are highly specialized and engage in intimate and manipulative feeding relations with the plant, whereas a few take bites or sips from different plant parts. Black mustard is an annual plant species which relies on insect pollinators for reproduction. The large fragrant inflorescences contain hundreds of small yellow flowers which attract various generalist pollinators, but also specialist florivores such as pollen beetles, Meligethes spp. Chapter 2 addresses the current knowledge on flower plasticity in response to herbivory and places flower plasticity in a community context. The chapter reviews the extent to which herbivore-induced plant responses affect multiple flower traits, and the molecular mechanisms underlying floral plasticity. To understand the adaptive value of flower plasticity with contrasting differences on pairwise interactions, it is important to adopt a community perspective. Chapter 3 evaluates specificity of plant responses to different herbivore species and how these plant responses affect flower visitors and plant fitness. The results show that attack of B. nigra by a range of different herbivores influenced plant interactions with mutualistic pollinators and an antagonistic florivore, the pollen beetle Meligethes aeneus, with consequences for plant reproduction. In Chapter 4, my aim was to investigate whether herbivore - flower-visitor interactions and associated plant fitness consequences are different when timing of herbivore attack varies over plant ontogeny. My data shows that the indirect interaction web between herbivores and flower visitors is dynamic and variable over plant ontogeny, and that consequences of herbivory for plant reproductive output are strongest when plants are attacked by herbivores early in life. Chapter 5 explored the underlying mechanisms of specificity in herbivore – flower-visitor interactions. I found that flowers show extensive plasticity in response to herbivores, that herbivore-induced changes in flower traits are mostly herbivore-species specific, and have contrasting effects on pollinators. In Chapter 6, I use manipulative experiments to explore whether herbivore choice for a given feeding site determines the outcome of plant-mediated herbivore-pollinator interactions. The results show that variation in herbivore feeding site has profound impact on the outcome of herbivore-pollinator interactions. The data presented in this thesis contribute to our understanding of the complex ecological and evolutionary dynamics in multispecies communities with antagonists and mutualists, and this is discussed in Chapter 7