Abstract
Terrestrial tri-trophic interactions account for a large part of biodiversity, with approximately 75% represented in plant–insect–parasitoid interactions. Herbivore diet breadth is an important factor mediating these tri-trophic interactions, as specialisation can influence how herbivore fitness is affected by plant traits. We investigated how phytochemistry, herbivore immunity, and herbivore diet breadth mediate plant–caterpillar–parasitoid interactions on the tropical plant genus Piper (Piperaceae) at La Selva Biological station in Costa Rica and at Yanayacu Biological Station in Ecuador. We collected larval stages of one Piper generalist species, Quadrus cerealis, (Lepidoptera: Hesperiidae) and 4 specialist species in the genus Eois (Lepidoptera: Geometridae) from 15 different species of Piper, reared them on host leaf material, and assayed phenoloxidase activity as a measure of potential larval immunity. We combined these data with parasitism and caterpillar species diet breadth calculated from a 19-year database, as well as established values of phytochemical diversity calculated for each plant species, in order to test specific hypotheses about how these variables are related. We found that phytochemical diversity was an important predictor for herbivore immunity, herbivore parasitism, and diet breadth for specialist caterpillars, but that the direction and magnitude of these relationships differed between sites. In Costa Rica, specialist herbivore immune function was negatively associated with the phytochemical diversity of the Piper host plants, and rates of parasitism decreased with higher immune function. The same was true for Ecuador with the exception that there was a positive association between immune function and phytochemical diversity. Furthermore, phytochemical diversity did not affect herbivore immunity and parasitism for the more generalised herbivore. Results also indicated that small differences in herbivore diet breadth are an important factor mediating herbivore immunity and parasitism success for Eois at both sites. These patterns contribute to a growing body of literature that demonstrate strong cascading effects of phytochemistry on higher trophic levels that are dependent on herbivore specialisation and that can vary in space and time. Investigating the interface between herbivore immunity, plant chemical defence, and parasitoids is an important facet of tri-trophic interactions that can help to explain the enormous amount of biodiversity found in the tropics.
Highlights
Tri-trophic interactions are an important feature of biotic communities and contribute to the maintenance of biodiversity as well as mediate ecosystem processes (Price et al, 1980; Hunter and Price, 1992; Agrawal, 2000; Price, 2002; Whitham et al, 2006)
Our results corroborate many other studies demonstrating that the chemistry of herbivore host plants, as well as herbivore diet breadth have strong effects on multiple aspects of herbivore ecology (Berenbaum and Neal, 1985; Haviola et al, 2007; Diamond and Kingsolver, 2011; Lampert and Bowers, 2015), including immunity and parasitism (Smilanich et al, 2009a; Hansen et al, 2017)
A focus on the immune response allows for investigation of an important physiological parameter that is directly linked to protection against natural enemies (Smilanich et al, 2009b), putting our results in a strong tri-tropic context
Summary
Tri-trophic interactions are an important feature of biotic communities and contribute to the maintenance of biodiversity as well as mediate ecosystem processes (Price et al, 1980; Hunter and Price, 1992; Agrawal, 2000; Price, 2002; Whitham et al, 2006). Plant chemical defence is one of the most important components of these bottom-up effects, and there is a rich literature documenting how chemistry affects plant–insect interactions (Fraenkel, 1959; Ehrlich and Raven, 1964; Schoonhoven et al, 2005; Hunter, 2016), via both negative and positive physiological and behavioural effects on herbivores and natural enemies (Smilanich et al, 2016). One clear gap in our knowledge of how phytochemistry influences tri-trophic interactions is empirical data that consider the entire suite of plant secondary metabolites in a species instead of focusing on one or two major compounds (Richards et al, 2010, 2016; Smilanich et al, 2016). We use phytochemical diversity as a metric of plant defence to investigate the effects on herbivore performance as measured by immune strength, and whether effects on the immune response cascade to impact parasitism success (Smilanich et al, 2009b; Richards et al, 2015; Hansen et al, 2017)
Sign-in/Register to view highlights & summary Sign-in/Register to access full text options 
Free) 
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a call
