TRICOMM: Structure, assembly and evolution of natural tritrophic communities

Communities of plants, insect herbivores, and their insect parasitoid enemies provide most of the known species on Earth. These communities include interactions that lead to economic damage, such as pests of crops, and others that benefit human societies, such as biocontrol agents. Despite their importance, we still know little about what determines which species eat, or are eaten by, other species. We know most about links between plants and herbivores, less about herbivores and parasitoids, and less again about patterns over all three levels combined. A key question is the extent to which such three level (tritrophic) species associations are structured from the 'bottom-up' by plant traits, from the 'top-down' by parasitoids, or some combination of these. The 'bottom-up' view regards herbivore-parasitoid interactions as structured by processes happening a trophic level lower, via the effects of plants on herbivores. In contrast, the 'top-down' view sees parasitoid-herbivore interactions as driving the evolution of herbivore defences, and these traits as more important for structuring parasitoid communities than the host plants on which they are found.

This project assesses the evidence for these alternative models, and their combinations, using state of the art statistical methods that require three types of data: (i) an interaction matrix, summarising links between species in one trophic level and those in another; (ii) herbivore defence trait data and (iii) complete species-level phylogenies for plants, herbivores and their parasitoids. Finding that plant phylogeny is a strong predictor of both plant-herbivore and herbivore-parasitoid interactions would support the bottom-up view. In contrast, finding that herbivore-parasitoid interactions are strongly predicted by herbivore defensive traits would support a top-down view.

First, we will estimate the effects of species identity and traits on plant-herbivore and herbivore-parasitoid interactions, providing the first test of the relative importance of bottom-up versus top-down processes. We will use over 50,000 records of specific plant-herbivore-parasitoid interactions for natural communities comprising trees, gallwasp herbivores, and chalcid parasitoids, sampled from three regional datasets that span the Northern Hemisphere. These communities have evolved independently for long enough to provide largely independent tests of our hypotheses.

Second, we ask whether herbivores in our three regional communities have independently evolved similar sets of defences. If top-down effects are strong, and herbivore defences target fundamental aspects of parasitoid attack behaviour, then selection should favour the repeated evolution of similar sets of defensive traits. Gallwasp herbivores live inside galls, complex novel plant tissues whose development the larval wasps induce. Parasitoids all attack gallwasps by drilling through gall tissues, and previous work suggests that some gall traits (such as coatings of spines or sticky resins) have evolved to make this more difficult. Our hypothesis is that such gall traits will both structure parasitoid communities and have evolved repeatedly.

Finally, we will assess how well our statistical models predict which parasitoids attack a novel or unsampled gallwasp herbivore when all we know about it are which plant it is on, which gall traits it has, and how it is related to other gallwasps. Our approach involves making model-based predictions for gallwasp-parasitoid interactions for which we have real data, so that via cross-validation we can assess the accuracy (i.e. whether predictions are unbiased) and precision (i.e. whether predictions are made with high confidence) of our model. This approach could be of particular value in predicting the natural enemies of emerging pests and the non-target victims of natural enemies, and we will apply it to predicting the enemies attacking oriental chestnut gallwasp, a global pest species.

Natural communities of plants, insect herbivores and their natural enemies make up most of the species on Earth and contribute to many crucial ecosystem functions. From a human perspective, these communities include both food crops and noxious weeds, useful pollinators and harmful pests, and useful biocontrol agents. This projects aims to improve understanding of why some species interact (in the sense of eating, or being eaten) with more species than others, and also what determines which species interact. The research focusses on natural communities of gallwasp herbivores and parasitoid natural enemies associated with oaks and related trees across the Northern Hemisphere. The work involves international collaborations with scientists in the USA, Australia, Hungary and China.

Our work will produce three major impacts.
1. We will generate a general framework for statistical prediction of which species interact in nature. We will assess the extent to which properties of species (their traits, and evolutionary relationships) can be used to predict what they eat, and who eats them. We see this output as being of potential impact value in predicting the natural enemies that might attack a new and emerging pest, or predicting the unintended non-target victims at risk from release of a biological control agent. Though developed for a specific model community, our approach should be generalisable to other three trophic level communities.
2. We will provide detailed natural enemy data on the natural enemies associated with a globally invasive pest gallwasp. Originating in China, the oriental chestnut gallwasp (OCGW)has become a pest across the Northern Hemisphere and reached the UK in 2015. We will provide the first detailed information on natural enemies attacking this pest in China, and apply our modelling approach to prediction of its natural enemies in Europe. We see this output as delivering impact by contributing to ongoing debates on potential for natural biological control of this pest in the UK, and the need to consider release of non-native biological control agents.
3. In collaboration with our Chinese project partners, we will generate the first Chinese language guides to gallwasp communities (including oriental chestnut gallwasp) and their natural enemies. We see this output as delivering impact through increasing stakeholder awareness of these organisms and their interactions.

Beneficiaries.
We see major UK beneficiaries as falling into three groups:
(i) Governmental organisations, particularly Defra (the Department for Environment, Food and Rural Affairs), SEPA (the Scottish Environment Protection Agency), and Natural Resources Wales).
(ii) Research agencies, particularly FERA (the Food and Environment Research Agency), which maintains the Plant Health Risk Register and coordinates collection of data on OCGW and associated control measures for Defra, and Forest Research, which coordinates many of the control measures for OCGW and other alien forest pests.
(iii) Charitable organisations, particularly the National Trust, National Trust for Scotland, and the Woodland Trust.
We see major international beneficiaries of our work as equivalent institutions in other countries who we will reach through our Chinese project partners and IUFRO (the International Union of Forest Research Organisations), which brings together a wide range of policy makers and practitioners in forest management (see below).

Our pathway to impact will be delivered through publications and two workshops (one in the UK, one in China) at the end of the project. This impact delivery is strongly supported by stakeholders in the UK government (Defra, Forest Research) and charitable sectors (The Woodland Trust), and in China.