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Plant adaptations to unpredictable attack by dynamic insect communities

Periodic Reporting for period 2 - MULTIATTACK (Plant adaptations to unpredictable attack by dynamic insect communities)

Reporting period: 2017-08-01 to 2019-01-31

Individual plants are exposed to many stresses with insect herbivores being a prominent one. The occurrence of insect herbivores may be unpredictable in terms of when, by which species, and in which order the attack will take place. To deal with unpredictability of attack, plants are phenotypically plastic in their defence. They respond to attackers with the induction of specific defences and saving costs of defence in their absence. However, the induced plant phenotype may attract additional herbivores, alter the entire community composition of attackers and limit physiological capabilities of plant responses to subsequent attackers. An optimal response to one attacker should thus anticipate these consequences of induced responses. To understand the adaptive nature of plant plasticity to herbivore attack, it is essential to assess fitness consequences of an induced response when plants are exposed to multi-herbivory by their entire insect community. This requires a novel approach of comparing plant species adaptations in defence plasticity to the level of predictability in the dynamics of their insect community, such as order of herbivore arrival. To do so, this research proposal has three objectives: 1) Identifying the predictability of dynamic attacker communities of Brassicaceae species, 2) Understanding physiological adaptations to (un)predictable multi-herbivore attack, and 3) Identifying consistency in responses of insect herbivores to induced phenotypes of different Brassicaceae. By integrating community ecology with network inference modelling of insect communities, the nature of predictability of insect communities of annual Brassicaceae plant species will be identified and linked to species-specific physiological adaptations to multi-herbivory. This multidisciplinary community approach will provide novel insights into the evolution of plant phenotypic plasticity in defence, which is a central paradigm in the field of plant-insect interactions. These fundamental insights are critical for breeding of crop varieties and design of sustainable cropping systems that are resilient to the multiple stress factors that typically co-occur in our agricultural systems.
In the first 18 months of the project:
We have conducted two large scale field experiments to elucidate the predictability of insect community structure on individual plants of different Brassicaceae species. We identified that plant species differ in the number of insect herbivore species, their order of arrival and predictability of these patterns in colonisation of individual plants. Early-season herbivore species alter plant colonisation in a specific direction for each herbivore species.
To measure plant species specific plasticity to multi-herbivore attack, we have developed a toolbox with primers for a set of genes related to defence signalling for over ten Brassicaceae species.
In a large greenhouse assay we explored how ten different herbivore species induce defensive responses in the plant species Brassica nigra and how these responses in turn affect performance of each of these herbivores. We are currently analysing these data.

The main published results in this period (18 months):
Results from an earlier greenhouse experiment in this project show that the plant response to two herbivore species affects preference and performance of a third herbivore (Stam et al. 2017 Ecological Entomology).
My team has also written a review on how plant interactions with multiple insect species affects behaviour of community members in a landscape context (Aartsma et al. 2017 New Phytologist).

After 30 months of the project:
We repeated the large scale field experiment to measure insect community assembly on different Brassicaceae species for a third year. In this field experiment we selected six Brassicaceae species that were the most different in their insect communities based on data of the first field season. We induced a part of the plants with early-season herbivory by aphids or caterpillars and monitorred the assembly of the insect community over the entire growth season of the plants. We tested whether the same early-season herbivores affect community assembly on six plant species similarly or differently. We further assesed whether the indirect interactions arrising from the induction treatments have plant fitness consequences. We have been able to build an extensive dataset to study the insect community objectives of the project. We are currently combining the three year dataset to make detailed analyses of i) plant species specific insect community assembly, ii) yearly variation in insect community assembly, iii) effect of early-season herbivory on community assembly, iv) insect species that affect plant fitness, and how indirect interactions among species is reflected in plant fitness consequences. We reserved the final two years of the project to do extensive data-analyses and manuscript writing (as planned).

We made extensive progress in studying the physiological response of plants to Multi-herbivore attack. In several large scale greenhouse experiments we have:
i) Identified general rules in pair-wise plkant mediated species interactions by comparing a matrix of full factorial pair-wise interactions between 10 different insect herbivores on Brassica nigra plants. The data collected show that especially the level of food plant specialisation of the herbivore feeding on an induced plant, predicts its performance on the induced plant. We are currently preparing a manuscript on these findings.
ii) Uncovered that plant responses to a higher diversity of insect attack, results in stronger plant defence responses. We are currently finalizing analyses of these data.
iii) Uncovered that plant responses to a sequence of attack by multiple herbivores are highly plastic. Interestingly, the identity of the last attacker, but also the identity of all previous events of attack determine the plant defence phenotype. We are currently finalizing analyses of these data.
iv) Identified that plant species differ in their plasticity to Multi-herbivore attack and are currently in the middle of a large greenhouse experiment to furth
The proposed study aims to identify which plastic defence strategies are deployed by plants to deal with unpredictable attack by dynamic multi-herbivore communities. My vision is that the ecological and physiological consequences of an induced response have been incorporated in evolution of defence plasticity and, therefore, plant species have adapted to the level of predictability in the structure of their dynamic attacker community such as the order of arrival of species and correlations among colonisation by different herbivores. This requires to integrate research in two fields: insect community ecology and plant physiology to multi herbivore attack. An important aspect will be to identify whether insect communities differ among plant species not only in composition, but especially in the predictability of the order of arrival of species and correlations among their likelihood of colonisation. In terms of plant physiology it remains to be identified how plants cope with more than two stressors. Standing questions are whether plants prioritize responses to particular attackers within their entire attacker community and to what extent plants can redirect their defences to current attackers when having responded to others before. It requires a major leap in complexity by including a large number of species to address these physiological questions that will in turn help to understand the adaptive value of plant physiological mechanisms currently identified for plants exposed to dual stress. Only very recently have different closely related plant species been found to vary in their capability to deal with simultaneous attack by aphids and caterpillars, providing support for plant adaptations to combined stresses. However, to understand the adaptive value of variation in defence plasticity, an evaluation of these responses should be made within the intact herbivore community.
By taking a comparative approach of plant species adaptations to attack by multi-herbivore communities, the results of this project will provide novel insights into how plants integrate complex problems of multi-species attack. We expect to show how predictability in the order of arrival of insect herbivores on individual plants is reflected in the adaptations of plants in defence plasticity.