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Plant adaptations to unpredictable attack by dynamic insect communities

Periodic Reporting for period 3 - MULTIATTACK (Plant adaptations to unpredictable attack by dynamic insect communities)

Reporting period: 2019-02-01 to 2020-07-31

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.
After 54 months of the project:
We have conducted five years of field experiments in which we reveal that early-season herbivory affect community assembly of insect herbivore communities and that these processes affect plant fitness. These effects differ for plant species and is strongly dependent on the predictability of insect community assembly on individual plants. In our modelling approaches, we identified that the impact of herbivore attack is strongly modified by plant competition for light and nutrients. By studying the physiological responses of plant species to different scenarios of multi-herbivore attack, we reveal that plants integrate responses to multiple herbivores to anticipate future herbivore attack. In these physiological studies we show that plant species have different repertoires to deal with sequential and simultaneous attack by multiple herbivores.

The main achievements of the project in this period (54 months):
Result from field studies reveal that the order of herbivore arrival on wild cabbage populations influences subsequent arthropod community development (Stam et al. 2018 Oikos).We discovered that herbivory in the first year for perennial plants has consequences for herbivore attack in the next year and affects plant fitness (Stam et al. 2019 Journal of Ecology)

We discovered that symbiotic virusses associated with parasitic wasps affect plant-mediated species interactions between herbivores (Cusumano et al. 2018 Ecology Letters) as well as higher trophic level organisms (Zhu et al. 2018 PNAS). We presented new synthesis of the role of micro-organisms associated with third trophic level organisms in affecting multi-trophic interaction in insect communities (Dicke et al. 2020 Annual Review of Entomology)

We presented a wide array of studies on parasitoid behavior in response to multi-herbivore attack and habitat complexity (Aartsman et al 2019 Current Opinion Insect Science; 2019 Oikos; 2020 Landscape Ecology; 2020 Oikos)

We used a new modelling approach to elucidate the interaction between plant competition for light and herbivore feeding patterns (de Vries et al. 2018 Annals of Botany). Results from our modelling approaches identified the intricate interplay between plant defence and competition for adaptiveness of plant defence strategies (de Vries et al. 2019 Functional Ecology; Douma et al 2019 Plant Cell and Environment)

We identified an important role for herbivore-pollinator interactions in determining indirect effects on plant fitness (Rusman et al. 2018 Functional Ecology; 2019 Oecologia; 2019 Plant Cell and Environment; 2019 Trends in Plant Science; 2020 Journal of Ecology)

We have several publications pending on the physiological capabilities of plants to attack by multiple herbivores.
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.
How do plants defend themselves against multi-herbivore attack?