Quantifying direct and indirect effects of early‐season herbivory on reproduction across four brassicaceous plant species

Author:

Mertens Daan12ORCID,Douma Jacob C.3ORCID,Kamps Bram B. J.1ORCID,Zhu Yunsheng14ORCID,Zwartsenberg Sophie A.15ORCID,Poelman Erik H.1ORCID

Affiliation:

1. Laboratory of Entomology Wageningen University and Research Wageningen The Netherlands

2. Department of Entomology and Nematology University of California Davis California USA

3. Centre for Crop Systems Analysis Wageningen University Wageningen The Netherlands

4. Institute for Resistance Research and Stress Tolerance, Julius Kühn Institut Quedlinburg Germany

5. Forest Ecology and Forest Management Group Wageningen University and Research Wageningen The Netherlands

Abstract

Abstract Insect herbivores can directly affect plant reproduction by feeding on reproductive tissues, or indirectly by feeding on vegetative tissues for which plants are unable to compensate. Additionally, early arriving herbivores may have cascading effects on plant reproduction by altering the later arriving community. However, the dynamic interplay between plant development and the assembly of herbivore communities remains underexplored. Hence, it is unclear whether non‐outbreak levels of ambient herbivory early in the development of plants can impact plant fitness and to what extent these effects are mediated through changes in plant development and subsequent herbivory. By excluding the herbivore community in an exclosure experiment and by manipulating early‐season herbivory in a common garden field experiment replicated across four Brassicaceae species and 2 years, we tested whether early‐season herbivory by caterpillars (Pieris rapae) or aphids (Myzus persicae) affected development, reproduction, and the herbivore communities associated with individual plants. In addition, we tested a causal hypothesis to assess the relative importance and temporal interplay between variation in herbivore communities and variation in plant development in determining plant reproduction. Early‐season herbivory affected plant reproduction in the exclosure experiment, with effects being highly dependent on the plant species, the herbivore species and the year. However, we found no such effects in the field experiment. The exploratory path analysis indicated that variation in plant reproduction is best predicted by variation in plant development, explaining 80% of the total effect on seed production. This suggests early‐season herbivory had limited effects on later plant development, and plants were able to attenuate the impact of early‐season herbivory. However, no clear compensatory mechanism could be identified. While early‐season herbivory has the potential to affect plant reproduction through changes in plant development or the subsequent development of the associated community, these effects were small and varied across closely related species. This suggests that plant species may be exposed to different levels of natural selection by early‐season herbivores through plant‐ or community‐mediated effects on reproduction. Read the free Plain Language Summary for this article on the Journal blog.

Funder

H2020 European Research Council

Publisher

Wiley

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