Insects on Individual Plants: Plant quality, plant diversity and aboveground-belowground effects Olga Kostenko Thesis committee Promotor Prof. Dr. W. H. Van der Putten Professor of Functional Biodiversity Laboratory of Nematology Wageningen University Co-promotor Dr. T. M. Bezemer Senior scientist Netherlands Institute of Ecology, Wageningen Other members Prof. Dr. D. Bonte, Ghent University, Belgium Prof. Dr. N. M. Van Dam, Radboud University Nijmegen Prof. Dr. L. Brussaard, Wageningen University Dr. E. H. Poelman, Wageningen University This research was conducted under the auspices of the C.T. de Wit Graduate School for Production Ecology & Resource Conservation (PE&RC) Insects on Individual Plants: Plant quality, plant diversity and aboveground-belowground effects Olga Kostenko Thesis submitted in fulfillment of the requirements for the degree of doctor at Wageningen University by the authority of the Rector Magnificus Prof. Dr. M.J. Kropff, in the presence of the Thesis Committee appointed by the Academic Board to be defended in public on Friday 14th February 2014 at 4 p.m. at the Aula. Olga Kostenko Insects on Individual Plants: Plant quality, plant diversity and aboveground- belowground effects, 232 pages. PhD thesis, Wageningen University, Wageningen, NL (2014) With references, with summaries in Dutch and English ISBN 978-94-6173-863-9 To my Mother Contents Abstract 9 Chapter 1 General introduction 11 Chapter 2 Effects of root herbivory on pyrrolizidine 33 alkaloid content and aboveground plant-herbivore- parasitoid interactions in Jacobaea vulgaris Chapter 3 Legacy effects of aboveground-belowground interactions 53 Chapter 4 Effects of diversity and identity of the neighbouring plant 73 community on the abundance of arthropods on individual ragwort (Jacobaea vulgaris) plants Chapter 5 Surrounding plants influence the nutritional quality of 89 focal plants in a field experiment Chapter 6 Behaviour of parasitoids in the field: effects of diversity 107 and complexity of the surrounding plant community Chapter 7 Plant diversity and identity effects on entomopathogenic 125 nematode infection and predatory nematode abundance in the soil Chapter 8 Intraspecific variation in plant size, secondary plant 147 compounds, herbivory and parasitoid assemblages during secondary succession Chapter 9 General discussion 167 References 191 Summary 210 Nederlandse samenvatting (Dutch summary) 215 Acknowledgements 221 Current affiliations of co-authors 226 Curriculum vitae 227 Education statement 230 9 Abstract The density and composition of insects on a given plant species can vary greatly among individuals of that species. Understanding factors causing this variability can help us to predict the composition of insect communities on plants and their responses to environmental changes. The main aim of this thesis was to elucidate factors that structure the insect community associated to individual plants. Plant quality and diversity are increasingly recognized as important determinants of the composition and abundance of terrestrial insects. Hence, I specifically examined how individual variation in plant quality and local variation in the diversity of the plant community determine the performance and abundance of insects on individual plants. As a model system I used aboveground and belowground communities associated to ragwort (Jacobaea vulgaris Gaertner synonym Senecio vulgaris), an outbreak plant species native to the Netherlands. In experiments under controlled greenhouse conditions I found that belowground herbivory caused a decrease in the concentration of the secondary plant compounds in the aboveground parts of J. vulgaris but did not affect the performance of aboveground insects that fed on the same plant. However, aboveground and belowground herbivores created unique soil legacy effects via herbivore-induced changes in the composition of the soil microbial community. These soil legacies affected the growth and secondary chemistry of plants that later grow in the same soil, as well as the aboveground multitrophic interactions occurring on those plants. It reveals that plant quality-mediated interactions between aboveground and belowground insects can also be important when they do not feed simultaneously on the same plant. Future studies should estimate the importance of these legacy effects in relation to other factors structuring insect communities on individual plants in the natural systems. Using a field experiment, where plant species diversity was manipulated experimentally, I demonstrated that both the presence and the diversity of the surrounding vegetation affected the nutritional and chemical quality and size of focal J. vulgaris plants growing in that community. However, the abundance of an aboveground specialist herbivore that naturally colonised the focal J. vulgaris plants was influenced directly by the surrounding plant community and not via the effects of surrounding vegetation on the performance of the focal plants. Parasitoid foraging behaviour in the diversity plots was not affected by plant diversity, but by the structural complexity of the plant community surrounding the host-infested J. vulgaris plants. Belowground, increasing plant species diversity enhanced the level of predation of root herbivores indirectly by modifying the prey densities, but there were no effects of plant diversity on 9 predator abundance. Finally, in a chronosequence consisting of ten ex-arable fields that are restored to grasslands, the abundance and diversity of insects reared out from individual J. vulgaris plants differed among fields but did not correlate with the intraspecific changes in plant size or quality. I conclude that the role of plant quality in structuring insect communities on individual plants in natural settings is subordinate to the effects of the surrounding plants on the aboveground and belowground communities associated to individual plants. Therefore, individual plant-insect interactions should be considered from the community perspective and future studies should aim at further disentangling the role of plant quality in structuring insect communities in natural settings. 10 Chapter 1 General introduction 10 Chapter 1 General introduction 12 13 Chapter 1 General introduction Insects are the largest group of macroscopic organisms on Earth and they inhabit a range of trophic levels and functional groups. Insects are involved in a variety of ecological interactions with almost all other living organisms as they consume plants and dead organic matter, but also predate or parasite on other consumers including human being. The interactions between plants and insects have attracted scientific interest of ecologists for more than a century. This is not surprising, as plants harbour diverse multitrophic insect communities with myriad interactions that form the foundation of communities and ecosystems. Furthermore, these multitrophic insect communities are responsible for a variety of important functions within ecosystems, and can help us understand the relationship between plant diversity and ecosystem functioning (Price et al. 2011). Besides, insects are fascinating to study and many of them are still to be discovered. Ecological communities can be defined as “groups of species that interact, or have the potential to interact, with each other” (Strong et al. 1984). Here, I use the term “insect community” to delineate a group of herbivorous insects and their natural enemies (predators and parasitoids) associated to an individual plant. During the past three decades, ecologists and entomologists have become increasingly aware that the density and composition of insects on a given plant species can vary greatly among individuals of that species. Understanding how species interactions contribute to community composition and ecosystem functioning constitutes a central topic in ecology. Therefore, the question what determines the composition of an insect community on a plant has received considerable attention (Strong et al. 1984; Lawton et al. 1993; Lewinsohn et al. 2005). Different approaches have been employed to study how host plants influence the composition of the insect community associated to those plants. One line of research has focussed on the effects of intraspecific differences in plant quality as a factor structuring insect communities. Plant quality is extremely important in every aspect of plant-insect interactions, including host- plant selection, growth, survivorship, and reproduction (reviewed in Awmack & Leather 2002). However, what the importance is of plant quality in structuring insect communities in natural habitats remains unknown. Another line of research has focussed on how characteristics of the habitat or plant community can structure the insect assemblages on plants growing in that community. In nature, plants usually occur in mixed plant communities, where aboveground and belowground communities of insects and other biota associated to a plant are also influenced by interactions that occur on the neighbouring plants. The importance of the surrounding vegetation in determining how many insects are found on a particular plant was already recognized in the early seventies 12 13 Chapter 1 General introduction (Tahvanainen & Root 1972; Feeny 1976; Atsatt & O’Dowd 1976). These studies reported that the probability that a plant is found by an insect often depends not only on its own inherent characteristics (such as plant quality), but also on the chemistry, morphology, distribution, and abundance