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Multitrophic Interactions on a Range-Expanding Plant Species Multitrophic interactions on a range-expanding plant species Taiadjana Filipa Marques Fortuna Thesis committee Promotors Prof. Dr Louise E. M. Vet Professor of Evolutionary Ecology Wageningen University Prof. Dr Jeffrey A. Harvey Professor of Nature Conservation and Environmental Advocacy VU University Amsterdam Other members: Prof. Dr Harro J. Bouwmeester, Wageningen University Dr Tom de Jong, Leiden University Dr Jacqui Shykoff, Paris-Sud XI University, France Prof. Dr Nicole M. van Dam, Radboud University, Nijmegen This research was conducted under the auspices of the Graduate School of Production Ecology and Resource Conservation (PE&RC) Multitrophic interactions on a range-expanding plant species Taiadjana Filipa Marques Fortuna Thesis submitted in fulfilment 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 Tuesday 19 November 2013 at 11a.m. in the Aula. Taiadjana Filipa Marques Fortuna Multitrophic interactions on a range-expanding plant species, 229 pages PhD thesis, Wageningen University, Wageningen, NL (2013) With references, with summaries in English, Dutch and Portuguese ISBN 978-94-6173-765-6 The path of a PhD is like an insect metamorphosis. A young caterpillar emerged from the egg of knowledge passes through several phases in the quest for results, reaches a pupal phase while writing and writing and writing And in the end, it emerges as a butterfly with wings to fly.. (Taia 2013) À minha mãe, guerreira e sonhadora.. Abstract Studies on the ecological impacts of exotic invasive plants have mainly focused on inter- continental invasions. However due to global environmental changes, a rapid increase in intra-continental range-expanding plants has been observed. In this context, multitrophic interactions between exotic plants, native herbivores and their natural enemies have been largely ignored. This thesis aimed at examining how an exotic range-expanding plant interacts with aboveground insect herbivores and their natural enemies and how it can contribute to the successful establishment of the exotic plant. In addition, it examines how resistance traits of different populations of the range-expander affect the behaviour and performance of herbivores and their natural enemies in the new habitat. Bunias orientalis (Capparales: Brassicaceae) is perennial plant from extreme south-eastern Europe and Asia that has recently expanded its range and become invasive in northern and central parts of Europe. In the Netherlands, it is considered naturalized but non-invasive. Firstly, using a community approach, I found that Bu. orientalis suffered less herbivore damage and harboured smaller invertebrate communities than sympatric native Brassicaceae in the Netherlands. The exotic plant has been found of low quality for the larval growth of the specialist herbivore (Pieris brassicae). Furthermore, two of its gregarious parasitoids were differentially affected by the quality of the exotic plant. The pupal parasitoid (Pteromalus puparum) survived better than the larval parasitoid (Cotesia glomerata), and the latter parasitized less hosts on the exotic than on native plants. Therefore, the herbivore can be selected to adapt to the new plant by conferring an enemy free space to the herbivore. In this case, a plant shift by the specialist herbivore might occur and thus preventing the further spread of the exotic plant. Conversely, in the field I found greater carnivore pressure on Bu. orientalis compared to other native Brassicaceae, particularly in the peak of arthropod abundance. Hence, top-down forces exerted by herbivore natural enemies may act in concert with bottom-up control of plant resistance traits to counteract herbivore plant shift and promote the successful range expansion of the exotic plant. Secondly, using a biogeographical approach, I found a considerable intraspecific variation in defence traits (trichomes, glucosinolates, metabolic fingerprints) of Bu. orientalis populations from the native and the exotic range. Plants collected in the native range were better defended than their exotic conspecifics. This variation matched with the performance of a generalist herbivore (Mamestra brassicae) and its parasitoid (Microplitis mediator), which developed poorly in plants from the native range. The results suggest that the defensive mechanisms of Bu. orientalis might have been counter-selected during the range expansion of the exotic plant. Further studies, however, need to examine if enemy release in the new range is followed by an increase in performance of the exotic plant. Finally, a comparative study of multitrophic interactions, both above- and belowground, in the plant native range and along the transect of its range expansion can help to clarify the mechanisms underlying the invasive success of Bu. orientalis. 5 Contents Abstract 5 CHAPTER 1 General Introduction 7 CHAPTER 2 Comparing vegetation diversity and invertebrate communities 25 on an exotic range-expanding plant and related natives CHAPTER 3 Chemical and structural effects of invasive plants on herbivore– 80 parasitoid⁄predator interactions in native communities CHAPTER 4 Effects of an invasive plant on the performance of two 99 parasitoids with different host exploitation strategies CHAPTER 5 A tritrophic approach to the preference-performance hypothesis 116 involving an exotic and a native plant CHAPTER 6 Variation in plant defences among populations of a range- 144 expanding plant: consequences for native trophic interactions CHAPTER 7 Synthesis and General Discussion 171 References 190 Summary 210 Samenvatting (Dutch Summary) 214 Sumário (Portuguese Summary) 219 Acknowledgements 223 About the author 226 Publication list 227 PE&RC Education Certificate 228 6 CHAPTER 1 General Introduction Taiadjana M. Fortuna 7 Introduction Due to current global changes driven in part by anthropogenic processes, many plant species are being intentionally or accidentally moved from their native ranges, transported across the world or within land masses and introduced into novel environments (Vitousek et al. 1997). Some of these species find favourable abiotic and biotic conditions to establish in the new range. Exotic species may also establish in an environment where biotic factors, such as absence of their co-evolved enemies, can give them competitive advantages in the new community. This process can contribute to the rapid increase in abundance of the exotic species, which can become invasive and disruptive pest in the new range (Mack et al. 2000). Although a considerable body of research has reported the ecological impacts of invasive plant species (Vila et al. 2011 for review), most of these studies have, thus far, focused on inter-continental invasions, whereas there is relatively little known about mechanisms of invasions within the same continent, known as intra-continental range expansions. This is important, because some plant species have been rapidly increasing their range in recent decades due to climate change and other environmental changes (van der Putten 2012). Therefore, the main aim of this thesis was to study how such an exotic range-expanding plant species interacts with biotic conditions in the new range and how plant-herbivore-carnivore interactions are affected by the novel plant species. Process of plant invasion Exotic plant species can become established and increase in abundance in new habitats via a phased process, in which the exotic species has to overcome various abiotic and biotic barriers or filters in order to persist in the invaded environment. First, the exotic plant (or its propagule) is introduced accidentally by humans through long-distance transport (e.g. via water bodies, rails, roads) or intentionally for ornamental or horticultural proposes, passing a major geographical barrier (Vitousek et al. 1997; Mack et al. 2000; Richardson et al. 2000a). Upon introduction, exotic plants have to colonize and establish in a given habitat. In the colonization phase, exotic species often do not form self-replacing populations and instead rely on repeated introductions for their persistence (Richardson et al. 2000a). The survival of propagules is determined by propagule pressure (also termed introduction effort) and abiotic filters, such as the climate of the new region (Theoharides and Dukes 2007). The more propagules that are introduced in the new area, the greater the chance that an exotic plant will 8 survive during the next steps of invasion (Lockwood et al. 2005; Colautti et al. 2006; but see Nunez et al. 2011). In the establishment or naturalized phase, exotic populations reproduce consistently and are sustained over many life cycles with freely recruited offspring usually close to adult plants (Richardson et al. 2000a). Several processes can create biotic resistance to the establishment and reproduction of the exotic plant (Theoharides and Dukes 2007). For example, exotic populations may be inhibited by competing with native plant species, interacting with enemies (e.g. herbivores, pathogens) or by being unable to establish important mutualistic associations (e.g. mycorrhiza, pollinators) (Richardson et al. 2000b; Levine et al. 2004). Nevertheless, although biotic resistance in the native community significantly reduce establishment of exotic plants, species interactions are unlikely to completely repel invasions (Levine et al. 2004). A lag-phase
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