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Generalist Predators, Food Web Complexities and Biological Pest Control in Greenhouse Crops Messelink, G.J UvA-DARE (Digital Academic Repository) Generalist predators, food web complexities and biological pest control in greenhouse crops Messelink, G.J. Link to publication Citation for published version (APA): Messelink, G. J. (2012). Generalist predators, food web complexities and biological pest control in greenhouse crops General rights It is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), other than for strictly personal, individual use, unless the work is under an open content license (like Creative Commons). Disclaimer/Complaints regulations If you believe that digital publication of certain material infringes any of your rights or (privacy) interests, please let the Library know, stating your reasons. In case of a legitimate complaint, the Library will make the material inaccessible and/or remove it from the website. Please Ask the Library: http://uba.uva.nl/en/contact, or a letter to: Library of the University of Amsterdam, Secretariat, Singel 425, 1012 WP Amsterdam, The Netherlands. You will be contacted as soon as possible. UvA-DARE is a service provided by the library of the University of Amsterdam (http://dare.uva.nl) Download date: 02 Oct 2017 Gerben-omslag.qxd 16-4-2012 12:13 Page 1 Gerben Messelink Generalist predators, food web complexities and biological pest control in greenhouse crops in greenhouse food web complexities and biological pest control Generalist predators, Generalist predators, food web complexities and biological pest control in greenhouse crops 2012 Gerben Messelink Gerben-Voorwerk.qxd 13-4-2012 12:38 Page 1 Generalist predators, food web complexities and biological pest control in greenhouse crops Gerben-Voorwerk.qxd 13-4-2012 12:38 Page 2 G.J. Messelink, 2012. Generalist predators, food web complexities and biological pest control in greenhouse crops PhD thesis, University of Amsterdam, The Netherlands Publication of this thesis was financially supported by Koppert Biological Systems (www.koppert.nl) ISBN: 978 94 91407 04 8 Lay-out: Jan Bruin (www.bred.nl) Gerben-Voorwerk.qxd 13-4-2012 12:38 Page 3 Generalist predators, food web complexities and biological pest control in greenhouse crops ACADEMISCH PROEFSCHRIFT ter verkrijging van de graad van doctor aan de Universiteit van Amsterdam op gezag van de Rector Magnificus prof. dr. D.C. van den Boom ten overstaan van een door het college voor promoties ingestelde commissie, in het openbaar te verdedigen in de Agnietenkapel op dinsdag 5 juni 2012, te 14:00 uur door Gerben Jaap Messelink geboren te Doornspijk Gerben-Voorwerk.qxd 13-4-2012 12:38 Page 4 Promotiecommissie Promotor: Prof. dr. M.W. Sabelis Co-promotor: Dr. A.R.M. Janssen Overige leden: Prof. dr. W. Admiraal Prof. dr. J. Brodeur Prof. dr. T. Hance Prof. dr. S.B.J. Menken Dr. E. Palevsky Dr. P.C.J. van Rijn Dr. M. Venzon Faculteit der Natuurwetenschappen, Wiskunde en Informatica Gerben-Voorwerk.qxd 13-4-2012 12:38 Page 5 Contents 6 Author addresses 7 1 Introduction 33 2 Evaluation of phytoseiid predators for control of western flower thrips on greenhouse cucumber 47 3 Biological control of thrips and whiteflies by a shared predator: Two pests are better than one 63 4 Positive and negative indirect interactions between prey sharing a predator population 77 5 Pest species diversity enhances control of spider mites and whiteflies by a generalist phytoseiid predator 95 6 Hyperpredation by generalist predatory mites disrupts biological control of aphids by the aphidophagous gall midge Aphidoletes aphidimyza 111 7 Biological control of aphids in the presence of thrips and their enemies 129 8 General discussion 137 Summary 141 Samenvatting 145 Curriculum vitae 145 Publications 147 Dankwoord Gerben-Voorwerk.qxd 13-4-2012 12:38 Page 6 Author addresses Institute for Biodiversity and Ecosystem Dynamics, Section Population Biology, Science Park 904, 1098 XH Amsterdam, The Netherlands Janssen, Arne van Maanen, Roos Sabelis, Maurice W. Wageningen UR Greenhouse Horticulture, PO Box 20, 2265 ZG Bleiswijk, The Netherlands Bloemhard, Chantal M.J. Cortes, Juan A. van Holstein-Saj, Renata Messelink, Gerben J. Ramakers, Pierre M.J. van Steenpaal, Sebastiaan E.F. Gerben-chap1.qxd 13-4-2012 12:37 Page 7 1 Introduction iological control of pest species has traditionally mainly focused on specific nat- Bural enemies for each pest (Huffaker & Messenger, 1976; Hokkanen & Pimentel, 1984; van Lenteren & Woets, 1988; Hoy, 1994). However, pest-enemy interactions are often embedded in rich communities of multiple interacting pests and natural enemies (e.g., Helle & Sabelis, 1985b; Minks & Harrewijn, 1989; Sabelis, 1992), and the interactions among these species affect the efficacy of biological control (Sih et al., 1985; Janssen et al., 1998; Prasad & Snyder, 2006; Evans, 2008). The effect of interactions among various species of predators and parasitoids on biological con- trol of a shared pest species has received ample attention (see Letourneau et al., 2009), showing that it can range from larger to smaller than the effect of each enemy species separately (Rosenheim et al., 1995, 1998; Losey & Denno, 1998; Colfer & Rosenheim, 2001; Venzon et al., 2001; Cardinale et al., 2003; Snyder & Ives, 2001, 2003; Finke & Denno, 2004; Cakmak et al., 2009). However, it is not only predator diversity, but also the diversity of herbivorous prey that may affect the suppression of a particular pest species through competition, or indirect interactions mediated by host plant or shared predators (Holt, 1977; Karban & Carey, 1984). Hence, designing effective biological control programs for more than one pest species requires an understanding of all interactions occurring among species within biocontrol commu- nities, not just those among pests and their natural enemies or among different species of natural enemies. Greenhouse crops are often considered as simple ecosystems with low biodiver- sity (Enkegaard & Brødsgaard, 2006). Especially modern greenhouses appear sterile compared to outdoor crops, as plants are grown on hydroponic systems in green- houses that are isolated from the environment because of modern energy saving techniques (Bakker, 2008). However, the general experience is that infestations by several small pest species cannot be avoided, and the release of natural enemies against these pests adds to the diversity (van Lenteren et al., 2000; Cock et al., 2010). Thus, apparently ‘clean’ greenhouse crops often accommodate complex arti- ficial communities of multiple pests and natural enemies. Furthermore, there seems to be a tendency that the diversity of these communities increased during the last decades (Enkegaard & Brødsgaard, 2006). One reason for this increased diversity is the invasion of exotic pest species (global trade, global warming) (Roques et al., 2009). Second, more species than before develop into pests as a result of the reduced use of pesticides and the use of more selective pesticides (van der Blom et 7 Gerben-chap1.qxd 13-4-2012 12:37 Page 8 CHAPTER 1 | INTRODUCTION al., 2009; Pijnakker & Leman, 2011). A third reason is that biological control programs increasingly include generalist predators (Gerson & Weintraub, 2007; Sabelis et al., 2008), and such generalists potentially interfere more with other natural enemies than specialists. Thus, recent developments further increase food web complexity in bio- logical control programs and emphasize that such complexities need to be consid- ered when designing biological control programs. The advantage of greenhouse crops is that they offer the unique possibility to create the desired communities of natural enemies by choosing and releasing natural enemies out of the many species that are commercially available nowadays (van Lenteren, 2000; Enkegaard & Brødsgaard, 2006). In other words, biodiversity can be created and manipulated to maximise sustainable pest control. At the same time, such systems can be used to study the manipulation of biodiversity on the dynamics of communities of plant- inhabiting arthropods under relatively controlled conditions and at larger spatial scales than can usually be realized with communities under field conditions. Here, I review the ecological theory relevant to interactions in food webs occur- ring within arthropod communities and I discuss the possible implications for biolog- ical control in greenhouses. The subsequent chapters contain studies that focus on the most important greenhouse pests, namely aphids, thrips, spider mites and white- flies, as well as their natural enemies (see BOXES with pest descriptions). Food web theory and effects in greenhouse crops Consumption (i.e., herbivory, predation and parasitism) and competition are consid- ered the two most important interactions determining the structure of communities (Chase et al., 2002). Within communities of natural enemies and pests, species may interact through exploitative competition, through predation and parasitism (includ- ing omnivory, intraguild predation and hyperpredation or hyperparasitism), but also through apparent competition or apparent mutualism via shared natural enemies (FIGURE 1.1). Besides these density-mediated interactions, species interactions can be modified through trait changes of the interacting individuals (which includes changes in behaviour and induced plant responses). In the following, I summarize the current theory on these interactions and their relevance to biological control. Exploitative competition and induced plant responses Herbivores
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