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Thesis, University of Amsterdam, the Netherlands UvA-DARE (Digital Academic Repository) What lies beneath? Linking litter and canopy food webs to protect ornamental crops Muñoz Cárdenas, K.A. Publication date 2017 Document Version Final published version License Other Link to publication Citation for published version (APA): Muñoz Cárdenas, K. A. (2017). What lies beneath? Linking litter and canopy food webs to protect ornamental 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: https://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 (https://dare.uva.nl) Download date:26 Sep 2021 What lies beneath? Linking litter and canopy food webs to protect ornamental crops What lies beneath? Linking litter and canopy food webs to protect ornamental crops Karen A. Muñoz Cárdenas What lies beneath? Linking litter and canopy food webs to protect ornamental crops ACADEMISCH PROEFSCHRIFT ter verkrijging van de graad van doctor aan de Universiteit van Amsterdam op gezag van de Rector Magnificus Prof. dr. ir. K.I.J. Maex ten overstaan van een door het College voor Promoties ingestelde commissie, in het openbaar te verdedigen in de Aula der Universiteit op woensdag 21 juni 2017, te 11:00 uur door Karen Andrea Muñoz Cárdenas K.A. Muñoz Cárdenas, 2017. What lies beneath? Linking litter and canopy food webs to protect geboren te Bogotá, Colombia ornamental 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 47 5 Cover design: Jan van Arkel (IBED) Thesis lay-out: Jan Bruin (www.bred.nl) Promotiecommissie Contents Promotor 6 Author addresses Prof. Dr. P.C. de Ruiter Universiteit van Amsterdam 7 0 Copromotor General introduction Dr. A.R.M. Janssen Universiteit van Amsterdam Overige leden 27 1 Prof. Dr. E.T. Kiers Vrije Universiteit Amsterdam Generalist red velvet mite predator (Balaustium leanderi) performs Prof. Dr. S.B.J. Menken Universiteit van Amsterdam better on a mixed diet Dr. W.E. Morriën Universiteit van Amsterdam 57 Prof. Dr. W.H. van der Putten Wageningen Universiteit 2 Dr. I.M. Smallegange Universiteit van Amsterdam Supplying high-quality alternative prey in the litter increases control Prof. Dr. F.L. Wäckers Lancaster University, UK of an above-ground plant pest by a generalist predator 81 Faculteit der Natuurwetenschappen, Wiskunde en Informatica 3 Alternative food for litter-inhabiting predators decreases pest densities and above-ground plant damage 101 4 Single and combined predator releases with alternative food increases thrips control in an ornamental crop 123 General discussion 132 Author contributions and project funding 133 Summary 137 Samenvatting 141 Curriculum vitae and publications 143 Acknowledgements 0 General introduction Author addresses Department of Population Biology, Institute for Biodiversity and Ecosystem Dynamics, University of This thesis is on biological control, which is the use of live organisms to keep agri- Amsterdam, Science Park 904, 1098 XH Amsterdam, The Netherlands cultural pests, diseases, and weeds at low levels (DeBach 1974). Since ancient Duarte, Marcus V. A.; Ersin, Firdevs; Janssen, Arne; Muñoz-Cárdenas, Karen; Sabelis, Maurice W. times, humans have utilized natural enemies to control pests. Thousands of years ago, ants and spiders were used in China to protect tree crops from herbivore pests. Programa de Biología Aplicada, Facultad de Ciencias Básicas, Universidad Militar Nueva Granada, Km 3 via Cajicá-Zipaquirá, Cajicá, Colombia Through history, there have been many successful programs of biological control Muñoz-Cárdenas, Karen; Cantor, R. Fernando; Rodríguez, C. Daniel worldwide (Van Driesche & Bellows 1996). Only after World War II, the use of chem- ical pesticides replaced natural and biological control (Bale et al. 2008). Thanks to the Centro de Biosistemas, Universidad Jorge Tadeo Lozano, Carretera Central del Norte, 3 kms al norte del pressure of consumers for pesticide-free agricultural products, biological control has puente de La Caro, Chía, Cundinamarca, Colombia again become a key component for pest control (Calvo et al. 2015). Moreover, grow- Fuentes, Luz Stella ers have actively chosen to use biological control because of the advent of pests resistant to chemical pesticides (Bolckmans 1999). Nowadays, biological control is a Department of Plant Protection, Faculty of Agriculture, University of Ege, 35100 Bornova, Izmir, Turkey viable alternative to chemical pest control. Ersin, Firdevs Currently, there is a wide range of biological control agents commercially avail- able, such as parasitoids, entomopathogens and predators. Parasitoids are wasps Biobest Belgium, Ilse Velden 18, 2260 Westerlo, Belgium and flies that deposit their eggs in or on their host. In the case of biological control, Pijnakker, Juliette these hosts are insect pests. The developing parasitoid larva feeds on the Wageningen UR Greenhouse Horticulture, PO Box 20, 2265 ZG Bleiswijk, The Netherlands haemolymph of the host, affecting the host’s development and finally causing its Leman, Ada; Messelink, Gerben J.; Pijnakker, Juliette dead (Godfray 1994). Entomopathogens used in biological control are viruses, fungi, bacteria, and protozoa that cause diseases in insects and mites (Federici 1999). Koppert Biological Systems, PO Box 155, 2650 AD Berkel en Rodenrijs, The Netherlands These pathogens infect arthropod pests, eventually killing them (Federici 1999). In Hoogerbrugge, Hans; van Houten, Yvonne this thesis I focus on arthropod natural enemies. Arthropod predators living on crop plants can be either specialist, attacking one or a few closely related pest species, Department of Agricultural Development, Laboratory of Agricultural Entomology and Zoology, Democritus or generalist, attacking a wider range of pests. In the past, biological pest control has University of Thrace, Pantazidou 193, 68 200 Orestiada, Greece focused on the use of one or a few specialist natural enemies for each pest species Pappas, Maria L. (Huffaker & Messenger 1976; Hokkanen & Pimentel 1984; van Lenteren & Woets Department of Entomology, Federal University of Viçosa, Viçosa, Minas Gerais, Brazil 1988; Hoy 1994) because the use of generalist predators was judged to be more Duarte, Marcus V. A. risky as they could also target non-pest species (van Lenteren et al. 2003). Moreover, they were considered inferior enemies to parasitoids because their dynamics would Mitox Consultants/Eurofins, Science Park 406, 1098 XH Amsterdam, The Netherlands not be synchronized with the pest, and because they usually do not have a high Faraji, Farid potential for increase (Murdoch et al. 1985). Nevertheless, generalist predators are widely used in biological control nowadays (Symondson et al. 2002). These preda- Laboratorio de Acarología, Departamento de Entomología y Acarología, ESALQ, Univer si dade de São Paulo, tors have the advantage of being able to feed on food sources different than the tar- Piracicaba, Av. Pádua Dias, 11, São Paulo, Brazil get pest. Thus, they are able to establish in the crop before pest invasions Rueda-Ramirez, Diana (Symondson et al. 2002). The introduction of different natural enemies (either gener- 7 CHAPTER 0 | GENERAL INTRODUCTION GENERAL INTRODUCTION | CHAPTER 0 alists, specialists, or both) results in artificial communities in the crops, and the mem- with all pests and predators present in a crop. In this thesis, I studied the combined bers of those communities can interact in complex ways. Not only do natural ene- effect of multiple predator species on the control of one pest species. mies interact with the target pest, but interactions also occur among different pest species and among natural enemy species (Helle & Sabelis 1985; Minks & Harrewijn Interactions among pest organisms 1989; Sabelis 1992), and these interactions can affect biological control (Sih et al. Herbivorous prey might compete among each other for plant resources, but this only 1985; Janssen et al. 1998; Prasad & Snyder 2004; Evans 2008). A lot of attention has occurs at high pest densities, which is undesirable in agriculture because it would been given to the effects of interactions among various species of natural enemies. certainly result in exceeding the economic damage threshold. For this reason, I will Compared to the effect of each enemy species separately, the effect of such interac- not further discuss resource competition among herbivores in this thesis. Herbivores tions can be negative, neutral or positive for biological control (Rosenheim et al. can also affect each other indirectly by inducing plant defence responses: the attack 1995; Losey & Denno 1998; Rosenheim 1998; Colfer & Rosenheim 2001; Snyder & of an herbivore triggers a plant defensive response that does not only affect the
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