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Guy Smagghe · Otto Boecking  Bettina Maccagnani · Marika Mänd  Peter G. Kevan Editors Entomovectoring for Precision Biocontrol and Enhanced Pollination of Crops Entomovectoring for Precision Biocontrol and Enhanced Pollination of Crops Guy Smagghe • Otto Boecking Bettina Maccagnani • Marika Mänd Peter G. Kevan Editors Entomovectoring for Precision Biocontrol and Enhanced Pollination of Crops Editors Guy Smagghe Otto Boecking Department of Plants and Crops, Lower Saxony State Office for Consumer Faculty of Bioscience Engineering Protection and Food Safety Ghent University Institute for Apiculture Ghent, Belgium Celle, Germany Bettina Maccagnani Marika Mänd Centro Agricoltura Ambiente “Giorgio Nicoli” Institute of Agricultural and Environmental Crevalcore, Bologna, Italy Sciences Estonian University of Life Sciences Peter G. Kevan Tartu, Estonia School of Environmental Sciences University of Guelph Guelph, ON, Canada ISBN 978-3-030-18916-7 ISBN 978-3-030-18917-4 (eBook) https://doi.org/10.1007/978-3-030-18917-4 © Springer Nature Switzerland AG 2020 This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors, and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, expressed or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. This Springer imprint is published by the registered company Springer Nature Switzerland AG. The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland Preface We are happy to present this unique book, not only because of its novelty and inter- disciplinary content but also because it provides a different view on bees and how we can employ their pollination behaviour for biodiversity and sustainability on our planet. Yes, the major evolutionary diversification of nectaries in late Cretaceous flowers, about 120 million years ago, also signals the beginning of the mutualism between Hymenoptera and angiosperms. Bees are the best example of this mutual- ism. When bees go from flower to flower collecting pollen, they also deposit pollen grains onto the flowers, thereby pollinating them. Indeed, today, the role of insects in pollinating flowers is a commonplace. Pollinating insects by their very activity spread tiny particles (pollen grains) between plants, so why not using them to disseminate other tiny particles, such as microbes, that can serve to suppress plant pests and pathogens? This book is a collection of papers that reviews the concepts and technology that have been developed over the past recent decades and explains some specific applications for crop protection. Chapter 1 introduces some of the newer approaches to using managed pollinators and conserving wild pollinators in agricultural settings. The diversification of approaches to using managed pollination and the roles of wild pollinators in agri- culturally dominated landscapes set the stage for the scope of using pollinators for other beneficial roles, including pest management. Chapter 2 places the concepts of “bee vectoring technology” (BVT) as “entomovectoring” or “apivectoring” into the framework of “ecological intensification”, a newly coined concept of using and managing biodiversity and ecosystem complexity in agriculture. It also explores, with comprehensive thoroughness, the scope of apivectoring science with respect to the kinds of pollinators that can be used and the kinds of biocontrol agents that can be disseminated by pollinators for suppression of crop pathogens and pest arthro- pods. It recognizes the potential of using technology in protecting managed pollina- tors from diseases and parasites and also introduces the multifactorial issues of using the technology in responsible ways from assessing the agents, the diluents, the delivery systems and the possible consequences in the human food chain and envi- ronment as they pertain to practical application for food security. Of course, there are regulatory issues to be considered, and they are reviewed in useful detail in v vi Preface Chap. 14. Moreover, it also recognizes that arthropods used in biocontrol pro- grammes could serve as vectors of other beneficial microbes. Chapters 3 and 15 introduce the value and service of bees as pollinators of crops. Chapter 15 focuses on commercially available managed bumblebees. As such, both chapters serve to cement the links between Chaps. 1 and 2. Chapter 4 delves deeper into pollinator diversity and focuses on the use and potential of the diversity of solitary bees that are used for crop pollination. As such, Chap. 4 is an important segue, especially for Chap. 6 which explores the diversity of dispensing devices that can be used on the wide diversity of managed pollinator domiciles. These range from the familiar beehive through to domiciles for bumble- bees and to the challenges posed by various artificially produced nesting arrange- ments for solitary bees. Chapter 5, as a specific example, explores the successful use of bumblebees in open field conditions for entomovectoring fungal disease sup- pressing agents for strawberry crop protection. This chapter is the first in the book that addresses specific examples. Chapter 7 zeroes in on the successful application of the technology in greenhouse vegetable and fruit production. Chapter 8 presents a case study for the utility of the technology in setting the stage for addressing apple storage rot problems at the time of apple pollination. Chapter 9 suggests that an invasive species of pestiferous fruit fly could be suppressed by using pollinators as entomovectors of entomopathogenic microbes. This chapter further expands the potential of entomovectoring against agricultural insect pests as reviewed in Chap. 2. Coffee is globally the most traded and valuable agricultural commodity and benefits from the activities of managed and wild pollinators. Chapter 10 addresses the poten- tial for the use of pollinator entomovectoring by Africanized (“killer” or “assassin”) honeybees for the suppression of several coffee diseases and insect pests on the basis of practical research experience in Brazil, Mexico and Ecuador. Chapter 11 explains how bumblebees have been used successfully in Serbia (and in Canada) to suppress sunflower head rot, potentially a very valuable technology for high value- added hybrid seed and confection seed production. In Chap. 12, a comprehensive study from Colombia is reviewed. It explains the successes achieved by using Africanized honeybees as vectors of a biological control agent against fungus dis- eases on commercially operating strawberry farms. The work is explained from the conceptual base through to the economic advantages to farmers. In Chap. 13, it is recognized that certain pest insects spread crop diseases but that they could also be used to spread microbes that fight the very diseases the pest insects also carry. Throughout the book, the authors have made specific mention of the funding agencies that have supported their research and development. Important was the ERA-Net named “Coordination of European Transnational Research in Organic Food and Farming Systems” with the “Bicopoll” project. Special and general thanks are extended to the “International Commission for Plant-Pollinator Relationships” (ICP-PR) and the “International Union of Biological Sciences” (IUBS) for their overarching support on a global level and especially for the sessions at the “XI International Symposium on Pollination” in Berlin (2018) and sponsoring the “International Advanced Course on Using Managed Pollinators for Dissemination Preface vii of Biological Control Agents for Suppression of Insect, Fungal & Other Pests of Crops” held in Belgrade, Serbia, 6–10 May 2019. Thank you for sharing with us this introduction to a complex, yet easily acces- sible subject of great fascination! This book is intended for people with interest in bees, nature, agriculture and novel technologies to students, teachers, experts and the common man/woman worldwide. Guelph, ON, Canada Peter G. Kevan Ghent, Belgium Guy Smagghe 17 June 2020 Contents Agroecosystem Design Supports the Activity of Pollinator Networks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 Bettina Maccagnani, Eve Veromann, Roberto Ferrari, Luca Boriani, and Otto Boecking Ecological Intensification: Managing Biocomplexity and Biodiversity in Agriculture Through Pollinators, Pollination and Deploying Biocontrol Agents against Crop and Pollinator Diseases, Pests and Parasites . . . . . . . . . . . . . . . . . . . 19 Peter G. Kevan, Les Shipp, and Guy Smagghe Bee Pollination of Crops: A Natural and Cost-Free Ecological Service . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 53 Otto Boecking and Eve Veromann Solitary Bees As Pollinators . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63 Bettina Maccagnani and Fabio Sgolastra Bumble Bees and Entomovectoring in Open Field Conditions . . . . . . . . . 81 Marika Mänd, Reet Karise, and Guy Smagghe Dispensers for Entomovectoring: For Every Bee a Different Type? . . . . . 95 Bettina Maccagnani, Matti Pisman, and Guy Smagghe Case Studies on Entomovectoring in the Greenhouse and Open Field . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 123 Guy Smagghe A Case Study: Use of Prestop® Mix Biofungicide in Entomovectoring on Apple Against Storage Rot Diseases . . . . . . . . . . . 137 Marja-Leena Lahdenperä ix x Contents Threat of Drosophila suzukii as an Invasive Species and the Potential of Entomovectoring . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 147 Clauvis N. T. Taning and Guy Smagghe The Potential of Bee Vectoring on Coffee in Brazil . . . . . . . . . . . . . . . . . . . 165 Juliana Macedo, Blandina Viana, Breno Freitas, Adriana Medeiros, Peter G. Kevan, and Carlos H. Vergara Using Bumblebees (Bombus terrestris) as Bioagent Vectors to Control Sclerotinia Head Rot on Sunflower in Serbia . . . . . . . . . . . . . . 183 Sreten Terzić, Boško Dedić, Sonja Tančić Živanov, Željko Milovac, Filip Franeta, Miroslav Zorić, Ljubiša Stanisavljević, and Peter G. Kevan Advances in the Implementation of Apivectoring Technology in Colombia: Strawberry Case (Fragaria x ananassa) . . . . . . . . . . . . . . . . 201 Saira Espinosa, Judith Figueroa, Peter G. Kevan, Carlos Baéz, Victor Solarte, Guy Smagghe, and Andres Sánchez Making a Pest Beneficial: Fungus Gnats [Bradysia impatiens (Diptera: Sciaridea)] as Potential Vectors of Microbial Control Agents to Suppress Pathogens they Also Spread . . . . . . . . . . . . . . . . . . . . . 239 Jean-Pierre Kapongo, Peter G. Kevan, Les Shipp, and Hisatomo Taki Regulatory Processes Surrounding the Risk Assessment of Microbial Pesticides for Pollinators . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 251 Emily A. McVey and Jacoba Wassenberg Flying Doctors for a Better Quality in Fruit Production . . . . . . . . . . . . . . 263 Maria I. Pozo, Julien Vendeville, Veerle Mommaerts, and Felix Wackers Agroecosystem Design Supports the Activity of Pollinator Networks Bettina Maccagnani, Eve Veromann, Roberto Ferrari, Luca Boriani, and Otto Boecking 1 Some Principle Needs of Honey Bees and Wild Bees Throughout Europe, farmland comprises the major part of land use, namely 48% of the land is agricultural land (European Commission 2016). Traditionally, agricul- tural land use and biodiversity have been thought to be at opposite extremes, but arable land can be heterogeneous also. Intensively cultivated areas should ideally interchange with non-cultivated and semi-natural elements (green-veins) such as field margins, set asides, woods, hedgerows, brooks, ditches etc. and provide many suitable habitats and resources for the wide range of species common in agricultural landscapes (Bennett et al. 2006; Diekötter et al. 2008; Meek et al. 2002; Tscharntke et al. 2008). These resources include mating and overwintering habitats, food and alternative host resources, shelters and protection from agro-technical activities (Holland et al. 2016). Certainly, the majority of arthropods in agricultural land- scapes are reliant on the existence of semi-natural habitats. Thus, semi-natural habi- tats have the potential to provide and/or support several ecosystem services that are Bettina Maccagnani - Scientific advisor for the Automobili Lamborghini project “Environmental Biomonitoring with Honey Bees: Science and Education” B. Maccagnani (*) · R. Ferrari (*) · L. Boriani Centro Agricoltura Ambiente “Giorgio Nicoli”, Crevalcore, Bologna, Italy e-mail: [email protected]; [email protected]; [email protected] E. Veromann Department Plant Protection, Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences, Tartu, Estonia e-mail: [email protected] O. Boecking Lower Saxony State Office for Consumer Protection and Food Safety, Institute for Apiculture, Celle, Germany e-mail: [email protected] © Springer Nature Switzerland AG 2020 1 G. Smagghe et al. (eds.), Entomovectoring for Precision Biocontrol and Enhanced Pollination of Crops, https://doi.org/10.1007/978-3-030-18917-4_1

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