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Multitrophic Ecosystem Services of Hoverflies in Strawberry

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Multitrophic Ecosystem Services of Hoverflies in Strawberry Multitrophic ecosystem services of hoverflies in strawberry Thesis submitted for the degree of Doctor of Philosophy (PhD) Royal Holloway University of London February 2020 Dylan James Hodgkiss 2 To all the people (and insects and flowering plants) who made this project possible. And to my family and friends for humouring me through the hard times and the good. 3 Acknowledgements I would like to thank my supervisors Michelle Fountain and Mark Brown for their expert advice, patient support and guidance over the course of this PhD programme. Without your input and feedback, completing this project would quite simply have been impossible for me. I have learned so much from you both. I would also like to thank Beth Clare for her clear explanations of molecular methods, as well as her time and efforts more generally, with the hoverfly gut content analysis chapter. I am also deeply indebted to my colleagues and friends at RHUL and NIAB EMR for their advice, support and good humour: Callum Martin, Alvaro Delgado, Hauke Koch, Adrian Harris, Gemma Baron, Phil Brain, Fabio Manfredini, Beth Shaw, Emily Bailes, Graham Caspell, Arran Folly, Maddie Cannon, Ash Samuelson, David Buss, Judy Bagi, Dilly Rogers, Eva Muiruri, Megan McKerchar, Harry Siviter, Julien Lecourt, Dara Stanley, Roger Payne, Elli Leadbeater, Karen Thurston, Tracey Jeffries, Adam Whitehouse, Rob Prouse, Jean Fitzgerald, Charles Whitfield, Chantelle Jay and Zeus Mateos. Outside of RHUL and NIAB EMR, I am also very grateful to Mark Jitlal for his statistical advice, Roger Morris and Chris Raper for their expert advice with fly identification, and to the eight fruit farmers who granted me access to their strawberry fields for field surveys in 2015: Jackie Clews, James Dearing, Tom Maynard, Richard Pendry, Marion Regan, Greg Secrett, John Tobutt and Andrej Zygora. Among them, I am particularly indebted to Marion Regan, Lance Mansell and Tom Pearson at Hugh Lowe Farms Ltd., as they provided assistance and study sites in both the 2015 and 2016 growing seasons. Without the assistance of the farm managers, the project would not have been nearly as applicable to current commercial strawberry growing conditions. In addition, I am very grateful to RHUL and NIAB EMR for providing me with the funding necessary to carry out this PhD. Last but not least, I would like to express my deepest gratitude to my family and friends for their support throughout the PhD project and in life more generally in these past four and a half years. 4 Abstract Agricultural advances in the last half-century have enabled the production of larger harvests. However, farmland is now at greater risk of pest outbreaks due to losses of genetic diversity within crops rendering crop plants more vulnerable to disease. Moreover, declines in biodiversity in the wider landscape mean that fewer predators of crop pests are present to control pest species. Equally worrying are recent declines in wild and managed insects that are necessary for the pollination of 84% of crop species in Europe. In commercial strawberry (Fragaria x ananassa), aphid damage is estimated to cost growers at least £2.5 million per year in the UK alone. Moreover, in the absence of pollinating insects, strawberry yields would fall by approximately £112.5 million per year. In order to counteract these threats, I investigated the pollinator assemblages in commercial strawberry crops; the pollination effectiveness of aphidophagous hoverflies (Diptera, Syrphidae, Syrphinae); the effectiveness of planting wildflowers within strawberry fields to improve pollination and aphid pest control throughout the crop; and the gut contents of potential pest-controlling hoverflies within strawberry crops. Retail and pick-your-own fruit farms have dynamic pollinator assemblages, including hoverflies. In cage studies, pollination by aphid-eating hoverflies doubled proportions of marketable strawberries when compared to insect-excluded controls. Coriander (Coriandrum sativum) planted within strawberry crops reduced aphid infestations and encouraged aphid predators to lay more eggs near aphid colonies. Furthermore, higher counts of pollinators were recorded in coriander plots, though no differences were found in fruit quality across all treatments. Finally, aphid DNA was recovered from the digestive tracts of hoverfly larvae. Prey DNA detection rates were greater near forget-me-not plots than coriander plots. These findings suggest that hoverflies act as pollinators and pest-controllers in strawberry, and that by integrating coriander within strawberry crops their effects may be enhanced. Future work 5 should focus on how to augment hoverfly populations in strawberry crops to further enhance their efficacy so that pesticide use can be further reduced. 6 Table of Contents Chapter 1: Introduction .................................................................................................. 13 Crop pollination ecology ................................................................................................................... 15 Role of wild pollinators ................................................................................................................. 15 Pollinator behaviours on flowers .................................................................................................. 16 Pollinator diversity ........................................................................................................................ 17 Plant pollinators ............................................................................................................................ 19 Pollinator distributions ................................................................................................................. 20 Hoverflies as pollinators of strawberry ............................................................................................. 21 Strawberry pollinators .................................................................................................................. 22 Integrated Pest Management ........................................................................................................... 23 Aphid predators in strawberry crops ............................................................................................ 25 Documenting trophic interactions ................................................................................................ 26 Habitat management for beneficial insects ...................................................................................... 27 Sown wildflower strips .................................................................................................................. 28 Crop quality ................................................................................................................................... 30 Wildflower selection ..................................................................................................................... 30 References ........................................................................................................................................ 33 Chapter 2: The relative frequency of insect flower visitors in open and polythene-clad strawberry crops ............................................................................................................ 49 Abstract ............................................................................................................................................. 50 Introduction ...................................................................................................................................... 51 Methods ............................................................................................................................................ 53 Data analysis ................................................................................................................................. 56 Results ............................................................................................................................................... 59 Abundance .................................................................................................................................... 59 Diversity ........................................................................................................................................ 60 Species dominance ....................................................................................................................... 61 Discussion.......................................................................................................................................... 66 References ........................................................................................................................................ 70 Chapter 3: Syrphine hoverflies are effective pollinators of commercial strawberry .......... 74 Abstract ............................................................................................................................................. 75 Introduction ...................................................................................................................................... 76 Methods ............................................................................................................................................ 77 Pollination effectiveness of a mix of hoverfly species on strawberry flowers ............................. 77 7 Comparison of pollination effectiveness
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