A Thesis Submitted for the Degree of Doctor of Philosophy at Harper Adams University Copyright and moral rights for this thesis and, where applicable, any accompanying data are retained by the author and/or other copyright owners. A copy can be downloaded for personal non-commercial research or study, without prior permission or charge. This thesis and the accompanying data cannot be reproduced or quoted extensively from without first obtaining permission in writing from the copyright holder/s. The content of the thesis and accompanying research data (where applicable) must not be changed in any way or sold commercially in any format or medium without the formal permission of the copyright holder/s. When referring to this thesis and any accompanying data, full bibliographic details including the author, title, awarding institution and date of the thesis must be given. HARPER ADAMS UNIVERSITY IMPROVING BIOLOGICAL CONTROL IN PROTECTED CROPS Aidan D. Thomas A THESIS SUBMITTED FOR THE DEGREE OF DOCTOR OF PHILOSOPHY NOVEMBER 2020 Harper Adams University Abstract Management of the leafhopper Hauptidia maroccana is inadequate. Despite not being a regular pest in glasshouses, H. maroccana is capable of significant damage. Current conrol methods rely on one chemical agent (Indoxacarb) and a putative predator. In the face of widespread chemical resistance and unreliability of generalist predators, the risk to growers under these conditions is increased. Part of the problem facing growers is that only very basic information about this pest is known, with few studies on the ecological interactions that will be vital for suffifcient control. It is these knowledge gaps that this thesis addresses. A summary literature review introduces the main topics of study and examines the failure of a previously attempted biological control agent. Chapter 2 builds on evidence from similar species and looks at improving trapping of the pest in glasshouses. Non-yellow traps are tested for efficacy and selectivity under laboratory conditions, and indicate that there is scope for improvement in this area. The visual ecology of this pest is examined again in Chapter 4 where the use of LED technology to increase the visual signal of traps is examined. The results of which again indicate that there is more complexity to the visual cues evaluated by H. maroccana than the consensus implies. The importance of plant volatiles to herbivores is well studied. For H. maroccana however, much is not known. Of particular importance is the ability of this pest to detect and respond to the volatile blends released by plants under attack by conspecifics. Growers have reported that H. maroccana forms hotspots within crops. Whether this is due to aggregation or a lack of migration is unknown. Information from experiments here suggests that it is largely due to lack of emigration rather than aggregative behaviours. The use of the generalist predator Macrolophus caliginosus for control of leafhopper is critically examined and tested under laboratory conditions. The overall picture is mixed with predation of leafhopper nymphs approaching levels of consumption seen for other pests, but predation on adults being almost zero. Furthermore, the response of Macrolophus to plant volatiles from infested plants was mixed, which may indicate that under a more complex environment, the ability of this predator to locate H. maroccana is reduced. In the final chapter the project is reviewed as a whole against the objectives and summarised. 1 Acknowledgements The production of this thesis would not have been possible without the funding provided by BBSRC and AHDB. From AHDB, particular thanks are extended to Georgina Key and Joe Martin. Guidance and industry consultation was provided generously by Vitacress Herbs and Cantelo Nurseries. Within those companies support was gratefully received from Simon Budge and Neal Ward respectively. The project took place on Harper Adams University sites and thanks are extended to the staff and fellow students of that place for assistance, advice and companionship. There are people who have contributed greatly to the project and to my own personal wellbeing during this time. These people are too many to list in completion, so to avoid leaving anyone out, the list will remain unstated. Above and beyond all others are my supervisory team, Dr Tom Pope, and Professor Simon Leather. For these gentlemen I was probably one student among others, but for me they were in a league of their own. Finally, the confidence to undertake this work in the first place was hard to find, and harder still to maintain. At any point when my stores were running low, I knew I could turn to my family. To Michelle, Hefin and Bryce, an unpayable debt is owed. But that’s what family is for, right? Per Ardua, mutatio. 2 Table of contents Abstract .......................................................................................................................... 1 Acknowledgements ........................................................................................................ 2 Table of contents ............................................................................................................ 3 List of figures in text ....................................................................................................... 7 List of tables in text ........................................................................................................ 8 1 Literature review...................................................................................................... 9 1.1 Introduction ...................................................................................................... 9 1.2 Insect-Plant interactions ................................................................................. 10 1.2.1 Herbivory ................................................................................................ 10 1.2.2 Plant defences ........................................................................................ 11 1.2.3 Insect responses to plant volatiles ........................................................... 14 1.3 Insect colour vision ......................................................................................... 16 1.4 Leafhoppers ................................................................................................... 18 1.4.1 Hauptidia maroccana .............................................................................. 20 1.4.2 Pest status and controls .......................................................................... 21 1.5 Family Mymaridae .......................................................................................... 22 1.5.1 Genus Anagrus ....................................................................................... 23 1.5.2 Anagrus atomus ...................................................................................... 25 1.5.2.1 Biology ................................................................................................ 25 1.5.2.2 As a biocontrol agent ........................................................................... 25 1.6 Macrolophus spp. ........................................................................................... 27 1.6.1 Taxonomic status .................................................................................... 27 1.6.2 As a biocontrol agent .............................................................................. 28 1.7 Summary ....................................................................................................... 29 1.8 Aims of the thesis ........................................................................................... 30 1.8.1 Objectives ............................................................................................... 30 2 Non-yellow traps for glasshouse leafhopper monitoring; evidence for effective alternative colours ........................................................................................................ 31 2.1 Abstract .......................................................................................................... 31 3 2.2 Introduction .................................................................................................... 31 2.3 Materials and Methods ................................................................................... 33 2.3.1 Leafhopper cultures ................................................................................ 33 2.3.2 Sticky traps ............................................................................................. 33 2.3.3 Custom traps .......................................................................................... 34 2.3.4 Gold traps ............................................................................................... 34 2.4 Colour choice ................................................................................................. 35 2.5 Colour evaluation ........................................................................................... 36 2.6 Statistical tests ............................................................................................... 37 2.7 Results .......................................................................................................... 38 2.8 Discussion ..................................................................................................... 40 2.9 Conclusion ....................................................................................................