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Brevicoryne Brassicae) A University of Sussex DPhil thesis Available online via Sussex Research Online: http://sro.sussex.ac.uk/ This thesis is protected by copyright which belongs to the author. This thesis cannot be reproduced or quoted extensively from without first obtaining permission in writing from the Author The content must not be changed in any way or sold commercially in any format or medium without the formal permission of the Author When referring to this work, full bibliographic details including the author, title, awarding institution and date of the thesis must be given Please visit Sussex Research Online for more information and further details Plants signalling to herbivores: is there a link between chemical defence and visual cues? Rosie Foster Submitted for the degree of Doctor of Philosophy University of Sussex November 2012 2 Plants signalling to herbivores: is there a link between chemical defence and visual cues? Summary The use of visual cues by insect herbivores is likely to be an important component of plant- herbivore interactions in the wild, yet has until recently received little attention from researchers. In the last decade, however, interest in this topic has intensified following Hamilton & Brown’s (2001) autumn colouration hypothesis, which proposes that the intensity of colouration of trees at autumn time is a signal of their defensive commitment to potential herbivores. This idea remains controversial and to date robust empirical data linking colouration with chemical defence and herbivory have been lacking. This thesis begins with a meta-analysis, in which I synthesize and analyse previously published data to determine the evidence for the use of host plant colouration by herbivores. I then move to explore the relationship between chemical defences and colouration in a classic plant-herbivore system: the wild cabbage (Brassica oleracea) and its herbivores the cabbage white butterfly (Pieris rapae) and the cabbage aphid (Brevicoryne brassicae). Both species have colour vision, and I use spectral sensitivity data to model the colour of the host ‘through the eyes’ of the herbivores. First, I present data from a field study of wild cabbage populations showing significant relationships between herbivory, plant colouration and levels of glucosinolates defensive compounds. These results suggest that plant colouration could be used by herbivores to gain information about plant chemical defence. I then show colouration has a fixed genetic component in a common garden experiment; a necessary requirement for evolution of a colour signal. I explore the use of colouration in host choice by herbivores in more detail in a series of behavioural experiments. I show that cabbage aphids do not use leaf brightness as a cue when selecting among plants, but they do respond to different leaf colours. I also show that cabbage white butterflies do not choose hosts based on particular colour cues, even though this colouration potentially provides important information about host defence levels, which are shown to impact upon offspring fitness. Together, these results provide a clear demonstration of a link between plant chemistry and colouration in the wild cabbage system. However, the data presented in this thesis indicate that the use of colouration as a guide to host defence is limited, and I conclude by discussing possible reasons why this might be the case. 3 Declaration The model of Pieris rapae and Brevicoryne brassicae spectral sensitivities and the software to run the models were designed by Dr Lucas Wilkins at the University of Sussex. The common garden was established by Dr Dave Hodgson at the University of Exeter. CN samples collected in the field surveys were run by Debbie Coldwell at the University of York. However, the analysis and interpretations drawn from the data in all chapters are my own. I certify that, with the above qualifications, the work carried out in this thesis is entirely my own, and that any help by other individuals with data collection and analysis is fully acknowledged. In addition, I certify that this thesis has not been, and will not be, submitted in whole or in part to another university for the award of any other degree. Signature: Rosie Foster 4 Acknowledgements First, I would like to thank my supervisors Sue Hartley and Daniel Osorio for giving me the opportunity to do this PhD. I am grateful to the BBSRC for funding this project. I would like to dedicate this thesis to three people, without whom it would never have been possible. First, to Lucas Wilkins for his very patient teaching and state-of-the-art modelling. Second, to Lynne Robinson, my chemistry queen and great friend. Third, to my hero, Jonathan Green, for his advice, proof reading and immense support. Thank you, you guys are the best! I could write a thesis of thanks for all the people who have helped me along the way. Firstly, to my office buddies and lunch buddies who have kept me going with tea, laughs, badminton, hugs and advice: Dave Fisher-Barham, Eric Lucas, Stephanie Murphy, Jon Carruthers, Jasper van Heusden, Claudia Harflett, Lauren Holt, Citalli Morelos-Juarez, Claire Sanderson, Paul Davison, Tanya Pennell, Romain Blanc-Matthieu, Eduardo Medina-Barcenas, Alan Hodgkinson, Roger Schuerch, Hannah Pratt, Naomi Ewald, Elli Leadbeater, Mike Clease, Sam Jones, Keith Cornelius, Juul Othuis and Tomer Czaczkes. Extra thanks go to Jeremy Field whom I have often asked for stats advice, Adam Eyre-Walker, who I have often dropped in on for advice, and to Alan Stewart for insect advice. Thank you to Tim, my uncle, for several cheery discussions and for reading things through. I appreciate all your friendships so much. A number of people kindly gave their time to help with data collection, data analysis and useful commons on drafts of my chapters for which I am extremely grateful - thank you very much. Chapter 2. Adam Eyre Walker provided useful comments on the earlier draft of this chapter. Chapter 3 – Naomi Ewald gave useful statistical advice when planning the field survey. David Streeter advised on where to find wild B. oleracea populations in Dover. Erika Newton advised on cabbage sites and gave essential help on the phone when I couldn’t find them! She also provided me with the protocol for glucosinolate extraction. James Bullock introduced me to the Dorset sites. A massive thanks to Ailsa Lambert who endured three whole days of cabbaging in Dorset, although the odd pint of Guinness did help us along the way! Liz Hill gave very useful chemistry advice and allowed me use her lab space and ball mill. Jeremy Field allowed me to use his hot water bath. Camilla Liscio also provided very useful chemistry advice, especially with the use of standards. A huge thank you to Julia Horwood for her help, 5 especially with making up chemicals and designing the collection of leaf samples in the field. Lynne Robinson also gave invaluable chemistry advice. Holger Danner from the Radboud University of Nijmegen (Netherlands), provided me with the protocol for HPLC analysis of glucosinolates. Ali Abdul-Sada allowed me to use his HPLC machine, provided very useful advice and fixed the machine when it was not happy! He also ran the samples on the Mass Spec for me and advised with the interpretation of the output. Youssra Al-Hilaly taught me how to use the HPLC machine. Debbie Coldwell ran the samples on the CN machine and prepared the standards. Roger Schuerch assisted with the production of some plots in R, and advised on the analysis of within plant colour variation. Chapter 4 – Dave Hodgson allowed me to use his common garden experiment. His undergraduate students “cabbage patch kids!” helped with re-potting. Jonathan Green helped with taking the colour measurements. Nicole Goodey helped me to measure the size of the plants and conducted the herbivore survey. Jeremy Field provided useful comments on an earlier draft of this chapter. Chapter 5 – The BCH team at Rothamsted Research met with me to give me advice with my aphid experiment, and thanks go especially to Christine Woodcock who allowed me to take some aphids and plants. Thomas Doring met with me to provide advice about the aphids and their vision. Tomer Czaczkes provided advice for the design of the aphid experimental set-up and Mike Clease also gave lots of useful advice. Mike also came to help purchase Brussel sprout plants and very kindly helped to water my plants. Ailsa Lambert helped with inoculating plants with aphids and counting them after the experiment. Lauren Holt helped to re-inoculate plants with the aphids. Martyn Stenning and Andy Black provided technical support. Paul Graham allowed me to use his lab space. My grandma, mum, Sue Foster, and sister, Caroline Foster, provided the production line of muslin bag making. Adam Eyre Walker advised on the analysis of aphid choice with chromatic cues. Patrick Green provided very useful comments on an early draft of this chapter. Chapter 6 - My sister, Annie Foster, helped to re-pot the 400 plants in record time. Thanks to my parents who spent an afternoon with butterfly nets in an allotment catching my starting population. Tanya Pennell and Paul Davison helped to catch other populations. I would like to send an extra thank you to my family for their interest and encouragement with my DPhil “in cabbages!” Most importantly, a thank you bigger than I can express goes to 6 Jonathan. I am deeply indebted to his unwavering support, kindness and generosity. To all, thank you again and good luck with all your endeavours! 7 Table of contents Chapter One. Introduction .......................................................................................................... 11 1.1. Plant herbivore interactions ............................................................................................ 12 1.1.1. Plant defence ............................................................................................................ 12 1.1.2. Host selection ............................................................................................................ 15 1.2 Autumn colouration .......................................................................................................... 17 1.2.1.
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