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PDF/?Uri=CELEX:32014R1143&From=EN A University of Sussex PhD 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 i Ecological interactions of an invading insect: the planthopper Prokelisia marginata Claire Harkin Submitted for the degree of Doctor of Philosophy University of Sussex July 2016 iii For Indigo My greatest challenge and my deepest joy. “It seems to me that the natural world is the greatest source of excitement; the greatest source of visual beauty; the greatest source of intellectual interest. It is the greatest source of so much in life that makes life worth living.” Sir David Attenborough iv University of Sussex Claire Harkin, Doctor of Philosophy Ecological interactions of an invading insect: the planthopper Prokelisia marginata Summary The planthopper Prokelisia marginata Van Duzee is native to the eastern coast of North America, where densities on its foodplant, the cordgrass Spartina alterniflora, frequently exceed several thousand per square metre. It has little impact on its host plant in its native range where both species have co-evolved, however where the plant has been introduced and has had no recent exposure to the planthopper, it has a major impact and has been trialled as a biological control agent. P. marginata was recorded for the first time in Britain in 2008, where it feeds primarily on the widespread S. anglica, itself listed as one of the world’s 100 worst invasive species, as well as its progenitors S. alterniflora, S. maritima and S. x townsendii. P. marginata appears to be in the successful early stages of invasion in Britain, having already spread extensively. Significantly outnumbering all other saltmarsh arthropod groups, it is benefitting from partial natural enemy escape, and a high proportion of macropterous individuals in all populations indicates strong potential for further range expansion. Utilising both glasshouse and field manipulations, I show that exposure to P. marginata has a significant negative impact on S. anglica, an interaction which has the potential to destabilise Britain’s important saltmarsh habitat. I suggest that the four host species that occur in Britain represent a ‘gradient’ of shared co-evolutionary history with the planthopper. I show that, whilst all species are negatively impacted by P. marginata exposure, S. alterniflora, the species with which it shares the longest co- evolutionary history, is the least affected. I further show that P. marginata exhibits a preference for, and performs better on, S. anglica. As S. anglica is by far the most abundant of the four Spartina species in Britain, these results suggest P. marginata may be undergoing rapid evolution in its new range to take advantage of this widespread host species, thereby maximising its potential for further range expansion. v Acknowledgements My thanks are due first to my supervisor, Dr Alan Stewart, for his knowledgeable guidance and unwavering support, both professionally and personally, throughout the course of my studies. Admirably calm in the face of the nightmare combination of his student’s PhD stress and pregnancy hormones, he has both reassured me that I am a capable scientist, and inspired and challenged me to be a better one. Thanks also to my co-supervisor Professor Jeremy Field. A number of people have waded through mud during the course of my research to help dig up plants and suck up bugs: Tanya Pennell, Chris Accleton, Tom Wood, Essayas (Ash) Abraha, Alan Stewart, Will Harkin. Particular thanks go to Martin Rand, South Hampshire BSBI Recorder, and David Streeter, all-round plant genius, for their expert guidance in locating and confirming the identification of the different Spartina species. Thanks to Andy White for top bug cage repairing skills and to Andy Black for helping with transport. Thank you all for your invaluable assistance and good cheer in the face of landrover engine explosions, suspect navigation skills and welly-losing peril. Thanks also to Rosie Foster, Jonathan Green, David Castellano and Fiona Ingleby for the less muddy, but no less arduous, task of helping me develop my statistical modelling and R skills. Mike Hutchings provided expert insight on working with clonal plants. Jayne Field, Elaine Webster and Graham Johnstone from Natural England were all instrumental in obtaining permissions and arranging access for me to conduct my research in protected field sites. From North America, Fritzi Grevstad kindly gave detailed comment and advice on my initial research plan for which I am enormously grateful. Steve Pennings, Gina Wimp and Danny Lewis all gave invaluable advice on culturing Spartina spp. under glasshouse conditions. Specific practical help in the completion of data chapters was provided by a number of friends and colleagues for which I am very grateful: Chapter one: Alan Stewart provided the map of P. marginata’s British distribution using the DMAP software developed by Alan Morton; the map was adapted by Will Harkin. Chapter two: Will Harkin provided the map of field sites. Ash Abraha assisted in the collection of data on invertebrate composition at the secondary field sites. Tanya Pennell provided useful comments on an earlier draft of the chapter. Alan Stewart provided photographs of P. marginata eggs. vi Chapter three: Chris Accleton helped with the set up of the field experiment. Keith Cornelius assisted with harvesting the glasshouse experiment. Chapter four: Will Harkin provided the map of field sites. Chapter five: Ash Abraha assisted with the set up of the field assay. He also set up, harvested and collected the data for the experiments described in 5.2.2 and 5.2.3 whilst I was on maternity leave. Tanya Pennell assisted with data collection for the experiment described in 5.2.4. Fiona Ingleby and Jonathan Green provided useful comments on an earlier draft of the chapter. I would like to thank the Natural Environment Research Council, the University of Sussex School of Life Sciences, and the Gilchrist Educational Trust for funding my research. The opportunity to study at this level is an immense privilege, for which I am extremely grateful. On a more personal note, my time at Sussex would have been immeasurably poorer were it not for the friendship and camaraderie I have enjoyed as part of the wonderful 5th Floor JMS community. So many people deserve a mention, but I will especially single out Jonathan Green, Rosie Foster, Paul Davison, Tanya Pennell, Chris Accleton, Citlalli Morelos Juarez and Leanne Casey for making the good times great and the bad times less so. Lauren Holt – I never would have made it through without you. My deepest thanks go to my parents for the incredible love and support they have given me throughout my life and in all of my (often bemusing, I am sure) choices. My decision to give up a well-paid career to become a destitute student in my mid-thirties, and then to compound the folly by studying for my PhD, must have caused more than a little concern. Thank you for believing in me and letting only your pride (and not your alarm!) influence my path. If my daughter feels half as much love and support from me as I have felt from you, I will have done a great job. Finally, to my husband Will Harkin: well baby, that was an eventful few years! Thank you always for your love, friendship, belief and only ‘slightly’ annoying insistence that I get the thing done. Now the adventure really begins; I look forward to sharing every step with you and the lovely family we have created together. vii Table of Contents Summary ..................................................................................................................... iv Acknowledgements ....................................................................................................... v List of figures ............................................................................................................... xi List of tables ............................................................................................................... xiv Chapter one .................................................................................................................. 1 General introduction ..................................................................................................... 1 1.1 Biological invasions ............................................................................................. 1 1.2 Why are biological invasions important? .............................................................. 3 1.2.1 Ecological impacts and economic costs ........................................................ 3 1.2.2 Extinctions, biodiversity decline and biotic homogenization ........................... 4 1.2.3 Confounding factors ...................................................................................... 7 1.2.3.1 Climate change ...................................................................................... 7 1.2.3.2 Invasion lag ...........................................................................................
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