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The Winter Moth ( Operophtera Brumata) and Its Natural Enemies in Orkney

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The Winter Moth ( Operophtera Brumata) and Its Natural Enemies in Orkney Spatial ecology of an insect host-parasitoid-virus interaction: the winter moth ( Operophtera brumata) and its natural enemies in Orkney Simon Harold Submitted in accordance with the requirements for the degree of Doctor of Philosophy The University of Leeds Faculty of Biological Sciences September 2009 The candidate confirms that the work submitted is his own and that appropriate credit has been given where reference has been made to the work of others This copy has been supplied on the understanding that it is copyright material and that no quotation from the thesis may be published without proper acknowledgement ©2009 The University of Leeds and Simon Harold ii Acknowledgements I gratefully acknowledge the support of my supervisors Steve Sait and Rosie Hails for their continued advice and support throughout the duration of the project. I particularly thank Steve for his patience, enthusiasm, and good humour over the four years—and especially for getting work back to me so quickly, more often than not because I had sent it at the eleventh hour. I would also like to express my gratitude to the Earth and Biosphere Institute (EBI) at the University of Leeds for funding this project in the first instance. Steve Carver also helped secure funding. The molecular work was additionally funded by both a NERC short-term grant, and funding from UKPOPNET, to whom I am also grateful. None of the fieldwork, and indeed the scope and scale of the project, would have been possible if not for the stellar cast of fieldworkers that made the journey to Orkney. They were (in order of appearance): Steve Sait, Rosie Hails, Jackie Osbourne, Bill Tyne, Cathy Fiedler, Ed Jones, Mike Boots, Sandra Brand, Shaun Dowman, Rachael Simister, Alan Reynolds, Kim Hutchings, James Rosindell, Rob Brown, Catherine Bourne, Audrey Zannesse, Leo Graves and Steven White. I am grateful to you all for the help and enthusiasm you each brought to the project. The fieldwork would have been all but useless had it not been for the efforts—over and above the call of duty—of Helen Hesketh, Bill Tyne and Leo Graves at CEH Oxford. I would particularly like to extend my gratitude to Bill, who was a patient and understanding teacher of molecular methods. Bob Possee was also particularly helpful with his on-hand advice. I would also like to thank Mark Hussey and Jo McTigue for showing me the ropes of real-time PCR and DNA extraction robots, respectively. I am grateful to Tim Carty for all the thousands of pots of synthetic diet he made over the four years, and I am also indebted to Rob Graham, whose excellent previous work on the system has made the scope of this project possible. I would also like to thank all of my friends and family who have supported my decision to embark on this PhD project, and for continuing to do so in its duration: to Chris Avis and Alex Pulsford for good food, good company and accommodation; to Tim Harrison for miscellaneous fruitful discussions; to the Hutchings family for agreeing to house, feed, and put up with me, during the final stages of the writing-up period; to Pete Selhurst for essential computational support; to my family, especially Matt and Jen for all their love and support, and for generally making sure I looked presentable. I would also particularly like to thank Kim Hutchings, for being present at—or the cause of—most of the highs; for being at the coal-face during the lows; and for being almost entirely responsible for the size of my carbon footprint. Finally, it leaves to me to thank my parents, who have always shown me love, support, affection and belief, and to whom this thesis is dedicated. iii Thesis abstract Understanding the population dynamics of host-natural enemy interactions in spatially heterogeneous habitats may help mitigate the negative effects of environmental change. The aim of this thesis is to investigate the role of spatial processes in determining the distribution and abundance of two co-occurring Lepidoptera species of differing dispersal capabilities, and how this may affect interactions with natural enemies of differing transmission modes. Operophtera brumata is a resident species, attacked by a single parasitoid and three viral pathogens, all with differing transmission strategies; Abraxas grossulariata is a new coloniser, and may have escaped its parasitoid enemies. Both species feed on the same hostplant, Calluna vulgaris , in the Orkney isles, Northeast Scotland. Natural enemy prevalence was rarely related to host density of either species at any scale. Significant host density dependence in infection was detected only among horizontally transmitted pathogens infecting O. brumata, and only during high density outbreaks. Parasitoid prevalence was significantly negatively related to O. brumata host density, although only during outbreak years, either due to satiation or competition from pathogens. Conversely, two years following an outbreak, parasitoid prevalence was found to be positively related to host density. There was no evidence that O. brumata escapes parasitoid attack at higher elevations, although newly colonising A. grossulariata populations may be susceptible to microclimatic variation, mediated by topography. Such susceptibility may be a result of unfavourable conditions at the northward margin of the species’ range. A genetic signal of recent colonisation was detectable among A. grossulariata populations within Orkney when compared to mainland Britain. Genome scans also suggest that A. grossulariata may be under selective pressure from pathogenic infections , possibly due to their low genetic diversity. Local adaptation of O. brumata to individual patches was not apparent. The implications of these findings and potential areas of future research, are discussed. iv Contents Acknowledgements………………………………………………………………. ii Abstract……………………………………………………………………………. iii List of tables………………………………………………………………………. vii List of figures……….. ............................................................................................. ix 1. General introduction………………………………………………………… 1 1.1 Population ecology of insect herbivores in space and time …....... 2 1.2 Predators, parasitoids, and pathogens ……………………………. 4 1.2.1 Predators and parasitoids …………………………………… 4 1.2.2 Pathogens ..……………………………………...…………… 6 1.3 Heterogeneity in natural populations ……………………................. 11 1.3.1 Phenotypic, genotypic and temporal heterogeneity …….......... 12 1.3.2 Spatial heterogeneity ………………………………................ 15 1.4 Bottom-up and abiotic effects ………………………………………. 24 1.4.1 Bottom-up factors influencing abundance …………................ 24 1.4.2 Top-down factors influenced by bottom-up sources…………. 26 1.4.3 Exogenous factors……………………………………………. 28 1.4.4 Effects on population processes ………………..…………….. 30 1.5 The study system: two hosts, one foodplant, four pathogens, and a parasitoid ……………………………................................... 31 1.5.1 Orkney ……………………………………….……………….. 31 1.5.2 Winter moth (Operophtera brumata) ………………………… 32 1.5.3 Magpie moth (Abraxas grossulariata )……………………….. 35 1.5.4 Heather moorlands ……………………………….………….. 37 1.6 Thesis aims …………………………………………………………... 38 2. General methods …………………………………………………………….. 43 2.1 Larval sampling, collection, and storage ……………................ 44 2.2 Preparation of specimens ……………………………................ 45 2.3 Nucleic acid extraction and purification ………………………. 45 2.4 Virus identification …………………………………………….. 46 3. Within-generation insect host-natural enemy interactions ………….. 50 3.1 Abstract……………………………………………………………….. 51 3.2 Introduction…………………………………………………………… 53 v 3.3 Methods………………………………………………………………. 56 3.3.1 Sampling methods ……………………………………………. 56 3.3.2 Statistical analysis …………………………………................ 57 3.4 Results ………………………………………………………………... 59 3.5 Discussion ……………………………………………………………. 74 4. Local scale insect host-natural enemy interactions ……….………….. 80 4.1 Abstract ……………………………………………………………….. 81 4.2 Introduction …………………………………………………................ 84 4.3 Methods ………………………………………………………………. 87 4.3.1 Study sites ……………………………………...…………….. 87 4.3.2 Sampling methods ……………………………..……………... 88 4.3.3 Statistical analysis …………………………………………… 89 4.4 Results ………………………………………………………………... 94 4.5 Discussion ……………………………………………………………..113 5. Regional scale insect host-natural enemy interactions ………………. 122 5.1 Abstract …………………………………………………….................. 123 5.2 Introduction …………………………………………….……………... 125 5.3 Methods ………………………………………………………………. 128 5.3.1 Site identification ………………………………….................. 128 5.3.2 Sampling protocol …………………………………….……… 130 5.3.3 Statistical analysis ……………………………….................... 131 5.4 Results …………………………………………………..……………. 135 5.5 Discussion ……………………………………………………………. 153 6. Spatial population genetics of winter moth ( Operophtera brumata ) and magpie moth ( Abraxas grossulariata ) in Orkney……………. 164 6.1 Abstract ……………………………………………………………….. 165 6.2 Introduction …………………………………………………………… 167 6.3 Methods ………………………………………………………………. 169 6.3.1 Sample collection ………………………………….….……… 169 6.3.2 AFLP protocol ……………………………………...………... 169 6.3.3 Error rate analysis …………………………………… ……... 173 6.3.4 Non-spatial among-year analysis ………………..…………... 174 6.3.5 Spatial within-year analysis ………………………………….. 175 6.3.6 Genome scan for loci under selection ……………................... 178 vi 6.4 Results ………………………………………………………………... 181 6.5 Discussion ………………………………………………..…………... 199 7. General discussion ……………………………………………...…………... 211 7.1 Review of main findings ………………………………...…………… 213 7.1.1 Spatial patterns
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