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The EU-Protected Slug Geomalacus Maculosus: an Investigation Title Into Its Phylogenetics, Population Densities in Conifer Plantations and Its Gut Microbial Community

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The EU-Protected Slug Geomalacus Maculosus: an Investigation Title Into Its Phylogenetics, Population Densities in Conifer Plantations and Its Gut Microbial Community Provided by the author(s) and NUI Galway in accordance with publisher policies. Please cite the published version when available. The EU-protected slug geomalacus maculosus: an investigation Title into its phylogenetics, population densities in conifer plantations and its gut microbial community Author(s) Reich, Inga Publication Date 2016-04-04 Item record http://hdl.handle.net/10379/5631 Downloaded 2021-09-29T06:38:46Z Some rights reserved. For more information, please see the item record link above. The EU-protected slug Geomalacus maculosus: An investigation into its phylogenetics, population densities in conifer plantations and its gut microbial community A thesis submitted to the National University of Ireland for the degree of Doctor of Philosophy April 2016 Inga Reich Supervisors and affiliations: Professor Dr Mike Gormally, Applied Ecology Unit, Centre for Environmental Science, School of Natural Sciences, National University of Ireland, Galway Dr Cindy Smith, Microbiology, Centre for Environmental Science, School of Natural Sciences, National University of Ireland, Galway Table of Contents Acknowledgements v Abstract viii Chapter 1. General Introduction 1.1. Scope and objectives 1 1.2. Literature review 1.2.1. General information about G. maculosus 2 1.2.2. Legislation associated with G. maculosus 6 1.2.3. The Lusitanian question 8 1.2.4. Forestry practices in Ireland and implications for G. maculosus in conifer plantations 10 1.2.5. Gut microbial communities of invertebrates 11 1.3. Structure of thesis 13 Chapter 2. Genetic study reveals close link between Irish and Northern Spanish specimens of the protected Lusitanian slug Geomalacus maculosus 2.1. Abstract 15 2.2. Introduction 15 2.3. Materials and Methods 18 2.3.1. Sampling 18 2.3.2. DNA extraction, PCR and sequencing 19 2.3.3. Alignment and sequence analyses 20 2.3.4. Phylogenetic analyses 21 2.4. Results 24 i 2.4.1. Sequence analyses 24 2.4.2. Phylogenetic analyses 28 2.5. Discussion 30 2.5.1. The Iberian population of G. maculosus 30 2.5.2. The Irish population of G. maculosus 33 2.5.3. Possible ways of introduction 34 2.5.4. Implications 35 2.5.5. Conclusions and future work 35 Chapter 3. EU-protected slug Geomalacus maculosus and the sympatric Lehmannia marginata in commercial forests: What can the mark-recapture method tell us about their population densities? 3.1. Abstract 37 3.2. Introduction 37 3.3. Materials and Methods 41 3.3.1. Study Area 41 3.3.2. Experimental design 41 3.3.3. Methodology 43 3.4. Results 48 3.4.1. Population density estimates 49 3.4.2. Weather conditions and trapping success 52 3.5. Discussion 53 3.5.1. Population density estimates 53 3.5.2. Weather conditions and trapping success 55 3.5.3. Assessment of the methodology 56 3.5.4. Conclusions 58 ii Chapter 4. Microhabitat is likely to be the major determinant of the highly diverse microbiome found within faecal samples of the EU protected slug Geomalacus maculosus 4.1. Abstract 60 4.2. Introduction 61 4.3. Materials and Methods 63 4.3.1. Sampling 63 4.3.2. DNA extraction, PCR and sequencing 65 4.3.3. Sequence analyses 66 4.4. Results 67 4.4.1. Microbial diversity 67 4.4.2. The drivers of the gut microbiome diversity 71 4.4.3. Vertical transmission of microbes 74 4.5. Discussion 75 4.5.1. Conclusions and future work 79 Chapter 5. General Discussion 5.1. Discussion 80 5.2. Key findings and conclusions 91 5.3. Recommendations for future studies 93 References 95 iii Appendices Appendix 1. Mean p-distances within (diagonal, bold) and between (down) all sampled Geomalacus maculosus populations for 16S rRNA (a), COI (b) and ITS-1 (c) datasets. Appendix 2. Node ages in millions of years (Myr) and 95 % highest posterior density intervals (HPDI) for the 16S rRNA dataset and three different divergence rates obtained for gastropods from the literature in ascending order of age. Appendix 3. Environmental measurements at sites P1, P3 and P4. Appendix 4. Formulae of the Schnabel (a) and Jolly-Seber (b) methods. Appendix 5. Results from the goodness-of-fit tests for the Schnabel (a) and Jolly-Seber (b) methods. Appendix 6. Schnabel (a) and Jolly-Seber (b) population size estimates (PSE) with 95 % confidence intervals (CI). Appendix 7. Principal coordinate analysis plots based on the unweighted (a) and weighted (b) UniFrac distance matrices. Coloured by ‘substrate’ (1), ‘environment type’ (2), ‘OTU number’ (3) and ‘Simpson’s Index of Diversity’ (4). Appendix 8. The total amount of operational taxonomic units (OTUs) and the number and percentage of OTUs present in all individuals at each site except Raferigeen (a), in all individuals at each habitat for which more than one site was sampled (b) and in all individuals of reared slugs (c). Appendix 9. Schematic of the trees at the experimental site in relation to each other (a) and number of the tree behind which each micro-chipped slug was captured between 06.12.2013 and 26.06.2014 (b). iv Acknowledgements A huge thank you to my supervisors Mike Gormally and Cindy Smith for helping me in so many different ways with their encouragement, patience and good advice. It was great to have the opportunity to work with ecological as well as molecular methods. You are both so enthusiastic about what you do and were always willing to discuss new ideas for my project - at the beginning of my PhD I never would have thought I’ll do a chapter on microbes! Many thanks also to Rory McDonnell - the pioneer in Geomalacus maculosus research at the Applied Ecology Unit who has been very supportive throughout my PhD, and who provided me with lots of Kerry slug knowledge and feedback on papers and conference abstracts despite being all the way across the Atlantic. Chris Williams has been of great assistance with any kind of statistical analysis and Gesche Kindermann has been an immense help with all my GIS related problems. They and Caitriona Carlin were always supportive if I had any problems or queries – thank you so much guys! I am very grateful to Owen Doherty for assisting with fieldwork and organising all the materials for my second year students, to Angela Trayers-Lynagh for helping with all administrative queries, to Maurice Martin for ordering anything and everything and to Mike Coughlan and Ann Smyth for locating things within the department and helping out in any other possible way. Many thanks also to Louise Allcock for helping me with my phylogenetic analyses – I don’t think she knew how much work was in store for her when I first approached her but with her patience and great teaching skills I went from a complete newbie to a fairly confident BEAST user. v I am very grateful to the members of my Graduate Research Committee, Ger Fleming and Micheline Sheehy-Skeffington for providing me with feedback about my work. I couldn’t have asked for a nicer working atmosphere and throughout my four years in the Applied Ecology Unit my colleagues have been very supportive and great to work with. Thanks to Brendan Canning, John Staunton, Dave Clarke, Tracy Hynes, Margaret Hayes, Mesa Perry, John Carey, Irene Giordani, Erin Johnston, Collette Mulkeen, Aidan O’Hanlon, Lorenzo Sardo, Manuela Carnaghi and Allison Bistline-East for being such fantastic labmates. I’ll miss our ‘Cake- Tuesdays’, lunchtime sessions and general fun times in the lab! A special thanks to Kim O’Meara for being my field assistant in my first year of the PhD and for making fieldwork and writing so much more enjoyable. A pity you didn’t stick around longer. Thanks also to the many visiting students as well as fourth year students, in particular Maxime Poissonneau, Cian Blaix, Eugene Cush, Fiachra Tierney, Shane Callanan and Cathal McInerney for helping me with my fieldwork and laboratory experiments. Thanks to Aoife Duff, Agata Lisik, Cathy Abberton, Limei Zhang and Enrico Tatti for making my start in the world of genetics and microbiology so much easier with their friendly reception in the ‘microlab’ and by helping me with my gels, extractions and PCRs. My PhD would have been only half as much fun without my fieldwork in Spain and I am very grateful to José Castillejo and Javier Iglesias from the University of Santiago de Compostela for accompanying me on my sampling trip and showing me the best G. maculosus spots. They were such nice and helpful hosts and I’ll never forget the extended night sampling trips in the amazing countryside of Northern Iberia. Thanks also to Javier Quinteiro for letting me use his lab for sample preparation and for helping me with my population genetics vi analyses, to Jorge Rodríguez-Castro for collecting additional G. maculosus specimens and to María Córdoba Otero for help with sending tissue samples from Spain to Ireland. Many thanks to the National Parks and Wildlife Service for funding parts of my research and providing me with several G. maculosus sampling and killing licenses. A special thank you to Brian Nelson who was of great help during the preparation of the Wildlife Manual as well as of two other, sadly not yet published papers. Thanks to Barry Rintoul from Coillte for letting me conduct my work in Cloosh Forest and for providing me with management plans and information about the area. I am also very grateful to Paul Whelan for assisting me with lichen identification for the Wildlife Manual. I want to thank all my friends for being so supportive and providing plenty of distraction from my study when needed - even if it was just through a Skype call! Thanks to my family for their emotional and financial support, interest in my work and belief in me.
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