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Final Copy 2019 03 19 Deve This electronic thesis or dissertation has been downloaded from Explore Bristol Research, http://research-information.bristol.ac.uk Author: Devenish, Adam Title: Ant-mediated seed dispersal in an invaded landscape General rights Access to the thesis is subject to the Creative Commons Attribution - NonCommercial-No Derivatives 4.0 International Public License. A copy of this may be found at https://creativecommons.org/licenses/by-nc-nd/4.0/legalcode This license sets out your rights and the restrictions that apply to your access to the thesis so it is important you read this before proceeding. Take down policy Some pages of this thesis may have been removed for copyright restrictions prior to having it been deposited in Explore Bristol Research. However, if you have discovered material within the thesis that you consider to be unlawful e.g. breaches of copyright (either yours or that of a third party) or any other law, including but not limited to those relating to patent, trademark, confidentiality, data protection, obscenity, defamation, libel, then please contact [email protected] and include the following information in your message: •Your contact details •Bibliographic details for the item, including a URL •An outline nature of the complaint Your claim will be investigated and, where appropriate, the item in question will be removed from public view as soon as possible. Ant-mediated seed dispersal in an invaded landscape Adam John Mears Devenish A dissertation submitted to the University of Bristol in accordance with the requirements for the award of the degree of Doctor of Philosophy in the Faculty of Science. School of Biological Sciences December 2018 Word Count: 56572 i ABSTRACT Human activities are modifying our environments at an unprecedented rate and scale, leading to not only a loss of biodiversity, but also a loss of ecosystem functionality. Arguably, one of the most pervasive of these destructive forces can be seen in the rise of biological invasions, and the spread of non-native invasive ant species. Despite the clear potential of the detrimental ecological and economic pressures posed by these insects, we still lack a comprehensive understanding of their impacts on ecosystem services. One such service is ant-mediated seed dispersal – otherwise known as myrmecochory. In this thesis I address some of these shortcomings by investigating how invasive ants may disrupt the process of myrmecochory in native ecosystems, across a range of different scales. Firstly, I took a broad perspective by looking at evolutionary events of myrmecochory across the ant phylogeny: these analyses revealed that myrmecochory is a diffuse interaction between many ant-plant guilds. Secondly, in-depth analyses of the effects of the non-native invasive Argentine ants (Linepithema humile) on both ant and plant communities in South African and Spain suggested that these invaders are ill-equipped to replace the native seed dispersers that they displace. Field observations suggested that invaded ant communities dispersed fewer seeds than non-invaded ant communities, and that this inefficiency is evident at multiple stages in the seed dispersal process. Thirdly, the modifications to the natural ant-plant interactions due to invasive ants may be making these environments more vulnerable to secondary invasions by other invasive myrmecochorous plant species. Finally, I explore the mechanism that may be driving these changes in ant-seed interactions, by exploring how differences in a range of physical and chemical seed traits may explain ant preferences to disperse certain seeds. In conclusion, while myrmecochory may be considered a rather loose ant-plant mutualism, invasive ant species do appear to be altering the nature of the biotic interactions, with impacts permeating through different levels of the ecosystem, and potentially leaving their ecological mark well beyond the mere loss of native ant biodiversity. ii iii ACKNOWLEDGEMENTS Firstly, I would like to thank my supervisors: Dr Seirian Sumner, Dr Jon Bridle and Dr Rosemary Newton. I have been very fortunate to have had the opportunity to work with such a knowledgeable and diverse array of supervisors, who have always been ever willing to help and advise me throughout my research. Without their help and support, completion of this thesis would not have been possible. Secondly, I would like to thank my collaborators: Dr Louise Colville and Dr John Dickie from the Millennium Seed Bank at the Royal Botanic Gardens, Kew, for their helpful advice on seed traits and ecology; Dr Crisanto Gómez for the use of his laboratory and his helpful sharing of knowledge regarding Iberian myrmecochorous systems; Prof. Jeremy Midgley for the use of his laboratory and knowledgeable support during my fieldwork in South Africa; Victoria Wilman and the rest of the South African National Biodiversity Institute (SANBI) seed bank team for their help collecting and identifying myrmecochorous plant species; Dr Hamish Robertson for help with identification of South African ant species. Additionally, I’d like to thank all my field and laboratory assistants, starting with Dr Jan Chlumsky, Beatrice Dewenter, Micaela Gillespie, Nkoliso Ceej Magona, Matthew Granger, Albert Amer, Felipe Rocha, and Cindy van Heereden. You managed to survive in the field with me, putting up with my long hours and early starts. Thirdly, I’d like to thank all in the Sumner lab group and other students, past and present that I have worked with, both at Bristol and UCL; you have always been very welcoming and supportive. Also, Dr Pete Graystock and Dr Alessandro Cini for your help with setting up experiments; Dr Henry Ferguson-Gow and Dr Michael Bentley for putting up with my constant questions regarding phylogenies and the appropriate use of R; Dr Daisy Taylor, Dr Emily Bell, Sam Duckerin, Sandra Moreno, Benjamin Taylor, Sam Morris and Ryan Brock for putting up with my endless recital of facts about ants and seeds. Also, most importantly, Robin Southon, Patrick Kennedy and Andy Saxon for the banter, existential ponderings and frequent tea breaks, often the foundation for keeping me sane and on the path to completing my PhD. Finally, and by no means least, I would like to give a huge thanks to my family both in the UK and South Africa, and in particular my mother. They have been constantly supportive and encouraging, and without them I would not have reached the academic stage I am at now. iv v I declare that the work in this dissertation was carried out in accordance with the requirements of the University's Regulations and Code of Practice for Research Degree Programmes and that it has not been submitted for any other academic award. Except where indicated by specific reference in the text, the work is the candidate's own work. Work done in collaboration with, or with the assistance of, others, is indicated as such. Any views expressed in the dissertation are those of the author. SIGNED: ............................................................. DATE: .......................... vi vii TABLE OF CONTENTS Abstract ............................................................................................................ ii Acknowledgements ......................................................................................... iv List of Tables ................................................................................................... xi List of Figures ................................................................................................ xii Chapter One: General Introduction ...............................................................1 1.1 The Evolution of Myrmecochory .............................................................. 1 1.1.1 Dispersal ............................................................................................................... 1 1.1.2 Myrmecochory – a key ecosystem service ............................................................. 2 1.1.3 Phylogenetic distribution of myrmecochory ........................................................... 3 1.2 The Process of Myrmecochory ................................................................. 5 1.2.1 Cost and benefits of myrmecochory to plants......................................................... 6 1.2.2 Cost and benefits of myrmecochory to ants............................................................ 7 1.2.3 Obligate vs. facultative myrmecochory .................................................................. 8 1.2.4 Multi-stage process................................................................................................ 9 1.2.5 Myrmecochory in the Cape Floristic Region ........................................................ 10 1.2.6 Myrmecochory in the Iberian Peninsula ............................................................... 11 1.3 Partner Matching .................................................................................... 11 1.3.1 Not all ants interact with seeds in the same way ................................................... 11 1.3.2 What traits define a high-quality seed disperser? ................................................. 12 1.3.3 Black box of myrmecochory ................................................................................ 14 1.4 Impact of invasive ants on myrmecochory ............................................ 15 1.4.1 Direct effects ....................................................................................................... 15 1.4.2 Indirect
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