MACRO-ECOLOGICAL PATTERNS IN SEED REMOVAL BY ANIMALS Si-Chong Chen Thesis submitted for the degree of Doctor of Philosophy Evolution and Ecology Research Centre School of Biological, Earth and Environmental Sciences UNSW, Australia June 2016 PLEASE TYPE THE UNIVERSITY OF NEW SOUTH WALES Thesis/Dissertation Sheet Surname or Family name: Chen First name: Sichong Other name/s: Abbreviation for degree as given in the University calendar: PhD School: School of Biological, Earth and Environmental Sciences Faculty: Faculty of Science Title: Macro-ecological patterns in seed removal by animals Abstract 350 words maximum: (PLEASE TYPE) This thesis aims to improve our understanding of several long-held ideas concerning seed removal by animals across large-scale gradients. By assembling a database of 13,135 animal-seed interactions across all vertebrate taxa, I provided the first broad test of the idea that large animals ingest large seeds. Surprisingly, I found that the size of ingested seeds was significantly negatively correlated with animal body weight. This negative relationship was driven by large animals, particularly ungulates, ingesting small seeds. The resu lts show that the loss of large animals could have negative effects on the dispersal of small-seeded plants, in addition to the more widely acknowledged impacts on large­ seeded plants. Next, I used data for 4008 Australian species to provide the first quantitative analysis of the idea that fleshy fruits are more prevalent towards the tropics. Plants were more likely to bear fleshy fruits at low latitudes, and in regions with warm, wet and stable climates. Fruit type was more strongly affected by conditions during the parts of th e year in which they grow than by conditions during the harshest parts of the year, suggesting that some current theories on plant traits may focus on the wrong aspects of climate. Finally, I performed a field study across 25 sites spanning 28° of latitude along the east coast of Australia, to provide the first empirical test of the idea that seed predation and seed defense are greater towards the tropics. Contrary to traditional expectations, neither seed predation nor seed physical defence was more intense at low latitudes. In fact, pre-dispersal predation and defence were greater at higher latitudes. My results are consistent with recent findings on latitudinal gradients in herbivory and defences in leaves. My findings cast further doubt on the generality of latitudinal gradients in biotic interactions, and suggest that increased seed/seedling mortality as predicted by the Janzen-Connell hypothesis does not provide a plausible explanation for the greater diversity of tropical ecosystems. My thesis has tested several well-accepted ideas on seed removal by animals, and shown that our understanding of the factors that shape global patterns in biodiversity needs to be reshaped. Declaration relating to disposition of project thesis/dissertation I hereby grant to the University of New South Wales or its agents the right to archive and to make available my thesis or dissertation in whole or in part in the University libraries in all forms of media, now or here after known, subject to the provisions of the Copyright Act 1968. I retain all property rights, such as patent rights. I also retain the right to use in future works (such as articles or books) all or part of this thesis or dissertation. I also authorise University Microfilms to use the 350 word abstract of my thesis in Dissertation Abstracts International (this is applicable to doctoral theses only). The University recognises that there may be exceptional circumstances requiring restrictions on copying or conditions on use. Requests for restriction for a period of up to 2 years must be made in writing. Requests for a longer period of restriction may be considered in exceptional circumstances and require the approval of the Dean of Graduate Research. FOR OFFICE USE ONLY Date of completion of requirements for Award: THIS SHEET IS TO BE GLUED TO THE INSIDE FRONT COVER OF THE THESIS ORIGINALITY STATEMENT ‘I hereby declare that this submission is my own work and to the best of my knowledge it contains no materials previously published or written by another person, or substantial proportions of material which have been accepted for the award of any other degree or diploma at UNSW or any other educational institution, except where due acknowledgement is made in the thesis. Any contribution made to the research by others, with whom I have worked at UNSW or elsewhere, is explicitly acknowledged in the thesis. I also declare that the intellectual content of this thesis is the product of my own work, except to the extent that assistance from others in the project's design and conception or in style, presentation and linguistic expression is acknowledged.’ Signed …………………………………………….............. Date …………………………………………….............. COPYRIGHT STATEMENT ‘I hereby grant the University of New South Wales or its agents the right to archive and to make available my thesis or dissertation in whole or part in the University libraries in all forms of media, now or here after known, subject to the provisions of the Copyright Act 1968. I retain all proprietary rights, such as patent rights. I also retain the right to use in future works (such as articles or books) all or part of this thesis or dissertation. I also authorise University Microfilms to use the 350 word abstract of my thesis in Dissertation Abstract International (this is applicable to doctoral theses only). I have either used no substantial portions of copyright material in my thesis or I have obtained permission to use copyright material; where permission has not been granted I have applied/will apply for a partial restriction of the digital copy of my thesis or dissertation.' Signed ……………………………………………........................... Date ……………………………………………........................... AUTHENTICITY STATEMENT ‘I certify that the Library deposit digital copy is a direct equivalent of the final officially approved version of my thesis. No emendation of content has occurred and if there are any minor variations in formatting, they are the result of the conversion to digital format.’ Signed ……………………………………………........................... Date ……………………………………………........................... Acknowledgements How time flies and the moment when I landed in Australia seems like yesterday. I had never thought I might do a PhD in Australia, but now I have been living in Sydney for three and a half years, met many helpful people and had a lot of interesting stories. I constantly feel so lucky to have Angela Moles as my supervisor. She has been teaching me how to do good science and become a good scientist with great patience. She always encourages me to develop my own research ideas while also gives me a helpful hand when necessary. Her timely supervision is my lifeguard in postgraduate surf to overcome difficulties, keep enthusiasm, and (most importantly) learn swim myself. Besides the above aspects, Angela herself is the idol that encourages me to seek a research career. It is difficult to express my gratitude to her in just a few lines, so allow me to modify Titanic movie quotes (may seemingly funny, but I mean it): she supervised me in every way that a student can be supervised. Thank you, Angela! Many thanks to my co-supervisor Stephen Bonser, my panel chairperson Rob Brooks, and panel members David Eldridge and Mike Letnic, for giving me sufficient support and keeping my study on track. To my academic siblings Floret Meredith (my lab bestie is awesome!), Habacuc Flores- Moreno, Rhiannon Dalrymple, Claire Brandenburger, Stephanie Creer, Tim Hitchcock, Tom Meredith, Martin Kim, Marianne Tindall, to our lab postdocs Riin Tamme and Julia Cooke, i and to the visiting scholars Hong-Xiang Zhang and Yan-Hong Wang. You have made the Big Ecology Lab a real home, and you never let me sink in depression. Thank you for helping me in all aspects and witnessing every step of my progress. Thank you to Will Cornwell and Frank Hemmings for the awesome collaboration in my projects and the introduction to statistics and plants. Thank you to Casey Gibson, Charlotte Mills, Jie Yan, Linda Wong and Uncle Deng for being brilliant companions in my fieldtrip. I am sure the beautiful scenery and the hardworking sweat will all be treasured up in our hearts. Thank you to Yun-Hong Tan, Jia-Jia Liu, De-Li Zhai, Zhi-Cong Dai, Shan-Shan Qi and Yan- Jie Liu for constant encouragement and beneficial discussion. I thank E&ERC and School of BEES for providing me awards, prizes and numerous opportunities to make a fantastic postgraduate experience, as well as Ecological Society of Australia for the Student Research Grant. I also sincerely thank my thesis examiners, Anna Traveset and Marc Johnson, for the valuable comments on helping me to make this thesis a better one. Lastly, I want to sincerely thank my mum. She is the first teacher introducing me to the nature, and her persistence to seek her PhD (in molecular immunology) has greatly inspired me to seek my own. I moulted several times during these years (both literally and figuratively), but it is my mum’s love that helped me to conquer each “itch” and come back to a healthy life. She read my papers, assisted me in the fieldwork and constantly talked with me about my projects. Thank you, mum, for everything. ii Abstract This thesis aims to improve our understanding of several long-held ideas concerning seed removal by animals across large-scale gradients. By assembling a database of 13,135 animal-seed interactions across all vertebrate taxa, I provided the first broad test of the idea that large animals ingest large seeds. Surprisingly, I found that the size of ingested seeds was significantly negatively correlated with animal body weight. This negative relationship was driven by large animals, particularly ungulates, ingesting small seeds.