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Ficus Seed Dispersal Guilds: Ecology, Evolution and Conservation Implications

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Ficus Seed Dispersal Guilds: Ecology, Evolution and Conservation Implications Ficus seed dispersal guilds: ecology, evolution and conservation implications MICHAEL J. SHANAHAN Submitted in accordance with the requirements for the degree of Doctor of Philosophy The University of Leeds Centre for Biodiversity and Conservation School of Biology December 2000 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 1 ACKNOWLEDGEMENTS Firstly, I wish to thank my supervisor, Dr Steve Compton, for initially turning me on to the genus Ficus and for his guidance throughout my doctorate, especially during the write-up period. This research was conducted whilst I was a visiting research fellow at the Institute of Biodiversity and Environmental Conservation (IBEC) at Universiti Malaysia Sarawak (UNIMAS). For my appointment to this post I thank Professor Ghazally Ismail and Dr Stuart Davies and, for administrative help at UNIMAS, Yaziz and Dayang. Fieldwork conducted in Sarawak was undertaken with permission of the Forest Department Sarawak and for this I thank, in particular, Abdul Abang Hj. Hamid and Sapuan Hj. Ahmad. Logistical support in Lambir was provided by Johan and Mr Abdullah. Canopy studies were greatly aided by permission to use the walkways and towers of the Canopy Biology Program in Sarawak and I wish to acknowledge the assistance of Professor Tohru Nakashizuka and the late Professor Tamiji Inoue. For permission to live in the "American house" in Lambir I am grateful to the Center for Tropical Forest Science (Smithsonian Tropical Research Institute) and in particular, Drs Jim La Frankie and Elizabeth Losos. My work in Borneo was greatly aided by my first-rate research assistant Siba anak Aji whose constant hard work and high spirits were an inspiration to me. Further assistance was provided by Ruby and Hazel Oakley. Much of my Bornean research would not have been possible without the previous research and assistance of Rhett Harrison, to whom I am highly grateful. Life in the house in Lambir was made fun and interesting by the presence, at various times, of Rhett Harrison, Igor and Sophie Debski, Matt Potts, Tristram Seidler, Chuck Cannon, Supinda Bunyanavich, Hazel Oakley, Jose Nieto, Lisa de Lissio, Jenn Smith and Tim Laman, Kenta Tanaka, Yoko Inui, Kaori Murase, Kaori Sato, Aya Hatada, Yamauchi, Hideo and Michiko Nakagawa. The generosity and hospitality of my Iban neighbours, particularly Siba and family, Mama Susi, Mama Franklin and Ukat were greatly appreciated, as was all of the tuak. Chapter 6, on the figs of Long Island, was the result of a collaboration with Dr Rhett Harrison (Kyoto University), Ruby Yamuna (University of Papua New Guinea) and Professor Ian Thornton (La Trobe University). I am extremely grateful to Professor Thornton for inviting me to join the National Geographic funded research trip to Long Island. The other participants on the expedition (Simon Cook, Clinton Schipper, Ross Moore, Professor John Edwards, Rose Singadan and William Boen) ensured that we had good laughs and good poker in the face of the various calamities we endured. The management and staff of Jais Aben Resort provided assistance before and after our time on Long Island and sent emergency food supplies. Thanks are also due to the Christensen Research Institute (Madang) for access to their library and the Forest Research Institute in Lae for identification of specimens. Chapter 7, the global review of fig-eating by vertebrates, was completed in collaboration with Samson So (University of Hong Kong) and made use of unpublished data and other assistance kindly provided by many researchers to whom I am extremely grateful. These are alphabetically, Rauf Ali, Des Allen, Paul Aston, Ramana Athreya, Vidya Athreya, Yves Basset, Mark Bayley, Cornelis Berg, David Bishop, Lien-Siang Chou, Steve Compton, Ed Colijn, Nancylou Conklin-Brittain, James Cook, Richard Corlett, Jared Diamond, Ellen Dierenfeld, Francoise Dowsett-Lemaire, Dan Eisikowitch, R. Farrah, Mauro Galleti, Harish Gaonkar, Jennifer Garrison, Marc Gibernau, David Gorchov, Jaco Greeff, Tristan Guillosson, Britta Denise Hardesty, Allen Herre, Dan Hoare, Matt Heydon, Andrew Mack, Carmi Korine, Nick Helme, Ridwan Jafar, Rajah Jayapal, Elisabeth Kalko, Dhanjaya Katju, Ragupathy Kannan, Margaret Kinnaird, Cheryl Knott, Tim Laman, Mark Leighton, Carlos Machado, Tim Male, Kim McConkey, James MacPherson, Vojtech Novotny, James Paterson, Carlos Peres, Andrew Plumptre, Pilai Poonswad, Jackie Pritchard, S.M.A. Rashid, Vernon Reynolds, Monica Romo, Jana Schulz, Scott Silver, Ana Sosa-Asanza, Hugh Spencer, Sam Stier, S. Subramanya, Jingchuan Sun, Vivek Tawari, John Terborgh, Ian Thornton, George Weiblen, Robert Whittaker and David Wilson. The research was funded largely by the States of Jersey Education Committee to which I am most grateful. I am also grateful for additional funding in the form of a Bat Conservation International Student Scholarship (1998) and Water Chicken Foundation Travel Bursary. This thesis and publications arising from work described here benefited from discussions with many individuals especially John Altringham, John Grahame, Allen Herre, Dan Hoare, Nick Mawdsley, Jamie Moore and Jo Wong. I am also extremely grateful to Dr Andrew Carter for providing me with a home during the important final two months of my doctorate. Finally, I would like to thank my parents, Jennifer and John Shanahan, for all their love and support over the years I have spent in Leeds and overseas in the process of creating this thesis. 1 2 ABSTRACT Ficus (Moraceae) is a large plant genus of considerable ecological, evolutionary and conservation interest. This study focused on the interaction between Ficus species and the vertebrates that eat their fruit (figs), thereby acting as potential seed dispersers. Specifically, the study considered this interaction with regard to the mechanisms that allow different guilds of sympatric Ficus species to attract differentially subsets of frugivore communities. Fig packaging and presentation was studied in Borneo and on an island off New Guinea, the former study, of 43 Ficus species represents the largest ever characterisation of the fruiting ecology of sympatric congeners. The Ficus species studied exhibited considerable diversity in the size, colour, texture, height, water content, seed burden and relative yield of their figs. In both sites, figs were eaten by a large proportion of the vertebrate fauna present. However, that frugivores were not equally attracted to each Ficus species provided evidence of Ficus dispersal guilds. Guild membership was determined by differences in fig packaging and presentation, with fig size, colour and height of presentation being the strongest predictors of frugivore attraction. These traits, and therefore guild membership, showed strong phylogenetic associations. Nonetheless, apparent adaptations to seed dispersers were also documented. The differential attraction of frugivores means not only that competition for dispersal agents is reduced between guilds but also that guilds of Ficus species experience markedly different seed dispersal services from the frugivores they attract. These differences occur in terms of the number and diversity of frugivores attracted, the proportion of figs that are eaten by seed- predatory frugivores and the distance, density and heterogeneity of seed rain. Ficus species that attract relatively small subsets of frugivore communities (such as fruit bats, or large arboreal mammals) which are prone to anthropogenic threats face decreased seed dispersal associated with the continuing decline of these frugivores. Dependence for dispersal on subsets of frugivore communities also means that Ficus species differ in their abilities to colonise degraded habitats. A 12 month study of the phenology of fig production in the Bornean field site demonstrated that fig crops are initiated year-round and are thus a valuable resource for fruit-eating animals. However, patterns of fig production were not equal between Ficus species (because of a lack of pollination for some) and, so, the availability of the fig resource varied for the different animal groups attracted to each of the Ficus guilds. Globally, figs are eaten by at least ten percent of all bird species and six percent of all mammal species, many of which are capable of dispersing Ficus seeds. That these frugivores also disperse the seed of many other plant species appears to support the suggestion that Ficus species are of great conservation status. However, the 'keystone resource' epithet applied to figs as a whole need to be re-assessed as I show that, because of fig-frugivore partitioning, Ficus species are not equal resources for vertebrate frugivores. 2 3 TABLE OF CONTENTS ACKNOWLEDGEMENTS i ABSTRACT iii TABLE OF CONTENTS iv LIST OF FIGURES viii LIST OF TABLES x PAPERS ARISING FROM THIS THESIS xii DECLARATION xiii GLOSSARY xiv CHAPTER 1 GENERAL INTRODUCTION 1.1 THE BIOLOGY OF Ficus SPECIES 1 1.2 MUTUALISM AND CO-EVOLUTION 2 1.3 FRUGIVORY AND SEED DISPERSAL 2 1.4 FRUIT SYNDROMES AND ECOLOGICAL GUILDS 3 1.5 THE SCOPE OF THIS THESIS 4 CHAPTER 2 DESCRIPTION OF STUDY SITES 2.1 LAMBIR HILLS NATIONAL PARK, SARAWAK, MALAYSIA 5 2.2 LONG ISLAND, PAPUA NEW GUINEA 5 CHAPTER 3 PACKAGING AND PRESENTATION OF BORNEAN FIGS 3.1 INTRODUCTION 7 3.2 METHODS 7 3.2.1 Sampling 7 3.2.2 Fig design and presentation 8 3.3.3 Data analysis 8 3.3 RESULTS 8 3.3.1 Species studied 8 3.3.2 The diversity of fig design and presentation 9 3.3.3 Associations between
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