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ECOSYSTEM SERVICES OF PTEROPODID BATS, WITH SPECIAL ATTENTION TO FLYING FOXES (PTEROPUS AND ACERODON) IN SULAWESI, INDONESIA By SHEHERAZADE A THESIS PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE UNIVERSITY OF FLORIDA 2018 © 2018 Sheherazade To my mom Thank you for teaching me how to be an independent, strong, and happy woman ACKNOWLEDGMENTS I would like to thank my advisor, Dr. Holly Ober, for her guidance and patience during my study. I thank her for always encouraging me to maximize all learning opportunities to gain skills and knowledge that will be important for my future. I thank Dr. Bette Loiselle and Dr. Todd Palmer for their invaluable advice to this study and thesis. I thank the Center for International Forestry and United States Agency for International Development for funding my master program. I thank Dr. Steven Lawry, Ms. Dina Hubuddin, Ms. Rahayu Koesnadi, Ms. Raya Soendjoto, Dr. Karen Kainer, and Dr. Bette Loiselle for providing supports and managing administrative issues during my entire study. I thank Tropical Conservation and Development (TCD) University of Florida for allowing me to learn about the interdisciplinary aspects of conservation and awarding me a field research grant. I thank Rufford Small Grant, Bat Conservation International, and IdeaWild for also funding my research. I thank Government Agency of Maritime Affairs and Fisheries of Central Sulawesi, Integrated Permit Service Agency of Central and West Sulawesi, Longkoga Barat/Timur village, Bualemo Subdistrict, Batetangnga village and Binuang Subdistrict for permits. I thank Alliance for Tompotika Conservation and my team for their tremendous assistance in the field. I thank Dr. Susan M. Tsang and Asnim Alyoihana for being my lifetime mentors, collaborators, and best friends. I thank Tambora Muda Indonesia for trusting me as their president and working there voluntarily always give me the energy to finish my study. I especially would like to thank my best friends, Marsya, Ardian, Sapi, Nuy, Mita, Ridha, Yulia, and Ana for their encouragements, lessons, and of course, laughter. Thank you for being really patient with a difficult person like me! I thank Eight Gators, especially Ikbal, who have been good companies since the program started. Finally, I thank my 4 family, Mama, Oneng, and Ei, for all their support and unconditional loves. Thank you for respecting and believing in my dream to work for wildlife conservation in Indonesia. 5 TABLE OF CONTENTS page ACKNOWLEDGMENTS .................................................................................................. 4 LIST OF TABLES ............................................................................................................ 8 LIST OF FIGURES .......................................................................................................... 9 ABSTRACT ................................................................................................................... 10 CHAPTER 1 INTRODUCTION .................................................................................................... 12 2 BAT POLLINATION SERVICES TO DURIAN AND SIGNIFICANCE TO LOCAL ECONOMY IN SULAWESI, INDONESIA ................................................................ 16 Background ............................................................................................................. 16 Methods .................................................................................................................. 18 Study Sites ....................................................................................................... 18 Results .................................................................................................................... 24 Floral Characteristics of Durian ........................................................................ 24 Pollination Biology of Durian ............................................................................. 24 Significance of Each Flower Visitor as Durian Pollinators ................................ 25 Economic Contribution of Primary Pollinators to Durian Production ................. 27 Discussion .............................................................................................................. 27 Pollinator Assemblage of Durian in Sulawesi ................................................... 29 Resource Partitioning among Bat Species ....................................................... 31 Appeal for Bat Conservation ............................................................................. 33 3 ECOSYSTEM SERVICES PROVIDED BY ACERODON CELEBENSIS AND PTEROPUS GRISEUS IN SULAWESI, INDONESIA ............................................. 48 Background ............................................................................................................. 48 Methods .................................................................................................................. 50 Study Sites ....................................................................................................... 50 Pollen Collection from Flying Foxes ................................................................. 50 Resource Use of Flying Foxes ......................................................................... 52 Characterization of Ecosystem Services Provided by Flying Foxes ................. 54 Results .................................................................................................................... 55 Resource Use of Flying Foxes ......................................................................... 55 Ecosystem Services of Flying Foxes ................................................................ 56 Discussion .............................................................................................................. 57 Ecosystem Services: Cultivated Crops ............................................................. 58 Ecosystem Services: Native Plants .................................................................. 60 Ecosystem Services: Unique Contributions ...................................................... 61 6 4 CONCLUSION ........................................................................................................ 72 APPENDIX A A LIST OF ANIMAL VISITORS AND PRIMARY POLLINATORS OF SEMI-WILD DURIAN THROUGHOUT SOUTHEAST ASIA. ...................................................... 74 B RESULTS OF GENERALIZED LINEAR MIXED-EFFECT MODELS (GLMM) TO DETERMINE WHICH FACTORS CONTRIBUTE MOST TO DURIAN PRODUCTION ........................................................................................................ 76 LIST OF REFERENCES ............................................................................................... 77 BIOGRAPHICAL SKETCH ............................................................................................ 86 7 LIST OF TABLES Table page 2-1 Duration of nocturnal visits by each animal to durian flowers. ............................ 36 2-2 Comparison of number of durian fruit set under open pollination treatment across two pollinator groups. .............................................................................. 37 3-1 Morphometric measurement of a subset of the flying foxes found in the study sites: 18 adults of A. celebensis and 16 adults of P. griseus. ............................. 65 3-2 Plants visited by flying foxes, the resources flying foxes used (flowers, fruits), the pollen load, and the value of each plant to humans in the local community. ......................................................................................................... 66 A-1 A list of animal visitors and primary pollinators of semi-wild durian throughout Southeast Asia. .................................................................................................. 74 B-1 Results of Generalized Linear Mixed-effect Models (GLMM) to determine which factors contribute most to durian production. ............................................ 76 8 LIST OF FIGURES Figure page 2-1 Study site in Batetangnga Village, West Sulawesi, Indonesia. ........................... 38 2-2 A durian inflorescence (yellow circle) growing directly from the branch, consisting of tens of flowers................................................................................ 39 2-3 The treatments within the durian pollination exclusion experiment. .................... 40 2-4 An example of durian fruit set that was monitored at (a) Day 10; (b) Day 20; (c) Day 30); (d) Day 60. ...................................................................................... 41 2-5 Mean nectar volume per durian flower (±SE) calculated cumulatively (n=10). ... 42 2-6 The number of durian fruit set under three pollination treatments. ..................... 43 2-7 Different bat species fed on durian nectar. ......................................................... 44 2-8 Temporal overlap of foraging activity on durian between pairs of species. ......... 45 2-9 Strigocuscus celebensis visited a durian inflorescence and consumed the flowers. ............................................................................................................... 46 2-10 Other durian visitors. .......................................................................................... 47 3-1 The two study sites were islands off the coast of Central Sulawesi in Bualemo: Mantalu Daka Island and Tangkuladi Island.