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Fig Trees and Fig Wasps: Their Interactions with Non- mutualists By Jauharlina Submitted in accordance with the requirements for the degree of Doctor of Philosophy The University of Leeds Faculty of Biological Sciences School of Biology February 2014 ii The candidate confirms that the work submitted is her own, except where work which has formed part of jointly-authored publications has been included. The contribution of the candidate and the other authors to this work has been explicitly indicated below. The candidate confirms that appropriates credit has been given within the thesis where reference has been made to the work of others. The candidate wrote the manuscript including all analysis, figures, and tables for the publication. The candidate thanks E.E. Lindquist for identifying the mites and providing comments on their biology, H.G. Robertson for planning the sampling regime, R.J. Quinnell for statistic consultation of the paper, S.G. Compton for collecting the data in South Africa and for his advice and comments to make Chapter 3 was publishable. JAUHARLINA, J., E. E. LINDQUIST, R. J. QUINNELL, H. G. ROBERTSON and S. G. COMPTON 2012. Fig wasps as vectors of mites and nematodes. African Entomology, 20, 101-110. (http://www.bioone.org/doi/abs/10.4001/003.020.0113) This copy has been supplied on the understanding that is copyright material and that no quotation from the thesis may be published without proper acknowledgement. ©2014. The University of Leeds. Jauharlina. iii Acknowledgements It would not have been possible to write this thesis without the help and support of the kind people around me, and only some of them I could mention here. I would like to thank my supervisor, Dr. Stephen Compton for his support during these past four years. He was the one who introduced me to the fascinating fig world that I did not recognize earlier. His advice and suggestions during my PhD study are very much appreciated. The good advice, support and help particularly in solving statistical problems of my co-supervisor, Dr. Rupert Quinnell have been invaluable, for which I am extremely grateful. I am thankful for their understanding with my health problem when I had to undergo an operation last summer. I would like to express my special appreciation for the help of field work team in Indonesia, including Yus Maini, Eka Putra, Lukman, and Afriyani. Thanks for the adventure and the fun that we shared during a challenging work in the field. It would not have been possible for me to climb and introduce the pollinating wasps in high fig trees without their help. Special thanks to my dear friend, Dr. Rina Sriwati for helping me to develop the fig extraction methods with limited resources in her laboratory in Banda Aceh. I thank Dr. Natsumi Kanzaki (Forestry and Forest Products Research Institute, Tsukuba, Japan) and Dr. Kerrie Davies (The University of Adelaide, Australia) for their help in identifying nematodes species and providing some pictures of the nematodes. My acknowledgments would not be complete without giving sincerely gratitude to my late parents. Both have instilled many admirable qualities in me and given me a good foundation with which to meet life. They have taught me about hard work and self-respect, about persistence and about how to be independent. To my two late siblings who always gave me strength even when they are no longer with me. Our ‘world’ may be different now, but our love to each other never ends. My appreciation also goes to my only surviving sibling who is always there for me, even when he himself was in a great pain. Together we had gone through a very hard time. I am so proud of him. Last, but certainly not least, I am truly and deeply indebted to my dear husband, Yunardi, who always support me along the way, despite being thousands miles away from each other quite often in the last four years. Through his endless love, patience, and iv unwavering belief in me, I’ve been able to complete this long PhD journey. I never thought I would go back to school at this age, if it was not for him. He is always my biggest fan and supporter. I am also very touched for great supports that I had from my three children during my study. I am very thankful to my youngest son, Ilman, who willingly accompanied me during my first year in Leeds, to my only daughter, Dalila, who had been such a great house mate during her one year master study in Leeds. Last but not least, I am also grateful to my middle one, Irham, who always stayed in my bedside and patiently helped me to walk again during my recovery after surgery last summer. I love you all. I am very honoured to be part of University of Leeds academia. Leeds has become a very important part of my life and my family’s life. Finally, I am very thankful for The Indonesian Directorate General of Higher Education (DIKTI), Ministry of Education of Indonesia, for funding me to do my PhD. I thank the Rector of Syiah Kuala University, Banda Aceh, Indonesia for giving me a leave of absence during my study in Leeds. Finally I offer my sincerest apologies to anyone who helped me in during my PhD journey, but I did not acknowledge them in this page. Many thanks for you all. “Praise be to Allah, the Lord of the worlds.” v Abstract Non-mutualist species that interact with mutualists occur commonly in nature. Non-mutualists associated with the mutualism between fig trees and their pollinating fig wasps include mites and nematodes. This thesis focusses on the interaction of nematodes with fig trees and fig wasps in South Africa and Indonesia, with additional investigation on how mites, nematodes and fig pollination respond to highly seasonal environments. The reproduction of monoecious Ficus burtt-davyi in Grahamstown, South Africa slows down but does not stop in winter. There are fewer fig pollinating wasps Elisabethiella baijnathi flying in the air during winter, but most figs are probably pollinated by locally-produced fig wasps. Elisabethiella g5baijnathi females transport mites (Tarsonemella sp. nr. africanus) and nematodes (Parasitodiplogaster sp.) between figs. Contrasting dispersion patterns and relationships with fig wasp foundress numbers indicate that the mites, but not the nematodes, disperse between figs after being carried there by the pollinators. Three nematode species (Caenorhabditis sp., Schistonchus centerae, and S. guangzhouensis) developed inside both male and female figs of dioecious F. hispida tree in Sumatra, Indonesia. Caenorhabditis sp. was transferred between figs as juveniles, whereas Schistonchus spp. were transferred mostly as juveniles, and occasionally as adults. The nematode community of eight species in Sumatran monoecious F.racemosa was the most diverse recorded anywhere. No mites were found in both species of fig trees. Peak nematode populations occurred in D-phase figs, when the fig wasp offspring are ready to emerge. The nematodes attach themselves to newly-emerged female pollinators, which then carry them away. Usually more nematodes attached on the first fig wasps to emerge. Entry into figs by early-emerging pollinators resulted in higher numbers of the next generations of nematodes within the figs. Details of the ecology of each nematode species may be different, but as a group they did not seem to significantly affect seed and wasp development in both F. hispida and F. racemosa figs. vi Assistance provided I am thankful for assistance that I had during the course of my PhD. Data in Chapter 2 and Chapter 3 in this thesis were collected by Dr Stephen Compton in Grahamstown, South Africa. There were 1967 young figs of Ficus burtt-davyi collected from 146 crops and 99 trees during October 1987 until February 1990. The data were presented to me as raw data in spread sheets in which I started working from. I thank Eka Putra for climbing up several trees when I needed to introduce pollinating fig wasps into receptive figs and collected them in later phase for data collection in chapter 6. vii Table of Contents Acknowledgements .............................................................................................................. iii Abstract ................................................................................................................................. v Assistance provided ............................................................................................................. vi Table of Contents ............................................................................................................... vii List of Tables ..................................................................................................................... xiii Lists of Figures .................................................................................................................. xvi Chapter 1 General Introduction.................................................................................... 1 1.1 Interactions among species: mutualisms and exploitation of mutualisms .............. 1 1.2 Biology of fig trees and their pollinating wasps ...................................................... 2 1.3 Non-pollinating fig wasps ....................................................................................... 6 1.4 Other insects and invertebrates occupying the figs ................................................. 8 1.5 Fig trees and nematodes .......................................................................................... 8 1.6 Objectives and outline of thesis ............................................................................
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