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Chemical Ecology of the Behaviour of the Filariasis Mosquitoculex Quinquefasciatussay

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Chemical Ecology of the Behaviour of the Filariasis Mosquitoculex Quinquefasciatussay Chemical ecology ofth e behaviour ofth e filariasis mosquito Culex quinquefasciatus Say Promotor: dr. J.C. van Lenteren Hoogleraar ind e Entomologie Co-promotor: dr.ir. W. Takken, Universitair Docent Laboratorium voor Entomologie Departement Plantenwetenschappen yjrtOfc^ , et?0S Chemical ecology ofth e behaviour of the filariasis mosquito Culexquinquefasciatus Say Leonard Ernest Gustavin Mboera Proefschrift ter verkrijging van de graad van doctor op gezagva n derecto r magnificus, van deLandbouwuniversitei t Wageningen, Dr. CM. Karssen, opdinsda g 27apri l 1999 desnamiddag st e 16.00uu r ind eAul a trK X CIP-DATA KONINKLIJKE BIBLIOTHEEK, DEN HAAG Mboera, Leonard Ernest Gustavin Chemical ecology of the behaviour of the filariasis mosquito Culex quinquefasciatus Say / Leonard Ernest Gustavin Mboera. -[S.l. :sn.] . 111. Thesis Wageningen. -Wit h ref. -Wit h summary in Dutch. ISBN 90-5808-036-6 Subject headings: Mosquitoes / host-seeking / oviposition / filariasis The research described inthi s thesis was carried out atth e Laboratory of Entomology, Wageningen Agricultural University, The Netherlands, Ubwari Field Station of the National Institute for Medical Research, and Ifakara Health Research and Development Centre, Tanzania and was funded by the European Community, Wageningen Agricultural University, Tanzania Health Research Training Fund and National Institute for Medical Research. Copyright 1999 L.E.G. Mboera Cover design by Piet Kostense LANDIXXrWI;r;iY WAC-ENINJO; UWd&o* \*Z&T PROPOSITIONS (STELLINGEN) 1. Contrary to previous assumptions, host seeking of Culex quinquefasciatus and Anopheles gambiae, at close range, is not random and this affects mosquito catch size, parity rate and hence the estimation of entomological inoculation rates. Thisthesis . Lines,J.D . etal, 1991.BullEntomol. Res. 81,77-84. Mbogo, C.N.M. etal., 1993.J. Am. Mosq. ControlAssoc. 9,260-263 . Davis,J.S . etal, 1995.Med. Vet. Entomol.9 ,249-255 . 2. The species Culex quinquefasciatus has the fascinating characteristic that it is ornithophilic inNort h America and anthropophilic in East Africa. Thisthesis . Tempelis, C.H. 1974.J. Med. Entomol. 11,635-653 . White, G.B. 1971. Trans.R. Soc.Trop. Med. 65, 819-829. Beier, J.C. etal., 1990.J. Am.Mosq. ControlAssoc. 6, 207-212. 3. The observation that Culex quinquefasciatus responds synergistically to oviposition pheromone and waterborne stimuli suggests that the pheromone enhances the reliability of the identification of a suitable breeding site. Thisthesis . Millar, J.G. etal, 1994.J. Am. Mosq. ControlAssoc. 10,374-379 . 4. Assessing the transmission risk of malaria and bancroftian filariasis can be made more accurate by the use of odour-baited traps. Thisthesis . Macdonald, G. 1957. Theepidemiology and control of malaria. 5. Urbanisation and industrialisation have brought Culex quinquefasciatus and man close together, thereby increasing disease problems. 6. Vectors and vector-borne diseases are keeping Africa green and are responsible for the natural maintenance of the continent's eco-systems. 7. Man is a victim of his own odour in malaria and bancroftian filariasis transmission in Africa. Propositions with the thesis 'Chemical ecology of the behaviour of the filariasis mosquito Culex quinquefasciatus Say'. Leonard E.G. Mboera Wageningen, April 27, 1999. Table ofcontent s Preface 1 Summary 3 Samenvatting 7 1. General introduction 11 Part I: Chemical ecology of host-seeking behaviour 2. Carbon dioxide chemotropism inmosquitoe s (Diptera: Culicidae) and itspotentia l invecto r surveillance andmanagemen t programmes: arevie w 33 3. Olfactory responses offemal e Culex quinquefasciatus Say (Diptera: Culicidae) in adual-choic e olfactometer 55 4. Odour-mediated hostpreferenc e of Culex quinquefasciatus (Diptera: Culicidae) inTanzani a 63 5. The response of Culex quinquefasciatus, Anophelesgambiae an d An.funestus (Diptera: Culicidae) to tents baited with human odour orcarbo n dioxide inTanzani a 73 6. The response of Culex quinquefasciatus (Diptera: Culicidae) to traps baited with skin emanations, carbon dioxide, l-octen-3-ol, acetone and butyric acid in Tanzania 85 Part II: Chemical ecology ofovipositio n behaviour 7. The influence of synthetic oviposition pheromone and volatiles from soakage pits and grass infusions upon oviposition site-selection of Culexmosquitoe s inTanzani a 97 8. Oviposition and behavioural responses of Culex quinquefasciatus (Diptera: Culicidae) to skatole and synthetic oviposition pheromone inTanzani a 107 Part III: Semiochemicals in sampling of mosquitoes 9. The influence of Centers for Disease Control light-trap position, relative to ahuman-baite d bed net, oncatche so f Culex quinquefasciatus and Anophelesgambiae i n Tanzania 119 10. Comparison of carbon dioxide baited trapping systems for sampling outdoor mosquito populations in Tanzania 127 11. Sampling gravid Culex quinquefasciatus (Diptera: Culicidae) using traps baited with synthetic oviposition pheromone and grass infusions in Tanzania 139 12. General discussion and conclusions 147 List of publications 159 References 161 Curriculum vitae 189 Preface The time spent onpreparatio n ofthi s work constituted time taken from routine research activities and departmental administration, and I am extremely grateful for the extraordinary tolerance extended to me by my employer and colleagues. But of course, I have more than mere tolerance to applaud on Amani Medical Research Centre's part: several research scientists have been extremely encouraging and directly supportive throughout this effort. I would like to thank Yohana Matola and KatoNjunwa , former Centre's Directors, andFre d Salum, Williams Makunde, Martha Lemnge, Mathias Kamugisha, Robert Malima, William Kisinza and Julius Massaga for their word of encouragement and insight. Prof. Wen Kilama, former Director General,Nationa l Institute forMedica l Research (NIMR)i sthanke d forhi sinitiatives , support and encouragement in securing the PhD fellowship. Dr. Andrew Kitua, Director General, NIMR, is thanked for supporting the final part of this work. Ia m greatly indebted tothem . Some of the earliest work in this thesis was carried out while a collaborating scientist inth e European Community (EC)funde d project titled: Behaviouralstudies on malaria vectors,an dI than k theE Cfo r their support. Crucial to this work was the Ifakara Health Research andDevelopmen t Centre (IHRDC) andUbwar i Field Station. For two years, I had the distinct honour of being a visiting research scientist toth e IHRDC. I received thoughtful assistance from Dr. Andrew Kitua, theforme r Centre's Director, Edith Lyimo and Ikupa Akim, and the entire staff of the Centre. Japheth Kihonda, Aniseth Kihonda, Godwin Ulungi, Raphael Kapendamweni provided me with theexcellen t technical andfield assistanc e that produced parts ofthi s thesis.M y stay in Namawala, Kikulukutu, Njage and Mchombe was a memorable one. Many colleagues at Ubwari Field Station assisted along the way, providing field and technical assistance. I am extremely grateful to Kasembe Mdira, Grace Chuwa, Mayunga Maega, Edward Sambu, Azael Kimambo, Abdallah Telaki, Stephen Mkongewa, Benjamin Chambika, Josephine Nyongole, Jane Kayamba, Joseph Myamba and the entire staff of the station. In addition, I would like to thank the villagers ofKikulukutu , Njage andUbwar i forthei r co-operation andprovisio n of free accesst othei r house premises and pitlatrines . I amespeciall y indebted toProf . Joopva nLentere n andDr.ir . Willem Takken, first for accepting to be my promotor and co-promotor respectively, secondly for providing me with advice during my research work and writing of the thesis, and lastly for leaving meth efreedo m toconduc t experiments asI foun d them appropriate. The twoprovide d mewit h valuable comments onal lth echapters . Willem, thankyo u very much for your continuous support in the laboratory, field and for your most useful advice at various stages of this work. I would also like to thank Profs. Chris Curtis and John Pickett, Dr. Philip McCall, Paul Lyakurwa, Said Mgenzi, Marieta Braks, G. Mmbuji and Fikirini Msuya for their substantial contributions toward the successful execution of this work. Dr. Dan Kline is thanked for the permission to adopt figure 1 inchapte r6 . Special gratitude are duet o my colleague and friend, Dr.ir. Bart Knols,wh o assisted me throughout the study period, providing reading critiques, research guidance andcrucia l insight. Bart andIngeborg , you were myhost swhil e inHollan d Preface and Ifakara, and always ready to give a first hand assistance when I was stuck materially or morally. Bart, you have played a great role in refining some of the designs and ideas. You have reviewed all the chapters andpublication s resulting from this thesis despite your tight research schedule. Thank you very much. Indeed, I hope the collaboration we have had since 1993 shall continue, and the "Pwagu na Pwaguzi" company shall flourishthroughou t our research career. Various people provided invaluable assistance during my laboratory work and stay in Wageningen. Leo Koopman, Frans van Angelen, Andre Gidding and Piet Huisman are thanked for making sure my mosquito colony was healthy and the olfactometer was well maintained. I am grateful to Piet Kostense for drawing most of the figures in this thesis. I thank Henk Snellen and Menno de Lind van Wijngaarden for taking me to various interesting parts of the Netherlands. Francoise, Nicolas and Daniel Takken, for making me feel welcome at their home. Kido Mtunda, Hawa Msham,
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