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Odour-mediated host-seeking behaviour of the Afro-tropical malaria vector Anopheles gambiaeGiles PDF

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Odour-mediated host-seeking behaviour of the Afro-tropical malaria vector Anopheles gambiae Giles Promotor: dr. J.C. van Lenteren Hoogleraar in de Entomologie, in het bijzonder de Oecologie der Insekten Co-promotor: dr. ir. W. Takken Universitair docent Medische en Veterinaire Entomologie A/tJ'oêïoi, £°5£. Bart G.J. Knols Odour-mediated host-seeking behaviour of the Afro-tropical malaria vector Anopheles gambiae Giles Proefschrift ter verkrijging van de graad van doctor in de landbouw- en milieuwetenschappen op gezag van de rector magnificus, Dr. C.M. Karssen, in het openbaar te verdedigen op vrijdag 23 februari 1996 des namiddags te half twee in de Aula van de Landbouwuniversiteit te Wageningen. »soi ^££150 CIP-DATA KONINKLIJKE BIBLIOTHEEK, DEN HAAG Knols, Bart Geert Jan Odour-mediated host-seeking behaviour of the Afro-tropical malaria vector Anopheles gambiae Giles / Bart Geert Jan Knols. - [S.l. : s.n.]. - 111. Thesis Wageningen. - With ref. - With summary in Dutch. ISBN 90-5485-487-1 Subject headings: Mosquitoes / host-seeking behaviour / malaria BIBLIOTHEEK LANDBOUVvOJNIVER5IT£îT WAGENINGEN The research described in this thesis was carried out at the Department of Entomology, Wageningen Agricultural University, The Netherlands and The National Institute for Medical Research, Tanzania and was funded by the European Community as part of the project 'Behavioural studies on malaria vectors' under contract numbers TS3-CT92-0101 and TS3-CT91-0032. Copyright 1996 Bart G.J. Knols. Cover photograph: The African malaria mosquito Anopheles gambiae s.s. feeding on a human arm (copyright Berry Geerligs, DUOTONE, Wageningen, The Netherlands). Stellingen 1. Voor een juiste interpretatie van het gastheerzoekgedrag van de Afrikaanse malariavektor Anopheles gambiae sensu stricto dient dit bestudeerd te worden binnen een multipartite kontext. Dit proefschrift. 2. Het nauwkeurig observeren van het gedrag van muggen rond een gastheer kan informatie verschaffen omtrent de origine van kairomonen en eventueel de breedte van het gastheerspectrum. Dit proefschrift. 3. Het gezegde 'van een mug een olifant maken' is wellicht van toepassing op de interpretatie van de behaalde resultaten met het malaria-vaccin SPf66 in een holo-endemisch gebied in Tanzania. Alonso, P.L. et al., 1994. Lancet, 344, 1175-1181. D'Alessandro, U. et al., 1995. Lancet, 346, 462-467. 4. Het voorstel tot het introduceren van transgene muggen in Afrika typeert het gemak waarmee technologieën die in het Westen de toets der maatschappelijke kritiek niet zouden weerstaan worden toegepast in ontwikkelingslanden. Hancock, G., 1989. Lords of Poverty. Macmillan, London. 5. Aangezien vektor-bestrijding middels het gebruik van pyrethroiden op klamboes niet wezenlijk verschilt van het gebruik van persistente middelen als DDT op wanden is de ontdekking van muggen-resistentie ertegen niet opzienbarend en zal resistentie slechts toenemen. Vulule, J.M. et al., 1994. Med. Vet. Entomol, 8, 71-75. Magesa, S.M. et al., 1994. Bull. Wld. Hlth. Org., 72, 737-7'40. 6. Het voortbestaan van nationale parken in Afrikaanse landen kan slechts dan worden gegarandeerd wanneer de lokale bevolking direkt economisch belang heeft bij de instandhouding ervan. 7. Het vernietigen van enorme hoeveelheden ivoor door de Keniaanse overheid is een zinloze mediastunt; de ban op de handel in ivoor zal het uitsterven van de Afrikaanse olifant (Loxodonta africana L.) juist bespoedigen. Bonner, R., 1993. At the hand of man, peril and hope for Africa's wildlife. Simon & Schuster, London. 8. Het toevoegen van een Nederlandstalige samenvatting aan een Engelstalig proefschrift is overbodig. 9. Het schijfje citroen in een glas witbier blijft de indruk wekken gezond bezig te zijn. 10. Werken voor de armen is een snelle manier om rijk te worden. 11. De term 'muggezifter' is sympathiek jegens malaria-entomologen. Stellingen behorend bij het proefschrift 'Odour-mediated host-seeking behaviour of the Afro-tropical malaria vector Anopheles gambiae Giles', Bart G.J. Knols Wageningen, 23 Februari 1996 Table of contents Preface 7 1. General introduction 11 Part I: Selection of biting sites by mosquitoes on man: a new approach to kairomone identification. 2. Selection of biting sites on man by four mosquito vectors (Diptera: Culicidae) of disease 53 3. Influence of human breath on selection of biting sites by the malaria mosquito Anopheles albimanus Wiedemann (Diptera: Culicidae) 69 Part II: Odour-mediated host-seeking behaviour and kairomone identification: a laboratory approach. A trapping system for testing olfactory responses of the malaria mosquito Anopheles gambiae s.s. Giles (Diptera: Culicidae) in a windtunnel 79 Olfactory responses of female Anopheles gambiae s.s. Giles (Diptera: Culicidae) to human breath or Limburger cheese in a windtunnel bioassay 89 Behavioural and electrophysiological responses of female malaria mosquito Anopheles gambiae s.s. (Diptera: Culicidae) to Limburger cheese volatiles 105 table of contents Part III: Host attractiveness and odour-mediated host-seeking behaviour of mosquitoes: a field approach. 7. Differential attractiveness of isolated humans to mosquitoes in Tanzania 127 8. Species-specific attraction of Anopheles mosquitoes (Diptera: Culicidae) to different humans in South-East Tanzania 135 9. Electric nets for studying odour-mediated host-seeking behaviour of mosquitoes (Diptera: Culicidae) 143 10. The response of Anopheles gambiae s.l. and An. funestus (Diptera: Culicidae) to tents baited with human odour or carbon dioxide in South East Tanzania 161 11. General discussion and conclusions 175 List of publications 195 Summary 197 Samenvatting 205 Curriculum vitae 213 Preface During the days that I was down with malaria deep in the Tanzanian bush, staring at the ceiling during sleepless nights, and hoping that the drugs I had taken would still be effective against the parasites in my body, I experienced what grave effect this disease has on the well-being of man in Africa. The scenes I sometimes witnessed in Tanzanian hospitals are unforgettable and made clear that the outlook for malaria control is grim. No matter how small the contribution of the research presented in this thesis to malaria control would be, these moments have always strongly motivated me, regardless of how difficult the work sometimes was. Besides this, there have been many people that, through discussions, cooperation and friendship, induced a similar effect in me. For almost two years, I had the pleasure to collaborate with Ruurd de Jong and our mutual enthusiasm for this subject led to some extraordinary findings. Letizia Mattiacci, you were often part of all this and your cheerfulness always created a great atmosphere. For more than eight years my co-promotor, Dr. Willem Takken, has created endless opportunities for me to become a 'fully grown' medical/veterinary entomologist. Willem, through your efforts I got my first job in Zambia and subsequently the opportunity to do a PhD for which I will always be most grateful. I sincerely thank Prof. Joop van Lenteren, first of all for accepting to be my promotor. Joop, our contacts were always brief but fruitful, and it was great that you found time to see our work in the Kilombero valley last year. Various people provided invaluable assistance during my laboratory work in Wageningen. Leo Koopman, Frans van Aggelen and André Gidding conscientiously reared (and fed!) mosquitoes. Ineke Buunk, your help in organising international travel, visa, and filling forms that were abracadabra to me will always be highly appreciated. Ans Klunder and Truus de Vries are also acknowledged for their secretarial help. Gerrit van den Brink, Gerard Schuurman, Barend Tollenaar and Gert Nieuwboer displayed some excellent craftsmanship in constructing the windtunnel and electric nets. Piet Kostense made some brilliant drawings of some of these gadgets. My sincere gratitude goes to all other OBP staff for their support in whatever way during my stay at the Binnenhaven. Of the scientific staff, some people were more directly involved in my preface work. Richard Stouthamer often had useful suggestions to improve the quality of manuscripts and Joop van Loon had a most valuable input in chapter 6 of this thesis. More recently Jocelijn Meijerink and Marieta Braks have had significant and stimulating inputs in the line of research and atmosphere in the 'mosquito group'. During the past three years several MSc students participated in my work and have made major contributions to it, for which I am most grateful. A special word of thanks to all other scientific staff, in particular PhD students, for being excellent company on those typical Friday afternoons from 17.00 hrs onwards. My research was part of a European Community funded project and was linked to research groups in England, Italy and Tanzania. Drs. Alan Cork, Rosemary Robinson and David Hall of the Natural Resources Institute, Chatham, are gratefully acknowledged for their hospitality and fruitful collaboration. Alan, your work has been an enormous contribution to this thesis and despite your incredible workload you were always there to do chemical analyses or discuss results. Useful discussions were held with Drs. John Brady, Gabriella Gibson and Carlo Costantini of Imperial College, London, and Prof. Mario Coluzzi of the Instituto di Parassitologia, Rome, during our annual meetings. Dr. Alessandra della Torre from the latter institute had a major input in chapter 10 by doing PCR analyses on hundreds of mosquitoes. Drs. Barend Mons and Marc de Bruyker coordinated the project at EC headquarters in Brussels and are thanked for providing institutional support and guidelines. In Tanzania all research was carried out in collaboration with the National Institute for Medical Research. First and foremost I want to thank the Director General Prof. Wen Kilama for allowing me to do research at the institute's stations in Muheza and Ifakara. In Muheza the former Director Dr. Yohanna Matola and in Ifakara the Director Dr. Andrew Kitua are acknowledged for their hospitality and support. Dr. Edith Lyimo and Ikupa Akim played a significant role in making me (and Leonard) feel at home in Ifakara. Thank you both for your hospitality during the many times we gate crashed hungry and exhausted. Many of the staff of the Ifakara centre and Ubwari field station (Muheza) contributed in one or the other way to our work or social well-being for which you are all thanked. Special thanks to Dr. K. Njunwa, head of Ubwari field station and Tony and Dorothy Wilkes. Tony,

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Part III: Host attractiveness and odour-mediated host-seeking behaviour of mosquitoes: a field approach. 7. Differential attractiveness of isolated
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