MOSQUITOES AND THEIR CONTROL

MOSQUITOES AND THEIR CONTROL

MOSQUITOES AND THEIR CONTROL Norbert Becker German Mosquito Control Association (KABS) Waldsee, Germany and Dusan Petrie University of Novi Sad Novi Sad, Yugoslavia Clive Boase The Pest Management Consultancy Haverhill, UK John Lane London School of Hygiene and Tropical Medicine (retired) London, England Marija Zgomba University of Novi Sad Novi Sad, Yugoslavia Christine Dahl Uppsala University Uppsala, Sweden Achim Kaiser German Mosquito Control Association (KABS) Waldsee, Germany Springer Science+Business Media, LLC

ISBN 978-1-4757-5899-3 DOI 10.1007/978-1-4757-5897-9 ISBN 978-1-4757-5897-9 (ebook) 2003 Springer Science+ Business Media New York Originally published by Kluwer Academic/Plenum Publishers, New York in 2003 Softcover reprint of the hardcover 1st edition 2003 http://www.wkap.nl/ 10987654321 A C.I.P. record for this book is available from the Library of Congress All rights reserved No part of this book may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, microfilming, recording, or otherwise, without written permission from the Publisher. with the exception of any material supplied specifically for the purpose of being entered and executed on a computer system, for exclusive use by the purchaser of the work.

Foreword Mankind has been plagued by mosquitoes as nuisances and as vectors of mosquito-borne diseases for centuries, resulting in inestimable economic losses and indeterminable human suffering. Mosquitoes transmit some of the deadliest diseases known to man-malaria and yellow feveras well as dengue, encephalitis, filariasis and a hundred or so other maladies. In spite of decades of mosquito control efforts throughout affected regions worldwide, this scourge has not left us and our present-day overpopulated, jet-linked world remains on the edge of resurgence and outbreaks of old and new mosquito-borne disease epidemics. Ninety-two mosquito species of more than 3200 recorded worldwide, traverse the European continent. In Europe malaria was eradicated ca. 50 years ago. Current trends in re-emerging mosquito-borne infectious diseases, exemplified by increasing numbers of imported malaria cases and recent outbreaks of West Nile Fever (WNF) virus, however, have given rise to growing public concern. Seasonal outbreaks of nuisance mosquito populations, which plague ecologically sensitive tourist and urban areas cause significant economic damage and constitute the major problem in Europe. This book is the product of a monumental task of collecting, processing and organising vital information on the mosquito populations of Europe. It presents a multitude of information on the bionomics, systematics, ecology and control of both pestiferous (nuisance) and disease vectors in an easily readable style providing practical guidance and important information to both professional and layman alike. It is conveniently divided into four parts containing sixteen chapters. Part one deals with general information on systematics, morphology and biology of mosquitoes, their medical significance and a very useful subchapter on mosquito research that includes important techniques and technologies utilised in mosquito surveys for sampling eggs, larvae and adult mosquito populations. Part two contains keys to identification of larval and adult mosquito genera. Part three gives a very detailed and instructive account of the morphology, ecology and distribution of all 92 European species included in 8 genera: Anopheles, Aedes, Ochlerotatus, Culex, Culiseta, Coquillettidia, Orthopodomyia and Uranotaenia. This part is extremely important for species identification in any successful mosquito control or mosquito-borne disease surveillance programme. Part four dealing with control of mosquitoes is well ordered in seven sections: biological, chemical and physical control as well as personal protection, integrated pest management, implementation of survey methodologies and management. This information is particularly necessary for a comprehensive approach to both studying and controlling mosquitoes. This part distinctly demonstrates the tremendous experience that the authors possess over decades in mosquito biology and control. The section on biological control contains important information on predators, parasites and pathogens is of special significance in light of the increasing interest in replacing v

vi FOREWORD detrimental chemical pesticides with environmentally friendly integrated biological control (IBC) technologies. The authors of this book collectively possess a vast amount of knowledge and experience in the relevant topics and they have meticulously gathered and incorporated the experience and knowledge of others to compose the first and only comprehensive treatise on the subject of European mosquitoes. This book is a valuable tool for vector ecologists, entomologists, and all those involved with mosquito control, biology, ecology and systematics in Europe. It's primary beneficiaries will be the students, scientists and professionals dealing on a day-to-day basis with mosquitoes and their control. Society as a whole stands to gain from improved, environmentally responsible mosquito management programmes designed on the basis of the broader understanding of mosquitoes and their control provided in this enlightening book. Yoel Margalith, Ph.D Tyler Prize Laureate Center for Biological Control Ben Gurian University of the Negev, Israel

Preface Throughout the world, mosquitoes interact with man in many different ways. However, despite the very extensive research on these interactions, there remains much that is not yet fully understood. The attempt by the authors of this volume, is to highlight the importance of a basic knowledge of mosquito biology as a basis for successful control operations. When compared to the Curculionidae, the largest family in the animal kingdom, with 35 000 known species, the Culicidae, numbering more than 3200 species, could be ranked as a family of only small to moderate size. Even though yield losses caused by weevils could be estimated in billions of dollars, mosquitoes are able to carry many lethal diseases in their bodies. By the time you have read this Preface (5 min.) ten human lives will have been lost due to plasmodian infections. Apart from being the well known vectors of life-threatening diseases, in some parts of the world mosquitoes may also occur in enormous numbers thus causing a significant reduction in human life quality and serious economic damage for instance in livestock. Ramsdale and Snow (1999) published a list of currently recognised European mosquito taxa with synonyms. They included 98 species in 7 genera and 17 subgenera. The authors of this volume, in deciding upon the species which should be covered, have come to the conclusion that the pertinent species are those which were recorded on more than one occasion at least, where type specimens have been deposited, identification material has been available, and where the position regarding the validity of the species is satisfactory. In addition to these requirements, information about geographical distribution with substantiating references was considered. Accordingly to this, 92 species and subspecies belonging to 8 genera and 18 subgenera are described and included in the keys. The following species or subspecies previously reported from Europe are not included in the list: Ochlerotatus gilcolladoi (Villa, Rodrigez, and Llera, 1985), was named from a form from central Spain differing in certain features of larval chaetotaxy from both Oc. echinus and Oc. geniculatus. The position regarding the validity of this species is unsatisfactory. Type specimens were not deposited, and material is not available for examination (Ramsdale and Snow, 1999). Oc. thibaulti (Dyar and Knab, 1909) is a Nearctic species, in Europe recorded from the river Dnieper, Ukraine (Gutsevitch and Goritskaya, 1970), but no longer found there according to Gutsevitch and Dubitsky (1987). Oc. atropalpus (Coquillett, 1902) is not considered here because it was only once reported from Italy and it is not regarded as a permanent species in the European area. For the species Oc. krymmontanus Alekseev 1989, Oc. coluzzii Rioux, Guilvard and Pasteur 1998, Oc. duplex Martini 1926, and Culex deserticola short notes are given in the description of the species. The principal objective, regarding the taxonomy and morphology chapters, is to provide an identification key to both adult females and males as well as to fourth-instar larvae, which vii

viii PREFACE incorporate all 92 species. At the beginning of chapters 6-8, keys for the identification of genera are given. Recently, Reinert (2000c) divided the composite genus Aedes Meigen into 2 genera, Ochlerotatus Lynch Arribalzaga and Aedes. Adults of these genera are distinguished primarily on the characters of the genitalia that require dissection. For this reason, the species belonging to these genera are treated in a single key. The illustrated keys are followed by a detailed description of the morphology, biology and distribution of each species. The morphological terms engaged in this volume are somewhat changed from those used by Harbach and Knight (1980, 1981), taking into consideration homology, phylogeny and their general use among the dipterous insects. When a specimen has been keyed out, it should be compared with the description of that species to use the additional information as a cross-check. The description of the species is given according to the examination of the Peus collection, as well as a considerable number of species sampled in different European regions and various literature sources. Characters of fourth-instar larvae are often clearer than those of the adults, and many taxonomists prefer to identify mosquitoes in this stage. Since there is a certain degree of variation among larvae of a species, it is best to identify, if possible, from a series of specimens. Rare exceptions to key characters can almost always be found. More important variations and their relative frequency are indicated in the systematic section of the species. In the keys the larval chaetotaxy of the thorax and abdomen is not used to such an extent as by other authors. This seems to be a little bit "old fashioned", but on the other hand, quite often setae may be broken off, lying in a misleading or barely visible position in slide preparations or, in the worst case, are totally missing. If the latter occurs, an experienced eye is needed to see the alveola or tubercle of the missing seta. Although eggs, early instar larvae and pupae of most European species are known, they are more difficult to identify than adults and fourth-instar larvae. Rearing eggs to fourth-instar larvae and pupae to adults is easier and less time consuming than to identify them in the early stages. The authors suggest that the user should study the sections on general morphology before starting to identify specimens. The user should also be familiar with the proper sampling and mounting techniques of adults and larvae, because the presence of a full set of scales, setae and other features is essential for identification. Updated mosquito distribution throughout Europe, together with the bioecological conditions to be met for each species, should also help in the species identification. The territory of Europe, despite not being a distinct zoogeographical region, is chosen in an attempt to provide for the first time a unique key for the whole European region. The authors' intention is to encourage and give support to every person who intends to start, or already has some experience in, mosquito control. The concept of the book is also based on several fields of knowledge which are important for everyone who deals with mosquitoes. Overviews on mosquito taxonomy, morphology, biology, biological, physical and chemical control measures are given, to complete the information needed for a comprehensive approach to both studying and controlling mosquitoes. Mosquito control measures are dependent on many complex and interacting factors ranging from biological (species dependent), abiotic and physical factors influencing the phenology and abundance of mosquitoes (terrain features, climate, types of breeding sites etc.) to administrative, organisational and most certainly economical conditions. A decision to use one or another mosquito control measure is highly dependent on a basic knowledge of all aspects of the target species, and the impact of a chosen control method on the target and non-target organisms, as well as on the environment. A professional control programme should combine cost effectiveness,

PREFACE ix acceptable level of mosquito population suppression, and an environmentally sensitive approach. In some situations it is possible to rely on inexpensive and simple methods such as applying fragments of copper wire into flower pots for the control of Aedes albopictus larvae (Bellini, pers. comm.), while in others only pure biological, highly selective control measures are allowed, such as in the Upper Rhine Valley where almost the entire mosquito control programme in the river flood-plains has relied solely on Bacillus thuringiensis ssp. israelensis larviciding for several decades. Sections on different approaches in mosquito control (chemical, biological, physical, integrated or personal protection) provide basic information about different methods of using products with different formulation and toxicological features, effectiveness on target species, as well as their impact on non-target organisms. Information from this part of the volume attempts to serve as a basis for an appropriate mosquito control operation, allowing the user to live in relative safety from some vector-borne diseases, to alleviate the effects of abundant nuisance populations, to re-establish wetlands, and to share and enjoy nature by conserving the biodiversity, by using environmentally friendly control tools. Up to now a comprehensive book in which the taxonomy, biology and distribution of all currently known European mosquito species are described, as well as the options for their control, has been missing. This volume should fill the gap and be a valuable help to scientists and indeed all those interested in, or working in any of the fields related to the Culicidae. It should provide guidance to field workers concerned with mosquito control and who wish, for example, to learn more about the behaviour of the species in their region, about mosquito breeding sites, or about the mosquito control techniques and options that may be suitable for each specific environment. Since there is still much information which for some, despite greatly increased access to the Internet, may be difficult to acquire, we have tried to include and summarise all available information, so that entomologists can apply it to their own situations. The authors

Acknowledgements We are most indebted to Paul Schadler, President of the German Mosquito Control Association (KABS, Waldsee) and the members of the KABS, Herbert W. Ludwig (University of Heidelberg, Germany) and Wolfgang Schnetter (University of Heidelberg, Germany), who encouraged the preparation of this work. This book developed thanks to valuable information provided by our colleagues and friends worldwide. Herewith we would like to thank the following contributors who supplied a variety of information: Carlos Aranda (Consell Comarcal del Baix Llobregat, Spain), Andreas Arnold (KABS, Germany), Romeo Bellini (Centro Agricoltura Ambiente, Italy), Roger Eritja (SCM, Consell Comarcal del Baix Llobregat, Spain), Raul Escosa (CODE, Ebro Delta, Spain), Remi Foussadier (E.I.D., Rhone-Alpes, France), Jose Carlos Galvez (SCM, Huelva County Council, Spain), Aleksandra Gliniewicz (National Institute of Hygiene, Poland), Raymond Gruffaz (E.I.D., Rhone-Alpes, France), Klaus Hoffmann (KABS, Germany), Karch Sa.ld (SIIAP Paris, France), Beata Kubica-Biernat (University of Gdynia, Poland), Oszkar Kufcsak (Bay Zoltan Foundation, Szeged, Hungary), Christophe Lagneau (E.I.D. Mediterranee, France), Peter Luthy (University of Zurich, Switzerland), Jan Lundstrom (University of Uppsala, Sweden), Minoo B. Madon (Greater Los Angeles County Vector Control District, USA), Eduard Marques i Mora (SCM, Roses Bay and Lower Ter, Spain), Jean-Pierre Mas (E.I.D. Atlantique, France), Enrih Merdic (University of Osijek, Croatia), Spiros Mourelatos ((Environment, Public Health and Ecodevelopment, Greece), Odile Moussiegt (E.I.D. Mediterranee, France), Francoise Pfirsch (Mosquito Control Organization, Bas-Rhin, France), Dirk Reichle (KABS, Germany), Frantisek Rettich (National Institute of Public Health, Czech Republic), Martina Schafer (University of Uppsala, Sweden), Francis Schaffner (E.I.D. Mediterranee, France), Elzibeta Wegner (Institute of Zoology, Warszawa, Poland), and Thomas Weitzel (KABS, Germany). The authors express appreciation for the skillful and diligent preparations of the illustrations to Miguel Neri (University of San Carlos, Cebu, Philippines), Michael Gottwald (University of Heidelberg, Germany), Vlada Vojnic-Hajduk (University of Novi Sad, Serbia and Monte Negro) and Aung Moe (University of Heidelberg, Germany). We are grateful to numerous individuals and organizations who assisted in various ways towards the final form of this book, especially to Matthias Beck (Waldangelloch, Germany), Geoffrey L. Brown (Heidelberg, Germany), Djamal Chakhmaliev (Heidelberg, Germany), Jeff Charles (Institute Pasteur, Paris, France), A.D. Ciklonizacija (Novi Sad, Serbia and Monte Negro), Culinex GmbH (Ludwigshafen, Germany), Major Dhillon (Northwest MVCD, Corona, USA), Elisabeth and Albert Gasparich (Heidelberg, Germany), Gesellschaft zur Forderung der Stechmuckenbekampfung (GFS, Waldsee, Germany), Thomas Heeger (Bohl-Iggelheim, Germany), Mikael Henriksson (Borga, Finland), Icybac GmbH (Speyer, Germany), Thomas Imhof xi

xii ACKNOWLEDGEMENTS (Heidelberg, Germany), Michael Kinzig (Heidelberg, Germany), Roland Kuhn (University of Mainz, Germany), Milagros Mahilum (University of Heidelberg, Germany), Jessica Munns (Pioneer, USA), Charles M. Myers (Glendora, USA), Beate Ruch-Heeger (Bohl-lggelheim, Germany), Volker Storch (University of Heidelberg, Germany), Alexander Tahori (Ben Gurion University, Israel), Thin Thin Oo (University of Heidelberg, Germany), and Ute Timmermann (Weinheim, Germany).

Contents Introduction 1 I. GENERAL ASPECTS 1. Systematics s 2. Biology of Mosquitoes................................................ 9 2.1. Oviposition.................................................... 9 2.2. Embryonic development.......................................... 13 2.3. Hatching...................................................... 14 2.4. Larvae........................................................ 18 2.5. Pupae........................................................ 21 2.6. Adults........................................................ 21 2.6.1. Emergence.............................................. 21 2.6.2. Mating................................................. 22 2.6.3. Dispersal and host-seeking behaviour.......................... 23 2.6.4. Feeding................................................. 25 2.7. Hibernation.................................................... 26 2.7.1. Egg stage............................................... 27 2. 7.2. Larval stage.............................................. 27 2.7.3. Adult stage.............................................. 27 3. Medical Importance of Mosquitoes..................................... 29 3.1. Malaria....................................................... 29 3.2. Virosis........................................................ 34 3.2.1. Togaviridae (Alphavirus).................................... 36 (a) The Sindbis virus complex............................... 36 (b) Viruses of the Semliki forest complex....................... 36 3.2.2. Flaviviridae (Flavivirus).................................... 36 3.2.3. Bunyaviridae (Bunyavirus).................................. 37 3.3. Filariasis...................................................... 38 3.4. Conclusions.................................................... 39 xiii

xiv 4. Mosquito Research CONTENTS 41 4.1. Sampling of mosquito eggs.... 4.1.1. Anopheles eggs.... 4.1.2. Egg rafts.... 4.1.3. Aedes/Ochlerotatus eggs.... 4.1.4. Eggs in artificial ovipositon sites.... 4.2. Sampling of mosquito larvae.... 4.3. Sampling of adult mosquitoes.... 4.3.1. Bait catches.... 4.3.2. Carbon dioxide/light trap.... 4.3.3. The mosquito magnet.... 4.4. Preserving mosquitoes.... 4.4.1. Larvae.... 4.4.2. Pupae.... 4.4.3. Adults.... 4.5. Rearing mosquitoes.... 4.6. Methods for measuring the physiological stage.... 4. 7. Morphological studies.... 4.8. Cytodiagnostic methods for the identification of sibling species.... 4.9. Biochemical and molecular methods in studies on systematics.... 4.10. Ecological and behavioural studies.... 41 41 41 42 43 44 45 45 46 48 48 48 49 49 51 52 53 53 54 55 5. Morphology of Mosquitoes.... 5.1. Adults.... 5.1.1. Head.... 5.1.2. Thorax.... 5.1.3. Abdomen.... 5.2. Larvae.... 5.2.1. Head.... 5.2.2. Thorax.... 5.2.3. Abdomen.... 5.3. Pupae 57 57 59 61 68 72 74 76 76 81 II. THE IDENTIFICATION KEYS 6. Key to Female Mosquitoes............................................ 87 Genera............................................................ 87 6.1. Genus Anopheles................................................ 88 6.2. Genera Aedes and Ochlerotatus..................................... 92 6.3. Genus Culex................................................... 103

CONTENTS XV 6.4. Genus Culiseta.... 105 6.5. Genus Coquillettidia.... 108 7. Key to Male Mosquitoes.... 109 Genera.... 109 7.1. Genus Anopheles.... 111 7.2. Genera Aedes and Ochlerotatus.... 114 7.3. Genus Culex.... 125 7.4. Genus Culiseta.... 129 7.5. Genus Coquillettidia.... 131 8. Key to Mosquito Fourth-Instar Larvae.... 133 Genera.... 133 8.1. Genus Anopheles..... 135 8.2. Genera Aedes and Ochlerotatus.... 139 8.3. Genus Culex.... 152 8.4. Genus Culiseta.... 157 8.5. Genus Coquillettidia.... 160 III. MORPHOLOGY, ECOLOGY AND DISTRIBUTION OF EUROPEAN SPECIES 9. Subfamily Anophelinae............................................... 163 9.1. Genus Anopheles Meigen......................................... 164 9.1.1. Subgenus Anopheles Meigen................................ 165 Anopheles (Anopheles) algeriensis Theobald 1903............... 165 Anopheles Claviger Complex............................... 167 Anopheles (Anopheles) claviger s.s. (Meigen) 1804............. 167 Anopheles (Anopheles) petragnani Del Vecchio 1939........... 169 Anopheles (Anopheles) hyrcanus (Pallas) 1771.................. 170 Anopheles Maculipennis Complex............................ 172 Anopheles (Anopheles) atroparvus Van Thiel1927............. 175 Anopheles (Anopheles) beklemishevi Stegnii and Kabanova 1976.. 176 Anopheles (Anopheles) labranchiae Falleroni 1926............. 176 Anopheles (Anopheles) maculipennis s.s. Meigen 1818.......... 177 Anopheles (Anopheles) melanoon Hackett 1934................ 177 Anopheles (Anopheles) messeae Falleroni 1926................ 178 Anopheles (Anopheles) sacharovi Favre 1903................. 178 Anopheles (Anopheles) subalpinus Hackett and Lewis 1935... 179 Anopheles (Anopheles) marteri Senevet and Prunnelle 1927........ 180 Anopheles (Anopheles) plumbeus Stephens 1828................. 182

xvi CONTENTS 9.1.2. Subgenus Cellia Theobald.................................. 184 Anopheles (Cellia) cinereus Theobald 1901..................... 184 Anopheles (Cellia) cinereus hispaniola (Theobald) 1903........... 185 Anopheles (Cellia) multicolor Cambouliu 1902.................. 186 Anopheles (Cellia) sergentii (Theobald) 1907................... 188 Anopheles (Cellia) superpictus Grassi 1899..................... 190 10. Subfamily Culicinae................................................. 193 10.1. Genus Aedes Meigen............................................. 193 10.1.1. Subgenus Aedes Meigen................................... 194 Aedes (Aedes) cinereus Meigen 1818......................... 195 Aedes (Aedes) geminus Peus 1970............................ 198 Aedes (Aedes) rossicus Dolbeskin, Gorickaja and Mitrofanova 1930.. 199 10.1.2. Subgenus Aedimorphus Theobald............................ 201 Aedes (Aedimorphus) vexans (Meigen) 1830.................... 201 10.1.3. Subgenus Fredwardsius Reinert.............................. 204 Aedes (Fredwardsius) vittatus (Bigot) 1861..................... 204 10.1.4. Subgenus Stegomyia Theobald.............................. 206 Aedes (Stegomyia) aegypti (Linnaeus) 1762..................... 207 Aedes (Stegomyia) albopictus (Skuse) 1895..................... 210 Aedes (Stegomyia) cretinus Edwards 1921...................... 212 10.2. Genus Ochlerotatus Lynch Arribalzaga............................... 214 10.2.1. Subgenus Finlaya Theobald................................. 214 Ochlerotatus (Finlay a) echinus Edwards 1920................... 214 Ochlerotatus (Finlaya) geniculatus (Olivier) 1791................ 216 10.2.2. Subgenus Ochlerotatus Lynch Arribalzaga...................... 217 Ochlerotatus (Ochlerotatus) annulipes (Meigen) 1830............. 219 Ochlerotatus (Ochlerotatus) behningi (Martini) 1926.............. 221 Ochlerotatus (Ochlerotatus) berlandi (Seguy) 1921............... 223 Ochlerotatus ( Ochlerotatus) cantans (Meigen) 1818.............. 225 Ochlerotatus Caspius Complex.............................. 227 Ochlerotatus ( Ochlerotatus) caspius (Pallas) 1771.............. 227 Ochlerotatus (Ochlerotatus) cataphylla (Dyar) 1916.............. 230 Ochlerotatus Communis Complex............................ 231 Ochlerotatus (Ochlerotatus) communis (De Geer) 1776.......... 232 Ochlerotatus (Ochlerotatus) cyprius (Ludlow) 1920............... 233 Ochlerotatus Detritus Complex.............................. 235 Ochlerotatus (Ochlerotatus) detritus (Haliday) 1833............ 235 Ochlerotatus ( Ochlerotatus) diantaeus (Howard, Dyar and Knab) 1913.................................... 237 Ochlerotatus (Ochlerotatus) dorsalis (Meigen) 1830.............. 239 Ochlerotatus Excrucians Complex............................ 241 Ochlerotatus ( Ochlerotatus) euedes (Howard, Dyar and Knab) 1913................................... 241

CONTENTS xvii Ochlerotatus (Ochlerotatus) excrucians (Walker) 1856.......... 243 Ochlerotatus (Ochlerotatus) surcou.fi (Theobald) 1912........... 244 Ochlerotatus ( Ochlerotatus) jlavescens (Muller) 1764.............. 245 Ochlerotatus (Ochlerotatus) hexodontus (Dyar) 1916.............. 247 Ochlerotatus (Ochlerotatus) hungaricus (Mihalyi) 1955............ 249 Ochlerotatus (Ochlerotatus) impiger (Walker) 1848............... 250 Ochlerotatus (Ochlerotatus) intrudens (Dyar) 1919................ 252 Ochlerotatus (Ochlerotatus) leucomelas (Meigen) 1804............ 253 Ochlerotatus Mariae Complex................................ 255 Ochlerotatus (Ochlerotatus) mariae (Sergent and Sergent) 1903.... 255 Ochlerotatus ( Ochlerotatus) zammitii (Theobald) 1903........... 257 Ochlerotatus (Ochlerotatus) mercurator (Dyar) 1920.............. 257 Ochlerotatus (Ochlerotatus) nigrinus (Eckstein) 1918.............. 259 Ochlerotatus (Ochlerotatus) nigripes (Zetterstedt) 1838............ 260 Ochlerotatus (Ochlerotatus) pionips (Dyar) 1919................. 262 Ochlerotatus ( Ochlerotatus) pulcritarsis (Rondani) 1872........... 264 Ochlerotatus (Ochlerotatus) pullatus (Coquillett) 1904............. 265 Ochlerotatus (Ochlerotatus) punctodes (Dyar) 1922............... 267 Ochlerotatus (Ochlerotatus) punctor (Kirby) 1837................ 268 Ochlerotatus ( Ochlerotatus) riparius (Dyar and Knab) 1907......... 270 Ochlerotatus (Ochlerotatus) sticticus (Meigen) 1838.............. 272 10.2.3. Subgenus Rusticoidus Shevchenko and Prudkina................. 274 Ochlerotatus (Rusticoidus) lepidonotus (Edwards) 1920............ 274 Ochlerotatus (Rusticoidus) quasirusticus (Torres Canamares) 1951.... 276 Ochlerotatus (Rusticoidus) re.fiki (Medschid) 1928................ 277 Ochlerotatus (Rusticoidus) rusticus (Rossi) 1790................. 279 Ochlerotatus (Rusticoidus) subdiversus (Martini) 1926............. 281 10.3. Genus Culex Linnaeus............................................ 283 10.3.1. Subgenus Barraudius Edwards............................... 284 Culex (Barraudius) modestus Ficalbi 1889...................... 284 Culex ( Barraudius) pus ill us Macquart 1850..................... 286 10.3.2. Subgenus Culex Linnaeus................................... 288 Culex (Culex) brumpti Galliard 1931.......................... 289 Culex (Culex) laticinctus Edwards 1913........................ 290 Culex (Culex) mimeticus Noe 1899............................ 292 Culex (Culex) perexiguus Theobald 1903....................... 294 Culex Pipiens Complex..................................... 295 Culex (Culex) pipiens pipiens Linnaeus 1758.................. 296 Culex pipiens pipiens biotype molestus Forskal1775............ 298 Culex (Culex) torrentium Martini 1925....................... 299 Culex (Culex) theileri Theobald 1903.......................... 300 10.3.3. Subgenus Maillotia Theobald................................ 302 Culex (Maillotia) hortensis Ficalbi 1889........................ 303 10.3.4. Subgenus Neoculex Dyar................................... 305 Culex (Neoculex) impudicus Ficalbi 1890....................... 305

xviii CONTENTS Culex (Neoculex) martinii Medschid 1930...................... 307 Culex (Neoculex) territans Walker 1856........................ 308 10.4. Genus Culiseta Felt.............................................. 310 10.4.1. Subgenus Allotheobaldia Broelemann......................... 311 Culiseta (Allotheobaldia) longiareolata (Macquart) 1838.......... 311 10.4.2. Subgenus Culicella Felt.................................... 313 Culiseta (Culicella)fumipennis (Stephens) 1825................. 313 Culiseta (Culicella) litorea (Shute) 1928....................... 315 Culiseta (Culicella) morsitans (Theobald) 1901.................. 317 Culiseta (Culicella) ochroptera (Peus) 1935..................... 319 10.4.3. Subgenus Culiseta Felt.................................... 321 Culiseta (Culiseta) alaskaensis (Ludlow) 1906................... 322 Culiseta (Culiseta) annulata (Schrank) 1776.................... 324 Culiseta (Culiseta) bergrothi (Edwards) 1921.................... 326 Culiseta (Culiseta) glaphyroptera (Schiner) 1864................. 328 Culiseta (Culiseta) subochrea (Edwards) 1921................... 330 10.5. Genus Coquillettidia Dyar......................................... 332 10.5.1. Subgenus Coquillettidia Dyar............................... 333 Coquillettidia (Coquillettidia) buxtoni (Edwards) 1923............. 333 Coquillettidia (Coquillettidia) richiardii (Ficalbi) 1889............ 333 10.6. Genus Orthopodomyia Theobald.................................... 336 Orthopodomyia pulcripalpis (Rondani) 1872.................... 336 10.7. Genus Uranotaenia Lynch Arribalzaga............................... 338 10.7.1. Subgenus Pseudoficalbia Theobald........................... 339 Uranotaenia (Pseudoficalbia) unguiculata Edwards 1913.......... 339 IV. CONTROL OF MOSQUITOES 11. Biological Control 345 11.1. Introduction.................................................... 345 11.2. Predators...................................................... 346 11.2.1. Vertebrate predators....................................... 346 11.2.1.1. Fish (Osteichthyes)............................... 346 11.2.1.2. Amphibians (Amphibia)........................... 350 11.2.1.3. Birds (Aves).................................... 350 11.2.1.4. Bats (Mammalia)................................ 351 11.2.2. Invertebrate predators..................................... 353 11.2.2.1. Hydras (Coelenterata)............................. 353 11.2.2.2. Flatworms (Turbellaria)........................... 354 11.2.2.3. Freshwater snails (Gastropoda)...................... 354 11.2.2.4. Leeches (Hirudinea).............................. 354

CONTENTS xix 11.2.2.5. Spiders and mites (Arachnida).... 355 11.2.2.6. Crustaceans (Crustacea).... 355 11.2.2.7. Insects (Insecta).... 355 11.3. Parasites.... 359 11.3.1. Nematodes.... 359 11.4. Pathogens.... 360 11.4.1. Fungi.... 360 11.4.2. Protozoa.... 362 11.4.3. Bacteria.... 363 11.4.3.I. Bacillus thuringiensis israelensis.... 364 11.4.3.2. Bacillus sphaericus..... 365 11.4.4. Viruses.... 374 12. Chemical Control..... 377 12.1. History....................................................... 377 12.2. Insecticides.... 379 12.2.1. Classification of insecticides.... 380 12.2.2. Insecticide formulations.... 380 12.2.3. Insecticide application techniques.... 384 12.3. Different chemical groups of insecticides.... 386 12.3.I. Chlorinated hydrocarbons.................................. 386 12.3.2. Organophosphates.... 387 12.3.3. Carbamates.... 393 12.3.4. Pyrethroids.... 394 12.3.5. Insect growth regulators.... 398 12.3.6. Novel insecticide classes.... 402 12.4. Management and monitoring of insecticide resistance.... 403 12.4.1. Resistance mechanisms.... 403 12.4.2. Resistance surveillance.... 404 12.4.3. Resistance management..... 404 13. Physical Control................................................. 407 13.1. Sanitation.... 407 13.2. Water management.... 408 13.3. Modification of the water-air interface.... 408 13.3.1. Oil..... 408 13.3.2. Surface films.... 408 13.3.2.1. Liparol.... 409 13.3.2.2. Monomolecular surface films (MSF).... 409 13.3.3. Polystyrene beads.... 410 13.4. Reduction of human-mosquito contact.... 410

XX CONTENTS 14. Personal Protection................................................. 411 14.1. Impregnated bed nets............................................. 411 14.2. Repellents against mosquitoes...................................... 412 14.2.1. Repellents on skin or clothing............................... 412 14.2.2. Mosquito coils........................................... 414 14.2.3. Vapourising mats... 414 14.2.4. Liquid vapouriser........................................ 415 15. Integrated Pest Management.......................................... 417 15.1. Mosquito management research..................................... 417 15.2. Socio-economic aspects of mosquito control........................... 418 15.3. Action thresholds as a component of integrated mosquito management............................................ 419 15.4. Information dissemination......................................... 420 15.5. IPM techniques................................................. 421 15.6. Insecticide registration and usage.................................... 421 16. Implementation and Integration of Mosquito Control Measures into Routine Treatments.............................................. 425 16.1. Prerequisites for the successful implementation of the programme........... 427 16.1.1. Entomological studies..................................... 427 16.1.2. Mapping of the breeding sites............................... 428 16.1.3. Selection of appropriate tools............................... 429 16.1.4. Effective dosage assessment................................ 429 16.1.5. Design of the control strategy............................... 430 16.1.6. Training of field staff...................................... 431 16.1.7. Governmental application requirements........................ 431 16.1.8. Public information systems................................. 431 16.1.9. Community participation................................... 431 16.2. Routine treatments............................................... 432 16.2.1. Mosquito control in Croatia................................. 432 16.2.2. Mosquito control in Czech and Slovak Republics................ 433 16.2.3. Mosquito control in France................................. 434 16.2.4. Mosquito control in Germany............................... 434 16.2.5. Mosquito control in Greece................................. 438 16.2.6. Mosquito control in Hungary................................ 439 16.2.7. Mosquito control in Italy................................... 440 16.2.8. Mosquito control in Poland................................. 442 16.2.9. Mosquito control in Spain.................................. 443

CONTENTS xxi 16.2.10. Mosquito control in Sweden................................ 445 16.2.11. Mosquito control in Switzerland............................. 446 16.2.12. Mosquito control in Yugoslavia.............................. 449 References............................................................ 453 Subject Index.......................................................... 487 Taxonomic Index....................................................... 493