Medical Entomology for Stud (Z-Library).pdf

Medical Entomology for Students FIFTH EDITION Despite numerous scientiﬁc investigations on vector-borne human infec- tions such as malaria, ﬁlariasis, Lyme disease and typhus, these diseases continue to threaten human health. Understanding the role of vectors in disease transmission, and the most appropriate control strategies, is there- fore essential. This book provides information on the recognition, biology, ecology and medical importance of the arthropods that affect human health. The ﬁfth edition of this popular textbook is completely updated, incor- porating the latest strategies for controlling insects, ticks and mites. Numerous illustrations, with new colour photographs of some of the most important vectors, aid recognition. A glossary of entomological and epidemiological terms is included, along with a list of commonly used insecticides and their trade names. Clearly presented in a concise style, this text is aimed at students of medical entomology, tropical medicine, parasitology and pest control. It is also essential reading for physicians, health ofﬁcials and community health workers. mi ke s er vice is a world authority on medical entomology and has over 50 years’ experience of research and teaching in the ﬁeld. He is Emeritus Professor of Medical Entomology at the Liverpool School of Tropical Medicine. In 1997 he was awarded the Sir Rickard Christophers medal by the Royal Society of Tropical Medicine and Hygiene, and in 2002 the Harry Hoogstraal Medal by the American Society of Tropical Medicine and Parasitology, for research on medical vectors. Medical Entomology for Students Fifth Edition Mike Service Emeritus Professor of Medical Entomology, Liverpool School of Tropical Medicine, Liverpool, UK cambridge university press Cambridge, New York, Melbourne, Madrid, Cape Town, Singapore, São Paulo, Delhi, Mexico City Cambridge University Press The Edinburgh Building, Cambridge CB2 8RU, UK Published in the United States of America by Cambridge University Press, New York www.cambridge.org Information on this title: www.cambridge.org/9781107668188 © M. Service 2012 This publication is in copyright. Subject to statutory exception and to the provisions of relevant collective licensing agreements, no reproduction of any part may take place without the written permission of Cambridge University Press. First published by Chapman & Hall 1996 Second edition published by Cambridge University Press 2000 Third edition published 2004 Fourth edition published 2008 Fifth edition published 2012 Printed in the United Kingdom at the University Press, Cambridge A catalogue record for this publication is available from the British Library ISBN 978-1-107-66818-8 Paperback Cambridge University Press has no responsibility for the persistence or accuracy of URLs for external or third-party internet websites referred to in this publication, and does not guarantee that any content on such websites is, or will remain, accurate or appropriate. Every effort has been made in preparing this book to provide accurate and up-to-date information which is in accord with accepted standards and practice at the time of publication. Although case histories are drawn from actual cases, every effort has been made to disguise the identities of the individuals involved. Nevertheless, the authors, editors and publishers can make no warranties that the information contained herein is totally free from error, not least because clinical standards are constantly changing through research and regulation. The authors, editors and publishers therefore disclaim all liability for direct or consequential damages resulting from the use of material contained in this book. Readers are strongly advised to pay careful attention to information provided by the manufacturer of any drugs or equipment that they plan to use. To Wendy, for all her help over many years with this and previous publications Contents Preface to the ﬁrst edition page xi Preface to the second edition xiii Preface to the third edition xv Preface to the fourth edition xvii Preface to the ﬁfth edition xix Acknowledgements xx 1 Introduction to mosquitoes (Culicidae) 1 1.1 External morphology 2 1.2 Life cycle 6 1.3 Classiﬁcation of mosquitoes 12 1.4 Medical importance 22 1.5 Mosquito control 22 Further reading 31 2 Anopheline mosquitoes (Anophelinae) 34 2.1 External morphology 35 2.2 Life cycle 35 2.3 Medical importance 37 2.4 Control 48 Further reading 51 3 Culicine mosquitoes (Culicinae) 54 3.1 Culex mosquitoes 55 3.2 Aedes mosquitoes 57 3.3 Haemagogus mosquitoes 61 3.4 Sabethes mosquitoes 62 3.5 Mansonia mosquitoes 64 3.6 Coquillettidia mosquitoes 66 3.7 Psorophora mosquitoes 66 3.8 Medical importance 67 3.9 Control 79 Further reading 82 4 Black ﬂies (Simuliidae) 85 4.1 External morphology 86 4.2 Life cycle 88 4.3 Medical importance 92 viii Contents 4.4 Control 94 Further reading 96 5 Phlebotomine sand ﬂies (Phlebotominae) 98 5.1 External morphology 99 5.2 Life cycle 100 5.3 Medical importance 103 5.4 Control 105 Further reading 106 6 Biting midges (Ceratopogonidae) 108 6.1 External morphology 109 6.2 Life cycle 110 6.3 Medical importance 112 6.4 Control 114 Further reading 115 7 Horse ﬂies (Tabanidae) 116 7.1 External morphology 117 7.2 Life cycle 120 7.3 Medical importance 123 7.4 Control 124 Further reading 124 8 Tsetse ﬂies (Glossinidae) 126 8.1 External morphology 127 8.2 Life cycle 130 8.3 Medical importance 134 8.4 Control 136 Further reading 137 9 House ﬂies and stable ﬂies (Muscidae) and latrine ﬂies (Fanniidae) 139 9.1 The common house ﬂy (Musca domestica) 140 9.2 The greater house ﬂy (Muscina stabulans) 149 9.3 The stable ﬂy (Stomoxys calcitrans) 151 9.4 The lesser or little house ﬂy and the latrine ﬂy (Fannia species) 153 Further reading 155 10 Flies and myiasis 157 10.1 Types of myiasis 158 10.2 Classiﬁcation 159 10.3 Calliphoridae: non-metallic ﬂies 159 10.4 Calliphoridae: metallic ﬂies 162 Contents ix 10.5 Sarcophagidae: ﬂesh ﬂies 168 10.6 Oestridae: bot ﬂies 171 10.7 Other myiasis-producing ﬂies 173 Further reading 173 11 Fleas (Siphonaptera) 176 11.1 External morphology 177 11.2 Life cycle 180 11.3 Medical importance 182 11.4 Tunga penetrans 185 11.5 Control of ﬂeas 187 Further reading 189 12 Sucking lice (Anoplura) 191 12.1 The body louse (Pediculus humanus) 192 12.2 The head louse (Pediculus capitis) 197 12.3 The pubic louse (Pthirus pubis) 199 Further reading 201 13 Bedbugs (Cimicidae) 203 13.1 External morphology 204 13.2 Life cycle 205 13.3 Medical importance 207 13.4 Control 207 Further reading 208 14 Triatomine bugs (Triatominae) 210 14.1 External morphology 211 14.2 Life cycle 212 14.3 Medical importance 214 14.4 Control 215 Further reading 216 15 Cockroaches (Blattaria) 219 15.1 External morphology 220 15.2 Life cycle 221 15.3 Medical importance 222 15.4 Control 223 Further reading 224 16 Soft ticks (Argasidae) 226 16.1 External morphology 227 16.2 Internal anatomy 228 16.3 Life cycle 229 16.4 Medical importance 231 x Contents 16.5 Control 234 Further reading 234 17 Hard ticks (Ixodidae) 236 17.1 External morphology 237 17.2 Life cycle 238 17.3 Behaviour and habits 240 17.4 Medical importance 242 17.5 Control 249 Further reading 250 18 Scabies mites (Sarcoptidae) 252 18.1 External morphology 253 18.2 Life cycle 253 18.3 Recognition of scabies 256 18.4 Treatment of scabies 257 Further reading 258 19 Scrub typhus mites (Trombiculidae) 260 19.1 External morphology 261 19.2 Life cycle 263 19.3 Ecology 264 19.4 Medical importance 265 19.5 Control 266 Further reading 267 20 Miscellaneous mites 269 20.1 Demodicidae: follicle mites (Demodex species) 270 20.2 Pyroglyphidae: house-dust mites (Dermatophagoides and Euroglyphus species) 271 20.3 Other mites 272 Further reading 273 Appendix Names of some chemicals and microbials used in vector control 275 Glossary of common terms relevant to medical entomology 278 Select bibliography 291 Index 293 Colour plate section appears between pages 140 and 141. 1 Introduction to mosquitoes (Culicidae) 2 Introduction to mosquitoes (Culicidae) There are some 3530 species of mosquitoes, which are traditionally placed in 43 genera, all contained in the family Culicidae. However, some mos- quito experts recognize a different classiﬁcation that has many more (113) genera. For example, some mosquitoes previously in the genus Aedes have been transferred to genera such as Ochlerotatus and Stegomyia. This results in Aedes albopictus and Aedes aegypti becoming Ochlerotatus albopictus and Stegomyia aegypti. However, as these new names are not so well known to non-mosquito experts I have retained the older names such as Aedes albo- pictus and Aedes aegypti. Mosquitoes are divided into three subfamilies: Toxorhynchitinae, Anophelinae (anophelines) and Culicinae (culicines). Mosquitoes have a worldwide distribution, occurring throughout the tropical and temperate regions and northwards into the Arctic Circle. The only areas from which they are absent are Antarctica and a few islands. They have been found at elevations of 3500 m and down mines to depths of 1250 m below sea level. The most important pest and vector species belong to the genera Anopheles, Culex, Aedes, Psorophora, Mansonia, Haemagogus and Sabethes. Anopheles species, as well as transmitting malaria, are vectors of ﬁlariasis (Wuchereria bancrofti, Brugia malayi and Brugia timori) and a few arbovi- ruses. Some Culex species also transmit Wuchereria bancrofti as well as several arboviruses. Aedes species are important vectors of yellow fever, dengue, West Nile virus and many other arboviruses, and in a few restricted areas they also transmit Wuchereria bancrofti and Brugia malayi. Mansonia species transmit Brugia malayi and sometimes Wuchereria bancrofti and a few arboviruses. Haemagogus and Sabethes mosquitoes are vectors of yellow fever and a few other arboviruses in Central and South America, while the genus Psorophora contains a few species that transmit arboviruses and others that are troublesome biters in North and South America. Many mosquitoes which are not vectors can nevertheless be troublesome because of the serious biting nuisances they cause. 1.1 External morphology Mosquitoes possess only one pair of functional wings, the fore-wings. The hind-wings are represented by a pair of small, knob-like halteres. Mosquitoes are distinguished from other ﬂies of a somewhat similar shape and size by: (1) the possession of a conspicuous forward-projecting proboscis; (2) the presence of numerous appressed scales on the thorax, legs, abdomen and wing veins; and (3) a fringe of scales along the posterior margin of the wings. Mosquitoes are slender and relatively small insects, usually measuring about 3–6 mm in length. Some species, however, can be as small as 2 mm while others may be as long as 19 mm. The body is distinctly divided into a head, thorax and abdomen. External morphology 3 The head has a conspicuous pair of kidney-shaped compound eyes. Between the eyes arises a pair of ﬁlamentous and segmented antennae. In females the antennae have whorls of short hairs (i.e. pilose antennae), but in males, with a few exceptions in genera of no medical importance, the antennae have many long hairs giving them a feathery or plumose appearance. Mosquitoes can thus be conveniently sexed by examination of their antennae: individuals with feathery antennae are males, while those with only short and rather inconspicuous antennal hairs are females (Figs. 1.1, 1.13). Just below the antennae is a pair of palps, which in female anophelines are pointed apically while in males they are dilated. In female culicines the palps are very short while in males they are long (Fig. 1.13). Arising between the palps is the single long proboscis, which in females contains the piercing mouthparts. In mos- quitoes the proboscis characteristically projects forwards (Fig. 1.1). The thorax is covered, dorsally and laterally, with scales, which may be dull or shiny, white, brown, black or almost any colour. It is the arrange- ment of black and white, or coloured, scales on the dorsal surface of the thorax that gives many species, especially Aedes mosquitoes, their distinc- tive patterns (Fig. 3.3). The wings are long and relatively narrow, and the number and arrange- ment of the wing veins is virtually the same for all mosquito species (Fig. 1.1). The veins are covered with scales which are usually brown, black, white or yellowish, but more brightly coloured scales may occasion- ally be present. The shape of the scales and the pattern they create differs considerably between both genera and species of mosquitoes. Scales also project as a fringe along the posterior border of the wings. In life the wings of resting mosquitoes are placed across each other over the abdomen in the fashion of a closed pair of scissors. The legs are long and slender and are covered with scales which are usually brown, black or white and may be arranged in patterns, often in the form of rings (Fig. 3.4b). The tarsus usually terminates in a pair of toothed or simple claws. Some genera, such as Culex, have a pair of small ﬂeshy pulvilli (Fig. 1.2) between the claws in addition to the empodium. The abdomen is composed of 10 segments, but only the ﬁrst seven or eight are visible. Mosquitoes in the subfamily Culicinae usually have the abdomen covered dorsally and ventrally with mostly brown, blackish or whitish scales. In the Anophelinae, however, the abdomen is almost, or entirely, devoid of scales. The last abdominal segment of a female mosquito terminates in a pair of small ﬁnger-like cerci, whereas in males there is a pair of prominent claspers, comprising part of the male external genitalia. In unfed mosquitoes the abdomen is thin and slender, but after females have bitten a host and taken a blood-meal (only females bite) the abdomen becomes greatly distended and resembles an oval red balloon. When the abdomen is full of developing eggs it is also dilated, but whitish and not red in appearance. 4 Introduction to mosquitoes (Culicidae) Figure 1.1 Diagrammatic representation of a female adult mosquito. 1.1.1 Mouthparts and salivary glands The mouthparts are collectively known as the proboscis. In mosquitoes the proboscis is long and projects conspicuously forwards in both sexes – although males do not bite. The largest component of the mouthparts is the long and ﬂexible gutter-shaped labium, which terminates in a pair of small ﬂap-like structures called labella. In cross-section the labium is seen to almost encircle all other components of the mouthparts (Fig. 1.3), and it serves as a protective sheath. The individual components are held close External morphology 5 Figure 1.2 Tip of the last segment of the tarsus of a Culex mosquito showing claws, hair-like empodium and two large pulvilli. Figure 1.3 Diagram of a cross-section through the proboscis of a mos- quito, showing components of the mouthparts and food channel. together in life and only become partially separated during blood-feeding, or when they are teased apart for examination as illustrated in Figure 1.4. The uppermost structure, the labrum, is slender, pointed and grooved along its ventral surface. In between this ‘upper roof’ (labrum) and ‘lower gutter’ (labium) are ﬁve needle-like structures, namely a lower pair of toothed maxillae, an upper pair of mandibles, which usually lack teeth (although in Anopheles they are very ﬁnely toothed), and ﬁnally a single untoothed hollow stylet called the hypopharynx. When a female mosquito bites a host the labella, at the tip of the ﬂeshy labium, are placed on the skin and the labium, which cannot pierce the skin, curves backwards. This allows the paired mandibles, paired maxillae, labrum and hypopharynx to penetrate the host’s skin. Saliva from a pair of trilobed salivary glands (Fig. 1.14), situated ventrally in the anterior part of the thorax, is pumped 6 Introduction to mosquitoes (Culicidae) Figure 1.4 Diagram of the head of a female culicine mosquito, show- ing the components of the mouthparts spread out from the labium. down the hypopharynx. Saliva contains antihaemostatic enzymes that produce haematomas in the skin and facilitate the uptake of blood. Saliva also contains anticoagulants to prevent blood from clotting and obstructing the mouthparts as it is sucked up, and anaesthetic substances that help reduce the pain inﬂicted by the mosquito’s bite, so reducing the host’s defensive reactions. Although male mosquitoes have a proboscis, the maxillae and mandi- bles are usually reduced in size or the mandibles are absent, and conse- quently males cannot bite. 1.2 Life cycle 1.2.1 Blood-feeding and the gonotrophic cycle Most mosquitoes mate shortly after emergence from the pupa. Sperm from a male enter the spermotheca of a female, and this usually serves to fertilize all eggs laid during her lifetime; thus only one mating and insemination per female is required. With a few exceptions, a female mosquito must bite a host and take a blood-meal to obtain the necessary nutrients for the devel- opment of her eggs. This is the normal procedure and is referred to as anautogenous development. A few species, however, can develop the ﬁrst Life cycle 7 Figure 1.5 Diagrammatic representation of the gonotrophic cycle of a female mosquito. Each cycle begins with an unfed adult, which passes through a blood-fed, half-gravid and gravid condition. After oviposi- tion the female is again unfed and seeks another blood-meal. batch of eggs without a blood-meal, and more rarely subsequent batches. This process is called autogenous development. The speed of digestion of the blood-meal depends on temperature. In most tropical species it takes only 2–3 days, but in colder, temperate countries blood digestion often takes as long as 7–14 days. After a blood-meal the mosquito’s abdomen is dilated and bright red, but some hours later the abdomen becomes a much darker red. As the blood is digested and the white eggs in the ovaries enlarge, the abdomen becomes whitish posteriorly and dark reddish anteriorly. This condition represents a mid-point in blood digestion and ovarian development, and the mosquito is referred to as being half-gravid (Fig. 1.5). Eventually all blood is digested and the abdomen becomes dilated and whitish due to the formation of fully developed eggs (Fig. 1.5). The female is now said to be gravid, and she searches for suitable larval habitats in which to lay her eggs. After oviposition the female mosquito takes another blood-meal, and after 2–3 days (in the tropics) a further batch of eggs is matured and laid. This process of blood-feeding and egg-laying is repeated several times through- out the female’s life and is referred to as the gonotrophic cycle. Male mosquitoes cannot bite but feed on the nectar of ﬂowers and other naturally occurring sugary secretions. Males are consequently unable to transmit any diseases. Sugar-feeding is not, however, restricted to males: females may also feed on sugary substances to obtain energy for ﬂight and dispersal, but only in a few species (the autogenous ones) is this type of food sufﬁcient for egg development. 1.2.2 Oviposition and biology of the eggs Depending on the species, female mosquitoes lay about 30–300 eggs in one oviposition. Eggs are brown or blackish and 1 mm or less in length. In many Culicinae they are elongate or approximately ovoid in shape, but eggs of 8 Introduction to mosquitoes (Culicidae) Mansonia are drawn out into a terminal ﬁlament (Fig. 3.8). In the Anophelinae eggs are usually boat-shaped (Fig. 1.8). Many mosquitoes, such as species of Anopheles and Culex, lay their eggs directly on the water surface. In Anopheles the eggs are laid singly and ﬂoat on the water, whereas Culex eggs are laid vertically in several rows held together by surface tension to form an egg raft which ﬂoats on the water (Fig. 1.15). Mansonia species lay their eggs in a sticky mass that is glued to the underside of ﬂoating plants. None of the eggs of these mosquitoes can survive desicca- tion, and consequently they die if they become dry. In the tropics eggs hatch within 2–3 days, but in cooler temperate countries they may not hatch until after 7–14 days, or longer. Other mosquitoes, such as those belonging to the genera Aedes, Psorophora and Haemagogus, do not lay eggs on the water surface. Instead they deposit them just above the water line on damp surfaces, such as mud and leaf litter, or on the inside walls of tree-holes and clay water-storage pots. Eggs of these genera can withstand desiccation, especially those of Aedes and Psorophora, which can remain dry for months or even years but still remain viable and hatch when covered with water. Because their eggs are laid above the water line of larval habitats it may be many weeks or months before they become ﬂooded with water and can hatch. However, even when ﬂooded, hatching may extend over relatively long periods because the eggs hatch in instalments. Moreover, eggs of Aedes and Psorophora may require repeated immersions in water followed by short periods of desiccation before they will hatch. Aedes and Psorophora eggs may also enter a state of diapause, that is not hatching until some speciﬁc environmental stimulus such as a change in day length and/or temper- ature breaks diapause and the eggs hatch. In temperate regions many Aedes and Psorophora species overwinter as diapausing eggs. 1.2.3 Larval biology Mosquito larvae are distinguished from most other aquatic insects by being legless and having an enlarged thorax that is wider than both the head and the abdomen. There are four active larval instars. All mosquito larvae require water in which to develop; no mosquito has larvae that can with- stand desiccation, although they may be able to survive short periods, for example, in wet mud. Larvae have a well-developed head bearing a pair of antennae and a pair of compound eyes. Prominent mouthbrushes are present in most species and serve to sweep water containing minute food particles into the mouth. The thorax is roundish and has unbranched and branched hairs, which are usually long and conspicuous. The 10-segmented abdomen has nine visible segments, most of which have unbranched or branched hairs (Figs. 1.9, 1.16). The last segment, which differs in shape from the preceding eight Life cycle 9 segments, has two paired groups of long hairs forming the caudal setae, and a larger fan-like group comprising the ventral brush (Figs. 1.10, 1.16). This last segment ends in two pairs of transparent sausage-shaped anal papillae, which although often called gills are concerned not with respira- tion but with osmoregulation. Mosquito larvae, with the exception of Mansonia and Coquillettidia spe- cies (and a few other species), must come to the water surface to breathe. Atmospheric air is taken in through a pair of spiracles situated dorsally on the ninth abdominal segment. In the subfamilies Toxorhynchitinae and Culicinae these spiracles are situated at the end of a single dark-coloured and heavily sclerotized tube termed the siphon (Fig. 1.16). Mansonia and Coquillettidia larvae possess a specialized siphon that is more or less conical, pointed at the tip and supplied with prehensile hairs and serrated cutting structures (Fig. 3.9). These enable the siphon to be inserted into the roots or stems of aquatic plants, from which oxygen for larval respiration is obtained. In contrast, larvae of the Anophelinae do not have a siphon (Figs. 1.10, 1.13). Mosquito larvae feed on yeasts, bacteria, protozoans and numerous other microorganisms, as well as on decaying plant and animal material found in the water. Some, such as Anopheles species, are surface-feeders, whereas many others species browse over the bottoms of habitats. A few mosquitoes are carnivorous or cannibalistic. There are four larval instars, and in tropical countries larval development, that is the time from egg hatching to pupation, can be as short as 5–7 days, but many species require about 7–14 days. In temperate areas the larval period may last several weeks or months, and several species overwinter as larvae. 1.2.4 Larval habitats Mosquito larval habitats vary from large and usually permanent collections of water, such as freshwater swamps, marshes, riceﬁelds and borrow pits, to smaller collections of temporary water such as pools, puddles, water-ﬁlled car tracks and animal footprints, ditches, drains and gulleys. A great variety of ‘natural container-habitats’ also provide breeding places, such as water- ﬁlled tree-holes, rock-pools, bamboo stumps, bromeliads, pitcher plants, leaf axils in bananas, pineapples and other plants, water-ﬁlled split coconut husks and even snail shells. Larvae also occur in wells and ‘man-made container-habitats’, such as clay pots, water-storage jars, tin cans, discarded kitchen utensils and motor-vehicle tyres. Some species prefer shaded larval habitats whereas others like sunlit habitats. Many species cannot survive in water polluted with organic debris, whereas others occur in water contami- nated with excreta or rotting vegetation. A few mosquitoes are found almost exclusively in brackish or salt waters, such as saltwater marshes and man- grove swamps, and are consequently restricted to mostly coastal areas. 10 Introduction to mosquitoes (Culicidae) Some species are less speciﬁc in their requirements and can tolerate a wide range of different types of larval habitats. Almost any collection of permanent or temporary water can be a mos- quito larval habitat, but larvae are usually absent from large expanses of uninterrupted water such as lakes, especially if they have large numbers of ﬁsh and other predators. They are also usually absent from large rivers and fast-ﬂowing waters, but they may occur in marshy areas and isolated pools and puddles formed at the edges of ﬂowing water. 1.2.5 Pupal biology All mosquito pupae are aquatic and comma-shaped. The head and thorax are combined to form the cephalothorax, which dorsally has a pair of respiratory trumpets (Fig. 1.6). The abdomen is 10-segmented, although only eight segments are visible. Each segment has numerous short hairs, and the last segment terminates in a pair of oval and ﬂattened structures termed paddles (Figs. 1.11, 1.18). Some of the developing structures of the adult mosquito can be seen through the integument of the cephalothorax, the most conspicuous features being a pair of dark compound eyes, folded wings, legs and the proboscis (Fig. 1.6). Pupae do not feed but spend most of their time at the water surface taking in air through the respiratory trumpets. If disturbed they swim up and down in the water in a jerky fashion. Figure 1.6 Anopheles pupa. Life cycle 11 Pupae of Mansonia and Coquillettidia differ in that they have relatively long breathing trumpets, which are modiﬁed to enable them to pierce aquatic vegetation and obtain their oxygen in a similar fashion to the larvae (Fig. 3.9). As a consequence their pupae remain submerged and rarely come to the water surface. In the tropics the pupal period lasts only 2–3 days, but in cooler temper- ate regions pupal development may take 9–12 days, or longer. At the end of pupal life the skin on the dorsal surface of the cephalothorax splits, and the adult mosquito struggles out. 1.2.6 Adult biology and behaviour As already mentioned (page 6), females of most mosquito species require a blood-meal before the eggs can develop, and this is taken either before or more usually after mating. Many species bite humans to obtain their blood- meals, and a few feed on humans in preference to other animals. However, others prefer feeding on non-human hosts, and many species never bite people. Species that usually feed on humans are said to be anthropophagic in their feeding habits, whereas those feeding mainly on other animals are called zoophagic. Mosquitoes that feed on birds are sometimes called ornithophagic instead of zoophagic. Females are attracted to hosts by various stimuli emanating from their breath or sweat, such as carbon dioxide, lactic acid, octenol, as well as body odours and warmth. Vision usually plays only a minor role in host orientation. Some species feed more or less indiscriminately at any time of the day or night; others are mainly diurnal or nocturnal in their biting habits. A few species of mosquitoes frequently enter houses to feed and are said to be endophagic in their feeding habits, whereas those that bite their hosts outside houses are called exophagic. After having bitten humans, or other hosts, either inside or outside houses, mosquitoes seek resting places in which to shelter during digestion of the blood-meal. Some species rest inside houses during blood digestion and development of the eggs and are called endophilic. In contrast, mosquitoes that rest outdoors are termed exophilic. Female adults of Aedes aegypti (a vector of yellow fever and dengue), for example, are usually anthropophagic, exophagic and exo- philic, whereas adults of Anopheles gambiae (African malaria vector) are mainly anthropophagic, endophagic and endophilic. However, many spe- cies are not entirely anthropophagic or zoophagic, endophagic or exopha- gic, endophilic or exophilic, but show various degrees of these behavioural patterns; in other words all these terms are relative. The feeding behaviour of a species may also change. For example, in certain areas and at certain seasons a species may bite people predominantly (anthropophagic) inside houses (endophagic) and remain in houses afterwards (endophilic), but if there are few people but many animals in the area, the species may become 12 Introduction to mosquitoes (Culicidae) predominantly zoophagic, and also exophagic and exophilic. Many species are less adaptable in their feeding behaviour and will never rest in houses or enter them to feed on the occupants. The biting behaviour of female mosquitoes may be very important in the epidemiology of disease transmission. Mosquitoes feeding on people pre- dominantly out of doors and late at night will not bite many young children, because they will be indoors and asleep at this time. Consequently young children will be less likely to be infected with diseases that these mosquitoes might transmit. During hot and dry seasons sub- stantial numbers of people may sleep out of doors and as a consequence be bitten more frequently by exophagic mosquitoes. Some mosquitoes bite predominantly within forests or wooded areas, so people are likely to get bitten when they visit such sites. Clearly the behaviour of both people and mosquitoes may be relevant in disease transmission. The resting behaviour of adult mosquitoes may be important in planning control measures. In several malaria control campaigns the interior sur- faces of houses, such as walls and ceilings, are sprayed with residual insecticides to kill adult mosquitoes resting on them. This approach will, of course, only be effective in controlling malaria if the mosquito vectors are endophilic (see Chapter 2, page 49). Many mosquitoes probably disperse only a few hundred metres from their emergence sites, so in control programmes and epidemiological stud- ies it is usually safe to say that mosquitoes will not ﬂy further than about 2 km. There are records of mosquitoes being found 100 km or more from their larval habitats, but such dispersal is nearly always wind-assisted. Mosquitoes may get transported long distances in aeroplanes, and some- times this causes disease outbreaks, such as ‘airport malaria’. In tropical countries adult female mosquitoes probably live on average 1–2 weeks, whereas in temperate countries adult longevity is likely to be 3–4 weeks. Species that hibernate or aestivate live much longer: for exam- ple in Europe some fertilized female Culex pipiens survive in hibernation from August until May. Adult males usually have a shorter life span than females. 1.3 Classiﬁcation of mosquitoes 1.3.1 Subfamily Toxorhynchitinae The Toxorhynchitinae comprise a single genus, Toxorhynchites, which con- tains about 94 species that are mainly tropical, although a few species occur in North America, southeastern Russia and Japan. Adults are large (19 mm long, 24 mm wingspan) and colourful, being metallic bluish or greenish with black, white or red tufts of hair-like scales projecting from the posterior abdominal segments. Adults are easily Classiﬁcation of mosquitoes 13 Figure 1.7 Heads of Toxorhynchites adults: (a) female; (b) male. recognized by having a proboscis that is curved backwards in both sexes (Fig. 1.7) and that is incapable of piercing the skin. Consequently, since neither sex can bite, they are of no medical importance. Their larvae are also large (12–18 mm long), often dark reddish and, like those of the Culicinae, have a siphon. They are predaceous on larvae of other mosquitoes and on their own kind. They have occasionally been introduced into areas in the hope that their voracious larvae will help reduce the numbers of pest mosquitoes. Larvae are found mainly in container-habitats, such as tree- holes and bamboo stumps, tin cans and water-storage pots. 1.3.2 Subfamily Anophelinae Of the three genera included in the subfamily Anophelinae only the genus Anopheles (about 477 species) is medically important, for instance as malaria vectors. The following characters serve to separate anopheline from culicine mosquitoes. Anopheline eggs Eggs are laid singly on the water surface. In most species they are typically boat-shaped, and laterally have a pair of air-ﬁlled sacs called ﬂoats (Fig. 1.8). Anopheline eggs are unable to withstand desiccation. Anopheline larvae Larvae lack a siphon and lie parallel to the water surface, not subtended at an angle as are the culicines. They are surface-feeders and so spend most of their time at the water surface. Examination under a microscope shows that the abdomen has small, brown, sclerotized plates, called tergal plates, on the dorsal surface of abdominal segments 1–8; there may also be 1–3 small accessory plates behind a main tergal plate. In addition, most or all of these segments have a pair of well-developed palmate hairs, sometimes called ﬂoat hairs (Figs. 1.1, 1.9). These abdominal palmate hairs and a single pair 14 Introduction to mosquitoes (Culicidae) TOP VIEW SIDE VIEW Figure 1.8 Anopheles eggs. on the thorax come into contact with the water surface and aid in keeping larvae parallel to the surface. Laterally on each side of segment 8 (8 and 9 are combined) there is a sclerotized comb-like structure with teeth called the pecten. All these structures identify larvae as belonging to the genus Anopheles. Anopheline pupae The respiratory trumpets of anopheline pupae are short and broad distally, thus appearing conical (Figs. 1.6, 1.11a), whereas in most culicines the trumpets are narrower and more cylindrical. The most reliable character for identifying anopheline pupae is the presence of short, peg-like spines situated laterally near the distal margins of abdominal segments 2–7 or 3–7 (Fig. 1.11b); in culicines there are no such spines. Anopheline adults Adult Anopheles usually rest with their bodies at an angle to the surface, that is with the proboscis and abdomen in a straight line, or ‘head down bottom up’ (Fig. 1.13, Plate 1). In some species they rest at almost right angles to the surface, whereas in others such as the Indian mosquito Anopheles culicifacies the angle is much smaller. This is a very useful char- acter, allowing adults resting in houses and elsewhere to be readily iden- tiﬁed as Anopheles. Most, but not all, Anopheles mosquitoes have the dark (usually black) and pale (usually white or yellowish) scales on the wing veins arranged in ‘blocks’ or speciﬁc areas (Fig. 1.12) forming a distinctive spotted pattern which differs according to species. A few species, however, such as the Classiﬁcation of mosquitoes 15 Figure 1.9 Anopheles larva, dorsal view, showing diagnostic abdomi- nal tergal plates and palmate hairs. 16 Introduction to mosquitoes (Culicidae) Figure 1.10 Lateral view of the abdominal terminal segments of an Anopheles larva. Figure 1.11 Anopheles pupa: (a) short and broad respiratory trumpet; (b) part of abdomen showing diagnostic spines. European Anopheles claviger, have the veins covered more or less uniformly with dark (often brown) scales. The most reliable way to distinguish between adult Anopheles and Culicinae is by examination of their heads. The ﬁrst procedure is to determine the sex of the adults: female mosquitoes have non-plumose antennae whereas males have plumose antennae. If the adults are females and also Anopheles then the palps will be about as long as the proboscis and usually lie closely alongside it (Fig. 1.13). The palps are usually blackish with broad or narrow rings of pale scales, especially on the Classiﬁcation of mosquitoes 17 Figure 1.12 Anopheles wing, showing dark and pale scales arranged in ‘blocks’. apical half. In male Anopheles the palps are also about as long as the proboscis but are distinctly swollen at their ends and are said to be clubbed (Fig. 1.13); they may also have rings of pale scales apically. Other differences are that in Anopheles there is only a single spermotheca in females, and in both sexes the middle lobe of the salivary glands is considerably shorter than the two outer lobes (Fig. 1.14). Principal characters for separating the various stages in the life cycles of anopheline and culicine mosquitoes are given in Table 1.1. 1.3.3 Subfamily Culicinae There are some 3053 species in the large subfamily Culicinae (belonging to 38 or 110 genera, depending on the classiﬁcation used). The most important medically are the genera Aedes, Culex, Mansonia, Haemagogus, Sabethes and Psorophora. The following characters separate the Culicinae from Anopheles mosquitoes. Methods for distinguishing the more important genera within the Culicinae are given in Chapter 3. Culicine eggs Culicine eggs never have ﬂoats. They are laid either as a number of single eggs (e.g. Aedes) or in the form of egg rafts that ﬂoat on the water surface (e.g. Culex and Coquillettidia), or are deposited as sticky masses glued to the underside of ﬂoating vegetation (e.g. Mansonia) (Fig. 1.15). Culicine larvae All culicine larvae possess a siphon (Fig. 1.16), which may be long or short. They hang upside down at an angle from the water surface when they are getting air (Fig. 1.13), except for Mansonia and Coquillettidia larvae, which insert their specialized siphons into aquatic plants and remain submerged (Fig. 3.9). There are no abdominal palmate hairs or tergal plates on culicine larvae. 18 Introduction to mosquitoes (Culicidae) Figure 1.13 Chart of the principal characters of the stages in the life cycle that distinguish anopheline from culicine mosquitoes. Classiﬁcation of mosquitoes 19 Table 1.1 Principal characters distinguishing anopheline and culicine mosquitoes Stage Anophelinae Culicinae Eggs Laid singly, possess ﬂoats Laid singly or in egg rafts or masses. Never possess ﬂoats Larvae Never have a siphon. Lie All larvae have a short or parallel to water surface. long siphon. Subtend an Have abdominal palmate angle from the water hairs and tergal plates surface. No palmate hairs or tergal plates Pupae Breathing trumpets short and Breathing trumpets short or broad apically. Short peg-like long, opening not broad. spines on abdominal No spines on abdominal segments 2–7 or 3–7 segments 2–7 Adults (both Rest at an angle to any surface. Rest with body more or sexes) In most species dark and pale less parallel to the scales on wing veins arranged surface. Scales on wing in distinct ‘blocks’ veins not arranged in ‘blocks’; scales frequently all brown or blackish, or a mixture of pale and dark scales scattered on veins Adult females Palps about as long as proboscis Palps much shorter than (non-plumose proboscis antennae) Adult males Palps about as long as proboscis Palps about as long as (plumose and swollen at ends proboscis but never antennae) swollen at ends; palps may be hairy distally a b Figure 1.14 Salivary glands of adult mosquitoes: (a) culicine; (b) Anopheles. (Courtesy of Miss M. A. Johnson, and Blackwell Publishing, Oxford, publishers of Entomology for Students of Medicine (1962) by R. M. Gordon and M. M. J. Lavoipierre.) Culex Mansonia Aedes Figure 1.15 Mosquito eggs: Culex egg raft that ﬂoats on the water sur- face, Mansonia eggs glued to the undersurface of ﬂoating aquatic vege- tation, and individual Aedes eggs that are deposited on damp surfaces. Figure 1.16 Culicine larva, dorsal view but with abdominal segments 7–9 turned laterally to display important identiﬁcation features. Classiﬁcation of mosquitoes 21 Figure 1.17 Culicine pupa: (a) pupal position at the water surface; (b) one of the two elongated and relatively narrow respiratory trumpets. Figure 1.18 Part of the abdomen of a culicine pupa, showing hair-like setae. Note absence of lateral spines as found on anopheline pupae. Culicine pupae The length of the respiratory trumpets in culicine pupae is variable, but they are generally longer, more cylindrical and have narrower openings (Fig. 1.17) than in Anopheles. Abdominal segments 2–7 lack peg-like spines, although they have numerous setae (Fig. 1.18). Culicine adults Culicine adults rest with the thorax and abdomen more or less parallel to the surface (Fig. 1.13). The scales covering the wing veins are commonly uniformly brown or black. Sometimes there are contrasting dark and pale scales, but they are not arranged in distinctive areas or ‘blocks’, as found in many Anopheles adults. The most reliable method for identifying the Culicinae is to exam- ine their heads. In females (which have non-plumose antennae) the palps are shorter than the proboscis. In males (which have plumose antennae) the palps are about as long as the proboscis but are not 22 Introduction to mosquitoes (Culicidae) swollen distally and hence do not appear clubbed (Fig. 1.13). However, the palps may be turned upwards distally, and in many species they are covered with long hairs so that superﬁcially they can appear to be somewhat swollen apically, but more careful examina- tion shows that the palps in male culicines are not clubbed as they are in Anopheles. Other differences separating the Culicinae from Anopheles are that in culicines there are two or three spermathecae in females, but just one in anophelines. Also in culicines the middle lobe of the salivary glands is about as long as the other two, whereas in anophelines it is shorter (Fig. 1.14). 1.4 Medical importance Although in several temperate countries mosquitoes may be of little or no importance in transmitting diseases to humans they can, nevertheless, cause considerable annoyance because of their troublesome bites. The greatest numbers of mosquitoes are found in the northern areas of the temperate regions, especially near or within the Arctic Circle, where the numbers biting can be so great at certain times of the year as to make almost any outdoor activity impossible. Because of their elongated mouthparts female mosquitoes can easily bite through clothing such as socks, shirts, blouses, trousers and woollen garments, but clothing with a much closer weave may prevent biting. Mosquitoes are important as vectors of malaria, various forms of ﬁlar- iasis and numerous arboviruses such as dengue, yellow fever and West Nile virus. Their role in the transmission of these diseases is discussed in Chapters 2 and 3. 1.5 Mosquito control Control measures which are directed against speciﬁc vectors, such as anopheline malaria vectors, and Aedes aegypti and Culex quinquefasciatus, are described in more detail in Chapters 2 and 3; only the more basic principles of control are outlined here. Control measures can be directed at either the immature aquatic stages or the adults, or at both stages simultaneously. 1.5.1 Control directed at the immature stages Biological control Although often termed naturalistic control, there is little that is natu- ral about biological control. Either the numbers of predators, parasites or pathogens in larval habitats must be greatly increased to obtain Mosquito control 23 worthwhile control, or they have to be introduced into habitats from which they were originally absent; such environmental manipu- lations are not natural. Biological control of mosquitoes was very popular during the early twentieth century, but with the availability of powerful insecticides it was largely replaced by chemical control. However, because of insecticide resistance and greater awareness of environmental issues there has been renewed interest in biological (biocontrol) methods. They are, however, usually more difﬁcult to implement and maintain than insecticidal methods. Moreover, with predators it is unlikely that they will prey exclusively on mosquito larvae and pupae but will also eat harmless or even beneﬁcial insects. Finally, biological control does not lead to rapid control. It takes some days, or more often weeks, before mosquito populations are substan- tially reduced in size. Predators Larvivorous ﬁsh are the most widely used biological control agents, the most common being the top minnow or mosquitoﬁsh (Gambusia afﬁnis). This is a warm-water ﬁsh originally native to the southern USA and northern Mexico but which has been introduced to some 60 countries, including the Paciﬁc islands, Europe, the Middle East, India, Southeast Asia and Africa, in attempts to control mosquito larvae. They are aggres- sive ﬁsh which have sometimes destroyed indigenous species; conse- quently they should not now be introduced into new areas. Another commonly used ﬁsh is the South American guppy (Poecilia reticulata), which is not so voracious as G. afﬁnis but can better tolerate low levels of organic pollution and is more heat-tolerant. There are numerous other ﬁsh that have been used to eat mosquito larvae, such as carp (e.g. Cyprinus carpio and Ctenopharyngodon idella) in Chinese riceﬁelds, an edible catﬁsh (Clarias fuscus) in water-storage tanks in Myanmar to control Aedes aegypti, Oreochromis (= Tilapia) species in Africa and Aplocheilus species in Asia. Predatory ﬁsh, such as Aphanius dispar and Fundulus species, occur in saline waters and can therefore be introduced into saltwater habitats. Fish are unsuitable for controlling mosquitoes in small water containers and in pools and puddles that rapidly dry out. However, some ﬁsh, such as species of Nothobranchius and Cynolebias, which are the so-called instant or annual ﬁsh, have drought-resistant eggs, and these are more suitable for introducing into small temporary habitats that repeatedly dry out. Although ﬁsh have sometimes greatly reduced the numbers of larvae in certain habitats, such as borrow pits, ponds, wells and riceﬁelds, other than in parts of India and China they have rarely proved effective in reducing mosquito populations over relatively large areas. Nor is there usually much convincing evidence that they have signiﬁcantly decreased the incidence of mosquito-borne diseases – but see Chapter 2 (page 48) in relation to malaria. However, in New Jersey, USA, a biocontrol company routinely 24 Introduction to mosquitoes (Culicidae) uses ﬁve species of reared larvivorus ﬁsh in its mosquito control programme. Other predators of mosquito larvae include tadpoles of frogs and toads and various aquatic insect larvae, but these have rarely proved effective as control agents. There has been interest in predaceous copepods such as Mesocyclops species to control larvae in water containers such as tyres, but the impact is usually very localized. Nevertheless, in New Jersey and New Orleans, USA, the predaceous copepod Macrocyclops albidus is being used to control mosquitoes. A few mosquitoes, such as Toxorhynchites species, have predaceous larvae that have sometimes been introduced to control mosquito larvae in container-habitats such as tree-holes, but results have not been very encouraging. Pathogens and parasites There are numerous pathogens, such as iri- descent and cytoplasmic polyhedrosis viruses, protozoans (e.g. Bracheola (= Nosema) algerae and Vavraia culicis) and fungi (e.g. species of Coelomomyces, Lagenidium and Culicinomyces) that cause larval mortality. There are also several parasitic nematodes that kill mosquito larvae; the best known is Romanomermis culicivorax, which was commercially mass- produced, but because of non-viable sales is no longer commercially available. None of these biological agents has given satisfactory control of mosquitoes. In contrast, Bacillus thuringiensis var. israelensis (Bti) is undoubtedly the most effective pathogen, as it can be easily mass-produced, is toxicologi- cally safe to humans and wildlife, and is more or less speciﬁc in killing mosquito larvae (but it also kills simuliids: see Chapter 4). It is commonly formulated as slow-release briquettes that ﬂoat on the water surface and can give control for up to about 30 days. Sometimes Bti is formulated as a powder that is mixed with water and sprayed on larval habitats, but because there is no multiplication of the bacteria there must be repeated applications, as with most chemical larvicides. When Bti is ingested, mortality is caused by an endotoxin acting as a stomach poison. Bacillus sphaericus can be formulated much as for Bti and kills mosquito larvae in a similar fashion, but differs in that in some situations it can recycle in larval habitats. This species is also more effective in organ- ically polluted waters and is especially effective against Culex species. Both these Bacillus species are more like a microbial insecticide than a true biological (living) agent that recycles and maintains itself in the environment. Resistance to both Bti and B. sphaericus has been observed in laboratory colonies of a few mosquito species, especially Culex quinquefasciatus. Although ﬁeld populations of Cx. pipiens were recorded in New York State as being resistant to Bti, no resistance was recorded in ﬁeld popula- tions of Aedes vexans in Germany that had been exposed to Bti for over Mosquito control 25 25 years. Field populations of B. sphaericus have been reported as developing resistance in several countries including Brazil, China, India and Thailand, but Bti and B. sphaericus continue to be widely used. Recently genetic engineering techniques, such as the development of recombinant strains of these two bacteria, seem to have improved the larvicidal activity of the bacteria, and in addition the genes responsible for production of the poisonous endotoxin have been transferred to other bacteria. Genetic control Although genetic control methods are directed against the adults, it is convenient to discuss this strategy here because it is really a form of bio- logical control. There are basically two approaches to genetic control. One involves releasing into the ﬁeld male mosquitoes that have been laboratory-reared and sterilized by a variety of techniques, such as with ionizing radiation, crossing closely related species to produce infertile hybrid males, or intro- ducing chemosterilants into insectary rearing programmes which make emerging adults (both sexes) sterile. Large numbers of sterile males released into ﬁeld populations will hopefully compete with natural fertile males for female mates, resulting in large numbers of infertile insemina- tions. Eggs layed by such females are sterile and fail to hatch. In El Salvador Anopheles albimanus, an important malaria vector, had developed resistance to most insecticides so in the 1970s about 4.36 million chemosterilized males were released into an isolated coastal region of about 15 km2. More than a 97% reduction in the biting population was achieved. However, because enormous numbers of mosquitoes had to be reared to obtain control over a very small area there was later little interest in such methods. More recently this approach has been used against the vector of dengue (see Chapter 3, page 80). The second approach aims at introducing into ﬁeld populations species or strains of mosquitoes that are incapable of transmitting diseases. In 2010 a transgenic Anopheles stephensi was created that had both a reduced life span and complete resistance to infection with Plasmodium falciparum. However, mechanisms have to be found to drive the genes through wild populations when the transgenic mosquitoes are released into ﬁeld pop- ulations of a vector. Neither of these genetic approaches is simple, and they will be much more difﬁcult to implement than conventional insecticidal methods. Nevertheless, there has been some progress in developing transgenic Anopheles species that are refractory to malaria parasites and Aedes aegypti mosquitoes that are unable to transmit dengue viruses. 26 Introduction to mosquitoes (Culicidae) Physical control Filling in, source reduction and drainage This is sometimes referred to as mechanical or environmental control. A simple approach is to ﬁll in larval habitats and thus completely eliminate them. Larval habitats ranging in size from water-ﬁlled tree-holes to ponds and small marshes can be ﬁlled in with rubble, earth or sand. However, ﬁlling in tree-holes can be problematic because many are at considerable heights and difﬁcult to locate, or there can be too many for this method to be practical. Various container-habitats such as abandoned tin cans, metal drums, disused water-storage pots and old tyres can be removed: this approach is often referred to as source reduction. Mosquito breeding in water-storage pots that are in use can be reduced by covering up their openings, but this simple practice is often not popular and it soon becomes neglected. Introduction of a reliable piped water supply should help reduce people’s dependence on water-storage containers and thereby reduce breeding of mosquitoes such as Aedes aegypti. However, in many areas with piped water people continue to store water in containers as insurance against an unreliable water supply. In the Indian subcontinent water tanks are commonly sited on rooftops, and these are important breeding places of the vector (Anopheles stephensi) of urban malaria. Fitting these with mosquito screening would prevent breeding, but such covers usually become torn or are removed. Some mosquitoes, such as Culex quinquefasciatus, breed in damaged septic tanks and soakaway pits, but this is easily prevented if the tanks and pits are repaired so that egg-laying females cannot gain access. This mosquito also commonly breeds in pit latrines, but this can be stopped if small (2–3 mm) expanded polystyrene beads are tipped into latrines to form a ﬂoating layer about 1–2 cm thick. This suffocates larvae and pupae and also prevents mosquitoes laying their eggs on the water surface. In Zanzibar and India such beads substantially reduced Cx. quinquefasciatus breeding in pit latrines and soakage pits and contributed greatly to the prevention of a resurgence of bancroftian ﬁlariasis following mass drug treatment. Larval habitats such as ponds, borrow pits, freshwater and saltwater marshes can be drained. An advantage of ﬁlling in, draining or removing larval habitats is that this can lead to permanent control, but this approach is not always feasible. It is impossible, for example, to ﬁll in all the scattered, small and temporary collections of water such as pools, vehicle tracks and puddles which often appear during the rainy season. Larger and more permanent habitats such as swamps may prove too costly to drain. Moreover, the local people may, understandably, not want certain breed- ing places ﬁlled in if the water is needed for domestic purposes or the sites used as watering points for livestock. The feasibility of eradicating breed- ing places must be assessed individually in each area. Mosquito control 27 Environmental manipulation If it is not feasible to eliminate mosquito larval habitats it may be possible to alter them to make them unsuitable for mosquitoes. For example, some mosquitoes occur in isolated pools and small marshy areas formed at the edges of ditches and streams having winding courses. Realigning these water courses to increase water ﬂow and prevent the build-up of static pockets of water can greatly reduce mosquito breeding. The periodic opening of sluice gates can ﬂush out larvae from small isolated pools of water. Other environmental modiﬁcations include the removal of overhanging vegetation to reduce breeding by shade-loving mosquitoes; conversely, planting vegetation along reservoirs and streams may eliminate sun-loving species. Intermittent ﬂooding of riceﬁelds to allow drying out every 3–5 days can substantially reduce populations of several important vectors. Removal of rooted or ﬂoating vegetation will prevent breeding of Mansonia species, because they require plants to obtain their oxygen requirements. Instead of draining marshy areas, they can be excavated to form areas of relatively deep permanent water with well-deﬁned vertical banks. This proc- ess is called impoundment. It makes the habitat unsuitable for many mosqui- toes, especially Aedes and Psorophora species, which lay their eggs on wet muddy edges of pools that are scattered over extensive marshy areas. Both small and large freshwater and saltwater marshy areas can be converted into impounded waters. Sometimes such impounded waters are stocked with ﬁsh and ducks, which will feed, to some extent, on mosquito larvae. There is the danger, however, that larval habitats modiﬁed to reduce breeding of certain mosquito species may create conditions that support other mosquito species that were previously either absent or uncommon. Chemical control Most control directed against mosquitoes, except malaria vectors, consists of the application of larvicides. Oils Spraying oils such as diesel and kerosene (parafﬁn) to kill mosquito larvae has been practised for over 100 years. The addition of detergents or vegetable oils increases the spreading power of oils, thus allowing appli- cation rates to be reduced. Although such oils may sometimes still be used, formulated commercial high-spreading oils which are environmentally more friendly are increasingly used. Dosage rates are commonly 9–27 litres per hectare or less. Other larvicides commonly used are monomolecular ﬁlms of ethoxylated isostearyl alcohol derived from plant oils (commercial names are Arosurf, Agnique), which interfere with the properties of the air– water interface and cause larvae, pupae and even both emerging and ovipositing adults to drown. 28 Introduction to mosquitoes (Culicidae) Oils have to be sprayed on larval habitats about every 7–10 days in most tropical countries to ensure that larvae hatching from eggs are killed before they pupate and give rise to adults. Less frequent applications are made in cooler temperate areas because the aquatic life cycle is much longer. Insecticides With the availability of insecticides such as DDT in the mid 1940s, oiling was largely replaced with spraying larval habitats with these more modern chemicals. However, because of their persistence in the environment and accumulation in food chains, DDT and other organo- chlorine insecticides should not now be used as larvicides. Less persistent and biodegradable insecticides should be used. Recommended chemicals for larviciding include malathion, chlorpyri- fos, fenthion and temephos. Pyrethroids such as permethrin and delta- methrin can also be used as larvicides, but because they tend to kill greater numbers of other aquatic insects, crustaceans and even ﬁsh they should be used with caution and only in special circumstances. In organ- ically polluted waters insecticides are less effective, and so either higher dosage rates must be used or the more effective organophosphates such as fenthion or chlorpyrifos applied. Chlorpyrifos is more toxic to mosquito larvae than many other insecticides, but also causes higher mortalities of ﬁsh and other aquatic organisms, so needs to be used with caution. All the above insecticides usually have to be sprayed on larval habitats in tropical areas every 10–14 days, and more frequently on highly polluted waters. Because temephos has a very low mammalian toxicity, 1% sand granules or microencapsulated formulations, which slowly release the insecticide over days or even weeks, can be placed in containers holding potable water to control Aedes aegypti. This gives a concentration of 1 mg active ingredient per litre of water. However, people have sometimes refused to have their water pots treated with temephos, either because of the unpleasant odour or (understandably) because they consider any insecticide in drinking water as environmental contamination. This attitude is likely to spread. In addition, there are suggestions that temephos could be toxigenic and mutagenic. Mansonia larvae can be killed by spraying herbicides to destroy the aquatic vegetation on which they rely to obtain their oxygen. Larvicides are usually applied as emulsions or oil solutions, but gran- ules, pellets or gelatine capsules, often containing pyrethroids, can be used to penetrate dense growths of aquatic vegetation. Insecticides formulated as slow-release granules or pellets can be scattered over marshy areas when they are relatively dry, then when they become ﬂooded larvae hatching from drought-resistant aedine eggs, such as those of Aedes and Psorophora species, are killed as the granules release their toxicants into the water. Larvicides are usually delivered from knapsack-type sprayers car- ried on the backs of operators, but they are sometimes dispersed from Mosquito control 29 vehicle-mounted spraying machines. Large or inaccessible areas may require aerial spraying from helicopters or small ﬁxed-wing aircraft. Insect growth regulators (IGRs) These are compounds, such as methoprene, fenoxycarb and pyriproxyfen, that arrest larval development of insects, or compounds such as diﬂuben- zuron and novaluron, which inhibit chitin formation in the immature stages. When used as larvicides these chemicals have the beneﬁt of being environmentally friendly, because they are more or less speciﬁc in killing mosquitoes and possess extremely low toxicity to humans. Many IGRs can be formulated as liquids, granules or briquettes which can give control for more than 100 days. However, their relatively high cost may limit their use in poorer countries. Although mosquitoes have not been reported as developing resistance to IGRs, low-level resistance has been found in Musca domestica and Lucilia cuprina, the sheep blowﬂy. Integrated control It has become fashionable to advocate integrated control, which usually means combining biological and insecticidal methods: for example, the introduction of predaceous ﬁsh to breeding places which are also sprayed with insecticides that have minimum effect on the ﬁsh. However, it is better to regard integrated control as any approach that takes into consideration more than one method, whether these are directed at only the larvae or the adults, or both. 1.5.2 Control directed at adults Personal protection Much can be done to reduce biting by mosquitoes. Houses, hospitals and other buildings can have windows and doors covered with mosquito screen- ing, made of either strong plastic or non-corrosive metal. It is essential that screening is kept in good repair. Screens of 6–8 mesh (i.e. 6–8 holes/cm) will exclude most mosquitoes. Finer-mesh screening will keep out smaller biting ﬂies, some of which may be vectors, but will appreciably reduce ventilation and light. If houses are unscreened, or if screening is defective, mosquito nets can be used to protect against night-biting mosquitoes. Nets should be tucked in under mattresses or bedding, never allowed to drape loosely over beds. Torn nets are useless unless they have been impregnated with pyrethroid insecticides (see Chapter 2, page 50). Nets should be placed over beds before sunset. The main disadvantage of nets is that they can reduce ventilation. Small spray-guns (e.g. ﬂit-guns) ﬁlled with solutions of pyrethrum or permethrin can be used to spray bedrooms early in the evenings to kill 30 Introduction to mosquitoes (Culicidae) resting mosquitoes, but pressurized aerosol canisters containing pyreth- roids have replaced ﬂit-guns in many parts of the world, although they are more expensive. Mosquito coils impregnated with pyrethroid insecticides, especially fast-acting ones such as bioallethrin, which when ignited smoulder for 6–10 hours to produce an insecticidal smoke, are commonly used in tropical countries. A more sophisticated, but more expensive, method is to place small insecticide-impregnated tablets (called vaporizing or fumigant mats) on a mains-operated electric mini-heater, giving protec- tion for up to 8–12 hours. An effective repellent is DEET, which has been used for over 50 years. Although it has periodically been suggested that it may cause side effects, most people apply it infrequently and are consequently exposed to very low dosages. In brief, people can still use DEET, although more recently repellents based on piperidines have become available, marketed under the names of Autan, Cutter Advanced, Bayrepel, Picaridin and Icaridin. These piperidine-based repellents are about as effective as DEET, but unlike DEET they do not attack plastics. Under optimal conditions these repellents can provide protection for 6–10 hours, the duration depending on the quantity of active ingredient. Citronella oil and lemon eucalyptus oil can give protection against mosquitoes, but only for about an hour. A new botanical repellent known as PMD (para-menthane-3,8-diol), derived from lemon eucalyptus, is rec- ognized as the only botanical repellent that gives good protection from mosquito bites. Repellents are applied to the hands, arms, neck and face (taking care to avoid the eyes), and the ankles and legs, irrespective of whether socks or long trousers are worn. Sweating and rubbing usually reduce the period of effectiveness of repellents. Repellent- or insecticide-impregnated (e.g. per- methrin or allethrin) clothing, such as wide-mesh jackets and hoods (as used by military personnel) give longer protection than repellents applied to the skin. If treated clothing is kept in plastic bags when not in use it should remain effective for many months before re-impregnation is needed. Aerosols, mists and fogs Motorized knapsack mist-blowers, shoulder-carried thermal foggers or boat- or vehicle-mounted machines that generate insecticidal aerosols (< 50 μm) or mists (51–100 μm) can be used to kill outdoor-resting (exo- philic) adult mosquitoes. Fogs are produced when very ﬁne aerosol drop- lets (5–15 μm) are so numerous that they substantially reduce visibility. Indoor-resting (endophilic) adults are also occasionally killed by mist- blowers or thermal foggers. Several insecticides can be used, including organophosphates and pyrethroids. Although such applications can be Further reading 31 spectacular, and please the public, there is very little residual effect. Areas cleared of adult mosquitoes are rapidly invaded by newly emerged adults and mosquitoes ﬂying in from outside the treated area. Repeated applica- tions are needed to sustain control. Applications of aerosols and mists are best made in calm weather, and usually in the evenings or early mornings when there are fewer thermals rising from the ground and less turbulence. Aerial applications from heli- copters or ﬁxed-wing aircraft usually give better coverage and more effec- tive control than ground-based operations. Ultra-low-volume applications Ultra-low-volume (ULV) techniques apply the minimum of concentrated insecticides, often just 150–400 ml/ha, as against 5–25 litres/ha with conventional spraying. This allows trucks or air- craft to spray much larger areas with a tank of insecticide before the tank needs reﬁlling. Insecticides commonly used include organophosphates and pyreth- roids. With aerial applications droplet size of the insecticide is bigger (150–200 μm) than that used in ground-based applications (50–100 μm) because they decrease in size, due to evaporation, as they fall to the ground. Generally the size of droplets hitting mosquitoes should be 15–25 μm. In addition to rapidly reducing outdoor resting and biting mosquitoes, ULV spraying is used in potential or actual epidemic situations to prevent or control disease outbreaks. In emergency situations aerial spraying gives fast and effective vector control, and has been used to stop transmission of dengue, Japanese encephalitis, and in North America various encephalitis viruses. Indoor residual spraying (IRS) Some mosquitoes, such as many malaria vectors and Culex quinquefasciatus, rest in houses before and/or after blood-feeding. Their populations can be reduced by insecticidal spraying of houses, but as this approach is mainly used in malaria control operations it is described in Chapter 2. It should be emphasized that most countries have legislation regulating what insecticides can be used against pests and vectors, and this may not necessarily be in accordance with WHO proposals. Further reading Becker, N., Petric, D., Zgomba, M. et al. (eds) (2010) The Mosquitoes and Their Control, 2nd edn. Heidelberg: Springer. Bock, G. R. and Cardew, G. (eds) (1996) Olfaction in Mosquito–Host Interactions. Chichester: Wiley. Bowen, M. F. (1991) The sensory physiology of host-seeking behavior in mosquitoes. Annual Review of Entomology, 36: 139–58. Carroll, S. P. and Loye, J. (2006) PMD, a registered botanical mosquito repellent with DEET-like efﬁcacy. Journal of the American Mosquito Control Association, 22: 507–14. 32 Introduction to mosquitoes (Culicidae) Clark, G. G. (coordinator) (1994) Prevention of tropical diseases: status of new and emerging vector control strategies. Proceedings of a sympo- sium on vector control. American Journal of Tropical Medicine and Hygiene, 50 (6) (Suppl.): 1–159. Clements, A. N. (1992) The Biology of Mosquitoes. Volume 1: Development, Nutrition and Reproduction. London: Chapman & amp; Hall. Clements, A. N. (1999) The Biology of Mosquitoes. Volume 2: Sensory Reception and Behaviour. Wallingford: CABI. Clements, A. N. (2011) The Biology of Mosquitoes. Volume 3: Viral and Bacterial Pathogens and Bacterial Symbionts. Wallingford: CABI. Floore, T. G. (ed) (2007) Biorational control of mosquitoes. AMCA Bulletin No. 7. Journal of the American Mosquito Control Association, 23 (Suppl.): 1–330. Foster, W. A. and Walker, E. D. (2009) Mosquitoes (Culicidae). In G. R. Mullen and L. A. Durden (eds), Medical and Veterinary Entomology, 2nd edn. Amsterdam: Elsevier, pp. 207–59. Horsfall, W. R. (1972) Mosquitoes: Their Bionomics and Relation to Disease. New York, NY: Hafner Journal of the American Mosquito Control Association (1995) Vector con- trol without chemicals: has it a future? A symposium. Journal of the American Mosquito Control Association, 11: 247–93. Lacey, L. A. and Lacey, C. M. (1990) The medical importance of riceland mosquitoes and their control using alternatives to chemical insecticides. Journal of the American Mosquito Control Association, 6 (Suppl. 2): 1–93. Laird, M. (1988) The Natural History of Larval Mosquito Habitats. London: Academic Press. Laird, M. and Miles, J. W. (eds) (1983) Integrated Mosquito Control Methodologies. Volume 1: Experience and Components from Conventional Chemical Control. London: Academic Press. Laird, M. and Miles J. W. (eds) (1985) Integrated Mosquito Control Methodologies. Volume 2: Biocontrol and Other Innovative Components, and Future Directions. London: Academic Press. Pates, H. and Curtis, C. (2005) Mosquito behavior and vector control. Annual Review of Entomology, 50: 53–70. Service, M. W. (1989) Rice, a challenge to health. Parasitology Today, 5: 162–5. Service, M. W. (1993) Mosquitoes (Culicidae). In R. P. Lane and R. W. Crosskey (eds), Medical Insects and Arachnids. London: Chapman & Hall, pp. 120–40. Silver, J. B. (2008) Mosquito Ecology: Field Sampling Methods, 3rd edn. Dordrecht: Springer. Spielman, A. and d’Antonio, M. (2001) Mosquito: a Natural History of Our Most Persistent and Deadly Foe. London: Faber and Faber. Walter Reed Biosystematics Unit (2010; continually updated) Vector Identiﬁcation Resources. www.wrbu.org. World Health Organization (1992) Vector resistance to pesticides. Fifteenth report of the WHO Expert Committee on Vector Biology and Control. World Health Organization Technical Report Series, 818: 1–71. Further reading 33 World Health Organization (1996) Operational Manual on the Application of Insecticides for Control of the Mosquito Vectors of Malaria and Other Diseases. WHO/CTD/VBC/96.1000. Geneva: World Health Organization. World Health Organization (1997) Vector Control: Methods for Use by Individuals and Communities, prepared by J. A. Rozendaal. Geneva: World Health Organization. World Health Organization (2006) Equipment for Vector Control: Speciﬁcation Guidelines. Geneva: World Health Organization. See also references at the ends of Chapters 2 and 3. 2 Anopheline mosquitoes (Anophelinae) Life cycle 35 The subfamily Anophelinae contains three genera, but as explained in Chapter 1 only the genus Anopheles is of medical importance. Anopheles mosquitoes have an almost worldwide distribution, occurring in both tropical and temperate regions, but they are absent from most Paciﬁc islands including New Zealand. There are about 476 species. The most important disease transmitted by Anopheles mosquitoes is malaria. Some Anopheles species are vectors of ﬁlariasis, especially that caused by Wuchereria bancrofti, but other species transmit Brugia malayi and Brugia timori. A few species transmit arboviruses that are mainly of minor medical importance. 2.1 External morphology The main features distinguishing the Anophelinae from the Culicinae have been given in Chapter 1, but are brieﬂy summarized here. Anopheline eggs are laid singly and have air-ﬁlled ﬂoats (Fig. 1.8) that help them ﬂoat on the water surface. Larvae do not have a siphon and consequently lie parallel to the water surface (Fig. 1.13). A tergal plate and paired palmate hairs are present dorsally on most abdominal segments (Fig. 1.9). Pupal abdominal segments have numerous short setae, and segments 2–7 or 3–7 have in addition short peg-like spines (Fig. 1.11) which are absent in culicines. Most, but not all, adult Anopheles have spotted wings, that is the dark and pale scales are arranged in small blocks or areas on the veins (Fig. 1.12, Plate 1). The number, length and arrangement of these dark and pale areas differ considerably in different species and provide useful characters for species identiﬁcation. Unlike culicines, the dorsal and ventral surfaces of the abdomen are almost, or entirely, devoid of appressed scales. In both sexes the palps are about as long as the proboscis, and in males, but not females, they are enlarged (i.e. clubbed) apically (Fig. 1.13). See Chapter 1 (page 14) for minor differences distinguishing anophelines from culicines. 2.2 Life cycle After mating and blood-feeding Anopheles lay some 50–200 small brown or blackish boat-shaped eggs (Fig. 1.8) on the water surface. Anopheles eggs cannot withstand desiccation and in tropical countries hatch within 2–3 days, but in colder temperate climates hatching may not occur until after about 2–3 weeks, the duration depending on temperature. As in all mosquitoes there are four larval instars. Anopheles larvae are ﬁlter-feeders and unless disturbed remain at the water surface, feeding on bacteria, yeasts, protozoans and other microorganisms. When feeding, larvae rotate their heads through 180 degrees so that the ventrally posi- tioned mouthbrushes can sweep the underside of the water surface. Larvae 36 Anopheline mosquitoes (Anophelinae) are easily disturbed by shadows or vibrations and respond by swimming quickly to the bottom of the water. They resurface some seconds or minutes later. Unlike culicine larvae, they lack a siphon and so breathe in air through their posterior spiracles. Anopheles larvae occur in many different types of more or less permanent habitats, ranging from freshwater and saltwater marshes, mangrove swamps and riceﬁelds to grassy ditches, wells, edges of streams and rivers as well as ponds and borrow pits. Larvae are also found in small and often temporary habitats such as puddles, hoofprints, discarded tin cans and sometimes water-storage pots. A few species occur in water-ﬁlled tree- holes. In the Neotropical region (Central and South America and the West Indies) a few Anopheles breed in water that collects in the leaf axils of epiphytic plants such as bromeliads, which somewhat resemble pineapple plants, but grow on tree branches. Some Anopheles prefer habitats with aquatic vegetation while others favour waters without vegetation; some species like exposed sunlit waters whereas others prefer more shaded larval habitats. In general Anopheles are found in clean and unpolluted waters, usually being absent from habitats containing rotting plants or faeces. In tropical countries the larval period frequently lasts only about 7 days, but in cooler climates the larval period may be 2–4 weeks. In temperate areas some Anopheles overwinter as larvae and consequently may live many months. The comma-shaped pupae normally remain ﬂoating at the water surface, but when disturbed they swim vigorously down to the bottom with characteristic jerky movements. The pupal period lasts 2–3 days in tropical countries but sometimes as long as 1–2 weeks in cooler climates, after which the adult mosquito emerges. 2.2.1 Adult biology and behaviour Most Anopheles are crepuscular or nocturnal in their activities. Thus blood- feeding and oviposition normally occur in the evenings, at night or in the early mornings around sunrise. Some species, such as An. albimanus, a malaria vector in Central and South America, bite people mainly outdoors (exophagic) from about sunset to 21:00 hours. In contrast, in Africa species of the An. gambiae species complex, which contains probably the world’s most efﬁcient malaria vectors, bite mainly after 23:00 hours to just before sunrise, and this is mostly indoors (endophagic). As already discussed in Chapter 1, the times of biting, and whether adult mosquitoes are exophagic or endophagic, may be epidemiologically important. Both before and after blood-feeding some species rest in houses (endophilic), whereas others rest outdoors (exophilic) in a variety of shelters, such as amongst vegetation, in rodent burrows, in cracks and crevices in trees, under bridges, in termite mounds, in caves and rock ﬁssures, and in cracks in the ground. Most Anopheles species are not exclusively exophagic or Medical importance 37 endophagic, exophilic or endophilic, but exhibit a mixture of these extremes of behaviour. Similarly, few Anopheles feed exclusively on either humans or non-humans, most feeding on both people and animals, but the degree of anthropophagism and zoophagism varies according to species. For example, An. culicifacies, an important Indian malaria vector, commonly feeds on cattle as well as humans, whereas in Africa An. gambiae s. str. (a species of the An. gambiae species complex) feeds more infrequently on cattle and thus maintains a stronger mosquito–human contact. This is one of the reasons why An. gambiae is a more efﬁcient malaria vector than An. culicifacies. 2.3 Medical importance 2.3.1 Biting nuisance Although Anopheles mosquitoes may not be disease vectors in an area they may nevertheless be a biting nuisance. Usually, however, it is culicine mosquitoes, especially Aedes and Psorophora species, that cause biting problems. 2.3.2 Malaria Only mosquitoes of the genus Anopheles transmit the parasites causing human malaria. The most important malarial parasites are Plasmodium falci- parum, P. vivax, P. malariae and P. ovale, but recently it was discovered that a ﬁfth species, P. knowlesi, which infects mainly macaque monkeys (Macaca species) in South Asia, can also cause malaria in humans. Because the sexual cycle of the malaria parasite occurs in the vector, it is conventional to call the mosquito the deﬁnitive host, and humans the intermediate host. Male and female malaria gametocytes ingested by female mosquitoes during blood-feeding pass to the mosquito’s stomach, where they undergo cyclical development that includes a sexual cycle termed sporogony. Only gametocytes survive in the mosquito’s stomach; all other blood forms of the malaria parasites (the asexual forms) are destroyed. Male gametocytes (microgametocytes) extrude ﬂagella which are the male gametes (micro- gametes), and the process is called exﬂagellation. The microgametes break free and fertilize the female gametes (macrogametes) which have formed from the macrogametocytes. As a result of fertilization a zygote is formed, which elongates to become an ookinete. This penetrates the wall of the mosquito’s stomach and reaches its outer membrane, where it becomes spherical and develops into an oocyst, which can be seen on the stomach walls of vectors about 4–5 days after an infective blood-meal. The nucleus of the oocyst divides repeatedly to produce numerous spindle-shaped sporozoites. After about 8 days the oocyst is fully grown (about 40–80 μm) and ruptures to release thousands of sporozoites into the hae- mocoel of the mosquito. The sporozoites (10–15 μm) are carried in the 38 Anopheline mosquitoes (Anophelinae) insect’s haemolymph to all parts of the body, but most penetrate the salivary glands, where they are usually found after 9–14 days. However, the time required for this cyclical development (extrinsic cycle) depends on both temperature and Plasmodium species. At 30 °C sporogony in P. falciparum takes 9 days, at 25 °C 10 days, and at 20 °C 23 days, while below 17 °C it cannot be completed. With Plasmodium vivax sporogony develops faster: it is completed in 9 days at 25 °C and in 16 days at 20 °C. The mosquito is now infective, and sporozoites are inoculated into people the next time the mosquito bites. A single oocyst produces 1000 or more sporozoites, and it has been estimated that in heavy infections there may be as many as 60 000–70 000 sporozoites in the vector’s salivary glands. However, the number may be much smaller than this, and very few (sometimes just 5–10) are actually injected into a person during feeding. The sporozoite rate, that is the percentage of female vectors with sporo- zoites in their salivary glands, varies considerably from species to species of mosquito but also according to locality and season. Sporozoite rates are often about 1–5% in species such as An. gambiae and An. arabiensis of the An. gambiae species complex, but less than 1% in many other species such as An. albimanus and An. culicifacies. For practical purposes it can be said that once a vector becomes infective it remains so throughout its life. 2.3.3 Important malaria vectors Although there are some 476 species of Anopheles only about 70 transmit human malaria, and of these probably only about 40 are important ones. Malaria vectors are often divided into primary and secondary vectors, but this can be misleading because a species may be considered a primary vector in some areas but only a secondary vector in others. Although presenting a list of important malaria vectors is somewhat subjective I have nevertheless attempted to do this, and I provide notes on their principal larval habitats and biting behaviour. These notes are only a guide to their behaviour, which may vary in different parts of a species’ geographical range. Several species occur as species complexes, which comprise virtually identical-looking species that can be separated only by their chromosomal banding patterns, by biochemical procedures or by molecular methods. However, species within a complex may differ in their behaviour, distribution and vector status. The best known complex is probably the An. gambiae species complex. To give an example of the differences in biology and vector status that can occur in a species complex, mosquitoes of the An. gambiae complex are described next. (1) Sub-Saharan Africa Anopheles gambiae The most anthropophagic species and the most important malaria vector of the eight species comprising the An. gambiae Medical importance 39 species complex is An. gambiae s. str. Larval habitats are sunlit pools, puddles, hoofprints, borrow pits and riceﬁelds. Adults bite humans both indoors and outdoors, and also feed on domesticated animals. They rest mainly indoors, but sometimes outdoors. Other malaria vectors in the An. gambiae species complex are An. arabiensis, An. melas, An. merus, An. bwam- bae, An. quadriannulatus species A, An. quadriannulatus species B and An. comorensis, and these are very brieﬂy discussed below. Anopheles arabiensis Another important malaria vector. Larvae in the same habitats as An. gambiae. Adults bite humans indoors and outdoors but also cattle; after feeding they rest either indoors or outdoors. This species tends to occur in drier areas than An. gambiae, and is more likely to bite cattle and rest outdoors than An. gambiae. Anopheles melas and An. merus An. melas is found in West Africa, where it occurs in coastal salt waters such as mangrove swamps, while An. merus is a coastal saltwater species in East and southern Africa, but can also be found breeding in inland saltwater habitats. Adults of both species bite humans and rest both indoors and outdoors; they are both regarded as secondary malaria vectors. Anopheles bwambae A rare species restricted to breeding in the warm mineral springs in Semuliki National Park, Uganda. Not considered an important vector, although locally it can transmit malaria. Anopheles quadriannulatus and An. comorensis An. quadriannulatus species A and B both feed on cattle and are not considered malaria vectors. The ﬁnal member of the An. gambiae species complex is An. comorensis, a very rare species found only on Mayotte, Comoros archipelago; it is not considered to be a vector. Anopheles funestus Larvae occur in more or less permanent waters, especially those with vegetation, such as marshes, edges of streams, rivers and ditches, and riceﬁelds with mature plants providing shade. Prefers shaded habitats. Adults bite humans predominantly, but also domesticated animals. Feeds indoors and also outdoors; after feeding adults rest mainly indoors. (2) Europe, North Africa and the Middle East Anopheles atroparvus One of the species in the An. maculipennis species complex. Sunlit and exposed pools and ditches with either fresh or brackish water, also riceﬁelds. Adults bite humans and domesticated animals and usually rest in stables, cowsheds and piggeries. Adults hibernate in these 40 Anopheline mosquitoes (Anophelinae) and other shelters during the winter, but periodically emerge to take blood- meals. Anopheles labranchiae Another species in the An. maculipennis species complex. Brackish waters of coastal marshes, freshwater marshes, rice- ﬁelds, edges of grassy streams and ditches; prefers sunlight. Bites humans and domesticated animals indoors and outdoors; rests mainly in houses or animal shelters after feeding. Overwinters as hibernating adults. Anopheles pharoensis Marshes, ponds, especially those with abundant grassy or ﬂoating vegetation, also riceﬁelds. Adults bite humans and animals indoors or outdoors, and rest outdoors after feeding. Anopheles sacharovi Fresh or brackish waters of coastal or inland marshes, pools and ponds, especially those with vegetation. Prefers sunlit habitats. Bites humans and animals indoors or outdoors; usually rests in houses or animal shelters after feeding. Anopheles sergentii Borrow pits, riceﬁelds, ditches, seepage waters, slow- ﬂowing streams, sunlit or partially shaded habitats. Adults bite humans or animals indoors or outdoors, resting in houses and caves after feeding. Anopheles stephensi Probably a species within a complex. Can be an important vector locally, especially in towns. Apart from being found in Egypt, Iraq, Iran and Saudi Arabia it is common in the Indian subcontinent, where it is commonly the main vector of urban malaria. Larvae breed in fresh, brackish or even polluted waters in man-made habitats such as water tanks, cisterns, wells, gutters, water-storage jars and containers. Adults bite humans indoors or outdoors, and rest mainly indoors afterwards. Anopheles stephensi has a very wide distribution extending from the Middle East across Pakistan and India, to Myanmar, Thailand and China. Anopheles superpictus Flowing waters such as torrents of shallow water over rocky streams, pools in rivers, muddy hill streams. Vegetation may be present; prefers sunlight. Bites humans and animals indoors and out- doors, and after feeding rests mainly in houses and animal shelters, but also in caves. (3) Indian subcontinent Anopheles annularis A species in the An. annularis species complex. Can be an important vector in India. Larvae in ponds, especially those with vegetation, swamps and riceﬁelds. Adults bite humans and cattle outdoors and indoors, and rest mainly outdoors after feeding. Medical importance 41 Anopheles baimai Pools, small streams, ditches, animal footprints, in partial sunlight or in forests. Bites humans both indoors and outdoors, and also domesticated animals; often enters houses to feed, but rests outdoors. Anopheles culicifacies A species in the An. culicifacies species complex. Most important vector in the Indian subcontinent. Larvae in a variety of clean and unpolluted habitats, irrigation ditches, riceﬁelds, pools, wells, borrow pits, edges of streams, marshes, and occasionally in brackish waters. Adults prefer domesticated animals but commonly bite humans indoors or outdoors; rests mainly indoors after feeding. The main malaria vector in much of the region. Anopheles ﬂuviatilis A species in the An. ﬂuviatilis species complex. Flowing waters such as hill streams, pools in riverbeds, irrigation ditches, seepages; prefers sunlight. Bites humans and domesticated animals; feeds and rests either indoors or outdoors. Anopheles minimus A species in the An. minimus species complex. Flowing waters such as foothill streams, springs, irrigation ditches, rice- ﬁelds, seepages, borrow pits; prefers shaded areas. Feeds mainly on humans, but will bite domesticated animals; feeds and rests mainly indoors. Anopheles stephensi See entry under Europe, North Africa and the Middle East. Anopheles sundaicus A spe

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