FIGURE 12.18 Comparison of typical positions of mosquito adults resting on a vertical surface. (A) Culicine; (B) anopheline. Culicines typically hold the abdomen parallel to the substrate or pointed toward it, and the proboscis and abdomen form an angle. Anophelines characteristically tilt the body at a sharp angle to the substrate, with the abdomen pointing away from ic, and with the proboscis and abdomen in line. (From Marshall, 1938.)

Anophelines, on the other hand, hold the proboscis and abdomen in line, oblique to the substrate {Fig, 12.18B). This distinctive position also is apparent during feeding. While at rest, adults perform various stereotyped grooming movements and frequently wave their hindlegs.

Each mosquito species has a characteristic pattern of diel activityunder the control of an endogenous circa-dian rhythm that is entrained by the daily light-dark cycle. There are generally one or two flight periods each day, characterized as being diurnal, nocturnal, or crepuscular (dawn and dusk). During these periods, both sexes will take flight without external cues. It is likely that mosquitoes have a generalized search pattern during foraging flights, responding to stimuli associated with mating sites, sugar sources, hosts, or oviposition sites as they encounter them, depending on their needs. Mosquito species vary in the habitats where they forage for mates and food. Some fly over varied terrain; others tend to be active in either wooded or open areas; still others perform all activities close to larval and resting sites. There is some evidence that adult females become familiar with local habitats that provide both food and oviposition sites and tend to remain there.

Dispersal of some species is only a few dozen meters from their larval habitats, for most species less than 2 km. Such ranges are typical of domestic species and result from random elements in their repeated foraging flights for hosts, sugar sources, resting sites, and oviposition sites. Other species enter a specific dispersal mode that is wind-assisted or light-directed and carries them dozens or even hundreds of kilometers from their origins. These one-way movements are most obvious following massive adult emergences of species with quiescent eggs, such as the salt-marsh mosquito Ochlerotatus taeniorhynchus after high tides and floodwater mosquitoes such as Aedes vexans in bottomlands after heavy rain. The average dispersal distance of such broods is difficult to determine accurately, because efforts to recapture marked specimens must be made over vast areas, and relatively few are caught. Some salt-marsh species make extended, round-trip migrations to complete their gonotrophic cycles when breeding sites and blood feeding sites are many kilometers apart. Average flight speed also is difficult to determine under natural conditions. Ac. aegypti can fly upwind at air speeds up to 5.4 km/hr, while other species in a dispersing mode are estimated to fly much faster. However, their ground speed drops nearly to zero as headwind velocity approaches their maximum air speed. Thus mosquitoes tend to avoid flight under windy conditions, except when a tailwind assists their flight. Mosquito dispersal in its various forms has been reviewed by Service (1997),

Mating usually takes place a few days after adult emergence. The males typically form flight swarms at particular times at swarm markers (prominent objects or other contrasting features of the environment). Each male follows a looping flight path over the marker. In species such as Ae. aegypti and Ae. albopictus, the female's preferred host serves as the swarm marker. When a female enters a swarm, males detect the characteristic frequency of her wing beat and her position with their plumose antennae and Johnston's organs. Her tone varies from about 150 to 600 Hz, depending on the temperature and her size and species. It is about 100—250 Hz lower than the males' flight sound. The male turns toward the female, pursues her, and couples with her. Swarms are usually species-specific, but mixed swarms occur. If the female is of another species, males either do not respond to her flight tone or release her upon detecting that she lacks the appropriate species-specific contact pheromones. Otherwise, he may attempt copulation. Successful copulation usually occurs only with the first conspecific male to orient to the female, venter-to-venter, clasping her genitalia in his. The couple drifts or flies from the swarm, often shifting to an end-to-end position, with the female flying forward and the male facing backward, clinging to her only by his genitalia. Mating may be completed in the air or on vegetation. Copulation lasts from 12 sec to several minutes.

There are many exceptions to this standard method of mating. Males of Deinocerites and Opifex guard pupae at the water surface and mate with the females

as they emerge. Males of Cs. inornata remain at the emergence site for long periods and locate newly emerged females at random while crawling about, recognizing them by a specific contact pheromone on their legs. A male Eretmapodites chrysogaster will follow a female in tandem flight to a host, wait beside her while she takes a blood meal, then copulate when she is finished. Males of the sabethine genera Limatus, Sabethes, Wyeomyia., and Topomyia locate females at rest on vines, sticks, and tree trunks and perform a variety of leg-waving and genitalic courtship rituals before insemination. Several aspects of mosquito mating behavior have been reviewed by Downes (1969).

During copulation the male deposits a mixture of sperm and accessory gland secretion in the female's seminal bursa or genital chamber. The semen often produces a distinct seminal mass in the bursa or genital chamber, sometimes called a mating plug. It disappears in 1—2 days and therefore does not, by itself, prevent subsequent insemination. Within an hour the sperm move into the spermathecae, where they are stored. At least in culicine mosquitoes, the swollen bursa itself and, later, a substance in the accessory fluid called matrone cause the female to become unreceptive to males. Substances in the accessory fluid also can affect feeding behavior and promote egg development and oviposition. A single insemination usually is sufficient for the life of a female. Most evidence indicates that females only rarely receive sperm from more than one male.

Adult mosquitoes of both sexes of most species regularly feed on plant sugar throughout life, but only females feed on vertebrate blood. Water presumably is taken from the surface of moist substrates as well as in sugar meals and blood meals. Field studies and experiments indicate that some species are guided in their foraging flights by specific visual features along the horizon, or they fly along the edges of tree stands bordering open terrain. Others apparently simply fly crosswind or downwind, depending on wind speed. When they can see likely sources of sugar or blood, they alter their flight paths to move directly toward the object. If they detect odors of flowers or hosts in the absence of visual information about a food source, they turn to fly upwind within the downwind drifting odor plume, eventually arriving at the odor source.

Sugar feeding starts soon after emergence, usually before females begin responding to host stimuli. Sugar is taken frequently by both sexes throughout adult life, both between and during gonotrophic cycles. Females of some domestic species take sugar infrequently or never (e.g., Ae. aegypti and An.gambiae in some localities); they typically live in close association with their hosts and utilize blood for both energy and reproduction. Sugar sources include floral and extrafloral nectaries, homopteran hon-eydew, spoiled or damaged fruit, tree sap, and damaged or even undamaged plant leaves and stems. Malaya species solicit regurgitated nectar and honeydew from ants. Nectar and honeydew are the most important sugar sources. They contain not only sugar but also amino acids; these are insufficient to initiate egg development but probably promote longevity. Most mosquitoes obtain nectar from a variety of plant species; others seem to be fairly specific in their choices, and a few are important pollinators of particular plant species whose flowers they visit. Mosquitoes generally feed from fragrant, light-colored, clustered flowers with short corollas that allow easy access to the nectar. Details of sugar feeding have been reviewed by Foster (1995).

Female mosquitoes rarely begin responding to vertebrate hosts and taking blood meals until at least 1—3 days after adult emergence and often not until after mating and sugar feeding. Their hosts include all classes of vertebrates: mammals, birds, reptiles, amphibians, and even amphibious fish. They have been reported to take hemolymph from other insects, but perhaps this occurs only when the insects have been contaminated with vertebrate odors. Host specificity and host preference vary widely. Some species feed almost entirely on members of one genus of animal; others opportunistically attack members of two or three vertebrate classes. Blood-meal identification methods, used to determine mosquito—host specificity, have been reviewed by Washino and Tempelis (1983). Host specificity is a function of both the mosquito's innate host preference and the hosts available to the mosquito when and where it is active. Some species forage over a broad range of habitats. Others are active principally in either wooded or open areas or remain close to sites of larval development or adult resting. Still other species attack their hosts in rather narrowly defined zones within a habitat. For example, within tropical forests, different species feed in different strata: ground level, intermediate levels, and just below the leaf canopy.

Host-finding behavior in mosquitoes involves the use of volatile chemicals to locate vertebrate hosts. Carbon dioxide, lactic acid, and octenol are among the best-documented host attractants. Other skin emanations also are known to be important, because odors from live hosts are always more attractive than any combination of these chemicals in a warm, humid airstream. Fatty acids produced by the normal bacterial flora of the skin are particularly effective in attracting An. gambiae to human feet. Mixtures of these fatty acids probably play a major role in attracting most mosquitoes. Subtle differences in these odors of different host species and even different individuals undoubtedly play a role in host preference. These odors commonly have a combined effective range of 7— 30 m, but the range can be up to 60 m for some species. Vision also is important in orienting to hosts, particularly for diurnal species and especially in an open environment and at intermediate or close ranges. Dark, contrasting, and moving objects are particularly attractive. As the female approaches to within 1—2 m of a potential host, chemical and visual cues are still important, but convec-tive heat and humidity surrounding the body also come into play. Odor, carbon dioxide, heat, and humidity all are detected by sensilta on the antennae and palps. Host-finding behavior in mosquitoes was reviewed by Bowen (1991). Specific behavioral and physiological aspects of attraction have been reviewed by a series of authors in the proceedings of a symposium (Anon. 1994).

If the suite of host stimuli is acceptable, the female attempts to land on the host animal, often preferring certain body parts, such as the head or legs. Upon landing, she proceeds through four phases of feeding behavior: exploration, penetration and vessel-seeking, imbibing, and withdrawal. She typically remains motionless for a few seconds, then begins exploratory movements, including contacting the skin surface with her proboscis in probing motions. If the host is not suitable, she may wander for a considerable time and leave without feeding. Even on a suitable animal she usually explores at least briefly before selecting a spot that is likely to be well vascularized. Probing activity is stimulated by heat, moisture, and probably also by chemicals on the surface of the skin. As in the case of airborne attraction, these stimuli are detected by antenna! and palpal receptors, but receptors on the proboscis, tarsi, and elsewhere on the legs apparently also are important.

Mosquitoes can feed from a variety of skin surfaces, including the moist skin of frogs and the scaly legs of reptiles and birds. They can penetrate mucus, matted hair, light layers of feathers, and heavy cloth such as denim, provided it is not thicker than the length of the proboscis. Once a feeding site is selected, the fascicle of stylets pierces the skin white the labium serves as its guide and is bent backwards without penetrating (Fig. 12.19). The maxillae and mandibles on each side of the fascicle alternately slide by each other in quick stabbing/puncturing movements. White they do this, the tissue is gripped with the backward-directed maxillary teeth as the stylets penetrate epidermal and subepidermal tissue.

Saliva flows from the tip of the hypopharynx as the flexible end of the fascicle bends at sharp angles, probing in various directions within the subepidermal tissue in search of a small arteriole or venule. The saliva contains an antihemostatic enzyme, apyra.se, which inhibits platelet aggregation and causes randomly punctured vessels to bleed freely into the surrounding tissue spaces. This makes it easier for the mosquito to locate a vessel and shortens the total time on the host. The saliva also contains anticoagulants, which facilitate vessel location and blood ingestion by preventing the blood from clotting. Sensilla on the labrum and in the cibarium apparently

FIGURE 12.19 Femaie mosquito (Aides atsgypti), showing position of mouthparts during blood-feeding. The fascicle is exsheathed from the labium along part of its length while the labium buckles backward, allowing the fascicle to pierce the skin in search of a blood vessel. (Photo by W. A. Foster.)

FIGURE 12.19 Femaie mosquito (Aides atsgypti), showing position of mouthparts during blood-feeding. The fascicle is exsheathed from the labium along part of its length while the labium buckles backward, allowing the fascicle to pierce the skin in search of a blood vessel. (Photo by W. A. Foster.)

detect plasma and cellular factors, including adenyl nucleotides, such as adenosine triphosphate, which help the mosquito to locate a blood vessel and stimulate ingestion. Upon finding a vessel, the female slips the tip of her fascicle into the tumen and draws blood up through the food canal by pumps in the cibarium and pharynx. The blood accumulates in the midgut, allowing the mosquito to engorge fully in 1-4 min. During this time, the female begins to extract water from the blood meal and may deposit small droplets of urine on the host's skin. In some Anopheles species, copious fluid excretion begins early, including some blood cells from the accumulating meal, and it appears red. This is due to removal of liquid from the meal directly into the hindgut, a process known as prediuresis, rather than by way of the bemolymph and maipighian tubules. When abdominal stretch receptors signal the presence of sufficient blood in the midgut, the female pushes with her forelegs to withdraw her stylets and flies away. Usually she is too heavy to fly far until a substantial amount of water and salt in the btood meal has been excreted, after 1—2 hr.

White digesting the meal and developing eggs, females locate species-characteristic resting sites and may remain there until the eggs are mature. However, females of many species are known to leave their resting sites during each daily activity period throughout the gonotrophic cycle. These flights allow them to obtain sugar meals or supplementary blood meals, to relocate closer to an oviposition site, or perhaps simply to find a more suitable resting site. In at least some species, a hormone from the ovaries in the trophic phase inhibits the mosquito's responsiveness to host attractants by blocking host-odor receptors on the antennae, provided she has substantial energy reserves (see Klowden, 1996 for a brief review).

Oviposition generally occurs during the same part of the day as mating and feeding. Gravid females locate and evaluate suitable sites by using chemical and visual cues, including organic chemicals, salts, high humidity, dark cavities, and reflective surfaces. The organic chemical cues are derived from decaying organic matter, microorganisms, the chemical byproducts of larvae or pupae that have previously developed there, and the presence of mosquito eggs that have been deposited by other females. The apical droplets on the eggs of Cx. quinquefasciatus contain an oviposition-attractant pheromone.

Within each genus of mosquito, there is considerable variation among species in their oviposition-site preferences and, therefore, their larval habitats. In general, Anopheles species occur in permanent or semipermanent water, such as the edges of lakes, ponds, streams, and pools; others develop in temporary rain puddles, leaf axils, and tree holes. Culex typically lay eggs in permanent or semipermanent pools, ponds, and water containers. Several medically important species of both Anopheles and Culex develop in large bodies of surface water and take advantage of irrigated fields and of reservoirs created by dams. Culiseta are found in several kinds of permanent surface pools; some species have very narrow requirements. Coquillet-tidia and Mansonia oviposit in permanent bodies of water that contain floating or emergent aquatic plants to which the immatures can attach. Aedes, Ochlerotatus, Psorophora, and Haemagogus species lay their eggs on damp surfaces where they will be inundated by temporary water or a rising water level. Aedine species and ecologically similar mosquitoes form two general categories, according to typical habitat: (1) floodwater mosquitoes, which include floodplain species, salt-marsh species, and snowpool and spring species; some floodplain species have become prolific in rice fields and other forms of irrigation; and (2) container mosquitoes, including leaf-axil species, tree-hole species, and artificial-container species. Several medically important species utilize both tree holes and artificial containers. Among genera of minor importance, Toxorhyn-chites lay their eggs only in natural and artificial containers in wooded areas; Wyeomyia oviposits primarily in leaf axils; and Deinocerites oviposits exclusively in crab holes in tidal mudflats and mangrove swamps.

The distribution of mosquito eggs reflects the availability, size, and stability of the larval habitats used by a species. Though mosquito life histories are highly variable, the oviposition behavior of mosquitoes tends to follow along taxonomic lines. Most mosquitoes fall into one of three behavioral categories: (l)Eggs laid out of water. Species in this group may distribute eggs of a single clutch broadly among several potential development sites, particularly if those sites are common but small. Container species such as Ae. aegypti, Ae. albopictus, and Haemagogus species deposit the eggs at varying distances above the water line, and at least Ae. aegypti lays only a portion of the clutch in each water container. Floodwater species such as Ae. vexans, Ochlerotatus dorsalis, and the salt-marsh—inhabiting Oc. taeniorhychus generally scatter their eggs widely over areas where water will accumulate, inserting them into crevices of drying mud or plant debris in low ground. (2)Eggsplaced on or in water. Mosquitoes in this category lay the entire clutch in a clump at one site while standing on the water surface or on floating vegetation. The egg rafts of Culex, Culiseta, Coquillettidia, and Uranotaenia species are formed between the female's hindlegs as she deposits each egg on end in the water, one against the next. Some Armigeres species suspend the egg raft above the water with their hindlegs while forming it and then carry it with them before placing it on the water. Trichoprosopon digitatum females stand guard over the raft until the eggs hatch. Mansonia species prepare their egg clusters underwater, attached to a plant, while standing on the floating leaves of aquatic plants. Exceptional species in various genera deposit egg rafts on top of floating vegetation, lay their eggs singly underwater on the sides of rock pools, or enter beetle holes in bamboo and extrude the eggs in ribbons. (3)Eggs dropped onto water. Species in this group oviposit aerially while hovering. Anopheles drop all of them at one site or distribute them among several smaller sites. Toxorhynchites and most culicine species in the tribe Sabethini (e.g., Wyeomyia and Sabethes) propel a few eggs into each of many container habitats with a flick of the abdomen, often through very small openings in tree limbs or bamboo. If a mosquito cannot find suitable oviposition sites when the eggs are mature, it may lay them in suboptimal situations or retain them until a suitable site is found. Retained eggs gradually lose their viability over several weeks or months. An extensive review of oviposition behavior is given by Bentley and Day (1989).

Mosquito dormancy occurs in all but those tropical and subtropical habitats that provide conditions for year-round larval development. The life stage that becomes dormant depends on the severity of a region's winter or dry season and also on the species. Species of Aedes, Ochlerotatus, Psorophora, and Haemagogus, which all have quiescent eggs, typically overwinter (hibernate) or oversummer (aestivate) as eggs. Larvae serve as the dormant stage in mosquitoes whose adult activity is precluded seasonally but whose breeding sites are protected from severe cold or complete drying. When adults overwinter as the dormant stage, typically in Anopheles and Culex, they seclude themselves in well-protected harborages, or hibemacula. Prior to dormancy, mosquitoes often enter diapause, a physiological state of arrested development that is induced or broken only by specific environmental cues. Facultative egg diapause, a feature of multivol-tine species, is induced by exposure of the pupae or adult females to lowered temperatures and short photoperiods. They lay diapausing eggs, which will not hatch until the day length is appropriate, even during unseasonably warm periods in autumn, winter, or early spring, when the resulting larvae and adults might not survive. Obligate egg diapause occurs in univoltine species, regardless of preceding conditions, and is maintained despite warm, long-day conditions. This is typical of snowpool and spring Ochlerotatus species in cold and temperate climates. Diapause is broken after the eggs have been subjected to winter conditions (in the case of obligate diapause) and when favorable temperatures and long days resume. Larval diapause is similar to facultative egg diapause in its induction and termination. Diapausing larvae feed and grow little or not at all, and they do not molt.

Temperate species destined to overwinter as adult females emerge in a state of reproductive diapause induced by larval and pupal exposure to shortening photoperiod and cool temperatures. Although these females mate, their egg follicles do not reach the resting stage, despite frequent sugar feeding and accumulation of extensive fat reserves. Fattened female Culex species that hibernate through hard winters forego all further feeding until the onset of spring, whereas in milder climates they periodically leave their overwintering sites to take sugar meals. Although diapausing Culex adults rarely feed on blood, some Anopheles species may take blood meals fairly regularly from hosts near these sites. They develop no eggs, however, exhibiting gonotrophic dissociation. Other overwintering Anopheles continue to feed and develop eggs, but these are not laid. Similarly, some tropical Anopheles take blood repeatedly during the dry season and remain continually gravid because there is nowhere to oviposit. These phenomena are sometimes referred to as gonotrophic discordance, a term that also applies to the taking of nonvitellogenic or otherwise supplementary blood meals, mentioned previously.

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