Odor Mediated Behavior

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Annu. Rev. Entomol. 1999. 44:131–57 c 1999 by Annual Reviews. All rights reserved Copyright °

ODOR-MEDIATED BEHAVIOR OF AFROTROPICAL MALARIA MOSQUITOES Willem Takken Laboratory of Entomology, Wageningen Agricultural University, P.O. Box 8031, 6700 EH Wageningen, the Netherlands; e-mail: [email protected]

Bart G. J. Knols International Centre of Insect Physiology and Ecology, P.O. Box 30772, Nairobi, Kenya; e-mail: [email protected] KEY WORDS:

semiochemicals, mating, sugar feeding, host seeking, oviposition

ABSTRACT The African mosquito species Anopheles gambiae sensu lato s.l. and Anopheles funestus rank among the world’s most efficient vectors of human malaria. Their unique bionomics, particularly their anthropophilic, endophagic and endophilic characters, guarantee a strong mosquito-host interaction, favorable to malaria transmission. Olfactory cues govern the various behaviors of female mosquitoes and here we review the role of semiochemicals in the life history of African malaria vectors. Recent evidence points towards the existence of human-specific kairomones affecting host-seeking A. gambiae s.l., and efforts are under way to identify the volatiles mediating this behavior. Based on examples from other Culicidae spp., it is argued that there is good reason to assume that mating, sugar feeding, and oviposition behavior in Afrotropical malaria vectors may also be mediated by semiochemicals. It is foreseen that increased knowledge of odor-mediated behaviors will be applied in the development of novel sampling techniques and possibly alternative methods of intervention to control malaria.

131 0066-4170/99/0101-0131$08.00

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We dedicate this review to Prof. Jaap J. Laarman, pioneer researcher in olfactory behavior of malaria vectors, who passed away on November 23, 1997.

INTRODUCTION Malaria in Africa remains one of the most serious obstacles for development, with an estimated cost of $1.8 billion per annum. It represents 9% of the total disease burden and results in over one million deaths annually, mainly of young children (192). Widespread chloroquine resistance and general drug failure force governments to adopt more expensive drugs as first-line treatments. Advances in molecular biology have led to the development of new vaccines and identification of genes that code for refractoriness of mosquitoes to infection with Plasmodium parasites, but large-scale application of these techniques is not envisaged within the next two decades (30, 39, 63). Tolerance and resistance of malaria vectors to a variety of insecticides has been documented (49, 69). Recent large-scale trials with pyrethroid-impregnated bednets in Africa have demonstrated their impact on child morbidity and mortality (128), but it remains to be seen whether such effects can be sustained and obtained in regions with intense perennial transmission. Moreover, such systems select for behavioral resistance in mosquitoes and induce changes in their biting cycle and indoor/outdoor feeding behavior and may therefore render bednets useless in the long run (119). Our understanding of the dynamics of malaria vector populations in sub-Saharan Africa, their behavior and chemical ecology, and how these affect transmission of disease is still marginal. The current malaria situation is critical, development of alternative control strategies is slow, and existing methods are rapidly losing their efficacy. The above has recently called for worldwide integrated efforts to prevent further deterioration of the malaria situation (27, 131, 181). One such effort is the exploitation of what is known of the behavior and general ecology of malaria mosquitoes to reduce contact with human hosts, similar to the development of control strategies for tsetse flies (Glossina spp.) based on simple odor-baited traps and targets (182, 191). Novel methods, based on the interruption of odor-mediated behaviors such as sugar feeding and oviposition, are yet to be developed, as some of their most basic principles are still unknown (118). Because most of the world’s malaria cases are found in tropical Africa and such interventions are likely to be of most immediate effect there, we focus this review on the vectors Anopheles gambiae sensu lato and Anopheles funestus. Recent reviews on aspects of odor-mediated behavior of mosquitoes are, where relevant, taken as a starting point for the current review (11, 17, 28, 65). Whenever applicable to the target group, examples of odor-mediated behavior of other Culicidae are discussed.

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MALARIA VECTORS IN AFRICA Species and Distribution Of the several malaria vectors present in tropical Africa, only three are considered to be of major importance (77, 78, 94). These are Anopheles gambiae sensu stricto (henceforth A. gambiae), Anopheles arabiensis, and A. funestus. In vast areas of Africa, all three vectors may contribute significantly to malaria transmission, often in seasonal patterns (143, 169), which underlines the importance of developing tools effective against all vector species. Vectors of local importance include Anopheles bwambae, Anopheles melas, Anopheles merus, Anopheles moucheti, and Anopheles nili (77). Several of these belong to the A. gambiae complex, a group of at least six closely related and morphologically identical mosquitoes (190). Furthermore, in West Africa, A. gambiae appears to consist of five different chromosomal forms, some of which have been classified as incipient species (41, 64). A. gambiae and A. arabiensis have a panmictic distribution across tropical Africa, and even into the Arabian peninsula (A. arabiensis), whereas the other species have a more restricted distribution (77). A. funestus has an equally wide distribution as A. gambiae, although it is found further south into S. Africa than A. gambiae (38, 78). Like A. gambiae, it too consists of a species complex (85), but little is known about the biology of the group because of the difficulty of establishing a colony of this species.

Behavioral and Ecological Factors Affecting Malaria Transmission The ancestral species of the A. gambiae complex, Anopheles quadriannulatus, feeds mostly on animals and is not considered a vector (71, 77). The other species of the complex are all vectors, of which A. gambiae is the most efficient because of its highly anthropophilic character (66), accompanied by a preference for feeding indoors (endophagy) and resting indoors (endophily) and high susceptibility to infection with Plasmodium parasites. The remaining members of the A. gambiae complex are not host specific. A. arabiensis, notably, is known to vary from being anthropophilic to largely zoophilic depending on the geographic location (22, 35, 81, 158, 190). Furthermore, it has been reported that different karyotypes of this species differ in their host-seeking behavior, i.e. indoor versus outdoor biting (40, 43, 142). A. funestus is also anthropophilic, endophagic, and endophilic. It is reportedly less susceptible to infection with Plasmodium spp. than A. gambiae, but because of the high densities in which it may occur, it can be a very important vector locally (34). The combination of anthropophily and endophily puts both A. gambiae and A. funestus in a special place among malaria vectors. Coupled with a relatively high survival rate, these

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behaviors ensure that across Africa, both species are responsible for most of the malaria transmission.

OVERVIEW OF MOSQUITO BEHAVIOR For their survival and reproductive success, mosquitoes depend on a series of characteristic behaviors such as mating, foraging, and oviposition, which are governed by internal and external cues. Whereas the type of response to these cues is mostly genetically determined, there is a certain plasticity in these that is governed by physiological conditions and external stimuli. For instance, the nutritional state of the insect may determine whether the foraging response to host stimuli occurs selectively to one host species only, a specialistic behavior, or to a larger group of potential hosts, a more indiscriminate behavior. Similarly, the resting site selected following the blood meal may be highly specific or just anywhere, provided certain environmental conditions are met. The mosquito’s response to behavioral cues depends on its physiological state. This is determined by age, size, and physiological status with regard to nutrition, digestion, and gonotrophic stage (111). Once the threshold value for responding has been reached, the insect will usually react with a predetermined series of steps (176). External cues will activate the mosquito to engage in a certain behavior, for instance sugar feeding, and this will usually be followed by a flight that brings the insect near the vicinity of the source of a specific cue. During flight the mosquito will continue to respond to external stimuli for orientation and anemotaxis. Host-seeking diurnal mosquitoes respond to visual cues such as contours against background (3), but they do not seem to respond to colors (145, 188). Nocturnal mosquitoes respond to vertical targets and ground patterns during upwind odor-mediated flight (12) and are often more active during full moon than at other times of the lunar phase, suggesting that they can better orient under brighter light conditions (161, 167, 170). Gibson (70) demonstrated that A. gambiae responds to alternating black and white stripes at a light intensity of 10−3 W m−2 in red light. Visual cues thus aid the mosquito during upwind flight even at night during low-light conditions. Physical cues such as heat and moisture play a crucial role in orientation and induction of a landing response in the vicinity of a vertebrate host (61, 104, 124, 168, 193). There is, however, no consensus regarding over what distances these cues influence mosquito behavior. Olfactory cues are undoubtedly the most important group of external stimuli affecting mosquito behavior (Figure 1). Receptors for semiochemicals are located on the antennae and maxillary palpi (137). Male mosquitoes respond mostly to plant odors (65), although in some species responses to vertebrate odors are known (98, 139). The latter may have evolved in connection with

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HOST SEEKING sex age body size diet health

age nutrition

Aggregation pheromones Host volatiles

? Oviposition pheromones Breeding site volatiles

Plant volatiles genetic make up age size mating condition gonotrophic status circadian rhythm flowering status extra-floral nectaries plant species

OVIPOSITION

REPRODUCTIVE BEHAVIOR

SUGAR FEEDING

FEEDING BEHAVIOR

Figure 1 Key behaviors of female mosquitoes and the role of semiochemicals therein.

mating behavior in the vicinity of the host (see below). In female mosquitoes, sugar feeding, host seeking, and oviposition are known to be mediated by olfactory cues. Salient features of these behaviors with respect to Afrotropical malaria mosquitoes are discussed below.

MATING BEHAVIOR Reproductive success of mosquitoes requires behavioral responses directed toward the location and recognition of conspecifics. For anophelines, predominantly monandrous mating (26, 83, 186) normally takes place within the first 3–5 days of adult life (184). A substantial proportion of Anopheles females takes a blood meal prior to mating (2, 25, 73, 74), which indicates that both host-seeking and mating behavior occur opportunistically during this period (151). The behavioral steps undertaken during the premating period are influenced by physiological status and age (101), circadian activity rhythms, and environmental conditions (102). Plasticity in these behavioral responses coupled to other isolating mechanisms (seasonal isolation, habitat differences) are

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thought to serve as precopulatory isolation barriers, which minimize interspecific hybridization (resulting in sterile male progeny) between siblings of the A. gambiae complex (42, 94, 130, 189). Restricted gene flow between sympatrically occurring chromosomal forms of A. gambiae in West Africa (64) must be based on precopulatory ethological barriers or differences in mating behavior, which affect speciation processes (41, 64). Similar systems apply to anophelines elsewhere, and an increasing number of species complexes are being identified (165, 173, 174), which contributes to increased understanding of vectorial dynamics and disease transmission.

Mate-Finding and Recognition A variety of reproductive strategies has evolved in the Culicidae, which, presumably, have effective mate-finding and recognition of conspecifics in common. Various male Aedes and Mansonia spp. are known to respond to host odors, and they intercept and mate with females at the host (98, 139, 154). It follows that close-range species recognition is necessary, as other mosquito species may also be present at the host. Indeed, the existence of species-specific contact pheromones has been described for Aedes aegypti, Aedes albopictus, and Culiseta inornata (105, 150). Whenever both sexes become spatially separated after emergence and prior to mating, they are required to actively search for each other. In this process, semiochemicals and/or distinct environmental features may serve as aggregation mechanisms. Mating in Anopheles mosquitoes is generally accepted to occur when virgin females fly close to or in a male swarm (32, 33, 59, 130). This usually takes place during twilight above specific features in the environment called swarm “markers.” Males, typically 50–100 (130), assemble above these markers and orient visually toward them to ensure coherence of the swarm. Females are thought to select similar sites and upon reaching the vicinity of the swarm are recognized by their flight tone, which is slightly lower than that of the males (37). One or several males subsequently dart toward the female and a couple then leaves the swarm in copula. In-flight mating may take up to 15 sec (33). Field studies have shown that swarms occur in A. gambiae, A. arabiensis, A. melas, and A. funestus (33, 89, 130). Although swarms may be commonly seen in some places, they may be extremely hard to detect in others (JD Charlwood, personal communication), suggesting that other mating strategies may also be employed. Marchand (130) studied swarms of sympatric populations of the former two siblings in Tanzania. He concluded that mixed swarms do occur but at very low frequencies. However, both siblings were observed to form swarms at similar sites and were active at the same time. As hybridization between both siblings occurs readily in laboratory cages, a yet unknown mechanism must prevent this under field conditions. Gomulski (82) failed to demonstrate the existence of a

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male-produced pheromone in laboratory studies, where he tested the response of virgin females towards dead males in a Y-tube olfactometer. As cuticular hydrocarbons differ between the siblings (YT Tour´e, personal communication), they may play a role in the field similar to the contact pheromones observed for Aedes spp., but considering hybridization in the laboratory, this seems unlikely. Also, since mating only occurs at dusk, it seems unlikely that females may locate a point source (the swarm) in an area without any cues leading her to that source. Even more surprising is the fact that the various chromosomal forms of A. gambiae in West Africa seem to be, at least partially, reproductively isolated (41). The mechanisms that prevent cross-mating between A. gambiae sibling species and most likely serve as the driving force behind speciation processes within the complex are yet to be discovered.

SUGAR-FEEDING BEHAVIOR Nectar produced by plants is used for metabolic processes such as meteostasis and flight (65). It is derived from flowers, extrafloral nectaries, and honeydew. Nectar is the only food source of male mosquitoes, while the females of many species take a sugar meal before engaging in blood feeding. For the host-seeking flight, sugar is presumably the energy source. During gonotrophic development, the females of many Culex and Culiseta species continue to take small sugar meals in between blood meals (5, 148). Blood-fed females of Anopheles freeborni frequently imbibe nectar during the last stage of gonotrophic development (93). However, most Aedes and Anopheles species do not imbibe nectar during the blood-fed or gravid stages and derive all their nutrients from the blood meal (10, 60, 171, 179, 194, 195). In the field, only 6.3% of 1183 indoor-resting and 14.4% of 236 host-seeking A. gambiae s.l. contained measurable amounts of fructose (10). Similar figures were obtained for Tanzanian A. gambiae s.l. (BGJ Knols & WA Foster, unpublished data). It may well be that a certain part of the population needs to supplement its energy reserves with sugars throughout life, although we do not know the physiological conditions that regulate sugar feeding. Takken et al (179) found that newly emerged small females of A. gambiae are energy deficient compared with larger females of the same cohort, as expressed by lipid and glycogen contents. Teneral small females, having had access to sugar for several days, also exhibit a significantly lower attraction to host odors than larger ones and require blood and not sugar to build up an energy reserve. These findings suggest that initial differences in energy reserves affect the response to host volatiles (179). It is assumed that mosquitoes locate their floral host by the odors emitted by the flowering plant (reviewed in 65). A. aegypti responds to the odors of oxeye daisy, Leucanthemum vulgare, as illustrated by upwind flight and landing

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on the odor source in a wind tunnel (100). When the larval diet was reduced, the resulting adult mosquitoes landed more often on the plant odor source compared with adults developed from well-nourished larvae. Healy & Jepson (92) reported responses of A. arabiensis to inflorescences and pentane extracts of entrained volatiles of Achillea millefolium. The major component of the floral odor was tentatively identified as a cyclic or bicyclic monoterpene. Culex pipiens females are attracted to thujone, a terpene and constituent of essential plant oils, in a cylinder through which odor-laden air is led (17). This species exhibits electrophysiological activity to a large group of bicyclic, monocyclic and acyclic terpenes, including the sesquiterpene farnesol, to green plant volatiles, fatty acids and a variety of plant volatiles (17). In the field, Aedes taeniorhynchus and Culex nigripalpus are attracted to the odors of a hexane honey extract (109). Whereas the role and chemical nature of plant volatiles in the sugar-feeding behavior of various mosquito species is well understood, it is less clear to what extent the malaria vectors A. gambiae s.l. and A. funestus use nectar-derived cues. The evidence to date suggests that early in adult life, most likely depending on size and nutritional reserves from the larval stage, these species may consume either vertebrate blood or nectar sugars for metabolic processes. The question whether sugars are essential for egg maturation or for other metabolic processes in these species remains to be solved.

HOST-SEEKING BEHAVIOR The principle of odor-mediated host seeking in mosquitoes was demonstrated by Rudolfs (162). Since then, it has been found that many anautogenous mosquitoes make use of host odors in search of blood. Takken (175) presented a comprehensive list of mammalian hosts, complex odors from specific body regions, and, where applicable, names of compounds to which mosquitoes show behavioral responses. Of these, carbon dioxide (henceforth abbreviated to CO2) is the best known mosquito kairomone (reviewed in 133). This compound is present in the expired breath of vertebrates and thus reliably signifies the presence of a potential host to host-seeking hematophagous arthropods. The behavioral role of other host volatiles is less well understood and subject of this review (Table 1). Almost all higher animals are attractive to mosquitoes, but hostseeking behavior is usually associated with the interaction between mosquitoes and mammals and birds. Early experiments suggested that human odors are involved in host seeking of Afrotropical malaria vectors (86): A house occupied by humans attracted significantly more A. gambiae and A. funestus than an unoccupied house, and there was a positive correlation between the number of occupants and the mosquito catch. A. melas was shown to be attracted to calf odor from a distance (79, 80). In both studies, the sampling devices were

No effect; bMore recent, see also 175; cmostly with CO2; dsynergism with CO2; ereduces effect of CO2.

a

45, 177 109 121, 123

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47, 53, 61, 67, 91, 114, 132, 177 177 18, 68, 109 103a, 107, 109, 110, 160a, 177, 178, 182a, 183, 186a, see also 106

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A. aegypti, A. arabiensis, A. funestus, A. gambiae, A. stephensi A. gambiae, A. stephensi A. aegypti, Culex pipiens A. aegypti, Aedes albopictus, Aedes atlanticus, Aedes dorsalis, Aedes dupreii, Aedes flavescens, Aedes infirmatus, Aedes procax, Aedes sollicitans, Aedes taeniorhynchus, Aedes triseriatus, Aedes trivittatus, Aedes vexans, Aedes vigilax, Anopheles atropus, Anopheles crucians, Anopheles farauti, Anopheles quadrimaculatus, A. stephensi, Coquillettidia perturbans, Culex erraticus, Culex nigripalpus, Culex opisthopus, Culex pilosus, C. pipiens, Culex quinquefasciatus, Culex salinarius, Culex sitiens, Culex tarsalis, Culex tritaeniorhynchus, Culiseta inornata, Culiseta melanura, Mansonia dyari, Mansonia titillans, Psorophora ciliata, Psorophora columbiae, Psorophora ferox, Psorophora howardi, Psorophora mathesoni, Wyeomyia mitchellii, Wyeomyia vanduzeei A. gambiae only: — A. gambiae

67, 68, 163 24, 61 180 46, 47, 115, 132 21, 52, 114, 122 47, 55 134a 52, 113

Reference

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Single compounds or synthetic mixturesb: CO2 Acetone Lactic acidc 1-Octen-3-old

Aedes aegypti A. aegypti, Anopheles gambiae A. gambiae Anopheles arabiensis, Anopheles funestus, A. gambiae Aedes bahamensis, Anopheles atroparvus, A. gambiaea A. arabiensis, A. gambiae, Anopheles quadriannulatus A. aegypti A. gambiae

Species

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Natural odors: Human skin residues Human sweat Human skin odor Human emanations Human breath Cattle odor Mouse odor Limburger cheese odor

Source

Table 1 Host volatiles to which behavioral and/or electrophysiological responses of mosquitoes have been reported

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baited with a live host, and mosquitoes may have responded to the combination of physical and chemical cues emanating from the host. Recently, it was shown that malaria mosquitoes are attracted to animal and human odors from a distance (46, 47, 132). Airborne human volatiles were collected by pumping them through tubing into a sampling device before assay. Therefore, the physical presence of the host (e.g. body heat and convection currents) had been removed and odors were the only cues to which the mosquitoes could respond. These studies suggest that the hypothetical objective of a synthetic human odor (i.e. “man in a bottle”), for trapping of host-seeking mosquitoes may become reality.

Behavioral Studies in the Laboratory Studies on the biting behavior of mosquitoes on naked, motionless volunteers have shown that this process is mostly nonrandom and may be odor mediated (54). A. gambiae showed a preference for biting the feet and ankles of an upright seated human, and for some, though not all, volunteers, this was shown to be mediated by odors from that body region (52, 57, 99). Other more generalist species showed a preference for biting the face (52, 122), which led to the hypothesis that zoophilic mosquitoes respond to exhaled breath (mainly its CO2 content) and consequently land and bite on the face. More specialist feeders, such as A. gambiae, will respond to human-specific volatiles such as odors from the foot region. This hypothesis is supported by the observation that the selection of biting sites by A. quadriannulatus, the zoophilic member of the A. gambiae complex, is affected by exhaled breath (57). Subsequently, it was observed that the odor of Limburger cheese, which to humans has an odor strongly reminiscent of human feet, was highly attractive to A. gambiae in a wind tunnel olfactometer (53, 113). Indeed, chemical analyses have shown a strong similarity in the composition of these odors (112, 117). A synthetic mixture of 12 of the more abundant aliphatic fatty acids, present in the head space of Limburger cheese as well as in human foot odors, have been implicated as attractive for A. gambiae (121). The behavioral activity of these fatty acids was complemented by strong dose-dependent electrophysiological responses (see below; 45, 123). Similar findings have been reported by Carlson et al (29), who showed that A. aegypti is attracted to a range of carboxylic acids, many of which are present in human skin emanations. Free fatty acids constitute a quarter of the skin surface lipid of humans and are the breakdown products of triglycerides to free glycerol by Corynebacterium and Malessezia (Pityrosporum) microorganisms residing in the sebaceous glands (149). The production of these acids is therefore linked to the metabolic activity of microorganisms, which varies between humans, and consequently has been suggested to cause differential attractiveness of humans to A. gambiae

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(112, 115). The level of hydrolysis of triglycerides to free fatty acids has been ascribed to the pH of the skin and its influence of the metabolic activity of the resident microflora (157). These results suggest that the human skin microflora affects mosquito-host interactions, although research in this field is still in its infancy. A. aegypti was found to be highly attracted to skin rubbings collected on glass beads or petri dishes (163, 164). Ethanol washings of human skin gave similar responses by this species (67, 68). Recently, it was found that A. aegypti, Culex quinquefasciatus, and A. gambiae are attracted to human skin emanations collected on a polyamide stocking worn on the foot of a human volunteer (LEG Mboera & W Takken, unpublished data; DL Kline, personal communication). Braks et al (24) found that A. gambiae is attracted to human sweat. Studies on the role of CO2 in the behavior of anophelines show varied results. In Anopheles stephensi, CO2 is a strong activator and attractant (177). The role of CO2 in the behavior of A. gambiae is less clear. Healy & Copland (91) found activation and upwind flight with a threshold value of 0.01% above background, similar to A. aegypti (61). However, Takken et al (177) found no activation effect of CO2, and orientation to the odor plume was seen in only 20% of the mosquitoes. These effects were significantly smaller than in A. stephensi. Knols et al (114) report attraction of A. gambiae to 4.5% CO2, but in a later study there was no response seen to 3.8% CO2 (53). In the same study, there was no effect of exhaled human breath on A. gambiae, although other mosquito species are known to respond well to it (21, 122). Other compounds that are present in human and animal emanations and to which attraction of anopheline mosquitoes has been reported include acetone, lactic acid, 1-octen-3-ol, estradiol, cadaverine, and lysine (15, 164, 177). Of these, positive responses with Afrotropical malaria vectors have been reported only with acetone and 1-octen-3-ol. Acetone is a chemical present in the breath of vertebrates, including humans. In a laboratory study, in the presence of CO2, it caused strong behavioral responses in A. gambiae and A. stephensi but at different concentrations. The former was attracted when acetone was offered in a human equivalent (120 ng per liter), while the latter only responded to a concentration of acetone equivalent to that of an animal (120 µg per liter). The fact that A. gambiae does not respond to human breath, which also contains CO2 and acetone, may be explained by the unknown behavioral role of other chemicals present in breath. The combination of CO2 and 1-octen-3-ol, released at a natural rate as found in the emanations of a cow, caused strong and positive attraction in A. stephensi but not in A. gambiae (177). Lactic acid is excreted through the skin of humans in large quantities and has been implicated as the main component responsible for the attraction of A. aegypti to human sweat. In the laboratory, lactic acid was found to be attractive

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for A. aegypti only in the presence of CO2 (1). However, recently, Geier & Boeckh (67) showed that lactic acid is responsible for 20–30% of the attraction of human skin residues, thus demonstrating the attractive action of lactic acid alone. Interestingly, there is no response of A. aegypti to skin residues when lactic acid is enzymatically removed from the skin washings. Only few other laboratory studies on the attractiveness of lactic acid to mosquitoes have been reported. Nondiapausing C. pipiens responded electrophysiologically to lactic acid (18, 20) and Schreck et al (164) suggested that the compound was attractive for Anopheles quadrimaculatus.

Sensory Physiology Studies Electroantennogram (EAG) and single sensillum studies are both used for the study of electrophysiological responses to olfactory cues in mosquitoes (reviewed in 16). Nearly all mosquitoes respond to CO2, and receptors for this compound are located on the maxillary palps (103, 138), while receptors for other semiochemicals are located on the antennae (19, 137). Grant et al (84) found that the response to CO2 is dose dependent but independent of background CO2 levels for several mosquito species. In a separate study the same result was obtained with A. gambiae (AJ Grant, personal communication). A. gambiae also gives strong EAG responses to compounds identified in human sweat (45). Compounds include aliphatic carboxylic acids, lactic acid, 1-octen-3-ol, and 4-methylphenol. The responses to carboxylic fatty acids and to 1-octen3-ol and 4-methylphenol are dose dependent (45, 123). These results suggest that A. gambiae responds physiologically to a wide range of chemicals present in human sweat, but this does not necessarily mean that these compounds affect the behavior of this mosquito. A. gambiae is attracted to human sweat (24), and currently, studies are under way to complement electrophysiological studies with behavioral assays in order to identify the compounds responsible for the behavioral responses to sweat (J Meijerink & MAH Braks, personal communication).

Behavioral Studies in the Field Considerable variation in attractiveness of human hosts to malaria mosquitoes has been reported (160, 166), and it is well known that adults are significantly more attractive to A. gambiae than children (14, 31, 146). Lindsay et al (129) found a significant difference in attractiveness between five men sleeping in artificial huts in the Gambia. Knols et al (115) showed in Tanzania that the difference in attraction between human hosts was entirely odor mediated. In a further study in Tanzania, it was found that the attraction between humans was different for various anopheline species: One person was significantly more attractive for A. funestus than any of the five others, while this person was at

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the same time the least attractive for Anopheles squamosus (120). The relative attractiveness of different men to anophelines in Burkina Faso was also found to be odor based (23). These studies show that variation in human odors is likely to be the cause of the differences in attraction found between humans. A. gambiae is attracted to the emanations of complete human bodies, as was found in West and East Africa (46–48, 115, 132). In contrast, human breath only plays a minor role in the attraction of A. gambiae (47, 116). A. quadriannulatus is repelled by human emanations, while at the same time it is highly attracted to CO2 and to cattle odor (55). In a study where the responses of A. gambiae and A. arabiensis to human and cattle emanations were compared, it was found that both responded equally strongly to human emanations, while the latter species was significantly more attracted to cattle odor than the former (47). These results suggest that the reported differences in host preference for the species within the A. gambiae complex are odor mediated. Similar findings have been reported for other mosquito species (136, 147, among others). Carbon dioxide has been widely proven to be a mosquito kairomone under field conditions (76). Indeed, most sampling tools for mosquitoes are being supplemented with CO2 as the attractant stimulus or to enhance the effect of the visual cues provided by the trap. Mosquitoes often respond to CO2 in a dose-dependent manner within the range of natural emission rates of vertebrate hosts (133). Kline et al (107, 109) reported an increase in the catch of several mosquito species between CO2 releases of 200 and 500 cc per min, and a dose-response relationship was established for several species ranging from 20 to 2000 cc per min, the amount of CO2 emitted by chicks and mature bovids, respectively (110). In Burkina Faso, A. gambiae, A. arabiensis, A. funestus, and Mansonia uniformis were attracted to CO2 released from an odor-baited entry trap (47, 72). When the CO2 doses were varied, all species gave a similar doseresponse curve. In a choice assay, A. gambiae alone preferred traps baited with CO2 and human odors more than the other species, which did not show a preference for CO2 only or CO2 plus human odor. These data suggest that human volatiles other than CO2 play an important role in the host-seeking behavior of A. gambiae and not necessarily in the other species studied. In Tanzania, however, A. gambiae and A. arabiensis showed a much reduced response to CO2, where only 9% of the catch in an odor-baited tent trap could be explained by CO2, with the remaining activity caused by human volatiles (132). In the same study, the catch index of A. funestus for CO2 was 27% of that of human emanations. A fivefold increase in the dose of CO2, from 300 to 1500 cc per min, did not affect the number of A. gambiae s.l. collected, but it did increase the catch of A. funestus significantly. In a choice assay in South Africa, it was found that A. quadriannulatus was significantly more attracted to a calf than to a human host (55). Comparing the response to human equivalents of CO2 with a human

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host, A. quadriannulatus was still attracted more to the CO2-baited traps than to the human host. In the same study, A. arabiensis was significantly more attracted to a human host than to CO2, where the CO2 concentration was adjusted to that present in human breath. However, A. arabiensis was attracted to CO2 alone from a distance. Other mosquitoes collected in this study responded to the odor baits according to their known host preference, with zoophilic species caught in calf and CO2 baited traps and C. quinquefasciatus entering human baited traps significantly more than CO2 or calf baited traps (55). Previously, Gillies (75) had shown that in a choice assay, A. gambiae was attracted more to a man and A. merus more to a calf. The combined response of members of the A. gambiae complex, summarized from the above studies, suggests that there is a strong association between the feeding preference of each species and the response to host odors (56). Clearly, A. gambiae is attracted to human volatiles, of which CO2 is not a very reliable constituent for this specialized mosquito, as it is present in the volatile emanations of all vertebrates. On the other hand, the zoophilic A. quadriannulatus is attracted more to CO2 or calf emanations than to human volatiles. Carbon dioxide is a major constituent of vertebrate emanations and therefore may be an important cue for mosquitoes that are not host specific. Therefore, opportunistic members of the A. gambiae complex respond to CO2, which to them is both a readily detectable (large quantity) and reliable (a potential blood host) cue (185). In contrast, CO2 is a detectable but not reliable cue for A. gambiae, and this species therefore should respond to other more host-specific cues. We do not know whether A. quadriannulatus is host specific, but it is likely that this mosquito feeds on a wide range of bovids and that CO2, which is emitted in large quantities by these large herbivores, is therefore an odor detectable from a distance. The results obtained with studies in West and southern Africa on A. arabiensis, which is known to have no specific host preference (22), fit in well with this theory. In both studies, A. arabiensis did not show a specific preference for human odor, although it was attracted to it in the absence of other chemical stimuli (47, 56). In addition to CO2, 1-octen-3-ol was the first reported semiochemical to which mosquitoes respond from a distance in the field (109, 178). It has been isolated from the emanations of large herbivores and humans (45, 87). The response to 1-octen-3-ol is not species specific, as many mosquito species are known to respond to it including some anophelines (106, 183). In Germany, however, Aedes vexans, Aedes rossicus, Aedes cinereus, and C. pipiens did not respond to 1-octen-3-ol (6). This may have been due to a different release method of the odors compared with those of the previous studies. From these studies it is clear that few mosquitoes respond to 1-octen-3-ol alone, but many species, including several anophelines, will respond only to the combination of 1-octen-3-ol and CO2. Kline & Lemire (108) found a significant increase in trap

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collections when CDC traps were baited with CO2 and 1-octen-3-ol and when heat was added as an additional stimulus. This suggests an interaction between heat and olfactory stimuli, as had been proposed by Laarman (124). One-octen3-ol is a common volatile in the emanations of herbivorous vertebrates, and therefore it is perhaps not surprising that it is an attractant for mosquitoes that feed predominantly on these animals. The compound has also been found in human sweat (45), but there is no information about its role on African malaria vectors in the field. Since it was not attractive to A. gambiae in the laboratory (177), we assume that it is unlikely to play a role in the host-seeking behavior of this anthropophilic mosquito. Lactic acid has been studied in the field on only a few occasions. Stryker & Young (172) could not establish an attractive effect of lactic acid in the presence of CO2 for a wide range of mosquitoes. In contrast, Kline et al (109) reported some attraction of several mosquito species to a combination of lactic acid with CO2 or with CO2 and 1-octen-3-ol. Perhaps the low volatility of lactic acid may prevent its action over a greater distance, as it was found to be a strong attractant, combined with CO2, in numerous laboratory studies (16, 175). In summary, there is strong evidence that the malaria vectors A. gambiae, A. arabiensis and A. funestus are attracted to human volatiles from a distance and that animal odors are not very attractive for A. gambiae. The role of CO2 in this behavior varies, depending on the species and its geographic origin. There is an urgent need to corroborate the recent laboratory studies, which have identified several groups of candidate odors (45, 123, 177), with field studies.

Mosquito-Host Interactions in a Multipartite Context The interaction between Anopheles malaria mosquitoes and their human hosts has, to date, only been considered in a bitrophic context (i.e. host-seeking mosquitoes utilize kairomones to detect and subsequently blood-feed on humans). Recent studies on A. gambiae have shown that human breath and CO2 play a limited role in its host-seeking behavior (53, 116, 132, 177) and that kairomones originate from the skin (24, 45, 180). Differential attractiveness of humans to A. gambiae has therefore been attributed to differing skin-odor profiles (115, 129). Attraction of the highly anthropophilic A. gambiae to a nonhuman odor source (Limburger cheese) (53, 113) provided the first evidence that not the substrate itself but rather the microflora on it is involved in the production of kairomones. The physiology of closely related Coryneform bacteria both on the cheese and human skin results in the production of similar fatty acids, recently implicated as attractive to A. gambiae (117, 123). If, therefore, intraspecific host-selection is based on the metabolic activity and/or density of the skin microflora, then this will bear a direct impact on the mosquito-host interaction (i.e. the number of bites received per person and the resulting chance

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of infection with malaria parasites). This justifies the recognition of the skin microflora as a separate entity in the interaction (112). Similar systems, whereby the interaction between insects and hosts is governed by odors produced by microorganisms, have been reported (36, 62, 88). A further interactant in the mosquito-host interaction is the Plasmodium parasite, and an increasing amount of evidence for behavioral modifications both of the mosquito and human in order to enhance transmission has become available. A field study recently showed that infectious A. gambiae take larger and more multiple blood meals than uninfected mosquitoes, which consequently favors transmission (123a). Field specimens of A. gambiae s.l. and A. funestus were found to probe more often on experimental hosts than uninfected mosquitoes did (187). Day & Edman (50, 51) have shown that gametocytemic mice are more prone to mosquito attack than are uninfected mice. Mice differ in their attractiveness to A. stephensi, depending on infection with Plasmodium gametocytes, and it was suggested that this may be mediated by parasite-related olfactory cues (H Hurd, personal communication). Clearly, such a system, whereby the parasite in its stage of being infectious to mosquitoes influences the odor-mediated interaction between its host and the vector, will have a strong selective advantage (95). It is clear from the above that both the human skin microflora and malaria parasite may influence the odor-mediated interaction between host-seeking mosquitoes and humans. Nevertheless, the concept of viewing mosquito-host interactions in a multipartite context is new (112) and research in this field has yet to start.

OVIPOSITION BEHAVIOR The selection of oviposition sites by many mosquitoes is, next to visual cues (3, 7), mediated by semiochemicals. Chemical cues can originate from natural water bodies as breakdown products of bacterial origin or from the mosquito itself as oviposition pheromone (11). Both sources of stimuli result in the aggregation of eggs in sites suitable for larval development (134). The oviposition pheromone erythro-6-acetoxy-5-hexadecanolide was first described by Laurence & Pickett (126, 127), who extracted it from the apical droplet left at the tip of the eggs by ovipositing C. quinquefasciatus. Gravid conspecifics as well as Culex tarsalis are highly attracted to the pheromone (140, 153, 155, 156). Mordue et al (144) demonstrated the presence of electrophysiological activity in C. quinquefasciatus in response to the pheromone. Other oviposition pheromones have not been described, although Osgood (152) reported a pheromonelike substance associated with the apical droplets of egg rafts of C. tarsalis. The chemical nature of this substance has not been elucidated, but available data

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suggest that it is related to erythro-6-acetoxy-5-hexadecanolide. On the other hand, many gravid culicines are attracted to chemical cues emitted by water with a high organic content such as soakage pits and hay and grass infusions. Bacteria present in the organic-rich water were shown to produce chemicals that are highly attractive to gravid mosquitoes. Positive responses to hay infusions have been found in A. aegypti, A. albopictus, and Aedes hendersoni (4, 44, 159) and C. quinquefasciatus, C. tarsalis, Culex stigmatosoma, C. pipiens, and Culex restuans (96, 97, 125, 141). Gravid Culex molestus is attracted to volatiles produced by the bacterium Pseudomonas vesicularis, which was isolated from water occupied by conspecific larvae (58). Millar et al (141) described five chemical compounds, phenol, 4-methylphenol, 4-ethylphenol, indole, and 3-methylindole (skatole), present in the volatiles of hay infusions to which C. quinquefasciatus is attracted. Significantly more egg rafts were deposited in water containing a synthetic blend of these compounds than in distilled water. The strongest oviposition response was elicited by 3-methylindole. Attraction and oviposition occurred at concentrations from 0.01 to 1 µg per liter in water. At concentrations above 10 µg per liter, 3-methylindole became repellent. An electrophysiological response to 3-methylindole, as well as to the egg raft pheromone, was present as well (13, 144). In field experiments, significantly more egg rafts of C. quinquefasciatus were deposited in traps containing the mixture than in untreated water (8). In the same study, C. quinquefasciatus, C. tarsalis, and C. stigmatosoma were all attracted to water containing 3-methylindole only at 0.12 and 0.6 mg per liter. Both A. albopictus and A. aegypti responded differently to these compounds, with A. albopictus responding to only one concentration of 3-methylindole and A. aegypti to phenol only (4). These compounds are produced by bacteria present in the hay infusions (9, 89, 90). When tested jointly with the pheromone 6-acetoxy-5-hexadecanolide, blends of the pheromone and 3-methylindole caused an increased oviposition response, which was additive rather than synergistic (140). These data suggest that the pheromone operates independently from the water-derived oviposition attractants. Similar results were obtained with a field study in Kenya (153). Recent field studies in Tanzania showed that there is a synergistic effect of the pheromone with volatiles from soakage pit water on ovipositing C. quinquefasciatus (LEG Mboera & W Takken, unpublished data). It is interesting that, to date, only one oviposition pheromone has been identified that, although it is produced by one species only (C. quinquefasciatus), acts cross-specifically in a number of congeneric Culex spp., whereas the water-derived attractants mediate oviposition behavior in many culicine species. Of the anophelines, however, only McCrae’s (135) work on A. gambiae provides a published reference that semiochemicals, in conjunction with visual stimuli, may mediate oviposition behavior in this group of mosquitoes.

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McCrae found that A. gambiae preferred a dark over a light background as an oviposition substrate and that water from a natural breeding site attracted more ovipositing females than tap or distilled water. Recent studies in western Kenya showed that more eggs of A. gambiae s.l. were laid in bowls containing clean water and mud from known breeding sites than in clean water only (N Minukawa & C Mutero, unpublished data), thus corroborating McCrae’s work. These data suggest that soil factors were present that mediate olfactory oviposition behavior in these mosquitoes. It seems timely to resolve the question whether anopheline females engage in olfactory behavior for oviposition. It is difficult to imagine how nocturnal mosquitoes would locate such sites by abiotic and visual cues only in the absence of chemical stimuli, particularly during the dry season when breeding sites become scarce.

PERSPECTIVES AND FUTURE CHALLENGES This review has focused on the current knowledge of key behaviors of African malaria vectors and identifies the gaps that need to be bridged in order to develop new mosquito control strategies. The enormous successes in the control of African trypanosomiasis that followed the development of simple odor-baited targets and traps for tsetse flies have shown convincingly that odor-mediated behavior can be exploited to our advantage, even in resource-poor rural areas of Africa. The reported findings on semiochemicals affecting host-seeking behavior of A. gambiae s.l. and A. funestus, as well as the wealth of information available on sugar feeding and oviposition mediating cues in other Culicidae, promises that ongoing research will enable the development of tools with which this behavior can be manipulated. We believe that in the near future, mosquito surveys can be conducted with odor-baited traps and that further research may lead to the development of odor-based systems with which host-seeking behavior can be interrupted. If evidence for odor-mediated behavior in mating, sugar feeding, and oviposition in African malaria vectors can be found, entirely new strategies for malaria intervention will be possible. Priorities for research on behavior and chemical ecology of malaria vectors include (a) the colonization of A. funestus and its siblings for behavioral research, (b) the chemical identification of skin odors (including those produced by microorganisms), (c) field evaluation of laboratory-identified candidate odors, (d) research on odor-baited (ovi-, mating, host-seeking) trap development, (e) studies on the factors affecting the selection of breeding sites, ( f ) research on mating behavior, in particular the possible role of olfaction in swarming and swarm location, and (g) research on sugar feeding. This research should be undertaken with the objective to develop simple, costeffective and environmentally sound sampling tools for monitoring and possibly

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control of malaria vector populations. Such tools may assist decision-making by health officials on when and where to apply their often limited resources most effectively. They may also play a crucial role in the entomological evaluation of vector control interventions such as impregnated bednets and vaccines. ACKNOWLEDGMENTS We thank Fran¸coise Kaminker for editorial comments and help in the preparation of this review. The advice on an earlier draft of the text by Derek Charlwood, Woody Foster, Ahmed Hassanali, Joop van Loon, and Jenny Mordue (Luntz) is much appreciated. Piet Kostense is gratefully acknowledged for drawing Figure 1. Visit the Annual Reviews home page at http://www.AnnualReviews.org

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