Odor Mediated Behavior

P1: APR/vks P2: APR/ary QC: KKK/anil T1: KKK
October 15, 1998 10:9 Annual Reviews AR074-06
Annu. Rev. Entomol. 1999. 44:131–57

Copyright °c 1999 by Annual Reviews. All rights reserved
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: willem.takken@medew.ento.wau.nl
Bart G. J. Knols
International Centre of Insect Physiology and Ecology, P.O. Box 30772,
Nairobi, Kenya; e-mail: bknols@icipe.org
KEY WORDS: semiochemicals, mating, sugar feeding, host seeking, oviposition
ABSTRACT
The African mosquito species Anopheles gambiae sensu lato s.l. and Anophe-
les funestus rank among the world’s most efficient vectors of human malaria.
Their unique bionomics, particularly their anthropophilic, endophagic and en-
dophilic 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 knowl-
edge 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
132 TAKKEN & KNOLS
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 to-
tal 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 treat-
ments. 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). Toler-
ance 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 mor-
tality (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 cur-
rent 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 strate-
gies 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.
BEHAVIOR OF MALARIA MOSQUITOES 133
MALARIA VECTORS IN AFRICA

Species and Distribution
Of the several malaria vectors present in tropical Africa, only three are con-
sidered 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 impor-
tance 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 morpholog-
ically 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 Ara-
bian 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 prefer-
ence 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
134 TAKKEN & KNOLS
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 deter-
mined 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 anemo-
taxis. 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, how-
ever, 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
MATING HOST SEEKING
sex
age age
nutrition body size
diet
health
Aggregation pheromones
? Host volatiles
Oviposition pheromones
Plant volatiles
Breeding site volatiles
genetic make up
age
size
mating condition
gonotrophic status
circadian rhythm
flowering status
extra-floral nectaries
plant species
OVIPOSITION SUGAR FEEDING
REPRODUCTIVE BEHAVIOR 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 to-
ward the location and recognition of conspecifics. For anophelines, predom-
inantly 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 influ-
enced by physiological status and age (101), circadian activity rhythms, and
environmental conditions (102). Plasticity in these behavioral responses cou-
pled to other isolating mechanisms (seasonal isolation, habitat differences) are
136 TAKKEN & KNOLS
thought to serve as precopulatory isolation barriers, which minimize interspe-

cific hybridization (resulting in sterile male progeny) between siblings of the
A. gambiae complex (42, 94, 130, 189). Restricted gene flow between sym-
patrically 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, pre-
sumably, have effective mate-finding and recognition of conspecifics in com-
mon. 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 sep-
arated 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
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 Touré, 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 free-
borni 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 through-
out 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 ox-
eye daisy, Leucanthemum vulgare, as illustrated by upwind flight and landing
138 TAKKEN & KNOLS
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 depend-
ing 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 compre-
hensive list of mammalian hosts, complex odors from specific body regions,
and, where applicable, names of compounds to which mosquitoes show behav-
ioral 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 host-
seeking 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 occu-
pied 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
P1: APR/vks
Table 1 Host volatiles to which behavioral and/or electrophysiological responses of mosquitoes have been reported
October 15, 1998
Source Species Reference
Natural odors:
P2: APR/ary
Human skin residues Aedes aegypti 67, 68, 163

10:9
Human sweat A. aegypti, Anopheles gambiae 24, 61

Human skin odor A. gambiae 180
Human emanations Anopheles arabiensis, Anopheles funestus, A. gambiae 46, 47, 115, 132
Human breath Aedes bahamensis, Anopheles atroparvus, A. gambiaea 21, 52, 114, 122
Cattle odor A. arabiensis, A. gambiae, Anopheles quadriannulatus 47, 55
QC: KKK/anil
Mouse odor A. aegypti 134a

Limburger cheese odor A. gambiae 52, 113
Single compounds or synthetic mixturesb:
Annual Reviews
CO2 A. aegypti, A. arabiensis, A. funestus, A. gambiae, A. stephensi 47, 53, 61, 67, 91, 114, 132, 177
T1: KKK
Acetone A. gambiae, A. stephensi 177

Lactic acidc A. aegypti, Culex pipiens 18, 68, 109
1-Octen-3-old A. aegypti, Aedes albopictus, Aedes atlanticus, Aedes dorsalis, Aedes 103a, 107, 109, 110, 160a, 177, 178,
dupreii, Aedes flavescens, Aedes infirmatus, Aedes procax, Aedes 182a, 183, 186a, see also 106
sollicitans, Aedes taeniorhynchus, Aedes triseriatus, Aedes trivittatus,
AR074-06
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: 45, 177
Butanonee — 109
Fatty acids A. gambiae 121, 123
a
No effect; bMore recent, see also 175; cmostly with CO2; dsynergism with CO2; ereduces effect of CO2.
140 TAKKEN & KNOLS
baited with a live host, and mosquitoes may have responded to the combina-
tion 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 phys-
ical 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 electrophysio-
logical 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 ac-
tivity of microorganisms, which varies between humans, and consequently has
been suggested to cause differential attractiveness of humans to A. gambiae
(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
142 TAKKEN & KNOLS
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 (re-
viewed 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. gam-
biae 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-octen-
3-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 af-
fect 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
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 sev-
eral 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 dose-
response 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 pref-
erence 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, how-
ever, 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 emana-
tions. 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
144 TAKKEN & KNOLS
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 at-
tracted 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
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-octen-
3-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 hu-
mans). 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 non-
human 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 produc-
tion 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 in-
teraction (i.e. the number of bites received per person and the resulting chance
146 TAKKEN & KNOLS
of infection with malaria parasites). This justifies the recognition of the skin mi-
croflora 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 par-
asite, 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 attrac-
tiveness 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 para-
site in its stage of being infectious to mosquitoes influences the odor-mediated
interaction between its host and the vector, will have a strong selective advan-
tage (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 ovipo-
sition 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 phero-
mones have not been described, although Osgood (152) reported a pheromone-
like 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
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 in-
fusions have been found in A. aegypti, A. albopictus, and Aedes hendersoni
(4, 44, 159) and C. quinquefasciatus, C. tarsalis, Culex stigmatosoma, C. pip-
iens, 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 dis-
tilled 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 be-
came repellent. An electrophysiological response to 3-methylindole, as well
as to the egg raft pheromone, was present as well (13, 144). In field experi-
ments, 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 syn-
ergistic (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, unpub-
lished data). It is interesting that, to date, only one oviposition pheromone has
been identified that, although it is produced by one species only (C. quinquefas-
ciatus), 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. gam-
biae provides a published reference that semiochemicals, in conjunction with
visual stimuli, may mediate oviposition behavior in this group of mosquitoes.
148 TAKKEN & KNOLS
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 ovipo-
sition 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, cost-
effective and environmentally sound sampling tools for monitoring and possibly
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 Françoise Kaminker for editorial comments and help in the prepara-
tion 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
Literature Cited
1. Acree F Jr, Turner RB, Couck HK, J. Chem. Ecol. 20:281–91

Beroza M, Smith N. 1968. L-Lactic acid: 9. Beehler JW, Millar JG, Mulla MS. 1994.
a mosquito attractant isolated from hu- Protein hydrolysates and associated bac-
mans. Science 161:1346–47 terial contaminants as oviposition attrac-
2. Adam J-P, Hamon J, Bailly-Choumara tants for the mosquito Culex quinquefas-
H. 1960. Observations sur la biolo- ciatus. Med. Vet. Entomol. 8:381–85
gie et le pouvoir vecteur d’une popu- 10. Beier JC. 1996. Frequent blood-feeding
lation d’Anopheles gambiae résistante à and restricted sugar-feeding behavior
la dieldrine en Haute-Volta. Bull. Soc. enhance the malaria vector potential of
Pathol. Exot. 53:1043–53 Anopheles gambiae s.l. and An. funestus
3. Allan SA, Day JF, Edman JD. 1987. (Diptera: Culicidae) in western Kenya.
Visual ecology of biting flies. Annu. Rev. J. Med. Entomol. 33:613–18
Entomol. 32:297–316 11. Bentley MD, Day JD. 1989. Chemi-
4. Allan SA, Kline DL. 1995. Evaluation cal ecology and behavioral aspects of
of organic infusions and synthetic com- mosquito oviposition. Annu. Rev. Ento-
pounds mediating oviposition in Aedes mol. 34:401–21
albopictus and Aedes aegypti (Diptera: 12. Bidlingmayer WL. 1994. How mosqui-
Culicidae). J. Chem. Ecol. 21:1847–60 toes see traps: role of visual responses.
5. Andersson IH, Jaenson TGT. 1987. Nec- J. Am. Mosq. Control Assoc. 10:272–79
tar feeding by mosquitoes in Sweden, 13. Blackwell A, Mordue (Luntz) AJ, Hans-
with special reference to Culex pipiens son BS, Wadhams LJ, Pickett JA. 1993.
and Cx torrentium. Med. Vet. Entomol. A behavioral and electrophysiological
1:59–64 study of oviposition cues for Culex quin-
6. Becker N, Zgomba M, Petric D, Ludwig quefasciatus. Physiol. Entomol. 18:434–
M. 1995. Comparison of carbon dioxide, 48
octenol and a host odour as mosquito at- 14. Boreham PFL, Chandler JA, Jolly J.
tractants in the upper Rhine valley, Ger- 1978. The incidence of mosquitoes feed-
many. Med. Vet. Entomol. 9:377–80 ing on mothers and babies at Kisumu,
7. Beehler J, Lohr S, DeFoliart G. 1992. Kenya. J. Trop. Med. Hyg. 81:63–67
Factors influencing oviposition in Aedes 15. Bos HJ, Laarman JJ. 1975. Guinea pig,
triseriatus (Diptera: Culicidae). Great lysine, cadaverine and estradiol as at-
Lakes Entomol. 25:259–64 tractants for the malaria mosquito Ano-
8. Beehler JW, Millar JG, Mulla MS. pheles stephensi. Entomol. Exp. Appl.
1994. Field evaluation of synthetic 18:161–72
compounds mediating oviposition in 16. Bowen MF. 1991. The sensory phy-
Culex mosquitoes (Diptera: Culicidae). siology of host-seeking behavior in
150 TAKKEN & KNOLS
mosquitoes. Annu. Rev. Entomol. 36: Godwin DR. 1973. Yellowfever mosqui-
139–58 toes: compounds related to lactic acid
17. Bowen MF. 1992. Terpene-sensitive that attract females. J. Econ. Entomol.
receptors in female Culex pipiens 66:329–31
mosquitoes: electrophysiology and be- 30. Carlson J, Olson K, Higgs S, Beaty B.
haviour. J. Insect Physiol. 38:759–64 1995. Molecular genetic manipulation
18. Bowen MF. 1992. Patterns of sugar of mosquito vectors. Annu. Rev. Ento-
feeding in diapausing and nondiapaus- mol. 40:359–88
ing Culex pipiens (Diptera: Culicidae) 31. Carnevale P, Frézil L, Bosseno MF,
females. J. Med. Entomol. 29:843–49 Le Pont F, Lancien J. 1978. Etude de
19. Bowen MF. 1995. Sensilla basico- l’agressivité d’Anopheles gambiae en
nica (grooved pegs) on the antennae of fonction de l’age et du sexe des sujets
female mosquitoes: electrophysiology humains. Bull. WHO 56:147–54
and morphology. Entomol. Exp. Appl. 32. Charlwood JD, Jones MDR. 1979. Mat-
77:233–38 ing behaviour in the mosquito, Anophe-
20. Bowen MF, Davis EE, Haggart DA. les gambiae s.l. I. Close-range and
1988. A behavioural and sensory anal- contact behaviour. Physiol. Entomol.
ysis of host-seeking behaviour in the di- 4:111–20
apausing mosquito Culex pipiens. J. In- 33. Charlwood JD, Jones MDR. 1980. Mat-
sect Physiol. 34:805–13 ing in the mosquito, Anopheles gambiae
21. Bowen MF, Haggart D, Romo J. 1995. s.l. II. Swarming behaviour. Physiol. En-
Long-distance orientation, nutritional tomol. 5:315–20
preference and electrophysiological re- 34. Charlwood JD, Smith T, Billingsley
sponsiveness in the mosquito Aedes ba- PF, Takken W, Lyimo EOK, Meuwis-
hamensis. J. Vector Ecol. 20:203–10 sen JHET. 1997. Survival and infection
22. Braack LEO, Coetzee M, Hunt RH, probabilities of anthropophagic anophe-
Biggs H, Cornel A, Gericke A. 1994. lines from an area of high prevalence
Biting pattern and host-seeking behavior of Plasmodium falciparum in humans.
of Anopheles arabiensis (Diptera: Culi- Bull. Entomol. Res. 87:445–53
cidae) in northeastern South Africa. J. 35. Charlwood JD, Smith T, Kihonda J,
Med. Entomol. 31:333–39 Heiz B, Billingsley PF, Takken W. 1995.
23. Brady J, Costantini C, Sagnon N, Gib- Density independent feeding success of
son G, Coluzzi M. 1997. The role of malaria vectors (Diptera: Culicidae) in
body odours in the relative attractive- Tanzania. Bull. Entomol. Res. 85:29–
ness of different men to malarial vectors 35
in Burkina Faso. Ann. Trop. Med. Para- 36. Chirico J, Jonsson P, Kjellberg S,
sitol. 91(Suppl. 1):S121–22 Thomas G. 1997. Summer mastitis ex-
24. Braks M, Cork A, Takken W. 1997. perimentally induced by Hydrotaea irri-
Olfactometer studies on the attraction tans exposed to bacteria. Med. Vet. En-
of Anopheles gambiae sensu stricto tomol. 11:187–92
(Diptera: Culicidae) to human sweat. 37. Clements AN. 1963. Reproductive be-
Proc. Exp. Appl. Entomol., NEV Ams- havior. In The Physiology of Mosquitoes,
terdam 8:99–104 16:292–310. Oxford, UK: Pergamon
25. Brenguez J, Coz J. 1973. Quelques 38. Coetzee M, Hunt RH, Braack LEO,
aspects fondamenteaux de la biolo- Davidson G. 1993. Distribution of
gie d’Anopheles gambiae Giles (Sp. mosquitoes belonging to the Anophe-
A) et d’Anopheles funestus Giles, en les gambiae complex, including malaria
zone de savane humide d’Afrique de vectors, south of latitude 15◦ S. S. Afr. J.
l’Ouest. Cah. ORSTOM Ser. Entomol. Sci. 89:227–31
Méd. 11:107–26 39. Collins FH, Paskewitz SM. 1995. Mal-
26. Bryan JH. 1968. Results of consecutive aria: current and future prospects for
matings of female An. gambiae species control. Annu. Rev. Entomol. 40:195–
B with fertile and sterile males. Nature 219
(London) 218:489 40. Coluzzi M. 1992. Malaria vector analy-
27. Butler D. 1997. Malaria: avoidable sis and control. Parasitol. Today 8:113–
catastrophe? Nature 386:535–41 18
28. Cardew G, ed. 1996. Olfaction in 41. Coluzzi M, Petrarca V, Di Deco
Mosquito-Host Interactions, Proc. Ciba MA. 1985. Chromosomal inversion in-
Found. Symp. 200. Chichester: Wiley. tergradation and incipient speciation in
331 pp. Anopheles gambiae. Boll. Zool. 52:45–
29. Carlson DA, Smith N, Gouck HK, 63
42. Coluzzi M, Sabatini A, Petrarca V. 1975. of biting sites by mosquitoes. See Ref.
Chromosomal investigations on species 28, pp. 89–103
A and B of the Anopheles gambiae com- 55. Dekker T, Takken W. 1998. Responses
plex in the Garki District (Kano State, of Anopheles arabiensis Patton and
Nigeria). Results of species identifica- Anopheles quadriannulatus Theobold to
tions from 1971–1974. MPD/TN75.1 carbon dioxide, a man and a calf. Med.
WHO Tech. Note 24:16–25 Vet. Entomol. 12:136–40
43. Coluzzi M, Sabatini A, Petrarca V, Di 56. Dekker T, Takken W. 1998. The role of
Deco MA. 1977. Behavioural diver- carbon dioxide in host-seeking Anophe-
gences between mosquitoes with differ- les gambiae sensu lato (Diptera, Culi-
ent inversion karyotypes in polymorphic cidae). Proc. Exp. Appl. Entomol., NEV
populations of the Anopheles gambiae Amsterdam 9:23–28
complex. Nature 266:832–33 57. Dekker T, Takken W, Knols BGJ,
44. Copeland RS, Craig GB Jr. 1992. Differ- Bouman E, Van der Laak S, et al. 1998.
ential oviposition by Aedes hendersoni Selection of biting sites on a human host
and Aedes triseriatus (Diptera: Culici- by Anopheles gambiae sensu stricto, An.
dae) in response to chemical cues as- arabiensis and An. quadriannulatus. En-
sociated with treehole water. J. Med. tomol. Exp. Appl. 87:295–300
Entomol. 29:33–36 58. Dhileepan K. 1997. Physical factors and
45. Cork A, Park KC. 1996. Identifica- chemical cues in the oviposition be-
tion of electrophysiologically-active havior of arboviral vectors Culex an-
compounds for the malaria mosquito, nulirostris and Culex molestus (Diptera:
Anopheles gambiae, in human sweat ex- Culicidae). Environ. Entomol. 26:318–
tracts. Med. Vet. Entomol. 10:269–76 26
46. Costantini C, Gibson G, Brady J, 59. Downes JA. 1969. The swarming and
Merzagora L, Coluzzi M. 1993. A new mating flight of Diptera. Annu. Rev. En-
odour-baited trap to collect host-seeking tomol. 14:271–98
mosquitoes. Parassitologia 35:5–9 60. Edman JD, Strickman D, Kittayapong
47. Costantini C, Gibson G, Sagnon N, Della P, Scott TW. 1992. Female Aedes ae-
Torre A, Brady J, Coluzzi M. 1996. gypti (Diptera: Culicidae) in Thailand
Mosquito responses to carbon dioxide in rarely feed on sugar. J. Med. Entomol.
a West African Sudan savanna village. 29:1035–38
Med. Vet. Entomol. 10:220–27 61. Eiras AE, Jepson PC. 1994. Responses
48. Costantini C, Sagnon N, Della Torre A, of female Aedes aegypti (Diptera: Culi-
Diallo M, Brady J, et al. 1998. Odor- cidae) to host odours and convection
mediated host preferences of West currents using an olfactometer bioassay.
African mosquitoes, with particular ref- Bull. Entomol. Res. 84:207–11
erence to malaria vectors. Am. J. Trop. 62. Eisemann CH, Rice MJ. 1987. The ori-
Med. Hyg. 58:56–63 gin of sheep blowfly, Lucilia cuprina
49. Curtis CF, Hill N, Kasim SH. 1993. Are (Wiedemann) (Diptera: Calliphoridae),
there effective resistance management attractants in media infested with larvae.
strategies for vectors of human disease? Bull. Entomol. Res. 77:287–94
Biol. J. Linn. Soc. 48:3–18 63. Engers HD, Godal T. 1998. Malaria vac-
50. Day JF, Edman JD. 1983. Malaria ren- cine development: current status. Para-
ders mice susceptible to mosquito feed- sitol. Today 14:56–64
ing when gametocytes are most infec- 64. Favia G, Della Torre A, Bagayoko M,
tive. J. Parasitol. 69:163–70 Lanfrancotti A, Sagnon NF, et al. 1997.
51. Day JF, Edman JD. 1984. The impor- Molecular identification of sympatric
tance of disease induced changes in chromosomal forms of Anopheles gam-
mammalian body temperature to mos- biae and further evidence of their re-
quito blood feeding. Comp. Biochem. productive isolation. Insect Mol. Biol.
Physiol. 77A:447–52 6:377–83
52. De Jong R, Knols BGJ. 1995. Selection 65. Foster WA. 1995. Mosquito sugar feed-
of biting sites on man by two malaria ing and reproductive energetics. Annu.
mosquito species. Experientia 51:80– Rev. Entomol. 40:443–74
84 66. Garrett-Jones C, Boreham PFL, Pant
53. De Jong R, Knols BGJ. 1995. Olfac- CP. 1980. Feeding habits of anophelines
tory responses of host-seeking Anophe- (Diptera: Culicidae) in 1971–78, with
les gambiae s.s. Giles (Diptera: Culici- reference to the human blood index: a
dae). Acta Trop. 59:333–35 review. Bull. Entomol. Res. 70:165–85
54. De Jong R, Knols BGJ. 1996. Selection 67. Geier M, Boeckh J. 1999. A new y-tube
152 TAKKEN & KNOLS
olfactometer for mosquitoes to measure Hawley WA, Vulule JM, et al. 1996.
the attractiveness of host odours. Ento- Some observations on the biting behav-
mol. Exp. Appl. In press ior of Anopheles gambiae s.s., Anophe-
68. Geier M, Sass H, Boeckh J. 1996. A les arabiensis, and Anopheles funestus
search for components in human body and their implications for malaria con-
odour that attract females of Aedes ae- trol. Exp. Parasitol. 82:306–15
gypti. See Ref. 28, pp. 132–48 82. Gomulski L. 1988. Aspects of mosquito
69. Georghiou GP. 1990. The effect of agro- mating behaviour. PhD thesis. Univ.
chemicals on vector populations. In Pes- London. 259 pp.
ticide Resistance in Arthropods, ed. RT 83. Gomulski L. 1990. Polyandry in nulli-
Roush, BE Tabashnik, pp. 183–202. parous Anopheles gambiae mosquitoes
New York: Chapman & Hall (Diptera: Culicidae). Bull. Entomol. Res.
70. Gibson G. 1995. A behavioural test of 80:393–96
the sensitivity of a nocturnal mosquito, 84. Grant AJ, Wigton BE, Aghajanian JG,
Anopheles gambiae, to dim white, red O’Connell RJ. 1995. Electrophysiolog-
and infra-red light. Physiol. Entomol. ical responses of receptor neurons in
20:224–28 mosquito maxillary palp sensilla to car-
71. Gibson G. 1996. Genetics, ecology and bon dioxide. J. Comp. Physiol. A 177:
behaviour of anophelines. See Ref. 28, 389–96
pp. 22–45 85. Green CA. 1982. Cladistic analysis of
72. Gibson G, Costantini C, Sagnon, F, mosquito chromosome data [Anopheles
Della Torre A, Coluzzi M. 1997. The re- (Cellia) Myzomyia]. J. Hered. 73:3–11
sponses of Anopheles gambiae and other 86. Haddow AJ. 1942. The mosquito fauna
mosquitoes in Burkina Faso to CO2— and climate of native huts at Kisumu,
The start of a search for synthetic hu- Kenya. Bull. Entomol. Res. 33:91–142
man odour. Ann. Trop. Med. Parasitol. 87. Hall DR, Beevor PS, Cork A, Nesbitt
91(Suppl. 1):S123–24 BF, Vale GA. 1984. 1-octen-3-ol, a po-
73. Gillies MT. 1954. The recognition tent olfactory stimulant and attractant for
of age-groups within populations of tsetse isolated from cattle odours. Insect
Anopheles gambiae by the pre-gravid Sci. Appl. 5:335–39
rate and the sporozoite rate. Ann. Trop. 88. Hammack L. 1990. Protein feeding
Med. Hyg. 48:58–74 and oviposition effects on attraction
74. Gillies MT. 1955. The pre-gravid phase of screwworm flies (Diptera: Calliphori-
of ovarian development in Anopheles fu- dae) to host fluids. Ann. Entomol. Soc.
nestus. Ann. Trop. Med. Hyg. 49:320–25 Am. 83:97–102
75. Gillies MT. 1967. Experiments on host 89. Hasselschwert D, Rockett CL. 1988.
selection in the Anopheles gambiae Bacteria as ovipositional attractants
complex. Ann. Trop. Med. Hyg. Parasit. for Aedes aegypti (Dipera: Culicidae).
61:68–75 Great Lakes Entomol. 21:163–68
76. Gillies MT. 1980. The role of carbon 90. Hazard EI, Mayer MS, Savage KE. 1967.
dioxide in host-finding by mosquitoes Attraction and oviposition stimulation
(Diptera: Culicidae): a review. Bull. En- of gravid female mosquitoes by bacte-
tomol. Res. 70:525–32 ria isolated from hay infusions. Mosq.
77. Gillies MT, Coetzee M. 1987. A Supple- News 27:133–36
ment to the Anophelinae of Africa South 91. Healy TP, Copland MJW. 1995. Activa-
of the Sahara. Johannesburg: S. Afr. tion of Anopheles gambiae mosquitoes
Inst. Med. Res. 143 pp. by carbon dioxide and human breath.
78. Gillies MT, De Meillon B. 1968. The Med. Vet. Entomol. 9:331–36
Anophelinae of Africa South of the Sa- 92. Healy TP, Jepson PC. 1988. The location
hara. Johannesburg: S. Afr. Inst. Med. of floral nectar sources by mosquitoes:
Res. 343 pp. the long-range responses of Anopheles
79. Gillies MT, Wilkes TJ. 1968. A com- arabiensis Patton (Diptera: Culicidae)
parison of the range of attraction of ani- to Achillea millefolium flowers and iso-
mal baits and of carbon dioxide for some lated floral odour. Bull. Entomol. Res.
West African mosquitoes. Bull. Ento- 78:651–57
mol. Res. 59:441–56 93. Holliday-Hanson ML, Yuval B, Washino
80. Gillies MT, Wilkes TJ. 1970. The range RK. 1997. Energetics and sugar-feeding
of attraction of single baits for some of field-collected anopheline females. J.
West African mosquitoes. Bull. Ento- Vector Ecol. 22:83–89
mol. Res. 60:225–35 94. Hunt RH, Coetzee M. 1995. Mosquito
81. Githeko AK, Adungo NI, Karanja DM, species concepts: their effect on the
understanding of malaria transmission 1-octen-3-ol. J. Am. Mosq. Control As-

in Africa. In Speciation and the Recog- soc. 10:280–87
nition Concept, ed. DM Lambert, HG 107. Kline DL, Dame DA, Meisch MV. 1991.
Spencer, pp. 90–102. Baltimore: Johns Evaluation of 1-octen-3-ol and carbon
Hopkins Univ. Press dioxide as attractants for mosquitoes
95. Hurd H. 1990. Physiological and be- associated with irrigated rice fields in
havioural interactions between parasites Arkansas. J. Am. Mosq. Control Assoc.
and invertebrate hosts. Adv. Parasitol. 7:165–69
29:271–317 108. Kline DL, Lemire GF. 1995. Field eval-
96. Isoe J, Millar JG. 1995. Characteriza- uation of heat as an added attractant
tion of factors mediating oviposion site to traps baited with carbon dioxide and
choice by Culex tarsalis. J. Am. Mosq. octenol for Aedes taeniorhynchus. J. Am.
Control Assoc. 11:21–28 Mosq. Control Assoc. 11:454–56
97. Isoe J, Millar JG, Beehler JW. 1995. 109. Kline DL, Takken W, Wood JR, Carlson
Bioassays for Culex (Diptera: Culicidae) DA. 1990. Field studies on the poten-
mosquito oviposition attractants and tial of butanone, carbon dioxide, honey
stimulants. J. Med. Entomol. 32:475–83 extract, 1-octen-3-ol, L-lactic acid and
98. Jaenson TGT. 1985. Attraction to mam- phenols as attractants for mosquitoes.
mals of male mosquitoes with special Med. Vet. Entomol. 4:383–91
reference to Aedes diantaeus in Sweden. 110. Kline DL, Wood JR, Cornell JA. 1991.
J. Am. Mosq. Control Assoc. 1:195–98 Interactive effects of 1-octen-3-ol and
99. Jeganathan N. 1997. Selection of biting carbon dioxide on mosquito (Diptera:
sites on man by two malaria mosquito Culicidae) surveillance and control. J.
species, Anopheles gambiae and An. Med. Entomol. 28:254–58
atroparvus. MS thesis. Univ. London. 36 111. Klowden MJ. 1996. Endogenous fac-
pp. tors regulating mosquito host-seeking
100. Jepson PC, Healy TP. 1988. The location behaviour. See Ref. 28, pp. 212–25
of floral nectar sources by mosquitoes: 112. Knols BGJ. 1996. Odour-mediated host-
an advanced bioassay for volatile plant seeking behaviour of the Afro-tropical
odours and initial studies with Aedes ae- malaria vector Anopheles gambiae
gypti (L.) (Diptera: Culicidae). Bull. En- Giles. PhD thesis. Wageningen Agric.
tomol. Res. 78:641–59 Univ., The Netherlands. 213 pp.
101. Jones MDR, Gubbins SJ. 1978. Changes 113. Knols BGJ, De Jong R. 1996. Limburger
in the circadian flight activity of the cheese as an attractant for the malaria
mosquito Anopheles gambiae in relation mosquito Anopheles gambiae s.s. Para-
to insemination, feeding and oviposi- sitol. Today 12:159–61
tion. Physiol. Entomol. 3:213–20 114. Knols BGJ, De Jong R, Takken W.
102. Jones MDR, Gubbins SJ, Cubbin CM. 1994. Trapping system for testing olfac-
1974. Circadian flight activity in four tory responses of the malaria mosquito
sibling species of the Anopheles gam- Anopheles gambiae in a wind tunnel.
biae complex (Diptera: Culicidae). Bull. Med. Vet. Entomol. 8:386–88
Entomol. Res. 64:241–46 115. Knols BGJ, De Jong R, Takken W. 1995.
103. Kellogg FE. 1970. Water vapour and car- Differential attractiveness of isolated hu-
bon dioxide receptors in Aedes aegypti. mans to mosquitoes in Tanzania. Trans.
J. Insect Physiol. 16:99–108 R. Soc. Trop. Med. Hyg. 89:604–6
103a. Kemme JA, Van Essen PHA, Ritchie SA, 116. Knols BGJ, Mboera LEG, Takken W.
Kay BH. 1993. Response of mosquitoes 1998. Electric nets for studying odour-
to carbon dioxide and 1-octen-3-ol in mediated host-seeking behaviour of
southeast Queensland, Australia. J. Am. mosquitoes. Med. Vet. Entomol. 12:116–
Mosq. Control Assoc. 9:431–35 20
104. Khan AA, Maibach HI, Strauss WG. 117. Knols BGJ, Meijerink J. 1997. Odors
1968. The role of convection currents influence mosquito behavior. Science
in mosquito attraction to human skin. Med. 4:56–63
Mosq. News 28:462–64 118. Knols BGJ, Takken W. 1997. Ross cen-
105. Kliewer JW, Miura T, Husbands RC, tenary: a perspective from a different
Hurst CH. 1966. Sex pheromones and angle. Parasitol. Today 13:489
mating behavior of Culiseta inornata 119. Knols BGJ, Takken W. 1998. The wide-
(Diptera: Culicidae). Ann. Entomol. Soc. scale use of impregnated bednets for
Am. 59:530–33 malaria control in Africa: impact on
106. Kline DL. 1994. Olfactory attractants mosquitoes. Proc. Exp. Appl. Entomol.,
for mosquito surveillance and control: NEV Amsterdam 9:15–22
154 TAKKEN & KNOLS
120. Knols BGJ, Takken W, Charlwood D, De malaria. Lancet 349:SIII1–SIII2

Jong R. 1995. Species-specific attrac- 132. Mboera LEG, Knols BGJ, Takken W,
tion of Anopheles mosquitoes (Diptera: Della Torre A. 1997. The response of
Culicidae) to different humans in south- Anopheles gambiae s.l. and A. funes-
east Tanzania. Proc. Exp. Appl. Ento- tus (Diptera: Culicidae) to tents baited
mol., NEV Amsterdam 6:201–6 with human odour or carbon dioxide in
121. Knols BGJ, Takken W, Cork A, De Jong Tanzania. Bull. Entomol. Res. 87:173–
R. 1997. Odour-mediated, host-seeking 78
behaviour of Anopheles mosquitoes: a 133. Mboera LEG, Takken W. 1997. Carbon
new approach. Ann. Trop. Med. Para- dioxide chemotropism in mosquitoes
sitol. 91:S117–18 (Diptera: Culicidae) and its potential
122. Knols BGJ, Takken W, De Jong R. 1994. in vector surveillance and management
Influence of human breath on selection programmes. Rev. Med. Vet. Entomol.
of biting sites by Anopheles albimanus. 85:355–68
J. Am. Mosq. Control Assoc. 10:423–26 134. McCall PJ, Cameron MM. 1995. Ovipo-
123. Knols BGJ, Van Loon JJA, Cork A, sition pheromones in insect vectors. Par-
Robinson RD, Adam W, et al. 1997. Be- asitol. Today 11:352–55
havioural and electrophysiological re- 134a. McCall PJ, Harding G, Roberta J, Auty
sponses of the female malaria mosquito B. 1996. Attraction and trapping of
Anopheles gambiae (Diptera: Culici- Aedes aegypti (Diptera: Culicidae) with
dae) to Limburger cheese volatiles. Bull. host odors in the laboratory. J. Med. En-
Entomol. Res. 87:151–59 tomol. 33:177–99
123a. Koella JC, Sorensen FL, Anderson RA. 135. McCrae AWR. 1984. Oviposition by
1998. The malaria parasite, Plasmodium African malaria vector mosquitoes. II.
falciparum, increases the frequency of Effects of site tone, water type and con-
multiple feeding of its mosquito vector, specific immatures on target selection
Anopheles gambiae. Proc. Royal Soc. by freshwater Anopheles gambiae Giles,
London Ser. B 265:763–68 sensu lato. Ann. Trop. Med. Parasitol.
124. Laarman JJ. 1958. The host-seeking be- 78:307–18
haviour of anopheline mosquitoes. Trop. 136. McIver SB. 1968. Host preferences and
Geogr. Med. 10:293–305 discrimination by the mosquitoes Aedes
125. Lampman RL, Novak RJ. 1996. Ovipo- aegypti and Culex tarsalis (Dipera:
sition preferences of Culex pipiens and Culicidae). J. Med. Entomol. 5:422–28
Culex restuans for infusion-baited traps. 137. McIver SB. 1982. Sensilla of mos-
J. Am. Mosq. Control Assoc. 12:23–32 quitoes (Diptera: Culicidae). J. Med.
126. Laurence BR, Pickett JA. 1982. Erythro- Entomol. 19:489–535
6-Acetoxy-5-hexadecanolide, the ma- 138. McIver SB, Charlton C. 1970. Studies
jor component of a mosquito oviposion the sense organs on the palps of se-
tion attractant pheromone. J. Chem. Soc. lected culicine mosquitoes. Can. J. Zool.
Chem. Commun. 1982:59–60 48:293–95
127. Laurence BR, Pickett JA. 1985. An 139. McIver SB, Wilkes TJ, Gillies MT. 1980.
oviposition attractant pheromone in Attraction to mammals of male Man-
Culex quinquefasciatus Say (Diptera: sonia (Mansonioides) (Diptera: Culici-
Culicidae). Bull. Entomol. Res. 75:283– dae). Bull. Entomol. Res. 70:11–16
90 140. Millar JG, Chaney JD, Beehler JW,
128. Lengeler C, Cattani J, Savigny D, eds. Mulla MS. 1994. Interaction of the Culex
1996. Net Gain, a New Method for Pre- quinquefasciatus egg raft pheromone
venting Malaria Deaths. Geneva: World with a natural chemical associated with
Health Org./IDRC. xiii + 189 pp. oviposition sites. J. Am. Mosq. Control
129. Lindsay SW, Adiamah JH, Miller JE, Assoc. 10:374–79
Pleass RJ, Armstrong JRM. 1993. Vari- 141. Millar JG, Chaney JD, Mulla MS. 1992.
ation in attractiveness of human subjects Identification of oviposition attractants
to malaria mosquitoes (Diptera: Culici- for Culex quiquefasciatus from fer-
dae) in the Gambia. J. Med. Entomol. mented Bermuda grass infusions. J. Am.
30:368–73 Mosq. Control Assoc. 8:11–17
130. Marchand RP. 1984. Field observations 142. Mnzava AEP, Mutinga MJ, Staak C.
on swarming and mating in Anopheles 1994. Host blood meals and chromoso-
gambiae mosquitoes in Tanzania. Neth. mal inversion polymorphism in Anophe-
J. Zool. 34:367–87 les arabiensis in the Baringo district
131. Marsh K, Snow RW. 1997. 30 years of of Kenya. J. Am. Mosq. Control Assoc.
science and technology: the example of 10:507–10
143. Molineaux L, Gramiccia G. 1980. The elicited by a synthetic attractant. Phy-

Garki Project, Research on the Epidemi- siol. Entomol. 16:77–85
ology and Control of Malaria in the Su- 156. Pile MM, Simmonds MSJ, Blaney WM.
dan Savanna of West Africa. Geneva: 1993. Odour-mediated upwind flight
World Health Org. 311 pp. of Culex quinquefasciatus mosquitoes
144. Mordue (Luntz) AJ, Blackwell A, Hans- elicited by a synthetic attractant: a reap-
son BS, Wadhams LJ, Pickett JA. 1992. praisal. Physiol. Entomol. 18:219–21
Behavioural and electrophysiological 157. Puhvel SM, Reisner RM, Sakamoto M.
evaluation of oviposition attractants for 1975. Analysis of lipid composition of
Culex quinquefasciatus Say (Dipera: isolated human sebaceous gland ho-
Culicidae). Experientia 48:1109–11 mogenates after incubation with cuta-
145. Muir LE, Kay BH,Thorne MJ. 1992. neous bacteria. Thin layer chromatogra-
Aedes aegypti (Diptera: Culicidae) visi- phy. J. Invest. Dermatol. 64:406–11
on: response to stimuli from the optical 158. Randrianasolo BOR, Coluzzi M. 1987.
environment. J. Med. Entomol. 29:445– Genetical investigations on zoophilic
50 and exophilic Anopheles arabiensis
146. Muirhead-Thomson RC. 1951. The dis- from Antananarivo area (Madagascar).
tribution of anopheline mosquito bites Parassitologia 29:93–97
among different age groups. A new fac- 159. Reiter P, Amador MA, Colon N. 1991.
tor in malaria epidemiology. Br. Med. J. Enhancement of the CDC ovitrap with
1951:1114–17 hay infusions for daily monitoring of
147. Nanda N, Joshi H, Subbarao SK, Ya- Aedes aegypti populations. J. Am. Mosq.
dav RS, Shukla RP, et al. 1996. Anophe- Control Assoc. 7:52–55
les fluviatilis complex: host feeding pat- 160. Ribbands CR. 1950. Studies on the at-
terns of species S, T, and U. J. Am. Mosq. tractiveness of human populations to
Control Assoc. 12:147–49 anophelines. Bull. Entomol. Res. 40:
148. Nasci RS, Edman JD. 1984. Culiseta 227–38
melanura (Diptera: Culicidae): popula- 160a. Ritchie SA, Kline DL. 1995. Compari-
tion structure and nectar feeding in son of CDC and EVS light traps baited
a freshwater swamp and surrounding with carbon dioxide and octenol for trap-
areas in southeastern Massachusetts, ping mosquitoes in Brisbane, Queens-
USA. J. Med. Entomol. 21:567–72 land (Diptera: Culicidae). J. Aust. Ento-
149. Nicolaides N. 1974. Skin lipids: their mol. Soc. 34:215–18
biochemical uniqueness. Science 186: 161. Rubio-Palis Y. 1992. Influence of moon-
19–26 light on light trap catches of the
150. Nijhout HF, Craig GB Jr. 1971. Re- malaria vector Anopheles nuneztovari in
productive isolation in Stegomyia mos- Venezuela. J. Am. Mosq. Control Assoc.
quitoes. III. Evidence for a sexual 8:178–80
pheromone. Entomol. Exp. Appl. 14: 162. Rudolfs W. 1922. Chemotropism in
399–412 mosquitoes. Bull. NJ Agric. Exp. Stn.
151. Onyabe DY, Roitberg BD, Friend WG. 367:4–23
1997. Feeding and mating strategies in 163. Schreck CE, Kline DL, Carlson DA.
Anopheles (Diptera: Culicidae): theo- 1990. Mosquito attraction to substances
retical modeling approach. J. Med. En- from the skin of different humans. J. Am.
tomol. 34:644–50 Mosq. Control Assoc. 6:406–10
152. Osgood CE. 1971. An oviposition phe- 164. Schreck CE, Smith N, Carlson DA, Price
romone associated with the egg rafts of GD, Haile D, Godwin DR. 1981. A ma-
Culex tarsalis. J. Econ. Entomol. 64: terial isolated from human hands that at-
1038–41 tracts female mosquitoes. J. Chem. Ecol.
153. Otieno WA, Onyango TO, Pile MM, 8:429–38
Laurence BR, Dawson GW, et al. 1988. 165. Service MW. 1988. Biosystematics of
A field trial of the synthetic oviposition Haematophagous Insects. Oxford: Ox-
pheromone with Culex quinquefasciatus ford Univ. Press. 360 pp.
(Diptera: Culicidae) in Kenya. Bull. En- 166. Shidrawi GR, Boulzaguet JR, Ashkar
tomol. Res. 78:463–78 TS, Bröger S. 1974. Night-bait collec-
154. Peyton EL. 1956. Biology of the Pacific tion: the variation between persons used
coast tree hole mosquito Aedes varipal- as collector-baits. MPD/TN/74.1 WHO
pus (Coq.). Mosq. News 16:220–24 Tech. Note 17:9–18
155. Pile MM, Simmonds MSJ, Blaney WM. 167. Singh N, Mishra AK, Curtis CF, Sharma
1991. Odour-mediated upwind flight VP. 1996. Influence of moonlight on
of Culex quinquefasciatus mosquitoes light-trap catches of the malaria vector
156 TAKKEN & KNOLS
Anopheles culicifacies (Diptera: Culici- 180. Takken W, Knols BGJ. 1990. Flight
dae) in central India. Bull. Entomol. Res. behaviour of Anopheles gambiae Giles
86:475–79 (Diptera: Culicidae) in response to host
168. Smart MR, Brown AWA. 1957. Studies stimuli: a wind tunnel study. Proc. Exp.
on the responses of the female Aedes Appl. Entomol., NEV Amsterdam 1:121–
mosquito. Part VII—the effect of skin 28
temperature, hue and moisture on the at- 181. Opinion page. 1997. Two cheers for
tractiveness of the human hand. Bull. En- the multilateral malaria initiative. Nature
tomol. Res. 47:89–101 388:211
169. Smith T, Charlwood JD, Kihonda J, 182. Vale GA. 1993. Development of baits
Mwankusye S, Billingsley PF, et al. for tsetse flies (Diptera: Glossinidae) in
1993. Absence of seasonal variation in Zimbabwe. J. Med. Entomol. 30:831–42
malaria parasitaemia in an area of in- 182a. Van Essen PHA, Kemme JA, Ritchie SA,
tense seasonal transmission. Acta Trop. Kay BH. 1994. Differential responses of
54:55–72 Aedes and Culex mosquitoes to octenol
170. Snow WF. 1987. Studies of house- or light in combination with carbon diox-
entering habits of mosquitoes in The ide in Queensland, Australia. Med. Vet.
Gambia, West Africa: experiments with Entomol. 8:63–67
prefabricated huts with varied wall aper- 183. Van den Hurk AF, Beebe NW, Ritchie,
tures. Med. Vet. Entomol. 1:9–21 SA. 1997. Responses of mosquitoes
171. Straif SC, Beier JC. 1996. Effects of of the Anopheles farauti complex to
sugar availability on the blood-feeding 1-octen-3-ol and light in combination
behavior of Anopheles gambiae (Dip- with carbon dioxide in northern Queens-
tera: Culicidae). J. Med. Entomol. 33: land, Australia. Med. Vet. Entomol. 11:
608–12 177–80
172. Stryker RG, Young WW. 1970. Effec- 184. Verhoek BA, Takken W. 1994. Age ef-
tiveness of carbon dioxide and L(+) lac- fects on the insemination rate of Anophe-
tic acid in mosquito light traps with and les gambiae s.l. in the laboratory. Ento-
without light. Mosq. News 30:388–93 mol. Exp. Appl. 72:167–72
173. Subbarao SK. 1988. The Anopheles culi- 185. Vet LEM, Dicke M. 1992. Ecology of
cifacies complex and control of malaria. infochemical use by natural enemies in
Parasitol. Today 4:72–75 a tritrophic context. Annu. Rev. Entomol.
174. Subbarao SK, Nanda N, Vasantha K, 37:141–72
Dua VK, Malhotra MS, et al. 1994. 186. Villarreal C, Fuentes-Maldonado G, Ro-
Cytogenetic evidence for three sibling driguez MH, Yuval B. 1994. Low rates of
species in Anopheles fluviatilis (Diptera: multiple fertilization in parous Anophe-
Culicidae). Ann. Entomol. Soc. Am. 87: les albimanus. J. Am. Mosq. Control As-
116–21 soc. 10:67–69
175. Takken W. 1991. The role of olfaction in 186a. Vythilingam I, Lian CG, Thim CS.
host-seeking of mosquitoes: a review. 1992. Evaluation of carbon dioxide and
Insect Sci. Appl. 12:287–95 1-octen-3-ol as mosquito attractants.
176. Takken W. 1996. Synthesis and future Southeast Asian J. Trop. Med. Public
challenges: the response of mosquitoes Health 23:328–31
to host odours. See Ref. 28, pp. 302–20 187. Wekesa JW, Copeland RS, Mwangi RW.
177. Takken W, Dekker T, Wijnholds YG. 1992. Effect of Plasmodium falciparum
1997. Odor-mediated flight behavior of on blood feeding behavior of naturally
Anopheles gambiae Giles sensu stricto infected Anopheles mosquitoes in west-
and An. stephensi Liston in response ern Kenya. Am. J. Trop. Med. Hyg. 47:
to CO2, acetone, and 1-octen-3-ol 484–88
(Diptera:Culicidae). J. Insect Behav. 188. Wen Y, Muir LE, Kay BH. 1997. Re-
10:395–407 sponse of Culex quinquefasciatus to vi-
178. Takken W, Kline DL. 1989. Carbon sual stimuli. J. Am. Mosq. Control Assoc.
dioxide and 1-octen-3-ol as mosquito at- 13:150–52
tractants. J. Am. Mosq. Control Assoc. 189. White GB. 1971. Chromosomal evi-
5:311–16 dence for natural interspecific hybridiza-
179. Takken W, Klowden MJ, Chambers GM. tion by mosquitoes of the Anopheles
1998. The effect of body size on host gambiae complex. Nature 231:184–85
seeking and blood meal utilization in 190. White GB. 1974. Anopheles gambiae
Anopheles gambiae s.s. (Diptera: Culi- complex and disease transmission in
cidae): the disadvantage of being small. Africa. Trans. R. Soc. Trop. Med. Hyg.
J. Med. Entomol. 35:In press 68:278–98
191. Willemse LPM, Takken W. 1994. Odor- feeding and host-seeking rhythms in
induced host location in tsetse flies mosquitoes (Diptera: Culicidae) under
(Diptera: Glossinidae). J. Med. Ento- laboratory conditions. J. Med. Entomol.
mol. 31:775–94 29:784–91
192. World Health Org. 1996. World malaria 195. Yee WL, Foster WA, Howe MJ, Hancock
situation in 1994. Part I. Wkly. Epi- RG. 1992. Simultaneous field compari-
demiol. Rec. 72:269–76 son of evening temporal distributitions
193. Wright RH, Kellogg FE. 1964. Host size of nectar and blood feeding by Aedes
as a factor in the attraction of malaria vexans and Aedes trivittatus (Diptera:
mosquitoes. Nature 202:321–22 Culicidae) in Ohio. J. Med. Entomol.
194. Yee WL, Foster WA. 1992. Diel sugar- 29:356–60

Odor Mediated Behavior

Загружено:

Сведения о документе

Исходное описание:

Авторское право

Доступные форматы

Поделиться этим документом

Поделиться или встроить документ

Параметры публикации

Этот документ был вам полезен?

Это неприемлемый материал?

Авторское право:

Доступные форматы

Odor Mediated Behavior

Загружено:

Авторское право:

Доступные форматы

P1: APR/vks P2: APR/ary QC: KKK/anil T1: KKK

October 15, 1998 10:9 Annual Reviews AR074-06

Annu. Rev. Entomol. 1999. 44:131–57

KEY WORDS: semiochemicals, mating, sugar feeding, host seeking, oviposition

132 TAKKEN & KNOLS

BEHAVIOR OF MALARIA MOSQUITOES 133

MALARIA VECTORS IN AFRICA

Behavioral and Ecological Factors Affecting

134 TAKKEN & KNOLS

OVERVIEW OF MOSQUITO BEHAVIOR

BEHAVIOR OF MALARIA MOSQUITOES 135

MATING HOST SEEKING

OVIPOSITION SUGAR FEEDING

REPRODUCTIVE BEHAVIOR FEEDING BEHAVIOR

136 TAKKEN & KNOLS

thought to serve as precopulatory isolation barriers, which minimize interspe-

Mate-Finding and Recognition

BEHAVIOR OF MALARIA MOSQUITOES 137

male-produced pheromone in laboratory studies, where he tested the response

138 TAKKEN & KNOLS

Source Species Reference

Human skin residues Aedes aegypti 67, 68, 163

Human sweat A. aegypti, Anopheles gambiae 24, 61

Mouse odor A. aegypti 134a

Acetone A. gambiae, A. stephensi 177

Aedes vexans, Aedes vigilax, Anopheles atropus, Anopheles crucians,

140 TAKKEN & KNOLS

Behavioral Studies in the Laboratory

BEHAVIOR OF MALARIA MOSQUITOES 141

142 TAKKEN & KNOLS

Sensory Physiology Studies

Behavioral Studies in the Field

BEHAVIOR OF MALARIA MOSQUITOES 143

144 TAKKEN & KNOLS

BEHAVIOR OF MALARIA MOSQUITOES 145

Mosquito-Host Interactions in a Multipartite Context

146 TAKKEN & KNOLS

BEHAVIOR OF MALARIA MOSQUITOES 147

suggest that it is related to erythro-6-acetoxy-5-hexadecanolide. On the other

148 TAKKEN & KNOLS

McCrae found that A. gambiae preferred a dark over a light background as

PERSPECTIVES AND FUTURE CHALLENGES

BEHAVIOR OF MALARIA MOSQUITOES 149

control of malaria vector populations. Such tools may assist decision-making

Visit the Annual Reviews home page at

1. Acree F Jr, Turner RB, Couck HK, J. Chem. Ecol. 20:281–91

150 TAKKEN & KNOLS

BEHAVIOR OF MALARIA MOSQUITOES 151

152 TAKKEN & KNOLS

BEHAVIOR OF MALARIA MOSQUITOES 153

understanding of malaria transmission 1-octen-3-ol. J. Am. Mosq. Control As-

154 TAKKEN & KNOLS

120. Knols BGJ, Takken W, Charlwood D, De malaria. Lancet 349:SIII1–SIII2

BEHAVIOR OF MALARIA MOSQUITOES 155

143. Molineaux L, Gramiccia G. 1980. The elicited by a synthetic attractant. Phy-

156 TAKKEN & KNOLS

BEHAVIOR OF MALARIA MOSQUITOES 157

Вам также может понравиться