Mosquito Behavior and Vector Control

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10.1146/annurev.ento.50.071803.130439

Annu. Rev. Entomol. 2005. 50:53–70
doi: 10.1146/annurev.ento.50.071803.130439
c 2005 by Annual Reviews. All rights reserved
Copyright

First published online as a Review in Advance on July 13, 2004

MOSQUITO BEHAVIOR AND VECTOR CONTROL
Helen Pates and Christopher Curtis

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London School of Hygiene & Tropical Medicine, London WC1E 7HT,
United Kingdom; email: [email protected]; [email protected]

Key Words endophily, biting time, oviposition site choice, mosquito dispersal,
competitive mating, monogamy
■ Abstract Effective indoor residual spraying against malaria vectors depends on
whether mosquitoes rest indoors (i.e., endophilic behavior). This varies among species
and is affected by insecticidal irritancy. Exophilic behavior has evolved in certain populations exposed to prolonged spraying programs. Optimum effectiveness of insecticidetreated nets presumably depends on vectors biting at hours when most people are in
bed. Time of biting varies among different malaria vector species, but so far there is
inconclusive evidence for these evolving so as to avoid bednets. Use of an untreated
net diverts extra biting to someone in the same room who is without a net. Understanding choice of oviposition sites and dispersal behavior is important for the design of
successful larval control programs including those using predatory mosquito larvae.
Prospects for genetic control by sterile males or genes rendering mosquitoes harmless
to humans will depend on competitive mating behavior. These methods are hampered
by the immigration of monogamous, already-mated females.

RESTING BEHAVIOR IN RELATION
TO HOUSE SPRAYING
The spraying of the walls and ceilings of houses with residual insecticides such
as DDT reduces the survival prospects of indoor resting Anopheles mosquitoes
sufficiently to greatly reduce the chance of malaria transmission (47); this was
the key method by which malaria was eradicated in the temperate zones and in
reducing malaria incidence in India from 75 million cases per year in the 1930s to
110,000 per year in the 1960s (99.8% reduction). There are now serious problems
of physiological resistance to DDT in some Indian vector species (79). In addition, behavioral resistance in vectors in some countries has arisen in response to
prolonged spraying programs. This can have an impact on a control effort and may
result from an immediate response to the irritant insecticides (DDT or pyrethroids),
or it may be a genetic trait evolved under selection from the presence of insecticides in houses. Insecticide irritancy can be demonstrated by a strong stimulation
to take off and fly, a high proportion of mosquitoes exiting from a treated house,
or both.
0066-4170/05/0107-0053$14.00

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The irritating effect of DDT was demonstrated in verandah trap huts (82), where
mosquitoes inside sprayed huts were irritated and exited huts sooner than those
in unsprayed huts. This “bite and run” behavior has been shown in populations of
Anopheles gambiae sensu stricto in the Tanga region of Tanzania (31), where high
proportions leaving the sprayed house were fully engorged and displayed a high
flight activity. Similarly, a 94% exit rate of An. gambiae and An. funestus from
pyrethroid-treated huts was observed in Burkina Faso (23). A change in the place
of egress for A. gambiae s.s. mosquitoes, from the windows to the eaves, has also
been recorded in huts sprayed with tetramethrin (81).
In Tanzania, Mnzava et al. (55) found that a higher number of fed Anopheles
arabiensis were exiting DDT-sprayed houses than lambda-cyhalothrin-sprayed
houses, from which most exiting mosquitoes were unfed. This difference was
considered to be partly due to the excitorepellent properties of DDT, although host
availability also influenced the response of An. arabiensis to the two chemicals. In
the DDT-sprayed areas, most cows were kept indoors, and mosquitoes therefore
had to go inside to take a blood meal and were then driven out by the effects of the
DDT. Fewer cows were kept indoors in the lambda-cyhalothrin-treated area, and
this insecticide had a higher impact on malaria transmission than did DDT because
it acted rapidly by either deterring mosquitoes from feeding or killing them.
Irritancy may not always be counterproductive. DDT was reintroduced in the
1980s in India, where Anopheles culicifacies is DDT resistant. Some reduction in
malaria transmission was achieved because the irritant effect of DDT lasts much
longer than the toxic effect (92). A comparison of DDT and bendiocarb in Mexico found that both insecticides had a similar impact on the incidence of malaria
(45), but the mode of action of the two insecticides on the local vector, Anopheles
pseudopunctipennis, was different (DDT is a much more irritant insecticide than
bendiocarb; 26). DDT caused a decrease in the indoor resting densities and a tendency to avoid biting humans (46), whereas bendiocarb resulted in high mortality
but no significant reduction in the number of indoor biting mosquitoes.

Naturally Endophilic Anopheles Species
The term endophily refers to the preference of a female mosquito to rest indoors
during the period between the end of feeding and the onset of the search for
an oviposition site. Residual house spraying is likely to be effective only if the
mosquito species concerned is endophilic or at least partially endophilic, because
the mosquito needs to rest on the insecticide-treated walls for a sufficient time if
it is to pick up a lethal dose. Naturally endophilic species include An. gambiae
s.s. and An. funestus in Africa, An. culicifacies in India, and An. minimus in East
and Southeast Asia. DDT house-spraying programs in the 1940s and 1950s in
Venezuela and Guyana (32) were successful in the coastal areas because houses
provided the only safe resting place for Anopheles darlingi mosquitoes. However,
eradication was impossible in forested areas because of the existence of “wild”
populations outside human settlements. In Suriname and Colombia, An. darlingi

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appears to have developed a shorter indoor resting period owing to insecticide
pressure (76).
In Greece in the 1950s, DDT spraying programs led to exophilic behavior in the
originally endophilic local vector, Anopheles sacharovi. It was considered that the
survival of this species was due to a high level of irritability and physiological resistance (24). However, it is also possible that An. sacharovi became more zoophilic
during the spraying campaign (4). Similarly, malaria transmission by Anopheles
sundaicus in southern Java was not controlled by DDT house spraying, because
of increased exophily (84). A decrease in the number of An. sundaicus resting on
sprayed walls at night was observed, yet large numbers were still recovered from
human bait.
In India, malaria control is based on indoor spraying of insecticides. A major
resurgence of malaria occurred after the slackening of the eradication program
in the 1970s (2) and increased problems of physiological resistance (79). This
was exacerbated by the development of irrigation schemes and the movement of
susceptible human populations into risk areas as well as the existence of outdoor
resting populations of the major malaria vector, An. culicifacies. DDT spraying in
Karnataka state began in 1945, and in one district in the 1970s, Anopheles fluviatilis
(naturally endophilic) was found resting largely outdoors and only entering houses
to take blood. Similarly, in the state of Tamil Nadu, outdoor resting populations
of An. culicifacies with DDT resistance were found. Malathion spraying in 1978
replaced DDT spraying, which successfully reduced the indoor biting density.
However, owing to the high gametocyte load in the community and the presence
of outdoor transmission, a low-grade transmission in the area was maintained.
In Hainan Island, China, residual house spraying, launched in 1959, eliminated
the main malaria vector, An. minimus, but recent malaria outbreaks have incriminated this vector again. Entomological surveys have shown a complete change
in the behavior of An. minimus, which is now exophagic (i.e., it enters human
dwellings to take its blood meal) exophilic and has an equal preference for humans and cattle (41a).

Endophagic-Exophilic Anopheles Species
Control of exophilic vectors by residual house spraying is usually ineffective.
However, if the vector species is endophagic, then there is still a good chance that
house spraying will be at least partially effective if a suitable chemical is used,
such as fenitrothion, which has a fumigant effect.
Important successes have been achieved by using impregnated bednets against
another endophagic but exophilic vector, Anopheles dirus, in Hainan Province,
China, where the malaria incidence was high despite DDT residual spraying until
the introduction of deltamethrin-treated bednets (17).
Predominantly endophilic mosquito populations may include varieties that exhibit exophilic tendencies. This tendency may be selected for by the use of insecticides or other human interventions such as deforestation; it was considered

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the reason for the failure of a World Health Organization (WHO) house spraying
control program in the district of Garki, Nigeria, to interrupt malaria transmission
as had been the declared aim of the project (56). It was estimated that before
spraying began in Garki, only about half the blood meals were followed by indoor
resting (57). Populations composed of some consistently endophilic individuals
and other consistently exophilic ones apparently led to nonuniform exposure of the
mosquito population to the insecticide; the exposed fraction of the population may
be so much affected that it nearly disappears. However, the unexposed fraction
of the population persisted to ensure that sufficient transmission continued, even
though major reductions in malaria mortality were noted.

Culex and Aedes Mosquitoes
Residual house spraying is now rarely used as a control method against Culex or
Aedes mosquitoes. This is partly because many vector species have outdoor resting
habits or rest indoors on unsprayed objects such as clothes or curtains. Culex
mosquitoes exhibit an innate tolerance to residual insecticide deposits, possibly
owing to the pulvilli beneath Culex tarsi (6).

MOSQUITO BEHAVIOR IN RELATION TO
INSECTICIDE-TREATED NETS
Insecticide-treated bednets or curtains have a remarkable impact on the incidence
of malaria in several Asian countries and on African child mortality (41, 63). In
1910 Ross (75) had recommended bednets as a protection against malaria because
of the late-night biting tendency of most anophelines. For most efficient anthropophilic vector species such as An. gambiae (35), An. funestus (35), and An. nili (35)
(Figure 1a) in Africa; An. dirus (74) and An. minimus (38) (Figure 1b) in Southeast Asia; and An. anthropophagus (69; Xu Bozhao, unpublished data) in China
−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−→
Figure 1 Percentage of the night’s biting by the anopheline vector species in various
parts of the world that occurred starting at the times indicated on the x axis. Data based
on human landing catches outside houses except in the case of An. anthropophagus,
in which the catches were inside, and An. albimanus, in which indoor and outdoor
catches are compared. (a) Africa (Bobo-Dioulasso, Burkina Faso) (35). (b) Southeast
Asia [An. dirus in Thailand (74); An. minimus in Assam, India (38)]. (c) China [data
on An. anthropophagus from Anhui, Hubei, Zeijiang, Guizhou, and Yunnan Provinces
(69) and on An. sinensis from Hubei and Hunan Provinces (Xu Bozhao, unpublished
data)]. (d) Indian subcontinent (An. culicifacies species A and An. stephensi in Punjab,
Pakistan; cold months: November–March; hot months: April–October) (66). (e) South
America [An. darlingi in southern Brazil (29) and Suriname (36); An. nuneztovari in
Venezuela (77)]. ( f ) Central America (An. albimanus: indoor and outdoor biting in
Guatemala, Honduras, Nicaragua, Costa Rica, and Panama) (60).

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Figure 1

(Continued)

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(Figure 1c), the biting rhythm and the times when most people go to bed and
get up (assumed to be 2200 and 0500 h in rural areas) should ensure that more
than 75% of anopheline bites would be prevented by mosquito-proof bednets. The
same applies to An. culicifacies (66) in Pakistan in hot weather, but in cold weather
almost all biting is completed before 2000 h, presumably before low temperatures
inactivate the mosquitoes (Figure 1d). In South America (Figure 1e) more than
75% of the biting of Anopheles nuneztovari (77) is between 2200 and 0500 h, but
An. darlingi populations have different biting rhythms in different areas (29, 36).
In Suriname the rhythm is similar to that of An. nuneztovari, but in southern Brazil
much of the biting occurs before 2200 h and after 0500 h.
In Central America, much of the biting by An. albimanus occurs outdoors and
before 2200 h (60) (Figure 1f ). There is a strong tendency for older, parous An.
albimanus (which are the only ones that can carry infective sporozoites) to bite
earlier than the rest of the population (60). The mean parity rate was 49% before
2200 h, 30% from then until 0500 h, and 17% thereafter. The early high parity
rate would further reduce the protection from malaria transmitted by this species
that one would expect to be achievable with bednets. Surprisingly, however, a
considerable effect of nets on malaria transmitted by An. albimanus has been
reported (71).
Tendencies for significantly higher parity or sporozoite rates among earlier
biters have been recorded in several studies on An. gambiae and Anopheles farauti
(see tabulation in Reference 53). The proportion of the night’s sporozoite positive
bites by An. gambiae s.s. and An. funestus occurring between 2200 and 0500 h
was about 88% (53).
It has been feared that the effectiveness of nets may be reduced if the biting
rhythm changes in a community where net use is widespread (40). Charlwood &
Graves (12) found a marked shift toward earlier biting by An. farauti when nets
were introduced in Papua New Guinea. They attributed this not to a genetic change
in the population but to the fact that mosquitoes returning to a netted village from
egg laying during the night would have difficulty in obtaining a blood meal before
dawn. Thus many would remain hungry during the day and would attempt to find
a meal as soon as dusk fell.
For An. gambiae s.l. two studies comparing treated and untreated villages have
reported little or no difference in biting rhythm (49, 64), but two other studies (54,
58) reported a marked shift in biting time in those houses.
The above-mentioned studies were carried out soon after net introduction, when
selection for genetic changes in behavior could hardly be expected. However, biting
times of An. funestus have recently been recorded (59), nearly three years after
introduction of treated nets into a village, which might be expected to be long
enough for genetic changes to occur. The same percentage of the night’s biting
occurred between 2300 and 0500 h in this village and in a village without nets.
Furthermore, studies conducted six years after net introduction (5) showed that the
mean biting time remained unchanged but that there were indications of a wider
range of biting times after dusk and before dawn.

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In comparison with untreated nets, pyrethroid-treated nets are much more effective in reducing malaria incidence (38, 41, 52) presumably because of one or
a combination of the following effects of pyrethroids on mosquitoes. (a) Contact
with the nets may drive mosquitoes away before they have had a chance to penetrate the nets and bite (43), thus enhancing the physical protection provided by
the net. This effect is due to the excito-repellency and rapid knockdown effect of
pyrethroids. Such diversion away from treated nets may lead to more blood feeds
taken from nonhuman hosts (12) from which the Plasmodium species that infect
humans could not be acquired. However, highly anthropophilic species refuse to be
diverted from humans, and the human blood index remains high even when almost
everyone in a village is using a treated net (49). (b) Mosquitoes attracted to the odor
of sleeping humans may be killed in sufficient numbers so that widespread use of
nets in a community leads to a decline in vector population density and survival,
which results in few mosquitoes surviving long enough for malarial sporozoites to
mature inside them. In village-scale studies in which almost everyone was provided
with a treated net, major reductions in vectorial capacity of the village mosquito
populations have been observed in Tanzania (18, 49–52), Burkina Faso (10),
D.R. Congo (39), Guinea Bissau (37), and Assam, India (38). However, in Sierra
Leone the results were equivocal (48), and in The Gambia (42, 65) and Thailand
(83) such effects have not been found. The explanation of the latter results may be
that the mosquito populations of treated and untreated control villages shared the
same breeding places, thus leading to continual mixing of the populations so that
the effects of mass mosquito killing may be obscured in the trial results (65).
A study in Tanzania in which one person in a room was provided with a treated
net showed that this markedly reduced the amount of biting by An. arabiensis (a
member of the An. gambiae complex) on another person in the same room without
a net, compared with when neither had nets (43). This is presumably because many
mosquitoes, which would have attacked the unprotected person in the absence of
nets, rested on the treated net long enough to be killed or repelled from the hut.
However, when a person with an untreated net sleeps in the same hut as someone
without a net, more biting is diverted to the latter person than would occur if
neither person had a net (43). There are indications (C.A. Maxwell, unpublished
data) that current efforts in northeast Tanzania to increase net usage by social
marketing are leading to a situation in which a considerable proportion of adults
buy nets for their own use, but seldom buy nets for their children and few of the
nets are treated with insecticide. Nets used in this way are expected to lead to an
increase in the malaria risk for vulnerable children. This contrasts with programs
of organized free provision that can ensure that all age groups are provided with
effective insecticidal nets (19).

BEHAVIOR IN RELATION TO LARVAL CONTROL
Identification of breeding sites is necessary for control measures such as source
reduction, commonly used for Aedes aegypti control. Knowledge of oviposition
behavior can help identify breeding sites and monitor populations. When using

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chemicals for control of immatures, choosing the correct larvicide and larvicide
formulation is critical. For example, oviposition traps containing a high concentration of emulsifiable chlorpyrifos were repellent to ovipositing Aedes triseriatus
(3). Because granular formulations of chlorpyrifos and temephos are not repellent,
it may be that the additives and/or solvents in the emulsifiable concentrate were
repellent, rather than the insecticidally active ingredient. Ovitraps can help monitor oviposition activity (68) and are also useful for collecting samples of adults
for the detection of arboviruses (13).

Choice of Oviposition Sites
The distribution of larvae is generally determined by the oviposition site selected
by the female. For example, mosquitoes may selectively avoid oviposition in water
containing notonectids, fish, and tadpoles (72). A release-and-recapture study with
Ae. aegypti in Puerto Rico (25) showed significantly higher rates of recapture in
houses where suitable breeding containers had been added than in houses where
containers had been removed. This is taken as indirect evidence that dispersal of
Ae. aegypti is driven by the search for oviposition sites. This has important implications because vector control efforts with this species center on source reduction,
i.e., removal or destruction of breeding sites. Increased adult dispersal caused by
females searching for a suitable breeding site may increase the spread of viruses
such as dengue (67).
An. dirus, the main malaria vector in parts of Southeast Asia, is generally
exophilic and lives in forests, where it feeds on primates. Movement of people into
forested areas creates ideal transmission conditions because they provide a ready
food supply and create many of the small, stagnant transitory pools used as breeding
sites by this mosquito (73). It is extremely difficult to find and destroy all these
breeding sites. In Bangladesh, larvae appear to exhibit a particular behavior (73)
to aid survival under harsh conditions. Immatures appeared to be adapted to and
possibly dependent on small temporary pools. Females were observed depositing
eggs at the water line, where they embryonate and can remain viable for up to
two weeks. Heavy rain results in a synchronous hatch that leads to complete
development in 5–6 days and hence waves of biting females. During dry periods,
larvae were observed leaving a draining pool before it became completely dry and
crawling as far as 53 cm, sometimes successfully finding another pool. Larvae
were also recovered alive from drained pools, up to 94 h after being stranded.
Many of the metazoan cohabitants that would have preyed on them or competed
with them for food were eliminated in the same pool as it dried up. Fourth instars
were also observed cannibalizing the first or second instars of the same species.

Larvivorous Fish and Arthropods
Much effort has been devoted to optimizing biological control by metazoan predators such as fish, Toxorhynchites, and Mesocyclops. However, larvivorous marsh
fish are often ineffective in controlling synchronous mosquito broods during periods of heavy rainfall or tidal intrusion because of the immediate hatching of large

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numbers of mosquito eggs, the dilution of predatory fish densities due to increased
water levels, and a delayed increase in fish numbers (9). Ae. taeniorhynchus normally oviposits on exposed salt marsh and mangrove soil and has been observed
avoiding ovipositing near water with a high fish concentration (72). It is possible
that in such areas prolonged wet weather can result in smaller mosquito populations, because there is a decrease in the number of sites free of fish when the water
table rises (9).
Toxorhynchites brevipalpis is a tree-hole-breeding mosquito widely distributed
in tropical Africa (89) that feeds on both surface prey (small animals sharing the
habitat or other animals on the water surface or trapped in the air-water interface)
and subsurface prey (mosquito larvae and other small animals) (44). On detection
of surface prey, T. brevipalpis assesses both the angle and the distance to its prey
and uses this information to optimize the approach path (44). The effectiveness of
this predatory behavior seems dependent on temperature, because in the laboratory
it has been found that one T. brevipalpis destroys an average of 154 Ae. aegypti
larvae when reared at 26◦ C and up to 359 larvae at 32◦ C (9). Toxorhynchites spp. exhibit “killing behavior” both in the field and in the laboratory (86). This behavior is
characterized by the killing but not consumption of prey larvae and conspecifics.
One proposed explanation of this behavior is the vulnerable pupa hypothesis,
whereby larvae are protecting their own interests before pupation by slaughtering
as many of their competitors as possible, because the onset of killing begins when
the larva reaches a critical weight in the fourth instar, which also permits pupation
(14). Killing of prey larvae also deprives earlier instars of food, slowing development and increasing the chance of cannibalism (14). Toxorhynchites spp. appear
to have a level of efficacy similar to that obtained with larvivorous fish and they
would probably be good biological control agents in thick rain forests or peridomestic habitats (89). Studies on the oviposition behavior of T. rutilus rutilus in
Louisiana, United States, indicated that this species has little value as a biocontrol
agent of Ae. aegypti and Culex quinquefasciatus in the urban environment because
the primary larval habitat of the latter two species is artificial containers, whereas
T. rutilus rutilus preferentially breeds in tree-holes (27). However, a 45% reduction
in Ae. aegypti densities in New Orleans, Louisiana, was achieved with weekly releases of Toxorhynchites ambionensis (Doleschall) (28). The degree of control
achieved did not increase by increasing the number of T. ambionensis adults released each week and little movement of T. ambionensis between each study site
was observed. The results from this study indicate that use of T. ambionensis as
a biocontrol agent against container-breeding mosquitoes in urban situations may
be feasible.

GENETIC CONTROL
The term genetic control covers all methods by which a mechanism for pest or
vector control is introduced into a wild population through mating. These include
(a) the sterile insect release method or sterile insect technique (SIT), in which

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males are sterilized by irradiation or other means and released to mate with wild
females, causing them to lay sterile eggs; and (b) introduction of genetic factors
into wild populations that render pests harmless to humans.

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Sterile Insect Technique
Much research was carried out about 30 years ago, especially in India and El Salvador, on the application of SIT to mosquitoes, but this research virtually stopped
in the mid-1970s, not because the method was a technical failure, but because of
political problems in India (91) and the intensifying civil wars in Central America.
There is now a revival of interest, especially in the use of transgenesis to improve
sex separation so that only nonbiting males are released and to ensure that their
female progeny die without the need for radiation or chemosterilization (1, 87).
Three issues of mosquito behavior are especially relevant to SIT: (a) mating
competitiveness of artificially reared, sterilized males; (b) dispersal/migration; and
(c) female monogamy/polygamy.
Doubts about whether sterilization or artificial rearing might lead to behavioral abnormalities not detectable in cages led to field
tests in which fluorescently marked males were released and the population was
then sampled to ascertain the sterile:fertile male ratio for comparison with the
sterile:fertile mating ratio, as shown by the fertility of the eggs laid by captured
females. To ensure that the females tested were not immigrants but had mated in
the presence of the sterile males, virgin females of wild origin were released into
the area, given time to mate, and then as many as possible were collected and
allowed to oviposit. This procedure was used with (a) chemosterilized Anopheles quadrimaculatus (22), (b) chemosterilized An. albimanus carrying a genetic
sex separating system (21), (c) chemosterilized or cytoplasmically incompatible
Cx. quinquefasciatus (33), and (d) chemosterilized or chromosomally translocated
and sex ratio–distorting Ae. aegypti (34, 78). All showed moderately good mating
competitiveness. Thus, adequately large releases well mixed with isolated wild
populations might have been expected to yield high levels of egg sterility. However, in practice they frequently did not do so. This has been attributed to an influx
of already-mated females from outside the sterile-male release area.
The first cage tests of the fitness of transgenic Anopheles and Aedes yielded poor
results (11, 36a) possibly because of inbreeding depression. Whether transgenic
mosquitoes with adequate competitiveness can be selected is now a key research
question.

MATING COMPETITIVENESS

Dispersal ability is a major concern for the SIT (a) to
ensure that sterile males are released near enough to all emerging wild females
so that they have a fair chance of mating with them; and (b) to assess whether
there are appreciable numbers of immigrant females that have already had fertile
matings and will lay fertile eggs and nullify the effect of the sterile releases.

DISPERSAL/MIGRATION

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Ae. aegypti was considered a poorly dispersing species and sterile males would
need to be released at intervals of about 50 m along urban streets to find all the
local females (70, 80). However, more recent studies with rubidium labeling found
labeled eggs from the same group of released females scattered over more than an
800-m radius (67). With Cx. quinquefasciatus a 3-km-wide barrier zone around
release villages was expected to be adequate to isolate them, but fluorescently
marked sterile males were frequently found 7 km from their release point and egg
rafts continued to be laid throughout the barrier zone, within which great efforts
had been made using larvicides to eliminate all emergence of adults (93). For
An. albimanus, release of competitive sterile males into a 20 km2 area protected by a
barrier zone in which breeding was prevented by methoprene treatment of potential
breeding sites had a major suppressing effect on the population compared with the
upward seasonal trend seen in an untreated area. However, even though the barrier
was 4 km wide, it seemed insufficient to ensure isolation (21). Thus, there seems to
be a tendency to consider immigration negligible until the indigenous population
is eliminated by sterile releases, after which immigrants make their presence felt.
Clarification of the true proportion of immigrants in a population is important not
only for the SIT, but also for assessing whether local efforts at larval control with
insecticides or environmental management could have a worthwhile impact on the
adult vector population or whether they are likely to be swamped by immigration.
Most laymen and some scientists believe that
successful application of SIT is limited to species in which the females are monogamous. This belief is based on an incorrect assumption that radiation or chemical
sterilization involves elimination of sperm so that a female mated to a sterile and a
fertile male would be fully fertile. However, dominant lethal mutations in Diptera
do not inactivate sperm but kill after zygote formation, so that some eggs of a
multiply-mated female are sterilized (90). Thus, female polygamy is no barrier to
the successful application of SIT. On the contrary, it would be a great advantage
because after arrival in the release area, immigrant inseminated females would
be willing to accept sterilizing matings. However, unfortunately, for mosquitoes
monogamy is the rule.
In Ae. aegypti, monogamy appears to result from the action of a peptide, given
the name matrone (15, 30), that is carried in the seminal fluid produced in the male
accessory glands and inhibits the reception of sperm from second and subsequent
matings. However, Klowden (39a) has recently shown that in An. gambiae and
An. albimanus, in contrast to Ae. aegypti, implantation of male accessory glands
into females did not prevent them from receiving sperm when they were mated.
Bryan (7, 8) studied the effects of mating females of the An. gambiae complex to
sterile aspermic hybrids that are produced by laboratory crosses between different
members of the complex. The females that had been mated to aspermic hybrids
were subsequently mated to fertile males, and these females were tested for ability
to lay fertile eggs. When the hybrid males used in these experiments had An. melas
as their female parent, these hybrids could inhibit their mates from being fertilized

FEMALE MONOGAMY/POLYGAMY

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in their subsequent matings. However, when the hybrid males had An. melas as
their male parent, the hybrids failed to inhibit fertilization in the subsequent mating.
Bryan (8) explained these contrasting results with the different hybrids as being due
to the underdeveloped male accessory glands observed in the latter type of hybrid
but not the former, and she assumed that the latter type could not produce matrone
but the former type could do so. However, in view of the above-mentioned recent
evidence for the apparent irrelevance of male accessory glands (39a) to monogamy
in Anopheles, the interpretation of the data of Bryan (7, 8) needs to be reconsidered,
especially if hybrids in the An. gambiae complex are ever to be tried again as a
means of genetic control (23a).

Introduction of Genetic Factors into Wild Populations
It is the strong tendency toward monogamy of mosquitoes that renders local efforts at genetic control futile, unless one can either (a) guarantee isolation of the
population, as may be the case with urban populations that are surrounded by rural
populations of a different species; (b) afford a huge rolling program of release,
as with the screwworm program, so that immigrant females mostly receive sterile
matings before they can reach the area in which the eradication effort is currently in
progress; or (c) replace SIT with the use of insects genetically engineered to carry
a genetic driving system tightly linked to a gene that renders the insect harmless
to humans (16). The twin aims of the latter concept are that the desirable gene will
be driven to spread from a modest initial “seeding” and that the driving action will
counteract the effect of immigration. Among the challenges facing such a scheme
are behavioral barriers to free cross-mating in the field, such as those between
the Mopti, Savannah, Bamako, and other chromosomally recognizable forms of
An. gambiae s.s. in West Africa (88). Clearly, one would have to ensure that the
released mosquitoes belong to the same form as the target population. Further considerations of behavioral-ecological issues surrounding this method are discussed
in a recent book (85).
The genetics of effective driving factors and genes for physiological nonsusceptibility to malaria, or other pathogens, are beyond the scope of this review. It must be
recognized that such genes would place strong selection on the pathogen to evolve
evasion mechanisms. This problem could be avoided by using a genetic factor
that renders a mosquito harmless by making it willing to bite only nonhuman animals (i.e., zoophily). Marked differences in the degree of zoophily/anthropophily
exist between An. gambiae and An. quadriannulatus (61, 62), which can be crossmated in the laboratory with fertile female progeny, so that crossing genes causing
zoophily into the genetic background of An. gambiae may be possible.
ACKNOWLEDGMENTS
We are grateful to colleagues who provided us with unpublished or inaccessible
information. Present address for Dr. Helen Pates is Ubwari Research Centre of
the Tanzanian National Institute for Medical Research, Box 81, Muheza, Tanga,
Tanzania.

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The Annual Review of Entomology is online at http://ento.annualreviews.org

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LITERATURE CITED
1. Alphey L, Andreasen M. 2002. Dominant lethality and insect population control. Mol. Biochem. Parasitol. 121:173–78
2. Barai D, Hyma B, Ramesh A. 1982. The
scope and limitations of insecticide spraying in rural vector control programmes in
the states of Karnataka and Tamil Nadu in
India. Ecol. Dis. 1:243–55
3. Beehler JW, Mulla MS. 1993. Effect of the
insect growth regulator methoprene on the
ovipositional behavior of Aedes aegypti
and Culex quinquefasciatus. J. Am. Mosq.
Control Assoc. 9:13–16
4. Boreham PFL, Garrett-Jones C. 1973.
Prevalence of mixed blood meals and double feeding in a malaria vector (Anopheles
sacharovi Favre) Bull. World Health Organ. 48:605–14
5. Braimah N, Maxwell CA. 2003. Assessment of the effect of long term use
of treated bednets on biting time of
mosquitoes using bednets and light traps.
Trans. R. Soc. Trop. Med. Hyg. 97:263
6. Brown AWA, Pal R. 1971. Insecticide resistance in arthropods. W.H.O. Monogr. 38
7. Bryan JH. 1968. Results of consecutive
matings of female Anopheles gambiae
species B with fertile and sterile males.
Nature 218:489
8. Bryan JH. 1972. Further studies on consecutive matings in the Anopheles gambiae complex. Nature 239:519–20
9. Carlson DB, Vigliano RR. 1985. The effects of two different water management
regimes on flooding and mosquito production in a salt marsh impoundment J. Am.
Mosq. Control Assoc. 1:203–11
10. Carnevale P, Robert V, Boudin C, Halna
JM, Pazart L, et al. 1988. Control of
malaria using mosquito nets impregnated
with pyrethroids in Burkina Faso. Bull.
Soc. Pathol. Exot. 81:832–46
11. Catteruccia F, Godfray HC, Crisanti A.
2003. Impact of genetic manipulation

12.

13.

14.

15.

16.

17.

18.

19.

20.
21.

on the fitness of Anopheles stephensi
mosquitoes. Science 299:1225–27
Charlwood JD, Graves PM. 1987. The effect of permethrin-impregnated bednets
on a population of Anopheles farauti in
coastal Papua New Guinea. Med. Vet. Entomol. 1:319–27
Clark CG, Crabbs CL, Elias BT. 1986. Absence of La Crosse virus in the presence of
Aedes triseriatus on the Delmarva Peninsula. J. Am. Mosq. Control Assoc. 2:33–37
Corbett PS, Griffiths A. 1963. Observations on the aquatic stages of two species
of Toxorhynchites in Uganda. Proc. R. Entomol. Soc. London 38:125–35
Craig GB. 1967. Mosquitoes: female
monogamy induced by male accessory
gland substance. Science 156:1499–501
Curtis CF. 1994. The case for malaria control by genetic manipulation of its vectors.
Parasitol. Today 10:371–74
Curtis CF, Lines JD, Carnevale P, Robert
V, Boudin C, et al. 1990. Impregnated nets
and curtains against malaria mosquitoes.
In Appropriate Technology in Vector Control, ed. CF Curtis, pp. 5–46. Boca Raton,
FL: CRC Press
Curtis CF, Maxwell CA, Finch RT,
Njunwa KJ. 1998. A comparison of use of
a pyrethroid either for house spraying or
for bednet treatment against malaria vectors. Trop. Med. Int. Health 3:619–31
Curtis CF, Maxwell C, Lemnge M, Kilama
WL, Steketee RW, et al. 2003. Scalingup coverage with insecticide-treated nets
against malaria in Africa: Who should
pay? Lancet Infect. Dis. 3:304–7
Deleted in proof
Dame DA, Lowe RE, Williamson DL.
1980. Assessment of released Anopheles
albimanus and Glossina morsitans. In Cytogenetics and Genetics of Vectors, (Proc.
XVI Int. Cong. Entomol., Kyoto), ed. R
Pal, JB Kitzmiller, T Kanda, pp. 231–47.

27 Oct 2004 14:10

AR

AR234-EN50-03.tex

AR234-EN50-03.sgm

LaTeX2e(2002/01/18)

MOSQUITO BEHAVIOR AND CONTROL

22.

23.

Annu. Rev. Entomol. 2005.50:53-70. Downloaded from arjournals.annualreviews.org
by INFLIBNET Master on 04/18/09. For personal use only.

23a.

24.

25.

26.

27.

28.

29.

30.

Amsterdam: Kodansha, Tokyo, and Elsevier Biomedical Press
Dame DA, Woodard DB, Ford HR, Wedhaas DE. 1964. Field behavior of sexually
sterile Anopheles quadrimaculatus males.
Mosq. News 24:6–14
Darriet F. 1991. Field trial of the efficacy of three pyrethroids in the control of
malaria vectors. Parassitologia 33:111–
19
Davidson G, Odetoyinbo JA, Colussa B,
Cox J. 1970. A field trial to assess the mating competitiveness of sterile males produced by crossing two members of the
Anopheles gambiae complex. Bull. World
Health Organ. 42:55–67
de Zulueta J. 1959. Insecticide resistance in Anopheles sacharovi. Bull. World.
Health Organ. 20:797–822
Edman JD, Scott TW, Costero A, Morrison AC, Harrington LC, Clark GG. 1998.
Aedes aegypti (Diptera: Culicidae) movement influenced by availability of oviposition sites. J. Med. Entomol. 35:578–83
Evans RG. 1993. Laboratory evaluation
of the irritancy of bendiocarb, lambdacyhalothrin and DDT to Anopheles gambiae. J. Am. Mosq. Control Assoc. 9:285–
93
Focks DA, Sackett SR, Dame DA, Bailey DL. 1983. Toxorhynchites rutilus rutilus (Diptera: Culicidae): field studies
on dispersal and oviposition in the context of the biocontrol of urban containerbreeding mosquitoes. J. Med. Entomol.
20:383–90
Focks DA, Sackett SR, Dame DA, Bailey DL. 1985. Effect of weekly releases of
Toxorhynchites amboinensis (Doleschall)
on Aedes aegypti (L.) (Diptera: Culicidae)
in New Orleans, Louisiana. J. Econ. Entomol. 78:622–26
Forattini O. 1987. Comportamento exofilo
de Anopheles darlingi Root, em regi˜ao
meridional do Brasil. Rev. Sa´ude P´ubl.
S˜ao Paulo 21:291–304
Fuchs MS, Craig GB, Despommier DD.
1969. The protein nature of the substance

31.

32.

33.

34.

35.

36.

36a.

37.

38.

P1: GCE

67

inducing female monogamy in Aedes aegypti. J. Insect Physiol. 15:701–9
Gerold JL. 1977. Evaluation of some
parameters of house-leaving behaviour
of Anopheles gambiae s.l. Acta Leiden.
45:79–90
Giglioli G. 1956. Biological variations in
Anopheles darlingi and Anopheles gambiae. Their effect on practical malaria
control in the Neotropical Region. Bull.
World. Health Org. 15:461–71
Grover KK, Curtis CF, Sharma VP, Singh
KRP, Dietz K, et al. 1976. Competitiveness of chemosterilized males and cytoplasmically incompatible-translocated
(IS31B) males of Culex pipiens fatigans
in the field. Bull. Entomol. Res. 66:469–
80
Grover KK, Suguna SG, Uppal DK, Singh
KRP, Ansari MA, et al. 1976. Field experiments on the competitiveness of males
carrying genetic control systems for Aedes
aegypti. Entomol. Exp. Appl. 20:8–18
Hamon J. 1963. Les moustiques anthropophiles de la r´egion de Bobo Dioulasso
(R´epublique de Haute-Volta). Cycles
d’agressivit´e et variations saisonni`eres.
Ann. Soc. Entomol. France 132:85–144
Hudson JE. 1984. Anopheles darlingi
Root (Diptera: Culicidae) in the Suriname
rain forest. Bull. Entomol. Res. 74:129–42
Irvin N, Hoddle MS, O’Brochta DA,
Carey B, Atkinson PW. 2004. Assessing fitness costs for transgenic Aedes aegypti expressing GFP marker and transposase genes. Proc. Natl. Acad. Sci. USA
101:891–96
Jaenson TG, Gomes MJ, Barreto dos
Santos RC, Petrarca V, Fortini D, et al.
1994. Control of endophagic Anopheles
mosquitoes and human malaria in Guinea
Bissau, West Africa, by permethrintreated bed nets. Trans. R. Soc. Trop. Med.
Hyg. 88:620–26
Jana-Kara BR, Wajihullah, Shahi B,
Dev V, Curtis CF, Sharma VP. 1995.
Deltamethrin
impregnated
bednets
against Anopheles minimus transmitted

27 Oct 2004 14:10

68

39.

39a.

Annu. Rev. Entomol. 2005.50:53-70. Downloaded from arjournals.annualreviews.org
by INFLIBNET Master on 04/18/09. For personal use only.

40.

41.

41a.

42.

43.

44.

45.

AR

PATES

AR234-EN50-03.tex




AR234-EN50-03.sgm

LaTeX2e(2002/01/18)

P1: GCE

CURTIS

malaria in Assam, India. J. Trop. Med.
Hyg. 98:73–83
Karch S, Garin B, Asidi N, Manzambi Z,
Salaun JJ, Mouchet J. 1993. Mosquito nets
impregnated against malaria in Zaire. Ann.
Soc. Belge M´ed. Trop. 73:37–53
Klowden MJ. 2001. Sexual receptivity in
Anopheles gambiae mosquitoes: absence
of control by male accessory gland substances. J. Insect Physiol. 47:661–66
Knols BGJ, Takken W. 1998. The widescale use of impregnated bednets for
malaria control in Africa: impact on
mosquitoes. Proc. Exp. Appl. Entomol. 8:
15–20
Lengeler C. 1998. Insecticide treated bednets and curtains for malaria control. In
The Cochrane Library, Issue 3. Oxford,
UK: Update Software
Li M, Liang LT, Zhang HS, Chen TY.
1983. The bionomics of Anopheles minimus in the Zhougsha area of Hainan Island. Ann. Bull. Parasit. Soc. Guangdong
Prov. pp. 180–83. Curtis CF, Zhang K.
1988. (Abstr.) Trop. Dis. Bull. 85:662–
63
Lindsay SW, Alonso P, ArmstrongSchellenberg JRM, Hemingway J, Adiamak JH, et al. 1993. A malaria control trial
using insecticide-treated bed nets and targeted chemoprophylaxis in a rural area of
The Gambia, West Africa. Trans. R. Soc.
Trop. Med. Hyg. 87(Suppl.):45–52
Lines JD, Myamba J, Curtis CF. 1987.
Experimental hut trials of permethrinimpregnated mosquito net and curtains
against malaria vectors in Tanzania. Med.
Vet. Entomol. 1:37–51
Linley J. 1995. Behavior on approach to
surface prey by larvae of Toxorhynchites
amboinensis and T. brevipalpis (Diptera:
Culicidae). J. Med. Entomol. 32:53–65
Loyola EG, Rodriguez MH, Gonzalez L,
Arredondo JI, Bown DN, Vaca MA. 1990.
Effect of indoor residual spraying of DDT
and Bendiocarb on the feeding patterns
of Anopheles pseudopunctipennis in Mexico. J. Am. Mosq. Control Assoc. 6:635–40

46. Loyola EG, Vaca MA, Bown DN, Perez E,
Rodriguez MH. 1991. Comparative use of
bendiocarb and DDT to control Anopheles
pseudopunctipennis in a malarious area of
Mexico. Med. Vet. Entomol. 5:233–42
47. MacDonald G. 1957. The Epidemiology
and Control of Malaria. London: Oxford
Univ. Press
48. Magbity E, Marbiah N, Maude G, Curtis C, Bradley D, et al. 1997. Effects
of community-wide use of lambdacyhalothrin-impregnated bednets on malaria
vectors in rural Sierra Leone. Med. Vet.
Entomol. 11:79–86
49. Magesa SM, Wilkes TJ, Mnzava AEP,
Njunwa KJ, Myamba J, et al. 1991. Trial
of pyrethroid impregnated bednets in an
area of Tanzania holoendemic for malaria.
Part 2. Effects on the malaria vector population. Acta Trop. 49:97–108
50. Maxwell CA, Chambo W, Mwaimu
M, Magogo F, Carneiro IA, et al.
2003. Variation of malaria transmission
and morbidity with altitude in Tanzania and with introduction of alphacypermethrin treated nets. Malaria J. 2:28.
http://www.malariajournal.com/
51. Maxwell CA, Msuya E, Sudi M, Njunwa
KJ, Carneiro IA, et al. 2002. Effect
of community-wide use of insecticidetreated nets for 3–4 years on malarial morbidity in Tanzania. Trop. Med. Int. Health
7:1003–8
52. Maxwell CA, Myamba J, Njunwa KJ,
Greenwood B, Curtis CF. 1999. Comparison of bednets impregnated with different
pyrethroids for their impact on mosquitoes
and on re-infection with malaria after
clearance of pre-existing infections with
chlorproguanil-dapsone. Trans. R. Soc.
Trop. Med. Hyg. 93:4–11
53. Maxwell CA, Wakibara J, Tho S, Curtis
CF. 1998. Malaria-infective biting at different hours of the night. Med. Vet. Entomol. 12:325–27
54. Mbogo CNM, Baya NM, Ofulla AVO,
Githure JI, Snow RW. 1996. The impact of permethrin-impregnated bednets

27 Oct 2004 14:10

AR

AR234-EN50-03.tex

AR234-EN50-03.sgm

LaTeX2e(2002/01/18)

MOSQUITO BEHAVIOR AND CONTROL

55.

Annu. Rev. Entomol. 2005.50:53-70. Downloaded from arjournals.annualreviews.org
by INFLIBNET Master on 04/18/09. For personal use only.

56.

57.

58.

59.

60.

61.

62.

63.

on malaria vectors of the Kenyan coast.
Med. Vet. Entomol. 10:251–59
Mnzava AE, Rwegoshora RT, Wilkes TJ,
Tanner M, Curtis CF. 1995. Anopheles
arabiensis and An. gambiae chromosomal inversion polymorphism, feeding and
resting behaviour in relation to insecticide
house-spraying in Tanzania. Med. Vet. Entomol. 9:316–24
Molineaux L, Grammiccia G. 1980. The
Garki project: Research on the Epidemiology and Control of Malaria in the Sudan
Savanna of West Africa. Geneva: World
Health Organization
Molineaux L, Shidrawi GR, Clarke JL,
Boulzaguet JR, Ashkar TR. 1979. Assessment of insecticidal impact on the
malaria mosquito’s vectorial capacity,
from data on the man-biting rate and agecomposition. Bull. World Health Organ.
57:265–74
Njau RJA, Mosha FW, Nguma JFM. 1993.
Field trials of pyrethroid impregnated bednets in northern Tanzania. 1. Effects on
malaria transmission Insect Sci. Appl. 5:
575–84
Paine T, Maxwell CA, Curtis CF. 1999.
Does prolonged use of insecticide-treated
bednets lead to a change in the biting-time
of malaria vectors? Trans. R. Soc. Trop.
Med. Hyg. 93:120
Pan American Health Organization. 1996.
Biology and ecology of Anopheles albimanus in Central America. Tech. Pap. No.
43
Pates HV, Takken W, Curtis CF. 2004.
Laboratory studies on the olfactory behaviour of Anopheles quadriannulatus.
Entomol. Exp. Appl. In press
Pates HV, Takken W, Suike K, Curtis CF.
2001. Differential behaviour of Anopheles
gambiae sensu stricto to cow and human
odours in the laboratory. Bull. Entomol.
Res. 91:289–96
Phillips-Howard PA, Nahlen BL, Kolczak
MS, Hightower AW, Ter Kuile FO, et al.
2003. Efficacy of permethrin-treated bed
nets in the prevention of mortality in

64.

65.

66.

67.

68.

69.
70.

71.

72.

P1: GCE

69

young children in an area of high perennial
malaria transmission in Western Kenya.
Am. J. Trop. Med. Hyg. 68(Suppl. 4):23–
29
Qui˜nones M, Lines J, Thomson M, Jawara
M, Greenwood B. 1998. Permethrintreated bed nets do not have a ‘masskilling effect’ on village populations of
Anopheles gambiae s. l. in The Gambia.
Trans. R. Soc. Trop. Med. Hyg. 92:373–
78
Qui˜nones M, Lines J, Thomson M, Jawara
M, Morris J, et al. 1997. Anopheles
gambiae gonotrophic cycle duration, biting and exiting behaviour unaffected by
permethrin-impregnated bednets in The
Gambia. Med. Vet. Entomol. 11:71–78
Reisen WK, Aslamkhan M. 1978. Biting rhythms of some Pakistani mosquitoes
(Diptera: Culicidae). Bull. Entomol. Res.
68:313–30
Reiter P, Amador MA, Anderson RA,
Clark GC. 1995. Short report: dispersal of Aedes aegypti in an urban area
after blood feeding as demonstrated by
rubidium-marked eggs. Am. J. Trop. Med.
Hyg. 52:177–79
Reiter P, Amador MA, Colon N. 1991. Enhancement of the CDC ovitrap with hay
infusions for daily monitoring of Aedes
aegypti populations. J. Am. Mosq. Control
Assoc. 7:52–55
Ren Min Health Publication. 1991. Research and Control of Malaria in China.
Reuben R, Rahman K, Panicker P, Das P,
Brooks G. 1975. The development of a
strategy for large-scale releases of sterile
males of Aedes aegypti. J. Commun. Dis.
7:313–26
Richards FO Jr, Klein RE, Flores RZ,
Weller S, Gatica M, et al. 1993.
Permethrin-impregnated bed nets for
malaria control in northern Guatemala:
epidemiologic impact and community acceptance. Am. J. Trop. Med. Hyg. 49:410–
18
Ritchie SA, Laidlaw-Bell C. 1994.
Do fish repel oviposition by Aedes

27 Oct 2004 14:10

70

73.

74.

Annu. Rev. Entomol. 2005.50:53-70. Downloaded from arjournals.annualreviews.org
by INFLIBNET Master on 04/18/09. For personal use only.

75.
76.

77.

78.

79.
80.

81.

82.

83.

AR

PATES

AR234-EN50-03.tex




AR234-EN50-03.sgm

LaTeX2e(2002/01/18)

P1: GCE

CURTIS

taeniorhynchus? J. Am. Mosq. Control Assoc. 10:380–84
Rosenberg R. 1982. Forest malaria in
Bangladesh. III. Breeding habits of
Anopheles dirus. Am. J. Trop. Med. Hyg.
31:192–201
Rosenberg R, Andre RG, Somchit L.
1990. Highly efficient dry season transmission of malaria in Thailand. Trans. R.
Soc. Med. Hyg. 84:22–28
Ross R. 1910. The Prevention of Malaria.
London: Murray
Rozendaal JA, Van Hoof JPM, Voorham
J, Oostburg BFJ. 1989. Behavioral responses of Anopheles darlingi in Suriname to DDT residues on house walls. J.
Am. Mosq. Control Assoc. 5:339–50
Rubio-Palis Y, Curtis CF. 1992. Biting and
resting behaviour of anophelines in western Venezuela and implications for control
of malaria transmission. Med. Vet. Entomol. 6:325–34
Seawright JA, Kaiser PE, Dame DA. 1977.
Mating competitiveness of chemosterilized hybrid males of Aedes aegypti (L.)
in field tests. Mosq. News 37:615–19
Sharma VP. 2003. DDT: the fallen angel.
Curr. Sci. 85:1532–37
Singh KRP, Brooks GD. 1975. Semiautomatic release system for distribution
of mosquitoes during genetic control operations. J. Commun. Dis. 7:288–93
Smith A, Chabeda PI. 1969. A
verandah-trap hut for studying the
house-frequenting habits of mosquitoes
and for assessing insecticides. IV. The
effect of tetramethrin on the behaviour
and mortality of Anopheles gambiae
Giles. Bull. Entomol. Res. 59:457–63
Smith A, Webley DJ. 1968. A
verandah-trap hut for studying the
house-frequenting habits of mosquitoes
and for assessing insecticides. III. The
effect of DDT on the behaviour and
mortality. Bull. Entomol. Res. 59:33–46
Somboon P, Lines J, Aramrattana A, Chitprarop U, Prajakwong S, et al. 1995. Entomological evaluation of community-wide

84.

85.

86.

87.

88.

89.

90.

91.

92.

93.

use of lambdacyhalothrin-impregnated
bed nets against malaria in a border area of
north-west Thailand. Trans. R. Soc. Trop.
Med. Hyg. 89:248–54
Sundavaraman S. 1958. The behaviour
of A. sundaicus Rodenwaldt in relation
to the application of residual insecticides
in Tjilatjap, Indonesia. Ind. J. Malariol.
12:129–56
Takken W, Scott T. 2003. Ecological Aspects for Application of Genetically Modified Mosquitoes. UR Frontis Ser., Vol. 2.
Dordrecht: Kluwer
Taylor DS. 1989. Preliminary field observations on the killing behavior of Toxorhynchites amboinensis larvae. J. Am.
Mosq. Control Assoc. 5:444–45
Thomas DD, Donnelly CA, Wood RJ,
Alphey LS. 2000. Insect population control using a dominant, repressible, lethal
genetic system. Science 287:2474–76
Tour´e Y, Petrarca V, Traor´e SF, Coulibaly
A, Maiga HM, et al. 1998. The distribution
and inversion polymorphism of chromosomally recognized taxa of the Anopheles
gambiae complex in Mali, West Africa.
Parassitologia 40:477–511
Trpis M. 1973. Interaction between the
predator Toxorhynchites brevipalpis and
its prey Aedes aegypti. Bull. World Health
Organ. 49:359–65
von Borstel RC. 1960. Population control by release of irradiated males. Science
131:878–82
World Health Organisation. 1976. WHOsupported collaborative research in India:
the facts. WHO Chron. 30:131–39
World Health Organisation. 1986. Resistance of vectors, and reservoirs of disease
to pesticides. World Health Organ. Tech.
Rep. Ser. 737
Yasuno M, Macdonald WW, Curtis CF,
Grover KK, Rajagopalan PK, et al. 1978.
A control experiment with chemosterilised male Culex pipiens fatigans in a
village near Delhi surrounded by a
breeding-free zone. Jpn. J. Sanit. Zool.
29:325–43

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Annual Review of Entomology
Volume 50, 2005

CONTENTS
Annu. Rev. Entomol. 2005.50:53-70. Downloaded from arjournals.annualreviews.org
by INFLIBNET Master on 04/18/09. For personal use only.

BIOLOGY AND MANAGEMENT OF INSECT PESTS IN NORTH AMERICAN
INTENSIVELY MANAGED HARDWOOD FOREST SYSTEMS,
David R. Coyle, T. Evan Nebeker, Elwood R. Hart,
and William J. Mattson

THE EVOLUTION OF COTTON PEST MANAGEMENT PRACTICES IN
CHINA, K.M. Wu and Y.Y. Guo
MOSQUITO BEHAVIOR AND VECTOR CONTROL, Helen Pates
and Christopher Curtis

1
31
53

THE GENETICS AND GENOMICS OF THE SILKWORM, BOMBYX MORI,
Marian R. Goldsmith, Toru Shimada, and Hiroaki Abe

TSETSE GENETICS: CONTRIBUTIONS TO BIOLOGY, SYSTEMATICS, AND
CONTROL OF TSETSE FLIES, R.H. Gooding and E.S. Krafsur
MECHANISMS OF HOPPERBURN: AN OVERVIEW OF INSECT TAXONOMY,
BEHAVIOR, AND PHYSIOLOGY, Elaine A. Backus, Miguel S. Serrano,
and Christopher M. Ranger

71
101

125

FECAL RESIDUES OF VETERINARY PARASITICIDES: NONTARGET
EFFECTS IN THE PASTURE ENVIRONMENT, Kevin D. Floate,
Keith G. Wardhaugh, Alistair B.A. Boxall, and Thomas N. Sherratt

153

THE MEVALONATE PATHWAY AND THE SYNTHESIS OF JUVENILE
HORMONE IN INSECTS, Xavier Bell´es, David Mart´ın,
and Maria-Dolors Piulachs

181

FOLSOMIA CANDIDA (COLLEMBOLA): A “STANDARD” SOIL
ARTHROPOD, Michelle T. Fountain and Steve P. Hopkin
CHEMICAL ECOLOGY OF LOCUSTS AND RELATED ACRIDIDS,

201

Ahmed Hassanali, Peter G.N. Njagi, and Magzoub Omer Bashir

223

THYSANOPTERA: DIVERSITY AND INTERACTIONS, Laurence A. Mound
EFFECTS OF PLANTS GENETICALLY MODIFIED FOR INSECT
RESISTANCE ON NONTARGET ORGANISMS, Maureen O’Callaghan,
Travis R. Glare, Elisabeth P.J. Burgess, and Louise A. Malone

247

271

vii

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October 28, 2004

viii

21:8

Annual Reviews

AR234-FM

CONTENTS

INVASIVE PHYTOPHAGOUS PESTS ARISING THROUGH A RECENT
TROPICAL EVOLUTIONARY RADIATION: THE BACTROCERA DORSALIS
COMPLEX OF FRUIT FLIES, Anthony R. Clarke, Karen F. Armstrong,
Amy E. Carmichael, John R. Milne, S. Raghu, George K. Roderick,
and David K. Yeates

293

PHEROMONE-MEDIATED AGGREGATION IN NONSOCIAL ARTHROPODS:
AN EVOLUTIONARY ECOLOGICAL PERSPECTIVE, Bregje Wertheim,

Annu. Rev. Entomol. 2005.50:53-70. Downloaded from arjournals.annualreviews.org
by INFLIBNET Master on 04/18/09. For personal use only.

Erik-Jan A. van Baalen, Marcel Dicke, and Louise E.M. Vet

EGG DUMPING IN INSECTS, Douglas W. Tallamy
ECOLOGICAL, BEHAVIORAL, AND BIOCHEMICAL ASPECTS OF INSECT
HYDROCARBONS, Ralph W. Howard and Gary J. Blomquist
THE EVOLUTION OF MALE TRAITS IN SOCIAL INSECTS,
Jacobus J. Boomsma, Boris Baer, and J¨urgen Heinze

321
347
371
395

EVOLUTIONARY AND MECHANISTIC THEORIES OF AGING,
Kimberly A. Hughes and Rose M. Reynolds

421

TYRAMINE AND OCTOPAMINE: RULING BEHAVIOR AND METABOLISM,
Thomas Roeder

447

ECOLOGY OF INTERACTIONS BETWEEN WEEDS AND ARTHROPODS,
Robert F. Norris and Marcos Kogan

NATURAL HISTORY OF PLAGUE: PERSPECTIVES FROM MORE THAN A
CENTURY OF RESEARCH, Kenneth L. Gage and Michael Y. Kosoy
EVOLUTIONARY ECOLOGY OF INSECT IMMUNE DEFENSES,
Paul Schmid-Hempel

SYSTEMATICS, EVOLUTION, AND BIOLOGY OF SCELIONID AND
PLATYGASTRID WASPS, A.D. Austin, N.F. Johnson, and M. Dowton

479
505
529
553

INDEXES
Subject Index
Cumulative Index of Contributing Authors, Volumes 41–50
Cumulative Index of Chapter Titles, Volumes 41–50

ERRATA
An online log of corrections to Annual Review of Entomology
chapters may be found at http://ento.annualreviews.org/errata.shtml

583
611
616