- J. Carlson (1)
- J.M.O. Depinay (1)
- J. Dushoff (1)
- W.A. Foster (1)
- G. Gheysens (1)
- A.K. Githeko (1)
- J. Githure (1)
- B.H. Hahn (1)
- G. Killeen (1)
- B.G.J. Knols (1)
- J.J.A. Loon van (5)
- J.A.C.M. Loonen (1)
- D.E. Loy (1)
- P.A. Mbadi (1)
- C.M. Mbogo (1)
- F.E. McKenzie (1)
- J. Meijerink (1)
- D.M. Menya (1)
- W.R. Mukabana (5)
- H. Mwambi (1)
- C.K. Mweresa (2)
- P. Omusula (2)
- B.O. Orindi (1)
- B. Otieno (1)
- Y.T. Qiu (2)
- K.J. Roey van (1)
- W.H. Schmied (1)
- T.W. Scott (1)
- R.C. Smallegange (4)
- H.M. Smid (1)
- J. Spitzen (1)
- W. Takken (12)
- A.M. Toure (1)
- N.O. Verhulst (4)
- P.M. Wamae (1)
- L.J. Zwiebel (1)
Mosquito host preferences affect their response to synthetic and natural odour blends
Busula, A.O. ; Takken, W. ; Loy, D.E. ; Hahn, B.H. ; Mukabana, W.R. ; Verhulst, N.O. - \ 2015
Malaria Journal 14 (2015). - ISSN 1475-2875 - 9 p.
polymerase-chain-reaction - vector anopheles-gambiae - rice irrigation scheme - sensu-stricto diptera - human skin microbiota - treated bed nets - carbon-dioxide - western kenya - plasmodium-falciparum - semifield conditions
Background The anthropophilic malaria mosquito Anopheles gambiae sensu stricto (hereafter termed Anopheles gambiae) primarily takes blood meals from humans, whereas its close sibling Anopheles arabiensis is more opportunistic. Previous studies have identified several compounds that play a critical role in the odour-mediated behaviour of An. gambiae. This study determined the effect of natural and synthetic odour blends on mosquitoes with different host preferences to better understand the host-seeking behaviour of mosquitoes and the potential of synthetic odour blends for standardized monitoring. Methods Odour blends were initially tested for their attractiveness to An. gambiae and An. arabiensis in a semi-field system with MM-X traps baited with natural and synthetic odours. Natural host odours were collected from humans, cows and chickens. The synthetic odour blends consisted of three or five previously identified compounds released with carbon dioxide. These studies were continued under natural conditions where odour blends were tested outdoors to determine their effect on species with different host preferences. Results In the semi-field experiments, human odour attracted significantly higher numbers of both mosquito species. However, An. arabiensis was also attracted to cow and chicken odours, which confirms its opportunistic behaviour. A five-component synthetic blend was highly attractive to both mosquito species. In the field, the synthetic odour blend caught significantly more An. funestus than traps baited with human odour, while no difference was found for An. arabiensis. Catches of An. arabiensis and Culex spp. contained large numbers of blood-fed mosquitoes, mostly from cows, which indicates that these mosquitoes had fed outdoors. Conclusions Different odour baits elicit varying responses among mosquito species. Synthetic odour blends are highly effective for trapping mosquitoes; however, not all mosquitoes respond equally to the same odour blend. Combining fermenting molasses with synthetic blends in a trap represents the most effective tool to catch blood-fed mosquitoes outside houses, which is essential for understanding outdoor malaria transmission.
Evaluation of textile substrates for dispensing synthetic attractants for malaria mosquitoes
Mweresa, C.K. ; Mukabana, W.R. ; Omusula, P. ; Otieno, B. ; Gheysens, G. ; Takken, W. ; Loon, J.J.A. van - \ 2014
Parasites & Vectors 7 (2014). - ISSN 1756-3305 - 10 p.
vector anopheles-gambiae - sensu-stricto diptera - baited entry traps - western kenya - semifield conditions - carbon-dioxide - host - arabiensis - behavior - nets
Background The full-scale impact of odour-baited technology on the surveillance, sampling and control of vectors of infectious diseases is partly limited by the lack of methods for the efficient and sustainable dispensing of attractants. In this study we investigated whether locally-available and commonly used textiles are efficient substrates for the release of synthetic odorant blends attracting malaria mosquitoes. Methods The relative efficacy of (a) polyester, (b) cotton, (c) cellulose¿+¿polyacrylate, and (d) nylon textiles as substrates for dispensing a synthetic odour blend (Ifakara blend 1(IB1)) that attracts malaria mosquitoes was evaluated in western Kenya. The study was conducted through completely randomized Latin square experimental designs under semi-field and field conditions. Results Traps charged with IB1-impregnated polyester, cotton and cellulose¿+¿polyacrylate materials caught significantly more female Anopheles gambiae sensu stricto (semi-field conditions) and An. gambiae sensu lato (field conditions) mosquitoes than IB1-treated nylon (P¿=¿0.001). The IB1-impregnated cellulose¿+¿polyacrylate material was the most attractive to female An. funestus mosquitoes compared to all other dispensing textile substrates (P¿
Advances in methods for colour marking of mosquitoes
Verhulst, N.O. ; Loonen, J.A.C.M. ; Takken, W. - \ 2013
Parasites & Vectors 6 (2013). - ISSN 1756-3305 - 7 p.
sensu-stricto diptera - anopheles-gambiae - release-recapture - aedes-aegypti - fluorescent powder - dispersal - culicidae - population - queensland - arabiensis
Background: Different techniques are available for colour marking insects and each technique may be suitable for different insect species. Mosquitoes can be marked to determine population size, distribution and flight distance or distinguish closely related species. In this study, two methods of colour marking mosquitoes were described in detail and the impact of both methods on the survival and host-seeking behaviour of the malaria mosquito Anopheles gambiae sensu stricto was investigated. Methods: Mosquitoes were marked in groups with fluorescent powder or fluorescent dye. The powder was applied by creating a cloud of powder in a paper cup and the dye was applied with an airbrush. The effect of marking on the survival of mosquitoes of different age groups was tested under controlled conditions. The effect of marking on the host seeking response of the mosquitoes was tested in an olfactometer with human and cow odour as baits. Results: No effect of either of the marking methods was found on the survival of mosquitoes that were treated 1 or 3 days after emergence, however, the survival of mosquitoes treated 5 or 9 days after emergence was significantly reduced. The host-seeking response of mosquitoes to human or cow odour was tested in a dual-port olfactometer and was not found to be affected by treatment with fluorescent powder or dye. Conclusions: Both methods are suitable for colour marking large groups of mosquitoes. Marking with fluorescent powder, however, is preferred because the method is simpler, visible without a UV light and no specific materials are required.
Evaluation of low density polyethylene and nylon for delivery of synthetic mosquito attractants.
Mukabana, W.R. ; Mweresa, C.K. ; Omusula, P. ; Orindi, B.O. ; Smallegange, R.C. ; Loon, J.J.A. van; Takken, W. - \ 2012
Parasites & Vectors 5 (2012). - ISSN 1756-3305 - 18 p.
vector anopheles-gambiae - sensu-stricto diptera - human skin microbiota - semifield conditions - carbon-dioxide - traps - odor - behavior - culicidae - volatiles
BACKGROUND: Synthetic odour baits present an unexploited potential for sampling, surveillance and control of malaria and other mosquito vectors. However, application of such baits is impeded by the unavailability of robust odour delivery devices that perform reliably under field conditions. In the present study the suitability of low density polyethylene (LDPE) and nylon strips for dispensing synthetic attractants of host-seeking Anopheles gambiae mosquitoes was evaluated. METHODS: Baseline experiments assessed the numbers of An. gambiae mosquitoes caught in response to low density polyethylene (LDPE) sachets filled with attractants, attractant-treated nylon strips, control LDPE sachets, and control nylon strips placed in separate MM-X traps. Residual attraction of An. gambiae to attractant-treated nylon strips was determined subsequently. The effects of sheet thickness and surface area on numbers of mosquitoes caught in MM-X traps containing the synthetic kairomone blend dispensed from LDPE sachets and nylon strips were also evaluated. Various treatments were tested through randomized 4¿×¿4 Latin Square experimental designs under semi-field conditions in western Kenya. RESULTS: Attractant-treated nylon strips collected 5.6 times more An. gambiae mosquitoes than LDPE sachets filled with the same attractants. The attractant-impregnated nylon strips were consistently more attractive (76.95%; n¿=¿9,120) than sachets containing the same attractants (18.59%; n¿=¿2,203), control nylon strips (2.17%; n¿=¿257) and control LDPE sachets (2.29%; n¿=¿271) up to 40¿days post-treatment (P¿
Feeding strategies of anthropophilic mosquitoes result in increased risk of pathogen transmission
Scott, T.W. ; Takken, W. - \ 2012
Trends in Parasitology 28 (2012)3. - ISSN 1471-4922 - p. 114 - 121.
aedes-aegypti diptera - anopheles-gambiae diptera - ideal free distribution - sensu-stricto diptera - puerto-rico - human-blood - body-size - plasmodium-falciparum - dengue vector - defensive behavior
Vector-borne disease specialists have traditionally assumed that in each egg-laying cycle mosquitoes take a single bloodmeal that is used for egg development and feed on plant sugars for flight and production of energy reserves. Here we review research showing that for two of the most important vectors of human pathogens (Anopheles gambiae and Aedes aegypti) imbibing multiple bloodmeals during a gonotrophic cycle while foregoing sugar feeding is a common behaviour, not an exception. By feeding preferentially and frequently on human blood these species increase their fitness and exponentially boost the basic reproduction rate of pathogens they transmit. Although the epidemiological outcome is similar, there are important differences in processes underlying frequent human contact by these species that merit more detailed investigation.
Improvement of a synthetic lure for Anopheles gambiae using compounds produced by human skin microbiota
Verhulst, N.O. ; Mbadi, P.A. ; Bukovinszkine-Kiss, G. ; Mukabana, W.R. ; Loon, J.J.A. van; Takken, W. ; Smallegange, R.C. - \ 2011
Malaria Journal 10 (2011). - ISSN 1475-2875 - 9 p.
yellow-fever mosquito - sensu-stricto diptera - mm-x traps - malaria mosquito - aedes-aegypti - carbon-dioxide - electrophysiological responses - lactic-acid - host-odor - culicidae
Background - Anopheles gambiae sensu stricto is considered to be highly anthropophilic and volatiles of human origin provide essential cues during its host-seeking behaviour. A synthetic blend of three human-derived volatiles, ammonia, lactic acid and tetradecanoic acid, attracts A. gambiae. In addition, volatiles produced by human skin bacteria are attractive to this mosquito species. The purpose of the current study was to test the effect of ten compounds present in the headspace of human bacteria on the host-seeking process of A. gambiae. The effect of each of the ten compounds on the attractiveness of a basic blend of ammonia, lactic and tetradecanoic acid to A. gambiae was examined. Methods- The host-seeking response of A. gambiae was evaluated in a laboratory set-up using a dual-port olfactometer and in a semi-field facility in Kenya using MM-X traps. Odorants were released from LDPE sachets and placed inside the olfactometer as well as in the MM-X traps. Carbon dioxide was added in the semi-field experiments, provided from pressurized cylinders or fermenting yeast. Results - The olfactometer and semi-field set-up allowed for high-throughput testing of the compounds in blends and in multiple concentrations. Compounds with an attractive or inhibitory effect were identified in both bioassays. 3-Methyl-1-butanol was the best attractant in both set-ups and increased the attractiveness of the basic blend up to three times. 2-Phenylethanol reduced the attractiveness of the basic blend in both bioassays by more than 50%. Conclusions - Identification of volatiles released by human skin bacteria led to the discovery of compounds that have an impact on the host-seeking behaviour of A. gambiae. 3-Methyl-1-butanol may be used to increase mosquito trap catches, whereas 2-phenylethanol has potential as a spatial repellent. These two compounds could be applied in push-pull strategies to reduce mosquito numbers in malaria endemic areas.
Shading by Napier grass reduces malaria vector larvae in natural habitats in western Kenya highlands
Wamae, P.M. ; Githeko, A.K. ; Menya, D.M. ; Takken, W. - \ 2010
EcoHealth 7 (2010)4. - ISSN 1612-9202 - p. 485 - 497.
anopheles-gambiae complex - sensu-stricto diptera - land-cover types - dar-es-salaam - spatial-distribution - microbial larvicides - oviposition site - culex mosquitos - aquatic stages - culicidae
Increased human population in the Western Kenya highlands has led to reclamation of natural swamps resulting in the creation of habitats suitable for the breeding of Anopheles gambiae, the major malaria vector in the region. Here we report on a study to restore the reclaimed swamp and reverse its suitability as a habitat for malaria vectors. Napier grass-shaded and non-shaded water channels in reclaimed sites in Western Kenya highlands were studied for the presence and density of mosquito larvae, mosquito species composition, and daily variation in water temperature. Shading was associated with 75.5% and 88.4% (P <0.0001) reduction in anopheline larvae densities and 78.1% and 88% (P <0.0001) reduction in Anopheles gambiae sensu lato (s.l.) densities in two sites, respectively. Shading was associated with a 5.7°C, 5.0°C, and 4.7°C, and 1.6°C, 3.9°C, and 2.8°C (for maximum, minimum, and average temperatures, respectively) reduction (P <0.0001) in water temperatures in the two locations, respectively. An. gambiae s.l. was the dominant species, constituting 83.2% and 73.1%, and 44.5% and 42.3%, of anophelines in non-shaded and shaded channels, respectively, in the two sites, respectively. An. gambiae sensu stricto (s.s.) constituted the majority (97.4%) of An. gambiae s.l., while the rest (2.6%) comprised of Anopheles arabiensis. Minimum water temperature decreased with increasing grass height (P = 0.0039 and P = 0.0415 for Lunyerere and Emutete sites, respectively). The results demonstrate how simple environmental strategies can have a strong impact on vector densities
Sugar-fermenting yeast as an organic source of carbon dioxide to attract the malaria mosquito Anopheles gambiae
Smallegange, R.C. ; Schmied, W.H. ; Roey, K.J. van; Verhulst, N.O. ; Spitzen, J. ; Mukabana, W.R. ; Takken, W. - \ 2010
Malaria Journal 9 (2010). - ISSN 1475-2875 - 15 p.
sensu-stricto diptera - human skin emanations - chromatography-mass-spectrometry - mm-x traps - western kenya - aedes-aegypti - electrophysiological responses - odor plumes - human sweat - light trap
Background - Carbon dioxide (CO2) plays an important role in the host-seeking process of opportunistic, zoophilic and anthropophilic mosquito species and is, therefore, commonly added to mosquito sampling tools. The African malaria vector Anopheles gambiae sensu stricto is attracted to human volatiles augmented by CO2. This study investigated whether CO2, usually supplied from gas cylinders acquired from commercial industry, could be replaced by CO2 derived from fermenting yeast (yeast-produced CO2). Methods - Trapping experiments were conducted in the laboratory, semi-field and field, with An. gambiae s.s. as the target species. MM-X traps were baited with volatiles produced by mixtures of yeast, sugar and water, prepared in 1.5, 5 or 25 L bottles. Catches were compared with traps baited with industrial CO2. The additional effect of human odours was also examined. In the laboratory and semi-field facility dual-choice experiments were conducted. The effect of traps baited with yeast-produced CO2 on the number of mosquitoes entering an African house was studied in the MalariaSphere. Carbon dioxide baited traps, placed outside human dwellings, were also tested in an African village setting. The laboratory and semi-field data were analysed by a ¿2-test, the field data by GLM. In addition, CO2 concentrations produced by yeast-sugar solutions were measured over time. Results - Traps baited with yeast-produced CO2 caught significantly more mosquitoes than unbaited traps (up to 34 h post mixing the ingredients) and also significantly more than traps baited with industrial CO2, both in the laboratory and semi-field. Adding yeast-produced CO2 to traps baited with human odour significantly increased trap catches. In the MalariaSphere, outdoor traps baited with yeast-produced or industrial CO2 + human odour reduced house entry of mosquitoes with a human host sleeping under a bed net indoors. Anopheles gambiae s.s. was not caught during the field trials. However, traps baited with yeast-produced CO2 caught similar numbers of Anopheles arabiensis as traps baited with industrial CO2. Addition of human odour increased trap catches. Conclusions - Yeast-produced CO2 can effectively replace industrial CO2 for sampling of An. gambiae s.s.. This will significantly reduce costs and allow sustainable mass-application of odour-baited devices for mosquito sampling in remote areas
Interindividual variation in the attractiveness of human odours to the malaria mosquito Anopheles gambiae s.s.
Qiu, Y.T. ; Smallegange, R.C. ; Loon, J.J.A. van; Braak, C.J.F. ter; Takken, W. - \ 2006
Medical and Veterinary Entomology 20 (2006)3. - ISSN 0269-283X - p. 280 - 287.
sensu-stricto diptera - human skin emanations - aedes-aegypti - differential attractiveness - pregnant-women - host-seeking - lactic-acid - human sweat - culicidae - behavior
Differences between human individuals in their attractiveness to female mosquitoes have been reported repeatedly, but the underlying mechanisms are not well understood. Skin emanations from 27 human individuals, collected on glass marbles, were tested against ammonia in a dual-choice olfactometer to establish their degrees of attractiveness to anthropophilic Anopheles gambiae s.s. Giles (Diptera: Culicidae) mosquitoes. Ammonia was used as a standard odour source because of its proven attractiveness to An. gambiae s.s. Skin emanations from most volunteers attracted significantly more mosquitoes than ammonia. There were clear differences in the attractiveness of skin emanations from different volunteers relative to that of ammonia, as well as in the strength of the trap entry response. Consistent differences were observed when emanations from the three most and the three least attractive volunteers were tested pairwise. No gender or age effect was found for relative attractiveness or trap entry response. Emanations from volunteers with higher behavioural attractiveness elicited higher electroantennogram response amplitudes in two pairs, but in a third pair a higher electroantennogram response was found for the less attractive volunteer. These results confirm that odour contributes to the differences in attractiveness of humans to mosquitoes
Olfactory coding in antennal neurons of the malaria mosquito, Anopheles gambiae
Qiu, Y.T. ; Loon, J.J.A. van; Takken, W. ; Meijerink, J. ; Smid, H.M. - \ 2006
Chemical Senses 31 (2006)9. - ISSN 0379-864X - p. 845 - 863.
sensu-stricto diptera - spodoptera-littoralis lepidoptera - culex-tarsalis diptera - host-seeking behavior - human skin emanations - l-lactic acid - aedes-aegypti - human-sweat - sex-pheromone - drosophila-antenna
Olfactory receptor neurons (ORNs) in the antenna of insects serve to encode odors in action potential activity conducted to the olfactory lobe of the deuterocerebrum. We performed an analysis of the electrophysiological responses of olfactory neurons in the antennae of the female malaria mosquito Anopheles gambiae s.s. and investigated the effect of blood feeding on responsiveness. Forty-four chemicals that are known to be present in human volatile emanations were used as odor stimuli. We identified 6 functional types of trichoid sensilla and 5 functional types of grooved-peg sensilla (GP) based on a hierarchical cluster analysis. Generalist ORNs, tuned to a broad range of odors, moderate specialist ORNs and 2 ORNs tuned to only one odor were identified in different sensilla types. Neurons in GP were tuned to more polar compounds including the important behavioral attractant ammonia and its synergist L-lactic acid, responses to which were found only in GP. Combinatorial coding is the most plausible principle operating in the olfactory system of this mosquito species. We document for the first time both up- and downregulation of ORN responsiveness after blood feeding. Modulation of host-seeking and oviposition behavior is associated with both qualitative and quantitative changes in the peripheral sensory system
A simulation model of African Anopheles ecology and population dynamics for the analysis of malaria transmission
Depinay, J.M.O. ; Mbogo, C.M. ; Killeen, G. ; Knols, B.G.J. ; Beier, J. ; Carlson, J. ; Dushoff, J. ; Billingsley, P. ; Mwambi, H. ; Githure, J. ; Toure, A.M. ; McKenzie, F.E. - \ 2004
Malaria Journal 3 (2004). - ISSN 1475-2875 - 21 p.
sensu-stricto diptera - western kenya - body-size - gambiae complex - larval survival - culicidae - temperature - habitats - density - arabiensis
Background: Malaria is one of the oldest and deadliest infectious diseases in humans. Many mathematical models of malaria have been developed during the past century, and applied to potential interventions. However, malaria remains uncontrolled and is increasing in many areas, as are vector and parasite resistance to insecticides and drugs. Methods: This study presents a simulation model of African malaria vectors. This individual-based model incorporates current knowledge of the mechanisms underlying Anopheles population dynamics and their relations to the environment. One of its main strengths is that it is based on both biological and environmental variables. Results: The model made it possible to structure existing knowledge, assembled in a comprehensive review of the literature, and also pointed out important aspects of basic Anopheles biology about which knowledge is lacking. One simulation showed several patterns similar to those seen in the field, and made it possible to examine different analyses and hypotheses for these patterns; sensitivity analyses on temperature, moisture, predation and preliminary investigations of nutrient competition were also conducted. Conclusions: Although based on some mathematical formulae and parameters, this new tool has been developed in order to be as explicit as possible, transparent in use, close to reality and amenable to direct use by field workers. It allows a better understanding of the mechanisms underlying Anopheles population dynamics in general and also a better understanding of the dynamics in specific local geographic environments. It points out many important areas for new investigations that will be critical to effective, efficient, sustainable interventions.
Olfactory regulation of mosquito-host interactions
Zwiebel, L.J. ; Takken, W. - \ 2004
Insect Biochemistry and Molecular Biology 34 (2004)7. - ISSN 0965-1748 - p. 645 - 652.
odorant-binding-proteins - malaria vector mosquito - anopheles-gambiae-s.s. - sensu-stricto diptera - aedes-aegypti - human-sweat - seeking behavior - carbon-dioxide - drosophila-melanogaster - differential attractiveness
Mosquitoes that act as disease vectors rely upon olfactory cues to direct several important behaviors that are fundamentally involved in establishing their overall vectorial capacity. Of these, the propensity to select humans for blood feeding is arguably the most important of these olfactory driven behaviors in so far as it significantly contributes to the ability of these mosquitoes to transmit pathogens that cause diseases such as dengue, yellow fever and most significantly human malaria. Here, we review significant advances in behavioral, physiological and molecular investigations into mosquito host preference, with a particular emphasis on studies that have emerged in the post-genomic era that seek to combine these approaches. (C) 2004 Elsevier Ltd. All rights reserved.
Nectar-related vs human-related volatiles: behavioural response and choice by female and male Anopheles gambiae (Diptera: Culicidae) between emergence and first feeding
Foster, W.A. ; Takken, W. - \ 2004
Bulletin of Entomological Research 94 (2004)2. - ISSN 0007-4853 - p. 145 - 157.
aedes-aegypti diptera - sensu-stricto diptera - culex nigripalpus mosquitos - blood plus sugar - malaria mosquito - body-size - host-seeking - human sweat - blood/nectar choice - olfactory responses
The close association of Anopheles gambiae Giles with humans and its females’ ability to live on human blood alone suggest that females may ignore sources of sugar in favour of human blood as a source of energy. They have limited energy reserves at emergence, and at 27°C both sexes generally die if they do not feed during night 1, 24–36 h after emergence. Food preferences during this critical period were tested by measuring responses to volatiles from honey and soiled socks, which served as surrogates for nectar-related and human-related volatiles in a wind-tunnel olfactometer. Both sexes responded more strongly to honey than to human volatiles, and given a choice, preferred honey over human volatiles. After 5 days of sugar access and maturation, males continued to prefer honey volatiles, whereas females changed behaviour, responding almost exclusively to human volatiles. Night 1 experiments also demonstrated that: (i) females previously having had sugar during the night of emergence responded more strongly to human volatiles; (ii) large-bodied mosquitoes of both sexes responded more strongly to honey than small-bodied ones; and (iii) females were equally responsive to honey in both early and late scotophase but were slightly more responsive to human volatiles in late scotophase. These results indicate that for a female’s first meal, sugar is a viable option and is preferred when nectar-related stimuli are strong. This supports field evidence that sugar-feeding is a significant component of A. gambiae female behaviour.