- T.A. Beek van (1)
- C.J.F. Braak ter (2)
- G. Bukovinszkine Kiss (1)
- G. Bukovinszkine-Kiss (1)
- M. Dicke (1)
- A.M.S. Galimard (1)
- M. Jawara (1)
- B.G.J. Knols (2)
- J.J.A. Loon van (7)
- P.A. Mbadi (1)
- J. Meijerink (1)
- P. Milligan (1)
- W.R. Mukabana (3)
- C.K. Mweresa (1)
- P. Omusula (1)
- B. Otieno (2)
- Y.T. Qiu (5)
- K.J. Roey van (1)
- W.H. Schmied (1)
- R.C. Smallegange (7)
- H.M. Smid (1)
- J. Spitzen (2)
- W. Takken (9)
- N.O. Verhulst (2)
- B.T. Weldegergis (1)
Understanding the long-lasting attraction of malaria mosquitoes to odor baits
Mweresa, C.K. ; Otieno, B. ; Omusula, P. ; Weldegergis, B.T. ; Verhulst, N.O. ; Dicke, M. ; Loon, J.J.A. van; Takken, W. ; Mukabana, W.R. - \ 2015
PLoS One 10 (2015)3. - ISSN 1932-6203 - 16 p.
gambiae-sensu-stricto - human skin emanations - anopheles-gambiae - human pathogen - aedes-aegypti - human sweat - identification - culicidae - volatiles - behavior
The use of odor baits for surveillance and control of malaria mosquitoes requires robust dispensing tools. In this study, the residual activity of a synthetic mosquito attractant blend dispensed from nylon or low density polyethylene (LDPE) sachets was evaluated at weekly intervals for one year without re-impregnation. The potential role of bacteria in modulating the attraction of mosquitoes to odor-treated nylon that had been used repeatedly over the one year study period, without re-impregnation, was also investigated. Significantly higher proportions of female Anopheles gambiae sensu stricto mosquitoes were consistently attracted to treated nylon strips than the other treatments, up to one year post-treatment. Additional volatile organic compounds and various bacterial populations were found on the treated nylon strips after one year of repeated use. The most abundant bacteria were Bacillus thuringiensis and Acinetobacter baumannii. Autoclaving of treated nylon strips prior to exposure had no effect on trap collections of laboratory-reared female An. Gambiae (P = 0.17) or wild female An. Gambiae sensu lato (P = 0.26) and Mansonia spp. (P = 0.17) mosquitoes. Trap catches of wild female An. Funestus (P <0.001) and other anophelines (P <0.007) were higher when treated strips had been autoclaved prior to deployment as opposed to when the treated nylon strips were not autoclaved. By contrast, wild female Culex mosquitoes were more strongly attracted to non-autoclaved compared to autoclaved treated nylon strips (P <0.042). This study demonstrates the feasibility of using odor baits for sampling and surveillance of malaria as well as other mosquito vectors over prolonged periods of time. Preliminary evidence points towards the potential role of bacteria in sustaining prolonged use of nylon material for dispensing synthetic attractant odorants for host-seeking malaria and other mosquito vectors but further investigations are required.
Identification of candidate volatiles that affect the behavioural response of the malaria mosquito Anopheles gambiae sensu stricto to an active kairomone blend: laboratory and semi-field assays
Smallegange, R.C. ; Bukovinszkine Kiss, G. ; Otieno, B. ; Mbadi, P.A. ; Takken, W. ; Mukabana, W.R. ; Loon, J.J.A. van - \ 2012
Physiological Entomology 37 (2012)1. - ISSN 0307-6962 - p. 60 - 71.
human skin emanations - integrated pest-management - mm-x traps - carbon-dioxide - vector control - aedes-aegypti - organic-compounds - chemical-composition - flight maneuvers - culex mosquitos
Anopheles gambiae Giles sensu stricto (Diptera: Culicidae) is the most important vector of human malaria in sub-Saharan Africa, affecting the lives of millions of people. Existing tools such as insecticide-treated nets and indoor-residual sprays are not only effective, but also have limitations as a result of the development of resistance to insecticides and behavioural adaptations in biting time. Therefore, novel mosquito-control tools are needed. Odour-releasing traps have a potential for both trapping and surveillance purposes. Based on the outcome of ex vivo gene expression assays and in vivo electrophysiological assays on hundreds of volatile organic compounds, 29 ‘candidate behaviourally-disruptive organic compounds' (cBDOCs) are selected, belonging to 10 chemical categories, to be assayed in the laboratory using dual-choice olfactometers for the ability to modify the ‘attractiveness’ (i.e. significantly more insects being caught in the associated trap) of a basic volatile blend consisting of ammonia, lactic acid and tetradecanoic acid but without additional carbon dioxide. Compounds that either reduce or increase trap catches by the basic blend in the olfactometer experiments are tested under African conditions in choice experiments in a semi-field facility in Kenya. The release rates of cBDOCs are determined gravimetrically to allow the calculation of aerial concentrations at the trap outlet. Aerial concentrations in the sub-p.p.m. range are reported for the first time to influence mosquito behaviour. The results of the olfactometer and semi-field assays generally correspond. Under semi-field conditions, three compounds, 3-heptanol (0.025 p.p.m.), 2-methylpropanal (0.05 p.p.m.) and 4,5-dimethylthiazole (0.73 p.p.m.), significantly increase trap catches relative to the basic blend consisting of ammonia, lactic acid, tetradecanoic acid and carbon dioxide. 2-Acetylthiophene, 2-nonanone and 2-phenylethanol decrease the number of mosquitoes caught at all concentrations tested under semi-field conditions. These compounds hold promise as attractants and spatial repellents to be applied in mosquito control programmes.
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
Effectiveness of synthetic versus natural human volatiles as attractants for Anopheles gambiae (Diptera: Culicidae) sensu stricto
Smallegange, R.C. ; Knols, B.G.J. ; Takken, W. - \ 2010
Journal of Medical Entomology 47 (2010)3. - ISSN 0022-2585 - p. 338 - 344.
human skin emanations - yellow-fever mosquito - gas chromatography/mass spectrometry - malaria mosquito - aedes-aegypti - human sweat - host-seeking - human odors - electrophysiological responses - semifield conditions
Females of the African malaria vector, Anopheles gambiae Giles sensu stricto, use human volatiles to find their blood-host. Previous work has shown that ammonia, lactic acid, and aliphatic carboxylic acids significantly affect host orientation and attraction of this species, In the current study, these compounds were tested for their attractiveness relative to human emanations in vivo and in vitro. Emanations from a human hand, incubated sweat, and foot skin residues on a nylon sock were significantly attractive when tested against clean air. In a dual-choice test, foot skin residues were significantly more attractive than emanations from a human hand in vivo. Ammonia alone attracted more mosquitoes than fresh or incubated sweat, However, the odor of a human hand or of foot skin residues were more attractive than ammonia. A known attractive blend of ammonia with lactic acid and carboxylic acids was less effective than natural foot odorants, The results demonstrate that the synthetic blend based on skin odor is attractive for An. gambiae, but that in a choice situation in vitro natural skin odors are still preferred by the mosquito. Differences in volatile organic compound abundances between a worn sock and the synthetic blend may have resulted in stronger attraction to the sock. This suggests that candidate attractants should be evaluated with consideration of the strength of natural odorant sources, The data furthermore suggest that additional unidentified compounds from the human foot are involved in the host-seeking behavior of this mosquito species.
The effect of aliphatic carboxylic acids on olfaction-based host-seeking of the malaria mosquito Anopheles gambiae sensu stricto
Smallegange, R.C. ; Qiu, Y.T. ; Bukovinszkine-Kiss, G. ; Loon, J.J.A. van; Takken, W. - \ 2009
Journal of Chemical Ecology 35 (2009)8. - ISSN 0098-0331 - p. 933 - 943.
human skin emanations - l-lactic acid - aedes-aegypti diptera - volatile organic-compounds - yellow-fever mosquito - human sweat - electrophysiological responses - tsetse-flies - culicidae - odor
The role of aliphatic carboxylic acids in host-seeking response of the malaria mosquito Anopheles gambiae sensu stricto was examined both in a dual-choice olfactometer and with indoor traps. A basic attractive blend of ammonia + lactic acid served as internal standard odor. Single carboxylic acids were tested in a tripartite blend with ammonia + lactic acid. Four different airflow stream rates (0.5, 5, 50, and 100 ml/min) carrying the compounds were tested for their effect on trap entry response in the olfactometer. In the olfactometer, propanoic acid, butanoic acid, 3-methylbutanoic acid, pentanoic acid, heptanoic acid, octanoic acid, and tetradecanoic acid increased attraction relative to the basic blend. While several carboxylic acids were attractive only at one or two flow rates, tetradecanoic acid was attractive at all flow rates tested. Heptanoic acid was attractive at the lowest flow rate (0.5 ml/min), but repellent at 5 and 50 ml/min. Mixing the air stream laden with these 7 carboxylic acids together with the headspace of the basic blend increased attraction in two quantitative compositions. Subtraction of single acids from the most attractive blend revealed that 3-methylbutanoic acid had a negative effect on trap entry response. In the absence of tetradecanoic acid, the blend was repellent. In assays with MM-X traps, both a blend of 7 carboxylic acids + ammonia + lactic acid (all applied from low density polyethylene-sachets) and a simple blend of ammonia + lactic acid + tetradecanoic acid were attractive. The results show that carboxylic acids play an essential role in the host-seeking behavior of An. gambiae, and that the contribution to blend attractiveness depends on the specific compound studied
Attractiveness of MM-X traps baited with human or synthetic odor to mosquitoes (Diptera: Culicidae) in The Gambia
Qiu, Y.T. ; Smallegange, R.C. ; Braak, C.J.F. ter; Spitzen, J. ; Loon, J.J.A. van; Jawara, M. ; Milligan, P. ; Galimard, A.M.S. ; Beek, T.A. van; Knols, B.G.J. ; Takken, W. - \ 2007
Journal of Medical Entomology 44 (2007)6. - ISSN 0022-2585 - p. 970 - 983.
vector anopheles-gambiae - yellow-fever mosquito - aedes-aegypti diptera - host-seeking behavior - human skin emanations - l-lactic acid - carbon-dioxide - malaria mosquito - carboxylic-acids - human sweat
Chemical cues play an important role in the host-seeking behavior of blood-feeding mosquitoes (Diptera: Culicidae). A field study was carried out in The Gambia to investigate the effects of human odor or synthetic odor blends on the attraction of mosquitoes. MM-X traps baited with 16 odor blends to which carbon dioxide (CO2) was added were tested in four sets of experiments. In a second series of experiments, MM-X traps with 14 odor blends without CO2 were tested. A blend of ammonia and L-lactic acid with or without CO2 was used as control odor in series 1 and 2, respectively. Centers for Disease Control and Prevention (CDC) traps were placed in a traditional house and an experimental house to monitor mosquito densities during the experiments. The MM-X traps caught a total number of 196,756 mosquitoes, with the most abundant species belonging to the genera Mansonia (70.6%), Anopheles (17.5%), and Culex (11.5%). The most abundant mosquito species caught by the CDC traps (56,290 in total) belonged to the genera Mansonia (59.4%), Anopheles (16.0% An. gambiae s.l. Giles, and 11.3% An. ziemanni Grünberg), and Culex (11.6%). MM-X traps baited with synthetic blends were in many cases more attractive than MM-X traps baited with human odors. Addition of CO2 to synthetic odors substantially increased the catch of all mosquito species in the MM-X traps. A blend of ammonia + L-lactic acid + CO2 + 3-methylbutanoic acid was the most attractive odor for most mosquito species. The candidate odor blend shows the potential to enhance trap collections so that traps will provide better surveillance and possible control.
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
Synergism between ammonia, lactic acid and carboxylic acids as kairomones in the host-seeking behaviour of the malaria mosquito Anopheles gambiae sensu stricto (Diptera: Culicidae)
Smallegange, R.C. ; Qiu, Y.T. ; Loon, J.J.A. van; Takken, W. - \ 2005
Chemical Senses 30 (2005)2. - ISSN 0379-864X - p. 145 - 152.
yellow-fever mosquito - aedes-aegypti diptera - human skin emanations - human sweat - olfactory responses - carbon-dioxide - wind-tunnel - odor - identification - spectrometry
Host odours play a major role in the orientation and host location of blood-feeding mosquitoes. Anopheles gambiae Giles sensu stricto, which is the most important malaria vector in Africa, is a highly anthropophilic mosquito species, and the host-seeking behaviour of the females of this mosquito is guided by volatiles of human origin. Ammonia, lactic acid and several carboxylic acids are known to be present in the human odour blend. We investigated the effect of these compounds on naïve female mosquitoes using a dual-port olfactometer. Ammonia was an attractant on its own, whereas lactic acid was not attractive. Carboxylic acids, offered as a mixture of 12 compounds, were repellent at the concentration tested. The addition of ammonia to the carboxylic acid mixture overruled the repellent effect of the latter. Combining ammonia with either lactic acid or the carboxylic acids did not enhance the attractiveness of ammonia alone. However, a synergistic effect was found when ammonia, lactic acid and the carboxylic acids were applied as a blend. Our findings indicate that An. gambiae s.s. relies on the combination of ammonia, lactic acid and carboxylic acids in its orientation to human hosts. The role of lactic acid in this tripartite synergism differs from that reported for the yellow fever mosquito Aedes aegypti