- S.P. Brugge van (1)
- G. Bukovinszkine Kiss (1)
- G. Bukovinszkine-Kiss (1)
- L.F. Chaves (1)
- D.J. Conway (1)
- F. Grieco (1)
- M. Jawara (1)
- D. Jeffries (1)
- G.F. Killeen (1)
- B.G.J. Knols (3)
- C.J.M. Koenraadt (1)
- S. Kranenbarg (1)
- J.L. Leeuwen van (1)
- J.J.A. Loon van (4)
- P.A. Mbadi (2)
- D.J. Menger (1)
- W.R. Mukabana (5)
- W.R. Mukabana (1)
- C.K. Mweresa (1)
- L. Noldus (1)
- D.C. Nwakanma (1)
- P. Omusula (1)
- B. Otieno (3)
- M. Rijk de (1)
- K.J. Roey van (1)
- W.H. Schmied (2)
- G. Schraa (1)
- R.C. Smallegange (7)
- J. Spitzen (2)
- C.W. Spoor (1)
- W. Takken (10)
- N.O. Verhulst (4)
Molasses as a source of carbon dioxide for attracting the malaria mosquitoes Anopheles gambiae and Anopheles funestus
Mweresa, C.K. ; Omusula, P. ; Otieno, B. ; Loon, J.J.A. van; Takken, W. ; Mukabana, W.R. - \ 2014
Malaria Journal 13 (2014). - ISSN 1475-2875 - 13 p.
human skin microbiota - human-landing catches - mm-x traps - western kenya - semifield conditions - diptera-culicidae - sensu-stricto - odor - tanzania - behavior
Background. Most odour baits for haematophagous arthropods contain carbon dioxide (CO2). The CO2 is sourced artificially from the fermentation of refined sugar (sucrose), dry ice, pressurized gas cylinders or propane. These sources of CO2 are neither cost-effective nor sustainable for use in remote areas of sub-Saharan Africa. In this study, molasses was evaluated as a potential substrate for producing CO2 used as bait for malaria mosquitoes. Methods. The attraction of laboratory-reared and wild Anopheles gambiae complex mosquitoes to CO2 generated from yeast-fermentation of molasses was assessed under semi-field and field conditions in western Kenya. In the field, responses of wild Anopheles funestus were also assessed. Attraction of the mosquitoes to a synthetic mosquito attractant, Mbita blend (comprising ammonia, L-lactic acid, tetradecanoic acid and 3-methyl-1-butanol) when augmented with CO2 generated from yeast fermentation of either molasses or sucrose was also investigated. Results. In semi-field, the release rate of CO2 and proportion of An. gambiae mosquitoes attracted increased in tandem with an increase in the quantity of yeast-fermented molasses up to an optimal ratio of molasses and dry yeast. More An. gambiae mosquitoes were attracted to a combination of the Mbita blend plus CO2 produced from fermenting molasses than the Mbita blend plus CO2 from yeast-fermented sucrose. In the field, significantly more female An. gambiae sensu lato mosquitoes were attracted to the Mbita blend augmented with CO2 produced by fermenting 500 g of molasses compared to 250 g of sucrose or 250 g of molasses. Similarly, significantly more An. funestus, Culex and other anopheline mosquito species were attracted to the Mbita blend augmented with CO2 produced from fermenting molasses than the Mbita blend with CO2 produced from sucrose. Augmenting the Mbita blend with CO2 produced from molasses was associated with high catches of blood-fed An. gambiae s.l. and An. funestus mosquitoes. Conclusion. Molasses is a suitable ingredient for the replacement of sucrose as a substrate for the production of CO2 for sampling of African malaria vectors and other mosquito species. The finding of blood-fed malaria vectors in traps baited with the Mbita blend and CO2 derived from molasses provides a unique opportunity for the study of host-vector interactions.
A push-pull system to reduce house entry of malaria mosquitoes
Menger, D.J. ; Otieno, B. ; Rijk, M. de; Mukabana, W.R. ; Loon, J.J.A. van; Takken, W. - \ 2014
Malaria Journal 13 (2014). - ISSN 1475-2875 - 8 p.
vector anopheles-gambiae - host-seeking behavior - mm-x traps - spatial repellency - field-evaluation - western kenya - lactic-acid - culicidae - diptera - strategies
Background. Mosquitoes are the dominant vectors of pathogens that cause infectious diseases such as malaria, dengue, yellow fever and filariasis. Current vector control strategies often rely on the use of pyrethroids against which mosquitoes are increasingly developing resistance. Here, a push-pull system is presented, that operates by the simultaneous use of repellent and attractive volatile odorants. Method/Results. Experiments were carried out in a semi-field set-up: a traditional house which was constructed inside a screenhouse. The release of different repellent compounds, para-menthane-3,8-diol (PMD), catnip oil e.o. and delta-undecalactone, from the four corners of the house resulted in significant reductions of 45% to 81.5% in house entry of host-seeking malaria mosquitoes. The highest reductions in house entry (up to 95.5%), were achieved by simultaneously repelling mosquitoes from the house (push) and removing them from the experimental set-up using attractant-baited traps (pull). Conclusions. The outcome of this study suggests that a push-pull system based on attractive and repellent volatiles may successfully be employed to target mosquito vectors of human disease. Reductions in house entry of malaria vectors, of the magnitude that was achieved in these experiments, would likely affect malaria transmission. The repellents used are non-toxic and can be used safely in a human environment. Delta-undecalactone is a novel repellent that showed higher effectiveness than the established repellent PMD. These results encourage further development of the system for practical implementation in the field.
A 3D Analysis of Flight Behavior of Anopheles gambiae sensu stricto Malaria Mosquitoes in Response to Human Odor and Heat
Spitzen, J. ; Spoor, C.W. ; Grieco, F. ; Braak, C.J.F. ter; Beeuwkes, J. ; Brugge, S.P. van; Kranenbarg, S. ; Noldus, L. ; Leeuwen, J.L. van; Takken, W. - \ 2013
PLoS One 8 (2013)5. - ISSN 1932-6203
female culex-quinquefasciatus - fine-scale structure - mm-x traps - carbon-dioxide - upwind flight - host odor - diptera-culicidae - pheromone plumes - aedes-aegypti - tsetse-flies
Female mosquitoes use odor and heat as cues to navigate to a suitable landing site on their blood host. The way these cues affect flight behavior and modulate anemotactic responses, however, is poorly understood. We studied in-flight behavioral responses of females of the nocturnal malaria mosquito Anopheles gambiae sensu stricto to human odor and heat. Flight-path characteristics in a wind tunnel (flow 20 cm/s) were quantified in three dimensions. With wind as the only stimulus (control), short and close to straight upwind flights were recorded. With heat alone, flights were similarly short and direct. The presence of human odor, in contrast, caused prolonged and highly convoluted flight patterns. The combination of odor+heat resulted in longer flights with more landings on the source than to either cue alone. Flight speed was greatest (mean groundspeed 27.2 cm/s) for odor+heat. Odor alone resulted in decreased flight speed when mosquitoes arrived within 30 cm of the source whereas mosquitoes exposed to odor+heat maintained a high flight speed while flying in the odor plume, until they arrived within 15 cm of the source. Human odor evoked an increase in crosswind flights with an additive effect of heat at close range (
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.
Human skin microbiota and their volatiles as odour baits for the malaria mosquito Anopheles gambiae s.s
Verhulst, N.O. ; Mukabana, W.R. ; Takken, W. ; Smallegange, R.C. - \ 2011
Entomologia Experimentalis et Applicata 139 (2011)2. - ISSN 0013-8703 - p. 170 - 179.
gas chromatography/mass spectrometry - human axillary odor - rift-valley-fever - mm-x traps - western kenya - sensu-stricto - aedes-aegypti - carbon-dioxide - host-seeking - tsetse-flies
Host seeking by the malaria mosquito Anopheles gambiae Giles sensu stricto (Diptera: Culicidae) is mainly guided by volatile chemicals present in human odours. The skin microbiota plays an important role in the production of these volatiles, and skin bacteria grown on agar plates attract An. gambiae s.s. in the laboratory. In this study, the attractiveness of volatiles produced by human skin bacteria to An. gambiae s.s. was tested in laboratory, semi-field, and field experiments to assess these effects in increasing environmental complexity. A synthetic blend of 10 compounds identified in the headspace of skin bacteria was also tested for its attractiveness. Carbon dioxide significantly increased mosquito catches of traps baited with microbial volatiles in the semi-field experiments and was therefore added to the field traps. Traps baited with skin bacteria caught significantly more An. gambiae s.s. than control traps, both in the laboratory and semi-field experiments. Traps baited with the synthetic blend caught more mosquitoes than control traps in the laboratory experiments, but not in the semi-field experiments. Although bacterial volatiles increased mosquito catches in the field study, trapping several mosquito vector species, these effects were not significant for An. gambiae s.l. It is concluded that volatiles from skin bacteria affect mosquito behaviour under laboratory and semi-field conditions and, after fine tuning, have the potential to be developed as odour baits for mosquitoes.
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.
Climate Change and Highland Malaria: Fresh Air for a Hot Debate
Chaves, L.F. ; Koenraadt, C.J.M. - \ 2010
Quarterly Review of Biology 85 (2010)1. - ISSN 0033-5770 - p. 27 - 55.
anopheles-gambiae s.s. - western kenya highlands - east-african highlands - entomological inoculation rates - plasmodium-falciparum malaria - nino southern-oscillation - mosquito-borne disease - medium-sized town - mm-x traps - risk-factors
In recent decades, malaria has become established in zones at the margin of its previous distribution, especially in the highlands of East Africa. Studies in this region have sparked a heated debate over the importance of climate change in the territorial expansion of malaria, where positions range from its neglect to the reification of correlations as causes. Here, we review studies supporting and rebutting the role of climatic change as a driving force for highland invasion by malaria. We assessed the conclusions from both sides of the argument and found that evidence for the role of climate in these dynamics is robust. However, we also argue that over-emphasizing the importance of climate is misleading for setting a research agenda, even one which attempts to understand climate change impacts on emerging malaria patterns. We review alternative drivers for the emergence of this disease and highlight the problems still calling for research if the multidimensional nature of malaria is to be adequately tackled. We also contextualize highland malaria as an ongoing evolutionary process. Finally, we present Schmalhausen's law, which explains the lack of resilience in stressed systems, as a biological principle that unifies the importance of climatic and other environmental factors in driving malaria patterns across different spatio-temporal scales.
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
Optimizing odor-baited trap methods for collecting mosquitoes during the malaria season in The Gambia
Jawara, M. ; Smallegange, R.C. ; Jeffries, D. ; Nwakanma, D.C. ; Awolola, T.S. ; Knols, B.G.J. ; Takken, W. ; Conway, D.J. - \ 2009
PLoS One 4 (2009)12. - ISSN 1932-6203 - 6 p.
volatile organic-compounds - vector anopheles-gambiae - mm-x traps - carbon-dioxide - human skin - semifield conditions - molecular-forms - complex - diptera - attractiveness
Background: Baited traps are potential tools for removal or surveillance of disease vectors. To optimize the use of counterflow traps baited with human odor (nylon socks that had been worn for a single day) to capture wild mosquitoes in the Gambia, investigations were conducted at a field experimental site. Methodology/Principal Findings: Experiments employing Latin square design were conducted with a set of six huts to investigate the effects of the following on overnight mosquito trap catches: (1) placement of traps indoors or immediately outdoors, CO2 supply, and presence of a human subject in the hut; (2) trap height for collecting mosquitoes immediately outdoors; (3) height and distance from hut; (4) interaction between multiple traps around a single hut and entry of mosquitoes into huts. A total of 106,600 adult mosquitoes (9.1% Anopheles gambiae s.l., 4.0% other Anopheles species) were collected over 42 nights. The high numbers of An. gambiae s.l. and other mosquitoes collected by odor-baited traps required CO2 but were largely independent of the presence of a person sleeping in the hut or of trap placement indoors or outdoors. For outdoor collection that is considered less intrusive, traps opening 15 cm above the floor of the hut veranda were more highly effective than traps at other heights or further from the hut. There was no significant evidence of saturation or competition by the traps, with multiple traps around a hut each collecting almost as many mosquitoes as single traps and no effect on the numbers of mosquitoes entering the huts. Conclusions/Significance: The outdoor trapping protocol is convenient to compare attractiveness of different odors or synthetic chemicals to malaria vectors and other wild mosquitoes. The finding that such traps are reliably attractive in the presence or absence of a human volunteer encourages their potential development as standardised surveillance tools.
Cultured skin microbiota attracts malaria mosquitoes
Verhulst, N.O. ; Beijleveld, H. ; Knols, B.G.J. ; Takken, W. ; Schraa, G. ; Bouwmeester, H.J. ; Smallegange, R.C. - \ 2009
Malaria Journal 8 (2009). - ISSN 1475-2875 - 12 p.
gambiae-sensu-stricto - gas chromatography/mass spectrometry - volatile organic-compounds - mm-x traps - anopheles-gambiae - aedes-aegypti - axillary odor - human sweat - limburger cheese - tsetse-flies
Background - Host-seeking of the African malaria mosquito, Anopheles gambiae sensu stricto, is guided by human odours. The precise nature of the odours, and the composition of attractive blends of volatiles, remains largely unknown. Skin microbiota plays an important role in the production of human body odours. It is hypothesized that host attractiveness and selection of An. gambiae is affected by the species composition, density, and metabolic activity of the skin microbiota. A study is presented in which the production and constituency of volatile organic compounds (VOCs) by human skin microbiota is examined and the behavioural responses of An. gambiae to VOCs from skin microbiota are investigated. Methods - Blood agar plates incubated with skin microbiota from human feet or with a reference strain of Staphylococcus epidermidis were tested for their attractiveness to An. gambiae in olfactometer bioassays and indoor trapping experiments. Entrained air collected from blood agar plates incubated with natural skin microbiota or with S. epidermidis were analysed using GC-MS. A synthetic blend of the compounds identified was tested for its attractiveness to An. gambiae. Behavioural data were analysed by a ¿2-test and GLM. GC-MS results were analysed by fitting an exponential regression line to test the effect of the concentration of bacteria. Results - More An. gambiae were caught with blood agar plates incubated with skin bacteria than with sterile blood agar plates, with a significant effect of incubation time and dilution of the skin microbiota. When bacteria from the feet of four other volunteers were tested, similar effects were found. Fourteen putative attractants were found in the headspace of the skin bacteria. A synthetic blend of 10 of these was attractive to An. gambiae. Conclusions - The discovery that volatiles produced by human skin microorganisms in vitro mediate An. gambiae host-seeking behaviour creates new opportunities for the development of odour-baited trapping systems. Additionally, identification of bacterial volatiles provides a new method to develop synthetic blends, attractive to An. gambiae and possibly other anthropophilic disease vectors.
Evaluation of two counterflow traps for testing behaviour-mediating compounds for the malaria vector Anopheles gambiae s.s. under semi-field conditions in Tanzania
Schmied, W.H. ; Takken, W. ; Killeen, G.F. ; Knols, B.G.J. ; Smallegange, R.C. - \ 2008
Malaria Journal 7 (2008). - ISSN 1475-2875 - 9 p.
adult aedes-aegypti - human landing catch - mm-x traps - western kenya - field-evaluation - carbon-dioxide - essential oils - bg-sentinel - light trap - insect repellents
Background Evaluation of mosquito responses towards different trap-bait combinations in field trials is a time-consuming process that can be shortened by experiments in contained semi-field systems. Possible use of the BG Sentinel (BGS) trap to sample Anopheles gambiae s.s. was evaluated. The efficiency of this trap was compared with that of the Mosquito Magnet-X (MM-X) trap, when baited with foot odour alone or combinations of foot odour with carbon dioxide (CO2) or lemongrass as behaviour-modifying cues. Methods Female An. gambiae s.s. were released in an experimental flight arena that was placed in a semi-field system and left overnight. Catch rates for the MM-X and BGS traps were recorded. Data were analysed by fitting a generalized linear model to the (n+1) transformed catches. Results Both types of traps successfully captured mosquitoes with all odour cues used. When the BGS trap was tested against the MM-X trap in a choice assay with foot odour as bait, the BGS trap caught about three times as many mosquitoes as the MM-X trap (P = 0.002). Adding CO2 (500 ml/min) to foot odour increased the number of mosquitoes caught by 268% for the MM-X (P <0.001) and 34% (P = 0.051) for the BGS trap, compared to foot odour alone. When lemongrass leaves were added to foot odour, mosquito catches were reduced by 39% (BGS, P <0.001) and 38% (MM-X, P = 0.353), respectively. Conclusion The BGS trap shows high potential for field trials due to its simple construction and high catch rate when baited with human foot odour only. However, for rapid screening of different baits in a contained semi-field system, the superior discriminatory power of the MM-X trap is advantageous.