- U. Groenhagen (1)
- B.G.J. Knols (1)
- J.Y. Kwon (1)
- H.W. Kwon (1)
- J.J.A. Loon van (6)
- T. Lu (1)
- P.A. Mbadi (1)
- J. Meijerink (1)
- W.R. Mukabana (2)
- R.J. Pitts (1)
- Y.T. Qiu (3)
- K.J. Roey van (1)
- J.P. Rospars (1)
- M. Rutzler (1)
- W.H. Schmied (1)
- G. Schraa (1)
- S. Schulz (1)
- R.C. Smallegange (5)
- H.M. Smid (1)
- J. Spitzen (1)
- W. Takken (8)
- A. Torricelli (1)
- N.O. Verhulst (3)
- Q. Wang (1)
- L.J. Zwiebel (1)
Effects of blood-feeding on olfactory sensitivity of the malaria mosquito Anopheles gambiae: application of mixed linear models to account for repeated measurements
Qiu, Y.T. ; Gort, G. ; Torricelli, A. ; Takken, W. ; Loon, J.J.A. van - \ 2013
Journal of Insect Physiology 59 (2013). - ISSN 0022-1910 - p. 1111 - 1118.
l-lactic acid - host-seeking behavior - human-sweat - diptera-culicidae - aedes-aegypti - sensu-stricto - electrophysiological responses - limburger cheese - odor - receptors
Olfaction plays an important role in the host-seeking behavior of the malaria mosquito Anopheles gambiae. After a complete blood meal, female mosquitoes will not engage in host-seeking behavior until oviposition has occurred. We investigated if peripheral olfactory sensitivity changed after a blood meal by recording electroantennograms (EAGs) of female mosquitoes at three time points (2h, 48 h and 72 h) to 15 volatile kairomones of either human origin or documented to emanate from oviposition sites. The EAG-sensitivity was compared with that of females of similar age post eclosion. As is common practice in electrophysiological studies, the EAG recordings were obtained by repeated stimulation of the same antennal preparations. We introduce mixed linear modeling as an improved statistical analysis for electrophysiological data. Two hours after blood ingestion, olfactory sensitivity as quantified through EAG-recording increased significantly and selectively, i.e. for seven compounds, compared to unfed females of the same age. Such short-term electrophysiological sensitization in the olfactory system as a result of feeding has not been documented before for insects. Sensitization to six compounds persisted until 48 h or 72 h post-blood meal at one or more concentrations. Desensitization was observed at 48 and 72 h pbm in response to two and three kairomones, respectively. For several compounds, sensitization at the EAG-level corresponded with sensitization found previously in single sensillum studies on olfactory neurons in antennal sensilla trichodea of An. gambiae females. These effects are likely to reflect sensitization to oviposition cues, as eggs have matured 48-72 h pbm. Knowledge of changes in olfactory sensitivity to kairomones can be applied to increase trap catches of malaria mosquitoes that have taken a blood meal and need to locate oviposition sites.
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.
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
Differential attraction of malaria mosquitoes to volatile blends produced by human skin bacteria
Verhulst, N.O. ; Andriessen, R. ; Groenhagen, U. ; Bukovinszkine-Kiss, G. ; Schulz, S. ; Takken, W. ; Loon, J.J.A. van; Schraa, G. ; Smallegange, R.C. - \ 2010
PLoS One 5 (2010)12. - ISSN 1932-6203 - 9 p.
gambiae-sensu-stricto - human axillary odor - l-lactic acid - anopheles-gambiae - aedes-aegypti - pseudomonas-aeruginosa - diptera-culicidae - electrophysiological responses - pyruvate fermentation - oviposition responses
The malaria mosquito Anopheles gambiae sensu stricto is mainly guided by human odour components to find its blood host. Skin bacteria play an important role in the production of human body odour and when grown in vitro, skin bacteria produce volatiles that are attractive to A. gambiae. The role of single skin bacterial species in the production of volatiles that mediate the host-seeking behaviour of mosquitoes has remained largely unknown and is the subject of the present study. Headspace samples were taken to identify volatiles that mediate this behaviour. These volatiles could be used as mosquito attractants or repellents. Five commonly occurring species of skin bacteria were tested in an olfactometer for the production of volatiles that attract A. gambiae. Odour blends produced by some bacterial species were more attractive than blends produced by other species. In contrast to odours from the other bacterial species tested, odours produced by Pseudomonas aeruginosa were not attractive to A. gambiae. Headspace analysis of bacterial volatiles in combination with behavioural assays led to the identification of six compounds that elicited a behavioural effect in A. gambiae. Our results provide, to our knowledge, the first evidence for a role of selected bacterial species, common on the human skin, in determining the attractiveness of humans to malaria mosquitoes. This information will be used in the further development of a blend of semiochemicals for the manipulation of mosquito behaviour.
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
Odor coding in the maxillary palp of the malaria vector mosquito Anopheles gambiae
Lu, T. ; Qiu, Y.T. ; Wang, Q. ; Kwon, J.Y. ; Rutzler, M. ; Kwon, H.W. ; Pitts, R.J. ; Loon, J.J.A. van; Takken, W. ; Carlson, J.R. ; Zwiebel, L.J. - \ 2007
Current Biology 17 (2007)18. - ISSN 0960-9822 - p. 1533 - 1544.
carbon-dioxide - drosophila-antenna - electrophysiological responses - behavioral-responses - receptor neurons - molecular-basis - sex-pheromone - olfaction - sensilla - culicidae
Background: Many species of mosquitoes, including the major malaria vector Anopheles gambiae, utilize carbon dioxide (CO2) and 1-octen-3-ol as olfactory cues in host-seeking behaviors that underlie their vectorial capacity. However, the molecular and cellular basis of such olfactory responses remains largely unknown. Results: Here, we use molecular and physiological approaches coupled with systematic functional analyses to define the complete olfactory sensory map of the An. gambiae maxillary palp, an olfactory appendage that mediates the detection of these compounds. In doing so, we identify three olfactory receptor neurons (ORNs) that are organized in stereotyped triads within the maxillary-palp capitate-peg-sensillum population. One ORN is CO2-responsive and characterized by the coexpression of three receptors that confer CO2 responses, whereas the other ORNs express characteristic odorant receptors (AgORs) that are responsible for their in vivo olfactory responses. Conclusions: Our results describe a complete and highly concordant map of both the molecular and cellular olfactory components on the maxillary palp of the adult female An. gmnbiae mosquito. These results also facilitate the understanding of how An. gambiae mosquitoes sense olfactory cues that might be exploited to compromise their ability to transmit malaria.
Central projections of olfactory receptor neurons from single antennal and palpal sensilla in mosquitoes
Anton, S. ; Loon, J.J.A. van; Meijerink, J. ; Smid, H.M. ; Takken, W. ; Rospars, J.P. - \ 2003
Arthropod Structure & Development 32 (2003). - ISSN 1467-8039 - p. 319 - 327.
aedes-aegypti - anopheles-gambiae - malaria mosquito - lactic-acid - drosophila-melanogaster - maxillary palp - electrophysiological responses - manduca-sexta - sensory map - fly brain
In insects, olfactory receptor neurons (ORNs) are located in cuticular sensilla, that are present on the antennae and on the maxillary palps. Their axons project into spherical neuropil, the glomeruli, which are characteristic structures in the primary olfactory center throughout the animal kingdom. ORNs in insects often respond specifically to single odor compounds. The projection patterns of these neurons within the primary olfactory center, the antennal lobe, are, however, largely unknown. We developed a method to stain central projections of intact receptor neurons known to respond to host odor compounds in the malaria mosquito, Anopheles gambiae. Terminal arborizations from ORNs from antennal sensilla had only a few branches apparently restricted to a single glomerulus. Axonal arborizations of the different neurons originating from the same sensillum did not overlap. ORNs originating from maxillary palp sensilla all projected into a dorso-medial area in both the ipsi- and contralateral antennal lobe, which received in no case axon terminals from antennal receptor neurons. Staining of maxillary palp receptor neurons in a second mosquito species (Aedes aegypti) revealed unilateral arborizations in an area at a similar position as in An. gambiae. (C) 2003 Elsevier Ltd. All rights reserved.