Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
Malaria Journal
Published in: Malaria Journal 1/2010

Open Access 01-12-2010 | Research

Sugar-fermenting yeast as an organic source of carbon dioxide to attract the malaria mosquito Anopheles gambiae

Authors: Renate C Smallegange, Wolfgang H Schmied, Karel J van Roey, Niels O Verhulst, Jeroen Spitzen, Wolfgang R Mukabana, Willem Takken

Published in: Malaria Journal | Issue 1/2010

Login to get access

Abstract

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 χ2-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.
Appendix
Available only for authorised users
Literature
1.
Gillies MT: The role of carbon dioxide in host-finding by mosquitoes (Diptera: Culicidae): a review. Bull Entomol Res. 1980, 70: 525-532. 10.1017/S0007485300007811.CrossRef
2.
Mboera LEG, Takken W: Carbon dioxide chemotropism in mosquitoes (Diptera: Culicidae) and its potential in vector surveillance and management programmes. Rev Med Vet Entomol. 1997, 85: 355-368.
3.
Dekker T, Takken W, Cardé RT: Structure of host-odour plumes influences catch of Anopheles gambiae s.s. and Aedes aegypti in a dual-choice olfactomer. Physiol Entomol. 2001, 26: 124-134. 10.1046/j.1365-3032.2001.00225.x.CrossRef
4.
Dekker T, Geier M, Cardé RT: Carbon dioxide instantly sensitizes female yellow fever mosquitoes to human skin odours. J Exp Biol. 2005, 208: 2963-2972. 10.1242/jeb.01736.CrossRefPubMed
5.
Qiu YT, Smallegange RC, ter Braak CJF, Spitzen J, Van Loon JJA, Jawara M, Milligan P, Galimard AM, Van Beek TA, Knols BGJ, Takken W: Attractiveness of MM-X traps baited with human or synthetic odor to mosquitoes (Diptera: Culicidae) in The Gambia. J Med Entomol. 2007, 44: 970-983. 10.1603/0022-2585(2007)44[970:AOMTBW]2.0.CO;2.PubMedCentralCrossRefPubMed
6.
Spitzen J, Smallegange RC, Takken W: Effect of human odours and positioning of CO2 release point on trap catches of the malaria mosquito Anopheles gambiae sensu stricto in an olfactometer. Physiol Entomol. 2008, 33: 116-122. 10.1111/j.1365-3032.2008.00612.x.CrossRef
7.
Kline DL: Traps and trapping techniques for adult mosquito control. J Am Mosq Control Assoc. 2006, 22: 490-496. 10.2987/8756-971X(2006)22[490:TATTFA]2.0.CO;2.CrossRefPubMed
8.
Kline DL: Semiochemicals, traps/targets and mass trapping technology for mosquito management. J Am Mosq Control Assoc. 2007, 23: 241-251. 10.2987/8756-971X(2007)23[241:STAMTT]2.0.CO;2.CrossRefPubMed
9.
Qiu YT, Spitzen J, Smallegange RC, Knols BGJ: Monitoring systems for adult insect pests and disease vectors. Emerging Pests and Vector-borne Diseases in Europe. Edited by: Takken W, Knols BGJ. 2007, Wageningen, Wageningen Academic Publishers, 329-354.
10.
Dekker T, Takken W: Differential responses of mosquito sibling species Anopheles arabiensis and An. quadriannulatus to carbon dioxide, a man or a calf. Med Vet Entomol. 1998, 12: 136-140. 10.1046/j.1365-2915.1998.00073.x.CrossRefPubMed
11.
Costantini C, Gibson G, Sagnon N, Della Torre A, Brady J, Coluzzi M: Mosquito responses to carbon dioxide in a west African Sudan savanna village. Med Vet Entomol. 1996, 10: 220-227. 10.1111/j.1365-2915.1996.tb00734.x.CrossRefPubMed
12.
Schmied W, Takken W, Killeen G, Knols BGJ, Smallegange RC: Evaluation of two counterflow traps for testing behaviour-mediating compounds for the malaria vector Anopheles gambiae s.s. under semi-field conditions in Tanzania. Malar J. 2008, 7: 230-10.1186/1475-2875-7-230.PubMedCentralCrossRefPubMed
13.
Jawara M, Smallegange RC, Jeffries D, Nwakanma DC, Awolola TS, Knols BGJ, Takken W, Conway DJ: Optimizing odor-baited trap methods for collecting mosquitoes during the malaria season in The Gambia. PLoS ONE. 2009, 4: e8167-10.1371/journal.pone.0008167.PubMedCentralCrossRefPubMed
14.
White GB: Anopheles gambiae complex and disease transmission in Africa. Trans R Soc Trop Med Hyg. 1974, 68: 278-299. 10.1016/0035-9203(74)90035-2.CrossRefPubMed
15.
Kline DL: Evaluation of various models of propane-powered mosquito traps. J Vector Ecol. 2002, 27: 1-7.PubMed
16.
Saitoh Y, Hattori J, Chinone S, Nihei N, Tsuda Y, Kurahashi H, Kobayashi M: Yeast-generated CO2 as a convenient source of carbon dioxide for adult mosquito sampling. J Am Mosq Control Assoc. 2004, 20: 261-264.PubMed
17.
Van Dijken JP, Weusthuis RA, Pronk JT: Kinetics of growth and sugar consumption in yeasts. Antonie van Leeuwenhoek. 1993, 63: 343-352. 10.1007/BF00871229.CrossRefPubMed
18.
Barnett JA: A history of research on yeasts 5: the fermentation pathway. Yeast. 2003, 20: 509-543. 10.1002/yea.986.CrossRefPubMed
19.
Walker G, Dijck P: Physiological and molecular responses of yeasts to the environment. Yeasts in Food and Beverages. Edited by: Querol A, Fleet GH. 2006, Berlin Heidelberg, Springer-Verlag, 111-152. full_text.CrossRef
20.
Hazelwood LA, Daran J-M, van Maris AJA, Pronk JT, Dickinson JR: The Ehrlich pathway for fusel alcohol production: a century of research on Saccharomyces cerevisiae metabolism. Appl Environ Microbiol. 2008, 74: 2259-2266. 10.1128/AEM.02625-07.PubMedCentralCrossRefPubMed
21.
Kline DL: Comparison of two American biophysics mosquito traps: the professional and a new counterflow geometry trap. J Am Mosq Control Assoc. 1999, 15: 276-282.PubMed
22.
Cooperband MF, Cardé RT: Comparison of plume structures of carbon dioxide emitted from different mosquito traps. Med Vet Entomol. 2006, 20: 1-10. 10.1111/j.1365-2915.2006.00614.x.CrossRefPubMed
23.
Cooperband MF, Cardé RT: Orientation of Culex mosquitoes to carbon dioxide-baited traps: flight manoeuvres and trapping efficiency. Med Vet Entomol. 2006, 20: 11-26. 10.1111/j.1365-2915.2006.00613.x.CrossRefPubMed
24.
Knols B, Njiru B, Mathenge E, Mukabana W, Beier J, Killeen G: MalariaSphere: A greenhouse-enclosed simulation of a natural Anopheles gambiae (Diptera: Culicidae) ecosystem in western Kenya. Malar J. 2002, 1: 19-10.1186/1475-2875-1-19.PubMedCentralCrossRefPubMed
25.
Sudia WD, Chamberlain RW: Battery-operated light trap, an improved model. By W. D. Sudia and R. W. Chamberlain, 1962. J Am Mosq Control Assoc. 1988, 4: 536-538.PubMed
26.
De Jong R, Knols BGJ: Selection of biting sites on man by two malaria mosquito species. Cell Mol Life Sciences (CMLS). 1995, 51: 80-84. 10.1007/BF01964925.CrossRef
27.
Pates H, Takken W, Stuke K, Curtis CF: Differential behaviour of Anopheles gambiae sensu stricto (Diptera: Culicidae) to human and cow odours in the laboratory. Bull Entomol Res. 2001, 91: 289-296.CrossRefPubMed
28.
Qiu YT, Smallegange RC, Hoppe S, van Loon JJA, Bakker EJ, Takken W: Behavioural and electrophysiological responses of the malaria mosquito Anopheles gambiae Giles sensu stricto (Diptera: Culicidae) to human skin emanations. Med Vet Entomol. 2004, 18: 429-438. 10.1111/j.0269-283X.2004.00534.x.CrossRefPubMed
29.
Njiru B, Mukabana W, Takken W, Knols B: Trapping of the malaria vector Anopheles gambiae with odour-baited MM-X traps in semi-field conditions in western Kenya. Malar J. 2006, 5: 39-10.1186/1475-2875-5-39.PubMedCentralCrossRefPubMed
30.
Smallegange RC, Takken W: Host-seeking behaviour of mosquitoes: responses to olfactory stimuli in the laboratory. Olfaction in vector-host interactions. Edited by: Takken W, Knols BGJ. 2010, Wageningen, Wageningen Academic Publishers, 143-180.
31.
Haddow AJ, Ssenkubuge Y: The mosquito of bwamba county, Uganda. IX. Further studies on the biting behaviour of an outdoor population of the Anopheles gambiae Giles complex. Bull Entomol Res. 1973, 62: 407-414. 10.1017/S0007485300003928.CrossRef
32.
Maxwell C, Wakibara J, Tho S, Curtis C: Malaria-infective biting at different hours of the night. Med Vet Entomol. 1998, 12: 325-327. 10.1046/j.1365-2915.1998.00108.x.CrossRefPubMed
33.
Killeen G, Kihonda J, Lyimo E, Oketch F, Kotas M, Mathenge E, Schellenberg J, Lengeler C, Smith T, Drakeley C: Quantifying behavioural interactions between humans and mosquitoes: Evaluating the protective efficacy of insecticidal nets against malaria transmission in rural Tanzania. BMC Infect Dis. 2006, 6: 161-10.1186/1471-2334-6-161.PubMedCentralCrossRefPubMed
34.
Snow WF: Studies of house-entering habits of mosquitoes in The Gambia, West Africa: experiments with prefabricated huts with varied wall apertures. Med Vet Entomol. 1987, 1: 9-21. 10.1111/j.1365-2915.1987.tb00318.x.CrossRefPubMed
35.
Njie M, Dilger E, Lindsay SW, Kirby MJ: Importance of eaves to house entry by anopheline, but not culicine, mosquitoes. J Med Entomol. 2009, 46: 505-510. 10.1603/033.046.0314.CrossRefPubMed
36.
Mboera L, Kihonda J, Braks M, Knols B: Short report: Influence of centers for disease control light trap position, relative to a human-baited bed net, on catches of Anopheles gambiae and Culex quinquefasciatus in Tanzania. Am J Trop Med Hyg. 1998, 59: 595-596.PubMed
37.
Minakawa N, Mutero C, Githure J, Beier J, Yan G: Spatial distribution and habitat characterization of anopheline mosquito larvae in Western Kenya. Am J Trop Med Hyg. 1999, 61: 1010-1016.PubMed
38.
Minakawa N, Seda P, Yan G: Influence of host and larval habitat distribution on the abundance of African malaria vectors in western Kenya. Am J Trop Med Hyg. 2002, 67: 32-38.PubMed
39.
Takken W, Geene R, Adam W, Jetten TH, van der Velden JA: Distribution and dynamics of larval populations of Anopheles messeae and A. atroparvus in the delta of the rivers Rhine and Meuse, The Netherlands. Ambio. 2002, 31: 212-218.CrossRefPubMed
40.
Scott JA, Brogdon WG, Collins FH: Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. Am J Trop Med Hyg. 1993, 4: 520-529.
41.
Kirby MJ, Ameh D, Bottomley C, Green C, Jawara M, Milligan PJ, Snell PC, Conway DJ, Lindsay SW: Effect of two different house screening interventions on exposure to malaria vectors and on anaemia in children in The Gambia: a randomised controlled trial. The Lancet. 2009, 374: 998-1009. 10.1016/S0140-6736(09)60871-0.CrossRef
42.
Okumu FO, Killeen GF, Ogoma S, Biswaro L, Smallegange RC, Mbeyela E, Titus E, Munk C, Ngonyani H, Takken W, Hassan M, Mukabana WR, Moore SJ: Development and field evaluation of a synthetic mosquito lure that is more attractive than humans. PLoS ONE. 2010, 5: e8951-10.1371/journal.pone.0008951.PubMedCentralCrossRefPubMed
43.
Qiu YT: Sensory and behavioural responses of the malaria mosquito Anopheles gambiae to human odours. PhD thesis. 2005, Wageningen University, Laboratory of Entomology
44.
Smallegange RC, Qiu YT, van Loon JJA, Takken W: 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). Chem Senses. 2005, 30: 145-152. 10.1093/chemse/bji010.CrossRefPubMed
45.
Smallegange RC, Qiu YT, Bukovinszkine-Kiss G, Van Loon JJA, Takken W: The effect of aliphatic carboxylic acids on olfaction-based host-seeking of the malaria mosquito Anopheles gambiae sensu stricto. J Chem Ecol. 2009, 35: 933-943. 10.1007/s10886-009-9668-7.PubMedCentralCrossRefPubMed
46.
Verhulst N, Beijleveld H, Knols B, Takken W, Schraa G, Bouwmeester H, Smallegange R: Cultured skin microbiota attracts malaria mosquitoes. Malar J. 2009, 8: 302-10.1186/1475-2875-8-302.PubMedCentralCrossRefPubMed
47.
Murlis J, Jones CD: Fine-scale structure of odour plumes in relation to insect orientation to distant pheromone and other attractant sources. Physiol Entomol. 1981, 6: 71-86. 10.1111/j.1365-3032.1981.tb00262.x.CrossRef
48.
Voskamp KE: Electroantennogram responses of tsetse flies (Glossina pallidipes) to host odours in an open field and riverine woodland. Physiol Entomol. 1998, 23: 176-183. 10.1046/j.1365-3032.1998.232070.x.CrossRef
49.
Murlis J, Willis MA, Cardé RT: Spatial and temporal structures of pheromone plumes in fields and forests. Physiol Entomol. 2000, 25: 211-222. 10.1046/j.1365-3032.2000.00176.x.CrossRef
50.
Cardé RT, Willis MA: Navigational strategies used by insects to find distant, wind-borne sources of odor. J Chem Ecol. 2008, 34: 854-866. 10.1007/s10886-008-9484-5.CrossRefPubMed
51.
Grant AJ, Aghajanian JG, O'Connell RJ, Wigton BE: Electrophysiological responses of receptor neurons in mosquito maxillary palp sensilla to carbon dioxide. J Comp Physiol A: Neuroethology, Sensory, Neural, and Behavioral Physiol. 1995, 177: 389-396.CrossRef
52.
Cardé RT, Gibson G: Host finding by female mosquitoes: Mechanisms of orientation to host odours and other cues. Olfaction in vector-host interactions. Edited by: Takken W, Knols BGJ. 2010, Wageningen, Wageningen Academic Publishers, 115-142.
53.
Oli K, Jeffery J, Vythilingam I: A comparative study of adult mosquito trapping using dry ice and yeast generated carbon dioxide. Trop Biomed. 2005, 22: 249-251.PubMed
54.
Ellin RI, Farrand RL, Oberst FW, Crouse CL, Billups NB, Koon WS, Musselman NP, Sidell FR: An apparatus for the detected and quantitation of volatile human effluents. J Chromatogr A. 1974, 100: 137-152. 10.1016/S0021-9673(00)86048-3.CrossRef
55.
Meijerink J, Braks MAH, Brack AA, Adam W, Dekker T, Posthumus MA, Van Beek TA, Van Loon JJA: Identification of Olfactory Stimulants for Anopheles gambiae from Human Sweat Samples. J Chem Ecol. 2000, 26: 1367-1382. 10.1023/A:1005475422978.CrossRef
56.
Deng C, Zhang X, Li N: Investigation of volatile biomarkers in lung cancer blood using solid-phase microextraction and capillary gas chromatography-mass spectrometry. J Chromatogr B. 2004, 808: 269-277. 10.1016/j.jchromb.2004.05.015.CrossRef
57.
Bernier UR, Kline DL, Barnard DR, Schreck CE, Yost RA: Analysis of human skin emanations by gas chromatography/mass spectrometry. 2. Identification of volatile compounds that are candidate attractants for the yellow fever mosquito (Aedes aegypti). Anal Chem. 2000, 72: 747-756. 10.1021/ac990963k.CrossRefPubMed
58.
Bernier UR, Booth MM, Yost RA: Analysis of human skin emanations by gas chromatography/mass spectrometry. 1. Thermal desorption of attractants for the yellow fever mosquito (Aedes aegypti) from handled Glass beads. Anal Chem. 1999, 71: 1-7. 10.1021/ac980990v.CrossRefPubMed
59.
Savelev SU, Antony-Babu S, Roberts SC, Wang H, Clare AS, Gosling LM, Petrie M, Goodfellow M, O'Donnell AG, Ward AC: Individual variation in 3-methylbutanal: A putative link between human leukocyte antigen and skin microflora. J Chem Ecol. 2008, 34: 1253-1257. 10.1007/s10886-008-9524-1.CrossRefPubMed
60.
Perry TL, Hansen S, Diamond S, Bullis B, Mok C, Melancon SB: Volatile fatty acids in normal human physiological fluids. Clin Chim Acta. 1970, 29: 369-374. 10.1016/0009-8981(70)90004-5.CrossRefPubMed
61.
Healy TP, Copland MJW: Human sweat and 2-oxopentanoic acid elicid a landing response from Anopheles gambiae. Med Vet Entomol. 2000, 14: 195-200. 10.1046/j.1365-2915.2000.00238.x.CrossRefPubMed
62.
Gallagher M, Wysocki CJ, Leyden JJ, Spielman AI, Sun X: Analyses of volatile organic compounds from human skin. Br J Dermatol. 2008, 159: 780-791. 10.1111/j.1365-2133.2008.08748.x.PubMedCentralCrossRefPubMed
63.
Penn DJ, Oberzaucher E, Grammer K, Fischer G, Soini HA, Wiesler D, Novotny MV, Dixon SJ, Xu Y, Brereton RG: Individual and gender fingerprints in human body odour. J R Soc Interface. 2007, 4: 331-340. 10.1098/rsif.2006.0182.PubMedCentralCrossRefPubMed
Metadata
Title
Sugar-fermenting yeast as an organic source of carbon dioxide to attract the malaria mosquito Anopheles gambiae
Authors
Renate C Smallegange
Wolfgang H Schmied
Karel J van Roey
Niels O Verhulst
Jeroen Spitzen
Wolfgang R Mukabana
Willem Takken
Publication date
01-12-2010
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2010
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-9-292

Other articles of this Issue 1/2010

Malaria Journal 1/2010 Go to the issue

Research

Immunoglobulin GM 3 23 5,13,14 phenotype is strongly associated with IgG1 antibody responses to Plasmodium vivax vaccine candidate antigens PvMSP1-19 and PvAMA-1

Research

Efficacy of an insecticide paint against malaria vectors and nuisance in West Africa - Part 2: Field evaluation

Case study

Using the social entrepreneurship approach to generate innovative and sustainable malaria diagnosis interventions in Tanzania: a case study

Research

Apoptosis of non-parasitized red blood cells in malaria: a putative mechanism involved in the pathogenesis of anaemia

Research

Using the entomological inoculation rate to assess the impact of vector control on malaria parasite transmission and elimination

Review

Anti-folate drug resistance in Africa: meta-analysis of reported dihydrofolate reductase (dhfr) and dihydropteroate synthase (dhps) mutant genotype frequencies in African Plasmodium falciparum parasite populations
Obesity Clinical Trial Summary

At a glance: The STEP trials

Read more

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Pediatric Cardiology Video

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

Cardiopulmonary Comorbidity Video

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Valvular Heart Disease Video

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.

Watch now

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits