Identification of Human-Derived Volatile Chemicals that Interfere with Attraction of Aedes aegypti Mosquitoes

  • James G. Logan
  • Michael A. Birkett
  • Suzanne J. Clark
  • Stephen Powers
  • Nicola J. Seal
  • Lester J. Wadhams
  • A. Jennifer Mordue (Luntz)
  • John A. PickettEmail author


It is known that human individuals show different levels of attractiveness to mosquitoes. In this study, we investigated the chemical basis for low attractiveness. We recorded behaviors of Aedes aegypti toward the hands of human volunteers and toward the volatile chemicals produced by their bodies. Some individuals, and their corresponding volatiles, elicited low upwind flight, relative attraction, and probing activity. Analyzing the components by gas chromatography coupled to electrophysiological recordings from the antennae of Aedes aegypti, enabled the location of 33 physiologically relevant compounds. The results indicated that higher levels of specific compounds may be responsible for decreased “attractiveness.” In behavioral experiments, five of the compounds caused a significant reduction in upwind flight of Aedes aegypti to attractive human hands. Thus, unattractiveness of individuals may result from a repellent, or attractant “masking,” mechanism.


Mosquito Differential attraction Semiochemical Attractant “masking” effect 



J. G. Logan was supported by a BBSRC Studentship. We thank all the volunteers who participated in this study and Lifesystems™ for providing the foil bags. This study was approved by the Bedfordshire and Hertfordshire Strategic Health Authority Local Research Ethics Committee, UK (Reference number: EC03652), and informed consent was obtained from all volunteers. Rothamsted receives grant-aided support from the BBSRC. We also thank Professor Lin Field for her helpful comments on this manuscript.


  1. Acree, F. Jr., Turner, R. B., Gouck, H. K., Beroza, M., and Smith, N. 1968. L-Lactic acid—a mosquito attractant isolated from humans. Science 161:1346.PubMedCrossRefGoogle Scholar
  2. Allan, S. A., Day, J. F., and Edman, J. D. 1987. Visual ecology of biting flies. Annu. Rev. Entomol. 32:297–316.PubMedCrossRefGoogle Scholar
  3. Bernier, U. R., Kline, D. L., Barnard, D. R., Schreck, C. E., and Yost, R. A. 2000. 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. 72:747.PubMedCrossRefGoogle Scholar
  4. Bernier, U., Kline, D. L., Schreck, C. E., Yost, R. A., and Barnard, D. R. 2002. Chemical analysis of human skin emanations: comparison of volatiles from humans that differ in attraction of Aedes aegypti (Diptera: Culicidae). J. Am. Mosq. Control Assoc. 18:186.PubMedGoogle Scholar
  5. Bernier, U. R., Kline, D. L., Posey, K. H., Booth, M. M., Yost, R. A., and Barnard, D. R. 2003. Synergistic attraction of Aedes aegypti (L.) to binary blends of L-lactic acid and acetone, dichloromethane, or dimethyl disulfide. J. Med. Entomol. 40:653–656.PubMedCrossRefGoogle Scholar
  6. Besansky, N. J., Hill, C. A., and Costantini, C. 2004. No accounting for taste: host preference in malaria vectors. Trends Parasitol. 20:249–251.PubMedCrossRefGoogle Scholar
  7. Bhasin, A., Mordue (Luntz), A. J., and Mordue, W. 2000. Responses of the biting midge Culicoides impunctatus to acetone, CO2 and 1-octen-3-ol in a wind tunnel. Med. Vet. Entomol. 14:300–307.PubMedCrossRefGoogle Scholar
  8. Bhasin, A., Mordue (Luntz), A. J., and Mordue, W. 2001. Field studies on efficacy of host odour baits for the biting midge Culicoides impunctatus in Scotland. Med. Vet. Entomol. 15:147–156.PubMedCrossRefGoogle Scholar
  9. Birkett, M. A., Agelopoulos, N., Jensen, V., Jespersen, M. B., Pickett, J. J. A., Prijs, J., Trapman, H. T. G. J., Wadhams, J. L. J., and Woodcock, C. M. 2004. The role of volatile semiochemicals in mediating host location and selection by nuisance and disease-transmitting cattle flies. Med. Vet. Entomol. 18:313–322.PubMedCrossRefGoogle Scholar
  10. Brady, J., Costantini, C., Sagnon, N., Gibson, G., and Coluzzi, M. 1997. The role of body odours in the relative attractiveness of different men to malarial vectors in Burkina Faso. Ann. Trop. Med. Parasitol. 91:121.CrossRefGoogle Scholar
  11. Braks, M. A. H., and Takken, W. 1999. Incubated human sweat but not fresh sweat attracts the malaria mosquito Anopheles gambiae sensu stricto. J. Chem. Ecol. 25:663–672.CrossRefGoogle Scholar
  12. Braks, M. A. H., Meijerink, J., and Takken, W. 2001. The response of the malaria mosquito, Anopheles gambiae, to two components of human sweat, ammonia and L-lactic acid, in an olfactometer. Physiol. Entomol. 26:142–148.CrossRefGoogle Scholar
  13. Brouwer, R. 1960. Variations in human body odour as a cause of individual differences of attraction for malaria mosquitoes. Trop. Geogr. Med. 12:186.Google Scholar
  14. Burkot, T. R. 1988. Non-random host selection by Anopheline mosquitoes. Parasitol. Today 4:156.PubMedCrossRefGoogle Scholar
  15. Cork, A., and Park, K. C. 1996. Identification of electrophysiologically-active compounds for the malaria mosquito, Anopheles gambiae, in human sweat extracts. Med. Vet. Entomol. 10:269–276.PubMedCrossRefGoogle Scholar
  16. Costantini, C., Gibson, G., and Coluzzi, M. 1997. The role of body odours in the relative attractiveness of different men to malarial vectors in Burkino Faso. Ann. Trop. Med. Parasitol. 91:s121–s122.CrossRefGoogle Scholar
  17. Costantini, C., Sagnon, N., Dellatorre, A., Diallo, M., Brady, J., Gibson, G., and Coluzzi, M. 1998. Odor-mediated host preferences of West African mosquitoes, with particular reference to malaria vectors. Am. J. Trop. Med. Hyg. 58:56–63.PubMedGoogle Scholar
  18. Costantini, C., Birkett, M. A., Gibson, G., Ziesmann, J., Sagnon, N. F., Mohammed, H. A., Coluzzi, M., and Pickett, J. A. 2001. Electroantennogram and behavioural responses of the malaria vector Anopheles gambiae to human-specific sweat components. Med. Vet. Entomol. 15:259–266.PubMedCrossRefGoogle Scholar
  19. Curran, A. M., Rabin, S. I., Prada, P. A., and Furton, K. G. 2005. Comparison of the volatile organic compounds present in human odor using SPME-GC-MS. J. Chem. Ecol. 31:1607–1619.PubMedCrossRefGoogle Scholar
  20. Dekker, T., Takken, W., and Cardé, R. T. 2001. Structure of host-odour plumes influences catch of Anopheles gambiae s.s. and Aedes aegypti in a dual-choice olfactometer. Physiol. Entomol. 26:124–134.CrossRefGoogle Scholar
  21. Dekker, T., Geir, M., and Cardé, R. T. 2005. Carbon dioxide instantly sensitizes female yellow fever mosquitoes to human skin odours. J. Exp. Biol. 208:293–2972.CrossRefGoogle Scholar
  22. Douglas, H. D., Co, J. E., Jones, T. H., Conner, W. E., and Day, J. F. 2005. Chemical odorant of colonial seabird repels mosquitoes. J. Med. Entomol. 42:647–651.PubMedCrossRefGoogle Scholar
  23. Eiras, A. E., and Jepson, P. C. 1994. Responses of female Aedes aegypti (Diptera: Culicidae) to host odors and convection currents using an olfactometer bioassay. Bull. Entomol. Res. 84:207–211.CrossRefGoogle Scholar
  24. Freyvogel, T. A. 1961. Ein Beitrag zu den Problemen um die Blutmahlzeit von Stechmücken. Acta Trop. 18:201–251.PubMedGoogle Scholar
  25. Geier, M., and Boeckh 1999. A new Y-tube olfactometer for mosquitoes to measure the attractiveness of host odours. J. Entomol. Exp. Appl. 92:9.CrossRefGoogle Scholar
  26. Geier, M., Sass, H., and Boeckh, J. 1996. A search for components in human body odour that attract females of Aedes aegypti. Ciba F Symp. 200:132–148.Google Scholar
  27. Gikonyo, N. K., Hassanali, A., Njagi, P. G. N., Gitu, P. M., and Midiwo, J. O. 2002. Odor composition of preferred (buffalo and ox) and nonpreferred (waterbuck) hosts of some savanna tsetse flies. J. Chem. Ecol. 28:969–981.PubMedCrossRefGoogle Scholar
  28. Gikonyo, N. K., Hassanali, A., Njagi, P. G. N., and Saini, R. K. 2003. Responses of Glossina morsitans morsitans to blends of electroantennographically active compounds in the odors of its preferred (buffalo and ox) and nonpreferred (waterbuck) hosts. J. Chem. Ecol. 29:2331–2345.PubMedCrossRefGoogle Scholar
  29. Hamilton, J. G. C., and Ramsoondar, T. M. C. 1994. Attraction of Lutzomyia longipalpis to human skin odors. Med. Vet. Entomol. 8:375–380.PubMedCrossRefGoogle Scholar
  30. Healy, T. P., Copland, M. J. W., Cork, A., Przyborowska, A., and Halket, J. M. 2002. Landing responses of Anopheles gambiae elicited by oxocarboxylic acids. Med. Vet. Entomol. 16:126–132.PubMedCrossRefGoogle Scholar
  31. Jensen, K. M. V., Jespersen, J. B., Birkett, M. A., Pickett, J. A., Thomas, G., Wadhams, L. J., and Woodcock, C. M. 2004. Variation in the load of the horn fly, Haematobia irritans, in cattle herds is determined by the presence or absence of individual heifers. J. Med. Entomol. 18:275–280.CrossRefGoogle Scholar
  32. Khan, A. A., Maibach, H. I., Strauss, W. G., and Fenley, W. R. 1966. Quantitation of effect of several stimuli on approach of Aedes aegypti. J. Econ. Entomol. 59:690.PubMedGoogle Scholar
  33. Khan, A. A., Maibach, H. I., and Strauss, W. G. 1968. Role of convection currents in mosquito attraction to human skin. Mosq. News 28:462–464.Google Scholar
  34. Kline, D. L., Takken, W., Wood, J. R., and Carlson, D. A. 1990. Field studies on the potential of butanone, carbon-dioxide, honey extract, 1-octen-3-ol, L-lactic acid and phenols as attractants for mosquitoes. Med. Vet. Entomol. 4:383–391.PubMedCrossRefGoogle Scholar
  35. Lindsay, S. W., Adiamah, J. H., Miller, J. E., Pleass, R. J., and Armstrong, J. R. 1993. Variation in attractiveness of human-subjects to malaria mosquitoes (Diptera: Culicidae) in the Gambia. J. Med. Entomol. 30:368–373.PubMedGoogle Scholar
  36. Logan, J. G. 2006. Differential responses of the yellow fever mosquito, Aedes aegypti and the Scottish biting midge, Culicoides impunctatus to human host odours. PhD dissertation, Rothamsted Research and University of Aberdeen.Google Scholar
  37. Mayer, M. S., and James, J. D. 1969. Attraction of Aedes aegypti (L)—responses to human arms carbon dioxide and air currents in a new type of olfactometer. B. Entomol. Res. 58:629.CrossRefGoogle Scholar
  38. Pickett, J., Wadhams, L. J., and Woodcock, C. M. 1998. Mate and host location by insect model systems for exploiting olfactory interactions. The Biochemist, August, 8–13.Google Scholar
  39. Qiu, Y. T., Smallegange, R. C., Hoppe, S., Van, Loon, J. J., Bakker, E. J., and Takken, W. Y. T. 2004. Behavioural and electrophysiological responses of the malaria mosquito Anopheles gambiae Giles sensu stricto (Diptera: Culicidae) to human skin emanations. Med. Vet. Entomol. 18:429.PubMedCrossRefGoogle Scholar
  40. Quiroz, A., Pettersson, J., Pickett, J. A., Wadhams, L. J., and Niemeyer, H. M. 1997. Semiochemicals mediating spacing behavior of bird cherry-oat aphid, Rhopalosiphum padi feeding on cereals. J. Chem. Ecol. 23:2599–2607.CrossRefGoogle Scholar
  41. Sastry, S. D., Buck, K. T., Janak, J., Dressler, M., and Preti, G. 1980. Volatiles emitted by humans. In Biochemical Applications of Mass Spectrometry. Wiley, New York.Google Scholar
  42. Schofield, S. W., and Sutcliffe, J. F. 1996. Human individuals vary in attractiveness for host-seeking black flies (Diptera: Simuliidae) based on exhaled carbon dioxide. J. Med. Entomol. 33:102–108.PubMedGoogle Scholar
  43. Schreck, C. E., Smith, N., Carlson, D. A., Price, G. D., Haile, D., and Godwin, D. R. 1981. A material isolated from human hands that attracts female mosquitoes. J. Chem. Ecol. 8:429–438.CrossRefGoogle Scholar
  44. Schreck, C. E., Kline, D. L., and Carlson, D. A. 1990. Mosquito attraction to substances from the skin of different humans. J. Am. Mosq. Control Assoc. 6:406–410.PubMedGoogle Scholar
  45. Steelman, C. D., Gbur, E. E., Tolley, G., and Brown, A. H. 1993. Individual variation within breeds of beef-cattle in resistance to horn fly (Diptera: Muscidae). J. Med. Entomol. 30:414–420.PubMedGoogle Scholar
  46. Steib, B. M., Geier, M., and Boeckh, J. 2001. The effect of lactic acid on odour-related host preference of yellow fever mosquitoes. Chem. Senses 26:523–528.PubMedCrossRefGoogle Scholar
  47. Takken, W. 1991. The role of olfaction in host-seeking of mosquitoes - a review. Insect Sci. Appl. 12:287–295.Google Scholar
  48. Takken, W., and Knols, B. G. J. 1999. Odor-mediated behavior of Afrotropical malaria mosquitoes. Annu. Rev. Entomol. 44:131–157.PubMedCrossRefGoogle Scholar
  49. Wood, W. F., and Weldon, P. J. 2002. The scent of the reticulated giraffe (Giraffa camelopardalis reticulata). Biochem. Sys. Ecol. 30:913–917.CrossRefGoogle Scholar
  50. Zar, J. H. 1984. Biostatistical Analysis. Prentice Hall, New Jersey.Google Scholar
  51. Zeng, X. N., Leyden, J. J., Lawley, H. J., Sawano, K., Nohara, I., and Preti, G. 1991. Analysis of characteristic odors from human male axillae. J. Chem. Ecol. 17:1469–1492.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • James G. Logan
    • 1
  • Michael A. Birkett
    • 1
  • Suzanne J. Clark
    • 1
  • Stephen Powers
    • 1
  • Nicola J. Seal
    • 2
  • Lester J. Wadhams
    • 1
  • A. Jennifer Mordue (Luntz)
    • 2
  • John A. Pickett
    • 1
    Email author
  1. 1.Rothamsted ResearchHertfordshireUK
  2. 2.School of Biological SciencesUniversity of AberdeenAberdeenUK

Personalised recommendations