Journal of Chemical Ecology

, Volume 36, Issue 7, pp 709–719

Oviposition Responses of the Mosquitoes Aedes aegypti and Aedes albopictus to Experimental Plant Infusions in Laboratory Bioassays

  • Loganathan Ponnusamy
  • Ning Xu
  • Katalin Böröczky
  • Dawn M. Wesson
  • Luma Abu Ayyash
  • Coby Schal
  • Charles S. Apperson
Article

Abstract

Attraction of the mosquitoes Aedes aegypti and Ae. albopictus to plant infusions was evaluated by using a modified sticky-screen bioassay that improved the resolution of mosquito responses to odorants. Under bioassay conditions, solid-phase microextraction-gas chromatographic analyses of the volatile marker chemical indole showed that odorants diffused from bioassay cups, forming a concentration gradient. Infusions were prepared by separately fermenting senescent leaves of eight plant species in well water. Plant infusions were evaluated over an 8-fold range of leaf biomass and/or a 28 d fermentation period. The responses of gravid females of both mosquito species varied with the plant species and biomass of plant materials used to make infusions, and with the length of the fermentation period. Infusions made from senescent bamboo (Arundinaria gigantea) and white oak (Quercus alba) leaves were significantly attractive to both mosquitoes. In general, infusions prepared by using low biomass of plant material over a 7–14 d fermentation period were most attractive to Ae. aegypti. In contrast, Ae. albopictus was attracted to infusions made using a wider range of plant biomass and over a longer fermentation period. Both mosquito species were more attracted to a non-sterile white oak leaf infusion than to white oak leaf infusion that was prepared using sterilized plant material and water, thus suggesting a role for microbial activity in the production of odorants that mediate the oviposition response of gravid mosquitoes.

Key Words

Aedes aegypti Aedes albopictus Oviposition Attractants Plant infusion Fermentation Microbe-insect interactions 

References

  1. Allan, S. A., and Kline, D. L. 1995. Evaluation of organic infusions and synthetic compounds mediating oviposition in Aedes albopictus and Aedes aegypti (Diptera: Culicidae). J. Chem. Ecol. 21:1847–1860.CrossRefGoogle Scholar
  2. Bentley, M. D., and Day, J. F. 1989. Chemical ecology and behavioral aspects of mosquito oviposition. Annu. Rev. Entomol. 34: 401–421.CrossRefPubMedGoogle Scholar
  3. Benzon, G. L., and Apperson, C. S. 1988. Reexamination of chemically mediated oviposition behavior in Aedes aegypti (L.) (Diptera: Culicidae). J. Med. Entomol. 25:158–164.PubMedGoogle Scholar
  4. Brunel, B., Perissol, C., Fernandez, M., Boeufgras, J. M., and Le Petit, J. 1994. Occurrence of Bacillus species on evergreen oak leaves. FEMS Microbiol. Ecol. 14:331–342.CrossRefGoogle Scholar
  5. Chadee, D. D., Lakkan, A., Ramdath, W. R., and Persad, R. C. 1993. Oviposition response of Aedes aegypti mosquitoes to different concentrations of hay infusion in Trinidad, West Indies. J. Am. Mosq. Control Assoc. 9:346–348.PubMedGoogle Scholar
  6. Gubler, D. J. 2002. The global emergence/resurgence of arboviral diseases as public health problems. Arch. Med. Res. 33:330–342.CrossRefPubMedGoogle Scholar
  7. Hazard, E. I., Mayer, M. S., and Savage, K. E. 1967. Attraction and oviposition stimulation of gravid female mosquitoes by bacteria isolated from hay infusion. Mosq. News 27:133–136.Google Scholar
  8. Isoe, J., and Millar, J. G. 1995. Characterization of factors mediating oviposition site choice by Culex tarsalis. J. Am. Mosq. Control Assoc. 11:21–28.PubMedGoogle Scholar
  9. Isoe, J., Millar, J. G., and Beehler, J. W. 1995a. Bioassays for Culex (Diptera: Culicidae) mosquito oviposition attractants and stimulants. J. Med. Entomol. 32:475–483.PubMedGoogle Scholar
  10. Isoe, J., Millar, J. G., Beehler, J. W., and Mulla, M. S. 1995b. Oviposition responses of Culex tarsalis and Culex quinquefasciatus to aged Bermuda grass infusions. J. Am. Mosq. Control Assoc. 11:39–44.PubMedGoogle Scholar
  11. Kramer, W. L., and Mulla, M. S. 1979. Oviposition attractants and repellents of mosquitoes: oviposition responses of Culex mosquitoes to organic infusions. Environ. Entomol. 8:1111–1117.Google Scholar
  12. Lambais, M. R., Crowley, D. E., Cury, J. C., Bull, R. C., and Rodrigues, R. R. 2006. Bacterial diversity in tree canopies of the Atlantic forest. Science 312:1917.CrossRefPubMedGoogle Scholar
  13. Lampman, R. L., and Novak, R. J. 1996a. Ovipositional preferences of Culex pipiens and Culex restuans in Illinois. J. Am. Mosq. Control Assoc. 12:23–32.PubMedGoogle Scholar
  14. Lampman, R. L., and Novak, R. J. 1996b. Attraction of Aedes albopictus adults to sod infusion. J. Am. Mosq. Control Assoc. 12:119–124.PubMedGoogle Scholar
  15. Maw, M. G. 1970. Capric acid as a larvicide and an oviposition stimulant for mosquitoes. Nature (Lond.) 227:1154–1155.CrossRefGoogle Scholar
  16. Mboera, L. E. G., Takken, W., Mdira, K. Y., and Pickett, J. A. 2000. Sampling gravid Culex quinquefasciatus (Diptera: Culicidae) in Tanzania with traps baited with synthetic oviposition pheromone and grass infusions. J. Med. Entomol. 37:172–176.CrossRefPubMedGoogle Scholar
  17. Millar, J. G., Chaney, J. D., and Mulla, M. S. 1992. Identification of oviposition attractants for Culex quinquefasciatus from fermented Bermuda grass infusions. J. Am. Mosq. Control Assoc. 8:11–17.PubMedGoogle Scholar
  18. Nasci, R. S., Komar, N., Marfin, A. A., Ludwig, G. V., Kramer, L. D., Daniels, T. J., Falco, R. C., Campbell, S. R., Brookes, K., Gottfried, K. L., Burkhalter, K. L., Aspen, S. E., Kerst, A. J., Lanciotti, R. S., and Moore, C. G. 2002. Detection of West Nile virus-infected mosquitoes and seropositive juvenile birds in the vicinity of virus-positive dead birds. Am. J. Trop. Med. Hyg. 67:492–496.PubMedGoogle Scholar
  19. Navarro, D. M. A. F., De Oliveira, P. E. S., Potting, R. P. J., Brito, A. C., Fital, S. J. F., and Goulart Sant’Ana, A. E. 2003. The potential attractant or repellent effects of different water types on oviposition in Aedes aegypti L. (Diptera: Culicidae). J. Appl. Entomol. 127:46–50.CrossRefGoogle Scholar
  20. Pickett, J. A., Birkett, M. A., Dewhirst, S. Y., Logan, J. G., Omolo, M. O., Torto, B., Pelletier, J., Zainulabeuddin, S., and Leal, W. S. 2010. Chemical ecology of animal and human pathogen vectors in a changing global climate. J. Chem. Ecol. 36:113–121.CrossRefPubMedGoogle Scholar
  21. Polson, K. A., Curtis, C., Seng, C. M., Olson, J. G., Chantha, M., and Rawlins, S. C. 2002. The use of ovitraps baited with hay infusion for surveillance of Aedes aegypti in Cambodia. Dengue Bull. 26:178–184.Google Scholar
  22. Ponnusamy, L., Xu, N., Nojima, S., Wesson, D. M., Schal, C., and Apperson, C. S. 2008. Identification of bacteria and bacteria-associated chemical cues that mediate oviposition site preferences by Aedes aegypti. Proc. Natl. Acad. Sci. USA. 105:9262–9267.CrossRefPubMedGoogle Scholar
  23. Ponnusamy, L., Wesson, D. M., Arellano, C., Schal, C., and Apperson, C. S. 2010. Species composition of bacterial communities influences attraction of mosquitoes to experimental plant infusions. Microb. Ecol. 59:158–173.CrossRefPubMedGoogle Scholar
  24. Rawlins, S. C., Martinez, R., Wiltshire, S., and Legall, G. 1998. A comparison of surveillance systems for the dengue vector Aedes aegypti in Port of Spain, Trinidad. J. Am. Mosq. Control Assoc. 14:131–136.Google Scholar
  25. Reiter, P. 1986. A standardized procedure for the quantitative surveillance of certain Culex mosquitoes by egg raft collection. J. Am. Mosq. Control Assoc. 2:219–221.PubMedGoogle Scholar
  26. Reiter, P., Amador, M. A., and Colon, N. 1991. Enhancement of the CDC ovitrap with hay infusions for daily monitoring of Aedes aegypti populations. J. Am. Mosq. Control. Assoc. 7:52–55.PubMedGoogle Scholar
  27. Ritchie, S. A. 1984. Hay infusion and isopropyl alcohol baited CDC light trap: a simple effective trap for gravid Culex mosquitoes. Mosq. News 44:404–407.Google Scholar
  28. Ritchie, S. A. 2001. Effect of some animal feeds and oviposition substrates on Aedes oviposition in ovitraps in Cairns, Australia. J. Am. Mosq. Control Assoc. 17:206–208.PubMedGoogle Scholar
  29. Sant’Ana, A. L., Roque, R. A., and Eiras, A. E. 2006. Characteristics of grass infusions as oviposition attractants to Aedes (Stegomyia) (Diptera: Culicidae). J. Med. Entomol. 43:214–220.CrossRefGoogle Scholar
  30. Savage, H. M., Smith, G. C., Moore, C. G., Mitchell, C. J., Townsend, M., and Marfin, A. A. 1993. Entomological investigations of an epidemic of St. Louis encephalitis in Pine Bluff, Arkansas, 1991. Am. J. Trop. Med. Hyg. 49: 38–45.PubMedGoogle Scholar
  31. Sumba, L. A., Guda, T. O., Deng, A. L., Hassanali, A., Beier, J. C., and Knols, B. G. J. 2004. Mediation of oviposition site selection in the African malaria mosquito Anopheles gambiae (Diptera: Culicidae) by semiochemicals of microbial origin. Int. J. Trop. Insect Sci. 24:260–265.CrossRefGoogle Scholar
  32. Szumlas, D. E., Apperson, C. S., and Powell, E. E. 1996. Seasonal occurrence and abundance of Aedes triseriatus and other mosquitoes in a La Crosse virus-endemic area of western North Carolina. J. Am. Mosq. Control Assoc. 12:184–193.PubMedGoogle Scholar
  33. Tsai, T. F., Smith, G. C., Happ, C. M., Kirk, L. J., Jakob, W. L., Bolin, R. A., Francy, D. B., and Lampert, K. J. 1989. Surveillance of St. Louis encephalitis virus vectors in Grand Junction, Colorado in 1987. J. Am. Mosq. Contr. Assoc. 5:161–165.Google Scholar
  34. Trexler, J. D., Apperson, C. S., and Schal, C. 1998. Laboratory and field evaluations of oviposition responses of Aedes albopictus and Aedes triseriatus (Diptera: Culicidae) to oak leaf infusions. J. Med. Entomol. 35:967–976.PubMedGoogle Scholar
  35. Trexler, J. D., Apperson, C. S., Zurek, L., Gemeno, C., Schal, C., Kaufman, M., Walker, E., Watson, D. W., and Wallace, L. 2003. Role of bacteria in mediating the oviposition responses of Aedes albopictus (Diptera: Culicidae). J. Med. Entomol. 40:841–848.CrossRefPubMedGoogle Scholar
  36. Yang, C.-H., Crowley, D. E., Borneman J., and Keen, N. T. 2001. Microbial phyllosphere populations are more complex than previously realized. Proc. Natl. Acad. Sci. USA 98:3889–3894.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Loganathan Ponnusamy
    • 1
  • Ning Xu
    • 1
  • Katalin Böröczky
    • 1
  • Dawn M. Wesson
    • 2
  • Luma Abu Ayyash
    • 1
  • Coby Schal
    • 1
  • Charles S. Apperson
    • 1
  1. 1.Department of EntomologyNorth Carolina State UniversityRaleighUSA
  2. 2.Department of Tropical MedicineTulane UniversityNew OrleansUSA

Personalised recommendations