Journal of Chemical Ecology

, Volume 34, Issue 11, pp 1430–1436

Regulation of Oviposition in Anopheles gambiae s.s.: Role of Inter- and Intra-Specific Signals

  • Leunita A. Sumba
  • C. Brandon Ogbunugafor
  • Arop L. Deng
  • Ahmed Hassanali
Article

Abstract

Females of Anopheles gambiae Giles normally oviposit in a large number of fresh, small, sunlit, and spatially spread temporary pools. Such pools are associated with lower levels of predation compared to large, longer-lasting habitats. We compared oviposition levels on preferred (water collected from natural anopheline larval habitats) and non-preferred (distilled water) aqueous substrates by gravid females that contained different densities of conspecific eggs or early and late instar larvae. The presence of conspecific larvae, but not eggs, had a positive or negative effect on the ovipositional responses of gravid An. gambiae females, depending on the quality (preferred or non-preferred by the mosquito) of the oviposition water and the density of larvae. Presence of larvae, at all densities, in distilled water deterred oviposition. However, in natural anopheline pool water, a low density of larvae increased oviposition, whereas a higher density inhibited oviposition. Our results suggest that two signals produced by this mosquito may be involved in regulating oviposition: a volatile pheromone emitted by conspecific larvae, which augments the effect of a volatile signal emitted by preferred habitats, and a non-olfactory cue associated with high densities of larvae that deters oviposition.

Keywords

Anopheles gambiae Giles Oviposition Intra-specific signals Larval pheromone 

References

  1. Allan, S. A., and Kline, D. L. 1998. Larval rearing water and pre-existing eggs influence oviposition by Aedes aegypti and Ae. albopictus (Diptera: Culicidae). J. Med. Entomol. 35:943–947.PubMedGoogle Scholar
  2. Bentley, M. D., McDaniel, T. N., Lee, H.-P., Stiehl, B., and Yatagai, M. 1976. Studies of Aedes triseriatus oviposition attractants producted by larvae of Aedes triseriatus and Aedes atropalpus (Diptera: Culicidae). J. Med. Entomol. 13:112–115.PubMedGoogle Scholar
  3. Benzon, G. L., and Apperson, C. S. 1988. Re-examination of chemically mediated oviposition behavior in Aedes aegypti (L.) (Diptera: Culicidae). J. Med. Entomol. 25:158–164.PubMedGoogle Scholar
  4. Blackwell, A., Mordue, A. J., Hansson, B. S., Wadhams, L. J., and Pickett, J. A. 1993. A behavioural and electrophysiological study of oviposition cues for Culex quinquefasciatus. Physiol. Entomol. 18:343–348.Google Scholar
  5. Chadee, D. D. 1993. Oviposition response of Aedes aegypti (L.) to the presence of conspecific eggs in the field in Trinidad, W.I. J. Fl. Med. Assoc. 64:63–66.Google Scholar
  6. Clements, A. N. 1999. The Biology of Mosquitoes Sensory Reception and Behaviour, 2. p. 756. CABI, UK.Google Scholar
  7. Gillies, M. T., and De Meillon, B. 1968. The Anophelinae of Africa South of the Sahara (Ethiopian zoogeographical region). p. 343. South African Institute for Medical Research, Johannesburg.Google Scholar
  8. Gomez, K. A., and Gomez, A. A. 1984. Statistical Procedure for Agricultural Research. pp. 3–15. Wiley, New York.Google Scholar
  9. Gimnig, J. E., Ombok, M., Kamau, L., and Hawley, W. A. 2001. Characteristics of larval anopheline (Diptera: Culicidae) habitats in Western Kenya. J. Med. Entomol. 38:282–288.PubMedGoogle Scholar
  10. Gimnig, J. E., Ombok, M., Otieno, S., Kaufman, M., Vulule, J. M., and Walker, E. D. 2002. Density-dependent development of Anopheles gambiae (Diptera: Culicidae) larvae in artificial habitats. J. Med. Entomol. 39:162–172.PubMedCrossRefGoogle Scholar
  11. Hwang, Y. S. 1980. Oviposition attractants and repellents of mosquitoes. Isolation and Identification of oviposition repellents for Culex mosquitoes. J. Chem. Ecol. 6:71–80.CrossRefGoogle Scholar
  12. Kalpage, K. S. P., and Brust, R. A. 1973. Oviposition attractant produced by immature Aedes atropalpus. Env. Entomol. 2:729–730.Google Scholar
  13. Kiflawi, M., Blaustein, L., and Mangel, M. 2003. Oviposition habitat selection by the mosquito Culiseta longiareolata in response to risk of predation and conspecific larval density. Ecol. Entomol. 28:168–173.CrossRefGoogle Scholar
  14. Koenraadt, C. J. M., and Takken, W. 2003. Cannibalism and predation among larvae of Anopheles gambiae complex. Med. Vet. Entomol. 17:61–66.PubMedCrossRefGoogle Scholar
  15. Kramer, W. L., and Mulla, M. S. 1979. Oviposition attractants and repellents of mosquitoes: Oviposition responses of Culex mosquitoes to organic infusions. Env. Entomol. 8:1111–1117.Google Scholar
  16. Laurence, B. R., and Pickett, J. A. 1985. An oviposition attractant pheromone in Culex quinquefasciatus Say (Diptera: Culicidae). Bull. Entomol. Res. 75:283–290.Google Scholar
  17. McCrae, A. W. 1984. Oviposition by African malaria vector mosquitoes. II. Effects of site tone, water type and conspecific immatures on target selection by freshwater Anopheles gambiae Giles, sensu lato. Ann. Trop. Med. Parasitol. 78:307–318.PubMedGoogle Scholar
  18. Merritt, R. W., Dadd, R. H., and Walker, E. D. 1992. Feeding behavior, natural food, and nutritional relationships of larval mosquitoes. Annu. Rev. Entomol. 37:349–376.PubMedGoogle Scholar
  19. Minakawa, N., Mutero, C. M., Githure, J. C., Beier, J. C., and Yan, G. 1999. Spatial distribution and habitat characterization of anopheline mosquito larvae in western Kenya. Ann. Trop. Med. Hyg. 61:1010–1016.Google Scholar
  20. Minakawa, N., Sonye, G., and Yan, G. 2005a. Relationships between occurrence of Anopheles gambiae s.l. (diptera:Culicidae) and size and stability of larval habitats. J. Med. Entomol. 42:295–300.PubMedCrossRefGoogle Scholar
  21. Minakawa, N., Munga, S., Atieli, E., Mushinzimana, E., Zhou, Z., Githeko, A. K., and Yan, G. 2005b. Spatial distribution of anopheline larval habitats in western Kenya highlands: effects of land cover types and topography. Am. J. Trop. Med. Hyg. 73:157–165.PubMedGoogle Scholar
  22. Muirhead-Thomson, R. C. 1945. Studies on the breeding places and control of Anopheles gambiae and Anopheles gambiae Var. melas in the coastal district of Sierra Leone. Bull. Entomol. Res. 36:185–252.CrossRefGoogle Scholar
  23. Munga, S., Minakawa, M., Zhosu, G., Barrack, J. O-O., Githeko, A. K., and Yan, G. 2006. Effects of larval competitors and predators on oviposition site selection of Anopheles gambiae Sensu Stricto. J. Med. Entomol. 43:221–224.PubMedCrossRefGoogle Scholar
  24. Osgood, C. E. 1971. An oviposition pheromone associated with the egg rafts of Culex tarsalis. J. Econ. Entomol. 64:1038–1041.PubMedGoogle Scholar
  25. Poonam, S., Paily, K. P., and Balaraman, K. 2002. Oviposition attractancy of bacterial culture filtrates-Response of Culex quinquefasciatus. Mem. Inst. Oswaldo Cruz 97:359–362.PubMedCrossRefGoogle Scholar
  26. Reisen, W. K., and Siddiqui, T. F. 1978. The influence of conspecific immatures on the oviposition preferences of the mosquitoes Anopheles stephensi and Culex tritaeniorhynchus. Pak. J. Zool. 10:31–41.Google Scholar
  27. Rejmankova, E. R., Higashi, R., Grieco, J., Achee, N., and Roberts, D. 2005. Volatile substances from larval habitats mediate species-specific oviposition in Anopheles mosquitoes. J. Med. Entomol. 42:95–103.PubMedCrossRefGoogle Scholar
  28. SAS INSTITUTE INC. 2003. Proceedings of the Twenty-Eight Annual SAS Users Group International Conference. Cary, NC: SAS Institute Inc.Google Scholar
  29. Service, M. W. 1977. Mortalities of the immature stages of species of the Anopheles gambiae complex in Kenya: comparison between rice fields and temporary pools, identification of predators, and effects of insecticidal spraying. J. Med. Entomol. 13:535–545.PubMedGoogle Scholar
  30. Service, M. W. 1993. Mosquito Ecology: Field Sampling Methods. p. 988. Chapman and Hall, London.Google Scholar
  31. Seyoum, A., Pålsson, K., Kung'a, S., Kabiru, E. W., Lwande, W., Killeen, G. F., Hassanali, A., and Knols, B. G. J. 2002. Traditional use of mosquito-repellent plants in western Kenya and their evaluation in semi-field experimental huts against Anopheles gambiae: ethnobotanical studies and application by thermal expulsion and direct burning. Trans. Royal Soc. Trop. Med. Hygiene 96:225–231.CrossRefGoogle Scholar
  32. Spencer, M. L., Blaustein, L., and Cohen, J. E. 2002. Oviposition habitat selection by mosquitoes (Culiseta longiareolata) and consequences for population size. Ecology 83:669–679.CrossRefGoogle Scholar
  33. Sumba, L. A., Okoth, K., Deng, A. L., Githure, J., Knols, B. G. J., Beier, J. C., and Hassanali, A. 2004a. Daily oviposition patterns of the African malaria mosquito Anopheles gambiae Giles (Diptera: Culicidae) on different types of aqueous substrates. J. Circadian Rhythms 2:6.PubMedCrossRefGoogle Scholar
  34. Sumba, L. A., Guda, T. O., Deng, A. L., Hassanali, A., Beier, J. C., and Knols, B. G. J. 2004b. Mediation of oviposition site selection in the African malaria mosquito Anopheles gambiae (Diptera: Culicidae) by semiochemicals of microbial origin. Int. J. Trop. Insec. Sci. 24:260–265.Google Scholar
  35. Sunahara, T., Ishizaka, K., and Mogi, M. 2002. Habitat size: a factor determining the opportunity for encounters between mosquito larvae and aquatic predators. J. Vector Ecol. 27:8–20.PubMedGoogle Scholar
  36. Trimble, R. M., and Wellington, W. G. 1980. Oviposition stimulant associated with fourth-instar larvae of Aedes togoi (Dipetera: Culicidae). J. Med. Entomol. 17:509–514.Google Scholar
  37. Washburn, J. O. 1995. Regulatory factors affecting larval mosquito populations in container and pool habitats: implications for biological control. J. Am. Mosq. Contol Assoc. 11:279–283.Google Scholar
  38. Zahiri, N., and Rau, M. E. 1998. Oviposition attraction and repellency of Aedes aegypti (Diptera: Culicidae) to waters from conspecific larvae subjected to crowding, confinement, starvation, or infection. J. Med. Entomol. 35:782–787.PubMedGoogle Scholar
  39. Zahiri, N., Rau, M. E., and Lewis, D. J. 1997. Oviposition responses of Aedes aegypti and Ae. atropalpus (Diptera: Culicidae) females to waters from conspecific and heterospecific normal larvae and from larvae infected with Plagiorchis elegans (Trematoda: Plagiorchiidae). J. Med. Entomol. 34:565–568.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • Leunita A. Sumba
    • 1
    • 2
  • C. Brandon Ogbunugafor
    • 1
    • 3
  • Arop L. Deng
    • 4
  • Ahmed Hassanali
    • 1
  1. 1.International Centre of Insect Physiology and Ecology (ICIPE)NairobiKenya
  2. 2.Kenya Water Institute (KEWI)NairobiKenya
  3. 3.Yale University School of MedicineNew HavenUSA
  4. 4.Department of Biological SciencesEgerton UniversityNjoroKenya

Personalised recommendations