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

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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.

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References

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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 

  • 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 

  • Clements, A. N. 1999. The Biology of Mosquitoes Sensory Reception and Behaviour, 2. p. 756. CABI, UK.

    Google Scholar 

  • 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 

  • Gomez, K. A., and Gomez, A. A. 1984. Statistical Procedure for Agricultural Research. pp. 3–15. Wiley, New York.

    Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Kalpage, K. S. P., and Brust, R. A. 1973. Oviposition attractant produced by immature Aedes atropalpus. Env. Entomol. 2:729–730.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • Koenraadt, C. J. M., and Takken, W. 2003. Cannibalism and predation among larvae of Anopheles gambiae complex. Med. Vet. Entomol. 17:61–66.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Laurence, B. R., and Pickett, J. A. 1985. An oviposition attractant pheromone in Culex quinquefasciatus Say (Diptera: Culicidae). Bull. Entomol. Res. 75:283–290.

    CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Osgood, C. E. 1971. An oviposition pheromone associated with the egg rafts of Culex tarsalis. J. Econ. Entomol. 64:1038–1041.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • SAS INSTITUTE INC. 2003. Proceedings of the Twenty-Eight Annual SAS Users Group International Conference. Cary, NC: SAS Institute Inc.

  • 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.

    PubMed  CAS  Google Scholar 

  • Service, M. W. 1993. Mosquito Ecology: Field Sampling Methods. p. 988. Chapman and Hall, London.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    PubMed  Google Scholar 

  • 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 

  • 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.

    CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

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Acknowledgements

We thank K. Okoth, E. Obudho, J. Wauna, and the staff of the malaria vector program at Thomas Odhiambo campus-ICIPE for their technical assistance. This research was partly supported by funds from the National Institutes of Health (NIH) grant U19 AI45511 and the ABC Fogarty through grant number D43TWØ1142. LS acknowledges a PhD scholarship from the German Academic Exchange Service (DAAD) (through the ICIPE African Regional Post-graduate Program in Insect Science, ARPPIS). CBO wishes to acknowledge the US William J. Fulbright Program and the Yale Institute for Biospheric Studies (YIBS) Field Ecology Award.

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Correspondence to Ahmed Hassanali.

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Sumba, L.A., Ogbunugafor, C.B., Deng, A.L. et al. Regulation of Oviposition in Anopheles gambiae s.s.: Role of Inter- and Intra-Specific Signals. J Chem Ecol 34, 1430–1436 (2008). https://doi.org/10.1007/s10886-008-9549-5

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