Weather variability impacts on oviposition dynamics of the southern house mosquito at intermediate time scales | Bulletin of Entomological Research | Cambridge Core (original) (raw)

Abstract

Oviposition is a major event in the life history of mosquitoes, shaping both individual fitness and vectorial capacity. Several exogenous factors have been shown as important for the dynamic forcing of oviposition at finely (hourly) and coarsely (monthly or season to season) grained temporal scales. However, field studies addressing the interplay of weather factors on oviposition dynamics at the intermediate (days to weeks) time scale are missing. Here, we present the results from a field study that showed the oviposition dynamics of the southern house mosquito, Culex quinquefasciatus Say (Diptera: Culicidae), to be: (i) primarily dictated by relative humidity; and (ii) disrupted by rainfall events that resulted in a modified sensitivity to relative humidity. Rainfall changed the concentration of ammonia, a major limiting resource of microbes used as food by mosquito larvae. Following major rainfall events, the importance of relative humidity in forcing the oviposition dynamics also changed. Finally, our results indicate that qualitative changes in oviposition habitats modify the importance of weather variables as predictors of mosquito oviposition dynamics.

References

Awerbuch, T., Kiszewski, A.E. & Levins, R. (2002) Surprise, nonlinearity and complex behaviour. pp. 96–119 in Martens, P. & McMichael, A.J. (Eds) Environmental Change, Climate and Health. Cambridge, UK, Cambridge University Press.CrossRefGoogle Scholar

Beehler, J.W. & Mulla, M.S. (1995) Effects of organic enrichment on temporal distribution and abundance of culicine egg rafts. Journal of the American Mosquito Control Association 11, 167–171.Google ScholarPubMed

Beehler, J.W., Millar, J.G. & Mulla, M.S. (1994) Field-evaluation of synthetic compounds mediating oviposition in Culex mosquitos (Diptera, Culicidae). Journal of Chemical Ecology 20, 281–291.CrossRefGoogle Scholar

Beman, J.M., Arrigo, K.R. & Matson, P.A. (2005) Agricultural runoff fuels large phytoplankton blooms in vulnerable areas of the ocean. Nature 434, 211–214.CrossRefGoogle Scholar

Blaustein, L. & Chase, J.M. (2007) Interactions between mosquito larvae and species that share the same trophic level. Annual Review of Entomology 52, 489–507.CrossRefGoogle ScholarPubMed

Braks, M., Leal, W. & Cardé, R. (2007) Oviposition responses of gravid female Culex quinquefasciatus to egg rafts and low doses of oviposition pheromone under semifield conditions. Journal of Chemical Ecology 33, 567–578.CrossRefGoogle ScholarPubMed

Calhoun, L.M., Avery, M., Jones, L., Gunarto, K., King, R., Roberts, J. & Burkot, T.R. (2007) Combined sewage overflows (CSO) are major urban breeding sites for Culex quinquefasciatus in Atlanta, Georgia. American Journal of Tropical Medicine and Hygiene 77, 478–484.CrossRefGoogle ScholarPubMed

Cazelles, B., Chavez, M., de Magny, G.C., Guegan, J.F. & Hales, S. (2007) Time-dependent spectral analysis of epidemiological time-series with wavelets. Journal of the Royal Society Interface 4, 625–636.CrossRefGoogle ScholarPubMed

Chaves, L.F. (2010) An entomologist guide to demystify pseudoreplication: data analysis of field studies with design constraints. Journal of Medical Entomology 47, 291–298.CrossRefGoogle ScholarPubMed

Chaves, L.F. & Koenraadt, C.J.M. (2010) Climate change and highland malaria: fresh air for a hot debate. Quarterly Review of Biology 85, 27–55.CrossRefGoogle ScholarPubMed

Chaves, L.F. & Pascual, M. (2006) Climate cycles and forecasts of cutaneous leishmaniasis, a nonstationary vector-borne disease. Plos Medicine 3, 1320–1328.CrossRefGoogle ScholarPubMed

Chaves, L.F., Keogh, C.L., Vazquez-Prokopec, G.M. & Kitron, U.D. (2009) Combined sewage overflow enhances oviposition of Culex quinquefasciatus (Diptera: Culicidae) in urban areas. Journal of Medical Entomology 46, 220–226.CrossRefGoogle ScholarPubMed

Chesson, J. (1984) Effect of notonectids (Hemiptera, Notonectidae) on mosquitos (Diptera, Culicidae) – predation or selective oviposition. Environmental Entomology 13, 531–538.CrossRefGoogle Scholar

Day, J.F. & Curtis, G.A. (1989) Influence of rainfall on Culex nigripalpus (Diptera: Culicidae) blood feeding behavior in Indian river County, Florida. Annals of the Entomological Society of America 82, 32–37.CrossRefGoogle Scholar

Day, J.F. & Curtis, G.A. (1994) When it rains they soar – and that makes Culex nigripalpus a dangerous mosquito. American Entomologist 40, 162–167.CrossRefGoogle Scholar

Day, J.F. & Curtis, G.A. (1999) Blood feeding and oviposition by Culex nigripalpus (Diptera: Culicidae) before, during, and after a widespread St. Louis encephalitis virus epidemic in Florida. Journal of Medical Entomology 36, 176–181.CrossRefGoogle ScholarPubMed

Day, J.F., Curtis, G.A. & Edman, J.D. (1990) Rainfall-directed oviposition behavior of Culex nigripalpus (Diptera: Culicidae) and its influence on St. Louis encephalitis virus transmission in Indian River County, Florida. Journal of Medical Entomology 27, 43–50.CrossRefGoogle Scholar

de Meillon, B., Sebastian, A. & Khan, Z.H. (1967) Time of arrival of gravid Culex pipiens fatigans at an oviposition site, the oviposition cycle and the relationship between time of feeding and time of oviposition. Bulletin of the World Health Organization 36, 39–46.Google ScholarPubMed

Dow, R.P. & Gerrish, G.M. (1970) Day-to-day change in relative humidity and activity of Culex nigripalpus (Diptera: Culicidae). Annals of the Entomological Society of America 63, 995–999.CrossRefGoogle ScholarPubMed

Dye, C. (1992) The analysis of parasite transmission by bloodsucking insects. Annual Review of Entomology 37, 1–19.CrossRefGoogle ScholarPubMed

Edgerly, J.S., McFarland, M., Morgan, P. & Livdahl, T. (1998) A seasonal shift in egg-laying behaviour in response to cues of future competition in a treehole mosquito. Journal of Animal Ecology 67, 805–818.Google Scholar

Edman, J.D., Scott, T.W., Costero, A., Morrison, A.C., Harrington, L.C. & Clark, G.G. (1998) Aedes aegypti (Diptera: Culicidae) movement influenced by availability of oviposition sites. Journal of Medical Entomology 35, 578–583.CrossRefGoogle ScholarPubMed

Faraway, J.J. (2006) Extending the Linear Model with R: Generalized Linear, Mixed Effects and Nonparametric Regression Models. Boca Raton, FL, USA, CRC Press.Google Scholar

Grinsted, A., Moore, J.C. & Jevrejeva, S. (2004) Application of the cross wavelet transform and wavelet coherence to geophysical time series. Nonlinear Processes in Geophysics 11, 561–566.CrossRefGoogle Scholar

Hayes, J. & Downs, T.D. (1980) Seasonal changes in an isolated population of Culex pipiens quinquefasciatus (Diptera: Culicidae): A time series analysis. Journal of Medical Entomology 17, 63–69.CrossRefGoogle Scholar

Hayes, J. & Hsi, B.P. (1975) Interrelationships between selected meteorologic phenomena and immature stages of Culex pipiens quinquefasciatus Say: Study of an isolated population. Journal of Medical Entomology 12, 299–308.CrossRefGoogle ScholarPubMed

Kiflawi, M., Blaustein, L. & Mangel, M. (2003) Oviposition habitat selection by the mosquito Culiseta longiareolata in response to risk of predation and conspecific larval density. Ecological Entomology 28, 168–173.Google Scholar

Levins, R. (1968) Evolution in Changing Environments: Some theoretical explorations. Princeton, NJ, USA, Princeton University Press.CrossRefGoogle Scholar

Macdonald, R.S., Madder, D.J. & Surgeoner, G.A. (1981) Diel periodicity of oviposition by Culex pipiens and Culex restuans in southern Ontario. Proceedings of the Entomological Society of Ontario 112, 39–40.Google Scholar

Mangel, M. (1987) Oviposition site selection and clutch size in insects. Journal of Mathematical Biology 25, 1–22.CrossRefGoogle Scholar

Merritt, R.W., Dadd, R.H. & Walker, E.D. (1992) Feeding behavior, natural food, and nutritional relationships of larval mosquitoes. Annual Review of Entomology 37, 349–374.CrossRefGoogle ScholarPubMed

Millar, J.G., Chaney, J.D., Beehler, J.W. & Mulla, M.S. (1994) Interaction of the Culex quinquefasciatus egg raft pheromone with a natural chemical associated with oviposition sites. Journal of the American Mosquito Control Association 10, 374–379.Google ScholarPubMed

Platt, R.B., Collins, C.L. & Witherspoon, J.P. (1957) Reactions of Anopheles quadrimaculatus Say to moisture, temperature, and light. Ecological Monographs 27, 303–324.CrossRefGoogle Scholar

Platt, R.B., Love, G.J. & Williams, E.L. (1958) A positive correlation between relative humidity and the distribution and abundance of Aedes vexans. Ecology 39, 167–169.CrossRefGoogle Scholar

Reddy, M.R., Lepore, T.J., Pollack, R.J., Kiszewski, A.E., Spielman, A. & Reiter, P. (2007) Early evening questing and oviposition activity by the Culex (Diptera: Culicidae) vectors of West Nile virus in northeastern North America. Journal of Medical Entomology 44, 211–214.CrossRefGoogle ScholarPubMed

Rowley, W.A. & Graham, C.L. (1968) The effect of temperature and relative humidity on the flight performance of female Aedes aegypti. Journal of Insect Physiology 14, 1251–1257.CrossRefGoogle ScholarPubMed

Scheffer, M., Carpenter, S., Foley, J.A., Folke, C. & Walker, B. (2001) Catastrophic shifts in ecosystems. Nature 413, 591–596.Google Scholar

Schmalhausen, I.I. (1949) Factors of Evolution: The Theory of Stabilizing Selection. Philadelphia, PA, USA, Blakiston Co.Google Scholar

Shaman, J. & Day, J.F. (2007) Reproductive phase locking of mosquito populations in response to rainfall frequency. PLoS ONE 2(3), e331.CrossRefGoogle ScholarPubMed

Shaman, J., Day, J.F. & Stieglitz, M. (2002) Drought-induced amplification of Saint Louis encephalitis virus, Florida. Emerging Infectious Diseases 8, 575–580.CrossRefGoogle ScholarPubMed

Shaman, J., Day, J.F. & Stieglitz, M. (2005) Drought-induced amplification and epidemic transmission of West Nile Virus in southern Florida. Journal of Medical Entomology 42, 134–141.CrossRefGoogle ScholarPubMed

Shumway, R.H. & Stoffer, D.S. (2000) Time Series Analysis and Its Applications. New York, NY, USA, Springer.CrossRefGoogle Scholar

Silver, J.B. (2008) Mosquito Ecology: Field Sampling Methods. 3rd edn. New York, NY, USA, Springer.CrossRefGoogle Scholar

Solow, A.R. & Beet, A.R. (2005) A test for a regime shift. Fisheries Oceanography 14, 236–240.CrossRefGoogle Scholar

Spencer, M., Blaustein, L. & Cohen, J.E. (2002) Oviposition habitat selection by mosquitoes (Culiseta longiareolata) and consequences for population size. Ecology 83, 669–679.CrossRefGoogle Scholar

Strickman, D. (1983) Preliminary report of seasonal oviposition by Culex quinquefasciatus in San Antonio, Texas. Mosquito News 43, 226–230.Google Scholar

Strickman, D. (1988) Rate of oviposition by Culex quinquefasciatus in San Antonio, Texas, during three years. Journal of the American Mosquito Control Association 4, 339–344.Google Scholar

Styer, L.M., Carey, J.R., Wang, J.L. & Scott, T.W. (2007a) Mosquitoes do senesce: Departure from the paradigm of constant mortality. American Journal of Tropical Medicine and Hygiene 76, 111–117.CrossRefGoogle ScholarPubMed

Styer, L.M., Meola, M.A. & Kramer, L.D. (2007b) West Nile virus infection decreases fecundity of Culex tarsalis females. Journal of Medical Entomology 44, 1074–1085.CrossRefGoogle ScholarPubMed

Suleman, M. & Shirin, M. (1981) Laboratory studies on oviposition behaviour of Culex quinquefasciatus Say (Diptera: Culicidae): choice of oviposition medium and oviposition cycle. Bulletin of Entomological Research 71, 361–369.CrossRefGoogle Scholar

Vandermeer, J. & Yodzis, P. (1999) Basin boundary collision as a model of discontinuous change in ecosystems. Ecology 80, 1817–1827.CrossRefGoogle Scholar

Walker, E.D., Lawson, D.L., Merritt, R.W., Morgan, W.T. & Klug, M.J. (1991) Nutrient dynamics, bacterial populations, and mosquito productivity in tree hole ecosystems and microcosms. Ecology 72, 1529–1546.CrossRefGoogle Scholar