Seasonal weather, nutrients, and conspecific presence impacts on the southern house mosquito oviposition dynamics in combined sewage overflows

Journal of Medical Entomology

Volumn 49, Issue 6, 2012, Pages 1328-1338

  Nguyen, An T ^a   Williams Newkirk, Amanda J ^a   Kitron, Uriel D ^a   Chaves, Luis F ^a,b,c  

^a EMORY UNIVERSITY   (United States)

^b HOKKAIDO UNIVERSITY   (Japan)

^c UNIVERSIDAD NACIONAL   (Costa Rica)

Author keywords

Atlanta; combined sewage overflow; Culex quinquefasciatus; habitat selection; linear mixed effects model

Indexed keywords

ANIMAL; ARTICLE; CULEX; ECOSYSTEM; EGG LAYING; FEMALE; RIVER; SEASON; SEWAGE; STATISTICAL MODEL; UNITED STATES; WATER POLLUTION; WATER QUALITY; WEATHER;

ANIMALS; CULEX; ECOSYSTEM; FEMALE; GEORGIA; LINEAR MODELS; OVIPOSITION; RIVERS; SEASONS; SEWAGE; WATER POLLUTION; WATER QUALITY; WEATHER;

CULEX PIPIENS QUINQUEFASCIATUS; CULICIDAE; DIPTERA;

EID: 84869778259     PISSN: 00222585     EISSN: None     Source Type: Journal    
DOI: 10.1603/ME12090     Document Type: Article

References (66)

1. Barker, C. M., B. F. Eldridge, and W. K. Reisen. 2010. Seasonal abundance of Culex tarsalis and Culex pipiens complex mosquitoes (Diptera: Culicidae) in California. J. Med. Entomol. 47: 759-768.
2. Beehler, J. W., and M. S. Mulla. 1993. The effect of organic enrichment and ßooding duration on the oviposition behavior of Culex mosquitoes. Proc. Calif. Mosq. Vector Control Assoc. 61: 121-124.
3. Beehler, J. W., and M. S. Mulla. 1995. Effects of organic enrichment on temporal distribution and abundance of culicine egg rafts. J. Am. Mosq. Control Assoc. 11: 167- 171.
4. Beehler, J. W., J. P. Webb, and M. S. Mulla. 1993. Spatial and circadian oviposition patterns in an urban-population of Culex quinquefasciatus. J. Am. Mosq. Control Assoc. 9: 38-388.
5. Beehler, J. W., J. G. Millar, and M. S. Mulla. 1994. Protein hydrolysates and associated bacterial contaminants as oviposition attractants for the mosquito Culex quinquefasciatus. Med. Vet. Entomol. 8: 381-385. (Pubitemid 2139597)
6. Bentley, M. D., and J. F. Day. 1989. Chemical ecology and behavioral aspects of mosquito oviposition. Annu. Rev. Entomol. 34: 401-421.
7. Bernhardt, E. S., L. E. Band, C. J. Walsh, and P. E. Berke. 2008. Understanding, managing, and minimizing urban impacts on surface water nitrogen loading. Ann. N.Y. Acad. Sci. 1134: 61-96. (Pubitemid 351852802)
8. Blaustein, L., and B. P. Kotler. 1993. Oviposition habitat selection by the mosquito, Culiseta longiareolata: effects of conspecics, food and green toad tadpoles. Ecol. Entomol. 18: 104-108. (Pubitemid 24412533)
9. Bock, M. E., and M. M. Milby. 1981. Seasonal variation of wing length and egg raft size in Culex tarsalis. Proc. Calif. Mosq. Vector Control Assoc. 49: 64-66.
10. Britton, W. E. 1914. A remarkable outbreak of Culex pipiens Linn. J. Econ. Entomol. 7: 257-260.
11. Bruno, D. W., and B. R. Laurence. 1979. Inßuence of the apical droplet of Culex egg rafts on oviposition of Culex pipiens fatigans (Diptera, Culicidae). J. Med. Entomol. 16: 300-305. (Pubitemid 10206525)
12. Burke, R., R. Barrera, M. Lewis, T. Kluchinsky, and D. Claborn. 2010. Septic tanks as larval habitats for the mosquitoes Aedes aegypti and Culex quinquefasciatus in Playa-Playita, Puerto Rico. Med. Vet. Entomol. 24: 117- 123.
13. Calhoun, L. M., M. Avery, L. Jones, K. Gunarto, R. King, J. Roberts, and T. R. Burkot. 2007. Combined sewage overßows (CSO) are major urban breeding sites for Culex quinquefasciatus in Atlanta, Georgia. Am. J. Trop. Med. Hyg. 77: 478-484. (Pubitemid 351844322)
14. Carpenter, S. R. 1982. Stemßow chemistry: effects on population dynamics of detritivorous mosquitoes in tree-hole ecosystems. Oecologia 53: 1-6. (Pubitemid 13283935)
15. Chaves, L. F. 2010. An entomologist guide to demystify pseudoreplication: data analysis of eld studies with design constraints. J. Med. Entomol. 47: 291-298.
16. Chaves, L. F., and C.J.M. Koenraadt. 2010. Climate change and highland malaria: fresh air for a hot debate. Quart. Rev. Biol. 85: 27-55.
17. Chaves, L. F., and U. D. Kitron. 2011. Weather variability impacts on oviposition dynamics of the southern house mosquito at intermediate time scales. Bull. Entomol. Res. 101: 633-641.
18. Chaves, L. F., C. L. Keogh, G. M. Vazquez-Prokopec, and U. D. Kitron. 2009. Combined sewage overßow enhances oviposition of Culex quinquefasciatus (Diptera: Culicidae) in urban areas. J. Med. Entomol. 46: 220-226.
19. Chaves, L. F., G. L. Hamer, E. D. Walker, W. M. Brown, M. O. Ruiz, and U. D. Kitron. 2011a. Climatic variability and landscape heterogeneity impact urban mosquito diversity and vector abundance and infection. Ecosphere 2: art70.
20. Chaves, L. F., C. L. Keogh, A. M. Nguyen, G. M. Decker, G. M. Vazquez-Prokopec, and U. D. Kitron. 2011b. Combined sewage overßow accelerates immature development and increases body size in the urban mosquito Culex quinquefasciatus. J. Appl. Entomol. 135: 611-620.
21. Day, J. F., G. A. Curtis, and J. D. Edman. 1990. Rainfalldirected oviposition behavior of Culex nigripalpus (Diptera: Culicidae) and its inßuence on St. Louis Encephalitis virus transmission in Indian River County, Florida. J. Med. Entomol. 27: 43-50.
22. de Meillon, B., A. Sebastian, and Z. H. Khan. 1967a. Duration of egg larval and pupal stages of Culex pipiens fatigans in Rangoon Burma. Bull. W.H.O. 36: 7-14.
23. de Meillon, B., A. Sebastian, and Z. H. Khan. 1967b. 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. Bull. W.H.O. 36: 39-46.
24. Faraway, J. J. 2004. Linear models with R. CRC, Boca Raton, FL.
25. Faraway, J. J. 2006. Extending the linear model with R: generalized linear, mixed effects and nonparametric regression models. CRC, Boca Raton, FL.
26. Hegner, R. 1929. Experimental studies of bird malaria. Q. Rev. Biol. 4: 59-82.
27. Hu, W., S. Tong, K. Mengersen, B. Oldenburg, and P. Dale. 2006. Mosquito species (Diptera: Culicidae) and the transmission of Ross River Virus in Brisbane, Australia. J. Med. Entomol. 43: 37-381.
28. Ikemoto, T., and I. Sakaki. 1979. Physico-chemical characters of the water in rice elds in relation to their suitability of the mosquito larvae, Anopheles sinensis. Jpn. J. Sanit. Zool. 30: 87-92.
29. Ikeshoji, T. 1966. Attractant and stimulant factors for oviposition of Culex pipiens fatigans in natural breeding-sites. Bull. W.H.O. 35: 90-912.
30. Kiflawi, M., L. Blaustein, and M. Mangel. 2003a. Oviposition habitat selection by the mosquito Culiseta longiareolata in response to risk of predation and conspecic larval density. Ecol. Entomol. 28: 168-173. (Pubitemid 36463411)
31. Kiflawi, M., L. Blaustein, and M. Mangel. 2003b. Predationdependent oviposition habitat selection by the mosquito Culiseta longiareolata: a test of competing hypotheses. Ecol. Lett. 6: 3-40.
32. Kumada, N., K. Makiya, and H. Matsuno. 1972. An outbreak of the house mosquito, Culex pipiens pallens, due probably to water pollution, with a note on the control measures. Jpn. J. Sanit. Zool. 23: 23-33.
33. Leisnham, P. T., and D. P. Slaney. 2005. Increased larval mosquito densities from modied landuses in the Kapiti Region, New Zealand: vegetation, water quality, and predators as associated environmental factors. EcoHealth 2: 313-322. (Pubitemid 41712853)
34. Macdonald, R. S., D. J. Madder, and G. A. Surgeoner. 1981. Diel periodicity of oviposition by Culex pipiens and Culex restuans in Southern Ontario. Proc. Entomol. Soc. Ont. 112: 39-40.
35. Mackay, A. J., M. Amador, A. Diaz, J. Smith, and R. Barrera. 2009. Dynamics of Aedes aegypti and Culex quinquefasciatus in septic tanks. J. Am. Mosq. Control Assoc. 25: 409-416.
36. Makiya, K. 1973. Population dynamics of mosquitoes in Nagoya district V. Seasonal change of composition rate of Culex pipiens molestus and Culex pipiens pallens observed in a midtown building. Jpn. J. Sanit. Zool. 24: 89-96.
37. Mangel, M. 1987. Oviposition site selection and clutch size in insects. J. Math. Biol. 25: 1-22.
38. Millar, J. G., J. D. Chaney, J. W. Beehler, and M. S. Mulla. 1994. Interaction of the Culex quinquefasciatus egg raft pheromone with a natural chemical associated with oviposition sites. J. Am. Mosq. Control Assoc. 10: 374-379.
39. Mogi, M., and T. Okazawa. 1990. Factors inßuencing development and survival of Culex pipiens pallens larvae (Diptera, Culicidae) in polluted urban creeks. Res. Popul. Ecol. 32: 13-149.
40. Mogi, M., and T. Sota. 1996. Physical and biological attributes of water channels utilized by Culex pipiens pallens immatures in Saga City southwest Japan. J. Am. Mosq. Control Assoc. 12: 206-214. (Pubitemid 126604504)
41. Mogi, M., T. Sota, andM.Motomura. 1995. Macroconditions of channel segments utilized by Culex pipiens pallens immatures in Saga City, southwest Japan. J. Am. Mosq. Control Assoc. 11: 448-453.
42. Monath, T. P., and T. F. Tsai. 1987. St. Louis Encephalitis: lessons from the last decade. Am. J. Trop. Med. Hyg. 37: 40S-59S. (Pubitemid 18018446)
43. Munstermann, L. E., and G. B. Craig. 1977. Culex mosquito population in the catch basins of northern St. Joseph County, Indiana. Proc. Indiana Acad. Sci. 86: 246-252.
44. Nayar, J. K., and D.M.Sauerman. 1970. Acomparative study of growth and development in Florida mosquitoes. 3. Effects of temporary crowding on larval aggregation formation, pupal ecdysis and adult characteristics at emergence. J. Med. Entomol. 7: 521-528.
45. Olden, J. D., J. J. Lawler, and N. LeRoy-Poff. 2008. Machine learning methods without tears: a primer for ecologists. Q. Rev. Biol. 83: 171-193.
46. Rajagopalan, J. K., M. Yasuno, and P.K.B. Menon. 1976. Density effect on survival of immature stages of Culex pipiens fatigans in breeding sites in Delhi Villages. Indian J. Med. Res. 64: 688-708.
47. Rajagopalan, J. K., P.K.B. Menon, T. R. Mani, and G. D. Brooks. 1975. Measurement of density of immatures of Culex pipiens fatigans in efßuent drains. J. Commun. Dis. 7: 327-337.
48. Reiskind, M. H., and M. L. Wilson. 2004. Culex restuans (Diptera: Culicidae) oviposition behavior determined by larval habitat quality and quantity in southeastern Michigan. J. Med. Entomol. 41: 179-186. (Pubitemid 38403258)
49. Richards, S. L., C. C. Lord, K. Pesko, and W. J. Tabachnick. 2009. Environmental and biological factors inßuencing Culex pipiens quinquefasciatus Say (Diptera: Culicidae) vector competence for St. Louis Encephalitis virus. Am. J. Trop. Med. Hyg. 81: 264-272.
50. Richards, S. L., C. C. Lord, K. N. Pesko, and W. J. Tabachnick. 2010. Environmental and biological factors inßuencing Culex pipiens quinquefasciatus (Diptera: Culicidae) vector competence for West Nile virus. Am. J. Trop. Med. Hyg. 83: 126-134.
51. Rockett, C. L. 1987. Bacteria as ovipositional attractants for Culex pipiens (Diptera, Culicidae). Gt. Lakes Entomol. 20: 151-155.
52. Sasa, M. 1965. Mosquito as the vector of lariasis. Jpn. J. Sanit. Zool. 16: 171.
53. Scorza, J. V. 1972. Observaciones bionomicas sobre Culex pipiens fatigans Wied, 1821 de Venezuela. Universidad de Los Andes, Merida, Venezuela.
54. Spencer, M., L. Blaustein, and J. E. Cohen. 2002. Oviposition habitat selection by mosquitoes (Culiseta longiareolata) and consequences for population size. Ecology 83: 669-679. (Pubitemid 36524155)
55. Spielman, A. 2001. Structure and seasonality of nearctic Culex pipiens populations. Ann. N.Y. Acad. Sci. 951: 220- 234. (Pubitemid 34060047)
56. Strickman, D. 1983. Preliminary report of seasonal oviposition by Culex quinquefasciatus in San Antonio, Texas. Mosq. News 43: 226-230.
57. Strickman, D. 1988. Rate of oviposition by Culex quinquefasciatus in San Antonio, Texas, during three years. J. Am. Mosq. Control Assoc. 4: 339-344.
58. Suenaga, O., W. Liu, J. Miao, and W. Xu. 1982. Seasonal change in the oviposition activity of Culex pipiens pallens in Shangai, China. Tropical Med. 24: 229-234. (Pubitemid 13135125)
59. Sunish, I. P., and R. R. Reuben. 2001. Factors inßuencing the abundance of Japanese encephalitis vectors in riceelds in India. Med. Vet. Entomol. 15: 381-392. (Pubitemid 34025621)
60. Sunish, I. P., R. D. Raghunatha, and A. Gajanana. 1998. Nitrogenous fertilizers, neem and vectors of Japanese encephalitis virus. Curr. Sci. 75: 1107.
61. Takken, W. 1999. Chemical signals affecting mosquito behaviour. Invertebr. Reprod. Dev. 36: 67-71. (Pubitemid 29407566)
62. Turell, M. J., M. R. Sardelis, D. J. Dohm, and M. L. O'Guinn. 2001. Potential North American vectors of West Nile virus. Ann. N.Y. Acad. Sci. 951: 317-324. (Pubitemid 34060055)
63. Venables, W. N., and B. D. Ripley. 2002. Modern applied statistics with S. Springer, New York, NY.
64. Wada, Y., and K. Ofuji. 1962. Studies on the Culex pipiens group of Japan: VI. On a case of the outbreak of Culex pipiens molestus Forskal in Nagasaki City. Endemic Dis. Bull. Nagasaki Univ. 4: 31-37.
65. Walker, E. D., D. L. Lawson, R. W. Merritt, W. T. Morgan, and M. J. Klug. 1991. Nutrient dynamics, bacterial-populations, and mosquito productivity in tree hole ecosystems and microcosms. Ecology 72: 1529-1546.
66. Weber, R. M., and R. G. Weber. 1985. The egg raft seam as an indicator of species in Culex pipiens and Culex restuans. Mosq. Syst. 17: 363-370.