Volume 88, Issue 3
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645



Temperature is one of the most important environmental factors affecting biological processes of mosquitoes, including their interactions with viruses. In these studies, we show independent effects of rearing temperature on the immature aquatic stages and holding temperature on the adult terrestrial stage in terms of alterations in adult survival and progression of dengue-1 virus infection in the Asian tiger mosquito () . Our studies show that adult survival was determined by adult-holding temperature, regardless of rearing conditions of the immature stages. In contrast, spread of virus throughout the body of the mosquito, a pre-requisite for transmission, was reduced when the immature stages were reared in cool conditions. These results show that immature-rearing temperature selectively modified mosquito traits that influence competency for viruses, and they further our understanding of the nature of temperature effects on interactions between mosquitoes and virus pathogens and risk of disease transmission.


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  1. Benedict MQ, Levine RS, Hawley WA, Lounibos LP, , 2007. Spread of the tiger: global risk of invasion by the mosquito Aedes albopictus . Vector Borne Zoonotic Dis 7: 7685.[Crossref] [Google Scholar]
  2. Effler PW, Pang L, Kitsutani P, Vorndam V, Nakata M, Ayers T, Elm J, Tom T, Reiter P, Rigau-Perez JG, Hayes JM, Mills K, Napier M, Clark GG, Gubler DJ, Hawaii Dengue Outbreak Investigation Team, , 2005. Dengue fever, Hawaii, 2001–2002. Emerg Infect Dis 11: 742749.[Crossref] [Google Scholar]
  3. Arankalle VA, Shrivastava S, Cherian S, Gunjikar RS, Walimbe AM, Jadhav SM, Sudeep AB, Mishra AC, , 2007. Genetic divergence of chikungunya viruses in India (1963–2006) with special reference to the 2005–2006 explosive epidemic. J Gen Virol 88: 19671976.[Crossref] [Google Scholar]
  4. Paquet C, Quatresovs I, Solet J-L, Sissoko D, Renault P, Pierre V, Cordel H, Lassalle C, Thiria J, Zeller H, , 2006. Chikungunya outbreak in reunion: epidemiology and surveillance, 2005 to early January 2006. Euro Surveill 11: E0602023. [Google Scholar]
  5. Rezza G, Nicoletti L, Angelini R, Romi R, Finarelli AC, Panning M, Cordioli P, Fortuna C, Boros S, Magurano F, Silvi G, Angelini P, Dottori M, Ciufolini MG, Majori GC, Cassone A, CHIKV study group, , 2007. Infection with chikungunya virus in Italy: an outbreak in a temperate region. Lancet 370: 18401846.[Crossref] [Google Scholar]
  6. Seneviratne SL, Gurugama P, Perera J, , 2007. Chikungunya viral infections: an emerging problem. J Travel Med 14: 320325.[Crossref] [Google Scholar]
  7. Ibañez-Bernal S, Briseño B, Mutebi J-P, Argot E, Rodriguez G, Martinez-Camposc C, Paz R, de la Fuente-San Roman P, Tapia-Conyer R, Flisser A, , 1997. First record in America of Aedes albopictus naturally infected with dengue virus during the 1995 outbreak at Reynosa, Mexico. Med Vet Entomol 11: 305309.[Crossref] [Google Scholar]
  8. Méndez F, Barreto M, Arias JF, Renfigo G, Muñoz J, Burbano ME, Parra B, , 2006. Human and mosquito infections by dengue viruses during and after epidemics in a dengue-endemic region of Colombia. Am J Trop Med Hyg 74: 678683. [Google Scholar]
  9. Lambrechts L, Scott TW, Gubler DJ, , 2010. Consequences of the expanding global distribution of Aedes albopictus for dengue virus transmission. PLoS Negl Trop Dis 4: e646.[Crossref] [Google Scholar]
  10. Holick J, Kyle A, Ferraro W, Delaney RR, Iwaseczko M, , 2002. Discovery of Aedes albopictus infected with West Nile virus in southeastern Pennsylvania. J Am Mosq Control Assoc 18: 131. [Google Scholar]
  11. Gerhardt RR, Gottfied KL, Apperson CS, Davis BS, Erwin PC, Smith AB, Panella NA, Powell EE, Nasci RS, , 2001. First isolation of La Crosse virus from naturally infected Aedes albopictus . Emerg Infect Dis 7: 807811.[Crossref] [Google Scholar]
  12. Mitchell CJ, Niebylski ML, Karabatsos N, Martin D, Mutebi J-P, Craig GB, Mahler MJ, , 1992. Isolation of eastern equine encephalitis from Aedes albopictus in Florida. Science 257: 526527.[Crossref] [Google Scholar]
  13. Barrera R, , 1996. Competition and resistance to starvation in larvae of container-inhabiting Aedes mosquitoes. Ecol Entomol 21: 117127.[Crossref] [Google Scholar]
  14. Juliano SA, , 1998. Species introduction and replacement among mosquitoes: interspecific resource competition or apparent competition? Ecology 79: 255268.[Crossref] [Google Scholar]
  15. Braks MAH, Honório NA, Lounibos LP, Lourenco-de-Oliveira R, Juliano SA, , 2004. Interspecific competition between two invasive species of container mosquitoes, Aedes aegypti and Aedes albopictus (Diptera: Culicidae), in Brazil. Ann Entomol Soc Am 97: 130139.[Crossref] [Google Scholar]
  16. Juliano SA, Lounibos LP, O'Meara GF, , 2004. A field test for competitive effects of Aedes albopictus on Aedes aegypti in south Florida: differences between sites of coexistence and exclusion? Oecologia 139: 583593.[Crossref] [Google Scholar]
  17. Murrell EG, Juliano SA, , 2008. Detritus type alters the outcome of interspecific competition between Aedes aegypti and Aedes albopictus (Diptera: Culicidae). J Med Entomol 45: 375383.[Crossref] [Google Scholar]
  18. Nawrocki SJ, Hawley WA, , 1987. Estimation of the northern limits of distribution of Aedes albopictus in North America. J Am Mosq Control Assoc 3: 314317. [Google Scholar]
  19. Davis NC, , 1932. The effect of various temperatures in modifying the extrinsic incubation period of the yellow fever virus in Aedes aegypti . Am J Hyg 16: 163176. [Google Scholar]
  20. Chamberlain RW, Sudia WD, , 1955. The effects of temperature upon the extrinsic incubation of eastern equine encephalitis in mosquitoes. Am J Hyg 62: 295305. [Google Scholar]
  21. Kay BH, Fanning ID, Mottram P, , 1989. The vector competence of Culex annulirostris, Aedes sagax and Aedes alboannulatus for Murray Valley encephalitis virus at different temperatures. Med Vet Entomol 3: 107112.[Crossref] [Google Scholar]
  22. Kay BH, Fanning ID, Mottram P, , 1989. Rearing temperature influences flavivirus vector competence of mosquitoes. Med Vet Entomol 3: 415422.[Crossref] [Google Scholar]
  23. Turell MJ, , 1993. Effect of environmental temperature on the vector competence of Aedes taeniorhynchus for Rift Valley fever and Venezuelan equine encephalitis viruses. Am J Trop Med Hyg 49: 672676. [Google Scholar]
  24. Richards SL, Mores CN, Lord CC, Tabachnick WJ, , 2007. Impact of extrinsic incubation temperature and virus exposure on vector competence of Culex pipiens quinqefasciatus (Diptera: Culicidae) for West Nile virus. Vector Borne Zoonotic Dis 7: 629636.[Crossref] [Google Scholar]
  25. Richards SL, Lord CC, Pesko KA, Tabachnick WJ, , 2009. Environmental and biological factors influencing Culex pipiens quinqefasciatus Say (Diptera: Culicidae) vector competence for Saint Louis encephalitis virus. Am J Trop Med Hyg 81: 264272. [Google Scholar]
  26. Kilpatrick MA, Meola MA, Moudy RM, Kramer LD, , 2008. Temperature, viral genetics, and the transmission of West Nile virus by Culex pipiens mosquitoes. PLoS Pathog 4: e1000092.[Crossref] [Google Scholar]
  27. Anderson SL, Richards SL, Smartt CT, Tabachnick WJ, , 2010. The effects of West Nile virus dose on temporal progression of vector competence in Culex pipiens quinquefasciatus Say (Diptera: Culicidae). J Am Mosq Control Assoc 26: 103107.[Crossref] [Google Scholar]
  28. Kramer LD, Hardy JL, Presser SB, , 1983. Effect of temperature of extrinsic incubation on the vector competence of Culex tarsalis for western equine encephalomyelitis virus. Am J Trop Med Hyg 32: 11301139. [Google Scholar]
  29. Hardy JL, Meyer RP, Presser SB, Milby MM, , 1990. Temporal variations in the susceptibility of a semi-isolated population of Culex tarsalis to peroral infection with western equine encephalomyelitis and St. Louis encephalitis viruses. Am J Trop Med Hyg 42: 500511. [Google Scholar]
  30. Hess AD, Cherubin CE, LaMotte LC, , 1963. Relation of temperature to activity of western and St. Louis encephalitis viruses. Am J Trop Med Hyg 12: 657667. [Google Scholar]
  31. Hardy JL, Rosen L, Kramer LD, Presser SB, Shroyer DA, Turell MJ, , 1980. Effect of rearing temperature on transovarial transmission of St. Louis encephalitits virus in mosquitoes. Am J Trop Med Hyg 29: 963968. [Google Scholar]
  32. Muturi EJ, Alto BW, , 2011. Larval environmental temperature and insecticide exposure alters Aedes aegypti competence for arboviruses. Vector Borne Zoonotic Dis 11: 11571163.[Crossref] [Google Scholar]
  33. Muturi EJ, Costanzo KS, Kesavaraju B, Lampman R, Alto BW, , 2011. Effect of temperature and insecticide stress on life-history traits of Culex restuans and Aedes albopictus (Diptera: Culicidae). J Med Entomol 48: 243250.[Crossref] [Google Scholar]
  34. Shang C-S, Fang C-T, Liu C-M, Wen T-H, Tsai K-H, King C-C, , 2010. The role of imported cases and favorable meteorological conditions in the onset of dengue epidemics. PLoS Negl Trop Dis 4: e775.[Crossref] [Google Scholar]
  35. Johansson MA, Dominici F, Glass GE, , 2009. Local and global effects of climate on dengue transmission in Puerto Rico. PLoS Negl Trop Dis 3: e382.[Crossref] [Google Scholar]
  36. Tsuzuki A, Duoc VT, Higa Y, Yen NT, Takagi M, , 2009. High potential risk of dengue transmission during the hot-dry season in Nha Trang City, Vietnam. Acta Trop 111: 325329.[Crossref] [Google Scholar]
  37. Watts DM, Burke DS, Harrison BA, Whitmire RE, Nisalak A, , 1987. Effect of temperature on the vector efficiency of Aedes aegypti for dengue 2 virus. Am J Trop Med Hyg 36: 143152. [Google Scholar]
  38. Wright RE, Knight KL, , 1966. Effect of environmental factors on biting activity of Aedes vexans (Meigen) and Aedes trivittatus (Coquillett). Mosq News 26: 565578. [Google Scholar]
  39. Rowley WA, Graham CL, , 1968. The effect of temperature and relative humidity on the flight performance of female Aedes aegypti . J Insect Physiol 14: 12511257.[Crossref] [Google Scholar]
  40. Meyer RP, Hardy JL, Reisen WK, , 1990. Diel changes in adult mosquito microhabitat temperatures and their relationship to the extrinsic incubation of arbovirues in mosquitoes in Kern County, California. J Med Entomol 27: 607614.[Crossref] [Google Scholar]
  41. Gray KM, Burkett-Cadena ND, Eubanks MD, Unnasch TR, , 2011. Crepuscular flight activity of Culex erraticus (Diptera: Culicidae). J Med Entomol 48: 167172.[Crossref] [Google Scholar]
  42. Briegel H, Timmermann SE, , 2001. Aedes albopictus (Diptera: Culicidae): physiological aspects of development and reproduction. J Med Entomol 38: 566571.[Crossref] [Google Scholar]
  43. Briegel H, Waltert A, Kuhn R, , 2001a. Reproductive physiology of Aedes (Aedimorphus) vexans (Diptera: Culicidae) in relation to flight potential. J Med Entomol 38: 557565.[Crossref] [Google Scholar]
  44. Briegel H, Knusel I, Timmermann SE, , 2001b. Aedes aegypti: size, reserves, survival, and flight potential. J Vector Ecol 26: 2131. [Google Scholar]
  45. O'Meara GF, Vose FE, Carlson DB, , 1989. Environmental factors influencing oviposition by Culex (Culex) (Diptera: Culicidae) in two types of traps. J Med Entomol 26: 528534.[Crossref] [Google Scholar]
  46. National Oceanic and Atmospheric Administration (NOAA). Available at: http://www.cpc.ncep.noaa.gov/products/analysis_monitoring/regional_monitoring/. Accessed July 1, 2012.
  47. Callahan JD, Wu S-JL, Dion-Schultz A, Mangold BV, Peruski LF, Watts DM, Porter KR, Murphy GR, Suharyono W, King C-C, Hayes CG, Temenak JJ, , 2001. Development and evaluation of serotype- and group-specific fluorogenic reverse transcriptase PCR (TaqMan) assays for dengue virus. J Clin Microbiol 39: 41194124.[Crossref] [Google Scholar]
  48. Alto BW, Lounibos LP, Mores CN, Reiskind MH, , 2008. Larval competition alters susceptibility of adult Aedes mosquitoes to dengue infection. Proc Biol Sci 275: 463471.[Crossref] [Google Scholar]
  49. Bustin SA, , 2000. Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. J Mol Endocrinol 25: 169193.[Crossref] [Google Scholar]
  50. Lounibos LP, Suárez S, Menéndez A, Nishimura N, Escher RL, O'Connell SM, Rey JR, , 2002. Does temperature affect the outcome of larval competition between Aedes aegypti and Aedes albopictus? J Vector Ecol 27: 8695. [Google Scholar]
  51. Delatte H, Gimonneau G, Triboire A, Fontenille D, , 2009. Influence of temperature on immature development, survival, longevity, fecundity, and gonotrophic cycles of Aedes albopictus, vector of chikungunya and dengue in the Indian Ocean. J Med Entomol 46: 3341.[Crossref] [Google Scholar]
  52. Westbrook CJ, Reiskind MH, Pesko KN, Green KE, Lounibos LP, , 2010. Larval environmental temperature and the susceptibility of Aedes albopictus Skuse (Diptera: Culicidae) to chikungunya virus. Vector Borne Zoonotic Dis 10: 241247.[Crossref] [Google Scholar]
  53. Reiskind MH, Zarrabi AA, , 2012. Is bigger really bigger? Differential responses to temperature in measures of body size of the mosquito, Aedes albopictus . J Insect Physiol 58: 911917.[Crossref] [Google Scholar]
  54. Nasci RC, , 1986. The size of emerging and host-seeking Aedes aegypti and the relation of size to blood-feeding success in the field. J Am Mosq Control Assoc 2: 6162. [Google Scholar]
  55. Hawley WA, , 1985. The effect of larval density on adult longevity of a mosquito, Aedes sierrensis: epidemiological consequences. J Anim Ecol 54: 955964.[Crossref] [Google Scholar]
  56. Haramis LD, Lounibos LP, Rey JR, Frank JH, , 1985. Larval nutrition, adult body size, and the biology of Aedes triseriatus . , eds. Ecology of Mosquitoes: Proceedings of a Workshop. Vero Beach, FL: Florida Medical Entomology Laboratory, 431437. [Google Scholar]
  57. Blanc G, Caminopetros J, , 1930. Recherches experimentales sur la dengue. Ann Inst Pasteur (Paris) 44: 392395. [Google Scholar]
  58. Rohani A, Wong YC, Zamre I, Lee HL, Zurainee MN, , 2009. The effect of extrinsic incubation temperature on development of dengue serotype 2 and 4 viruses in Aedes aegypti (L.). Southeast Asian J Trop Med Public Health 40: 942950. [Google Scholar]
  59. Fang-zhen X, Yi Z, Han-guo X, Wen-qi S, Si H, Yan-qin D, Xiao-nong Z, Yan-sheng Y, , 2012. Effect of temperatures on extrinsic incubation period of dengue virus type 2 in Aedes albopictus . Chin J Zoonoses 28: 108110. [Google Scholar]
  60. Grimstad PR, Walker ED, , 1991. Aedes triseriatus (Dipera: Culicidae) and La Crosse virus. IV. Nutritional deprivation of larvae affects the adult barriers to infection and transmission. J Med Entomol 28: 378386.[Crossref] [Google Scholar]
  61. Yadav P, Barde PV, Gokhale MD, Vipat V, Mishra AC, Pal JK, Mourya DT, , 2005. Effect of temperature and insecticide stresses on Aedes aegypti larvae and their influence on the susceptibility of mosquitoes to dengue-2 virus. Southeast Asian J Trop Med Public Health 36: 11391144. [Google Scholar]
  62. Muturi EJ, Kim C-H, Alto BW, Berenbaum M, Schuler M, , 2011b. Larval environmental stress alters Aedes aegypti competence for Sindbis virus. Trop Med Int Health 16: 955964.[Crossref] [Google Scholar]
  63. Lambrechts L, Paaijmans KP, Fansiri T, Carrington LB, Kramer LD, Thomas MB, Scott TW, , 2011. Impact of daily temperature fluctuations on dengue virus transmission by Aedes aegypti . Proc Natl Acad Sci USA 108: 74607465.[Crossref] [Google Scholar]
  64. Paaijmans KP, Read AF, Thomas MB, , 2009. Understanding the link between malaria risk and climate. Proc Natl Acad Sci USA 106: 1384413849.[Crossref] [Google Scholar]
  65. Paaijmans KP, Blanford S, Bell AS, Blanford JI, Read AF, Thomas MB, , 2010. Influence of climate on malaria transmission depends on daily temperature variation. Proc Natl Acad Sci USA 107: 1513515139.[Crossref] [Google Scholar]
  66. Focks DA, Daniels E, Haile DG, Keesling JE, , 1995. A simulation model of the epidemiology of urban dengue fever: literature analysis, model development, preliminary validation, and samples of simulation results. Am J Trop Med Hyg 53: 489506. [Google Scholar]
  67. Lu L, Lin H, Tian L, Yang W, Sun J, Liu Q, , 2009. Time series analysis of dengue fever and weather in Guangzhou, China. BMC Public Health 9: 395.[Crossref] [Google Scholar]
  68. Richards SL, Anderson SL, Lord CC, Smart CT, Tabachnick WJ, , 2012. Relationships between infection, dissemination, and transmission of West Nile virus RNA in Culex pipiens quinquefasciatus (Diptera: Culicidae). J Med Entomol 49: 132142.[Crossref] [Google Scholar]
  69. Murdock CC, Paaijman KP, Bell AS, King JG, Hillyer JF, Read AF, Thomas MB, , 2012. Complex effects of temperature on mosquito immune function. Proc Biol Sci 279: 33573366.[Crossref] [Google Scholar]
  70. Adams B, Boots M, , 2010. How important is vertical transmission in mosquitoes for the persistence of dengue? Insights from a mathematical model. Epidemics 2: 110.[Crossref] [Google Scholar]
  71. Thongrungkiat S, Maneekan P, Wasinpiyamongkol L, Prummongkol S, , 2010. Prospective field study of transovarial dengue-virus transmission by two different forms of Aedes aegypti in an urban area of Bangkok, Thailand. J Vector Ecol 36: 147152.[Crossref] [Google Scholar]

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  • Received : 09 Jul 2012
  • Accepted : 18 Nov 2012
  • Published online : 06 Mar 2013

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