Reduction of Aedes aegypti Vector Competence for Dengue Virus under Large Temperature Fluctuations

Lauren B. Carrington Department of Entomology, University of California, Davis, Califronia; Insects and Infectious Diseases, Centre National de la Recherche Scientifique, Unite de Recherche Associee 3012, Institut Pasteur, Paris, France; Fogarty International Center, National Institutes of Health, Bethesda, Maryland

Search for other papers by Lauren B. Carrington in
Current site
Google Scholar
PubMed
Close
,
Stephanie N. Seifert Department of Entomology, University of California, Davis, Califronia; Insects and Infectious Diseases, Centre National de la Recherche Scientifique, Unite de Recherche Associee 3012, Institut Pasteur, Paris, France; Fogarty International Center, National Institutes of Health, Bethesda, Maryland

Search for other papers by Stephanie N. Seifert in
Current site
Google Scholar
PubMed
Close
,
M. Veronica Armijos Department of Entomology, University of California, Davis, Califronia; Insects and Infectious Diseases, Centre National de la Recherche Scientifique, Unite de Recherche Associee 3012, Institut Pasteur, Paris, France; Fogarty International Center, National Institutes of Health, Bethesda, Maryland

Search for other papers by M. Veronica Armijos in
Current site
Google Scholar
PubMed
Close
,
Louis Lambrechts Department of Entomology, University of California, Davis, Califronia; Insects and Infectious Diseases, Centre National de la Recherche Scientifique, Unite de Recherche Associee 3012, Institut Pasteur, Paris, France; Fogarty International Center, National Institutes of Health, Bethesda, Maryland

Search for other papers by Louis Lambrechts in
Current site
Google Scholar
PubMed
Close
, and
Thomas W. Scott Department of Entomology, University of California, Davis, Califronia; Insects and Infectious Diseases, Centre National de la Recherche Scientifique, Unite de Recherche Associee 3012, Institut Pasteur, Paris, France; Fogarty International Center, National Institutes of Health, Bethesda, Maryland

Search for other papers by Thomas W. Scott in
Current site
Google Scholar
PubMed
Close
Restricted access

Diurnal temperature fluctuations can fundamentally alter mosquito biology and mosquito-virus interactions in ways that impact pathogen transmission. We investigated the effect of two daily fluctuating temperature profiles on Aedes aegypti vector competence for dengue virus (DENV) serotype-1. A large diurnal temperature range of 18.6°C around a 26°C mean, corresponding with the low DENV transmission season in northwestern Thailand, reduced midgut infection rates and tended to extend the virus extrinsic incubation period. Dissemination was first observed at day 7 under small fluctuations (7.6°C; corresponding with high DENV transmission) and constant control temperature, but not until Day 11 for the large diurnal temperature range. Results indicate that female Ae. aegypti in northwest Thailand are less likely to transmit DENV during the low than high transmission season because of reduced DENV susceptibility and extended virus extrinsic incubation period. Better understanding of DENV transmission dynamics will come with improved knowledge of temperature effects on mosquito-virus interactions.

Author Notes

* Address correspondence to Lauren B. Carrington, Department of Entomology, University of California, 1 Shields Avenue, Davis, CA 95616. E-mail: lbcarrington@ucdavis.edu

Financial support: The study was supported by grant EF-0914384 from the Ecology of Infectious Disease Program of the National Science Foundation. Thomas W. Scott acknowledges funding from the Research and Policy for Infectious Disease Dynamics Program.

Authors' addresses: Lauren B. Carrington, Nossal Institute for Global Health, University of Melbourne, Carlton, VIC, Australia, E-mail: lbcarrington@gmail.com. M. Veronica Armijos, Department of Entomology, University of California, Davis, CA, E-mail: mvarmijos@ucdavis.edu. Stephanie N. Seifert, Department of Biology, University of Pennsylvania, Philadelphia, PA, E-mail: seifst@sas.upenn.edu. Louis Lambrechts, Insects and Infectious Diseases, Centre National de la Recherche Scientifique, Unite de Recherche Associee 3012, Institut Pasteur, Paris Cedex 15, France, E-mail: louis.lambrechts@pasteur.fr. Thomas W. Scott, Department of Entomology, University of California, Davis, CA, and Fogarty International Center, National Institutes of Health, Bethesda, MD, E-mail: twscott@ucdavis.edu.

  • 1.

    Nisalak A, Endy TP, Nimmannitya S, Kalayanarooj UT, Scott RM, Burke DS, Hoke CH, Innis BL, Vaughn DW, 2003. Serotype-specific dengue virus circulation and dengue disease in Bangkok, Thailand from 1973 to 1999. Am J Trop Med Hyg 68: 191202.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2.

    McLean DM, Miller MA, Grass PN, 1975. Dengue virus transmission by mosquitoes incubated at low temperatures. Mosq News 35: 322327.

  • 3.

    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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    Bates M, Roca-Garcia M, 1946. The development of the virus of yellow fever in haemagogus mosquitoes. Am J Trop Med Hyg 26: 585605.

  • 6.

    Chamberlain RW, Sudia WD, 1955. The effects of temperature upon the extrinsic incubation of eastern equine encephalitis in mosquitoes. Am J Hyg 62: 295305.

  • 7.

    Turell MJ, Lundstrom JO, 1990. Effect of environmental temperature on the vector competence of Aedes aegypti and Ae. taeniorhynchus for Ockelbo virus. Am J Trop Med Hyg 43: 543550.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8.

    Lundstrom JO, Turell MJ, Niklasson B, 1990. Effect of environmental temperature on the vector competence of Culex pipiens and Cx. torrentium for Ockelbo virus. Am J Trop Med Hyg 43: 534542.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Parton WJ, Logan JE, 1981. A model for diurnal variation in soil and air temperature. Agric Meteorol 23: 205216.

  • 11.

    Maciel-de-Freitas R, Koella JC, Lourenço-de-Oliveira R, 2009. Lower survival rate, longevity and fecundity of Aedes aegypti (Diptera: Culicidae) females orally challenged with dengue virus serotype 2. Trans R Soc Trop Med Hyg 105: 452458.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Lambrechts L, Scott TW, 2009. Mode of transmission and the evolution of arbovirus virulence in mosquito vectors. Proc R Soc Lond B Biol Sci 276: 13691378.

  • 13.

    Alto BW, Reiskind MH, Lounibos LP, 2008. Size alters susceptibility of vectors to dengue virus infection and dissemination. Am J Trop Med Hyg 79: 688695.

  • 14.

    Westbrook CJ, Reiskind MH, Pesko K, Greene KE, Lounibos LP, 2010. Larval environmental temperature and the susceptibility of Aedes albopiictus Skuse (Diptera: Culicidae) to Chikungunya virus. Vector Borne Zoonotic Dis 10: 241247.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Muturi EJ, Alto BW, 2011. Larval environmental temperature and insecticide exposure alter Aedes aegypti competence for arboviruses. Vector Borne Zoonotic Dis 11: 11571163.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16.

    Carrington LB, Seifert SN, Willits NH, Lambrechts L, Scott TW, 2013. Large diurnal temperature fluctuations negatively influence Aedes aegypti (Diptera: Culicidae) life history traits. J Med Entomol 50: 4351.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    Harrington LC, Scott TW, Lerdthusnee K, Coleman RC, Costero A, Clark GG, Jones JJ, Kitthawee S, Kittayapong P, Sithiprasasna R, Edman JD, 2005. Dispersal of the dengue vector Aedes aegypti within and between rural communities. Am J Trop Med Hyg 72: 209220.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Payne AF, Binduga-Gajewska I, Kauffman EB, Kramer LD, 2006. Quantitation of falviviruses by fluorescent focus assay. J Virol Methods 134: 183189.

  • 19.

    Lambrechts L, Chevillon C, Albright RG, Thaisomboonsuk B, Richardson JH, Jarman RG, Scott TW, 2009. Genetic specificity and potential for local adaptation between dengue viruses and mosquito vectors. BMC Evol Biol 9: 160.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Gubler DJ, Suharyono W, Lubis I, Eram S, Gunarso S, 1981. Epidemic dengue 3 in central Java, associated with low viremia in man. Am J Trop Med Hyg 30: 10941099.

  • 21.

    Gubler DJ, Suharyono W, Tan R, Abidin M, Sie A, 1981. Viraemia in patients with naturally acquired dengue infection. Bull World Health Organ 59: 623630.

  • 22.

    Lambrechts L, Fansiri T, Pongsiri A, Thaisomboonsuk B, Klungthong C, Richardson JH, Ponlawat A, Jarman RG, Scott TW, 2012. Dengue-1 virus clade replacement in Thailand associated with enhanced mosquito transmission. J Virol 86: 18531861.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    McLean DM, Clarke AM, Coleman JC, Montalbetti CA, Skidmore AG, Walters TE, Wise R, 1974. Vector capability of Aedes aegypti mosquitoes for California encephalitis and dengue viruses at various temperatures. Can J Microbiol 20: 255262.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24.

    Styer LM, Carey JR, Wang J-L, Scott TW, 2007. Mosquitoes do senesce: departure from the paradigm of constant mortality. Am J Trop Med Hyg 76: 111117.

  • 25.

    Harrington LC, Vermeylen F, Jones JJ, Kitthawee S, Sithiprasasna R, Edman JD, Scott TW, 2008. Age-dependent survival of the dengue vector Aedes aegypti (Diptera: Culicidae) demonstrated by simultaneous release-recapture of different age cohorts. J Med Entomol 45: 307313.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Feder ME, Hoffman GE, 1999. Heat shock proteims, molecular chaperones and the heat shock response: evolutionary and ecological physiology. Annu Rev Physiol 61: 243282.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    Ciota AT, Styer LM, Meola MA, Kramer LD, 2011. The costs of resistance and infection as determinants of West Nile virus susceptibility in Culex mosquitoes. BMC Ecol 11: 23.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    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.

    • PubMed
    • Search Google Scholar
    • Export Citation
Past two years Past Year Past 30 Days
Abstract Views 1270 990 174
Full Text Views 695 26 0
PDF Downloads 315 26 0
 

 

 

 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save