Effects of the Environmental Temperature on Aedes aegypti and Aedes albopictus Mosquitoes: A Review

Joanna M Reinhold, Claudio R Lazzari, Chloé Lahondère, Joanna M Reinhold, Claudio R Lazzari, Chloé Lahondère

Abstract

The temperature of the environment is one of the most important abiotic factors affecting the life of insects. As poikilotherms, their body temperature is not constant, and they rely on various strategies to minimize the risk of thermal stress. They have been thus able to colonize a large spectrum of habitats. Mosquitoes, such as Ae. aegypti and Ae. albopictus, vector many pathogens, including dengue, chikungunya, and Zika viruses. The spread of these diseases has become a major global health concern, and it is predicted that climate change will affect the mosquitoes' distribution, which will allow these insects to bring new pathogens to naïve populations. We synthesize here the current knowledge on the impact of temperature on the mosquito flight activity and host-seeking behavior (1); ecology and dispersion (2); as well as its potential effect on the pathogens themselves and how climate can affect the transmission of some of these pathogens (3).

Keywords: West Nile virus; Zika virus; blood-feeding; chikungunya virus; dengue virus complex; dispersion; gonotrophic cycle; pathogen transmission; thermotolerance; yellow fever virus.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
The temperature of the environment (Ta) affects the mosquito development (blue), its activity including host-seeking and blood-meal intake (red), as well as pathogen development and transmission (purple). Consequently, Ta affects species geographic repartition, spatial distribution, and population dynamics (green). The dashed square represents the cycles related to mosquito biology.

References

    1. Denlinger D.L., Yocum G.D. Physiology of heat sensitivity. In: Hallman G.J., Denlinger D.L., editors. Temperature Sensitivity in Insects and Application in Integrated Pest Management. Westview Press; Boulder, CO, USA: Oxford, UK: 1998. pp. 7–53.
    1. Heinrich B. The Hot-Blooded Insects: Strategies and Mechanisms of Thermoregulation. Harvard University Press; Cambridge, MA, USA: 1993. p. 600.
    1. Huey R.B., Stevenson R.D. Integrating thermal physiology and ecology of ectotherms: A discussion of approaches. Am. Zool. 1979;19:357–366. doi: 10.1093/icb/19.1.357.
    1. Benoit J.B., Lopez-Martinez G., Patrick K.R., Phillips Z.P., Krause T.B., Denlinger D.L. Drinking a hot blood meal elicits a protective heat shock response in mosquitoes. Proc. Natl. Acad. Sci. USA. 2011 doi: 10.1073/pnas.1105195108.
    1. Lahondère C., Lazzari C.R. Mosquitoes cool down during blood feeding to avoid overheating. Curr. Biol. 2012;22:40–45. doi: 10.1016/j.cub.2011.11.029.
    1. Angilletta M.J. Thermal Adaptation: A Theoretical and Empirical Synthesis. Oxford University Press; New York, NY, USA: 2009. p. 304.
    1. World Health Statistics (WHO) Monitoring Health for the SDGs, Sustainable Development Goals. World Health Organization; Geneva, Switzerland: 2018. Licence: CC BY-NC-SA 3.0 IGO.
    1. World Health Organization . Handbook for Integrated Vector Management. World Health Organization; Geneva, Switzerland: 2012.
    1. Matthews G. Integrated Vector Management: Controlling Vectors of Malaria and Other Insect Vector Borne Diseases. John Wiley & Sons; Hoboken, NJ, USA: 2011.
    1. Janzen D.H. On ecological fitting. Oikos. 1985;45:308–310. doi: 10.2307/3565565.
    1. IPCC . In: Climate Change 2014: Synthesis Report. Pachauri R.K., Meyer L.A., editors. IPCC; Geneva, Switzerland: 2014. 151p Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change.
    1. Christophers S.R. Aedes aegypti (L.) the Yellow Fever Mosquito. Cambridge University Press; London, UK: 1960.
    1. Delatte H., Desvars A., Bouétard A., Bord S., Gimonneau G., Vourc’h G., Fontenille D. Blood-feeding behavior of Aedes albopictus, a vector of Chikungunya on La Réunion. Vector-Borne Zoonotic. 2010;10:249–258. doi: 10.1089/vbz.2009.0026.
    1. Harrington L.C., Edman J.D., Scott T.W. Why do female Aedes aegypti (Diptera: Culicidae) feed preferentially and frequently on human blood? J. Med. Entomol. 2001;38:411–422. doi: 10.1603/0022-2585-38.3.411.
    1. Lewis D.J. Observations on Aedes aegypti, L. (Dipt. Culic.) under controlled atmospheric conditions. B Entomol. Res. 1933;24:363–372. doi: 10.1017/S0007485300031692.
    1. Otto M., Neumann R.O. Studien über Gelbfieber in Brasilien. Z. Hyg. InfektKr. 1905;51:357–506. doi: 10.1007/BF02141134.
    1. Rowley W.A., Graham C.L. The effect of temperature and relative humidity on the flight performance of female Aedes aegypti. J. Insect Physiol. 1968;14:1251–1257. doi: 10.1016/0022-1910(68)90018-8.
    1. Bowen M.F. The sensory physiology of host-seeking behavior in mosquitoes. Annu. Rev. Entomol. 1991;36:139–158. doi: 10.1146/annurev.en.36.010191.001035.
    1. Corfas R.A., Vosshall L.B. The cation channel TRPA1 tunes mosquito thermotaxis to host temperatures. eLife. 2015;4:e11750. doi: 10.7554/eLife.11750.
    1. Zermoglio P.F., Robuchon E., Leonardi M.S., Chandre F., Lazzari C.R. What does heat tell a mosquito? Characterization of the orientation behaviour of Aedes aegypti towards heat sources. J. Insect Physiol. 2017;100:9–14. doi: 10.1016/j.jinsphys.2017.04.010.
    1. Bishop A., Gilchrist B.M. Experiments upon the feeding of Aedes aegypti through animal membranes with a view to applying this method to the chemotherapy of malaria. Parasitology. 1946;37:85–100. doi: 10.1017/S0031182000013202.
    1. Connor M.E. Suggestions for Developing a Campaign to Control Yellow Fever. Am. J. Trop. Med. Hyg. 1924;1:277–307. doi: 10.4269/ajtmh.1924.s1-4.277.
    1. Cossio V. Observations sobre al Aedes aegypti (Stegomyia) mosquito de la febbre amarilla en Montevideo. Bol. Cons. Nat. Hig. Uruguay. 1931;23:1664.
    1. Marchoux E., Salimbeni A.T., Simond P.L. La Fièvre Jaune: Rapport de la Mission Française. Annales de l’Institut Pasteur; Paris, France: 1903.
    1. Scott T.W., Clark G.G., Amerasinghe P.H., Lorenz L.H., Reiter P., Edman J.D. Detection of multiple blood feeding patterns in Aedes aegypti (Diptera: Culicidae) during a single gonotrophic cycle using a histological technique. J. Med. Entomol. 1993;30:94–99. doi: 10.1093/jmedent/30.1.94.
    1. Scott T.W., Amerasinghe P.H., Morrison A.C., Lorenz L.H., Clark G.G., Strickman D., Kittayapong P., Edman J.D. Longitudinal studies of Aedes aegypti (Diptera: Culicidae) in Thailand and Puerto Rico: Blood feeding frequency. J. Med. Entomol. 2000;37:89–101. doi: 10.1603/0022-2585-37.1.89.
    1. Yasuno M., Pant C. Seasonal changes in biting and larval infestation rates of Aedes aegypti in Bangkok, Thailand in 1969. Bull. WHO. 1970;43:319–325.
    1. Delatte H., Gimonneau G., Triboire A., Fontenille D. 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. 2009;46:33–41. doi: 10.1603/033.046.0105.
    1. Löwenberg Neto P., Navarro-Silva M.A. Development, longevity, gonotrophic cycle and oviposition of Aedes albopictus Skuse (Diptera: Culicidae) under cyclic temperatures. Neotrop. Entomol. 2004;33:29–33. doi: 10.1590/S1519-566X2004000100006.
    1. Carrington L.B., Armijos M.V., Lambrechts L., Barker C.M., Scott T.W. Effects of fluctuating daily temperatures at critical thermal extremes on Aedes aegypti life-history traits. PLoS ONE. 2013;8:e58824. doi: 10.1371/journal.pone.0058824.
    1. Carrington L.B., Seifert S.N., Willits N.H., Lambrechts L., Scott T.W. Large diurnal temperature fluctuations negatively influence Aedes aegypti (Diptera: Culicidae) life history traits. J. Med. Entomol. 2013;50:43–51. doi: 10.1603/ME11242.
    1. Couret J., Benedict M.Q. A meta-analysis of the factors influencing development rate variation in Aedes aegypti (Diptera: Culicidae) BMC Ecol. 2014;14:3. doi: 10.1186/1472-6785-14-3.
    1. Couret J., Dotson E., Benedict M.Q. Temperature, larval diet, and density effects on development rate and survival of Aedes aegypti (Diptera: Culicidae) PLoS ONE. 2014;9:e87468. doi: 10.1371/journal.pone.0087468.
    1. Bar-Zeev M. The effect of temperature on the growth rate and survival of the immature stages of Aedes aegypti (L.) Bull. Entomol. Res. 1958;49:157–163. doi: 10.1017/S0007485300053499.
    1. Bar-Zeev M. The effect of extreme temperatures on different stages of Aedes aegypti (L.) Bull. Entomol. Res. 1957;48:593–599. doi: 10.1017/S0007485300002765.
    1. Teng H.J., Apperson C.S. Development and survival of immature Aedes albopictus and Aedes triseriatus (Diptera: Culicidae) in the laboratory: Effects of density, food, and competition on response to temperature. J. Med. Entomol. 2000;37:40–52. doi: 10.1603/0022-2585-37.1.40.
    1. Mori A., Oda T., Wada Y. Studies on the egg diapause and overwintering of Aedes albopictus in Nagasaki. Trop. Med. 1981;23:79–90.
    1. Higa Y., Toma T., Araki Y., Onodera I., Miyagi I. Seasonal changes in oviposition activity, hatching and embryonation rates of eggs of Aedes albopictus (Diptera: Culicidae) on three islands of the Ryukyu Archipelago, Japan. Med. Entomol. Zool. 2007;58:1–10. doi: 10.7601/mez.58.1_1.
    1. Hawley W.A., Pumpuni C.B., Brady R.H., Craig G.B., Jr. Overwintering survival of Aedes albopictus (Diptera: Culicidae) eggs in Indiana. J. Med. Entomol. 1989;26:122–129. doi: 10.1093/jmedent/26.2.122.
    1. Hanson S.M., Craig G.B., Jr. Cold acclimation, diapause, and geographic origin affect cold hardiness in eggs of Aedes albopictus (Diptera: Culicidae) J. Med. Entomol. 1994;31:192–201. doi: 10.1093/jmedent/31.2.192.
    1. Soper F.L. Dynamics of Aedes aegypti distribution and density. Seasonal fluctuations in the Americas. Bull. WHO. 1967;36:536.
    1. Rozeboom L.E. Overwintering of Aedes aegypti in Stillwater. Proc. Okla. Acad. Sci. 1938;19:81–82.
    1. Lima A., Lovin D.D., Hickner P.V., Severson D.W. Evidence for an overwintering population of Aedes aegypti in Capitol Hill neighborhood, Washington, DC. Am. J. Trop. Med. Hyg. 2016;94:231–235. doi: 10.4269/ajtmh.15-0351.
    1. Tsunoda T., Cuong T.C., Dong T.D., Yen N.T., Le N.H., Phong T.V., Minakawa N. Winter refuge for Aedes aegypti and Ae. albopictus mosquitoes in Hanoi during Winter. PLoS ONE. 2014;9:e95606. doi: 10.1371/journal.pone.0095606.
    1. Lambrechts L., Paaijmans K.P., Fansiri T., Carrington L.B., Kramer L.D., Thomas M.B., Scott T.W. Impact of daily temperature fluctuations on dengue virus transmission by Aedes aegypti. Proc. Natl. Acad. Sci. USA. 2011;108:7460–7465. doi: 10.1073/pnas.1101377108.
    1. Elbers A.R.W., Koenraadt C.J., Meiswinkel R. Mosquitoes and Culicoides biting midges: Vector range and the influence of climate change. Rev. Sci. Tech. Off. Int. Epizoot. 2015;34:123–137. doi: 10.20506/rst.34.1.2349.
    1. Suwonkerd W., Tsuda Y., Takagi M., Wada Y. Seasonal occurrence of Aedes aegypti and Ae. albopictus in used tires in 1992–1994, Chiangmai, Thailand. Trop. Med. 1997;38:101–105.
    1. Mogi M. Overwintering strategies of mosquitoes (Diptera: Culicidae) on warmer islands may predict impact of global warming on Kyushu, Japan. J. Med. Entomol. 1996;33:438–444. doi: 10.1093/jmedent/33.3.438.
    1. Tsunoda T., Chaves L.F., Nguyen G.T.T., Nguyen Y.T., Takagi M. Winter Activity and Diapause of Aedes albopictus (Diptera: Culicidae) in Hanoi, Northern Vietnam. J. Med. Entomol. 2015;52:1203–1212. doi: 10.1093/jme/tjv122.
    1. Tsuda Y., Suwonkerd W., Chawprom S., Prajakwong S., Takagi M. Different spatial distribution of Aedes aegypti and Aedes albopictus along an urban–rural gradient and the relating environmental factors examined in three villages in northern Thailand. J. Am. Mosq. Control. 2006;22:222–228. doi: 10.2987/8756-971X(2006)22[222:DSDOAA];2.
    1. Weaver S.C., Reisen W.K. Present and future arboviral threats. Antivir. Res. 2010;85:328–345. doi: 10.1016/j.antiviral.2009.10.008.
    1. Jansen C.C., Beebe N.W. The dengue vector Aedes aegypti: What comes next. Microbes Infect. 2010;12:272–279. doi: 10.1016/j.micinf.2009.12.011.
    1. Chaves L.F., Morrison A.C., Kitron U.D., Scott T.W. Nonlinear impacts of climatic variability on the density-dependent regulation of an insect vector of disease. Glob. Chang. Biol. 2012;18:457–468. doi: 10.1111/j.1365-2486.2011.02522.x.
    1. Chaves L.F., Scott T.W., Morrison A.C., Takada T. Hot temperatures can force delayed mosquito outbreaks via sequential changes in Aedes aegypti demographic parameters in autocorrelated environments. Acta Trop. 2014;129:15–24. doi: 10.1016/j.actatropica.2013.02.025.
    1. Lewontin R., Levins R. Schmalhausen’s law. Capital. Natl. Soc. 2000;11:103–108. doi: 10.1080/10455750009358943.
    1. Chaves L.F. Globally invasive, withdrawing at home: Aedes albopictus and Aedes japonicus facing the rise of Aedes flavopictus. Int. J. Biometeorol. 2016;60:1727–1738. doi: 10.1007/s00484-016-1162-7.
    1. Chaves L.F. Climate change and the biology of insect vectors of human pathogens. Glob. Clim. Chang. Terr. Invertebr. 2017:126–147. doi: 10.1002/9781119070894.ch8.
    1. Higa Y., Thi Yen N., Kawada H., Hai Son T., Thuy Hoa N., Takagi M. Geographic distribution of Aedes aegypti and Aedes albopictus collected from used tires in Vietnam. J. Am. Mosq. Control. 2010;26:1–9. doi: 10.2987/09-5945.1.
    1. Kraemer M.U., Sinka M.E., Duda K.A., Mylne A.Q., Shearer F.M., Barker C.M., Moore C.G., Carvalho R.G., Coelho G.E., Van Bortel W., et al. The global distribution of the arbovirus vectors Aedes aegypti and Ae. albopictus. eLife. 2015;4:e08347. doi: 10.7554/eLife.08347.
    1. Romi R., Di Luca M., Marjori G. Current status of Aedes albopictus and Aedes atropalpus in Italy. J. Am. Mosq. Control. 1999;15:425–427.
    1. Benedict M.Q., Levine R.S., Hawley W.A., Lounibos L.P. Spread of the tiger: Global risk of invasion by the mosquito Aedes albopictus. Vector-Borne Zoonotic. 2007;7:76–85. doi: 10.1089/vbz.2006.0562.
    1. Kearney M., Porter W.P., Williams C., Ritchie S., Hoffmann A.A. Integrating biophysical models and evolutionary theory to predict climatic impacts on species’ ranges: The dengue mosquito Aedes aegypti in Australia. Funct. Ecol. 2009;23:528–538. doi: 10.1111/j.1365-2435.2008.01538.x.
    1. Alto B.W., Juliano S.A. Precipitation and temperature effects on populations of Aedes albopictus (Diptera: Culicidae): Implications for range expansion. J. Med. Entomol. 2001;38:646–656. doi: 10.1603/0022-2585-38.5.646.
    1. Yang H.M., Macoris M.D.L.D.G., Galvani K.C., Andrighetti M.T.M., Wanderley D.M.V. Assessing the effects of temperature on the population of Aedes aegypti, the vector of dengue. Epidemiol. Infect. 2009;137:1188–1202. doi: 10.1017/S0950268809002040.
    1. O’meara G.F., Evans L.F., Jr., Gettman A.D., Cuda J.P. Spread of Aedes albopictus and decline of Ae. aegypti (Diptera: Culicidae) in Florida. J. Med. Entomol. 1995;32:554–562. doi: 10.1093/jmedent/32.4.554.
    1. Lounibos L.P., Suárez S., Menéndez Z., Nishimura N., Escher R.L., OConnell S.M., Rey J.R. Does temperature affect the outcome of larval competition between Aedes aegypti and Aedes albopictus? J. Vector Ecol. 2002;27:86–95.
    1. Kobayashi M., Nihei N., Kurihara T. Analysis of northern distribution of Aedes albopictus (Diptera: Culicidae) in Japan by geographical information system. J. Med. Entomol. 2002;39:4–11. doi: 10.1603/0022-2585-39.1.4.
    1. Mogi M., Tuno N. Impact of climate change on the distribution of Aedes albopictus (Diptera: Culicidae) in northern Japan: Retrospective analyses. J. Med. Entomol. 2014;51:572–579. doi: 10.1603/ME13178.
    1. Epstein P.R., Diaz H.F., Elias S., Grabherr G., Graham N.E., Martens W.J., MosIey-Thompson E., Susskind J. Biological and physical signs of climate change: Focus on mosquito-borne diseases. Bull. Am. Meteorol. Soc. 1998;79:409–417. doi: 10.1175/1520-0477(1998)079<0409:BAPSOC>;2.
    1. Ostfeld R.S. Climate change and the distribution and intensity of infectious diseases. Ecology. 2009;90:903–905. doi: 10.1890/08-0659.1.
    1. Patz J.A., Martens W.J., Focks D.A., Jetten T.H. Dengue fever epidemic potential as projected by general circulation models of global climate change. Environ. Health Perspect. 1998;106:147. doi: 10.1289/ehp.98106147.
    1. Sutherst R.W. Implications of global change and climate variability for vector-borne diseases: Generic approaches to impact assessments. Int. J. Parasitol. 1998;28:935–945. doi: 10.1016/S0020-7519(98)00056-3.
    1. Rochlin I., Ninivaggi D.V., Hutchinson M.L., Farajollahi A. Climate change and range expansion of the Asian tiger mosquito (Aedes albopictus) in Northeastern USA: Implications for public health practitioners. PLoS ONE. 2013;8:e60874. doi: 10.1371/journal.pone.0060874.
    1. Kramer L.D., Ebel G.D. Dynamics of flavivirus infection in mosquitoes. Adv. Virus Res. 2003;60:187–232.
    1. Gratz N.G. Critical review of the vector status of Aedes albopictus. Med. Vet. Entomol. 2004;18:215–227. doi: 10.1111/j.0269-283X.2004.00513.x.
    1. Vega-Rúa A., Zouache K., Girod R., Failloux A.B., Lourenço-de-Oliveira R. High vector competence of Aedes aegypti and Aedes albopictus from ten American countries as a crucial factor of the spread of Chikungunya. J. Virol. 2014:JVI-00370. doi: 10.1128/JVI.00370-14.
    1. Brady O.J., Golding N., Pigott D.M., Kraemer M.U., Messina J.P., Reiner R.C., Jr., Scott T.W., Smith D.L., Gething P.W., Hay S.I. Global temperature constraints on Aedes aegypti and Aedes albopictus persistence and competence for dengue virus transmission. Parasite Vector. 2014;7:338. doi: 10.1186/1756-3305-7-338.
    1. Patz J.A., Githeko A.K., McCarty J.P., Hussein S., Confalonieri U., De Wet N. Climate change and infectious diseases. Clim. Chang. Hum. Health Risks Responses. 2003;6:103–137.
    1. Lafferty K.D. The ecology of climate change and infectious diseases. Ecology. 2009;90:888–900. doi: 10.1890/08-0079.1.
    1. McMichael A.J., Woodruff R.E. Climate change and infectious diseases. Soc. Ecol. Infect. Dis. 2008:378–407. doi: 10.1016/B978-012370466-5.50019-4.
    1. World Health Organization Dengue and Severe Dengue. [(accessed on 13 September 2018)]; Available online: .
    1. Bhatt S., Gething P.W., Brady O.J., Messina J.P., Farlow A.W., Moyes C.L., Drake J.M., Brownstein J.S., Hoen A.G., Sankoh O. The global distribution and burden of dengue. Nature. 2013;496:504. doi: 10.1038/nature12060.
    1. Brady O.J., Gething P.W., Bhatt S., Messina J.P., Brownstein J.S., Hoen A.G., Moyes C.L., Farlow A.W., Scott T.W., Hay S.I. Refining the global spatial limits of dengue virus transmission by evidence-based consensus. PLoS NTDs. 2012;6:e1760. doi: 10.1371/journal.pntd.0001760.
    1. Watts D.M., Burke D.S., Harrison B.A., Whitmire R.E., Nisalak A. Effect of temperature on the vector efficiency of Aedes aegypti for dengue 2 virus. Am. J. Trop. Med. Hyg. 1987;36:143–152. doi: 10.4269/ajtmh.1987.36.143.
    1. Rohani A., Wong Y.C., Zamre I., Lee H.L., Zurainee M.N. The effect of extrinsic incubation temperature on development of dengue serotype 2 and 4 viruses in Aedes aegypti (L.) SE Asian J. Trop. Med. 2009;40:942.
    1. Alto B.W., Bettinardo D. Temperature and dengue virus infection in mosquitoes: Independent effects of the immature and adult stages. Am. J. Trop. Med. Hyg. 2013;88:497–505. doi: 10.4269/ajtmh.12-0421.
    1. Whitehorn J., Kien D.T., Nguyen N.M., Nguyen H.L., Kyrylos P.P., Carrington L.B., Tran C.N., Quyen N.T., Thi L.V., Le Thi D., et al. Comparative susceptibility of Aedes albopictus and Aedes aegypti to dengue virus infection after feeding on blood of viremic humans: Implications for public health. J. Infect. Dis. 2015;212:1182–1190. doi: 10.1093/infdis/jiv173.
    1. Thu H.M., Aye K.M., Thein S. The effect of temperature and humidity on dengue virus propagation in Aedes aegypti mosquitoes. Southeast Asian J. Trop. Med. Public Health. 1998;29:280–284.
    1. World Health Organization Chikungunya. [(accessed on 12 April 2017)]; Available online: .
    1. Renault P., Solet J.L., Sissoko D., Balleydier E., Larrieu S., Filleul L., Lassalle C., Thiria J., Rachou E., de Valk H., et al. A major epidemic of chikungunya virus infection on Reunion Island, France, 2005–2006. Am. J. Trop. Med. Hyg. 2007;77:727–731. doi: 10.4269/ajtmh.2007.77.727.
    1. Yoon I.K., Alera M.T., Lago C.B., Tac-An I.A., Villa D., Fernandez S., Thaisomboonsuk B., Klungthong C., Levy J.W., Velasco J.M., et al. High rate of subclinical chikungunya virus infection and association of neutralizing antibody with protection in a prospective cohort in the Philippines. PLoS NTDs. 2015;9:e0003764. doi: 10.1371/journal.pntd.0003764.
    1. Becker N. Influence of climate change on mosquito development and mosquito-borne diseases in Europe. Parasitol. Res. 2008;103:19–28. doi: 10.1007/s00436-008-1210-2.
    1. Paupy C., Delatte H., Bagny L., Corbel V., Fontenille D. Aedes albopictus, an arbovirus vector: From the darkness to the light. Microbes Infect. 2009;11:1177–1185. doi: 10.1016/j.micinf.2009.05.005.
    1. Zouache K., Fontaine A., Vega-Rua A., Mousson L., Thiberge J.M., Lourenco-De-Oliveira R., Caro V., Lambrechts L., Failloux A.B. Three-way interactions between mosquito population, viral strain and temperature underlying chikungunya virus transmission potential. Proc. R. Soc. Lond. B Biol. Sci. 2014;281:20141078. doi: 10.1098/rspb.2014.1078.
    1. Li C.X., Guo X.X., Deng Y.Q., Xing D., Sun A.J., Liu Q.M., Wu Q., Zhang Y.M., Zhang H.D., Cao W.C., et al. Vector competence and transovarial transmission of two Aedes aegypti strains to Zika virus. Emerg. Microbes Infec. 2017;6:e23. doi: 10.1038/emi.2017.8.
    1. Niyas K.P., Abraham R., Unnikrishnan R.N., Mathew T., Nair S., Manakkadan A., Issac A., Sreekumar E. Molecular characterization of Chikungunya virus isolates from clinical samples and adult Aedes albopictus mosquitoes emerged from larvae from Kerala, South India. Virol. J. 2010;7:189. doi: 10.1186/1743-422X-7-189.
    1. Mavale M., Parashar D., Sudeep A., Gokhale M., Ghodke Y., Geevarghese G., Arankalle V., Mishra A.C. Venereal transmission of chikungunya virus by Aedes aegypti mosquitoes (Diptera: Culicidae) Am. J. Trop. Med. Hyg. 2010;83:1242–1244. doi: 10.4269/ajtmh.2010.09-0577.
    1. Cauchemez S., Ledrans M., Poletto C., Quenel P.D., De Valk H., Colizza V., Boëlle P.Y. Local and regional spread of chikungunya fever in the Americas. Euro Surveillance: Bulletin Europeen sur les Maladies Transmissibles=Eur. Commun. Dis. Bull. 2014;19:20854. doi: 10.2807/1560-7917.ES2014.19.28.20854.
    1. Kendrick K., Stanek D., Blackmore C., Centers for Disease Control and Prevention (CDC) Notes from the field: Transmission of chikungunya virus in the continental United States—Florida, 2014. MMWR Morb. Mortal. Wkly. Rep. 2014;63:1137.
    1. Center for Disease Control and Prevention Chikungunya Virus Home: Geographic Distribution. [(accessed on 29 May 2018)]; Available online: .
    1. Barba-Spaeth G., Dejnirattisai W., Rouvinski A., Vaney M.C., Medits I., Sharma A., Simon-Lorière E., Sakuntabhai A., Cao-Lormeau V.M., Haouz A., et al. Structural basis of potent Zika–dengue virus antibody cross-neutralization. Nature. 2016;536:48. doi: 10.1038/nature18938.
    1. World Health Organization Zika Virus. [(accessed on 20 July 2018)]; Available online: .
    1. Benelli G., Romano D. Mosquito vectors of Zika virus. Entomol. Gen. 2017;36:309–318. doi: 10.1127/entomologia/2017/0496.
    1. Hayes E.B. Zika virus outside Africa. Emerg. Infect. Dis. 2009;15:1347. doi: 10.3201/eid1509.090442.
    1. Haddow A.D., Schuh A.J., Yasuda C.Y., Kasper M.R., Heang V., Huy R., Guzman H., Tesh R.B., Weaver S.C. Genetic characterization of Zika virus strains: Geographic expansion of the Asian lineage. PLoS NTDs. 2012;6:e1477. doi: 10.1371/journal.pntd.0001477.
    1. Petersen L.R., Jamieson D.J., Powers A.M., Honein M.A. Zika virus. New Engl. J. Med. 2016;374:1552–1563. doi: 10.1056/NEJMra1602113.
    1. Haddow A.D., Schuh A.J., Yasuda C.Y., Kasper M.R., Heang V., Huy R., Guzman H., Tesh R.B., Weaver S.C. On the seasonal occurrence and abundance of the Zika virus vector mosquito Aedes aegypti in the contiguous United States. PLoS Curr. 2016;8 doi: 10.1371/currents.outbreaks.50dfc7f46798675fc63e7d7da563da76.
    1. Mordecai E.A., Cohen J.M., Evans M.V., Gudapati P., Johnson L.R., Lippi C.A., Miazgowicz K., Murdock C.C., Rohr J.R., Ryan S.J., et al. Detecting the impact of temperature on transmission of Zika, dengue, and chikungunya using mechanistic models. PLoS NTDs. 2017;11:e0005568. doi: 10.1371/journal.pntd.0005568.
    1. Azar S.R., Roundy C.M., Rossi S.L., Huang J.H., Leal G., Yun R., Fernandez-Salas I., Vitek C.J., Paploski I.A., Stark P.M., et al. Differential vector competency of Aedes albopictus populations from the Americas for Zika virus. Am. J. Trop. Med. Hyg. 2017;97:330–339. doi: 10.4269/ajtmh.16-0969.
    1. Gendernalik A., Weger-Lucarelli J., Luna S.M.G., Fauver J.R., Rückert C., Murrieta R.A., Burgren N., Samaras D., Nguyen C., Kading R.C., Ebel G.D. American Aedes vexans mosquitoes are competent vectors of Zika virus. Am. J. Trop. Med. Hyg. 2017;96:1338–1340. doi: 10.4269/ajtmh.16-0963.
    1. Ayres C.F. Identification of Zika virus vectors and implications for control. Lancet Infect. Dis. 2016;16:278–279. doi: 10.1016/S1473-3099(16)00073-6.
    1. Gardner L.M., Chen N., Sarkar S. Global risk of Zika virus depends critically on vector status of Aedes albopictus. Lancet Infect. Dis. 2016;16:522–523. doi: 10.1016/S1473-3099(16)00176-6.
    1. World Health Organization West Nile Virus. [(accessed on 3 October 2017)]; Available online: .
    1. Klenk K., Snow J., Morgan K., Bowen R., Stephens M., Foster F., Gordy P., Beckett S., Komar N., Gubler D., et al. Alligators as West Nile virus amplifiers. Emerg. Infect. Dis. 2004;10:2150. doi: 10.3201/eid1012.040264.
    1. Campbell G.L., Marfin A.A., Lanciotti R.S., Gubler D.J. West Nile virus. Lancet Infect. Dis. 2002;2:519–529. doi: 10.1016/S1473-3099(02)00368-7.
    1. Turell M.J., O’Guinn M.L., Dohm D.J., Jones J.W. Vector competence of North American mosquitoes (diptera: Culicidae) for West Nile virus. J. Med. Entomol. 2001;38:130–134. doi: 10.1603/0022-2585-38.2.130.
    1. Turell M.J., Dohm D.J., Sardelis M.R., O’guinn M.L., Andreadis T.G., Blow J.A. An update on the potential of North American mosquitoes (Diptera: Culicidae) to transmit West Nile virus. J. Med. Entomol. 2005;42:57–62. doi: 10.1093/jmedent/42.1.57.
    1. Richards S.L., Mores C.N., Lord C.C., Tabachnick W.J. Impact of extrinsic incubation temperature and virus exposure on vector competence of Culex pipiens quinquefasciatus Say (Diptera: Culicidae) for West Nile virus. Vector-Borne Zoonotic. 2007;7:629–636. doi: 10.1089/vbz.2007.0101.
    1. Dohm D.J., O’Guinn M.L., Turell M.J. Effect of environmental temperature on the ability of Culex pipiens (Diptera: Culicidae) to transmit West Nile virus. J. Med. Entomol. 2002;39:221–225. doi: 10.1603/0022-2585-39.1.221.
    1. World Health Organization Yellow Fever Virus. [(accessed on 1 May 2018)]; Available online: .
    1. Rogers D.J., Wilson A.J., Hay S.I., Graham A.J. The global distribution of yellow fever and dengue. Adv. Parasit. 2006;62:181–220.
    1. Aitken T.H., Tesh R.B., Beaty B.J., Rosen L. Transovarial transmission of yellow fever virus by mosquitoes (Aedes aegypti) Am. J. Trop. Med. Hyg. 1979;28:119–121. doi: 10.4269/ajtmh.1979.28.119.
    1. Center for Disease Control and Prevention Transmission of Yellow Fever Virus. [(accessed on 13 August 2015)]; Available online: .
    1. Gubler D.J. The changing epidemiology of yellow fever and dengue, 1900 to 2003: Full circle? Comp. Immunol. Microb. 2004;27:319–330. doi: 10.1016/j.cimid.2004.03.013.
    1. Davis N.C. The Effect of Various Temperatures in modifying the Extrinsic Incubation Period of the Yellow Fever Virus in Aedes aegypti. Am. J. Hyg. 1932;16:163–176. doi: 10.1093/oxfordjournals.aje.a117853.
    1. Moore C.G., Mitchell C.J. Aedes albopictus in the United States: Ten-year presence and public health implications. Emerg. Infect. Dis. 1997;3:329. doi: 10.3201/eid0303.970309.
    1. Mitchell C.J., Niebylski M.L., Smith G.C., Karabatsos N., Martin D., Mutebi J.P., Craig G.B., Mahler M.J. Isolation of eastern equine encephalitis virus from Aedes albopictus in Florida. Science. 1992;257:526–527. doi: 10.1126/science.1321985.
    1. Komar N., Dohm D.J., Turell M.J., Spielman A. Eastern equine encephalitis virus in birds: Relative competence of European starlings (Sturnus vulgaris) Am. J. Trop. Med. Hyg. 1999;60:387–391. doi: 10.4269/ajtmh.1999.60.387.
    1. Chamberlain R., Sudia W. The Effects of Temperature upon the Extrinsic Incubation of Eastern Equine Encephalitis in Mosquitoes. Am. J. Hyg. 1955;62:295–305.
    1. Lednicky J., De Rochars V.M.B., Loeb J., Telisma T., Chavannes S., Anilis G., Cella E. Ciccozzi, M.; Okech, B.; Salemi, M.; et al. Mayaro virus in child with acute febrile illness, Haiti, 2015. Emerg. Infect. Dis. 2016;22:2000. doi: 10.3201/eid2211.161015.
    1. Da Costa Carvalho M.D.G., Fournier M.V. Effect of heat shock on gene expression of Aedes albopictus cells infected with Mayaro virus. Res. Virol. 1991;142:25–31. doi: 10.1016/0923-2516(91)90024-W.
    1. Hotez P.J., Murray K.O. Dengue, West Nile virus, chikungunya, Zika—And now Mayaro? PLoS Negl. Trop. Dis. 2017;11:e005462. doi: 10.1371/journal.pntd.0005462.
    1. Kartman L. Factors influencing infection of the mosquito with Dirofilaria immitis (Leidy, 1856) Exp. Parasitol. 1953;2:27–78. doi: 10.1016/0014-4894(53)90005-8.
    1. McGreevy P.B., Kolstrup N., Tao J., McGreevy M.M., de C. Marshall T.F. Ingestion and development of Wuchereria bancrofti in Culex quinquefasciatus, Anopheles gambiae and Aedes aegypti after feeding on humans with varying densities of microfilariae in Tanzania. Trans. R. Soc. Trop. Med. Hyg. 1982;76:288–296. doi: 10.1016/0035-9203(82)90170-5.
    1. Simón F., López-Belmonte J., Marcos-Atxutegi C., Morchón R., Martín-Pacho J.R. What is happening outside North America regarding human dirofilariasis? Vet. Parasitol. 2005;133:181–189. doi: 10.1016/j.vetpar.2005.03.033.
    1. Ledesma N., Harrington L. Mosquito vectors of dog heartworm in the United States: Vector status and factors influencing transmission efficiency. Top. Companion Anim. Med. 2011;26:178–185. doi: 10.1053/j.tcam.2011.09.005.
    1. Ledesma N., Harrington L. Fine-scale temperature fluctuation and modulation of Dirofilaria immitis larval development in Aedes aegypti. Vet. Parasitol. 2015;209:93–100. doi: 10.1016/j.vetpar.2015.02.003.
    1. Mas-Coma S., Valero M.A., Bargues M.D. Effects of climate change on animal and zoonotic helminthiases. Rev. Sci. Tech. 2008;27:443–457. doi: 10.20506/rst.27.2.1822.
    1. Beck-Johnson L.M., Nelson W.A., Paaijmans K.P., Read A.F., Thomas M.B., Bjørnstad O.N. The effect of temperature on Anopheles mosquito population dynamics and the potential for malaria transmission. PLoS ONE. 2013;8:e79276. doi: 10.1371/journal.pone.0079276.
    1. Paaijmans K.P., Blanford S., Bell A.S., Blanford J.I., Read A.F., Thomas M.B. Influence of climate on malaria transmission depends on daily temperature variation. Proc. Natl. Acad. Sci. USA. 2010;107:15135–15139. doi: 10.1073/pnas.1006422107.
    1. Vanderberg J.P., Yoeli M. Effects of temperature on sporogonic development of Plasmodium berghei. J. Parasitol. 1966;52:559–564. doi: 10.2307/3276326.

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