Skip to main content

Aedes japonicus japonicus (Diptera: Culicidae) from Germany have vector competence for Japan encephalitis virus but are refractory to infection with West Nile virus

Abstract

The interplay between arthropod-borne (arbo) viruses and their vectors is usually complex and often exert unique relationships. Aedes japonicus japonicus (Hulecoeteomyia japonica or Ochlerotatus japonicus japonicus), an invasive mosquito species with laboratory proven vector competence for a number of emerging viruses has been newly introduced to Germany and is currently expanding its range throughout the country. On the other hand, West Nile virus (WNV), an emerging arbovirus originating from Africa, is already circulating in several European countries and might soon be introduced to Germany. Because newly introduced and rapidly expanding vector species pose a potential risk for public health in Germany, we assessed the vectorial capacity of German Ae. j. japonicus populations for WNV and Japanese encephalitis virus (JEV). The results indicate that German Ae. j. japonicus are susceptible for JEV but are refractory to infection with WNV. Of 67 Ae. j. japonicus females challenged by feeding of WNV-containing blood, none had measurable amounts of WNV-RNA (0 % infection rate) on day 14 post-infection. In contrast, all females challenged with JEV were positive for JEV-RNA (100 % infection rate) on day 14 post-infection. The reason for WNV resistance remains to be determined but is independent from co-infection with other flaviviruses or the presence of endosymbiotic Wolbachia, since we found no evidence for other flavivirus infections within 1,033 tested A. j. japonicus females from the sampling region, nor detectable Wolbachia infection within 30 randomly selected individuals.

This is a preview of subscription content, access via your institution.

References

  • Becker N, Geier M, Balczun C, Bradersen U, Huber K, Kiel E, Krüger A, Lühken R, Orendt C, Plenge-Bönig A, Rose A, Schaub GA, Tannich E (2013) Repeated introduction of Aedes albopictus into Germany, July to October 2012. Parasitol Res 112:1787–1790

    PubMed  Article  Google Scholar 

  • Bunning ML, Bowen RA, Cropp B, Sullivan K, Davis B, Komar N, Godesey M, Baker D, Hettler D, Holmes D, Mitchell CJ (2001) Experimental infection of horses with West Nile virus and their potential to infect mosquitoes and serve as amplifying hosts. Ann NY Acad Sci 951:338–339

    CAS  PubMed  Article  Google Scholar 

  • Calisher CH, Karabatsos N, Dalrymple JM, Shope RE, Porterfield JS, Westaway EG, Brandt WE (1989) Antigenic relationships between flaviviruses as determined by cross-neutralization tests with polyclonal antisera. J Gen Virol 70(Pt 1):37–43

    PubMed  Article  Google Scholar 

  • Campbell GL, Marfin AA, Lanciotti RS, Gubler DJ (2002) West Nile virus. Lancet Infect Dis 2:519–529

    PubMed  Article  Google Scholar 

  • Chao DY, Davis BS, Chang GJ (2007) Development of multiplex real-time reverse transcriptase PCR assays for detecting eight medically important flaviviruses in mosquitoes. J Clin Microbiol 45:584–589

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Glaser RL, Meola MA (2010) The native Wolbachia endosymbionts of Drosophila melanogaster and Culex quinquefasciatus increase host resistance to West Nile virus infection. PLoS One 5:e11977

    PubMed Central  PubMed  Article  Google Scholar 

  • Gyure KA (2009) West Nile virus infections. J Neuropathol Exp Neurol 68:1053–1060

    PubMed  Article  Google Scholar 

  • Hardy JL, Houk EJ, Kramer LD, Reeves WC (1983) Intrinsic factors affecting vector competence of mosquitoes for arboviruses. Annu Rev Entomol 28:229–262

    CAS  PubMed  Article  Google Scholar 

  • Jia XY, Briese T, Jordan I, Rambaut A, Chi HC, Machenzie JS, Hall RA, Scherret J, Lipkin WI (1999) Genetic analysis of West Nile New York 1999 encephalitis virus. Lancet 354:1971–1972

    CAS  PubMed  Article  Google Scholar 

  • Kampen H, Kronefeld M, Zielke D, Werner D (2013) Further specimens of the Asian tiger mosquito Aedes albopictus (Diptera, Culicidae) trapped in southwest Germany. Parasitol Res 112:905–907

    PubMed  Article  Google Scholar 

  • Kampen H, Zielke D, Werner D (2012) A new focus of Aedes japonicus japonicus (Theobald, 1901) (Diptera, Culicidae) distribution in Western Germany: rapid spread or a further introduction event? Parasites Vectors 5:284

    PubMed Central  PubMed  Article  Google Scholar 

  • Kaufman MG, Fonseca DM (2014) Invasion biology of Aedes japonicus japonicus (Diptera: Culicidae). Annu Rev Entomol 59:31–49

    CAS  PubMed  Article  Google Scholar 

  • Kent RJ, Crabtree MB, Miller BR (2010) Transmission of West Nile virus by Culex quinquefasciatus (Say) infected with Culex Flavivirus Izabal. PLoS Negl Trop Dis 4:e671

    PubMed Central  PubMed  Article  Google Scholar 

  • Kramer LD, Styer LM, Ebel GD (2008) A global perspective on the epidemiology of West Nile virus. Annu Rev Entomol 53:61–81

    CAS  PubMed  Article  Google Scholar 

  • Linke S, Niedrig M, Kaiser A, Ellerbrok H, Müller K, Müller T, Conraths FJ, Mühle RU, Schmidt D, Köppen U, Bairlein F, Berthold P, Pauli G (2007) Serologic evidence of West Nile virus infections in wild birds captured in Germany. Am J Trop Med Hyg 77:358–364

    PubMed  Google Scholar 

  • Lourenco de Oliveira R, Vazeille M, de Filippis AM, Failloux AB (2003) Large genetic differentiation and low variation in vector competence for dengue and yellow fever viruses of Aedes albopictus from Brazil, the United States, and the Cayman Islands. Am J Trop Med Hyg 69:105–114

    PubMed  Google Scholar 

  • Moreira LA, Iturbe-Ormaetxe I, Jeffery JA, Lu G, Pyke AT, Hedges LM, Rocha BC, Hall-Mendelin S, Day A, Riegler M, Hugo LE, Johnson KN, Kay BH, McGraw EA, van den Hurk AF, Ryan PA, O´Neill SC (2009) A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium. Cell 139:1268–1278

    PubMed  Article  Google Scholar 

  • Pesko K, Mores CN (2009) Effect of sequential exposure on infection and dissemination rates for West Nile and St. Louis encephalitis viruses in Culex quinquefasciatus. Vector Borne Zoonotic Dis 9:281–286

    PubMed Central  PubMed  Article  Google Scholar 

  • Peyton EL, Campbell SR, Candeletti TM, Romanowski M, Crans WJ (1999) Aedes (Finlaya) japonicus japonicus (Theobald), a new introduction into the United States. J Am Mosq Control Assoc 15:238–241

    CAS  PubMed  Google Scholar 

  • Reinert JF (2000) New classification for the composite genus Aedes (Diptera: Culicidae: Aedini), elevation of subgenus Ochlerotatus to generic rank, reclassification of the other subgenera, and notes on certain subgenera and species. J Am Mosq Control Assoc 16:175–188

    CAS  PubMed  Google Scholar 

  • Richards SL, Lord CC, Pesko KN, Tabachnick WJ (2010) Environmental and biological factors influencing Culex pipiens quinquefasciatus (Diptera: Culicidae) vector competence for West Nile Virus. Am J Trop Med Hyg 83:126–134

    PubMed Central  PubMed  Article  Google Scholar 

  • Rozeboom LE, Kassira EN (1969) Dual infections of mosquitoes with strains of West Nile virus. J Med Entomol 6:407–411

    CAS  PubMed  Google Scholar 

  • Savage HM, Smith GC (1994) Identification of damaged adult female specimens of Aedes albopictus and Aedes aegypti in the New World. J Am Mosq Control Assoc 10:440–442

    CAS  PubMed  Google Scholar 

  • Schaffner F, Chouin S, Guilloteau J (2003) First record of Ochlerotatus (Finlaya) japonicus japonicus (Theobald, 1901) in metropolitan France. J Am Mosq Control Assoc 19:1–5

    PubMed  Google Scholar 

  • Schaffner F, Medlock JM, Van Bortel W (2013) Public health significance of invasive mosquitoes in Europe. Clin Microbiol Infect 19:685–692

    CAS  PubMed  Article  Google Scholar 

  • Schaffner F, Vazeille M, Kaufmann C, Failloux AB, Mathis A (2011) Vector competence of Aedes japonicus for chikungunya and dengue viruses. Eur Mosq Bull 29:141–142

    Google Scholar 

  • Takashima I, Rosen L (1989) Horizontal and vertical transmission of Japanese encephalitis virus by Aedes japonicus (Diptera: Culicidae). J Med Entomol 26:454–458

    CAS  PubMed  Google Scholar 

  • Tanaka K, Mizusawa K, Saugstad ES (1979) A revision of the adult and larval mosquitoes of Japan (including the Ryukyu archipelago and the Ogasawara islands) and Korea (Diptera: Culicidae). Contrib Amer Ent Inst:1–987

  • Tesh RB, Gubler DJ, Rosen L (1976) Variation among geographic strains of Aedes albopictus in susceptibility to infection with chikungunya virus. Am J Trop Med Hyg 25:326–335

    CAS  PubMed  Google Scholar 

  • Turell MJ, O’Guinn ML, Dohm DJ, Jones JW (2001) Vector competence of North American mosquitoes (Diptera: Culicidae) for West Nile virus. J Med Entomol 38:130–134

    CAS  PubMed  Article  Google Scholar 

  • Walker T, Johnson PH, Moreira LA, Iturbe-Ormaetxe I, Frentiu FD, McMeniman CJ, Leong YS, Dong Y, Axford J, Kriesner P, Lloyd AL, Ritchie SA, O´Neill SL, Hoffmann AA (2011) The wMel Wolbachia strain blocks dengue and invades caged Aedes aegypti populations. Nature 476:450–453

    CAS  PubMed  Article  Google Scholar 

  • Werner D, Kampen H (2013) The further spread of Aedes japonicus japonicus (Diptera, Culicidae) towards northern Germany. Parasitol Res 112:3665–3668

    PubMed  Article  Google Scholar 

  • Werner D, Kronefeld M, Schaffner F, Kampen H (2012) Two invasive mosquito species, Aedes albopictus and Aedes japonicus japonicus, trapped in south-west Germany, July to August 2011. Euro Surveill 17

  • Zhou W, Rousset F, O’Neil S (1998) Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proc Biol Sci 265:509–515

    CAS  PubMed Central  PubMed  Article  Google Scholar 

Download references

Acknowledgments

This work was financially supported by the Leibniz Association, grant number SAW-2011-BNI-3 and the German Federal Ministry for Environment, Nature Conservation, Building and Nuclear Safety (BMUB) through the Federal Environment Agency (UBA), grant number FKZ371148404. We thank Andreas Krüger for the critical reading of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stefanie C. Becker.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Fig. S1

Quality control of RNAs used for WNV detection by 28S RT-PCT. RNA isolates from single WNV infection experiments (4 mosquitoes/experiment) were subjected to a 28S RNA RT-PCR. PCR products are separated by agarose gel. The gel shows the PCR products for the single specimens in lanes 1–29 and a 1 kb ladder in lane L. All RNAs tested yielded the expected 250 bp fragment

High resolution image

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Huber, K., Jansen, S., Leggewie, M. et al. Aedes japonicus japonicus (Diptera: Culicidae) from Germany have vector competence for Japan encephalitis virus but are refractory to infection with West Nile virus. Parasitol Res 113, 3195–3199 (2014). https://doi.org/10.1007/s00436-014-3983-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-014-3983-9

Keywords

  • Aedes japonicus japonicus
  • Vector competence
  • West Nile virus