Abstract
Aedes japonicus japonicus is endemic in a number of countries in eastern Asia but has been accidently introduced into many regions of the world including Europe. It was first detected in Hungary in 2012. In 2017, robust populations of the species were found at Lake Balaton, one of the most important tourist destinations in Central Europe. Based on the experience gathered in the above localities, habitat requirements, dispersion abilities and human biting behaviour of the species were studied in western Hungary during 2017 and 2018. Our results show that (a) a few years after its detection at the Slovenian-Hungarian border, Ae. j. japonicus is widespread in at least two-thirds of the western half of Hungary; (b) the species spreads quickly in ecological corridors formed by mosaics of rural areas, detached houses, gardens and small forest patches; (c) Ae. j. japonicus occupies artificial containers; (d) expansion of the species into new areas is slowed by extensive closed forest patches.
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References
Andreadis TG, Anderson JF, Munstermann LE, Wolfe RJ, Florin DA (2001) Discovery, distribution, and abundance of the newly introduced mosquito Ochlerotatus japonicus (Diptera: Culicidae) in Connecticut, USA. J Med Entomol 38:774–779. https://doi.org/10.1603/0022-2585-38.6.774
Andreadis TG, Wolfe RJ (2010) Evidence for reduction of native mosquitoes with increased expansion of invasive Ochlerotatus japonicus japonicus (Diptera: Culicidae) in the northeastern United States. J Med Entomol 47:43–52. https://doi.org/10.1603/033.047.0106
Apperson CS, Hassan HK, Harrison BA, Savage HM, Aspen SE, Farajollahi A, Crans W, Daniels TJ, Falco RC, Benedict M, Anderson M, McMillen L, Unnasch TR (2004) Host feeding patterns of established and potential mosquito vectors of West Nile virus in the eastern United States. Vector Borne Zoonotic Dis 4:71–82. https://doi.org/10.1089/153036604773083013
Bartlett-Healy K, Unlu I, Obenauer P, Hughes T, Healy S, Crepeau T, Farajollahi A, Kesavaraju B, Fonseca D, Schoeler G, Gaugler R, Strickman D (2012) Larval mosquito habitat utilization and community dynamics of Aedes albopictus and Aedes japonicus (Diptera: Culicidae). J Med Entomol 49:813–824. https://doi.org/10.1603/ME11031
Becker N, Petric D, Zgomba M, Boase C, Dahl C, Lane J, Kaiser A (2003) Mosquitoes and their control. Kluwer Academic/Plenum Publishers, New York, pp 39–40
Bevins SN (2007) Establishment and abundance of a recently introduced mosquito species Ochlerotatus japonicus (Diptera: Culicidae) in the southern Appalachians, USA. J Med Entomol 44:945–952. https://doi.org/10.1603/0022-2585(2007)44[945:EAAOAR]2.0.CO;2
Büttner G, Maucha G, Bíró M, Kosztra B, Pataki R, Petrik O (2004) National land cover database at scale 1:50,000 in Hungary. EARSeL eProceedings 3:323–330
Crans WJ, McNelly JR (1999) An update on the distribution of Aedes japonicus in the northeast. Vector Ecol Newsl 30:14–15
Damiens D, Ayrinhac A, Van Bortel W, Versteirt V, Dekoninck W, Hance T (2014) Invasive process and repeated cross-sectional surveys of the mosquito Aedes japonicus japonicus establishment in Belgium. PLoS One 9:e89358. https://doi.org/10.1371/journal.pone.0089358
Deblauwe I, Sohier C, Schaffner F, Rakotoarivony RM, Coosemans M (2014) Implementation of surveillance of invasive mosquitoes in Belgium according to the ECDC guidelines. Parasit Vectors 7:201. https://doi.org/10.1186/1756-3305-7-201
Derraik JGB (2004) Exotic mosquitoes in New Zealand: a review of species intercepted, their pathways and ports of entry. Aust N Z J Public Health 28:433–444. https://doi.org/10.1111/j.1467-842X.2004.tb00025.x
Eritja R, Arrondo I, Delacour S, Schaffner F, Álvarez-Chachero J, Bengoa M, Puig M, Melero Alcibar R, Oltra A, Bartumeus F (2019) First detection of Aedes japonicus in Spain: an unexpected finding triggered by citizen science. Parasit Vectors 12:53–59. https://doi.org/10.1186/s13071-019-3317-y
Falco RC, Daniels TJ, Slameck MC (2002) Prevalence and distribution of Ochlerotatus japonicus (Diptera: Culicidae) in two counties in southern New York State. J Med Entomol 39:920–925. https://doi.org/10.1603/0022-2585-39.6.920
Gingrich JB, Anderson RD, Williams GM, O’Connor L, Harkins K (2006) Stormwater ponds, constructed wetlands, and other best management practices as potential breeding sites for West Nile virus vectors in Delaware during 2004. J Am Mosq Control Assoc 22:282–291. https://doi.org/10.2987/8756-971X(2006)22[282:SPCWAO]2.0.CO;2
Ibañez-Justicia A, Kampen H, Braks M, Schaffner F, Steeghs M, Werner D, Zielke D, den Hartog W, Brooks M, Dik M, van de Vossenberg B, Scholte E-J (2014) First report of established population of Aedes japonicus japonicus (Theobald, 1901) (Diptera, Culicidae) in the Netherlands. J Eur Mosq Control Assoc 32:9–13
Ibañez-Justicia A, Teekema S, den Hartog W, Jacobs F, Dik M, Stroo A (2018) The effectiveness of Asian bush mosquito (Aedes japonicus japonicus) control actions in colonised peri-urban areas in the Netherlands. J Med Entomol 5:673–680
Iriate WLZ, Tsuda Y, Wada Y, Takagi M (1991) Distribution of mosquitoes on a hill of Nagasaki City, with emphasis to the distance from human dwellings. Trop Med 33:55–60
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? Parasit Vectors 5:284. https://doi.org/10.1186/1756-3305-5-284
Kampen H, Werner D (2014) Out of the bush: the Asian bush mosquito Aedes japonicus japonicus (Theobald, 1901) (Diptera, Culicidae) becomes invasive. Parasit Vectors 7:59. https://doi.org/10.1186/1756-3305-7-59
Kaufman MG, Fonseca DM (2014) Invasion biology of Aedes japonicus japonicus (Diptera: Culicidae). Annu Rev Entomol 59:31–49. https://doi.org/10.1146/annurev-ento-011613-162012
Kenyeres Z, Tóth S (2008) Csípőszúnyog-határozó II. (Imágók). [Identification keys to Mosquitoes II. (Adults).]. Pannónia Füzetek 2:1–96 [In Hungarian]
Kenyeres Z, Tóth S, Bauer N, Sáringer-Kenyeres T (2012) Life-strategy based structural features of the larval mosquito metacommunities in Hungary. Ekológia 31:210–230. https://doi.org/10.4149/ekol_2012_02_210
Koban MB, Kampen H, Scheuch DE, Frueh L, Kuhlisch C, Janssen N, Steidle JLM, Schaub GA, Werner D (2019) The Asian bush mosquito Aedes japonicus japonicus (Diptera: Culicidae) in Europe, 17 years after its first detection, with a focus on monitoring methods. Parasit Vectors 12:109. https://doi.org/10.1186/s13071-019-3349-3
Krebs T, Bindler P, L’Ambert G, Toty C, Perrin Y, Jourdain F (2014) First establishment of Aedes japonicus japonicus (Theobald, 1901) (Diptera: Culicidae) in France in 2013 and its impact on public health. J Vector Ecol 39:437–440
Medlock JM, Hansford KM, Versteirt V, Cull B, Kampen H, Fontenille D, Hendrickx G, Zeller H, Van Bortel W, Schaffner F (2015) An entomological review of invasive mosquitoes in Europe. Bull Entomol Res 105:637–663. https://doi.org/10.1017/S0007485315000103
Mezősi G (2017) The physical geography of Hungary. Geography of the physical environment. Springer International Publishing AG, Cham. https://doi.org/10.1007/978-3-319-45183-1
Miyagi I (1971) Notes on the Aedes (Finlaya) chrysolineatus subgroup in Japan and Korea (Diptera: Culicidae). Trop Med 13:141–151
Molaei G, Farajollahi A, Scott JJ, Gaugler R, Andreadis TG (2009) Human bloodfeeding by the recently introduced mosquito, Aedes japonicus japonicus, and public health implications. J Am Mosq Control Assoc 25:210–214. https://doi.org/10.2987/09-0012.1
Montarsi F, Martini S, Michelutti A, Da Rold G, Mazzucato M, Qualizza D, Di Gennaro D, Di Fant M, Dal Pont M, Palei M, Capelli G (2019) The invasive mosquito Aedes japonicus japonicus is spreading in northeastern Italy. Parasit Vectors 12:120. https://doi.org/10.1186/s13071-019-3387-x
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
QGIS Development Team (2016) QGIS geographic information system. OpenSource Geospatial Foundation Project. http://qgis.osgeo.org
Ries C, Pfeiffenschneider M (2019) Aedes japonicus (Theobald, 1901). In: neobiota.Lu - invasive alien species in Luxembourg. National Museum of Natural History, Luxembourg https://neobiota.lu/aedes-japonicus/ [Accessed 2019-11-16]
Sáringer-Kenyeres M, Kenyeres Z (2018) Invazív csípőszúnyog fajok (Diptera: Culicidae) Magyarországon. [Invasive mosquito species (Diptera: Culicidae) in Hungary] Conference: XXIV Ifjúsági Tudományos Fórum, Pannon Egyetem Georgikon Kar, Keszthely, 24 May 2018 [In Hungarian]
Sáringer-Kenyeres M, Tóth S, Kenyeres Z (2018) Updated checklist of the mosquitoes (Diptera: Culicidae) of Hungary. J Eur Mosq Control Assoc 36:14–16
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
Schaffner F, Kaufmann C, Hegglin D, Mathis A (2009) The invasive mosquito Aedes japonicus in Central Europe. Med Vet Entomol 23:448–451. https://doi.org/10.1111/j.1365-2915.2009.00825.x
Scott JJ, Crans WJ (2003) Expanded polystyrene (EPS) floats for surveillance of Ochlerotatus japonicus. J Am Mosq Control Assoc 19:376–381
Scott JJ, Frank LC, Crans WJ (2001) Ochlerotatus japonicus collected from natural rockpools in New Jersey. J Am Mosq Control Assoc 17:91–92
Scott JJ, McNelly JR, Crans WJ (1999) Aedes japonicus overwinters in New Jersey. Vector Ecol Newsl 30:6–7
Seidel B, Duh D, Nowotny N, Allerberger F (2012) First record of the mosquitoes Aedes (Ochlerotatus) japonicus japonicus (Theobald, 1901) in Austria and Slovenia 2011 and for Aedes (Stegomyia) albopictus (Skuse, 1895) in Austria 2012. Entomol Z 5:123–226
Seidel B, Nowotny N, Bakonyi T, Allerberger F, Schaffner F (2016) Spread of Aedes japonicus japonicus (Theobald, 1901) in Austria, 2011–2015, and first records of the subspecies for Hungary, 2012, and the principality of Liechtenstein, 2015. Parasit Vectors 9:356–362. https://doi.org/10.1186/s13071-016-1645-8
Soltész Z, Zöldi V (2017) Behurcolt és invazív csípőszúnyogok Magyarországon. [Introduced and invasive animals in Hungary.]. Magyar Tudomány 4:410–412 [In Hungarian]
Sota T, Mogi M, Hayamizu E (1994) Habitat stability and the larval mosquito community in treeholes and other containers on a temperate island. Res Popul Ecol 36:93–104. https://doi.org/10.1007/BF02515090
Sunahara T, Ishizaka K, Mogi M (2002) Habitat size: a factor determining the opportunity for encounters between mosquito larvae and aquatic predators. J Vector Ecol 27:8–20
Sztikler J, Weisz M, Zöldi V (2015) A magyarországi invazív szúnyog-surveillance rendszer elindítása és első eredményei. [Actuation and first results of the invasive mosquito surveillance system in Hungary.]. Egészségtudomány 4:146–147 [In Hungarian]
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 Am Entomol Inst 16:1–987
Thielman A, Hunter FF (2006) Establishment of Ochlerotatus japonicus (Diptera: Culicidae) in Ontario, Canada. J Med Entomol 43:138–142. https://doi.org/10.1603/0022-2585(2006)043[0138:EOOJDC]2.0.CO;2
Tóth S (2004) Magyarország csípőszúnyog-faunája (Diptera: Culicidae). [Mosquito fauna of Hungary.]. Natura Somogyiensis 6:1–327 [In Hungarian]
Tóth S (2007) Csípőszúnyog-határozó I. (Lárvák). [Identification keys to mosquitoes I. (Larvae).]. Pannónia Füzetek 1:1–96 [In Hungarian]
Tóth S, Kenyeres Z (2012) Revised checklist and distribution maps of mosquitoes (Diptera, Culicidae) of Hungary. J Eur Mosq Control Assoc 30:30–65
Versteirt V, Schaffner F, Garros C, Dekoninck W, Coosemans M, Van Bortel W (2009) Introduction and establishment of the exotic mosquito species Aedes japonicus japonicus (Diptera: Culicidae) in Belgium. J Med Entomol 46:1464–1467. https://doi.org/10.1603/033.046.0632
Versteirt V, Pecor EJ, Fonseca MD, Coosemans M, Van Bortel W (2012) Confirmation of Aedes koreicus (Diptera: Culicidae) in Belgium and description of morphological differences between Korean and Belgian specimens valiated by molecular identification. Zootaxa 3191:21–32 https://doi.org/10.11646/zootaxa.3191.1.2
Williges E, Farajollahi A, Scott JJ, McCuiston LJ, Crans WJ, Gaugler R (2008) Laboratory colonization of Aedes japonicus japonicus. J Am Mosq Control Assoc 24:591–593. https://doi.org/10.2987/5714.1
Acknowledgements
The authors would like to express their huge gratitude to Sándor Tóth for his help in planning of the study and in identification of some of the specimens. Our thanks go to Zoltán Soltész for allowing the first author to examine the mosquito collection of the Hungarian Natural History Museum.
Special thanks go to the working network, whose dedication ensured that larval collections were widespread and extensive—Judit Bajzáth (Mány), Zsolt Bernáth (Cserszegtomaj), snr. Zoltán Kenyeres (Tapolca), Előd Kondorosy (Cserszegtomaj), Péter Kovács (Mecsér), Szilvia Kovács (Felsőpáhok), András Márkus (Pécs), Péter Sári-Kovács (Hidegkút), Tamás Sáringer-Kenyeres (Keszthely), Béla Takács (Tömörd), Imre Tanai (Csabrendek), Sándor Tóth (Zirc).
We thank reviewers of earlier versions of the manuscript for their valuable comments and suggestions.
Our great thanks go to David Hunter, president of the Orthopterists’ Society, for his help in linguistic and stylistic issues of the manuscript.
Funding
The publication was supported by the EFOP-3.6.3-VEKOP-16-2017-00008 project (co-financed by the European Union and the European Social Fund).
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Human landing collections were carried out by the authors, using themselves as attractors. All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
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Sáringer-Kenyeres, M., Bauer, N. & Kenyeres, Z. Active dispersion, habitat requirements and human biting behaviour of the invasive mosquito Aedes japonicus japonicus (Theobald, 1901) in Hungary. Parasitol Res 119, 403–410 (2020). https://doi.org/10.1007/s00436-019-06582-6
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DOI: https://doi.org/10.1007/s00436-019-06582-6