ORIGINAL PAPER

Aedes albopictus breeding in southern Germany, 2014

Doreen Werner & Helge Kampen

Received: 14 November 2014 /Accepted: 18 November 2014# Springer-Verlag Berlin Heidelberg 2014

Abstract Larvae, pupae and eggs of the Asian tiger mosquitoAedes albopictus were found in Freiburg, southern Germany,after submission of an adult mosquito specimen from that areato the ‘Mückenatlas’, a German instrument of passive mos-quito surveillance. While previously collected Ae. albopictusin Germany were trapped on, or close to, service stations onmotorways, suggesting introduction by vehicles from south-ern Europe, these new specimens were out of flight distancefrom the motorway on the one hand and indicate local repro-duction on the other. The findings call for a thorough activeand passive surveillance in exposed geographic regions suchas the relatively warm German Upper Rhine Valley to preventAe. albopictus from establishing.

Keywords Aedes albopictus . Asian tiger mosquito .

Germany .Mückenatlas . Passive surveillance . Population .

Reproduction

Background

Being one of the top-ranked invasive species of the world, theAsian tiger mosquito Aedes (Stegomyia) albopictus (Skuse,1895) has been reported from at least 20 European countries innumerous of which establishment took place (Medlock et al.2012). It is commonly introduced from overseas via the used tyreand the lucky bamboo trade but an important mode ofintracontinental transportation is also by vehicles (Medlock

et al. 2012). Aedes albopictus is an efficient vector of more than20 pathogenic viruses and Dirofilaria spec. (Gratz 2004) andwas recently made responsible for an outbreak of chikungunyaand several cases of dengue in southern Europe (Schaffner et al.2013). Concern is therefore growing regarding the furtherspread of this species and the associated public health impact.

Findings and discussion

In mid-August 2014, a male Ae. albopictus specimen collectedin southwestern Germanywas submitted for identification to theGerman ‘Mückenatlas’ (www.mueckenatlas.de), an instrumentof passive mosquito surveillance contributing to a German-widemonitoring programme (Kampen et al. 2014). Since the‘Mückenatlas’-assisted detection of twoAe. japonicus japonicuspopulations in western and northern Germany in 2012 and 2013(Kampen et al. 2012;Werner and Kampen 2013), this is the firsttime that Ae. albopictus has been registered in the framework ofthis surveillance approach. The finding is not the first of Ae.albopictus in Germany in general, as the species had been foundalong the motorway A5 in the South German federal state ofBaden-Württemberg as eggs as early as in 2007 and had beentrapped as females repeatedly afterwards (Pluskota et al. 2008;Werner et al. 2012; Becker et al. 2013; Kampen et al. 2013). Inaddition, adult specimens were collected at motorway servicestations in the federal state of Bavaria (Becker et al. 2013). Onone occasion in 2013, several larvae were also found in a gardennext to a Bavarian motorway service station where adults hadbeen trapped (Rose, pers. comm.). In all cases, the collectionsites were close to the German borders with Switzerland andAustria, and it was assumed that the collected adults had beenimported by vehicles coming from southern Europe where Ae.albopictus is abundant and wide-spread (Kampen et al. 2013).Despite these findings, establishment of the species in Germanyhas not yet been demonstrated.

D. Werner (*)Leibniz-Centre for Agricultural Landscape Research, EberswalderStr. 84, 15374 Muencheberg, Germanye-mail: dwerner@zalf.de

H. KampenFriedrich-Loeffler-Institut, Federal Research Institute for AnimalHealth, Greifswald - Insel Riems, Germany

Parasitol ResDOI 10.1007/s00436-014-4244-7

The Ae. albopictus specimen submitted to the‘Mückenatlas’ was only processed for identification aftersome delay in late September 2014. It had been captured inFreiburg, which is also located in Baden-Württemberg, not farfrom the motorway A5. However, the specific collection sitewas in the eastern part of the city of Freiburg, approximately13 km in a direct line from the nearest motorway servicestation accessible when coming from the south (Fig. 1). Asthe activity radius of Ae. albopictus is only a few hundredmetres (Turell et al. 2005), it can hardly be assumed that themosquito left a vehicle entering Germany from the south atthat service station and actively moved to Freiburg-East. Also,a transport to its collection site after leaving a vehicle at theservice station and entering another vehicle going to Freiburg-East is unlikely since the mosquito was a male. In contrast tofemales, males do not usually follow humans into cars as theydo not feed on blood. Only exceptionally, they may followfemales entering cars for copulation. More probably, the mos-quito came directly to that part of Freiburg by a vehicle fromsouthern Europe or an introduced Ae. albopictus left a car onthe motorway service station and was able to reproduce andspread in the Upper Rhine Valley during the summer. To testthe latter possibility, an on-site inspection was carried out in

the surroundings of the collection site in early October.Numerous natural and artificial containers potentially servingas breeding sites were checked in the settlement, includingflower vases, flower pot pans and pottery in various nearbycemeteries. Finally, in the closest cemetery, some 500 m awayfrom the collection site of the submitted male, a total of 28larvae and pupae were found in two flower vases and a flowerdish which were morphologically and genetically confirmedto be Ae. albopictus after adult emergence. Thus, it is highlyprobable that the submitted male had already passed itspreimaginal development in the area and belonged to a gen-eration of mosquitoes successive to the introduced one. In thatcase, reproduction and propagation must have taken place inGermany.

To check for the further occurrence ofAe. albopictus, a gridpattern of 250 ovitraps was operated in the infested area,according to the ECDC guidelines for the surveillance ofinvasive mosquitoes in Europe (ECDC 2012), starting on theday of the on-site inspection. After 2 weeks, Aedes eggs wereregistered in three ovitraps (n=9, 14 and 40, respectively) inthe cemetery where the immature stages had previously beendetected, in addition to another Ae. albopictus pupa found in aflower vase. Further Aedes eggs (n=25), adhering to a clay

Fig. 1 Greater Freiburg area (quadrangle on the German map) withcollection sites of the Ae. albopictus adults (asterisk), the preimaginaldevelopmental stages (triangle), the eggs (triangle and square), and

nearest resting station on the motorway A5 (dot). Map taken fromGoogle®

Parasitol Res

flower pot, were detected in another cemetery about 800 m ina direct line from the first cemetery. The eggs of two ovitrapsfrom the first cemetery and those of the clay pot from thesecond cemetery turned out to be Ae. albopictus after geneticanalysis while the eggs of the third positive ovitrap from thefirst cemetery were Ae. j. japonicus. Another twoweeks later, atthe end of October, Ae. albopictus eggs (n=3 and 35, respec-tively) were again demonstrated in one ovitrap of these twocemeteries, each, in addition to several ovitraps with Ae. j.japonicus eggs and one ovitrap with Ochlerotatus geniculatuseggs. Considering the numerous competing breeding places inthe affected cemeteries, both the number of ovitraps positive forAe. albopictus eggs and the total number of eggs found suggestthe presence of enough individuals to make up a founder popu-lation. This is underlined by another submission of an adult Ae.albopictus specimen (a female) to the ‘Mückenatlas’ in mid-October 2014 from exactly the same collection site as before.

It remains to be seen whether Ae. albopictuswill still occurin that part of Freiburg in the early mosquito season of 2015,suggesting or rejecting hibernation. So far, the overwinteringby Ae. albopictus in Germany has been considered ratherunlikely due to the temperature preferences of the species. Incontrast to tropical strains, however, diapausing eggs ofEuropean Ae. albopictus have been shown to be able tosurvive a cold spell of −10 °C (Thomas et al. 2012).Therefore, the possible establishment in Freiburg-East willbe further checked, starting in spring 2015, by ovitrap andBG sentinel surveillance. It is likely that, if Ae. albopictussucceeds in establishing in Germany, this will initially takeplace in the Upper Rhine Valley in the federal state of Baden-Württemberg, not only because of a major motorway enteringGermany from the south and representing a possible entry portfor mosquitoes travelling by vehicles but also because of themild climate (Becker 2008).

To the best of the authors’ knowledge, Freiburg-East is thenorthernmost site in Europe ever detected with Ae. albopictusbreeding in the field, detached from tyre storage facilities,horticultural companies and motorways where larvae hadbeen collected more northerly before (Schaffner et al. 2001;Scholte et al. 2007; Šebesta et al. 2012). The northernmostestablished field populations can presently be found in Ticino,southern Switzerland (Neteler et al. 2013). However, modelsexist that predict suitability of the climate for the tiger mos-quito over central northwestern Europe, in particular Beneluxand the western part of Germany, in the near future (Caminadeet al. 2012).

Conclusions

The finding of Ae. albopictus preimaginal stages in the field asfar north as Freiburg, Germany, clearly indicates that condi-tions in Central Europeans countries are favourable to the

development of this invasive mosquito species at least duringsummer time and that establishment must be expected in thefuture while adaptation of the mosquito to temperate climatescontinues. The collection of the adult specimens far from themotorway and its implications demonstrate the significancethe ‘Mückenatlas’ or similar citizen science projects may havefor passive mosquito surveillance. As active surveillance bytrapping is usually very focussed in space and time due tofinancial constraints, it is usually the general public who willdetect changes in the mosquito fauna first, even if thesedetections are not obvious to them.

Acknowledgments The ‘Mückenatlas’ is part of a mosquito monitor-ing project financially supported by the German FederalMinistry of Foodand Agriculture (BMEL) through the Federal Office for Agriculture andFood (BLE), grant number 2810HS022. We are grateful to Adrian Pont,Oxford University Museum for Natural History, for critically reading themanuscript.

References

Becker N (2008) Influence of climate change on mosquito developmentand mosquito-borne diseases in Europe. Parasitol Res 103(Suppl 1):S19–S28

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 ofAedes albopictus into Germany, July to October 2012.Parasitol Res 112:1787–1790

Caminade C, Medlock JM, Ducheyne E, McIntyre KM, Leach S, BaylisM, Morse AP (2012) Suitability of European climate for the Asiantiger mosquito Aedes albopictus: recent trends and future scenarios.J R Soc Interface 9:2708–2717

ECDC (European Centre for Disease Prevention and Control) (2012)Guidelines for the surveillance of invasive mosquito species inEurope. ECDC Technical Report, Stockholm

Gratz NG (2004) Critical review of the vector status of Aedes albopictus.Med Vet Entomol 18:215–227

Kampen H, Zielke D, Werner D (2012) A new focus of Aedes japonicusjaponicus (Theobald 1901) (Diptera, Culicidae) distribution in west-ern Germany: Rapid spread or a further introduction event? ParasitVectors 5:284

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

Kampen H, Medlock JM, Vaux AGC, Koenraadt CJM, van Vliet AJH,Bartumeus F, Oltra A, Sousa CA, Chouin S, Werner D (2014)Approaches to passive mosquito surveillance in the EU. ParasitVectors, submitted

Medlock JM, Hansford KM, Schaffner F, Versteirt V, HendrickxG, ZellerH, Van Bortel W (2012) A review of the invasive mosquitoes inEurope: Ecology, public health risks, and control options. Vector-Borne Zoon Dis 12:435–447

Neteler M,Metz M, Rocchini D, Rizzoli A, Flacio E, Engeler L, Guidi V,Lüthy P, TonollaM (2013) Is Switzerland suitable for the invasion ofAedes albopictus? PLoS One 8:e82090

Pluskota B, Storch V, Braunbeck T, BeckM, Becker N (2008) First recordof Stegomyia albopicta (Skuse) (Diptera: Culicidae) in Germany.Eur Mosq Bull 26:1–5

Parasitol Res

Schaffner F, Boulétreau B, Guillet B, Guilloteau J, Karch S (2001) Aedesalbopictus (Skuse, 1894) established in metropolitan France. EurMosq Bull 9:1–3

Schaffner F,Medlock JM, VanBortelW (2013) Public health significanceof invasivemosquitoes in Europe. ClinMicrobiol Infect 19:685–692

Scholte EJ, Jacobs F, Linton YM, Dijkstra E, Fransen J, TakkenW (2007)First record of Aedes (Stegomyia) albopictus in the Netherlands. EurMosq Bull 22:5–9

Šebesta O, Rudolf I, Betášová L, Peško J, Hubálek Z (2012) An invasivemosquito species Aedes albopictus found in the Czech Republic,2012. Euro Surveill 17:20301

Thomas SM,Obermayr U, Fischer D, Kreyling J, Beierkuhnlein C (2012)Low-temperature threshold for egg survival of a post-diapause and

non-diapause European aedine strain, Aedes albopictus (Diptera:Culicidae). Parasit Vectors 5:100

Turell MJ, Dohm DJ, Sardelis MR, O’Guinn ML, Andreadis TG,Blow JA (2005) An update on the potential of NorthAmerican mosquitoes to transmit West Nile virus. J MedEntomol 42:57–62

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

Werner D, Kronefeld M, Schaffner F, Kampen H (2012) Two invasivemosquito species, Aedes albopictus and Aedes japonicus japonicus,trapped in south-west Germany, July to August 2011. Euro Surveill17:20067

Parasitol Res