First record of Stegomyia albopicta (Skuse) (Diptera: Culicidae) in Germany

Abstract

With the help of the international used tyre trade, the Asian tiger mosquito, Stegomyia albopicta, has been able to expand its range world-wide. In 1979, the species was recorded in Europe for the first time in Albania, and has since been reported in 14 European countries. In addition to its rapid spread, St. albopicta is of particular interest due to its vector capacity for certain infectious viral diseases. Due to the increasing threat of an introduction of St. albopicta from neighbouring countries, a national monitoring programme was initiated in Germany by KABS (German Mosquito Control Organization) in 2005. In addition to used tyre trading companies, sampling was carried out at container terminals at inland ports along the Rhine, terminals receiving trains from Italy, and rest areas and parking lots along the German highway A5 coming from the south. At the end of September 2007, five eggs from the non-indigenous species St. albopicta were found on oviposition substrate in an ovitrap in the southern section of this major north-south highway. This is the first report of this non-indigenous species in Germany and demonstrates that live adults can be transported over long distances within motor vehicles.

Full text

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European Mosquito Bulletin, 26 (2008), 1-5.
Journal of the European Mosquito Control Association
ISSN 1460-6127; w.w.w.europeanmosquitobulletin.com
First published online 1 September 2008
First record of Stegomyia a lbopicta (Skuse)
(Diptera: Culicidae) in Germany
Björn Pluskota
1,2
, Volker Storch
2
, Thomas Braunbeck
2
, Matthias Beck
1
and
Norbert Becker
1,2
1
German Mosquito Control Association (GMCA/KABS), Ludwigstr. 99, D-67165 Waldsee, Germany;
2
Department of Zoology, University of Heidelberg, Im Neuenheimer Feld 230, D-69120 Heidelberg, Germany.
Abstract
With the help of the international used tyre trade, the Asian tiger mosquito, Stegomyia albopicta, has
been able to expand its range world-wide. In 1979, the species was recorded in Europe for the first
time in Albania, and has since been reported in 14 European countries. In addition to its rapid spread,
St. albopicta is of particular interest due to its vector capacity for certain infectious viral diseases. Due
to the increasing threat of an introduction of St. albopicta from neighbouring countries, a national
monitoring programme was initiated in Germany by KABS (German Mosquito Control Organization)
in 2005. In addition to used tyre trading companies, sampling was carried out at container terminals at
inland ports along the Rhine, terminals receiving trains from Italy, and rest areas and parking lots
along the German highway A5 coming from the south. At the end of September 2007, five eggs from
the non-indigenous species St. albopicta were found on oviposition substrate in an ovitrap in the
southern section of this major north-south highway. This is the first report of this non-indigenous
species in Germany and demonstrates that live adults can be transported over long distances within
motor vehicles.
Keywords: mosquito, Stegomyia albopicta, Aedes albopictus, Germany
Introduction
The mosquito Stegomyia albopicta, previously
Aedes albopictus (Reinert & Harbach 2005),
originating from Southeast Asia, has
undergone a noteworthy expansion of its range
in the last few decades (Hawley 1988). Mainly
with the help of the international used tyre
trade, the so-called “Asian tiger mosquito” has
been able to travel across very large distances
and between continents (Reiter 1998). Due to
its ability to colonise a wide range of natural
and artificial breeding places, and coupled with
the resistance of its eggs to desiccation and the
relative lack of host preference (Hawley 1988),
this species has been able to rapidly build up
populations in new geographic regions large
enough to successfully establish stable
populations. Once consolidated, national trade
and traffic has facilitated subsequent rapid
spread into further regions within these new
countries (Moore & Mitchell 1997).
In Europe, St. albopicta was first reported in
Albania in 1979 (Adhami 1998) and later in
Italy in 1990, where it was introduced through
the import of used tyres from the USA into the
port town of Genoa (Sabatini et al. 1990, Dalla
Pozza and Majori 1992). Within the next few
years, the species rapidly dispersed to other
regions of Italy (Romi 1994), and in the
meantime it has been reported from France
(Schaffner & Karch 2000), Serbia and
Montenegro (Petric et al. 2001), Belgium
(Schaffner et al 2004), Switzerland (Flacio et
al. 2004), Greece (Samanidou et al. 2005),
Croatia (Klobucar et al. 2006), Spain (Aranda
et al. 2006) and the Netherlands (Scholten et
al. 2007).

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Apart from its rapid geographical dispersion,
St. albopicta is of special interest due to its
vector capacity for infectious viral diseases
(Reiter et al. 2006). It is, for example, assumed
that this species was involved in the spread of
chikungunya virus to humans in Italy in 2007
(Beltrame et al. 2007).
An analysis of the literature and preliminary
unpublished laboratory data suggests that,
given the current climatic conditions, the only
region in Germany where St. albopicta might
be expected to establish persistent populations
is the Upper Rhine valley. This region is
located in southwestern Germany, is
approximately 300 km long and on average 30
km wide, and has an especially mild climate
compared to central European standards
(Liedtke 2002).
In May 2005, KABS (German Mosquito
Control Organization) initiated a project to
take action against the increasing threat of St.
albopicta introduction into and its
establishment in Germany. The primary goal
of the project is to analyse the pathways of
introduction into Germany, thereby identifying
sites that have the highest probability of being
colonized by St. albopicta, and to regularly
monitor these “hot spots”.
The primary mode of dispersal of St. albopicta
by human activity has been through transport
of desiccation-resistant eggs with cargo that
previously contained water serving as breeding
sites. The most important type of cargo is old
tyres that have been stored outdoors (Knudsen
1995). Therefore, companies processing or
trading used tyres are most likely to introduce
St. albopicta and were therefore given high
monitoring priority.
Another type of cargo in which a large number
of eggs or larvae can be transported over great
distances is the so-called Lucky Bamboo
(Dracaena spp.). For instance, the trade in this
ornamental plant, which is boxed with standing
water, permits an “ideal insectary in transit”
and was the reason for the introduction of St.
albopicta from Asia to California (Madon et
al. 2004). Similarly, multiple introductions of
the Asian tiger mosquito to the Netherlands in
greenhouses of horticulture companies could
be traced back to intensive trade of this plant
(Scholten et al. 2007). However, we were not
able to locate any intermediate trading
companies for Lucky Bamboo within our
monitoring area or in other parts of Germany.
Due to high humidity and cool air temperature,
freight containers offer conditions suitable for
the transport of living insects (Reiter 1984).
Therefore, container terminals at inland ports
along the Rhine as well as terminals receiving
trains from Italy were regularly monitored.
Rest areas and parking lots along the German
highway A5 have a high potential to serve as
sites of introduction and were, therefore, major
components of the monitoring programme.
This highway runs from south to north through
the entire Upper Rhine valley and is part of the
most important continuous south-north
highway in Europe, running from Sicily to
Stockholm. It is a main truck and tourist route
for those returning from Italy and southern
France to Germany, the Benelux and
Scandinavia. Transportation of adult St.
albopicta by cars and trucks was documented
during a monitoring programme in 2003, when
the species was detected for the first time in
Switzerland (Flacio et al. 2004). Since then,
multiple introductions of Asian Tiger
mosquitoes from Italy to southern Switzerland
have been observed, and, in autumn 2007, it
was first recorded in northern Switzerland
(Bundesamt für Gesundheit 2007). There are
indications that the number of mosquitoes
transported correlates with traffic volume
(Flacio et al. 2006).
Materials and Methods
During 2007, the monitoring programme
employed 80-100 ovitraps at 47 trapping sites.
The number of ovitraps used per location
varied between one and six, depending on
suitable habitats and the probability of St.
albopicta being introduced to the site.
From the beginning of May to the end of
September of each year, potential sites are
monitored using ovitraps, which are examined
for eggs and larvae every 14 days. In addition,
in the areas surrounding the traps, promising
shrubs and trees are checked for mosquitoes
using the human bait method. Eggs are
preliminarily identified microscopically and
are kept in the laboratory at 25°C and 80%
humidity for one week to ensure complete
embryonic development. Deoxygenated tap
water, enriched with a small amount of

3
brewer’s yeast, is used as a hatching stimulus.
Following hatching, larvae are reared to the
adult stage, if possible. Identification keys of
Becker et al. (2003) are used to determine the
species.
Results
In total, four species from the family Culicidae
have been collected since the monitoring
programme was initiated. Most of the
mosquitoes collected were of the indigenous
dendrolimnobiotic species Ochlerotatus
geniculatus and Anopheles plumbeus, as well
as Culex pipiens in isolated cases. During the
last trap inspection, at the end of September
2007, five eggs from the non-indigenous St.
albopicta were found on the oviposition
substrate in one of the traps at a parking lot in
the southern part of the German highway A5
(Latitude 47°42’22”N, Longitude 7°31’28”E).
Only two of the eggs hatched after being
flooded three times for 72 hours at weekly
intervals and partial drying between flooding.
Both hatched larvae developed into adults and
were conclusively identified as St. albopicta.
No St. albopicta eggs were found in the second
ovitrap at the same site, nor were adults found
up to 200 m around the traps using the human
bait method.
Discussion
The discovery of eggs of St. albopicta! in an
ovitrap located at a parking lot on a highway
used by tourists and transport vehicles coming
from southern Europe is the first documented
case of this non-indigenous species in
Germany. Furthermore, it demonstrates that
living adults can be transported over extended
distances within these vehicles. Through
regular monitoring and the initiation of control
measures, St. albopicta!has only been reported
sporadically and in small numbers in parts of
southern and, since autumn 2007, also in
northern Switzerland. The female, which laid
the above-mentioned eggs, thus most likely
came from more distant populations in
northern Italy.
Particularly at the end of vacation periods in
Germany, Scandinavia and Benelux, a large
number of tourists drive back from Italy on the
German highway A5, a major south-north
route. In vacation areas St. albopicta! is most
likely attracted to the campers and caravans by
human olfactory cues. Since these mobile
living spaces are mostly unused while driving,
mosquitoes attempting to feed during transport
are less likely to be discovered than in cars and
truck cabins.
The fact that only five eggs were found in only
one trap and that no adults were collected
implies that the eggs were laid by a single
transported female that was already
inseminated. According to Gubler (1970), St.
albopicta! females lay an average of 62.5 eggs
and tend to deposit these in multiple
oviposition sites (Hawley 1988). Therefore, it
is likely that more eggs from this female could
have been found in natural or human-made
containers at this site. Nevertheless, the
probability of successful colonization of an
empty habitat patch depends, besides species-
specific and environmental factors, mainly on
the number of immigrants and the initial size
of the founder population (Hanski 1999).
Therefore, the establishment of a stable
population on the basis of such a small number
of eggs the next spring is rather unlikely.
Cornel & Hunt (1991) also assumed that, even
though St. albopicta!has been reported to have
been transported into South Africa several
times, due to the small numbers transported at
each occurrence, a breeding population has not
been established there.
However, additional mosquitoes introduced in
the next year could supplement the small
founder population genetically as well as
quantitatively, preventing them from dying
out. Such a mechanism, by which so-called
“sink populations” with negative population
growth (r < 0) do not expire due to regular
immigration from distant “source populations”
(r > 0), is known from metapopulation ecology
(Hanski 1999) and is also described as the
“rescue effect” in island biogeography (Brown
& Kodric-Brown 1977). In addition, with
increasing population density and an
expanding range in Italy, the number of “blind
passengers” and consequently successful
introductions to hitherto unsettled areas and
also immigrations in existing small founder
populations along human-made distribution
routes increases. For example, Flacio et al.
(2006) reported that the invasion of the
mosquitoes from Italy to southern Switzerland
continues to grow; the number of positive
cases increased by 35% from 2005 to 2006.

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It has been shown that, after an introduction
and establishment of a sufficiently large
population, St. albopicta! can rapidly increase
its population size and range (Fontenille &
Toto 2001). If control measures are initiated
too late, there is a great risk of stable
establishment of an originally small and
locally restricted population and dispersion of
St. albopicta! to other climatically suitable
regions.
Therefore, in 2008, the number of surveillance
traps will be increased at the positive site,
potential breeding sites will be mapped and
appropriate control measures will be
implemented. Furthermore, monitoring will be
intensified in general and international
cooperation will be initiated, especially with
the countries neighbouring Germany. Public
relations measures such as an information
homepage and information brochures will be
prepared in order to activate community
participation.
References
Adhami, J. & Reiter, P. (1998) Introduction
and Establishment of Aedes (Stegomyia)
albopictus Skuse (Diptera: Culicidae) in
Albania. Journal of the American Mosquito
Control Association, 14, 340-343.
Aranda, C., Eritja, R. & Roiz, D. (2006) First
record and establishment of Aedes
albopictus in Spain. Medical and
Veterinary Entomology, 20, 150-152.
Becker, N., Petric, D., Zgomba, M., Boase, C.,
Dahl, C., Lane, J. & Kaiser, A. (2003)
Mosquitoes and their control. Kluwer
Academic / Plenum Publisher, New
York.498 pp.
Beltrame, A., Angheben, A., Bisoffi, Z.,
Monteiro, G., Marocco, S., Calleri, G. et al.
(2007) Imported chikungunya infection,
Italy. Emerging Infectious Diseases.
Available from
http://www.cdc.gov/EID/content/13/8/1264
.htm.
Brown, J.H., & Kodric-Brown, A. (1977)
Turnover rates in insular biogeography:
effect of immigration on extinction.
Ecology, 58, 445-449.
Bundesamt für Gesundheit, Schweiz. (2007)
Epi-Notiz: Chikungunya-Fieber. Bulletin,
48, 857-859.
Cornel, A.J. & Hunt, R.H. (1991) Aedes
albopictus in Africa? First records of live
specimens in imported tires in Cape Town.
Journal of the American Mosquito Control
Association, 7, 107-108.
Dalla Pozza, G.L. & Majori, G. (1992) First
record of Aedes albopictus establishment in
Italy. Journal of the American Mosquito
Control Association, 8, 318-320.
Flacio, E., Lüthy, P., Patocchi, N., Guidotti, F.,
Tonolla, M. & Peduzzi R. (2004) Primo
ritrovamento di Aedes albopictus in
Svizzera. Bollettino della Societa` Ticinese
di Scienze Naturali, 92, 141–142.
Flacio, E., Lüthy, P., Patocchi, N., Peduzzi, R.,
Guidotti, F. & Radczuweit, S. (2006)
Bericht 2006 zur Überwachung und
Bekämpfung der asiatischen Tigermücke,
Aedes albopictus, im Kanton Tessin.
Jahresbericht 2006 Gruppo lavoro zanzare,
Divisione della salute publica, 6501
Bellinzona, 1-10.
Fontenille, D., Toto, J.C. (2001) Aedes
(Stegomyia) albopictus (Skuse), a potential
new dengue vector in Southern Cameroon.
Emerging Infectious Diseases, 7, 1066-
1067.
Gubler, D.J. (1970) Comparison of
reproduction potentials of Aedes
(Stegomyia) albopictus Skuse and Aedes
(Stegomyia) polynesiensis Marks. Mosquito
News, 30, 201-209.
Hawley, W.A. (1988) The biology of Aedes
albopictus. Journal of the American
Mosquito Control Association (Suppl.), 4,
1-39.
Hanski, I. (1999) Metapopulation Ecology.
Oxford University Press, Oxford.
Klobucar, A., Merdic, E., Benic, N., Baklaic,
Z. & Krcmar, S. (2006) First record of
Aedes albopictus in Croatia. Journal of the
American Mosquito Control Association,
22, 147-148.
Knudsen, A.B. (1995) Global distribution and
continuing spread of Aedes albopictus.
Parassitologia, 37, 91-97.!
Petric, D., Pajovic, I., Ignjatovic Cupina, A. &
Zgomba, M. (2001) Aedes albopictus
(Skuse, 1894) new mosquito species
(Diptera, Culicidae) in entomofauna of
Yugoslavia. Symposia of the entomologists
of Serbia, Entomological Society of Serbia,
Belgrade, Serbia and Montenegro, Goc, pp.
26-29.
Liedtke, H. & Marcinek, J. (2002) Physische
Geographie Deutschlands, Gotha, Stuttgart,
Klett-Perthes-Verlag.

5
Madon, M.B., Hazalrigg, J.E., Shaw, M.W.,
Kluh, S. & Mulla, M.S. (2004) Has Aedes
albopictus established in California?
Journal of the American Mosquito Control
Association, 19, 298.
Moore, C.G. & Mitchell C.J. (1997) Aedes
albopictus in the United States: Ten-year
presence and public health implications.
Emerging Infectious Diseases, 3, 329-334.
Reinert, J.F. & Harbach, R.E. (2005) Generic
changes affecting European aedine
mosquitoes (Diptera: Culicidae: Aedini)
with a checklist of species. European
Mosquito Bulletin, 19, 1–4.
Reiter, P. & Darsie, R.F., Jr. (1984) Aedes
albopictus in Memphis, Tennessee (USA):
An achievement of modern transportation?
Journal of the American Mosquito Control
Association, 44, 396-399.
Reiter, P. (1998) Aedes albopictus and the
world trade in used tires, 1988-1995: The
shape of things to come. Journal of the
American Mosquito Control Association,
14, 83-94.
Reiter, P., Fontenille, D., & Paupy, C. (2006)
Aedes albopictus as an epidemic vector of
chikungunya virus: another emerging
problem? The Lancet Infectious Diseases,
6, 463-464.
Romi, R. (1994) Aedes albopictus in Italia:
problemi sanitari, strategie di controllo e
aggiornamento della distribuzione al 30
settembre 1994. Notiziario I.S.S., 7, 7-11.
Sabatini, A., V. Raineri, V.G. Trovato & M.
Coluzzi. (1990) Aedes albopictus in Italia e
possibile diffusione della specie nell`area
Mediterranea. Parassitologia, 32, 301-304.
Samanidou-Voyadjoglou, A., Patsoula, E.,
Spanakos, G. & Vakalis, N.C. (2005)
Confirmation of Aedes albopictus (Skuse)
(Diptera: Culicidae) in Greece. European
Mosquito Bulletin, 19, 10–12.
Schaffner, F., Boulètreau, B., Guillet B.,
Guilloteau J., & Karch, S. (2000) Premiere
observation d`Aedes albopictus (Skuse,
1894) en France métropolitaine. Comptes
Rendus de l´Academie des Sciences, Paris,
Sciences de la Vie, 323, 373-375.
Schaffner, F., Van Bortel, W. & Coosemans,
M. (2004) First record of Aedes
(Stegomyia) albopictus in Belgium. Journal
of the American Mosquito Control
Association, 20, 201-203.
Scholten, E-J., Jacobs, F., Linton, Y-M.,
Dijkstra, E., Fransen, J. & Takken, W.
(2007) First record of Aedes (Stegomyia)
albopictus in the Netherlands. European
Mosquito Bulletin, 22, 5-9.