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First Detection of the Asian Tiger Mosquito, Aedes ( Stegomyia ) albopictus

(Diptera: Culicidae), in Tunisia

Article in Journal of Medical Entomology · April 2019

DOI: 10.1093/jme/tjz026

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 Journal of Medical Entomology, XX(X), 2019, 1–4
doi: 10.1093/jme/tjz026
Vector-Borne Diseases, Surveillance, Prevention Research

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First Detection of the Asian Tiger Mosquito, Aedes
(Stegomyia) albopictus (Diptera: Culicidae), in Tunisia
Ali Bouattour,1 Fatma Khrouf, Adel Rhim, and Youmna M’ghirbi

Laboratoire d’entomologie Médicale, Institut Pasteur de Tunis, Université de Tunis El Manar, 13, Place Pasteur, 1002 Tunis-
Bélvédère, Tunisia, and 1Corresponding author, e-mail: ali.bouattour@pasteur.tn

Subject Editor: Thomas Scott

Received 19 October 2018; Editorial decision 16 February 2019

Abstract
Aedes albopictus (Skuse) is a widespread invasive mosquito vector species with a distribution including
tropical and temperate climates; its range is still expanding. Aedes albopictus populations were recently
detected in Morocco and Algeria, the countries neighboring Tunisia, but never in Tunisia. In 2018, we initiated
an intensive field study using BG-Sentinel Traps, ovitraps, larval surveys, and citizens’ reports to determine
whether Ae. albopictus populations exist in Tunisia. In October 2018, we collected adults and larval stages of
Ae. albopictus in Carthage, Amilcar, and La Marsa, less than 20 km, northeast of Tunis, the Tunisian capital.
These Ae. albopictus larvae were primarily collected from Phoenician funeral urns at the archeological site of
Carthage. This is, to our knowledge, the first detection of Ae. albopictus in Tunisia.

Key words: Aedes albopictus, invasive mosquito, BG-Sentinel, ovitrap, Tunisia

The Asian tiger mosquito, Aedes (Stegomyia) albopictus (Skuse), is
thought to have evolved in the tropical and subtropical forests of
southeastern Asia (Hawley 1988, Shaikevich and Talbalaghi 2013).
Currently, one of the world’s most threatening invasive species
(Goubert et al. 2016), it is a vector for several arboviruses including
dengue (DENV), chikungunya (CHKV), Zika (ZIKV), and yellow
fever virus and Dirofilaria parasites (Cancrini et al. 2007, Paupy
et al. 2009, Medlock et al. 2012, Heitmann et al. 2017, Amraoui
et al. 2018). Aedes albopictus, of significant public health threat,
was introduced into Africa in 1991 (Gratz 2004). This mosquito was
detected in Gabon in 2007 where its invasion probably contributed
to the emergence of CHIKV and was considered to be the main
ZIKV epidemic vector (Grard et al. 2014).
In the Mediterranean region, Ae. albopictus was first detected in
Albania in 1979 (Adhami and Reiter 1998). This invasive mosquito was
already well established in large areas of Southern Europe (Heitmann
et al. 2017) and has been reported in all European Mediterranean
countries; it has caused autochthonous cases of DENV and CHIKV
in Italy, France, and Spain (Calba et al. 2017, ECDC 2018). Several
cases of imported ZIKV were reported among travelers returning
to European countries including Croatia (Vilibić-čavlek et al. 2017)
and Spain (Millet et al. 2017). Despite the large number of viraemic
travelers in areas where Ae. albopictus is established, there have
been no reports of local vector-borne transmission in Europe. The
European populations of Ae. albopictus are probably not efficient
vectors of ZIKV. Indeed, based on experimental infections of Ae.
albopictus populations from France and Italy, Jupille et al. (2016)
and Di Luca et al. (2016) have demonstrated that the Asian tiger
mosquito is less suitable to sustained local transmission of ZIKV than
Aedes aegypti (Linnaeus) (Diptera: Culicidae).
Aedes albopictus is considered to be one of the fastest-spreading
insect species of the past few decades, having spread to several
countries on every continent except Antarctica.
This invasive species typically moves within and between countries
through the transport of its cold-hardy, desiccation-resistant, long-
lived eggs in natural and artificial containers (Hawley 1988, Juliano
et al. 2002). The international trade of tires, decorative plants (such
as bamboo), and other goods thus inadvertently transports the eggs
of Ae. albopictus (Knudsen 1995). The species was introduced into
the Torres Strait and the southern Fly River region in Australia
through water supplies on foreign fishing boats (Van den Hurk et al.
2016). In Europe, where the first record of the species was made
in Albania in 1979 (Adhami and Reiter 1998) followed by Italy
in 1991 (Dalla Pozza and Majori 1992). The apparent vehicle of
invasion and colonization is the transport of used tires. Established
populations of Ae. albopictus were also found in two tire dumps
in France in 1999 (Schaffner and Karch 2000). Aedes albopictus is
now present in all Mediterranean European countries as well as in
parts of Turkey and the Middle East (Bonizzoni et al. 2013). The
changing climate, especially in arid regions, and global trade using
rapid conveyances, together with the expansion of port cities, have
contributed to its global spread over the past two decades.
The Asian tiger mosquito was recently reported in Algeria
(Benallal et al. 2016) and Morocco (Bennouna et al. 2017). The

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2 Journal of Medical Entomology, 2019, Vol. 00, No. 00
expansion of this species to our region led the Ministry of Heath
of Tunisia, in collaboration with WHO-EMRO, to begin mosquito
monitoring and surveillance programs. To participate actively in
this program from northern to southern Tunisia, we carried out a
monitoring and early detection of invasive mosquito species focused
especially on the introduction of Ae. albopictus.
Materials and Methods
We conducted a control and surveillance program of Ae. albopictus,
from northern to southern Tunisia from April 2015 to September
2018, placing a total of 350 standard ovitraps at different points
of entry to the country (ports and airports), in border areas and in
several urban and suburban sites controlled by environmental and
public health partners; we examined the egg paddle on a weekly
basis. Map showing the distribution of ovitraps was constructed
using VECMAP desktop software (AVIAGIS; Fig. 1). The ovitraps
were small black plastic containers (2 liters) partially filled with
water and baited with hay and leaves. In each container, we placed a
masonite rough paddle for Aedes females to lay eggs. For Aedes adult
capture, BG-Sentinel Traps (Biogents AG, Regensburg, Germany)
baited by BG-Lure dispenser cartridge were installed in the gardens
of individuals in neighborhoods near points of entry.
In addition, we prospected various potential breeding
containers for Ae. albopictus including barrels, used tires, mud
pots, buckets, tanks, and wells. In parallel, other mosquito
breeding sites (wadis, natural water sources, and hill lakes)
were also investigated. Mosquito larvae were collected using a
Fig. 1. Map of spatial distribution of ovitraps in Tunisia.
commercial mosquito-dipper (350 ml). Where a dipper could not
be used, a siphon collector for mosquito larvae was used for small
containers such as tires. Larvae and adults were identified using the
identification key and interactive CD ROM of the Mosquitoes of
Europe (Schaffner et al. 2001).
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Ovitraps cannot cover an entire country. They are extremely
time-consuming and labor intensive. Some ovitraps may go entirely
unnoticed to gravid female (Kampen et al. 2015). We therefore
completed our monitoring by passive surveillance, incorporating
the observations of alerted citizens, “Citizen science” (Dickinson
et al. 2012, Kampen et al. 2015). This surveillance is considered
to be an effective way to find rare organisms, track invasions such
as mosquitoes, and has been used in many countries to monitor
invasive Aedes (ECDC 2014, Kampen et al. 2015). The public was
informed through social media about the risk of Ae. albopictus
being introduced into Tunisia and its role as a vector of dangerous
pathogens. Its typical morphology, behavior (aggression), and
breeding sites were all described. Public responses were received
through Institute Pasteur website and Facebook, Messenger, Twitter,
and LinkedIn accounts of laboratory members.
Results
No Ae. albopictus were detected during the period of investigation
from April 2015 to September 2018. However, in early October
2018, a Facebook post was made about the presence of mosquitoes
not typically seen in Carthage (20 km from Tunis; 36° 51′ 25.51″
N; 10° 20′ 4.78″ E). At different outdoor points in Carthage and
its neighboring cities, we carried out an entomological investigation
using BG-traps and prospected suitable breeding sites. We collected
a total of 76 Ae. albopictus adults (70 females and 6 males) in
Carthage, a wealthy coastal city and home to approximately 22,000
inhabitants who typically live in single-family homes surrounded
by gardens with fruit trees (orange, olive, loquats) and decorative
plants. In addition to these adults, 20 of 23 prospected Phoenician
funeral urns (Fig. 2), in the Phoenician and Roman archaeological
sites of Carthage, revealed the presence of Ae. albopictus, Culex
pipiens (Linnaeus) (Diptera: Culicidae), and Culiseta longiareolata
(Macquart) (Diptera: Culicidae) larvae. Aedes albopictus adults
were also collected in Amilcar (adjacent to Carthage) and La Marsa
(36° 52′ 58.98″ N; 10° 19′ 15.88″ E) as well as larvae in a plastic
bucket and in one used tire (Table 1).
Discussion
Alerted to and educated about the problem, the public was the first
to detect Ae. albopictus in Tunisia; passive surveillance thus offers an
effective tool for tracking invasive mosquitoes. The meteorological
conditions of September 2018 may have helped to establish Ae.
albopictus, which may have been introduced by pleasure boats
coming from Italy that dock in the port of Sidi Boussaid 3 km from
Carthage. In September and October 2018, 17 confirmed cases of
West Nile meningitis (leading to one death) were reported in the
region of Sousse (central coastal; ONMNE 2018). Our entomological
investigations around West Nile cases showed high densities of Cx.
pipiens and Cx. perexiguus (Theobald) (Diptera: Culicidae), but no
Ae. albopictus, confirming that climatic conditions were suitable for
the development of mosquitoes. It was not surprising to detect the
Asian tiger mosquito in Carthage and its neighboring cities, given that
the mosquito is well established in the Italian islands of Pantelleria
and Lampedusa, the final bit of Europe facing northern Tunisia (Di
Luca et al. 2017). In addition, suitability models using Random
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Fig. 2. Phoenician funeral urns, positive breeding sites of Aedes albopictus larvae in the archeological site of Carthage, Tunisia.

Table 1. Number of collected mosquito larvae and adults in References Cited

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