What Do We Know About the Invasive Mosquitoes Aedes atropalpus and Aedes triseriatus?

Mosquito-borne diseases are a serious concern in Europe since the proliferation of invasive mosquito species increases the risk of epidemics. Aedes spp. (Diptera: Culicidae) are among the most dangerous mosquito vectors in Europe. Among Aedes spp., less attention has been paid to the North American invasive species, Aedes atropalpus and Aedes triseriatus, although these species are vectors of serious diseases. This article aims to provide information about the current status and prospective of these species in Europe. While the presence of Ae. atropalpus in the European continent is still debated, Ae. triseriatus is no longer present in the European continent, but accidental introductions have been recently reported. Nevertheless, the climatic changes and global market increase the possibility of introduction of North American Aedes species in Europe. The present article contains a brief overview of the biology, ecology, and vector competence of these two mosquito vectors, outlining their potential to invade new areas and medical importance. We highlighted some bioecological traits that need to be considered to design surveillance programs tailored for these species. Lastly, research challenges aimed to improve basic knowledge and control programs targeting these species are presented.


Introduction
Since the first report of Aedes albopictus (Skuse) in Europe, dating back to 1979 in Albania, concerns about the establishment of invasive mosquito vectors started rising [1]. The subsequent detection of this species in Italy in 1990 revealed how much the risk was real and increased the concerns also about the possible role of invasive Aedes spp. in the transmission and diffusion of exotic pathogens and parasites [2,3]. Mosquito vectors are responsible for the transmission of several human and animal pathogens. The majority of mosquitoes of epidemiological importance are invasive species, such as Ae. albopictus, Aedes aegypti (L.), and Culex quinquefasciatus Say [4][5][6]. Nevertheless, almost 20 years have passed since the first cases of pathogen transmission to humans by Aedes species in the European continent, when chikungunya virus (CHIKV) first spread in Northern Italy in 2007, causing more than 200 reported cases [7][8][9]. Subsequent CHIKV and dengue virus (DENV) outbreaks were also reported in Southern France in 2010 [10,11]. In this scenario, surveillance and preventive programs have been carried out to assess the presence and establishment of invasive mosquito species, although less attention has been paid to North American Aedes species.

Invasive Mosquito Vectors in Europe: Let Us Make the Point
Through the last two decades, European countries have faced repeated outbreaks of diseases transmitted by invasive mosquito vectors, due to sporadic inoculation, as well as permanent establishment among the native fauna, of invasive alien Aedes species [2]. The emergence of vector-borne diseases could be ascribed to several factors, including global trade, urbanization processes, as well as climate changes [12••]. The reduced biodiversity of urban areas and favourable conditions for mosquito proliferation, coupled with the increase in human population density and availability of artificial breeding sites can facilitate the proliferation of mosquito vector species. Consequently, species adapted to urban environments can potentially expand their range to densely populated non-endemic regions increasing the risk of arbovirus outbreaks [13].
In Europe, the native African species, Ae. aegypti, and the three indigenous Asian species, Ae. albopictus, Ae. japonicus japonicus (Theobald), and Ae. koreicus (Edwards) are the most widely known invasive vector mosquitoes. These species have the highest epidemiological importance in the region and are commonly targeted species by the local health authorities [14]. Moreover, two additional Aedes species native to the North American continent have been detected in Europe, Aedes atropalpus (Coquillett) and Ae. triseriatus (Say). These species can add another layer of complexity to the already complex epidemiology of arbovirus transmission in European countries [2].

North American Invasive Aedes Species
In Europe, two Aedes invasive species from North America have been reported, Ae. atropalpus and Ae. triseriatus. The presence of Ae. atropalpus in the continent is still debated, while Ae. triseriatus is no longer present in the European continent ( Fig. 1) [2,15,16]. The occurrence of periodical invasions, driven by commercial exchanges, should be carefully considered to inform surveillance activities and improve arbovirus preparedness and response. Indeed, the lack of reliable information and the limitations of mosquito surveillance techniques can lead to the failure to detect or to the underestimating of the presence and abundance of species with low population densities or if their biology and behaviors are dissimilar from the attractants used by the mosquito traps designed for anthropophilic species [17,18]. Unfortunately, this could be the case for the two North American species Ae. atropalpus and Ae. triseriatus.
This article provides a short overview of the invasion potential, biology, ecology, and vector competence of Ae. atropalpus and Ae. triseriatus. In the last sections, vector control challenges for public health are outlined.

Aedes atropalpus
Aedes atropalpus, also known as the American rock pool mosquito (Fig. 2), is a riparian species native to North-East America (Fig. 1), which adapted to develop also in urban areas using artificial containers as breeding sites [2]. Aedes atropalpus is a competent vector for several pathogens, including La Crosse and West Nile virus, although it seems to have limited medical importance in the field [19••, 20, 21].
The species is widely present in the North American continent [22], and it has been introduced several times in Europe through the importation of used tires containing non-desiccating eggs of Ae. atropalpus [23]. The first documented detections occurred in 1996 and 1997 in northern Italy [24•, 25], followed by France and the Netherlands in the 2000s [2,20]. It has been reported that Ae. atropalpus was able to develop and reproduce for a short period of time in well-defined areas [2]; then, it has been eliminated by public health authorities from France in 2003 and 2005 and Switzerland in 2008 [15]. However, information on the presence of Ae. atropalpus in Italy and the Netherlands are contrasting. Indeed, it has been affirmed that the species has been eliminated from both countries through insecticidebased interventions [2, 16, 20, 24•, 25]. However, according to WRBU [15], Ae. atropalpus is established in Italy and the Netherlands (Fig. 1). The low dispersal ability due to Ae. atropalpus limited flight ability makes this species more abundant around natural aquatic habitats [21]. In addition, although this species prefers warm aquatic environments [26], its ability to acclimate to colder climates in Northern Europe cannot be discarded due to its distribution in Northern America [27].
Conversely to many other Aedes species, Ae. atropalpus females do not require blood meals to produce fertile eggs, which are usually oviposited directly on the water surface [28]. However, Ae. atropalpus are active biters both during day and night and can feed on several mammalian and bird hosts, including humans [21]. Nevertheless, the ability to reproduce independently from blood meals permits this species to produce eggs earlier in the spring season compared to other Aedes mosquitoes and to gain a competitive advantage [22,28].

Aedes triseriatus
Aedes triseriatus (Fig. 3) is a species native to hardwood forests of Eastern and Central North America (Fig. 1) [29] and was detected in Europe once in 2004 in France. It is believed that it was introduced throughout the importation of used tires from the USA and promptly eliminated [30]. Aedes triseriatus is specifically a diurnal biter [21] and a zoophilic species, which can opportunistically bite humans [31••]. In the North American continent, this species is the key vector for the La Crosse virus [29,32], and it is a competent vector for several pathogens, including West Nile virus and dengue [31••, 33-36].
There is still no evidence that this species can successfully invade and colonize Europe; nevertheless, despite its preference for tree holes in rural and forest areas, it is able to easily breed in artificial containers in sub-urban areas [37]. Furthermore, Ae. triseriatus can produce diapausing overwintering eggs and the hatched larvae are even able to overwinter in semi-frozen aquatic habitats [29,37], suggesting that this species adapt to the colder climate of Northern Europe competing with the other invasive mosquito species Ae. japonicus japonicus [38].

Conclusions and Future Challenges
The dispersion, establishment, and colonization of new areas by alien mosquito species are well documented in Europe; however, the mechanisms employed by invasive mosquito species to invade and colonize urban and rural environments still need to be clarified. Furthermore, guidelines to prevent the invasion of new areas by populations of vector mosquito species are still largely neglected by institutions, in comparison to surveillance and monitoring campaigns [17]. Nevertheless, the common surveillance techniques used for invasive mosquito vector species concentrate on artificial container breeding species and in urban areas, where the risk of disease transmission is higher. Furthermore, by neglecting mosquito surveillance at important points of entry to allow the early detection of invasive species, the effort needed to eradicate the target invasive species upon detection in populous urban areas would be considerably higher [39]. On the other hand, the two above-described invasive mosquito species preferentially breed in rural and natural habitats, where the monitoring implies higher operational and labor costs. In this context, digital technologies and smart trap development can be useful to facilitate monitoring activity in marginal and remote environments [40,41]. Indeed, capillary surveillance programs in the rural areas would probably reveal differences in the relative abundance of invasive vector mosquitoes compared to urban areas. The marginality of those areas should not make underestimate their potentiality as reservoir and habitat for several noxious mosquito species, including preferential zoophilic species which can contribute to spillover events.
Aedes atropalpus and Ae. triseriatus are among the most important native North American mosquito vectors, transmitting several endemic pathogens, such as California encephalitis virus, La Crosse virus, Jamestown Canyon virus, Rift Valley fever virus, and St. Louis encephalitis virus [19 ••, 20, 29, 32, 34, 42]. However, the danger of these invasive species pose to Europe could be underestimated or set aside compared to other invasive mosquito vector species. Thus, further studies about the basic ecology and behavior of these species should be encouraged to unveil their potential to invade Europe and their importance as vectors to assess the current and future risks related to these invasive species [43].