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Invasive Aedes mosquitoes in an urban—peri-urban gradient in northern Spain: evidence of the wide distribution of Aedes japonicus

Parasites & Vectors volume 16, Article number: 234 (2023) Cite this article

Abstract

Background

The expansion of invasive mosquitoes throughout Europe has increased in recent decades. In northern Spain, Aedes albopictus was detected for the first time in 2014, and Aedes japonicus was detected in the three Basque provinces in 2020. This study aimed to evaluate the distribution of these mosquito species and their association with factors related to urbanization.

Methods

In 2021, a total of 568 ovitraps were deployed in 113 sampling sites from 45 municipalities with > 10,000 inhabitants. Oviposition substrate sticks were replaced each fortnight and examined for Aedes eggs from June to November. Aedes eggs were counted, and the eggs from a selection of positive oviposition sticks, encompassing at least one stick from each positive ovitrap, were hatched following their life cycle until the adult stage. When egg hatching was not successful, PCR targeting the COI gene and sequencing of amplicons were carried out.

Results

Eggs were detected in 66.4% of the sampling sites and in 32.4% of the ovitraps distributed in the three provinces of the Basque Country. Aedes albopictus and Ae. japonicus were widespread in the studied area, confirming their presence in 23 and 26 municipalities, respectively. Co-occurrence of both species was observed in 11 municipalities. The analysis of the presence of Aedes invasive mosquitoes and the degree of urbanization (urban, suburban, peri-urban) revealed that Ae. albopictus showed a 4.39 times higher probability of being found in suburban areas than in peri-urban areas, whereas Ae. japonicus had a higher probability of being found in peri-urban areas. Moreover, the presence of Ae. albopictus was significantly associated with municipalities with a higher population density (mean = 2983 inh/km2), whereas Ae. japonicus was associated with lower population density (mean = 1590 inh/km2).

Conclusions

The wide distribution of Ae. albopictus and Ae. japonicus observed confirmed the spread and establishment of these species in northern Spain. A new colonization area of Ae. japonicus in Europe was confirmed. Due to the potential impact of Aedes invasive mosquitoes on public health and according to our results, surveillance programs and control plans should be designed considering different urbanization gradients, types of environments, and population density.

Graphical Abstract

Background

Mosquitoes are of paramount significance in terms of animal and public health due to their role as vectors of several pathogens and because of the impact they have as biting and annoying insects. Globalization, human travel, and global trade have facilitated the spread of exotic invasive mosquitoes of the genus Aedes [1]. Additionally, climatic and environmental changes increase the possibility of the spread and establishment of some species in new regions. In Europe, six species of Aedes invasive mosquitoes (AIM) (Aedes albopictus, Aedes aegypti, Aedes japonicus, Aedes koreicus, Aedes atropalpus, and Aedes triseriatus) have been introduced since the 1970s [2], and some have known established populations [3, 4]. Among them, only two species are present in Spain [2].

Aedes albopictus (Skuse, 1894) is an exotic invasive species that was introduced into Albania during the late 1970s and later in Italy in 1990 [5, 6] and is currently widely distributed in Europe. Its ability to adapt to cold temperatures and overwinter in temperate regions and its plasticity to adapt to different habitats, together with globalization and climate change, contribute to the successful invasion of this multivoltine species [7]. Urban emplacements provide suitable habitats and resources for Ae. albopictus development, allowing them to colonize and proliferate; it is considered a container-breeding mosquito, and its ability to occupy habitats in urban environments is noticeable. This species represents a public health concern since it can act as a vector of some arboviruses, most notably dengue, chikungunya, and Zika [7]. In fact, several autochthonous outbreaks have been recently reported in Europe, thus confirming local transmission of these diseases in places where Ae. albopictus has been established [8,9,10,11,12]. The epidemiology of vector-borne pathogen transmission is driven by the interaction among vector, host, and pathogen and is profoundly affected by urbanization processes. As urbanization processes increase globally, many countries are experiencing the re-emergence and introduction of vector-borne diseases [13]. In addition, the aggressive biting behavior of Ae. albopictus jeopardizes the quality of life of local citizens and can even have a direct impact on the regional economy. In Spain, after the first detection of Ae. albopictus in Catalonia in 2004, the Spanish Ministry of Health launched a surveillance campaign in 2007 in several Mediterranean Spanish regions [14]. In northern Spain, Ae. albopictus was identified for the first time in 2014 in the Basque Country, on the border with France, and since then, it has been expanding toward new areas [15].

Aedes japonicus (Theobald, 1901) was first detected in 2000 in France in a storage yard of imported tires [16]. Since then, this species has been reported mostly in central Europe [17, 18]. Aedes japonicus is well adapted to temperate climates and is capable of withstanding cold and snowy winters. It is a multivoltine species, and larval hatching occurs early in the year as soon as breeding sites lose their ice cover at water temperatures of 4.0–4.5 °C [17]. This species has an adaptive capacity, and they have been observed to displace other indigenous mosquito species [19]. The activity period of adult mosquitoes can last until early December. In contrast to Ae. albopictus, this species prefers forested and bushy areas, and larvae can be found in tree holes, tree stumps, rainwater pools [17], and other natural or artificial containers. Aedes japonicus is a potential vector of several viruses of medical and veterinary importance, such as chikungunya, dengue, Zika, and West Nile [20]. This species is not considered a primary nuisance species to humans [21], but it is of particular concern because of its ability to rapidly adapt to new habitats given its high tolerance to a broad range of climate conditions [19, 22]. Aedes japonicus was detected in northern Spain (Asturias) in 2018 through the citizen science platform Mosquito Alert [23] and 2 years later was identified in two close regions (Cantabria and the Basque Country) [2, 24], suggesting a new colonization area in Europe.

Urbanization processes have a major impact on mosquito communities by decreasing species richness and increasing the abundance of selected mosquito species such as Ae. albopictus, which are very well adapted to urban and suburban ecosystems [13, 25]. Until now, during the surveillance program carried out in the Basque Country, the selection of sampling areas was focused on places with heavy road traffic (such as car parks, petrol stations, or logistics platforms, among others) to increase the probability of detecting Ae. albopictus [15]. However, recent findings [2, 24] lead us to think that Ae. japonicus could also be established in this area. Thus, considering that Ae. japonicus inhabits areas with abundant vegetation, being more abundant in rural settings [25], this study focuses on (i) evaluating the association of the presence of AIM with factors related to the type of environment, urbanization degree and population density and (ii) investigating the range of distribution of Ae. japonicus in the Basque country.

Methods

Study area

The Basque Country is a small region in northern Spain with ca. 7200 km2 divided into three administrative provinces: Gipuzkoa, Bizkaia, and Araba. The average annual temperature and rainfall are 13.4 °C and 1610 mm in Gipuzkoa, 13.8 °C and 1278 mm in Bizkaia, and 11.5 °C and 878 mm in Araba. The population of the Basque Country is ca. 2,188,017 inhabitants, and industry and tourism are some of the driving forces of the Basque economy [26]. There is a network of highly trafficked motorways structured around the main routes that connect the Basque Country with France, central Spain, and the Mediterranean coast, facilitating the introduction of AIM to new areas by passive transportation.

Sampling approach

The sampling strategy to monitor AIM presence in 2021 encompassed the placement of ovitraps in 45 municipalities, most of them with > 10,000 inhabitants. Two sampling zones were selected in each municipality, with the exception of the three main cities (Bilbao, Donostia/San Sebastian, and Vitoria-Gasteiz), where the number of selected zones increased to 8, 17, and 4, respectively. A total of 113 sampling areas were selected.

Fieldwork was carried out by a network of health officers from the Public Health Directorate of the Basque Government and from the municipalities of Bilbao, Donostia/San Sebastian, Vitoria-Gasteiz, and Laguardia. Sampling started on June 1 and finished on November 18. Thus, each municipality and area was sampled from 11 to 12 times over a period of 23 weeks (June–November).

Sampling methodology

The presence of Aedes spp. eggs was investigated using oviposition traps (ovitraps) [27]. A total of 568 ovitraps were deployed (Gipuzkoa: 275 ovitraps, 19 municipalities, 55 sampling areas; Bizkaia: 235 ovitraps, 22 municipalities, 47 sampling areas; Araba: 58 ovitraps, 4 municipalities, 11 sampling areas) (Table 1). Five ovitraps were placed in each sampling area, always in shady places and hidden in the vegetation. Each ovitrap contained dechlorinated water and a wooden stick (masonite; 12 cm long and 2.5 cm width) as oviposition substrate. Oviposition sticks were removed and replaced by new sticks every 15 days.

Table 1 Number of municipalities, sampling areas, ovitraps, and oviposition sticks examined in the three Basque provinces and prevalence of eggs of Aedes spp.
Full size table

Information on each sampling area was compiled, including geographic coordinates and type of environment (parking, green park, petrol station, city center, industrial zone). Sampling sites were also categorized according to the urbanization degree: urban, suburban, and peri-urban areas. Based on Loibl et al. [28] and adjusted to the socio-geographical reality of the region, the sampling areas were categorized as follows: Urban areas were those in the town center, including urban core and inner urban areas; suburban areas were mainly residential, not densely compacted, and located near an inner urban area; peri-urban areas were spaces located on the boundaries of the town with scarce urban development, and including both urban-fringe and urban periphery.

Laboratorial methods

Oviposition sticks were examined in the laboratory under a stereomicroscope (zoom magnification range of 7.5–135 ×). If eggs were observed, they were counted, and positive sticks were preserved for egg hatching by immersion in a petri dish with dechlorinated water. Emerged larvae were placed in mosquito breeders (Bioquip®, Compton, CA, USA) at room temperature (ca. 23 °C) until becoming adult mosquitoes. The identification of Aedes mosquitoes was performed using taxonomic keys [29]. In the case of unsuccessful egg hatching, 5–10 eggs were collected from selected sticks, and DNA extraction was performed using a commercial kit (NZY Tissue gDNA isolation kit, NZYtech, Lisboa, Portugal), followed by PCR targeting the cytochrome c oxidase I subunit (COI) gene [30]. Amplicons were sequenced by external services using the Sanger technique. Sequences were compared with those available in GenBank by BLAST analysis to confirm the species. A selection of sequences is deposited in GenBank with the reference numbers OQ884140-OQ884148.

Statistical analyses

The positive ovitrap index (POI) [(number of positive traps/number of inspected traps) × 100] was estimated for each sampling area [31]. A sampling area was considered positive when the presence of Aedes spp. eggs was detected in at least one oviposition trap in at least one sampling. To represent the overall egg-laying kinetics of AIMs over the sampling period (week 24–week 46), the means of eggs counted each fortnight were calculated and represented in a graph with a smoothed trend line based on LOESS (locally estimated scatterplot smoothing). Associations between the presence of Ae. albopictus and Ae. japonicus (as a dependent binomial variable) with province, urbanization (urban/suburban/peri-urban) and type of environment (town, petrol station, parking, green parks and industrial areas) were analyzed using logistic regression models (GLM), and odds ratios (OR) were calculated using the ORci function of the CIplot package. Censuses from each municipality included in the study were compiled. Thus, the presence of each species according to the human population density of the municipality (inh/km2) was evaluated by the Wilcoxon rank-sum test. All statistical analyses were performed using R statistical software version 3.6.1 [32].

Results

Distribution of invasive mosquitoes

A total of 5896 oviposition sticks were examined in 2021 (2853 from Gipuzkoa, 2484 from Bizkaia; 559 from Araba). Eggs of Aedes spp. were detected in 66.4% of the sampling sites, and 32.4% of the ovitraps were distributed in the three territories of the Basque Country (Table 1). In 18 sampling sites from 13 municipalities, only one positive ovitrap and one oviposition stick were positive throughout the surveillance period. In contrast, in 10 sampling sites from 6 municipalities, the five ovitraps harbored Aedes eggs during more than 8 samplings. The province of Gipuzkoa showed a higher percentage of positive ovitraps (42.5%) than Bizkaia (27.7%) and Araba (3.4%). Likewise, the percentage of oviposition sticks with eggs was higher in Gipuzkoa (12.2% vs. 5.0% in Bizkaia and 0.4% in Araba) (Table 1).

Notably, 100% of the municipalities in Gipuzkoa were positive for the presence of Aedes spp., while in Araba, Aedes eggs were detected only in one of the four municipalities investigated (Table 2).

Table 2 Municipalities included in the surveillance programme and the number of them harboring AIM, Aedes albopictus, Ae. japonicus, or both species simultaneously
Full size table

The establishment of Aedes spp. according to POI was confirmed in several municipalities (Fig. 1a). The most intense red color indicates that between 75 and 100% of the ovitraps of the municipality were positive for the presence of Aedes eggs.

Fig. 1
figure 1

Distribution of Aedes spp. eggs in each sampling site according to the POI (Positive Ovitrap Index), represented in a gradient of color (A). Distribution of Aedes albopictus (red dots), Ae. japonicus (green dots), and coexistence of both species (yellow dots) (B)

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Identification of Aedes spp.

To identify the species of Aedes in each sampling site, a total of 195 oviposition sticks with eggs were submitted to molting to obtain adult mosquitoes that were identified by morphological keys, as described above. When adult emergence failed, PCRs of the eggs and sequencing were carried out. The species of Aedes was identified in 40.2% of the positive oviposition sticks (191/475, 69 from Bizkaia, 120 from Gipuzkoa, 2 from Araba), confirming the presence of Ae. albopictus in 44 sampling areas from 23 municipalities, and Ae. japonicus in 39 sampling areas from 26 municipalities (Table 2; Fig. 1b).

Aedes albopictus was concentrated around large urban centers such as Bilbao and Donostia/San Sebastian, where the population density is higher and industrialized areas are abundant in the surrounding areas. Aedes japonicus predominated in less populated areas (Fig. 1b). Concurrence of both species was observed in 11 municipalities (Table 2). Both Ae. japonicus and Ae. albopictus were simultaneously present on the same oviposition stick on just one occasion. Eggs from Aedes geniculatus (Olivier, 1971) were identified by molecular methods in only one oviposition stick. No other Aedes species were identified by morphological or molecular methods.

Oviposition activity of Aedes spp.

Aedes egg-laying activity progressively increased throughout the sampling period, with a maximum between September and November. Aedes egg laying was significantly higher in the province of Gipuzkoa than in Bizkaia and Araba (Kruskal-Wallis χ2 = 230.02, P < 0.0001) (Fig. 2a). Considering the 12 municipalities where only Ae. albopictus was identified, egg laying peaked between September and October (Fig. 2b). Similarly, considering the 15 municipalities with the only detection of Ae. japonicus, egg-laying activity showed a more stable pattern throughout the study period, with an earlier peak in July (Fig. 2c).

Fig. 2
figure 2

Mean Aedes spp. egg laying in the three Basque provinces (A). Aedes albopictus (B) and Ae. japonicus egg laying (C) considering only the municipalities where each species was exclusively found (12 and 15, respectively)

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Distribution of AIM by urbanization degree and characteristics of the environment

The probability of Ae. albopictus occurrence was higher in Bizkaia (OR = 14.62) and Gipuzkoa (OR = 18.36) than in Araba, while that for Ae. japonicus was significantly high in Gipuzkoa (OR = 11.40) (Table 3). Interestingly, the presence of Ae. albopictus was associated with municipalities with a higher population density (mean = 2983 inh/km2) (P < 0.001), and the presence of Ae. japonicus was associated with lower population density (mean = 1590 inh/km2) (P < 0.05) (Fig. 3).

Table 3 Summary of logistic regression models for Aedes albopictus and Ae. japonicus regarding province, urbanization degree, and type of environment
Full size table
Fig. 3
figure 3

Presence of each species according to the population density (inh/km2) (A); occurrence probability of Aedes albopictus and Ae. japonicus according to the urbanization gradient (B)

Full size image

The analysis between the presence of AIM and the degree of urbanization (urban, suburban, peri-urban) revealed that, whereas Ae. albopictus showed a 4.39 times higher probability of being found in suburban areas (P = 0.001) than in peri-urban areas, Ae. japonicus had a higher probability of being found in peri-urban areas than in suburban or urban areas (P = 0.001) (Table 3; Fig. 3).

Considering the characteristics of the environment, the distribution of both species relied on the type of site. Thus, the probability of finding Ae. albopictus was significantly higher in areas surrounding parking lots (P < 0.05), while the probability of finding Ae. japonicus was higher in areas surrounding petrol stations and industrial areas (P < 0.05) (Table 3).

Discussion

Mosquitoes are of public health relevance when they populate in high densities, which causes a nuisance, or when they transmit pathogens. The successful establishment of invasive mosquito populations in new environments is a complex process influenced by several factors, including climate, habitat, and human activity [1]. Six invasive species have been established in Europe [2, 7], and among them, Ae. albopictus and Ae. japonicus are becoming widespread [7, 18]. The wide distribution observed in the Basque Country (northern Spain) confirms the spread and establishment of these species of invasive mosquitoes in the region. Our results demonstrate that Ae. albopictus predominated around the two main cities (Bilbao and San Sebastián) that harbor a larger population per km2 and more traffic and important industrial ring roads, which favor the introduction and distribution of this species [33, 34]. The province of Gipuzkoa was the probable point of entry of Ae. albopictus in the Basque Country [15], and since then, significantly higher activity has been detected in this province, as shown in the current study. Until recently, the AIM surveillance program in this region was focused on placing ovitraps in areas with high concentrations of traffic, which favored the detection of Ae. albopictus [15]. In 2020, the surveillance was extended to municipalities that were less populated and less industrialized, enabling the detection of Ae. japonicus in four municipalities [2]. Furthermore, the sampling strategy carried out in the present study (2021), which encompassed urban, suburban, and peri-urban areas, showed a wide distribution of Ae. japonicus in the studied region. It is difficult to know how long this species has been part of the entomofauna of the Basque Country and the possible route of entry. However, in the 2 years since its first detection [24], established populations of Ae. japonicus have been detected in a higher number of municipalities than Ae. albopictus.

In contrast to Ae. albopictus, which is distributed by passive dispersal through motorized vehicles, Ae. japonicus seems to be distributed over time by active dispersal [35], with an estimation of spreading more than 100 km within a few years [19, 22]. Thus, in countries such as Hungary or Italy, Ae. japonicus spread rapidly in a short period by appropriate ecological corridors, finding natural and artificial containers to breed [22, 36]. Considering that in our study the occurrence probability of Ae. japonicus is greater in Gipuzkoa (province bordering France), it could be speculated that this species may have come from France. However, Ae. japonicus seem to be established only in northeastern France [3], and there are no reports in southern France bordering our study area. It is important to highlight that, as this study demonstrates, if AIM surveillance is focused only on urban areas, the presence and distribution of Ae. japonicus may be underestimated.

Climatic and demographic variables, such as temperature, precipitation, and population density, are key factors in mosquito distribution [37]. In this study, a widespread presence of both species was observed in northern regions with a mesothermal Atlantic climate (moderate temperatures and extensive rainfall); however, no specimens were detected in the southern area with a transitional climate toward the Mediterranean (drier and warmer summers). Aedes albopictus has strong ecological plasticity, can be established in a wide range of different habitats with different climatic conditions, and is better adapted to warmer climates than Ae. japonicus [7]. These could be the reasons for the establishment of Ae. japonicus in regions of Spain with temperate Atlantic climates, such as northern Spain [24]. In addition, larvae of Ae. japonicus do not tolerate water temperatures > 30 °C [38], which occur during the summer in central and southern Spain.

In northern Italy, which enjoys colder winters and snow and relatively warm summers, the seasonal activity period of Ae. japonicus lasts at least 7 months between April and November [22]. However, in the study area, with milder winters, larvae were found in February and March in human-made containers around farmhouses in the provinces of Bizkaia and Gipuzkoa (unpublished data). This study also indicates that egg laying starts earlier for Ae. japonicus than Ae. albopictus. In fact, the predictions of species distribution according to the habitat suitability under climate change are different for both AIM species; whereas Ae. albopictus is promoted by climate change, the area modeled to be climatically suitable for Ae. japonicus is projected to decrease in Europe [39] as it would not be able to adapt to warmer climatic conditions.

In addition, landscape structure is key to facilitating the occurrence of Ae. japonicus, even in a climatically unsuitable region, and vice versa [40]. In general, the presence of Ae. japonicus is more prevalent in vegetation-rich [17, 41] and rural areas compared to urban and suburban areas [25] or in the transition zones between forest and settlements [42]. This study also showed a higher probability of finding Ae. japonicus in petrol stations and industrial areas. Both locations are usually surrounded by shrubs and vegetation-rich areas. Moreover, these areas offer optimal resting places for mosquitos in addition to a wide variety of artificial breeding containers. In contrast, the probability of finding Ae. albopictus has been higher in parking lots, which may be due to the role of terrestrial vehicles enabling the passive dispersion of this species [43, 44].

Urbanization processes modify the environment, have a major impact on the mosquito species community, and lead to biodiversity loss caused by anthropogenic changes [45]. The more urbanized a given area is, the fewer species are found, but mosquito species adapted to urban environments increase in abundance [46]. This is especially applicable to container-breeding and invasive mosquitoes [47, 48]. In the current study, the presence of Ae. albopictus and Ae. japonicus varied depending on the degree of urbanization. Thus, Ae. albopictus appeared concentrated in urban and suburban areas, probably because of the higher availability and density of artificial breeding sites, its tolerance to hotter and drier climate conditions, and the presence of a wider blood-feeding host range, including humans [49, 50]. In fact, this mosquito species is considered strongly anthropophilic, and in urban areas where the human population is greater, a higher blood-feeding rate has been observed [51]. In this study, Ae. albopictus showed a higher presence in municipalities with higher population densities. In contrast, Ae. japonicus showed a preference for municipalities with lower population density, such as peri-urban environments and rural settings [50]. Urban areas are occasionally colonized by Ae. japonicus, but hotter and drier summer conditions caused by the effect known as ‘urban heat island” [52] would negatively impact its life cycle. In addition, a higher variety of available mammal hosts to feed on could be the reason that they prefer peri-urban and rural settings [50]. Although the two species seem to coexist without much evidence of displacement, the potential competitive interaction between the larval stages of the two species should not be ignored and should be further investigated.

Conclusions

This study confirms a new colonization area in Europe for Ae. japonicus. Even though Ae. japonicus is not considered a high-risk mosquito for public health, it is unknown whether the role of the species could change if its distribution and abundance increase. In addition, Ae. albopictus is expected to be fully established in the coming years, causing nuisance [15] and increasing the likelihood of autochthonous arbovirus transmission. The present results may have practical applications for the design of AIM surveillance. Due to the potential impact on public health and according to our findings, surveillance programs should be designed considering different types of environments, including municipalities with low population density and peri-urban areas. Mosquito surveillance and control activities will continue in the study area to keep population density at minimum. Special attention will be paid on the characterization of the Aedes breeding sites to better understand the distribution pattern of these two species of invasive mosquitoes.

Availability of data and materials

All data generated and analysed during this study are included in this published article.

References

  1. Medlock JM, Hansford KM, Schaffner F, Versteirt V, Hendrickx G, Zeller H, et al. A review of the invasive mosquitoes in Europe: ecology, public health risks, and control options. Vector Borne Zoonotic Dis. 2012;12:435–47.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Miranda MA, Barcelo C, Arnoldi D, Augsten X, Bakran-Lebl K, Balatsos G, et al. AIMSurv: first pan-European harmonized surveillance of Aedes invasive mosquito species of relevance for human vector-borne diseases. GigaByte. 2022;2022:1–13.

    Article  Google Scholar 

  3. European Centre for Disease Prevention and Control. Distribution maps of invasive mosquitoes. 2023. https://www.ecdc.europa.eu/en/disease-vectors/surveillance-and-disease-data/mosquito-maps. Accessed: 12 Jun 2023.

  4. Medlock JM, Hansford KM, Versteirt V, Cull B, Kampen H, Fontenille D, et al. An entomological review of invasive mosquitoes in Europe. Bull Entomol Res. 2015;105:637–63.

    Article  CAS  PubMed  Google Scholar 

  5. Adhami J, Reiter P. Introduction and establishment of Aedes (Stegomyia) albopictus skuse (Diptera: Culicidae) in Albania. J Am Mosq Control Assoc. 1998;14:340–3.

    CAS  PubMed  Google Scholar 

  6. Dalla PG, Majori G. First record of Aedes albopictus establishment in Italy. J Am Mosq Control Assoc. 1992;8:318–20.

    Google Scholar 

  7. Giunti G, Becker N, Benelli G. Invasive mosquito vectors in Europe: from bioecology to surveillance and management. Acta Trop. 2023;239:106832.

    Article  PubMed  Google Scholar 

  8. Cochet A, Calba C, Jourdain F, Grard G, Durand GA, Guinard A, et al. Autochthonous dengue in mainland France, 2022: geographical extension and incidence increase. Euro Surveill. 2022;2022:27.

    Google Scholar 

  9. Delisle E, Rousseau C, Broche B, Leparc-Goffart I, L’Ambert G, Cochet A, et al. Chikungunya outbreak in Montpellier, France, September to October 2014. Euro Surveill. 2015;2015:20.

    Google Scholar 

  10. Lazzarini L, Barzon L, Foglia F, Manfrin V, Pacenti M, Pavan G, et al. First autochthonous dengue outbreak in Italy, August 2020. Euro Surveill. 2020;2020:25.

    Google Scholar 

  11. Monge S, Garcia-Ortuzar V, Lopez HB, Lopaz Perez MA, Delacour-Estrella S, Sanchez-Seco MP, et al. Characterization of the first autochthonous dengue outbreak in Spain (August–September 2018). Acta Trop. 2020;205:105402.

    Article  PubMed  Google Scholar 

  12. Riccardo F, Venturi G, Di LM, Del MM, Severini F, Andrianou X, et al. Secondary autochthonous outbreak of chikungunya, Southern Italy, 2017. Emerg Infect Dis. 2019;25:2093–5.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Wilke ABB, Benelli G, Beier JC. Anthropogenic changes and associated impacts on vector-borne diseases. Trends Parasitol. 2021;37:1027–30.

    Article  CAS  PubMed  Google Scholar 

  14. Collantes F, Delacour S, Alarcon-Elbal PM, Ruiz-Arrondo I, Delgado JA, Torrell-Sorio A, et al. Review of ten-years presence of Aedes albopictus in Spain 2004–2014: known distribution and public health concerns. Parasit Vectors. 2015;8:655.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Goiri F, González MA, Goikolea J, Oribe M, Castro V, Delacour S, et al. Progressive invasion of Aedes albopictus in Northern Spain in the period 2013–2018 and a possible association with the increase in insect bites. Int J Environ Res Public Health. 2020;17:1678.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Schaffner F, Chouin S, Guilloteau J. First record of Ochlerotatus (Finlaya) japonicus japonicus (Theobald, 1901) in metropolitan France. J Am Mosq Control Assoc. 2003;19:1–5.

    PubMed  Google Scholar 

  17. Kampen H, Werner D. Out of the bush: the Asian bush mosquito Aedes japonicus japonicus (Theobald, 1901) (Diptera, Culicidae) becomes invasive. Parasit Vectors. 2014;7:59.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Koban MB, Kampen H, Scheuch DE, Frueh L, Kuhlisch C, Janssen N, et al. 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. 2019;12:109.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Kaufman MG, Fonseca DM. Invasion biology of Aedes japonicus japonicus (Diptera: Culicidae). Annu Rev Entomol. 2014;59:31–49.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Martinet JP, Ferte H, Failloux AB, Schaffner F, Depaquit J. Mosquitoes of North-Western Europe as potential vectors of arboviruses: a review. Viruses. 2019;2019:11.

    Google Scholar 

  21. Cebrian-Camison S, Martinez-de la Puente J, Figuerola J. A literature review of host feeding patterns of invasive Aedes mosquitoes in Europe. Insects. 2020;2020:11.

    Google Scholar 

  22. Montarsi F, Martini S, Michelutti A, Da RG, Mazzucato M, Qualizza D, et al. The invasive mosquito Aedes japonicus japonicus is spreading in northeastern Italy. Parasit Vectors. 2019;12:120.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Eritja R, Ruiz-Arrondo I, Delacour-Estrella S, Schaffner F, Alvarez-Chachero J, Bengoa M, et al. First detection of Aedes japonicus in Spain: an unexpected finding triggered by citizen science. Parasit Vectors. 2019;12:53.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Eritja R, Delacour-Estrella S, Ruiz-Arrondo I, González MA, Barceló C, García-Pérez AL, et al. At the tip of an iceberg: citizen science and active surveillance collaborating to broaden the known distribution of Aedes japonicus in Spain. Parasit Vectors. 2021;14:375.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Bartlett-Healy K, Unlu I, Obenauer P, Hughes T, Healy S, Crepeau T, et al. Larval mosquito habitat utilization and community dynamics of Aedes albopictus and Aedes japonicus (Diptera: Culicidae). J Med Entomol. 2012;49:813–24.

    Article  PubMed  Google Scholar 

  26. EUSTAT—Instituto Vasco de Estadística. Economy. 2020. https://en.eustat.eus/estadisticas/tema_351/opt_0/temas.html. Accessed: 13 Jun 2023.

  27. European Centre for Disease Prevention and Control. Guidelines for the surveillance of invasive mosquitoes in Europe. Stockholm, Sweden: ECDC; 2012.

  28. Loibl W, Ravetz J, Tosics I. Concepts and methods. In: Piorr A, Ravetz J, Tosics I, editors. Peri-Urbanisation in Europe. Copenhagen: University of Copenhagen/Academic Books Life Sciences; 2011. p. 24–9.

    Google Scholar 

  29. Becker N, Petric D, Zgomba M, Boase C, Dahl C, Madon MB, et al. Mosquitoes, identification, ecology and control. Berlin: Springer; 2020.

    Book  Google Scholar 

  30. Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P. Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann Entomol Soc Am. 1994;87:651–701.

    Article  CAS  Google Scholar 

  31. Nascimento KLC, da Silva JFM, Zequi JAC, Lopes J. Comparison between larval survey index and positive ovitrap index in the evaluation of populations of Aedes (Stegomyia) aegypti (Linnaeus, 1762) North of Parana. Brazil Environ Health Insights. 2020;14:1178630219886570.

    PubMed  Google Scholar 

  32. R Core Team. A language and environment for statistical computing. R Foundation for Statistical Computing. 2019. https://www.r-project.org/. Accessed: 27 Mar 2023.

  33. Lucientes-Curdi J, Molina-Moreno R, Amela-Heras C, Simon-Soria F, Santos-Sanz S, Sánchez-Gómez A, et al. Dispersion of Aedes albopictus in the Spanish Mediterranean area. Eur J Public Health. 2014;24:637–40.

    Article  PubMed  Google Scholar 

  34. Swan T, Russell TL, Staunton KM, Field MA, Ritchie SA, Burkot TR. A literature review of dispersal pathways of Aedes albopictus across different spatial scales: implications for vector surveillance. Parasit Vectors. 2022;15:303.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Müller P, Engeler L, Vavassori L, Suter T, Guidi V, Gschwind M, et al. Surveillance of invasive Aedes mosquitoes along Swiss traffic axes reveals different dispersal modes for Aedes albopictus and Ae. japonicus. PLoS Negl Trop Dis. 2020;14:e0008705.

    Article  PubMed  PubMed Central  Google Scholar 

  36. 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. 2020;119:403–10.

    Article  PubMed  Google Scholar 

  37. Brugueras S, Fernández-Martínez B, Martínez-de la Puente J, Figuerola J, Porro TM, Rius C, et al. Environmental drivers, climate change and emergent diseases transmitted by mosquitoes and their vectors in southern Europe: a systematic review. Environ Res. 2020;191:11038.

    Article  Google Scholar 

  38. Andreadis TG, Wolfe RJ. Evidence for reduction of native mosquitoes with increased expansion of invasive Ochlerotatus japonicus japonicus (Diptera: Culicidae) in the northeastern United States. J Med Entomol. 2010;47:43–52.

    Article  PubMed  Google Scholar 

  39. Cunze S, Koch LK, Kochmann J, Klimpel S. Aedes albopictus and Aedes japonicas—two invasive mosquito species with different temperature niches in Europe. Parasit Vectors. 2016;9:573.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Kerkow A, Wieland R, Fruh L, Holker F, Jeschke JM, Werner D, et al. Can data from native mosquitoes support determining invasive species habitats? Modelling the climatic niche of Aedes japonicus japonicus (Diptera, Culicidae) in Germany. Parasitol Res. 2020;119:31–42.

    Article  PubMed  Google Scholar 

  41. Chaves LF, Friberg MD, Moji K. Synchrony of globally invasive Aedes spp. immature mosquitoes along an urban altitudinal gradient in their native range. Sci Total Environ. 2020;734:139365.

    Article  CAS  PubMed  Google Scholar 

  42. Früh L, Kampen H, Koban MB, Pernat N, Schaub GA, Werner D. Oviposition of Aedes japonicus japonicus (Diptera: Culicidae) and associated native species in relation to season, temperature and land use in western Germany. Parasit Vectors. 2020;13:623.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Eritja R, Palmer JRB, Roiz D, Sanpera-Calbet I, Bartumeus F. Direct evidence of adult Aedes albopictus dispersal by car. Sci Rep. 2017;7:14399.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Ibañez-Justicia A. Pathways for introduction and dispersal of invasive Aedes mosquito species in Europe: a review. J Eur Mosq Control Assoc. 2020;38:1–10.

    Google Scholar 

  45. Ferraguti M, Martinez-de la Puente J, Roiz D, Ruiz S, Soriguer R, Figuerola J. Effects of landscape anthropization on mosquito community composition and abundance. Sci Rep. 2016;6:29002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Wilke ABB, Vasquez C, Carvajal A, Moreno M, Fuller DO, Cardenas G, et al. Urbanization favors the proliferation of Aedes aegypti and Culex quinquefasciatus in urban areas of Miami-Dade County. Florida Sci Rep. 2021;11:22989.

    Article  CAS  PubMed  Google Scholar 

  47. Wilke ABB, Chase C, Vasquez C, Carvajal A, Medina J, Petrie WD, et al. Urbanization creates diverse aquatic habitats for immature mosquitoes in urban areas. Sci Rep. 2019;9:15335.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Wilke ABB, Vasquez C, Carvajal A, Medina J, Chase C, Cardenas G, et al. Proliferation of Aedes aegypti in urban environments mediated by the availability of key aquatic habitats. Sci Rep. 2020;10:12925.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Li Y, Kamara F, Zhou G, Puthiyakunnon S, Li C, Liu Y, et al. Urbanization increases Aedes albopictus larval habitats and accelerates mosquito development and survivorship. PLoS Negl Trop Dis. 2014;8:e3301.

    Article  PubMed  PubMed Central  Google Scholar 

  50. Mogi M, Armbruster PA, Tuno N. Differences in responses to urbanization between invasive mosquitoes, Aedes japonicus japonicus (Diptera: Culicidae) and Aedes albopictus, in their native range, Japan. J Med Entomol. 2020;57:104–12.

    Article  PubMed  Google Scholar 

  51. Valerio L, Marini F, Bongiorno G, Facchinelli L, Pombi M, Caputo B, et al. Host-feeding patterns of Aedes albopictus (Diptera: Culicidae) in urban and rural contexts within Rome province, Italy. Vector Borne Zoonotic Dis. 2010;10:291–4.

    Article  PubMed  Google Scholar 

  52. LaDeau SL, Allan BF, Leisnham PT, Levy MZ. The ecological foundations of transmission potential and vector-borne disease in urban landscapes. Func Ecol. 2015;29:889–901.

    Article  Google Scholar 

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Acknowledgements

We thank the participation of the staff of the Department of Public Health of the Basque Government in the field samplings.

Funding

This work was funded by the Department of Economic Development and Infrastructures of the Basque Government, the Ministry of Health, Social Policy, and Equality of the Government of Spain and the project EU-LIFE 18 IPC/ES/000001 (Urban Klima 2050). Aitor Cevidanes was supported by a ‘Ramón y Cajal’ post-doctoral grant RYC2021-033084-I funded by MCIN/AEI/https://doi.org/10.13039/501100011033 and by European Union NextGenerationEU/PRTR; Fatima Goiri was supported by a PhD award from the Department of Economic Development and Infrastructures of the Basque Government (FPI-2019).

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Authors and Affiliations

  1. Animal Health Department, NEIKER-Basque Institute for Agricultural Research and Development, Basque Research and Technology Alliance (BRTA), Derio, Bizkaia, Spain

    Aitor Cevidanes, Fátima Goiri, Jesús F. Barandika, Patricia Vázquez & Ana L. García-Pérez

  2. Subdirección de Salud Pública de Gipuzkoa, Eusko Jaurlaritza-Gobierno Vasco, Donostia, Gipuzkoa, Spain

    Joseba Goikolea

  3. Dirección de Sanidad Ambiental e Higiene Urbana, Área de Salud y Consumo del Ayuntamiento de Bilbao, Bilbao, Bizkaia, Spain

    Ander Zuazo

  4. Dirección de Medio Ambiente, Sección de Sanidad Alimentaria y Zoonosis del Ayuntamiento de Donostia, Donostia, Gipuzkoa, Spain

    Natalia Etxarri

  5. Departamento de Deporte y Salud, Servicio de Salud Pública, Unidad Sanitaria de Consumo del Ayuntamiento de Vitoria-Gasteiz, Vitoria-Gasteiz, Araba, Spain

    Gurutze Ocio

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  1. Aitor Cevidanes
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  9. Ana L. García-Pérez
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Contributions

Conceptualization, AC, JBA and ALGP; Methodology PV, FG, AC, JFB, AZ, JG, GO, NE, ALGP; Formal Analysis, AC; Investigation, PV, AC, FG, JFB, ALGP; Data Curation, AC, ALGP; Writing—Original Draft Preparation, AC, ALGP; Writing—Review and editing, AC, FG, JBA, ALGP; Supervision, AZ, JG, GO, NE, ALGP; Funding Acquisition, AZ, JG, GO, NE, ALGP.

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Correspondence to Ana L. García-Pérez.

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Cevidanes, A., Goiri, F., Barandika, J.F. et al. Invasive Aedes mosquitoes in an urban—peri-urban gradient in northern Spain: evidence of the wide distribution of Aedes japonicus. Parasites Vectors 16, 234 (2023). https://doi.org/10.1186/s13071-023-05862-6

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Parasites & Vectors

ISSN: 1756-3305

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