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Aedes Albopictus: a Mark‑Release‑Recapture Study Using Self‑Marking Units Laura Vavassori1,2*, Adam Saddler1,2,3 and Pie Müller1,2

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Aedes Albopictus: a Mark‑Release‑Recapture Study Using Self‑Marking Units Laura Vavassori1,2*, Adam Saddler1,2,3 and Pie Müller1,2 Vavassori et al. Parasites Vectors (2019) 12:583 https://doi.org/10.1186/s13071-019-3837-5 Parasites & Vectors RESEARCH Open Access Active dispersal of Aedes albopictus: a mark-release-recapture study using self-marking units Laura Vavassori1,2*, Adam Saddler1,2,3 and Pie Müller1,2 Abstract Background: Understanding the dispersal dynamics of invasive mosquito species is fundamental to improve vector surveillance and to target control eforts. Aedes albopictus has been deemed a poor fyer as its range of active dispersal is generally assumed to be limited to a few hundred metres, while laboratory studies suggest this mosquito could actually fy several kilometres. The discrepancy may be due to diferences in the local environment or to the methodo- logical approach. In Switzerland, Ae. albopictus has been present since 2003 and has since then expanded its range. While passive dispersal is a key driver, it remains unclear how far this mosquito spreads through active fight and what the age structure and size of the local population are, all important parameters for vector surveillance and control. Method: We investigated the active dispersal, daily survival rate and population size of Ae. albopictus in mark-release- recapture studies in Coldrerio and Lugano, two areas of intensive control in Switzerland. To mark mosquitoes emerg- ing from breeding sites, we used self-marking units with fuorescent pigment that have minimal impact on mosquito survival and behaviour. We recaptured the adult mosquitoes with BG-Sentinel traps within a radius of 1 km from the marking units over 22 consecutive days. Results: We found that 77.5% of the recaptured Ae. albopictus individuals few further than 250 m, the limit that is usually deemed sufcient for vector containment. The average age of females and males was 8.6 days and 7.8 days in Coldrerio and Lugano, respectively, while the estimated mosquito population densities were 134 mosquitoes/ha in Coldrerio and 767 mosquitoes/ha in Lugano. Conclusions: Self-marking units are an efective tool to mark wild mosquitoes. Using this approach, we found that mos- quitoes survive long enough to potentially transmit arboviral disease in our study area and that host-seeking Ae. albopictus females may travel further than previously assumed for European mosquito populations. This fnding has direct implications for vector control as emergency treatments around positive cases, as well as surveillance and control around detections of new infestations, might need to be extended beyond the usual recommended range of just a few hundred metres. Keywords: Population dynamics, Invasive mosquitoes, Flight range, Mosquito survival Background Ae. albopictus is a vector of several pathogens, including Te Asian tiger mosquito, Aedes albopictus (Skuse, 1894) chikungunya, dengue and Zika virus, as well as diroflar- is listed as one of the most invasive mosquito species ial worms [2, 3]. With its global spread and an increasing worldwide [1]. Besides the considerable biting nuisance, number of infected travellers returning from disease- endemic countries, outbreaks of tropical and subtropi- cal mosquito-borne diseases have become a reality also *Correspondence: [email protected] 1 Swiss Tropical and Public Health Institute, Socinstrasse 57, P.O. Box, in Europe, exemplifed by the autochthonous cases of 4002 Basel, Switzerland chikungunya in Italy [4, 5] and France, and dengue in Full list of author information is available at the end of the article © The Author(s) 2019. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Vavassori et al. Parasites Vectors (2019) 12:583 Page 2 of 14 Croatia, France and Spain [6–11] with Ae. albopictus In this study we aimed at estimating the dispersal identifed as the incriminated vector. patterns of Ae. albopictus in an area where control Due to desiccation resistant eggs, Ae. albopictus is pas- measures are in place, while overcoming the draw- sively spread across the globe through the international backs of commonly used methods to mark released trade of used tyres and other artifcial containers. At a mosquitoes. Our results provide the first data on more regional scale, adults are travelling as blind passen- active dispersal in Switzerland and we discuss them in gers in vehicles and are dispersed particularly along the the framework of risk assessment of disease transmis- main trafc routes [12–14]. In contrast, Ae. albopictus sion and effective vector control. has been deemed a poor fyer as its range of active dis- persal is generally assumed to be limited to a few hun- Methods dred metres (Table 1), while laboratory studies suggest Study sites the mosquito could actually fy several kilometres [15], We conducted our MRR experiments at two sites in leaving some uncertainties as to whether its actual fight southern Switzerland in the Canton of Ticino, Coldrerio range might have been underestimated. and Lugano (Fig. 1) from 9th to 31st of August and from Understanding the dispersal dynamics of invasive mos- 8th to 28th of September 2018, respectively. Tese dates quito species is fundamental to improve vector surveillance coincide with the peak of the Ae. albopictus season in and to target control eforts. Whether being used to control Ticino [25]. a new or existing mosquito infestation, the dispersal poten- Coldrerio (45°51″N, 8°59″E, 351 m) is a municipality tial of a mosquito species will have important implications in the district of Mendrisio and in 2017 had a popula- for the spatial scale at which control interventions need to tion of 2892 inhabitants [26]. Coldrerio covers an area be deployed. For example, if a returning traveller presents of 246 ha of which 20% (47 ha) are woods, 50% (124 ha) viremia in an area where the local mosquito population is are agricultural areas and 30% (74 ha) are urban. Te competent to transmit the virus, control measures may be landscape is representative for a municipality of south- deployed within the vector’s fight range in order to mini- ern Switzerland, where the land is primarily used for mise the risk of further spread. Current guidelines recom- agricultural purposes (i.e. mainly vineyards). Te high- mend vector control measures to be implemented within a way E35, connecting Rome with Amsterdam, crosses the radius of 100 m from the residence of a suspected or con- municipality of Coldrerio where the frst specimens of frmed case or 300 m of a cluster of cases [16–19]. Ae. albopictus in Switzerland were found in an ovitrap Active dispersal, population size and other mosquito placed at the motorway service station in 2003 [23]. population related parameters have frequently been Lugano (46°00″N, 8°57″E, 273 m) is the largest city in investigated in mark-release-recapture (MRR) studies, the canton and had a population of 63,932 in 2017 [26]. where adult mosquitoes are coloured with fuorescent Lugano city centre lies on Lake Lugano and is surrounded pigment, released and then recaptured in traps [20, 21]. by two mountains, Monte Brè (925 m) and San Salvatore In most studies with Ae. albopictus, the mosquitoes were (912 m) that overlook the lake. Lugano covers a surface of sourced from laboratory colonies that had been reared 30,811 ha, of which 66% (20,288 ha) are covered by for- over many generations (Table 1). However, rearing con- ests, 12% (3654 ha) are agricultural areas, 17% (5126 ha) ditions have a strong infuence on mosquito physiol- are urban land and 5% (1730 ha) are covered by water. ogy, which will also infuence dispersal behaviour [22]. Additionally, mosquitoes have mostly been individu- Self‑marking units ally marked with tedious and time-consuming methods, We investigated the active dispersal behaviour of Ae. involving direct manipulation of mosquitoes, casting albopictus using a unit in which mosquitoes emerg- doubt on the validity of such MRR studies. ing from a breeding site mark themselves with fuores- In Switzerland Ae. albopictus was frst detected in 2003 cent pigment (Fig. 2). Te unit was originally developed at a motorway service area [23] and since then has contin- for Culex mosquitoes [27] and has also already been ued to spread across larger areas of the Canton of Ticino deployed in a study to mark emerging Ae. albopictus [28] [13]. Despite an intensive control programme based on in the feld. public awareness campaigns, larval source reduction and In the present study, the self-marking units consisted larviciding, the mosquito has spread across many areas in of three parts: an aluminium structure, a removable Ticino. Nevertheless, relative population densities have exit grid and cheese cloth strips of 55 × 20 cm that are been shown to be twice as high in non-intervention areas impregnated with fuorescent pigment (Fig. 2). Te alu- in neighbouring regions in Italy, supporting the hypothe- minium structure supports the removable exit grid that sis that the vector control eforts still have a major impact is made of a wooden frame and aluminium rods while the on mosquito density [24].
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