Geospatial risk analysis of mosquito-borne disease vectors in the Netherlands Adolfo Ibáñez-Justicia Thesis committee Promotor Prof. Dr W. Takken Personal chair at the Laboratory of Entomology Wageningen University & Research Co-promotors Dr C.J.M. Koenraadt Associate professor, Laboratory of Entomology Wageningen University & Research Dr R.J.A. van Lammeren Associate professor, Laboratory of Geo-information Science and Remote Sensing Wageningen University & Research Other members Prof. Dr G.M.J. Mohren, Wageningen University & Research Prof. Dr N. Becker, Heidelberg University, Germany Prof. Dr J.A. Kortekaas, Wageningen University & Research Dr C.B.E.M. Reusken, National Institute for Public Health and the Environment, Bilthoven, The Netherlands This research was conducted under the auspices of the C.T. de Wit Graduate School for Production Ecology & Resource Conservation Geospatial risk analysis of mosquito-borne disease vectors in the Netherlands Adolfo Ibáñez-Justicia Thesis submitted in fulfilment of the requirements for the degree of doctor at Wageningen University by the authority of the Rector Magnificus, Prof. Dr A.P.J. Mol, in the presence of the Thesis Committee appointed by the Academic Board to be defended in public on Friday 1 February 2019 at 4 p.m. in the Aula. Adolfo Ibáñez-Justicia Geospatial risk analysis of mosquito-borne disease vectors in the Netherlands, 254 pages. PhD thesis, Wageningen University, Wageningen, the Netherlands (2019) With references, with summary in English ISBN 978-94-6343-831-5 DOI https://doi.org/10.18174/465838 Table of contents Abstract 9 Chapter 1 11 General introduction Chapter 2 21 National Mosquito (Diptera: Culicidae) Survey in The Netherlands 2010–2013 Chapter 3 45 Modelling the spatial distribution of the nuisance mosquito species Anopheles plumbeus (Diptera: Culicidae) in the Netherlands Chapter 4 61 Pathways for introduction and dispersal of invasive mosquito species in Europe: a review Chapter 5 79 Evaluating perceptions of risk in mosquito experts and identifying undocumented pathways for the introduction of invasive mosquito species into Europe Chapter 6 109 Risk-based and adaptive surveillance at Lucky bamboo and used tire importers to prevent the establishment of invasive mosquitoes in the Netherlands Chapter 7 131 The first detected airline introductions of yellow fever mosquitoes (Aedes aegypti) to Europe, at Schiphol International airport, the Netherlands Chapter 8 149 The effectiveness of Asian bush mosquito (Aedes japonicus japonicus) control actions in colonised peri-urban areas in the Netherlands Chapter 9 167 Habitat suitability modelling to assess the introductions of Aedes albopictus (Diptera, Culicidae) in the Netherlands Chapter 10 187 General discussion References 205 Summary 229 Acknowledgments 237 Curriculum vitae 241 List of publications 245 Training and education statement 251 Abstract 8 Abstract: The availability of data on distribution and density of mosquito vectors of disease is needed to understand the risk of mosquito-borne diseases. In case of an outbreak of a newly introduced mosquito-borne pathogen of medical or veterinary importance, such information is required in order to decide on a contingency and eventual control plan. In the recent decade, several exotic mosquito species have become established in European countries and they have rapidly expanded their distribution. The rationale for the present study was the increasingly frequent reporting of invasive mosquito species (IMS) in the Netherlands, some of which are known vectors of infectious diseases, as well as the lack of detailed knowledge on the spatio-temporal distribution of the indigenous mosquito fauna. The aim was therefore to develop methodologies for acquiring accurate information on the actual and potential distribution of indigenous and exotic mosquito species in the Netherlands, and to evaluate the surveillance and control methodologies applied after IMS findings. To establish a baseline for the spatio-temporal distribution of the indigenous mosquito fauna present in the Netherlands, a survey was conducted at the start of the study. Cross-sectional mosquito field surveys were carried out over a period of four years (2010-2013). These surveys provided occurrence maps for 26 indigenous species. One invasive mosquito species, Aedes japonicus, was discovered using this strategy. Furthermore, data on seasonality of the species, biodiversity and habitat preferences were also provided. Using the collected data on occurrence and abundance, a special study using random forest models was done to investigate the potential spatial distribution and population density of Anopheles plumbeus, a native nuisance mosquito species. I found a high environmental suitability and abundance of this species in the south-eastern provinces, mostly associated with abandoned pig farm buildings, and reports of biting nuisance. The identification of pathways for introduction of IMS was investigated in a next step taking into account the current knowledge and expert opinion. This was done in order to decide on the surveillance strategies needed to reduce the risk of future IMS introductions and/or potential outbreaks of mosquito-borne diseases. Four main routes for IMS introduction and dispersal were identified: the trade in used tires, the import of Lucky bamboo plants from Asia, the passive transport of IMS in vehicles (traffic by road, airplanes, and sea), and the natural dispersal of IMS. The results of the risk-based surveillance of IMS revealed yearly introductions of Ae. albopictus since 2010 at used tire companies and Lucky bamboo greenhouses, sporadic findings of Ae. japonicus associated with used tire trade, the first aircraft associated import of Ae. aegypti in Europe, and the first associated Ae. japonicus import with Lucky bamboo plants from elsewhere in the world. The control of these IMS, implemented after detection, has proven effective to avoid proliferation at these locations and their surroundings. Due to the yearly findings of Ae. albopictus, the potential risk of establishment of this invasive species was further investigated using habitat suitability models. Results show that the current average climatic conditions limit the overwintering of eggs of Ae. albopictus and their survival as adults in many inland areas of the country. However, due to the expected increase of the temperatures in the next decades as a result of climate change, these parts of the Netherlands will offer climatic conditions suitable for sustain populations of this species. The results presented in this thesis show that nationwide surveillance of mosquitoes is pivotal to gain detailed information on the spatio-temporal distribution and abundance of mosquito species, which is useful to study the habitat suitability of vector species. Furthermore, this thesis highlights the main pathways for introduction and dispersal of IMS, designed a risk- based surveillance of IMS, and evaluated the surveillance and control measures applied in the Netherlands against IMS introductions. The work presented provides essential insights for identifying locations at risk of vector-borne disease transmission, and for designing targeted control of newly introduced IMS in the Netherlands, which is expected in the future. 9 Chapter 1 General introduction Chapter 1 Mosquito-borne diseases in Europe Outbreaks of mosquito-borne diseases (MBD) can cause considerable animal and human suffering, and high economic damage (Rich and Wanyoike 2010, Tarantola et al. 2014). With the eradication of dengue and malaria from Europe in the 1950’s, the threat from MBD was considered then to be limited only to countries in the tropics. However, during the first years of the 21st century, this situation changed in Europe due to several MBD outbreaks. Some MBD are transmitted by indigenous European mosquito species and are known to occur frequently in Europe, such as Tahyna (Hubalek et al. 2010), tularaemia (Rijks et al. 2013), Sindbis/Ockelbo, Batai, Inkoo and West Nile (Lundstrom 1999). However, in the last years malaria re-emerged in some parts of Europe (Danis et al. 2011), and dengue appeared in France (La Ruche et al. 2010), Croatia (Gjenero-Margan et al. 2010) and Madeira (Sousa et al. 2012). Furthermore, several outbreaks of MBD that originate from (sub)tropical areas also recently occurred in Europe, such as chikungunya in Italy (Rezza et al. 2007, Venturi et al. 2017) and France (Calba et al. 2017), and Usutu outbreaks in Austria (Weissenbock et al. 2003), Italy (Calzolari et al. 2010), Germany (Becker et al. 2012) and The Netherlands (Rijks et al. 2016). Of the above MBD, dengue and chikungunya are exclusively transmitted in Europe by established populations of the invasive mosquitoes species (IMS) Aedes aegypti (Linnaeus) or Ae. albopictus (Skuse) (Medlock et al. 2012). The well-known main driver of these pathogen introductions in the last decades is the accelerating increase in trade and travel (Kilpatrick and Randolph 2012). Nowadays, the growth in air travel has accelerated introductions allowing pathogens to reach other continents within the few days that hosts are infectious, and even during the latent period for some diseases (Kilpatrick et al. 2006). There is concern that other MBD, not indigenous to Europe, might be introduced causing outbreaks, such as Zika, Rift Valley Fever, or Japanese encephalitis. Data from Italy suggest that Japanese encephalitis was already introduced into Europe in 2010 (Ravanini et al. 2012), and until