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Mosquitoes, Midges and Microbiota and Midges Mosquitoes Mosquitoes, midges and microbiota Mosquitoes, midges and microbiota midges and microbiota Mosquitoes, European vector diversity and the spread of pathogens Tim W.R. Möhlmann Tim W.R. Möhlmann W.R. Tim Mosquitoes, midges and microbiota European vector diversity and the spread of pathogens Tim W.R. Möhlmann Thesis committee Promotor Prof. Dr M. Dicke Professor of Entomology Wageningen University & Research Co-promotors Dr C.J.M. Koenraadt Associate Professor, Laboratory of Entomology Wageningen University & Research Dr L.S. van Overbeek Senior researcher, Biointeractions and Plant Health Wageningen University & Research Other Members Prof. Dr H.F.J. Savelkoul, Wageningen University & Research Prof. Dr P.A. van Rijn, Wageningen Bioveterinary Research Dr M.J.J. Schrama, Leiden University Dr S. Carpenter, Pirbright Institute, Pirbright, UK This research was conducted under the auspices of the C.T. de Wit Graduate School for Production Ecology & Resource Conservation. Mosquitoes, midges and microbiota European vector diversity and the spread of pathogens Tim W.R. Möhlmann 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 22 March 2019 at 4 p.m. in the Aula. Tim W.R. Möhlmann Mosquitoes, midges and microbiota European vector diversity and the spread of pathogens 280 pages. PhD thesis, Wageningen University, Wageningen, The Netherlands (2019) With references, with summary in English ISBN 978-94-6343-395-2 DOI: 10.18174/466379 Table of contents Chapter 1 9 General introduction Chapter 2 27 Community analysis of the abundance and diversity of mosquito species (Diptera: Culicidae) in three European countries at different latitudes Chapter 3 47 Latitudinal diversity of Culex pipiens biotypes and hybrids in farm, peri-urban, and wetland habitats in Europe Chapter 4 59 Community analysis of the abundance and diversity of biting midge species (Diptera: Ceratopogonidae) in three European countries at different latitudes Chapter 5 75 Latitudinal diversity of biting midge species within the Obsoletus group across three habitats in Europe Chapter 6 89 Biting midge dynamics and bluetongue transmission: A multiscale model linking catch data with climate and disease outbreaks Chapter 7 129 Species identity, life history, and geographic distance influence gut bacterial communities in lab-reared and European field-collected Culicoides biting midges Chapter 8 159 Impact of gut bacteria on the infection and transmission of pathogenic arboviruses by biting midges and mosquitoes Chapter 9 181 Vector competence of biting midges and mosquitoes for Shuni virus Chapter 10 201 General discussion References 217 Summary 255 Acknowledgements 261 Curriculum Vitae 269 List of publications 273 Education statement 277 Chapter 1 General introduction Chapter 1 Introduction A community is an assemblage of organisms found in a certain place and time. Often communities are dominated by a few very common species. However, the composition of a community can change over time (Morin, 2009). Communities occur on a large scale as well as on a more local scale such as an insect community around a livestock farm. Even the smallest organisms such as bacteria and viruses form communities within larger scale environments. The close interaction among species in a community means that a shift in species occurrence within a community can be expected to have an effect on the other species within the same community, as well as the environment or ecosystem that supports this community (Chapin et al., 2000; Ives & Cardinale, 2004; Wang et al., 2011). Both on a large scale, as well as on a small scale, these changes can have a profound impact on the community composition and their effects on the ecosystem at large. Insects play a crucial role in many ecosystems and the communities therein. With an estimation of several millions of insect species worldwide, they can be found almost everywhere in the world (Stork, 2018). Several insect species have become dependent on blood from other animals for their own reproduction (Lehane, 2005; Shaw et al., 2015). Females of these so- called haematophagous insects take a blood meal from a host to develop their eggs. A female can develop several egg batches during her lifetime and, therefore, has to take multiple blood meals (Lehane, 2005). During a blood meal, the female can take up pathogens that circulate in the host’s blood. Some pathogens utilize these blood-feeding insects as a vehicle to get to a new host. Insects that can transmit pathogens in this way are, therefore, referred to as vectors. Some of the well-known insect vectors of human and animal pathogens are mosquitoes, ticks and biting midges (Lehane, 2005). One Health With a constantly growing human population, increased travel and trade around the globe and global climate change, we face new challenges such as food security and food safety as well as increased risks of infectious diseases (Purse et al., 2008; Costello et al., 2009; Keesing et al., 2010; Kilpatrick & Randolph, 2012; McMichael, 2013). In a One Health approach, these challenges are tackled with the inclusion of human, veterinary, wildlife, environmental and ecological aspects. These aspects cannot be considered separately if we want to develop durable solutions for these global challenges. For example, to secure sufficient food production for a growing human population, crop production and livestock farms are expanded and intensified. Higher densities of domestic animals can lead to increased risks of animal-disease outbreaks. Often these diseases originate from wildlife populations and are initiated by direct or indirect contacts between wildlife and domesticated animals (Gortázar et al., 2007). To tackle these global problems a One Health approach is key. Prevention of large disease outbreaks in both wildlife and livestock will also protect human health. 10 General introduction Diseases cause major losses in animal production and simultaneously pose a threat to human health due to their zoonotic potential. Over 200 zoonotic diseases that infect both animals and humans are recognized as a threat for animal and human health. Of all emerging infectious 1 diseases, over 60% is zoonotic and of these zoonotic diseases more than 70% originates from wildlife animals (Jones et al., 2008). Vector-borne pathogens are responsible for more than 15% of all emerging infectious diseases and can harm both animals and humans (Jones et al., 2008; WHO, 2017). Combatting vector-borne infectious diseases is, therefore, a perfect example of requiring an transdisciplinary approach due to the complex epidemiology of the diseases, interactions with humans, livestock, wildlife and insect vectors, economic importance, and the multifaceted management of control and prevention (Costello et al., 2009). Due to increased travel and trade, exotic vector species are repeatedly introduced into new environments. Simultaneously, global rising temperatures provide favourable conditions for these exotic vector species at new locations where the vectors may become established. In addition, increased temperatures accelerate the development of insect vectors, thereby boosting their populations. Finally, higher temperatures increase virus proliferation in the vector, thereby reducing the extrinsic incubation period, which leads to a higher vectorial capacity. These factors all increase the potential of vector-borne pathogen transmission, and consequently increase the risk of disease outbreaks (Kilpatrick & Randolph, 2012). The global challenges associated with vector-borne diseases need integrated solutions to improve animal and human health. Identification of endemic and exotic vector species, monitoring of vector abundance, predictions of pathogen transmission by vectors, optimization of existing and development of new control methods and testing vector competence of endemic vector species for emerging virus strains will all support preparedness for future disease outbreaks. Only through an integrated approach that involves experts from different scientific disciplines can such solutions be achieved and our preparedness for future disease risks be improved (Garros et al., 2018). Vectors Mosquitoes (Culicidae) and biting midges (Culicoides spp.) are important vectors of pathogens. Mosquitoes can transmit pathogens such as Plasmodium, Zika virus (ZIKV), Chikungunya virus (CHIKV) and West Nile virus (WNV). Biting midges are known to transmit Oropouche virus (OROV), African horse sickness virus (AHSV), Schmallenberg virus (SBV) and bluetongue virus (BTV) (Mellor, 1990; Hubálek & Halouzka, 1999; Rasmussen et al., 2012; Weaver & Lecuit, 2015; Benelli & Romano, 2017; Vogels et al., 2017). Only female mosquitoes and biting midges take blood meals for the development of their eggs. The eggs are deposited in, or close to water or a moist environment. The larvae and pupae of mosquitoes and biting midges have a (semi-)aquatic lifestyle. Larvae of mosquitoes prefer (small) standing water bodies, whereas larvae of biting midges inhabit moist environments rich in organic material, 11 Chapter 1 such as mud, tree holes or animal dung (Murray, 1957; Foxi & Delrio, 2010; Steinke et al., 2016). The larvae of both mosquitoes and biting midges are detritivorous or omnivorous and feed on animal- and plant-derived material in their environment (Conte et al., 2007).
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