Staff Publications

Staff Publications

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    'Staff publications' is the digital repository of Wageningen University & Research

    'Staff publications' contains references to publications authored by Wageningen University staff from 1976 onward.

    Publications authored by the staff of the Research Institutes are available from 1995 onwards.

    Full text documents are added when available. The database is updated daily and currently holds about 240,000 items, of which 72,000 in open access.

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    A DNA-Binding Bromodomain-Containing Protein Interacts with and Reduces Rx1-Mediated Immune Response to Potato Virus X
    Sukarta, Octavina C.A. ; Townsend, Philip D. ; Llewelyn, Alexander ; Dixon, Christopher H. ; Slootweg, Erik J. ; Pålsson, Lars-Olof ; Takken, Frank L.W. ; Goverse, Aska ; Cann, Martin J. - \ 2020
    Plant Communications 1 (2020)4. - ISSN 2590-3462 - p. 100086 - 100086.
    Plant NLR proteins enable the immune system to recognize and respond to pathogen attack. An early consequence of immune activation is transcriptional reprogramming. Some NLRs have been shown to act in the nucleus and interact with transcription factors. The Rx1 NLR protein of potato binds and distorts double-stranded DNA. However, the components of the chromatin-localized Rx1 complex are largely unknown. Here, we report a physical and functional interaction between Rx1 and NbDBCP, a bromodomain-containing chromatin-interacting protein. NbDBCP accumulates in the nucleoplasm and nucleolus, interacts with chromatin, and redistributes Rx1 to the nucleolus in a subpopulation of imaged cells. Rx1 overexpression reduces the interaction between NbDBCP and chromatin. NbDBCP is a negative regulator of Rx1-mediated immune responses to potato virus X (PVX), and this activity requires an intact bromodomain. Previously, Rx1 has been shown to regulate the DNA-binding activity of a Golden2-like transcription factor, NbGlk1. Rx1 and NbDBCP act synergistically to reduce NbGlk1 DNA binding, suggesting a mode of action for NbDBCP’s inhibitory effect on immunity. This study provides new mechanistic insight into the mechanism by which a chromatin-localized NLR complex co-ordinates immune signaling after pathogen perception.
    The Genetic Architecture of Post-Zygotic Reproductive Isolation Between Anopheles coluzzii and An. quadriannulatus
    Deitz, Kevin C. ; Takken, Willem ; Slotman, Michel A. - \ 2020
    Frontiers in Genetics Livestock Genomics 11 (2020). - ISSN 1664-8021
    Anopheles gambiae complex - Dobzhansky–Muller incompatibilities - hybrid - inviability - post-zygotic reproductive isolation - speciation - sterility

    The Anopheles gambiae complex is comprised of eight morphologically indistinguishable species and has emerged as a model system for the study of speciation genetics due to the rapid radiation of its member species over the past two million years. Male hybrids between most An. gambiae complex species pairs are sterile, and some genotype combinations in hybrid males cause inviability. We investigated the genetic basis of hybrid male inviability and sterility between An. coluzzii and An. quadriannulatus by measuring segregation distortion and performing a QTL analysis of sterility in a backcross population. Hybrid males were inviable if they inherited the An. coluzzii X chromosome and were homozygous at one or more loci in 18.9 Mb region of chromosome 3. The An. coluzzii X chromosome has a disproportionately large effect on hybrid sterility when introgressed into an An. quadriannulatus genetic background. Additionally, an epistatic interaction between the An. coluzzii X and a 1.12 Mb, pericentric region of the An. quadriannulatus 3L chromosome arm has a statistically significant contribution to the hybrid sterility phenotype. This same epistatic interaction occurs when the An. coluzzii X is introgressed into the genetic background of An. arabiensis, the sister species of An. quadriannulatus, suggesting that this may represent one of the first Dobzhansky–Muller incompatibilities to evolve early in the radiation of the Anopheles gambiae species complex. We describe the additive effects of each sterility QTL, epistatic interactions between them, and genes within QTL with protein functions related to mating behavior, reproduction, spermatogenesis, and microtubule morphogenesis, whose divergence may contribute to post-zygotic reproductive isolation between An. coluzzii and An. quadriannulatus.

    Citizen science for malaria vector surveillance in Rwanda
    Murindahabi, Marilyn Milumbu - \ 2020
    Wageningen University. Promotor(en): W. Takken, co-promotor(en): C.J.M. Koenraadt; A.J.H. van Vliet; L. Mutesa. - Wageningen : Wageningen University - ISBN 9789463953993 - 185

    Rwanda made tremendous achievements in reducing malaria morbidity and mortality through the scale up of vector control interventions including long lasting insecticide nets (LLINs) and indoor residual spraying (IRS) from 2005 up to 2011. However, malaria remains a major public health concern in the country. With the resurgence of malaria since 2012, improving vector control is urgent. Inadequate financial resources and ecological changes which increase the risk of malaria transmission are among factors that have caused this upsurge. Hence, malaria resurgence has hindered to sustain the progress made in malaria reduction and control.

    Entomological surveillance is one of the most important strategies for malaria prevention and control being undertaken in Rwanda. Although, mosquito monitoring programmes are established in 12 sentinel sites, maps of malaria risk for the whole country is needed. In this way available resources for malaria control can be deployed in an efficient way. However, there are significant costs associated with the expansion of the mosquito monitoring programmes. The implementation of a citizen science programme for (malaria) mosquito surveillance has the potential to overcome these limitations.

    In this thesis biological, environmental and institutional factors have been described as contributors to the malaria resurgence in Rwanda. citizen science approach as a new and alternative strategy to contribute to the improvement of malaria mosquito surveillance in low resource settings for the vector control surveillance system in Rwanda are presented. The implementation of a sustainable citizen science programme for malaria vector surveillance requires the participation of citizens. Prior the implementation of citizen science, entomological and household surveys conducted in the studied areas demonstrate that mosquito abundance and species composition of malaria vectors collected using Centers for Disease Control and Prevention (CDC) light traps inside houses combined with demographic characteristics such as building materials of the houses (for example tiled roofs, walls made of mud and wood), as well as the number of occupants in the house, predicted the number of mosquitoes (Culicidae) in the houses. While the presence of eaves plus walls made of mud and wood predicted malaria vector abundance. The results suggest that the perception of mosquito nuisance denoted in a questionnaire could be used as a global indicator of malaria vector hotspots. Hence, involving citizens in reporting mosquito nuisance can complement malaria mosquito surveillance and control.

    Results also demonstrate that prior the implementation of a citizen science programme for malaria vector surveillance , co-designing processes of a citizen science programme (CSP) with citizens who have valuable context-specific knowledge and skills is required in order a CSP in a rural area to be feasible. The results suggest that the handmade plastic bottle trap baited with CO2 and light represents an option for inclusion in mosquito surveillance activities in a citizen science context in rural areas. Additionally, the spatio-temporal distribution of mosquito nuisance and malaria vectors collected through citizen science described in this thesis provide insight into the ecology of malaria vectors and can thereby help to better understand malaria transmission patterns in Rwanda. The applicability of using remote sensing and citizen science data in determining the environmental predictors of malaria vector distribution in the studied areas are also presented. Malaria hotspots were found more in the southern part of Ruhuha, especially in Busasamana and Kibaza, the villages that also reported the highest mosquito abundance and nuisance levels.

    Use of semiochemicals for surveillance and control of hematophagous insects
    Mweresa, Collins K. ; Mukabana, W.R. ; Loon, J.J.A. van; Dicke, M. ; Takken, W. - \ 2020
    Chemoecology (2020). - ISSN 0937-7409
    Attraction - Behavior - Flies - Kairomones - Monitoring - Mosquitoes - Repellence - Semiochemicals

    Reliance on broad-spectrum insecticides and chemotherapeutic agents to control hematophagous insect vectors, and their related diseases is threatened by increasing insecticide and drug resistance, respectively. Thus, development of novel, alternative, complementary and effective technologies for surveillance and control of such insects is strongly encouraged. Semiochemicals are increasingly developed for monitoring and intervention of insect crop pests, but this has not been adequately addressed for hematophagous insects of medical and veterinary importance. This review provides an insight in the application of semiochemicals for control of hematophagous insects. Here, we provide specific information regarding the isolation and identification of semiochemical compounds, optimization approaches, detection, perception and discrimination by the insect olfactory system. Navigation of insects along wind-borne odor plumes is discussed and methods of odor application in field situations are reviewed. Finally, we discuss prospects and future challenges for the application of semiochemical-based tools with emphasis on mosquitoes. The acquired knowledge can guide development of more effective components of integrated vector management, safeguard against emerging resistance of insects to existing insecticides and reduce the burden of vector-borne diseases.

    Characterisation of anopheline larval habitats in southern Malawi
    Gowelo, Steven ; Chirombo, James ; Koenraadt, Constantianus J.M. ; Mzilahowa, Themba ; Berg, Henk van den; Takken, Willem ; McCann, Robert S. - \ 2020
    Acta Tropica 210 (2020). - ISSN 0001-706X
    Habitat characterization - Larval ecology - Malaria mosquito

    Introduction: Increasing the knowledgebase of anopheline larval ecology could enable targeted deployment of malaria control efforts and consequently reduce costs of implementation. In Malawi, there exists a knowledge gap in anopheline larval ecology and, therefore, basis for targeted deployment of larval source management (LSM) for malaria control, specifically larvicides. We set out to characterize anopheline larval habitats in the Majete area of Malawi on the basis of habitat ecology and anopheline larval productivity to create a basis for larval control initiatives in the country. Methods: Longitudinal surveys were conducted in randomly selected larval habitats over a period of fifteen months in Chikwawa district, southern Malawi. Biotic and abiotic parameters of the habitats were modelled to determine their effect on the occurrence and densities of anopheline larvae. Results: Seventy aquatic habitats were individually visited between 1-7 times over the study period. A total of 5,123 immature mosquitoes (3,359 anophelines, 1,497 culicines and 267 pupae) were collected. Anopheline and culicine larvae were observed in sympatry in aquatic habitats. Of the nine habitat types followed, dams, swamps, ponds, borehole runoffs and drainage channels were the five most productive habitat types for anopheline mosquitoes. Anopheline densities were higher in aquatic habitats with bare soil making up part of the surrounding land cover (p<0.01) and in aquatic habitats with culicine larvae (p<0.01) than in those surrounded by vegetation and not occupied by culicine larvae. Anopheline densities were significantly lower in highly turbid habitats than in clearer habitats (p<0.01). Presence of predators in the aquatic habitats significantly reduced the probability of anopheline larvae being present (p=0.04). Conclusions: Anopheline larval habitats are widespread in the study area. Presence of bare soil, culicine larvae, predators and the level of turbidity of water are the main determinants of anopheline larval densities in aquatic habitats in Majete, Malawi. While the most productive aquatic habitats should be prioritised, for the most effective control of vectors in the area all available aquatic habitats should be targeted, even those that are not characterized by the identified predictors. Further research is needed to determine whether targeted LSM would be cost-effective when habitat characterisation is included in cost analyses and to establish what methods would make the characterisation of habitats easier.

    Community factors affecting participation in larval source management for malaria control in Chikwawa District, Southern Malawi
    Gowelo, Steven ; McCann, Robert S. ; Koenraadt, Constantianus J.M. ; Takken, Willem ; Berg, Henk van den; Manda-Taylor, Lucinda - \ 2020
    Malaria Journal 19 (2020)1. - ISSN 1475-2875 - 1 p.
    Bacillus thuringiensis israelensis - Community - Larval source management - Malaria - Malawi

    BACKGROUND: To further reduce malaria, larval source management (LSM) is proposed as a complementary strategy to the existing strategies. LSM has potential to control insecticide resistant, outdoor biting and outdoor resting vectors. Concerns about costs and operational feasibility of implementation of LSM at large scale are among the reasons the strategy is not utilized in many African countries. Involving communities in LSM could increase intervention coverage, reduce costs of implementation and improve sustainability of operations. Community acceptance and participation in community-led LSM depends on a number of factors. These factors were explored under the Majete Malaria Project in Chikwawa district, southern Malawi. METHODS: Separate focus group discussions (FGDs) were conducted with members from the general community (n = 3); health animators (HAs) (n = 3); and LSM committee members (n = 3). In-depth interviews (IDIs) were conducted with community members. Framework analysis was employed to determine the factors contributing to community acceptance and participation in the locally-driven intervention. RESULTS: Nine FGDs and 24 IDIs were held, involving 87 members of the community. Widespread knowledge of malaria as a health problem, its mode of transmission, mosquito larval habitats and mosquito control was recorded. High awareness of an association between creation of larval habitats and malaria transmission was reported. Perception of LSM as a tool for malaria control was high. The use of a microbial larvicide as a form of LSM was perceived as both safe and effective. However, actual participation in LSM by the different interviewee groups varied. Labour-intensiveness and time requirements of the LSM activities, lack of financial incentives, and concern about health risks when wading in water bodies contributed to lower participation. CONCLUSION: Community involvement in LSM increased local awareness of malaria as a health problem, its risk factors and control strategies. However, community participation varied among the respondent groups, with labour and time demands of the activities, and lack of incentives, contributing to reduced participation. Innovative tools that can reduce the labour and time demands could improve community participation in the activities. Further studies are required to investigate the forms and modes of delivery of incentives in operational community-driven LSM interventions.

    A participatory approach for malaria control in southern Malawi : Effects of the environment and community on larval source management
    Gowelo, Steven A. - \ 2020
    Wageningen University. Promotor(en): W. Takken, co-promotor(en): C.J.M. Koenraadt. - Wageningen : Wageningen University - ISBN 9789463953641 - 155

    Current trends in the fight against malaria suggest that further progress will be difficult with  the use of insecticide-based control measures alone. Without major reductions in the burden of malaria registered in the past few years, the use of additional interventions with synergistic effects on the current standard measures is required. Currently, interest in employing Larval Source Management (LSM) as a complementary tool is growing as it has shown to significantly reduce larval densities and consequently adult populations in settings where it has been applied along other interventions. LSM is commonly executed via 1) habitat modification, which includes physical transformation of a larval habitat through draining, filling and land levelling and 2) larviciding, commonly using an endotoxin-producing bacterial larvicide, Bacillus thuringiensis var. israelensis (Bti). Knowledge on the ecology of anopheline larval habitats is therefore important as it informs where LSM should be targeted. Also, knowledge about community acceptance and participation in LSM is important as it affects the scalability and future sustainability of the intervention. The study described in this thesis focused on the potential of community-led LSM in Malawi. Chapter 2 describes the habitat ecology of malaria vectors in the Majete area, southern Malawi. In this area, anopheline larvae develop in habitats with little silt, surrounded by bare-grounds and occupied by culicine larvae. I conclude that larval control should be directed towards such anopheline-productive habitats which sustain malaria transmission. In Chapter 3, I investigated whether application of Bti induces discrimination of treated sites by gravid females seeking oviposition sites. I found that treatment of the sites with the bacterial larvicide does not repel ovipositing females from laying eggs in such sites. This finding implies that the female mosquitoes did not detect the presence of the larvicide in aquatic sites. In Chapter 4, we explored whether application of lower doses (sublethal) of Bti in larval habitats can negatively affect fitness parameters of malaria vectors and hence their ability to successfully transmit malaria. Sublethal Bti doses are likely to occur when applications are done under field conditions, especially by local communities who may lack the desired expertise in comparison with trained experts. Immature and adult life history parameters, including larval survival, adult longevity, wing size and oviposition of An. coluzzii, an important African malaria vector, were assessed in a laboratory setting. Our results show that larval densities were reduced when exposed to the sublethal doses. When exposed to Bti LC70 as larvae, the proportional hazard rate for mortality as adult females was about three times higher than in the control group. At the same LC70 dose rate, the mean wing length of the adult females increased by 12% compared to that of the control group. These findings are valuable as they demonstrate that larval exposure to Bti, even at lower doses, reduces the longevity of emerging adults which also reduces their vectorial capacity as they may not live long enough to effectively transmit the malaria parasite. In Chapter 5, we assessed whether communities would  accept and are willing to participate in community-led LSM activities. Specifically, we explored factors that would motivate community acceptance and participation in LSM. Our results show that community involvement in LSM as an additional tool for malaria control increases local awareness of malaria as a health problem, its risk factors and control strategies. The results also show that specially trained members of the community easily accepted the intervention and were more willing to participate in the associated activities than the rest of the community. Further, the findings highlight the need to make activities less demanding in terms of time and labour. It was also observed that the community needs incentives to participate in community-led interventions but though critical, forms and modes of delivery of incentives need to be further studied. In Chapter 6, we investigated whether community involvement in LSM is feasible and can result in reduced larval vector densities. Our results showed that groups from the community, which received tailored training from the research team, participated more actively in the LSM activities than the rest of the community. Also, larviciding using Bti was the more preferred component of LSM by the community than habitat modification. Interestingly, application of Bti reduced larval densities in intervention villages. The findings of this study suggest that community involvement in LSM is only feasible when the community understands their malaria risk factors and control methods. Also, the study demonstrates that community involvement in application of Bti has the potential to reduce larval densities but should be implemented after proper training of the spraying teams. In Chapter 7, the key findings of this research and the implications for community-led LSM in Malawi are addressed and recommendations for future investigations are provided. In conclusion, the results of the research described in this thesis show that participation of communities in LSM is feasible and can reduce the malaria burden via reduced larval densities.

    Effects of larval exposure to sublethal doses of Bacillus thuringiensis var. israelensis on body size, oviposition and survival of adult Anopheles coluzzii mosquitoes
    Gowelo, Steven ; Chirombo, James ; Spitzen, Jeroen ; Koenraadt, Constantianus J.M. ; Mzilahowa, Themba ; Berg, Henk Van Den; Takken, Willem ; McCann, Robert - \ 2020
    Parasites & Vectors 13 (2020)1. - ISSN 1756-3305
    Bacillus thuringiensis var. israelensis - Larval source management - Mosquito - Sublethal dose - Vector control

    Background: Application of the larvicide Bacillus thuringiensis var. israelensis (Bti) is a viable complementary strategy for malaria control. Efficacy of Bti is dose-dependent. There is a knowledge gap on the effects of larval exposure to sublethal Bti doses on emerging adult mosquitoes. The present study examined the effect of larval exposure to sublethal doses of Bti on the survival, body size and oviposition rate in adult Anopheles coluzzii. Methods: Third-instar An. coluzzii larvae were exposed to control and sublethal Bti concentrations at LC20, LC50 and LC70 for 48 h. Surviving larvae were reared to adults under standard colony conditions. Thirty randomly selected females from each treatment were placed in separate cages and allowed to blood feed. Twenty-five gravid females from the blood-feeding cages were randomly selected and transferred into new cages where they were provided with oviposition cups. Numbers of eggs laid in each cage and mortality of all adult mosquitoes were recorded daily. Wing lengths were measured of 570 mosquitoes as a proxy for body size. Results: Exposure to LC70 Bti doses for 48 h as third-instar larvae reduced longevity of adult An. coluzzii mosquitoes. Time to death was 2.58 times shorter in females exposed to LC70 Bti when compared to the control females. Estimated mortality hazard rates were also higher in females exposed to the LC50 and LC20 treatments, but these differences were not statistically significant. The females exposed to LC70 concentrations had 12% longer wings than the control group (P < 0.01). No differences in oviposition rate of the gravid females were observed between the treatments. Conclusions: Exposure of An. coluzzii larvae to sublethal Bti doses reduces longevity of resultant adults and is associated with larger adult size and unclear effect on oviposition. These findings suggest that anopheline larval exposure to sublethal Bti doses, though not recommended, could reduce vectorial capacity for malaria vector populations by increasing mortality of resultant adults.[Figure not available: See fulltext.]

    Habitat suitability modelling to assess the introductions of Aedes albopictus (Diptera : Culicidae) in the Netherlands
    Ibáñez-Justicia, Adolfo ; Alcaraz-Hernández, Juan Diego ; Lammeren, Ron van; Koenraadt, Constantianus J.M. ; Bergsma, Aldo ; Delucchi, Luca ; Rizzoli, Annapaola ; Takken, Willem - \ 2020
    Parasites & Vectors 13 (2020)1. - ISSN 1756-3305 - 13 p.
    GIS - Habitat suitability models - Invasive mosquitoes - Land surface temperature - MaxEnt

    BACKGROUND: In the Netherlands, Aedes albopictus has been found each year since 2010 during routine exotic mosquito species surveillance at companies that import used tires. We developed habitat suitability models to investigate the potential risk of establishment and spread of this invasive species at these locations. METHODS: We used two methodologies: first, a species distribution model based on the maximum entropy modelling approach (MaxEnt) taking into consideration updated occurrence data of the species in Europe, and secondly, a spatial logic conditional model based on the temperature requirements of the species and using land surface temperature data (LST model). RESULTS: Suitability assessment obtained with the MaxEnt model at European level accurately reflect the current distribution of the species and these results also depict moderately low values in parts of the Netherlands, Belgium, Denmark, the British islands and southern parts of Scandinavia. Winter temperature was the variable that contributed most to the performance of the model (47.3%). The results of the LST model showed that: (i) coastal areas are suitable for overwintering of eggs; (ii) large areas in the northern part of the country have a low suitability for adult survival; and (iii) the entire country is suitable for successful completion of the life-cycle if the species is introduced after the winter months. Results of the LST model revealed that temperatures in 2012 and 2014 did not limit the overwintering of eggs or survival of adults at the locations where the species was found. By contrast, for the years 2010, 2011 and 2013, overwintering of eggs at these locations is considered unlikely. CONCLUSIONS: Results using two modelling methodologies show differences in predicted habitat suitability values. Based on the results of both models, the climatic conditions could hamper the successful overwintering of eggs of Ae. albopictus and their survival as adults in many areas of the country. However, during warm years with mild winters, many areas of the Netherlands offer climatic conditions suitable for developing populations. Regular updates of the models, using updated occurrence and climatic data, are recommended to study the areas at risk.

    Chemical Mediation of Oviposition by Anopheles Mosquitoes : a Push-Pull System Driven by Volatiles Associated with Larval Stages
    Schoelitsz, Bruce ; Mwingira, Victor ; Mboera, Leonard E.G. ; Beijleveld, Hans ; Koenraadt, Constantianus J.M. ; Spitzen, Jeroen ; Loon, Joop J.A. van; Takken, Willem - \ 2020
    Journal of Chemical Ecology 46 (2020)4. - ISSN 0098-0331 - p. 397 - 409.
    2,4-pentanedione - An. gambiae s.s - Anopheles coluzzii - Behavior - Dimethyldisulfide - Dimethyltrisulfide - Malaria - Mosquito - Nonane - Oviposition

    The oviposition behavior of mosquitoes is mediated by chemical cues. In the malaria mosquito Anopheles gambiae, conspecific larvae produce infochemicals that affect this behavior. Emanations from first instar larvae proved strongly attractive to gravid females, while those from fourth instars caused oviposition deterrence, suggesting that larval developmental stage affected the oviposition choice of the female mosquito. We examined the nature of these chemicals by headspace collection of emanations of water in which larvae of different stages were developing. Four chemicals with putative effects on oviposition behavior were identified: dimethyldisulfide (DMDS) and dimethyltrisulfide (DMTS) were identified in emanations from water containing fourth instars; nonane and 2,4-pentanedione (2,4-PD) were identified in emanations from water containing both first and fourth instars. Dual-choice oviposition studies with these compounds were done in the laboratory and in semi-field experiments in Tanzania. In the laboratory, DMDS and DMTS were associated with oviposition-deterrent effects, while results with nonane and 2,4-PD were inconclusive. In further studies DMDS and DMTS evoked egg retention, while with nonane and 2,4-PD 88% and 100% of female mosquitoes, respectively, laid eggs. In dual-choice semi-field trials DMDS and DMTS caused oviposition deterrence, while nonane and 2,4-PD evoked attraction, inducing females to lay more eggs in bowls containing these compounds compared to the controls. We conclude that oviposition of An. gambiae is mediated by these four infochemicals associated with conspecific larvae, eliciting either attraction or deterrence. High levels of egg retention occurred when females were exposed to chemicals associated with fourth instar larvae.

    Olfactory mediation of oviposition in Anopheles mosquitoes : A new strategy for malaria vector control
    Mwingira, Victor Saturnus - \ 2020
    Wageningen University. Promotor(en): W. Takken; M. Dicke, co-promotor(en): L.E.G. Mboera. - Wageningen : Wageningen University - ISBN 9789463953634 - 216

    Mosquito-borne diseases are among the most serious infectious diseases in the world caused by parasites and pathogens. The African mosquito Anopheles gambiae transmits malaria parasites as well as filarial worms. The mosquitoes feed on humans inside and outside houses, which complicates control strategies. Current control strategies focus mostly on reducing contact with host-seeking mosquitoes through the use of long-lasting insecticide-impregnated nets (LLINs) and indoor residual spraying (IRS). Despite the fact that these tools have lowered the burden of malaria in many parts of the world, transmission is sustained by vectors that bite outdoors. This thesis proposes a new strategy for malaria vector control to be added to existing control tools. It goes beyond blood-feeding processes and it targets all mosquitoes which are feeding indoors and outdoors. The proposed strategy is based on manipulation of oviposition behaviour using chemical cues that mimic olfactory cues emitted by breeding sites. Mosquitoes are attracted to lay their eggs on selected water bodies with specific biotic and abiotic factors. Organic chemical cues, emitted by these sites, are presumed to act as infochemicals enabling these mosquitoes to find suitable breeding sites. Identification of the odours that mediate the site-seeking behaviour of mosquitoes can lead to the development of novel intervention methods for mosquito-borne disease control.

    My study marked an important progress in the development of mosquito surveillance and control strategies using infochemicals by: (1) generating knowledge on the biology and ecology of immature stages of Anopheles mosquitoes in the study area, (2) providing evidence that mosquitoes select breeding sites preferentially and lay eggs on suitable sites while avoiding unsuitable ones, (3) identifying and characterizing volatile organic chemicals that mediate oviposition behaviour in mosquitoes, (4) generating evidence that oviposition infochemicals can be used to divert oviposition activities to specific breeding sites, which can be targeted by an environmentally safe larvicide: a lure-and-kill method.

    The research aimed to understand the reasons that prevent early and late larval stages from sharing breeding sites, and also why breeding sites with late stage larvae are not immediately succeeded by early stage larvae (Chapter 5). Several studies have indicated a possible role of habitat materials in the production of volatiles chemicals which either attract or deter egg-laying mosquitoes. A review of recently published studies showed that oviposition attractants and deterrents are produced by biotic factors present in breeding sites (Chapter 2). In my study it was found that breeding sites which are occupied by larvae play an important role in the production of odours that mediate oviposition behaviour of mosquitoes (Chapter 3). These infochemicals can potentially be used for manipulation of mosquito behaviour by making protected resources unsuitable for mosquitoes, while luring them towards attractive sources. Such push and pull strategies using ovipostion infochemicals for other mosquitoes were reviewed in order to develop similar surveillance and control strategies for malaria vectors. Among other larviciding products reviewed, bacterial products such as Bacillus sphaericus (Bs) and Bacillus thuringiensis israelensis (Bti) emerged with the potential to be combined with attractive infochemicals in the development of a lure and kill strategy (Chapter 2).

    To understand the factors influencing oviposition behaviour of Anopheles mosquitoes, a series of dual-choice behavioural experiments were conducted in the laboratory using larval habitats materials. Results show that the presence of larvae in breeding sites mediates oviposition behaviour of Anopheles mosquitoes (Chapter 3). The presence of early-stage larvae in oviposition cups attracted conspecific gravid mosquitoes to lay eggs, whereas the presence of late-stage larvae in the cups deterred conspecific gravid mosquitoes to lay eggs. The response was density dependent: as larval density increased so did the response, until reaching a threshold. Moreover, this behaviour was manifested more profoundly in the presence of larvae than larval-conditioned water. To test whether larval habitats produce volatiles that mediate oviposition behaviour, the oviposition cups containing larvae were covered by a filter paper to prevent gravid females from seeing the larvae in the cups. Results show that both olfactory and visual cues are involved in mediating the oviposition behaviour of anopheline mosquitoes.

    To confirm the findings that larval habitats emit infochemicals that mediate oviposition behaviour of  gravid mosquitoes, larval habitats containing early- or late-stage larvae were placed in containers in the laboratory. Headspace volatiles of the larval microcosm were entrained and analyzed by gas chromatography - mass spectrometry (GC-MS). Analysis of the volatiles emitted by larvae in-vitro led to the identification of 16 compounds, and four of them, when tested with An. gambiae, had an effect on oviposition behaviour (Chapter 4). Volatile chemicals extracted from headspace collections of larvae mediated similar behaviour; volatiles entrapped from young larvae attracted conspecific gravid mosquitoes, whereas those from late-stage larvae deterred conspecific gravid mosquitoes to lay eggs. Nonane and 2,4-pentenedione, which were isolated from headspace collection of larvae, enhanced the attractiveness of a synthetic solution and could be used to increase mosquito egg deposition for monitoring or vector control purposes. Dimethyldisulphide (DMDS) and dimethyltrisulphide (DMTS), which were isolated from headspace collection of late-stage larvae only, decreased mosquito egg deposition in a synthetic solution and may act as a spatial deterrent. Laboratory and semi-field experiments in Tanzania showed similar results and suggested that nonane and 2,4-pentanedione can be used as mid-range cues for oviposition.

    The study described in Chapter 5 provided ecological characteristics of the field site where observations on the behaviour and distribution pattern of larvae were done. This is the field site where initial observations on succession of larvae in breeding sites and the actual testing of infochemicals took place. The factors influencing the selection of breeding sites by gravid females and distribution patterns of mosquito larvae were explored. Human activities such as brick-making and rice production were found to influence oviposition site selection and hence constitute a risk factor for malaria and other mosquito-borne diseases. The presence of larvae of Anopheles mosquitoes in breeding sites was associated with vegetation, presence of culicine larvae, shallowness and sunlight. The association between anopheline and culicine larvae is a vital finding that suggests that gravid mosquitoes of the two species use similar cues in selecting suitable breeding sites. Moreover, results from the study suggested that productivity of anopheline larvae in the field can be reduced by introducing larval predators, water management, or water pollution with rotting vegetation. The findings obtained after careful observation of the field site helped to design surveillance and larval control strategies using synthetic infochemicals identified in Chapter 4.

    Field experiments in east-central Tanzania showed results similar to the laboratory and semi-field studies and suggested that larval habitat volatiles also attract other disease vectors (Chapter 6). This study showed that infochemicals from selected sites can induce an oviposition response in mosquitoes under natural conditions, and that soil from a breeding site and nonane both induced oviposition in An. gambiae and Cx. quinquefasciatus with a synergistic effect caused by nonane + soil in An. gambiae. Therefore, the study also revealed that the oviposition-site-selection process of gravid mosquitoes is mediated by a combination of infochemicals derived from natural breeding sites. This knowledge can be exploited to develop a control strategy based on the push-pull or attract-and-kill concept. Furthermore, the knowledge can be utilized to develop other surveillance tools for mosquito vectors of human and animal diseases.

    In order to explore the potential of using a push-pull system for mosquito control, the attractants were combined with environmentally friendly biolarvicides in order to achieve more effective control of their aquatic larval offspring (Chapter 7). As an attractant for gravid mosquitoes, nonane, which originated from An. gambiae larvae, was selected. As toxicant for mosquito larvae, Bacillus thuringiensis var israeliensis (Bti) and Temephos were selected. Mosquitoes were successfully attracted to lay eggs in water-filled clay pots treated with attractants and combined with larvicides. Therefore, a lure-and-kill system was successfully implemented; mosquitoes were attracted to lay eggs in intervention pots containing toxicants, consequently, all emerged larvae died before reaching the pupal stage.

    The results presented in this thesis create new opportunities for applied research, especially on the development of novel vector-borne disease control strategies using infochemicals (Chapter 8). The volatiles produced by the larval habitats play an important role in the site-selection behaviour of An. gambiae and Cx. quinquefasciatus mosquitoes. The attractiveness of the synthetic chemicals identified in this study may be improved by making blends of attractants or in combination with other infochemicals identified elsewhere. Identified compounds can be used in push-pull and/or lure-and-kill strategies for the manipulation of mosquitoes; thereby reducing the abundance of mosquitoes, the human-biting frequency, and the intensity of pathogen transmission. Research on the role of oviposition-based infochemicals in the site-seeking behaviour of mosquitoes may lead to a better understanding of vector behaviour and contribute to the fight against vector-borne diseases.

    The main conclusions from this thesis can be summarized as follows:

    Volatiles produced by larval habitats play an important role in the mediation of oviposition behaviour of An. gambiae and in the dispersal of mosquito species. The analysis of the headspace from larval microcosms led to the identification of 16 compounds. Out of these, four (DMDS, DMTS, nonane and 2,4-pentanedione) had behavioural effects on An. gambiae. Nonane acts as an oviposition cue for Cx. quinquefasciatus as well. Mosquitoes are governed by multiple cues in the selection of suitable breeding sites, thus further research on the role of combined infochemicals to optimize selection of breeding sites should be initiated. These infochemicals can be used in push-pull or attract–and-kill strategies for surveillance and control of malaria mosquito larvae. Thus, odour-based technologies can improve the surveillance, sampling and control strategies for disease vectors. In this way the burden resulting from mosquito-borne diseases such as morbidity, mortality and economic losses will be decreased.

    Species and sex-specific chemosensory gene expression in Anopheles coluzzii and An. quadriannulatus antennae
    Athrey, Giridhar ; Popkin-Hall, Zachary ; Cosme, Luciano Veiga ; Takken, Willem ; Slotman, Michel Andre - \ 2020
    Parasites & Vectors 13 (2020)1. - ISSN 1756-3305
    Anopheles - Chemosensation - Host seeking - Mating - Olfaction

    Background: Olfactory cues drive mosquito behaviors such as host-seeking, locating sugar sources and oviposition. These behaviors can vary between sexes and closely related species. For example, the malaria vector Anopheles coluzzii is highly anthropophilic, whereas An. quadriannulatus is not. These behavioral differences may be reflected in chemosensory gene expression. Methods: The expression of chemosensory genes in the antennae of both sexes of An. coluzzii and An. quadriannulatus was compared using RNA-seq. The sex-biased expression of several genes in An. coluzzii was also compared using qPCR. Results: The chemosensory expression is mostly similar in the male antennae of An. coluzzii and An. quadriannulatus, with only a few modest differences in expression. A handful of chemosensory genes are male-biased in both species; the highly expressed gustatory receptor AgGr33, odorant binding proteins AgObp25, AgObp26 and possibly AgObp10. Although the chemosensory gene repertoire is mostly shared between the sexes, several highly female-biased AgOrs, AgIrs, and one AgObp were identified, including several whose expression is biased towards the anthropophilic An. coluzzii. Additionally, the expression of several chemosensory genes is biased towards An. coluzzii in both sexes. Conclusions: Chemosensory gene expression is broadly similar between species and sexes, but several sex- biased/specific genes were identified. These may modulate sex- and species-specific behaviors. Although the male behavior of these species remains poorly studied, the identification of sex- and species-specific chemosensory genes may provide fertile ground for future work.[Figure not available: see fulltext.]

    Effect of rodent density on tick and tick-borne pathogen populations: Consequences for infectious disease risk
    Krawczyk, Aleksandra I. ; Duijvendijk, Gilian L.A. Van; Swart, Arno ; Heylen, Dieter ; Jaarsma, Ryanne I. ; Jacobs, Frans H.H. ; Fonville, Manoj ; Sprong, Hein ; Takken, Willem - \ 2020
    Parasites & Vectors 13 (2020)1. - ISSN 1756-3305
    Disease risk - Ixodes ricinus - Rodent density - Tick-borne pathogens - Transmission dynamics

    Background: Rodents are considered to contribute strongly to the risk of tick-borne diseases by feeding Ixodes ricinus larvae and by acting as amplifying hosts for pathogens. Here, we tested to what extent these two processes depend on rodent density, and for which pathogen species rodents synergistically contribute to the local disease risk, i.e. the density of infected nymphs (DIN). Methods: In a natural woodland, we manipulated rodent densities in plots of 2500 m2 by either supplementing a critical food source (acorns) or by removing rodents during two years. Untreated plots were used as controls. Collected nymphs and rodent ear biopsies were tested for the presence of seven tick-borne microorganisms. Linear models were used to capture associations between rodents, nymphs, and pathogens. Results: Investigation of data from all plots, irrespective of the treatment, revealed a strong positive association between rodent density and nymphal density, nymphal infection prevalence (NIP) with Borrelia afzelii and Neoehrlichia mikurensis, and hence DIN's of these pathogens in the following year. The NIP, but not the DIN, of the bird-associated Borrelia garinii, decreased with increasing rodent density. The NIPs of Borrelia miyamotoi and Rickettsia helvetica were independent of rodent density, and increasing rodent density moderately increased the DINs. In addition, NIPs of Babesia microti and Spiroplasma ixodetis decreased with increasing rodent density, which had a non-linear association with DINs of these microorganisms. Conclusions: A positive density dependence for all rodent- A nd tick-associated tick-borne pathogens was found, despite the observation that some of them decreased in prevalence. The effects on the DINs were variable among microorganisms, more than likely due to contrasts in their biology (including transmission modes, host specificity and transmission efficiency). The strongest associations were found in rodent-associated pathogens that most heavily rely on horizontal transmission. Our results draw attention to the importance of considering transmission mode of a pathogen while developing preventative measures to successfully reduce the burden of disease.

    The importance of vector control for the control and elimination of vector-borne diseases
    Wilson, Anne L. ; Courtenay, Orin ; Kelly-Hope, Louise A. ; Scott, Thomas W. ; Takken, Willem ; Torr, Steve J. ; Lindsay, Steve W. - \ 2020
    PLoS Neglected Tropical Diseases 14 (2020)1. - ISSN 1935-2727 - p. e0007831 - e0007831.

    Vector-borne diseases (VBDs) such as malaria, dengue, and leishmaniasis exert a huge burden of morbidity and mortality worldwide, particularly affecting the poorest of the poor. The principal method by which these diseases are controlled is through vector control, which has a long and distinguished history. Vector control, to a greater extent than drugs or vaccines, has been responsible for shrinking the map of many VBDs. Here, we describe the history of vector control programmes worldwide from the late 1800s to date. Pre 1940, vector control relied on a thorough understanding of vector ecology and epidemiology, and implementation of environmental management tailored to the ecology and behaviour of local vector species. This complex understanding was replaced by a simplified dependency on a handful of insecticide-based tools, particularly for malaria control, without an adequate understanding of entomology and epidemiology and without proper monitoring and evaluation. With the rising threat from insecticide-resistant vectors, global environmental change, and the need to incorporate more vector control interventions to eliminate these diseases, we advocate for continued investment in evidence-based vector control. There is a need to return to vector control approaches based on a thorough knowledge of the determinants of pathogen transmission, which utilise a range of insecticide and non-insecticide-based approaches in a locally tailored manner for more effective and sustainable vector control.

    The Influence of Larval Stage and Density on Oviposition Site-Selection Behavior of the Afrotropical Malaria Mosquito Anopheles coluzzii (Diptera: Culicidae)
    Mwingira, Victor ; Spitzen, Jeroen ; Mboera, Leonard E.G. ; Torres-Estrada, José ; Takken, Willem ; Reisen, William - \ 2020
    Journal of Medical Entomology 57 (2020)3. - ISSN 0022-2585 - p. 657 - 666.
    In the selection of oviposition sites female mosquitoes use various cues to assess site quality to optimize survival of progeny. The presence of conspecific larvae influences this process. Interactive effects of oviposition site selection were studied in the malaria mosquito Anopheles coluzzii Coetzee & Wilkerson in dual- and no-choice assays, by exposing single gravid mosquitoes to oviposition cups containing 1) larvae of different developmental stages, 2) larvae-conditioned water (LCW), and 3) cups where visual cues of conspecific larvae were absent. Early-stage conspecific larvae had a positive effect on the oviposition response. By contrast, late stages of conspecific larvae had a negative effect. Oviposition choice was dependent on larval density. Moreover, in oviposition cups where larvae were hidden from view, late-stage larvae had a significant negative effect on oviposition suggesting the involvement of olfactory cues. LCW had no effect on oviposition response, indicating involvement of chemicals produced by larvae in vivo. It is concluded that the presence of larvae in a breeding site affects the oviposition response depending on the development stage of the larvae. These responses appear to be mediated by olfactory cues emitted by the larval habitat containing live larvae, resulting in the enhanced reproductive fitness of the females.
    Attraction of mosquitoes to primate odours and implications for zoonotic Plasmodium transmission
    Bakker, J.W. ; Loy, D.E. ; Takken, W. ; Hahn, B.H. ; Verhulst, N.O. - \ 2020
    Medical and Veterinary Entomology 34 (2020)1. - ISSN 0269-283X - p. 17 - 26.
    Anopheles - bridge vectors - chimpanzee - Congo - mosquito host preference - Plasmodium - transmission dynamics

    Vector-borne diseases often originate from wildlife and can spill over into the human population. One of the most important determinants of vector-borne disease transmission is the host preference of mosquitoes. Mosquitoes with a specialised host preference are guided by body odours to find their hosts in addition to carbon dioxide. Little is known about the role of mosquito host preference in the spillover of pathogenic agents from humans towards animals and vice versa. In the Republic of Congo, the attraction of mosquitoes to primate host odours was determined, as well as their possible role as malaria vectors, using odour-baited traps mimicking the potential hosts of mosquitoes. Most of the mosquito species caught showed a generalistic host preference. Anopheles obscurus was the most abundant Anopheles mosquito, with a generalistic host preference observed from the olfactory response and the detection of various Plasmodium parasites. Interestingly, Culex decens showed a much higher attraction towards chimpanzee odours than to human or cow odours. Human Plasmodium parasites were observed in both human and chimpanzee blood, although not in the Anopheles mosquitoes that were collected. Understanding the role of mosquito host preference for cross-species parasite transmission provides information that will help to determine the risk of spillover of vector-borne diseases.

    Evaluating synthetic odours and trap designs for monitoring Anopheles farauti in Queensland, Australia
    Straat, Bram van de; Hiscox, Alexandra ; Takken, Willem ; Burkot, Thomas R. - \ 2019
    Wageningen University & Research
    Anopheles farauti - Vector surveillance - Synthetic odours - Fan-powered trapping
    Background Monitoring of malaria vectors is important for designing and maintaining effective control interventions as changes in vector-feeding habits can threaten the efficacy of interventions. At present, human landing catches remain the most common method for monitoring malaria vectors of the Anopheles punctulatus complex, including the Anopheles farauti group. The aims of this study were to evaluate the efficacy of different lures and fan-powered traps, including an odour blend that has been demonstrated to be attractive to African anophelines, in Queensland, Australia. Methods To evaluate the performance of different lures in trapping An. farauti in the field, four Suna traps were baited with either: CO2-alone, a synthetic lure (MB5 or BG-Lure) plus CO2, or a human odour plus CO2 and set in the field in Cairns, eastern Australia. A second study evaluated the performance of four traps: a Passive Box trap, BG-Suna trap, BG-Sentinel 2 trap, and BG-Bowl trap, for their ability to trap An. farauti using the best lure from the first experiment. In both experiments, treatments were rotated according to a Latin square design over 16 nights. Trapped mosquitoes were identified on the basis of their morphological features. Results BG-Suna traps baited with CO2 alone, a BG-Lure plus CO2 or a natural human odour plus CO2 captured comparable numbers of An. farauti. However, the number of An. farauti sensu lato captured when the MB5 lure was used with CO2 was three times lower than when the other odour lures were used. The BG-Sentinel 2 trap, BG-Suna trap and BG-Bowl trap all captured high numbers of An. farauti, when baited with CO2 and a BG-Lure. The morphological condition of captured mosquitoes was affected by mechanical damage caused by all fan-powered traps but it was still possible to identify the specimens. Conclusions The BG-Sentinel 2 trap, BG-Suna trap and the BG-Bowl trap captured high numbers of An. farauti in the field, when equipped with CO2 and an odour lure (either the BG-Lure or a natural odour). The most important attractant was CO2. This study shows that fan-powered traps, baited with CO2 plus an appropriate odour lure, can be a promising addition to current vector monitoring methods in the Southwest Pacific.
    Co-Designing a Citizen Science Program for Malaria Control in Rwanda
    Asingizwe, Domina ; Milumbu Murindahabi, Marilyn ; Koenraadt, Constantianus J.M. ; Poortvliet, Marijn ; Vliet, Arnold J.H. Van; Ingabire, Chantal M. ; Hakizimana, Emmanuel ; Mutesa, Leon ; Takken, Willem ; Leeuwis, Cees - \ 2019
    Sustainability 11 (2019)24. - ISSN 2071-1050
    Good health and human wellbeing is one of the sustainable development goals. To achieve this goal, many efforts are required to control infectious diseases including malaria which remains a major public health concern in Rwanda. Surveillance of mosquitoes is critical to control the disease, but surveillance rarely includes the participation of citizens. A citizen science approach (CSA) has been applied for mosquito surveillance in developed countries, but it is unknown whether it is feasible in rural African contexts. In this paper, the technical and social components of such a program are described. Participatory design workshops were conducted in Ruhuha, Rwanda. Community members can decide on the technical tools for collecting and reporting mosquito species, mosquito nuisance, and confirmed malaria cases. Community members set up a social structure to gather observations by nominating representatives to collect the reports and send them to the researchers. These results demonstrate that co-designing a citizen science program (CSP) with citizens allows for decision on what to use in reporting observations. The decisions that the citizens took demonstrated that they have context-specific knowledge and skills, and showed that implementing a CSP in a rural area is feasible. View Full-Text
    Does artemether–lumefantrine administration affect mosquito olfactory behaviour and fitness?
    Boer, Jetske G. de; Busula, Annette Obukosia ; Berge, Jet ten; Dijk, Tessa S. van; Takken, Willem - \ 2019
    Netherlands Institute of Ecology (NIOO-KNAW)
    skin odour - olfaction - host-searching - antimalarial medication - epidemiology - Post-treatment transmission - gametocytes
    Background Artemisinin-based combination therapy (ACT) is the recommended treatment against uncomplicated Plasmodium falciparum infections, and ACT is widely used. It has been shown that gametocytes may be present after ACT and transmission to mosquitoes is still possible. Artemether–lumefantrine (AL) is a broadly used artemisinin-based combination medicine. Here, it is tested whether AL influences behaviour and fitness of Anopheles mosquitoes, which are the main vectors of P. falciparum. Results Dual-choice olfactometer and screenhouse experiments showed that skin odour of healthy human individuals obtained before, during and after AL-administration was equally attractive to Anopheles coluzzii and Anopheles gambiae sensu stricto, apart from a small (but significant) increase in mosquito response to skin odour collected 3 weeks after AL-administration. Anopheles coluzzii females fed on parasite-free blood supplemented with AL or on control-blood had similar survival, time until oviposition and number of eggs produced. Conclusions Based on the results, AL does not appear to influence malaria transmission through modification of vector mosquito olfactory behaviour or fitness. Extending these studies to Plasmodium-infected individuals and malaria mosquitoes with parasites are needed to further support this conclusion.
    Mosquito attractants
    Boer, J.G. de; Robinson, Ailie ; Logan, James G. ; Loon, J.J.A. van; Takken, W. - \ 2019
    Octrooinummer: WO2019186123, gepubliceerd: 2019-12-05.
    A mosquito attractant composition is described comprising heptanal, octanal, nonanal, (E)-2-octenal and (E)-2-decenal. More particularly a composition wherein the compounds are present in the following proportions: nonanal1.00, octanal 0.32 ± 0.16, heptanal 0.06 ± 0.03, (E)-2-octenal 0.04 ± 0.02 and (E)-2-decenal 0.13 ± 0.065.
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