Characterization of mosquito community assemblages and vector species ecology to inform control interventions at hotel settings in Zanzibar

Abstract

Zanzibar archipelago has made significant advances in reducing the burden of mosquito-borne diseases (MBDs). However, the archipelago is still affected by residual foci of malaria outbreaks two decades after being declared a near elimination region. Widespread physiological and behavioural resistance in the vector populations is one of the main causes of postponed malaria elimination in the region. In addition, an increasing body of hospital surveys suggest that life-threatening mosquito-borne viral diseases, notably dengue and chikungunya, are being transmitted silently among foreigners and Zanzibar residents. These findings corroborate previous studies pointing to a higher risk of re-emergence of mosquito-borne viral outbreaks in Zanzibar. Rapid demographic growth coupled with high connectivity between Zanzibar and other endemic regions may exacerbate the risk of explosive epidemics with detrimental impact on the Zanzibar economy and health system. The tourism industry is among the main driving factors of economic and demographic growth of Zanzibar. However, evidence has shown that tourism activities also create the landscape for emergence of MBD outbreaks either by the introduction of infected hosts and vectors, or by causing environmental changes, notably accumulation of solid waste that is conducive to proliferation of mosquito vectors and, eventually, pathogen transmission. The human-mediated introduction of pathogens via tourism has the potential to trigger epidemics of novel MBDs with devastating economic consequences, as observed in other tourism-dependent economies. Therefore, understanding the extent to which tourism associated activities represent a risk of MBD epidemics in Zanzibar is crucial for the design and implementation of measures that reduce the tension between tourism promoted economic growth and risk of MBD epidemics. As such, the works comprising this thesis results from a long quest to identify and characterize tourism associated foci of potential MBD epidemic risks in Zanzibar and use the produced knowledge to design a framework for hotel-based risk assessment and evaluation of innovative approaches for larval sources reduction. This thesis comprises six chapters. In introductory Chapter 1 the global situation of MBDs, and determinants of transmission and expansion are reviewed. Relevant ecological aspects of three major mosquito vector taxa from the standpoint of pathogen transmission are also presented. In addition, traditional and innovative vector control measures are summarized. This chapter ends with updated information about MBDs in Zanzibar and discusses potential links between tourism activities and MBD risk in Zanzibar. In Chapter 2 the structure and environmental correlates of mosquito community assemblages at hotels and the degree of vulnerability to mosquito larval habitat removal is reported. The findings demonstrate that hotels in Zanzibar provide a suitable environment for production and maintenance of highly important mosquito vector species. Analysis of mosquito community vulnerabilities to systematic loss of larval habitats indicates that community assemblages can be rapidly disrupted by removal of larval habitats sustaining high species diversity. In Chapter 3, investigations were focused on Aedes mosquito taxa to characterize local environment associated drivers of Aedes mosquito occurrence and abundance, with emphasis on the vector species Ae. aegypti and Ae. bormeliae. The findings show that the main sources of these two vectors are improperly disposed small and medium sized plastic containers, and containers used in gardening tasks. Furthermore, open spaces, gardens and residential areas for hotel staff are associated with higher abundance of vector species. The status of insecticide susceptibility in Ae. aegypti, the most dominant vector species identified at the hotels is reported in Chapter 4. An overview of mosquito control practices at the hotels indicate that the key mosquito control practices have been residual spraying and open spaces fumigation with insecticides of the classes pyrethroids, carbamates and organophosphates. The findings indicate that the phenotypic resistance to DDT (all hotels) and deltamethrin (some hotels) observed in Ae. aegypti does not align with the limited presence of kdr mutations, as gene allele V1016G was found in only five of 541 specimens analysed. These findings open avenues for further investigations into causes of DDT/deltamethrin resistance and consequences of an emerging V1016G mutation in the Ae. aegypti population of Zanzibar. In Chapter 5 a framework for evaluating the impact of larval source reduction when used as an intervention against mosquitoes at hotel compounds is proposed. A summarising discussion and conclusion are presented in Chapter 6. This thesis increases our knowledge on the ecology of mosquito vectors in Zanzibar and reveals how the archipelago may act as a potential epicentre of future mosquito-borne viral diseases epidemics in the region. It also provides a basis for designing comprehensive mosquito vector surveillance and emerging epidemic risk assessment in Zanzibar.