Population composition and seasonal dynamics of mosquito communities across landscape gradients in southern Africa, with emphasis on selected arbovirus vector species and their role in disease transmission

Abstract

Mosquito-borne arboviruses are of considerable public health importance as they cause some of the most important emerging and re-emerging infectious diseases affecting humans and animals in many parts of the world including southern Africa. The threat of large epidemics of mosquito-borne arboviruses are often associated with climatic conditions, global warming, animal migrations, surface water, wind, topography, harbourage, vegetation, food supply and abundance of competent mosquito vectors. The goal of this project is to provide an in depth understanding of mosquito community dynamics and the importance of mosquito vector populations in the maintenance and transmission of mosquito-borne diseases in southern Africa.

Firstly, a review of past and current literature was conducted to highlight: (a) the current state of knowledge regarding the most important mosquito-borne viruses of medical significance in southern Africa (b) lesser known mosquito-borne arboviruses with the potential of causing zoonotic health threats for humans in southern Africa. (c) key aspects of the ecology of mosquito vectors of medically significant mosquito-borne viruses in southern Africa. d) gaps in knowledge regarding southern African arbovirus mosquito vectors. Most of the studies on mosquito-borne viruses in southern Africa can be clustered into specific programmes led by Kokernot and Smithburn in the 1950s, McIntosh in the 1970s and 1980s, Swanepoel in the 1970s, Venter and others in more recent years, and have largely been restricted to South Africa, Mozambique and Zimbabwe. Twenty-six (26) arboviruses have been isolated from mosquitoes in southern Africa. Of these, Chikungunya (CHIK), Sindbis (SIN), West Nile (WN), Wesselsbron (WES), Spondweni (SPO), Banzi (BAN), Dengue (DEN), Bunyamwera (BUN), Germiston (GER) and Rift Valley fever (RVF) viruses are known to cause human illness. Middelburg (MID) and Shuni (SHUN) viruses are also important, causing neurological symptoms in animals with zoonotic potential for humans in South Africa. There are eight mosquito-borne arboviral infections most likely to impact humans in southern Africa (CHIK, MID, SIN, DEN, WES, WN, SHUN and RVF viruses). Mosquitoes in the subfamily Culicinae (mostly Aedes and Culex mosquitoes) are the most frequently associated with arbovirus transmission (115 and 105 types of arbovirus, respectively). Understanding the role of mosquito vector species in arbovirus transmission is vital for the development of new strategies to control the spread of arboviral diseases. In southern Africa, a few species in the genera Anopheles, Coquillettidia and Mansonia have also been implicated as vectors of arboviruses. Surveys over multiple decades across southern Africa have provided an insight regarding which species of mosquitoes are involved in the transmission of at least the most common of the mosquito-borne zoonotic arboviruses. These cluster within the genera Aedes and Culex, each representing a different transmission strategy. Aedes-borne viruses such as CHIK, DEN and WES tend to have primate or human reservoir hosts (McIntosh, 1986), while Culex-borne viruses often use birds as reservoir hosts, and these factors influence the distribution and epidemiology of the diseases they cause in humans and animals. Aedes and Culex have different breeding strategies and preferences which also represent fundamental differences. These mosquitoes are Aedes aegypti, Aedes furcifer/cordellieri, Aedes circumluteolus, Aedes unidentatus, Aedes mcintoshi, Aedes caballus, Aedes juppi, Culex theileri, Culex zombaensis, Culex univittatus, Culex neavei and Culex rubinotus.

To determine mosquito community dynamics and mosquito vector distributions, sampling mosquito vectors at six sentinel sites in three provinces in the northern part of South Africa where recent cases had been detected in animals. Adult mosquitoes were collected from two horse properties in Gauteng Province; two wildlife reserves in Limpopo Province and at Orpen Gate in Kruger National Park and Mnisi Area in Mpumalanga Province between 2014–2017, using carbon dioxide-baited light and tent traps. Culex poicilipes, was the most abundant species caught during the study period. Highest diversity and species richness were found at Lapalala Wilderness Reserve, while the lowest diversity and abundances were at Orpen in Kruger National Park. Aedes aegypti, Ae. mcintoshi, Ae. metallicus, Ae. vittatus, Cx. pipiens sensu lato, Cx. theileri and Cx. univittatus, which are potential arbovirus vectors, had the widest geographical distribution in northern South Africa. Also collected were Anopheles arabiensis and An. vaneedeni, both known malaria vectors in South Africa. Therefore, arbovirus surveillance and vector control programs should be augmented in peri-urban and mixed rural settings where there is greater risk for arbovirus transmission to humans and domestic stock.

Since climate has reportedly been associated with disease transmission, it’s important to understand the extent of its influence on mosquito abundance and distribution in northern South Africa. Thus, population composition, abundance and diversity of mosquitoes collected over a three-year period were determined and correlated to diverse climatic conditions during those years in order to determine seasonal trends in occurrence, abundance and distribution. Marked differences in the temporal distribution and seasonal abundances of the seven medically important mosquito vectors encountered from the two distinct geographic regions and climates. Statistical models have shown that climatic factors play a crucial role in shaping the population dynamics of Ae. mcintoshi, Ae. vittatus, An. arabiensis, Cx. pipiens s.l., Cx. poicilipes, Cx. theileri and Cx. univittatus both in Highveld Grassland and Middleveld Bushveld regions of northern South Africa. High summer temperatures and rainfall lead to increased vector density which might trigger outbreaks of RVF, SIN and WN viruses on the inland plateau of South Africa. This study also showed that abundances of RVF and WN virus vectors are related to elevation. These findings will be important in predicting the timing of onset and spread of future epidemics such as WN and RVF viruses, in southern Africa and other geographical settings with similar climates.