Impact of natural and anthropogenic factors on the trophic interactions of molluscivores and Schistosoma host snails

Summary With a global disease burden of 240 million infected people, of which 90% live in sub-Saharan Africa, schistosomiasis is one of the most prevalent Neglected Tropical Diseases affecting people in the tropical and sub-tropical regions of the world. Schistosoma parasites are the causative agents of schistosomiasis. They complete their asexual life stages in susceptible aquatic snails while the sexual stages are completed in susceptible mammals including man. Control of this disease is targeted at killing the worms in man through chemotherapy using drug praziquantel or disrupting transmission from snails to humans through provision of improved sanitation and clean water, health education or eliminating of susceptible snails. Praziquantel is effective against adult worms but not against the Schistosomula. Due to this limitation and coupled with presence of contaminated water and susceptible snails transmission of schistosomiasis continues. Therefore snail control is viewed as an essential complementary strategy to chemotherapy. Use of chemicals, environmental modification and biological control methods can eliminate host snails but suitability of any of these methods depend on many considerations of the environmental and socio-economic setting of the target areas. The biological control of schistosomiasis using predator-prey interactions is the subject of this thesis. The main premise of this focus is the fact that schistosomiasis occurs among poor people in poor countries who have limited capacity to avoid contaminated water. Chemicals and environmental management are often expensive and out of reach for affected communities. Given this background this thesis aims to contribute to the body of knowledge on the predator-prey interactions of Schistosoma host snails and their predators, and the factors affecting these interactions. A clear understanding of the factors affecting predator-prey interactions is fundamental in recommending suitable organisms as biocontrol agents in schistosomiasis control programmes. Chapter 2 begins by exploring the potential of host-environment relationships in the control of schistosomiasis in Africa through a literature review. A number of human diseases including schistosomiasis are supported by host-parasite-environment interactions. Schistosoma parasites are transmitted between the snail intermediate hosts and mammalian definitive hosts in an aquatic environment. This host-environment link determines the parasite transmission dynamics and is a route through which control of the transmission can be achieved. Understanding interacting factors determining host snail population dynamics and what control options through the host-environment interface are available was the focus of the review. The main result of the review was that quite a large number of factors, both environmental and socioeconomic, affect the transmission dynamics of schistosomiasis. However, temperature and water flow velocity seem to be the more important environmental factors while occupational and recreational activities are the more significant human factors. Control options through the snail intermediate hosts are done through the use of chemicals, environmental modification and by using competitor or predatory organisms. Given the fact that schistosomiasis is a disease of poverty, it became apparent that sustainable management of the disease would require low cost interventions. Biological control is, therefore, better suited as a complementary strategy to chemotherapy. However, it was apparent from the literature that, there was need to study the effect of natural and human factors on the trophic interactions associated with the biocontrol of host snails. To appreciate the specific factors that may influence the transmission of schistosomiasis in affected communities, two monitoring case studies were conducted in Zambia ( Chapter 3 ). From these case studies, we confirm the importance of site specific investigations because the transmission of schistosomiasis is highly focal and neatly linked to the socioeconomic parameters of the affected community. While, in broad terms, occupational, domestic and recreational activities predispose people to infection, the importance of these factors vary from place to place. From these case studies in Chapter 3 the culture of the communities involved is a significant exposure pathway and influences exposure between gender. For the predominantly cassava growing zone, the processing of cassava exposes females more to contaminated water than males. For the cattle rearing zone on the other hand, pastoralism exposes the males more to contaminated water than females. We also saw that host snails are euryok in nature, being able to adapt to a lot of environmental conditions. In Chapter 4 , we shifted our focus from the field to the lab by studying the potential of alternative predatory organisms. Our aim was to broaden the choice base for candidate predators owing to the fact that many organisms that were reported in chapter 2 have limitations in different situations. For instance, the red swamp crayfish’s burrowing tendencies does not make them suitable for use in aquaculture and water development projects. The cichlids are important and the most available sources of protein for poor people. These are often caught for food and their depletion allows the growth of the host snail populations. We therefore, studied the potential of the red claw crayfish which does not possess the destructive burrowing characteristic and the catfish which on comparative basis is less demanded for than cichlids. Both these species feed on the host snails but their efficiency is compromised by presence of alternative food. However, in suitable conditions they can reduce the populations of host snails. Agriculture is an important activity for the rural communities of sub-Saharan Africa. Therefore pollution of the aquatic bodies by agrochemicals is a common feature. We examined in Chapter 5 the effect of a pesticide on the predator-prey interactions of host snails. The aim was to appreciate how endosulfan may impact on biological control of host snails, hence schistosomiasis. Our findings were that fish are more sensitive to endosulfan toxicity than host snails. We also observed inhibition of predation of snails by catfish at sub-lethal concentrations of endosulfan. Our conclusion is that since the fish are more susceptible to endosulfan toxicity and that endosulfan is found in the field at concentrations known to cause both lethal and sub-lethal reactions, the level of pollution must be taken into consideration when designing control programmes. Finally, I discuss the results of the various studies in Chapter 6. The main conclusion is that identification of suitable predators and understanding the functioning of the predator-prey interactions is important in the biological control of Schistosoma host snails and therewith schistosomiasis transmission. This thesis has contributed to this requirement by outlining i) the role of two alternative organisms as predators of host snails, ii) the effect of alternative prey on the efficiency of the predators and iii) the effect of pesticide pollution on the predator-prey interactions. From these studies, it is recommended that more efforts should be put towards identification of more suitable predators to be used as snail control agents. Additionally, due to the multifaceted nature of the schistosomiasis disease, affected country governments should adopt an interdisciplinary approach towards the control of both the disease and its transmission.