Influence of human-associated tsetse habitat degradation on tsetse fly (Diptera: Glossinidae) populations and prevalence of infection with trypanosomes in North-Eastern Zambia.

Abstract

African trypanosomiasis is among the most important parasitic diseases of livestock and humans caused by several species of trypanosomes, and the disease occurs in 36 countries in sub-Saharan Africa. Human African Trypanosomiasis (HAT) causes a considerable public health burden on rural populations, and Animal African Trypanosomiasis (AAT) is an important constraint to livestock production and full utilization of land for agricultural production, such that if not controlled the disease can induce important losses through limiting crop production and access to land, and diminishing income from meat, milk and other livestock products, consequently resulting in poverty. In Zambia, approximately 40% of the country’s land is tsetse-infested and the infestation in the Luangwa valley is among the most important with respect to occurrence of both human and animal trypanosomiais. In affected areas, occurrence of trypanosomiasis in humans and in livestock normally correlates with the prevalence of trypanosome infection in tsetse flies. Laboratory studies have shown that among the major factors that affect such trypanosome infection in tsetse flies, is occurrence of stress in tsetse flies. Occurrence of stress in wild tsetse fly populations is associated with unfavourable environmental conditions for the flies, and this is usually a consequence of tsetse habitat degradation. In many parts of Zambia’s eastern tsetse belt, human-associated degradation of the tsetse habitat has been on the increase over the last decades. This suggests that research to determine the effects of such human-associated tsetse habitat degradation, on tsetse populations and prevalence of trypanosome infection in the tsetse population in the area, could provide some insights into the epidemiology of trypanosomiasis in the area. In this study undertaken in three sites, Mpika, Lundazi and Rufunsa sites, in north-eastern Zambia (in parts of the eastern tsetse belt), the objectives were, to determine and measure (i) variation in size, age and hunger stages in tsetse flies and (ii) variation in prevalence of trypanosome infection in the tsetse flies, with increase in distance away from the edge into the inner parts of tsetse belt, and in relation to the distribution of human settlements; and (iii) to detect, assess and evaluate the contribution and importance of existing agricultural and other forms of ecosystem utilization, to tsetse-habitat degradation in the three sites. Three study sites were selected based on level and pattern of human settlement, i.e. Mpika and Rufunsa sites with human settlement concentrated at or close to the edge of the tsetse belt, and Lundazi site with human settlement evenly distributed from the edge into the innermost parts of the tsetse belt. Samples of two species of tsetse flies found in the sample sites, i.e. Glossina morsitans morsitans and G. pallidipes, were collected and (i) size, age and hunger stage in the tsetse flies were recorded and assessed with reference to distance away from the edge of the tsetse belt; (ii) variation in prevalence of trypanosome infection in the tsetse population in the study sites, with reference to distance away from the edge of the tsetse belt, and in relation to distribution of human settlements; and (ii) key land-use and socioeconomic factors in the human settlements, with reference to human-associated tsetse habitat degradation in the study sites. Trapping of the tsetse flies was done in defined sample points, identified with use of a Global Position System (GPS) unit, in the transect line, with use of the Black-screen fly round (BFR) and Epsilon traps. From the sampled flies, the following were recorded; species of fly, sex, body size, age and hunger stage (as indicators of levels of occurrence of stress), and screening for trypanosome infection using microscopy and the loop-mediated isothermal amplification (LAMP). A semi-structured questionnaire was administered in each of the settlements within our study location, and national land cover maps for the years 2000 and 2010, produced by the country’s Forest Department, were used to estimate vegetation cover change during the period 2000 to 2010 in each of the sites. Regression models were applied to determine and measure the level of association of the distance from the edge into the inner parts of the tsetse belt with; size, age and hunger stages of tsetse samples, and prevalence of trypanosome infection in the tsetse flies. In each settlement, data were collected on key land-use and socio-economic factors that may be linked to human-associated habitat degradation and changes in the vegetation cover during the period 2000 and 2010, was calculated in QGIS. The results showed that in the Mpika and Rufunsa sites, the number of Glossina morsitans morsitans tsetse flies caught increased along with the increase in distance from the edge into the inner parts of the tsetse belt. This was also associated with increase in the body size (p < 0.0001 in both sites), and reduction in the age (p < 0.001 in each site) and the hunger stages (p < 0.0001 in both sites), and reduction in the prevalence of trypanosome infection (p = 0.024 and p = 0.012 in the case of all sub-species of trypanosomes tested for in the Mpika and Rufunsa sites respectively; and p = 0.013 and p = 0.025 in the case of only nannomonas sub-species in the two sites, respectively). The level of vegetation cover change was insignificant in each of the sites, such that it was unlikely to have had any significant impact on the quality of the tsetse habitat in each of the sites. In the Mpika and Rufunsa sites, human activities associated with access to resources might have had significant effect on the distribution of wild mammals that served as tsetse hosts in the area, such that numbers (of wild mammals) were low in locations that were close to the settlements and high in locations that were furthest from the settlements – giving rise to a gradient of increasing levels of availability of tsetse hosts with increase in distance away from the human settlements. This same trend was observed with regard to the distribution of body size of the flies, age, hunger stages, and prevalence of nannomonas and trypanozoon trypanosome infection, in G. m. morsitans in the Mpika and Rufunsa sites. This was indication that (in the Mpika and Rufunsa sites) increase in the levels of availability of tsetse hosts was associated with increase in levels of tsetse wellbeing – in turn associated with increase in levels of tsetse habitat quality. With regard to the findings in the Lundazi site (where human settlement was evenly distributed in transect line), the absence of any such variation (in each of the respective attributes in G. m. morsitans) with distance from the edge of the belt, could be taken as supportive to the reason indicated above as the likely basis for the existence of a gradient of reducing levels of tsetse habitat degradation in the Mpika and Rufunsa sites. In the case of G. pallidipes, the results showed no variation in the respective features in the tsetse flies, with increase in distance from the edge of the tsetse belt, and factors such as the relatively fewer numbers of the species caught, and a large proportion of the transect length not having registered any catch of the species, in each site in the study, likely contributed to this outcome.