Tsetse flies occur in much of sub-Saharan Africa where they transmit the trypanosomes that cause the diseases of sleeping sickness in humans and nagana in livestock. One of the most economical and effective methods of tsetse control is the use of insecticide-treated screens, called targets, that simulate hosts. Targets have been ~1m2, but recently it was shown that those tsetse that occupy riverine situations, and which are the main vectors of sleeping sickness, respond well to targets only ~0. 06m2. The cheapness of these tiny targets suggests the need to reconsider what intensity and duration of target deployments comprise the most cost-effective strategy in various riverine habitats. A deterministic model, written in Excel spreadsheets and managed by Visual Basic for Applications, simulated the births, deaths and movement of tsetse confined to a strip of riverine vegetation composed of segments of habitat in which the tsetse population was either self-sustaining, or not sustainable unless supplemented by immigrants. Results suggested that in many situations the use of tiny targets at high density for just a few months per year would be the most cost-effective strategy for rapidly reducing tsetse densities by the ~90% expected to have a great impact on the incidence of sleeping sickness. Local elimination of tsetse becomes feasible when targets are deployed in isolated situations, or where the only invasion occurs from populations that are not self-sustaining. Seasonal use of tiny targets deserves field trials. The ability to recognise habitat that contains tsetse populations which are not self-sustaining could improve the planning of all methods of tsetse control, against any species, in riverine, savannah or forest situations. Criteria to assist such recognition are suggested.
Tsetse flies (Glossina spp.) occur in 36 countries of Africa where they transmit species of Trypanosoma which cause the potentially fatal diseases of sleeping sickness in humans and nagana in domestic stock [1,2]. Vector control can be important in managing these diseases [2]. Of the several techniques recommended for this the cheapest and simplest is the use of pyrethroid-treated cattle [3]. However, this technique is applicable only where the numbers and distribution of cattle are adequate, and where the veterinary authorities approve the treatments. In other circumstances it can be cheapest to use insecticide-treated screens of cloth, called targets [4], as an alternative or supplement to cattle baits. For many years the targets that have been employed against tsetse in either riverine, savannah or forest areas have consisted of screens of ~1m2 that are maintained in steady effectiveness for a year or more, through visits every few months to repair or replace damaged or stolen targets and to clear vegetation growth [4]. Recently, however, field experiments [5] and theoretical studies [6] have shown that much smaller targets, of ~0. 06m2, are especially suitable for use against those particular tsetse that are the main vectors of sleeping sickness, i. e. , riverine species such as Glossina fuscipes fuscipes, at least when the flies are occupying their common habitat consisting of strips of woodland bordering rivers or lakes. These tiny targets are convenient to deploy and relatively cheap to manufacture [3], so that they have reinforced the interest in tackling sleeping sickness by vector control [7,8]. They also suggest a need to reconsider several aspects of vector control strategy. First, since the tiny targets are cheap they could be regarded as disposable, so avoiding the costs of retrieving them when the target operation is over. Second, the cheapness could allow the targets to be deployed at increased density, provided control were then so rapid as to be achieved before maintenance visits were required. Such a policy would be best served if the target deployments took place at the start of seasons in which the risk of floods and the degree of vegetation growth were minimal. Third, we need to intensify the debate about whether to aim for local elimination of tsetse, as against the mere reduction of local abundance [3]. Certainly the technical ideal in any locality is to eliminate the flies in a once-off operation, but that requires the tsetse to be isolated naturally in an area small enough to be covered all at once [9,10]. Usually, however, operations must be conducted in large infestations so that only part can be tackled at any one time. In that case, as soon as the control operation is over the treated area can be re-populated by flies invading from adjacent untreated areas. One means of dealing with this problem is to establish artificial barriers to invasion, as exemplified by deploying baits in the invasion route [11,12,13], perhaps as temporary expedients before renewed control operations move into the invasion source [14]. Such barriers are likely to be most effective when tackling tsetse in riverine situations where the linear habitat reduces tsetse mobility [6,15] and ensures that invasion can occur only along the river, not from all directions as commonly happens in large blocks of savannah or forest. However, the cheaper, simpler and quicker our control methods become the less important it is to eradicate tsetse from whole infestations or to maintain perfect and permanent barriers to invasion. Instead, the more appropriate strategy could be to hit the flies in quick local operations that are not expected to eliminate tsetse completely, but which can be repeated readily when the tsetse population recovers to unacceptable densities. The credibility of this strategy is supported by models showing that trypanosomiasis in livestock can be tackled effectively by tsetse control that stops well short of elimination [16], and that the required levels of control to deal with human trypanosomiasis can be even more modest [17,18]. These indications are important because tsetse control is primarily a means of disease prevention, not an end in itself. The readiness with which a suitable level of tsetse control can be achieved will depend on the way that the habitats in or near the operational area affect the natural population dynamics of tsetse. For example, the feasibility of countering invasion will improve if the invasion source is poor habitat that can support only low densities of tsetse, thus reducing the invasion pressure. The invasion problem becomes even less important if the tsetse population in habitats adjacent to the operational area are sustainable only because they are supplemented by flies immigrating from the operational area [19]. The ability to benefit from these matters is likely to be greatest when tsetse are limited to narrow riverine situations. This is because the more restricted the invasion route the greater the chances of locating the operational area where the immediate source of invading flies is relatively poor habitat offering a narrow invasion front [13]. The upshot of all of the above matters is that the planning of the most cost-effective control of tsetse in riverine situations should consider a wide range of options for the intensity, duration, scale and spatial relationships of operations, especially now that the efficacy of tiny targets is recognised. To explore these options we first simulated different sorts of habitat associated with distinctive population dynamics of tsetse. We then modelled the efficacies of various strategies for using targets in a variety of riverine scenarios involving such habitats and different types of invasion problem.
There were no ethical issues since all work was theoretical. The tsetse population was considered to be confined entirely to a narrow strip of riverine habitat although, in accord with field conditions [20], it was allowed that various segments of the strip varied in the suitability of the habitat they provided. The daily abundances of various components of the tsetse population in each 1km-long segment of the strip were tracked deterministically in Microsoft Excel spreadsheets, in essentially the same way as in the Tsetse Muse model, detailed by [21] and available at www. tsetse. org. However, the present model differed from Tsetse Muse in that the death rates that targets imposed on adult tsetse were not always constant but were allowed to vary from day to day, to reflect changes in the efficacy and/or abundance of targets during the control campaign.
To explore various types of poor habitat, each was considered never to degenerate into a seasonal no-go area and was modelled as a strip at least 40km long adjoining end to end with a similarly long strip of good habitat. Isolated populations were considered to be those occurring in places entirely surrounded by a no-go area, or those in the centre of very extensive operations, covering say ≥50km of river so that the centre is ≥25km from any invasion front. In isolated situations it is possible to achieve the ideal of local elimination of tsetse. Hence, in studying such situations most attention was directed at identifying what was needed for the ideal. Whereas the above simulations dealt with operational areas that embraced the whole tsetse population, the next simulations considered operations covering only part of it. In such circumstances it was pertinent to distinguish two sorts of area: (i) the intervention area in which targets were always deployed for at least some of the time and where it was intended to reduce tsetse densities substantially, and (ii) the invasion source which was separated from the intervention area by the invasion front and which might or might not have targets in it to counter the invasion pressure. Additionally, it was pertinent to recognise two main sorts of invasion pressure. First, there is sustained pressure from a source containing a self-sustaining population of tsetse. In this case the continual invasion means that tsetse cannot be eliminated, so that the success of operations must be measured against the 90% level of critical control. Second, there is non-sustained pressure from a source where the population can be maintained only if supplemented by immigration from the intervention area. In this second case the population in the invasion source would decrease when the flies in the intervention area declined, so that treatment of the intervention area alone could eliminate tsetse from that area and the invasion source [19,23]. Thus, with non-sustained invasion it is feasible to adopt local elimination as the criterion for success. With these yardsticks in mind, we explored the relative efficacies of normal steady control and standard seasonal control in operational areas subject to the two types of invasion pressure. The sustained pressure was considered to come from self-sustaining populations in good habitat or poor habitat of type S, in a variety of arrangements. These led to distinctive abundances and distributions of the untreated tsetse population, and complex patterns in the degree of control in space (Fig. 5) and time (Fig. 6). In the above simulations the invasion sources with self-sustaining populations of tsetse were immediately adjacent to the intervention area, so that the intervention area received the full invasion pressure. We explored what happened when the self-sustaining population in the invasion source was separated from the intervention area by poor habitat forming a partial buffer to invasion. Such situations can be produced by fragmented habitats along the length of the river [20,24] In all of the above simulations tsetse always remained in the invasion source and could invade once control stopped, so being able to restore eventually the pre-treatment levels of infestation. The only hope of a permanent end to the invasion problem occurred when the arrangement of poor habitat ensured that the sustainability of the population in any part of the invasion source depended on immigrants that came entirely from the intervention area. With such an arrangement, a year of standard steady control in the good habitat was just sufficient to bring the tsetse population there to its collapse point (Fig. 6, D). Tsetse still remained in the invasion source then (Fig. 6, D), but at a density too low to give an invasion pressure that was sufficiently strong and sustained to re-establish a population in the good habitat. Hence, if all control halted after a year of standard steady control the population density in the 10km on either side of the invasion front dropped naturally to <0. 01% after another 16 months, at which time the tsetse population could not recover even if the poor habitat were improved by, say, an increase in host numbers or an improvement in vegetation. If the poor habitat in the invasion source were worsened by allowing that all death rates there were three times the standard levels, the initial population density in the first 5km of the invasion source was reduced to an average of 8% (range 1–23%) of the density in the first 5km of the good habitat. In this scenario the population in the first 10km of the intervention area dropped to <0. 01% on day 329 of standard steady control and day 123 of standard seasonal control. In the first 10km of the invasion source the population declined to this level on days 247 and 164, respectively. Allowing that overall elimination could not be regarded as achieved until population densities in both the invasion source and the intervention area were reduced beyond possible recovery, the steady control was effective in 11 months and the seasonal control in half that time. Targets used as barriers to invasion are most economical and effective when deployed in the invasion source at densities recommended for tsetse elimination [12]. Hence, in the present work the target deployments intended to simulate barriers were extensions of the deployments in the intervention area.
The present model was basically the same as the Tsetse Muse model that appears to perform well in predicting the impact of control measures against self-sustaining populations of tsetse existing in isolated and non-isolated situations [21]. It is hardly surprising that good predictions of such matters are possible since models can be fed with much reliable detail about the dynamics of self-sustaining populations [22]. The salient features of such dynamics are that the natural daily death rates of adult tsetse cannot exceed about 3% per day and that the rates need to be increased by only about 1% in order to cause a population to expire [28]. For most of the time the actual death rates imposed by control measures are several times greater than this, so swamping any error in the model' s understanding of the natural death rates and their degree of density dependence. Hence, present indications for the effects of steady or seasonal use of targets against naturally self-sustaining populations appear valid. The validity of models is more questionable when simulating the natural sustainability of tsetse in various habitats in the invasion sources since this can depend on relatively slight changes in natural death rates and the patterns and extents to which such changes are modified by density dependence. Nevertheless, the present modelling suggests the various types of natural phenomena and the control results that can occur when populations near the operational area are or are not self-sustaining, without arguing about exactly what levels of natural mortality actually occur in various habitats and at different population densities. In many situations it is likely to be cheaper and more convenient to operate tiny targets seasonally, at high density for a short time, as against the normal use of relatively few targets for extended periods. Hence, seasonal control would be the preferred option provided its efficacy were at least as good as steady control. In general, since the seasonal use of targets imposes the same pattern of mortality as the seasonal spraying of habitat with residual insecticides, the huge successes achieved by such spraying [29,30] enhance greatly the credibility of seasonal targets. Nevertheless, present work shows that the relative efficacy of seasonal as against steady use of targets depends on the aims and location of operations. In operational areas that are free of any invasion, and where the most sensible aim is local elimination, the seasonal control can be advantageous in eliminating the flies in about a third or half of the time required by the normal steady use of targets. This could be particularly advantageous in countering a rapidly growing epidemic of sleeping sickness. Where the operational area is not entirely isolated, seasonal control could be highly beneficial if there were the sort of seasonal isolation in which the entire tsetse population concentrates in the operational area at certain seasons, as was commonly exploited in seasonal spraying campaigns [29,30]. In other cases where the invasion problem is not seasonal it can be feasible to aim for elimination provided the tsetse population in the invasion source is not self-sustaining, but in this case the seasonal work can be disadvantageous in allowing relatively little time for the population in the invasion source to expire. In yet other situations where the invasion pressure is maintained all year round by a self-sustaining population in the invasion source, so that only feasible aim is the partial reduction in tsetse abundance, not elimination, there may be little to choose between the efficacies of seasonal and steady control in respect of the mean reduction of tsetse densities during the year. It is mainly the annual pattern of reduction that differs. Seasonal control gives the greatest initial reduction, but then allows the flies to recover so that at the end of a year the population density is least with steady control. It is only in respect of target barriers that seasonal control seems markedly less effective than steady control. Present simulations show that in choosing the location and aims of operations, and then deciding whether to adopt steady or seasonal deployments, it is important to assess quickly the degree to which various habitats in or near the operational area contain self-sustaining populations of tsetse. Such an ability is especially important since it bears also on the relative feasibility of other control measures that differ in their time frames and potential location, such as steady control by insecticide-treated cattle [31] and seasonal control by various sorts of insecticidal sprays [32]. For example, the fuller consideration of this matter might have avoided the aerial spraying of several thousand square kilometres on the margins of the main infestations in Zimbabwe in the 1980s [32]. In other infestations of the region the populations on the edge were not self-sustaining and needed no direct treatment [19,23]. In some cases a decision on sustainability is easy. For example, any population, even a very sparse one, can be taken as self-sustaining if it has inhabited an isolated habitat for several years with no signs of population decrease or habitat degradation. The more difficult problem occurs when poor habitat with persistent tsetse adjoins other habitat where population densities are much greater, so raising uncertainty as to whether the population of the poor habitat is critically dependent on immigration. Correlations of the presence of tsetse with various habitat features can be of background interest [20,33], but it is more important to understand the dynamics of the tsetse population in various parts of the overall infestation, so explaining why tsetse are present in each place. Unfortunately, the production of suitable data for the births and deaths of tsetse in just one isolated type of habitat is daunting enough [22], so that full investigation of tsetse dynamics, including movement, in several contiguous habitats is beyond reasonable expectation. Against this, present simulations suggest that relatively simple inspection of tsetse catches, to assess the abundance and composition of the tsetse population in different places might offer useful clues. It seems that non-self-sustaining populations could be identified not only by being sparse, but also by showing: (i) densities that decline continuously on moving further from the better habitat, (ii) high mean ages of females and (iii) high proportions of females. It is difficult to find field data to confirm or refute these criteria since there are scant field data for sampling of populations that are known to be non-self-sustaining. Even such data that do exist refer to savannah tsetse that are not confined entirely to riverine habitat. Some of the most useful data are those produced by trapping G. pallidipes at Nguruman, Kenya, where for most of the year the flies are partially restricted to good habitat composed of riverine forest [34] seemingly because the more open habitat further from the river limits the outward diffusion of tsetse by providing reflective contacts. About 10km of the river was treated with traps for a year, at a density sufficient to eliminate the flies if there had been no invasion [11]. However, invasion meant that the flies were not in fact eliminated but showed apparent densities that had roughly stabilized after a year, at around 1–5% of the pre-treatment level. In keeping with current expectations for a non-self-sustaining population that has approached stability, the percent of females in catches was then very high, at about 80%, with increased proportions of old females [11]. Perhaps the greatest problem in using catches to assess the sustainability of tsetse populations is that in many places where the population is suspected of being unable to sustain itself it is difficult to catch enough tsetse for satisfactory studies. However, very low catches suggest a sparse population under severe stress and so offer prima facie evidence for a lack of self sustainability. Thus, while scientific research in such situations should be encouraged as much as possible, most of the demand at present might be for bold action to build up an empirical body of knowledge of what works satisfactorily in various situations. This empirical approach might not be elegant scientifically, but its usefulness has been demonstrated many times in the past, as in helping the evolution of highly effective policies for control by insecticidal sprays [30]. In conclusion, the seasonal use of tiny targets deserves field trials. Whether control is seasonal or steady, involves targets or any other method, and irrespective of what tsetse species is tackled, there could be much benefit in improving our ability to identify populations that are not self-sustaining.
We employed a deterministic model to simulate the efficacy of various ways of using the tiny, ~0. 06m2, insecticide-treated targets recently recommended as replacements for the larger, ~1m2, types previously used to control riverine species of tsetse fly, the main vectors of sleeping sickness in humans. Results suggested that in many situations the use of tiny targets at treble the normal density for a third of the normal time could be the most cost-effective strategy for rapidly reducing or eliminating tsetse populations, so helping with disease control. In deciding whether to aim for local control or elimination, and in planning the operations, it would be highly advantageous to distinguish those parts of the tsetse infestation that support self-sustaining populations, and those containing populations that cannot be sustained unless supplemented by immigrants. Sorts of information that can help to assess the type of sustainability in field habitats are identified. These findings can assist the planning of any method of tsetse control used against any species of tsetse, including those important as vectors of livestock disease.
Optimal Strategies for Controlling Riverine Tsetse Flies Using Targets: A Modelling Study