Background
The rapid decline of malaria prevalence and parasitaemia in sub-Saharan Africa and many other malaria endemic countries has been noted in the last decade, from a mortality of 2.0 million to 436,000 per year in 2018 [
1‐
3]. This has been mainly associated with wide use of malaria vector control measures, such as long-lasting insecticidal nets (LLINs) and indoor residual spray (IRS) as well as prompt diagnosis and effective treatment using artemisinin-based combination therapy [
3‐
6]. However, the observed decline is faced by challenges of resurgence of residual malaria transmission [
7], which are mainly attributed to changes in malaria vector behaviours [
8], such as avoidance of house entry, diversion from contact with indoor treated surfaces or nets and early exit from houses [
8‐
10]. There is also development of drug resistant in malaria parasites [
11] and insecticide resistance among malaria vectors [
12,
13]. In response to these challenges, the World Health Organization (WHO) is recommending the development and use of complementary measures to further reduce and possibly eliminate malaria [
14]. One of such complementary control measure is the larval source management (LSM) using biolarvicides, which are considered to be relatively safe to human health and the environment [
15,
16].
Bacillus thuringiensis var
israelensis (
Bti) is one of the recommended biolarvicides [
17] and has been proved to be effective for field control of mosquito larvae [
18]. Different formulation of this biolarvicide have been developed and tested in laboratory, semi-fields conditions and fields condition at variable ecological settings [
18]. The
Bacillus thuringiensis var
israelensis biolarvicides based on Bti H-14 serotype, is a water dispersible granular formulation evaluated by the World Health Organization Pesticides Evaluation Scheme (WHOPES) and has been found to be effective for 2–7 days for malaria vectors larvae control in open water bodies and for container breeding mosquitoes (
Aedes aegypti and
Aedes albopictus) for 4–9 weeks [
18].
Bti has been demonstrated to be safe to human, wildlife and other nontargeted organisms [
18]. In general the efficacy of
Bti preparation against malaria vectors larvae depends on the formulation suited to the biology and habitat of the targeted mosquito species [
18]. Field studies in Tanzania have demonstrated the effects of biolarvicides on malaria vectors larvae density [
19], malaria prevalence [
20,
21] and have proved to be the most cost-effective mosquito interventions in rural setting [
22].
Although the WHO emphasizes on integrated vector management (IVM) [
23], targeting both immature and adult mosquitoes, the utilization of LSM have received little attention in malaria endemic countries [
18]. Most of National Malaria Control Programmes (NMCP) in African countries have not implemented this approach. The available reports indicate that 48 malaria-endemic countries worldwide use larval control interventions in only defined foci for malaria transmission, of which only 18 countries are in sub-Saharan Africa [
5]. A number of challenges that hinders the adoption of this approach by most of the NMCP in sub-Saharan Africa have been described elsewhere [
24,
25]. The need for intensive labour forces to reach multiple malaria vectors breeding sites, especially in rural area, high operational costs of this intervention, poor knowledge on methods of implementing and monitoring the intervention, the short residual effect of biolarvicides formulations and small number of public health professional, present significant challenges in implementing this control approach [
24,
25]. To overcome some of these challenges, especially the need for labour-intensive activities to reach multiple malaria breeding sites, integration of biolarvicides (
Bti) and fertilizer application was recommended to rice farmers so that both fertilizer and biolarvicides can be concurrently applied to paddy fields, which coincidentally constitute the largest proportion of malaria vectors breeding sites. The objective of this study was to determine the effect of applying a mixture of biolarvicide and fertilizer on mosquito larvae density and rice grain outputs under semi-field conditions in a rural area of central Tanzania.
Discussion
To achieve malaria elimination goals, the current malaria control approaches needs to be complemented with intervention measures which target the mosquito aquatic stages. The findings indicate that, in general application of biolarvicides as a single product or as a mixture of biolarvicides and fertilizer (DAP/urea) resulted into decline in mosquito larvae density. In comparison to intervention arms, the control arm had the highest mosquito larvae density. These findings noted a significant difference in An. gambiae s.l. larvae abundance between treatment arms with the control arm having the highest abundance. The treatment arm 3, 4 and 5 had the lowest An. gambiae s.l. larvae abundance. This study further assessed the best timing for application of biolarvicide either as a single product or combined with fertilizer and its effects on mosquito larvae density. These findings indicated that application of biolarvicide either as a single product or mixed with fertilizer at every 7 or 10 days had significant impact in reducing mosquito larvae density compared to the arm where biolarvicide and fertilizer were applied following rice farmers schedule for applying fertilizer. These findings indicate further that application of biolarvicide and fertilizer combination had no effect on rice grain harvest.
The findings on the reduction of mosquito larvae density following application of biolarvicides as a single product or mixed with fertilizer on mosquito larvae density are corroborated by previous studies elsewhere in Africa [
17,
30]. In Tanzania, in rice field application of
Bti only or in combination with
Bacillus sphaericus have shown to provide more than 80% reduction of later instars of
Anopheles and
Culex species [
15,
19]. In Western Kenya, application of
Bti and
Bacillus sphaericus biolarvicides in aquatic habitats reduced the proportion of aquatic habitats containing Anopheles larvae from 51% during the no-intervention periods to 7% during the intervention [
15,
30]. The wide distribution of malaria vectors breeding sites in the tropical areas which are created by human activities such as in rice farming present a significant challenge to achieve maximum application of biolarvicides to these areas. To control mosquito density and reduce malaria transmission in rice farming agro-ecosystem, our innovation of mixing biolarvicides with fertilizers and use the farmer’s fertilizer application skills to reach multiple breeding sites in rice farms offers an opportunity to expand this intervention. This field experimental results clearly show that the efficacy of
Bti on mosquito larvae stage is not affected by fertilizer. Thus, it is possible to incorporate the
Bti granules in fertilizer bags at manufacturing stage and distribute a mixed product to rice farmers to apply it in rice fields during farming to control malaria vector density. This in turn, will have impact on incidence of clinical malaria and malaria vectors abundance [
15,
17].
The findings on the best timing for applying biolarvicides either as a single product or in combination with fertilizer revealed that there was no mean difference in mosquito larvae density, especially
An. gambiae s.l. larvae when biolarvicide was applied after every 7 or 10 days. However, when a mixture of biolarvicide and fertilizer was applied following the rice farmer’s schedule (at day 0, 28 and 60), the intervention arm was heavily re-populated by mosquito larvae 7–10 days post-application. This indicates that, the
Bti remained only effective for 7–10 days. Previous studies in East Africa have shown some variation of the effective time period (residual effect) for
Bti in field conditions. In Tanzania, field experiments in rice fields have reported that
Bti remained effective for up to 14 days [
15,
19]. In coastal areas of Kenya [
31,
32] and in field experiments in India
Bti was reported to remain effective for 2–9 days [
33]. Cumulatively, current study results and those of others agree that, the best timing for biolarvicides either as a single product or a mixed product with fertilizer on average is between 7 and 10 days. The low residual effect of
Bti raises the need for re-applying
Bti after every 7–10 days [
17,
30], which present a significant challenge to rice farmers and may affect the performance of the intervention. The invention of the long-lasting biolarvicides formulation that combines
Bti and
Bacillus sphaericus with potential for sustained release of the active ingredients for up to 6 months [
33,
34], present a significant opportunity for the current innovation to be improved and make it more friendly and cost-effective, without the need for rice farmers to re-apply. However, this observation needs to be investigated.
On the other hand, the application of the mixture of
Bti and fertilizer, did not affects the health of paddy plants and productivity of rice grains. These findings on the effects of fertilizer application as measured in terms of mean rice grain harvest per 10 panicles or mean weight per intervention arm was comparable to findings of similar studies in India [
29] and Iran [
35]. These indicate that,
Bti mixed in fertilizer did not affect the efficacy of the fertilizer on plant health and rice grain productivity. On the other hand, the findings in Kenya that
Anopheles arabiensis and
Culex quinquefasciatus have preference to oviposit in fertilizer treated areas [
36] is likely to be useful in the approach of using biolarvicide and fertilizer mixture in the control of mosquitoes. The fertilizer is likely to attract mosquitoes to lay their eggs in biolarvide treated areas, and hence maximize its killing effect.
Conclusion
The findings of this study suggest that, application of Bti as single product or as mixture of Bti and fertilizer at an interval of 7–10 days reduce mosquito larvae density in rice fields. Using this innovation, Bti can be applied in a large area at a very low costs and this in turn will have impact on malaria prevalence while improving rice grain output. Further studies are recommended on the following areas (i) integrate the slow releasing long acting biolarvicides into rice farmer’s fertilizer application skills and assess its effects on malaria transmission indices, (ii) the fact that Bti and fertilizer have different pH range, it is important to understand if the pH of the fertilizer affects the effectiveness of the Bti when the two product are mixed together and stored for long time and (iii) assesses the impact of the innovation in areas with different malaria transmission levels or in areas with wide coverage of other malaria intervention measures, to assess its contribution in reducing clinical malaria, malaria vectors larvae abundance and indoor adult density.
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