Large-scale use of mosquito larval source management for malaria control in Africa: a cost analysis

Background

At present, large-scale use of two malaria vector control methods, long-lasting insecticidal nets (LLINs) and indoor residual spraying (IRS) is being scaled up in Africa with substantial funding from donors. A third vector control method, larval source management (LSM), has been historically very successful and is today widely used for mosquito control globally, except in Africa. With increasing risk of insecticide resistance and a shift to more exophilic vectors, LSM is now under re-evaluation for use against afro-tropical vector species. Here the costs of this intervention were evaluated.

Methods

The 'ingredients approach' was used to estimate the economic and financial costs per person protected per year (pppy) for large-scale LSM using microbial larvicides in three ecologically diverse settings: (1) the coastal metropolitan area of Dar es Salaam in Tanzania, (2) a highly populated Kenyan highland area (Vihiga District), and (3) a lakeside setting in rural western Kenya (Mbita Division). Two scenarios were examined to investigate the cost implications of using alternative product formulations. Sensitivity analyses on product prices were carried out.

Results

The results show that for programmes using the same granular formulation larviciding costs the least pppy in Dar es Salaam (US$0.94), approximately 60% more in Vihiga District (US$1.50) and the most in Mbita Division (US$2.50). However, these costs are reduced substantially if an alternative water-dispensable formulation is used; in Vihiga, this would reduce costs to US$0.79 and, in Mbita Division, to US$1.94. Larvicide and staff salary costs each accounted for approximately a third of the total economic costs per year. The cost pppy depends mainly on: (1) the type of formulation required for treating different aquatic habitats, (2) the human population density relative to the density of aquatic habitats and (3) the potential to target the intervention in space and/or time.

Conclusion

Costs for LSM compare favourably with costs for IRS and LLINs, especially in areas with moderate and focal malaria transmission where mosquito larval habitats are accessible and well defined. LSM presents an attractive tool to be integrated in ongoing malaria control effort in such settings. Further data on the epidemiological health impact of larviciding is required to establish cost effectiveness.     

Avoidance of occupied hosts by the Hessian fly: oviposition behaviour and consequences for larval survival

Abstract 1. Unoccupied wheat plants and wheat plants occupied by conspecific eggs or larvae were presented to ovipositing female Hessian flies in choice tests.
2. The presence of conspecific eggs on the leaf surfaces of wheat plants did not appear to have any effect on the responses of ovipositing Hessian fly females.
3. The presence of conspecific larvae at the base and nodes of wheat plants for 1, 6, or 11 days had significant effects on Hessian fly oviposition. Eggs oviposited on plants were inversely proportional to larval densities and days of larval occupation.
4. Feeding by Hessian fly larvae is associated with several changes in wheat plants. One of these changes, the growth arrestment of the plant, was measured by recording the heights of plants used in oviposition tests. Plant heights were inversely proportional to both larval densities and days of occupation. Plant heights were directly proportional to eggs oviposited on plants.
5. The consequences of adult female avoidance of plants occupied by conspecific larvae were investigated by allowing females to oviposit on unoccupied plants and 1-day, 6-day, and 11-day larval occupied plants, then scoring at the end of the first larval instar the survival of the offspring that resulted from this oviposition.
6. Survival during the first larval instar was 88% for the offspring of females that oviposited on unoccupied plants, decreasing to 82, 31, and 4% on the 1-day, 6-day, and 11-day occupied plant treatments. On these four plant treatments, a positive correlation was found between larval performance (i.e. survival) and the preferences of ovipositing females.
7. On the four plant treatments, relationships between first-instar larval density and first-instar larval survival varied significantly. On unoccupied plants, survival was inversely proportional to density. On plants oviposited on at 6 days of larval occupation, survival was directly proportional to density.     

Group size in a gregarious tortoise beetle: patterns of oviposition vs. larval behaviour

In laboratory and garden experiments, we tested for the existence of adaptive patterns of oviposition and larval behaviour regarding group size in the gregarious tortoise beetle Chelymorpha varians Blanchard (Coleoptera: Chrysomelidae: Cassidinae) on its host plant Calystegia sepium L. (Convolvulaceae). Specifically, we addressed the following questions: (i) Which is the more frequent egg cluster size? (ii) Does cluster size fully predict larval group size? (iii) Are newborn larvae attracted or repelled to conspecific groupings? and (iv) Which is the group size associated with enhanced larval development and adult mass? We found that the mean cluster size was 21.4 eggs. Egg hatch time was significantly shorter in larger clusters. A regression analysis of larval group size against cluster size showed non‐significant results. Thus, original cluster size did not totally determine the larval group size. The mean larval group size was 17.1. Choice tests in an experimental arena showed that larvae clearly preferred leaves of a host plant rather than moistened papers, and that larvae preferred a small group of conspecifics (four larvae per leaf) over larger groups (12 or 20 larvae). Empty leaves of the host plant showed an intermediate level of preference. Development time and beetle performance (adult mass) were affected by larval group size. Larvae in the smallest group (one per leaf) took four more days to attain adulthood than larvae in the larger groups (12 and 20 larvae). Adult C. varians reared in the 12‐larvae group were significantly larger than those reared at the other densities. Comparison of patterns across experimental groups, excluding the 12‐larvae group, showed a tendency for a greater final mass with slower developmental rate.     

Feeding and indoor resting behaviour of the mosquito Anopheles longipalpis in an area of hyperendemic malaria transmission in southern Zambia

Anopheles longipalpis (Theobald) (Diptera: Culicidae) is a predominantly zoophilic mosquito that has not been implicated in malaria transmission. However, this species was collected indoors with An. funestus s.l. in southern Zambia, where transmission of Plasmodium falciparum is hyperendemic, and we initially misidentified it morphologically and molecularly as An. funestus s.l. The indoor resting density and blood-feeding behaviour of An. longipalpis were investigated during the 2004-05 and 2005-06 transmission seasons in Mufwafwi village in southern Zambia. Numbers of endophilic An. longipalpis increased towards the end of the rainy season. Although specimens were collected during human landing catches, the feeding behaviour of An. longipalpis was significantly biased towards cattle (88.7%), with other bloodmeals originating from dogs, goats and chickens. None of the 177 specimens of An. longipalpis were infected with P. falciparum. These data are consistent with existing reports that An. longipalpis is not involved in malaria transmission. However, more extensive sampling is necessary. Importantly, the correct identification of An. longipalpis is crucial for malaria control programmes in areas where An. funestus s.l and An. longipalpis exist sympatrically so that scarce resources are not wasted on the control of a non-vector.     

The relative importance and distribution of Aedes polynesiensis and Ae.aegypti larval habitats in Samoa

Abstract. In preparation for a Filariasis Control programme in Samoa, during 1978 monthly larval surveys of the vector mosquito Aedes polynesiensis were carried out in four study villages in the main island of Upolu. A more extensive survey of larval habitat distribution was then made in twenty-two villages of Upolu and eighteen of Savai'i island, to determine the importance of habitat types according to their abundance, volume of water and whether their productivity was permanent or seasonal. Ae.aegypti larval densities and habitat distribution were also monitored and the occurrence of predatory Toxorhynchites amboinensis larvae in northern Upolu was recorded from forty-one collections. Aedes Breteau and container indices fluctuated with the pattern of rainfall in two coastal villages and an inland bush village, but not in a coconut plantation community. The five main Aedes larval habitat types encountered were: 200 litre water-storage drums, discarded tins and bottles, coconut shells, automobile tyres and treeholes. Aedes immatures occurred perennially in drums and tree holes, but breeding discontinued in tins, bottles and coconut shells during the driest month of July. For Ae.polynesiensis in Upolu the Breteau and container indices of 104.5 ± SD 80.9 and 35.3 ± 12.4 respectively were significantly higher than those in Savai'i: 33.1 ±25.0 and 24.3 ±20.0 respectively. Likewise for Ae.aegypti the Breteau and container indices of 50.8 ± 32.5 and 23.9 ± 15.6, respectively, were also significantly higher than those in Savai'i: 12.7 ± 17.1 and 9.4 ±13.2 respectively. Habitat types greater or lesser importance were determined by plotting the percentage of each type of container utilized for Aedes breeding against the percentage of each type amongst all larva-positive containers. Ae.polynesiensis preferred tree-holes but not water-storage drums. Ae.aegypti preferred drums and tyres; mixed populations of larvae of both species were commonest in these two types of habitat. Ae.polynesiensis occurred in every village. Ae.aegypti was encountered in all twenty-two villages surveyed in Upolu and nine of eighteen villages in Savai'i. Total larval surveys revealed that drums and tree-holes contained the highest numbers of Aedes larvae. The study provided criteria for planning a control programme.     

The effects of host plant defoliation and fertilizer application on larval growth and oviposition behaviour in cinnabar moth

Summary Defoliated ragwort plants produced regrowth foliage that was higher in alkaloid, but lower in amino acid concentrations than primary foliage. Total N was not affected. 2) Plants fertilized with nitrogen (as ammonium sulphate) had lower amino acid concentrations than unfertilized control plants, slightly increased alkaloid levels but similar total N concentrations. 3) Ovipositing females laid eggs upon plants with equal probability for controls, regrowth and fertilized foliage (one rosette in 5 received an egg batch). However, the probability of receiving eggs was significantly lower on the primary leaves of cut-back plants that had had their lower leaves removed a few days before egg laying (only one rosette in 13 was selected). 4) Egg batch size was higher on fertilized control foliage than on other treatments. 5) Larvae attained greater final weights when fed a diet of regrowth foliage, despite the higher levels of alkaloid they contained. Larval development rate was not affected by experimental treatment of the foliage. 6) Larval growth was lowest on the leaves of fertilized plants. This was associated with significant reductions in the concentrations of three amino acids (methionine down 29%, tyrosine 33% and lysine 25%).     

The effect of water turbidity on the near-surface water temperature of larval habitats of the malaria mosquito <Emphasis Type="Italic">Anopheles gambiae</Emphasis>

Water temperature is an important determinant in many aquatic biological processes, including the growth and development of malaria mosquito (Anopheles arabiensis and A. gambiae) immatures. Water turbidity affects water temperature, as suspended particles in a water column absorb and scatter sunlight and hence determine the extinction of solar radiation. To get a better understanding of the relationship between water turbidity and water temperature, a series of semi-natural larval habitats (diameter 0.32 m, water depth 0.16 m) with increasing water turbidity was created. Here we show that at midday (1300 hours) the upper water layer (thickness of 10 mm) of the water pool with the highest turbidity was on average 2.8°C warmer than the same layer of the clearest water pool. Suspended soil particles increase the water temperature and furthermore change the temperature dynamics of small water collections during daytime, exposing malaria mosquito larvae, which live in the top water layer, longer to higher temperatures.     

Advantages of larval control for African malaria vectors: Low mobility and behavioural responsiveness of immature mosquito stages allow high effective coverage

Background  

Based on sensitivity analysis of the MacDonald-Ross model, it has long been argued that the best way to reduce malaria transmission is to target adult female mosquitoes with insecticides that can reduce the longevity and human-feeding frequency of vectors. However, these analyses have ignored a fundamental biological difference between mosquito adults and the immature stages that precede them: adults are highly mobile flying insects that can readily detect and avoid many intervention measures whereas mosquito eggs, larvae and pupae are confined within relatively small aquatic habitats and cannot readily escape control measures.     

Reduction of oviposition time and enhanced larval feeding: two potential benefits of aggregative oviposition for the viburnum leaf beetle

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The cell biology of malaria infection of mosquito: advances and opportunities

Recent reviews (Feachem et al.; Alonso et al.) have concluded that in order to have a sustainable impact on the global burden of malaria, it is essential that we knowingly reduce the global incidence of infected persons. To achieve this we must reduce the basic reproductive rate of the parasites to < 1 in diverse epidemiological settings. This can be achieved by impacting combinations of the following parameters: the number of mosquitoes relative to the number of persons, the mosquito/human biting rate, the proportion of mosquitoes carrying infectious sporozoites, the daily survival rate of the infectious mosquito and the ability of malaria‐infected persons to infect mosquito vectors. This paper focuses on our understanding of parasite biology underpinning the last of these terms: infection of the mosquito. The article attempts to highlight central issues that require further study to assist in the discovery of useful transmission‐blocking measures.     

The effects of mosquito transmission and population bottlenecking on virulence, multiplication rate and rosetting in rodent malaria

Malaria parasites vary in virulence, but the effects of mosquito transmission on virulence phenotypes have not been systematically analysed. Using six lines of malaria parasite that varied widely in virulence, three of which had been serially blood-stage passaged many times, we found that mosquito transmission led to a general reduction in malaria virulence. Despite that, the between-line variation in virulence remained. Forcing serially passaged lines through extreme population bottlenecks (<5 parasites) reduced virulence in only one of two lines. That reduction was to a level intermediate between that of the virulent parental and avirulent ancestral line. Mosquito transmission did not reverse the increased parasite replication rates that had accrued during serial passage, but it did increase rosetting frequencies. Re-setting of asexual stage genes during the sexual stages of the life cycle, coupled with stochastic sampling of parasites with variable virulence during population bottlenecks, could account for the virulence reductions and increased rosetting induced by mosquito transmission.     

The journey of the malaria parasite in the mosquito: hopes for the new century

In this review, Anil Ghosh, Marten Edwards and Marcelo Jacobs-Lorena follow the journey of the Plasmodium parasite in the mosquito vector. At each developmental step, they highlight some of the major unanswered questions currently challenging cell and molecular biologists. A more thorough understanding of Plasmodium-mosquito interactions might lead to the development of mosquitoes unable to support parasite development.     

Fallen retention aspen trees on clear-cuts can be important habitats for red-listed polypores: a case study in Finland

Green-tree retention is a relatively new forestry application, which aims at decreasing the negative effects of clear-cut logging on forest biodiversity. In this study, the value of retained aspens in maintaining diverse assemblages of wood-decaying fungi (polypores; Basidiomycota) on clear-cuts was investigated, after the retention trees had died, fallen and started to decay. A total of 110 fallen aspen trunks were investigated on clear-cuts and within old-growth forests in eastern Finland, southern boreal zone; and 499 records of polypores belonging to 46 species were made. The intermediately decayed trunks on a clear-cut area hosted more species and more red-listed species than did trunks within forests. Most of the polypore species with more than two records were found in both habitats. These results suggest that many aspen-associated polypores are able to live and reproduce in sun-exposed habitats, if the quality and quantity of dead wood fulfill the species-specific requirements. This unexpected result, however, may be partly due to the exceptionally great abundance of aspen in the study area. Furthermore, in the long term, the local benefits of fallen retention trees can be limited, unless the local continuity of large aspens, both living and dead, is ensured.     

Biting and resting behaviour of anophelines in western Venezuela and implications for control of malaria transmission

A study was conducted in three villages in western Venezuela between February 1988 and October 1989 to determine the biting and resting activity of anophelines in relation to human habits, rainfall and fenitrothion spraying of houses. Mosquitoes were collected landing on humans inside and outside experimental huts throughout the night. Only three mosquitoes were found resting in the huts in the morning, but 2470 were collected resting on vegetation in the early morning. The collections yielded eleven species of anopheline, the most abundant being Anopheles nuneztovari, comprising over 75% of the total anophelines collected, followed by An.triannulatus, An.albitarsis s.l. and An.oswaldoi. The four most abundant species showed different diel patterns of biting. For An.nuneztovari the peak of activity was close to midnight indoors and outdoors, for An.triannulatus between 19.00 and 20.00 hours outdoors, for An.albitarsis mainly before midnight indoors and outdoors and for An.oswaldoi outdoors at 19.00 hours, with an additional smaller peak indoors at midnight. Most of the human population use bednets, go to bed before 22.00 hours and are therefore most exposed to mosquitoes that bite outdoors early in the night. Fenitrothion house-spraying failed to prevent large mosquito populations developing in the wet season, presumably because of their exophilic resting habits. The possible advantages of impregnation of existing bednets with pyrethroids, and provision of nets for people who do not have them, are discussed.     

The vasa regulatory region mediates germline expression and maternal transmission of proteins in the malaria mosquito Anopheles gambiae: a versatile tool for genetic control strategies

Background  

Germline specific promoters are an essential component of potential vector control strategies which function by genetic drive, however suitable promoters are not currently available for the main human malaria vector Anopheles gambiae.     

The importance of an invasive tree fruit as a resource for mosquito larvae

Invasive plants are common and may provide resources through litter for container mosquito larvae. Invasive plant reproductive parts can make up a substantial part of litter but have mostly been ignored as a resource for mosquito larvae. We hypothesized that the reproductive fruits of the invasive eastern red cedar, Juniperus virginiana, provide high quality resources for the invasive, container mosquito Aedes albopictus at the western margin of its invasive range in North America. To test this hypothesis, we performed two laboratory experiments. The first examined the response of individual larvae of Ae. albopictus to different amounts of J. virginiana leaf (fresh and senesced) and J. virginiana fruit (ripe and unripe), as well as to a control leaf (Quercus virginiana, live oak). The second experiment examined the response of different densities of Ae. albopictus larvae to each litter type. We found significant differences in response by individual larvae to different amounts of litter and litter types. We also found J. virginiana litter components could support positive population growth rates as a function of initial larval density where the control leaf could not. We conclude that invasive plants may provide high quality resources, and that the reproductive parts (fruits, flowers, cones) may be an important and overlooked component in provisioning larval habitats. Therefore, the expansion of J. virginiana into grassland areas may contribute to the expansion of Ae. albopictus westward in North America.     

Seasonal profiles of Aedes aegypti (Diptera: Culicidae) larval habitats in an urban area of Costa Rica with a history of mosquito control

Dengue is the most important arboviral disease worldwide and the principal vector-borne disease in Costa Rica. Control of Aedes aegypti populations through source reduction is still considered the most effective way of prevention and control, although it has proven ineffective or unsustainable in many areas with a history of mosquito control. In this study, seasonal profiles and productivity of Aedes aegypti were analyzed in the city of Puntarenas, Costa Rica, where vector control has been practiced for more than ten years. Households contained more than 80% of larval habitats identified, although presence of habitats was more likely in other locations like lots and streets. In the wet season, habitats in the "other" category, like appliances, small manholes, and miscellaneous containers, were the most frequent habitats observed as well as the most common and productive habitats for Ae. aegypti. In the dry season, domestic animal drinking containers were very common, although concrete washtubs contained 79% of Ae. aegypti pupae collected. Individually, non-disposable habitats were as likely or more likely to contain mosquito larvae, and large containers were more likely to harbor mosquito larvae than the small ones only in the dry season. Considering various variables in the logistic regressions, predictors for Ae. aegypti in a habitat were habitat type (p < 0.001), setting (p = 0.043), and disposability (p = 0.022) in the wet season and habitat capacity in the dry season (p = 0.025). Overall, traditional Ae. aegypti larval indices and pupal indices in Puntarenas were high enough to allow viral transmission during the wet season. In spite of continued vector control, it has not been possible to reduce vector densities below threshold levels in Puntarenas, and the habitat profiles show that non-household locations, as well as non-disposable containers, should be targeted in addition to the standard control activities.