Potential causes and consequences of behavioural resilience and resistance in malaria vector populations: a mathematical modelling analysis

Abstract

Background: The ability of mosquitoes to evade fatal exposure to insecticidal nets and sprays represents the primary obstacle to eliminating malaria. However, it remains unclear which behaviours are most important for buffering mosquito and parasite populations against vector control.

Methods: Simulated life histories were used to compare the impact of alternative feeding behaviour strategies upon overall lifetime feeding success, and upon temporal distributions of successful feeds and biting rates experienced by unprotected humans, in the presence and absence of insecticidal nets. Strictly nocturnal preferred feeding times were contrasted with 1) a wider preference window extending to dawn and dusk, and 2) crepuscular preferences wherein foraging is suppressed when humans sleep and can use nets but is maximal immediately before and after. Simulations with diversion and mortality parameters typical of endophagic, endophilic African vectors, such as Anopheles gambiae and Anopheles funestus, were compared with those for endophagic but exophilic species, such as Anopheles arabiensis, that also enter houses but leave earlier before lethal exposure to insecticide-treated surfaces occurs.

Results: Insecticidal nets were predicted to redistribute successful feeding events to dawn and dusk where these were included in the profile of innately preferred feeding times. However, predicted distributions of biting unprotected humans were unaffected because extended host-seeking activity was redistributed to innately preferred feeding times. Recently observed alterations of biting activity distributions therefore reflect processes not captured in this model, such as evolutionary selection of heritably modified feeding time preferences or phenotypically plastic expression of feeding time preference caused by associative learning. Surprisingly, endophagy combined with exophily, among mosquitoes that enter houses but then feed and/or rest briefly before rapidly exiting, consistently attenuated predicted insecticide impact more than any feeding time preference trait.

Conclusions: Regardless of underlying cause, recent redistributions of host-biting activity to dawn and dusk necessitate new outdoor control strategies. However, persistently indoor-feeding vectors, that evade intradomiciliary insecticide exposure, are at least equally important. Fortunately, recent evaluations of occupied houses or odour-baited stations, with baffled entrances that retain An. arabiensis within insecticide-treated structures, illustrate how endophagic but exophilic vectors may be more effectively tackled using existing insecticides.

Figure 1

A schematic representation of the model structure, processes and equations. Solid arrows represent processes occurring within a single age interval of one hour (a) while dashed arrows represent processes linking one age interval to a later one. See Table 1 for detailed description of the basic input parameter definitions and values, as well as table 2 for the definitions and equations for derived process, state and life history parameters.

Figure 2

Lifetime mean distributions of vector feeding success (F to J), and measurable biting activity upon non-users of long-lasting, insecticidal nets (K to O), as a function of preferred feeding suitability profiles and recruitment time (A to E), as well as evasion of insecticide contact once inside houses (dashed versus solid thin lines) under conditions of host availability estimated for Anopheles arabiensis in rural Tanzania (Table1). The large arrows denote the times at which all mosquitoes were initially recruited to the adult host-seeking population as described in the methods section.

Figure 3

Distributions of vector feeding success (A to E), and measurable biting activity on non-users of long-lasting insecticidal nets (F to J), over the first eight days of life (30 days were simulated but are not presented in the interests of clarity) as a function of preferred feeding suitability profiles, recruitment time and evasion of insecticide contact once inside houses, under conditions of host availability estimated for Anopheles arabiensis in rural Tanzania (Table1).

Figure 4

Vector lifetime total feeding success (A), and measurable biting activity upon non-users of long-lasting insecticidal nets (B), as well the proportion of these totals which occur indoors (C and D, respectively), as a function of preferred feeding suitability profiles, recruitment time and evasion of insecticide contact once inside houses, under conditions of host availability estimated for Anopheles arabiensis in rural Tanzania (Table 1).

Figure 5

Lifetime mean distributions of vector feeding success (A to E and K to O), and measurable biting activity upon non-users of long-lasting insecticidal nets (F to J and P to T), as a function of preferred feeding suitability profiles, recruitment time and evasion of insecticide contact once inside houses, under conditions of lower (×1/3) and higher (×3) host availability, and therefore maximum encounter rates (E_max), than field estimates for Anopheles arabiensis in rural Tanzania (Table 1). The large arrows denote the times at which all mosquitoes were initially recruited to the adult host-seeking population as described in the methods section.

Figure 6

Distributions of vector feeding success (A to E and K to O), and measurable biting activity (F to J and P to T) on non-users of long-lasting insecticidal nets, over the first eight days of life (30 days were simulated but are not presented in the interests of clarity) as a function of preferred feeding suitability profiles, recruitment time and evasion of insecticide contact once inside houses, under conditions of lower (×1/3) and higher (×3) host availability, and therefore maximum encounter rates (E _max ), than field estimates for Anopheles arabiensis in rural Tanzania (Table 1).

Figure 7

Vector lifetime total feeding success (A and C), and measurable biting activity upon non-users of long-lasting insecticide-treated bed nets (B and D), as well the proportion of these totals which occur indoors (E, F, G and H), as a function of preferred feeding suitability profiles, recruitment time and evasion of insecticide contact once inside houses under conditions of lower (×1/3) and higher (×3) host availability and therefore maximum encounter rates (E _max ), than field estimates for Anopheles arabiensis in rural Tanzania (Table 1).