Consequences of larval competition and exposure to permethrin for the development of the rodent malaria Plasmodium berghei in the mosquito Anopheles gambiae.

BACKGROUND: Mosquitoes and other vectors are often exposed to sublethal doses of insecticides. Larvae can be exposed to the run-off of agricultural use, and adults can be irritated by insecticides used against them and move away before they have picked up a lethal dose. This sublethal exposure may affect the success of control of insect-borne diseases, for it may affect the competence of insects to transmit parasites, in particular if the insects are undernourished. METHODS: We assessed how exposure of larvae and adults to a sublethal dose of permethrin (a pyrethroid) and how larval competition for food affect several aspects of the vector competence of the mosquito Anopheles gambiae for the malaria parasite Plasmodium berghei. We infected mosquitoes with P. berghei and measured the longevity and the prevalence and intensity of infection to test for an effect of our treatments. RESULTS: Our general result was that the exposure to the insecticide helped mosquitoes deal with infection by malaria. Exposure of either larvae or adults decreased the likelihood that mosquitoes were infected by about 20%, but did not effect the parasite load. Exposure also increased the lifespan of infected mosquitoes, but only if they had been reared in competition. Larval competition had no effect on the prevalence of infection, but increased parasite load. These effects may be a consequence of the machinery governing oxidative stress, which underlies the responses of mosquitoes to insecticides, to food stress and to parasites. CONCLUSIONS: We conclude that insecticide residues are likely to affect the ability of mosquitoes to carry and transmit pathogens such as malaria, irrespective of the stage at which they are exposed to the insecticide. Our results stress the need for further studies to consider sublethal doses in the context of vector ecology and vector-borne disease epidemiology.

Larval exposure to a pyrethroid insecticide and competition for food modulate the melanisation and antibacterial responses of adult Anopheles gambiae.

The insecticides we use for agriculture and for vector control often arrive in water bodies, where mosquito larvae may be exposed to them. Not only will they then likely affect the development of the larvae, but their effects may carry over to the adults, potentially affecting their capacity at transmitting infectious diseases. Such an impact may be expected to be more severe when mosquitoes are undernourished. In this study, we investigated whether exposing larvae of the mosquito Anopheles gambiae to a sub-lethal dose of permethrin (a pyrethroid) and forcing them to compete for food would affect the immune response of the adults. We found that a low dose of permethrin increased the degree to which individually reared larvae melanised a negatively charged Sephadex bead and slowed the replication of injected Escherichia coli. However, if mosquitoes had been reared in groups of three (and thus had been forced to compete for food) permethrin had less impact on the efficacy of the immune responses. Our results show how larval stressors can affect the immune response of adults, and that the outcome of exposure to insecticides strongly depends on environmental conditions.

The ability of Anopheles gambiae mosquitoes to bite through a permethrin-treated net and the consequences for their fitness.

Insecticide-treated bed-nets (ITNs) control malaria by keeping mosquitoes from reaching people sleeping under a net and by killing mosquitoes. Most tests of ITNs consider their overall epidemiological outcome without considering the different behaviors underlying their effects. Here we consider one of these behaviors: that mosquitoes can bite through the net if its user is touching it. We assayed the ability of an insecticide-sensitive strain of the mosquito Anopheles gambiae to bite through a permethrin-treated or an untreated net, and their subsequent survival and fecundity. Despite the irritancy of permethrin, 71% of the mosquitoes took blood through the ITN (vs. 99% through the untreated net). The ITN reduced the time spent biting, the blood-meal size and the fecundity, and it killed about 15% of the mosquitoes within 24 hours of feeding (vs. 5% on the untreated net). However, the mosquito's survival was much higher than what we found in WHO cone assays, suggesting that the bloodmeal increased the mosquito's resistance to the insecticide. Thus, our results suggest that the irritancy and the toxicity of ITNs are reduced when mosquitoes contact and feed on their host, which will affect our understanding of the personal and community protection offered by the ITNs.

Malaria load affects the activity of mosquito salivary apyrase.

Mosquitoes infected by sporozoites, the infectious stage of malaria, bite more frequently than uninfected mosquitoes. One of the mechanisms underlying this behavioural change appears to be that the sporozoites decrease the activity of apyrase, an ADP-degrading enzyme that helps the mosquitoes to locate blood. Using the parasite Plasmodium berghei and the mosquito Anopheles gambiae, we confirmed that sporozoite infection alters the host-seeking behaviour of mosquitoes by making them more likely to refeed after a first blood meal, and that apyrase activity is one of the mechanisms of the increased biting persistence and motivation of infectious mosquitoes. We further showed that apyrase activity decreases as the sporozoite load increases, and that mosquitoes with lower apyrase activity take up less blood, making it more likely that they would return to top up their blood meal. Finally, by comparing full-sib families of mosquitoes, we showed that there was genetic variation for apyrase activity, but not for the resistance of parasites to be manipulated. Our results give new insights in understanding how malaria parasites change their hosts to affect their own transmission.

The interaction between permethrin exposure and malaria infection affects the host-seeking behaviour of mosquitoes.

BACKGROUND: Insecticide-treated bed nets (ITNs) help to control malaria by mechanically impeding the biting of mosquitoes, by repelling and irritating them and by killing them. In contrast to spatial repellency, irritancy implies that mosquitoes contact the ITN and are exposed to at least a sub-lethal dose of insecticide, which impedes their further blood-seeking. This would weaken the transmission of malaria, if mosquitoes are infectious. METHODS: It was therefore tested whether sub-lethal exposure to permethrin impedes blood-feeding differently in uninfected mosquitoes and in mosquitoes carrying the non-transmissible stage (oocysts) or the infectious stage (sporozoites) of the malaria parasite Plasmodium berghei. In addition, as the degree of irritancy determines the dose of insecticide the mosquitoes may receive, the irritancy to permethrin of infected and uninfected mosquitoes was compared. RESULTS: In this laboratory setting, sub-lethal exposure to permethrin inhibited the blood-seeking behaviour of Anopheles gambiae mosquitoes for almost 48 h. Although infection by malaria did not affect the irritancy of the mosquitoes to permethrin at either the developmental stage or the infectious stage, both stages of infection shortened the duration of inhibition of blood-seeking. CONCLUSIONS: The results suggest that the impact of ITNs may be weaker for malaria-infected than for uninfected mosquitoes. This will help to understand the global impact of ITNs on the transmission of malaria and gives a more complete picture of the effectiveness of that vector control measure.

Influence of climatic factors on Ixodes ricinus nymph abundance and phenology over a long-term monthly observation in Switzerland (2000-2014).

BACKGROUND: One of the major public health challenges in the field of communicable diseases consists of being able to predict where and when a population is at risk of being infected by a pathogen. In the case of vector-borne diseases, such predictions often require strong ecological knowledge of the vector life-cycle and the environmental conditions promoting or preventing its establishment and maintenance. In this study, we analyse how climatic factors influence the abundance and phenology of the Lyme borreliosis vector Ixodes ricinus in a Swiss temperate forest, based on a long-term monthly observation over a period of 15 years (2000 and 2014). RESULTS: Our results show that questing nymph density significantly decreased during the study period in the sampling area. Although the analyses of climatic variables point out the relative importance of air temperature, relative humidity and saturation deficit on nymph questing activity, the global trends followed by these variables over the study period failed to fully explain the observed decline. However, nymph phenology was additionally explained by the presence of climatic thresholds that limit the questing behaviours of ticks. Most notably, we found that the presumed upper threshold of air saturation deficit, which strongly limits the increase of questing nymph density and is typically reached in the middle of spring, was reached significantly earlier and earlier over years. CONCLUSIONS: In addition to phenology per se, the use of climatic thresholds may help to predict the presence and abundance of questing ticks in Lyme borreliosis endemic areas. Tick sensitivity to temperature or saturation deficit thresholds also suggests that extreme climatic events more than global trends may affect tick population dynamics. These two points may be of high importance in epidemiological short-term as well as long-term predictions. However, the highly unexplained variability in nymph density underlines the need for further studies that include other factors such as tick host abundance or tick microhabitats, two potentially influent factors that were not assessed in the present study.