Background
Throughout the Southwest Pacific region where malaria occurs, one of the primary vectors is
Anopheles farauti [
1]. It has a wide distribution, being found from the Moluccas (Indonesia) in the west, throughout Papua New Guinea (PNG), Solomon Islands, Vanuatu and northern Australia.
Anopheles farauti is a coastal species rarely found more than 5 km from the coast with brackish swamps being the preferred oviposition site, although it is commonly found in fresh water sites [
2].
With regard to malaria transmission,
An. farauti has a reputation for being difficult to control in the Solomon Islands using the traditional malaria vector control methods of indoor residual spraying (IRS) [
3‐
5] and insecticide-treated nets (ITNs). The feeding behaviour of this species, documented by several studies before the introduction of DDT IRS, shows
An. farauti starting to feed at dusk and progressing to a peak around midnight: in the D’Entrecasteaux Islands (PNG) [
6], New Britain (PNG) [
7] and the Solomon Islands [
8,
9]. Following the introduction of DDT IRS into PNG and the Solomon Islands during the 1960s and 1970s,
An. farauti shifted its peak biting time forward to between 18.00 and 20.00 h. In New Britain (PNG), after five spray cycles (across two years) with DDT IRS, there was a distinct shift in the peak biting time from the middle part of the night to between 18.00 and 19.00, with 76% of feeding occurring before 21.00 [
7]. Similar studies in the Solomon Islands also saw a shift in biting activity moving from midnight to an early night peak followed by a second peak just before sunrise [
8,
9].
More recent studies in the Solomon Islands confirm the early night biting peak occurring before 21.00 remains in these populations despite the cessation of DDT spraying in the 1980s [
5,
10]. The lack of a reversion to the original phenotype of biting through the night after the IRS selection pressure ended is interesting as there would be populations of
An. farauti extant on the islands where malaria control activities did not take place. However, a possible reversion did occur on Buka Island (PNG) where 19 years after the DDT IRS control campaign (1961–1980) ceased, the
An. farauti population exhibited a peak biting time of 00.00–01.00 [
11,
12].
Molecular identification methods suggest
An. farauti in the Solomon Islands to be a single species [
4,
13,
14], and so it remains unclear why these populations would not revert back to an original feeding phenotype after the Global Eradication Campaign in the 1970s in the Solomon Islands, but could possibly be attributed the strong selection on small island populations. More recent use of long-lasting insecticidal nets (LLINs) has likely reinforced this early evening biting behaviour [
10,
15]. A better understanding of the feeding behaviour of
An. farauti in malaria control naive populations may shed some light on this phenomenon.
Despite the use of LLINs in the Southwest Pacific, malaria has been increasing since 2015 with the largest increases seen in the Solomon Islands [
16]. Communities in PNG and the Solomon Islands spend much of the early part of the night outdoors [
15,
17], and
An. farauti, by feeding early, can obtain a bloodmeal without entering houses. Thus, these shifts in peak feeding suggest changes in mosquito biting behaviour to avoid the insecticide, resulting in uncontrolled outdoor malaria transmission. Additionally, day time biting has been recorded with
An. farauti [
18,
19] using collections from 07.00 to 10.00 [
19]; although the numbers collected were small, no specific attempt was made to assess day time biting activity during these early studies.
Unlike PNG and the Solomon Islands, malaria on mainland Australia is not a serious problem [
20]. Thus, DDT IRS was never employed for malaria control and anophelines in Australia have not encountered sustained indoor insecticide selection pressures.
Anopheles farauti is thought to be the main vector of malaria in Australia [
21], with the last outbreak by this mosquito being
Plasmodium vivax in 2002 [
22]. The host-seeking behaviour and night-biting profile of this species in Australia is not well understood. Additionally, there are other aspects of the host-seeking behaviour of
An. farauti that have not been studied in any part of its range, such as the exact time host seeking commences and then ceases. Traditionally, human landing catches (HLC) commence at 18.00 and finish at 06.00, but does host seeking occur before and after these times? What triggers this host-seeking behaviour, does the relationship between light intensity and times of biting in relation to sunset and sunrise have an effect? There are limited studies to date that has explored how light can affect biting behaviour. Also, what effect does temperature and humidity have on host seeking?
The aim of this study is to determine the biting profile of a population of An. farauti that has not encountered indoor malaria-control based insecticide treatments. It was hypothesized that the populations in north Queensland will show host-seeking activities throughout the night with a peak around midnight as has been found in other An. farauti populations prior to indoor insecticide pressure.
Discussion
Accurate knowledge of the biting profile or the night biting profile of malaria vectors is important as the two main control strategies currently used against malaria vectors remain controlling the host-seeking females with IRS and LLINs. For these measures to be effective, the vector should be seeking a bloodmeal when humans are either indoors and/or under an ITN. Under these conditions the vector should come into contact with the insecticide, either on the walls or the net and die. If the vector feeds before this time, it will likely feed outdoors and avoid contact with insecticide and outdoor transmission will continue despite the intervention measures.
This study of
An. farauti at CBTA was carried out over four years in both wet (April) and dry (October) seasons. The night biting profile of this
An. farauti population, which has not been subjected to IRS or ITNs appears to show a similar biting profile to other population that were subjected to insecticidal pressure IRS or ITNs [
5,
7,
32]., When more extreme ambient temperature is considered, a decreasing temperature below 18 °C through the night reduces biting activity with most activity limited to the warmer early evening window. On warmer nights (above 25 °C), where the temperature is constant, biting appears to occur through the night, similar to other populations in the region that had not been subjected to indoor insecticidal pressure, as in pre-spray PNG [
12,
19,
33] and the Solomon Islands [
8,
32]. In this, the mean temperature in the equatorial coastal lowlands of PNG and the Solomon Islands is around ~ 25 °C (min 22 °C-max 31 °C) [
34] and biting activity does not usually occur at temperatures below 20 °C. The observation in Queensland, a population at a higher latitude and thus encountering a broader temperature fluctuation, sees the first record of a relationship between a reduction in the biting activity of
An. farauti and decreasing temperature during the night. Mosquitoes are ectotherms and metabolism is dictated by ambient temperature [
35,
36], with tropical mosquitoes sensitive to lower ambient temperatures affecting flight and biting activity. Temperature and biting activity studies on another tropical mosquito also found in Queensland, Australia,
Aedes aegypti, suggests biting activity decreases and can even stop at between 15 °C and 18 °C [
37] and may help understand the biting profile of
An. farauti on these cooler nights.
Anopheles farauti shows a tight coastal distribution with the ability to utilize both brackish and fresh water larval sites [
2,
38]. This mosquito can display higher population densities during the dry season as observed in studies in the Solomon Islands [
10,
39]. Also seen is a similar seasonal influence in the CBTA study site, where adult productivity is higher during the dry season and this pattern is probably due to larvae being flushed out to the sea by heavy tropical rainfall during the wet season.
Ecological niche modelling of
An. farauti in Australia found a strong correlation between parameters of temperature (i.e., minimum, diurnal, seasonal and annual temperature range as well as sea temperature), which, apart from sea temperature, are moderated along the coast by the sea temperature [
40]. The observed decrease in female host-seeking activity with cooler ambient temperatures complements a similar finding [
40], that these environmental parameters may help define the range for
An. farauti and may prevent the species moving inland where larger temperature variation would be encountered, although temperature fluctuations decrease in more equatorial regions.
The tight feeding timing consistency appears more tied to a 24-h clock rather than light intensity and complements the findings of Duffield et al. [
41], in that
An. farauti daily nocturnal flight activity is underpinned by the circadian clock—a research area in mosquitoes now beginning to unfold with new genomic and transcriptomic tools available [
42‐
45].
Conclusion
Anopheles farauti is one of the most important malaria vectors in the Southwest Pacific and has shown consistent behavioural resistance to indoor malaria control strategies such as IRS and ITNs, with populations moving to earlier evening biting under this selection pressure.
This population displays biting time plasticity with early biting preference observable when night temperature drops below 18 °C to biting through the night on warmer nights that maintain temperatures above 25 °C. It would be interesting to consider how this feeding time plasticity is controlled and if there is any connection with observed behavioural insecticide resistance in this malaria vector.
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