Chapter 1 General Introduction
1.7 Behavioural Resistance
In Africa, the two most widely used control tools, LLINs and IRS, target mosquitoes that feed indoors at night such as An. gambiae s.s. and An. funestus. Fewer
interventions are designed to counter exophagic and zoophagic mosquitoes such as An. arabiensis. High coverage with LLINs and IRS provides a strong selection pressure for behavioural changes which would reduce mosquito contact with insecticide: earlier biting times, outdoor biting, and zoophagy, which could undermine progress made in malaria control (Lockwood et al., 1984; Govella & Ferguson, 2012; Gatton et al., 2013).
1.7.1 Biting Times
Use of LLINs protects the human population at night when they are sleeping. This intervention exploits the nocturnal biting behaviour of Anopheles mosquitoes (Clements, 1999). However some initial evidence has suggested that An. gambiae s.l. and An. funestus in south-eastern Tanzania may be adapting to high use of indoor control by biting earlier in the evening when nets will not be in use by most people (Russell et al., 2011), presenting an obvious challenge for control. That study did not clarify whether the shift in biting times observed was a result of
changes in behaviour in An. gambiae s.s. or whether vector control has changed the proportions of different sibling species present, selecting for higher proportions of
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An. arabiensis. Comparing recent population surveys against analyses of archived dried specimens and historical data favours the latter explanation as An. gambiae s.s. numbers appear to have decreased relative to An. arabiensis at a similar site in north-eastern Tanzania(Derua et al., 2012). However there is also historic evidence for similar behavioural changes evolving in populations in response to insecticide selection pressure. On islands in the southwest Pacific, Anopheles farauti was found to change its biting times to attack earlier in the evening following widespread use of IRS (Russell et al., 2013). This behaviour was maintained following cessation of IRS which suggests that, rather than responding flexibly to circumstances, thepopulation had undergone genetic selection for earlier biting times. Changes in a species’ behaviour, and/ or an increase in population of species with ‘behaviourally resistant’ characteristics have the potential to maintain residual malaria transmission (Killeen, 2014).
Shifts in biting times have thus far only been recorded in a few sites in sub-Saharan Africa (Russell et al., 2011; Moiroux et al., 2012). Recently some sites have noted Anopheles populations with early biting times that are not typical of the species, but lack historical data to document this as a change from past behaviour (Yohannes & Boelee, 2012; Ojuka et al., 2015). Other studies have not found such changes. A recent survey of six sites in both West and East Africa where LLINs have been in use found that in the majority of cases mosquito activity still peaked late at night when most people are indoors and likely to be protected by LLINs (Huho et al., 2013).
1.7.2 Exophagy and Exophily
One of the first reports of exophily following vector control found increased numbers of An. gambiae resting outdoors following IRS with an organochloride insecticide in Zimbabwe (Muirhead-Thomson, 1960). However this and other studies published after large scale IRS campaigns, lacked sufficient evidence to indicate change, did not distinguish between sibling species and, in some cases, could not exclude the possibility that ‘adaptations’ observed might have resulted from irritant or repellent properties of insecticide used in houses (Muirhead-Thomson, 1960).
Similar problems have also affected more recent data. Huho et al. (2013) found evidence for increased early evening and outdoor biting in An. funestus s.l. populations in Burkina Faso sites (though the same trend was not found in Tanzania, Kenya, or Zambia). Again, this change may result from behavioural adaptation or a change in sibling species composition.
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In both Russell et al. (2011) and Huho et al. (2013), changes to earlier biting times and exophagic behaviour were found to occur together in the same mosquito population, but in other cases such changes were found to be independent. One recent study from western Kenya found that after ten years of LLIN use, there had been some subtle shifts towards outdoor biting in An. arabiensis and An. funestus, but the peak of activity was still late at night when most people would be indoors under insecticide-treated nets (Bayoh et al., 2014).1.7.3 Zoophagy
Highly or entirely anthropophilic vectors can adapt their host preferences when humans are protected from bites (Bøgh et al., 1998; Lefèvre et al., 2009a; Lyimo & Ferguson, 2009). Such a switch could impact on mosquito fitness by reducing fecundity or longevity (Lyimo & Ferguson, 2009; Lyimo et al., 2012, 2013). There is some evidence for host choice changing according to host abundance or following IRS in An. funestus and An. arabiensis, but An. gambiae s.s. appears less flexible in its preferences and therefore more vulnerable to existing control methods (Bruce- Chwatt et al., 1966; Iwashita et al., 2014). Simple models of other insect
populations suggest that behavioural adaptations which avoid insecticide contact will slow the development of physiological resistance, and likewise that a population with physiological resistance will be less likely to develop behavioural resistance (Gould, 1984). However data collected on populations of various insect species has found that physiological and behavioural resistance may occur at the same time, and that traits are sometimes linked, making the relationship between the two adaptations harder to predict (Lockwood et al., 1984).
Independently of behavioural changes, mosquito species such as An. arabiensis which exhibit exophagic and zoophagic tendencies already present a problem for control. Where large scale control programs predominantly use IRS and LLINs, residual malaria transmission may persist as a result of species which are less affected by indoor interventions (Killeen, 2014). In order to decrease malaria transmission to non-self-sustaining levels it will be necessary to use interventions capable of impacting these behaviourally resilient mosquitoes, such as larviciding and odour baited traps (Ferguson et al., 2010; Govella & Ferguson, 2012). Any control strategy which fails to consider mosquito behaviour and behavioural change risks dulled impact, and will be vulnerable to disease rebound if control is not sustained (Ferguson et al., 2010; Killeen, 2014).