Host-seeking behaviour of Anopheles mosquitoes in response to olfactory and visual cue

Abstract

Chapter 18 IntroductionSuccess in malaria vector control in recent years has been attributed largely to the widespread distribution and utilization of long lasting insecticide-treated nets (LLINs) and indoor residual spraying (IRS)(WHO, 2019). The disruption of contact between the human host and the vector remains a very effective mechanism of controlling mosquito-borne diseases when applied in combination with other tools such as effective diagnosis, prevention of mother to child transmission and prompt medical treatment (WHO, 1975; Lindsay et al., 2002; Russell et al., 2011; Bhatt et al., 2015b; WHO, 2019). While LLINs and IRS have contributed to the reduction in malaria disease burden, the widespread emergence of mosquitoes resistant to pyrethroids, the main insecticide group used on LLINs and IRS, and other insecticides threatens the continued success of these tools (Townson et al., 2005; Tanner et al., 2008; Sande et al., 2015; Awolola et al., 2018; Cook et al., 2018; Deletre et al., 2019; WHO, 2019; Hancock et al., 2020). Increased pyrethroid resistance of mosquitoes in malaria endemic areas prompted the modification of formulations used on LLINs to include synergists such as piperonyl butoxide (PBO) that inhibit the enzymes that detoxify insecticides and have increased the effectiveness of existing insecticides (LeClair et al., 2017; Matowo et al., 2017; Gleave et al., 2018; Rakotondranaivo et al., 2018; Birhanu et al., 2019). This solution, however, is considered to be a delay and not a preventive measure to the spread of insecticide resistance, with studies already showing decreasing efficiency of synergist-included insecticide formulations on bed nets (Djouaka et al., 2016; Gleave et al., 2018; Riveron et al., 2019). Another challenge in malaria control is the apparent shift of dominant malaria vector populations from predominantly indoor-biting and resting populations to those that rest and bite outdoors and/or bite earlier in the night when people are not yet protected by LLINs (Antonio-Nkondjio et al., 2006; Moore et al., 2012; Moirouxet al., 2014; Sougoufara et al., 2014; Moshi et al., 2017; Limwagu et al., 2019; Mburu et al., 2019; Sherrard-Smith et al., 2019). This change in vector behaviour is expected to increase the likelihood of receiving an infectious bite during the evening while conducting outdoor activities, before retiring indoors where protection from either LLINs or IRS is present (Killeen, 2014; Mathania et al., 2016; Moshi et al., 2017). Studies have shown that socio-economic activities such as fishing, cooking and harvesting in rural areas are associated with an increased risk of exposure to outdoor malaria transmission (Sande et al., 2015; Moshi et al., 2017; Moshi et al., 2018). The need to identify alternative tools that can be applied promptly towards management of physiologically and behaviourally resistant outdoor-biting mosquitoes is urgent to further reduce malaria incidence (Sangoro et al., 2014a; Sherrard-Smith et al., 2019). Chapter 19Mosquitoes utilize very specific chemical and physical cues when conducting various physiological functions such as mating (Vaníčkováet al., 2017), location of an ideal breeding habitat (Okalet al., 2013; Lindhet al., 2015; Asmareet al., 2017), identification of a plant for sugar feeding (Foster, 2008; Nyasembeet al., 2012; Nyasembeet al., 2018)and the successful location of a host for a blood meal (Takkenet al., 1997; Takkenet al., 1999; Carde, 2015; Liuet al., 2019). Understanding the very complex mechanisms involved in host-seeking (Hawkeset al., 2016; Hawkeset al., 2017)is key to developing tools that manipulate mosquitoes to move away from potential human hosts and on to non-human hosts (Donnellyet al., 2015; Njorogeet al., 2017)or to trap and kill devices that mimic human cues (Takkenet al., 1999;Mukabanaet al., 2002; Qiuet al., 2007; Olangaet al., 2010). Mosquito perception of olfactory cues takes place in receptors located on antennae and maxillary palps which inform the mosquito of the potential availability of the blood meal host prior to utilization of complementary cues of physical nature, i.e.temperature, moisture, and air speed, to guide landing and contact chemical cues perceived upon landing on the skin, in particular tastants, that elicit feeding (Takkenet al., 1999; Turneret al., 2011; Websteret al., 2015; Rajiet al., 2017).Repellents are chemical compounds that have been in use since antiquity to deter biting insects away from humans usually by interfering with the normal perception and response of insects to humans (Charlwood, 2003; Paluchet al., 2010; Maiaet al., 2011; Maiaet al., 2018). Usually applied either topically, on clothes or as volatile or spatial chemicals, repellents provide opportunities for controlling malaria (Wilsonet al., 2014; Maiaet al., 2018). Topical repellents exert their effect on their targets once direct interaction of mosquitoes with treated areas takes place (Norriset al., 2017; Denniset al., 2019)and are characterized as being only slightly volatile which extends their effective action from a treated surface (usually: the skin)(Griecoet al., 2007; Sathantriphopet al., 2014). Insecticide treated clothes have been shown to reduce the risk of malaria by 50% and can provide protection in areas where LLINs cannot be in use such as in disaster areas (Maiaet al., 2018). Volatile or spatial chemicals represent a promising solution in reducing the spread of mosquito-borne disease due to their ability to disrupt normal host-vector interactions within a particular area (Acheeet al., 2012; Sangoroet al., 2014a; Norriset al., 2017; Bowmanet al., 2018; Moshiet al., 2018). Some insecticides have lethal, sub-lethal and excito-repellent properties though the effects of these in vector control are understudied (Chareonviriyaphapet al., 2013). In the face of insecticide resistance, vectors may respond less to toxicity of insecticides due to innate mechanisms that reduce the toxic effects but may still respond to sub-lethal and excito-repellent effects of the same insecticides (Guedeset al., 2017; Cooket al., 2018; Thieventet al., 2019). Sub-lethal concentrations of insecticides present opportunities for application as they reduce host-vector contact even when mosquito populations are Chapter 18Introduction