24 Dengue Vector Bionomics: Why Aedes Aegypti Is Such a Good Vector
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24 Dengue Vector Bionomics: Why Aedes aegypti is Such a Good Vector Scott A. Ritchie James Cook University, Cairns, Australia Introduction dengue (Gubler, 1998; Lambrechts et al., 2010). What is unique about Ae. aegypti that makes Dengue remains the leading arbovirus cause of it such an effective vector of dengue? morbidity in man. There are 3.6 billion people Ae. aegypti is arguably the most anthropo- living in areas of dengue risk, with an estimated philic mosquito (Tabachnick, 1991). Most of its 390 million infections and 96 million sympto- behavior – from immatures residing within matic cases annually (Beatty et al., 2009, Bhatt man-made, water-holding containers to adult et al., 2013). Dengue is vectored by mosquitoes, females living inside human domains where with several members of the Aedes Stegomyia they feed almost exclusively on human blood – subgenus serving as vectors. For example, Ae. is tightly linked to man. Its high domesticity albopictus is an excellent vector of dengue in truly makes Ae. aegypti the ‘cockroach’ of mosqui- the laboratory, and outbreaks in Hawaii (Effler toes, and contributes greatly to its capacity to et al., 2005) and Taiwan (Lambrechts et al., 2010) vector dengue. This chapter will describe attest to their ability to vector the virus in the Ae. aegypti’s close association with man based on field. Differences in the ability for Ae. albopictus the published scientific literature tempered with to develop disseminated infections of dengue my own personal experience with the mosquito: viruses may explain its lower vector compe- I have lived in an unscreened Queenslander tence status relative to Ae. aegypti (Lambrechts house where Ae. aegypti are encountered al et al., 2010). Ae. scutellaris complex members Ae. most daily, and have directed the dengue con- polynesiensis (Rosen et al., 1954), Ae. katheriensis trol program in north Queensland, Australia for (Leake, 1984) and Ae. scutellaris (Moore et al., Queensland Health from 1994 to 2010. For an 2007) have been shown to be potential vectors excellent discussion of the evolution of anthropo- of dengue virus in the laboratory. Ae. polynesienis phily in mosquitoes, especially the malaria vector is suspected of vectoring outbreaks in French Anopheles gambiae s.s., see Costantini et al. (1999). Polynesia (Rosen et al., 1954), while Ae. hensilli (Savage et al., 1998) and Ae. scutellaris (Mackerras, 1946) have been linked to dengue transmission Adult Behavior in Yap and New Guinea, respectively. However, it is another Aedes (Stegomyia) spp., Ae. aegypti, Blood feeding that is responsible for the bulk of dengue trans- mission worldwide – and is almost exclusively Nearly exclusive blood feeding on humans the vector in large, explosive urban epidemics of drives Ae. aegypti’s role as principal vector © CAB International 2014. Dengue and Dengue Hemorrhagic Fever, 2nd Edition (eds D.J. Gubler et al.) 455 456 S.A. Ritchie of dengue and yellow fever (Lambrechts Thus, female Ae. aegypti have evolved to prefer- et al., 2010). Mosquitoes that feed almost entially feed on the lower limbs and feet, which exclusively on man, such as An. gambiae s.s. are physically farthest away from swatting (Besansky et al., 2004; Lefèvre et al., 2009) and hands. There is evidence that these areas are Ae. aegypti, maintain their respective patho- exceptionally rich in lactic and carboxylic acids gens within a tight, efficient mosquito–man created by bacteria interacting with human transmission cycle (Lambrechts et al., 2010). eccrine sweat, and that these compounds are Blood-meal analysis studies have shown that especially attractive to both An. gambiae s.s Ae. aegypti feeds predominantly on man in and Ae. aegypti in olfactometer experiments Puerto Rico (Scott et al., 2000b), Thailand (Scott (Smallegange et al., 2011). Ae. aegypti are also et al., 1993, 2000b; Ponlawat and Harrington, extremely nervous feeders, alighting at the 2005) and Cairns (Jansen et al., 2009). This slightest movement, only to preferentially selective feeding on human blood, at the attack again (Lenahan and Boreham, 1976). expense of animal blood, plant nectar and fruit Thus, because female Ae. aegypti continue juice, is thought to be associated with greater blood feeding until a nearly full blood meal egg production after imbibing isoleucine- is obtained (Klowden and Lea, 1978), they are poor human blood (Harrington et al., 2001). persistent biters (Canyon et al., 1998) and often Reliance on blood rather than fructose for take several partial blood meals within a house metabolic energy necessitates repeated blood and within a day (Scott et al., 2000a). feeding on an almost daily basis (Scott et al., 2000a; Harrington et al., 2001). This repeated blood feeding on man along with a relatively high daily survival (Reiter, Adult harborage 2007) collectively contributes to the capacity for Ae. aegypti to cause explosive epidemics of Much of the basic key behavioral activities dengue and yellow fever in urban areas. Most of Ae. aegypti take place within or near the mosquitoes have a daily survival of <0.9 per house. Ae. aegypti also preferentially reside, day (Clements and Paterson, 1981). Reiter and are attracted to, buildings where humans (2007) reports on several studies that, using reside (Reiter and Gubler, 1997; Perich et al., the length of the gonotrophic cycle, the time 2000). In an elegant study, Suwonkerd et al. between successive oviposition events, esti- (2006) examined the exit and entry of female mate the daily survival of female Ae. aegypti Ae. aegypti to huts containing humans, a dog and as 0.91 to 0.93. Critically, oviposition, and an unbaited control. Female Ae. aegypti not thus the gonotrophic cycle, is extended over only preferred to enter huts with humans, but several days as females skip oviposit at many they also significantly remained in such huts. sites. This extended gonotrophic cycle math- Within a premise, Ae. aegypti preferentially ematically increases daily survival estimates rest in dark, shady areas (Schoof, 1967). Reiter (Reiter, 2007). By surviving longer, infected and Gubler (1997) describe Ae. aegypti as a females can bite more hosts, transmitting virus furtive, skulking insect that spends much of to a greater number of susceptible humans. its time sequestered in heavily sheltered indoor However, multiple blood feeding and skip refuges that are devoid of air movement. The oviposition may confound measurements of preferential attraction of both male and female the length of the gonotrophic cycle, and thus Ae. aegypti to black, red and dark shades estimates of age in Ae. aegypti. Clearly, more is well known (Muir et al., 1992a,b), and direct methods to measure mosquito age, such likely reflects mosquito attraction to the micro- as proteins and gene expression (Cook et al., climate of dark, shady areas – minimal wind, 2007; Hugo et al., 2010), need further develop- cooler temperatures and high humidity – that ment and refinement. would minimize desiccation to resting insects The intensive biting activity on man (Fig. 24.1). The selective insecticidal spraying exposes female Ae. aegypti to host defensive of dark objects likely to harbor resting Ae. aegypti behavior such as swats and slaps as the host has been used to successfully control Ae. aegypti attempts to kill or disperse the attacking female. and stop dengue transmission (Ritchie et al., 2002; Dengue Vector Bionomics 457 (A) Outdoors Bathroom Lounge Indoors 32 30 C) ∞ ( 28 26 24 emperature 22 20 11th 12th 13th 14th Outdoors (B) Bathroom Lounge Indoors 100 )T 90 80 e humidity (% 70 60 Relativ 50 11th 12th 13th 14th Fig. 24.1. Microclimates within a ‘Queenslander house’. Data logger readings were taken with an Esis Hygrocon DS1923 (Esis Pty Ltd, PO Box 450, Pennant Hills NSW 1715, Australia) at height of 0.3 m; relative humidity readings were capped at 95%. (A) Recordings of temperature and (B) relative humidity were made within a ground floor bathroom on 11–12 November 2007 and adjacent downstairs lounge room on 13–14 November 2007. Outdoor readings were taken in undercover ground floor area within 1 m of the house. The bathroom was dark and poorly ventilated, with a porous tile floor that absorbed moisture, increasing humidity while reducing temperature fluctuations. Such dark, still locations minimize desiccation and are sought out by adult Ae. aegypti for harborage sites. Vazquez-Prokopec et al., 2010). Male Ae. aegypti and oviposition sites. This is in contrast to aggregate on dark objects inside premises dispersal behavior exhibited by many other (Reiter and Gubler, 1997), and are also at mosquitoes, some of which are renowned for tracted to humans where they may intercept long-distance flight and migration. The primary and copulate with females (Hartberg, 1971). saltmarsh mosquitoes of Florida and Australia, They may also encounter females at other Ae. taeniorhynchus (Ritchie and Montague, domestic locations including oviposition sites 1995; Vlach et al., 2006) and Ae. vigilax (Ritchie, and resting sites (Hartberg, 1971; Ponlawat and 1993), respectively, engage in long dispersive Harrington, 2009). flights of up to tens of kilometers from their larval habitat. The Japanese encephalitis vec- tors Culex tritaeniorhynchus and Cx. annuliro- Adult flight behavior stris are also known to fly, at height, over considerable distances (van den Hurk et al., Ae. aegypti flight behavior ensures that they 2009). However, Ae. aegypti typically fly only remain close to humans and, literally, proxi- a few hundred meters, often less (Harrington mal to blood-meal sources, harborage areas et al., 2005; Russell et al., 2005). This ensures 458 S.A. Ritchie that they stay near human habitats, facilitating distances than normal. Furthermore, Bellini house-to-house flights in search of blood-meal et al. (2010) found that male Ae. albopictus dusted or oviposition sites, where they may aggregate with fluorescent powders had significantly (Edman et al., 1998). Furthermore, low-level reduced recovery and distance travelled com- flight prevents the adult mosquito from pa red to undusted male Ae.