Malaria Vectors of Madagascar

Anopheles arabiensis – Secondary Vector


Anopheles arabiensis is the most widespread malaria vector in Madagascar, likely owing to their tolerance for arid temperatures, ability to live at higher altitudes, and capacity to breed extensively in rice fields (Simard, 1999; Duchemin, 2001; Antonio-Nkondjio, 2006). Despite its ubiquity, An. arabiensis is considered a secondary vector across the island (Duchemin, 2001; Le Goff, 2003). In addition to Plasmodium, this species is found infected with Bwamba virus, Ganjam virus, Ilesha virus, Mengo virus, O’nyong-nyong virus, and Tataguine virus (Cordellier, 1976; Cornet, 1979; Fontenille, 1989; Gordon, 1992; Vanlandingham, 2005). Anopheles arabiensis is more abundant than An. gambiae s.s. in the central highlands (Pock Tsy, 2003; Tantely, 2012), possibly due to the differential effects of IRS and ITNs on these two species. These mosquito control strategies are most effective for the endophilic/endophagic An. gambiae s.s., with negligible impacts for the exophilic/exophagic An. arabiensis (Bayoh, 2010; Gatton, 2013).  Densities for this species peak in March, coinciding with peak densities of An. gambiae s.s. (Andrianaivolambo, 2010). Spikes in An. arabiensis usually result in lower parity, potentially mitigating the effects of high vector density (Marrama, 2004). This species is highly anthropophilic in West and South Africa (Constantini, 1998), unless numerous alternative hosts are available (Coluzzi, 1979; Lindsay, 1993). In Madagascar, the species tends to be zoophilic (Fontinelle, 1990; Duchemin, 2001; Le Goff, 2003), possibly because alternate hosts such as cattle are numerous (Duchemin, 2001).


Anopheles coustani – Secondary Vector


Anopheles coustani is emerging as a potentially important malaria vector in Madagascar (Nepomichene, 2015a). This species is also infected with Setaria roundworms, Wuchereria bancrofti, Babanki virus, Périnet virus, Rift Valley fever virus, West Nile virus, and Zika virus (Brunhes, 1969; Brunhes, 1972; Fontenille, 1989; Ratovonjato, 2011; Diallo, 2014; Maquart, 2016). This species is abundant in the Central Highlands, breeding in rivers, canals, ponds, swamps, rice fields, and hoof prints (Grjebine, 1953; Grjebine, 1966). Anopheles coustani is highly exophilic, though its density in the Central Highlands can still make this species responsible for the majority of indoor bites (Nepomichene, 2015a). Current vector management strategies (ITNs and IRS) do little to mitigate this species, owing to the exophiliy, exophagy, and early biting exhibited by this species (Andrianaivolambo, 2010; Nepomichene, 2015). Populations for this species peak in February (Randriamaherijaona, 2017). Though considered zoophilic (Duchemin, 2001), this species will readily feed on humans (Nepomichene, 2015).


Anopheles gambiae sensu stricto– Primary Vector

Anopheles gambiae s.s. may be the most important vector of malaria (Coetzee, 2004). In addition to Plasmodium, this species is found infected with Bwamba virus, Ganjam virus, Ilesha virus, Mengo virus, O’nyong-nyong virus, and Tataguine virus (Cordellier, 1976; Cornet, 1979; Fontenille, 1989; Gordon, 1992; Vanlandingham, 2005). There are three members of the Anopheles gambiae sensu lato cryptic complex present in Madagascar, An. gambiae s.s. (formerly S-form), An. merus, and An. arabiensis (Tantely, 2012). Anopheles gambiae s.s. is the most important vector on the East and West coast of Madagascar (Mouchet, 1993; Duchemin, 2001; Rakotoson, 2017), but is nearly absent from the highlands (Tantely, 2012). This species is found in wetter climates compared toAn. arabiensis and An. merus (Pock Tsy, 2003), and is often found at the edge of the forests rather than within villages (Tantely, 2012). Densities for this species peak in March (Andrianaivolambo, 2010). This species lacks the longevity of An. funestus, with only 10% of An. gambiae s.s. females surviving long enough to facilitate transmission of Plasmodium parasites. Unlike continental An. gambiae s.s. that typically prefer to feed on humans, An. gambiae s.s. in Madagascar have been described as zoophilic (Duchemin, 2001).


Anopheles funestus – Primary Vector


An. funestus is the most important vector in Madagascar, acting as a primary vector across the island (Fontenille, 1990; Rakotoson, 2017). This species is considered highly susceptible to Plasmodium parasites, achieving infection rates as high as 22% (Gillies, 1968). In fact, we observed infection rates as high as 20% in the Southwest of Madagascar. In addition to Plasmodium, this species is responsible for the transmission of Akabane virus, Bozo Virus, Bwamba virus, Chikungunya virus, Nyando virus, O’Nyong nyong virus, Orungo virus, Pongola virus, Tanga virus, Tataguine virus, and Wesselsbron virus. (Adam, 2005; Cornet, 1979; Lutwama, 1999). Anopheles funestus has only moderate genetic differentiation at great distances, and the Malagasy population is most similar to An. funestus in Mozambique and Tanzania (Michel, 2005), from which they may have been carried by steamships or hurricanes (Simard, 1999). Larval habitats for this species include lakes, ponds, marshes, river-banks, streams and rice fields (Grjebine, 1966). This species is part of an extensive cryptic species complex containing An. parensisAn. aruniAn. confusus, An. vaneedeniAn. rivulorumAn. fuscivenosusAn.leesoni , and An. brucei (Gillies, 1987). Only An. funestus is recognized as a competent vector, and represents the only member of this complex in Madagascar (Ayala, 2006). Extensive environmental reshaping of the island provided numerous breeding grounds for An. funestus (Simard, 1999), facilitating its invasion of the highlands. Unlike populations in continental Africa, An. funestus breeds readily in the rice fields of Madagascar (Duchemin, 2001; Marrama, 2004, Muturi, 2008). The An. funestus population peaks in April, and extends further into the dry season than other primary vectors. (Andrianaivolambo, 2010). Most vectors experience a decline in longevity at higher population densities, reducing the likelihood of transmitting Plasmodium. However, older An. funestus females are consistently captured even amidst population spikes (Marrama, 2004). This species is known for its anthropophilic tendencies (Duchemin, 2001), yet several surveys in Madagascar reveal moderate to low numbers of human fed An. funestus (Andrianaivolambo, 2010; Nepomichene, 2015).

Anopheles maculipalpis – Secondary Vector



Anopheles maculipalpis occurs across Madagascar (Grjebine, 1966; Fontenille, 1989), with larvae for this species found in lakes, streams, ponds, marshes, riverbanks, irrigation drains, tire tracks, cattle hoofprints, and rice fields (Grjebine, 1966). Anopheles maculipalpis has been found positive for Plasmodium, Wuchereria bancrofti, and West Nile virus (Hamon, 1961; Brengues, 1968; Fontenille, 1989). This mosquito appears to be attracted to both humans and livestock (Fontenille, 1989; Tantely, 2016).

Anopheles mascarensis – Secondary Vector


Anopheles mascarensis is predominant in the humid regions of Madagascar (Marrama, 2004), but occurs across the island (Fontenille, 1989). This species exhibits morphological and behavioral variation across its range (Fontenille, 1992), a possible indication of an underlying cryptic species complex. Larvae for this species occur in streams, lakes, ponds, pools, marshes, riverbanks, and rice fields (Grjebine, 1953; Grjebine, 1966; Robert, 2002). This species was found to be circumsporozoite protein positive for P. falciparum, P. malariae, and P. vivax (Fontenille, 1992; Andrianaivolambo, 2010; Nepomichene, 2015a). In conjunction with its relative longevity (Robert, 2006), An. mascarensis may represent an efficient emerging vector. In a survey in the southern humid regions of Madagascar, An. mascarensis was occasionally the vector with the highest EIR (Marrama, 2004). Like many mosquitoes in Madagascar, the exophilic/exophagic behavior of An. mascarensis limits its exposure to primary mosquito control strategies (Andrianaivolambo, 2010). Other than Plasmodium, this species is found naturally infected with Ngari virus and Wuchereria bancrofti (Fontenille, 1989; Brunhes, 1972). This species is typically zoophilic (Le Goff, 2003).

Anopheles squamosus – Secondary Vector


Anopheles squamosus occurs throughout Madagascar. It is morphologically indistinguishable from Anopheles cydippis but for several differences in the clypeal setae of the larval stage (Tantely, 2016). Larvae for this species are found in lagoons, rivers, ponds, marshes, irrigation drains, and rice fields (Grjebine, 1953; Grjebine, 1966; Grjebine, 1958). This species is occasionally infected with Plasmodium sporozoites, though this has only been detected in continental Africa (Gillies, 64; Gillies, 68; Stevenson, 2016). Anopheles squamosus is involved in the transmission of Wuchereria bancrofti, Andasibe virus, Babanki virus, Bluetongue virus, Birao virus, and Rift Valley fever virus (Adam, 2005; Andriamandimby, 2015; Brunhes, 1972; Cordellier, 1976; Fontenille, 1989; Hamon, 1964; Ratovonjato, 2010; Tantely, 2013). This species is typically zoophilic (Tantely, 2013).