Bionomics of malaria vectors in Mutare and Mutasa districts of Manicaland province, Zimbabwe

Abstract

Bionomics of malaria vectors including species composition, resting and biting behaviour and insecticide resistance are important for insecticide-based malaria control and interventions. The lack of data on malaria vector species composition and relative abundance, resting and biting behaviour, as well as insecticide resistance, make the development of target control measures problematic in Mutare and Mutasa Districts. It is imperative to elucidate, characterize, and identify all members of the An. funestus group and the An. gambiae complex to determine their resting and biting behaviour, host-seeking activities, disease relationships, and resistance to insecticides. A longitudinal study was carried out to investigate the bionomics of malaria vector mosquitoes in Mutare and Mutasa Districts. Anopheline larval and adult sampling was conducted from May 2013 to December 2014 using scooping, pyrethrum spray catch, prokopac aspirator, exit window trap, pit shelter, and Centers for Disease Control (CDC) light trap methods. Indoor and outdoor resting mosquitoes were collected in randomly selected houses and pit shelters, respectively. Mosquitoes sampled by light traps were divided into two cohorts. In one cohort, traps were left overnight and mosquitoes collected the following morning, while in the other set, mosquitoes were collected hourly throughout the night. Mosquito samples for insecticide resistance testing were divided into two subsamples. One subsample was used immediately for WHO susceptibility assays and the other batch was allowed to oviposit in the insectary at the National Institute of Health Research, and females from the F1 progeny were used in further susceptibility assays. Mosquitoes were identified using morphological keys and polymerase chain reaction (PCR) techniques. The PCR-based assays showed the presence of four sibling species: Anopheles funestus sensu stricto (90.8%, 267/294) and An. leesoni (5.1%, 15/294) of the An. funestus group and An. arabiensis (41.9%, 13/31) and An. quadriannulatus (48.4%, 15/31) of the An. gambiae complex. Of the two malaria vectors, An. funestus sensu stricto was more abundant (95.4%, 267/280) than An. arabiensis (4.6%, 13/280). Endophilic collections of the An. funestus group and the An. gambiae complex were five times greater than exophilic catches. Nearly 90% endophilic An. funestus populations were collected on sprayable surfaces and the remainder was caught on unsprayable surfaces. Of the sprayable surfaces catches, 56% were collected on the roofs; with 44% on the walls. Of the gravid An. funestus caught, nearly two-thirds (218/330) were collected exiting recently pyrethroid-treated structures, with a 24-hour mortality of less than 10%. The CDC light trap catches were more abundant indoors (68%) than outdoors (32%). Anopheles funestus showed variable indoor and outdoor flight activity rhythms, with two peaks during the night; between 22:00-23:00 hours and 02:00-04:00 hours. Human blood index was 64.3%, with Plasmodium falciparum infection rate of 1.8%. Wild caught females showed resistance to lambda-cyhalothrin (3.3% mortality), deltamethrin (12.9% mortality), etofenprox (9.2% mortality), and bendiocarb (11.7% mortality).F1 An. funestus females showed resistance to deltamethrin (14.5% mortality), lambda-cyhalothrin (6.9 % mortality), etofenprox (8.3% mortality), and bendiocarb (16.8% mortality), but were susceptible to DDT and pirimiphos-methyl (100% mortality). Intensity resistance assay to bendiocarb had 100% mortality, while deltamethrin, lambda-cyhalothrin, and etofenprox had increased knockdown times with mortalities ranging between 66.7 and 92.7% after 24-hour exposures. The present work revealed important information on the behaviour of malaria vector mosquitoes in Mutare and Mutasa Districts, which if not addressed might threaten gains made in malaria control in the study area. It is imperative to change house-spraying insecticide from pyrethroids to organophosphates or DDT (organochlorine), develop an insecticide resistance management plan, provide extension lances to the house-spraying programme, complement mosquito nets with the use of mosquito repellents and long clothes, and establish a monitoring programme to determine the occurrence and distribution of An. funestus populations in Manicaland Province.