Measuring, manipulating and exploiting behaviours of adult mosquitoes to optimise malaria vector control impact

Residual malaria transmission can persist despite high coverage with effective long-lasting insecticidal nets (LLINs) and/or indoor residual spraying (IRS), because many vector mosquitoes evade them by feeding on animals, feeding outdoors, resting outdoors or rapidly exiting from houses after entering them. However, many of these behaviours that render vectors resilient to control with IRS and LLINs also make them vulnerable to some emerging new alternative interventions. Furthermore, vector control measures targeting preferred behaviours of mosquitoes often force them to express previously rare alternative behaviours, which can then be targeted with these complementary new interventions. For example, deployment of LLINs against vectors that historically fed predominantly indoors on humans typically results in persisting transmission by residual populations that survive by feeding outdoors on humans and animals, where they may then be targeted with vapour-phase insecticides and veterinary insecticides, respectively. So while the ability of mosquitoes to express alternative behaviours limits the impact of LLINs and IRS, it also creates measurable and unprecedented opportunities for deploying complementary additional approaches that would otherwise be ineffective. Now that more diverse vector control methods are finally becoming available, well-established entomological field techniques for surveying adult mosquito behaviours should be fully exploited by national malaria control programmes, to rationally and adaptively map out new opportunities for their effective deployment.

[1]  Environmentally friendly tool to control mosquito populations without risk of insecticide resistance: the Lehmann’s funnel entry trap , 2013, Malaria Journal.

[2]  John M. Marshall,et al.  Developing an expanded vector control toolbox for malaria elimination , 2017, BMJ Global Health.

[3]  K. Dietz,et al.  The impact of propoxur on Anopheles gambiae s.1. and some other anopheline populations, and its relationship with some pre-spraying variables. , 1976, Bulletin of the World Health Organization.

[4]  R. Elliott Studies on man vector contact in some malarious areas in Colombia. , 1968, Bulletin of the World Health Organization.

[5]  R. Elliott The influence of vector behavior on malaria transmission. , 1972, The American journal of tropical medicine and hygiene.

[6]  G. Killeen,et al.  Human Exposure to Early Morning Anopheles funestus Biting Behavior and Personal Protection Provided by Long-Lasting Insecticidal Nets , 2014, PloS one.

[7]  G. Killeen,et al.  Rationalizing historical successes of malaria control in Africa in terms of mosquito resource availability management. , 2004, The American journal of tropical medicine and hygiene.

[8]  S. James,et al.  Considerations for the Use of Human Participants in Vector Biology Research: A Tool for Investigators and Regulators , 2015, Vector borne and zoonotic diseases.

[9]  W. Takken,et al.  Eave Screening and Push-Pull Tactics to Reduce House Entry by Vectors of Malaria. , 2016, American Journal of Tropical Medicine and Hygiene.

[10]  J. Grieco,et al.  The field evaluation of a push-pull system to control malaria vectors in Northern Belize, Central America , 2015, Malaria Journal.

[11]  Nakul Chitnis,et al.  Made-to-measure malaria vector control strategies: rational design based on insecticide properties and coverage of blood resources for mosquitoes , 2014, Malaria Journal.

[12]  F. Okumu,et al.  Efficacy and user acceptability of transfluthrin-treated sisal and hessian decorations for protecting against mosquito bites in outdoor bars , 2017, Parasites & Vectors.

[13]  W. Takken,et al.  Exploiting the behaviour of wild malaria vectors to achieve high infection with fungal biocontrol agents , 2012, Malaria Journal.

[14]  Tanya L Russell,et al.  Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania , 2011, Malaria Journal.

[15]  N. Beebe,et al.  Barrier screens: a method to sample blood-fed and host-seeking exophilic mosquitoes , 2013, Malaria Journal.

[16]  M. Kenward,et al.  Comparative field evaluation of combinations of long-lasting insecticide treated nets and indoor residual spraying, relative to either method alone, for malaria prevention in an area where the main vector is Anopheles arabiensis , 2013, Parasites & Vectors.

[17]  John M. Marshall,et al.  THE IMPORTANCE OF MOSQUITO BEHAVIOURAL ADAPTATIONS TO MALARIA CONTROL IN AFRICA , 2013, Evolution; international journal of organic evolution.

[18]  R. Cibulskis,et al.  Achieving the malaria MDG target: Reversing the incidence of malaria 2000-2015. , 2015 .

[19]  J. Nájera Malaria control: achievements, problems and strategies. , 2001, Parassitologia.

[20]  G. Killeen,et al.  Entomological surveillance of behavioural resilience and resistance in residual malaria vector populations , 2013, Malaria Journal.

[21]  Thomas A. Smith,et al.  Survival and infection probabilities of anthropophagic anophelines from an area of high prevalence of Plasmodium falciparum in humans. , 1997 .

[22]  S. Moore,et al.  The Mode of Action of Spatial Repellents and Their Impact on Vectorial Capacity of Anopheles gambiae sensu stricto , 2014, PloS one.

[23]  P. Eckhoff,et al.  Mathematical Models of Within-Host and Transmission Dynamics to Determine Effects of Malaria Interventions in a Variety of Transmission Settings , 2013, The American journal of tropical medicine and hygiene.

[24]  C. Garrett-Jones,et al.  THE HUMAN BLOOD INDEX OF MALARIA VECTORS IN RELATION TO EPIDEMIOLOGICAL ASSESSMENT. , 1964, Bulletin of the World Health Organization.

[25]  G. Killeen,et al.  Comparative assessment of diverse strategies for malaria vector population control based on measured rates at which mosquitoes utilize targeted resource subsets , 2014, Malaria Journal.

[26]  G. Killeen,et al.  A low technology emanator treated with the volatile pyrethroid transfluthrin confers long term protection against outdoor biting vectors of lymphatic filariasis, arboviruses and malaria , 2017, PLoS neglected tropical diseases.

[27]  Stefan Dongus,et al.  Malaria vectors and their blood-meal sources in an area of high bed net ownership in the western Kenya highlands , 2016, Malaria Journal.

[28]  L. F. Chaves,et al.  Push by a net, pull by a cow: can zooprophylaxis enhance the impact of insecticide treated bed nets on malaria control? , 2014, Parasites & Vectors.

[29]  T. Russell,et al.  The impact of livestock on the abundance, resting behaviour and sporozoite rate of malaria vectors in southern Tanzania , 2015, Malaria Journal.

[30]  G. Killeen,et al.  Impregnating hessian strips with the volatile pyrethroid transfluthrin prevents outdoor exposure to vectors of malaria and lymphatic filariasis in urban Dar es Salaam, Tanzania , 2015, Parasites & Vectors.

[31]  R. C. Muirhead-Thomson The significance of irritability, behaviouristic avoidance and allied phenomena in malaria eradication. , 1960, Bulletin of the World Health Organization.

[32]  G. Killeen,et al.  Eliminating malaria vectors , 2013, Parasites & Vectors.

[33]  John-hwa Lee,et al.  Cloning and characterization of a new cysteine proteinase secreted by Paragonimus westermani adult worms. , 2004, American Journal of Tropical Medicine and Hygiene.

[34]  P. Boreham,et al.  Feeding habits of anophelines (Diptera: Culicidae) in 1971–78, with reference to the human blood index: a review , 1980 .

[35]  C. Garrett-Jones,et al.  Malaria vectorial capacity of a population of Anopheles gambiae: an exercise in epidemiological entomology. , 1969, Bulletin of the World Health Organization.

[36]  G. Killeen,et al.  Control of Malaria Vector Mosquitoes by Insecticide-Treated Combinations of Window Screens and Eave Baffles , 2017, Emerging infectious diseases.

[37]  J. Garcia-Guinea,et al.  Framboidal pyrites in antique books , 1997, Nature.

[38]  G. White,et al.  Comparative studies on sibling species of the Anopheles gambiae Giles complex (Dipt., Culicidae): bionomics and vectorial activity of species A and species B at Segera, Tanzania , 1972 .

[39]  H. Overgaard,et al.  Increasing outdoor host-seeking in Anopheles gambiae over 6 years of vector control on Bioko Island , 2016, Malaria Journal.

[40]  G. Killeen,et al.  Mathematical evaluation of community level impact of combining bed nets and indoor residual spraying upon malaria transmission in areas where the main vectors are Anopheles arabiensis mosquitoes , 2013, Parasites & Vectors.

[41]  M. Coosemans,et al.  Residual transmission of malaria : an old issue for new approaches , 2013 .

[42]  Thomas A. Smith,et al.  Impact of promoting longer-lasting insecticide treatment of bed nets upon malaria transmission in a rural Tanzanian setting with pre-existing high coverage of untreated nets , 2010, Malaria Journal.

[43]  John M. Marshall,et al.  Going beyond personal protection against mosquito bites to eliminate malaria transmission: population suppression of malaria vectors that exploit both human and animal blood , 2017, BMJ Global Health.

[44]  I. Kleinschmidt,et al.  Outdoor biting by Anopheles mosquitoes on Bioko Island does not currently impact on malaria control , 2015, Malaria Journal.

[45]  G. Killeen,et al.  Insecticide-Treated Nets Can Reduce Malaria Transmission by Mosquitoes Which Feed Outdoors , 2010, The American journal of tropical medicine and hygiene.

[46]  G. Killeen,et al.  Simplified Models of Vector Control Impact upon Malaria Transmission by Zoophagic Mosquitoes , 2012, PloS one.

[47]  R. C. Thomson,et al.  Mosquito Behaviour in Relation to Malaria Transmission and Control in the Tropics. , 1951 .

[48]  Christine Woodcock,et al.  Intercropping increases parasitism of pests , 1997, Nature.

[49]  M. Rowland,et al.  Species Shifts in the Anopheles gambiae Complex: Do LLINs Successfully Control Anopheles arabiensis? , 2012, PloS one.

[50]  J. Sachs,et al.  A global index representing the stability of malaria transmission. , 2004, The American journal of tropical medicine and hygiene.

[51]  Pedro L. Alonso,et al.  Some Lessons for the Future from the Global Malaria Eradication Programme (1955–1969) , 2011, PLoS medicine.

[52]  Vincent Sluydts,et al.  Re-imagining malaria: heterogeneity of human and mosquito behaviour in relation to residual malaria transmission in Cambodia , 2015, Malaria Journal.

[53]  Stella T. Kessy,et al.  Eave tubes for malaria control in Africa: initial development and semi-field evaluations in Tanzania , 2016, Malaria Journal.

[54]  I. Kleinschmidt,et al.  The evidence for improving housing to reduce malaria: a systematic review and meta-analysis , 2015, Malaria Journal.

[55]  Fredros O. Okumu,et al.  Consistently high estimates for the proportion of human exposure to malaria vector populations occurring indoors in rural Africa , 2013, International journal of epidemiology.

[56]  G. Yan,et al.  Indoor residual spray and insecticide-treated bednets for malaria control: theoretical synergisms and antagonisms , 2011, Journal of The Royal Society Interface.

[57]  J. Vulule,et al.  Use of insecticide-treated clothes for personal protection against malaria: a community trial , 2006, Malaria Journal.

[58]  N. Chitnis,et al.  Effects of changing mosquito host searching behaviour on the cost effectiveness of a mass distribution of long-lasting, insecticidal nets: a modelling study , 2013, Malaria Journal.

[59]  T. Lefèvre,et al.  Beyond nature and nurture: phenotypic plasticity in blood-feeding behavior of Anopheles gambiae s.s. when humans are not readily accessible. , 2009, The American journal of tropical medicine and hygiene.

[60]  Muirhead-Thomson Rc The significance of irritability, behaviouristic avoidance and allied phenomena in malaria eradication. , 1960 .

[61]  G. Killeen,et al.  The epidemiology of residual Plasmodium falciparum malaria transmission and infection burden in an African city with high coverage of multiple vector control measures , 2016, Malaria Journal.

[62]  G. Killeen,et al.  Predicting Scenarios for Successful Autodissemination of Pyriproxyfen by Malaria Vectors from Their Resting Sites to Aquatic Habitats; Description and Simulation Analysis of a Field-Parameterizable Model , 2015, PloS one.

[63]  N. Beebe,et al.  Anopheles farauti is a homogeneous population that blood feeds early and outdoors in the Solomon Islands , 2016, Malaria Journal.

[64]  K. MacIntyre,et al.  A new tool for malaria prevention?: Results of a trial of permethrin-impregnated bedsheets (shukas) in an area of unstable transmission. , 2003, International journal of epidemiology.

[65]  U. Dalrymple,et al.  The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015 , 2015, Nature.

[66]  G. Killeen,et al.  Biologically meaningful coverage indicators for eliminating malaria transmission , 2012, Biology Letters.

[67]  Thomas A. Smith,et al.  Density independent feeding success of malaria vectors (Diptera: Culicidae) in Tanzania. , 1995 .

[68]  G. Killeen,et al.  Most outdoor malaria transmission by behaviourally-resistant Anopheles arabiensis is mediated by mosquitoes that have previously been inside houses , 2016, Malaria Journal.

[69]  T. Russell,et al.  Bionomics of the malaria vector Anopheles farauti in Temotu Province, Solomon Islands: issues for malaria elimination , 2011, Malaria Journal.

[70]  G. Killeen,et al.  Characterizing, controlling and eliminating residual malaria transmission , 2014, Malaria Journal.

[71]  C. Stone,et al.  Effects of bed net use, female size, and plant abundance on the first meal choice (blood vs sugar) of the malaria mosquito Anopheles gambiae , 2012, Malaria Journal.

[72]  David L. Smith,et al.  Vectorial capacity and vector control: reconsidering sensitivity to parameters for malaria elimination , 2016, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[73]  An improved mosquito electrocuting trap that safely reproduces epidemiologically relevant metrics of mosquito human-feeding behaviours as determined by human landing catch , 2016, Malaria Journal.

[74]  Eleazar Eskin,et al.  The Genetic Basis of Host Preference and Resting Behavior in the Major African Malaria Vector, Anopheles arabiensis , 2016, PLoS genetics.

[75]  G. Killeen,et al.  Potential causes and consequences of behavioural resilience and resistance in malaria vector populations: a mathematical modelling analysis , 2014, Malaria Journal.