in

Emergence of behavioural avoidance strategies of malaria vectors in areas of high LLIN coverage in Tanzania

  • 1.

    Bhatt, S. et al. The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature 526, 207–211 (2015).

    CAS  Article  ADS  Google Scholar 

  • 2.

    World Health Organization. World Malaria Report 2019 (World Health Organization, Geneva, 2019).

    Google Scholar 

  • 3.

    Sinka, M. E. et al. A global map of dominant malaria vectors. Parasit. Vectors 5, 69 (2012).

    Article  Google Scholar 

  • 4.

    Killeen, G. F. et al. Measuring, manipulating and exploiting behaviours of adult mosquitoes to optimise malaria vector control impact. BMJ Glob. Health https://doi.org/10.1136/bmjgh-2016-000212 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  • 5.

    Bayoh, M. N. et al. Anopheles gambiae: Historical population decline associated with regional distribution of insecticide-treated bed nets in western Nyanza Province, Kenya. Malar. J. 9, 62. https://doi.org/10.1186/1475-2875-9-62 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  • 6.

    Mwangangi, J. M. et al. Shifts in malaria vector species composition and transmission dynamics along the Kenyan coast over the past 20 years. Malar. J. https://doi.org/10.1186/1475-2875-12-13 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  • 7.

    Russell, T. L. 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. Malar. J. 9, 20 (2010).

    Article  Google Scholar 

  • 8.

    Killeen, G. F. Characterizing, controlling and eliminating residual malaria transmission. Malar. J. https://doi.org/10.1186/1475-2875-13-330 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  • 9.

    Sherrard-Smith, E. et al. Mosquito feeding behavior and how it influences residual malaria transmission across Africa. Proc. Natl. Acad. Sci. 116, 15086–15095. https://doi.org/10.1073/pnas.1820646116 (2019).

    CAS  Article  PubMed  Google Scholar 

  • 10.

    Knox, T. B. et al. An online tool for mapping insecticide resistance in major Anopheles vectors of human malaria parasites and review of resistance status for the Afrotropical region. Parasit. Vectors 7, 76. https://doi.org/10.1186/1756-3305-7-76 (2014).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 11.

    Moyes, C. L. et al. Analysis-ready datasets for insecticide resistance phenotype and genotype frequency in African malaria vectors. Sci. Data 6, 121. https://doi.org/10.1038/s41597-019-0134-2 (2019).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 12.

    Russell, T. L., Beebe, N. W., Cooper, R. D., Lobo, N. F. & Burkot, T. R. Successful malaria elimination strategies require interventions that target changing vector behaviours. Malar. J. https://doi.org/10.1186/1475-2875-12-56 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  • 13.

    Govella, N. J. & Ferguson, H. Why use of interventions targeting outdoor biting mosquitoes will be necessary to achieve malaria elimination. Front. Physiol. https://doi.org/10.3389/fphys.2012.00199 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  • 14.

    Killeen, G. F. & Chitnis, N. Potential causes and consequences of behavioural resilience and resistance in malaria vector populations: A mathematical modelling analysis. Malar. J. https://doi.org/10.1186/1475-2875-13-97 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  • 15.

    Gatton, M. L. et al. The importance of mosquito behavioural adaptations to malaria control in Africa. Evolution https://doi.org/10.1111/evo.12063 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  • 16.

    Ranson, H. & Lissenden, N. Insecticide resistance in African Anopheles mosquitoes: A worsening situation that needs urgent action to maintain malaria control. Trends Parasitol. 32, 187–196. https://doi.org/10.1016/j.pt.2015.11.010 (2016).

    CAS  Article  PubMed  Google Scholar 

  • 17.

    Pates, H. & Curtis, C. Mosquito behavior and vector control. Annu. Rev. Entomol. https://doi.org/10.1146/annurev.ento.50.071803.130439 (2005).

    Article  PubMed  Google Scholar 

  • 18.

    Gordicho, V. et al. First report of an exophilic Anopheles arabiensis population in Bissau City, Guinea-Bissau: Recent introduction or sampling bias?. Malar. J. 13, 423. https://doi.org/10.1186/1475-2875-13-423 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  • 19.

    Kitau, J. et al. Species shifts in the Anopheles gambiae complex: Do LLINs successfully control Anopheles arabiensis?. PLoS One 7, e31481 (2012).

    CAS  Article  ADS  Google Scholar 

  • 20.

    Smith, A. The preferential indoor resting habitats of Anopheles gambiae in the Umbugwe area of Tanganyika. East Afr. Med. J. 39, 631–635 (1962).

    CAS  PubMed  Google Scholar 

  • 21.

    Govella, N., Chaki, P. & Killeen, G. Entomological surveillance of behavioural resilience and resistance in residual malaria vector populations. Malar. J. 12, 124 (2013).

    Article  Google Scholar 

  • 22.

    Coluzzi, M. & Sabatini, A. Chromosomal differentiation and adaptation to human environments in the Anopheles gambiae complex. Trans. R. Soc. Trop. Med. Hyg. 73, 483–497 (1979).

    CAS  Article  Google Scholar 

  • 23.

    Main, B. J. et al. The genetic basis of host preference and resting behavior in the major African Malaria vector, Anopheles arabiensis. PLOS Genet. 12, e1006303. https://doi.org/10.1371/journal.pgen.1006303 (2016).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 24.

    Lindblade, K. et al. Impact of sustained use of insecticide-treated bednets on malaria vector species distribution and culicine mosquitoes. J. Med. Entomol. 43, 428–432 (2006).

    CAS  Article  Google Scholar 

  • 25.

    Russell, T. et al. Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania. Malar. J. 10, 80 (2011).

    Article  Google Scholar 

  • 26.

    Norris, L. C. & Norris, D. E. Heterogeneity and changes in inequality of malaria risk after introduction of insecticide-treated bed nets in Macha, Zambia. Am. J. Trop. Med. Hyg. https://doi.org/10.4269/ajtmh.11-0595 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  • 27.

    Tirados, I., Costantini, C., Gibson, G. & Torr, S. J. Blood-feeding behaviour of the malarial mosquito Anopheles arabiensis: Implications for vector control. Med. Vet. Entomol. 20, 425–437. https://doi.org/10.1111/j.1365-2915.2006.652.x (2006).

    CAS  Article  PubMed  Google Scholar 

  • 28.

    Pates, H. & Curtis, C. Mosquito behavior and vector control. Ann. Rev. Entomol. 50, 53–70 (2004).

    Article  Google Scholar 

  • 29.

    Gillies, M. & Meillon, B. The Anophelinae of Africa south of the Sahara (Ethiopian Zoogeographical Region). S. Afr. Inst. Med. Res. 20, 20 (1968).

    Google Scholar 

  • 30.

    Meyrowitsch, D. W. et al. Is the current decline in malaria burden in sub-Saharan Africa due to a decrease in vector population?. Malar. J. 10, 188 (2011).

    Article  Google Scholar 

  • 31.

    Kaindoa, M. N. et al. Interventions that effectively target Anopheles funestus mosquitoes could significantly improve control of persistent malaria transmission in south–eastern Tanzania. PLoS One 12(5), e0177807. https://doi.org/10.1371/journal.pone.0177807 (2017).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 32.

    Port, G. R. & Boreham, P. F. L. The effects of bednets on feeding by Anopheles gambiae Giles (Diptera: Culicidae). Bull. Entomol. Res. 72, 20 (1982).

    Article  Google Scholar 

  • 33.

    Lefevre, T. et al. Beyond nature and nurture: Phenotypic plasticity in blood-feeding behavior of Anopheles gambiae s.s. when humans are not readily accessible. Am. J. Trop. Med. Hyg. 81, 1023–1029 (2009).

    Article  Google Scholar 

  • 34.

    Moiroux, N. et al. Changes in Anopheles funestus biting behavior following universal coverage of long-lasting insecticidal nets in Benin. J. Infect. Dis. https://doi.org/10.1093/infdis/jis565 (2012).

    Article  PubMed  Google Scholar 

  • 35.

    Petrarca, V. & Beier, J. C. Intraspecific chromosomal polymorphism in the Anopheles gambiae complex as a factor affecting malaria transmission in the Kisumu area of Kenya. Am. J. Trop. Med. Hyg. 46, 20 (1992).

    Article  Google Scholar 

  • 36.

    Faye, O. et al. Impact of the use of permethrin pre-impregnated mosquito nets on malaria transmission in a hyperendemic village of Senegal. Med. Trop. (Mars) 58, 355–360 (1998).

    CAS  Google Scholar 

  • 37.

    Cuzin-Ouattara, N. et al. Wide-scale installation of insecticide-treated curtains confers high levels of protection against malaria transmission in a hyperendemic area of Burkina Faso. Trans. R. Soc. Trop. Med. Hyg. 93, 473–479. https://doi.org/10.1016/S0035-9203(99)90343-7 (1999).

    CAS  Article  PubMed  Google Scholar 

  • 38.

    Ilboudo-Sanogo, E. et al. Insecticide-treated materials, mosquito adaptation and mass effect: Entomological observations after five years of vector control in Burkina Faso. Trans. R. Soc. Trop. Med. Hyg. 95, 353–360. https://doi.org/10.1016/S0035-9203(01)90179-8 (2001).

    CAS  Article  PubMed  Google Scholar 

  • 39.

    Mathenge, E. et al. Effect of permethrin-impregnated nets on exiting behavior, blood feeding success and time of feeding of malaria mosquitoes (Diptera: Culicidae) in western Kenya. J. Med. Entomol. https://doi.org/10.1603/0022-2585-38.4.531 (2001).

    Article  PubMed  Google Scholar 

  • 40.

    Renggli, S. et al. Design, implementation and evaluation of a national campaign to deliver 18 million free long-lasting insecticidal nets to uncovered sleeping spaces in Tanzania. Malar. J. 12, 20 (2013).

    Article  Google Scholar 

  • 41.

    Kramer, K. et al. Effectiveness and equity of the Tanzania National Voucher Scheme for mosquito nets over 10 years of implementation. Malar. J. 16, 255. https://doi.org/10.1186/s12936-017-1902-0 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  • 42.

    Schmidt, C. A., Comeau, G., Monaghan, A. J., Williamson, D. J. & Ernst, K. C. Effects of desiccation stress on adult female longevity in Aedes aegypti and Ae. albopictus (Diptera: Culicidae): Results of a systematic review and pooled survival analysis. Parasit. Vectors 11, 267 (2018).

    Article  Google Scholar 

  • 43.

    Kalra, B. & Parkash, R. Effects of saturation deficit on desiccation resistance and water balance in seasonal populations of the tropical drosophilid Zaprionus indianus. J. Exp. Biol. 219, 3237. https://doi.org/10.1242/jeb.141002 (2016).

    Article  PubMed  Google Scholar 

  • 44.

    Lwetoijera, H. C. et al. Increasing role of Anopheles funestus and Anopheles arabiensis in malaria transmission in the Kilombero Valley, Tanzania. Malar. J. 331, 20 (2014).

    Google Scholar 

  • 45.

    Mayagaya, V. et al. The impact of livestock on the abundance, resting behaviour and sporozoite rate of malaria vectors in southern Tanzania. Malar. J. 14, 17 (2015).

    Article  Google Scholar 

  • 46.

    Mayagaya, V. The impact of livestock on the ecology of malaria vectors and malaria transmission in the Kilombero Valley. Tanzania MSc thesis, University of Dar es Salaam (2010).

  • 47.

    Corbel, V. et al. Combination of malaria vector control interventions in pyrethroid resistance area in Benin: A cluster randomised controlled trial. Lancet Infect. Dis. https://doi.org/10.1016/s1473-3099(12)70081-6 (2012).

    Article  PubMed  Google Scholar 

  • 48.

    Ngowo, H., Kaindoa, E., Matthiopoulos, J., Ferguson, H. & Okumu, F. Variations in household microclimate affect outdoor-biting behaviour of malaria vectors [version 1; referees: 1 approved, 1 approved with reservations]. Vol. 2 (2017).

  • 49.

    Russell, T. et al. Impact of promoting long-lasting insecticide treatment of bednets upon malaria transmission in a rural Tanzania setting with pre existing high coverage of untreated nets. Malar. J. 9, 187 (2010).

    Article  Google Scholar 

  • 50.

    Katharina Sophia, K. et al. Impact of ENSO 2016–17 on regional climate and malaria vector dynamics in Tanzania. Environ. Res. Lett. 20, 20 (2019).

    Google Scholar 

  • 51.

    Kessler, S. & Guerin, P. M. Responses of Anopheles gambiae, Anopheles stephensi, Aedes aegypti, and Culex pipiens mosquitoes (Diptera: Culicidae) to cool and humid refugium conditions. J. Vector Ecol. https://doi.org/10.3376/1081-1710(2008)33[145:roagas]2.0.co;2 (2008).

    Article  PubMed  Google Scholar 

  • 52.

    Chaccour, C. & Killeen, G. F. Mind the gap: Residual malaria transmission, veterinary endectocides and livestock as targets for malaria vector control. Malar. J. 15, 24 (2016).

    Article  Google Scholar 

  • 53.

    Lyimo, I. N., Kessy, S. T., Mbina, K. F., Daraja, A. A. & Mnyone, L. L. Ivermectin-treated cattle reduces blood digestion, egg production and survival of a free-living population of Anopheles arabiensis under semi-field condition in south-eastern Tanzania. Malar. J. https://doi.org/10.1186/s12936-017-1885-x (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  • 54.

    Meza, F. C. et al. Mosquito electrocuting traps for directly measuring biting rates and host-preferences of Anopheles arabiensis and Anopheles funestus outdoors. Malar. J. 18, 83. https://doi.org/10.1186/s12936-019-2726-x (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  • 55.

    Iwashita, H. et al. Push by a net, pull by a cow: Can zooprophylaxis enhance the impact of insecticide treated bed nets on malaria control?. Parasit. Vectors 7, 52 (2014).

    Article  Google Scholar 

  • 56.

    Tirados, I., Gibson, G., Young, S. & Torr, S. Are herders protected by their herds? An experimental analysis of zooprophylaxis against the malaria vector Anopheles arabiensis. Malar. J. 10, 68 (2011).

    Article  Google Scholar 

  • 57.

    Donnelly, B., Berrang-Ford, L., Ross, N. A. & Michel, P. A systematic, realist review of zooprophylaxis for malaria control. Malar. J. 14, 313. https://doi.org/10.1186/s12936-015-0822-0 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  • 58.

    Killeen, G. F. et al. Developing an expanded vector control toolbox for malaria elimination. BMJ Glob. Health 2, e000211. https://doi.org/10.1136/bmjgh-2016-000211 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  • 59.

    Ayala, D., Ullastres, A. & Gonzalez, J. Adaptation through chromosomal inversions in Anopheles. Front. Genet. https://doi.org/10.3389/fgene.2014.00129 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  • 60.

    Carrasco, D. et al. Behavioural adaptations of mosquito vectors to insecticide control. Curr. Opin. Insect Sci. 34, 48–54. https://doi.org/10.1016/j.cois.2019.03.005 (2019).

    Article  PubMed  Google Scholar 

  • 61.

    Matowo, N. S. et al. Fine-scale spatial and temporal heterogeneities in insecticide resistance profiles of the malaria vector, Anopheles arabiensis in rural south-eastern Tanzania. Wellcome Open Res. 2, 20 (2017).

    Article  Google Scholar 

  • 62.

    Okumu, F. 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. Parasit. Vectors 6, 46 (2013).

    Article  Google Scholar 

  • 63.

    Briët, O. J. T. et al. Applications and limitations of Centers for Disease Control and Prevention miniature light traps for measuring biting densities of African malaria vector populations: A pooled-analysis of 13 comparisons with human landing catches. Malar. J. 14, 1–13. https://doi.org/10.1186/s12936-015-0761-9 (2015).

    Article  Google Scholar 

  • 64.

    Clark, G. G., Seda, H. & Gubler, D. J. Use of the “CDC backpack aspirator” for surveillance of Aedes aegypti in San Juan, Puerto Rico. J. Am. Mosq. Control Assoc. 10, 119–124 (1994).

    CAS  PubMed  Google Scholar 

  • 65.

    Kreppel, K. S. et al. Comparative evaluation of the Sticky-Resting-Box-Trap, the standardised resting-bucket-trap and indoor aspiration for sampling malaria vectors. Parasit. Vectors 8, 462. https://doi.org/10.1186/s13071-015-1066-0 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  • 66.

    Allen, R., Pereira, L. S., Raes, D., & Smith, M. Crop evapotranspiration—guidelines for computing crop water requirements. Food and Agriculture Organization (FAO); United Nations, FAO, Irrigation and Drainage Paper 56 (1998).

  • 67.

    Funk, C. et al. The climate hazards infrared precipitation with stations—a new environmental record for monitoring extremes. Sci. Data 2, 150066. https://doi.org/10.1038/sdata.2015.66 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  • 68.

    Scott, J., Brodgon, W. & Collins, F. Identification of single specimens of Anopheles gambiae complex by polymerase chain reaction. Am. J. Trop. Med. Hyg. 49, 520–529 (1993).

    CAS  Article  Google Scholar 

  • 69.

    Kaindoa, E. W. et al. New evidence of mating swarms of the malaria vector, Anopheles arabiensis in Tanzania. Wellcome Open Res. 2, 88. https://doi.org/10.12688/wellcomeopenres.12458.1 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  • 70.

    Lee, Y., Weakley, A. M., Nieman, C. C., Malvick, J. & Lanzaro, G. C. A multi-detection assay for malaria transmitting mosquitoes. J. Vis. Exp. https://doi.org/10.3791/52385 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  • 71.

    Cameron, A. C. & Trivedi, P. K. Regression-based tests for overdispersion in the Poisson model. J. Econom. 46, 347–364. https://doi.org/10.1016/0304-4076(90)90014-K (1990).

    MathSciNet  Article  Google Scholar 

  • 72.

    R-Core-Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, 2016).

    Google Scholar 

  • 73.

    Pinheiro, J., Bates, D., DebRoy, S. & Sarkar, D. Linear and nonlinear mixed effects models. R Packag. Vers. 3, 57 (2007).

    Google Scholar 

  • 74.

    Brooks, M. E. et al. Modeling zero-inflated count data with glmmTMB. BioRxiv 132753, 20 (2017).

    Google Scholar 


  • Source: Ecology - nature.com

    Lessons from the Clean Air Car Race 50 years later

    “The Emerald Tutu” wins NSF grant for design to protect Boston’s coastline