Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

The influence of feeding behaviour and temperature on the capacity of mosquitoes to transmit malaria


Insecticide-treated bed nets reduce malaria transmission by limiting contact between mosquito vectors and human hosts when mosquitoes feed during the night. However, malaria vectors can also feed in the early evening and in the morning when people are not protected. Here, we explored how the timing of blood feeding interacts with environmental temperature to influence the capacity of Anopheles mosquitoes to transmit the human malaria parasite Plasmodium falciparum. In laboratory experiments, we found no effect of biting time itself on the proportion of mosquitoes that became infectious (vector competence) at constant temperature. However, when mosquitoes were maintained under more realistic fluctuating temperatures, there was a significant increase in competence for mosquitoes feeding in the evening (18:00), and a significant reduction in competence for those feeding in the morning (06:00), relative to those feeding at midnight (00:00). These effects appear to be due to thermal sensitivity of malaria parasites during the initial stages of parasite development within the mosquito, and the fact that mosquitoes feeding in the evening experience cooling temperatures during the night, whereas mosquitoes feeding in the morning quickly experience warming temperatures that are inhibitory to parasite establishment. A transmission dynamics model illustrates that such differences in competence could have important implications for malaria prevalence, the extent of transmission that persists in the presence of bed nets, and the epidemiological impact of behavioural resistance. These results indicate that the interaction of temperature and feeding behaviour could be a major ecological determinant of the vectorial capacity of malaria mosquitoes.

This is a preview of subscription content

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Fig. 1: Effects of the time of day of the blood meal and diurnal temperature fluctuation on the vector competence of A. gambiae mosquitoes infected with P. falciparum malaria.
Fig. 2: Model outputs illustrating the potential epidemiological significance of altered vector competence arising from biting time.
Fig. 3: Effect of exposure to high temperatures on vector competence of Anopheles mosquitoes infected with P. falciparum malaria.
Fig. 4: Behavioural assay to investigate thermal avoidance behaviour of A. gambiae mosquitoes following a blood meal.

Data availability

The raw data that support the findings of this study are available in Dryad with the identifier b2rbnzsb5 (ref. 93).

Code availability

The code used for modelling in this study is available at Any changes to this code are described within this paper.


  1. 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  PubMed  PubMed Central  Google Scholar 

  2. 2.

    Churcher, T. S., Lissenden, N., Griffin, J. T., Worrall, E. & Ranson, H. The impact of pyrethroid resistance of the efficacy and effectiveness of bednets for malaria control in Africa. eLife 5, e16090 (2016).

    PubMed  PubMed Central  Google Scholar 

  3. 3.

    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 (2016).

    CAS  PubMed  Google Scholar 

  4. 4.

    Hemingway, J. et al. Averting a malaria disaster: will insecticide resistance derail malaria control? Lancet 387, 1785–1788 (2016).

    PubMed  PubMed Central  Google Scholar 

  5. 5.

    Moiroux, N. et al. Changes in Anopheles funestus biting behavior following universal coverage of long-lasting insecticidal nets in Benin. J. Infect. Dis. 206, 1622–1629 (2012).

    CAS  PubMed  Google Scholar 

  6. 6.

    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).

    PubMed  PubMed Central  Google Scholar 

  7. 7.

    Thomsen, E. K. et al. Mosquito behavior change after distribution of bednets results in decreased protection against malaria exposure. J. Infect. Dis. 215, 790–797 (2017).

    PubMed  Google Scholar 

  8. 8.

    Carrasco, D. et al. Behavioural adaptations of mosquito vectors to insecticide control. Curr. Opin. Insect Sci. 34, 48–54 (2019).

    PubMed  Google Scholar 

  9. 9.

    Protopopoff, N. et al. Effectiveness of a long-lasting piperonyl butoxide-treated insecticidal net and indoor residual spray interventions, separately and together, against malaria transmitted by pyrethroid-resistant mosquitoes: a cluster, randomised controlled, two-by-two factorial design trial. Lancet 391, 1577–1588 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  10. 10.

    Uragayala, S. et al. Village-scale (phase III) evaluation of the efficacy and residual activity of SumiShield® 50 WG (Clothianidin 50%, w/w) for indoor spraying for the control of pyrethroid-resistant Anopheles culicifacies Giles in Karnataka State, India. Trop. Med. Int. Health 23, 605–615 (2018).

    CAS  PubMed  Google Scholar 

  11. 11.

    Mashauri, F. M. et al. Indoor residual spraying with micro-encapsulated pirimiphos-methyl (Actellic® 300CS) against malaria vectors in the Lake Victoria basin, Tanzania. PLoS ONE 12, e0176982 (2017).

    PubMed  PubMed Central  Google Scholar 

  12. 12.

    Bayili, K. et al. Evaluation of efficacy of Interceptor® G2, a long-lasting insecticide net coated with a mixture of chlorfenapyr and alpha-cypermethrin, against pyrethroid resistant Anopheles gambiae s.l. in Burkina Faso. Malar. J. 16, 190 (2017).

    PubMed  PubMed Central  Google Scholar 

  13. 13.

    Tiono, A. B. et al. Efficacy of Olyset Duo, a bednet containing pyriproxyfen and permethrin, versus a permethrin-only net against clinical malaria in an area with highly pyrethroid-resistant vectors in rural Burkina Faso: a cluster-randomised controlled trial. Lancet 392, 569–580 (2018).

    PubMed  Google Scholar 

  14. 14.

    Gatton, M. L. et al. The importance of mosquito behavioural adaptations to malaria control in Africa. Evolution 67, 1218–1230 (2013).

    PubMed  PubMed Central  Google Scholar 

  15. 15.

    Killeen, G. F. Characterizing, controlling and eliminating residual malaria transmission. Malar. J. 13, 330 (2014).

    PubMed  PubMed Central  Google Scholar 

  16. 16.

    Sherrard-Smith, E. et al. Mosquito feeding behavior and how it influences residual malaria transmission across Africa. Proc. Natl Acad. Sci. USA 116, 15086–15095 (2019).

    CAS  PubMed  Google Scholar 

  17. 17.

    Durnez, L. & Coosemans, M. Residual Transmission of Malaria: an Old Issue for New Approaches (Intech, 2013).

  18. 18.

    Lambrechts, L. Quantitative genetics of Aedes aegypti vector competence for Dengue viruses: towards a new paradigm? Trends Parasitol. 27, 111–114 (2011).

    CAS  PubMed  Google Scholar 

  19. 19.

    Baton, L. A. & Ranford-Cartwright, L. C. Spreading the seeds of million-murdering death: metamorphoses of malaria in the mosquito. Trends Parasitol. 21, 573–580 (2005).

    PubMed  Google Scholar 

  20. 20.

    Beier, J. C. Malaria parasite development in mosquitoes. Annu. Rev. Entomol. 43, 519–543 (1998).

    CAS  PubMed  Google Scholar 

  21. 21.

    Lefevre, T., Vantaux, A., Dabire, K. R., Mouline, K. & Cohuet, A. Non-genetic determinants of mosquito competence for malaria parasites. PLoS Pathog. 9, e1003365 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  22. 22.

    Westwood, M. L. et al. The evolutionary ecology of circadian rhythms in infection. Nat. Ecol. Evol. 3, 552–560 (2019).

    PubMed  Google Scholar 

  23. 23.

    Rund, S. S. C., O’Donnell, A. J., Gentile, J. E. & Reece, S. E. Daily rhythms in mosquitoes and their consequences for malaria transmission. Insects 7, E14 (2016).

    PubMed  Google Scholar 

  24. 24.

    Rund, S. S. C., Hou, T. Y., Ward, S. M., Collins, F. H. & Duffield, G. E. Genome-wide profiling of diel and circadian gene expression in the malaria vector Anopheles gambiae. Proc. Natl Acad. Sci. USA 108, E421–E430 (2011).

    CAS  PubMed  Google Scholar 

  25. 25.

    Blanford, J. I. et al. Implications of temperature variation for malaria parasite development across Africa. Sci. Rep. 3, 1300 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. 26.

    Glunt, K. D., Blanford, J. I. & Paaijmans, K. P. Chemicals, climate, and control: increasing the effectiveness of malaria vector control tools by considering relevant temperatures. PLoS Pathog. 9, e1003602 (2013).

    PubMed  PubMed Central  Google Scholar 

  27. 27.

    Paaijmans, K. P. et al. Downscaling reveals diverse effects of anthropogenic climate warming on the potential for local environments to support malaria transmission. Clim. Change 125, 479–488 (2014).

    Google Scholar 

  28. 28.

    Thomas, S. et al. Microclimate variables of the ambient environment deliver the actual estimates of the extrinsic incubation period of Plasmodium vivax and Plasmodium falciparum: a study from a malaria-endemic urban setting, Chennai in India. Malar. J. 17, 201 (2018).

    PubMed  PubMed Central  Google Scholar 

  29. 29.

    Eling, W., Hooghof, J., van de Vegte-Bolmer, M., Sauerwein, R. & van Gemert, G.-J. Tropical temperatures can inhibit development of the human malaria parasite Plasmodium falciparum in the mosquito. Proc. Exp. Appl. Entomol. 12, 151–156 (2001).

    Google Scholar 

  30. 30.

    Noden, B. H., Kent, M. D. & Beier, J. C. The impact of variations in temperature on early Plasmodium falciparum development in Anopheles stephensi. Parasitology 111, 539–545 (1995).

    PubMed  Google Scholar 

  31. 31.

    Murdock, C. C., Moller-Jacobs, L. L. & Thomas, M. B. Complex environmental drivers of immunity and resistance in malaria mosquitoes. Proc. R. Soc. B Biol. Sci. 280, 20132030 (2013).

    Google Scholar 

  32. 32.

    Gillies, M. T. & De Meillon, B. The Anophelinae of Africa South of the Sahara (Ethiopian Zoogeographical Region) 2nd edn (South African Institute for Medical Research, 1968).

  33. 33.

    Paaijmans, K. P. et al. Influence of climate on malaria transmission depends on daily temperature variation. Proc. Natl Acad. Sci. USA 107, 15135–15139 (2010).

    CAS  PubMed  Google Scholar 

  34. 34.

    Paaijmans, K. P., Read, A. F. & Thomas, M. B. Understanding the link between malaria risk and climate. Proc. Natl Acad. Sci. USA 106, 13844–13849 (2009).

    CAS  PubMed  Google Scholar 

  35. 35.

    Ohm, J. R. et al. Rethinking the extrinsic incubation period of malaria parasites. Parasites Vectors 11, 178 (2018).

    PubMed  PubMed Central  Google Scholar 

  36. 36.

    Waite, J. L., Suh, E., Lynch, P. A. & Thomas, M. B. Exploring the lower thermal limits for development of the human malaria parasite, Plasmodium falciparum. Biol. Lett. 15, 20190275 (2019).

    PubMed  PubMed Central  Google Scholar 

  37. 37.

    Griffin, J. T. et al. Reducing Plasmodium falciparum malaria transmission in Africa: a model-based evaluation of intervention strategies. PLoS Med. 7, e1000324 (2010).

    PubMed  PubMed Central  Google Scholar 

  38. 38.

    White, M. T. et al. Modelling the impact of vector control interventions on Anopheles gambiae population dynamics. Parasites Vectors 4, 153 (2011).

    PubMed  PubMed Central  Google Scholar 

  39. 39.

    Griffin, J. T., Ferguson, N. M. & Ghani, A. C. Estimates of the changing age-burden of Plasmodium falciparum malaria disease in sub-Saharan Africa. Nat. Commun. 5, 3136 (2014).

    PubMed  PubMed Central  Google Scholar 

  40. 40.

    Griffin, J. T. et al. Gradual acquisition of immunity to severe malaria with increasing exposure. Proc. R. Soc. B Biol. Sci. 282, 20142657 (2015).

    Google Scholar 

  41. 41.

    Killeen, G. F. et al. Made-to-measure malaria vector control strategies: rational design based on insecticide properties and coverage of blood resources for mosquitoes. Malar. J. 13, 146 (2014).

    PubMed  PubMed Central  Google Scholar 

  42. 42.

    Janko, M. M., Churcher, T. S., Emch, M. E. & Meshnick, S. R. Strengthening long-lasting insecticidal nets effectiveness monitoring using retrospective analysis of cross-sectional, population-based surveys across sub-Saharan Africa. Sci. Rep. 8, 17110 (2018).

    PubMed  PubMed Central  Google Scholar 

  43. 43.

    Kirby, M. J. & Lindsay, S. W. Responses of adult mosquitoes of two sibling species, Anopheles arabiensis and A. gambiae s.s. (Diptera: Culicidae), to high temperatures. Bull. Entomol. Res. 94, 441–448 (2004).

    CAS  PubMed  Google Scholar 

  44. 44.

    Benoit, J. B. et al. Drinking a hot blood meal elicits a protective heat shock response in mosquitoes. Proc. Natl Acad. Sci. USA 108, 8026–8029 (2011).

    CAS  PubMed  Google Scholar 

  45. 45.

    Lahondere, C. & Lazzari, C. R. Mosquitoes cool down during blood feeding to avoid overheating. Curr. Biol. 22, 40–45 (2012).

    CAS  PubMed  Google Scholar 

  46. 46.

    Ferguson, H. M. et al. Selection of mosquito life-histories: a hidden weapon against malaria? Malar. J. 11, 106 (2012).

    PubMed  PubMed Central  Google Scholar 

  47. 47.

    Murdock, C. C., Paaijmans, K. P., Cox-Foster, D., Read, A. F. & Thomas, M. B. Rethinking vector immunology: the role of environmental temperature in shaping resistance. Nat. Rev. Microbiol. 10, 869–876 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  48. 48.

    Murdock, C. C., Blanford, S., Hughes, G. L., Rasgon, J. L. & Thomas, M. B. Temperature alters Plasmodium blocking by Wolbachia. Sci. Rep. 4, 3932 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  49. 49.

    Lyons, C. L., Coetzee, M., Terblanche, J. S. & Chown, S. L. Thermal limits of wild and laboratory strains of two African malaria vector species, Anopheles arabiensis and Anopheles funestus. Malar. J. 11, 226 (2012).

    PubMed  PubMed Central  Google Scholar 

  50. 50.

    Sternberg, E. D. & Thomas, M. B. Local adaptation to temperature and the implications for vector-borne diseases. Trends Parasitol. 30, 115–122 (2014).

    PubMed  Google Scholar 

  51. 51.

    Siddons, L. B. Observations on the influence of atmospheric temperature and humidity on the infectivity of Anopheles culicifacies Giles. J. Malar. Inst. India 5, 375–388 (1944).

    Google Scholar 

  52. 52.

    Knowles, R. & Basu, B. C. Laboratory studies on the infectivity of Anopheles stephensi. J. Malar. Inst. India 5, 1–29 (1943).

    Google Scholar 

  53. 53.

    Okech, B. A. et al. Resistance of early midgut stages of natural Plasmodium falciparum parasites to high temperatures in experimentally infected Anopheles gambiae (Diptera: Culicidae). J. Parasitol. 90, 764–768 (2004).

    PubMed  Google Scholar 

  54. 54.

    Bradley, J. et al. Predicting the likelihood and intensity of mosquito infection from sex specific Plasmodium falciparum gametocyte density. eLife 7, e34463 (2018).

    PubMed  PubMed Central  Google Scholar 

  55. 55.

    Pathak, A. K., Shiau, J. C., Thomas, M. B. & Murdock, C. Field relevant variation in ambient temperature modifies density-dependent establishment of Plasmodium falciparum gametocytes in mosquitoes. Front. Microbiol. 10, 2651 (2019).

    PubMed  PubMed Central  Google Scholar 

  56. 56.

    Schneider, P. et al. Adaptive plasticity in the gametocyte conversion rate of malaria parasites. PLoS Pathog. 14, e1007371 (2018).

    PubMed  PubMed Central  Google Scholar 

  57. 57.

    Schneider, P. et al. Adaptive periodicity in the infectivity of malaria gametocytes to mosquitoes. Proc. R. Soc. B Biol. Sci. 285, 20181876 (2018).

    Google Scholar 

  58. 58.

    Githeko, A. K. et al. Confirmation that Plasmodium falciparum has asperiodic infectivity to Anopheles gambiae. Med. Vet. Entomol. 7, 373–376 (1993).

    CAS  PubMed  Google Scholar 

  59. 59.

    Magesa, S. M., Mdira, Y. K., Akida, J. A., Bygbjerg, I. C. & Jakobsen, P. H. Observations on the periodicity of Plasmodium falciparum gametocytes in natural human infections. Acta Trop. 76, 239–246 (2000).

    CAS  PubMed  Google Scholar 

  60. 60.

    Ferguson, H. M. et al. Ecology: a prerequisite for malaria elimination and eradication. PLoS Med. 7, e1000303 (2010).

    PubMed  PubMed Central  Google Scholar 

  61. 61.

    Thomas, M. B. et al. Lessons from agriculture for the sustainable management of malaria vectors. PLoS Med. 9, e1001262 (2012).

    PubMed  PubMed Central  Google Scholar 

  62. 62.

    Lefevre, T. et al. Transmission traits of malaria parasites within the mosquito: genetic variation, phenotypic plasticity, and consequences for control. Evol. Appl. 11, 456–469 (2018).

    PubMed  Google Scholar 

  63. 63.

    Stratman-Thomas, W. K. The influence of temperature on Plasmodium vivax. Am. J. Trop. Med. Hyg. S1–S20, 703–715 (1940).

    Google Scholar 

  64. 64.

    Ball, G. H. & Chao, J. Temperature stresses on the mosquito phase of Plasmodium relictum. J. Parasitol. 50, 748–752 (1964).

    CAS  PubMed  Google Scholar 

  65. 65.

    Vanderberg, J. P. & Yoeli, M. Effects of temperature on sporogonic development of Plasmodium berghei. J. Parasitol. 52, 559–564 (1966).

    CAS  PubMed  Google Scholar 

  66. 66.

    Simoes, M. L., Caragata, E. P. & Dimopoulos, G. Diverse host and restriction factors regulate mosquito–pathogen interactions. Trends Parasitol. 34, 603–616 (2018).

    PubMed  Google Scholar 

  67. 67.

    Riehle, M. M. et al. Natural malaria infection in Anopheles gambiae is regulated by a single genomic control region. Science 312, 577–579 (2006).

    CAS  PubMed  Google Scholar 

  68. 68.

    Molina-Cruz, A. et al. Plasmodium evasion of mosquito immunity and global malaria transmission: the lock-and-key theory. Proc. Natl Acad. Sci. USA 112, 15178–15183 (2015).

    CAS  PubMed  Google Scholar 

  69. 69.

    Van Tol, S. & Dimopoulos, G. in Progress in Mosquito Research Vol. 51 (ed. Raikhel, A. S.) 243–291 (Academic Press and Elsevier Science, 2016).

  70. 70.

    Wang, S. B. et al. Driving mosquito refractoriness to Plasmodium falciparum with engineered symbiotic bacteria. Science 357, 1399–1402 (2017).

    CAS  PubMed  Google Scholar 

  71. 71.

    Cirimotich, C. M. et al. Natural microbe-mediated refractoriness to Plasmodium infection in Anopheles gambiae. Science 332, 855–858 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  72. 72.

    Bugoro, H. et al. Bionomics of the malaria vector Anopheles farauti in Temotu Province, Solomon Islands: issues for malaria elimination. Malar. J. 10, 133 (2011).

    PubMed  PubMed Central  Google Scholar 

  73. 73.

    Geissbuhler, Y. et al. Interdependence of domestic malaria prevention measures and mosquito–human interactions in urban Dar es Salaam, Tanzania. Malar. J. 6, 126 (2007).

    PubMed  PubMed Central  Google Scholar 

  74. 74.

    Russell, T. L. et al. Frequent blood feeding enables insecticide-treated nets to reduce transmission by mosquitoes that bite predominately outdoors. Malar. J. 15, 156 (2016).

    PubMed  PubMed Central  Google Scholar 

  75. 75.

    Seyoum, A. et al. Human exposure to anopheline mosquitoes occurs primarily indoors, even for users of insecticide-treated nets in Luangwa Valley, South-East Zambia. Parasites Vectors 5, 101 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  76. 76.

    Bayoh, M. N. et al. Persistently high estimates of late night, indoor exposure to malaria vectors despite high coverage of insecticide treated nets. Parasites Vectors 7, 380 (2014).

    PubMed  Google Scholar 

  77. 77.

    Killeen, G. F. et al. Quantifying behavioural interactions between humans and mosquitoes: evaluating the protective efficacy of insecticidal nets against malaria transmission in rural Tanzania. BMC Infect. Dis. 6, 161 (2006).

    PubMed  PubMed Central  Google Scholar 

  78. 78.

    Mordecai, E. A. et al. Optimal temperature for malaria transmission is dramatically lower than previously predicted. Ecol. Lett. 16, 22–30 (2013).

    PubMed  Google Scholar 

  79. 79.

    Shapiro, L. L. M., Murdock, C. C., Jacobs, G. R., Thomas, R. J. & Thomas, M. B. Larval food quantity affects the capacity of adult mosquitoes to transmit human malaria. Proc. R. Soc. B Biol. Sci. 283, 20160298 (2016).

    Google Scholar 

  80. 80.

    Parton, W. J. & Logan, J. A. A model for diurnal variation in soil and air temperature. Agric. Meteorol. 23, 205–216 (1981).

    Google Scholar 

  81. 81.

    Detinova, T. Age-grouping methods in Diptera of medical importance with special reference to some vectors of malaria. Monogr. Ser. World Health Organ. 47, 13–91 (1962).

    CAS  PubMed  Google Scholar 

  82. 82.

    Shapiro, L. L. M., Whitehead, S. A. & Thomas, M. B. Quantifying the effects of temperature on mosquito and parasite traits that determine the transmission potential of human malaria. PLoS. Biol. 15, e2003489 (2017).

    PubMed  PubMed Central  Google Scholar 

  83. 83.

    Walker, P. G. T., Griffin, J. T., Ferguson, N. M. & Ghani, A. C. Estimating the most efficient allocation of interventions to achieve reductions in Plasmodium falciparum malaria burden and transmission in Africa: a modelling study. Lancet Glob. Health 4, E474–E484 (2016).

    PubMed  Google Scholar 

  84. 84.

    Winskill, P., Slater, H. C., Griffin, J. T., Ghani, A. C. & Walker, P. G. T. The US President’s Malaria Initiative, Plasmodium falciparum transmission and mortality: a modelling study. PLoS Med. 14, e1002448 (2017).

    PubMed  PubMed Central  Google Scholar 

  85. 85.

    Slater, H. C., Walker, P. G. T., Bousema, T., Okell, L. C. & Ghani, A. C. The potential impact of adding ivermectin to a mass treatment intervention to reduce malaria transmission: a modelling study. J. Infect. Dis. 210, 1972–1980 (2014).

    CAS  PubMed  Google Scholar 

  86. 86.

    Huho, B. et al. Consistently high estimates for the proportion of human exposure to malaria vector populations occurring indoors in rural Africa. Int. J. Epidemiol. 42, 235–247 (2013).

    PubMed  PubMed Central  Google Scholar 

  87. 87.

    Wat’senga, F. et al. Nationwide insecticide resistance status and biting behaviour of malaria vector species in the Democratic Republic of Congo. Malar. J. 17, 129 (2018).

    PubMed  PubMed Central  Google Scholar 

  88. 88.

    Reddy, M. R. et al. Outdoor host seeking behaviour of Anopheles gambiae mosquitoes following initiation of malaria vector control on Bioko Island, Equatorial Guinea. Malar. J. 10, 184 (2011).

    PubMed  PubMed Central  Google Scholar 

  89. 89.

    Cooke, M. K. et al. ‘A bite before bed’: exposure to malaria vectors outside the times of net use in the highlands of western Kenya. Malar. J. 14, 259 (2015).

    PubMed  PubMed Central  Google Scholar 

  90. 90.

    Garske, T., Ferguson, N. M. & Ghani, A. C. Estimating air temperature and its influence on malaria transmission across Africa. PLoS ONE 8, e56487 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  91. 91.

    West, B., Welch, K. & Galecki, A. Linear Mixed Models: a Practical Guide Using Statistical Software 2nd edn (Chapman & Hall, 2007).

  92. 92.

    Gill, J. & King, G. What to do when your hessian is not invertible: alternatives to model respecification in nonlinear estimation. Sociol. Methods Res. 33, 54–87 (2004).

    Google Scholar 

  93. 93.

    Suh, E. et al. Dryad Data from: The influence of feeding behaviour and temperature on the capacity of mosquitoes to transmit malaria. (Dryad Digital Repository, 2020);

Download references


We thank D. C. Soergel, J. L. Teeple and F. Ware-Gilmore for technical assistance, and D. A. Kennedy, E. D. Sternberg and L. Ge for advice on statistical analyses. This study was supported by NIH NIAID grant R01AI110793 and National Science Foundation Ecology and Evolution of Infectious Diseases grant DEB-1518681. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.

Author information




E.S., J.L.W., E.S.-S., T.S.C. and M.B.T. designed the research. E.S., J.L.W., N.L.D. and E.S.-S. performed the research. E.S., M.K.G., E.S.-S. and T.S.C. analysed the data. E.S., E.S.-S., T.S.C. and M.B.T. wrote the manuscript with input from M.K.G., J.L.W. and N.L.D.

Corresponding author

Correspondence to Eunho Suh.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Figs. 1–7 and Tables 1–13.

Reporting Summary

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Suh, E., Grossman, M.K., Waite, J.L. et al. The influence of feeding behaviour and temperature on the capacity of mosquitoes to transmit malaria. Nat Ecol Evol 4, 940–951 (2020).

Download citation


Quick links