Effect of non-human hosts on the human biting rate of primary and secondary malaria vectors in Tanzania

Abstract Background Malaria vectors vary in feeding preference depending on their innate behaviour, host availability and abundance. Host preference and human biting rate in malaria vectors are key factors in establishing zooprophylaxis and zoopotentiation. This study aimed at assessing the impact o...

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Main Authors: Godfrey C. Katusi, Marie R. G. Hermy, Samwely M. Makayula, Rickard Ignell, Ladslaus L. Mnyone, Sharon R. Hill, Nicodem J. Govella
Format: Article
Language:English
Published: BMC 2023-11-01
Series:Malaria Journal
Subjects:
Online Access:https://doi.org/10.1186/s12936-023-04778-x
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author Godfrey C. Katusi
Marie R. G. Hermy
Samwely M. Makayula
Rickard Ignell
Ladslaus L. Mnyone
Sharon R. Hill
Nicodem J. Govella
author_facet Godfrey C. Katusi
Marie R. G. Hermy
Samwely M. Makayula
Rickard Ignell
Ladslaus L. Mnyone
Sharon R. Hill
Nicodem J. Govella
author_sort Godfrey C. Katusi
collection DOAJ
description Abstract Background Malaria vectors vary in feeding preference depending on their innate behaviour, host availability and abundance. Host preference and human biting rate in malaria vectors are key factors in establishing zooprophylaxis and zoopotentiation. This study aimed at assessing the impact of non-human hosts in close proximity to humans on the human biting rate of primary and secondary malaria vectors, with varying host preferences. Methods The effect of the presence of non-human hosts in close proximity to the human host on the mean catches per person per night, as a proxy for mosquito biting rate, was measured using mosquito-electrocuting traps (METs), in Sagamaganga, Kilombero Valley, Tanzania. Two experiments were designed: (1) a human versus a calf, each enclosed in a MET, and (2) a human surrounded by three calves versus a human alone, with each human volunteer enclosed individually in a MET spaced 10 m apart. Each experiment was conducted on alternate days and lasted for 36 nights per experiment. During each experiment, the positions of hosts were exchanged daily (except the human in experiment 2). All anopheline mosquitoes caught were assayed for Plasmodium sporozoites using enzyme-linked immunosorbent assay. Results A total of 20,574 mosquitoes were captured and identified during the study, of which 3608 were anophelines (84.4% primary and 15.6% secondary malaria vectors) and 17,146 were culicines. In experiment 1, the primary malaria vector, Anopheles arabiensis, along with Culex spp. demonstrated a preference for cattle, while the primary vectors, Anopheles funestus, preferred humans. In experiment 2, both primary vectors, An. arabiensis and An. funestus, as well as the secondary vector Anopheles rivolurum, demonstrated behaviours amenable to zooprophylaxis, whereas Culex spp. increased their attraction to humans in the presence of nearby cattle. All anopheline mosquitoes tested negative for sporozoites. Conclusions The findings of this study provide support for the zooprophylaxis model for malaria vectors present in the Kilombero Valley, and for the zoopotentiation model, as it pertains to the Culex spp. in the region. However, the factors regulating zooprophylaxis and zoopotentiation are complex, with different species-dependent mechanisms regulating these behaviours, that need to be considered when designing integrated vector management programmes.
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spelling doaj.art-d1c35308a05a4842ad79aad67cfa347e2023-11-12T12:07:17ZengBMCMalaria Journal1475-28752023-11-012211910.1186/s12936-023-04778-xEffect of non-human hosts on the human biting rate of primary and secondary malaria vectors in TanzaniaGodfrey C. Katusi0Marie R. G. Hermy1Samwely M. Makayula2Rickard Ignell3Ladslaus L. Mnyone4Sharon R. Hill5Nicodem J. Govella6Department of Environmental Health and Ecological Sciences, Ifakara Health InstituteDisease Vector Group, Unit of Chemical Ecology, Department of Plant Protection Biology, Swedish University of Agricultural SciencesDepartment of Environmental Health and Ecological Sciences, Ifakara Health InstituteDisease Vector Group, Unit of Chemical Ecology, Department of Plant Protection Biology, Swedish University of Agricultural SciencesInstitute of Pest Management, Sokoine University of AgricultureDisease Vector Group, Unit of Chemical Ecology, Department of Plant Protection Biology, Swedish University of Agricultural SciencesDepartment of Environmental Health and Ecological Sciences, Ifakara Health InstituteAbstract Background Malaria vectors vary in feeding preference depending on their innate behaviour, host availability and abundance. Host preference and human biting rate in malaria vectors are key factors in establishing zooprophylaxis and zoopotentiation. This study aimed at assessing the impact of non-human hosts in close proximity to humans on the human biting rate of primary and secondary malaria vectors, with varying host preferences. Methods The effect of the presence of non-human hosts in close proximity to the human host on the mean catches per person per night, as a proxy for mosquito biting rate, was measured using mosquito-electrocuting traps (METs), in Sagamaganga, Kilombero Valley, Tanzania. Two experiments were designed: (1) a human versus a calf, each enclosed in a MET, and (2) a human surrounded by three calves versus a human alone, with each human volunteer enclosed individually in a MET spaced 10 m apart. Each experiment was conducted on alternate days and lasted for 36 nights per experiment. During each experiment, the positions of hosts were exchanged daily (except the human in experiment 2). All anopheline mosquitoes caught were assayed for Plasmodium sporozoites using enzyme-linked immunosorbent assay. Results A total of 20,574 mosquitoes were captured and identified during the study, of which 3608 were anophelines (84.4% primary and 15.6% secondary malaria vectors) and 17,146 were culicines. In experiment 1, the primary malaria vector, Anopheles arabiensis, along with Culex spp. demonstrated a preference for cattle, while the primary vectors, Anopheles funestus, preferred humans. In experiment 2, both primary vectors, An. arabiensis and An. funestus, as well as the secondary vector Anopheles rivolurum, demonstrated behaviours amenable to zooprophylaxis, whereas Culex spp. increased their attraction to humans in the presence of nearby cattle. All anopheline mosquitoes tested negative for sporozoites. Conclusions The findings of this study provide support for the zooprophylaxis model for malaria vectors present in the Kilombero Valley, and for the zoopotentiation model, as it pertains to the Culex spp. in the region. However, the factors regulating zooprophylaxis and zoopotentiation are complex, with different species-dependent mechanisms regulating these behaviours, that need to be considered when designing integrated vector management programmes.https://doi.org/10.1186/s12936-023-04778-xAnophelesCulexZooprophylaxisZoopotentiationHost preferenceCattle
spellingShingle Godfrey C. Katusi
Marie R. G. Hermy
Samwely M. Makayula
Rickard Ignell
Ladslaus L. Mnyone
Sharon R. Hill
Nicodem J. Govella
Effect of non-human hosts on the human biting rate of primary and secondary malaria vectors in Tanzania
Malaria Journal
Anopheles
Culex
Zooprophylaxis
Zoopotentiation
Host preference
Cattle
title Effect of non-human hosts on the human biting rate of primary and secondary malaria vectors in Tanzania
title_full Effect of non-human hosts on the human biting rate of primary and secondary malaria vectors in Tanzania
title_fullStr Effect of non-human hosts on the human biting rate of primary and secondary malaria vectors in Tanzania
title_full_unstemmed Effect of non-human hosts on the human biting rate of primary and secondary malaria vectors in Tanzania
title_short Effect of non-human hosts on the human biting rate of primary and secondary malaria vectors in Tanzania
title_sort effect of non human hosts on the human biting rate of primary and secondary malaria vectors in tanzania
topic Anopheles
Culex
Zooprophylaxis
Zoopotentiation
Host preference
Cattle
url https://doi.org/10.1186/s12936-023-04778-x
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