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Research Article

A new malaria vector in Africa: Predicting the expansion range of Anopheles stephensi and identifying the urban populations at risk

View ORCID ProfileM. E. Sinka, View ORCID ProfileS. Pironon, N. C. Massey, View ORCID ProfileJ. Longbottom, View ORCID ProfileJ. Hemingway, View ORCID ProfileC. L. Moyes, and K. J. Willis
PNAS October 6, 2020 117 (40) 24900-24908; first published September 14, 2020; https://doi.org/10.1073/pnas.2003976117
M. E. Sinka
aDepartment of Zoology, University of Oxford, Oxford, United Kingdom, OX1 3SZ;
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  • ORCID record for M. E. Sinka
  • For correspondence: marianne.sinka@zoo.ox.ac.uk janet.hemingway@lstmed.ac.uk
S. Pironon
bBiodiversity Informatics and Spatial Analysis Department, Royal Botanic Gardens Kew, Richmond, Surrey, United Kingdom, TW9 3DS;
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N. C. Massey
cBig Data Institute, Li Ka Shing Centre for Health Information and Discovery, University of Oxford, Oxford, United Kingdom, OX3 7LF;
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J. Longbottom
dDepartment of Vector Biology, Liverpool School of Tropical Medicine, Liverpool, United Kingdom, L3 5QA
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J. Hemingway
dDepartment of Vector Biology, Liverpool School of Tropical Medicine, Liverpool, United Kingdom, L3 5QA
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  • ORCID record for J. Hemingway
  • For correspondence: marianne.sinka@zoo.ox.ac.uk janet.hemingway@lstmed.ac.uk
C. L. Moyes
cBig Data Institute, Li Ka Shing Centre for Health Information and Discovery, University of Oxford, Oxford, United Kingdom, OX3 7LF;
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K. J. Willis
aDepartment of Zoology, University of Oxford, Oxford, United Kingdom, OX1 3SZ;
bBiodiversity Informatics and Spatial Analysis Department, Royal Botanic Gardens Kew, Richmond, Surrey, United Kingdom, TW9 3DS;
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  1. Edited by Nils Chr. Stenseth, University of Oslo, Norway, and approved July 27, 2020 (received for review March 26, 2020)

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    Fig. 1.

    The new “out of range” occurrence of An. stephensi in the Arabian Peninsula and Horn of Africa showing the 358 An. stephensi site locations used in our final species distribution models (SDMs) color coded by the decade in which they were sampled. The yellow shaded area shows the 2011 expert opinion range based on data published up to 31 October 2009 (9). Data showing the presence of An. stephensi more westerly across the Arabian peninsula (sampled in 2005 to 2006) were published after 2010. Thus An. stephensi may have been present but unreported or been expanding its range into western areas of the Arabian peninsula over the last 30 y.

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    Fig. 2.

    Exclusive map: Environmental suitability map of An. stephensi using the updated occurrence database but without African sites. Red indicates a higher probability of environmental suitability whereas the blue indicates environments with a lower probability, i.e., more likely to be unsuitable for the species to occur. The environmental variables selected by the model as relevant to An. stephensi habitat suitability, in descending order (based on correlation score): Ann. Mean Temp. = 0.459, Human Popn Dens. = 0.325, Precip (season) = 0.171, enhanced vegetation index (EVI) = 0.161, Irrigation= 0.155, tasselled cap wetness (TCW) = 0.110, Crop mosaic = 0.011. Dark gray circles indicate the location of all 358 occurrence data used in the final inclusive map (Fig. 3) including those in Africa (not used in this exclusive model).The thumbnail map shows the coefficient of variation calculated per pixel across the predicted range, indicating where the ensemble model provides the most reliable (higher confidence: dark green) and least reliable (lower confidence: red) predictions.

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    Fig. 3.

    Inclusive map: Environmental suitability map of An. stephensi using the updated occurrence database including all African sites. Red indicates a higher probability of environmental suitability whereas the blue indicates environments with a lower probability, i.e., more likely to be unsuitable for the species to occur. The environmental variables selected by the model as relevant to An. stephensi habitat suitability, in descending order (based on correlation score): Ann. Mean Temp. = 0.461, Human Popn Dens. = 0.370, EVI = 0.174, Precip (season) = 0.161, TCW = 0.134, Irrigation= 0.130, Crop mosaic = 0.010. Turquoise circles indicate the location of cities with a population > 1 million. The thumbnail map shows the coefficient of variation calculated per pixel across the predicted range, indicating where the ensemble model provides the most reliable (higher confidence: dark green) and least reliable (lower confidence: red) predictions.

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    Fig. 4.

    The inclusive map focusing on the malaria (P. falciparum and P. vivax [PfPv]) endemic areas in Africa: Environmental suitability map of An. stephensi using the updated occurrence database including all African sites, masked (dark gray) using the Malaria Atlas Project (MAP) PfPv endemicity mask (16). Red indicates a higher probability of environmental suitability whereas the blue indicates environments with a lower probability, i.e., more likely to be unsuitable for the species to occur. Turquoise circles indicate the location of cities with a population > 1 million.

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    Fig. 5.

    Mosquito biting activity summarized from published studies (MAP bionomics database) comparing the Asian (open triangles) An. stephensi with the African (open circles) DVS (An. arabiensis, An. gambiae, and An. funestus) showing the peak activity periods as the proportion of mosquitoes biting in the first, second, third and fourth quarters of the night (from 6 PM to 6 AM).

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    Table 1.

    Abridged table showing the populations at risk if An. stephensi were to establish in urban cities of Africa (full table in SI Appendix)*

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    • The cities are listed in order of increasing distance from confirmed An. stephensi presences in Africa and many of the cities that are not shown in the abridged version are identified as highly suitable (SI Appendix, Table S3). The habitat suitability for An. stephensi classification was evaluated from the predicted habitat suitability map (Fig. 3). The quartiles for the full distribution of predicted values within the current species range were calculated and used to assign suitability class. Class 4 (below the lower quartile, indicating lowest suitability) is not found in any listed city (full table in SI Appendix, Table S3). Classes 3 (indicated as pale blue) and 2 (pale yellow) indicate increasing increments of suitability, with class 1 (red) indicating the highest suitability (i.e., predictions greater than the upper quartile value). Population data are taken from Brinkoff (40) listing urban agglomerations with ≥ 1 million inhabitants. The distance from An. stephensi records (data collated by this study) was calculated in QGIS (41) using United Nations (UN) sourced city coordinates which were also used to evaluate the distance from P. falciparum and P. vivax endemic zones (16). The 11 cities closest to the current An. stephensi distribution are all within the malaria endemic zone.

    • ↵* Addis Ababa is within the area of the malaria endemic zone, but due to its altitude (∼2300 m) is considered nonendemic.

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A new malaria vector in Africa: Predicting the expansion range of Anopheles stephensi and identifying the urban populations at risk
M. E. Sinka, S. Pironon, N. C. Massey, J. Longbottom, J. Hemingway, C. L. Moyes, K. J. Willis
Proceedings of the National Academy of Sciences Oct 2020, 117 (40) 24900-24908; DOI: 10.1073/pnas.2003976117

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A new malaria vector in Africa: Predicting the expansion range of Anopheles stephensi and identifying the urban populations at risk
M. E. Sinka, S. Pironon, N. C. Massey, J. Longbottom, J. Hemingway, C. L. Moyes, K. J. Willis
Proceedings of the National Academy of Sciences Oct 2020, 117 (40) 24900-24908; DOI: 10.1073/pnas.2003976117
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