First report of heterogeneity and sympatry of malaria vectors in Southern Gombe, Northeastern Nigeria: its implications for malaria vector control

Document Type : Paper, English

Authors

1 Department of Zoology, Faculty of Science, Gombe State University, PMB 127, Gombe, Nigeria

2 Department of Zoology, Faculty of Life Science, Modibbo Adama University, Yola, Nigeria

3 Molecular Entomology and Vector Control Research Laboratory, Nigerian Institute of Medical Research, Yaba, Lagos, Nigeria

4 Zoology Department, Faculty of Science, Gombe State University, Gombe, Nigeria

5 Department of Zoology, University of Ilorin, Ilorin, Kwara State, Nigeria

10.61186/jesi.44.2.3

Abstract

 A survey of the malaria vectors in an area is a critical component of an effective vector control strategy. This study aimed to investigate the malaria vectors in four communities of Southern Gombe, Northeastern Nigeria. A total of 3200 adult female Anopheles reared from larvae in the four communities from two Local Government Areas (LGAs) in Southern Gombe were identified. Anopheles pretoriensis were dominant 1662 (51.9%) followed by An. gambiae sl 868(27.1%), An. maculipalpis 267(8.3), An. rufipes 252(7.9) and An. coustani 10(0.3%), and the least were An. pharoensis 6(0.2%). The remaining 135(4.3%) were unidentified. Of the 262 An. gambiae sl identified by species-specific PCR method, 135(51.5%) were found to be An. coluzzi, 60(22.9%) An. gambiae and only 1(0.4%) was An. arabiensis whereas hybrid constitutes 16(6.1%). To determine significant differences in species composition, the results from the four study sites were pooled together. Anopheles pretoriensis was significantly different from all the other species identified (p = <0.0001 - 0.0454). An. gambiae sl. was significantly different from An. coustani and An. pharoensis (p = 0.0258, 0.0249 respectively). There was no significant difference between An. maculipalpis, An. rufipes, An. coustani and An. pharoensis (p = 0.9261 - >0.9999). There was a significant difference between the number of species identified as An. coluzzi and An. arabiensis (p = 0.0025). But there was no significant difference between An. coluzzi and An. gambiae (p = 0.1212).  The heterogeneity and sympatry of Anopheles species observed is a threat to malaria control as the secondary vectors have behaviour that evades the current vector control interventions. It is expedient to re-strategize the vector control interventions in the study area.

Graphical Abstract

First report of heterogeneity and sympatry of malaria vectors in Southern Gombe, Northeastern Nigeria: its implications for malaria vector control

Keywords

Main Subjects

© 2024 by Author(s), Published by the Entomological Society of Iran

This Work is Licensed under Creative Commons Attribution-Non Commercial 4.0 International Public License

References

Adeogun, A., Babalola, A. S., Okoko, O. O., Oyeniyi, T., Omotayo, A., Izekor, R. T., Adetunji, O., Olakiigbe, A., Olagundoye, O., Adeleke, M., Ojianwuna, C., Adamu, D., Daskum, A., Musa, J., Sambo, O., Adedayo, O., Inyama, P. U., Samdi, L., Obembe, A., Dogara, M., Kennedy, P., Mohammed, S., Samuel, R., Amajoh, C,. Adesola, M., Bala, M., Esema, M., Omo-Eboh, M., Sinka, M., Idowu, O. A., Ande, A., Olayemi, I., Yayo, A., Uhomoibhi, P., Awolola, S. & Salako, B. (2023) Spatial distribution and ecological niche modeling of geographical spread of Anopheles gambiae complex in Nigeria using real time data. Scientific Reports, 13(1), 1–18. https://doi.org/10.1038/s41598-023-40929-5
Adeogun, A. O., Popoola, K. O. K., Olakiigbe, A. K. & Awolola, S. T. (2019) Distribution of Members of the Anopheles Gamibiae s.l. In Oyo State, South West Nigeria. Pan African Journal of Life Sciences, 3(1), 138–144. https://doi.org/10.36108/pajols/9102/30(0140)
Afrane, Y. A., Bonizzoni, M. & Yan, G. (2016) Secondary Malaria Vectors of Sub-Saharan Africa: Threat to Malaria Elimination on the Continent? In Current Topics in Malaria (pp. 474–490). https://doi.org/10.5772/65359
Antonio-Nkondjio, C., Kerah, C. H., Simard, F., Awono-Ambene, P., Chouaibou, M., Tchuinkam, T. & Fontenille, D. (2006) Complexity of the malaria vectorial system in Cameroon: Contribution of secondary vectors to malaria transmission. Journal of Medical Entomology, 43(6), 1215–1221. https://doi.org/10.1603/0022-2585(2006)43[1215:COTMVS]2.0.CO;2
Assa, A., Eligo, N. & Massebo, F. (2023) Anopheles mosquito diversity, entomological indicators of malaria transmission and challenges of morphological identification in southwestern Ethiopia. Tropical Medicine and Health, 51(1), 1–8. https://doi.org/10.1186/s41182-023-00529-5
Awolola, T. S., Adeogun, A., Olakiigbe, A. K., Oyeniyi, T., Olukosi, Y. A., Okoh, H., Arowolo, T., Akila, J., Oduola, A. & Amajoh, C. N. (2018) Pyrethroids resistance intensity and resistance mechanisms in Anopheles gambiae from malaria vector surveillance sites in Nigeria. PLoS ONE, 13(12), 1–13. https://doi.org/10.1371/journal.pone.0205230
Awolola, T. S., Oyewole, I. O., Amajoh, C. N., Idowu, E. T., Ajayi, M. B., Oduola, A., Manafa, O. U., Ibrahim, K., Koekemoer, L. L. & Coetzee, M. (2005) Distribution of the molecular forms of Anopheles gambiae and pyrethroid knock down resistance gene in Nigeria. Acta Tropica, 95(3), 204–209. https://doi.org/10.1016/j.actatropica.2005.06.002
Bedasso, A. H., Gutto, A. A., Waldetensai, A., Eukubay, A., Bokore, G. E., Kinde, S., Gemechu, F., Debebe, Y., Aklilu, M., Tasew, G., Massebo, F., Teshome, A., Kebede, T., Abdulatif, B., Sisay, A., Solomon, H. & Kweka, E. J. (2022) Malaria vector feeding, peak biting time and resting place preference behaviors in line with Indoor based intervention tools and its implication: scenario from selected sentinel sites of Ethiopia. Heliyon, 8(12). https://doi.org/10.1016/j.heliyon.2022.e12178
Braack, L., Bornman, R., Kruger, T., Dahan‐moss, Y., Gilbert, A., Kaiser, M., Oliver, S. V., Cornel, A. J., Lee, Y., Norris, D. E., Coetzee, M., Brooke, B. & de Jager, C. (2020) Malaria vectors and vector surveillance in Limpopo province (South Africa): 1927 to 2018. International Journal of Environmental Research and Public Health, 17(11), 1–21. https://doi.org/10.3390/ijerph17114125
Caminade, C., McIntyre, K. M. & Jones, A. E. (2019) Impact of recent and future climate change on vector-borne diseases. In Annals of the New York Academy of Sciences (Vol. 1436, Issue 1, pp. 157–173). Blackwell Publishing Inc. https://doi.org/10.1111/nyas.13950
Campos, M., Patel, N., Marshall, C., Gripkey, H., Ditter, R. E., Crepeau, M. W., Toilibou, A., Amina, Y., Cornel, A. J., Lee, Y. & Lanzaro, G. C. (2023) Population genetics of Anopheles pretoriensis in Grande Comore Island. Insects, 14(1), 1–8. https://doi.org/10.3390/insects14010014
Ciubotariu, I. I., Jones, C. M., Kobayashi, T., Bobanga, T., Muleba, M., Pringle, J. C., Stevenson, J. C., Carpi, G. & Norris, D. E. (2020) Genetic diversity of Anopheles coustani (Diptera: Culicidae) in malaria transmission foci in southern and central africa. Journal of Medical Entomology, 57(6), 1782–1792. https://doi.org/10.1093/jme/tjaa132
Coetzee, M. (2020). Key to the females of Afrotropical Anopheles mosquitoes (Diptera: Culicidae). Malaria Journal, 19(1), 1–20. https://doi.org/10.1186/s12936-020-3144-9
Ebenezer, A., Noutcha, A. E. M., Agi, P. I., Okiwelu, S. N. & Commander, T. (2014) Spatial distribution of the sibling species of Anopheles gambiae sensu lato (Diptera: Culicidae) and malaria prevalence in Bayelsa State, Nigeria. Parasites and Vectors 7(1), 1–6. https://doi.org/10.1186/1756-3305-7-32
Ebenezer, A., Okiwelu, S. N., Agi, P. I., Noutcha, M. A. E., Awolola, T. S. & Oduola, A. O. (2012) Species composition of the Anopheles gambiae complex across eco-vegetational zones in Bayelsa state, Niger Delta region, Nigeria. Journal of Vector Borne Diseases, 49(3), 164–167.
Epopa, P. S., Collins, C. M., North, A., Millogo, A. A., Benedict, M. Q., Tripet, F. & Diabate, A. (2019) Seasonal malaria vector and transmission dynamics in western Burkina Faso. Malaria Journal, 18(1), 1–13. https://doi.org/10.1186/s12936-019-2747-5
Garba, L. C., Oyieke, F. A., Owino. EA., Mwansat, G. S., Houmsou, R. S., Darda, F. & Chintem, D. (2017) Species Diversity and Relative Abundance of Anopheline Vectors of Malaria on the Highlands of Mambilla Plateau Northeast, Nigeria. Journal of Biotechnology and Bioengineering 1(1), 37–42.
Goupeyou-Youmsi, J., Rakotondranaivo, T., Puchot, N., Peterson, I., Girod, R., Vigan-Womas, I., Paul, R., Ndiath, M. O. & Bourgouin, C. (2020) Differential contribution of Anopheles coustani and Anopheles arabiensis to the transmission of Plasmodium falciparum and Plasmodium vivax in two neighbouring villages of Madagascar. Parasites and Vectors, 13(1), 1–16. https://doi.org/10.1186/s13071-020-04282-0
Mwangangi, J. M., Muturi, E. J., Muriu, S. M., Nzovu, J., Midega, J. T & Mbogo, C. (2013) The role of Anopheles arabiensis and Anopheles coustani in indoor and outdoor malaria transmission in Taveta District, Kenya. Parasites and Vectors 6(114), 1–9. https://doi.org/10.1186/1756-3305-6-114
Lafferty, K. D. & Mordecai, E. A. (2016) The rise and fall of infectious disease in a warmer world. In F1000Research (Vol. 5). Faculty of 1000 Ltd. https://doi.org/10.12688/F1000RESEARCH.8766.1
Lobo, N. F., St. Laurent, B., Sikaala, C. H., Hamainza, B., Chanda, J., Chinula, D., Krishnankutty, S. M., Mueller, J. D., Deason, N. A., Hoang, Q. T., Boldt, H. L., Thumloup, J., Stevenson, J., Seyoum, A. & Collins, F. H. (2015) Unexpected diversity of Anopheles species in Eastern Zambia: Implications for evaluating vector behavior and interventions using molecular tools. Scientific Reports, 5(December), 1–10. https://doi.org/10.1038/srep17952
National Malaria Control Programme. (2020) National Malaria Strategic Plan, 2021 – 2025. In National Malaria Strategic Plan, 2021 – 2025.
National Malaria Elimination Programme, & Federal Ministry of Health Nigeria. (2014) Nigeria National Malaria Strategic Plan (2014-2020) (pp. 1–132).
Nelly Armanda Kala-Chouakeu, Edmond Kopya, Vasileia Balabanidou, Borel Tchamen Djiappi, Kyriaki Maria Papapostolou, Timoléon Tchuinkam, & Christophe Antonio-Nkondjio. (2022) DDT Resistance in Anopheles pharoensis from Northern Cameroon Associated with High Cuticular Hydrocarbon Production. Genes, 13, 1–8. https://doi.org/doi: 10.3390/genes13101723
Nkya, T. E., Fillinger, U., Sangoro, O. P., Marubu, R., Chanda, E. & Mutero, C. M. (2022) Six decades of malaria vector control in southern Africa: a review of the entomological evidence-base. Malaria Journal, 21(1), 1–16. https://doi.org/10.1186/s12936-022-04292-6
Olatunbosun-Oduola, A., Abba, E., Adelaja, O., Taiwo-Ande, A., Poloma-Yoriyo, K. & Samson-Awolola, T. (2019) Widespread report of multiple insecticide resistance in Anopheles gambiae s.l. mosquitoes in eight communities in southern Gombe, north-eastern Nigeria. Journal of Arthropod-Borne Diseases, 13(1), 50–61. https://doi.org/10.18502/jad.v13i1.932
Oyewole, I. O., Awolola, T. S., Ibidapo, C. A., Oduola, A. O., Okwa, O. O. & Obansa, J. A. (2007) Behaviour and population dynamics of the major anopheline vectors in a malaria endemic area in southern Nigeria. Journal of Vector Borne Diseases, 44(1), 56–64.
Oyewole, I. O., Ibidapo, C. A., Okwa, O. O., Oduola, A. O., Adeoye, G. O., Okoh, H. I. & Awolola, T. S. (2010). Species composition and role of anopheles mosquitoes in malaria transmission along badagry axis of  lagos lagoon, Lagos, Nigeria. International Journal of Insect Science, 2, IJIS.S4698. https://doi.org/10.4137/ijis.s4698
PMI. (2021) The PMI VectorLink Nigeria 2019-2020 Annual Entomology Report. September. https://d1u4sg1s9ptc4z.cloudfront.net/uploads/2021/08/Entomological-Monitoring-Report-Nigeria-2019-2020.pdf
Saili, K., de Jager, C., Sangoro, O. P., Nkya, T. E., Masaninga, F., Mwenya, M., Sinyolo, A., Hamainza, B., Chanda, E., Fillinger, U. & Mutero, C. M. (2023) Anopheles rufipes implicated in malaria transmission both indoors and outdoors alongside Anopheles funestus and Anopheles arabiensis in rural south-east Zambia. Malaria Journal, 22(1), 1–12. https://doi.org/10.1186/s12936-023-04489-3
Sinka, M. E. (2013) Global distribution of the dominant vector species of malaria, \textit{Anopheles} mosquitoes. In New insights into malaria vectors (pp. 109–143).
Sinka, M. E., Bangs, M. J., Manguin, S., Coetzee, M., Mbogo, C. M., Hemingway, J., Patil, A. P., Temperley, W. H., Gething, P. W., Kabaria, C. W., Okara, R. M., Van Boeckel, T., Godfray, H. C. J., Harbach, R. E. & Hay, S. I. (2010) The dominant Anopheles vectors of human malaria in Africa, Europe and the Middle East: Occurrence data, distribution maps and bionomic précis. Parasites and Vectors, 3(1). https://doi.org/10.1186/1756-3305-3-117
Suh, P. F., Elanga-Ndille, E., Tchouakui, M., Sandeu, M. M., Tagne, D., Wondji, C. & Ndo, C. (2023) Impact of insecticide resistance on malaria vector competence: a literature review. In Malaria Journal (Vol. 22, Issue 1). BioMed Central Ltd. https://doi.org/10.1186/s12936-023-04444-2
Tabue, R. N., Awono-Ambene, P., Etang, J., Atangana, J., Antonio-Nkondjio, C., Toto, J. C., Patchoke, S., Leke, R. G. F., Fondjo, E., Mnzava, A. P., Knox, T. B., Tougordi, A., Donnelly, M. J. & Bigoga, J. D. (2017) Role of Anopheles (Cellia) rufipes (Gough, 1910) and other local anophelines in human malaria transmission in the northern savannah of Cameroon: a cross-sectional survey. Parasites and Vectors 10(1), 1–11. https://doi.org/10.1186/s13071-016-1933-3
Wahedi, J. A., Ande, A. T., Oduola, A. O. & Obembe, A. (2021) Bendiocarb resistance and, associated deltamethrin and DDT resistance in Anopheles gambiae s.l. populations from North Eastern Adamawa State, Nigeria. Ceylon Journal of Science 50(1), 63. https://doi.org/10.4038/cjs.v50i1.7848
Wahedi, J. A., Ande, A. T., Oduola, A. O., Obembe, A., Tola, M., Oyeniyi, T. A. & Awolola, T. S. (2020) Dynamics of malaria vector indices in two vegetation zones within North Eastern Adamawa State, Nigeria. Tropical Biomedicine, 37(3), 637–649. https://doi.org/10.47665/tb.37.3.637
WHO. (2023) World malaria report 2023. World Health Organization. https://www.wipo.int/amc/en/mediation/
Wilkins, E. E., Howell, P. I. & Benedict, M. Q. (2006) IMP PCR primers detect single nucleotide polymorphisms for Anopheles gambiae species identification, Mopti and Savanna rDNA types, and resistance to dieldrin in Anopheles arabiensis. Malaria Journal, 5, 1–7. https://doi.org/10.1186/1475-2875-5-125
World Health Organization. (2016) Test procedures for insecticide resistance monitoring in malaria vector mosquitoes Second edition (2nd ed.). World Health Organization.
Yoriyo, K. P., Alo, E. B., Naphtali, R. S., Samdi, L. M., Oduola A. O. & Awolola T. S. (2014) Anopheles species abundance and vectorial competence in four local government areas of Gombe state, Northeastern Nigeria. International Journal of Advanced Studies in Engineering and Scientific Inventions, 2(1), 19–25.
Journal of Entomological Society of Iran
Volume 44, Issue 2
March 2024
Pages 141-151

Files

Share

How to cite

Statistics