Skip to main content

Advertisement

Log in

Exploring phytoplankton management for controlling the malaria vector Anopheles gambiae in Benin

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

The relationship between different species of phytoplankton and Anopheles gambiae mosquito larvae was studied in order to improve malaria control. Anopheles gambiae larval habitat was surveyed by sampling phytoplankton at 51 sites. The deleterious effect of Scenedesmus quadricauda on third instar larvae was evaluated in the laboratory. 27 phytoplankton species were encountered in the field survey. Anopheles gambiae larvae had a positive association with high densities of Spirogyra (Pearson chi-square = 25.56, P < 0.0001) and a negative association with high densities of green algae (Spirogyra, Elakotothrix, Coelastrum, Ankystrodesmus, Chlorella, Kirchneriella, Selanastrum, and Scenedesmus) and cyanobacteria (Oscillatoria, and Nostoc). Laboratory bioassays revealed that S. quadricauda is indigestible and toxic to An. gambiae larvae that ingest it. The larval mortality was 100% when larvae ingested only S. quadricauda and 85.6% if larvae were exposed to a mixture of S. quadricauda and cat food. The findings of this study indicate that phytoplankton management with S. quadricauda or other green algae offers a possible way to eliminate An. gambiae production. Complementary studies are needed to investigate the deleterious effect of these algae on An. gambiae under semi-natural and natural conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data Availability

The raw datasets are available at the corresponding author on reasonable demand.

References

  • Adjahouinou D, Liady M, Fiogbe E (2012) Diversité phytoplanctonique et niveau de pollution des eaux du collecteur de Dantokpa (Cotonou-Bénin). Int J Biol Chem Sci 6:1938–1949

    Google Scholar 

  • Ahmad R, Chu W-L, Lee H-L, Phang S-M (2001) Effect of four chlorophytes on larval survival, development and adult body size of the mosquito Aedes aegypti. J Appl Phycol 13:369–374

    Article  Google Scholar 

  • Ahmad R, Chu WL, Ismail Z, Lee HL, Phang SM (2004) Effect of ten chlorophytes on larval survival, development and adult body size of the mosquito Aedes aegypti. Southeast Asian J Trop Med Public Health 35:79–87

    Google Scholar 

  • Akogbéto H, Zanklan A, Adjahouinou D, Fiogbe E (2019) Degré d’eutrophisation et diversité phytoplanctonique de la lagune de Porto-Novo, République du Bénin

  • Andersen RA, Kawachi M (2005) Traditional isolation techniques. In: Andersen RA (ed) Algal culturing techniques. Elsevier Academic Press, London, pp 83–101

    Google Scholar 

  • Banerjee S, Rembold H (1992) Azadirachtin A interferes with control of serotonin pools in the neuroendocrine system of locusts. Naturwissenschaften 79:81–84

    Article  CAS  Google Scholar 

  • Bennett KD (1990) Textbook of pollen analysis. K. FAEGRI, J. IVERSEN (4th edn by K. Faegri, P. E. Kaland, K. Krzywinski), Publisher John Wiley and Sons, Chichester 1989 (328 pp) £51.00 ISBN 0 471 92178 5 (book review). J Quat Sci 5:254–255.

  • Bond JG, Rojas JC, Arredondo-Jiménez JI, Quiroz-Martínez H, Valle J, Williams T (2004) Population control of the malaria vector Anopheles pseudopunctipennis by habitat manipulation. Proc R Soc Lond B 271:2161–2169

    Article  Google Scholar 

  • Bond JG, Arredondo-Jimenez JI, Rodriguez MH, Quiroz-Martínez H, Williams T (2005) Oviposition habitat selection for a predator refuge and food source in a mosquito. Ecol Entomol 30:255–263

    Article  Google Scholar 

  • Bourrelly P (1972) Les Algues D'eau Douce. Tome 1. Les Algues Vertes. Editions N. Boubee & Co, Paris

  • Charles V, Vijayan VA, Aivazi AA, Hosmani SP (2011) Feeding habitats of mosquito larvae and their gut flora at Mysore. Nat Environ Pollut Technol 10:219–224

    Google Scholar 

  • Chukwuekezie O, Nwosu E, Nwangwu U, Dogunro F, Onwude C, Agashi N, Ezihe E, Anioke C, Anokwu S, Eloy E, Attah P, Orizu F, Ewo S, Okoronkwo A, Joseph A, Ikeakor L, Haruna S, Gnanguenon V (2020) Resistance status of Anopheles gambiae (s.l.) to four commonly used insecticides for malaria vector control in South-East Nigeria. Parasit Vectors 13:152.

  • Cole J, Findlay S, Pace M (1988) Bacterial production in fresh and saltwater ecosystems – a cross-system overview. Mar Ecol Prog Ser 43:1–10

    Article  Google Scholar 

  • Dabbadie L (1992) Cultures intensives de microalgues sur lisier de porc : performances, contraintes, utilisation des biomasses. Thesis, ENSAM [Ecole Nationale Supérieure Agronomique De Montpellier]

  • Dejoux C (1998) La pollution des eaux continentales africaines: Expérience acquise, situation actuelle et perspectives. Institut de Recherche pour le Développement, Paris

    Google Scholar 

  • Dhillon MS, Mulla MS (1981) Biological activity of the green alga Chlorella ellipsoidea against immature stages of mosquitoes. Mosq News 41:368–372

    Google Scholar 

  • Dhillon MS, Mulla MS (1982) Impact of green alga, Chlorella ellipsoidea, on development and survival of mosquitoes breeding in cemetery vases. Environ Entomol 112:292–296

    Article  Google Scholar 

  • Dhillon S, Mulla MS, Hwang YS (1982) Biocidal activity of algal toxins against immature mosquitoes. J Chem Ecol 8:557–566

    Article  CAS  Google Scholar 

  • Everts JW, Koeman JH (2020) The ecological impact of insecticides in connection to the control of tsetse flies in Africa: A review. In: Cavalloro R (ed) Integrated Tse-Tse Fly Control. CRC Press, London, pp 49–56

    Chapter  Google Scholar 

  • Garcia E de S, Rembold H (1984) Effects of azadirachtin on ecdysis of Rhodnius prolixus. J Insect Physiol 30:939–941

    Article  CAS  Google Scholar 

  • Garcia-Sánchez DC, Pinilla GA, Quintero J (2017) Ecological characterization of Aedes aegypti larval habitats (Diptera: Culicidae) in artificial water containers in Girardot, Colombia. J Vector Ecol 42:289–297

    Article  Google Scholar 

  • Garros C, Ngungi N, Githeko AE, Tuno N, Yan G (2008) Gut content identification of larvae of the Anopheles gambiae complex in western Kenya using a barcoding approach. Mol Ecol Resour 8:512–518

    Article  CAS  Google Scholar 

  • Iltis A (1980) Les algues. In: Durand J-R, Lévêque C (eds) Flore et faune aquatiques de l’Afrique sahélosoudanienne: tome 1. ORSTOM, Paris, pp 9–61

  • INSAE (2016) Cahier des villages et quartiers de ville du département de l’Ouémé [Institut National de la Statistique et de la Démographie] P41

  • Kant R, Pandey SD, Sharma SK (1996) Mosquito breeding in relation to aquatic vegetation and some physico-chemical parameters in rice fields of central Gujarat. Indian J Malariol 33:30–40

    CAS  Google Scholar 

  • Kaufman MG, Wanja E, Maknojia S, Maknojia S, Bayoh MN, Vulule JM, Walker ED (2006) Importance of algal biomass to growth and development of Anopheles gambiae larvae. J Med Entomol 43:669–676

    Article  Google Scholar 

  • Kay B, Nam VS (2005) New strategy against Aedes aegypti in Vietnam. Lancet 365:613–617

    Google Scholar 

  • Khawaled K, Mulla MS, Zaritsky A (1989) Distribution and abundance of algae in mosquito developmental sites. Bull Soc Vector Ecol 14:71–80

    Google Scholar 

  • Kiviranta J, Abdel-Hameed A (1994) Toxicity of the blue-green alga Oscillatoria agardhii to the mosquito Aedes aegypti and the shrimp Artemia salina. World J Microbiol Biotechnol 10:517–520

    Article  CAS  Google Scholar 

  • Laplace-Treyture C, Peltre MC, Lambert E, Rodriguez S, Vergon JP, Chauvin C (2014) Guide pratique de détermination des algues macroscopiques d’eau douce et de quelques organismes hétérotrophes. Les Éditions d'Irstea Bordeaux, Cestas

  • Lévêque C (1990) Impact de la lutte antivectorielle sur l’environnement aquatique. Ann Parasitol Hum Comparée 65:119–124

    Article  Google Scholar 

  • Liady MND, Goussanou BK, Adandé R, Noumavo ADP, Kouadio LA, Zouhir F, Aïna MP, Fiogbe ED (2020) Valorisation du surnageant d’effluents de brasserie dans la production de planctons pour la pisciculture : une alternative pour la protection de l’environnement dans les pays du Sud. Biotechnol Agron Soc Environ 24:235–239

  • Marten GG (1984) Impact of the copepod Mesocyclops leuckarti pilosa and the green alga Kirchneriella irregularis upon larval Aedes albopictus (Diptera: Culicidae). Bull Soc Vector Ecol 9:1–5

    Google Scholar 

  • Marten GG (1986a) Mosquito control by plankton management: the potential of indigestible green algae. J Trop Med Hyg 89:213–222

    CAS  Google Scholar 

  • Marten GG (1986b) Indigestible phytoplankton for mosquito control. Parasitol Today 2:150–151

    Article  CAS  Google Scholar 

  • Marten GG (1987) The potential of mosquito-indigestible phytoplankton for mosquito control. J Am Mosq Control Assoc 3:105–106

    CAS  Google Scholar 

  • Marten GG, Astaiza R, Suárez MF, Monje C, Reid JW (1989) Natural control of larval Anopheles albimanus (Diptera: Culicidae) by the predator Mesocyclops (Copepoda: Cyclopoida). J Med Entomol 26:624–627

    Article  CAS  Google Scholar 

  • Marten G, Suárez M, Astaeza R (1996) An ecological survey of Anopheles albimanus larval habitats in Colombia. J Vector Ecol 21:122–131

    Google Scholar 

  • Marten GG, Nguyen M, Ngo G (2000) Copepod predation on Anopheles quadrimaculatus larvae in rice fields. J Vector Ecol 25:1–6

    CAS  Google Scholar 

  • Marten GG, Reid JW (2007) Larvicidal algae. In Floore T (ed.) Biorational Control of Mosquitoes. Amer Mosquito Control Assoc Bull 7:179–185

  • Marten GG, Caballero X, Larios A, Bendaña H (2022) Proof of concept for eliminating Aedes aegypti production by means of integrated control including turtles, copepods, tilapia, larvicides, and community participation in Monte Verde, Honduras. Acta Tropica 227:106269. https://www.sciencedirect.com/science/article/pii/S0001706X21004472?via%3Dihub. Accessed 19 May 2022

  • Mekhlif AF, Khudhair GT (2016) Bioactivity of three cyanobacterial blooms against Culex pipens molestus (Diptera: Culiciday). Int J Res 3:354–363

    Google Scholar 

  • N’Guessan R, Corbel V, Akogbéto M, Rowland M (2007) Reduced efficacy of insecticide-treated nets and indoor residual spraying for malaria control in pyrethroid resistance area, Benin. Emerg Infect Dis 13:199–206

    Article  Google Scholar 

  • Okumu FO, Knols BGJ, Fillinger U (2007) Larvicidal effects of a neem (Azadirachta indica) oil formulation on the malaria vector Anopheles gambiae. Malar J 6:63

    Article  Google Scholar 

  • Rai SV, Rajashekhar M (2015) Effect of twelve species of marine phytoplankton on larval survival and development of the mosquito Culex quinquefasciatus. Int J Mar Sci 5(56):1–5

  • Rembold H, Sharma GK, Czoppelt Ch, Schmutterer H (1982) Azadirachtin: A potent insect growth regulator of plant origin. Z Angew Entomol 93:12–17

    Article  CAS  Google Scholar 

  • Rettich F, Popovský J, Cepák V (2001) Algae and blue-green algae as mosquito food [in Czech]. Fottea 1:93–101

    Google Scholar 

  • Riaz MA, Chandor-Proust A, Dauphin-Villemant C, Poupardin R, Jones CM, Strode C, Régent-Kloeckner M, David JP, Reynaud S (2012) Molecular mechanisms associated with increased tolerance to the neonicotinoid insecticide imidacloprid in the dengue vector Aedes aegypti. Aquat Toxicol Amst Neth 126:326–337

    Article  Google Scholar 

  • Rodhain F, Perez C (1985) Precis d’entomologie medicale et veterinaire; notions d’epidemiologie des maladies a vecteurs. Maloine, Paris

  • Rudolfs W, Lackey JB (1929) The composition of water and mosquito breeding. Am J Epidemiol 9:160–180

    Article  CAS  Google Scholar 

  • Saario E, Abdel-Hameed A, Kiviranta J (1994) Larvicidal microcystin toxins of cyanobacteria affect midgut epithelial cells of Aedes aegypti mosquitoes. Med Vet Entomol 8:398–400

    Article  CAS  Google Scholar 

  • Sen P (1938) On some physico-chemical and vegetation factors of the breeding places of Anopheles sundaicus Rodenw. J Malar Inst India 1(3):257–260

  • Sen P (1941) Aquatic plants in the ecology of anopheline mosquitoes. J Malar Inst India 4:113–137

    Google Scholar 

  • Su T, Mulla M (2000) Effects of neem products containing azadirachtin on blood feeding, fecundity, and survivorship of Culex tarsalis and Culex quinquefasciatus (Diptera: Culicidae). J Soc Vector Ecol 24:202–215

    Google Scholar 

  • Tuno N, Githeko A, Nakayama T, Minakawa N, Takagi M, Yan G (2005) The association between the phytoplankton, Rhopalosolen species (Chlorophyta; Chlorophyceae), and Anopheles gambiae sensu lato (Diptera: Culicidae) larval abundance in western Kenya. Ecol Res 21:476–482

    Article  Google Scholar 

  • Vázquez-Martínez MG, Rodríguez MH, Arredondo-Jiménez JI, Méndez-Sanchez JD, Bond-Compeán JG, Cold-Morgan M (2002) Cyanobacteria associated with Anopheles albimanus (Diptera: Culicidae) larval habitats in southern Mexico. J Med Entomol 39:825–832

    Article  Google Scholar 

  • WHO (2015) Stratégie technique mondiale de lutte contre le paludisme 2016–2030. World Health Organization, Geneva

    Google Scholar 

  • WHO (2020) World Malaria Report 2020. World Health Organization, Geneva. https://www.who.int/teams/global-malaria-programme/reports/world-malaria-report-2020. Accessed 22 Feb 2021

  • WHO (2021) Rapport 2021 sur le paludisme dans le monde, Principaux messages. World Health Organisation, Geneva pp 1–24

  • Zebitz CPW (1986) Effects of three different neem seed kernel extracts and azadirachtin on larvae of different mosquito species. J Appl Entomol 102:455–463

    Article  CAS  Google Scholar 

  • Zoh DD, Alou LPA, Toure M, Pennetier C, Camara S, Traore DF, Koffi AA, Adja AM, Yapi A, Chandre F (2018) The current insecticide resistance status of Anopheles gambiae (sl)(Culicidae) in rural and urban areas of Bouaké, Côte d’Ivoire. Parasites Vectors 11:118

    Article  Google Scholar 

Download references

Acknowledgements

Thanks to Noël HOUNTY, Sebatien KOUDENOUKPO, Sêdomèdji HOUNMASSE, Armand KPODO, Darius TOSSAVI and Yaovi ZOUNNON for their participation in this study.

Author information

Authors and Affiliations

Authors

Contributions

DA, SE, LMND, AR, BA, SC, AM, FED and HL conceived and designed the study. DA and SE coordinated the study. HL sampled and identified the phytoplankton in all potential mosquitoes breeding habitat in the selected sites. LMND, AR and HL participated in the monospecific production of Scenedesmus quadricauda and in the monitoring of culture. DA, BA, SC and HL participated in the Bioassays in laboratory and to collect the data. DA, LMND and HL analyzed and interpreted data, and prepared the draft manuscript. HL wrote the original draft. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Lenucthadius Yao Houessou.

Ethics declarations

Competing interests

The authors declare that they have 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

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 195 kb)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Houessou, L.Y., Djènontin, A., Sossoukpè, E. et al. Exploring phytoplankton management for controlling the malaria vector Anopheles gambiae in Benin. J Appl Phycol 35, 495–508 (2023). https://doi.org/10.1007/s10811-022-02883-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-022-02883-z

Keywords

Navigation