The effect of pollution on the competitive dynamics of Anopheles arabiensis Patton, 1905 and Culex quinquefasciatus Say, 1823 (Diptera: Culicidae)

Authors

  • Alexander CSN Jeanrenraud Centre for Emerging Zoonotic and Parasitic Diseases, National Institute for Communicable Diseases of the National Health Laboratory Service, Johannesburg, South Africa; Wits Research Institute for Malaria, School of Pathology, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa https://orcid.org/0000-0002-4230-9976
  • Blaženka D Letinić Wits Research Institute for Malaria, School of Pathology, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa https://orcid.org/0000-0002-2659-4324
  • Jean Mollett School of Molecular and Cell Biology, Faculty of Science, University of the Witwatersrand, Johannesburg, South Africa
  • Basil D Brooke Centre for Emerging Zoonotic and Parasitic Diseases, National Institute for Communicable Diseases of the National Health Laboratory Service, Johannesburg, South Africa; Wits Research Institute for Malaria, School of Pathology, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa https://orcid.org/0000-0002-8857-1304
  • Shüné Oliver Centre for Emerging Zoonotic and Parasitic Diseases, National Institute for Communicable Diseases of the National Health Laboratory Service, Johannesburg, South Africa; Wits Research Institute for Malaria, School of Pathology, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa https://orcid.org/0000-0002-2140-2725

DOI:

https://doi.org/10.17159/2254-8854/2023/a10656

Keywords:

copper nitrate , detoxification enzymes , inorganic fertiliser , maximum acceptable toxicity concentration , tolerance

Abstract

Culex quinquefasciatus Say, 1823 and Anopheles arabiensis Patton, 1905 (Diptera: Culicidae) are often found breeding in the same water sources and engage in interspecific competition. Although Cx. quinquefasciatus is known to proliferate in a range of polluted environments, the ability of An. arabiensis to proliferate in polluted water has only been reported relatively recently. The effects of pollution and insecticide resistance on this competitive interaction are unknown. This study examined the effect of pollution on the dynamics of the interspecific competition. Three laboratory strains were used in this study: an insecticide susceptible and an insecticide resistant An. arabiensis, and an insecticide resistant Cx. quinquefasciatus. Larval pollutant tolerances of each strain were assessed and compared by determining the lethal concentration at 50% mortality (LC50). The larvae from each strain were exposed to either inorganic fertiliser or copper nitrate, following which eclosion success was assessed. The results showed that the insecticide resistant strains had higher emergence rates when reared in polluted conditions without competition, with the Cx. quinquefasciatus strain showing the highest rate of eclosion. This species also had a higher tolerance for metal pollution than the An. arabiensis strains. The effects of pollutants on oviposition choice were examined. Pollution altered adult oviposition choice. The effect of larval metal exposure had variable effects on the activity of metabolic detoxification enzymes. An insecticide resistant phenotype had greater tolerance to pollutants and possibly developmental advantages based on a variable detoxification response to the pollutant. Pollution can therefore alter interspecific competition dynamics between the malaria vector An. arabiensis and Cx. quinquefasciatus

Downloads

Download data is not yet available.

Metrics

Metrics Loading ...

References

Abbott WS. 1925. A method of computing the effectiveness of an insecticide. Journal of Economic Entomology 18(2): 265–267. https://10.1093/jee/18.2.265a

Alto BW, Lampman RL, Kesavaraju B, Muturi EJ. 2013. Pesticide-induced release from competition among competing Aedes aegypti and Aedes albopictus (Diptera: Culicidae). Journal of Medical Entomology 50(6): 1240–1249. https://10.1603/ME12135

Antonio-Nkondjio C, Fossog BT, Ndo C, Djantio BM, Togouet SZ, Awono-Ambene P, Costantini C, Wondji CS, Ranson H. 2011. Anopheles gambiae distribution and insecticide resistance in the cities of Douala and Yaounde (Cameroon): influence of urban agriculture and pollution. Malaria Journal 10(1): 154. https://10.1186/1475-2875-10-154

Awolola TS, Oduola AO, Obansa JB, Chukwurar NJ, Unyimadu JP. 2007. Anopheles gambiae s.s. breeding in polluted water bodies in urban Lagos, southwestern Nigeria. Journal Vector Borne Diseases 44:2 41–244.

Bartlow AW, Manore C, Xu C, Kaufeld KA, Del Valle S, Ziemann A, Fairchild G, Fair JM. 2019. Forecasting zoonotic infectious disease response to climate change: Mosquito vectors and a changing environment. Veterinary Sciences 6(2): 40. https://10.3390/vetsci6020040

Bartlett MS. 1937. Properties of sufficiency and statistical tests. Proceedings of the Royal Society of London. Series A, Mathematical and Physical Sciences 160: 268–282.

Bashir A, Hassan AA, Salmah MR, Rahman WA. 2008. Efficacy of agnique (mmf) monomolecular surface film against immature stages of Anopheles arabiensis Patton and Culex spp (Diptera: Culicidae) in Khartoum, Sudan. The Southeast Asian Journal of Tropical Medicine and Public Health 39: 222–228.

Calhoun LM, King R, Gunarto K, Burkot TR, Jones LA, Roberts J, Avery M. 2007 Combined sewage overflows (CSO) are major urban breeding sites for Culex quinquefasciatus in Atlanta, Georgia. The American Journal of Tropical Medicine and Hygiene 77(3): 478–484. https://10.4269/ajtmh.2007.77.478

Camara DC, Codeco CT, Juliano SA, Lounibos LP, Riback TI, Pereira GR, Honorio NA. 2016. Seasonal differences in density but similar competitive impact of Aedes albopictus (Skuse) on Aedes aegypti (L.) in Rio de Janeiro, Brazil. PLoS One 11(6): e0157120. https://10.1371/journal.pone.0157120

Charlwood JD. 1994. The control of Culex quinquefasciatus breeding in septic tanks using expanded polystyrene beads in southern Tanzania. Transactions of the Royal Society of Tropical Medicine and Hygiene 88(4): 380. https://10.1016/0035-9203(94)90390-5

Correia JC, Barbosa RM, Oliveira CM, Albuquerque CM. 2012. Residential characteristics aggravating infestation by Culex quinquefasciatus in a region of Northeastern Brazil. Revista de Saude Publica 46(6): 935–941. https://10.1590/S0034-89102013005000010

Davies C, Coetzee M, Lyons CL. 2016. Effect of stable and fluctuating temperatures on the life history traits of Anopheles arabiensis and An. quadriannulatus under conditions of inter- and intra-specific competition. Parasites & Vectors 9(1): 342. https://10.1186/s13071-016-1630-2

Donohue I, Garcia Molinos J. 2009. Impacts of increased sediment loads on the ecology of lakes. Biological Reviews of the Cambridge Philosophical Society 84(4): 517–531. https://10.1111/j.1469-185X.2009.00081.x

Elimam AM, Elmalik KH, Ali FS. 2009a. Larvicidal, adult emergence inhibition and oviposition deterrent effects of foliage extract from Ricinus communis L. against Anopheles arabiensis and Culex quinquefasciatus in Sudan. Tropical Biomedicine 26: 130–139.

Elimam AM, Elmalik KH, Ali FS. 2009b. Efficacy of leaves extract of Calotropis procera Ait. (Asclepiadaceae) in controlling Anopheles arabiensis and Culex quinquefasciatus mosquitoes. Saudi Journal of Biological Sciences 16(2): 95–100. https://10.1016/j.sjbs.2009.10.007

Farjana T, Tuno N, Higa Y. 2012. Effects of temperature and diet on development and interspecies competition in Aedes aegypti and Aedes albopictus. Medical and Veterinary Entomology 26(2): 210–217. https://10.1111/j.1365-2915.2011.00971.x

Finney DJ. 1952. Probit Analysis. 2nd ed. New York: Cambridge University Press.

Gillies, M. T. & Meillon, B. D. 1968. The Anophelinae of Africa south of the Sahara (Ethiopian Zoogeographical Region). Publications of the South African Institute for Medical Research. No. 54. Johannesburg: SAIMR.

Gimonneau G, Brossette L, Mamai W, Dabire RK, Simard F. 2014. Larval competition between An. coluzzii and An. gambiae in insectary and semi-field conditions in Burkina Faso. Acta Tropica 130: 155–161. https://10.1016/j.actatropica.2013.11.007

Githeko AK, Service MW, Mbogo CM, Atieli FK. 1996. Resting behaviour, ecology and genetics of malaria vectors in large scale agricultural areas of Western Kenya. Parassitologia 38: 481–489.

Hunt RH, Brooke BD, Pillay C, Koekemoer LL, Coetzee M. 2005. Laboratory selection for and characteristics of pyrethroid resistance in the malaria vector Anopheles funestus. Medical and Veterinary Entomology 19(3): 271–275. https://10.1111/j.1365-2915.2005.00574.x

Ijumba JN, Lindsay SW. 2001. Impact of irrigation on malaria in Africa: paddies paradox. Medical and Veterinary Entomology 15(1): 1–11. https://10.1046/j.1365-2915.2001.00279.x

Impoinvil DE, Keating J, Mbogo CM, Potts MD, Chowdhury RR, Beier JC. 2008. Abundance of immature Anopheles and culicines (Diptera: Culicidae) in different water body types in the urban environment of Malindi, Kenya. Journal of Vector Ecology 33(1): 107–116. https://10.3376/1081-1710(2008)33[107:AOIAAC]2.0.CO;2

Jacob BG, Arheart KL, Griffith DA, Mbogo CM, Githeko AK, Regens JL, Githure JI, Novak R, Beier JC. 2005. Evaluation of environmental data for identification of Anopheles (Diptera: Culicidae) aquatic larval habitats in Kisumu and Malindi, Kenya. Journal of Medical Entomology 42(5): 751–755. https://10.1093/jmedent/42.5.751

Jones CM, Toe HK, Sanou A, Namountougou M, Hughes A, Diabate A, Dabire R, Simard F, Ranson H. 2012. Additional selection for insecticide resistance in urban malaria vectors: DDT resistance in Anopheles arabiensis from Bobo-Dioulasso, Burkina Faso. PLoS One 7(9):e45995. https://10.1371/journal.pone.0045995

Kibuthu TW, Njenga SM, Mbugua AK, Muturi EJ. 2016. Agricultural chemicals: Life changer for mosquito vectors in agricultural landscapes? Parasites & Vectors 9(1): 500. https://10.1186/s13071-016-1788-7

Killeen GF. 2014. Characterizing, controlling and eliminating residual malaria transmission. Malaria Journal 13(1): 330. https://10.1186/1475-2875-13-330

Kirby MJ, Lindsay SW. 2009. Effect of temperature and inter-specific competition on the development and survival of Anopheles gambiae sensu stricto and An. arabiensis larvae. Acta Tropica 109(2): 118–123. https://10.1016/j.actatropica.2008.09.025

Kitau J, Oxborough RM, Tungu PK, Matowo J, Malima RC, Magesa SM, Bruce J, Mosha FW, Rowland MW. 2012. Species shifts in the Anopheles gambiae complex: do LLINs successfully control Anopheles arabiensis? PLoS One 7(3): e31481. https://10.1371/journal.pone.0031481

Koenraadt CJ, Takken W. 2003. Cannibalism and predation among larvae of the Anopheles gambiae complex. Medical and Veterinary Entomology 17(1): 61–66. https://10.1046/j.1365-2915.2003.00409.x

Kweka EJ, Zhou G, Beilhe LB, Dixit A, Afrane Y, Gilbreath TM 3rd, Munga S, Nyindo M, Githeko AK, Yan G. 2012. Effects of co-habitation between Anopheles gambiae s.s. and Culex quinquefasciatus aquatic stages on life history traits. Parasites & Vectors 5(1): 33. https://10.1186/1756-3305-5-33

Kramer WL, Mulla MS. 1979. Oviposition attractants and repellents of mosquitoes: oviposition responses of Culex mosquitoes to organic infusions. Environmental Entomology 8(6): 1111–1117. https://10.1093/ee/8.6.1111

Lounibos LP, Bargielowski I, Carrasquilla MC, Nishimura N. 2016. Coexistence of Aedes aegypti and Aedes albopictus (Diptera: Culicidae) in Peninsular Florida two decades after competitive displacements. Journal of Medical Entomology 53(6): 1385–1390. https://10.1093/jme/tjw122

Matson P, Lohse KA, Hall SJ. 2002. The globalization of nitrogen deposition: consequences for terrestrial ecosystems. Ambio 31(2): 113–119. https://10.1579/0044-7447-31.2.113

Mireji PO, Keating J, Hassanali A, Mbogo CM, Muturi MN, Githure JI, Beier JC. 2010. Biological cost of tolerance to heavy metals in the mosquito Anopheles gambiae. Medical and Veterinary Entomology 24(2): 101–107. https://10.1111/j.1365-2915.2010.00863.x.

Mireji PO, Keating J, Hassanali A, Mbogo CM, Nyambaka H, Kahindi S, Beier JC. 2008. Heavy metals in mosquito larval habitats in urban Kisumu and Malindi, Kenya, and their impact. Ecotoxicology and Environmental Safety 70(1): 147–153. https://10.1016/j.ecoenv.2007.03.012

Musasia FK, Isaac AO, Masiga DK, Omedo IA, Mwakubambanya R, Ochieng R, Mireji PO. 2013. Sex-specific induction of CYP6 cytochrome P450 genes in cadmium and lead tolerant Anopheles gambiae. Malaria Journal 12(1): 97. https://10.1186/1475-2875-12-97

Muturi EJ, Costanzo K, Kesavaruju B, Lampman R, Alto BW. 2010. Interaction of a pesticide and larval competition on life history traits of Culex pipiens. Acta Tropica 116: 141–146.

Muturi EJ, Kim CH, Jacob B, Murphy S, Novak RJ. 2010, Interspecies predation between Anopheles gambiae s.s. and Culex quinquefasciatus larvae. Journal of Medical Entomology 47(2): 287–290. https://10.1093/jmedent/47.2.287

Muturi EJ, Mwangangi J, Shililu J, Jacob BG, Mbogo C, Githure J, Novak RJ. 2008. Environmental factors associated with the distribution of Anopheles arabiensis and Culex quinquefasciatus in a rice agro-ecosystem in Mwea, Kenya. Journal of Vector Ecology 33(1): 56–63. https://10.3376/1081-1710(2008)33[56:EFAWTD]2.0.CO;2

Muturi EJ, Mwangangi J, Shililu J, Muriu S, Jacob B, Kabiru E, Gu W, Mbogo C, Githure J, Novak R. 2007. Mosquito species succession and physicochemical factors affecting their abundance in rice fields in Mwea, Kenya. Journal of Medical Entomology 44(2): 336–344. https://10.1093/jmedent/44.2.336

Mutero CM, Ng’ang’a PN, Wekoyela P, Githure J, Konradsen F. 2004. Ammonium sulphate fertiliser increases larval populations of Anopheles arabiensis and culicine mosquitoes in rice fields. Acta Tropica 89(2): 187–192. https://10.1016/j.actatropica.2003.08.006

Mwangangi JM, Muturi EJ, Shililu J, Muriu SM, Jacob B, Kabiru EW, Mbogo CM, Githure J, Novak R. 2008. Contribution of different aquatic habitats to adult Anopheles arabiensis and Culex quinquefasciatus (Diptera: Culicidae) production in a rice agroecosystem in Mwea, Kenya. Journal of Vector Ecology 33(1): 129–138. https://10.3376/1081-1710(2008)33[129:CODAHT]2.0.CO;2

Mwangangi J, Shililu J, Muturi E, Gu W, Mbogo C, Kabiru E, Jacob B, Githure J, Novak R. 2006. Dynamics of immature stages of Anopheles arabiensis and other mosquito species (Diptera: Culicidae) in relation to rice cropping in a rice agro-ecosystem in Kenya. Journal of Vector Ecology 31(2): 245–251. https://10.3376/1081-1710(2006)31[245:DOISOA]2.0.CO;2

Noden BH, O’Neal PA, Fader JE, Juliano SA. 2016. Impact of inter- and intra-specific competition among larvae on larval, adult, and life-table traits of Aedes aegypti and Aedes albopictus females. Ecological Entomology 41(2): 192–200. https://10.1111/een.12290

Oliver SV. 2021. The effect of larval cigarette exposure on the life history of the major malaria vector Anopheles arabiensis (Diptera: Culicidae). Transactions of the Royal Society of South Africa 76(2): 117–125. https://10.1080/0035919X.2021.1887004

Oliver SV, Brooke BD. 2013. The effect of larval nutritional deprivation on the life history and DDT resistance phenotype in laboratory strains of the malaria vector Anopheles arabiensis. Malaria Journal 12(1): 44. https://10.1186/1475-2875-12-44

Oliver SV, Brooke BD. 2017,The effect of elevated temperatures on the life history and insecticide resistance phenotype of the major malaria vector Anopheles arabiensis (Diptera: Culicidae). Malaria Journal 16(1): 73. https://10.1186/s12936-017-1720-4

Oliver SV, Brooke BD. 2018a. The effect of commercial herbicide exposure on the life history and insecticide resistance phenotypes of the major malaria vector Anopheles arabiensis (Diptera: Culicidae). Acta Tropica 188: 152–160. https://10.1016/j.actatropica.2018.08.030

Oliver SV, Brooke BD. 2018b. The effect of metal pollution on the life history and insecticide resistance phenotype of the major malaria vector Anopheles arabiensis (Diptera: Culicidae). PLoS One 13(2): e0192551. https://10.1371/journal.pone.0192551

Reiskind MH, Lounibos LP. 2009. Effects of intraspecific larval competition on adult longevity in the mosquitoes Aedes aegypti and Aedes albopictus. Medical and Veterinary Entomology 23(1): 62–68. https://10.1111/j.1365-2915.2008.00782.x

Samuel M, Brooke BD, Oliver SV. 2020. Effects of inorganic fertilizer on larval development, adult longevity and insecticide susceptibility in the malaria vector Anopheles arabiensis (Diptera: Culicidae). Pest Management Science 76(4): 1560–1568. https://10.1002/ps.5676

Schneider P, Takken W, Mccall PJ. 2000. Interspecific competition between sibling species larvae of Anopheles arabiensis and An. gambiae. Medical and Veterinary Entomology 14(2): 165–170. https://10.1046/j.1365-2915.2000.00204.x

Shapiro SS, Wilk MB. 1965. An analysis of variance test for normality (complete samples). Biometrika 52(3-4): 591–611. https://10.1093/biomet/52.3-4.591

Sheehan D, Meade G, Foley VM, Dowd CA. 2001. Structure, function and evolution of glutathione transferases: implications for classification of non-mammalian members of an ancient enzyme superfamily. The Biochemical Journal 360(1): 1–16. https://10.1042/bj3600001

Sinka ME, Bangs MJ, Manguin S, Coetzee M, Mbogo CM, Hemingway J, Patil AP, Temperley WH, Gething PW, Kabaria CW, et al. 2010. The dominant Anopheles vectors of human malaria in Africa, Europe and the Middle East: occurrence data, distribution maps and bionomic precis. Parasites & Vectors 3(1): 117. https://10.1186/1756-3305-3-117

Tukey JW. 1949. Comparing individual means in the analysis of variance. Biometrics 5(2): 99–114. https://10.2307/3001913

WHO [World Health Organisation]. 2005. Guidelines for laboratory and field testing of mosquito larvicides. Geneva: WHO

Yee DA, Himel E, Reiskind MH, Vamosi SM. 2014;. Implications of saline concentrations for the performance and competitive interactions of the mosquitoes Aedes aegypti (Stegomyia aegypti) and Aedes albopictus (Stegomyia albopictus). Medical and Veterinary Entomology 28(1): 60–69. https://10.1111/mve.12007

Downloads

Published

2023-05-10

How to Cite

1.
Jeanrenraud AC, Letinić BD, Mollett J, Brooke BD, Oliver S. The effect of pollution on the competitive dynamics of Anopheles arabiensis Patton, 1905 and Culex quinquefasciatus Say, 1823 (Diptera: Culicidae). Afr. Entomol. [Internet]. 2023 May 10 [cited 2024 May 27];31. Available from: https://www.africanentomology.com/article/view/10656

Issue

Section

Articles