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Published in: Malaria Journal 1/2017

Open Access 01-12-2017 | Research

Does mosquito mass-rearing produce an inferior mosquito?

Authors: Dieudonné D. Soma, Hamidou Maïga, Wadaka Mamai, Nanwintoun S. Bimbile-Somda, Nelius Venter, Adel B. Ali, Hanano Yamada, Abdoulaye Diabaté, Florence Fournet, Georges A. Ouédraogo, Rosemary S. Lees, Roch K. Dabiré, Jeremie R. L. Gilles

Published in: Malaria Journal | Issue 1/2017

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Abstract

Background

The success of the sterile insect technique depends, among other things, on continuous releases of sexually competitive sterile males within the target area. Several factors (including high rearing density and physical manipulation, such as larvae and pupae separation) can influence the quality of males produced in mass-rearing facilities. The different steps in mass production in the laboratory may modify the behaviour of mosquitoes, directly or through loss of natural characters as a result of adaptation to lab rearing, and lead to the competitiveness of sterile male being reduced. In the present study, the objective was to evaluate the effect of mass-rearing conditions on sterile male sexual competitiveness in semi-field cages compared to routine small scale laboratory rearing methods.

Methods

Anopheles arabiensis immature stages were reared both on a large scale using a rack and tray system developed by the FAO/IAEA (MRS), and on a small scale using standard laboratory rearing trays (SRS). Mosquito life history traits such as pupation rate, emergence rate, adult size as well as the effect of irradiation on adult longevity were evaluated. Moreover, 5–6 day old mosquitoes were released into field cages and left for two nights to mate and the mating competitiveness between sterile mass-reared males and fertile males reared on a small scale when competing for small scale reared virgin females was investigated. Resulting fertility in a treatment ratio of 1:1:1 (100 irradiated males: 100 non-irradiated males: 100 virgin females) was compared to control cages with 0:100:100 (non-irradiated control) and 100:0:100 (irradiated control).

Results

No significant differences in life history parameters were observed between rearing methods. The competitiveness index of mass reared males (0.58) was similar to males reared on a small scale (0.59). A residual fertility rate of 20% was observed in the irradiated control (100:0:100), measured as the percentage of eggs collected from the cages which developed to adulthood. No significant difference was observed (t = 0.2896, df = 4, P = 0.7865) between the rearing treatments (MRS and SRS) in the fertility rate, a measure of mating competitiveness.

Conclusions

The results showed that the FAO/IAEA mass-rearing process did not affect mosquito life history parameters or the mating competitiveness of males.
Literature
2.
go back to reference Brady OJ, Godfray HCJ, Tatem AJ, Gething PW, Cohen JM, Ellis McKenzie F, et al. Adult vector control, mosquito ecology and malaria transmission. Int Health. 2015;7:121–9.CrossRefPubMedPubMedCentral Brady OJ, Godfray HCJ, Tatem AJ, Gething PW, Cohen JM, Ellis McKenzie F, et al. Adult vector control, mosquito ecology and malaria transmission. Int Health. 2015;7:121–9.CrossRefPubMedPubMedCentral
3.
go back to reference Dabiré KR, Diabaté A, Djogbenou L, Ouari A, Guessan RN, Ouédraogo J, et al. Dynamics of multiple insecticide resistance in the malaria vector. Malar J. 2008;7:188.CrossRefPubMedPubMedCentral Dabiré KR, Diabaté A, Djogbenou L, Ouari A, Guessan RN, Ouédraogo J, et al. Dynamics of multiple insecticide resistance in the malaria vector. Malar J. 2008;7:188.CrossRefPubMedPubMedCentral
4.
go back to reference Namountougou M, Simard F, Baldet T, Diabaté A, Ouédraogo JB, Martin T, et al. Multiple insecticide resistance in Anopheles gambiae s.l. populations from Burkina Faso, West Africa. PLoS ONE. 2012;7:e48412.CrossRefPubMedPubMedCentral Namountougou M, Simard F, Baldet T, Diabaté A, Ouédraogo JB, Martin T, et al. Multiple insecticide resistance in Anopheles gambiae s.l. populations from Burkina Faso, West Africa. PLoS ONE. 2012;7:e48412.CrossRefPubMedPubMedCentral
5.
go back to reference Mosqueira B, Soma DD, Namountougou M, Poda S, Diabaté A, Ali O, et al. Pilot study on the combination of an organophosphate-based insecticide paint and pyrethroid-treated long lasting nets against pyrethroid resistant malaria vectors in Burkina Faso. Acta Trop. 2015;148:162–9.CrossRefPubMed Mosqueira B, Soma DD, Namountougou M, Poda S, Diabaté A, Ali O, et al. Pilot study on the combination of an organophosphate-based insecticide paint and pyrethroid-treated long lasting nets against pyrethroid resistant malaria vectors in Burkina Faso. Acta Trop. 2015;148:162–9.CrossRefPubMed
6.
go back to reference Reid MC, McKenzie FE. The contribution of agricultural insecticide use to increasing insecticide resistance in African malaria vectors. Malar J. 2016;15:107.CrossRefPubMedPubMedCentral Reid MC, McKenzie FE. The contribution of agricultural insecticide use to increasing insecticide resistance in African malaria vectors. Malar J. 2016;15:107.CrossRefPubMedPubMedCentral
7.
go back to reference Agomo CO, Oyibo WA, Sutherland C, Hallet R, Oguike M. Assessment of markers of antimalarial drug resistance in Plasmodium falciparum isolates from pregnant women in Lagos, Nigeria. PLoS ONE. 2016;11:e0146908.CrossRefPubMedPubMedCentral Agomo CO, Oyibo WA, Sutherland C, Hallet R, Oguike M. Assessment of markers of antimalarial drug resistance in Plasmodium falciparum isolates from pregnant women in Lagos, Nigeria. PLoS ONE. 2016;11:e0146908.CrossRefPubMedPubMedCentral
8.
go back to reference Enayati A, Lines J, Maharaj R HJ. Shrinking the Malaria Map: A prospectus on malaria elimination. Feachem RGA, Phillips AA, Targett GA, editors. Chapt. 9: Suppressing the Vector. San Francisco: The Global Health Group, 2009. p. 140–54. Enayati A, Lines J, Maharaj R HJ. Shrinking the Malaria Map: A prospectus on malaria elimination. Feachem RGA, Phillips AA, Targett GA, editors. Chapt. 9: Suppressing the Vector. San Francisco: The Global Health Group, 2009. p. 140–54.
10.
go back to reference Lees RS, Knols B, Bellini R, Benedict MQ, Bheecarry A, Bossin HC, et al. Review: improving our knowledge of male mosquito biology in relation to genetic control programmes. Acta Trop. 2014;132:S2–11.CrossRefPubMed Lees RS, Knols B, Bellini R, Benedict MQ, Bheecarry A, Bossin HC, et al. Review: improving our knowledge of male mosquito biology in relation to genetic control programmes. Acta Trop. 2014;132:S2–11.CrossRefPubMed
11.
go back to reference Dame DA, Lowe RE. Assessment of released sterile Anopheles albimanus and Glossina morsitans morsitans. In: Pal R, Kitzmiller J, Kanda TA, editors. Cytogenetics and genetics of vectors. Netherlands: Elsevier Biomedical; 1981. p. 231–48. Dame DA, Lowe RE. Assessment of released sterile Anopheles albimanus and Glossina morsitans morsitans. In: Pal R, Kitzmiller J, Kanda TA, editors. Cytogenetics and genetics of vectors. Netherlands: Elsevier Biomedical; 1981. p. 231–48.
12.
go back to reference Helinski H, Knols J. Mating competitiveness of male Anopheles arabiensis mosquitoes irradiated with a partially or fully sterilizing dose in small and large laboratory cages. J Med Entomol. 2008; 698–705. Helinski H, Knols J. Mating competitiveness of male Anopheles arabiensis mosquitoes irradiated with a partially or fully sterilizing dose in small and large laboratory cages. J Med Entomol. 2008; 698–705.
14.
15.
go back to reference Maïga H, Damiens D, Niang A, Sawadogo SP, Fatherhaman O, Lees RS, et al. Mating competitiveness of sterile male Anopheles coluzzii in large cages. Malar J. 2014;13:460.CrossRefPubMedPubMedCentral Maïga H, Damiens D, Niang A, Sawadogo SP, Fatherhaman O, Lees RS, et al. Mating competitiveness of sterile male Anopheles coluzzii in large cages. Malar J. 2014;13:460.CrossRefPubMedPubMedCentral
16.
go back to reference Yamada H, Vreysen MJB, Gilles JRL, Munhenga G, Damiens DD. The effects of genetic manipulation, dieldrin treatment and irradiation on the mating competitiveness of male Anopheles arabiensis in field cages. Malar J. 2014;13:318.CrossRefPubMedPubMedCentral Yamada H, Vreysen MJB, Gilles JRL, Munhenga G, Damiens DD. The effects of genetic manipulation, dieldrin treatment and irradiation on the mating competitiveness of male Anopheles arabiensis in field cages. Malar J. 2014;13:318.CrossRefPubMedPubMedCentral
17.
go back to reference Munhenga G, Brooke BD, Gilles JRL, Slabbert K, Kemp A, Dandalo LC, et al. Mating competitiveness of sterile genetic sexing strain males (GAMA) under laboratory and semi-field conditions: steps towards the use of the Sterile Insect Technique to control the major malaria vector Anopheles arabiensis in South Africa. Parasit Vectors. 2016;9:122.CrossRefPubMedPubMedCentral Munhenga G, Brooke BD, Gilles JRL, Slabbert K, Kemp A, Dandalo LC, et al. Mating competitiveness of sterile genetic sexing strain males (GAMA) under laboratory and semi-field conditions: steps towards the use of the Sterile Insect Technique to control the major malaria vector Anopheles arabiensis in South Africa. Parasit Vectors. 2016;9:122.CrossRefPubMedPubMedCentral
18.
go back to reference Maiga H, Bimbilé-Somda NS, Yamada H, Wood O, Damiens D, Mamai W, et al. Enhancements to the mass rearing cage for the malaria vector, Anopheles arabiensis for improved adult longevity and egg production. Entomol Exp Appl. 2017. 10.1111/eea.12614. Maiga H, Bimbilé-Somda NS, Yamada H, Wood O, Damiens D, Mamai W, et al. Enhancements to the mass rearing cage for the malaria vector, Anopheles arabiensis for improved adult longevity and egg production. Entomol Exp Appl. 2017. 10.​1111/​eea.​12614.
19.
go back to reference Cosgrove JB, Wood RJ, Petric D, Evans DT, Abbott RH. A convenient mosquito membrane feeding system. J Am Mosq Control Assoc. 1994;10:434–6.PubMed Cosgrove JB, Wood RJ, Petric D, Evans DT, Abbott RH. A convenient mosquito membrane feeding system. J Am Mosq Control Assoc. 1994;10:434–6.PubMed
20.
go back to reference Maïga H, Damiens D, Diabaté A, Dabiré R, Ouédraogo G, Lees R, et al. Large-scale Anopheles arabiensis egg quantification methods for mass rearing operations. Malar J. 2016;15:72.CrossRefPubMedPubMedCentral Maïga H, Damiens D, Diabaté A, Dabiré R, Ouédraogo G, Lees R, et al. Large-scale Anopheles arabiensis egg quantification methods for mass rearing operations. Malar J. 2016;15:72.CrossRefPubMedPubMedCentral
21.
go back to reference Balestrino F, Benedict MQ. A new larval tray and rack system for improved mosquito mass rearing. J Med Entomol. 2012;49:595–605.CrossRefPubMed Balestrino F, Benedict MQ. A new larval tray and rack system for improved mosquito mass rearing. J Med Entomol. 2012;49:595–605.CrossRefPubMed
22.
go back to reference Damiens D, Benedict MQ, Wille M. An inexpensive and effective larval diet for Anopheles arabiensis (Diptera: Culicidae): eat like a horse, a bird, or a fish? Entomol Soc Am. 2012;49:1001–11. Damiens D, Benedict MQ, Wille M. An inexpensive and effective larval diet for Anopheles arabiensis (Diptera: Culicidae): eat like a horse, a bird, or a fish? Entomol Soc Am. 2012;49:1001–11.
23.
go back to reference IAEA. Guidelines for standardised mass rearing of Anopheles Mosquitoes. Vienna: International Atomic Energy Agency; 2015. IAEA. Guidelines for standardised mass rearing of Anopheles Mosquitoes. Vienna: International Atomic Energy Agency; 2015.
24.
go back to reference Mamai W, Lees RS, Maiga H, Gilles JRL. Reusing larval rearing water and its effect on development and quality of Anopheles arabiensis mosquitoes. Malar J. 2016;15:169.CrossRefPubMedPubMedCentral Mamai W, Lees RS, Maiga H, Gilles JRL. Reusing larval rearing water and its effect on development and quality of Anopheles arabiensis mosquitoes. Malar J. 2016;15:169.CrossRefPubMedPubMedCentral
25.
go back to reference MR4. Separating larvae and pupae. In: Methods in Anopheles research. 4th edition. Atlanta: Centers for Disease Control and Prevention; 2014. MR4. Separating larvae and pupae. In: Methods in Anopheles research. 4th edition. Atlanta: Centers for Disease Control and Prevention; 2014.
26.
go back to reference Lyimo EO, Koella JC. Relationship between body size of adult Anopheles gambiae s.l. and infection with the malaria parasite Plasmodium falciparum. Parasitology. 1992;104(Pt 2):233–7.CrossRefPubMed Lyimo EO, Koella JC. Relationship between body size of adult Anopheles gambiae s.l. and infection with the malaria parasite Plasmodium falciparum. Parasitology. 1992;104(Pt 2):233–7.CrossRefPubMed
27.
go back to reference Koella JC, Lyimo EO. Variability in the relationship between weight and wing length of Anopheles gambiae (Diptera: Culicidae). J Med Entomol. 1996;33:261–4.CrossRefPubMed Koella JC, Lyimo EO. Variability in the relationship between weight and wing length of Anopheles gambiae (Diptera: Culicidae). J Med Entomol. 1996;33:261–4.CrossRefPubMed
28.
go back to reference Curtis CF. Induced sterility in insects. Adv Reprod Physiol. 1971;5:119–65.PubMed Curtis CF. Induced sterility in insects. Adv Reprod Physiol. 1971;5:119–65.PubMed
29.
go back to reference Fried M. Determination of sterile insect competitiveness. J Econ Entomol. 1971;64:869–72.CrossRef Fried M. Determination of sterile insect competitiveness. J Econ Entomol. 1971;64:869–72.CrossRef
31.
go back to reference Vreysen MJ, Saleh KM, Ali MY, Abdulla AM, Zhu ZR, Juma KG, et al. Glossina austeni (Diptera: Glossinidae) eradicated on the island of Unguja, Zanzibar, using the sterile insect technique. J Econ Entomol. 2000;93:123–35.CrossRefPubMed Vreysen MJ, Saleh KM, Ali MY, Abdulla AM, Zhu ZR, Juma KG, et al. Glossina austeni (Diptera: Glossinidae) eradicated on the island of Unguja, Zanzibar, using the sterile insect technique. J Econ Entomol. 2000;93:123–35.CrossRefPubMed
32.
go back to reference Anderson M. Sexual selection. Princeton: Princeton University Press; 1994. Anderson M. Sexual selection. Princeton: Princeton University Press; 1994.
33.
go back to reference Charlwood JD, Pinto J, Sousa CA, Madsen H. Ferreira C, do Rosario VE. The swarming and mating behaviour of Anopheles gambiae s.s. (Diptera: Culicidae) from Sao Tome Island. J Vector Ecol. 2002;27:178–83.PubMed Charlwood JD, Pinto J, Sousa CA, Madsen H. Ferreira C, do Rosario VE. The swarming and mating behaviour of Anopheles gambiae s.s. (Diptera: Culicidae) from Sao Tome Island. J Vector Ecol. 2002;27:178–83.PubMed
34.
go back to reference Maïga H, Dabiré RK, Lehmann T, Tripet F, Diabaté A. Variation in energy reserves and role of body size in the mating system of Anopheles gambiae. J Vector Ecol. 2012;37:289–97.CrossRefPubMed Maïga H, Dabiré RK, Lehmann T, Tripet F, Diabaté A. Variation in energy reserves and role of body size in the mating system of Anopheles gambiae. J Vector Ecol. 2012;37:289–97.CrossRefPubMed
35.
go back to reference Damiens D, Soliban SM, Balestrino F, Alsir R, Vreysen MJB. Different blood and sugar feeding regimes affect the productivity of Anopheles arabiensis colonies (Diptera: Culicidae). Entomol Soc Am. 2013;50:336–43. Damiens D, Soliban SM, Balestrino F, Alsir R, Vreysen MJB. Different blood and sugar feeding regimes affect the productivity of Anopheles arabiensis colonies (Diptera: Culicidae). Entomol Soc Am. 2013;50:336–43.
36.
go back to reference Helinski MEH, Parker AG, Knols BGJ. Radiation-induced sterility for pupal and adult stages of the malaria mosquito Anopheles arabiensis. Malar J. 2006;5:41.CrossRefPubMedPubMedCentral Helinski MEH, Parker AG, Knols BGJ. Radiation-induced sterility for pupal and adult stages of the malaria mosquito Anopheles arabiensis. Malar J. 2006;5:41.CrossRefPubMedPubMedCentral
37.
go back to reference Baeshen R, Ekechukwu NE, Toure M, Paton D, Coulibaly M, Traoré SF, et al. Differential effects of inbreeding and selection on male reproductive phenotype associated with the colonization and laboratory maintenance of Anopheles gambiae. Malar J. 2014;13:19.CrossRefPubMedPubMedCentral Baeshen R, Ekechukwu NE, Toure M, Paton D, Coulibaly M, Traoré SF, et al. Differential effects of inbreeding and selection on male reproductive phenotype associated with the colonization and laboratory maintenance of Anopheles gambiae. Malar J. 2014;13:19.CrossRefPubMedPubMedCentral
38.
go back to reference Ndo C, Yamada H, Damiens DD, N’do S, Seballos G, Gilles JRL. X-ray sterilization of the An. arabiensis genetic sexing strain “ANO IPCL1” at pupal and adult stages. Acta Trop. 2014;131:124–8.CrossRefPubMed Ndo C, Yamada H, Damiens DD, N’do S, Seballos G, Gilles JRL. X-ray sterilization of the An. arabiensis genetic sexing strain “ANO IPCL1” at pupal and adult stages. Acta Trop. 2014;131:124–8.CrossRefPubMed
39.
go back to reference Damiens D, Tjeck PO, Lebon C, Le Goff G, Gouagna LC. The effects of age at first mating and release ratios on the mating competitiveness of gamma sterilised Aedes albopictus males under semi field conditions. Vector Biol J. 2016;1:1–6.CrossRef Damiens D, Tjeck PO, Lebon C, Le Goff G, Gouagna LC. The effects of age at first mating and release ratios on the mating competitiveness of gamma sterilised Aedes albopictus males under semi field conditions. Vector Biol J. 2016;1:1–6.CrossRef
40.
go back to reference Ekechukwu NE, Baeshen R, Traorè SF, Coulibaly M, Diabate A, Catteruccia F, et al. Heterosis increases fertility, fecundity, and survival of laboratory-produced F1 hybrid males of the malaria mosquito Anopheles coluzzii. G3 (Bethesda). 2015;5:2693–709.CrossRefPubMedPubMedCentral Ekechukwu NE, Baeshen R, Traorè SF, Coulibaly M, Diabate A, Catteruccia F, et al. Heterosis increases fertility, fecundity, and survival of laboratory-produced F1 hybrid males of the malaria mosquito Anopheles coluzzii. G3 (Bethesda). 2015;5:2693–709.CrossRefPubMedPubMedCentral
Metadata
Title
Does mosquito mass-rearing produce an inferior mosquito?
Authors
Dieudonné D. Soma
Hamidou Maïga
Wadaka Mamai
Nanwintoun S. Bimbile-Somda
Nelius Venter
Adel B. Ali
Hanano Yamada
Abdoulaye Diabaté
Florence Fournet
Georges A. Ouédraogo
Rosemary S. Lees
Roch K. Dabiré
Jeremie R. L. Gilles
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2017
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-017-2012-8

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