Transgenerational and Sexual Auto-Dissemination within Anopheles Mosquitoes of the Malaria Parasite Transmission Blocking Microsporidia Sp MB in Burkina Faso — Oak Academic Publishing
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Transgenerational and Sexual Auto-Dissemination within Anopheles Mosquitoes of the Malaria Parasite Transmission Blocking Microsporidia Sp MB in Burkina Faso
Institut de Recherche en Sciences de la Santé Direction Régionale de l’Ouest (IRSS/DRO), Centre National de Recherche des Sciences et Technologies (CNRST), Bobo-Dioulasso, Burkina Faso
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Institut de Recherche en Sciences de la Santé Direction Régionale de l’Ouest (IRSS/DRO), Centre National de Recherche des Sciences et Technologies (CNRST), Bobo-Dioulasso, Burkina Faso
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Institut de Recherche en Sciences de la Santé Direction Régionale de l’Ouest (IRSS/DRO), Centre National de Recherche des Sciences et Technologies (CNRST), Bobo-Dioulasso, Burkina Faso
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Institut de Recherche en Sciences de la Santé Direction Régionale de l’Ouest (IRSS/DRO), Centre National de Recherche des Sciences et Technologies (CNRST), Bobo-Dioulasso, Burkina Faso
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Institut de Recherche en Sciences de la Santé Direction Régionale de l’Ouest (IRSS/DRO), Centre National de Recherche des Sciences et Technologies (CNRST), Bobo-Dioulasso, Burkina Faso
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Institut de Recherche en Sciences de la Santé Direction Régionale de l’Ouest (IRSS/DRO), Centre National de Recherche des Sciences et Technologies (CNRST), Bobo-Dioulasso, Burkina Faso
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Ecole Doctorale des Sciences Naturelles et Agronomie (ED-SNA), Université Nazi BONI, Bobo-Dioulasso, Burkina Faso
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Institut de Recherche en Sciences de la Santé Direction Régionale de l’Ouest (IRSS/DRO), Centre National de Recherche des Sciences et Technologies (CNRST), Bobo-Dioulasso, Burkina Faso
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Institut Nationale de Santé Publique (INSP), Centre Muraz, Bobo-Dioulasso, Burkina Faso
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Laboratoire d’Entomologie Fondamentale et Appliquée (LEFA), Université Joseph Ki-ZERBO, Ougadougou, Burkina Faso
1 Institut de Recherche en Sciences de la Santé Direction Régionale de l’Ouest (IRSS/DRO), Centre National de Recherche des Sciences et Technologies (CNRST), Bobo-Dioulasso, Burkina Faso
2 Institut de Recherche en Sciences de la Santé Direction Régionale de l’Ouest (IRSS/DRO), Centre National de Recherche des Sciences et Technologies (CNRST), Bobo-Dioulasso, Burkina Faso
3 Institut de Recherche en Sciences de la Santé Direction Régionale de l’Ouest (IRSS/DRO), Centre National de Recherche des Sciences et Technologies (CNRST), Bobo-Dioulasso, Burkina Faso
4 Institut de Recherche en Sciences de la Santé Direction Régionale de l’Ouest (IRSS/DRO), Centre National de Recherche des Sciences et Technologies (CNRST), Bobo-Dioulasso, Burkina Faso
5 Institut de Recherche en Sciences de la Santé Direction Régionale de l’Ouest (IRSS/DRO), Centre National de Recherche des Sciences et Technologies (CNRST), Bobo-Dioulasso, Burkina Faso
6 Institut de Recherche en Sciences de la Santé Direction Régionale de l’Ouest (IRSS/DRO), Centre National de Recherche des Sciences et Technologies (CNRST), Bobo-Dioulasso, Burkina Faso
7 Ecole Doctorale des Sciences Naturelles et Agronomie (ED-SNA), Université Nazi BONI, Bobo-Dioulasso, Burkina Faso
8 Institut de Recherche en Sciences de la Santé Direction Régionale de l’Ouest (IRSS/DRO), Centre National de Recherche des Sciences et Technologies (CNRST), Bobo-Dioulasso, Burkina Faso
9 Institut Nationale de Santé Publique (INSP), Centre Muraz, Bobo-Dioulasso, Burkina Faso
10 Laboratoire d’Entomologie Fondamentale et Appliquée (LEFA), Université Joseph Ki-ZERBO, Ougadougou, Burkina Faso
I ntroduction: Malaria control needs the development of complementary and/or alternative strategies such as biological controls. Despite, malaria’s current control efforts, the spread and the emergence of insecticide resistance in vectors undermine the fight against vectors. Endonsymbiotic fungi can be a good candidate to include in the existence of Arsenal. However, we know little about endosymbiotic fungi transmission and its impact on malaria transmission. In this paper, the authors aimed to investigate Microsporidia sp MB transgenerational and sexual autodissemination and malaria parasites within Anopheline mosquitoes. Methods : An entomology survey was conducted in Burkina Faso for one year (June 2020 to June 2021) using the Residual Fauna Capture method. Infection rates in collected females, sexual autodissemination of Microsporidia sp MB in both Microsporidia sp MB negative females and Microsporidia sp MB negative males through mating, transgenerational prevalence from parents to offsprings and the correlation between Microsporidia sp MB and Plasmodium falciparum were investigated . Results: Results show Microsporidia sp MB infection in An. gambaie s.l in Burkina Faso. The prevalence was significantly higher (21.78%) in An. coluzzii than An. gambiae s.s (16.89%) ( p-value = 0.03) . Sexual auto-dissemination of Micr osporidia sp MB in Microsporidia sp MB uninfected females was significantly 3-fold lower than those in Microsporidia sp MB uninfected males (9.23% and 33.33%, p-value = 0.03) during mating for An. coluzzii lines. Microsporidia sp MB prevalence was significantly higher through mosquitos’ generations in An. gambaie s.s than An. coluzzii (30.23% vs 26.41%, p-value < 0.001). A significant negative correlation was observed between Microsporidia sp MB and Plasmodium infection rate with 73% of Microsporidia sp MB positive mosquitoes which were negative at Plasmodium infection (p-value < 0.01). Conclusions : Our findings pave the road to developing new malaria control technologies by making Microsporidia sp MB -positive males sexually competitive with wild males to spread the fungus to wild female mosquitoes.
WHO (2022) World Malaria Report 2022, Geneva. Licence: CC BY-NC-SA 3.0 IGO.
WHO (2023) World Malaria Report 2023, Geneva. No. 112.
WHO (2021) World Malaria Report 2021.
WHO (2020) World Malaria Report 2020: 20 Years of Global Progress and Challenges.
Dabiré, K.R., Baldet, T., Diabaté, A., Dia, I., Costantini, C., Cohuet, A., et al . (2007) Anopheles funestus (Diptera: Culicidae) in a Humid Savannah Area of Western Burkina Faso: Bionomics, Insecticide Resistance Status, and Role in Malaria Transmission. Journal of Medical Entomology , 44, 990-997. https://doi.org/10.1093/jmedent/44.6.990
Bhatt, S., Weiss, D.J., Cameron, E., Bisanzio, D., Mappin, B., Dalrymple, U., et al . (2015) The Effect of Malaria Control on Plasmodium falciparum in Africa between 2000 and Nature , 526, 207-211. https://doi.org/10.1038/nature15535
Saleh, J.A., Saddiq, A. and Uchenna, A.A. (2018) LLIN Ownership, Utilization, and Malaria Prevalence: An Outlook at the 2015 Nigeria Malaria Indicator Survey. Open Access Library Journal , 5, e4280. https://doi.org/10.4236/oalib.1104280
WHO (2023) WHO Guidelines for Malaria, 2023 (WHO/UCN/GMP/2023.01).
Dattani, M. and Kurien, G. (2014) Malaria Treatment, Compliance and Cure in Gandhinagar, Gujarat. Health , 6, 6-9. https://doi.org/10.4236/health.2014.61002
Mathias, D.K., Ochomo, E., Atieli, F., Ombok, M., Nabie Bayoh, M., Olang, G., et al . (2011) Spatial and Temporal Variation in the kdr Allele L1014S in Anopheles gambia e S.S. and Phenotypic Variability in Susceptibility to Insecticides in Western Kenya. Malaria Journal , 10, Article No. 10. https://doi.org/10.1186/1475-2875-10-10
Vontas, J., Grigoraki, L., Morgan, J., Tsakireli, D., Fuseini, G., Segura, L., et al . (2018) Rapid Selection of a Pyrethroid Metabolic Enzyme CYP9K1 by Operational Malaria Control Activities. Proceedings of the National Academy of Sciences , 115, 4619-4624. https://doi.org/10.1073/pnas.1719663115
Cook, J., Hergott, D., Phiri, W., Rivas, M.R., Bradley, J., Segura, L., et al . (2018) Trends in Parasite Prevalence Following 13 Years of Malaria Interventions on Bioko Island, Equatorial Guinea: 2004-2016. Malaria Journal , 17, Article No. 62. https://doi.org/10.1186/s12936-018-2213-9
Ismail, B.A., Kafy, H.T., Sulieman, J.E., Subramaniam, K., Thomas, B., Mnzava, A., et al . (2018) Temporal and Spatial Trends in Insecticide Resistance in Anopheles arabiensis in Sudan: Outcomes from an Evaluation of Implications of Insecticide Resistance for Malaria Vector Control. Parasites & Vectors , 11, Article No. 122. https://doi.org/10.1186/s13071-018-2732-9
Plasmodium Falciparum
Malaria
Burkina Faso
Diabate, A., Baldet, T., Chandre, F., Akoobeto, M., Guiguemde, T.R., Darriet, F., et al . (2002) The Role of Agricultural Use of Insecticides in Resistance to Pyrethroids in Anopheles gambiae S.L. in Burkina Faso. The American Journal of Tropical Medicine and Hygiene , 67, 617-622. https://doi.org/10.4269/ajtmh.2002.67.617
Howard, A.F., Zhou, G. and Omlin, F.X. (2007) Malaria Mosquito Control Using Edible Fish in Western Kenya: Preliminary Findings of a Controlled Study. BMC Public Health , 7, Article No. 199. https://doi.org/10.1186/1471-2458-7-199
Huang, Y., Higgs, S. and Vanlandingham, D. (2017) Biological Control Strategies for Mosquito Vectors of Arboviruses. Insects , 8, Article No. 21. https://doi.org/10.3390/insects8010021
Bilgo, E., Lovett, B., St. Leger, R.J., Sanon, A., Dabiré, R.K. and Diabaté, A. (2018) Native Entomopathogenic metarhizium spp. from Burkina Faso and Their Virulence against the Malaria Vector Anopheles coluzzii and Non-Target Insects. Parasites & Vectors , 11, Article No. 209. https://doi.org/10.1186/s13071-018-2796-6
Schenker, W., Maier, W.A. and Seitz, H.M. (1992) The Effects of Nosema algerae on the Development of Plasmodium yoelii nigeriensis in Anopheles stephensi . Parasitology Research , 78, 56-59. https://doi.org/10.1007/bf00936182
Bargielowski, I. and Koella, J.C. (2009) A Possible Mechanism for the Suppression of Plasmodium berghei Development in the Mosquito Anopheles gambiae by the Microsporidian Vavraia culicis . PLOS ONE , 4, e4676. https://doi.org/10.1371/journal.pone.0004676
Gomes, F.M., Hixson, B.L., Tyner, M.D.W., Ramirez, J.L., Canepa, G.E., Alves e Silva, T.L., et al . (2017) Effect of Naturally Occurring Wolbachia in Anopheles gambiae S.L . Mosquitoes from Mali on Plasmodium falciparum Malaria Transmission. Proceedings of the National Academy of Sciences , 114, 12566-12571. https://doi.org/10.1073/pnas.1716181114
Kambris, Z., Cook, P.E., Phuc, H.K. and Sinkins, S.P. (2009) Immune Activation by Life-Shortening Wolbachia and Reduced Filarial Competence in Mosquitoes. Science , 326, 134-136. https://doi.org/10.1126/science.1177531
McMeniman, C.J., Lane, R.V., Cass, B.N., Fong, A.W.C., Sidhu, M., Wang, Y., et al . (2009) Stable Introduction of a Life-Shortening Wolbachia Infection into the Mosquito Aedes aegypti . Science , 323, 141-144. https://doi.org/10.1126/science.1165326
Audsley, M.D., Seleznev, A., Joubert, D.A., Woolfit, M., O’Neill, S.L. and McGraw, E.A. (2017) Wolbachia Infection Alters the Relative Abundance of Resident Bacteria in Adult Aedes aegypti Mosquitoes, but Not Larvae. Molecular Ecology , 27, 297-309. https://doi.org/10.1111/mec.14436
Moreira, L.A., Iturbe-Ormaetxe, I., Jeffery, J.A., Lu, G., Pyke, A.T., Hedges, L.M., et al . (2009) A Wolbachia Symbiont in Aedes aegypti Limits Infection with Dengue, Chikungunya, and Plasmodium . Cell , 139, 1268-1278. https://doi.org/10.1016/j.cell.2009.11.042
Joshi, D., Pan, X., McFadden, M.J., Bevins, D., Liang, X., Lu, P., et al . (2017) The Maternally Inheritable Wolbachia wAlbB Induces Refractoriness to Plasmodium berghei in Anopheles stephensi . Frontiers in Microbiology , 8, Article No. 366. https://doi.org/10.3389/fmicb.2017.00366
Ryan, P.A., Turley, A.P., Wilson, G., Hurst, T.P., Retzki, K., Brown-Kenyon, J., et al . (2019) Establishment of wMel Wolbachia in Aedes aegypti Mosquitoes and Reduction of Local Dengue Transmission in Cairns and Surrounding Locations in Northern Queensland, Australia. Gates Open Research , 3, Article No. 1547. https://doi.org/10.12688/gatesopenres.13061.1
Zélé, F., Denoyelle, J., Duron, O. and Rivero, A. (2017) Can Wolbachia Modulate the Fecundity Costs of Plasmodium in Mosquitoes? Parasitology , 145, 775-782. https://doi.org/10.1017/s0031182017001330
Ahmad, N.A., Mancini, M., Ant, T.H., Martinez, J., Kamarul, G.M.R., Nazni, W.A., et al . (2020) Wolbachia Strain w AlbB Maintains High Density and Dengue Inhibition Following Introduction into a Field Population of Aedes aegypti . Philosophical Transactions of the Royal Society B: Biological Sciences , 376, Article 20190809. https://doi.org/10.1098/rstb.2019.0809
Walker, T., Quek, S., Jeffries, C.L., Bandibabone, J., Dhokiya, V., Bamou, R., et al . (2021) Stable High-Density and Maternally Inherited Wolbachia Infections in Anopheles moucheti and Anopheles demeilloni Mosquitoes. Current Biology , 31, 2310-2320.E5. https://doi.org/10.1016/j.cub.2021.03.056
Wilke, A.B.B. and Marrelli, M.T. (2015) Paratransgenesis: A Promising New Strategy for Mosquito Vector Control. Parasites & Vectors , 8, Article No. 342. https://doi.org/10.1186/s13071-015-0959-2
Bian, G., Joshi, D., Dong, Y., Lu, P., Zhou, G., Pan, X., et al . (2013) Wolbachia Invades Anopheles stephensi Populations and Induces Refractoriness to Plasmodium Infection. Science , 340, 748-751. https://doi.org/10.1126/science.1236192
Gonzalez-Ceron, L., Santillan, F., Rodriguez, M.H., Mendez, D. and Hernandez-Avila, J.E. (2003) Bacteria in Midguts of Field-Collected Anopheles albimanus Block Plasmodium vivax Sporogonic Development. Journal of Medical Entomology , 40, 371-374. https://doi.org/10.1603/0022-2585-40.3.371
Cirimotich, C.M., Dong, Y., Clayton, A.M., Sandiford, S.L., Souza-Neto, J.A., Mulenga, M., et al . (2011) Natural Microbe-Mediated Refractoriness to Plasmodium Infection in Anopheles gambiae . Science , 332, 855-858. https://doi.org/10.1126/science.1201618
Bai, L., Wang, L., Vega-Rodríguez, J., Wang, G. and Wang, S. (2019) A Gut Symbiotic Bacterium Serratia marcescens Renders Mosquito Resistance to Plasmodium Infection through Activation of Mosquito Immune Responses. Frontiers in Microbiology , 10, Article No. 1580. https://doi.org/10.3389/fmicb.2019.01580
Herren, J.K., Mbaisi, L., Mararo, E., Makhulu, E.E., Mobegi, V.A., Butungi, H., et al . (2020) A Microsporidian Impairs Plasmodium falciparum Transmission in Anopheles arabiensis Mosquitoes. Nature Communications , 11, Article No. 2187. https://doi.org/10.1038/s41467-020-16121-y
Akorli, J., Akorli, E.A., Tetteh, S.N.A., Amlalo, G.K., Opoku, M., Pwalia, R., et al . (2021) Microsporidia MB Is Found Predominantly Associated with Anopheles gambiae s.s and Anopheles Coluzzii in Ghana. Scientific Reports , 11, Article No. 18658. https://doi.org/10.1038/s41598-021-98268-2
Nattoh, G., Bargul, J.L., Magoma, G., Mbaisi, L., Butungi, H., Mararo, E., et al . (2021) The Fungus Leptosphaerulina Persists in Anopheles gambiae and Induces Melanization. PLOS ONE , 16, e0246452. https://doi.org/10.1371/journal.pone.0246452
Nattoh, G., Onyango, B., Omoke, D., Makhulu, E., Mbaisi, L., Kamau, L., et al . (2023) Microsporidia MB in the Primary Malaria Vector Anopheles gambiae s.s. Is Avirulent and Undergoes Maternal and Horizontal Transmission. Preprint. https://doi.org/10.21203/rs.3.rs-2664771/v1
Moustapha, L.M., Sadou, I.M., Arzika, I.I., Maman, L.I., Gomgnimbou, M.K., Konkobo, M., et al . (2024) First Identification of Microsporidia MB in Anopheles coluzzii from Zinder City, Niger. Parasites & Vectors , 17, Article No. 39. https://doi.org/10.1186/s13071-023-06059-7
Ahouandjinou, M.J., Sovi, A., Sidick, A., Sewadé, W., Koukpo, C.Z., Chitou, S., et al . (2024) First Report of Natural Infection of Anopheles gambiae s.s. and Anopheles coluzzii by Wolbachia and Microsporidia in Benin: A Cross-Sectional Study. Malaria Journal , 23, Article No. 72. https://doi.org/10.1186/s12936-024-04906-1
Bationo, C.S., Gaudart, J., Dieng, S., Cissoko, M., Taconet, P., Ouedraogo, B., et al . (2021) Spatio-Temporal Analysis and Prediction of Malaria Cases Using Remote Sensing Meteorological Data in Diébougou Health District, Burkina Faso, 2016-2017. Scientific Reports , 11, Article No. 20027. https://doi.org/10.1038/s41598-021-99457-9
INSD (2003) Burkina Faso Enquête Démographique et de Santé, 2003.
Millogo, A.A., Yaméogo, L., Kassié, D., de Charles Ouédraogo, F., Guissou, C. and Diabaté, A. (2022) Spatial Modelling of Malaria Prevalence Associated with Geographical Factors in Houet Province of Burkina Faso, West Africa. GeoJournal , 88, 1769-1783. https://doi.org/10.1007/s10708-022-10692-7
Gillies, M. (1968) The Anophelinae of Africa South of Sahara (Ethiopian Zoogeographical Region). The South Africa Institute for Medical Research.
Gillies, M.T. and Coetzee, M. (1987) A Supplement to the Anophelinae of Africa South of the Sahara. South African Institute for Medical Research, No. 55. http://www.metoffice.gov.uk/public/weather/climate/u1214qgj0
Santolamazza, F., Mancini, E., Simard, F., Qi, Y., Tu, Z. and della Torre, A. (2008) Insertion Polymorphisms of SINE200 Retrotransposons within Speciation Islands of Anopheles gambiae Molecular Forms. Malaria Journal , 7, Article No. 163. https://doi.org/10.1186/1475-2875-7-163
Dabiré, R.K., Namountougou, M., Sawadogo, S.P., Yaro, L.B., Toé, H.K., Ouari, A., et al . (2012) Population Dynamics of Anopheles gambiae s.l. in Bobo-Dioulasso City: Bionomics, Infection Rate and Susceptibility to Insecticides. Parasites & Vectors , 5, Article No. 127. https://doi.org/10.1186/1756-3305-5-127
Epopa, P.S., Collins, C.M., North, A., Millogo, A.A., Benedict, M.Q., Tripet, F., et al . (2019) Seasonal Malaria Vector and Transmission Dynamics in Western Burkina Faso. Malaria Journal , 18, Article No. 113. https://doi.org/10.1186/s12936-019-2747-5
Favia, G., Ricci, I., Marzorati, M., Negri, I., Alma, A., Sacchi, L., et al . (2008) Bacteria of the Genus Asa i a : A Potential Potential Paratransgenic Weapon against Malaria. In: Aksoy, S., Ed., Transgenesis and the Management of Vector - Borne Disease , Springer, 49-59. https://doi.org/10.1007/978-0-387-78225-6_4
Wang, S., Dos-Santos, A.L.A., Huang, W., Liu, K.C., Oshaghi, M.A., Wei, G., et al . (2017) Driving Mosquito Refractoriness to Plasmodium falciparum with Engineered Symbiotic Bacteria. Science , 357, 1399-1402. https://doi.org/10.1126/science.aan5478
Moran, N.A. and Dunbar, H.E. (2006) Sexual Acquisition of Beneficial Symbionts in Aphids. Proceedings of the National Academy of Sciences of the United States of America , 103, 12803-12806. https://doi.org/10.1073/pnas.0605772103
Damiani, C., Ricci, I., Crotti, E., Rossi, P., Rizzi, A., Scuppa, P., et al . (2008) Paternal Transmission of Symbiotic Bacteria in Malaria Vectors. Current Biology , 18, R1087-R1088. https://doi.org/10.1016/j.cub.2008.10.040
Soper, D.M., King, K.C., Vergara, D. and Lively, C.M. (2014) Exposure to Parasites Increases Promiscuity in a Freshwater Snail. Biology Letters , 10, Article 20131091. https://doi.org/10.1098/rsbl.2013.1091
McLachlan, A. (1999) Parasites Promote Mating Success: The Case of a Midge and a Mite. Animal Behaviour , 57, 1199-1205. https://doi.org/10.1006/anbe.1999.1087
Abbot, P. and Dill, L.M. (2001) Sexually Transmitted Parasites and Sexual Selection in the Milkweed Leaf Beetle, Labidomera clivicollis . Oikos , 92, 91-100. https://doi.org/10.1034/j.1600-0706.2001.920111.x
House, P.K., Vyas, A. and Sapolsky, R. (2011) Predator Cat Odors Activate Sexual Arousal Pathways in Brains of Toxoplasma Gondii Infected Rats. PLOS ONE , 6, e23277. https://doi.org/10.1371/journal.pone.0023277
Dunn, A.M., Hatcher, M.J., Terry, R.S. and Tofts, C. (1995) Evolutionary Ecology of Vertically Transmitted Parasites: Transovarial Transmission of a Microsporidian Sex Ratio Distorter in Gammarus duebeni . Parasitology , 111, S91-S109. https://doi.org/10.1017/s0031182000075843
Vale, T., Dowling, M. and Cloonan, M. (1992) Infection and Multiplication of Ross River Virus in the Mosquito Vector Aedes-Vigilax (Skuse). Australian Journal of Zoology , 40, 35-41. https://doi.org/10.1071/zo9920035
Bouyer, J. and Vreysen, M.J.B. (2020) Yes, Irradiated Sterile Male Mosquitoes Can Be Sexually Competitive! Trends in Parasitology , 36, 877-880. https://doi.org/10.1016/j.pt.2020.09.005
Kellen, W.R., Chapman, H.C., Clark, T.B. and Lindegren, J.E. (1965) Host-Parasite Relationships of Some Thelohania from Mosquitoes (Nosematidae: Microsporidia). Journal of Invertebrate Pathology , 7, 161-166. https://doi.org/10.1016/0022-2011(65)90030-3