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EFFECTS OF NOSEMOSIS DISEASE ON COLONY IN HONEY BEES

Yıl 2024, Cilt: 3 Sayı: 1, 17 - 27, 27.06.2024

Öz

Nosema cerenae and Nosema apis, which are obligate intracellular fungi belonging to the Microsporidia species, infect honey bees and cause nosemosis disease. The disease causes excellent damage to honey bee colonies. N. cerenae is the most dangerous and common cause of nosemosis worldwide. Shortening of the average lifespan of bees in the colony, deterioration of the queen bee's egg-laying pattern due to the inability of worker bees to fulfill their duties, failure to care for the brood regularly, weakening of the mobility of the bees, and accordingly deterioration of the nutrient supply, hunger, diarrhea, increase in winter losses, decrease in honey production and Weakening of pollen collection activities and
therefore insufficient carbohydrate and protein intake, digestive system disorders occur as a result of nosemosis disease. In particular, N. cerenae’s rapid spread and high virulence cause colonies to disappear. The disease can also occur together with viral, bacterial, and protozoal diseases. N. apis is characterized by dysentery and some clinical symptoms are noticed late. Still, the rate of spread of N. cerenae and the fact that it does not show clinical symptoms indicate the magnitude of the danger. The limited and insufficient treatment methods for the disease reveal that prevention and control methods are essential.

Kaynakça

  • Bigliardi, E., Selmi, M. G., Lupetti, P., Corona, S., Gatti, S., Scaglia, M., & Sacchi, L. (1996). Microsporidian spore wall: ultrastructural findings on Encephalitozoon hellem exospore. Journal of Eukaryotic Microbiology, 43(3), 181-186.
  • Alaux, C., Brunet, J. L., Dussaubat, C., Mondet, F., Tchamitchan, S., Cousin, M., ... & Le Conte, Y. (2010). Interactions between Nosema microspores and a neonicotinoid weaken honeybees (Apis mellifera). Environmental microbiology, 12(3), 774-782.
  • Botías, C., Martín-Hernández, R., Garrido-Bailón, E., González-Porto, A., Martínez-Salvador, A., De La Rúa, P., ... & Higes, M. (2012). The growing prevalence of Nosema ceranae in honey bees in Spain, an emerging problem for the last decade. Research in Veterinary Science, 93(1), 150-155.
  • Büyük, M., Tunca, R. İ., & Taşkın, A. (2014). Türkiye’de Nosema spp. varlığına yönelik yapılmış çalışmalar. Türk Tarım ve Doğa Bilimleri Dergisi, 1(2), 234-238.
  • Cali, A., & Takvorian, P. M. (2014). Developmental morphology and life cycles of the microsporidia. Microsporidia: Pathogens of opportunity, 71-133.
  • Chen, Y. P., Evans, J. D., Murphy, C., Gutell, R., Zuker, M., Gundensen‐Rindal, D. A. W. N., & Pettis, J. S. (2009). Morphological, Molecular, and Phylogenetic Characterization of Nosema ceranae, a Microsporidian Parasite Isolated from the European Honey Bee, Apis mellifera 1. Journal of Eukaryotic Microbiology, 56(2), 142-147.b
  • Chen, Y.P., Evans, J.D., Zhou, L., Boncristiani, H., Kimura, K., Xiao, T.G., Litkowski, A.M., Pettis, J.S., 2009. Asymmetrical coexistence of Nosema ceranae and Nosema apis in honey bees. J. Invertebr. Pathol. 101, 204–209.a
  • Evans, J. D., & Schwarz, R. S. (2011). Bees brought to their knees: microbes affecting honey bee health. Trends in microbiology, 19(12), 614-620.
  • Feng, F., da Silva, A., Slemenda, S. B., & Pieniazek, N. J. (1996). Nosema ceranae n. sp.(Microspora, Nosematidae), morphological and molecular characterization of a microsporidian parasite of the Asian honey bee Apis cerana (Hymenoptera, Apidae). European Journal of Protistology, 32(3), 356-365.
  • Forsgren, E., & Fries, I. (2010). Comparative virulence of Nosema ceranae and Nosema apis in individual European honey bees. Veterinary parasitology, 170(3-4), 212-217. Franzen, C. (2005). How do microsporidia invade cells?. Folia parasitologica, 52(1/2), 36.
  • Fries, I. (1993). Nosema apis—a parasite in the honey bee colony. Bee World, 74(1), 5-19.
  • Fries, I., & Feng, F. (1995). Crossinfectivity of Nosema apis in Apis mellifera and Apis cerana. In Proceedings of the Apimondia 34th International Apicultural Congress, Bucharest, Romania (pp. 151-155).
  • Fries, I., Feng, F., da Silva, A., Slemenda, S. B., & Pieniazek, N. J. (1996). Nosema ceranae n. sp.(Microspora, Nosematidae), morphological and molecular characterization of a microsporidian parasite of the Asian honey bee Apis cerana (Hymenoptera, Apidae). European Journal of Protistology, 32(3), 356-365.
  • Galajda, R., Valenčáková, A., Sučik, M., & Kandráčová, P. (2021). Nosema disease of European honey bees. Journal of Fungi, 7(9), 714.
  • Genersch, E. (2010). Honey bee pathology: current threats to honey bees and beekeeping. Applied microbiology and biotechnology, 87, 87-97.
  • Giersch, T., Berg, T., Galea, F., & Hornitzky, M. (2009). Nosema ceranae infects honey bees (Apis mellifera) and contaminates honey in Australia. Apidologie, 40(2), 117-123.
  • Gisder, S., Möckel, N., Linde, A., & Genersch, E. (2011). A cell culture model for Nosema ceranae and Nosema apis allows new insights into the life cycle of these important honey bee‐pathogenic microsporidia. Environmental microbiology, 13(2), 404-413.
  • Higes, M., García-Palencia, P., Martín-Hernández, R., & Meana, A. (2007). Experimental infection of Apis mellifera honeybees with Nosema ceranae (Microsporidia). Journal of invertebrate pathology, 94(3), 211-217.
  • Higes, M., Martín, R., & Meana, A. (2006). Nosema ceranae, a new microsporidian parasite in honeybees in Europe. Journal of invertebrate pathology, 92(2), 93-95.
  • Higes, M., Martín-Hernández, R., & Meana, A. (2010). Nosema ceranae in Europe: an emergent type C nosemosis. Apidologie, 41(3), 375-392.
  • Higes, M., Martín-Hernández, R., Garrido-Bailon, E., García-Palencia, P., & Meana, A. (2008). Detection of infective Nosema ceranae (Microsporidia) spores in corbicular pollen of forager honeybees. Journal of Invertebrate Pathology, 97(1), 76-78.
  • Huang, W. F., Jiang, J. H., Chen, Y. W., & Wang, C. H. (2007). A Nosema ceranae isolate from the honeybee Apis mellifera. Apidologie, 38(1), 30-37.
  • Keeling, P. J., & Fast, N. M. (2002). Microsporidia: biology and evolution of highly reduced intracellular parasites. Annual Reviews in Microbiology, 56(1), 93-116.
  • Keohane, E. M., & Weiss, L. M. (1999). The structure, function, and composition of the microsporidian polar tube. The microsporidia and microsporidiosis, 196-224. Fries, I.,
  • Keohane, E. M., & Weiss, L. M. (1999). The structure, function, and composition of the microsporidian polar tube. The microsporidia and microsporidiosis, 196-224.
  • Klee, J., Besana, A. M., Genersch, E., Gisder, S., Nanetti, A., Tam, D. Q., ... & Paxton, R. J. (2007). Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. Journal of invertebrate pathology, 96(1), 1-10.
  • Klein, A. M., Vaissière, B. E., Cane, J. H., Steffan-Dewenter, I., Cunningham, S. A., Kremen, C., & Tscharntke, T. (2007). Importance of pollinators in changing landscapes for world crops. Proceedings of the royal society B: biological sciences, 274(1608), 303-313.
  • Lopes, A. R., Martín-Hernández, R., Higes, M., Segura, S. K., Henriques, D., & Pinto, M. A. (2023). First detection of Nosema ceranae in honey bees (Apis mellifera L.) of the Macaronesian archipelago of Madeira. Journal of Apicultural Research, 62(3), 514-517.
  • Martín-Hernández, R., Botías, C., Barrios, L., Martínez-Salvador, A., Meana, A., Mayack, C., & Higes, M. (2011). Comparison of the energetic stress associated with experimental Nosema ceranae and Nosema apis infection of honeybees (Apis mellifera). Parasitology research, 109, 605-612.
  • Martín-Hernández, R., Meana, A., García-Palencia, P., Marín, P., Botías, C., Garrido-Bailón, E., ... & Higes, M. (2009). Effect of temperature on the biotic potential of honeybee microsporidia. Applied and environmental microbiology, 75(8), 2554-2557.
  • Meixner, M. D. (2010). A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. Journal of invertebrate pathology, 103, S80-S95.
  • Paxton, R. J. (2010). Does infection by Nosema ceranae cause “Colony Collapse Disorder” in honey bees (Apis mellifera)?. Journal of Apicultural Research, 49(1), 80-84.
  • Paxton, R. J., Klee, J., Korpela, S., & Fries, I. (2007). Nosema ceranae has infected Apis mellifera in Europe since at least 1998 and may be more virulent than Nosema apis. Apidologie, 38(6), 558-565.
  • Smith, M. L. (2012). The Honey Bee Parasite Nosema ceranae: Transmissible via Food Exchange? PLoS ONE 2012, 7, e43319.
  • Vidau, C., Panek, J., Texier, C., Biron, D. G., Belzunces, L. P., Le Gall, M., ... & El Alaoui, H. (2014). Differential proteomic analysis of midguts from Nosema ceranae-infected honeybees reveals manipulation of key host functions. Journal of Invertebrate Pathology, 121, 89-96.
  • Xu, Y., & Weiss, L. M. (2005). The microsporidian polar tube: a highly specialised invasion organelle. International journal for parasitology, 35(9), 941-953.
  • Yazar, S., Özgür, K., Hamamcı, B., Çetinkaya, Ü., Karaman, Ü., & Salih, K. U. K. (2013). Microsporidia and microsporidiosis. Türkiye Parazitolojii Dergisi, 37(2), 123.
  • Zander, E. (1909). Tierische parasiten als krankenheitserreger bei der biene. Münchener Bienenzeitung, 1909, 31: 196-204.
  • Marmaras, V. J., & Lampropoulou, M. (2009). Regulators and signalling in insect haemocyte immunity. Cellular signalling, 21(2), 186-195.
  • Schmid-Hempel, P. Parasites in Social Insects; Princeton University Press: Princeton, NJ, USA, 1998; pp. 119–123. ISBN 9780691059242.
  • Özgör, E., Güzerin, E., & Keskin, N. (2015). Determination and comparison of Nosema apis and Nosema ceranae in terms of geographic and climatic factors. Hacettepe Journal of Biology and Chemistry, 43(1), 9-15.
  • Martín-Hernández, R., Meana, A., Prieto, L., Salvador, A. M., Garrido-Bailón, E., & Higes, M. (2007). Outcome of colonization of Apis mellifera by Nosema ceranae. Applied and environmental microbiology, 73(20), 6331-6338.
  • Simeunovic, P., Stevanovic, J., Cirkovic, D., Radojicic, S., Lakic, N., Stanisic, L., & Stanimirovic, Z. (2014). Nosema ceranae and queen age influence the reproduction and productivity of the honey bee colony. Journal of Apicultural Research, 53(5), 545-554.
  • Traver, B. E., & Fell, R. D. (2011). Nosema ceranae in drone honey bees (Apis mellifera). Journal of invertebrate pathology, 107(3), 234-236.
  • Peng, Y., Grassl, J., Millar, A. H., & Baer, B. (2016). Seminal fluid of honeybees contains multiple mechanisms to combat infections of the sexually transmitted pathogen Nosema apis. Proceedings of the Royal Society B: Biological Sciences, 283(1823), 20151785.
  • Chen, Y. P., & Huang, Z. Y. (2010). Nosema ceranae, a newly identified pathogen of Apis mellifera in the USA and Asia. Apidologie, 41(3), 364-374.
  • Webster, T. C., Pomper, K. W., Hunt, G., Thacker, E. M., & Jones, S. C. (2004). Nosema apis infection in worker and queen Apis mellifera. Apidologie, 35(1), 49-54.
  • Fries, I., Chauzat, M. P., Chen, Y. P., Doublet, V., Genersch, E., Gisder, S., ... & Williams, G. R. (2013). Standard methods for Nosema research. Journal of apicultural research, 52(1), 1-28.
  • Formato, G., Rivera-Gomis, J., Bubnic, J., Martín-Hernández, R., Milito, M., Croppi, S., & Higes, M. (2022). Nosemosis prevention and control. Applied Sciences, 12(2), 783.
  • Özüiçli, M., & Aydın, L. (2018). Türkiye bal arılarında ciddi tehlike; nosemosis. Uludağ Üniversitesi Veteriner Fakültesi Dergisi, 37(2), 151-157.
  • Karahan, A., Kutlu, M. A., Gül, A., & Karaca, İ. (2018, October). The Effect of pesticides on honey bees. In 6th International Muğla Beekeeping and Pine Honey Congress (pp. 15-19).
  • Vilmos, P., & Kurucz, E. (1998). Insect immunity: evolutionary roots of the mammalian innate immune system. Immunology letters, 62(2), 59-66.
  • Zheng, H., Steele, M. I., Leonard, S. P., Motta, E. V., & Moran, N. A. (2018). Honey bees as models for gut microbiota research. Lab animal, 47(11), 317-325.

BAL ARILARINDA NOSEMOSİS HASTALIĞININ KOLONİ ÜZERİNE ETKİLERİ

Yıl 2024, Cilt: 3 Sayı: 1, 17 - 27, 27.06.2024

Öz

Mikrosporidia türüne ait zorunlu hücre içi mantar grubundan olan Nosema cerenae ve Nosema apis bal arılarını enfekte ederek nosemosis hastalığı meydana getirmektedir. Hastalık bal arısı kolonilerine büyük zararlar vermektedir. N. cerenae Dünya’da nosemosis hastalığının en tehlikeli ve yaygın etkenidir. Kolonide arıların ortalama yaşam sürelerinin kısalması, işçi arıların görevlerini yerine getirememesiyle birlikte ana arının yumurtalama düzeninin bozulması, yavru bakımlarının düzenli bir şekilde yapılamaması, arılardaki hareket kabiliyetinin zayıflaması ve buna bağlı olarak besin maddesi tedariğinin bozulması, açlık, ishal, kış kayıplarının yükselmesi, bal üretiminin ve polen toplama faaliyetlerinin zayıflaması ve buna bağlı olarak yetersiz karbonhidrat ve protein alımı, sindirim sistemi bozuklukları nosemosis hastalığı sonucunda meydana gelmektedir. Özellikle N. cerenae’nın oldukça hızlı yayılım göstermesi ve virulansının yüksek olması kolonilerin sönmesine neden olmaktadır. Hastalık aynı zamanda viral, bakteriyel ve protozoal hastalıklarla beraber de seyredebilmektedir. N. apis dizanteri ile karakterizedir ve bazı klinik belirtiler geçte olsa farkedilmektedir fakat N. cerenae’nın yayılım hızı ve klinik belirti göstermemesi tehlikenin büyüklüğünü göstermektedir. Hastalıkla ilgili tedavi yöntemlerinin kısıtlı ve yetersiz olması koruma ve kontrol yöntemlerinin oldukça önemli olduğunu ortaya koymaktadır.

Kaynakça

  • Bigliardi, E., Selmi, M. G., Lupetti, P., Corona, S., Gatti, S., Scaglia, M., & Sacchi, L. (1996). Microsporidian spore wall: ultrastructural findings on Encephalitozoon hellem exospore. Journal of Eukaryotic Microbiology, 43(3), 181-186.
  • Alaux, C., Brunet, J. L., Dussaubat, C., Mondet, F., Tchamitchan, S., Cousin, M., ... & Le Conte, Y. (2010). Interactions between Nosema microspores and a neonicotinoid weaken honeybees (Apis mellifera). Environmental microbiology, 12(3), 774-782.
  • Botías, C., Martín-Hernández, R., Garrido-Bailón, E., González-Porto, A., Martínez-Salvador, A., De La Rúa, P., ... & Higes, M. (2012). The growing prevalence of Nosema ceranae in honey bees in Spain, an emerging problem for the last decade. Research in Veterinary Science, 93(1), 150-155.
  • Büyük, M., Tunca, R. İ., & Taşkın, A. (2014). Türkiye’de Nosema spp. varlığına yönelik yapılmış çalışmalar. Türk Tarım ve Doğa Bilimleri Dergisi, 1(2), 234-238.
  • Cali, A., & Takvorian, P. M. (2014). Developmental morphology and life cycles of the microsporidia. Microsporidia: Pathogens of opportunity, 71-133.
  • Chen, Y. P., Evans, J. D., Murphy, C., Gutell, R., Zuker, M., Gundensen‐Rindal, D. A. W. N., & Pettis, J. S. (2009). Morphological, Molecular, and Phylogenetic Characterization of Nosema ceranae, a Microsporidian Parasite Isolated from the European Honey Bee, Apis mellifera 1. Journal of Eukaryotic Microbiology, 56(2), 142-147.b
  • Chen, Y.P., Evans, J.D., Zhou, L., Boncristiani, H., Kimura, K., Xiao, T.G., Litkowski, A.M., Pettis, J.S., 2009. Asymmetrical coexistence of Nosema ceranae and Nosema apis in honey bees. J. Invertebr. Pathol. 101, 204–209.a
  • Evans, J. D., & Schwarz, R. S. (2011). Bees brought to their knees: microbes affecting honey bee health. Trends in microbiology, 19(12), 614-620.
  • Feng, F., da Silva, A., Slemenda, S. B., & Pieniazek, N. J. (1996). Nosema ceranae n. sp.(Microspora, Nosematidae), morphological and molecular characterization of a microsporidian parasite of the Asian honey bee Apis cerana (Hymenoptera, Apidae). European Journal of Protistology, 32(3), 356-365.
  • Forsgren, E., & Fries, I. (2010). Comparative virulence of Nosema ceranae and Nosema apis in individual European honey bees. Veterinary parasitology, 170(3-4), 212-217. Franzen, C. (2005). How do microsporidia invade cells?. Folia parasitologica, 52(1/2), 36.
  • Fries, I. (1993). Nosema apis—a parasite in the honey bee colony. Bee World, 74(1), 5-19.
  • Fries, I., & Feng, F. (1995). Crossinfectivity of Nosema apis in Apis mellifera and Apis cerana. In Proceedings of the Apimondia 34th International Apicultural Congress, Bucharest, Romania (pp. 151-155).
  • Fries, I., Feng, F., da Silva, A., Slemenda, S. B., & Pieniazek, N. J. (1996). Nosema ceranae n. sp.(Microspora, Nosematidae), morphological and molecular characterization of a microsporidian parasite of the Asian honey bee Apis cerana (Hymenoptera, Apidae). European Journal of Protistology, 32(3), 356-365.
  • Galajda, R., Valenčáková, A., Sučik, M., & Kandráčová, P. (2021). Nosema disease of European honey bees. Journal of Fungi, 7(9), 714.
  • Genersch, E. (2010). Honey bee pathology: current threats to honey bees and beekeeping. Applied microbiology and biotechnology, 87, 87-97.
  • Giersch, T., Berg, T., Galea, F., & Hornitzky, M. (2009). Nosema ceranae infects honey bees (Apis mellifera) and contaminates honey in Australia. Apidologie, 40(2), 117-123.
  • Gisder, S., Möckel, N., Linde, A., & Genersch, E. (2011). A cell culture model for Nosema ceranae and Nosema apis allows new insights into the life cycle of these important honey bee‐pathogenic microsporidia. Environmental microbiology, 13(2), 404-413.
  • Higes, M., García-Palencia, P., Martín-Hernández, R., & Meana, A. (2007). Experimental infection of Apis mellifera honeybees with Nosema ceranae (Microsporidia). Journal of invertebrate pathology, 94(3), 211-217.
  • Higes, M., Martín, R., & Meana, A. (2006). Nosema ceranae, a new microsporidian parasite in honeybees in Europe. Journal of invertebrate pathology, 92(2), 93-95.
  • Higes, M., Martín-Hernández, R., & Meana, A. (2010). Nosema ceranae in Europe: an emergent type C nosemosis. Apidologie, 41(3), 375-392.
  • Higes, M., Martín-Hernández, R., Garrido-Bailon, E., García-Palencia, P., & Meana, A. (2008). Detection of infective Nosema ceranae (Microsporidia) spores in corbicular pollen of forager honeybees. Journal of Invertebrate Pathology, 97(1), 76-78.
  • Huang, W. F., Jiang, J. H., Chen, Y. W., & Wang, C. H. (2007). A Nosema ceranae isolate from the honeybee Apis mellifera. Apidologie, 38(1), 30-37.
  • Keeling, P. J., & Fast, N. M. (2002). Microsporidia: biology and evolution of highly reduced intracellular parasites. Annual Reviews in Microbiology, 56(1), 93-116.
  • Keohane, E. M., & Weiss, L. M. (1999). The structure, function, and composition of the microsporidian polar tube. The microsporidia and microsporidiosis, 196-224. Fries, I.,
  • Keohane, E. M., & Weiss, L. M. (1999). The structure, function, and composition of the microsporidian polar tube. The microsporidia and microsporidiosis, 196-224.
  • Klee, J., Besana, A. M., Genersch, E., Gisder, S., Nanetti, A., Tam, D. Q., ... & Paxton, R. J. (2007). Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. Journal of invertebrate pathology, 96(1), 1-10.
  • Klein, A. M., Vaissière, B. E., Cane, J. H., Steffan-Dewenter, I., Cunningham, S. A., Kremen, C., & Tscharntke, T. (2007). Importance of pollinators in changing landscapes for world crops. Proceedings of the royal society B: biological sciences, 274(1608), 303-313.
  • Lopes, A. R., Martín-Hernández, R., Higes, M., Segura, S. K., Henriques, D., & Pinto, M. A. (2023). First detection of Nosema ceranae in honey bees (Apis mellifera L.) of the Macaronesian archipelago of Madeira. Journal of Apicultural Research, 62(3), 514-517.
  • Martín-Hernández, R., Botías, C., Barrios, L., Martínez-Salvador, A., Meana, A., Mayack, C., & Higes, M. (2011). Comparison of the energetic stress associated with experimental Nosema ceranae and Nosema apis infection of honeybees (Apis mellifera). Parasitology research, 109, 605-612.
  • Martín-Hernández, R., Meana, A., García-Palencia, P., Marín, P., Botías, C., Garrido-Bailón, E., ... & Higes, M. (2009). Effect of temperature on the biotic potential of honeybee microsporidia. Applied and environmental microbiology, 75(8), 2554-2557.
  • Meixner, M. D. (2010). A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. Journal of invertebrate pathology, 103, S80-S95.
  • Paxton, R. J. (2010). Does infection by Nosema ceranae cause “Colony Collapse Disorder” in honey bees (Apis mellifera)?. Journal of Apicultural Research, 49(1), 80-84.
  • Paxton, R. J., Klee, J., Korpela, S., & Fries, I. (2007). Nosema ceranae has infected Apis mellifera in Europe since at least 1998 and may be more virulent than Nosema apis. Apidologie, 38(6), 558-565.
  • Smith, M. L. (2012). The Honey Bee Parasite Nosema ceranae: Transmissible via Food Exchange? PLoS ONE 2012, 7, e43319.
  • Vidau, C., Panek, J., Texier, C., Biron, D. G., Belzunces, L. P., Le Gall, M., ... & El Alaoui, H. (2014). Differential proteomic analysis of midguts from Nosema ceranae-infected honeybees reveals manipulation of key host functions. Journal of Invertebrate Pathology, 121, 89-96.
  • Xu, Y., & Weiss, L. M. (2005). The microsporidian polar tube: a highly specialised invasion organelle. International journal for parasitology, 35(9), 941-953.
  • Yazar, S., Özgür, K., Hamamcı, B., Çetinkaya, Ü., Karaman, Ü., & Salih, K. U. K. (2013). Microsporidia and microsporidiosis. Türkiye Parazitolojii Dergisi, 37(2), 123.
  • Zander, E. (1909). Tierische parasiten als krankenheitserreger bei der biene. Münchener Bienenzeitung, 1909, 31: 196-204.
  • Marmaras, V. J., & Lampropoulou, M. (2009). Regulators and signalling in insect haemocyte immunity. Cellular signalling, 21(2), 186-195.
  • Schmid-Hempel, P. Parasites in Social Insects; Princeton University Press: Princeton, NJ, USA, 1998; pp. 119–123. ISBN 9780691059242.
  • Özgör, E., Güzerin, E., & Keskin, N. (2015). Determination and comparison of Nosema apis and Nosema ceranae in terms of geographic and climatic factors. Hacettepe Journal of Biology and Chemistry, 43(1), 9-15.
  • Martín-Hernández, R., Meana, A., Prieto, L., Salvador, A. M., Garrido-Bailón, E., & Higes, M. (2007). Outcome of colonization of Apis mellifera by Nosema ceranae. Applied and environmental microbiology, 73(20), 6331-6338.
  • Simeunovic, P., Stevanovic, J., Cirkovic, D., Radojicic, S., Lakic, N., Stanisic, L., & Stanimirovic, Z. (2014). Nosema ceranae and queen age influence the reproduction and productivity of the honey bee colony. Journal of Apicultural Research, 53(5), 545-554.
  • Traver, B. E., & Fell, R. D. (2011). Nosema ceranae in drone honey bees (Apis mellifera). Journal of invertebrate pathology, 107(3), 234-236.
  • Peng, Y., Grassl, J., Millar, A. H., & Baer, B. (2016). Seminal fluid of honeybees contains multiple mechanisms to combat infections of the sexually transmitted pathogen Nosema apis. Proceedings of the Royal Society B: Biological Sciences, 283(1823), 20151785.
  • Chen, Y. P., & Huang, Z. Y. (2010). Nosema ceranae, a newly identified pathogen of Apis mellifera in the USA and Asia. Apidologie, 41(3), 364-374.
  • Webster, T. C., Pomper, K. W., Hunt, G., Thacker, E. M., & Jones, S. C. (2004). Nosema apis infection in worker and queen Apis mellifera. Apidologie, 35(1), 49-54.
  • Fries, I., Chauzat, M. P., Chen, Y. P., Doublet, V., Genersch, E., Gisder, S., ... & Williams, G. R. (2013). Standard methods for Nosema research. Journal of apicultural research, 52(1), 1-28.
  • Formato, G., Rivera-Gomis, J., Bubnic, J., Martín-Hernández, R., Milito, M., Croppi, S., & Higes, M. (2022). Nosemosis prevention and control. Applied Sciences, 12(2), 783.
  • Özüiçli, M., & Aydın, L. (2018). Türkiye bal arılarında ciddi tehlike; nosemosis. Uludağ Üniversitesi Veteriner Fakültesi Dergisi, 37(2), 151-157.
  • Karahan, A., Kutlu, M. A., Gül, A., & Karaca, İ. (2018, October). The Effect of pesticides on honey bees. In 6th International Muğla Beekeeping and Pine Honey Congress (pp. 15-19).
  • Vilmos, P., & Kurucz, E. (1998). Insect immunity: evolutionary roots of the mammalian innate immune system. Immunology letters, 62(2), 59-66.
  • Zheng, H., Steele, M. I., Leonard, S. P., Motta, E. V., & Moran, N. A. (2018). Honey bees as models for gut microbiota research. Lab animal, 47(11), 317-325.
Toplam 53 adet kaynakça vardır.

Ayrıntılar

Birincil Dil Türkçe
Konular Biyokimya ve Hücre Biyolojisi (Diğer), Klinik Kimya, Gıda Mühendisliği, Ziraat Mühendisliği (Diğer)
Bölüm Derlemeler
Yazarlar

Sadık Çıvracı 0000-0002-0750-1823

Erken Görünüm Tarihi 13 Haziran 2024
Yayımlanma Tarihi 27 Haziran 2024
Gönderilme Tarihi 30 Mayıs 2024
Kabul Tarihi 10 Haziran 2024
Yayımlandığı Sayı Yıl 2024 Cilt: 3 Sayı: 1

Kaynak Göster

APA Çıvracı, S. (2024). BAL ARILARINDA NOSEMOSİS HASTALIĞININ KOLONİ ÜZERİNE ETKİLERİ. Arı Ve Arıcılık Teknolojileri Dergisi, 3(1), 17-27.