Molecular detection and seasonal dynamics of Nosema ceranae in Apis mellifera (honey bee) colonies in Central Punjab, Pakistan
DOI:
https://doi.org/10.5281/zenodo.23302697Keywords:
Honey bee, Nosema apis, Nosema ceranae, microscopy, qPCR, Hsp70 gene, 16S rRNA geneAbstract
Nosema ceranae is an important microsporidian pathogen that causes reduced colony health and productivity in Apis mellifera (honey bee) globally. But little information is available on its prevalence, seasonal fluctuations, and risk factors in honey bee colonies of Central Punjab, Pakistan. This study aimed to identify, differentiate, and quantify Nosema spp. infections using microscopy and quantitative real-time PCR (qPCR). We sampled 60 honey bee hives across four seasons in 2023-2024 from institutional apiaries in three districts of Punjab: Okara, Kasur, and Lahore. Adult worker bees were collected, examined under a microscope for Nosema spores, and then tested at the molecular level using qPCR specific for the Hsp70 gene and the 16S rRNA gene for N. ceranae and N. apis, respectively. Chi-square tests were also used to record and analyze environmental and colony-level risk factors. Microscopy detected Nosema spores in seven (11.6%) hives, while qPCR detected N. ceranae in 36 (60%) hives. None of the samples were positive for N. apis. Okara (13, 65%) and Kasur (12, 60%) had the highest prevalence, followed by Lahore (11, 55%). Prevalence in summer and spring was higher (10, 66.6%) than in autumn (9, 60%) and winter (7, 46.6%). Infection levels ranged significantly from undetectable to 5.1 × 10⁶ copies/bee. Infection prevalence was significantly related to both internal and external hive temperature (P < 0.05), while colony strength, colony brood, humidity, precipitation, and Varroa mite infestation were not significant. The study showed that N. ceranae was present in honey bee colonies across Central Punjab and was significantly affected by the seasons and environment. qPCR detection of the pathogen was significantly more sensitive than microscopy. These results provide a baseline for improved disease monitoring, management, and sustainable apiculture in Pakistan.
References
Alam, S., Khan, M. N., Rafique, K., & Malik, S. (2021). The incidence of Nosema spp. on honey bees (Apis mellifera) colonies in Pakistan. Journal of Applied Entomology, 1(2), 1-4.
Anjum, S. I., Shah, A. H., Aurongzeb, M., Kori, J., Azim, M. K., Ansari, M. J., & Bin, L. (2018). Characterization of gut bacterial flora of Apis mellifera from northwest Pakistan. Saudi Journal of Biological Sciences, 25(2), 388-392. https://doi.org/10.1016/j.sjbs.2017.05.008
Ansari, M. J., Al-Ghamdi, A., Nuru, A., Khan, K. A., & Alattal, Y. (2017). Geographical distribution and molecular detection of Nosema ceranae from indigenous honey bees of Saudi Arabia. Saudi Journal of Biological Sciences, 24(5), 983-991. https://doi.org/10.1016/j.sjbs.2017.01.054
Bigliardi, E., & Sacchi, L. (2001). Cell biology and invasion of the microsporidia. Microbes and Infection, 3(5), 373-379. https://doi.org/10.1016/S1286-4579(01)01393-4
Botías, C., Martín-Hernández, R., Barrios, L., Meana, A., & Higes, M. (2013). Nosema spp. infection and its negative effects on honey bees (Apis mellifera iberiensis) at the colony level. Veterinary research, 44(1), 25. http://www.veterinaryresearch.org/content/44/1/25
Botías, C., Martín-Hernández, R., Días, J., García-Palencia, P., Matabuena, M., Juarranz, Á., Barrios, L., Meana, A., Nanetti, A., & Higes, M. (2012). The effect of induced queen replacement on Nosema spp. infection in honey bee (Apis mellifera iberiensis) colonies. Environmental Microbiology, 14(4), 845-859. https://doi.org/10.1111/j.1462-2920.2011.02647.x
Bourgeois, A. L., Rinderer, T. E., Beaman, L. D., & Danka, R. G. (2010). Genetic detection and quantification of Nosema apis and Nosema ceranae in the honey bee. Journal of Invertebrate Pathology, 103(1), 53-58. https://doi.org/10.1016/j.jip.2009.10.009
Bourgeois, L., Beaman, L., Holloway, B., & Rinderer, T. E. (2012). External and internal detection of Nosema ceranae on honey bees using real-time PCR. Journal of invertebrate pathology, 109(3), 323-325. https://doi.10.1016/j.jip.2012.01.002
Broadrup, R. L., Mayack, C., Schick, S. J., Eppley, E. J., White, H. K., & Macherone, A. (2019). Honey bee (Apis mellifera) exposomes and dysregulated metabolic pathways associated with Nosema ceranae infection. PLOS ONE, 14(3), e0213249. https://doi.org/10.1371/journal.pone.0213249
Cantwell, G. E. (1970). Standard methods for counting Nosema spores. American Bee Journal, 110, 222-223.
Chemurot, M., De Smet, L., Brunain, M., De Rycke, R., & de Graaf, D. C. (2017). Nosema neumanni n. sp. (Microsporidia, Nosematidae), a new microsporidian parasite of honeybees (Apis mellifera) in Uganda. European Journal of Protistology, 61, 13-19. https://doi.org/10.1016/j.ejop.2017.07.002
Chen, Y. P., Evans, J. D., Murphy, C., Gutell, R., Zuker, M., Gundensen-Rindal, D. A., & Pettis, J. S. (2009). Morphological, molecular, and phylogenetic characterization of Nosema ceranae, a microsporidian parasite isolated from the European honey bee, Apis mellifera. Journal of Eukaryotic Microbiology, 56(2), 142-147. https://doi.org/10.1111/j.1550-7408.2008.00374.x
Chen, Y. W., Chung, W. P., Wang, C. H., Solter, L. F., & Huang, W. F. (2012). Nosema ceranae infection intensity highly correlates with temperature. Journal of Invertebrate Pathology, 111(3), 264-267. https://doi.org/10.1016/j.jip.2012.08.014
Chen, Y., Evans, J. D., Smith, I. B., & Pettis, J. S. (2008). Nosema ceranae is a long-present and widespread microsporidian infection of the European honey bee (Apis mellifera) in the United States. Journal of Invertebrate Pathology, 97(2), 186-188. https://doi.org/10.1016/j.jip.2007.07.010
Cilia, G., Cabbri, R., Maiorana, G., Cardaio, I., Dall’Olio, R., & Nanetti, A. (2018). A novel TaqMan® assay for Nosema ceranae quantification in honey bee, based on the protein coding gene Hsp70. European Journal of Protistology, 63, 44-50. https://doi.org/10.1016/j.ejop.2018.01.007
Cilia, G., Garrido, C., Bonetto, M., Tesoriero, D., & Nanetti, A. (2020). Effect of Api-Bioxal® and ApiHerb® treatments against Nosema ceranae infection in Apis mellifera investigated by two qPCR methods. Veterinary Sciences, 7(3), 125. https://doi.org/10.3390/vetsci7030125
Cilia, G., Luchetti, G., & Nanetti, A. (2022). Polymorphism of 16s rRNA gene: any effect on the biomolecular quantitation of the honey bee (Apis mellifera L., 1758) pathogen Nosema ceranae? Applied Sciences, 12(1), 422. https://doi.org/10.3390/app12010422
Cilia, G., Sagona, S., Giusti, M., Dos Santos, P. E., Nanetti, A., & Felicioli, A. (2019). Nosema ceranae infection in honeybee samples from Tuscanian Archipelago (Central Italy) investigated by two qPCR methods. Saudi Journal of Biological Sciences, 26(7), 1553-1556. https://doi.org/10.1016/j.sjbs.2018.11.017
Copley, T. R., Chen, H., Giovenazzo, P., Houle, E., & Jabaji, S. H. (2012). Prevalence and seasonality of Nosema species in Québec honey bees. Canadian Entomologist, 144(4), 577-588.
Corradi, N., & Keeling, P. J. (2009). Microsporidia: A journey through radical taxonomical revisions. Fungal Biology Reviews, 23(1–2), 1–8. https://doi.org/10.1016/j.fbr.2009.05.001
Dainat, B., Evans, J. D., Chen, Y. P., Gauthier, L., & Neumann, P. (2012). Predictive markers of honey bee colony collapse. PLOS ONE, 7(2), e32151. https://doi.org/10.1371/journal.pone.0032151
de Graaf, D. C., & Jacobs, F. J. (1991). Tissue specificity of Nosema apis. Journal of Invertebrate Pathology, 58(2), 277-278.
Duquesne, V., Gastaldi, C., Del Cont, A., Cougoule, N., Bober, A., Brunain, M., Chioveanu, G., Demicoli, N., Paulus, P. D., Somalo, P. F., & Filipova, M. (2021). An international inter-laboratory study on Nosema spp. spore detection and quantification through microscopic examination of crushed honey bee abdomens. Journal of Microbiological Methods, 184, 106183. https://doi.org/10.1016/j.mimet.2021.106183
Dussaubat, C., Maisonnasse, A., Crauser, D., Beslay, D., Costagliola, G., Soubeyrand, S., Kretzschmar, A., & Le Conte, Y. (2013). Flight behavior and pheromone changes associated with Nosema ceranae infection of honey bee workers (Apis mellifera) in field conditions. Journal of Invertebrate Pathology, 113(1), 42-51. https://doi.org/10.1016/j.jip.2013.01.002
Eiri, D. M., Suwannapong, G., Endler, M., & Nieh, J. C. (2015). Nosema ceranae can infect honey bee larvae and reduces subsequent adult longevity. PLOS ONE, 10(5), e0126330. https://doi.org/10.1371/journal.pone.0126330
Evans, J. D., & Schwarz, R. S. (2011). Bees brought to their knees: Microbes affecting honey bee health. Trends in Microbiology, 19(12), 614-620. https://doi.org/10.1016/j.tim.2011.09.003
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. https://doi.org/10.1016/j.vetpar.2010.02.010
Francis, R. M., Nielsen, S. L., & Kryger, P. (2013). Varroa-virus interaction in collapsing honey bee colonies. PLOS ONE, 8(3), e57540. https://doi.org/10.1371/journal.pone.0057540
Fries, I. (1988). Infectivity and multiplication of Nosema apis Z. in the ventriculus of the honey bee. Apidologie, 19(3), 319-328. https://doi.org/10.1051/apido:19880310
Fries, I. (1993). Nosema apis—A parasite in the honey bee colony. Bee World, 74(1), 5-19. https://doi.org/10.1080/0005772X.1993.11099149
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. European Journal of Protistology, 32(3), 356-365. https://doi.org/10.1016/S0932-4739(96)80059-9
Galajda, R., Valencakova, A., Sucik, M., & Kandracova, P. (2021). Nosema disease of European honey bees. Journal of Fungi, 7(9), 714. https://doi.org/10.3390/jof7090714
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. https://doi.org/10.1051/apido/2008065
Gisder, S., & Genersch, E. (2015). Identification of candidate agents active against N. ceranae infection in honey bees: establishment of a medium throughput screening assay based on N. ceranae infected cultured cells. PLOS ONE, 10(2), e0117200. https://doi.org/10.1371/journal.pone.0117200
Gisder, S., Hedtke, K., Möckel, N., Frielitz, M. C., Linde, A., & Genersch, E. (2010). Five-year cohort study of Nosema spp. in Germany: Does climate shape virulence and assertiveness of Nosema ceranae? Applied and Environmental Microbiology, 76(9), 3032-3038. https://doi.org/10.1128/AEM.03097-09
Grupe, A. C., & Quandt, C. A. (2020). A growing pandemic: A review of Nosema parasites in globally distributed domesticated and native bees. PLOS pathogens, 16(6), e1008580. https://doi.org/10.1371/journal.ppat.1008580
Haddad, N. (2014). First detection of Nosema ceranae in Jordan. European Scientific Journal, 10(33), 91-96.
Hasan, A., Qazi, J. I., Muzaffer, N., Jabeen, S., & Hussain, A. (2022). Effect of organic acids and probiotics on growth of Apis mellifera workers. Pakistan Journal of Zoology, 54(6), 2577-2583. https://dx.doi.org/10.17582/journal.pjz/20210803100802
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. https://doi.org/10.1016/j.jip.2006.11.001
Higes, M., García-Palencia, P., Urbieta, A., Nanetti, A., & Martín-Hernández, R. (2020). Nosema apis and Nosema ceranae tissue tropism in worker honey bees (Apis mellifera). Veterinary pathology, 57(1), 132-138. https://doi.org/10.1177/0300985819864302
Higes, M., Martín-Hernández, R., Botías, C., Bailón, E. G., González-Porto, A. V., Barrios, L., Del Nozal, M. J., Bernal, J. L., Jiménez, J. J., Palencia, P. G., & Meana, A. (2008). How natural infection by Nosema ceranae causes honeybee colony collapse. Environmental Microbiology, 10(10), 2659-2669. https://doi.org/10.1111/j.1462-2920.2008.01687.x
Higes, M., Martín-Hernández, R., Garrido-Bailón, E., González-Porto, A. V., García-Palencia, P., Meana, A., Del Nozal, M. J., Mayo, R., & Bernal, J. L. (2009). Honeybee colony collapse due to Nosema ceranae in professional apiaries. Environmental Microbiology Reports, 1(2), 110-113. https://doi.org/10.1111/j.1758-2229.2009.00014.x
Inglis, G. D., Enkerli, J. U., & Goettel, M. S. (2012). Laboratory techniques used for entomopathogenic fungi: Hypocreales. Journal of Invertebrate Pathology, 2, 189-253.
Kadri, S. M., Fulton, J. C., Prouty, C., Epperson, K. J., Orsi, R. O., & Ellis, J. D. (2025). Nosema ceranae prevalence in high and low honey producing colonies of African-derived honey bees (Apis mellifera) in Brazil. Journal of Apicultural Research, 64(4), 1101-1104. https://doi.org/10.1080/00218839.2025.2471118
Kartal, S., Tunca, R. I., Ozgül, O., Karabag, K., & Koc, H. (2021). Microscopic and molecular detection of Nosema spp. in the Southwest Aegean Region. Uludag Bee Journal, 21(1), 8-20. https://doi.org/10.31467/uluaricilik.880380
Khezri, M., Moharrami, M., Modirrousta, H., Torkaman, M., Salehi, S., Rokhzad, B., & Khanbabai, H. (2018). Molecular detection of Nosema ceranae in the apiaries of Kurdistan province, Iran. Veterinary Research Forum, 9(3), 273-278. https://doi.org/10.30466/vrf.2018.32086
Klee, J., Besana, A. M., Genersch, E., Gisder, S., Nanetti, A., Tam, D. Q., Chinh, T. X., Puerta, F., Ruz, J. M., Kryger, P., & Message, D. (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. https://doi.org/10.1016/j.jip.2007.02.014
Le Conte, Y., Ellis, M., & Ritter, W. (2010). Varroa mites and honey bee health: can Varroa explain part of the colony losses? Apidologie, 41(3), 353-363. https://doi.org/10.1051/apido/2010017
Lee, S. C., Corradi, N., Byrnes, E. J., Torres-Martinez, S., Dietrich, F. S., Keeling, P. J., & Heitman, J. (2008). Microsporidia evolved from ancestral sexual fungi. Current Biology, 18(21), 1675-1679. https://doi.org/10.1016/j.cub.2008.09.030
Martínez, J., Leal, G., & Conget, P. (2012). Nosema ceranae, an emergent pathogen of Apis mellifera in Chile. Parasitology Research, 111, 601-607. https://doi.org/10.1007/s00436.012.2875.0
Martín‐Hernández, R., Bartolomé, C., Chejanovsky, N., Le Conte, Y., Dalmon, A., Dussaubat, C., García‐Palencia, P., Meana, A., Pinto, M.A., Soroker, V. and Higes, M. (2018). Nosema ceranae in Apis mellifera: a 12 years postdetection perspective. Environmental microbiology, 20(4), 1302-1329. https://doi.org/10.1111/1462-2920.14103
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(3), 605-612. https://doi.org/10.1007/s00436-011-2292-9
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. https://doi.org/10.1128/AEM.00270-07
Milbrath, M. O., van Tran, T., Huang, W. F., Solter, L. F., Tarpy, D. R., Lawrence, F., & Huang, Z. Y. (2015). Comparative virulence and competition between Nosema apis and Nosema ceranae in honey bees (Apis mellifera). Journal of Invertebrate Pathology, 125, 9-15. https://doi.org/10.1016/j.jip.2014.12.006
Moshaverinia, A., Abedi, V., & Safaei, H. (2012). A survey of Nosema apis infection in apiaries of North Khorasan province, Iran. Iranian Journal of Veterinary Science and Technology, 4(2), 25-30. https://doi.org/10.22067/veterinary.v4i2.17418
Mustafa, G., Iqbal, A., Javid, A., Hussain, A., Bukhari, S. M., Ali, W., Saleem, M., Azam, S. M., Sughra, F., Ali, A., & Rehman, K. U. (2021). Variations in nutritional profile of honey produced by various species of genus Apis. Brazilian Journal of Biology, 83, e246651. https://doi.org/10.1590/1519-6984.246651
Nabian, S., Ahmadi, K., Shirazi, M. N., & Sadeghian, A. G. (2011). First detection of Nosema ceranae, a microsporidian protozoa of European honeybees (Apis mellifera) in Iran. Iranian Journal of Parasitology, 6(3), 89-95.
Nanetti, A., Cilia, G., Bonetto, M., Tesoriero, D., & Garrido, C. (2019). Efficacy of Api-Bioxal and ApiHerb against Nosema ceranae investigated by two q-PCR methods. BeeSafe, CREA. https://doi.org/10.13140/RG.2.2.29188.27522
Nazir, S., Manzoor, F., Perveen, I., Rana, A., Naureen, I., Nadeem, A. A., & Naeem, H. N. (2023). Isolation, screening and characterization of the viral pathogens from Apis mellifera colonies. Journal of Innovative Science, 9(1), 88-94. https://doi.org/10.17582/journal.jis/2023/9.1.88.94
Neumann, P., & Carreck, N. L. (2010). Honey bee colony losses. Journal of Apicultural Research, 49(1), 1-6. https://doi.org/10.3896/IBRA.1.49.1.01
Neumann, P., Pettis, J. S., & Schafer, M. O. (2016). The small hive beetle (Aethina tumida): Biology and control of small hive beetles. Apidologie, 47, 427-466. https://doi.org/10.1007/s13592-016-0426-x
Oğuz, B., Karapinar, Z., Dincer, E., & DEĞER, M. S. (2017). Molecular detection of Nosema spp. and black queen-cell virus in honeybees in Van Province, Turkey. Turkish Journal of Veterinary and Animal Sciences, 41(2), 221-227. https://doi.org/10.3906/vet-1604-92
Ostap-Chec, M., Cait, J., Scott, R. W., Arct, A., Moroń, D., Rapacz, M., & Miler, K. (2024). Nosemosis negatively affects honeybee survival: experimental and meta-analytic evidence. Parasitology, 151(14), 1530-1542. https://doi.org/10.1017/S0031182024001446
Ptaszyńska, A. A., & Gancarz, M. (2023). Microsporidiosis causing necrotic changes in the honeybee intestine. Applied Sciences, 13(8), 4957. https://doi.org/10.3390/app13084957
Ptaszyńska, A. A., Borsuk, G., Anusiewicz, M., & Mułenko, W. (2012). Location of Nosema spp. spores within the body of the honey bee. Medycyna Weterynaryjna, 68(10), 618-621.
Ptaszyńska, A. A., Borsuk, G., Mułenko, W., & Demetraki-Paleolog, J. (2014). Differentiation of Nosema apis and Nosema ceranae spores under Scanning Electron Microscopy (SEM). Journal of Apicultural Research, 53(5), 537-544. https://doi.org/10.3896/IBRA.1.53.5.02
Retschnig, G., Williams, G. R., Schneeberger, A., & Neumann, P. (2017). Cold ambient temperature promotes Nosema spp. intensity in honey bees (Apis mellifera). Insects, 8(1), 1-20. http://doi.org/10.3390/insects8010020
Rodríguez, M., Vargas, M., Antúnez, K., Gerding, M., Ovídio Castro, F., & Zapata, N. (2014). Prevalence and phylogenetic analysis of honey bee viruses in the Biobío Region of Chile and their association with other honey bee pathogens. Chilean Journal of Agricultural Research, 74(2), 170-177. http://doi.org/10.4067/S0718.58392014000200007
Rodríguez-Vásquez, S., Bejar, A. A., Romo-Chacón, A., García-Hernández, J., González-Ríos, H., & Orozco-Avitia, J. A. (2024). Hive temperature regulation by honeybees in response to extreme conditions. Agrociencia. https://doi.org/10.47163/agrociencia.v58i3.3082
Salman, A. M., Mohd, M. H., Almansoori, A. K. K., & Manmi, K. M. (2026). Nonlinear dynamics of Nosema ceranae and the fragile resilience of honeybee colonies under environmental strain. Scientific Reports, 16, 10905. https://doi.org/10.1038/s41598-026-45351-1
Sharma, D., Katna, S., Sharma, R., Rana, B. S., Sharma, H. K., Bhardwaj, V., & Chauhan, A. (2019). First detection of Nosema ceranae infecting Apis mellifera in India. Journal of Apicultural Science, 63(1), 165-170. https://doi.org/10.2478/jas-2019-0002
Shirzadi, A., & Razmi, G. (2021). A microscopy and molecular studies of Nosema ceranae infection in Mazandaran Province of Iran. Uludag Bee Journal, 21(2), 198-205. https://doi.org/10.31467/uluaricilik.991579
Smart, M. D., & Sheppard, W. S. (2012). Nosema ceranae in age cohorts of the western honey bee (Apis mellifera). Journal of Invertebrate Pathology, 109(1), 148-151. https://doi.org/10.1016/j.jip.2011.09.009
Tesovnik, T., Zorc, M., Ristanic, M., Glavinic, U., Stevanovic, J., Narat, M., & Stanimirovic, Z. (2020). Exposure of honey bee larvae to thiamethoxam and its interaction with Nosema ceranae infection in adult honey bees. Environmental Pollution, 256, 113443. https://doi.org/10.1016/j.envpol.2019.113443
Tiritelli, R., Flaminio, S., Zavatta, L., Ranalli, R., Giovanetti, M., Grasso, D. A., Leonardi, S., Bonforte, M., Boni, C. B., Cargnus, E., & Catania, R. (2024). Ecological and social factors influence interspecific pathogens occurrence among bees. Scientific Reports, 14(1), 5136-5152. https://doi.org/10.1038/s41598-024-55718-x
Tosun, O., & Yaman, M. (2016). The effects of temperature and humidity around the beehives on the distribution of Nosema ceranae, and also geographical and seasonal activity of the infection in the eastern Black Sea Region of Turkey. Mellifera, 6(7), 513-522. https://doi.org/10.17265/2162-5263/2016.11.001
Traver, B. E., & Fell, R. D. (2011). Nosema ceranae in drone honey bees (Apis mellifera). Journal of Invertebrate Pathology, 107(3), 234-236.
Traver, B. E., & Fell, R. D. (2012). Low natural levels of Nosema ceranae in Apis mellifera queens. Journal of Invertebrate Pathology, 110(3), 408-410. https://doi.org/10.1016/j.jip.2012.04.001
Traver, B. E., & Fell, R. D. (2014). Nosema and honey bee colony health. Virginia Tech, ENTO-66NP, 1-7.
Truong, A. T., Sevin, S., Kim, S., Yoo, M. S., Cho, Y. S., & Yoon, B. (2021). Rapidly quantitative detection of Nosema ceranae in honeybees using ultra-rapid real-time quantitative PCR. Journal of Veterinary Science, 22(3), e40. https://doi.org/10.4142/jvs.2021.22.e40
Vargas, M., Arismendi, N., Riveros, G., Zapata, N., Bruna, A., Vidal, M., Rodriguez, M., & Gerding, M. (2017). Viral and intestinal diseases detected in Apis mellifera in Central and Southern Chile. Chilean Journal of Agricultural Research, 77(3), 243-249. http://doi.org/10.4067/S0718-58392017000300243
Wang, Q., Dai, P., Guzman-Novoa, E., Wu, Y., Hou, C., & Diao, Q. (2019). Nosema ceranae, the most common microsporidium infecting Apis mellifera in the main beekeeping regions of China since at least 2005. Journal of Apicultural Research, 58(4), 562-566. https://doi.org/10.1080/00218839.2019.1632148
Yoko, L. D., Nuno, C., Per, K., Joana, A., Jorgen, A. A., Mette, G. B., Marianne, B., Silvia, C., Julie, F., Geoff, B. G., & Annika, S. J. (2021). Research project on field data collection for honey bee colony model evaluation. EFSA Support Publications, 18(7), 6695-6801. https://doi.org/10.2903/sp.efsa.2021.EN-6695
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2022 Journal of Wildlife and Biodiversity

This work is licensed under a Creative Commons Attribution 4.0 International License.