Acknowledgement
This work was supported by the "Cooperative Research Program for Agriculture Science and Technology Development (Project No. PJ01408002)" Rural Development Administration of the Republic of Korea, as well as by the Korea Institute of Planning and Evaluation for Technology in Food, Agriculture and Forestry, through the Agri-Bio Industry Technology Development Program (318093-03), partially funded by the Animal and Plant Quarantine Agency (Grant No. B-1543081-2019-21-03).
References
- Fries I, Feng F, Da Silva A, Slemeda SB, Pieniazek NJ. Nosema ceranae n. sp. (Microspora, Nosematidae), morphological and molecular characterization of a microsporidian parasite of the Asian honey bee Apis cerana (Hymenoptera, Apidae). Eur J Protistol. 1996;32(3):356-365. https://doi.org/10.1016/S0932-4739(96)80059-9
- Higes M, Martin R, Meana A. Nosema ceranae, a new microsporidian parasite in honeybees in Europe. J Invertebr Pathol. 2006;92(2):93-95. https://doi.org/10.1016/j.jip.2006.02.005
- Higes M, Martin-Hernandez R, Botias C, Bailon EG, Gonzalez-Porto AV, Barrios L, et al. How natural infection by Nosema ceranae causes honeybee colony collapse. Environ Microbiol. 2008;10(10):2659-2669. https://doi.org/10.1111/j.1462-2920.2008.01687.x
- Klee J, Besana AM, Genersch E, Gisder S, Nanetti A, Tam DQ, et al. Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. J Invertebr Pathol. 2007;96(1):1-10. https://doi.org/10.1016/j.jip.2007.02.014
- Martin-Hernandez R, Meana A, Prieto L, Salvador AM, Garrido-Bailon E, Higes M. Outcome of colonization of Apis mellifera by Nosema ceranae. Appl Environ Microbiol. 2007;73(20):6331-6338. https://doi.org/10.1128/AEM.00270-07
- Williams GR, Shafer AB, Rogers RE, Shutler D, Stewart DT. First detection of Nosema ceranae, a microsporidian parasite of European honey bees (Apis mellifera), in Canada and central USA. J Invertebr Pathol. 2008;97(2):189-192. https://doi.org/10.1016/j.jip.2007.08.005
- Chen Y, Huang ZY. Nosema ceranae, a newly identified pathogen of Apis mellifera in the USA and Asia. Apidologie (Celle). 2010;41(3):364-374. https://doi.org/10.1051/apido/2010021
- Fries I. Nosema ceranae in European honey bees (Apis mellifera). J Invertebr Pathol. 2010;103 Suppl 1:S73-S79. https://doi.org/10.1016/j.jip.2009.06.017
- Urbieta-Magro A, Higes M, Meana A, Gomez-Moracho T, Rodriguez-Garcia C, Barrios L, et al. The levels of natural Nosema spp. infection in Apis mellifera iberiensis brood stages. Int J Parasitol. 2019;49(8):657-667. https://doi.org/10.1016/j.ijpara.2019.04.002
- Gallai N, Salles JM, Settele J, Vaissiere BE. Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol Econ. 2009;68(3):810-821. https://doi.org/10.1016/j.ecolecon.2008.06.014
- Ollerton J, Winfree R, Tarrant S. How many flowering plants are pollinated by animals? Oikos. 2011;120(3):321-326. https://doi.org/10.1111/j.1600-0706.2010.18644.x
- Glenny W, Cavigli I, Daughenbaugh KF, Radford R, Kegley SE, Flenniken ML. Honey bee (Apis mellifera) colony health and pathogen composition in migratory beekeeping operations involved in California almond pollination. PLoS One. 2017;12(8):e0182814. https://doi.org/10.1371/journal.pone.0182814
- Botias C, Anderson DL, Meana A, Garrido-Bailon E, Martin-Hernandez R, Higes M. Further evidence of an oriental origin for Nosema ceranae (Microsporidia: Nosematidae). J Invertebr Pathol. 2012;110(1):108-113. https://doi.org/10.1016/j.jip.2012.02.014
- Lee ML, Choi JY, Lee MY, Kim YS. Infection level of honeybee Nosema disease in Korea. Korean J Apic. 2003;18(2):151-154.
- Hong IP, Lee MY, Woo SO, Sim HS, Choi YS, Han SM, et al. Prevalence of honeybee Nosema disease and black queen cell virus on flowering period of Robinia pseudoacacia in 2013. Korean J Apic. 2013;28(3):199-203.
- Annual report of honeybee diseases in Korea [Internet]. Gimcheon: Animal and Plant Quarantine Agency; http://www.qia.go.kr/anp/rchStatus/listwebQiaCom.do?type=79_1hbedp&clear=1. Updated 2020. Accessed 2020 Sep 18.
- Fries I, Chauzat MP, Chen YP, Doublet V, Genersch E, Gisder S, et al. Standard methods for Nosema research. J Apic Res. 2013;52(1):1-28.
- Human H, Brodschneider R, Dietemann V, Dively G, Ellis JD, Forsgren E, et al. Miscellaneous standard methods for Apis mellifera research. J Apic Res. 2013;52(4):1-53.
- Cantwell G. Standard methods for counting Nosema spores. Am Bee J. 1970;110:222-223.
- Ptaszynska A, Borsuk G, Mulenko W, Demetraki-Paleolog J. Differentiation of Nosema apis and Nosema ceranae spores under scanning electron microscopy (SEM). J Apic Res. 2014;53(5):537-544. https://doi.org/10.3896/IBRA.1.53.5.02
- Chen YP, Evans JD, Murphy C, Gutell R, Zuker M, Gundensen-Rindal D, et al. Morphological, molecular, and phylogenetic characterization of Nosema ceranae, a microsporidian parasite isolated from the European honey bee, Apis mellifera. J Eukaryot Microbiol. 2009;56(2):142-147. https://doi.org/10.1111/j.1550-7408.2008.00374.x
- Riviere MP, Ribiere M, Chauzat MP. Recent molecular biology methods for foulbrood and nosemosis diagnosis. Rev Sci Tech. 2013;32(3):885-892. https://doi.org/10.20506/rst.32.2.2207
- Hamiduzzaman MM, Guzman-Novoa E, Goodwin PH. A multiplex PCR assay to diagnose and quantify Nosema infections in honey bees (Apis mellifera). J Invertebr Pathol. 2010;105(2):151-155. https://doi.org/10.1016/j.jip.2010.06.001
- Bourgeois AL, Rinderer TE, Beaman LD, Danka RG. Genetic detection and quantification of Nosema apis and N. ceranae in the honey bee. J Invertebr Pathol. 2010;103(1):53-58. https://doi.org/10.1016/j.jip.2009.10.009
- Forsgren E, Fries I. Comparative virulence of Nosema ceranae and Nosema apis in individual European honey bees. Vet Parasitol. 2010;170(3-4):212-217. https://doi.org/10.1016/j.vetpar.2010.02.010
- Ptaszynska AA, Borsuk G, Wozniakowski G, Gnat S, Malek W. Loop-mediated isothermal amplification (LAMP) assays for rapid detection and differentiation of Nosema apis and N. ceranae in honeybees. FEMS Microbiol Lett. 2014;357(1):40-48. https://doi.org/10.1111/1574-6968.12521
- Chupia V, Patchanee P, Krutmuang P, Pikulkaew S. Development and evaluation of loop-mediated isothermal amplification for rapid detection of Nosema ceranae in honeybee. Asian Pac J Trop Dis. 2016;6(12):952-956. https://doi.org/10.1016/S2222-1808(16)61163-5
- Urbieta-Magro A, Higes M, Meana A, Barrios L, Martin-Hernandez R. Age and method of inoculation influence the infection of worker honey bees (Apis mellifera) by Nosema ceranae. Insects. 2019;10(12):417. https://doi.org/10.3390/insects10120417
- Rubanov A, Russell KA, Rothman JA, Nieh JC, McFrederick QS. Intensity of Nosema ceranae infection is associated with specific honey bee gut bacteria and weakly associated with gut microbiome structure. Sci Rep. 2019;9(1):3820. https://doi.org/10.1038/s41598-019-40347-6
- Wang J, Lee D, Ku SJ, Peak MC, Min SH, Lim SJ, et al. Development of a detection method against 11 major pathogens of honey bee using amplification of multiplex PCR and specific DNA-chip. J Apic. 2016;31(2):133-146.
- Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, et al. Clustal W and Clustal X version 2.0. Bioinformatics. 2007;23(21):2947-2948. https://doi.org/10.1093/bioinformatics/btm404
- Williams G, Alaux C, Costa C, Csaki T, Doublet V, Eisenhardt D, et al. Standard methods for maintaining adult Apis mellifera in cages under in vitro laboratory conditions. J Apic Res. 2013;52(1):1-36.
- Yucel B, Gogaroglu M. The impact of Nosema apis Z. infestation of honey bee (Apis mellifera L.) colonies after using different treatment methods and their effects on the population levels of workers and honey production on consecutive years. Pak J Biol Sci. 2005;8(8):1142-1145. https://doi.org/10.3923/pjbs.2005.1142.1145
- Gray FH, Cali A, Briggs JD. Intracellular stages in the life cycle of the microsporidian Nosema apis. J Invertebr Pathol. 1969;14(3):391-394. https://doi.org/10.1016/0022-2011(69)90167-0
- Refardt D, Ebert D. Quantitative PCR to detect, discriminate and quantify intracellular parasites in their host: an example from three microsporidians in Daphnia. Parasitology. 2006;133(Pt 1):11-18. https://doi.org/10.1017/S0031182006000060
- Fu Z, He X, Cai S, Liu H, He X, Li M, et al. Quantitative PCR for detection of Nosema bombycis in single silkworm eggs and newly hatched larvae. J Microbiol Methods. 2016;120:72-78. https://doi.org/10.1016/j.mimet.2015.12.003
- Erler S, Lommatzsch S, Lattorff HM. Comparative analysis of detection limits and specificity of molecular diagnostic markers for three pathogens (Microsporidia, Nosema spp.) in the key pollinators Apis mellifera and Bombus terrestris. Parasitol Res. 2012;110(4):1403-1410. https://doi.org/10.1007/s00436-011-2640-9
- Lawyer FC, Stoffel S, Saiki RK, Chang SY, Landre PA, Abramson RD, et al. High-level expression, purification, and enzymatic characterization of full-length Thermus aquaticus DNA polymerase and a truncated form deficient in 5' to 3' exonuclease activity. PCR Methods Appl. 1993;2(4):275-287. https://doi.org/10.1101/gr.2.4.275