Distribution of Nosema Spp. in climatic regions of Iran

Document Type: Original Article


1 Department of Animal Science Research, Kurdistan Agricultural and Natural Resources Research and Education Center, (AREEO), Sanandaj, Iran

2 Department of Food Hygiene and Quality Control, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran

3 Department of Honeybee, Silk Worm and wildlife Diseases, Razi Vaccine and Serum Research Institute, Agricultural Research, Education and Extension Organization (AREEO), Karaj, Iran

4 Department of Parasitology, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran

5 Directorate of Health and Control of Bird, Honeybee and Silk Worm, Veterinary Organization, Tehran, Iran


Nosemosis is one of the most prevalent bee diseases in the world causing significant ‎economic losses in the global bee-keeping industry. This cross-sectional study was conducted during April-September, 2016 to investigate the prevalence of nosemosis in different climatic regions of Iran. A total of 183 ‎apiaries were selected based on cluster sampling and the climate of apiaries under study was classified using Domarten method. In each apiary, five percent of the colonies were ‎ randomly sampled. A total of 183 adult bee samples were taken and examined by microscopic and polymerase chain reaction (PCR) methods for the presence of Nosema infections. According to the results, infection caused by Nosema ceranae was observed in all regions under study. The prevalence of N. ceranae was 46.40% (42.70–50.10). However, infection with Nosema apis was not observed in the samples in either pure form or as ‎associated infection. Based on the results of PCR, the prevalenceof N. ceranae was ‎53.80% (46.60– 61.00) ‎ in ‎humid, ‎71.00% (53.70–77.50) ‎ in semi-humid‎, ‎68.10% (61.40–74.80) ‎ in very humid, ‎29.40% (22.70–36.10) in arid, ‎34.30% (27.40–41.20) in semi-‎arid and ‎24.00% (17.90–30.00)‎ in Mediterranean climates. The prevalence of ‎infection in different climatic zones of the country was found to have significant ‎differences (p < 0.001). ‎ According to the findings, N. ceranae ‎ was the only Nosema species in honeybees with a broad geographical dispersion in Iran. It seems that climate can influence the prevalence of mentioned parasite. ‎


Main Subjects


  1. Webster T, Pomper K, Hunt G, et al. Nosema apis infection in worker and queen Apis mellifera. Apidologie 2004; 35(1): 49-54.
  2. Fries I. Nosema apis - a parasite in the honeybee colony. Bee World 1993; 74: 5-19.
  3. Oranlar E, Lotfi A, Aghdam Shahryar H. Seasonal incidence of some economic bee diseases (varroosis, nosemosis and American foulbrood) in honeybee colonies of northwestern Iran. Uludag Bee J 2011; 11: 25.
  4. Paxton R., Klee J, Korpela S, et al. Nosema ceranae has infected Apis mellifera in Europe since at least 1998 and may be more virulent than Nosema apis. Apidologie 2007; 38: 558-565.
  5. Chen YP, Evans JD, Murphy C, et al. Morphological, molecular and phylogenetic characterization of Nosema ceranae, a microsporidian parasite isolated from the European honey bee Apis mellifera. J Eukar Microbiol 2009; 56: 142-147.
  6. Weiss LM, Vossbrinck CR. Molecular biology, molecular phylogeny, and molecular diagnostic approaches to the microsporidia. In: Wittner M, Weiss LM (Eds). The microsporidia and microsporidiosis. Washington DC, USA: American society for microbiology 1999; 129-171.
  7. Martín-Hernández R, Meana A, Prieto L, et al. Outcome of colonization of Apis mellifera by Nosema ceranae. Appl Environ Microbiol 2007; 73(20): 6331-6338.
  8. Higes M, Martín-Hernández R, Meana A. Nosema ceranae in Europe: An emergent type C Nosemosis. Apidologie 2010; 41: 375-392.
  9. Klee J, Besana AM, Genersch E, 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.
  10. Higes M, Martín-Hernández R, Meana A. Nosema ceranae, a new microsporidian parasite in honeybees in Europe. J Invertebr Pathol 2006; 92: 81-83.
  11. Higes M, Martin-Hernandez R, Garrido-Bailon E, et al. Honeybee colony collapse due to Nosema ceranae in professional apiaries. Environ Microbiol Rep 2009; 1: 110-113.
  12. Nabian S, Ahmadi K, Shirazi MN, et al. First detection of Nosema ceranae, a microsporidian protozoa of European honeybees (Apis mellifera) in Iran. Iran J Parasitol 2011; 6(3): 89-95.
  13. Razmaraii N, Sadegh-Eteghad S, Babaei H, et al. Molecular identification of Nosema species in East Azerbaijan province, Iran. Arch Razi Inst 2013; 68(1): 23-27.
  14. Modirrousta H, Moharrami M, Mansouri MA. Retrospective study of the Nosema ceranae infection of honey bee colonies in Iran (2004-2013). Arch Razi Inst 2014; 69(2): 197-200.
  15. Aroee F, Azizi H, Shiran B, et al. Molecular identification of Nosema species in ‎provinces of Fars, Chaharmahal and ‎Bakhtiari and Isfahan (Southwestern Iran). Asian Pac J Trop Biomed 2017; 7(1): 10-13.
  16. Kamyabi S, Farahani S. Effective climatic factors in mountainous regions of Iran for urban planning: A case study in Rudbar Qasran in the central Alborz. e-Bangi: J Soc Sci Humanit 2011; 6(1): 17-28.
  17. Office international des epizooties, manual of diagnostic tests and vaccines for terrestrial animals. 2008; Chap. 2.2.4., Nosemosis of honey bees. http:// www.oie.int/fileadmin/Home/eng/Health_standards/tahm/2.02.04_nosemosis.pdf. Accessed June 25, 2017.
  18. Fries I. Nosema ceranae in European honey bees (Apis mellifera). J Invertebr Pathol 2010; 103(S1): S73-S79.
  19. Lotfi A, Jamshidi R, Aghdam Shahryar H, et al. The prevalence of nosemosis in honey bee colonies in Arasbaran region (northwestern Iran). American-Eurasian J Agric Environ Sci 2009; 5(2): 255-257.
  20. Razmaraii N, Karimi H. A survey of nosema disease of honey bee (Apis mellifera) in East Azarbaijan province of Iran. J Anim Vet Adv 2010; 9(5): 879-882.
  21. Davoudi J, Naderi A, Mohammadpour F, et al. Study of infection rate of suburb bee hives to parasites Nosema apis, Varroa spp. and Acarapis woodi in Miyaneh, Iran. J New Agric Sc 2009; 4(13): 39-43.
  22. Tavassoli M, Eiganinejad S, Alizadeh Asl S. A survey on Nosema apis infection in apiaries of Urmia, north-west of Iran. Iran J Vet Sci Technol 2009; 1(1): 35
  23. Moshaverinia A, Abedi V, Safaei H. A survey of Nosema apis infection in apiaries of North Khorasan province, Iran. Iran J Vet Sci Technol 2012; 4(2): 25-30.
  24. Oǧuz B, Karapinar Z, Dinerç E, et al. Molecular detection of Nosema spp. and black queen-cell virus in honeybees in Van province, Turkey. Turk J Vet Anim Sci 2017; 41: 221-227.
  25. Gajger IT, Vugrek O, Grilec D, et al. Prevalence and distribution of Nosema ceranae in Croatian honeybee colonies. Vet Med 2010; 55: 457-462.
  26. Chen YW, Chung WP, Wang CH, et al. Nosema ceranae infection intensity highly correlates with temperature. J Invertebr Pathol 2012; 111; 264-267.
  27. Invernizzia C, Abuda C, Tomascoa I, et al. Presence of Nosema ceranae in honeybees (Apismellifera) in Uruguay. J Invertebr Pathol 2009; 101: 150-153.
  28. Chen Y, Evans JD, Smith IB, et al. Nosema ceranae is a long-present and wide-spread microsporidean infection of the European honey bee (Apis mellifera) in the United States. J Invertebr Pathol 2008; 97: 186-188.
  29. Özgör E, Güzerin E, Keskin N. Determination and comparison of Nosema apis and Nosema ceranae in terms of geographic and climatic factors. Hacettepe J Biol Chem 2015; 43(1): 9-15.
  30. de La Rocque S, Rioux JA, Slingenbergh J. Climate change: Effects on animal disease systems and implications for surveillance and control. Rev Sci Tech Off Int Epizoot 2008; 27(2): 339-354.
  31. Fenoy S, Rueda C, Higes M, et al. High-level resistance of Nosema ceranae, a parasite of the honeybee, to temperature and desiccation. Appl Environ Microbiol 2009; 75: 6886-6889.
  32. Stevanovic J, Simeunovic P, Gajic B, et al. Characteristics of Nosema ceranae infection in Serbian honey bee colonies. Apidologie 2013; 44: 522-536.
  33. Cepero A, Martín-Hernández R, Bartolomé C, et al. Passive laboratory surveillance in Spain: Pathogens as risk factors for honey bee colony collapse. J Apic Res 2015; 54: 525-531.
  34. Cornman RS, Chen YP, Schatz MC, et al. Genomic analyses of the microsporidian Nosema ceranae, an emergent pathogen of honey bees. PLoS Pathogens 2009; 5(6): 1-14.
  35. Cox-Foster DL, Conlan S, Holmes EC, et al. A metagenomic survey of microbes in honey bee colony collapse disorder. Science 2007; 318: 283-287.
  36. Higes M, Meana A, Bartolomé C, et al. Nosema ceranae (Microsporidia), a controversial 21st century honey bee pathogen. Environ Microbiol Rep 2013; 5: 17-29.