First Detection of Nosema ceranae, a Microsporidian Protozoa of European Honey­bees (Apis mellifera) In Iran

  • S Nabian Department of Parasitology, Faculty of Veterinary Medicine, University of Tehran, Iran
  • K Ahmadi Veterinary Organization of Iran, Tehran, Iran
  • MH Nazem Shirazi Veterinary Organization of Iran, Tehran, Iran
  • A Gerami Sadeghian Department of Parasitology, Faculty of Veterinary Medicine, University of Tehran, Iran
Keywords: Honeybee, Nosema apis, Nosema ceranae, PCR

Abstract

Background: Nosemosis of European honey bee (Apis mellifera) is present in bee colonies world­wide. Until recently, Nosema apis had been regarded as the causative agent of the disease, that causes heavy economic losses in apicultures. Nosema ceranae is an emerging microsporidian para­site of European honeybees, A. mellifera, but its distribution is not well known. Previously, nosemosis in honeybees in Iran was attributed exclusively to N. apis.Methods: Six Nosema positive samples (determined from light microscopy of spores) of adult worker bees from one province of Iran (Savadkouh- Mazandaran, northern Iran) were tested to determine Nosema species using previously- developed PCR primers of the 16 S rRNA gene. As it is difficult to distinguish N. ceranae and N. apis morphologically, a PCR assay based on 16 S ribosomal RNA has been used to differentiate N. apis and N. ceranae.Results: Only N. ceranae was found in all samples, indicating that this species present in Iran apiar­ies.Conclusion: This is the first report of N. ceranae in colonies of A. mellifera in Iran. It seems that intensive surveys are needed to determine the distribution and prevalence of N. ceranae in differ­ent regions of Iran.

References

Zander ET. Parasiten als Krankheitserreger bei der Biene. Munch Bien Z. 1909; 31: 196-204.

Faucon JP. La nosemose. Sant Abei. 2005; 209:343-367.

Higes M, Martin R, Sanz A. Chronic] nosemosis in Apis mellifera: an increasing problem. 2004; 637-638. In Mas-Coma, M.D. Bargues, JG Esteban,Valero MA(ed), Mulyidisciplinarity for parasites, vectors and parasitic diseases. Proceedings of the IX European Multicolloquium of Parasitology.

Martin R,Meana A, HigesM. Increase of nosemosis in Spain. 2005; 49-50. In A.J.dos Santos Gracio (ed.), Acta Parasitologica Portuguesa. Socidedade Portuguesa de Parasitologia, Lisboa, Portugal.

HigesM,Martin R, Meana A. Nosema ceranae, a newmicrosporidian parasite in honey bees in Europe. J Invertebr Pathol. 2006; 92:93-95.

Fries I, Martin R, Meana A, Garcia- Palencia P, Higes M. Natural infections of Nosema ceranae in European honey bees. J Apicult Res. 2006; 45: 230-233.

Chauzat MP, Higes M, Martin- Hernandez R, Meana M, Cougoule N, Faucon JP. Presence of Nosema ceranae in French honey bee colonies. J ApicultRes. 2007; 46: 127-128.

Cox-Foster DL,Conlan S, Holmes EC, Palacios G, Evans JD, Moran NA, Quan PL, Briese T, Hornig M, Geiser DM, Martinson V, VanEngelsdorp D, Kalkstein AL, Drysdale A, Hui J, Zhai J, Cui L, Hutchison SK, Simons JF, Egholm M, Pettis JS, Lipkin WI. A metagenomic survey of microbs in honey bee colony collapse disorder. Sci. 2007; 318: 283-287.

Klee J, Besana AM, Genersch E, Gisder S, Nanetti A, Tam DQ, Chinh TX, Puerta F, Ruz JM, Kryger P, Message D, Hatjina F, Korpela S, Fries I, Paxton RJ, Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. J Invertebr Pathol. 2007; 96: 1-10.

Huang WF, Jiang JH, Chen YW, Wang CH, A Nosema ceranae isolate from the honey bee Apis mellifera. Apidol. 2007; 38: 30-37.

Paxton RJ, Klee J, Korpela S, Fries I, Nosema ceranae has infected Apis mellifera in Europe since at least 1998 andmay be more virulent than Nosema apis. Apidol. 2007; 38: 558-565.

Chen Y, Evans JD, Smith IB, Pettis JS. Nosema ceranae is a long –present and wide –spread microsporidian infection of the European honey bee (Apis mellifera) in the United States. J Invertebr Pathol. 2008; 97:186- 188.

Sarlo E, Medici SK, Braunstein M, Eguaras M, Presencia Y distribucion de Nosema ceranae en la region sudeste de la provincial de Buenos Arires. In: Actas del Segundo Congreso Argentino de Apicultura, Mar del Plata, Argentina, Agosto,2008;26.

Williams GR, Shafer ABA, Rogers REL, Shutler D, Stewart DT, First detection of Nosema ceranae, a microsporidean parasite of European honey bees (Apis mellifera), in Canada and Central USA, J Invertebr Pathol. 2008; 97: 189-192.

Higes M, Garcia- Palencia P, Martin- Hernandez R , Meana A. Experimental infection of Apis mellifera honey bees with Nosema ceranae( Microsporidia). J Invertebr Pathol. 2007; 94: 211-217.

HigesM,Martin R, Sanz A, Avarez N, Garcia M P, Meana A. El syndrome de despoblamiento de las colmenas en Espana. Consideraciones sobre su origen.nVidaApicola . 2005; 133 : 15-21.

Martin- Hernandez R, Meana A, Prieto L, Martinez Salvador A, Garrido- Bailon E, Higes M, Outcome of colonization of Apis mellifera by Nosema ceranae. Appl Environ Microbiol. 2007; 73, 6331-6338.

Weiss LM, VossbrinckCR, Molecular biology, Molecular phylogeny and molecular diagnostic approaches to the microsporidia. 1999; 129-171. In M. Winter andWeiss LM(ed.), Themicrosporidia and microsporidiosis. Am Soc Microbiol, Washington,DC.

Tay WT, Omahony EM, Paxton J . Complete rRNA gene sequence reveals that the microsporidiun Nosema bombi infects diverse bumble bee ( Bombus spp.) hosts yet contains multiple polymorphic sites. J Eukaryot Microbiol. 2005; 52.

Lotfi A, Jamshidi R, Aghdam Shahryar H, YousefkhaniM. The prevalence of nosemosis in honey bee colonies in Arasbaran region (Northwestern Iran). Am Eurasian J Agri Enviro Sci. 2008; 5(2):255-257.

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; 879-882.

OIE, Manual for diagnostic tests and vaccines for terrestrial animals, Chapter 2.2.4, Nosemosis of honey bees. OIE, Paris, France;2008.p. 23.

De Graaf DC, Masschelein G, Vandergeynst F, De Bravander HF, Jacobs FJ . In Vitro germination of Nosema apis ( Microspora : Nosematidae) spores and its effects on their αα – trehalose/D—glucose ratio. J Invertebr Pathol. 1993; 62:220-225.

Rice R. Nosema disease in honey bees. Genetic variation and control.; RIRDC 1/46. Rural Industries Research and Development Corporation, Kingston,Australia; 2001.

Fries I, Protozoa. In: Morse RA, Flottum K, Editors, Honey Bee Pests, Predators and Diseases, AI Root Company, Medina, Ohio, USA. 1997; 59-76.

How to Cite
1.
Nabian S, Ahmadi K, Nazem Shirazi M, Gerami Sadeghian A. First Detection of Nosema ceranae, a Microsporidian Protozoa of European Honey­bees (Apis mellifera) In Iran. Iran J Parasitol. 6(3):89-95.
Section
Articles