Molecular identification of Nosema species in the apiary of Kurdistan province of Iran

Authors

1 Veterinary Research Department, Kurdistan , Agricultural Research Education and Extension (AREEO), Sanandaj, Iran

2 Department of Honey Bee, Silk Worm and Wildlife Research Diseases, Razi Vaccine and Serum Research Institute,Agricultural Research Education and Extension Organization(AREEO) , Karaj, Iran

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

4 Department of Honey Bee, Silk Worm and Wildlife Research Diseases, Razi Vaccine and Serum Research Institute, Karaj, Iran

5 Veterinary Research Department, Kurdistan, Agricultural Research Education and Extension (AREEO), Sanandaj, Iran

Abstract

Nosema disease is the most important adult bee disease but is mostly by beekeepers as there are no
characteristic obvious symptoms. Hence, Nosema disease is also referred to as "the silent killer". The aim of
the present study was to determine the molecular identification of Nosema spices in Kurdistan province of
Iran. 100 samples were collected from apiaries (870 hives) of Kurdistan. Samples were examined by a light
microscope and polymerase chain reaction (PCR) assay. The light microscope was used for determination of
the presence of Nosema spores in all of the collected samples. PCR assay based on 16S ribosomal RNA has
been used to differentiate between Nosema apis and Nosema ceranae. Only Nosema ceranae was found in
all samples, indicating that this species present in Kurdistan

Keywords

References

Adl, S.M.  Simpson, A.G.B.  Farmer, M.A.  Andersen, R.A.  Anderson, O.R.  Barta, J.R.  Bowser, S.S.  Brugerolle, G.  Fensome, R.A.  Fredericq, S.  James, T.Y.  Karpov, S.  Kugrens, P.  Krug, J.  Lane, C.E.  Lewis, L.A.  Lodge, J.  Lynn, D.H.  Mann, D.G.  McCourt, R.M.  Mendoza, L.  Moestrup, O.  Mozley-Standridge, S.E.  Nerad, T.A.  Shearer, C.A.  Smirnov, A.V.  Spiegel, F.W. Taylor, M.F.J.R.  (2005). The New Higher Level Classification of Eukaryotes with Emphasis on the Taxonomy of Protists. J Eukar Microbiol 52 399–451.
Bailey, L.  (1955). The epidemiology and control of Nosema disease of the honeybee. Ann Appl Biol 43: 379–389.
Bailey, L.  (1967). Nosema apis and dysentery of the honeybee. Journal of Apicultural Research 6: 121-125.
Bailey, L. Ball, B.V.  (1981). Honeybee Pathology. Harcourt Brace Jovanovich, sidcup, Kent, UK.
Bermejo, F.J.O. Fernández, P.G.  (1997). Nosema disease in the honey bee (Apis mellifera L) infested with varroa mites in southern Spain. Apidologie 28: 105-112.
Bokaie, S.  Sharifi, L. Mehrabadi, M.  (2014). Prevalence and Epizootical Aspects of Varroasis in Golestan Province, Northern Iran. J. Arthropod Borne Dis. 8: 102-107.
Borneck, R.  Viry, A.  Martín-Hernández, R. Higes, M.  (2010). Honey bee colony losses in the Jura Region, France and related pathogens. Journal of Apicultural Research 49: 334-336.
Bradbear, N.  (2009). Bees and their role in forest livelihoods: a guide to the services provided by bees and the sustainable harvesting, processing and marketing of their products. Non-wood Forest Products.
Budge, G.  Powell, M.  Roberts, K.  Adams, I.  Jones, B.  Marris, G.  Laurenson, L.  Wilkins, S.  Pietravalle, S. Brown, M.  (2010). What has Nosema got to do with losses? Monitoring both Nosema species in the UK. In In Proceedings of the 4th European Conference of Apidology, Kence, M., ed. (Ankara Turkey).
Chen, Y.P.  Evans, J.D.  Smith, J.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. J. Invertebr. Pathol. 97: 186-188.
Chen, Y.P. Huang, Z.Y.  (2010). Nosema ceranae, a newly identified pathogen of Apis mellifera in the USA and Asia. Apidologie 41: 364-374.
COLOSS, w.  (Year) of Conference. Conclusions, Proc. Workshop “Nosema disease: lack of knowledge and work standardization”. In, accessed on 20 Nov. 2009.
Farrar, C.L.  (1942). Nosema disease contributes to winter losses and queen supersedure. Gleanings in Bee Culture 70: 660-661,701.
Farrar, C.L.  (1947). Nosema losses in package bees as related to queen supersedure and honey yields. J Econ Entomol 40: 333-338.
Faucon, J.P.  (2005). La Nosémose. La Santé de l’Abeille 209: 344-368.
Fries, I.  (1988). Comb replacement and Nosema disease (Nosema apis Z.) in honey bee colonies. Apidologie 19: 343-354.
Fries, I.  (2010). Nosema ceranae in European honey bees (Apis mellifera). J. Invertebr. Pathol. 103: S73-S79.
Fries, I.  Ekbohm, G. Villumstad, E. (1984). Nosema apis, sampling techniques and honey yield. Journal of Apicultural Research 23: 102-105.
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). Eur. J. Protistol. 32: 356-365.
Fries, I.  Martín, R.  Meana, A.  GarcíaPalencia, P. Higes, M.  (2006). Natural infections of Nosema ceranae in European honey bees. J. Apic. Res. 47: 230-233.
Furgala, B. Mussen, E.C.  (1978). Protozoa, In:  Morse, R. (Ed.) Honey bee pests, predators and diseases. Cornell University Press, Ithaca, USA, pp. 63-77.
Giersch, T.  Berg, T.  Galea, F. Hornitzky, M.  (2009). Nosema ceranae infects honey bees (Apis mellifera) and contaminates honey in Australia. Apidologie 40: 117-123.
Gisder, S.  Hedtke, K.  Mo¨ckel, 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? Appl Environ Microbiol 76: 3032–3038.
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: 211-217.
Higes, M.  Martín-Hernández, R.  Botías, C.  GarridoBailón, E.  González-Porto, A.V.  Barrios, L.  del Nozal, M.  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: 2659–2669.
Higes, M.  Martín-Hernández, R.  Garrido-Bailón, E.  Botías, C. Meana, A.  (2009a). First detection of Nosema ceranae (Microsporidia) in African Honey bees (Apis mellifera intermissa). Journal of Apicultural Research 48: 217-219.
Higes, M.  Martin-Hernandez, R. Meana, A.  (2010). Nosema ceranae in Europe: an emergent type C nosemosis. Apidologie 41: 375-392.
Higes, M.  Martín‐Hernández, R.  García‐Palencia, P.  Marín, P. Meana, A.  (2009b). Horizontal transmission of Nosema ceranae (Microsporidia) from worker honeybees to queens (Apis mellifera). Environmental microbiology reports 1: 495-498.
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.  (2009c). Honeybee colony collapse due to Nosema ceranae in professional apiaries. Environmental Microbiology Reports 1: 110-113.
Higes, M.  Martín, R. Meana, A.  (2006). Nosema ceranae, a new microsporidian parasite in honeybees in Europe. J. Invertebr. Pathol. 92: 93-95.
Higes, M.  Meana, A.  Bartolomé, C.  Botías, C. Martín‐Hernández, R.  (2013). Nosema ceranae (Microsporidia), a controversial 21st century honey bee pathogen. Environmental microbiology reports 5: 17-29.
Huang, W.-F.  Jiang, J.-H.  Chen, Y.-W. Wang, C.-H.  (2007). A Nosema ceranae isolate from the honeybee Apis mellifera. Apidologie 38: 30-37.
Keeling, P.  (2009). Five questions about Microsporidia. Plos Pathog 5: 1-3.
Klee, J.  Besana, A.M.  Genersch, E.  Gisder, S.  Nanetti, A.  Tam, D.Q.  Chinh, T.X.  Puerta, F.  Ruz, J.M. Kryger, P.  (2007). Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. J. Invertebr. Pathol. 96: 1-10.
Lotfi, A.R.  Jamshidi, R.  Aghdam Shahryar, H. Yousefkhani, M.  (2009). The Prevalence of Nosemosis in Honey Bee Colonies in Arasbaran Region (Northwestern Iran). American-Eurasian Journal of Agricultural & Environmental Sciences 5: 255-257.
Martín-Hernández, R.  Meana, A.  García-Palencia, P.  Marín, P.  Botías, C.  Garrido-Bailón, E.  Barrios, L. Higes, M.  (2009). Effect of temperature on the biotic potential of honeybee microsporidia. Applied and Environmental Microbiology 75: 2554-2557.
Martín-Hernández, R.  Meana, A. Higes, M.  (2005). Increase of nosemosis in Spain. Acta Parasitol Portuguesa 12: 49-50.
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. Appl. Environ. Microbiol. 73: 6331-6338.
Martín‐Hernández, R.  Botías, C.  Bailón, E.G.  Martínez‐Salvador, A.  Prieto, L.  Meana, A. Higes, M.  (2012). Microsporidia infecting Apis mellifera: coexistence or competition. Is Nosema ceranae replacing Nosema apis? Environmental microbiology 14: 2127-2138.
Martínez, J.  Leal, G. Conget, P.  (2012). Nosema ceranae an emergent pathogen of Apis mellifera in Chile. Parasitology research 111: 601-607.
Medici, S.K.  Sarlo, E.G.  Porrini, M.P.  Braunstein, M. Eguaras, M.J.  (2012). Genetic variation and widespread dispersal of Nosema ceranae in Apis mellifera apiaries from Argentina. Parasitology research 110: 859-864.
Menaker, J.  Stein, D.M. Scalea, T.M.  (2007). Incidence of early pulmonary embolism after injury. J Trauma 63: 620-624.
Modirrousta, H.  Moharrami, M. Mansouri, M.A.  (2014). Retrospective study of the Nosema ceranae infection of honey bee colonies in Iran (2004-2013). Archives of Razi Institute 69: 197-200.
Moeller, F.E.  (1962). Nosema disease control in package bees. American Bee Journal 102: 390-392.
Mohammadian, B.  (2017). Investigation of Prevalence and some effective factors of Colony Collapse Disorder in Apiaries of Iran. Tehran University, Tehran, Iran.
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: 25-30.
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. Iran. J. Parasitol. 6: 89.
Nixon, M.  (1982). Preliminary world maps of honeybee diseases and parasites. Bee world 63: 23-42.
OIE  (2013). Nosemosis of Honey Bees, In:   OIE Terrestrial Manual.
Pajuelo, A.G.  Torres, C. Bermejo, F.J.O.  (2008). Colony losses: a double blind trial on the influence of supplementary protein nutrition and preventative treatment with fumagillin against Nosema ceranae. J Apic Res 47: 84–86.
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: 558-565.
Razmaraii, N. Karimi, H.  (2010). A survey of Nosema disease of honey bee (Apis mellifera) in East Azarbaijan province of Iran. J. Anim. Vet. Adv. 9: 879-882.
Razmaraii, N.  Sadegh-Eteghad, S.  Babaei, H.  Paykari, H.  Esmaeilnia, K. Froghy, L.  (2013). Molecular Identification of Nosema species in EastAzerbaijan province, Iran. Archives of Razi Institute 68: 23-27.
Runckel, C.  Flenniken, M.L.  Engel, J.C.  Ruby, J.G.  Ganem, D.  Andino, R. DeRisi, J.L.  (2011). Temporal analysis of the honey bee microbiome reveals four novel viruses and seasonal prevalence of known viruses, Nosema, and Crithidia. PloS one 6: e20656.
Stevanovic, J.  Stanimirovic, Z.  Genersch, E.  Kovacevic, S.R.  Ljubenkovic, J.  Radakovic, M. Aleksic, N.  (2010). Dominance of Nosema ceranae in honey bees in the Balkan countries in the absence of symptoms of colony collapse disorder. Apidologie.
Wang, D.-I. Moeller, F.E.  (1970). The division of labor and queen attendance behavior of nosema-infected worker honey bees. Journal of Economic Entomology 63: 1539-1541.
Zander, E.  (1909). Tierische parasiten als krankenheitserreger bei der biene. Münchener Bienenzeitung 31: 196-204.
Honeybee Science Journal
Volume 09, Issue 16
September 2018
Pages 2-11

Files

Share

How to cite

Statistics