Identification of the Nosema spp., a microsporidian parasite isolated from the honey bees (Apis mellifera) and its association with honey bee colony losses in apiaries of Iran

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Published: Apr 29, 2022
DOI: https://doi.org/10.12681/jhvms.25393
Keywords:
Colony Collapse Disorder Honeybee Nosema cerenae Iran
Sahar Moeini
Farnaz Malekifard
Assistant Professor
https://orcid.org/0000-0002-4809-3782
Mousa Tavassoli
Professor
Abstract
The aim of this study was to determine the Nosema species by microscopic and molecular method and its association with honeybee colony losses (Colony Collapse Disorder) in apiaries of Urmia, Northwest of Iran. For this purpose, honeybee samples were collected from 840 colonies kept in 120 apiaries in five different location of Urmia. The specimens were examined for the presence of Nosema spores. After DNA isolation, the 16S rRNA gene was evaluated using multiplex PCR. Total infection prevalence with the microscopic evaluation was 32% while in PCR test was 58.2%. Nosema positive samples were evaluated by PCR sequencing. Based on the results of PCR, all identified cases were N. ceranae. The obtained sequences were transferred to GenBank/NCBI (samples accession numbers MT001887 and MT001893). The results showed the prevalence of Colony Collapse Disorder like symptoms in the studied honeybee colonies were 13.33%. N. ceranae was detected by PCR in 20.28 % of honeybee colonies with Colony Collapse Disorder like signs. Our findings showed that there was a significant relation between Colony Collapse Disorder and presence of N. ceranae. The results of this study concluded that N. ceranae is the only specie that affects the honeybees which may have an important role in the occurrence of collapse of bee families and depopulation of hives in this area.
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References
Antúnez K, Martín‐Hernández R, Prieto L, Meana A, Zunino P, Higes M (2009) Immune suppression in the honey bee (Apis mellifera) following infection by Nosema ceranae (Microsporidia). Environmental Microbiology 11(9): 2284–2290.
Aroee F, Azizi H, Shiran B, Kheirabadi KP (2017): Molecular identification of Nosema species in provinces of Fars, Chaharmahal and Bakhtiari and Isfahan (Southwestern Iran). Asian Pacific Journal of Tropical Biomedicine 7(1): 10–13.
Bailey L, Ball BV (1997): Honey Bee Pathology. 3rd ed. Academic Press, London, 59–76.
Chaimanee V, Warrit N, Chantawannakul P (2010): Infections of Nosema ceranae in four different honeybee species. Journal of Invertebrate Pathology 105(2): 207–210.
Chauzat M, Higes M, Martín-Hernández R, Meana A, Cougoule N, Faucon J (2007) Presence of Nosema ceranae in French honey bee colonies. Journal of Apicultural Research 46(2): 127.
Chen Y, Evans JD, Smith IB, Pettis JS (2008) Nosema ceranae is a long-present and wide-spread microsporidian infection of the European honey bee (Apis mellifera) in the United States. Journal of Invertebrate Pathology 97(2): 186–188.
Chen YP, Evans JD, Murphy C, Gutell R, Zuker M, Gundensen‐Rindal D, Pettis JS (2009): Morphological, Molecular, and Phylogenetic Characterization of Nosema ceranae, a Microsporidian Parasite Isolated from the European Honey Bee, Apis mellifera 1. Journal of Eukaryotic Microbiology 56(2): 142–147.
CoxFoster DL, Conlan S, Holmes EC, Palacios G, Evans JD, Moran NA, Quan P-L, Briese T, Hornig M, Geiser DM (2007): A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318(5848): 283–287.
Emsen B, Guzman-Novoa E, Hamiduzzaman M.M, Eccles L, Lacey B, Ruiz-Pérez R.A, Nasr M (2016) Higher prevalence and levels of Nosema ceranae than Nosema apis infections in Canadian honey bee colonies. Parasitology Research 115 :175–181.
Fries I, Martin R, Meana A, Garcia-Palencia P, Higes M (2006) Natural infections of Nosema ceranae in European honey bees. Journal of Apicultural Research 45(4): 230–233.
Fries I, Feng F, da Silva A, Slemenda SB, Pieniazek NJ (1996) Nosema ceranae n. sp.(Microspora, Nosematidae), morphological and molecular characterization of a microsporidian parasite of the Asian honey bee Apis cerana (Hymenoptera, Apidae). European Journal of Protistology 32(3): 356–365.
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.
Higes M, Martín‐Hernández R, Botías C, Bailón EG, González‐Porto AV, Barrios L, Del Nozal MJ, Bernal JL, Jiménez JJ, Palencia PG (2008) How natural infection by Nosema ceranae causes honeybee colony collapse. Environmental Microbiology Reports 10(10): 2659–2669.
Higes M, Martín‐Hernández R, Garrido‐Bailón E, González‐Porto AV, García‐Palencia P, Meana A, Del Nozal MJ, Mayo R, Bernal JL (2009) Honeybee colony collapse due to Nosema ceranae in professional apiaries. Environmental Microbiology Reports 1(2): 110–113.
Higes M, Martín R, Meana A (2006) Nosema ceranae, a new microsporidian parasite in honeybees in Europe. Journal of Invertebrate Pathology 92(2): 93–95.
Hornitzky M (2008) Nosema disease. Literature Review and Three Year Survey of Beekeepers. Part, 2. Rural Industries Research and Development Corporation 8(006):3507-3516.
Huang WF, Jiang JH, Chen YW, Wang CH (2007) A Nosema ceranae isolate from the honeybee Apis mellifera. Apidologie 38(1): 30–37.
Invernizzi C, Abud C, Tomasco IH, Harriet J, Ramallo G, Campá J, Katz H, Gardiol G, Mendoza Y (2009) Presence of Nosema ceranae in honeybees (Apis mellifera) in Uruguay. Journal of Invertebrate Pathology 101(2): 150–153.
Klee J, Besana AM, Genersch E, Gisder S, Nanetti A, Tam DQ, Chinh TX, Puerta F, Ruz JM, Kryger P (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.
Lotfi A, 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, Prieto L, Salvador AM, Garrido-Bailón E, Higes M (2007) Outcome of colonization of Apis mellifera by Nosema ceranae. Applied and environmental microbiology 73(20): 6331–6338.
Matheson A (1996) World bee health update 1996. Bee World 77(1): 45–51.
Mohammadian B, Bokaie S, Moharrami M, Nabian S, Forsi M (2019) Prevalence of Honeybee Colony Collapse Disorder and its Relation to Nosema Spp. and Climate in Apiaries of Iran. Journal of Veterinary Research 74(1): 11–18.
Nabian S, Ahmadi K, Shirazi MHN, Sadeghian AG (2011) First detection of Nosema ceranae, a microsporidian protozoa of European honeybees (Apis mellifera) in Iran. Iranian Journal of Parasitology 6(3): 89.
OIE (2008) Manual of Diagnostic Tests and Vaccines for Terrestrial Animals, Chap. 2.2.4., Nosemosis of Honey Bees, http://www.oie.int/fr/normes/ mmanual/2008/pdf/2.02.04_NOSEMOSIS.pdf.
Paxton RJ (2010) Does infection by Nosema ceranae cause “Colony Collapse Disorder” in honey bees (Apis mellifera)? Journal of Apicultural Research 49(1): 80–84.
Paxton RJ, 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(6): 558–565.
Razmaraii N, Karimi H (2010) A Survey of Nosema of Honey Bees (Apis mellifera) in East Azerbaijan Province of Iran. Journal of Animal and Veterinary Advances 9(5): 879–882.
Razmaraii N, Sadegh ES, Babaei H, Paykari H, Esmaeilnia K, Froghy L (2013) Molecular identification of Nosema species in East-Azerbaijan province, Iran. Archives of Razi Institute 68(1): 23-27.
Tavassoli M, Eiganinejad S, Alizadeh-Asl S (2009) A survey on Nosema apis infection in apiaries of Urmia, North-West of Iran. Iranian Journal of Veterinary Science and Technology 1(1): 35–40.
Teixeira E.W, Santos L.G, Sattler A, Message, D, Alves M.L, Martins M.F, Grassi Sella M.L, Francoy T.M (2013) Nosema ceranae has been present in Brazil for more than three decades infecting Africanized honey bees. Journal of Invertebrate Pathology 114 :250–254.
TUNCA RI, Oskay D, Gosterit A, Tekin OK (2016) Does Nosema ceranae Wipe Out Nosema apis in Turkey? Iranian Journal of Parasitology 11(2): 259.
Whitaker J, Szalanski AL, Kence M (2011) Molecular detection of Nosema ceranae and N. apis from Turkish honey bees. Apidologie 42(2): 174–180.
Williams GR, Shafer ABA, Rogers REL, Shutler D, Stewart DT (2008) First detection of Nosema ceranae, a microsporidian parasite of European honey bees (Apis mellifera), in Canada and central USA. Journal of Invertebrate Pathology 97(2): 189–192.
Yakhchali M, Hosseine A (2006) Prevalence and ectoparasites fauna of sheep and goats flocks in Urmia suburb, Iran. Veterinarski Arhiv 76(5): 431–442.