A comparative study of the frequency and intensity of nosemosis based on individual and composite samples of live bees in the apiaries of the cities of East Azerbaijan province
Subject Areas :
Veterinary Clinical Pathology
Abbas Imani Baran
1
,
Gholamreza Hamidian
2
1 - Associate Professor, Department of Pathobiology, Faculty of Veterinary Medicine, University of Tabriz, Tabriz, Iran.
2 - Associate Professor, Department of Basic Sciences, Faculty of Veterinary Medicine, University of Tabriz, Tabriz, Iran.
Received: 2022-09-10
Accepted : 2022-12-20
Published : 2022-11-22
Keywords:
Intensity,
frequency,
Nosemosis,
Individual sampling,
Composite sampling,
Abstract :
Due to the lack of an international standard method to determine the frequency, prevalence and intensity of nosemosis, the researchers are still using individual or composite sampling methods. This study was aimed to compare the frequency and intensity of nosemosis based on the above mentioned methods in the apiaries of East Azerbaijan province. To this end, 5 apiaries from 5 cities of East Azerbaijan province were randomly selected. Three hives from each apiary and 10 bees from each hive (equally from inside and outside) were sampled. To determine the frequency, the spore presence in the samples was evaluated. To determine the intensity, the spore count in one bee was calculated in the individual samples and mean spore count per bee in the composite samples. In both methods, 100% frequency was obtained for all samples. To compare infection intensity in both sampling methods, one-way analysis of variance and Tukey's post hoc test were used. To compare the results of two methods, generally, and also in each city, separately, independent T-test was used. In both methods, the highest intensity was related to samples from Tabriz (p<0.05). However, in the individual sampling method, the infection intensity in Osku samples was significantly lower (p<0.001). Also, in comparison of the two sampling methods, there was generally no statistical difference between the sampling methods and even in one city (p>0.05). In individual samples, overall, the intensity was higher in bees outside of the hive. Based on the average results, the intensity of nosemosis in composite samples was much higher than individual samples.
References:
Anzabi, Y. and Shaghaghi, S. (2015). In vitro evaluation of antibacterial properties of propolis alcoholic extract on bovine mastitis isolates. Veterinary Clinical Pathology, 9(34): 117-129. [In Persian]
Bailey, L. (1954). The control of nosema disease. Bee World, 35(6): 111-113.
Bailey, L. (1955). The epidemiology and control of nosema disease of the honey bee. Annals of Applied Biology, 43(1-2): 379-389.
Bailey, L. (1959). The natural mechanism of suppression of Nosema apis in enzootically infected colonies of the honey bee, Apis mellifera Linnaeus. Journal of Insect Pathology, 1(4): 347-350.
Botías, C., Martín-Hernández, R., Barrios, L., Meana, A. and Higes, M. (2013). Nosema spp. infection and its negative effects on honey bees (Apis mellifera iberiensis) at the colony level. Veterinary Research, 44(25):1-14.
Cantwell, G.E. (1970). Standard methods for counting Nosema spores. American Bee Journal, 110: 222-223.
Chauzat, M.P., Higes, M., Martín-Hernández, R., Meana, A., Cougoule, N. and Faucon, J.P. (2007). Presence of Nosema ceranae in French honey bee colonies. Journal of Apicultural Research, 46(2): 127-128.
Chen, Y., Evans, J.D., Zhou, L. and Boncristiani, H. (2009). Asymmetrical coexistence of Nosema ceranae and Nosema apis in honey bees. Journal of Invertebrate Pathology, 101(3): 204-209.
Choobkar, N., Sari, A., Bolandnazar, A.R., Heshmati, H., Mohammadi, F., Shahbazian, N., et al. (2014). The effect of different concentrations of bee propolis on skin wound healing and immune response and survival of Common carp (Cyprinus carpio). Journal of Veterinary Clinical Pathology, 7(28): 300-312. [In Persian]
Cilia, G., Sagona, S., Giusti, M., dos Santos, P.E.J., Nanetti, A. and Felicioli, A. (2019). Nosema ceranae infection in honeybee samples from Tuscanian Archipelago (Central Italy) investigated by two qPCR methods. Saudi Journal of Biology Sciences, 26(7): 1553-1556.
Copley, T.R., Giovenazzo, P. and Jabaji, S.H. (2012). Detection of Nosema apis and ceranae in honeybee bottom scraps and frass in naturally infected hives. Apidologie, 43: 753-760.
Doull, K.M. (1965). The effects of time of day and method of sampling on the determination of nosema disease in beehives. Journal of Invertebrate Pathology, 7(1): 1-4.
Doull, K.M. and Eckert, J.E. (1962). A survey of the incidence of Nosema disease in California. Journal of Economic Entomology, 55(3): 313-317.
Doull, K.M. and Cellier, K.M. (1961) A survey of the incidence of Nosema disease (Nosema apis Zander) in honey bees in South Australia. Journal of Insect Pathology 3(3): 280-288.
Emsen, B., Guzman-Novoa, E., Hamiduzzaman, M.M., Eccles, L., Lacey, B., Ruiz-Pérez, R.A., et al (2016). Higher prevalence and levels of Nosema ceranae than Nosema apis infections in Canadian honey bee colonies. Parasitology Research, 115(1): 175-181.
Fries, I. (2010). Nosema ceranae in European honey bees (Apis mellifera). Journal of Invertebrate Pathology, 103: 73-79.
Fries, I., Chauzat, M.P., Chen, Y.P., Doublet, V., Genersch, E., Gisder, S., et al. (2013). Standard methods for Nosema research. Journal of Apicultural Research, 52(1):1-28.
Fries, I., Ekbohm, G. and Villumstad, E. (1984). Nosema apis, sampling techniques and honey yield. Journal of Apicultural Research, 23(2): 102-105.
Gisder, S., Hedtke, K., Mockel, N., Frielitz, M.C., Linde, A. and Genersch, E. (2010). Five-Year cohort study of Nosema spp. in Germany: Does climate shape virulence and assertiveness of Nosema ceranae? Applied Environmental Microbiology, 76(9): 3032-3038.
Gochnauer, T.A. and Fumidil, B. (1957). Nosema control in wintering colonies. Glean. Bee Culture, 85: 528-529.
Hamiduzzaman, M.M., Guzmán-Novoa, E. and Goodwin, P.H. (2010). A multiplex PCR assay to diagnose and quantify Nosema infections in honey bees (Apis mellifera). Journal of Invertebrate Patholology, 105(2): 151-155.
Higes, M., García-Palenci, P., Martín-Hernández, R. and Meana, A. (2007). Experimental infection of Apis mellifera honey bees with the microsporidia Nosema ceranae. Journal of Invertebrate Pathology, 94(3): 211-217.
Higes, M., Martín-Hernández, R., Botías, C., Bailón, E.G., González-Porto, A.V., Barrios, L., et al. (2008). How natural infection by Nosema ceranae causes honeybee colony collapse. Environmental Microbiology, 10(1): 2659-2669.
Higes, M., Martín-Hernández, R. and Meana, A. (2010). Nosema ceranae in Europe: an emergent type C nosemosis. Apidologie, 41(3): 375-392.
Langridge, D.F. (1961). Nosema disease of the honeybee and some investigations into its control in Victoria, Australia. Bee World, 42(2): 36-40.
L'Arrivee, J.C.M. (1963). Comparison of composite versus individual bee sampling for Nosema apis Journal of Insect Pathology, 5(4): 349-355.
Meana, A., Martín-Hernández, R. and Higes, M. (2010). The reliability of spore counts to diagnose Nosema ceranae infections in honey bees. Journal of Apicultural Research, 49(2): 212-214.
Mulholland, G.E., Traver, B.E., Johnson, N.G. and Fell, R.D. (2012). Individual variability of Nosema ceranae infections in Apis mellifera colonies. Insects, 3(4): 1143-1155.
Ostroverkhova, N.V., Konusova, O.L., Kucher, A.N., Kireeva, T.N. and Rosseykina, S.A. (2020). Prevalence of the microsporidian Nosema spp. in honey bee populations (Apis mellifera) in some ecological regions of north Asia. Veterinary Sciences, 7(3): 111.
Özkırım, A., Schiesser, A. and Keskin, N. (2019). Dynamics of Nosema apis and Nosema ceranae co-infection seasonally in honey bee (Apis mellifera) colonies. Journal of Apicultral Sciences, 63(1): 41-48.
Papini, R., Mancianti, F., Canovai, R., Cosci, F., Rocchigiani, G., Benelli, G., et al. (2017). Prevalence of the microsporidian Nosema ceranae in honeybee (Apis mellifera) apiaries in central Italy. Saudi Journal of Biolology Sciences, 24(5): 979-982.
Paxton, R.J., Klee, J. and Korpela, S. (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.
Pickard, R.S. and El-Shemy, A.A.M. (1989). Seasonal variation in the infection of honeybee colonies with Nosema apis Journal of Apicultural Research, 28(2): 93-100.
Porrini, L.P., Porrini, M.P., Garrido, M.P., Müller, F., Arrascaeta, L., Iriarte, P.J.F., et al. (2020). Infectivity and virulence of Nosema ceranae (Microsporidia) isolates obtained from various Apis mellifera Entomologia Experimentalis et Applicata, 168(4): 286-294.
Sharma, D., Katna, S., Sharma, R., Rana, B.S., Sharma, H.K., Bhardwaj, V., et al. (2019). First detection of Nosema ceranae infecting Apis mellifera in India. Journal of Apicultral Sciences, 63(1):165-170.
Smart, M.D. and Sheppard, W.S. (2012). Nosema ceranae in age cohorts of the western honey bee (Apis mellifera). Journal of Invertebrate Pathology, 109(1): 148-151.
Teixeira, E.W., dos Santos, L.G., Sattler, A., Message, D., Alves, M., Martins, M.F., et al. (2013). Nosema ceranae has been present in Brazil for more than three decades infecting Africanized honey bees. Journal of Invertebrate Pathology, 114(3): 250-254.
Traver, B.E. and Fell, R.D. (2011). Prevalence and infection intensity of Nosema in honey bee (Apis mellifera) colonies in Virginia. Journal of Invertebrate Pathology, 107(1): 43-49.
Traver, B.E., Williams, M.R. and Fell, R.D. (2012). Comparison of within hive sampling and seasonal activity of Nosema ceranae in honey bee colonies. Journal of Invertebrate Pathology, 109(2): 187-193.
Wang, Q., Dai, P., Guzmán-Novoa, E., Wu, Y., Hou, C. and Diao, Q. (2019). Nosema ceranae, the most common microsporidium infecting Apis mellifera in the main beekeeping regions of China since at least 2005. Journal of Apicultural Research, 58(4): 562-566.
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Anzabi, Y. and Shaghaghi, S. (2015). In vitro evaluation of antibacterial properties of propolis alcoholic extract on bovine mastitis isolates. Veterinary Clinical Pathology, 9(34): 117-129. [In Persian]
Bailey, L. (1954). The control of nosema disease. Bee World, 35(6): 111-113.
Bailey, L. (1955). The epidemiology and control of nosema disease of the honey bee. Annals of Applied Biology, 43(1-2): 379-389.
Bailey, L. (1959). The natural mechanism of suppression of Nosema apis in enzootically infected colonies of the honey bee, Apis mellifera Linnaeus. Journal of Insect Pathology, 1(4): 347-350.
Botías, C., Martín-Hernández, R., Barrios, L., Meana, A. and Higes, M. (2013). Nosema spp. infection and its negative effects on honey bees (Apis mellifera iberiensis) at the colony level. Veterinary Research, 44(25):1-14.
Cantwell, G.E. (1970). Standard methods for counting Nosema spores. American Bee Journal, 110: 222-223.
Chauzat, M.P., Higes, M., Martín-Hernández, R., Meana, A., Cougoule, N. and Faucon, J.P. (2007). Presence of Nosema ceranae in French honey bee colonies. Journal of Apicultural Research, 46(2): 127-128.
Chen, Y., Evans, J.D., Zhou, L. and Boncristiani, H. (2009). Asymmetrical coexistence of Nosema ceranae and Nosema apis in honey bees. Journal of Invertebrate Pathology, 101(3): 204-209.
Choobkar, N., Sari, A., Bolandnazar, A.R., Heshmati, H., Mohammadi, F., Shahbazian, N., et al. (2014). The effect of different concentrations of bee propolis on skin wound healing and immune response and survival of Common carp (Cyprinus carpio). Journal of Veterinary Clinical Pathology, 7(28): 300-312. [In Persian]
Cilia, G., Sagona, S., Giusti, M., dos Santos, P.E.J., Nanetti, A. and Felicioli, A. (2019). Nosema ceranae infection in honeybee samples from Tuscanian Archipelago (Central Italy) investigated by two qPCR methods. Saudi Journal of Biology Sciences, 26(7): 1553-1556.
Copley, T.R., Giovenazzo, P. and Jabaji, S.H. (2012). Detection of Nosema apis and ceranae in honeybee bottom scraps and frass in naturally infected hives. Apidologie, 43: 753-760.
Doull, K.M. (1965). The effects of time of day and method of sampling on the determination of nosema disease in beehives. Journal of Invertebrate Pathology, 7(1): 1-4.
Doull, K.M. and Eckert, J.E. (1962). A survey of the incidence of Nosema disease in California. Journal of Economic Entomology, 55(3): 313-317.
Doull, K.M. and Cellier, K.M. (1961) A survey of the incidence of Nosema disease (Nosema apis Zander) in honey bees in South Australia. Journal of Insect Pathology 3(3): 280-288.
Emsen, B., Guzman-Novoa, E., Hamiduzzaman, M.M., Eccles, L., Lacey, B., Ruiz-Pérez, R.A., et al (2016). Higher prevalence and levels of Nosema ceranae than Nosema apis infections in Canadian honey bee colonies. Parasitology Research, 115(1): 175-181.
Fries, I. (2010). Nosema ceranae in European honey bees (Apis mellifera). Journal of Invertebrate Pathology, 103: 73-79.
Fries, I., Chauzat, M.P., Chen, Y.P., Doublet, V., Genersch, E., Gisder, S., et al. (2013). Standard methods for Nosema research. Journal of Apicultural Research, 52(1):1-28.
Fries, I., Ekbohm, G. and Villumstad, E. (1984). Nosema apis, sampling techniques and honey yield. Journal of Apicultural Research, 23(2): 102-105.
Gisder, S., Hedtke, K., Mockel, N., Frielitz, M.C., Linde, A. and Genersch, E. (2010). Five-Year cohort study of Nosema spp. in Germany: Does climate shape virulence and assertiveness of Nosema ceranae? Applied Environmental Microbiology, 76(9): 3032-3038.
Gochnauer, T.A. and Fumidil, B. (1957). Nosema control in wintering colonies. Glean. Bee Culture, 85: 528-529.
Hamiduzzaman, M.M., Guzmán-Novoa, E. and Goodwin, P.H. (2010). A multiplex PCR assay to diagnose and quantify Nosema infections in honey bees (Apis mellifera). Journal of Invertebrate Patholology, 105(2): 151-155.
Higes, M., García-Palenci, P., Martín-Hernández, R. and Meana, A. (2007). Experimental infection of Apis mellifera honey bees with the microsporidia Nosema ceranae. Journal of Invertebrate Pathology, 94(3): 211-217.
Higes, M., Martín-Hernández, R., Botías, C., Bailón, E.G., González-Porto, A.V., Barrios, L., et al. (2008). How natural infection by Nosema ceranae causes honeybee colony collapse. Environmental Microbiology, 10(1): 2659-2669.
Higes, M., Martín-Hernández, R. and Meana, A. (2010). Nosema ceranae in Europe: an emergent type C nosemosis. Apidologie, 41(3): 375-392.
Langridge, D.F. (1961). Nosema disease of the honeybee and some investigations into its control in Victoria, Australia. Bee World, 42(2): 36-40.
L'Arrivee, J.C.M. (1963). Comparison of composite versus individual bee sampling for Nosema apis Journal of Insect Pathology, 5(4): 349-355.
Meana, A., Martín-Hernández, R. and Higes, M. (2010). The reliability of spore counts to diagnose Nosema ceranae infections in honey bees. Journal of Apicultural Research, 49(2): 212-214.
Mulholland, G.E., Traver, B.E., Johnson, N.G. and Fell, R.D. (2012). Individual variability of Nosema ceranae infections in Apis mellifera colonies. Insects, 3(4): 1143-1155.
Ostroverkhova, N.V., Konusova, O.L., Kucher, A.N., Kireeva, T.N. and Rosseykina, S.A. (2020). Prevalence of the microsporidian Nosema spp. in honey bee populations (Apis mellifera) in some ecological regions of north Asia. Veterinary Sciences, 7(3): 111.
Özkırım, A., Schiesser, A. and Keskin, N. (2019). Dynamics of Nosema apis and Nosema ceranae co-infection seasonally in honey bee (Apis mellifera) colonies. Journal of Apicultral Sciences, 63(1): 41-48.
Papini, R., Mancianti, F., Canovai, R., Cosci, F., Rocchigiani, G., Benelli, G., et al. (2017). Prevalence of the microsporidian Nosema ceranae in honeybee (Apis mellifera) apiaries in central Italy. Saudi Journal of Biolology Sciences, 24(5): 979-982.
Paxton, R.J., Klee, J. and Korpela, S. (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.
Pickard, R.S. and El-Shemy, A.A.M. (1989). Seasonal variation in the infection of honeybee colonies with Nosema apis Journal of Apicultural Research, 28(2): 93-100.
Porrini, L.P., Porrini, M.P., Garrido, M.P., Müller, F., Arrascaeta, L., Iriarte, P.J.F., et al. (2020). Infectivity and virulence of Nosema ceranae (Microsporidia) isolates obtained from various Apis mellifera Entomologia Experimentalis et Applicata, 168(4): 286-294.
Sharma, D., Katna, S., Sharma, R., Rana, B.S., Sharma, H.K., Bhardwaj, V., et al. (2019). First detection of Nosema ceranae infecting Apis mellifera in India. Journal of Apicultral Sciences, 63(1):165-170.
Smart, M.D. and Sheppard, W.S. (2012). Nosema ceranae in age cohorts of the western honey bee (Apis mellifera). Journal of Invertebrate Pathology, 109(1): 148-151.
Teixeira, E.W., dos Santos, L.G., Sattler, A., Message, D., Alves, M., Martins, M.F., et al. (2013). Nosema ceranae has been present in Brazil for more than three decades infecting Africanized honey bees. Journal of Invertebrate Pathology, 114(3): 250-254.
Traver, B.E. and Fell, R.D. (2011). Prevalence and infection intensity of Nosema in honey bee (Apis mellifera) colonies in Virginia. Journal of Invertebrate Pathology, 107(1): 43-49.
Traver, B.E., Williams, M.R. and Fell, R.D. (2012). Comparison of within hive sampling and seasonal activity of Nosema ceranae in honey bee colonies. Journal of Invertebrate Pathology, 109(2): 187-193.
Wang, Q., Dai, P., Guzmán-Novoa, E., Wu, Y., Hou, C. and Diao, Q. (2019). Nosema ceranae, the most common microsporidium infecting Apis mellifera in the main beekeeping regions of China since at least 2005. Journal of Apicultural Research, 58(4): 562-566.
