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Beekeeping practice-related factors that impact nosemosis prevalence in honey bees in the Republic of Tatarstan, Russia

Yıl 2025, Cilt: 72 Sayı: 3, 365 - 376, 01.07.2025

Nikolai Shamaev , Eduard Shuralev Oleg Nikitin Malik Mukminov

https://doi.org/10.33988/auvfd.1594759

Öz

To ensure pollination services for agriculture and implement effective management strategies to protect honey bee populations, it is necessary to understand the prevalence of pathogens and pests and the factors that impact their occurrence. The aim of this study is to investigate potential links of nosemosis prevalence in the Republic of Tatarstan, Russia. Multivariate logistic regression was used to evaluate the following factors as potential risk factors for Nosema apis and N. ceranae PCR positivity: district, wintering type, honey bee breed, hive material, varroosis, ascosferosis or nosemosis observed in the previous year, colony strength, feeding in winter, and amitraz, fluvalinate, or thymol usage. Our results show that only the variable counting for thymol usage fits the data well, where the actual observed prevalence of N. ceranae infection is significantly higher in honey bee populations that use thymol compared to those that do not. Honey bee populations with thymol usage in the current study with decreased, but not eliminated, N. ceranae infection, possibly faced preventive, uncontrolled, and excessive use of miticide in beekeeping practice.

Anahtar Kelimeler

Apis mellifera multinomial logistic regression Nosema spp nosemosis thymol usage

Kaynakça

  • Aguila RD, Gonzalez Ramirez AR (2014): Sample size calculation. Allergol Immunopathol (Madr), 42, 485–492.
  • Altman DG, Bland JM (2011): Statistics notes: How to obtain the P value from a confidence interval. BMJ, 343,7825.
  • Bhusal S, Thapa R (2006): Response of colony strength to honey production: regression and correlation analysis. J Inst Agric Anim, 27, 133–137.
  • Borges D, Guzman-Novoa E, Goodwin PH (2020): Control of the microsporidian parasite Nosema ceranae in honey bees (Apis mellifera) using nutraceutical and immuno-stimulatory compounds. PLOS ONE, 15, e0227484.
  • Botias C, Martín-Hernández R, Barrios L, et al (2013): Nosema spp. infection and its negative effects on honey bees (Apis mellifera iberiensis) at the colony level. Vet Res, 44, 1-15.
  • Bourgeois АL, Rinderer TE, Sylvester HA, et al (2012): Patterns of Apis mellifera infestation by Nosema ceranae support the parasite hypothesis for the evolution of extreme polyandry in eusocial insects. Apidologie, 43, 539-548.
  • Brandorf AZ, Shestakova AI, Larkina EO, et al (2023): Effect of acaricide treatment on body weight and reproductive characteristics of drones of the Prioksky breed type of Central Russian honeybees (Apis mellifera Linnaeus, 1758). Sel’skokhozyaistvennaya Biol, 58, 345–354.
  • Chaimanee V, Warrit N, Chantawannakul P (2010): Infections of Nosema ceranae in four different honeybee species. J Invertebr Pathol, 105, 207–210.
  • Claing G, Dubreuil P, Bernier M, et al (2024): Prevalence of pathogens in honey bee colonies and association with clinical signs in southwestern Quebec, Canada. Can J Vet Res, 88, 45–54.
  • Costello A B, Osborne J (2005): Best practices in exploratory factor analysis: four recommendations for getting the most from your analysis. Pract Assess Res Eval, 10, 7.
  • Cox-Foster DL, Conlan S, Holmes EC, et al (2007): A metagenomic survey of microbes in honey bee colony collapse disorder. Science, 318, 283–287.
  • D’Alvise P, Böhme F, Codrea MC, et al (2018): The impact of winter feed type on intestinal microbiota and parasites in honey bees. Apidologie, 49, 252–264.
  • Fontbonne R, Garnery L, Vidau C, et al (2013): Comparative susceptibility of three Western honeybee taxa to the microsporidian parasite Nosema ceranae. Infect Gen Evol, 17, 188–194.
  • Formato G, Rivera-Gomis J, Bubnic J, et al (2022): Nosemosis prevention and control. Appl Sci, 12, 783.
  • Galiullina AV, Nizamov RN, Vagin KN, et al (2017): Accumulation and redistribution of radionuclides in honey bees and apiary products in the Republic of Tatarstan, Russia. Astra Salvensis, 2017, 581–590.
  • Glavinic U, Blagojevic J, Ristanic M, et al (2022): Use of thymol in Nosema ceranae control and health improvement of infected honey bees. Insects, 13, 574.
  • Glavinic U, Rajkovic M, Ristanic M, et al (2023): Genotoxic potential of thymol on honey bee DNA in the Comet Assay. Insects, 14, 451.
  • Goblirsch M (2018): Nosema ceranae disease of the honey bee (Apis mellifera). Apidologie. 49, 131-150.
  • Gunes N, Aydın L, Belenli D, et al (2017): Stress responses of honey bees to organic acid and essential oil treatments against varroa mites. J Apic Res, 56, 175–181.
  • Haritonov NN (2006): Selekciya ustojchivyhk zabolevaniyam linij pchel. Pchelovodstvo, 7, 14–16.
  • Hasbieva DR, Kambale EM, Ndayishimiye EW, et al (2025): Nosemosis in Rwandan mining areas. 272–278. In: Proceedings of the International Scientific and Practical Conference. Rybnoye, Russia. (in Russ.).
  • Hillier NK, Frost EH, Shutler D (2013): Fate of dermally applied miticides fluvalinate and amitraz within honey bee (Hymenoptera: Apidae) bodies. J Econ Entomol, 106, 558–565.
  • Ilyasov RA, Gajfullina LR, Saltykova ES, et al (2014): Biology, distribution and prevention of microsporidians of Nosema genus, parasites of honey bees. Biomika, 6, 145–154 (in Russ.).
  • Ilyasov RA, Shareeva ZV (2014): Effect of fluvalinate and amitraz on bee colonies. Beekeeping, 6, 24–26. (in Russ.).
  • Kashkovskii VG, Plakhova AA, Kropachev DV (2019): Features of the development of beekeeping in the Narym region of Russia. Adv Anim Vet Sci, 7, 50–59.
  • Kaskinova M, Saltykova E, Poskryakov A, et al (2021): The current state of the protected Apis mellifera mellifera population in Russia: hybridization and Nosematosis. Animals, 11, 2892.
  • Ministry of Agriculture and Food of the Republic of Tatarstan (2022): Beekeeping registry. Available at https://agro.tatarstan.ru/reestr-po-pchelovodstvu-4701889.htm. (Accessed March 2, 2024).
  • Mukminov MN, Shuralev EA, Kazaryan GG, et al (2023): Microsporidia associated with infections of honey bees. 113–118. In: Proceedings of the International Scientific and Practical Conference. Rybnoye, Russia. (in Russ.).
  • Ostroverhova NV, Konusova OL, Pogorelov Yu L (2015): Morphometric and molecular-genetic characteristics of bee colonies of Tomsk region infected with nosemosis. In: Materials of the Regional Scientific-Practical Conference. Krasnoyarsk, Russia. (in Russ.).
  • Owen R (2017): Role of human action in the spread of honey bee (Hymenoptera: Apidae) pathogens. J Econ Entomol, 110, 797–801.
  • Petuhov AV, Popov AS, Kazakova AN (2014): Resistance to nosemosis in bees of different species. In: Proceedings of International Scientific-Practical Conference. Kirov, Russia. (in Russ.).
  • Punko RN, Currie RW, Nasr ME, et al (2021): Epidemiology of Nosema spp. and the effect of indoor and outdoor wintering on honey bee colony population and survival in the Canadian Prairies. PLOS ONE, 16, e0258801.
  • Shamaev ND (2024): Background to the existence of variation in the innate immune response in Galleria mellonella. Agrarian Bull of Urals, 24, 1492‒1501. (In Russ.).
  • Shamaev ND, Batanova T, Iwatake Yu, et al (2024): Diversity of genes encoding immune-related GTPase B2 protein, an inherited element responsible for resistance against virulent Toxoplasma gondii strains, among wild Mus musculus in local area of Japan. J Vet Med Sci, 86, 1056–1062.
  • Shamaev ND, Kambale EM, Valiakhmetov DI, et al (2024): Biodiversity of Nosema ceranae genovars in the Apis mellifera population with hybrid traits under apiary conditions. Prob Vet San Hyg Ecol, 4, 597–605. (in Russ.).
  • Shamaev ND, Potapov KO, Mukminov MN, et al (2025): Ganoderma applanatum extract biopesticidal properties evaluation against greater wax moth Galleria mellonella. Vet Med, 5, 55–59. (In Russ.).
  • Shamaev ND, Salnikov VV, Yuzmanova LA, et al (2024): Regular occurrence of atypically small spores in Apis mellifera carnica (Hymenoptera: Apidae), naturally infected with Nosema spp. (Microsporidia). Inverteb Zool, 21, 478–486.
  • Shamaev ND, Shuralev EA, Nikitin OV, et al (2021): Prevalence of Toxoplasma gondii infection among small mammals in Tatarstan, Russian Federation. Sci Rep, 11, 22184.
  • Shamaev ND, Shuralev EA, Mukminov MN (2024): Current status of Nosema spp. infection cases in Apis mellifera in Eurasian countries and Ptp3 gene haplotypes in the Republic of Tatarstan, Russia. Vet Res Commun, 48, 2691–2698.
  • Shamaev ND, Shuralev EA, Mukminov MN (2024): Distribution of Nosema apis haplotypes in a single apiary of the Republic of Tatarstan. Bulletin Ryazan State Agrotech Uni P.A. Kostycheva, 16, 92–101. (in Russ.).
  • Shamaev ND, Tretiakova AB, Kambale EM, et al (2025): Melissococcus plutonius pathogen indication and identification using exogenous DNA isolated from the veterinary supervision objects of individual apiaries. Prob Vet San Hyg Ecol, 1, 81–87. (In Russ.).
  • Shuralev EA, Khammadov NI, Osyanin KA, et al (2021): Initial multi-target approach shows importance of improved caprine arthritis-encephalitis virus control program in Russia for hobbyist goat farms. Vet World. 14, 1718–1726.
  • Team, RDC (2010): R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
  • Tokarev YS, Ignatyeva AN, Zinatullina ZY (2010): Molecular diagnostics of nosemosis. Beekeeping, 5, 18–19. (in Russ.).
  • Tozkar CÖ (2015): Prevalence of pathogens and other associated microorganisms in Turkish honey bee subspecies and differential responses to Nosema ceranae infection. PhD thesis, Middle East Technical University.
  • Yudakhina MA (2022): Ecological features and the influence of hive materials on the viability of bee colonies in Eastern Siberia. IOP Conference Series: Earth and Environmental Science, 981.
  • Zalilova ZA, Mannapov AG, Lukyanova MT, et al (2021): Strategies of Regional Economic and Sustainable Development: The Case of the Beekeeping Industry. In: Bogoviz AV (Ed) The Challenge of Sustainability in Agricultural Systems. Springer International Publishing.
  • Zerek A, Yaman M, Dik B (2022): Prevalence of nosemosis in honey bees (Apis province in Turkey. J Apic Res, 61, 368–374.
  • Zufriategui C, Porrini MP, Eguaras MJ, et al (2024): Detrimental effects of amitraz exposure in honey bees (Apis mellifera) infected with Nosema ceranae. Parasitol Res, 123, 204.

Rusya'nın Tataristan Cumhuriyeti'nde bal arılarında nosemosis yaygınlığını etkileyen arıcılık uygulamasıyla ilgili faktörler

Yıl 2025, Cilt: 72 Sayı: 3, 365 - 376, 01.07.2025

Nikolai Shamaev , Eduard Shuralev Oleg Nikitin Malik Mukminov

https://doi.org/10.33988/auvfd.1594759

Öz

Tarımda tozlaşma hizmetlerinin sağlanması ve bal arısı popülasyonlarının korunması için etkili yönetim stratejilerinin uygulanması için patojen ve zararlıların yaygınlığını ve bunların oluşumunu etkileyen faktörleri anlamak gerekir. Nosemosis, Nosema spp. mikrosporidian parazitlerinin neden olduğu, bağırsak hasarına, yetersiz beslenmeye, ishale ve bal arılarının ölümüne yol açan ve en sonunda koloni çöküş bozukluğuna yol açan bir hastalıktır. Nosemosis, arı sağlığı ve genel kovan verimliliği üzerindeki olumsuz etkisi nedeniyle dünya çapındaki arıcılar için önemli bir endişe kaynağı olmuştur. Nosema apis ve N. ceranae PCR pozitifliği için potansiyel risk faktörleri olarak aşağıdaki faktörleri değerlendirmek için çok değişkenli lojistik regresyon kullanıldı: ilçe, kışlama tipi, bal arısı cinsi, kovan materyali, varroa, daha önce bildirilen askozferoz veya nosemoz, koloni gücü, kışın besleme, amitraz, fluvalinat veya timol kullanımı. Bulgularımız, yalnızca timol kullanımı için değişken sayımının verilere iyi uyduğunu, N. ceranae enfeksiyonunun gerçek gözlemlenen yaygınlığının timol kullanan bal arısı popülasyonunda, timol kullanmayan popülasyona göre önemli ölçüde daha yüksek olduğunu göstermektedir. Mevcut çalışmada timol kullanan ve N. ceranae enfeksiyonu azalmış ancak ortadan kaldırılmamış bal arısı popülasyonları, arıcılık uygulamasında muhtemelen önleyici, kontrolsüz ve aşırı akarisit kullanımıyla karşı karşıya kalmıştır.

Anahtar Kelimeler

Apis mellifera bal arısı paraziti multinomial lojistik regresyon Nosema spp nosemosis timol kullanımı

Kaynakça

  • Aguila RD, Gonzalez Ramirez AR (2014): Sample size calculation. Allergol Immunopathol (Madr), 42, 485–492.
  • Altman DG, Bland JM (2011): Statistics notes: How to obtain the P value from a confidence interval. BMJ, 343,7825.
  • Bhusal S, Thapa R (2006): Response of colony strength to honey production: regression and correlation analysis. J Inst Agric Anim, 27, 133–137.
  • Borges D, Guzman-Novoa E, Goodwin PH (2020): Control of the microsporidian parasite Nosema ceranae in honey bees (Apis mellifera) using nutraceutical and immuno-stimulatory compounds. PLOS ONE, 15, e0227484.
  • Botias C, Martín-Hernández R, Barrios L, et al (2013): Nosema spp. infection and its negative effects on honey bees (Apis mellifera iberiensis) at the colony level. Vet Res, 44, 1-15.
  • Bourgeois АL, Rinderer TE, Sylvester HA, et al (2012): Patterns of Apis mellifera infestation by Nosema ceranae support the parasite hypothesis for the evolution of extreme polyandry in eusocial insects. Apidologie, 43, 539-548.
  • Brandorf AZ, Shestakova AI, Larkina EO, et al (2023): Effect of acaricide treatment on body weight and reproductive characteristics of drones of the Prioksky breed type of Central Russian honeybees (Apis mellifera Linnaeus, 1758). Sel’skokhozyaistvennaya Biol, 58, 345–354.
  • Chaimanee V, Warrit N, Chantawannakul P (2010): Infections of Nosema ceranae in four different honeybee species. J Invertebr Pathol, 105, 207–210.
  • Claing G, Dubreuil P, Bernier M, et al (2024): Prevalence of pathogens in honey bee colonies and association with clinical signs in southwestern Quebec, Canada. Can J Vet Res, 88, 45–54.
  • Costello A B, Osborne J (2005): Best practices in exploratory factor analysis: four recommendations for getting the most from your analysis. Pract Assess Res Eval, 10, 7.
  • Cox-Foster DL, Conlan S, Holmes EC, et al (2007): A metagenomic survey of microbes in honey bee colony collapse disorder. Science, 318, 283–287.
  • D’Alvise P, Böhme F, Codrea MC, et al (2018): The impact of winter feed type on intestinal microbiota and parasites in honey bees. Apidologie, 49, 252–264.
  • Fontbonne R, Garnery L, Vidau C, et al (2013): Comparative susceptibility of three Western honeybee taxa to the microsporidian parasite Nosema ceranae. Infect Gen Evol, 17, 188–194.
  • Formato G, Rivera-Gomis J, Bubnic J, et al (2022): Nosemosis prevention and control. Appl Sci, 12, 783.
  • Galiullina AV, Nizamov RN, Vagin KN, et al (2017): Accumulation and redistribution of radionuclides in honey bees and apiary products in the Republic of Tatarstan, Russia. Astra Salvensis, 2017, 581–590.
  • Glavinic U, Blagojevic J, Ristanic M, et al (2022): Use of thymol in Nosema ceranae control and health improvement of infected honey bees. Insects, 13, 574.
  • Glavinic U, Rajkovic M, Ristanic M, et al (2023): Genotoxic potential of thymol on honey bee DNA in the Comet Assay. Insects, 14, 451.
  • Goblirsch M (2018): Nosema ceranae disease of the honey bee (Apis mellifera). Apidologie. 49, 131-150.
  • Gunes N, Aydın L, Belenli D, et al (2017): Stress responses of honey bees to organic acid and essential oil treatments against varroa mites. J Apic Res, 56, 175–181.
  • Haritonov NN (2006): Selekciya ustojchivyhk zabolevaniyam linij pchel. Pchelovodstvo, 7, 14–16.
  • Hasbieva DR, Kambale EM, Ndayishimiye EW, et al (2025): Nosemosis in Rwandan mining areas. 272–278. In: Proceedings of the International Scientific and Practical Conference. Rybnoye, Russia. (in Russ.).
  • Hillier NK, Frost EH, Shutler D (2013): Fate of dermally applied miticides fluvalinate and amitraz within honey bee (Hymenoptera: Apidae) bodies. J Econ Entomol, 106, 558–565.
  • Ilyasov RA, Gajfullina LR, Saltykova ES, et al (2014): Biology, distribution and prevention of microsporidians of Nosema genus, parasites of honey bees. Biomika, 6, 145–154 (in Russ.).
  • Ilyasov RA, Shareeva ZV (2014): Effect of fluvalinate and amitraz on bee colonies. Beekeeping, 6, 24–26. (in Russ.).
  • Kashkovskii VG, Plakhova AA, Kropachev DV (2019): Features of the development of beekeeping in the Narym region of Russia. Adv Anim Vet Sci, 7, 50–59.
  • Kaskinova M, Saltykova E, Poskryakov A, et al (2021): The current state of the protected Apis mellifera mellifera population in Russia: hybridization and Nosematosis. Animals, 11, 2892.
  • Ministry of Agriculture and Food of the Republic of Tatarstan (2022): Beekeeping registry. Available at https://agro.tatarstan.ru/reestr-po-pchelovodstvu-4701889.htm. (Accessed March 2, 2024).
  • Mukminov MN, Shuralev EA, Kazaryan GG, et al (2023): Microsporidia associated with infections of honey bees. 113–118. In: Proceedings of the International Scientific and Practical Conference. Rybnoye, Russia. (in Russ.).
  • Ostroverhova NV, Konusova OL, Pogorelov Yu L (2015): Morphometric and molecular-genetic characteristics of bee colonies of Tomsk region infected with nosemosis. In: Materials of the Regional Scientific-Practical Conference. Krasnoyarsk, Russia. (in Russ.).
  • Owen R (2017): Role of human action in the spread of honey bee (Hymenoptera: Apidae) pathogens. J Econ Entomol, 110, 797–801.
  • Petuhov AV, Popov AS, Kazakova AN (2014): Resistance to nosemosis in bees of different species. In: Proceedings of International Scientific-Practical Conference. Kirov, Russia. (in Russ.).
  • Punko RN, Currie RW, Nasr ME, et al (2021): Epidemiology of Nosema spp. and the effect of indoor and outdoor wintering on honey bee colony population and survival in the Canadian Prairies. PLOS ONE, 16, e0258801.
  • Shamaev ND (2024): Background to the existence of variation in the innate immune response in Galleria mellonella. Agrarian Bull of Urals, 24, 1492‒1501. (In Russ.).
  • Shamaev ND, Batanova T, Iwatake Yu, et al (2024): Diversity of genes encoding immune-related GTPase B2 protein, an inherited element responsible for resistance against virulent Toxoplasma gondii strains, among wild Mus musculus in local area of Japan. J Vet Med Sci, 86, 1056–1062.
  • Shamaev ND, Kambale EM, Valiakhmetov DI, et al (2024): Biodiversity of Nosema ceranae genovars in the Apis mellifera population with hybrid traits under apiary conditions. Prob Vet San Hyg Ecol, 4, 597–605. (in Russ.).
  • Shamaev ND, Potapov KO, Mukminov MN, et al (2025): Ganoderma applanatum extract biopesticidal properties evaluation against greater wax moth Galleria mellonella. Vet Med, 5, 55–59. (In Russ.).
  • Shamaev ND, Salnikov VV, Yuzmanova LA, et al (2024): Regular occurrence of atypically small spores in Apis mellifera carnica (Hymenoptera: Apidae), naturally infected with Nosema spp. (Microsporidia). Inverteb Zool, 21, 478–486.
  • Shamaev ND, Shuralev EA, Nikitin OV, et al (2021): Prevalence of Toxoplasma gondii infection among small mammals in Tatarstan, Russian Federation. Sci Rep, 11, 22184.
  • Shamaev ND, Shuralev EA, Mukminov MN (2024): Current status of Nosema spp. infection cases in Apis mellifera in Eurasian countries and Ptp3 gene haplotypes in the Republic of Tatarstan, Russia. Vet Res Commun, 48, 2691–2698.
  • Shamaev ND, Shuralev EA, Mukminov MN (2024): Distribution of Nosema apis haplotypes in a single apiary of the Republic of Tatarstan. Bulletin Ryazan State Agrotech Uni P.A. Kostycheva, 16, 92–101. (in Russ.).
  • Shamaev ND, Tretiakova AB, Kambale EM, et al (2025): Melissococcus plutonius pathogen indication and identification using exogenous DNA isolated from the veterinary supervision objects of individual apiaries. Prob Vet San Hyg Ecol, 1, 81–87. (In Russ.).
  • Shuralev EA, Khammadov NI, Osyanin KA, et al (2021): Initial multi-target approach shows importance of improved caprine arthritis-encephalitis virus control program in Russia for hobbyist goat farms. Vet World. 14, 1718–1726.
  • Team, RDC (2010): R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
  • Tokarev YS, Ignatyeva AN, Zinatullina ZY (2010): Molecular diagnostics of nosemosis. Beekeeping, 5, 18–19. (in Russ.).
  • Tozkar CÖ (2015): Prevalence of pathogens and other associated microorganisms in Turkish honey bee subspecies and differential responses to Nosema ceranae infection. PhD thesis, Middle East Technical University.
  • Yudakhina MA (2022): Ecological features and the influence of hive materials on the viability of bee colonies in Eastern Siberia. IOP Conference Series: Earth and Environmental Science, 981.
  • Zalilova ZA, Mannapov AG, Lukyanova MT, et al (2021): Strategies of Regional Economic and Sustainable Development: The Case of the Beekeeping Industry. In: Bogoviz AV (Ed) The Challenge of Sustainability in Agricultural Systems. Springer International Publishing.
  • Zerek A, Yaman M, Dik B (2022): Prevalence of nosemosis in honey bees (Apis province in Turkey. J Apic Res, 61, 368–374.
  • Zufriategui C, Porrini MP, Eguaras MJ, et al (2024): Detrimental effects of amitraz exposure in honey bees (Apis mellifera) infected with Nosema ceranae. Parasitol Res, 123, 204.
Toplam 49 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Veteriner Parazitoloji
Bölüm Araştırma Makalesi
Yazarlar

Nikolai Shamaev 0000-0002-0575-3760

Eduard Shuralev 0000-0003-0650-3090

Oleg Nikitin 0000-0002-6753-0597

Malik Mukminov 0000-0002-5996-0271

Erken Görünüm Tarihi 13 Haziran 2025
Yayımlanma Tarihi 1 Temmuz 2025
Gönderilme Tarihi 5 Aralık 2024
Kabul Tarihi 15 Mayıs 2025
Yayımlandığı Sayı Yıl 2025 Cilt: 72 Sayı: 3

Kaynak Göster

APA Shamaev, N., Shuralev, E., Nikitin, O., Mukminov, M. (2025). Beekeeping practice-related factors that impact nosemosis prevalence in honey bees in the Republic of Tatarstan, Russia. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 72(3), 365-376. https://doi.org/10.33988/auvfd.1594759
AMA Shamaev N, Shuralev E, Nikitin O, Mukminov M. Beekeeping practice-related factors that impact nosemosis prevalence in honey bees in the Republic of Tatarstan, Russia. Ankara Univ Vet Fak Derg. Temmuz 2025;72(3):365-376. doi:10.33988/auvfd.1594759
Chicago Shamaev, Nikolai, Eduard Shuralev, Oleg Nikitin, ve Malik Mukminov. “Beekeeping Practice-Related Factors That Impact Nosemosis Prevalence in Honey Bees in the Republic of Tatarstan, Russia”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 72, sy. 3 (Temmuz 2025): 365-76. https://doi.org/10.33988/auvfd.1594759.
EndNote Shamaev N, Shuralev E, Nikitin O, Mukminov M (01 Temmuz 2025) Beekeeping practice-related factors that impact nosemosis prevalence in honey bees in the Republic of Tatarstan, Russia. Ankara Üniversitesi Veteriner Fakültesi Dergisi 72 3 365–376.
IEEE N. Shamaev, E. Shuralev, O. Nikitin, ve M. Mukminov, “Beekeeping practice-related factors that impact nosemosis prevalence in honey bees in the Republic of Tatarstan, Russia”, Ankara Univ Vet Fak Derg, c. 72, sy. 3, ss. 365–376, 2025, doi: 10.33988/auvfd.1594759.
ISNAD Shamaev, Nikolai vd. “Beekeeping Practice-Related Factors That Impact Nosemosis Prevalence in Honey Bees in the Republic of Tatarstan, Russia”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 72/3 (Temmuz 2025), 365-376. https://doi.org/10.33988/auvfd.1594759.
JAMA Shamaev N, Shuralev E, Nikitin O, Mukminov M. Beekeeping practice-related factors that impact nosemosis prevalence in honey bees in the Republic of Tatarstan, Russia. Ankara Univ Vet Fak Derg. 2025;72:365–376.
MLA Shamaev, Nikolai vd. “Beekeeping Practice-Related Factors That Impact Nosemosis Prevalence in Honey Bees in the Republic of Tatarstan, Russia”. Ankara Üniversitesi Veteriner Fakültesi Dergisi, c. 72, sy. 3, 2025, ss. 365-76, doi:10.33988/auvfd.1594759.
Vancouver Shamaev N, Shuralev E, Nikitin O, Mukminov M. Beekeeping practice-related factors that impact nosemosis prevalence in honey bees in the Republic of Tatarstan, Russia. Ankara Univ Vet Fak Derg. 2025;72(3):365-76.
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