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Investigation of Some Pathogens "Colony Loss Syndrome" Resembled Losses Apiaries in Tekirdağ

Yıl 2017, Cilt: 10 Sayı: 1, 21 - 28, 01.03.2017

Öz

Colony losses, which are remarkable in the world for more than ten years, are regarded as bee health problems arising from the interaction of different factors and agents. The viruses, Nosema ceranae and Varroa destructor among the disease agents threaten the colony health, have significant importance. In this study, the honeybee samples delivered to our laboratory from different apiaries in Tekirdağ province between 2015 and 2016, were examined. Samples were sent by complaints with "unexpected decrease in colony populations or sudden colony loss". A total of 510 honey bee samples from 17 apiaries were tested for Deformed Wing Virus (DWV), Nosema cerenae and Varroa destructor. DWV and N.cerena were detected in 15 and 5 apiaries, respectively while varroosis was detected in all apiaries. N. ceranae was not be detected in the DWV negative two apiaries. In this study, it was concluded that considering the presence of DWV, Nosema cerena and Varroa destructor in sudden colony losses resemble case, and it would be advantageous the precaution and treatment strategies for bees against these pathogens.

Kaynakça

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  • Amiri E, Meixner MD, Kryger P. Deformed wing virus can be transmitted during natural mating in honey bees and infect the queens. Sci Rep. 2016; 9(6):33065.
  • Akkaya H. "Balarısı Kolonilerinin Varroatosis’Ine Flumethrin’In Etkisi. “The Efficacy Of Flumethrin (Bayvarol-Strips) On Varroasis In Honeybee Colonies. Acta Parasitologica Turcica”. Türkiye Parazitoloji Dergisi. 1996; 20: 457-460.
  • Akkaya H, Alkan S. "Turkish Bee Researchers Request Help", American Bee Journal. 2002;142: 549-550.
  • Akkaya H. "Arıcılıkta İlaç Kullanımı: Varroasis". Arıcılık Araştırma. 2014; 6:19-21.
  • Aydın L, Güleğen E, Çetinbaş H. Prevalence of Nosema apis in Southern Marmara Regıon in Turkey. Apimondia. Proceedings of the 37th International Apicultural Congress, 28 October – 1 November 2001.
  • Aydın L, Çakmak İ, Güleğen E, Korkut M. Güney Marmara Bölgesi’nde arı hastalık ve zararlıları anket sonuçları. U. Arı Drg./U. Bee J. 2003; 3(1): 38-41.
  • Bacandritsos N, Granato A, Budge G, Papanastasiou I, Roinioti E, Caldon M, Falcaro C, Gallina A, Mutinelli F. Sudden deaths and colony population decline in Greek honey bee colonies. J Invertebr Pathol. 2010; 105(3):335-40.Bailey L, Ball BV. Honey bee pathology. 1991, Academic Press, London. Pp:10-34.
  • Bailey L, Ball BV. Honey bee pathology. 1991, Academic Press, London. Pp:10-34. Balkaya I, Gülbaz H, Avcıoğlu H, Güven E. Honeybee (Apis mellifera) Diseases in Turkey. Atatürk Üniversitesi Vet. Bil. Dergisi. 2016; 11(3): 339-347.
  • Benaets K, Van Geystelen A, Cardoen D, De Smet L, de Graaf DC, Schoofs L, Larmuseau MH, Brettell LE, Martin SJ, Wenseleers T. Covert deformed wing virus infections have long-term deleterious effects on honeybee foraging and survival. Proc Biol Sci. 2017; 8; 284(1848).
  • Berenyi O, Bakonyi T, Derakhshifar I, Koglberger H, Nowotny N. Occurrence of six honeybee viruses in diseased Austrian apiaries. Appl Environ Microbiol. 2006; 72 (4): 2414-20.
  • Botias C, Martín-Hernández R, Barrios L, Meana A, Higes M. Nosema spp. infection and its negative effects on honey bees (Apis mellifera iberiensis) at the colony level. Vet Res. 2013; 10: 44:25.
  • Brodschneider R, Gray A, van der Zee R, Adjlane N, Brusbardis V, Charrière JD. Preliminary analysis of loss rates of honey bee colonies during winter 2015/16 from the COLOSS survey. J of Apicultural Res. 2016; 55: 375-378.
  • Bromenshenk JJ, Henderson CB, Wick CH, Stanford MF, Zulich AW, Jabbour RE, Deshpande SV, McCubbin PE, Seccomb RA, Welch PM, Williams T, Firth DR, Skowronski E, Lehmann MM, Bilimoria SL, Gress J, Wanner KW, Cramer RA. Iridovirus and microsporidian linked to honey bee colony decline. PLoS One. 2010; 5. Büyük M, Tunca İvgin R, Taşkın T. Kırşehir İlindeki Arılıklarda Nosema Hastalığının Belirlenmesi. Türk Tarım – Gıda Bilim ve Teknoloji Dergisi. 2017; 5(1): 1-5.
  • Cepero A, Ravoet J, Gómez-Moracho T, Bernal JL, Del Nozal MJ, Bartolomé C, Maside X, Meana A, González-Porto AV, de Graaf DC, Martín-Hernández R, Higes M. Holistic screening of collapsing honey bee colonies in Spain: a case study. BMC Res Notes. 2014; 15(7): 649.
  • Çakmak I, Aydin L, Seven S, Korkut M. Beekeeping Survey in Southern Marmara Region of Turkey. Uludag Bee Journal. 2003; 3(1): 31-36.
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  • Cox-Foster DL, Conlan S, Holmes EC, Palacios G, Evans JD, Moran NA, Quan PL, Briese T, Hornig M. A metagenomic survey of microbes in honey bee colony collapse disorder. Science. 2007; 318: 283–287.
  • Dainat B, Evans JD, Chen YP, Gauthier L, Neumann P. Predictive markers of honey bee colony collapse. PLoS One.2012; 7(2). Dainat B, Neumann P. Clinical signs of deformed wing virus infection are predictive markers for honey bee colony losses. J Invertebr Pathol. 2013; 112(3):278-80.
  • Desai SD, Currie RW. Effects of Wintering Environment and Parasite-Pathogen Interactions on Honey Bee Colony Loss in North Temperate Regions. PLoS One. 2016; 2;11(7).
  • Doublet V, Natsopoulou ME, Zschiesche L, Paxton RJ. Within-host competition among the honey bees pathogens Nosema ceranae and Deformed wing virus is asymmetric and to the disadvantage of the virus. J Invertebr Pathol. 2015. 124:31-4.
  • Doublet V, Paxton RJ, McDonnell CM, Dubois E, Nidelet S, Moritz RF, Alaux C, Le Conte Y. Brain transcriptomes of honey bees (Apis mellifera) experimentally infected by two pathogens: Black queen cell virus and Nosema ceranae. Genom Data. 2016; 28(10):79-82.
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Tekirdağ’da “Koloni Kaybı Sendromu” Benzeri Kayıp Görülen Arılıklarda Bazı Patojenlerinin Araştırılması

Yıl 2017, Cilt: 10 Sayı: 1, 21 - 28, 01.03.2017

Öz

Dünya’da on yıldan fazla süredir dikkat çeken koloni kayıpları, farklı etken ve faktörlerin etkileşimi ile ortaya çıkan arı sağlığı sorunu olarak kabul edilmektedir. Bal arısı koloni sağlığını tehdit eden hastalık etkenleri arasında viruslar, Nosema ceranae ve Varroa destructor ciddi öneme sahiptir. Bu çalışmada 2015 ve 2016 yıllarında Tekirdağ ilindeki farklı arılıklardan gönderilen balarısı numuneleri incelenmiştir. Örnekler “koloni populasyonundaki beklenmeyen azalma veya ani koloni kaybı” şikâyetleriyle gönderilmiştir. Buna göre 17 arılıktan gönderilen 510 bal arısı örneği, Deforme kanat virusu (Deformed Wing Virus – DWV), Nosema cerenae ve Varroa destructor yönünden kontrol edilmiştir. Bu arılıkların tamamında varroosis tespit edilirken, DWV 15 arılıkta, N. ceranae ise 5 arılıkta tespit edilmiştir. DWV tespit edilemeyen iki arılıkta N. ceranae da tespit edilememiştir. Bu araştırmada, ani koloni kaybı sendromuna benzer şekilde görülen koloni kayıplarında DWV, Nosema cerena ve Varroa destructor’a rastlanma oranlarının araştırılarak bu konuda güncel veri sağlanması hedeflenmiştir.

Kaynakça

  • Aizen MA, Garibaldi LA, Cunningham SA, Klein AM. How much does agriculture depend on pollinators? Lessons from long-term trends in crop production. Annals of Botany. 2009; 103: 1579–1588.
  • Amiri E, Meixner MD, Kryger P. Deformed wing virus can be transmitted during natural mating in honey bees and infect the queens. Sci Rep. 2016; 9(6):33065.
  • Akkaya H. "Balarısı Kolonilerinin Varroatosis’Ine Flumethrin’In Etkisi. “The Efficacy Of Flumethrin (Bayvarol-Strips) On Varroasis In Honeybee Colonies. Acta Parasitologica Turcica”. Türkiye Parazitoloji Dergisi. 1996; 20: 457-460.
  • Akkaya H, Alkan S. "Turkish Bee Researchers Request Help", American Bee Journal. 2002;142: 549-550.
  • Akkaya H. "Arıcılıkta İlaç Kullanımı: Varroasis". Arıcılık Araştırma. 2014; 6:19-21.
  • Aydın L, Güleğen E, Çetinbaş H. Prevalence of Nosema apis in Southern Marmara Regıon in Turkey. Apimondia. Proceedings of the 37th International Apicultural Congress, 28 October – 1 November 2001.
  • Aydın L, Çakmak İ, Güleğen E, Korkut M. Güney Marmara Bölgesi’nde arı hastalık ve zararlıları anket sonuçları. U. Arı Drg./U. Bee J. 2003; 3(1): 38-41.
  • Bacandritsos N, Granato A, Budge G, Papanastasiou I, Roinioti E, Caldon M, Falcaro C, Gallina A, Mutinelli F. Sudden deaths and colony population decline in Greek honey bee colonies. J Invertebr Pathol. 2010; 105(3):335-40.Bailey L, Ball BV. Honey bee pathology. 1991, Academic Press, London. Pp:10-34.
  • Bailey L, Ball BV. Honey bee pathology. 1991, Academic Press, London. Pp:10-34. Balkaya I, Gülbaz H, Avcıoğlu H, Güven E. Honeybee (Apis mellifera) Diseases in Turkey. Atatürk Üniversitesi Vet. Bil. Dergisi. 2016; 11(3): 339-347.
  • Benaets K, Van Geystelen A, Cardoen D, De Smet L, de Graaf DC, Schoofs L, Larmuseau MH, Brettell LE, Martin SJ, Wenseleers T. Covert deformed wing virus infections have long-term deleterious effects on honeybee foraging and survival. Proc Biol Sci. 2017; 8; 284(1848).
  • Berenyi O, Bakonyi T, Derakhshifar I, Koglberger H, Nowotny N. Occurrence of six honeybee viruses in diseased Austrian apiaries. Appl Environ Microbiol. 2006; 72 (4): 2414-20.
  • Botias C, Martín-Hernández R, Barrios L, Meana A, Higes M. Nosema spp. infection and its negative effects on honey bees (Apis mellifera iberiensis) at the colony level. Vet Res. 2013; 10: 44:25.
  • Brodschneider R, Gray A, van der Zee R, Adjlane N, Brusbardis V, Charrière JD. Preliminary analysis of loss rates of honey bee colonies during winter 2015/16 from the COLOSS survey. J of Apicultural Res. 2016; 55: 375-378.
  • Bromenshenk JJ, Henderson CB, Wick CH, Stanford MF, Zulich AW, Jabbour RE, Deshpande SV, McCubbin PE, Seccomb RA, Welch PM, Williams T, Firth DR, Skowronski E, Lehmann MM, Bilimoria SL, Gress J, Wanner KW, Cramer RA. Iridovirus and microsporidian linked to honey bee colony decline. PLoS One. 2010; 5. Büyük M, Tunca İvgin R, Taşkın T. Kırşehir İlindeki Arılıklarda Nosema Hastalığının Belirlenmesi. Türk Tarım – Gıda Bilim ve Teknoloji Dergisi. 2017; 5(1): 1-5.
  • Cepero A, Ravoet J, Gómez-Moracho T, Bernal JL, Del Nozal MJ, Bartolomé C, Maside X, Meana A, González-Porto AV, de Graaf DC, Martín-Hernández R, Higes M. Holistic screening of collapsing honey bee colonies in Spain: a case study. BMC Res Notes. 2014; 15(7): 649.
  • Çakmak I, Aydin L, Seven S, Korkut M. Beekeeping Survey in Southern Marmara Region of Turkey. Uludag Bee Journal. 2003; 3(1): 31-36.
  • Çakmak I. Foraging Ecology of Bees and Their Role in Crop Production. Veterinarni Medicina, 2014; 59(1): 1–10.
  • Cox-Foster DL, Conlan S, Holmes EC, Palacios G, Evans JD, Moran NA, Quan PL, Briese T, Hornig M. A metagenomic survey of microbes in honey bee colony collapse disorder. Science. 2007; 318: 283–287.
  • Dainat B, Evans JD, Chen YP, Gauthier L, Neumann P. Predictive markers of honey bee colony collapse. PLoS One.2012; 7(2). Dainat B, Neumann P. Clinical signs of deformed wing virus infection are predictive markers for honey bee colony losses. J Invertebr Pathol. 2013; 112(3):278-80.
  • Desai SD, Currie RW. Effects of Wintering Environment and Parasite-Pathogen Interactions on Honey Bee Colony Loss in North Temperate Regions. PLoS One. 2016; 2;11(7).
  • Doublet V, Natsopoulou ME, Zschiesche L, Paxton RJ. Within-host competition among the honey bees pathogens Nosema ceranae and Deformed wing virus is asymmetric and to the disadvantage of the virus. J Invertebr Pathol. 2015. 124:31-4.
  • Doublet V, Paxton RJ, McDonnell CM, Dubois E, Nidelet S, Moritz RF, Alaux C, Le Conte Y. Brain transcriptomes of honey bees (Apis mellifera) experimentally infected by two pathogens: Black queen cell virus and Nosema ceranae. Genom Data. 2016; 28(10):79-82.
  • Dussaubat C, Maisonnasse A, Crauser D, Tchamitchian S, Bonnet M, Cousin M, Kretzschmar A, Brunet JL, Le Conte Y. Combined neonicotinoid pesticide and parasite stress alter honeybee queens' physiology and survival. Sci Rep. 2016. 31; 6.
  • Evans JD, Pettis JS. Colony-level impacts of immune responsiveness in honey bees, Apis mellifera. Evolution 2005. 59(10):2270-4. Evans JD, Spivak M. Socialized medicine: individual and communal disease barriers in honey bees. J Invertebr Pathol. 2010; 103 (1):62-72.
  • Evans JD, Aronstein K, Chen YP, Hetru C, Imler JL, Jiang H, Kanost M, Thompson GJ, Zou Z., Hultmark D. Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol Biol. 2006; 15(5): 645–656.
  • Fievet J, Tentcheva D, Gauthier L, de Miranda J, Cousserans F, Colin ME, Bergoin M. Localization of deformed wing virus infection in queen and drone Apis mellifera L. Virol J. 2006; 3:16.
  • Fine JD, Cox-Foster DL, Mullin CA. An Inert Pesticide Adjuvant Synergizes Viral Pathogenicity and Mortality in Honey Bee Larvae. Sci Rep. 2017; 16(7):40499.
  • Gallai N, Salles JM, Settele J, Vaissiere BE. Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecological Economics. 2009; 68: 810– 821.
  • Gauthier L, Ravallec M, Tournaire M, Cousserans F, Bergoin M, Dainat B, de Miranda JR. Viruses associated with ovarian degeneration in Apis mellifera L. queens. PLoS One. 2011; 25;6(1).
  • Genersch E. Honey bee pathology: current threats to honey bees and beekeeping. Appl Microbiol Biotechnol. 2010; 87(1):87-97.
  • Genersch E, Evans JD, Fries I. Honey bee disease overview. J Invertebr Pathol.2010;103 Suppl 1:S2-4.
  • Girişgin AO, Aydın L. Varroa destructor ile Doğal Enfeste Balarılarında Organik Asitlerin Kullanımı ve Etkinliği. Kafkas Ün.Veteriner Fak.Derg. 2010; 16(6): 941-945.
  • Gülmez Y, Bursalı A, Tekin S. First molecular detection and characterization of deformed wing virus (DWV) in honeybees (Apis mellifera L.) and mites (Varroa destructor) in Turkey. African Journal of Biotechnology. 2009; 8: 3698–3702.
  • Higes M, Martín-Hernández R, Garrido-Bailón E, Botías C, Meana A. First detection of Nosema ceranae (Microsporidia) in African Honey bees (Apis mellifera intermissa). J. Apic. Res. 2009; 48: 217–219.
  • Hristov Y. Reasons for bee colony losses in Bulgaria and their relation with CCD. Comptes rendus de l’Acade'mie Bulgare des Sciences. 2014; 67 (5): 727-736.
  • Johnson RM, Evans JD, Robinson GE, Berenbaum MR. Changes in transcript abundance relating to colony collapse disorder in honey bees (Apis mellifera). Proceedings of the National Academy of Sciences of the United States of America. 2009; 106: 14790– 14795.
  • Kanbar G, Engels W. Communal use of integumental wounds in honey bee (Apis mellifera) pupae multiply infested by the ectoparasitic mite Varroa destructor.Genet Mol Res. 2005; 30;4(3):465-72.
  • Karahan A, Çakmak I, Hranitz JM, Karaca I, Wells H. Sublethal imidacloprid effects on honey bee flower choices when foraging. Ecotoxicology. 2015; 24(9):2017-25.
  • Klein AM, Vaissiere BE, Cane JH, Steffan- Dewenter I, Cunningham SA, Kremen C, Tscharntke T. Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B-Biological Sciences. 2007; 274: 303–313.
  • Lanzi G, Miranda JR, Boniotti MB, Cameron CE, Lavazza A, Capucci L, Camazine SM, Rossi C. Molecular and Biological Characterization of Deformed Wing Virus of Honeybees (Apis mellifera L.) J. Virol. 2006; 80(10): 4998-5009.
  • Martín-Hernández R, Meana A, Prieto L, Salvador AM, Garrido-Bailón E, Higes M. Outcome of colonization of Apis mellifera by Nosema ceranae. Appl Environ Microbiol. 2007;73(20):6331-8.
  • Mazzei M, Carrozza ML, Luisi E, Forzan M, Giusti M, Sagona S, Tolari F, Felicioli A. Infectivity of DWV associated to flower pollen: experimental evidence of a horizontal transmission route. PLoS One. 2014; 24;9(11).
  • Mondet F, Kim SH, de Miranda JR, Beslay D, Le Conte Y, Mercer AR. Specific cues associated With Honey Bee social defence against Varroa destructor infested brood. Sci Rep. 2016; 3 (6):25444.
  • Muz MN, Muz D. Occcurrence and genetic analysis of DWV (Deformed wing virus) and ABPV (Acute bee paralysis virus) and Varroa destructor-1 virus (VD-1) in Turkey. Proceedings of the 2nd Intenational Forum of Apimondia-Apiquality, 9-12 June 2008, Villa Mondragone, Rome, Italy. pp. 94.
  • Muz D, Muz MN. Survey of the occurrence of Deformed Wing Virus and multiple parasites of queens (Apis mellifera L.) in apiaries with collapsed colonies in Hatay, Turkey, Journal of Apıcultural Research. 2009; 48: 204-208.
  • Muz MN, Girişgin AO, Muz D, Aydın L. Molecular detection of Nosema ceranae and Nosema apis infections in Turkish apiaries with collapsed colonies, J of Apicultural Res. 2010; 49: 342-344.
  • Muz MN, Solmaz H, Yaman M, Karakavuk M. Kış Salkımı Erken Bozulan Arı Kolonilerinde Paraziter ve Bakteriyel Patojenler. YYU Veteriner Fakültesi Dergisi. 2012; 23 (3):147– 150.
  • Nazzi F, Le Conte Y. Ecology of Varroa destructor, the Major Ectoparasite of the Western Honey Bee, Apis mellifera. Annu Rev Entomol. 2016; 61:417-32.
  • Parvanov P, Rusenova N. Etiology and clinicoepidemiological profile of apiaries with colony collapse disorder-like symptoms in Bulgaria. Bulgarian Journal of Veterinary Medicine. 2014; 17(3): 199-206.
  • Pires CCS, Pereira FM, Lopes MTR, Nocelli RCF, Malaspina O, Pettis FS, Teixeira EW. Weakness and collapse of bee colonies in Brazil: are there cases of CCD? Pesq. agropec. bras. 2016; 51(5):422-442.
  • Richard FJ, Holt HL, Grozinger CM. Effects of immunostimulation on social behavior, chemical communication and genome-wide gene expression in honey bee workers (Apis mellifera). BMC Genomics. 2012; 16(13):558.
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  • Simone M, Evans JD, Spivak M. Resin collection and social immunity in honey bees. Evolution. 2009; 63(11):3016-22.
  • Singh R, Levitt AL, Rajotte EG, Holmes EC, Ostiguy N, Vanengelsdorp D, Lipkin WI, Depamphilis CW, Toth AL, Cox-Foster DL. RNA viruses in hymenopteran pollinators: evidence of inter-Taxa virus transmission via pollen and potential impact on non-Apis hymenopteran species. PLoS One. 2010; 22;5(12):e14357.
  • Stokstad, E. The case of the empty hives. Science. 2007a; 316: 970– 972.
  • Stokstad, E. Puzzling decline of U. S. bees linked to virus from Australia. Science. 2007b; 317: 1304–1305.
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  • Tunca R, Çimrin T, Büyük M, Taşkın A, Oskay D. A Survey on Beekeeping Activities and Colony Losses in Turkey. Journal of Agricultural Faculty of Gaziosmanpasa University. 2016; 33 (2), 56-62.
  • Ütük AE, Pişkin FÇ, Kurt M. First molecular detection of Nosema ceranae in Turkey. Ankara Univ Vet Fak Derg 2010; 57: 275-278.
  • Ütük AE, Piskin FC, Girisgin AO, Selcuk O, Aydın L. Microscopic and molecular detection of Nosema spp. in honeybees of Turkey. Apidologie (2016); 47: 267.
  • Van Der Zee R, Gray A, Pisa L, De Rijk T. An Observational Study of Honey Bee Colony Winter Losses and Their Association with Varroa destructor, Neonicotinoids and Other Risk Factors. PLoS One. 2015; 8;10(7)
  • Warrit N, Hagen TAR, Smith DR, Çakmak İ. A survey of Varroa destructor strains on Apis mellifera in Turkey. Journal of Apicultural Research. 2004; 43 (4): 190-191.
  • Wenning CJ. Experimenting with honey bees: Northern hive depopulation & wintering. American Bee Journal. 2002; 142(8), 587-590.
  • Whitaker J, Szalanski AL, Kence M. Molecular Detection of N. ceranae and N. apis from Turkish Honey Bees. Apidologie. 2010; 42(2): 174-180.
  • Winfree R, Williams NM, Dushoff J, Kremen C. Native bees provide insurance against ongoing honey bee losses. Ecol Lett. 2007; 10(11):1105-13.
  • Yalçınkaya A, Keskin N. The Investigation of Honey Bee Diseases After Colony Losses in Hatay and Adana Provinces of Turkey. Mellifera. 2010; 10-20:24-31.
  • Yanez O, Jaffe R, Jarosch A, Fries I, Moritz RFA, Paxton RJ, de Miranda JR. Deformed wing virus and drone mating flights in the honey bee (Apis mellifera): implications for sexual transmission of a major honey bee virus. Apidologie (Celle). 2012; 43: 17–30.
  • Yue C, Genersch E. RT-PCR analysis of Deformed wing virus in honeybees (Apis mellifera) and mites (Varroa destructor). J Gen Virol. 2005; 86:3419–3424.
  • Yue C, Schroder M, Bienefeld K, Genersch E. Detection of viral sequences in semen of honeybees (Apis mellifera): evidence for vertical transmission of viruses through drones. J Invertebr Pathol. 2006; 92: 105–108.
  • Yue C, Schroder M, Gisder S, Genersch E. Vertical transmission routes for deformed wing virus of honeybees (Apis mellifera). J Gen Virol. 2007; 88, 2329–2336.
  • Zhang X, He SY, Evans JD, Pettis JS, Yin GF, Chen YP. New evidence that deformed wing virus and black queen cell virus are multi-host pathogens. J Invertebr Pathol. 2012; 109(1):156-9.
  • Zheng HQ, Gong HR, Huang SK, Sohr A, Hu FL, Chen YP. Evidence of the synergistic interaction of honey bee pathogens Nosema ceranae and Deformed wing virus. Vet Microbiol. 2015; 15;177(1-2):1-6.
Toplam 72 adet kaynakça vardır.

Ayrıntılar

Bölüm ARAŞTIRMA MAKALESİ
Yazarlar

Dilek Muz Bu kişi benim

Mustafa Necati Muz Bu kişi benim

Yayımlanma Tarihi 1 Mart 2017
Kabul Tarihi 11 Mart 2017
Yayımlandığı Sayı Yıl 2017 Cilt: 10 Sayı: 1

Kaynak Göster

APA Muz, D., & Muz, M. N. (2017). Investigation of Some Pathogens "Colony Loss Syndrome" Resembled Losses Apiaries in Tekirdağ. Kocatepe Veterinary Journal, 10(1), 21-28.
AMA Muz D, Muz MN. Investigation of Some Pathogens "Colony Loss Syndrome" Resembled Losses Apiaries in Tekirdağ. kvj. Mart 2017;10(1):21-28.
Chicago Muz, Dilek, ve Mustafa Necati Muz. “Investigation of Some Pathogens ‘Colony Loss Syndrome’ Resembled Losses Apiaries in Tekirdağ”. Kocatepe Veterinary Journal 10, sy. 1 (Mart 2017): 21-28.
EndNote Muz D, Muz MN (01 Mart 2017) Investigation of Some Pathogens "Colony Loss Syndrome" Resembled Losses Apiaries in Tekirdağ. Kocatepe Veterinary Journal 10 1 21–28.
IEEE D. Muz ve M. N. Muz, “Investigation of Some Pathogens ‘Colony Loss Syndrome’ Resembled Losses Apiaries in Tekirdağ”, kvj, c. 10, sy. 1, ss. 21–28, 2017.
ISNAD Muz, Dilek - Muz, Mustafa Necati. “Investigation of Some Pathogens ‘Colony Loss Syndrome’ Resembled Losses Apiaries in Tekirdağ”. Kocatepe Veterinary Journal 10/1 (Mart 2017), 21-28.
JAMA Muz D, Muz MN. Investigation of Some Pathogens "Colony Loss Syndrome" Resembled Losses Apiaries in Tekirdağ. kvj. 2017;10:21–28.
MLA Muz, Dilek ve Mustafa Necati Muz. “Investigation of Some Pathogens ‘Colony Loss Syndrome’ Resembled Losses Apiaries in Tekirdağ”. Kocatepe Veterinary Journal, c. 10, sy. 1, 2017, ss. 21-28.
Vancouver Muz D, Muz MN. Investigation of Some Pathogens "Colony Loss Syndrome" Resembled Losses Apiaries in Tekirdağ. kvj. 2017;10(1):21-8.

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