Monitoring of Nosema Infections Levels During Hygienic Honey Bee Breeding Programs in Turkey

Bu çalışmada, Amerikan Yavru Çürüklüğü (Paenibacillus larvae) hastalığına dirençli olan hijyenik balarısı ıslah programında Nosema enfeksiyon düzeyinin takibi amaçlanmıştır. Islah programında Apis mellifera anatoliaca ekotipi olarak adlandırılan Muğla balarısında 2012-2014 yılları arasında 5 dönem boyunca Nosema türleri ve nosema enfeksiyon düzeyi belirlenmiştir. Islah çalışması süresince kolonilere nosema için her hangi bir ilaç uygulaması yapılmamıştır. Beş dönem boyunca 123 kovanın nosema sporu bulaşıklığı takip edilmiştir. Spor sayısı- sıcaklık arasında negatif korelasyon (r = -0.115; P>0.01) ve spor sayısı nispi nem arasında pozitif korelasyon (r = 0.013; P>0.01) bulunmasına karşın ilişki istatistiksel olarak önemli değildir. Moleküler tanımlamada, beş sezon boyunca alınan örneklerde yalnızca N. ceranae sporu tespit edilmiştir. Sonuç olarak, hijyenik arı yetiştirme programı süresince nosema enfeksiyon seviyeleri azaldığı gözlenmiştir. Fakat nosema sporlarının azalmasının nedeninin hijyenik davranışa bağlı olup olmadığına dair karar verebilmek için başka hijyenik çalışmalarda da gözlemler yapılmalıdır. Bu çalışma bugüne kadar Türkiye'deki ıslah program süresince Nosema düzeyinin takibini içeren en uzun süreli ve tek çalışmadır

Türkiye’deki Hijyenik Bal Arısı Islah Çalışması Süresince Nosema Enfeksiyon Düzeyinin Takibi

The objective of this study was to follow Nosema infection levels and species under hygienic bee breeding program for resistance to American foulbrood (Paenibacillus larvae). The incidence of Nosema parasite infection levels and detection of the species of Nosema were evaluated in 5 periods during 2012-2014 for Mugla honey bees known as an ecotype of Apis mellifera anatoliaca in the hygienic bee breeding program. During the hygienic breeding program, no organic or synthetic chemical treatments were applied against nosemosis in the colonies. The incidences of Nosema spores were followed in 123 colonies at five time periods. Although the correlations were negative for between spores-temperature (r = -0.115; P>0.01) and positive for spores- humidity (r = 0.013; P>0.01) but not significant statistically. Molecular diagnosis showed that only N. ceranae spores were detected from samples during 5 seasons. In conclusion, nosema infection levels decreased under hygienic bee breeding programme but further monitoring studies should be performed in order to decide whether the nosema spores decrease due to hygienic behavior. To our knowledge, this is the first long- term and unique study for observation of Nosema during breeding program in Turkey so far

___

  • 1. Canning, E. U: Microsporidia. In, Kreier JP, Baker JR (Eds): Parasitic protozoa. 2nd ed., Vol. 6, pp. 299-370. San Diego, CA: Academic Press, 1993.
  • 2. Chen YP, Evans JD, Murphy C, Gutell R, Zuker M, Gundensen-Rindal D, Pettis JS: Morphological, molecular, and phylogenetic characterization of Nosema ceranae, a microsporidian parasite isolated from the European honey bee, Apis mellifera. J Eukaryot Microbiol, 56,142-147, 2009. DOI: 10.1111/j.1550-7408.2008.00374.x
  • 3. Singh T, Bhat MM, Khan MA: Microsporidiosis in the silkworm, Bombyx mori L. (Lepidoptera: Bombycidae). Pertanika J Trop Agric Sci, 35 (3): 387-406, 2012.
  • 4. Canning EU, Curry A, Cheney SA, LafranchiTristem NJ, Kawakami Y, Hatakeyama Y, Iwano H, Ishihara R: Nosema tyriae and Nosema sp; Microsporidian parasites of Cinnabar moth Tyria jacobaeae. J Invertebr Pathol, 74, 29-38, 1999. DOI: 10.1006/jipa.1999.4861
  • 5. Higes M, Martin R, Meana A: Nosema ceranae, a new microsporidian parasite in honey bees in Europe. J Invertebr Pathol, 92, 93-95, 2006. DOI: 10.1016/j.jip.2006.02.005
  • 6. Klee J, Besana A, Genersch E, Gisder S, Nanetti A, Tam DQ, Chinh TX, Puerta F, Ruz JM, Kryger P, Message D, Hatjina F, Korpela S, Fries I, Paxton RJ: Widespread dispersal of the microsporidium Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. J Invertebr Pathol, 96, 1-10, 2007. DOI: 10.1016/j.jip.2007.02.014
  • 7. Fries I: Nosema ceranae in European honeybees (Apis mellifera). J Invertebr Pathol, 103 (Suppl. 1): S73-S79, 2010. DOI: 10.1016/j.jip.2009.06.017
  • 8. Paxton RJ, Klee J, Korpela S, Fries I: Nosema ceranae has infected Apis mellifera in Europe since at least 1998 and may be more virulent than Nosema apis. Apidologie, 38, 558-565, 2007. DOI: 10.1051/ apido:2007037
  • 9. Higes M, Martin-Hernández R, Meana A: Nosema ceranae in Europe: An emergent type C nosemosis. Apidologie, 41, 375-392, 2010. DOI: 10.1051/apido/2010019
  • 10. Martin-Hernandez R, Meana A, Prieto L, Martinez-Salvador A,Garrido- Bailon, Higes M: Outcome of colonization of Apis mellifera by Nosema ceranae. Appl Environ Microbiol, 73, 6331-6338, 2007. DOI: 10.1128/AEM.00270-07
  • 11. Higes M, Meana A, Bartolomé C, Botias C, Martin-Hernández R: Nosema ceranae (Microsporidia), a controversial 21st century honey bee pathogen. Environ Microbiol Rep, 5, 17-29, 2013. DOI: 10.1111/1758- 2229.12024
  • 12. Cox-Foster DL, Conlan S, Holmes EC, Palacios G, Evans JD, Moran NA, Quan PL, Briese T, Hornig M, Geiser DM, Martinson V, Vanengelsdorp D, Kalkstein AL, Drysdale A, Hui J, Zhai J, Cui L, Hutchison SK, Simons JF, Egholm M, Pettis JS, Lipkin WI: A meta genomic survey of microbes in honeybee colony collapse disorder. Science, 318, 283-287, 2007. DOI: 10.1126/science.1146498
  • 13. Higes M, Martin-Hernández R, Garrido-Bailón E, GonzálezPorto AV, Garcia-Palencia P, Meana A, Del Nozal MJ, Mayo R, Bernal JL: Honeybee colony collapse due to Nosema ceranae in professional apiaries. Environ Microbiol Rep, 1, 110-113, 2009. DOI: 10.1111/j.1758- 2229.2009.00014.x
  • 14. Alaux C, Brunet JL, Dussaubat C, Mondet F, Tchamitchan SS, Cousin M, Brillard J, Baldy A, Belzunces LP, Le Conte Y: Interactions between Nosema microspores and a neonicotinoid weaken honeybees (Apis mellifera). Environ Microbiol, 12, 774-782, 2010. DOI: 10.1111/j.1462- 2920.2009.02123.x
  • 15. Vidau C, Diogon M, Aufauvre J, Fontbonne R, Vigues B, Brunet JL, Texier C, Biron DG, Blot N, Alaouih E, Belzunces LP, Delbac F: Exposure to sublethal doses of fipronil and thiacloprid highly increases mortality of honeybees previously infected by Nosema ceranae. PLosONE, 6 (6): e21550, 2011. DOI: 10.1371/journal.pone.0021550
  • 16. Pettis JS, Vanengelsdorp D, Johnson J, Dively G: Pesticide exposure in honeybee results in increased levels of the gut pathogen Nosema. Naturwissenschaften, 99, 153-158, 2012. DOI: 10.1007/s00114-011-0881-1
  • 17. Forsgren E, Fries I: Comparative virulence of Nosema ceranae and Nosema apis in individual European honey bees. Vet Parasitol, 170, 212- 217, 2010. DOI: 10.1016/j.vetpar.2010.02.010
  • 18. Fenoy S, Rueda C, Higes M, Martín-Hernandez R, DelAguila C: High-level resistance of Nosema ceranae, a parasite of the honeybee, to temperature and desiccation. Appl Environ Microbiol, 75, 6886-6889, 2009. DOI: 10.1128/AEM.01025-09
  • 19. Martin-Hernandez R, Meana A, Garcia-Palencia P, Marin P, Botias C, Garrido-Bailon E, Barrios L, Higes M: Effect of temperature on the biotic potential of honeybee microsporidia. Appl Environ Microbiol, 75, 2554-2557, 2009. DOI: 10.1128/AEM.02908-08
  • 20. Antúnez K, Martín-Hernández R, Prieto L, Meana A, Zunino P, Higes M: Immune suppression in the honeybee (Apis mellifera) following infection by Nosema ceranae (Microsporidia). Environ Microbiol, 11, 2284- 2290, 2009. DOI: 10.1111/j.1462-2920.2009.01953.x
  • 21. Mayack C, Naug D: Energetic stress in the honeybee Apis mellifera from Nosema ceranae infection. J Invertebr Pathol, 100, 185-188, 2009. DOI: 10.1016/j.jip.2008.12.001
  • 22. Naug D, Gibbs A: Behavioral changes mediated by hunger in honeybees infected with Nosema ceranae. Apidologie, 40, 595-599 2009. DOI: 10.1051/apido/2009039
  • 23. Higes M, Martin-Hernández R, Botias C, Garrido-Bailón E, González-Porto AV, Barrios L, Del Nozal MJ, Bernal JL, Jiménez JJ, Palencia PG, Meana A: How natural infection by Nosema ceranae causes honeybee colony collapse. Environ Microbiol, 10, 2659-2669, 2008. DOI: 10.1111/j.1462-2920.2008.01687.x
  • 24. Spivak M, Giliam M: Hygienic behavior of honeybees and its application for control of brood diseases and varroa mites. Part I: Hygienic behavior and resistance to American foulbrood. Bee World, 79, 124-134, 1998. DOI: 10.1080/0005772X.1998.11099394
  • 25. Spivak M, Giliam M: Hygienic behavior of honeybees and it s application for control of brood diseases and varroa mites. Part II: Studies on hygienic behavior since the Rothenbuhler era. Bee World, 79, 165- 182, 1998. DOI: 10.1080/0005772X.1998.11099408
  • 26. Harbo JR, Harris JW: Selecting honey bees for resistance to Varroa jacobsoni. Apidologie, 30, 183-196, 1999
  • 27. Harbo JR, Harris JW: Resistance to Varroa destructor (Mesostigmata: Varroidae) when mite-resistant queen honeybees (Hymenoptera: Apidae) were free-mated with unselected drones. J Econ Entomol, 94, 1319-1323, 2001.
  • 28. Harbo JR, Harris JW: Responses to Varroa by honeybees with different levels of Varroa sensitive hygiene. J Apic Res, 48, 156-161, 2009. DOI: 10.3896/IBRA.1.48.3.02
  • 29. Spivak M, Reuter GS: Varroa jacobsoni infestation in untreated honeybee (Hymenoptera: Apidae) colonies selected for hygienic behavior. J Econ Entomol, 94, 326-331, 2001. DOI: 10.1603/0022-0493- 94.2.326
  • 30. Buchler R, Berg S, Le Conte Y: Breeding for resistance to Varroa destructor in Europe. Apidologie, 41, 393-408, 2010. DOI: 10.1051/ apido/2010011
  • 31. Office International des Epizooties (OIE): Manual of Standards for Diagnostic Test and Vaccines. 2008. http://www.oie.int/eng/normes/ mmanual/A_00123.htm; Accessed: 20.11.2009.
  • 32. Human H, Brodschneider R, Dietemann V, Dively G, Ellis JD, Forsgren E, Fries I, Hatjina F, Hu Fl, Jaffe R, Jensen A. B, Kohler A, Magyar JP, Ozkirim A, Pirk CWW, Rose R, Strauss U, Tanner G, Tarpy D.R, Steen JJ, Van Deer M, Vaudo A, Vejsnaes F, Wilde J De, Williams GR, Zheng HQ: Miscellaneous standard methods for Apis mellifera research. J Apic Res, 52, 1-53, 2013. DOI: 10.3896/IBRA.1.52.4.10
  • 33. Fries I, Chauzat MP, Chen YP, Doublet V, Genersch E, Gisder S, Higes M, Mcmahon DP, Martin-Hernández R, Natsopoulou M, Paxton RJ, Tanner G, Webster TC, Williams GR: Standard methods for Nosema research. Apicult Res, 52, 1-28, 2013. DOI: 10.3896/IBRA.1.52.1.14
  • 34. Oskay D, Kence A, Ferek O, Ivgin Tunca R: Breeding Muğla Honeybee (Apis mellifera anatoliaca) for Improving Resistance to Diseases. 4th International Mugla Beekeeping and Pine Honey Congress, 2014 p.146-147, Muğla, Turkey.
  • 35. Martin-Hernandez R, Botias C, Garrido Bailon E, MartinezSalvador A, Prieto L, Meana A, Higes M: Microsporidia infecting Apis mellifera: Coexistence or competition. Is Nosema ceranae replacing Nosema apis? Environ Microbiol, 14, 2127-2138, 2012. DOI: 10.1111/j.1462- 2920.2011.02645.x
  • 36. Gisder S, Hedtke K, Möckel N, Frielitz MC, Linde A, Genersch E: Five-year cohort study of Nosema spp. in Germany: Does climate shape virulence and assertiveness of Nosema ceranae? Appl Environ Microbiol, 6, 3032-3038, 2010. DOI: 10.1128/AEM.03097-09
  • 37. Gajda A, Grzęda U, Topolska G: The fourth year of research on type C nosemosis course in Poland. 8th COLOSS Conference/MC meeting Halle-Saale, Germany, 1-3 September, p.32, 2012.
  • 38. Chauzat MP, Higes M, Martín-Hernández R, Meana A, Cougoule N, Faucon JP: Presence of Nosema ceranae in French honeybee colonies. J Apic Res, 46, 127-128, 2007. DOI: 10.1080/00218839.2007.11101380
  • 39. Staroň M, Jurovčíková J, Čermáková T, Staroňová AA: Incidence of Nosema apis and Nosema ceranae in Slovakia during the years 2009 and 2010. Slovak J Anim Sci, 45 (1): 36-38, 2012.
  • 40. Lotfi A, Jamshidi R, Aghdam-Shahryar H, Yousefkhani M: The prevalence of Nosemosis in honey hee colonies in Arasbaran Region (Northwestern Iran). American-Eurasian J Agri Environ Sci, 5 (2): 255-257, 2009.
  • 41. Tavassoli M, Eiganinejad S, Alizadeh-Asl S: A survey on Nosema apis infection in apiaries of Urmia, North-West of Iran. Iranian J Vet Sci Technol, 1, 35-40, 2009.
  • 42. Razmaraii N, Karimi H: A study of nosema of honeybees (Apis mellifera) in east Azerbaijan province of Iran. J Anim Vet Adv, 9 (5): 879- 882, 2010.
  • 43. Razmaraii N, Sadegh-Eteghad S, Babaei H, Paykari H, Esmaeilnia K, Froghy L: molecular identification of Nosema species in East-Azerbaijan province. Iran Archives Razi Inst, 68 (1): 23-27, 2013.
  • 44. Sıralı R, Doğaroğlu M: Survey results on honeybee pests and diseases in Thracian region of Turkey. Uludag Bee J, 5, 71-78, 2005.
  • 45. Giray T, Kence M, Oskay D, Doke MA, Kence A: Scientific note: Colony losses survey in Turkey and causes of bee deaths. Apidologie, 41, 451-453, 2010. DOI: 10.1051/apido/2009077
  • 46. Utuk AE, Piskin FÇ, Kurt M: First molecular detection of Nosema ceranae in Turkey. Ankara Univ Vet Fak Derg, 57, 275-278, 2010. DOI: 10.1501/Vetfak_0000002439
  • 47. Whitaker J, Szalanski AL, Kence M: Molecular detection of Nosema ceranae and N. apis from Turkish honey bees. Apidologie, 42 (2): 174-180, 2011, DOI: 10.1051/apido/2010045
  • 48. Muz MN, Girisgin AO, Muz D, Aydin L: Molecular detection of Nosema ceranae and Nosema apis infections in Turkish apiaries with collapsed colonies. J Apicult Res, 49, 342, 2010. DOI: 10.3896/IBRA.1.49.4.09
  • 49. Tozkar CO, Kence M, Evans J, Kence A: Identification of Nosema spp. among honey bees from different regions of Turkey, WG2 Workshop: Nosema, from knowledge to experimental setup. p.25. 3rd-4th of March, Istanbul, Turkey. 2012.
  • 50. Yalçinkaya A, Martin-Hernandez R, Higes M, Ozkirim A: Epidemiology of Nosema spp. in Turkey, WG2 Workshop: Nosema, from knowledge to experimental setup. p.27, 3rd-4th of March, Istanbul, Turkey, 2012.
  • 51. Ivgin Tunca R, Oskay D, Gosterit A, Tekin O: Does Nosema ceranae wipe out Nosema apis in Turkey? Iran J Parasitol, 11 (2): 259-264, 2016.
  • 52. Traynor K, Traynor M: Bee breeding around the world. American Bee J, 48, 135-139, 2008.
Kafkas Üniversitesi Veteriner Fakültesi Dergisi-Cover
  • ISSN: 1300-6045
  • Yayın Aralığı: Yılda 6 Sayı
  • Başlangıç: 1995
  • Yayıncı: Kafkas Üniv. Veteriner Fak.
Sayıdaki Diğer Makaleler

Monitoring of Nosema Infections Levels During Hygienic Honey Bee Breeding Programs in Turkey

Rahşan İVGİN TUNCA, DEVRİM OSKAY, Sezai ERGINOGLU

Associations Between GH, PRL, STAT5A, OPN, PIT-1, LEP and FGF2 Polymorphisms and Fertility in Holstein-Friesian Heifers

YASEMİN ÖNER, ONUR YILMAZ, Hayrettin OKUT, NEZİH ATA, GÜLNAZ MECİTOĞLU, ABDULKADİR KESKİN

A Review of Machine Learning Applications in Veterinary Field

OYA KALIPSIZ, ERHAN GÖKÇE, PINAR CİHAN

Evaluation of Pulmonary Infection Risk in Dogs with Pulmonary Contusion

HAKAN SALCI, Serpi KAHYA, Melike ÇETİN, AHMET AKKOÇ, AHMET SAMİ BAYRAM

Antimicrobial Susceptibility Profiles and Coagulase Gene Polymorphism of Staphylococcus aureus Isolated from Bovine Subclinical Mastitis

BEYTULLAH KENAR, Arzu Funda BAĞCIGİL, YAHYA KUYUCUOĞLU, BEREN BAŞARAN KAHRAMAN, SELAHATTİN KONAK

(Bir Kedide Translasyonel Facet Eklem Kilitlenmesi)

Hakan SALCI, Hilal ÇEŞME

Bir Kedide Nasofarengeal Polip Traksiyon-Avulziyonu Sonucu Gelişen Geçici Horner Sendromu

F. Eser ÖZGENCİL, Çağrı GÜLTEKİN, Gökhan ULUKAN

Antimicrobial Resistance and Virulence Characteristics in Enterococcus Isolates from Dogs

Yılmaz BOYAR, Özkan ASLANTAŞ, SÜHEYLA TÜRKYILMAZ

Effect of Chitosan Oligosaccharides on Antioxidant Function, Lymphocyte Cycle and Apoptosis in Ileum Mucosa of Broiler

XİAOCONG LI, Xuemei DING, Xi PENG, Xiaofeng CHI, Hengmin CUI, Zhicai ZUO, Jing FANG

Telomeric Attrition with Increasing Age in Short- (Chihuahua Dog) and Long- (Asian Elephant) Life Span Animals

Kittisak BUDDHACHAT, Wannapimol KRIANGWANICH, Isaraporn KUMOUN, Janine L. BROWN, Sasisophin CHAILANGKARN, Chaleamchat SOMGIRD, Chatchote THITARAM, Sukon PRASITWATTANASEREE, Korakot NGANVONGPANIT